Login Register Cart 0
Generic placeholder image

Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

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

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Metalloproteinases Suppression Driven by the Curcumin Analog DM-1 Modulates Invasion in BRAF-Resistant Melanomas

Author(s): Nayane de Souza, Érica Aparecida de Oliveira, Fernanda Faião-Flores, Luciana A. Pimenta, José A.P. Quincoces, Sandra C. Sampaio and Silvya S. Maria-Engler*

Volume 20, Issue 9, 2020

Page: [1038 - 1050] Pages: 13

DOI: 10.2174/1871520620666200218111422

Price: $65

Abstract

Background: Melanoma is the most aggressive skin cancer, and BRAF (V600E) is the most frequent mutation that led to the development of BRAF inhibitors (BRAFi). However, patients treated with BRAFi usually present recidivism after 6-9 months. Curcumin is a turmeric substance, and it has been deeply investigated due to its anti-inflammatory and antitumoral effects. Still, the low bioavailability and biodisponibility encouraged the investigation of different analogs. DM-1 is a curcumin analog and has shown an antitumoral impact in previous studies.

Methods: Evaluated DM-1 stability and cytotoxic effects for BRAFi-sensitive and resistant melanomas, as well as the role in the metalloproteinases modulation.

Results: DM-1 showed growth inhibitory potential for melanoma cells, demonstrated by reduction of colony formation, migration and endothelial tube formation, and cell cycle arrest. Subtoxic doses were able to downregulate important Metalloproteinases (MMPs) related to invasiveness, such as MMP-1, -2 and -9. Negative modulations of TIMP-2 and MMP-14 reduced MMP-2 and -9 activity; however, the reverse effect is seen when increased TIMP-2 and MMP-14 resulted in raised MMP-2.

Conclusion: These findings provide essential details into the functional role of DM-1 in melanomas, encouraging further studies in the development of combinatorial treatments for melanomas.

Keywords: Curcumin-analogue, DM-1, melanoma, BRAF resistance, vemurafenib, BRAF inhibitor.

« Previous Next »
Graphical Abstract

[1]
Davies, H.; Bignell, G.R.; Cox, C.; Stephens, P.; Edkins, S.; Clegg, S.; Teague, J.; Woffendin, H.; Garnett, M.J.; Bottomley, W.; Davis, N.; Dicks, E.; Ewing, R.; Floyd, Y.; Gray, K.; Hall, S.; Hawes, R.; Hughes, J.; Kosmidou, V.; Menzies, A.; Mould, C.; Parker, A.; Stevens, C.; Watt, S.; Hooper, S.; Wilson, R.; Jayatilake, H.; Gusterson, B.A.; Cooper, C.; Shipley, J.; Hargrave, D.; Pritchard-Jones, K.; Maitland, N.; Chenevix-Trench, G.; Riggins, G.J.; Bigner, D.D.; Palmieri, G.; Cossu, A.; Flanagan, A.; Nicholson, A.; Ho, J.W.; Leung, S.Y.; Yuen, S.T.; Weber, B.L.; Seigler, H.F.; Darrow, T.L.; Paterson, H.; Marais, R.; Marshall, C.J.; Wooster, R.; Stratton, M.R.; Futreal, P.A. Mutations of the BRAF gene in human cancer. Nature, 2002, 417(6892), 949-954.
[http://dx.doi.org/10.1038/nature00766] [PMID: 12068308]
[2]
Flaherty, K.T.; Puzanov, I.; Kim, K.B.; Ribas, A.; McArthur, G.A.; Sosman, J.A.; O’Dwyer, P.J.; Lee, R.J.; Grippo, J.F.; Nolop, K.; Chapman, P.B. Inhibition of mutated, activated BRAF in metastatic melanoma. N. Engl. J. Med., 2010, 363(9), 809-819.
[http://dx.doi.org/10.1056/NEJMoa1002011] [PMID: 20818844]
[3]
Grob, J.J.; Amonkar, M.M.; Karaszewska, B.; Schachter, J.; Dummer, R.; Mackiewicz, A.; Stroyakovskiy, D.; Drucis, K.; Grange, F.; Chiarion-Sileni, V.; Rutkowski, P.; Lichinitser, M.; Levchenko, E.; Wolter, P.; Hauschild, A.; Long, G.V.; Nathan, P.; Ribas, A.; Flaherty, K.; Sun, P.; Legos, J.J.; McDowell, D.O.; Mookerjee, B.; Schadendorf, D.; Robert, C. Comparison of dabrafenib and trametinib combination therapy with vemurafenib monotherapy on health-related quality of life in patients with unresectable or metastatic cutaneous BRAF Val600-mutation-positive melanoma (COMBI-v): Results of a phase 3, open-label, randomised trial. Lancet Oncol., 2015, 16(13), 1389-1398.
[http://dx.doi.org/10.1016/S1470-2045(15)00087-X] [PMID: 26433819]
[4]
Paraiso, K.H.; Smalley, K.S. Fibroblast-mediated drug resistance in cancer. Biochem. Pharmacol., 2013, 85(8), 1033-1041.
[http://dx.doi.org/10.1016/j.bcp.2013.01.018] [PMID: 23376122]
[5]
Lu, H.; Liu, S.; Zhang, G.; Bin, W.; Zhu, Y.; Frederick, D.T.; Hu, Y.; Zhong, W.; Randell, S.; Sadek, N.; Zhang, W.; Chen, G.; Cheng, C.; Zeng, J.; Wu, L.W.; Zhang, J.; Liu, X.; Xu, W.; Krepler, C.; Sproesser, K.; Xiao, M.; Miao, B.; Liu, J.; Song, C.D.; Liu, J.Y.; Karakousis, G.C.; Schuchter, L.M.; Lu, Y.; Mills, G.; Cong, Y.; Chernoff, J.; Guo, J.; Boland, G.M.; Sullivan, R.J.; Wei, Z.; Field, J.; Amaravadi, R.K.; Flaherty, K.T.; Herlyn, M.; Xu, X.; Guo, W. PAK signalling drives acquired drug resistance to MAPK inhibitors in BRAF-mutant melanomas. Nature, 2017, 550(7674), 133-136.
[http://dx.doi.org/10.1038/nature24040] [PMID: 28953887]
[6]
Aloia, A.; Müllhaupt, D.; Chabbert, C.D.; Eberhart, T.; Flueckiger, S.; Vukolic, A. A fatty acid oxidation-dependent metabolic shift regulates the adaptation of BRAF-mutated melanoma to MAPK inhibitors. Clin Cancer Res., 2019, pii:. clincanres.0253.2019.
[7]
Hofmann, U.B.; Westphal, J.R.; Van Muijen, G.N.P.; Ruiter, D.J. Matrix metalloproteinases in human melanoma. J. Invest. Dermatol., 2000, 115(3), 337-344.
[http://dx.doi.org/10.1046/j.1523-1747.2000.00068.x] [PMID: 10951266]
[8]
Gross, J.; Lapiere, C.M. Collagenolytic activity in amphibian tissues: A tissue culture assay. Proc. Natl. Acad. Sci. USA, 1962, 48, 1014-1022.
[http://dx.doi.org/10.1073/pnas.48.6.1014] [PMID: 13902219]
[9]
Moro, N.; Mauch, C.; Zigrino, P. Metalloproteinases in melanoma. Eur. J. Cell Biol., 2014, 93(1-2), 23-29.
[http://dx.doi.org/10.1016/j.ejcb.2014.01.002] [PMID: 24530009]
[10]
Surgucheva, I.G.; Sivak, J.M.; Fini, M.E.; Palazzo, R.E.; Surguchov, A.P. Effect of g-synuclein expression on matrix metalloproteinases. Arch. Biochem. Biophys., 2003, 410, 167-176.
[http://dx.doi.org/10.1016/S0003-9861(02)00664-1] [PMID: 12559990]
[11]
Iida, J.; Wilhelmson, K.L.; Price, M.A.; Wilson, C.M.; Pei, D.; Furcht, L.T.; McCarthy, J.B. Membrane type-1 matrix metalloproteinase promotes human melanoma invasion and growth. J. Invest. Dermatol., 2004, 122(1), 167-176.
[http://dx.doi.org/10.1046/j.0022-202X.2003.22114.x] [PMID: 14962105]
[12]
Surgucheva, I.; Chidambaram, K.; Willoughby, D.A.; Surguchov, A. MicroRNA regulates MMP-9 expression. J. Ocular Biol. Diseases Bioinform., 2010, 3, 41-52.
[13]
Sandri, S.; Faião-Flores, F.; Tiago, M.; Pennacchi, P.C.; Massaro, R.R.; Alves-Fernandes, D.K.; Berardinelli, G.N.; Evangelista, A.F.; de Lima Vazquez, V.; Reis, R.M.; Maria-Engler, S.S. Vemurafenib resistance increases melanoma invasiveness and modulates the tumor microenvironment by MMP-2 upregulation. Pharmacol. Res., 2016, 111, 523-533.
[http://dx.doi.org/10.1016/j.phrs.2016.07.017] [PMID: 27436149]
[14]
Perrone, D.; Ardito, F.; Giannatempo, G.; Dioguardi, M.; Troiano, G.; Lo Russo, L.; DE Lillo, A.; Laino, L.; Lo Muzio, L. Biological and therapeutic activities, and anticancer properties of curcumin. Exp. Ther. Med., 2015, 10(5), 1615-1623.
[http://dx.doi.org/10.3892/etm.2015.2749] [PMID: 26640527]
[15]
Lelli, D.; Pedone, C.; Sahebkar, A. Curcumin and treatment of melanoma: The potential role of microRNAs. Biomed. Pharmacother., 2017, 88, 832-834.
[http://dx.doi.org/10.1016/j.biopha.2017.01.078] [PMID: 28167449]
[16]
Vollono, L.; Falconi, M.; Gaziano, R.; Iacovelli, F.; Dika, E.; Terracciano, C.; Bianchi, L.; Campione, E. Potential of curcumin in skin disorders. Nutrients, 2019, 11(9), E2169
[http://dx.doi.org/10.3390/nu11092169] [PMID: 31509968]
[17]
Panda, A.K.; Chakraborty, D.; Sarkar, I.; Khan, T.; Sa, G. New insights into therapeutic activity and anticancer properties of curcumin. J. Exp. Pharmacol., 2017, 9, 31-45.
[http://dx.doi.org/10.2147/JEP.S70568] [PMID: 28435333]
[18]
Quincoces, J.A.; Maria, D.A.; Rando, D.G.; Martins, C.A.; Souza, P.O. Methods to prepare penta-1,4-dien-3-ones and substituted cyclohexanones and derivatives with antitumoral and antiparasitic properties, the compounds and their uses., U.S. Patent 8,859,625 B2. 2014.
[19]
Quincoces, J.A.; Maria, D.A.; Rando, D.G.; Pardi, P.C.; Santos, R.P.; Faião-Flores, F. Pharmaceutical composition and use of the pharmaceutical composition for the treatment, prophylaxis or prevention of neoplastic diseases in humans and animals. , U.S. Patent 9,381,169 B2,. 2018.
[20]
Paulino, N.; Paulino, A.S.; Diniz, S.N.; de Mendonça, S.; Gonçalves, I.D.; Faião Flores, F.; Santos, R.P.; Rodrigues, C.; Pardi, P.C.; Quincoces Suarez, J.A. Evaluation of the anti-inflammatory action of curcumin analog (DM1): Effect on iNOS and COX-2 gene expression and autophagy pathways. Bioorg. Med. Chem., 2016, 24(8), 1927-1935.
[http://dx.doi.org/10.1016/j.bmc.2016.03.024] [PMID: 27010501]
[21]
Faião-Flores, F.; Suarez, J.A.; Soto-Cerrato, V.; Espona-Fiedler, M.; Pérez-Tomás, R.; Maria, D.A. Bcl-2 family proteins and cytoskeleton changes involved in DM-1 cytotoxic effect on melanoma cells. Tumour Biol., 2013, 34(2), 1235-1243.
[http://dx.doi.org/10.1007/s13277-013-0666-6] [PMID: 23341182]
[22]
Faião-Flores, F.; Suarez, J.A.; Maria-Engler, S.S.; Soto-Cerrato, V.; Pérez-Tomás, R.; Maria, D.A. The curcumin analog DM-1 induces apoptotic cell death in melanoma. Tumour Biol., 2013, 34(2), 1119-1129.
[http://dx.doi.org/10.1007/s13277-013-0653-y] [PMID: 23359272]
[23]
Faião-Flores, F.; Quincoces Suarez, J.A.; Fruet, A.C.; Maria-Engler, S.S.; Pardi, P.C.; Maria, D.A. Curcumin analog DM-1 in monotherapy or combinatory treatment with dacarbazine as a strategy to inhibit in vivo melanoma progression. PLoS One, 2015, 10(3), e0118702
[http://dx.doi.org/10.1371/journal.pone.0118702] [PMID: 25742310]
[24]
Oliveira, É.A.; Lima, D.S.; Cardozo, L.E.; Souza, G.F.; de Souza, N.; Alves-Fernandes, D.K. Toxicogenomic and bioinformatics platforms to identify key molecular mechanisms of a curcuminanalogue DM-1 toxicity in melanoma cells. Pharmacol. Res., 2017, 125(Pt B), 178-187.
[25]
Bussolino, F.; De Rossi, M.; Sica, A.; Colotta, F.; Wang, J.M.; Bocchietto, E.; Padura, I.M.; Bosia, A.; DeJana, E.; Mantovani, A. Murine endothelioma cell lines transformed by polyoma middle T oncogene as target for and producers of cytokines. J. Immunol., 1991, 147(7), 2122-2129.
[PMID: 1918946]
[26]
Williams, R.L.; Courtneidge, S.A.; Wagner, E.F. Embryonic lethalities and endothelial tumors in chimeric mice expressing polyoma virus middle T oncogene. Cell, 1988, 52(1), 121-131.
[http://dx.doi.org/10.1016/0092-8674(88)90536-3] [PMID: 3345558]
[27]
Uphoff, C.C.; Drexler, H.G. Detecting mycoplasma contamination in cell cultures by polymerase chain reaction. Methods Mol. Biol., 2011, 731, 93-103.
[http://dx.doi.org/10.1007/978-1-61779-080-5_8] [PMID: 21516400]
[28]
Tabatabaei-Qomi, R.; Sheykh-Hasan, M.; Fazaely, H.; Kalhor, N.; Ghiasi, M. Development of a PCR assay to detect mycoplasma contamination in cord blood hematopoietic stem cells. Iran. J. Microbiol., 2014, 6(4), 281-284.
[PMID: 25802713]
[29]
Brohem, C.A.; Massaro, R.R.; Tiago, M.; Marinho, C.E.; Jasiulionis, M.G.; de Almeida, R.L.; Rivelli, D.P.; Albuquerque, R.C.; de Oliveira, T.F.; de Melo Loureiro, A.P.; Okada, S.; Soengas, M.S.; de Moraes Barros, S.B.; Maria-Engler, S.S. Proteasome inhibition and ROS generation by 4-nerolidylcatechol induces melanoma cell death. Pigment Cell Melanoma Res., 2012, 25(3), 354-369.
[http://dx.doi.org/10.1111/j.1755-148X.2012.00992.x] [PMID: 22372875]
[30]
Pennacchi, P.C.; de Almeida, M.E.; Gomes, O.L.; Faião-Flores, F.; de Araújo Crepaldi, M.C.; Dos Santos, M.F.; de Moraes Barros, S.B.; Maria-Engler, S.S. Glycated reconstructed human skin as a platform to study the pathogenesis of skin aging. Tissue Eng. Part A, 2015, 21(17-18), 2417-2425.
[http://dx.doi.org/10.1089/ten.tea.2015.0009] [PMID: 26132636]
[31]
Franken, N.A.; Rodermond, H.M.; Stap, J.; Haveman, J.; van Bree, C. Clonogenic assay of cells in vitro. Nat. Protoc., 2006, 1(5), 2315-2319.
[http://dx.doi.org/10.1038/nprot.2006.339] [PMID: 17406473]
[32]
Paraiso, K.H.T.; Fedorenko, I.V.; Cantini, L.P.; Munko, A.C.; Hall, M.; Sondak, V.K.; Messina, J.L.; Flaherty, K.T.; Smalley, K.S. Recovery of phospho-ERK activity allows melanoma cells to escape from BRAF inhibitor therapy. Br. J. Cancer, 2010, 102(12), 1724-1730.
[http://dx.doi.org/10.1038/sj.bjc.6605714] [PMID: 20531415]
[33]
Koo, H.J.; Shin, S.; Choi, J.Y.; Lee, K.H.; Kim, B.T.; Choe, Y.S. Introduction of methyl groups at C2 and C6 positions enhances the antiangiogenesis activity of curcumin. Sci. Rep., 2015, 5, 14205.
[http://dx.doi.org/10.1038/srep14205] [PMID: 26391485]
[34]
Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Method. Methods, 2001, 25(4), 402-408.
[http://dx.doi.org/10.1006/meth.2001.1262] [PMID: 11846609]
[35]
Kunnumakkara, A.B.; Anand, P.; Aggarwal, B.B. Curcumin inhibits proliferation, invasion, angiogenesis and metastasis of different cancers through interaction with multiple cell signaling proteins. Cancer Lett., 2008, 269(2), 199-225.
[http://dx.doi.org/10.1016/j.canlet.2008.03.009] [PMID: 18479807]
[36]
Leonardo, G.P. Validation of the bioanalytical, pharmacokinetic and biodistribution method of DM-1 in mice., Master’s Thesis, Universidade Bandeirante de Sao Paulo: Sao Paulo,. 2010.
[37]
Leung, M.H.M.; Kee, T.W. Effective stabilization of curcumin by association to plasma proteins: Human serum albumin and fibrinogen. Langmuir, 2009, 25(10), 5773-5777.
[http://dx.doi.org/10.1021/la804215v] [PMID: 19320475]
[38]
Friedl, P.; Wolf, K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev. Cancer, 2003, 3(5), 362-374.
[http://dx.doi.org/10.1038/nrc1075] [PMID: 12724734]
[39]
Yadav, B.; Taurin, S.; Larsen, L.; Rosengren, R.J. RL71, a second-generation curcumin analog, induces apoptosis and downregulates Akt in ER-negative breast cancer cells. Int. J. Oncol., 2012, 41(3), 1119-1127.
[http://dx.doi.org/10.3892/ijo.2012.1521] [PMID: 22710975]
[40]
Shimazu, K.; Inoue, M.; Sugiyama, S.; Fukuda, K.; Yoshida, T.; Taguchi, D.; Uehara, Y.; Kuriyama, S.; Tanaka, M.; Miura, M.; Nanjyo, H.; Iwabuchi, Y.; Shibata, H. Curcumin analog, GO-Y078, overcomes resistance to tumor angiogenesis inhibitors. Cancer Sci., 2018, 109(10), 3285-3293.
[http://dx.doi.org/10.1111/cas.13741] [PMID: 30024080]
[41]
Guo, C.; Wang, L.; Jiang, B.; Shi, D. Bromophenol curcumin analog BCA-5 exerts an antiangiogenic effect through the HIF-1α/VEGF/Akt signaling pathway in human umbilical vein endothelial cells. Anticancer Drugs, 2018, 29(10), 965-974.
[http://dx.doi.org/10.1097/CAD.0000000000000671] [PMID: 30335638]
[42]
Morley, M.E.; Riches, K.; Peers, C.; Porter, K.E. Hypoxic inhibition of human cardiac fibroblast invasion and MMP-2 activation may impair adaptive myocardial remodelling. Biochem. Soc. Trans., 2007, 35(Pt 5), 905-907.
[http://dx.doi.org/10.1042/BST0350905] [PMID: 17956242]
[43]
Nelson, K.M.; Dahlin, J.L.; Bisson, J.; Graham, J.; Pauli, G.F.; Walters, M.A. The essential medicinal chemistry of curcumin. J. Med. Chem., 2017, 60(5), 1620-1637.
[http://dx.doi.org/10.1021/acs.jmedchem.6b00975] [PMID: 28074653]
[44]
Vemula, V.R.; Lagishetty, V.; Lingala, S. Solubility enhancement techniques. Int. J. Pharm. Sci. Rev. Res., 2010, 5(1), 41-51.
[45]
Savjani, K.T.; Gajjar, A.K.; Savjani, J.K. Drug solubility: Importance and enhancement techniques. ISRN Pharm., 2012, 2012, 195727
[http://dx.doi.org/10.5402/2012/195727] [PMID: 22830056]
[46]
Faião-Flores, F.; Suarez, J.A.; Pardi, P.C.; Maria, D.A. DM-1, sodium 4-[5-(4-hydroxy-3-methoxyphenyl)-3-oxo-penta-1,4-dienyl]-2-methoxy-phenolate: A curcumin analog with a synergic effect in combination with paclitaxel in breast cancer treatment. Tumour Biol., 2012, 33(3), 775-785.
[http://dx.doi.org/10.1007/s13277-011-0293-z] [PMID: 22194218]
[47]
Abel, E.V.; Basile, K.J.; Kugel, C.H., 3rd; Witkiewicz, A.K.; Le, K.; Amaravadi, R.K. Melanoma adapts to RAF/MEK inhibitors through FOXD3-mediated upregulation of ERBB3. JVI Insight, 2013, 123(5), 2155-2168.
[48]
Ferguson, J.; Arozarena, I.; Ehrhardt, M.; Wellbrock, C. Combination of MEK and SRC inhibition suppresses melanoma cell growth and invasion. Oncogene, 2013, 32(1), 86-96.
[http://dx.doi.org/10.1038/onc.2012.25] [PMID: 22310287]
[49]
Sabbatino, F.; Wang, Y.; Wang, X.; Flaherty, K.T.; Yu, L.; Pepin, D.; Scognamiglio, G.; Pepe, S.; Kirkwood, J.M.; Cooper, Z.A.; Frederick, D.T.; Wargo, J.A.; Ferrone, S.; Ferrone, C.R. PDGFRα up-regulation mediated by sonic hedgehog pathway activation leads to BRAF inhibitor resistance in melanoma cells with BRAF mutation. Oncotarget, 2014, 5(7), 1926-1941.
[http://dx.doi.org/10.18632/oncotarget.1878] [PMID: 24732172]
[50]
Smith, M.P.; Brunton, H.; Rowling, E.J.; Ferguson, J.; Arozarena, I.; Miskolczi, Z.; Lee, J.L.; Girotti, M.R.; Marais, R.; Levesque, M.P.; Dummer, R.; Frederick, D.T.; Flaherty, K.T.; Cooper, Z.A.; Wargo, J.A.; Wellbrock, C. Inhibiting drivers of non-mutational drug tolerance is a salvage strategy for targeted melanoma therapy. Cancer Cell, 2016, 29(3), 270-284.
[http://dx.doi.org/10.1016/j.ccell.2016.02.003] [PMID: 26977879]
[51]
Calvani, M.; Bianchini, F.; Taddei, M.L.; Becatti, M.; Giannoni, E.; Chiarugi, P.; Calorini, L. Etoposide-Bevacizumab a new strategy against human melanoma cells expressing stem-like traits. Oncotarget, 2016, 7(32), 51138-51149.
[http://dx.doi.org/10.18632/oncotarget.9939] [PMID: 27303923]
[52]
Kumar, D.; Gorain, M.; Kundu, G.; Kundu, G.C. Therapeutic implications of cellular and molecular biology of cancer stem cells in melanoma. Mol. Cancer, 2017, 16(1), 7.
[http://dx.doi.org/10.1186/s12943-016-0578-3] [PMID: 28137308]
[53]
Rappa, G.; Fodstad, O.; Lorico, A. The stem cell-associated antigen CD133 (Prominin-1) is a molecular therapeutic target for metastatic melanoma. Stem Cells, 2008, 26(12), 3008-3017.
[http://dx.doi.org/10.1634/stemcells.2008-0601] [PMID: 18802032]
[54]
Kakavand, H.; Wilmott, J.S.; Menzies, A.M.; Vilain, R.; Haydu, L.E.; Yearley, J.H.; Thompson, J.F.; Kefford, R.F.; Hersey, P.; Long, G.V.; Scolyer, R.A. PD-L1 expression and tumor-infiltrating lymphocytes define different subsets of MAPK inhibitor-treated melanoma patients. Clin. Cancer Res., 2015, 21(14), 3140-3148.
[http://dx.doi.org/10.1158/1078-0432.CCR-14-2023] [PMID: 25609064]
[55]
Johnson, D.B.; Flaherty, K.T.; Weber, J.S.; Infante, J.R.; Kim, K.B.; Kefford, R.F.; Hamid, O.; Schuchter, L.; Cebon, J.; Sharfman, W.H.; McWilliams, R.R.; Sznol, M.; Lawrence, D.P.; Gibney, G.T.; Burris, H.A., III; Falchook, G.S.; Algazi, A.; Lewis, K.; Long, G.V.; Patel, K.; Ibrahim, N.; Sun, P.; Little, S.; Cunningham, E.; Sosman, J.A.; Daud, A.; Gonzalez, R. Combined BRAF (Dabrafenib) and MEK inhibition (Trametinib) in patients with BRAFV600-mutant melanoma experiencing progression with single-agent BRAF inhibitor. J. Clin. Oncol., 2014, 32(33), 3697-3704.
[http://dx.doi.org/10.1200/JCO.2014.57.3535] [PMID: 25287827]
[56]
Rossi, A.; Roberto, M.; Panebianco, M.; Botticelli, A.; Mazzuca, F.; Marchetti, P. Drug resistance of BRAF-mutant melanoma: Review of up-to-date mechanisms of action and promising targeted agents. Eur. J. Pharmacol., 2019, 862, 172621
[http://dx.doi.org/10.1016/j.ejphar.2019.172621] [PMID: 31446019]
[57]
Kuttan, R.; Bhanumathy, P.; Nirmala, K.; George, M.C. Potential anticancer activity of turmeric (Curcuma longa). Cancer Lett., 1985, 29(2), 197-202.
[http://dx.doi.org/10.1016/0304-3835(85)90159-4] [PMID: 4075289]
[58]
Glaser, J.; Holzgrabe, U. Focus on PAINS: False friends in the quest for selective anti-protozoal lead structures from nature? MedChemComm, 2016, 7, 214-223.
[http://dx.doi.org/10.1039/C5MD00481K]
[59]
Liu, T.Y.; Tan, Z.J.; Jiang, L.; Gu, J.F.; Wu, X.S.; Cao, Y.; Li, M.L.; Wu, K.J.; Liu, Y.B. Curcumin induces apoptosis in gallbladder carcinoma cell line GBC-SD cells. Cancer Cell Int., 2013, 13(1), 64.
[http://dx.doi.org/10.1186/1475-2867-13-64] [PMID: 23802572]
[60]
Chendil, D.; Ranga, R.S.; Meigooni, D.; Sathishkumar, S.; Ahmed, M.M. Curcumin confers radiosensitizing effect in prostate cancer cell line PC-3. Oncogene, 2004, 23(8), 1599-1607.
[http://dx.doi.org/10.1038/sj.onc.1207284] [PMID: 14985701]
[61]
Xia, Y.Q.; Wei, X.Y.; Li, W.L.; Kanchana, K.; Xu, C.C.; Chen, D.H.; Chou, P.H.; Jin, R.; Wu, J.Z.; Liang, G. Curcumin analogue A501 induces G2/M arrest and apoptosis in non-small cell lung cancer cells. Asian Pac. J. Cancer Prev., 2014, 15(16), 6893-6898.
[http://dx.doi.org/10.7314/APJCP.2014.15.16.6893] [PMID: 25169542]
[62]
Hutzen, B.; Friedman, L.; Sobo, M.; Lin, L.; Cen, L.; De Angelis, S.; Yamakoshi, H.; Shibata, H.; Iwabuchi, Y.; Lin, J. Curcumin analogue GO-Y030 inhibits STAT3 activity and cell growth in breast and pancreatic carcinomas. Int. J. Oncol., 2009, 35(4), 867-872.
[PMID: 19724924]
[63]
Tima, S.; Ichikawa, H.; Ampasavate, C.; Okonogi, S.; Anuchapreeda, S. Inhibitory effect of turmeric curcuminoids on FLT3 expression and cell cycle arrest in the FLT3-overexpressing EoL-1 leukemic cell line. J. Nat. Prod., 2014, 77(4), 948-954.
[http://dx.doi.org/10.1021/np401028h] [PMID: 24689857]
[64]
Guan, F.; Ding, Y.; Zhang, Y.; Zhou, Y.; Li, M.; Wang, C. Curcumin suppresses proliferation and migration of MDA-MB-231 breast cancer cells through autophagy-dependent AKT degradation. PLoS One, 2016, 11(1), e0146553
[http://dx.doi.org/10.1371/journal.pone.0146553] [PMID: 26752181]
[65]
Lin, L.; Hutzen, B.; Ball, S.; Foust, E.; Sobo, M.; Deangelis, S.; Pandit, B.; Friedman, L.; Li, C.; Li, P.K.; Fuchs, J.; Lin, J. New curcumin analogues exhibit enhanced growth-suppressive activity and inhibit AKT and signal transducer and activator of transcription 3 phosphorylation in breast and prostate cancer cells. Cancer Sci., 2009, 100(9), 1719-1727.
[http://dx.doi.org/10.1111/j.1349-7006.2009.01220.x] [PMID: 19558577]
[66]
Nishida, N.; Yano, H.; Nishida, T.; Kamura, T.; Kojiro, M. Angiogenesis in cancer. Vasc. Health Risk Manag., 2006, 2(3), 213-219.
[http://dx.doi.org/10.2147/vhrm.2006.2.3.213] [PMID: 17326328]
[67]
Singh, A.K.; Sidhu, G.S.; Deepa, T.; Maheshwari, R.K. Curcumin inhibits the proliferation and cell cycle progression of human umbilical vein endothelial cell. Cancer Lett., 1996, 107(1), 109-115.
[http://dx.doi.org/10.1016/0304-3835(96)04357-1] [PMID: 8913274]
[68]
Nagaraju, G.P.; Zhu, S.; Ko, J.E.; Ashritha, N.; Kandimalla, R.; Snyder, J.P.; Shoji, M.; El-Rayes, B.F. Antiangiogenic effects of a novel synthetic curcumin analogue in pancreatic cancer. Cancer Lett., 2015, 357(2), 557-565.
[http://dx.doi.org/10.1016/j.canlet.2014.12.007] [PMID: 25497868]
[69]
Nikkola, J.; Vihinen, P.; Vuoristo, M.S.; Kellokumpu-Lehtinen, P.; Kähäri, V.M.; Pyrhönen, S. High serum levels of matrix metalloproteinase-9 and matrix metalloproteinase-1 are associated with rapid progression in patients with metastatic melanoma. Clin. Cancer Res., 2005, 11(14), 5158-5166.
[http://dx.doi.org/10.1158/1078-0432.CCR-04-2478] [PMID: 16033831]
[70]
Airola, K.; Karonen, T.; Vaalamo, M.; Lehti, K.; Lohi, J.; Kariniemi, A.L.; Keski-Oja, J.; Saarialho-Kere, U.K. Expression of collagenases-1 and -3 and their inhibitors TIMP-1 and -3 correlates with the level of invasion in malignant melanomas. Br. J. Cancer, 1999, 80(5-6), 733-743.
[http://dx.doi.org/10.1038/sj.bjc.6690417] [PMID: 10360651]
[71]
Redondo, P.; Lloret, P.; Idoate, M.; Inoges, S. Expression and serum levels of MMP-2 and MMP-9 during human melanoma progression. Clin. Exp. Dermatol., 2005, 30(5), 541-545.
[http://dx.doi.org/10.1111/j.1365-2230.2005.01849.x] [PMID: 16045689]

Rights & Permissions Print Cite
Article Metrics
38
© 2024 Bentham Science Publishers | Privacy Policy