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Current Cancer Drug Targets

Editor-in-Chief

ISSN (Print): 1568-0096
ISSN (Online): 1873-5576

Review Article

Insight into the Basic Mechanisms and Various Modulation Strategies Involved in Cancer Drug Resistance

Author(s): Devdhar Yadav, Gudhanti Siva Naga Koteswara Rao*, Deepika Paliwal, Amit Singh and Sumbul Shadab

Volume 23, Issue 10, 2023

Published on: 31 May, 2023

Page: [778 - 791] Pages: 14

DOI: 10.2174/1568009623666230508110258

Price: $65

Abstract

It is possible for tumors to develop resistance to currently used drugs. However, its increasing incidence necessitates further study and the development of novel therapies This review explores our current understanding of the factors that enable drug resistance, which include, inactivation of the drug, reduced drug uptake, increased drug efflux, metabolic effect, inhibition of apoptosis, epithelialmesenchymal transition, modified membrane transport, and heterogeneity of inherent tumor cell. This manuscript will also explore some genetic and epigenetic alterations that may encourage drug resistance and fundamental mechanisms of the reluctance of drugs in leukemia, ovarian and breast cancer and it concludes with a few solutions for managing drug resistance.

Graphical Abstract

[1]
Goldie, J.H.; Coldman, A.J. The genetic origin of drug resistance in neoplasms: Implications for systemic therapy. Cancer Res., 1984, 44(9), 3643-3653.
[PMID: 6744284]
[2]
Ramirez, M.S.; Tolmasky, M.E. Aminoglycoside modifying enzymes. Drug Resist. Updat., 2010, 13(6), 151-171.
[http://dx.doi.org/10.1016/j.drup.2010.08.003] [PMID: 20833577]
[3]
Greaves, M.; Maley, C.C. Clonal evolution in cancer. Nature, 2012, 481(7381), 306-313.
[http://dx.doi.org/10.1038/nature10762] [PMID: 22258609]
[4]
Nowell, P.C. The clonal evolution of tumor cell populations. Science, 1976, 194(4260), 23-28.
[http://dx.doi.org/10.1126/science.959840] [PMID: 959840]
[5]
Goldie, J.H.; Coldman, A.J. A mathematic model for relating the drug sensitivity of tumors to their spontaneous mutation rate. Cancer Treat. Rep., 1979, 63(11-12), 1727-1733.
[PMID: 526911]
[6]
Goldie, J.H.; Coldman, A.J. Genetic instability in the development of drug resistance. Semin. oncol., 1985, 12(3), 222-230.
[7]
Coldman, A.; Goldie, J. A stochastic model for the origin and treatment of tumors containing drug-resistant cells. Bull. Math. Biol., 1986, 48(3-4), 279-292.
[http://dx.doi.org/10.1016/S0092-8240(86)90028-5] [PMID: 3828558]
[8]
Woodhouse, J.R.; Ferry, D.R. The genetic basis of resistance to cancer chemotherapy. Ann. Med., 1995, 27(2), 157-167.
[http://dx.doi.org/10.3109/07853899509031953] [PMID: 7632408]
[9]
Angerer, W.P. An explicit representation of the Luria-Delbrück distribution. J. Math. Biol., 2001, 42(2), 145-174.
[http://dx.doi.org/10.1007/s002850000053] [PMID: 11261316]
[10]
Dewanji, A.; Luebeck, E.G.; Moolgavkar, S.H. A generalized Luria–Delbrück model. Math. Biosci., 2005, 197(2), 140-152.
[http://dx.doi.org/10.1016/j.mbs.2005.07.003] [PMID: 16137718]
[11]
Frank, S.A. Somatic mosaicism and cancer: Inference based on a conditional Luria–Delbrück distribution. J. Theor. Biol., 2003, 223(4), 405-412.
[http://dx.doi.org/10.1016/S0022-5193(03)00117-6] [PMID: 12875820]
[12]
Haeno, H.; Iwasa, Y.; Michor, F. The evolution of two mutations during clonal expansion. Genetics, 2007, 177(4), 2209-2221.
[http://dx.doi.org/10.1534/genetics.107.078915] [PMID: 18073428]
[13]
Iwasa, Y.; Nowak, M.A.; Michor, F. Evolution of resistance during clonal expansion. Genetics, 2006, 172(4), 2557-2566.
[http://dx.doi.org/10.1534/genetics.105.049791] [PMID: 16636113]
[14]
Komarova, N.L.; Mironov, V. On the role of endothelial progenitor cells in tumor neovascularization. J. Theor. Biol., 2005, 235(3), 338-349.
[http://dx.doi.org/10.1016/j.jtbi.2005.01.014] [PMID: 15882696]
[15]
Komarova, N.L.; Wodarz, D. Drug resistance in cancer: Principles of emergence and prevention. Proc. Natl. Acad. Sci. USA, 2005, 102(27), 9714-9719.
[http://dx.doi.org/10.1073/pnas.0501870102] [PMID: 15980154]
[16]
Beketic-Oreskovic, L.; Durán, G.E.; Chen, G.; Dumontet, C.; Sikic, B.I. Decreased mutation rate for cellular resistance to doxorubicin and suppression of mdr1 gene activation by the cyclosporin PSC 833. J. Natl. Cancer Inst., 1995, 87(21), 1593-1602.
[http://dx.doi.org/10.1093/jnci/87.21.1593] [PMID: 7563202]
[17]
Chen, K.G.; Jaffrézou, J.P.; Fleming, W.H.; Durán, G.E.; Sikic, B.I. Prevalence of multidrug resistance related to activation of the mdr1 gene in human sarcoma mutants derived by single-step doxorubicin selection. Cancer Res., 1994, 54(18), 4980-4987.
[PMID: 7915196]
[18]
Dumontet, C.; Duran, G.E.; Steger, K.A.; Beketic-Oreskovic, L.; Sikic, B.I. Resistance mechanisms in human sarcoma mutants derived by single-step exposure to paclitaxel (Taxol). Cancer Res., 1996, 56(5), 1091-1097.
[PMID: 8640766]
[19]
Jaffrézou, J.P.; Chen, G.; Durán, G.E.; Kühl, J.S.; Sikic, B.I. Mutation rates and mechanisms of resistance to etoposide determined from fluctuation analysis. J. Natl. Cancer Inst., 1994, 86(15), 1152-1158.
[http://dx.doi.org/10.1093/jnci/86.15.1152] [PMID: 8028036]
[20]
Matei, D.; Fang, F.; Shen, C.; Schilder, J.; Arnold, A.; Zeng, Y.; Berry, W.A.; Huang, T.; Nephew, K.P. Epigenetic resensitization to platinum in ovarian cancer. Cancer Res., 2012, 72(9), 2197-2205.
[http://dx.doi.org/10.1158/0008-5472.CAN-11-3909] [PMID: 22549947]
[21]
Balch, C.; Nephew, K.P. Epigenetic targeting therapies to overcome chemotherapy resistance. Adv. Exp. Med. Biol., 2013, 754, 285-311.
[http://dx.doi.org/10.1007/978-1-4419-9967-2_14]
[22]
Wilting, R.H.; Dannenberg, J.H. Epigenetic mechanisms in tumorigenesis, tumor cell heterogeneity and drug resistance. Drug Resist. Updat., 2012, 15(1-2), 21-38.
[http://dx.doi.org/10.1016/j.drup.2012.01.008] [PMID: 22356866]
[23]
Zeller, C.; Dai, W.; Steele, N.L.; Siddiq, A.; Walley, A.J.; Wilhelm-Benartzi, C.S.M.; Rizzo, S.; van der Zee, A.; Plumb, J.A.; Brown, R. Candidate DNA methylation drivers of acquired cisplatin resistance in ovarian cancer identified by methylome and expression profiling. Oncogene, 2012, 31(42), 4567-4576.
[http://dx.doi.org/10.1038/onc.2011.611] [PMID: 22249249]
[24]
Deaton, A.M.; Bird, A. CpG islands and the regulation of transcription. Genes Dev., 2011, 25(10), 1010-1022.
[http://dx.doi.org/10.1101/gad.2037511] [PMID: 21576262]
[25]
Bhatla, T.; Wang, J.; Morrison, D.J.; Raetz, E.A.; Burke, M.J.; Brown, P.; Carroll, W.L. Epigenetic reprogramming reverses the relapse-specific gene expression signature and restores chemosensitivity in childhood B-lymphoblastic leukemia. Blood, 2012, 119(22), 5201-5210.
[http://dx.doi.org/10.1182/blood-2012-01-401687] [PMID: 22496163]
[26]
Issa, M.E.; Takhsha, F.S.; Chirumamilla, C.S.; Perez-Novo, C.; Vanden Berghe, W.; Cuendet, M. Epigenetic strategies to reverse drug resistance in heterogeneous multiple myeloma. Clin. Epigenetics, 2017, 9(1), 17.
[http://dx.doi.org/10.1186/s13148-017-0319-5] [PMID: 28203307]
[27]
Yagüe, E.; Raguz, S. Drug resistance in cancer. Br. J. Cancer, 2005, 93(9), 973-976.
[http://dx.doi.org/10.1038/sj.bjc.6602821] [PMID: 16234820]
[28]
Nicholson, R.I.; Gee, J.M.W.; Knowlden, J.; McClelland, R.; Madden, T.A.; Barrow, D.; Hutcheson, I. The biology of antihormone failure in breast cancer. Breast Cancer Res. Treat., 2003, 80(S1)(Suppl. 1), 29-34.
[http://dx.doi.org/10.1023/A:1025467500433] [PMID: 14535532]
[29]
McDonald, S.L.; Stevenson, D.A.J.; Moir, S.E.; Hutcheon, A.W.; Haites, N.E.; Heys, S.D.; Schofield, A.C. Genomic changes identified by comparative genomic hybridisation in docetaxel-resistant breast cancer cell lines. Eur. J. Cancer, 2005, 41(7), 1086-1094.
[http://dx.doi.org/10.1016/j.ejca.2005.01.018] [PMID: 15862759]
[30]
Agarwal, R.; Kaye, S.B. Ovarian cancer: Strategies for overcoming resistance to chemotherapy. Nat. Rev. Cancer, 2003, 3(7), 502-516.
[http://dx.doi.org/10.1038/nrc1123] [PMID: 12835670]
[31]
Pluen, A.; Boucher, Y.; Ramanujan, S.; McKee, T.D.; Gohongi, T.; di Tomaso, E.; Brown, E.B.; Izumi, Y.; Campbell, R.B.; Berk, D.A.; Jain, R.K. Role of tumor–host interactions in interstitial diffusion of macromolecules: Cranial vs. subcutaneous tumors. Proc. Natl. Acad. Sci. USA, 2001, 98(8), 4628-4633.
[http://dx.doi.org/10.1073/pnas.081626898] [PMID: 11274375]
[32]
Green, S.K.; Frankel, A.; Kerbel, R.S. Adhesion-dependent multicellular drug resistance. Anticancer Drug Des., 1999, 14(2), 153-168.
[PMID: 10405642]
[33]
Longo-Sorbello, G.S. Current understanding of methotrexate pharmacology and efficacy in acute leukemias. Use of newer antifolates in clinical trials. Haematologica, 2001, 86(2), 121-127.
[34]
Gottesman, M.M. Mechanisms of cancer drug resistance. Annu. Rev. Med., 2002, 53(1), 615-627.
[http://dx.doi.org/10.1146/annurev.med.53.082901.103929] [PMID: 11818492]
[35]
Liu, Y.Y.; Han, T.Y.; Giuliano, A.; Cabot, M.C. Ceramide glycosylation potentiates cellular multidrug resistance. FASEB J., 2001, 15(3), 719-730.
[http://dx.doi.org/10.1096/fj.00-0223com] [PMID: 11259390]
[36]
Lowe, S.W.; Ruley, H.E.; Jacks, T.; Housman, D.E. p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell, 1993, 74(6), 957-967.
[http://dx.doi.org/10.1016/0092-8674(93)90719-7] [PMID: 8402885]
[37]
Synold, T.W.; Dussault, I.; Forman, B.M. The orphan nuclear receptor SXR coordinately regulates drug metabolism and efflux. Nat. Med., 2001, 7(5), 584-590.
[http://dx.doi.org/10.1038/87912] [PMID: 11329060]
[38]
Dalton, W.S.; Scheper, R.J. Lung resistance-related protein: Determining its role in multidrug resistance. J. Natl. Cancer Inst., 1999, 91(19), 1604-1605.
[http://dx.doi.org/10.1093/jnci/91.19.1604] [PMID: 10511581]
[39]
Kast, C.; Gros, P. Topology mapping of the amino-terminal half of multidrug resistance-associated protein by epitope insertion and immunofluorescence. J. Biol. Chem., 1997, 272(42), 26479-26487.
[http://dx.doi.org/10.1074/jbc.272.42.26479] [PMID: 9334225]
[40]
Kast, C.; Gros, P. Epitope insertion favors a six transmembrane domain model for the carboxy-terminal portion of the multidrug resistance-associated protein. Biochemistry, 1998, 37(8), 2305-2313.
[http://dx.doi.org/10.1021/bi972332v] [PMID: 9485377]
[41]
Dean, M.; Moitra, K.; Allikmets, R. The human ATP‐binding cassette (ABC) transporter superfamily. Hum. Mutat., 2022, 43(9), 1162-1182.
[http://dx.doi.org/10.1002/humu.24418] [PMID: 35642569]
[42]
Juliano, R.L.; Ling, V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim. Biophys. Acta Biomembr., 1976, 455(1), 152-162.
[http://dx.doi.org/10.1016/0005-2736(76)90160-7] [PMID: 990323]
[43]
Chen, C.; Chin, J.E.; Ueda, K.; Clark, D.P.; Pastan, I.; Gottesman, M.M.; Roninson, I.B. Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell, 1986, 47(3), 381-389.
[http://dx.doi.org/10.1016/0092-8674(86)90595-7] [PMID: 2876781]
[44]
Ueda, K.; Cardarelli, C.; Gottesman, M.M.; Pastan, I. Expression of a full-length cDNA for the human “MDR1” gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc. Natl. Acad. Sci. USA, 1987, 84(9), 3004-3008.
[http://dx.doi.org/10.1073/pnas.84.9.3004] [PMID: 3472246]
[45]
Gottesman, M.M.; Hrycyna, C.A.; Schoenlein, P.V.; Germann, U.A.; Pastan, I. Genetic analysis of the multidrug transporter. Annu. Rev. Genet., 1995, 29(1), 607-649.
[http://dx.doi.org/10.1146/annurev.ge.29.120195.003135] [PMID: 8825488]
[46]
Endicott, J.A.; Ling, V. The biochemistry of P-glycoprotein-mediated multidrug resistance. Annu. Rev. Biochem., 1989, 58(1), 137-171.
[http://dx.doi.org/10.1146/annurev.bi.58.070189.001033] [PMID: 2570548]
[47]
Higgins, C.F. ABC transporters: From microorganisms to man. Annu. Rev. Cell Biol., 1992, 8(1), 67-113.
[http://dx.doi.org/10.1146/annurev.cb.08.110192.000435] [PMID: 1282354]
[48]
Gottesman, M.M.; Pastan, I.; Ambudkar, S.V. P-glycoprotein and multidrug resistance. Curr. Opin. Genet. Dev., 1996, 6(5), 610-617.
[http://dx.doi.org/10.1016/S0959-437X(96)80091-8] [PMID: 8939727]
[49]
Gottesman, M.M.; Fojo, T.; Bates, S.E. Multidrug resistance in cancer: Role of ATP–dependent transporters. Nat. Rev. Cancer, 2002, 2(1), 48-58.
[http://dx.doi.org/10.1038/nrc706] [PMID: 11902585]
[50]
Cole, S.; Bhardwaj, G.; Gerlach, J.; Mackie, J.; Grant, C.; Almquist, K.; Stewart, A.; Kurz, E.; Duncan, A.; Deeley, R. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science, 1992, 258(5088), 1650-1654.
[http://dx.doi.org/10.1126/science.1360704] [PMID: 1360704]
[51]
Borst, P.; Evers, R.; Kool, M.; Wijnholds, J. A family of drug transporters: The multidrug resistance-associated proteins. J. Natl. Cancer Inst., 2000, 92(16), 1295-1302.
[http://dx.doi.org/10.1093/jnci/92.16.1295] [PMID: 10944550]
[52]
Cole, S.P.C.; Deeley, R.G. Multidrug resistance mediated by the ATP-binding cassette transporter protein MRP. BioEssays, 1998, 20(11), 931-940.
[http://dx.doi.org/10.1002/(SICI)1521-1878(199811)20:11<931:AID-BIES8>3.0.CO;2-J] [PMID: 9872059]
[53]
Litman, T.; Druley, T.E.; Stein, W.D.; Bates, S.E. From MDR to MXR: New understanding of multidrug resistance systems, their properties and clinical significance. Cell. Mol. Life Sci., 2001, 58(7), 931-959.
[http://dx.doi.org/10.1007/PL00000912] [PMID: 11497241]
[54]
Lecureur, V.; Sun, D.; Hargrove, P.; Schuetz, E.G.; Kim, R.B.; Lan, L.B.; Schuetz, J.D. Cloning and expression of murine sister of P-glycoprotein reveals a more discriminating transporter than MDR1/P-glycoprotein. Mol. Pharmacol., 2000, 57(1), 24-35.
[PMID: 10617675]
[55]
Kool, M.; van der Linden, M.; de Haas, M.; Baas, F.; Borst, P. Expression of human MRP6, a homologue of the multidrug resistance protein gene MRP1, in tissues and cancer cells. Cancer Res., 1999, 59(1), 175-182.
[PMID: 9892204]
[56]
Nooter, K.; Westerman, A.M.; Flens, M.J.; Zaman, G.J.; Scheper, R.J.; van Wingerden, K.E.; Burger, H.; Oostrum, R.; Boersma, T.; Sonneveld, P. Expression of the multidrug resistance-associated protein (MRP) gene in human cancers. Clin. Cancer Res., 1995, 1(11), 1301-1310.
[PMID: 9815925]
[57]
Homolya, L.; Váradi, A.; Sarkadi, B. Multidrug resistance-associated proteins: Export pumps for conjugates with glutathione, glucuronate or sulfate. Biofactors, 2003, 17(1-4), 103-114.
[http://dx.doi.org/10.1002/biof.5520170111] [PMID: 12897433]
[58]
Haimeur, A.; Conseil, G.; Deeley, R.; Cole, S. The MRP-related and BCRP/ABCG2 multidrug resistance proteins: Biology, substrate specificity and regulation. Curr. Drug Metab., 2004, 5(1), 21-53.
[http://dx.doi.org/10.2174/1389200043489199] [PMID: 14965249]
[59]
Zaman, G.J.; Lankelma, J.; van Tellingen, O.; Beijnen, J.; Dekker, H.; Paulusma, C.; Oude Elferink, R.P.; Baas, F.; Borst, P. Role of glutathione in the export of compounds from cells by the multidrug-resistance-associated protein. Proc. Natl. Acad. Sci. USA, 1995, 92(17), 7690-7694.
[http://dx.doi.org/10.1073/pnas.92.17.7690] [PMID: 7644478]
[60]
Fromm, M.F.; Kauffmann, H.M.; Fritz, P.; Burk, O.; Kroemer, H.K.; Warzok, R.W.; Eichelbaum, M.; Siegmund, W.; Schrenk, D. The effect of rifampin treatment on intestinal expression of human MRP transporters. Am. J. Pathol., 2000, 157(5), 1575-1580.
[http://dx.doi.org/10.1016/S0002-9440(10)64794-3] [PMID: 11073816]
[61]
Greiner, B.; Eichelbaum, M.; Fritz, P.; Kreichgauer, H.P.; von Richter, O.; Zundler, J.; Kroemer, H.K. The role of intestinal P-glycoprotein in the interaction of digoxin and rifampin. J. Clin. Invest., 1999, 104(2), 147-153.
[http://dx.doi.org/10.1172/JCI6663] [PMID: 10411543]
[62]
Mickley, L.A.; Spengler, B.A.; Knutsen, T.A.; Biedler, J.L.; Fojo, T. Gene rearrangement: A novel mechanism for MDR-1 gene activation. J. Clin. Invest., 1997, 99(8), 1947-1957.
[http://dx.doi.org/10.1172/JCI119362] [PMID: 9109439]
[63]
Hoffmeyer, S.; Burk, O.; von Richter, O.; Arnold, H.P.; Brockmöller, J.; Johne, A.; Cascorbi, I.; Gerloff, T.; Roots, I.; Eichelbaum, M.; Brinkmann, U. Functional polymorphisms of the human multidrug-resistance gene: Multiple sequence variations and correlation of one allele with P-glycoprotein expression and activity in vivo. Proc. Natl. Acad. Sci. USA, 2000, 97(7), 3473-3478.
[http://dx.doi.org/10.1073/pnas.97.7.3473] [PMID: 10716719]
[64]
Rosell, R.; Taron, M.; Ariza, A.; Barnadas, A.; Mate, J.L.; Reguart, N.; Margelí, M.; Felip, E.; Méndez, P.; García-Campelo, R. Molecular predictors of response to chemotherapy in lung cancer. Seminars in oncology, 2004, 31(Suppl 1), 20-27.
[http://dx.doi.org/10.1053/j.seminoncol.2003.12.011]
[65]
Chu, G. Cellular responses to cisplatin. The roles of DNA-binding proteins and DNA repair. J. Biol. Chem., 1994, 269(2), 787-790.
[http://dx.doi.org/10.1016/S0021-9258(17)42175-2] [PMID: 8288625]
[66]
Rixe, O.; Ortuzar, W.; Alvarez, M.; Parker, R.; Reed, E.; Paull, K.; Fojo, T. Oxaliplatin, tetraplatin, cisplatin, and carboplatin: Spectrum of activity in drug-resistant cell lines and in the cell lines of the national cancer institute’s anticancer drug screen panel. Biochem. Pharmacol., 1996, 52(12), 1855-1865.
[http://dx.doi.org/10.1016/S0006-2952(97)81490-6] [PMID: 8951344]
[67]
Dunn, T.A.; Schmoll, H.J.; Grünwald, V.; Bokemeyer, V.; Casper, J. Comparative cytotoxicity of oxaliplatin and cisplatin in non-seminomatous germ cell cancer cell lines. Invest. New Drugs, 1997, 15(2), 109-114.
[http://dx.doi.org/10.1023/A:1005800520747] [PMID: 9220289]
[68]
Gamcsik, M.P.; Dubay, G.R.; Cox, B.R. Increased rate of glutathione synthesis from cystine in drug-resistant MCF-7 cells. Biochem. Pharmacol., 2002, 63(5), 843-851.
[http://dx.doi.org/10.1016/S0006-2952(01)00931-5] [PMID: 11911835]
[69]
Deng, H.B.; Parekh, H.K.; Chow, K.C.; Simpkins, H. Increased expression of dihydrodiol dehydrogenase induces resistance to cisplatin in human ovarian carcinoma cells. J. Biol. Chem., 2002, 277(17), 15035-15043.
[http://dx.doi.org/10.1074/jbc.M112028200] [PMID: 11842089]
[70]
Dumontet, C.; Fabianowska-Majewska, K.; Mantincic, D.; Callet Bauchu, E.; Tigaud, I.; Gandhi, V.; Lepoivre, M.; Peters, G.J.; Rolland, M.O.; Wyczechowska, D.; Fang, X.; Gazzo, S.; Voorn, D.A.; Vanier-Viornery, A.; Mackey, J. Common resistance mechanisms to deoxynucleoside analogues in variants of the human erythroleukaemic line K562. Br. J. Haematol., 1999, 106(1), 78-85.
[http://dx.doi.org/10.1046/j.1365-2141.1999.01509.x] [PMID: 10444166]
[71]
Conze, D.; Weiss, L.; Regen, P.S.; Bhushan, A.; Weaver, D.; Johnson, P.; Rincón, M. Autocrine production of interleukin 6 causes multidrug resistance in breast cancer cells. Cancer Res., 2001, 61(24), 8851-8858.
[PMID: 11751408]
[72]
Song, S.; Wientjes, M.G.; Gan, Y.; Au, J.L.S. Fibroblast growth factors: An epigenetic mechanism of broad spectrum resistance to anticancer drugs. Proc. Natl. Acad. Sci. USA, 2000, 97(15), 8658-8663.
[http://dx.doi.org/10.1073/pnas.140210697] [PMID: 10890892]
[73]
Jain, R.K. Normalizing tumor vasculature with anti-angiogenic therapy: A new paradigm for combination therapy. Nat. Med., 2001, 7(9), 987-989.
[http://dx.doi.org/10.1038/nm0901-987] [PMID: 11533692]
[74]
Willett, C.G.; Boucher, Y.; di Tomaso, E.; Duda, D.G.; Munn, L.L.; Tong, R.T.; Chung, D.C.; Sahani, D.V.; Kalva, S.P.; Kozin, S.V.; Mino, M.; Cohen, K.S.; Scadden, D.T.; Hartford, A.C.; Fischman, A.J.; Clark, J.W.; Ryan, D.P.; Zhu, A.X.; Blaszkowsky, L.S.; Chen, H.X.; Shellito, P.C.; Lauwers, G.Y.; Jain, R.K. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat. Med., 2004, 10(2), 145-147.
[http://dx.doi.org/10.1038/nm988] [PMID: 14745444]
[75]
Ambudkar, S.V.; Dey, S.; Hrycyna, C.A.; Ramachandra, M.; Pastan, I.; Gottesman, M.M. Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu. Rev. Pharmacol. Toxicol., 1999, 39(1), 361-398.
[http://dx.doi.org/10.1146/annurev.pharmtox.39.1.361] [PMID: 10331089]
[76]
Altuvia, S.; Stein, W.D.; Goldenberg, S.; Kane, S.E.; Pastan, I.; Gottesman, M.M. Targeted disruption of the mouse mdr1b gene reveals that steroid hormones enhance mdr gene expression. J. Biol. Chem., 1993, 268(36), 27127-27132.
[http://dx.doi.org/10.1016/S0021-9258(19)74226-4] [PMID: 7903303]
[77]
Sorrentino, B.P. Gene therapy to protect haematopoietic cells from cytotoxic cancer drugs. Nat. Rev. Cancer, 2002, 2(6), 431-441.
[http://dx.doi.org/10.1038/nrc823] [PMID: 12189385]
[78]
Schoenfeld, A.; Luqmani, Y.; Sinnett, H.D.; Shousha, S.; Coombes, R.C. Keratin 19 mRNA measurement to detect micrometastases in lymph nodes in breast cancer patients. Br. J. Cancer, 1996, 74(10), 1639-1642.
[http://dx.doi.org/10.1038/bjc.1996.601] [PMID: 8932347]
[79]
Pantel, K.; von Knebel Doeberitz, M. Detection and clinical relevance of micrometastatic cancer cells. Curr. Opin. Oncol., 2000, 12(1), 95-101.
[http://dx.doi.org/10.1097/00001622-200001000-00016] [PMID: 10687736]
[80]
Croop, J.M.; Raymond, M.; Haber, D.; Devault, A.; Arceci, R.J.; Gros, P.; Housman, D.E. The three mouse multidrug resistance (mdr) genes are expressed in a tissue-specific manner in normal mouse tissues. Mol. Cell. Biol., 1989, 9(3), 1346-1350.
[PMID: 2471060]
[81]
Lothstein, L.; Hsu, S.H.; Horwitz, S.B.; Greenberger, L.M. Erratum: Alternate overexpression of two P-glycoprotein genes is associated with changes in multidrug resistance in a J774. 2 cell line (Vol. 264 (1989) 16054-16058). J. Biol. Chem., 1990, 265(3), 1821.
[82]
Goldstein, L.J.; Galski, H.; Fojo, A.; Willingham, M.; Lai, S.L.; Gazdar, A.; Pirker, R.; Green, A.; Crist, W.; Brodeur, G.M.; Lieber, M.; Cossman, J.; Gottesman, M.M.; Pastan, I. Expression of a multidrug resistance gene in human cancers. J. Natl. Cancer Inst., 1989, 81(2), 116-124.
[http://dx.doi.org/10.1093/jnci/81.2.116] [PMID: 2562856]
[83]
de Vree, J.M.L.; Jacquemin, E.; Sturm, E.; Cresteil, D.; Bosma, P.J.; Aten, J.; Deleuze, J.F.; Desrochers, M.; Burdelski, M.; Bernard, O.; Elferink, R.P.J.O.; Hadchouel, M. Mutations in the MDR 3 gene cause progressive familial intrahepatic cholestasis. Proc. Natl. Acad. Sci., 1998, 95(1), 282-287.
[http://dx.doi.org/10.1073/pnas.95.1.282] [PMID: 9419367]
[84]
Lee, C.G.; Gottesman, M.M. HIV-1 protease inhibitors and the MDR1 multidrug transporter. J. Clin. Invest., 1998, 101(2), 287-288.
[http://dx.doi.org/10.1172/JCI2575] [PMID: 9435298]
[85]
Ramachandra, M.; Ambudkar, S.V.; Chen, D.; Hrycyna, C.A.; Dey, S.; Gottesman, M.M.; Pastan, I. Human P-glycoprotein exhibits reduced affinity for substrates during a catalytic transition state. Biochemistry, 1998, 37(14), 5010-5019.
[http://dx.doi.org/10.1021/bi973045u] [PMID: 9538020]
[86]
Sauna, Z.E.; Ambudkar, S.V. Evidence for a requirement for ATP hydrolysis at two distinct steps during a single turnover of the catalytic cycle of human P-glycoprotein. Proc. Natl. Acad. Sci., 2000, 97(6), 2515-2520.
[http://dx.doi.org/10.1073/pnas.97.6.2515] [PMID: 10716986]
[87]
Sauna, Z.E.; Ambudkar, S.V. Characterization of the catalytic cycle of ATP hydrolysis by human P-glycoprotein. The two ATP hydrolysis events in a single catalytic cycle are kinetically similar but affect different functional outcomes. J. Biol. Chem., 2001, 276(15), 11653-11661.
[http://dx.doi.org/10.1074/jbc.M011294200] [PMID: 11154703]
[88]
Kreitman, R.J.; Pastan, I. Immunotoxins for targeted cancer therapy. Adv. Drug Deliv. Rev., 1998, 31(1-2), 53-88.
[http://dx.doi.org/10.1016/S0169-409X(97)00094-X] [PMID: 10837618]
[89]
Rueff, J.; Rodrigues, A.S. Cancer drug resistance: A brief overview from a genetic viewpoint. Cancer Drug Resistance. Methods in Molecular Biology; Humana Press: New York, 2016, 1395, pp. 1-8.
[http://dx.doi.org/10.1007/978-1-4939-3347-1]
[90]
Zahreddine, H.; Borden, K.L.B. Mechanisms and insights into drug resistance in cancer. Front. Pharmacol., 2013, 4, 28.
[http://dx.doi.org/10.3389/fphar.2013.00028] [PMID: 23504227]
[91]
Sampath, D.; Cortes, J.; Estrov, Z.; Du, M.; Shi, Z.; Andreeff, M.; Gandhi, V.; Plunkett, W. Pharmacodynamics of cytarabine alone and in combination with 7-hydroxystaurosporine (UCN-01) in AML blasts in vitro and during a clinical trial. Blood, 2006, 107(6), 2517-2524.
[http://dx.doi.org/10.1182/blood-2005-08-3351] [PMID: 16293603]
[92]
Momparler, R.L. Biochemical pharmacology of cytosine arabinoside. Med. Pediatr. Oncol., 1982, 10(S1), 45-48.
[http://dx.doi.org/10.1002/mpo.2950100707] [PMID: 7162466]
[93]
Shelton, J.; Lu, X.; Hollenbaugh, J.A.; Cho, J.H.; Amblard, F.; Schinazi, R.F. Metabolism, biochemical actions, and chemical synthesis of anticancer nucleosides, nucleotides, and base analogs. Chem. Rev., 2016, 116(23), 14379-14455.
[http://dx.doi.org/10.1021/acs.chemrev.6b00209] [PMID: 27960273]
[94]
Meijer, C.; Mulder, N.H.; Timmer-Bosscha, H.; Sluiter, W.J.; Meersma, G.J.; de Vries, E.G. Relationship of cellular glutathione to the cytotoxicity and resistance of seven platinum compounds. Cancer Res., 1992, 52(24), 6885-6889.
[PMID: 1458477]
[95]
Longley, D.B.; Johnston, P.G. Molecular mechanisms of drug resistance. J. Pathol., 2005, 205(2), 275-292.
[http://dx.doi.org/10.1002/path.1706]
[96]
Hughes, L.R.; Stephens, T.C.; Boyle, F.T.; Jackman, A.L. Raltitrexed (Tomudex TM), a highly polyglutamatable antifolate thymidylate synthase inhibitor. In: Antifolate Drugs in Cancer Therapy; Humana Press: Totowa, NJ, 1999; pp. 147-165.
[http://dx.doi.org/10.1007/978-1-59259-725-3_6]
[97]
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.
[http://dx.doi.org/10.1038/nrc3599] [PMID: 24060863]
[98]
Bonanno, L.; Favaretto, A.; Rosell, R. Platinum drugs and DNA repair mechanisms in lung cancer. Anticancer Res., 2014, 34(1), 493-501.
[PMID: 24403507]
[99]
Olaussen, K.A.; Dunant, A.; Fouret, P.; Brambilla, E.; André, F.; Haddad, V.; Taranchon, E.; Filipits, M.; Pirker, R.; Popper, H.H.; Stahel, R.; Sabatier, L.; Pignon, J.P.; Tursz, T.; Le Chevalier, T.; Soria, J.C. DNA repair by ERCC1 in non-small-cell lung cancer and cisplatin-based adjuvant chemotherapy. N. Engl. J. Med., 2006, 355(10), 983-991.
[http://dx.doi.org/10.1056/NEJMoa060570] [PMID: 16957145]
[100]
Selvakumaran, M.; Pisarcik, D.A.; Bao, R.; Yeung, A.T.; Hamilton, T.C. Enhanced cisplatin cytotoxicity by disturbing the nucleotide excision repair pathway in ovarian cancer cell lines. Cancer Res., 2003, 63(6), 1311-1316.
[PMID: 12649192]
[101]
Curtin, N.J. DNA repair dysregulation from cancer driver to therapeutic target. Nat. Rev. Cancer, 2012, 12(12), 801-817.
[http://dx.doi.org/10.1038/nrc3399] [PMID: 23175119]
[102]
Goode, E.L.; Ulrich, C.M.; Potter, J.D. Polymorphisms in DNA repair genes and associations with cancer risk. Cancer Epidemiol. Biomarkers Prev., 2002, 11(12), 1513-1530.
[PMID: 12496039]
[103]
Hirayama, C.; Watanabe, H.; Nakashima, R.; Nanbu, T.; Hamada, A.; Kuniyasu, A.; Nakayama, H.; Kawaguchi, T.; Saito, H. Constitutive overexpression of P-glycoprotein, rather than breast cancer resistance protein or organic cation transporter 1, contributes to acquisition of imatinib-resistance in K562 cells. Pharm. Res., 2008, 25(4), 827-835.
[http://dx.doi.org/10.1007/s11095-007-9376-3] [PMID: 17934801]
[104]
Shang, Y.; Cai, X.; Fan, D. Roles of epithelial-mesenchymal transition in cancer drug resistance. Curr. Cancer Drug Targets, 2013, 13(9), 915-929.
[http://dx.doi.org/10.2174/15680096113136660097] [PMID: 24168191]
[105]
Singh, A.; Settleman, J. EMT, cancer stem cells and drug resistance: An emerging axis of evil in the war on cancer. Oncogene, 2010, 29(34), 4741-4751.
[http://dx.doi.org/10.1038/onc.2010.215] [PMID: 20531305]
[106]
Chaffer, C.L.; Brueckmann, I.; Scheel, C.; Kaestli, A.J.; Wiggins, P.A.; Rodrigues, L.O.; Brooks, M.; Reinhardt, F.; Su, Y.; Polyak, K.; Arendt, L.M.; Kuperwasser, C.; Bierie, B.; Weinberg, R.A. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc. Natl. Acad. Sci., 2011, 108(19), 7950-7955.
[http://dx.doi.org/10.1073/pnas.1102454108] [PMID: 21498687]
[107]
Chaffer, C.L.; Weinberg, R.A. A perspective on cancer cell metastasis. Science, 2011, 331(6024), 1559-1564.
[108]
Sarkar, S.; Horn, G.; Moulton, K.; Oza, A.; Byler, S.; Kokolus, S.; Longacre, M. Cancer development, progression, and therapy: An epigenetic overview. Int. J. Mol. Sci., 2013, 14(10), 21087-21113.
[http://dx.doi.org/10.3390/ijms141021087] [PMID: 24152442]
[109]
Byler, S.; Goldgar, S.; Heerboth, S.; Leary, M.; Housman, G.; Moulton, K.; Sarkar, S. Genetic and epigenetic aspects of breast cancer progression and therapy. Anticancer Res., 2014, 34(3), 1071-1077.
[PMID: 24596345]
[110]
Byler, S.; Sarkar, S. Do epigenetic drug treatments hold the key to killing cancer progenitor cells? Epigenomics, 2014, 6(2), 161-165.
[http://dx.doi.org/10.2217/epi.14.4] [PMID: 24811783]
[111]
Bates, R.C.; Mercurio, A. The epithelial-mesenchymal tansition (EMT) and colorectal cancer progression. Cancer Biol. Ther., 2005, 4(4), 371-376.
[http://dx.doi.org/10.4161/cbt.4.4.1655] [PMID: 15846084]
[112]
Parkin, B.; Ouillette, P.; Li, Y.; Keller, J.; Lam, C.; Roulston, D.; Li, C.; Shedden, K.; Malek, S.N. Clonal evolution and devolution after chemotherapy in adult acute myelogenous leukemia. Blood, 2013, 121(2), 369-377.
[http://dx.doi.org/10.1182/blood-2012-04-427039] [PMID: 23175688]
[113]
Navin, N.; Krasnitz, A.; Rodgers, L.; Cook, K.; Meth, J.; Kendall, J.; Riggs, M.; Eberling, Y.; Troge, J.; Grubor, V.; Levy, D.; Lundin, P.; Månér, S.; Zetterberg, A.; Hicks, J.; Wigler, M. Inferring tumor progression from genomic heterogeneity. Genome Res., 2010, 20(1), 68-80.
[http://dx.doi.org/10.1101/gr.099622.109] [PMID: 19903760]
[114]
Campbell, P.J.; Yachida, S.; Mudie, L.J.; Stephens, P.J.; Pleasance, E.D.; Stebbings, L.A.; Morsberger, L.A.; Latimer, C.; McLaren, S.; Lin, M.L.; McBride, D.J.; Varela, I.; Nik-Zainal, S.A.; Leroy, C.; Jia, M.; Menzies, A.; Butler, A.P.; Teague, J.W.; Griffin, C.A.; Burton, J.; Swerdlow, H.; Quail, M.A.; Stratton, M.R.; Iacobuzio-Donahue, C.; Futreal, P.A. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature, 2010, 467(7319), 1109-1113.
[http://dx.doi.org/10.1038/nature09460] [PMID: 20981101]
[115]
Hutchison, DJ; Schmid, FA Cross-resistance and collateral sensitivity. Drug resistance and selectivity Biochemical and cellular basis,, 1973, 73-126.
[116]
Goldie, J.H.; Coldman, A.J. Drug resistance in cancer: Mechanisms and models; Cambridge University Press, 1998.
[http://dx.doi.org/10.1017/CBO9780511666544]
[117]
Giaccone, G.; Pinedo, H.M. Drug Resistance. Oncologist, 1996, 1(1-2), 82-87.
[http://dx.doi.org/10.1634/theoncologist.1-1-82] [PMID: 10387972]
[118]
Laurent, E.; Talpaz, M.; Kantarjian, H.; Kurzrock, R. The BCR gene and philadelphia chromosome-positive leukemogenesis. Cancer Res., 2001, 61(6), 2343-2355.
[PMID: 11289094]
[119]
Rodon Ahnert, J.; Gray, N.; Mok, T.; Gainor, J. What it takes to improve a first-generation inhibitor to a second-or third-generation small molecule. Am. Soc. Clin. Oncol. Educ. Book, 2019, 39(39), 196-205.
[http://dx.doi.org/10.1200/EDBK_242209] [PMID: 31099659]
[120]
Laurini, E.; Posocco, P.; Fermeglia, M.; Gibbons, D.L.; Quintás-Cardama, A.; Pricl, S. Through the open door: Preferential binding of dasatinib to the active form of BCR-ABL unveiled by in silico experiments. Mol. Oncol., 2013, 7(5), 968-975.
[http://dx.doi.org/10.1016/j.molonc.2013.06.001] [PMID: 23816609]
[121]
Lynch, T.J.; Bell, D.W.; Sordella, R.; Gurubhagavatula, S.; Okimoto, R.A.; Brannigan, B.W.; Harris, P.L.; Haserlat, S.M.; Supko, J.G.; Haluska, F.G.; Louis, D.N.; Christiani, D.C.; Settleman, J.; Haber, D.A. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N. Engl. J. Med., 2004, 350(21), 2129-2139.
[http://dx.doi.org/10.1056/NEJMoa040938] [PMID: 15118073]
[122]
Yun, C.H.; Mengwasser, K.E.; Toms, A.V.; Woo, M.S.; Greulich, H.; Wong, K.K.; Meyerson, M.; Eck, M.J. The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc. Natl. Acad. Sci., 2008, 105(6), 2070-2075.
[http://dx.doi.org/10.1073/pnas.0709662105] [PMID: 18227510]
[123]
Cross, D.A.E.; Ashton, S.E.; Ghiorghiu, S.; Eberlein, C.; Nebhan, C.A.; Spitzler, P.J.; Orme, J.P.; Finlay, M.R.V.; Ward, R.A.; Mellor, M.J.; Hughes, G.; Rahi, A.; Jacobs, V.N.; Brewer, M.R.; Ichihara, E.; Sun, J.; Jin, H.; Ballard, P.; Al-Kadhimi, K.; Rowlinson, R.; Klinowska, T.; Richmond, G.H.P.; Cantarini, M.; Kim, D.W.; Ranson, M.R.; Pao, W. AZD9291, an irreversible EGFR TKI, overcomes T790M-mediated resistance to EGFR inhibitors in lung cancer. Cancer Discov., 2014, 4(9), 1046-1061.
[http://dx.doi.org/10.1158/2159-8290.CD-14-0337] [PMID: 24893891]
[124]
Schoepfer, J.; Jahnke, W.; Berellini, G.; Buonamici, S.; Cotesta, S.; Cowan-Jacob, S.W.; Dodd, S.; Drueckes, P.; Fabbro, D.; Gabriel, T. Groell, JM Discovery of asciminib (ABL001), an allosteric inhibitor of the tyrosine kinase activity of BCR-ABL-1. J. Med. Chem., 2018, 61(18), 8120-8135.
[125]
Jacus, M.O.; Daryani, V.M.; Harstead, K.E.; Patel, Y.T.; Throm, S.L.; Stewart, C.F. Pharmacokinetic properties of anticancer agents for the treatment of central nervous system tumors: Update of the literature. Clin. Pharmacokinet., 2016, 55(3), 297-311.
[http://dx.doi.org/10.1007/s40262-015-0319-6] [PMID: 26293618]
[126]
Ni, W.; Chen, W.; Lu, Y. Emerging findings into molecular mechanism of brain metastasis. Cancer Med., 2018, 7(8), 3820-3833.
[http://dx.doi.org/10.1002/cam4.1667] [PMID: 29992751]
[127]
Wang, Q.; Rager, J.D.; Weinstein, K.; Kardos, P.S.; Dobson, G.L.; Li, J.; Hidalgo, I.J. Evaluation of the MDR-MDCK cell line as a permeability screen for the blood–brain barrier. Int. J. Pharm., 2005, 288(2), 349-359.
[http://dx.doi.org/10.1016/j.ijpharm.2004.10.007] [PMID: 15620875]
[128]
Kern, D.H.; Weisenthal, L.M. Highly specific prediction of antineoplastic drug resistance with an in vitro assay using suprapharmacologic drug exposures. J. Natl. Cancer Inst., 1990, 82(7), 582-588.
[http://dx.doi.org/10.1093/jnci/82.7.582] [PMID: 2313735]
[129]
McGuire, W.L.; Kern, D.H.; Von Hoff, D.D.; Weisenthal, L.M. In vitro assays to predict drug sensitivity and drug resistance. Breast Cancer Res. Treat., 1988, 12(1), 7-21.
[http://dx.doi.org/10.1007/BF01805735] [PMID: 3196887]
[130]
Zehentner, B.K. Detection of disseminatedtumor cells: Strategies and diagnostic implications. Expert Rev. Mol. Diagn., 2002, 2(1), 41-48.
[http://dx.doi.org/10.1586/14737159.2.1.41] [PMID: 11963801]
[131]
Mathur, P; Sathishkumar, K; Chaturvedi, M; Das, P; Sudarshan, KL; Santhappan, S; Nallasamy, V; John, A; Narasimhan, S; Roselind, FS ICMR-NCDIR-NCRP Investigator Group Cancer statistics., 2020, 2020, 1063-1075.

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