Generic placeholder image

Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5206
ISSN (Online): 1875-5992

Research Article

Trailing TRAIL Resistance in Human Breast Adenocarcinoma Cells with Trichostatin A and Zebularine

Author(s): Sonia How Ming Wong, Chee-Mun Fang, Hwei-San Loh and Siew Ching Ngai*

Volume 23, Issue 7, 2023

Published on: 13 December, 2022

Page: [817 - 831] Pages: 15

DOI: 10.2174/1871520623666221114095733

Price: $65

Abstract

Aims: The aim of this study was to sensitize the resistant breast adenocarcinoma cells towards Tumour Necrosis Factor-related Apoptosis-inducing Ligand (TRAIL)-induced apoptosis.

Background: Breast cancer is a heterogeneous disease involving complex mechanisms. TRAIL is a potential anticancer candidate for targeted treatment due to its selective killing effects on neoplastic cells. Nonetheless, resistance occurs in many cancers either intrinsically or after multiple treatments.

Objective: Therefore, this research investigated whether the combination of Trichostatin A (TSA) and Zebularine (Zeb) (TZ) followed by TRAIL (TZT) could sensitize the human breast adenocarcinoma cells towards apoptosis.

Methods: The breast adenocarcinoma cells, MDA-MB-231, MCF-7 and E-MDA-MB-231 (E-cadherin re-expressed MDA-MB-231) were treated with TSA, Zeb, TZ, TRAIL and TZT. The cells were subjected to hematoxylin and eosin (H & E) staining and FITC-Annexin V/Propidium Iodide apoptosis detection prior to proteome profiling.

Results: Based on morphological observation, apoptosis was induced in all cells treated with all treatment regimens though it was more evident for the TZT-treated cells. In the apoptosis detection analysis, TZ increased early apoptosis significantly in MDA-MB-231 and MCF-7 while TRAIL induced late apoptosis significantly in E-MDA-MB-231. Based on the proteome profiling on MDA-MB-231, TRAIL R2 and Fas expression was increased. For E-MDA-MB- 231, down-regulation of catalase, paraoxonase-2 (PON2), clusterin, an inhibitor of apoptosis proteins (IAPs) and cell stress proteins validated the notion that E-cadherin re-expression enhances TZT anti-cancer efficacy. Similar trend was observed in MCF-7 whereby TZT treatment down-regulated the anti-apoptotic catalase and PON2, increased the proapoptotic, B cell lymphoma 2 (Bcl-2)-associated agonist of cell death (Bad) and Bcl-2-associated X (Bax), second mitochondria-derived activator of caspase (SMAC) and HtrA serine peptidase 2 (HTRA2) as well as TRAIL receptors (TRAIL R1 and TRAIL R2).

Conclusion: TZ treatment serves as an efficient treatment regimen for MDA-MB-231 and MCF-7, while TRAIL serves as a better treatment option for E-MDA-MB-231. Therefore, future studies on E-cadherin’s positive regulatory role in TRAIL-induced apoptosis are warranted.

Keywords: TRAIL, trichostatin A, zebularine, apoptosis, breast cancer, resistance.

[1]
Pandey, S.S.; Singh, S.; Pathak, C.; Tiwari, B.S. Programmed cell death: A process of death for survival-How far terminology pertinent for cell death in unicellular organisms. J. Cell Death, 2018, 11, 1179066018790259.
[http://dx.doi.org/10.1177/1179066018790259] [PMID: 30116103]
[2]
Chen, Q.; Kang, J.; Fu, C. The independence of and associations among apoptosis, autophagy, and necrosis. Signal Transduct. Target. Ther., 2018, 3(1), 18.
[http://dx.doi.org/10.1038/s41392-018-0018-5] [PMID: 29967689]
[3]
Stuckey, D.W.; Shah, K. TRAIL on trial: Preclinical advances in cancer therapy. Trends Mol. Med., 2013, 19(11), 685-694.
[http://dx.doi.org/10.1016/j.molmed.2013.08.007] [PMID: 24076237]
[4]
Nagane, M.; Huang, H.J.S.; Cavenee, W.K. The potential of TRAIL for cancer chemotherapy. Apoptosis, 2001, 6(3), 191-197.
[http://dx.doi.org/10.1023/A:1011336726649] [PMID: 11388668]
[5]
Wang, F.; Lin, J.; Xu, R. The molecular mechanisms of TRAIL resistance in cancer cells: Help in designing new drugs. Curr. Pharm. Des., 2014, 20(42), 6714-6722. a
[http://dx.doi.org/10.2174/1381612820666140929100735] [PMID: 25269558]
[6]
Özören, N.; El-Deiry, W.S. Defining characteristics of Types I and II apoptotic cells in response to TRAIL. Neoplasia, 2002, 4(6), 551-557.
[http://dx.doi.org/10.1038/sj.neo.7900270] [PMID: 12407450]
[7]
Hetschko, H.; Voss, V.; Horn, S.; Seifert, V.; Prehn, J.H.M.; Kögel, D. Pharmacological inhibition of Bcl-2 family members reactivates TRAIL-induced apoptosis in malignant glioma. J. Neurooncol., 2008, 86(3), 265-272.
[http://dx.doi.org/10.1007/s11060-007-9472-6] [PMID: 17924059]
[8]
Huang, S.; Okumura, K.; Sinicrope, F.A. BH3 mimetic obatoclax enhances TRAIL-mediated apoptosis in human pancreatic cancer cells. Clin. Cancer Res., 2009, 15(1), 150-159.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-1575] [PMID: 19118042]
[9]
Kisim, A.; Atmaca, H.; Cakar, B.; Karabulut, B.; Sezgin, C.; Uzunoglu, S.; Uslu, R.; Karaca, B. Pretreatment with AT-101 enhances tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis of breast cancer cells by inducing death receptors 4 and 5 protein levels. J. Cancer Res. Clin. Oncol., 2012, 138(7), 1155-1163.
[http://dx.doi.org/10.1007/s00432-012-1187-1] [PMID: 22411600]
[10]
Chen, J.J.; Shen, H.C.J.; Rivera Rosado, L.A.; Zhang, Y.; Di, X.; Zhang, B. Mislocalization of death receptors correlates with cellular resistance to their cognate ligands in human breast cancer cells. Oncotarget, 2012, 3(8), 833-842.
[http://dx.doi.org/10.18632/oncotarget.542] [PMID: 22909995]
[11]
Rahman, M.; Davis, S.R.; Pumphrey, J.G.; Bao, J.; Nau, M.M.; Meltzer, P.S.; Lipkowitz, S. TRAIL induces apoptosis in triple-negative breast cancer cells with a mesenchymal phenotype. Breast Cancer Res. Treat., 2009, 113(2), 217-230.
[http://dx.doi.org/10.1007/s10549-008-9924-5] [PMID: 18266105]
[12]
Wong, S.H.M.; Kong, W.Y.; Fang, C.M.; Loh, H.S.; Chuah, L.H.; Abdullah, S.; Ngai, S.C. The TRAIL to cancer therapy: Hindrances and potential solutions. Crit. Rev. Oncol. Hematol., 2019, 143, 81-94.
[http://dx.doi.org/10.1016/j.critrevonc.2019.08.008] [PMID: 31561055]
[13]
Lu, M.; Marsters, S.; Ye, X.; Luis, E.; Gonzalez, L.; Ashkenazi, A. E-cadherin couples death receptors to the cytoskeleton to regulate apoptosis. Mol. Cell, 2014, 54(6), 987-998.
[http://dx.doi.org/10.1016/j.molcel.2014.04.029] [PMID: 24882208]
[14]
Gyrd-Hansen, M.; Meier, P. IAPs: from caspase inhibitors to modulators of NF-κB, inflammation and cancer. Nat. Rev. Cancer, 2010, 10(8), 561-574.
[http://dx.doi.org/10.1038/nrc2889] [PMID: 20651737]
[15]
Silke, J.; Meier, P. Inhibitor of apoptosis (IAP) proteins-modulators of cell death and inflammation. Cold Spring Harb. Perspect. Biol., 2013, 5(2), a008730.
[http://dx.doi.org/10.1101/cshperspect.a008730] [PMID: 23378585]
[16]
Allensworth, J.L.; Aird, K.M.; Aldrich, A.J.; Batinic-Haberle, I.; Devi, G.R. XIAP inhibition and generation of reactive oxygen species enhances TRAIL sensitivity in inflammatory breast cancer cells. Mol. Cancer Ther., 2012, 11(7), 1518-1527.
[http://dx.doi.org/10.1158/1535-7163.MCT-11-0787] [PMID: 22508521]
[17]
Lopes, R.B.; Gangeswaran, R.; McNeish, I.A.; Wang, Y.; Lemoine, N.R. Expression of the IAP protein family is dysregulated in pancreatic cancer cells and is important for resistance to chemotherapy. Int. J. Cancer, 2007, 120(11), 2344-2352.
[http://dx.doi.org/10.1002/ijc.22554] [PMID: 17311258]
[18]
Azijli, K.; van Roosmalen, I.A.M.; Smit, J.; Pillai, S.; Fukushima, M.; de Jong, S.; Peters, G.J.; Bijnsdorp, I.V.; Kruyt, F.A.E. The novel thymidylate synthase inhibitor trifluorothymidine (TFT) and TRAIL synergistically eradicate non-small cell lung cancer cells. Cancer Chemother. Pharmacol., 2014, 73(6), 1273-1283.
[http://dx.doi.org/10.1007/s00280-014-2465-1] [PMID: 24744163]
[19]
Conticello, C.; Adamo, L.; Vicari, L.; Giuffrida, R.; Iannolo, G.; Anastasi, G.; Caruso, L.; Moschetti, G.; Cupri, A.; Palumbo, G.A.; Gulisano, M.; De Maria, R.; Giustolisi, R.; Di Raimondo, F. Antitumor activity of bortezomib alone and in combination with TRAIL in human acute myeloid leukemia. Acta Haematol., 2008, 120(1), 19-30.
[http://dx.doi.org/10.1159/000151511] [PMID: 18716397]
[20]
Li, H.; Wang, X.; Li, N.; Qiu, J.; Zhang, Y.; Cao, X. hPEBP4 resists TRAIL-induced apoptosis of human prostate cancer cells by activating Akt and deactivating ERK1/2 pathways. J. Biol. Chem., 2007, 282(7), 4943-4950.
[http://dx.doi.org/10.1074/jbc.M609494200] [PMID: 17178731]
[21]
Castrogiovanni, C.; Waterschoot, B.; De Backer, O.; Dumont, P. Serine 392 phosphorylation modulates p53 mitochondrial translocation and transcription-independent apoptosis. Cell Death Differ., 2018, 25(1), 190-203.
[http://dx.doi.org/10.1038/cdd.2017.143] [PMID: 28937686]
[22]
Wu, S.Y.; Wu, A.T.H.; Liu, S.H.; Wu, S.Y.; Wu, A.T.H.; Liu, S-H. MicroRNA-17-5p regulated apoptosis-related protein expression and radiosensitivity in oral squamous cell carcinoma caused by betel nut chewing. Oncotarget, 2016, 7(32), 51482-51493.
[http://dx.doi.org/10.18632/oncotarget.9856] [PMID: 27285985]
[23]
Mayes, P.A.; Campbell, L.; Ricci, M.S.; Plastaras, J.P.; Dicker, D.T.; El-Deiry, W.S. Modulation of TRAIL-induced tumor cell apoptosis in a hypoxic environment. Cancer Biol. Ther., 2005, 4(10), 1068-1074.
[http://dx.doi.org/10.4161/cbt.4.10.2255] [PMID: 16294025]
[24]
Wang, X.; Chen, M.; Zhou, J.; Zhang, X. HSP27, 70 and 90, anti-apoptotic proteins, in clinical cancer therapy. Int. J. Oncol., 2014, 45(1), 18-30. b
[http://dx.doi.org/10.3892/ijo.2014.2399] [PMID: 24789222]
[25]
Wong, S.H.M.; Fang, C.M.; Loh, H.S.; Ngai, S.C. Trichostatin A and Zebularine along with E-cadherin re-expression enhance tumour necrosis factor-related apoptosis-inducing ligand (TRAIL)-mediated cell cycle arrest in human breast adenocarcinoma cells. Asia Pac. J. Mol. Biol. Biotechnol., 2021, 29(1), 26-41.
[http://dx.doi.org/10.35118/apjmbb.2021.029.1.04]
[26]
Kong, W.Y.; Yee, Z.Y.; Mai, C.W.; Fang, C.M.; Abdullah, S.; Ngai, S.C. Zebularine and trichostatin A sensitized human breast adenocarcinoma cells towards tumor necrosis factor-related apoptosis inducing ligand (TRAIL)-induced apoptosis. Heliyon, 2019, 5(9), e02468.
[http://dx.doi.org/10.1016/j.heliyon.2019.e02468] [PMID: 31687564]
[27]
Pan, Y.; Li, J.; Zhang, Y.; Wang, N.; Liang, H.; Liu, Y.; Zhang, C.Y.; Zen, K.; Gu, H. Slug-upregulated miR-221 promotes breast cancer progression through suppressing E-cadherin expression. Sci. Rep., 2016, 6(1), 25798.
[http://dx.doi.org/10.1038/srep25798] [PMID: 27174021]
[28]
Baig, S.; Seevasant, I.; Mohamad, J.; Mukheem, A.; Huri, H.Z.; Kamarul, T. Potential of apoptotic pathway-targeted cancer therapeutic research: Where do we stand? Cell Death Dis., 2016, 7(1), e2058.
[http://dx.doi.org/10.1038/cddis.2015.275] [PMID: 26775709]
[29]
Elmore, S. Apoptosis: a review of programmed cell death. Toxicol. Pathol., 2007, 35(4), 495-516.
[http://dx.doi.org/10.1080/01926230701320337] [PMID: 17562483]
[30]
Coleman, M.L.; Sahai, E.A.; Yeo, M.; Bosch, M.; Dewar, A.; Olson, M.F. Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat. Cell Biol., 2001, 3(4), 339-345.
[http://dx.doi.org/10.1038/35070009] [PMID: 11283606]
[31]
Saraste, A.; Pulkki, K. Morphologic and biochemical hallmarks of apoptosis. Cardiovasc. Res., 2000, 45(3), 528-537.
[http://dx.doi.org/10.1016/S0008-6363(99)00384-3] [PMID: 10728374]
[32]
Sanaei, M.; Kavoosi, F. Investigation of the effect of zebularine in comparison to and in combination with trichostatin A on p21Cip1/Waf1/Sdi1, p27Kip1, p57Kip2, DNA methyltransferases and histone deacetylases in colon cancer LS 180 Cell Line. Asian Pac. J. Cancer Prev., 2020, 21(6), 1819-1828.
[http://dx.doi.org/10.31557/APJCP.2020.21.6.1819] [PMID: 32592383]
[33]
Billam, M.; Sobolewski, M.D.; Davidson, N.E. Effects of a novel DNA methyltransferase inhibitor zebularine on human breast cancer cells. Breast Cancer Res. Treat., 2010, 120(3), 581-592.
[http://dx.doi.org/10.1007/s10549-009-0420-3] [PMID: 19459041]
[34]
Nakamura, K.; Aizawa, K.; Nakabayashi, K.; Kato, N.; Yamauchi, J.; Hata, K.; Tanoue, A. DNA methyltransferase inhibitor zebularine inhibits human hepatic carcinoma cells proliferation and induces apoptosis. PLoS One, 2013, 8(1), e54036.
[http://dx.doi.org/10.1371/journal.pone.0054036] [PMID: 23320119]
[35]
You, B.R.; Park, W.H. Zebularine inhibits the growth of A549 lung cancer cells via cell cycle arrest and apoptosis. Mol. Carcinog., 2014, 53(11), 847-857.
[http://dx.doi.org/10.1002/mc.22042] [PMID: 23661569]
[36]
Alao, J.P.; Stavropoulou, A.V.; Lam, E.W.F.; Charles Coombes, R.; Vigushin, D.M. Histone deacetylase inhibitor, Trichostatin A induces ubiquitin-dependent cyclin D1 degradation in MCF-7 breast cancer cells. Mol. Cancer, 2006, 5(1), 8.
[http://dx.doi.org/10.1186/1476-4598-5-8] [PMID: 16504004]
[37]
Sun, S.; Han, Y.; Liu, J.; Fang, Y.; Tian, Y.; Zhou, J.; Ma, D.; Wu, P. Trichostatin A targets the mitochondrial respiratory chain, increasing mitochondrial reactive oxygen species production to trigger apoptosis in human breast cancer cells. PLoS One, 2014, 9(3), e91610.
[http://dx.doi.org/10.1371/journal.pone.0091610] [PMID: 24626188]
[38]
Willis, S.N.; Fletcher, J.I.; Kaufmann, T.; van Delft, M.F.; Chen, L.; Czabotar, P.E.; Ierino, H.; Lee, E.F.; Fairlie, W.D.; Bouillet, P.; Strasser, A.; Kluck, R.M.; Adams, J.M.; Huang, D.C.S. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science, 2007, 315(5813), 856-859.
[http://dx.doi.org/10.1126/science.1133289] [PMID: 17289999]
[39]
Makki, M.S.; Heinzel, T.; Englert, C. TSA downregulates Wilms tumor gene 1 (Wt1) expression at multiple levels. Nucleic Acids Res., 2008, 36(12), 4067-4078.
[http://dx.doi.org/10.1093/nar/gkn356] [PMID: 18535006]
[40]
Sawa, H.; Murakami, H.; Ohshima, Y.; Sugino, T.; Nakajyo, T.; Kisanuki, T.; Tamura, Y.; Satone, A.; Ide, W.; Hashimoto, I.; Kamada, H. Histone deacetylase inhibitors such as sodium butyrate and trichostatin A induce apoptosis through an increase of the bcl-2-related protein Bad. Brain Tumor Pathol., 2001, 18(2), 109-114.
[http://dx.doi.org/10.1007/BF02479423] [PMID: 11908866]
[41]
Pompeia, C.; Hodge, D.R.; Plass, C.; Wu, Y.Z.; Marquez, V.E.; Kelley, J.A.; Farrar, W.L. Microarray analysis of epigenetic silencing of gene expression in the KAS-6/1 multiple myeloma cell line. Cancer Res., 2004, 64(10), 3465-3473.
[http://dx.doi.org/10.1158/0008-5472.CAN-03-3970] [PMID: 15150099]
[42]
Yap, Z.H.; Kong, W.Y.; Azeez, A.R.; Fang, C.M.; Ngai, S.C. Anti-cancer effects of epigenetics drugs scriptaid and zebularine in human breast adenocarcinoma cells. Anticancer. Agents Med. Chem., 2022, 22(8), 1582-1591.
[http://dx.doi.org/10.2174/1871520621666210608103251] [PMID: 34102995]
[43]
Kim, H.R.; Kim, E.J.; Yang, S.H.; Jeong, E.T.; Park, C.; Lee, J.H.; Youn, M.J.; So, H.S.; Park, R. Trichostatin A induces apoptosis in lung cancer cells via simultaneous activation of the death receptor-mediated and mitochondrial pathway. Exp. Mol. Med., 2006, 38(6), 616-624.
[http://dx.doi.org/10.1038/emm.2006.73] [PMID: 17202837]
[44]
Maecker, H.L.; Yun, Z.; Maecker, H.T.; Giaccia, A.J. Epigenetic changes in tumor Fas levels determine immune escape and response to therapy. Cancer Cell, 2002, 2(2), 139-148.
[http://dx.doi.org/10.1016/S1535-6108(02)00095-8] [PMID: 12204534]
[45]
Morinobu, A.; Wang, B.; Liu, J.; Yoshiya, S.; Kurosaka, M.; Kumagai, S. Trichostatin A cooperates with Fas-mediated signal to induce apoptosis in rheumatoid arthritis synovial fibroblasts. J. Rheumatol., 2006, 33(6), 1052-1060.
[PMID: 16755652]
[46]
Bockbrader, K.M.; Tan, M.; Sun, Y. A small molecule Smac-mimic compound induces apoptosis and sensitizes TRAIL- and etoposide-induced apoptosis in breast cancer cells. Oncogene, 2005, 24(49), 7381-7388.
[http://dx.doi.org/10.1038/sj.onc.1208888] [PMID: 16044155]
[47]
Finlay, D.; Vamos, M.; González-López, M.; Ardecky, R.J.; Ganji, S.R.; Yuan, H.; Su, Y.; Cooley, T.R.; Hauser, C.T.; Welsh, K.; Reed, J.C.; Cosford, N.D.P.; Vuori, K. Small-molecule IAP antagonists sensitize cancer cells to TRAIL-induced apoptosis: roles of XIAP and cIAPs. Mol. Cancer Ther., 2014, 13(1), 5-15.
[http://dx.doi.org/10.1158/1535-7163.MCT-13-0153] [PMID: 24194568]
[48]
Han, M.H.; Park, C.; Kwon, T.K.; Kim, G.Y.; Kim, W.J.; Hong, S.H.; Yoo, Y.H.; Choi, Y.H. The histone deacetylase inhibitor trichostatin A sensitizes human renal carcinoma cells to TRAIL-induced apoptosis through down-regulation of c-FLIPL. Biomol. Ther. (Seoul), 2015, 23(1), 31-38.
[http://dx.doi.org/10.4062/biomolther.2014.092] [PMID: 25593641]
[49]
Shin, D.Y.; Park, Y.S.; Yang, K.; Kim, G.Y.; Kim, W.J.; Han, M.H.; Kang, H.S.; Choi, Y.H. Decitabine, a DNA methyltransferase inhibitor, induces apoptosis in human leukemia cells through intracellular reactive oxygen species generation. Int. J. Oncol., 2012, 41(3), 910-918.
[http://dx.doi.org/10.3892/ijo.2012.1546] [PMID: 22767021]
[50]
Pietenpol, J.A.; Stewart, Z.A. Cell cycle checkpoint signaling. Toxicology, 2002, 181-182, 475-481.
[http://dx.doi.org/10.1016/S0300-483X(02)00460-2] [PMID: 12505356]
[51]
Wang, L.; Wang, G.; Yang, D.; Guo, X.; Xu, Y.; Feng, B.; Kang, J. Euphol arrests breast cancer cells at the G1 phase through the modulation of cyclin D1, p21 and p27 expression. Mol. Med. Rep., 2013, 8(4), 1279-1285. b
[http://dx.doi.org/10.3892/mmr.2013.1650] [PMID: 23969579]
[52]
Fandy, T.E.; Shankar, S.; Ross, D.D.; Sausville, E.; Srivastava, R.K. Interactive effects of HDAC inhibitors and TRAIL on apoptosis are associated with changes in mitochondrial functions and expressions of cell cycle regulatory genes in multiple myeloma. Neoplasia, 2005, 7(7), 646-657.
[http://dx.doi.org/10.1593/neo.04655] [PMID: 16026644]
[53]
Chopin, V.; Slomianny, C.; Hondermarck, H.; Le Bourhis, X. Synergistic induction of apoptosis in breast cancer cells by cotreatment with butyrate and TNF-alpha, TRAIL, or anti-Fas agonist antibody involves enhancement of death receptors’ signaling and requires P21waf1. Exp. Cell Res., 2004, 298(2), 560-573.
[http://dx.doi.org/10.1016/j.yexcr.2004.04.038] [PMID: 15265702]
[54]
Varshochi, R.; Halim, F.; Sunters, A.; Alao, J.P.; Madureira, P.A.; Hart, S.M.; Ali, S.; Vigushin, D.M.; Coombes, R.C.; Lam, E.W.F. ICI182,780 induces p21Waf1 gene transcription through releasing histone deacetylase 1 and estrogen receptor alpha from Sp1 sites to induce cell cycle arrest in MCF-7 breast cancer cell line. J. Biol. Chem., 2005, 280(5), 3185-3196.
[http://dx.doi.org/10.1074/jbc.M408063200] [PMID: 15557281]
[55]
Zuo, X.; Qin, Y.; Zhang, X.; Ning, Q.; Shao, S.; Luo, M.; Yuan, N.; Huang, S.; Zhao, X. Breast cancer cells are arrested at different phases of the cell cycle following the re-expression of ARHI. Oncol. Rep., 2014, 31(5), 2358-2364.
[http://dx.doi.org/10.3892/or.2014.3107] [PMID: 24676336]
[56]
Hrgovic, I.; Doll, M.; Kleemann, J.; Wang, X.F.; Zoeller, N.; Pinter, A.; Kippenberger, S.; Kaufmann, R.; Meissner, M. The histone deacetylase inhibitor trichostatin a decreases lymphangiogenesis by inducing apoptosis and cell cycle arrest via p21-dependent pathways. BMC Cancer, 2016, 16(1), 763.
[http://dx.doi.org/10.1186/s12885-016-2807-y] [PMID: 27716272]
[57]
Pietsch, E.C.; Perchiniak, E.; Canutescu, A.A.; Wang, G.; Dunbrack, R.L.; Murphy, M.E. Oligomerization of BAK by p53 utilizes conserved residues of the p53 DNA binding domain. J. Biol. Chem., 2008, 283(30), 21294-21304.
[http://dx.doi.org/10.1074/jbc.M710539200] [PMID: 18524770]
[58]
Hui, L.; Zheng, Y.; Yan, Y.; Bargonetti, J.; Foster, D.A. Mutant p53 in MDA-MB-231 breast cancer cells is stabilized by elevated phospholipase D activity and contributes to survival signals generated by phospholipase D. Oncogene, 2006, 25(55), 7305-7310.
[http://dx.doi.org/10.1038/sj.onc.1209735] [PMID: 16785993]
[59]
Greijer, A.E.; van der Wall, E. The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis. J. Clin. Pathol., 2004, 57(10), 1009-1014.
[http://dx.doi.org/10.1136/jcp.2003.015032] [PMID: 15452150]
[60]
Piret, J.P.; Mottet, D.; Raes, M.; Michiels, C. Is HIF-1α a pro- or an anti-apoptotic protein? Biochem. Pharmacol., 2002, 64(5-6), 889-892.
[http://dx.doi.org/10.1016/S0006-2952(02)01155-3] [PMID: 12213583]
[61]
Sermeus, A.; Michiels, C. Reciprocal influence of the p53 and the hypoxic pathways. Cell Death Dis., 2011, 2(5), e164.
[http://dx.doi.org/10.1038/cddis.2011.48] [PMID: 21614094]
[62]
Fulda, S.; Gorman, A.M.; Hori, O.; Samali, A. Cellular stress responses: Cell survival and cell death. Int. J. Cell Biol., 2010, 2010, 1-23.
[http://dx.doi.org/10.1155/2010/214074] [PMID: 20182529]
[63]
Voss, O.H.; Batra, S.; Kolattukudy, S.J.; Gonzalez-Mejia, M.E.; Smith, J.B.; Doseff, A.I. Binding of caspase-3 prodomain to heat shock protein 27 regulates monocyte apoptosis by inhibiting caspase-3 proteolytic activation. J. Biol. Chem., 2007, 282(34), 25088-25099.
[http://dx.doi.org/10.1074/jbc.M701740200] [PMID: 17597071]
[64]
Ferreira, A.C.; Suriano, G.; Mendes, N.; Gomes, B.; Wen, X.; Carneiro, F.; Seruca, R.; Machado, J.C. E-cadherin impairment increases cell survival through notch-dependent upregulation of Bcl-2. Hum. Mol. Genet., 2012, 21(2), 334-343.
[http://dx.doi.org/10.1093/hmg/ddr469] [PMID: 21989054]
[65]
Sasaki, C.Y.; Lin, H.; Passaniti, A. Expression of E-cadherin reduces Bcl-2 expression and increases sensitivity to etoposide-induced apoptosis. Int. J. Cancer, 2000, 86(5), 660-666.
[http://dx.doi.org/10.1002/(SICI)1097-0215(20000601)86:5<660:AID-IJC9>3.0.CO;2-X] [PMID: 10797287]
[66]
Fedor-Chaiken, M.; Hein, P.W.; Stewart, J.C.; Brackenbury, R.; Kinch, M.S. E-cadherin binding modulates EGF receptor activation. Cell Commun. Adhes., 2003, 10(2), 105-118.
[http://dx.doi.org/10.1080/cac.10.2.105.118] [PMID: 14681060]
[67]
Reddy, P.; Liu, L.; Ren, C.; Lindgren, P.; Boman, K.; Shen, Y.; Lundin, E.; Ottander, U.; Rytinki, M.; Liu, K. Formation of E-cadherin-mediated cell-cell adhesion activates AKT and mitogen activated protein kinase via phosphatidylinositol 3 kinase and ligand-independent activation of epidermal growth factor receptor in ovarian cancer cells. Mol. Endocrinol., 2005, 19(10), 2564-2578.
[http://dx.doi.org/10.1210/me.2004-0342] [PMID: 15928314]
[68]
Shen, X.; Kramer, R.H. Adhesion-mediated squamous cell carcinoma survival through ligand-independent activation of epidermal growth factor receptor. Am. J. Pathol., 2004, 165(4), 1315-1329.
[http://dx.doi.org/10.1016/S0002-9440(10)63390-1] [PMID: 15466396]
[69]
Gilmore, A.P.; Valentijn, A.J.; Wang, P.; Ranger, A.M.; Bundred, N.; O’Hare, M.J.; Wakeling, A.; Korsmeyer, S.J.; Streuli, C.H. Activation of BAD by therapeutic inhibition of epidermal growth factor receptor and transactivation by insulin-like growth factor receptor. J. Biol. Chem., 2002, 277(31), 27643-27650.
[http://dx.doi.org/10.1074/jbc.M108863200] [PMID: 12011069]
[70]
Chen, D.; Ping, Dou.Q The ubiquitin-proteasome system as a prospective molecular target for cancer treatment and prevention. Curr. Protein Pept. Sci., 2010, 11(6), 459-470.
[http://dx.doi.org/10.2174/138920310791824057] [PMID: 20491623]
[71]
Li, B.; Dou, Q.P. Bax degradation by the ubiquitin/proteasome-dependent pathway: Involvement in tumor survival and progression. Proc. Natl. Acad. Sci. USA, 2000, 97(8), 3850-3855.
[http://dx.doi.org/10.1073/pnas.070047997] [PMID: 10725400]
[72]
Reis, C.R.; Chen, P.H.; Bendris, N.; Schmid, S.L. TRAIL-death receptor endocytosis and apoptosis are selectively regulated by dynamin-1 activation. Proc. Natl. Acad. Sci. USA, 2017, 114(3), 504-509.
[http://dx.doi.org/10.1073/pnas.1615072114] [PMID: 28049841]
[73]
Zhang, Y.; Yoshida, T.; Zhang, B. TRAIL induces endocytosis of its death receptors in MDA-MB-231 breast cancer cells. Cancer Biol. Ther., 2009, 8(10), 917-922.
[http://dx.doi.org/10.4161/cbt.8.10.8141] [PMID: 19270498]
[74]
Jalving, M.; Heijink, D.M.; Koornstra, J.J.; Boersma-van Ek, W.; Zwart, N.; Wesseling, J.; Sluiter, W.J.; de Vries, E.G.E.; Kleibeuker, J.H.; de Jong, S. Regulation of TRAIL receptor expression by -catenin in colorectal tumours. Carcinogenesis, 2014, 35(5), 1092-1099.
[http://dx.doi.org/10.1093/carcin/bgt484] [PMID: 24379239]
[75]
Wong, S.H.M.; Fang, C.M.; Chuah, L.H.; Leong, C.O.; Ngai, S.C. E-cadherin: Its dysregulation in carcinogenesis and clinical implications. Crit. Rev. Oncol. Hematol., 2018, 121, 11-22.
[http://dx.doi.org/10.1016/j.critrevonc.2017.11.010] [PMID: 29279096]
[76]
Essers, M.A.G.; de Vries-Smits, L.M.M.; Barker, N.; Polderman, P.E.; Burgering, B.M.T.; Korswagen, H.C. Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science, 2005, 308(5725), 1181-1184.
[http://dx.doi.org/10.1126/science.1109083] [PMID: 15905404]
[77]
Hiscox, S.; Jiang, W.G. Association of the HGF/SF receptor, c-met, with the cell-surface adhesion molecule, E-cadherin, and catenins in human tumor cells. Biochem. Biophys. Res. Commun., 1999, 261(2), 406-411.
[http://dx.doi.org/10.1006/bbrc.1999.1002] [PMID: 10425198]
[78]
Kanai, Y.; Ochiai, A.; Shibata, T.; Oyama, T.; Ushijima, S.; Akimoto, S.; Hirohashi, S. c-erbB-2 gene product directly associates with β-catenin and plakoglobin. Biochem. Biophys. Res. Commun., 1995, 208(3), 1067-1072.
[http://dx.doi.org/10.1006/bbrc.1995.1443] [PMID: 7702605]
[79]
Li, Y.; Bharti, A.; Chen, D.; Gong, J.; Kufe, D. Interaction of glycogen synthase kinase 3beta with the DF3/MUC1 carcinoma-associated antigen and beta-catenin. Mol. Cell. Biol., 1998, 18(12), 7216-7224.
[http://dx.doi.org/10.1128/MCB.18.12.7216] [PMID: 9819408]
[80]
Grossmann, J. Molecular mechanisms of “detachment-induced apoptosis--Anoikis”. Apoptosis, 2002, 7(3), 247-260.
[http://dx.doi.org/10.1023/A:1015312119693] [PMID: 11997669]
[81]
Kim, R.K.; Suh, Y.; Yoo, K.C.; Cui, Y.H.; Kim, H.; Kim, M.J.; Gyu Kim, I.; Lee, S.J. Activation of KRAS promotes the mesenchymal features of basal-type breast cancer. Exp. Mol. Med., 2015, 47(1), e137.
[http://dx.doi.org/10.1038/emm.2014.99] [PMID: 25633745]
[82]
Hymowitz, S.G.; Malek, S. Targeting the MAPK pathway in RAS mutant cancers. Cold Spring Harb. Perspect. Med., 2018, 8(11), a031492.
[http://dx.doi.org/10.1101/cshperspect.a031492] [PMID: 29440321]
[83]
Sullivan, K.M.; Kozuch, P.S. Impact of KRAS mutations on management of colorectal carcinoma. Pathol. Res. Int., 2011, 2011, 1-11.
[http://dx.doi.org/10.4061/2011/219309] [PMID: 21437184]
[84]
Chao, Y.; Wu, Q.; Acquafondata, M.; Dhir, R.; Wells, A. Partial mesenchymal to epithelial reverting transition in breast and prostate cancer metastases. Cancer Microenviron., 2012, 5(1), 19-28.
[http://dx.doi.org/10.1007/s12307-011-0085-4] [PMID: 21892699]
[85]
Chao, Y.L.; Shepard, C.R.; Wells, A. Breast carcinoma cells re-express E-cadherin during mesenchymal to epithelial reverting transition. Mol. Cancer, 2010, 9(1), 179.
[http://dx.doi.org/10.1186/1476-4598-9-179] [PMID: 20609236]
[86]
Chen, L.; Jian, W.; Lu, L.; Zheng, L.; Yu, Z.; Zhou, D. Elevated expression of E-cadherin in primary breast cancer and its corresponding metastatic lymph node. Int. J. Clin. Exp. Med., 2015, 8(7), 11752-11758.
[PMID: 26380015]
[87]
Rodriguez, F.J.; Lewis-Tuffin, L.J.; Anastasiadis, P.Z. E-cadherin’s dark side: possible role in tumor progression. Biochim. Biophys. Acta, 2012, 1826(1), 23-31.
[PMID: 22440943]
[88]
Al-Rayyan, N.; Litchfield, L.M.; Ivanova, M.M.; Radde, B.N.; Cheng, A.; Elbedewy, A.; Klinge, C.M. 5-Aza-2-deoxycytidine and trichostatin A increase COUP-TFII expression in antiestrogen-resistant breast cancer cell lines. Cancer Lett., 2014, 347(1), 139-150.
[http://dx.doi.org/10.1016/j.canlet.2014.02.001] [PMID: 24513177]
[89]
Zhang, Y.; Zhang, B. TRAIL resistance of breast cancer cells is associated with constitutive endocytosis of death receptors 4 and 5. Mol. Cancer Res., 2008, 6(12), 1861-1871.
[http://dx.doi.org/10.1158/1541-7786.MCR-08-0313] [PMID: 19074831]
[90]
Kowalski, P.J.; Rubin, M.A.; Kleer, C.G. E-cadherin expression in primary carcinomas of the breast and its distant metastases. Breast Cancer Res., 2003, 5(6), R217-R222.
[http://dx.doi.org/10.1186/bcr651] [PMID: 14580257]
[91]
Fulga, V.; Rudico, L.; Balica, A.R.; Cimpean, A.M.; Saptefrati, L.; Margan, M.M.; Raica, M. Differential expression of e-cadherin in primary breast cancer and corresponding lymph node metastases. Anticancer Res., 2015, 35(2), 759-765.
[PMID: 25667455]
[92]
Ito, F.; Yoshimoto, C.; Yamada, Y.; Sudo, T.; Kobayashi, H. The HNF-1β-USP28-Claspin pathway upregulates DNA damage-induced Chk1 activation in ovarian clear cell carcinoma. Oncotarget, 2018, 9(25), 17512-17522.
[http://dx.doi.org/10.18632/oncotarget.24776] [PMID: 29707125]
[93]
Patil, M.; Pabla, N.; Dong, Z. Checkpoint kinase 1 in DNA damage response and cell cycle regulation. Cell. Mol. Life Sci., 2013, 70(21), 4009-4021.
[http://dx.doi.org/10.1007/s00018-013-1307-3] [PMID: 23508805]
[94]
Clarke, C.A.L.; Bennett, L.N.; Clarke, P.R. Cleavage of claspin by caspase-7 during apoptosis inhibits the Chk1 pathway. J. Biol. Chem., 2005, 280(42), 35337-35345.
[http://dx.doi.org/10.1074/jbc.M506460200] [PMID: 16123041]
[95]
Semple, J.I.; Smits, V A J.; Fernaud, J-R.; Mamely, I.; Freire, R. Cleavage and degradation of Claspin during apoptosis by caspases and the proteasome. Cell Death Differ., 2007, 14(8), 1433-1442.
[http://dx.doi.org/10.1038/sj.cdd.4402134] [PMID: 17431426]
[96]
Gibbons, J.A.; Kanwar, J.R.; Kanwar, R.K. Iron-free and iron-saturated bovine lactoferrin inhibit survivin expression and differentially modulate apoptosis in breast cancer. BMC Cancer, 2015, 15(1), 425.
[http://dx.doi.org/10.1186/s12885-015-1441-4] [PMID: 25998617]
[97]
Smeenk, L.; van Heeringen, S.J.; Koeppel, M.; Gilbert, B.; Janssen-Megens, E.; Stunnenberg, H.G.; Lohrum, M. Role of p53 serine 46 in p53 target gene regulation. PLoS One, 2011, 6(3), e17574.
[http://dx.doi.org/10.1371/journal.pone.0017574] [PMID: 21394211]
[98]
Benson, E.K.; Mungamuri, S.K.; Attie, O.; Kracikova, M.; Sachidanandam, R.; Manfredi, J.J.; Aaronson, S.A. p53-dependent gene repression through p21 is mediated by recruitment of E2F4 repression complexes. Oncogene, 2014, 33(30), 3959-3969.
[http://dx.doi.org/10.1038/onc.2013.378] [PMID: 24096481]
[99]
Wang, J.; Guo, W.; Zhou, H.; Luo, N.; Nie, C.; Zhao, X.; Yuan, Z.; Liu, X.; Wei, Y. Mitochondrial p53 phosphorylation induces Bak-mediated and caspase-independent cell death. Oncotarget, 2015, 6(19), 17192-17205.
[http://dx.doi.org/10.18632/oncotarget.3780] [PMID: 25980443]
[100]
Amaral, J.D.; Xavier, J.M.; Steer, C.J.; Rodrigues, C.M. The role of p53 in apoptosis. Discov. Med., 2010, 9(45), 145-152.
[PMID: 20193641]
[101]
Chandra, D.; Choy, G.; Tang, D.G. Cytosolic accumulation of HSP60 during apoptosis with or without apparent mitochondrial release: evidence that its pro-apoptotic or pro-survival functions involve differential interactions with caspase-3. J. Biol. Chem., 2007, 282(43), 31289-31301.
[http://dx.doi.org/10.1074/jbc.M702777200] [PMID: 17823127]
[102]
Zhu, X.F.; Li, W.; Ma, J.Y.; Shao, N.; Zhang, Y.J.; Liu, R.M.; Wu, W.B.; Lin, Y.; Wang, S.M. Knockdown of heme oxygenase-1 promotes apoptosis and autophagy and enhances the cytotoxicity of doxorubicin in breast cancer cells. Oncol. Lett., 2015, 10(5), 2974-2980.
[http://dx.doi.org/10.3892/ol.2015.3735] [PMID: 26722274]

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