Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

ABC Transporters: Regulation and Association with Multidrug Resistance in Hepatocellular Carcinoma and Colorectal Carcinoma

Author(s): María Paula Ceballos, Juan Pablo Rigalli, Lucila Inés Ceré, Mariana Semeniuk, Viviana Alicia Catania and María Laura Ruiz*

Volume 26, Issue 7, 2019

Page: [1224 - 1250] Pages: 27

DOI: 10.2174/0929867325666180105103637

Price: $65

Open Access Journals Promotions 2
Abstract

For most cancers, the treatment of choice is still chemotherapy despite its severe adverse effects, systemic toxicity and limited efficacy due to the development of multidrug resistance (MDR). MDR leads to chemotherapy failure generally associated with a decrease in drug concentration inside cancer cells, frequently due to the overexpression of ABC transporters such as P-glycoprotein (P-gp/MDR1/ABCB1), multidrug resistance-associated proteins (MRPs/ABCCs), and breast cancer resistance protein (BCRP/ABCG2), which limits the efficacy of chemotherapeutic drugs. The aim of this review is to compile information about transcriptional and post-transcriptional regulation of ABC transporters and discuss their role in mediating MDR in cancer cells.

This review also focuses on drug resistance by ABC efflux transporters in cancer cells, particularly hepatocellular carcinoma (HCC) and colorectal carcinoma (CRC) cells. Some aspects of the chemotherapy failure and future directions to overcome this problem are also discussed.

Keywords: ABCB1, ABCC2, ABCG2, chemotherapy, hepatocellular carcinoma, colorectal carcinoma, multidrug resistance, transcriptional regulation.

[1]
Baguley, B.C. Multiple drug resistance mechanisms in cancer. Mol. Biotechnol., 2010, 46(3), 308-316.
[2]
Schinkel, A.H.; Jonker, J.W. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: An overview. Adv. Drug Deliv. Rev., 2003, 55(1), 3-29.
[3]
Longley, D.B.; Johnston, P.G. Molecular mechanisms of drug resistance. J. Pathol., 2005, 205(2), 275-292.
[4]
Holohan, C.; Van Schaeybroeck, S.; Longley, D.B.; Johnston, P.G. Cancer drug resistance: An evolving paradigm. Nat. Rev. Cancer, 2013, 13(10), 714-726.
[5]
Kartal-Yandim, M.; Adan-Gokbulut, A.; Baran, Y. Molecular mechanisms of drug resistance and its reversal in cancer. Crit. Rev. Biotechnol., 2016, 36(4), 716-726.
[6]
Chen, Z.; Shi, T.; Zhang, L.; Zhu, P.; Deng, M.; Huang, C. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family in multidrug resistance: A review of the past decade. 2016, 370, 153-164.
[7]
El-Awady, R.; Saleh, E.; Hashim, A.; Soliman, N.; Dallah, A.; Elrasheed, A.; Elakraa, G. The role of eukaryotic and prokaryotic ABC transporter family in failure of chemotherapy. Front. Pharmacol., 2017, 7, 535.
[8]
Ueda, K.; Clark, D.P.; Chen, C.J.; Roninson, I.B.; Gottesman, M.M.; Pastan, I. The human multidrug resistance (mdr1) gene. cDNA cloning and transcription initiation. J. Biol. Chem., 1987, 262(2), 505-508.
[9]
Burk, O.; Arnold, K.A.; Geick, A.; Tegude, H.; Eichelbaum, M. A role for constitutive androstane receptor in the regulation of human intestinal MDR1 expression. Biol. Chem., 2005, 386(6), 503-513.
[10]
Cerveny, L.; Svecova, L.; Anzenbacherova, E.; Vrzal, R.; Staud, F.; Dvorak, Z.; Ulrichova, J.; Anzenbacher, P.; Pavek, P. Valproic acid induces CYP3A4 and MDR1 gene expression by activation of constitutive androstane receptor and pregnane X receptor pathways. Drug Metab. Dispos., 2007, 35(7), 1032-1041.
[11]
Luo, G.; Cunningham, M.; Kim, S.; Burn, T.; Lin, J.; Sinz, M.; Hamilton, G.; Rizzo, C.; Jolley, S.; Gilbert, D.; Downey, A.; Mudra, D.; Graham, R.; Carroll, K.; Xie, J.; Madan, A.; Parkinson, A.; Christ, D.; Selling, B.; LeCluyse, E.; Gan, L.S. CYP3A4 induction by drugs: correlation between a pregnane X receptor reporter gene assay and CYP3A4 expression in human hepatocytes. Drug Metab. Dispos., 2002, 30(7), 795-804.
[12]
Luo, G.; Guenthner, T.; Gan, L.S.; Humphreys, W.G. CYP3A4 induction by xenobiotics: Biochemistry, experimental methods and impact on drug discovery and development. Curr. Drug Metab., 2004, 5(6), 483-505.
[13]
Geick, A.; Eichelbaum, M.; Burk, O. Nuclear receptor response elements mediate induction of intestinal MDR1 by rifampin. J. Biol. Chem., 2001, 276(18), 14581-14587.
[14]
Haslam, I.S.; Jones, K.; Coleman, T.; Simmons, N.L. Rifampin and digoxin induction of MDR1 expression and function in human intestinal (T84) epithelial cells. Br. J. Pharmacol., 2008, 154(1), 246-255.
[15]
Watkins, R.E.; Wisely, G.B.; Moore, L.B.; Collins, J.L.; Lambert, M.H.; Williams, S.P.; Willson, T.M.; Kliewer, S.A.; Redinbo, M.R. The human nuclear xenobiotic receptor PXR: structural determinants of directed promiscuity. Science, 2001, 292(5525), 2329-2333.
[16]
Rigalli, J.P.; Ruiz, M.L.; Perdomo, V.G.; Villanueva, S.S.M.; Mottino, A.D.; Catania, V.A. Pregnane X receptor mediates the induction of P-glycoprotein by spironolactone in HepG2 cells. Toxicology, 2011, 285(1-2), 18-24.
[17]
Rigalli, J.P.; Perdomo, V.G.; Luquita, M.G.; Villanueva, S.S.M.; Arias, A.; Theile, D.; Weiss, J.; Mottino, A.D.; Ruiz, M.L.; Catania, V.A. Regulation of biotransformation systems and ABC transporters by benznidazole in HepG2 cells: Involvement of pregnane X-receptor. PLoS Negl. Trop. Dis., 2012, 6(12), e1951.
[18]
Baker, E.K.; Johnstone, R.W.; Zalcberg, J.R.; El-Osta, A. Epigenetic changes to the MDR1 locus in response to chemotherapeutic drugs. Oncogene, 2005, 24(54), 8061-8075.
[19]
Scotto, K.W. Transcriptional regulation of ABC drug transporters. Oncogene, 2003, 22(47), 7496-7511.
[20]
Mickley, L.A.; Lee, J.S.; Weng, Z.; Zhan, Z.; Alvarez, M.; Wilson, W.; Bates, S.E.; Fojo, T. Genetic polymorphism in MDR-1: a tool for examining allelic expression in normal cells, unselected and drug-selected cell lines, and human tumors. Blood, 1998, 91(5), 1749-1756.
[21]
Thottassery, J.V.; Zambetti, G.P.; Arimori, K.; Schuetz, E.G.; Schuetz, J.D. p53-dependent regulation of MDR1 gene expression causes selective resistance to chemotherapeutic agents. Proc. Natl. Acad. Sci. USA, 1997, 94(20), 11037-11042.
[22]
Sampath, J.; Sun, D.; Kidd, V.J.; Grenet, J.; Gandhi, A.; Shapiro, L.H.; Wang, Q.; Zambetti, G.P.; Schuetz, J.D. Mutant p53 cooperates with ETS and selectively up-regulates human MDR1 not MRP1. J. Biol. Chem., 2001, 276(42), 39359-39367.
[23]
Chin, K.V.; Ueda, K.; Pastan, I.; Gottesman, M.M. Modulation of activity of the promoter of the human MDR1 gene by Ras and p53. Science, 1992, 255(5043), 459-462.
[24]
Cornwell, M.M.; Smith, D.E. A signal transduction pathway for activation of the mdr1 promoter involves the proto-oncogene c-raf kinase. J. Biol. Chem., 1993, 268(21), 15347-15350.
[25]
Yang, J.M.; Vassil, A.D.; Hait, W.N. Activation of phospholipase C induces the expression of the multidrug resistance (MDR1) gene through the Raf-MAPK pathway. Mol. Pharmacol., 2001, 60(4), 674-680.
[26]
Arrigoni, E.; Galimberti, S.; Petrini, M.; Danesi, R.; Di Paolo, A. ATP-binding cassette transmembrane transporters and their epigenetic control in cancer: an overview. Expert Opin. Drug Metab. Toxicol., 2016, 12(12), 1419-1432.
[27]
Yang, T.; Zheng, Z.M.; Li, X.N.; Li, Z.F.; Wang, Y.; Geng, Y.F.; Bai, L.; Zhang, X.B. MiR-223 modulates multidrug resistance via downregulation of ABCB1 in hepatocellular carcinoma cells. Exp. Biol. Med. (Maywood), 2013, 238(9), 1024-1032.
[28]
Bruhn, O.; Drerup, K.; Kaehler, M.; Haenisch, S.; Röder, C.; Cascorbi, I. Length variants of the ABCB1 3′-UTR and loss of miRNA binding sites: possible consequences in regulation and pharmacotherapy resistance. Pharmacogenomics, 2016, 17(4), 327-340.
[29]
Ikemura, K.; Yamamoto, M.; Miyazaki, S.; Mizutani, H.; Iwamoto, T.; Okuda, M. MicroRNA-145 post-transcriptionally regulates the expression and function of P-glycoprotein in intestinal epithelial cells. Mol. Pharmacol., 2013, 83(2), 399-405.
[30]
Chen, Z.; Ma, T.; Huang, C.; Zhang, L.; Lv, X.; Xu, T.; Hu, T.; Li, J. MiR-27a modulates the MDR1/P-glycoprotein expression by inhibiting FZD7/β-catenin pathway in hepatocellular carcinoma cells. Cell. Signal., 2013, 25(12), 2693-2701.
[31]
Requenez-Contreras, J.L.; López-Castillejos, E.S.; Hernández-Flores, R.; Moreno-Eutimio, M.A.; Granados-Riveron, J.T.; Martinez-Ruiz, G.U.; Aquino-Jarquin, G. MiR-138 indirectly regulates the MDR1 promoter by NF-κB/p65 silencing. Biochem. Biophys. Res. Commun., 2017, 484(3), 648-655.
[32]
Ménez, C.; Mselli-Lakhal, L.; Foucaud-Vignault, M.; Balaguer, P.; Alvinerie, M.; Lespine, A. Ivermectin induces P-glycoprotein expression and function through mRNA stabilization in murine hepatocyte cell line. Biochem. Pharmacol., 2012, 83(2), 269-278.
[33]
Yague, E.; Armesilla, A.L.; Harrison, G.; Elliott, J.; Sardini, A.; Higgins, C.F.; Raguz, S. P-glycoprotein (MDR1) expression in leukemic cells is regulated at two distinct steps, mRNA stabilization and translational initiation. J. Biol. Chem., 2003, 278(12), 10344-10352.
[34]
Toscano-Garibay, J.D.; Aquino-Jarquin, G. Regulation exerted by miRNAs in the promoter and UTR sequences: MDR1/P-gp expression as a particular case. DNA Cell Biol., 2012, 31(8), 1358-1364.
[35]
Sparanese, D.; Lee, C.H. CRD-BP shields c-myc and MDR-1 RNA from endonucleolytic attack by a mammalian endoribonuclease. Nucleic Acids Res., 2007, 35(4), 1209-1221.
[36]
Tanaka, T.; Uchiumi, T.; Hinoshita, E.; Inokuchi, A.; Toh, S.; Wada, M.; Takano, H.; Kohno, K.; Kuwano, M. The human multidrug resistance protein 2 gene: Functional characterization of the 5′-flanking region and expression in hepatic cells. Hepatology, 1999, 30(6), 1507-1512.
[37]
Stöckel, B.; König, J.; Nies, A.T.; Cui, Y.; Brom, M.; Keppler, D. Characterization of the 5′-flanking region of the human multidrug resistance protein 2 (MRP2) gene and its regulation in comparison with the multidrug resistance protein 3 (MRP3) gene. Eur. J. Biochem., 2000, 267(5), 1347-1358.
[38]
Ruiz, M.L.; Villanueva, S.S.M.; Luquita, M.G.; Pellegrino, J.M.; Rigalli, J.P.; Arias, A.; Sánchez Pozzi, E.J.; Mottino, A.D.; Catania, V.A. Induction of intestinal multidrug resistance-associated protein 2 (Mrp2) by spironolactone in rats. Eur. J. Pharmacol., 2009, 623(1-3), 103-106.
[39]
di Masi, A.; Marinis, E. D.; Ascenzi, P.; Marino, M. Nuclear receptors CAR and PXR: Molecular, functional, and biomedical aspects. Mol. Aspects Med., 2009, 30, 297-343.
[40]
Johnson, D.R.; Klaassen, C.D. Regulation of rat multidrug resistance protein 2 by classes of prototypical microsomal enzyme inducers that activate distinct transcription pathways. Toxicol. Sci., 2002, 67(2), 182-189.
[41]
Kast, H.R.; Goodwin, B.; Tarr, P.T.; Jones, S.A.; Anisfeld, A.M.; Stoltz, C.M.; Tontonoz, P.; Kliewer, S.; Willson, T.M.; Edwards, P.A. Regulation of multidrug resistance-associated protein 2 (ABCC2) by the nuclear receptors pregnane X receptor, farnesoid X-activated receptor, and constitutive androstane receptor. J. Biol. Chem., 2002, 277(4), 2908-2915.
[42]
Vollrath, V.; Wielandt, A.M.; Iruretagoyena, M.; Chianale, J. Role of Nrf2 in the regulation of the Mrp2 (ABCC2) gene. Biochem. J., 2006, 395(3), 599-609.
[43]
Ji, L.; Li, H.; Gao, P.; Shang, G.; Zhang, D.D.; Zhang, N.; Jiang, T. Nrf2 pathway regulates multidrug-resistance-associated protein 1 in small cell lung cancer. PLoS One, 2013, 8(5), e63404.
[44]
Ghanem, C.I.; Rudraiah, S.; Bataille, A.M.; Vigo, M.B.; Goedken, M.J.; Manautou, J.E. Role of nuclear factor-erythroid 2-related factor 2 (Nrf2) in the transcriptional regulation of brain ABC transporters during acute acetaminophen (APAP) intoxication in mice. Biochem. Pharmacol., 2015, 94(3), 203-211.
[45]
Rigalli, J.P.; Perdomo, V.G.; Ciriaci, N.; Francés, D.E.A.; Ronco, M.T.; Bataille, A.M.; Ghanem, C.I.; Ruiz, M.L.; Manautou, J.E.; Catania, V.A. The trypanocidal benznidazole promotes adaptive response to oxidative injury: Involvement of the nuclear factor-erythroid 2-related factor-2 (Nrf2) and multidrug resistance associated protein 2 (MRP2). Toxicol. Appl. Pharmacol., 2016, 304, 90-98.
[46]
Hirai, T.; Fukui, Y.; Motojima, K. PPARalpha agonists positively and negatively regulate the expression of several nutrient/drug transporters in mouse small intestine. Biol. Pharm. Bull., 2007, 30(11), 2185-2190.
[47]
Kauffmann, H.M.; Pfannschmidt, S.; Zöller, H.; Benz, A.; Vorderstemann, B.; Webster, J.I.; Schrenk, D. Influence of redox-active compounds and PXR-activators on human MRP1 and MRP2 gene expression. Toxicology, 2002, 171(2-3), 137-146.
[48]
Huang, R.; Murry, D.J.; Kolwankar, D.; Hall, S.D.; Foster, D.R. Vincristine transcriptional regulation of efflux drug transporters in carcinoma cell lines. Biochem. Pharmacol., 2006, 71(12), 1695-1704.
[49]
König, J.; Rost, D.; Cui, Y.; Keppler, D. Characterization of the human multidrug resistance protein isoform MRP3 localized to the basolateral hepatocyte membrane. Hepatology, 1999, 29(4), 1156-1163.
[50]
Jiang, H.; Chen, K.; He, J.; Pan, F.; Li, J.; Chen, J.; Chen, W.; Liang, H. Association of pregnane X receptor with multidrug resistance-related protein 3 and its role in human colon cancer chemoresistance. J. Gastrointest. Surg., 2009, 13(10), 1831-1838.
[51]
Ruiz, M.L.; Rigalli, J.P.; Arias, A.; Villanueva, S.; Banchio, C.; Vore, M.; Mottino, A.D.; Catania, V.A. Induction of hepatic multidrug resistance-associated protein 3 by ethynylestradiol is independent of cholestasis and mediated by estrogen receptor. Drug Metab. Dispos., 2013, 41(2), 275-280.
[52]
Ruiz, M.L.; Rigalli, J.P.; Arias, A.; Villanueva, S.S.M.; Banchio, C.; Vore, M.; Mottino, A.D.; Catania, V.A. Estrogen receptor-α mediates human multidrug resistance associated protein 3 induction by 17α-ethynylestradiol. Role of activator protein-1. Biochem. Pharmacol., 2013, 86(3), 401-409.
[53]
Lee, C.H.; Bradley, G.; Ling, V. Increased P-glycoprotein messenger RNA stability in rat liver tumors in vivo. J. Cell. Physiol., 1998, 177(1), 1-12.
[54]
Trauner, M. Molecular alterations of canalicular transport systems in experimental models of cholestasis: Possible functional correlations. Yale J. Biol. Med., 1997, 70(4), 365-378.
[55]
Cao, J.; Huang, L.; Liu, Y.; Hoffman, T.; Stieger, B.; Meier, P.J.; Vore, M. Differential regulation of hepatic bile salt and organic anion transporters in pregnant and postpartum rats and the role of prolactin. Hepatology, 2001, 33(1), 140-147.
[56]
Liang, Z.; Wu, H.; Xia, J.; Li, Y.; Zhang, Y.; Huang, K.; Wagar, N.; Yoon, Y.; Cho, H.T.; Scala, S.; Shim, H. Involvement of miR-326 in chemotherapy resistance of breast cancer through modulating expression of multidrug resistance-associated protein 1. Biochem. Pharmacol., 2010, 79(6), 817-824.
[57]
Haenisch, S.; Laechelt, S.; Bruckmueller, H.; Werk, A.; Noack, A.; Bruhn, O.; Remmler, C.; Cascorbi, I. Down-regulation of ATP-binding cassette C2 protein expression in HepG2 cells after rifampicin treatment is mediated by microRNA-379. Mol. Pharmacol., 2011, 80(2), 314-320.
[58]
Molina-Pinelo, S.; Gutiérrez, G.; Pastor, M.D.; Hergueta, M.; Moreno-Bueno, G.; García-Carbonero, R.; Nogal, A.; Suárez, R.; Salinas, A.; Pozo-Rodríguez, F.; Lopez-Rios, F.; Agulló-Ortuño, M.T.; Ferrer, I.; Perpiñá, A.; Palacios, J.; Carnero, A.; Paz-Ares, L. MicroRNA-dependent regulation of transcription in non-small cell lung cancer. PLoS One, 2014, 9(3), e90524.
[59]
Markova, S.M.; Kroetz, D.L. ABCC4 is regulated by microRNA-124a and microRNA-506. Biochem. Pharmacol., 2014, 87(3), 515-522.
[60]
Wu, Q.; Yang, Z.; Xia, L.; Nie, Y.; Wu, K.; Shi, Y.; Fan, D. Methylation of miR-129-5p CpG island modulates multi-drug resistance in gastric cancer by targeting ABC transporters. Oncotarget, 2014, 5(22), 11552-11563.
[61]
Zhang, Y.; Li, W.; Vore, M. Translational regulation of rat multidrug resistance-associated protein 2 expression is mediated by upstream open reading frames in the 5′ untranslated region. Mol. Pharmacol., 2007, 71(1), 377-383.
[62]
Bailey-Dell, K.J.; Hassel, B.; Doyle, L.A.; Ross, D.D. Promoter characterization and genomic organization of the human breast cancer resistance protein (ATP-binding cassette transporter G2) gene. Biochim. Biophys. Acta, 2001, 1520(3), 234-241.
[63]
Natarajan, K.; Xie, Y.; Baer, M.R.; Ross, D.D. Role of breast cancer resistance protein (BCRP/ABCG2) in cancer drug resistance. Biochem. Pharmacol., 2012, 83(8), 1084-1103.
[64]
Wang, H.; Lee, E.W.; Zhou, L.; Leung, P.C.K.; Ross, D.D.; Unadkat, J.D.; Mao, Q. Progesterone receptor (PR) isoforms PRA and PRB differentially regulate expression of the breast cancer resistance protein in human placental choriocarcinoma BeWo cells. Mol. Pharmacol., 2008, 73(3), 845-854.
[65]
To, K.K.W.; Robey, R.; Zhan, Z.; Bangiolo, L.; Bates, S.E. Upregulation of ABCG2 by romidepsin via the aryl hydrocarbon receptor pathway. Mol. Cancer Res., 2011, 9(4), 516-527.
[66]
Krishnamurthy, P.; Ross, D.D.; Nakanishi, T.; Bailey-Dell, K.; Zhou, S.; Mercer, K.E.; Sarkadi, B.; Sorrentino, B.P.; Schuetz, J.D. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J. Biol. Chem., 2004, 279(23), 24218-24225.
[67]
Ee, P.L.; Kamalakaran, S.; Tonetti, D.; He, X.; Ross, D.D.; Beck, W.T. Identification of a novel estrogen response element in the breast cancer resistance protein (ABCG2) gene. Cancer Res., 2004, 64(4), 1247-1251.
[68]
Yasuda, S.; Itagaki, S.; Hirano, T.; Iseki, K. Expression level of ABCG2 in the placenta decreases from the mid stage to the end of gestation. Biosci. Biotechnol. Biochem., 2005, 69(10), 1871-1876.
[69]
Li, W.; Jia, M.; Qin, X.; Hu, J.; Zhang, X.; Zhou, G. Harmful effect of ERβ on BCRP-mediated drug resistance and cell proliferation in ERα/PR-negative breast cancer. FEBS J., 2013, 280(23), 6128-6140.
[70]
Imai, Y.; Ishikawa, E.; Asada, S.; Sugimoto, Y. Estrogen-mediated post transcriptional down-regulation of breast cancer resistance protein/ABCG2. Cancer Res., 2005, 65(2), 596-604.
[71]
Wang, H.; Zhou, L.; Gupta, A.; Vethanayagam, R.R.; Zhang, Y.; Unadkat, J.D.; Mao, Q. Regulation of BCRP/ABCG2 expression by progesterone and 17beta-estradiol in human placental BeWo cells. Am. J. Physiol. Endocrinol. Metab., 2006, 290(5), E798-E807.
[72]
Hartz, A.M.S.; Mahringer, A.; Miller, D.S.; Bauer, B. 17-β-Estradiol: a powerful modulator of blood-brain barrier BCRP activity. J. Cereb. Blood Flow Metab., 2010, 30(10), 1742-1755.
[73]
Mao, Q.; Unadkat, J.D. Role of the breast cancer resistance protein (BCRP/ABCG2) in drug transport--an update. AAPS J., 2015, 17(1), 65-82.
[74]
Turner, J.G.; Gump, J.L.; Zhang, C.; Cook, J.M.; Marchion, D.; Hazlehurst, L.; Munster, P.; Schell, M.J.; Dalton, W.S.; Sullivan, D.M. ABCG2 expression, function, and promoter methylation in human multiple myeloma. Blood, 2006, 108(12), 3881-3889.
[75]
To, K.K.W.; Zhan, Z.; Bates, S.E. Aberrant promoter methylation of the ABCG2 gene in renal carcinoma. Mol. Cell. Biol., 2006, 26(22), 8572-8585.
[76]
To, K.K.W.; Zhan, Z.; Litman, T.; Bates, S.E. Regulation of ABCG2 expression at the 3′ untranslated region of its mRNA through modulation of transcript stability and protein translation by a putative microRNA in the S1 colon cancer cell line. Mol. Cell. Biol., 2008, 28(17), 5147-5161.
[77]
To, K.K.W.W.; Robey, R.W.; Knutsen, T.; Zhan, Z.; Ried, T.; Bates, S.E. Escape from hsa-miR-519c enables drug-resistant cells to maintain high expression of ABCG2. Mol. Cancer Ther., 2009, 8(10), 2959-2968.
[78]
Wang, F.; Xue, X.; Wei, J.; An, Y.; Yao, J.; Cai, H.; Wu, J.; Dai, C.; Qian, Z.; Xu, Z.; Miao, Y. hsa-miR-520h downregulates ABCG2 in pancreatic cancer cells to inhibit migration, invasion, and side populations. Br. J. Cancer, 2010, 103(4), 567-574.
[79]
Pan, Y-Z.; Morris, M.E.; Yu, A-M. MicroRNA-328 negatively regulates the expression of breast cancer resistance protein (BCRP/ABCG2) in human cancer cells. Mol. Pharmacol., 2009, 75(6), 1374-1379.
[80]
Jiao, X.; Zhao, L.; Ma, M.; Bai, X.; He, M.; Yan, Y.; Wang, Y.; Chen, Q.; Zhao, X.; Zhou, M.; Cui, Z.; Zheng, Z.; Wang, E.; Wei, M. MiR-181a enhances drug sensitivity in mitoxantone-resistant breast cancer cells by targeting breast cancer resistance protein (BCRP/ABCG2). Breast Cancer Res. Treat., 2013, 139(3), 717-730.
[81]
Ma, M-T.; He, M.; Wang, Y.; Jiao, X-Y.; Zhao, L.; Bai, X-F.; Yu, Z.J.; Wu, H.Z.; Sun, M.L.; Song, Z.G.; Wei, M.J. MiR-487a resensitizes mitoxantrone (MX)-resistant breast cancer cells (MCF-7/MX) to MX by targeting breast cancer resistance protein (BCRP/ABCG2). Cancer Lett., 2013, 339(1), 107-115.
[82]
Ferlay, J.; Soerjomataram, I.; Dikshit, R.; Eser, S.; Mathers, C.; Rebelo, M.; Parkin, D.M.; Forman, D.; Bray, F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer, 2015, 136(5), E359-E386.
[83]
Chacko, S.; Samanta, S. Hepatocellular carcinoma: A life-threatening disease. Biomed. Pharmacother., 2016, 84, 1679-1688.
[84]
Balogh, J.; Victor, D., III; Asham, E.H.; Burroughs, S.G.; Boktour, M.; Saharia, A.; Li, X.; Ghobrial, R.M.; Monsour, H.P. Jr Hepatocellular carcinoma: a review. J. Hepatocell. Carcinoma, 2016, 3, 41-53.
[85]
Barretina, J.; Caponigro, G.; Stransky, N.; Venkatesan, K.; Margolin, A.A.; Kim, S.; Wilson, C.J.; Lehár, J.; Kryukov, G.V.; Sonkin, D.; Reddy, A.; Liu, M.; Murray, L.; Berger, M.F.; Monahan, J.E.; Morais, P.; Meltzer, J.; Korejwa, A.; Jané-Valbuena, J.; Mapa, F.A.; Thibault, J.; Bric-Furlong, E.; Raman, P.; Shipway, A.; Engels, I.H.; Cheng, J.; Yu, G.K.; Yu, J.; Aspesi, P., Jr; de Silva, M.; Jagtap, K.; Jones, M.D.; Wang, L.; Hatton, C.; Palescandolo, E.; Gupta, S.; Mahan, S.; Sougnez, C.; Onofrio, R.C.; Liefeld, T.; MacConaill, L.; Winckler, W.; Reich, M.; Li, N.; Mesirov, J.P.; Gabriel, S.B.; Getz, G.; Ardlie, K.; Chan, V.; Myer, V.E.; Weber, B.L.; Porter, J.; Warmuth, M.; Finan, P.; Harris, J.L.; Meyerson, M.; Golub, T.R.; Morrissey, M.P.; Sellers, W.R.; Schlegel, R.; Garraway, L.A. The cancer cell line encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature, 2012, 483(7391), 603-607.
[86]
Chen, B.; Sirota, M.; Fan-Minogue, H.; Hadley, D.; Butte, A.J. Relating hepatocellular carcinoma tumor samples and cell lines using gene expression data in translational research. BMC Med. Genomics, 2015, 8(Suppl. 2), S2-S5.
[87]
Wong, C-M.; Ng, I.O.L. Molecular pathogenesis of hepatocellular carcinoma. Liver Int., 2008, 28(2), 160-174.
[88]
Brito, A.F.; Abrantes, A.M.; Tralhão, J.G.; Botelho, M.F. Targeting hepatocellular carcinoma: What did we discover so far? Oncol. Rev., 2016, 10(2), 302.
[89]
Zhang, X.; Ng, H.L.H.; Lu, A.; Lin, C.; Zhou, L.; Lin, G.; Zhang, Y.; Yang, Z.; Zhang, H. Drug delivery system targeting advanced hepatocellular carcinoma: Current and future. Nanomedicine (Lond.), 2016, 12(4), 853-869.
[90]
Lyons, J.F.; Wilhelm, S.; Hibner, B.; Bollag, G. Discovery of a novel Raf kinase inhibitor. Endocr. Relat. Cancer, 2001, 8(3), 219-225.
[91]
Wilhelm, S.M.; Adnane, L.; Newell, P.; Villanueva, A.; Llovet, J.M.; Lynch, M. Preclinical overview of sorafenib, a multikinase inhibitor that targets both Raf and VEGF and PDGF receptor tyrosine kinase signaling. Mol. Cancer Ther., 2008, 7(10), 3129-3140.
[92]
Pan, J-J.; Javle, M.; Thinn, M.M.; Hsueh, C-T.; Hsueh, C-T. Critical appraisal of the role of sorafenib in the management of hepatocellular carcinoma. Hepat. Med., 2010, 2, 147-155.
[93]
Fernando, J.; Sancho, P.; Fernández-Rodriguez, C.M.; Lledó, J.L.; Caja, L.; Campbell, J.S.; Fausto, N.; Fabregat, I. Sorafenib sensitizes hepatocellular carcinoma cells to physiological apoptotic stimuli. J. Cell. Physiol., 2012, 227(4), 1319-1325.
[94]
Gadaleta-Caldarola, G.; Infusino, S.; Divella, R.; Ferraro, E.; Mazzocca, A.; De Rose, F.; Filippelli, G.; Abbate, I.; Brandi, M. Sorafenib: 10 years after the first pivotal trial. Future Oncol., 2015, 11(13), 1863-1880.
[95]
Chen, J.; Jin, R.; Zhao, J.; Liu, J.; Ying, H.; Yan, H.; Zhou, S.; Liang, Y.; Huang, D.; Liang, X.; Yu, H.; Lin, H.; Cai, X. Potential molecular, cellular and microenvironmental mechanism of sorafenib resistance in hepatocellular carcinoma. Cancer Lett., 2015, 367(1), 1-11.
[96]
Colagrande, S.; Inghilesi, A.L.; Aburas, S.; Taliani, G.G.; Nardi, C.; Marra, F. Challenges of advanced hepatocellular carcinoma. World J. Gastroenterol., 2016, 22(34), 7645-7659.
[97]
Samonakis, D.N.; Kouroumalis, E.A. Systemic treatment for hepatocellular carcinoma: Still unmet expectations. World J. Hepatol., 2017, 9(2), 80-90.
[98]
Avila, M.A.; Berasain, C.; Sangro, B.; Prieto, J. New therapies for hepatocellular carcinoma. Oncogene, 2006, 25(27), 3866-3884.
[99]
Su, Z.; Liu, G.; Fang, T.; Wang, Y.; Zhang, H.; Yang, S.; Wei, J.; Lv, Z.; Tan, L.; Liu, J. Silencing MRP1-4 genes by RNA interference enhances sensitivity of human hepatoma cells to chemotherapy. Am. J. Transl. Res., 2016, 8(6), 2790-2802.
[100]
Pérez-Tomás, R. Multidrug resistance: retrospect and prospects in anti-cancer drug treatment. Curr. Med. Chem., 2006, 13(16), 1859-1876.
[101]
Chow, A.K-M.; Ng, L.; Lam, C.S-C.; Wong, S.K-M.; Wan, T.M-H.; Cheng, N.S-M.; Yau, T.C.; Poon, R.T.; Pang, R.W. The enhanced metastatic potential of hepatocellular carcinoma (HCC) cells with sorafenib resistance. PLoS One, 2013, 8(11), e78675.
[102]
Sun, Z.; Zhao, Z.; Li, G.; Dong, S.; Huang, Z.; Ye, L.; Liang, H.; Qu, J.; Ai, X.; Zhang, W.; Chen, X. Relevance of two genes in the multidrug resistance of hepatocellular carcinoma: in vivo and clinical studies. Tumori, 2010, 96(1), 90-96.
[103]
Li, G.; Chen, X.; Wang, Q.; Xu, Z.; Zhang, W.; Ye, L. The roles of four multi-drug resistance proteins in hepatocellular carcinoma multidrug resistance. J. Huazhong Univ. Sci. Technolog. Med. Sci., 2007, 27(2), 173-175.
[104]
Hoffmann, K.; Shibo, L.; Xiao, Z.; Longerich, T.; Büchler, M.W.; Schemmer, P. Correlation of gene expression of ATP-binding cassette protein and tyrosine kinase signaling pathway in patients with hepatocellular carcinoma. Anticancer Res., 2011, 31(11), 3883-3890.
[105]
Nies, A.T.; König, J.; Pfannschmidt, M.; Klar, E.; Hofmann, W.J.; Keppler, D. Expression of the multidrug resistance proteins MRP2 and MRP3 in human hepatocellular carcinoma. Int. J. Cancer, 2001, 94(4), 492-499.
[106]
Effendi, K.; Mori, T.; Komuta, M.; Masugi, Y.; Du, W.; Sakamoto, M. Bmi-1 gene is upregulated in early-stage hepatocellular carcinoma and correlates with ATP-binding cassette transporter B1 expression. Cancer Sci., 2010, 101(3), 666-672.
[107]
Bonin, S.; Pascolo, L.; Crocé, L.S.; Stanta, G.; Tiribelli, C. Gene expression of ABC proteins in hepatocellular carcinoma, perineoplastic tissue, and liver diseases. Mol. Med., 2002, 8(6), 318-325.
[108]
Gao, B.; Yang, F-M.; Yu, Z-T.; Li, R.; Xie, F.; Chen, J.; Luo, H.J.; Zhang, J.C. Relationship between the expression of MDR1 in hepatocellular cancer and its biological behaviors. Int. J. Clin. Exp. Pathol., 2015, 8(6), 6995-7001.
[109]
Borel, F.; Han, R.; Visser, A.; Petry, H.; van Deventer, S.J.H.; Jansen, P.L.M.; Konstantinova, P. Adenosine triphosphate-binding cassette transporter genes up-regulation in untreated hepatocellular carcinoma is mediated by cellular microRNAs. Hepatology, 2012, 55(3), 821-832.
[110]
Vander Borght, S.; Komuta, M.; Libbrecht, L.; Katoonizadeh, A.; Aerts, R.; Dymarkowski, S.; Verslype, C.; Nevens, F.; Roskams, T. Expression of multidrug resistance-associated protein 1 in hepatocellular carcinoma is associated with a more aggressive tumour phenotype and may reflect a progenitor cell origin. Liver Int., 2008, 28(10), 1370-1380.
[111]
Wang, B-L.; Chen, X-P.; Zhai, S-P.; Chen, D-F. Clinical significance of mrp gene in primary hepatocellular carcinoma. HBPD INT, 2003, 2(3), 397-403.
[112]
Mizukoshi, E.; Honda, M.; Arai, K.; Yamashita, T.; Nakamoto, Y.; Kaneko, S. Expression of multidrug resistance-associated protein 3 and cytotoxic T cell responses in patients with hepatocellular carcinoma. J. Hepatol., 2008, 49(6), 946-954.
[113]
Carrasco-Torres, G.; Fattel-Fazenda, S.; López-Alvarez, G.S.; García-Román, R.; Villa-Treviño, S.; Vásquez-Garzón, V.R. The transmembrane transporter ABCC3 participates in liver cancer progression and is a potential biomarker. Tumour Biol., 2016, 37(2), 2007-2014.
[114]
Roelofsen, H.; Vos, T.A.; Schippers, I.J.; Kuipers, F.; Koning, H.; Moshage, H.; Jansen, P.L.; Müller, M. Increased levels of the multidrug resistance protein in lateral membranes of proliferating hepatocyte-derived cells. Gastroenterology, 1997, 112(2), 511-521.
[115]
Sukowati, C.H.; Rosso, N.; Pascut, D.; Anfuso, B.; Torre, G.; Francalanci, P.; Crocè, L.S.; Tiribelli, C. Gene and functional up-regulation of the BCRP/ABCG2 transporter in hepatocellular carcinoma. BMC Gastroenterol., 2012, 12(1), 160.
[116]
Chen, Y-L.; Chen, P-M.; Lin, P-Y.; Hsiau, Y-T.; Chu, P-Y. ABCG2 overexpression confers poor outcomes in hepatocellular carcinoma of elderly patients. Anticancer Res., 2016, 36(6), 2983-2988.
[117]
Zekri, A-R.N.; Hassan, Z.K.; Bahnassy, A.A.; Sherif, G.M. ELdahshan, D.; Abouelhoda, M.; Ali, A.; Hafez, M.M. Molecular prognostic profile of Egyptian HCC cases infected with hepatitis C virus. Asian Pac. J. Cancer Prev., 2012, 13(11), 5433-5438.
[118]
Zhou, J.; Cheng, S.C.; Luo, D.; Xie, Y. Study of multi-drug resistant mechanisms in a taxol-resistant hepatocellular carcinoma QGY-TR 50 cell line. Biochem. Biophys. Res. Commun., 2001, 280(5), 1237-1242.
[119]
Kamiyama, N.; Takagi, S.; Yamamoto, C.; Kudo, T.; Nakagawa, T.; Takahashi, M.; Nakanishi, K.; Takahashi, H.; Todo, S.; Iseki, K. Expression of ABC transporters in human hepatocyte carcinoma cells with cross-resistance to epirubicin and mitoxantrone. Anticancer Res., 2006, 26(2A), 885-888.
[120]
Tsang, W.P.; Kwok, T.T. Riboregulator H19 induction of MDR1-associated drug resistance in human hepatocellular carcinoma cells. Oncogene, 2007, 26(33), 4877-4881.
[121]
Ye, C-G.; Yeung, J.H-K.; Huang, G-L.; Cui, P.; Wang, J.; Zou, Y.; Zhang, X.N.; He, Z.W.; Cho, C.H. Increased glutathione and mitogen-activated protein kinase phosphorylation are involved in the induction of doxorubicin resistance in hepatocellular carcinoma cells. Hepatol. Res., 2013, 43(3), 289-299.
[122]
Meena, A.S.; Sharma, A.; Kumari, R.; Mohammad, N.; Singh, S.V.; Bhat, M.K. Inherent and acquired resistance to paclitaxel in hepatocellular carcinoma: Molecular events involved. PLoS One, 2013, 8(4), e61524.
[123]
Wakamatsu, T.; Nakahashi, Y.; Hachimine, D.; Seki, T.; Okazaki, K. The combination of glycyrrhizin and lamivudine can reverse the cisplatin resistance in hepatocellular carcinoma cells through inhibition of multidrug resistance-associated proteins. Int. J. Oncol., 2007, 31(6), 1465-1472.
[124]
Hoffmann, K.; Xiao, Z.; Franz, C.; Mohr, E.; Serba, S.; Büchler, M.W.; Schemmer, P. Involvement of the epidermal growth factor receptor in the modulation of multidrug resistance in human hepatocellular carcinoma cells in vitro. Cancer Cell Int., 2011, 11(1), 40.
[125]
Thomas, M.B.; O’Beirne, J.P.; Furuse, J.; Chan, A.T.C.; Abou-Alfa, G.; Johnson, P. Systemic therapy for hepatocellular carcinoma: cytotoxic chemotherapy, targeted therapy and immunotherapy. Ann. Surg. Oncol., 2008, 15(4), 1008-1014.
[126]
Soini, Y.; Virkajärvi, N.; Raunio, H.; Pääkkö, P. Expression of P-glycoprotein in hepatocellular carcinoma: a potential marker of prognosis. J. Clin. Pathol., 1996, 49(6), 470-473.
[127]
Kato, A.; Miyazaki, M.; Ambiru, S.; Yoshitomi, H.; Ito, H.; Nakagawa, K.; Shimizu, H.; Yokosuka, O.; Nakajima, N. Multidrug resistance gene (MDR-1) expression as a useful prognostic factor in patients with human hepatocellular carcinoma after surgical resection. J. Surg. Oncol., 2001, 78(2), 110-115.
[128]
Bradley, G.; Sharma, R.; Rajalakshmi, S.; Ling, V. P-glycoprotein expression during tumor progression in the rat liver. Cancer Res., 1992, 52(19), 5154-5161.
[129]
Wu, L.; Xu, X.; Shen, J.; Xie, H.; Yu, S.; Liang, T.; Wang, W.; Shen, Y.; Zhang, M.; Zheng, S. MDR1 gene polymorphisms and risk of recurrence in patients with hepatocellular carcinoma after liver transplantation. J. Surg. Oncol., 2007, 96(1), 62-68.
[130]
Zhao, J.; Yu, B-Y.; Wang, D-Y.; Yang, J-E. Promoter polymorphism of MRP1 associated with reduced survival in hepatocellular carcinoma. World J. Gastroenterol., 2010, 16(48), 6104-6110.
[131]
Zen, Y.; Fujii, T.; Yoshikawa, S.; Takamura, H.; Tani, T.; Ohta, T.; Nakanuma, Y. Histological and culture studies with respect to ABCG2 expression support the existence of a cancer cell hierarchy in human hepatocellular carcinoma. Am. J. Pathol., 2007, 170(5), 1750-1762.
[132]
Shi, G-M.; Xu, Y.; Fan, J.; Zhou, J.; Yang, X-R.; Qiu, S-J.; Liao, Y.; Wu, W.Z.; Ji, Y.; Ke, A.W.; Ding, Z.B.; He, Y.Z.; Wu, B.; Yang, G.H.; Qin, W.Z.; Zhang, W.; Zhu, J.; Min, Z.H.; Wu, Z.Q. Identification of side population cells in human hepatocellular carcinoma cell lines with stepwise metastatic potentials. J. Cancer Res. Clin. Oncol., 2008, 134(11), 1155-1163.
[133]
Yang, X-R.; Xu, Y.; Yu, B.; Zhou, J.; Qiu, S-J.; Shi, G-M.; Zhang, B.H.; Wu, W.Z.; Shi, Y.H.; Wu, B.; Yang, G.H.; Ji, Y.; Fan, J. High expression levels of putative hepatic stem/progenitor cell biomarkers related to tumour angiogenesis and poor prognosis of hepatocellular carcinoma. Gut, 2010, 59(7), 953-962.
[134]
Zhang, G.; Wang, Z.; Luo, W.; Jiao, H.; Wu, J.; Jiang, C. Expression of potential cancer stem cell marker ABCG2 is associated with malignant behaviors of hepatocellular carcinoma. Gastroenterol. Res. Pract., 2013, 2013, 782581.
[135]
Huang, W-C.; Hsieh, Y-L.; Hung, C-M.; Chien, P-H.; Chien, Y-F.; Chen, L-C.; Tu, C.Y.; Chen, C.H.; Hsu, S.C.; Lin, Y.M.; Chen, Y.J. BCRP/ABCG2 inhibition sensitizes hepatocellular carcinoma cells to sorafenib. PLoS One, 2013, 8(12), e83627.
[136]
Colombo, F.; Trombetta, E.; Cetrangolo, P.; Maggioni, M.; Razini, P.; De Santis, F.; Torrente, Y.; Prati, D.; Torresani, E.; Porretti, L. Giant lysosomes as a chemotherapy resistance mechanism in hepatocellular carcinoma cells. PLoS One, 2014, 9(12), e114787.
[137]
Rigalli, J.P.; Ciriaci, N.; Arias, A.; Ceballos, M.P.; Villanueva, S.S.M.; Luquita, M.G.M.G.; Mottino, A.D.; Ghanem, C.I.; Catania, V.A.; Ruiz, M.L. Regulation of multidrug resistance proteins by genistein in a hepatocarcinoma cell line: impact on sorafenib cytotoxicity. PLoS One, 2015, 10(3), e0119502.
[138]
Hoffmann, K.; Franz, C.; Xiao, Z.; Mohr, E.; Serba, S.; Büchler, M.W.; Schemmer, P. Sorafenib modulates the gene expression of multi-drug resistance mediating ATP-binding cassette proteins in experimental hepatocellular carcinoma. Anticancer Res., 2010, 30(11), 4503-4508.
[139]
Wu, C-H.; Wu, X.; Zhang, H-W. Inhibition of acquired-resistance hepatocellular carcinoma cell growth by combining sorafenib with phosphoinositide 3-kinase and rat sarcoma inhibitor. J. Surg. Res., 2016, 206(2), 371-379.
[140]
Tomonari, T.; Takeishi, S.; Taniguchi, T.; Tanaka, T.; Tanaka, H.; Fujimoto, S.; Kimura, T.; Okamoto, K.; Miyamoto, H.; Muguruma, N.; Takayama, T. MRP3 as a novel resistance factor for sorafenib in hepatocellular carcinoma. Oncotarget, 2016, 7(6), 7207-7215.
[141]
Wang, H.; Qian, Z.; Zhao, H.; Zhang, X.; Che, S.; Zhang, H.; Shang, H.; Bao, J.; Hao, C.; Liu, J.; Li, Z. CSN5 silencing reverses sorafenib resistance of human hepatocellular carcinoma HepG2 cells. Mol. Med. Rep., 2015, 12(3), 3902-3908.
[142]
Liang, Y.; Zheng, T.; Song, R.; Wang, J.; Yin, D.; Wang, L.; Liu, H.; Tian, L.; Fang, X.; Meng, X.; Jiang, H.; Liu, J.; Liu, L. Hypoxia-mediated sorafenib resistance can be overcome by EF24 through Von Hippel-Lindau tumor suppressor-dependent HIF-1α inhibition in hepatocellular carcinoma. Hepatology, 2013, 57(5), 1847-1857.
[143]
Jemal, A.; Bray, F.; Center, M.M.; Ferlay, J.; Ward, E.; Forman, D. Global cancer statistics. CA Cancer J. Clin., 2011, 61(2), 69-90.
[144]
Siegel, R.L.; Miller, K.D.; Fedewa, S.A.; Ahnen, D.J.; Meester, R.G.S.; Barzi, A.; Jemal, A. Colorectal cancer statistics, 2017. CA Cancer J. Clin., 2017, 67(3), 177-193.
[145]
Mandel, J.S. Screening for colorectal cancer. Gastroenterol. Clin. North Am., 2008, 37(1), 97-115. vii [vii.].
[146]
DeSantis, C.E.; Lin, C.C.; Mariotto, A.B.; Siegel, R.L.; Stein, K.D.; Kramer, J.L.; Alteri, R.; Robbins, A.S.; Jemal, A. Cancer treatment and survivorship statistics, 2014. CA Cancer J. Clin., 2014, 64(4), 252-271.
[147]
Kwak, E.L.; Chung, D.C. Hereditary colorectal cancer syndromes: An overview. Clin. Colorectal Cancer, 2007, 6(5), 340-344.
[148]
Lynch, H.T.; de la Chapelle, A.; Lynch, H.T.; de la Chapelle, A. Hereditary colorectal cancer. N. Engl. J. Med., 2003, 348(10), 919-932.
[149]
Brannon, A.R.; Vakiani, E.; Sylvester, B.E.; Scott, S.N.; McDermott, G.; Shah, R.H.; Kania, K.; Viale, A.; Oschwald, D.M.; Vacic, V.; Emde, A.K.; Cercek, A.; Yaeger, R.; Kemeny, N.E.; Saltz, L.B.; Shia, J.; D’Angelica, M.I.; Weiser, M.R.; Solit, D.B.; Berger, M.F. Comparative sequencing analysis reveals high genomic concordance between matched primary and metastatic colorectal cancer lesions. Genome Biol., 2014, 15(8), 454.
[150]
Cheung, A.F.; Carter, A.M.; Kostova, K.K.; Woodruff, J.F.; Crowley, D.; Bronson, R.T.; Haigis, K.M.; Jacks, T. Complete deletion of Apc results in severe polyposis in mice. Oncogene, 2010, 29(12), 1857-1864.
[151]
Su, L.K.; Kinzler, K.W.; Vogelstein, B.; Preisinger, A.C.; Moser, A.R.; Luongo, C.; Gould, K.A.; Dove, W.F. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science, 1992, 256(5057), 668-670.
[152]
Sansom, O.J.; Reed, K.R.; Hayes, A.J.; Ireland, H.; Brinkmann, H.; Newton, I.P.; Batlle, E.; Simon-Assmann, P.; Clevers, H.; Nathke, I.S.; Clarke, A.R.; Winton, D.J. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev., 2004, 18(12), 1385-1390.
[153]
Dow, L.E.; O’Rourke, K.P.; Simon, J.; Tschaharganeh, D.F.; van Es, J.H.; Clevers, H.; Lowe, S.W. Apc restoration promotes cellular differentiation and reestablishes Crypt homeostasis in colorectal cancer. Cell, 2015, 161(7), 1539-1552.
[154]
Colnot, S.; Niwa-Kawakita, M.; Hamard, G.; Godard, C.; Le Plenier, S.; Houbron, C.; Romagnolo, B.; Berrebi, D.; Giovannini, M.; Perret, C. Colorectal cancers in a new mouse model of familial adenomatous polyposis: influence of genetic and environmental modifiers. Lab. Invest., 2004, 84(12), 1619-1630.
[155]
Mirvish, S.S. Role of N-nitroso compounds (NOC) and N-nitrosation in etiology of gastric, esophageal, nasopharyngeal and bladder cancer and contribution to cancer of known exposures to NOC. Cancer Lett., 1995, 93(1), 17-48.
[156]
Cross, A.J.; Sinha, R. Meat-related mutagens/carcinogens in the etiology of colorectal cancer. Environ. Mol. Mutagen., 2004, 44(1), 44-55.
[157]
Stavric, B. Biological significance of trace levels of mutagenic heterocyclic aromatic amines in human diet: A critical review. Food Chem. Toxicol., 1994, 32(10), 977-994.
[158]
Layton, D.W.; Bogen, K.T.; Knize, M.G.; Hatch, F.T.; Johnson, V.M.; Felton, J.S. Cancer risk of heterocyclic amines in cooked foods: an analysis and implications for research. Carcinogenesis, 1995, 16(1), 39-52.
[159]
Dietrich, C.G.; de Waart, D.R.; Ottenhoff, R.; Bootsma, A.H.; van Gennip, A.H.; Elferink, R.P. Mrp2-deficiency in the rat impairs biliary and intestinal excretion and influences metabolism and disposition of the food-derived carcinogen 2-amino-1-methyl-6-phenylimidazo. Carcinogenesis, 2001, 22(5), 805-811.
[160]
van Herwaarden, A.E.; Jonker, J.W.; Wagenaar, E.; Brinkhuis, R.F.; Schellens, J.H.M.; Beijnen, J.H.; Schinkel, A.H. The breast cancer resistance protein (Bcrp1/Abcg2) restricts exposure to the dietary carcinogen 2-amino-1-methyl-6-phenylimidazo [4,5-b]pyridine. Cancer Res., 2003, 63(19), 6447-6452.
[161]
Hong, Y-J.; Yang, S-Y.; Nam, M-H.; Koo, Y.C.; Lee, K-W. Caffeic acid inhibits the uptake of 2-amino-1-methyl-6-phenylimidazo [4,5-b]pyridine (PhIP) by inducing the efflux transporters expression in Caco-2 cells. Biol. Pharm. Bull., 2015, 38(2), 201-207.
[162]
Mouradov, D.; Sloggett, C.; Jorissen, R.N.; Love, C.G.; Li, S.; Burgess, A.W.; Arango, D.; Strausberg, R.L.; Buchanan, D.; Wormald, S.; O’Connor, L.; Wilding, J.L.; Bicknell, D.; Tomlinson, I.P.; Bodmer, W.F.; Mariadason, J.M.; Sieber, O.M. Colorectal cancer cell lines are representative models of the main molecular subtypes of primary cancer. Cancer Res., 2014, 74(12), 3238-3247.
[163]
Barretina, J.; Caponigro, G.; Stransky, N.; Venkatesan, K.; Margolin, A.A.; Kim, S.; Wilson, C.J.; Lehár, J.; Kryukov, G.V.; Sonkin, D.; Reddy, A.; Liu, M.; Murray, L.; Berger, M.F.; Monahan, J.E.; Morais, P.; Meltzer, J.; Korejwa, A.; Jané-Valbuena, J.; Mapa, F.A.; Thibault, J.; Bric-Furlong, E.; Raman, P.; Shipway, A.; Engels, I.H.; Cheng, J.; Yu, G.K.; Yu, J.; Aspesi, P., Jr; de Silva, M.; Jagtap, K.; Jones, M.D.; Wang, L.; Hatton, C.; Palescandolo, E.; Gupta, S.; Mahan, S.; Sougnez, C.; Onofrio, R.C.; Liefeld, T.; MacConaill, L.; Winckler, W.; Reich, M.; Li, N.; Mesirov, J.P.; Gabriel, S.B.; Getz, G.; Ardlie, K.; Chan, V.; Myer, V.E.; Weber, B.L.; Porter, J.; Warmuth, M.; Finan, P.; Harris, J.L.; Meyerson, M.; Golub, T.R.; Morrissey, M.P.; Sellers, W.R.; Schlegel, R.; Garraway, L.A. The cancer cell line encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature, 2012, 483(7391), 603-607.
[164]
Cunningham, D.; Atkin, W.; Lenz, H-J.; Lynch, H.T.; Minsky, B.; Nordlinger, B.; Starling, N. Colorectal cancer. Lancet, 2010, 375(9719), 1030-1047.
[165]
Kozovska, Z.; Gabrisova, V.; Kucerova, L. Colon cancer: cancer stem cells markers, drug resistance and treatment. Biomed. Pharmacother., 2014, 68(8), 911-916.
[166]
Ychou, M.; Rivoire, M.; Thezenas, S.; Quenet, F.; Delpero, J-R.; Rebischung, C.; Letoublon, C.; Guimbaud, R.; Francois, E.; Ducreux, M.; Desseigne, F.; Fabre, J.M.; Assenat, E. A randomized phase II trial of three intensified chemotherapy regimens in first-line treatment of colorectal cancer patients with initially unresectable or not optimally resectable liver metastases. The METHEP trial. Ann. Surg. Oncol., 2013, 20(13), 4289-4297.
[167]
Glavinas, H.; Krajcsi, P.; Cserepes, J.; Sarkadi, B. The role of ABC transporters in drug resistance, metabolism and toxicity. Curr. Drug Deliv., 2004, 1(1), 27-42.
[168]
Fojo, A.T.; Ueda, K.; Slamon, D.J.; Poplack, D.G.; Gottesman, M.M.; Pastan, I. Expression of a multidrug-resistance gene in human tumors and tissues. Proc. Natl. Acad. Sci. USA, 1987, 84(1), 265-269.
[169]
Meschini, S.; Calcabrini, A.; Monti, E.; Del Bufalo, D.; Stringaro, A.; Dolfini, E.; Arancia, G. Intracellular P-glycoprotein expression is associated with the intrinsic multidrug resistance phenotype in human colon adenocarcinoma cells. Int. J. Cancer, 2000, 87(5), 615-628.
[170]
Spoelstra, E.C.; Dekker, H.; Schuurhuis, G.J.; Broxterman, H.J.; Lankelma, J. P-glycoprotein drug efflux pump involved in the mechanisms of intrinsic drug resistance in various colon cancer cell lines. Evidence for a saturation of active daunorubicin transport. Biochem. Pharmacol., 1991, 41(3), 349-359.
[171]
Polgar, O.; Bates, S.E. ABC transporters in the balance: is there a role in multidrug resistance? Biochem. Soc. Trans., 2005, 33(Pt 1), 241-245.
[172]
Andersen, V.; Svenningsen, K.; Knudsen, L.A.; Hansen, A.K.; Holmskov, U.; Stensballe, A.; Vogel, U. Novel understanding of ABC transporters ABCB1/MDR/P-glycoprotein, ABCC2/MRP2, and ABCG2/BCRP in colorectal pathophysiology. World J. Gastroenterol., 2015, 21(41), 11862-11876.
[173]
Johnson, R.L.; Fleet, J.C. Animal models of colorectal cancer. Cancer Metastasis Rev., 2013, 32(1-2), 39-61.
[174]
Dietrich, C.G.; Vehr, A-K.; Martin, I.V.; Gassler, N.; Rath, T.; Roeb, E.; Schmitt, J.; Trautwein, C.; Geier, A. Downregulation of breast cancer resistance protein in colon adenomas reduces cellular xenobiotic resistance and leads to accumulation of a food-derived carcinogen. Int. J. Cancer, 2011, 129(3), 546-552.
[175]
Hinoshita, E.; Uchiumi, T.; Taguchi, K.; Kinukawa, N.; Tsuneyoshi, M.; Maehara, Y.; Sugimachi, K.; Kuwano, M. Increased expression of an ATP-binding cassette superfamily transporter, multidrug resistance protein 2, in human colorectal carcinomas. Clin. Cancer Res., 2000, 6(6), 2401-2407.
[176]
Nakamura, T.; Sakaeda, T.; Ohmoto, N.; Tamura, T.; Aoyama, N.; Shirakawa, T.; Kamigaki, T.; Nakamura, T.; Kim, K.I.; Kim, S.R.; Kuroda, Y.; Matsuo, M.; Kasuga, M.; Okumura, K. Real-time quantitative polymerase chain reaction for MDR1, MRP1, MRP2, and CYP3A-mRNA levels in Caco-2 cell lines, human duodenal enterocytes, normal colorectal tissues, and colorectal adenocarcinomas. Drug Metab. Dispos., 2002, 30(1), 4-6.
[177]
Micsik, T.; Lőrincz, A.; Mersich, T.; Baranyai, Z.; Besznyák, I., Jr; Dede, K.; Zaránd, A.; Jakab, F.; Szöllösi, L.K.; Kéri, G.; Schwab, R.; Peták, I. Decreased functional activity of multidrug resistance protein in primary colorectal cancer. Diagn. Pathol., 2015, 10(1), 26.
[178]
Hlavata, I.; Mohelnikova-Duchonova, B.; Vaclavikova, R.; Liska, V.; Pitule, P.; Novak, P.; Bruha, J.; Vycital, O.; Holubec, L.; Treska, V.; Vodicka, P.; Soucek, P. The role of ABC transporters in progression and clinical outcome of colorectal cancer. Mutagenesis, 2012, 27(2), 187-196.
[179]
Potocnik, U.; Ravnik-Glavac, M.; Golouh, R.; Glavac, D. Naturally occurring mutations and functional polymorphisms in multidrug resistance 1 gene: correlation with microsatellite instability and lymphoid infiltration in colorectal cancers. J. Med. Genet., 2002, 39(5), 340-346.
[180]
van den Heuvel-Eibrink, M.M.; Sonneveld, P.; Pieters, R. The prognostic significance of membrane transport-associated multidrug resistance (MDR) proteins in leukemia. Int. J. Clin. Pharmacol. Ther., 2000, 38(3), 94-110.
[181]
Chan, H.S.; Haddad, G.; Thorner, P.S.; DeBoer, G.; Lin, Y.P.; Ondrusek, N.; Yeger, H.; Ling, V. P-glycoprotein expression as a predictor of the outcome of therapy for neuroblastoma. N. Engl. J. Med., 1991, 325(23), 1608-1614.
[182]
Weinstein, R.S.; Jakate, S.M.; Dominguez, J.M.; Lebovitz, M.D.; Koukoulis, G.K.; Kuszak, J.R.; Klusens, L.F.; Grogan, T.M.; Saclarides, T.J.; Roninson, I.B. Relationship of the expression of the multidrug resistance gene product (P-glycoprotein) in human colon carcinoma to local tumor aggressiveness and lymph node metastasis. Cancer Res., 1991, 51(10), 2720-2726.
[183]
Mochida, Y.; Taguchi, K.; Taniguchi, S.; Tsuneyoshi, M.; Kuwano, H.; Tsuzuki, T.; Kuwano, M.; Wada, M. The role of P-glycoprotein in intestinal tumorigenesis: disruption of mdr1a suppresses polyp formation in Apc(Min/+) mice. Carcinogenesis, 2003, 24(7), 1219-1224.
[184]
Pirker, R.; Wallner, J.; Gsur, A.; Götzl, M.; Zöchbauer, S.; Scheithauer, W.; Depisch, D. MDR1 gene expression in primary colorectal carcinomas. Br. J. Cancer, 1993, 68(4), 691-694.
[185]
Burger, H.; van Tol, H.; Brok, M.; Wiemer, E.A.; de Bruijn, E.A.; Guetens, G.; de Boeck, G.; Sparreboom, A.; Verweij, J.; Nooter, K. Chronic imatinib mesylate exposure leads to reduced intracellular drug accumulation by induction of the ABCG2 (BCRP) and ABCB1 (MDR1) drug transport pumps. Cancer Biol. Ther., 2005, 4(7), 747-752.
[186]
Harmsen, S.; Meijerman, I.; Febus, C.L.; Maas-Bakker, R.F.; Beijnen, J.H.; Schellens, J.H.M. PXR-mediated induction of P-glycoprotein by anticancer drugs in a human colon adenocarcinoma-derived cell line. Cancer Chemother. Pharmacol., 2010, 66(4), 765-771.
[187]
Kota, B.P.; Allen, J.D.; Roufogalis, B.D. The effect of vitamin D3 and ketoconazole combination on VDR-mediated P-gp expression and function in human colon adenocarcinoma cells: implications in drug disposition and resistance. Basic Clin. Pharmacol. Toxicol., 2011, 109(2), 97-102.
[188]
Singh, B.; Kumar, A.; Joshi, P.; Guru, S.K.; Kumar, S.; Wani, Z.A.; Mahajan, G.; Hussain, A.; Qazi, A.K.; Kumar, A.; Bharate, S.S.; Gupta, B.D.; Sharma, P.R.; Hamid, A.; Saxena, A.K.; Mondhe, D.M.; Bhushan, S.; Bharate, S.B.; Vishwakarma, R.A. Colchicine derivatives with potent anticancer activity and reduced P-glycoprotein induction liability. Org. Biomol. Chem., 2015, 13(20), 5674-5689.
[189]
Doyle, L.A.; Yang, W.; Abruzzo, L.V.; Krogmann, T.; Gao, Y.; Rishi, A.K.; Ross, D.D. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc. Natl. Acad. Sci. USA, 1998, 95(26), 15665-15670.
[190]
Volk, E.L.; Rohde, K.; Rhee, M.; McGuire, J.J.; Doyle, L.A.; Ross, D.D.; Schneider, E. Methotrexate cross-resistance in a mitoxantrone-selected multidrug-resistant MCF7 breast cancer cell line is attributable to enhanced energy-dependent drug efflux. Cancer Res., 2000, 60(13), 3514-3521.
[191]
Litman, T.; Brangi, M.; Hudson, E.; Fetsch, P.; Abati, A.; Ross, D.D.; Miyake, K.; Resau, J.H.; Bates, S.E. The multidrug-resistant phenotype associated with overexpression of the new ABC half-transporter, MXR (ABCG2). J. Cell Sci., 2000, 113(Pt 11), 2011-2021.
[192]
Miyake, K.; Mickley, L.; Litman, T.; Zhan, Z.; Robey, R.; Cristensen, B.; Brangi, M.; Greenberger, L.; Dean, M.; Fojo, T.; Bates, S.E. Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: demonstration of homology to ABC transport genes. Cancer Res., 1999, 59(1), 8-13.
[193]
Ross, D.D.; Yang, W.; Abruzzo, L.V.; Dalton, W.S.; Schneider, E.; Lage, H.; Dietel, M.; Greenberger, L.; Cole, S.P.; Doyle, L.A. Atypical multidrug resistance: Breast cancer resistance protein messenger RNA expression in mitoxantrone-selected cell lines. J. Natl. Cancer Inst., 1999, 91(5), 429-433.
[194]
Hsiang, Y.H.; Hertzberg, R.; Hecht, S.; Liu, L.F. Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I. J. Biol. Chem., 1985, 260(27), 14873-14878.
[195]
Pommier, Y. Topoisomerase I inhibitors: Camptothecins and beyond. Nat. Rev. Cancer, 2006, 6(10), 789-802.
[196]
Candeil, L.; Gourdier, I.; Peyron, D.; Vezzio, N.; Copois, V.; Bibeau, F.; Orsetti, B.; Scheffer, G.L.; Ychou, M.; Khan, Q.A.; Pommier, Y.; Pau, B.; Martineau, P.; Del Rio, M. ABCG2 overexpression in colon cancer cells resistant to SN38 and in irinotecan-treated metastases. Int. J. Cancer, 2004, 109(6), 848-854.
[197]
Xie, Z-Y.; Lv, K.; Xiong, Y.; Guo, W-H. ABCG2-meditated multidrug resistance and tumor-initiating capacity of side population cells from colon cancer. Oncol. Res. Treat., 2014, 37(11), 666-668, 670-672.
[198]
Bai, X.; Chen, Y.; Hou, X.; Huang, M.; Jin, J. Emerging role of NRF2 in chemoresistance by regulating drug-metabolizing enzymes and efflux transporters. Drug Metab. Rev., 2016, 48(4), 541-567.
[199]
Jeddi, F.; Soozangar, N.; Sadeghi, M.R.; Somi, M.H.; Samadi, N. Contradictory roles of Nrf2/Keap1 signaling pathway in cancer prevention/promotion and chemoresistance. DNA Repair (Amst.), 2017, 54, 13-21.
[200]
Taguchi, K.; Motohashi, H.; Yamamoto, M. Molecular mechanisms of the Keap1–Nrf2 pathway in stress response and cancer evolution. Genes Cells, 2011, 16(2), 123-140.
[201]
Choi, B.H.; Ryoo, I.G.; Kang, H.C.; Kwak, M-K. The sensitivity of cancer cells to pheophorbide a-based photodynamic therapy is enhanced by Nrf2 silencing. PLoS One, 2014, 9(9), e107158.
[202]
Arias, A.; Rigalli, J.P.; Villanueva, S.S.M.; Ruiz, M.L.; Luquita, M.G.; Perdomo, V.G.V.G.; Vore, M.; Catania, V.A.; Mottino, A.D. Regulation of expression and activity of multidrug resistance proteins MRP2 and MDR1 by estrogenic compounds in Caco-2 cells. Role in prevention of xenobiotic-induced cytotoxicity. Toxicology, 2014, 320(1), 46-55.
[203]
Liu, Z.; Qiu, M.; Tang, Q-L.; Liu, M.; Lang, N.; Bi, F. Establishment and biological characteristics of oxaliplatin-resistant human colon cancer cell lines. Chin. J. Cancer, 2010, 29(7), 661-667.
[204]
Tan, B.; Piwnica-Worms, D.; Ratner, L. Multidrug resistance transporters and modulation. Curr. Opin. Oncol., 2000, 12(5), 450-458.
[205]
Thomas, H.; Coley, H.M. Overcoming multidrug resistance in cancer: an update on the clinical strategy of inhibiting p-glycoprotein. Cancer Contr., 2003, 10(2), 159-165.
[206]
Twentyman, P.R.; Bleehen, N.M. Resistance modification by PSC-833, a novel non-immunosuppressive cyclosporin. Eur. J. Cancer, 1991, 27(12), 1639-1642.
[207]
te Boekhorst, P.A.; van Kapel, J.; Schoester, M.; Sonneveld, P. Reversal of typical multidrug resistance by cyclosporin and its non-immunosuppressive analogue SDZ PSC 833 in Chinese hamster ovary cells expressing the mdr1 phenotype. Cancer Chemother. Pharmacol., 1992, 30(3), 238-242.
[208]
Krishna, R.; Mayer, L.D. Multidrug resistance (MDR) in cancer. Mechanisms, reversal using modulators of MDR and the role of MDR modulators in influencing the pharmacokinetics of anticancer drugs. Eur. J. Pharm. Sci., 2000, 11(4), 265-283.
[209]
Bates, S.E.; Bakke, S.; Kang, M.; Robey, R.W.; Zhai, S.; Thambi, P.; Chen, C.C.; Patil, S.; Smith, T.; Steinberg, S.M.; Merino, M.; Goldspiel, B.; Meadows, B.; Stein, W.D.; Choyke, P.; Balis, F.; Figg, W.D.; Fojo, T. A phase I/II study of infusional vinblastine with the P-glycoprotein antagonist valspodar (PSC 833) in renal cell carcinoma. Clin. Cancer Res., 2004, 10(14), 4724-4733.
[210]
Wandel, C.; Kim, R.B.; Kajiji, S.; Guengerich, P.; Wilkinson, G.R.; Wood, A.J. P-glycoprotein and cytochrome P-450 3A inhibition: Dissociation of inhibitory potencies. Cancer Res., 1999, 59(16), 3944-3948.
[211]
Mistry, P.; Stewart, A.J.; Dangerfield, W.; Okiji, S.; Liddle, C.; Bootle, D.; Plumb, J.A.; Templeton, D.; Charlton, P. In vitro and in vivo reversal of P-glycoprotein-mediated multidrug resistance by a novel potent modulator, XR9576. Cancer Res., 2001, 61(2), 749-758.
[212]
Abraham, J.; Edgerly, M.; Wilson, R.; Chen, C.; Rutt, A.; Bakke, S.; Robey, R.; Dwyer, A.; Goldspiel, B.; Balis, F.; Van Tellingen, O.; Bates, S.E.; Fojo, T. A phase I study of the P-glycoprotein antagonist tariquidar in combination with vinorelbine. Clin. Cancer Res., 2009, 15(10), 3574-3582.
[213]
Coley, H.M. Overcoming multidrug resistance in cancer: Clinical studies of P-glycoprotein inhibitors. Methods Mol. Biol., 2010, 596, 341-358.
[214]
Takács, D.; Csonka, Á.; Horváth, Á.; Windt, T.; Gajdács, M.; Riedl, Z.; Hajós, G.; Amaral, L.; Molnár, J.; Spengler, G. Reversal of ABCB1-related multidrug resistance of colonic adenocarcinoma cells by phenothiazines. Anticancer Res., 2015, 35(6), 3245-3251.
[215]
Bartolini, G.; Orlandi, M.; Papi, A.; Ammar, K.; Guerra, F.; Ferreri, A.M.; Rocchi, P. A search for multidrug resistance modulators: The effects of retinoids in human colon carcinoma cells. In Vivo, 2006, 20(6A), 729-733.
[216]
Perego, P.; De Cesare, M.; De Isabella, P.; Carenini, N.; Beggiolin, G.; Pezzoni, G.; Palumbo, M.; Tartaglia, L.; Pratesi, G.; Pisano, C.; Carminati, P.; Scheffer, G.L.; Zunino, F. A novel 7-modified camptothecin analog overcomes breast cancer resistance protein-associated resistance in a mitoxantrone-selected colon carcinoma cell line. Cancer Res., 2001, 61(16), 6034-6037.
[217]
Hasanabady, M.H.; Kalalinia, F. ABCG2 inhibition as a therapeutic approach for overcoming multidrug resistance in cancer. J. Biosci., 2016, 41(2), 313-324.
[218]
Shukla, S.; Wu, C-P.; Ambudkar, S.V. Development of inhibitors of ATP-binding cassette drug transporters: present status and challenges. Expert Opin. Drug Metab. Toxicol., 2008, 4(2), 205-223.
[219]
Yokooji, T.; Murakami, T.; Yumoto, R.; Nagai, J.; Takano, M. Site-specific bidirectional efflux of 2,4-dinitrophenyl-S-glutathione, a substrate of multidrug resistance-associated proteins, in rat intestine and Caco-2 cells. J. Pharm. Pharmacol., 2007, 59(4), 513-520.
[220]
Abrahamse, S.L.; Rechkemmer, G. Identification of an organic anion transport system in the human colon carcinoma cell line HT29 clone 19A. Pflugers Arch., 2001, 441(4), 529-537.
[221]
Wissel, G.; Deng, F.; Kudryavtsev, P.; Ghemtio, L.; Wipf, P.; Xhaard, H.; Kidron, H. A structure-activity relationship study of ABCC2 inhibitors. Eur. J. Pharm. Sci., 2017, 103, 60-69.
[222]
Choi, Y.H.; Yu, A-M. ABC transporters in multidrug resistance and pharmacokinetics, and strategies for drug development. Curr. Pharm. Des., 2014, 20(5), 793-807.
[223]
Kathawala, R.J.; Gupta, P.; Ashby, C.R., Jr; Chen, Z-S. The modulation of ABC transporter-mediated multidrug resistance in cancer: A review of the past decade. Drug Resist. Updat., 2015, 18, 1-17.
[224]
Li, W.; Zhang, H.; Assaraf, Y.G.; Zhao, K.; Xu, X.; Xie, J.; Yang, D.H.; Chen, Z.S. Overcoming ABC transporter-mediated multidrug resistance: Molecular mechanisms and novel therapeutic drug strategies. Drug Resist. Updat., 2016, 27, 14-29.
[225]
Sun, J.; Yeung, C.A.; Co, N.N.; Tsang, T.Y.; Yau, E.; Luo, K.; Wu, P.; Wa, J.C.; Fung, K.P.; Kwok, T.T.; Liu, F. Clitocine reversal of P-glycoprotein associated multi-drug resistance through down-regulation of transcription factor NF-κB in R-HepG2 cell line. PLoS One, 2012, 7(8), e40720.
[226]
Sun, L.; Chen, W.; Qu, L.; Wu, J.; Si, J. Icaritin reverses multidrug resistance of HepG2/ADR human hepatoma cells via downregulation of MDR1 and Pglycoprotein expression. Mol. Med. Rep., 2013, 8(6), 1883-1887.
[227]
Yuan, F.; Liu, J.; Qiao, T.; Li, T.; Shen, Q.; Peng, F. The effects and mechanisms of periplaneta americana extract reversal of multi-drug resistance in BEL-7402/5-FU Cells. Molecules, 2016, 21(7), 852.
[228]
Wang, H.; Zhai, Z.; Li, N.; Jin, H.; Chen, J.; Yuan, S.; Wang, L.; Zhang, J.; Li, Y.; Yun, J.; Fan, J.; Yi, J.; Ling, R. Steroidal saponin of Trillium tschonoskii. Reverses multidrug resistance of hepatocellular carcinoma. Phytomedicine, 2013, 20(11), 985-991.
[229]
Wang, X-B.; Wang, S-S.; Zhang, Q-F.; Liu, M.; Li, H-L.; Liu, Y.; Wang, J.N.; Zheng, F.; Guo, L.Y.; Xiang, J.Z. Inhibition of tetramethylpyrazine on P-gp, MRP2, MRP3 and MRP5 in multidrug resistant human hepatocellular carcinoma cells. Oncol. Rep., 2010, 23(1), 211-215.
[230]
Wang, P-P.; Xu, D-J.; Huang, C.; Wang, W-P.; Xu, W-K. Astragaloside IV reduces the expression level of P-glycoprotein in multidrug-resistant human hepatic cancer cell lines. Mol. Med. Rep., 2014, 9(6), 2131-2137.
[231]
Chaudhary, H.; Jena, P.K.; Seshadri, S. Evaluation of hydro-alcoholic extract of Eclipta alba for its multidrug resistance reversal potential: an in vitro study. Nutr. Cancer, 2013, 65(5), 775-780.
[232]
Huang, C.; Xu, D.; Xia, Q.; Wang, P.; Rong, C.; Su, Y. Reversal of P-glycoprotein-mediated multidrug resistance of human hepatic cancer cells by Astragaloside II. J. Pharm. Pharmacol., 2012, 64(12), 1741-1750.
[233]
Tian, Q.E.; De Li, H.; Yan, M.; Cai, H-L.; Tan, Q-Y.; Zhang, W-Y. Effects of Astragalus polysaccharides on P-glycoprotein efflux pump function and protein expression in H22 hepatoma cells in vitro. BMC Complement. Altern. Med., 2012, 12(1), 94.
[234]
Hyuga, S.; Shiraishi, M.; Hori, A.; Hyuga, M.; Hanawa, T. Effects of Kampo medicines on MDR-1-mediated multidrug resistance in human hepatocellular carcinoma HuH-7/PTX cells. Biol. Pharm. Bull., 2012, 35(10), 1729-1739.
[235]
Li, S-L.; Huang, Z-N.; Hsieh, H-H.; Yu, W-C.; Tzeng, W-Y.; Lee, G-Y.; Chen, Y.P.; Chang, C.Y.; Chuu, J.J. The augmented anti-tumor effects of Antrodia camphorata co-fermented with Chinese medicinal herb in human hepatoma cells. Am. J. Chin. Med., 2009, 37(4), 771-783.
[236]
Chang, C-Y.; Huang, Z-N.; Yu, H-H.; Chang, L-H.; Li, S-L.; Chen, Y-P.; Lee, K.Y.; Chuu, J.J. The adjuvant effects of Antrodia Camphorata extracts combined with anti-tumor agents on multidrug resistant human hepatoma cells. J. Ethnopharmacol., 2008, 118(3), 387-395.
[237]
Jia, H.; Yang, Q.; Wang, T.; Cao, Y.; Jiang, Q.Y.; Ma, H.D.; Sun, H.W.; Hou, M.X.; Yang, Y.P.; Feng, F. Rhamnetin induces sensitization of hepatocellular carcinoma cells to a small molecular kinase inhibitor or chemotherapeutic agents. Biochim. Biophys. Acta, 2016, 1860(7), 1417-1430.
[238]
Li, M.; Zhang, L.; Ge, C.; Chen, L.; Fang, T.; Li, H.; Tian, H.; Liu, J.; Chen, T.; Jiang, G.; Xie, H.; Cui, Y.; Yao, M.; Li, J. An isocorydine derivative (d-ICD) inhibits drug resistance by downregulating IGF2BP3 expression in hepatocellular carcinoma. Oncotarget, 2015, 6(28), 25149-25160.
[239]
Gu, W.; Liu, L.; Fang, F-F.; Huang, F.; Cheng, B-B.; Li, B. Reversal effect of bufalin on multidrug resistance in human hepatocellular carcinoma BEL-7402/5-FU cells. Oncol. Rep., 2014, 31(1), 216-222.
[240]
Qian, J-Q.; Sun, P.; Pan, Z-Y.; Fang, Z-Z. Annonaceous acetogenins reverses drug resistance of human hepatocellular carcinoma BEL-7402/5-FU and HepG2/ADM cell lines. Int. J. Clin. Exp. Pathol., 2015, 8(9), 11934-11944.
[241]
Huang, H.Y.; Niu, J.L.; Zhao, L.M.; Lu, Y.H. Reversal effect of 2′,4′-dihydroxy-6′-methoxy-3′,5′-dimethylchalcone on multi-drug resistance in resistant human hepatocellular carcinoma cell line BEL-7402/5-FU. Phytomedicine, 2011, 18(12), 1086-1092.
[242]
Nishanth, R.P.; Ramakrishna, B.S.; Jyotsna, R.G.; Roy, K.R.; Reddy, G.V.; Reddy, P.K.; Reddanna, P. C-Phycocyanin inhibits MDR1 through reactive oxygen species and cyclooxygenase-2 mediated pathways in human hepatocellular carcinoma cell line. Eur. J. Pharmacol., 2010, 649(1-3), 74-83.
[243]
Sun, B.T.; Zheng, L.H.; Bao, Y.L.; Yu, C.L.; Wu, Y.; Meng, X.Y.; Li, Y.X. Reversal effect of Dioscin on multidrug resistance in human hepatoma HepG2/adriamycin cells. Eur. J. Pharmacol., 2011, 654(2), 129-134.
[244]
Wen, Y.; Zhao, R-Q.; Zhang, Y-K.; Gupta, P.; Fu, L-X.; Tang, A-Z.; Liu, B.M.; Chen, Z.S.; Yang, D.H.; Liang, G. Effect of Y6, an epigallocatechin gallate derivative, on reversing doxorubicin drug resistance in human hepatocellular carcinoma cells. Oncotarget, 2017, 8(18), 29760-29770.
[245]
Yue, G.G-L.; Kin-Ming Lee, J.; Cheng, L.; Chung-Lap Chan, B.; Jiang, L.; Fung, K-P.; Leung, P.C.; Bik-San Lau, C. Reversal of P-glycoprotein-mediated multidrug resistance in human hepatoma cells by hedyotiscone A, a compound isolated from Hedyotis corymbosa. Xenobiotica, 2012, 42(6), 562-570.
[246]
Zheng, L.H.; Bao, Y.L.; Wu, Y.; Yu, C.L.; Meng, X.; Li, Y.X. Cantharidin reverses multidrug resistance of human hepatoma HepG2/ADM cells via down-regulation of P-glycoprotein expression. Cancer Lett., 2008, 272(1), 102-109.
[247]
Zhu, J.; Wang, R.; Lou, L.; Li, W.; Tang, G.; Bu, X.; Yin, S. Jatrophane diterpenoids as modulators of p-glycoprotein-dependent Multidrug Resistance (MDR): Advances of structure-activity relationships and discovery of promising MDR reversal agents. J. Med. Chem., 2016, 59(13), 6353-6369.
[248]
Liu, D-L.; Li, Y-J.; Yang, D-H.; Wang, C-R.; Xu, J.; Yao, N.; Zhang, X.Q.; Chen, Z.S.; Ye, W.C.; Zhang, D.M. Ganoderma lucidum derived ganoderenic acid B reverses ABCB1-mediated multidrug resistance in HepG2/ADM cells. Int. J. Oncol., 2015, 46(5), 2029-2038.
[249]
Jin, Y-D.; Ren, Y.; Wu, M-W.; Chen, P.; Lu, J. Effect of shikonin on multidrug resistance in HepG2: The role of SIRT1. Pharm. Biol., 2015, 53(7), 1016-1021.
[250]
Chen, H-C.; Jeng, Y-M.; Yuan, R-H.; Hsu, H-C.; Chen, Y-L. SIRT1 promotes tumorigenesis and resistance to chemotherapy in hepatocellular carcinoma and its expression predicts poor prognosis. Ann. Surg. Oncol., 2012, 19(6), 2011-2019.
[251]
Li, Y.; Revalde, J.L.; Reid, G.; Paxton, J.W. Interactions of dietary phytochemicals with ABC transporters: possible implications for drug disposition and multidrug resistance in cancer. Drug Metab. Rev., 2010, 42(4), 590-611.
[252]
Hu, T.; To, K.K.W.; Wang, L.; Zhang, L.; Lu, L.; Shen, J.; Chan, R.L.; Li, M.; Yeung, J.H.; Cho, C.H. Reversal of P-glycoprotein (P-gp) mediated multidrug resistance in colon cancer cells by cryptotanshinone and dihydrotanshinone of Salvia miltiorrhiza. Phytomedicine, 2014, 21(11), 1264-1272.
[253]
Noratto, G.D.; Jutooru, I.; Safe, S.; Angel-Morales, G.; Mertens-Talcott, S.U. The drug resistance suppression induced by curcuminoids in colon cancer SW-480 cells is mediated by reactive oxygen species-induced disruption of the microRNA-27a-ZBTB10-Sp axis. Mol. Nutr. Food Res., 2013, 57(9), 1638-1648.
[254]
Neerati, P.; Sudhakar, Y.A.; Kanwar, J.R. Curcumin regulates colon cancer by inhibiting P-glycoprotein in in-situ cancerous colon perfusion rat model. J. Cancer Sci. Ther., 2013, 5, 313-319.
[255]
Zhang, Y.; Zhang, Y-K.; Wang, Y-J.; Vispute, S.G.; Jain, S.; Chen, Y.; Li, J.; Youssef, D.T.; El Sayed, K.A.; Chen, Z.S. Esters of the marine-derived triterpene sipholenol A reverse P-GP-mediated drug resistance. Mar. Drugs, 2015, 13(4), 2267-2286.
[256]
Rabindran, S.K.; Ross, D.D.; Doyle, L.A.; Yang, W.; Greenberger, L.M. Fumitremorgin C reverses multidrug resistance in cells transfected with the breast cancer resistance protein. Cancer Res., 2000, 60(1), 47-50.
[257]
Sheng, L.; Xiong, M.; Li, C.; Meng, X. Reversing multidrug-resistant by RNA interference through silencing MDR1 gene in human hepatocellular carcinoma cells subline Bel-7402/ADM. Pathol. Oncol. Res., 2014, 20(3), 541-548.
[258]
Li, H.; Zhou, S.; Li, T.; Liu, Z.; Wu, J.; Zeng, G. Suppression of BCRP expression and restoration of sensitivity to chemotherapy in multidrug-resistant hepatocellular carcinoma cell line HEPG2/ADM by RNA interference. Hepatogastroenterology, 2012, 59(119), 2238-2242.
[259]
Huesker, M.; Folmer, Y.; Schneider, M.; Fulda, C.; Blum, H.E.; Hafkemeyer, P. Reversal of drug resistance of hepatocellular carcinoma cells by adenoviral delivery of anti-MDR1 ribozymes. Hepatology, 2002, 36(4 Pt 1), 874-884.
[260]
Folmer, Y.; Schneider, M.; Blum, H.E.; Hafkemeyer, P. Reversal of drug resistance of hepatocellular carcinoma cells by adenoviral delivery of anti-ABCC2 antisense constructs. Cancer Gene Ther., 2007, 14(11), 875-884.
[261]
Chen, X-P.; Wang, Q.; Guan, J.; Huang, Z-Y.; Zhang, W-G.; Zhang, B-X. Reversing multidrug resistance by RNA interference through the suppression of MDR1 gene in human hepatoma cells. World J. Gastroenterol., 2006, 12(21), 3332-3337.
[262]
Zhuo, L.; Liu, J.; Wang, B.; Gao, M.; Huang, A. Differential miRNA expression profiles in hepatocellular carcinoma cells and drug-resistant sublines. Oncol. Rep., 2013, 29(2), 555-562.
[263]
Ma, J.; Wang, T.; Guo, R.; Yang, X.; Yin, J.; Yu, J.; Xiang, Q.; Pan, X.; Tang, H.; Lei, X. Involvement of miR-133a and miR-326 in ADM resistance of HepG2 through modulating expression of ABCC1. J. Drug Target., 2015, 23(6), 519-524.
[264]
Xu, Y.; Xia, F.; Ma, L.; Shan, J.; Shen, J.; Yang, Z.; Liu, J.; Cui, Y.; Bian, X.; Bie, P.; Qian, C. MicroRNA-122 sensitizes HCC cancer cells to adriamycin and vincristine through modulating expression of MDR and inducing cell cycle arrest. Cancer Lett., 2011, 310(2), 160-169.
[265]
Wang, D.; Zhang, N.; Ye, Y.; Qian, J.; Zhu, Y.; Wang, C. Role and mechanisms of microRNA503 in drug resistance reversal in HepG2/ADM human hepatocellular carcinoma cells. Mol. Med. Rep., 2014, 10(6), 3268-3274.
[266]
Robey, R.W.; To, K.K.K.; Polgar, O.; Dohse, M.; Fetsch, P.; Dean, M.; Bates, S.E. ABCG2: a perspective. Adv. Drug Deliv. Rev., 2009, 61(1), 3-13.
[267]
To, K.K.; Leung, W.W.; Ng, S.S. Exploiting a novel miR-519c-HuR-ABCG2 regulatory pathway to overcome chemoresistance in colorectal cancer. Exp. Cell Res., 2015, 338(2), 222-231.
[268]
Xu, K.; Liang, X.; Shen, K.; Cui, D.; Zheng, Y.; Xu, J.; Fan, Z.; Qiu, Y.; Li, Q.; Ni, L.; Liu, J. miR-297 modulates multidrug resistance in human colorectal carcinoma by down-regulating MRP-2. Biochem. J., 2012, 446(2), 291-300.
[269]
Liang, X-J.; Finkel, T.; Shen, D-W.; Yin, J-J.; Aszalos, A.; Gottesman, M.M. SIRT1 contributes in part to cisplatin resistance in cancer cells by altering mitochondrial metabolism. Mol. Cancer Res., 2008, 6(9), 1499-1506.
[270]
Chen, J.; Zhang, B.; Wong, N.; Lo, A.W.I.; To, K-F.; Chan, A.W.H.; Ng, M.H.; Ho, C.Y.; Cheng, S.H.; Lai, P.B.; Yu, J.; Ng, H.K.; Ling, M.T.; Huang, A.L.; Cai, X.F.; Ko, B.C. Sirtuin 1 is upregulated in a subset of hepatocellular carcinomas where it is essential for telomere maintenance and tumor cell growth. Cancer Res., 2011, 71(12), 4138-4149.
[271]
Roy, K.R.; Reddy, G.V.; Maitreyi, L.; Agarwal, S.; Achari, C.; Vali, S.; Reddanna, P. Celecoxib inhibits MDR1 expression through COX-2-dependent mechanism in human hepatocellular carcinoma (HepG2) cell line. Cancer Chemother. Pharmacol., 2010, 65(5), 903-911.
[272]
Lu, F.; Hou, Y-Q.; Song, Y.; Yuan, Z-J. TFPI-2 downregulates multidrug resistance protein in 5-FU-resistant human hepatocellular carcinoma BEL-7402/5-FU cells. Anat. Rec. (Hoboken), 2013, 296(1), 56-63.
[273]
Ling, S.; Tian, Y.; Zhang, H.; Jia, K.; Feng, T.; Sun, D.; Gao, Z.; Xu, F.; Hou, Z.; Li, Y.; Wang, L. Metformin reverses multidrug resistance in human hepatocellular carcinoma Bel7402/5fluorouracil cells. Mol. Med. Rep., 2014, 10(6), 2891-2897.
[274]
Wu, W.; Yang, J-L.; Wang, Y-L.; Wang, H.; Yao, M.; Wang, L.; Gu, J.J.; Cai, Y.; Shi, Y.; Yao, D.F. Reversal of multidrug resistance of hepatocellular carcinoma cells by metformin through inhibiting NF-κB gene transcription. World J. Hepatol., 2016, 8(23), 985-993.
[275]
Fouquet, G.; Debuysscher, V.; Ouled-Haddou, H.; Eugenio, M.S.; Demey, B.; Singh, A.R.; Ossart, C.; Al Bagami, M.; Regimbeau, J.M.; Nguyen-Khac, E.; Naassila, M.; Marcq, I.; Bouhlal, H. Hepatocyte SLAMF3 reduced specifically the multidrugs resistance protein MRP-1 and increases HCC cells sensitization to anti-cancer drugs. Oncotarget, 2016, 7(22), 32493-32503.
[276]
Zhu, M.M.; Tong, J.L.; Xu, Q.; Nie, F.; Xu, X.T.; Xiao, S.D.; Ran, Z.H. Increased JNK1 signaling pathway is responsible for ABCG2-mediated multidrug resistance in human colon cancer. PLoS One, 2012, 7(8), e41763.
[277]
Lee, Y-K.; Lin, T-H.; Chang, C-F.; Lo, Y-L. Galectin-3 silencing inhibits epirubicin-induced ATP binding cassette transporters and activates the mitochondrial apoptosis pathway via β-catenin/GSK-3β modulation in colorectal carcinoma. PLoS One, 2013, 8(11), e82478.
[278]
Ogretmen, B.; Safa, A.R. Negative regulation of MDR1 promoter activity in MCF-7, but not in multidrug resistant MCF-7/Adr, cells by cross-coupled NF-κ B/p65 and c-Fos transcription factors and their interaction with the CAAT region. Biochemistry, 1999, 38(7), 2189-2199.
[279]
Bentires-Alj, M.; Barbu, V.; Fillet, M.; Chariot, A.; Relic, B.; Jacobs, N.; Gielen, J.; Merville, M.P.; Bours, V. NF-kappaB transcription factor induces drug resistance through MDR1 expression in cancer cells. Oncogene, 2003, 22(1), 90-97.
[280]
Wang, W.; McLeod, H.L.; Cassidy, J. Disulfiram-mediated inhibition of NF-kappaB activity enhances cytotoxicity of 5-fluorouracil in human colorectal cancer cell lines. Int. J. Cancer, 2003, 104(4), 504-511.
[281]
Walther, W.; Kobelt, D.; Bauer, L.; Aumann, J.; Stein, U. Chemosensitization by diverging modulation by short-term and long-term TNF-α action on ABCB1 expression and NF-κB signaling in colon cancer. Int. J. Oncol., 2015, 47(6), 2276-2285.
[282]
Broxterman, H.J.; Kuiper, C.M.; Schuurhuis, G.J.; Tsuruo, T.; Pinedo, H.M.; Lankelma, J. Increase of daunorubicin and vincristine accumulation in multidrug resistant human ovarian carcinoma cells by a monoclonal antibody reacting with P-glycoprotein. Biochem. Pharmacol., 1988, 37(12), 2389-2393.
[283]
Hamada, H.; Tsuruo, T. Functional role for the 170- to 180-kDa glycoprotein specific to drug-resistant tumor cells as revealed by monoclonal antibodies. Proc. Natl. Acad. Sci. USA, 1986, 83(20), 7785-7789.
[284]
Pearson, J.W.; Fogler, W.E.; Volker, K.; Usui, N.; Goldenberg, S.K.; Gruys, E.; Riggs, C.W.; Komschlies, K.; Wiltrout, R.H.; Tsuruo, T. Reversal of drug resistance in a human colon cancer xenograft expressing MDR1 complementary DNA by in vivo administration of MRK-16 monoclonal antibody. J. Natl. Cancer Inst., 1991, 83(19), 1386-1391.
[285]
Naito, M.; Tsuge, H.; Kuroko, C.; Tomida, A.; Tsuruo, T. Enhancement of reversing effect of cyclosporin A on vincristine resistance by anti-P-glycoprotein monoclonal antibody MRK-16. Jpn. J. Cancer Res., 1993, 84(5), 489-492.
[286]
Leveille-Webster, C.R.; Arias, I.A. Establishment and serial quantification of intrahepatic xenografts of human hepatocellular carcinoma in severe combined immunodeficiency mice, and development of therapeutic strategies to overcome multidrug resistance. Clin. Cancer Res., 1996, 2(4), 695-706.
[287]
Zhai, B-J.; Shao, Z-Y.; Zhao, C-L.; Hu, K.; Shen, D-M.; Wu, F. Optimization of ultrasound-mediated in vitro reversal of multidrug resistance in human hepatocarcinoma cell line HepG2. Ultrasound Med. Biol., 2008, 34(10), 1697-1702.
[288]
Wu, F.; Shao, Z-Y.; Zhai, B-J.; Zhao, C-L.; Shen, D-M. Ultrasound reverses multidrug resistance in human cancer cells by altering gene expression of ABC transporter proteins and Bax protein. Ultrasound Med. Biol., 2011, 37(1), 151-159.
[289]
Shao, Z-Y.; Zhai, B-J.; Zhao, C-L.; Hu, K.; Shen, D-M.; Wu, F. Cytotoxic effects and in vitro reversal of multidrug resistance by therapeutic ultrasound in human hepatocarcinoma cell line (HepG2). Ultrasonics, 2008, 48(4), 297-302.
[290]
Niazi, M.; Zakeri-Milani, P.; Najafi Hajivar, S.; Soleymani Goloujeh, M.; Ghobakhlou, N.; Shahbazi Mojarrad, J.; Valizadeh, H. Nano-based strategies to overcome p-glycoprotein-mediated drug resistance. Expert Opin. Drug Metab. Toxicol., 2016, 12(9), 1021-1033.
[291]
Ahmad, J.; Akhter, S.; Greig, N.H.; Kamal, M.A.; Midoux, P.; Pichon, C. Engineered nanoparticles against MDR in cancer: The state of the art and its prospective. Curr. Pharm. Des., 2016, 22(28), 4360-4373.
[292]
Kapse-Mistry, S.; Govender, T.; Srivastava, R.; Yergeri, M. Nanodrug delivery in reversing multidrug resistance in cancer cells. Front. Pharmacol., 2014, 5, 159.
[293]
Zhao, X.; Chen, Q.; Li, Y.; Tang, H.; Liu, W.; Yang, X. Doxorubicin and curcumin co-delivery by lipid nanoparticles for enhanced treatment of diethylnitrosamine-induced hepatocellular carcinoma in mice. Eur. J. Pharm. Biopharm., 2015, 93, 27-36.
[294]
Zhao, X.; Chen, Q.; Liu, W.; Li, Y.; Tang, H.; Liu, X.; Yang, X. Codelivery of doxorubicin and curcumin with lipid nanoparticles results in improved efficacy of chemotherapy in liver cancer. Int. J. Nanomedicine, 2014, 10, 257-270.
[295]
Li, G.; Dong, S.; Qu, J.; Sun, Z.; Huang, Z.; Ye, L.; Liang, H.; Ai, X.; Zhang, W.; Chen, X. Synergism of hydroxyapatite nanoparticles and recombinant mutant human tumour necrosis factor-alpha in chemotherapy of multidrug-resistant hepatocellular carcinoma. Liver Int., 2010, 30(4), 585-592.
[296]
Zhang, G.; Shi, L.; Selke, M.; Wang, X. CdTe quantum dots with daunorubicin induce apoptosis of multidrug-resistant human hepatoma HepG2/ADM cells: in vitro and in vivo evaluation. Nanoscale Res. Lett., 2011, 6(1), 418.
[297]
Zhu, Q.L.; Zhou, Y.; Guan, M.; Zhou, X.F.; Yang, S.D.; Liu, Y.; Chen, W.L.; Zhang, C.G.; Yuan, Z.Q.; Liu, C.; Zhu, A.J.; Zhang, X.N. Low-density lipoprotein-coupled N-succinyl chitosan nanoparticles co-delivering siRNA and doxorubicin for hepatocyte-targeted therapy. Biomaterials, 2014, 35(22), 5965-5976.
[298]
Liu, T.; Zeng, L.; Jiang, W.; Fu, Y.; Zheng, W.; Chen, T. Rational design of cancer-targeted selenium nanoparticles to antagonize multidrug resistance in cancer cells. Nanomedicine (Lond.), 2015, 11(4), 947-958.
[299]
Guo, Y.; Chu, M.; Tan, S.; Zhao, S.; Liu, H.; Otieno, B.O.; Yang, X.; Xu, C.; Zhang, Z. Chitosan-g-TPGS nanoparticles for anticancer drug delivery and overcoming multidrug resistance. Mol. Pharm., 2014, 11(1), 59-70.
[300]
Jin, X.; Mo, R.; Ding, Y.; Zheng, W.; Zhang, C. Paclitaxel-loaded N-octyl-O-sulfate chitosan micelles for superior cancer therapeutic efficacy and overcoming drug resistance. Mol. Pharm., 2014, 11(1), 145-157.
[301]
Yuan, Y.; Zhang, Y.; Liu, B.; Wu, H.; Kang, Y.; Li, M.; Zeng, X.; He, N.; Zhang, G. The effects of multifunctional MiR-122-loaded graphene-gold composites on drug-resistant liver cancer. J. Nanobiotechnology, 2015, 13(1), 12.
[302]
Du, H.; Liu, M.; Yu, A.; Ji, J.; Zhai, G. Insight into the role of dual-ligand modification in low molecular weight heparin based nanocarrier for targeted delivery of doxorubicin. Int. J. Pharm., 2017, 523(1), 427-438.
[303]
Tsend-Ayush, A.; Zhu, X.; Ding, Y.; Yao, J.; Yin, L.; Zhou, J.; Yao, J. Lactobionic acid-conjugated TPGS nanoparticles for enhancing therapeutic efficacy of etoposide against hepatocellular carcinoma. Nanotechnology, 2017, 28(19), 195602.
[304]
Wang, R-H.; Bai, J.; Deng, J.; Fang, C-J.; Chen, X. TAT-modified gold nanoparticle carrier with enhanced anticancer activity and size effect on overcoming multidrug resistance. ACS Appl. Mater. Interfaces, 2017, 9(7), 5828-5837.
[305]
Zhang, X.; Guo, S.; Fan, R.; Yu, M.; Li, F.; Zhu, C.; Gan, Y. Dual-functional liposome for tumor targeting and overcoming multidrug resistance in hepatocellular carcinoma cells. Biomaterials, 2012, 33(29), 7103-7114.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy