Molecular mechanisms of cisplatin resistance in bladder cancer

Expert Review of Anticancer Therapy

Volumn 12, Issue 2, 2012, Pages 271-281

  Drayton, Ross M ^a   Catto, James W F ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

apoptosis; bladder cancer; cisplatin; cisplatin resistance; DNA repair; drug resistance; epigenetics

Indexed keywords

CISPLATIN; EPIDERMAL GROWTH FACTOR RECEPTOR; FAS LIGAND; FIBROBLAST GROWTH FACTOR RECEPTOR; GLUTATHIONE; GLYCOPROTEIN P; LYMPHOTOXIN; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 2; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN P53; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; BLADDER CANCER; CANCER CELL CULTURE; DNA DAMAGE; DNA REPAIR; DRUG DETOXIFICATION; DRUG DISTRIBUTION; DRUG UPTAKE; EPIGENETICS; GENE EXPRESSION REGULATION; GLUTATHIONE METABOLISM; HUMAN; INTRACELLULAR SIGNALING; PROTEIN EXPRESSION; REVIEW; TRANSITIONAL CELL CARCINOMA;

ANIMALS; ANTINEOPLASTIC AGENTS; CISPLATIN; DNA DAMAGE; DRUG RESISTANCE, NEOPLASM; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; SIGNAL TRANSDUCTION; URINARY BLADDER NEOPLASMS;

EID: 84856897209     PISSN: 14737140     EISSN: 17448328     Source Type: Journal    
DOI: 10.1586/era.11.201     Document Type: Review

References (129)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J. Clin. 60(5), 277-300 (2010).
2. Avritscher EB, Cooksley CD, Grossman HB et al. Clinical model of lifetime cost of treating bladder cancer and associated complications. Urology 68(3), 549-553 (2006). (Pubitemid 44436509)
3. Sangar VK, Ragavan N, Matanhelia SS, Watson MW, Blades RA. The economic consequences of prostate and bladder cancer in the UK. BJU Int. 95(1), 59-63 (2005). (Pubitemid 350020870)
4. Catto JW, Azzouzi AR, Rehman I et al. Promoter hypermethylation is associated with tumor location, stage, and subsequent progression in transitional cell carcinoma. J. Clin. Oncol. 23(13), 2903-2910 (2005). (Pubitemid 46224108)
5. Goebell PJ, Knowles MA. Bladder cancer or bladder cancers? Genetically distinct malignant conditions of the urothelium. Urol. Oncol. 28(4), 409-428 (2010).
6. Catto JW, Miah S, Owen HC et al. Distinct microRNA alterations characterize high and low grade bladder cancer. Cancer Res. 69(21), 8472-8481 (2009).
7. Catto JW, Rosario DJ. The road to cystectomy: Who, when and why? Eur. Urol.: EAU Update Series 3(4), 171-179 (2005).
8. Catto JW, Yates DR, Rehman I et al. Behavior of urothelial carcinoma with respect to anatomical location. J. Urol. 177(5), 1715-1720 (2007). (Pubitemid 46560675)
9. Stein JP, Lieskovsky G, Cote R et al. Radical cystectomy in the treatment of invasive bladder cancer: Long-term results in 1,054 patients. J. Clin. Oncol. 19(3), 666-675 (2001). (Pubitemid 32120143)
10. Von Der Maase H, Sengelov L, Roberts JT et al. Long-term survival results of a randomized trial comparing gemcitabine plus cisplatin, with methotrexate, vinblastine, doxorubicin, plus cisplatin in patients with bladder cancer. J. Clin. Oncol. 23(21), 4602-4608 (2005). (Pubitemid 46224062)
11. Sternberg CN, Donat SM, Bellmunt J et al. Chemotherapy for bladder cancer: Treatment guidelines for neoadjuvant chemotherapy, bladder preservation, adjuvant chemotherapy, and metastatic cancer. Urology 69(1 Suppl.), 62-79 (2007). (Pubitemid 46186484)
12. Advanced Bladder Cancer (ABC) Meta-analysis Collaboration. Adjuvant chemotherapy in invasive bladder cancer: A systematic review and meta-analysis of individual patient data Advanced Bladder Cancer (ABC) Meta-analysis Collaboration. Eur. Urol. 48(2), 189-199; discussion 199-201 (2005).
13. Von Der Maase H, Hansen SW, Roberts JT et al. Gemcitabine and cisplatin versus methotrexate, vinblastine, doxorubicin, and cisplatin in advanced or metastatic bladder cancer: Results of a large, randomized, multinational, multicenter, Phase III study. J. Clin. Oncol. 18(17), 3068-3077 (2000).
14. Advanced Bladder Cancer Meta-analysis Collaboration. Neoadjuvant chemotherapy in invasive bladder cancer: A systematic review and meta-analysis. Lancet 361(9373), 1927-1934 (2003).
15. Stewart DJ. Mechanisms of resistance to cisplatin and carboplatin. Crit. Rev. Oncol. Hematol. 63(1), 12-31 (2007). (Pubitemid 46810280)
16. Rosenberg B, Vancamp L, Krigas T. Inhibition of cell division in Escherichia coli by electrolysis products from a platinum electrode. Nature 205, 698-699 (1965).
17. Reed E, Ozols RF, Tarone R, Yuspa SH, Poirier MC. Platinum-DNA adducts in leukocyte DNA correlate with disease response in ovarian cancer patients receiving platinum-based chemotherapy. Proc. Natl Acad. Sci. USA 84(14), 5024-5028 (1987). (Pubitemid 17095857)
18. Zamble DB, Lippard SJ. Cisplatin and DNA repair in cancer chemotherapy. Trends Biochem. Sci. 20(10), 435-439 (1995).
19. Konstantakou EG, Voutsinas GE, Karkoulis PK, Aravantinos G, Margaritis LH, Stravopodis DJ. Human bladder cancer cells undergo cisplatin-induced apoptosis that is associated with p53-dependent and p53-independent responses. Int. J. Oncol. 35(2), 401-416 (2009).
20. Walker MC, Povey S, Parrington JM, Riddle PN, Knuechel R, Masters JR. Development and characterization of cisplatin-resistant human testicular and bladder tumour cell lines. Eur. J. Cancer 26(6), 742-747 (1990). (Pubitemid 20275116)
21. Yoon SJ, Park I, Kwak C, Lee E. UltRastructural change due to acquired cisplatin resistance in human bladder cancer cells. Oncol. Rep. 10(5), 1363-1367 (2003).
22. Pera MF, Koberle B, Masters JR. Exceptional sensitivity of testicular germ cell tumour cell lines to the new anti-cancer agent, temozolomide. Br. J. Cancer 71(5), 904-906 (1995).
23. Singh SV, Xu BH, Jani JP et al. Mechanism of cross-resistance to cisplatin in a mitomycin C-resistant human bladder cancer cell line. Int. J. Cancer 61(3), 431-436 (1995).
24. Singh SV, Xu BH, Gupta V, Emerson EO, Zaren HA, Jani JP. Characterization of a human bladder cancer cell line selected for resistance to BMY 25067, a novel analog of mitomycin C. Cancer Lett. 95(1-2), 49-56 (1995).
25. Tatokoro M, Koga F, Yoshida S et al. Potential role of Hsp90 inhibitors in overcoming cisplatin resistance of bladder cancer-initiating cells. Int. J. Cancer doi:10.1002/ijc.26475 (2011) (Epub ahead of print). .. Evidence of the existence of cisplatin-resistant bladder cancer stem cells and potential strategies for their resensitization.
26. Ishida S, Lee J, Thiele DJ, Herskowitz I. Uptake of the anticancer drug cisplatin mediated by the copper transporter Ctr1 in yeast and mammals. Proc. Natl Acad. Sci. USA 99(22), 14298-14302 (2002). (Pubitemid 35257666)
27. Samimi G, Safaei R, Katano K et al. Increased expression of the copper efflux transporter ATP7A mediates resistance to cisplatin, carboplatin, and oxaliplatin in ovarian cancer cells. Clin. Cancer Res. 10(14), 4661-4669 (2004). (Pubitemid 38955516)
28. Komatsu M, Sumizawa T, Mutoh M et al. Copper-transporting P-type adenosine triphosphatase (ATP7B) is associated with cisplatin resistance. Cancer Res. 60(5), 1312-1316 (2000). (Pubitemid 30152000)
29. Samimi G, Varki NM, Wilczynski S, Safaei R, Alberts DS, Howell SB. Increase in expression of the copper transporter ATP7A during platinum drug-based treatment is associated with poor survival in ovarian cancer patients. Clin. Cancer Res. 9(16 Pt 1), 5853-5859 (2003). (Pubitemid 38018067)
30. Takara K, Sakaeda T, Yagami T et al. Cytotoxic effects of 27 anticancer drugs in HeLa and MDR1-overexpressing derivative cell lines. Biol. Pharm. Bull. 25(6), 771-778 (2002). (Pubitemid 40036714)
31. Sandlow J, Cohen MB, Robinson RA, Dreicer R, Williams RD. DNA ploidy and P-glycoprotein expression as predictive factors of response to neoadjuvant chemotherapy for invasive bladder cancer. Urology 43(6), 787-791 (1994). (Pubitemid 24174466)
32. Bahnson RR, Becich M, Ernstoff MS, Sandlow J, Cohen MB, Williams RD. Absence of immunohistochemical metallothionein staining in bladder tumor specimens predicts response to neoadjuvant cisplatin, methotrexate and vinblastine chemotherapy. J. Urol. 152(6 Pt 2), 2272-2275 (1994). (Pubitemid 24346891)
33. Siu LL, Banerjee D, Khurana RJ et al. The prognostic role of p53, metallothionein, P-glycoprotein, and MIB-1 in muscle-invasive urothelial transitional cell carcinoma. Clin. Cancer Res. 4(3), 559-565 (1998). (Pubitemid 28193553)
34. Hoffmann AC, Wild P, Leicht C et al. MDR1 and ERCC1 expression predict outcome of patients with locally advanced bladder cancer receiving adjuvant chemotherapy. Neoplasia 12(8), 628-636 (2010).
35. Shen F, Chu S, Bence AK et al. Quantitation of doxorubicin uptake, efflux, and modulation of multidrug resistance (MDR) in MDR human cancer cells. J. Pharmacol. Exp. Ther. 324(1), 95-102 (2008). (Pubitemid 350294163)
36. Bruggemann EP, Currier SJ, Gottesman MM, Pastan I. Characterization of the azidopine and vinblastine binding site of P-glycoprotein. J. Biol. Chem. 267(29), 21020-21026 (1992).
37. De Graaf D, Sharma RC, Mechetner EB, Schimke RT, Roninson IB. P-glycoprotein confers methotrexate resistance in 3T6 cells with deficient carrier-mediated methotrexate uptake. Proc. Natl Acad. Sci. USA 93(3), 1238-1242 (1996). (Pubitemid 26052872)
38. Petrylak DP, Scher HI, Reuter V, O'brien JP, Cordon-Cardo C. P-glycoprotein expression in primary and metastatic transitional cell carcinoma of the bladder. Ann. Oncol. 5(9), 835-840 (1994). (Pubitemid 24341877)
39. Tada Y, Wada M, Migita T et al. Increased expression of multidrug resistance-associated proteins in bladder cancer during clinical course and drug resistance to doxorubicin. Int. J. Cancer 98(4), 630-635 (2002). (Pubitemid 34208567)
40. Kimiya K, Naito S, Soejima T et al. Establishment and characterization of doxorubicin-resistant human bladder cancer cell line, KK47/ADM. J. Urol. 148(2 Pt 1), 441-445 (1992).
41. Kim WJ, Kakehi Y, Hirai M et al. Multidrug resistance-associated protein-mediated multidrug resistance modulated by cyclosporin A in a human bladder cancer cell line. Jpn J. Cancer Res. 86(10), 969-977 (1995).
42. Clifford SC, Neal DE, Lunec J. Alterations in expression of the multidrug resistance-associated protein (MRP) gene in high-grade transitional cell carcinoma of the bladder. Br. J. Cancer 73(5), 659-666 (1996). (Pubitemid 26068874)
43. Taniguchi K, Wada M, Kohno K et al. A human canalicular multispecific organic anion transporter (cMOAT) gene is overexpressed in cisplatin-resistant human cancer cell lines with decreased drug accumulation. Cancer Res. 56(18), 4124-4129 (1996). (Pubitemid 26305002)
44. Kobayashi T, Fujii T, Jo Y, Kinugawa K, Fujisawa M. Possible mechanism responsible for the acquisition of resistance to cis-diamminedichloroplatinum (II) by cultured human testicular seminoma cells. J. Urol. 171(5), 1929-1933 (2004). (Pubitemid 38501046)
45. Nakamura M, Nakatani K, Uzawa K et al. Establishment and characterization of a cisplatin-resistant oral squamous cell carcinoma cell line, H-1R. Oncol. Rep. 14(5), 1281-1286 (2005).
46. Paulusma CC, Van Geer MA, Evers R et al. Canalicular multispecific organic anion transporter/multidrug resistance protein 2 mediates low-affinity transport of reduced glutathione. Biochem. J. 338( Pt 2), 393-401 (1999).
47. Reedijk J. Why does cisplatin reach guanine-n7 with competing s-donor ligands available in the cell? Chem. Rev. 99(9), 2499-2510 (1999).
48. Kasherman Y, Sturup S, Gibson D. Is glutathione the major cellular target of cisplatin? A study of the interactions of cisplatin with cancer cell extracts. J. Med. Chem. 52(14), 4319-4328 (2009).
49. Bahnson RR, Banner BF, Ernstoff MS et al. Immunohistochemical localization of metallothionein in transitional cell carcinoma of the bladder. J. Urol. 146(6), 1518-1520 (1991).
50. Satoh M, Kloth DM, Kadhim SA et al. Modulation of both cisplatin nephrotoxicity and drug resistance in murine bladder tumor by controlling metallothionein synthesis. Cancer Res. 53(8), 1829-1832 (1993). (Pubitemid 23127110)
51. Satoh M, Cherian MG, Imura N, Shimizu H. Modulation of resistance to anticancer drugs by inhibition of metallothionein synthesis. Cancer Res. 54(20), 5255-5257 (1994). (Pubitemid 24336008)
52. Wulfing C, Van Ahlen H, Eltze E, Piechota H, Hertle L, Schmid KW. Metallothionein in bladder cancer: Correlation of overexpression with poor outcome after chemotherapy. World J. Urol. 25(2), 199-205 (2007).
53. Griffith OW. Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radic. Biol. Med. 27(9-10), 922-935 (1999). (Pubitemid 29507466)
54. Hagrman D, Goodisman J, Souid AK. Kinetic study on the reactions of platinum drugs with glutathione. J. Pharmacol. Exp. Ther. 308(2), 658-666 (2004). (Pubitemid 38134229)
55. Peklak-Scott C, Smitherman PK, Townsend AJ, Morrow CS. Role of glutathione S-transferase P1-1 in the cellular detoxification of cisplatin. Mol. Cancer Ther. 7(10), 3247-3255 (2008).
56. Ishikawa T, Wright CD, Ishizuka H. GS-X pump is functionally overexpressed in cis-diamminedichloroplatinum (II)-resistant human leukemia HL-60 cells and down-regulated by cell differentiation. J. Biol. Chem. 269(46), 29085-29093 (1994).
57. Chen HH, Song IS, Hossain A et al. Elevated glutathione levels confer cellular sensitization to cisplatin toxicity by up-regulation of copper transporter hCtr1. Mol. Pharmacol. 74(3), 697-704 (2008).
58. Ochi J. [Establishment and characterization of a cis-diamminedichloro platinum-resistant human bladder cancer cell line]. Nippon Hinyokika Gakkai Zasshi 82(7), 1045-1052 (1991).
59. Kotoh S, Naito S, Yokomizo A et al. Increased expression of DNA topoisomerase I gene and collateral sensitivity to camptothecin in human cisplatin-resistant bladder cancer cells. Cancer Res. 54(12), 3248-3252 (1994). (Pubitemid 24208937)
60. Bedford P, Shellard SA, Walker MC, Whelan RD, Masters JR, Hill BT. Differential expression of collateral sensitivity or resistance to cisplatin in human bladder carcinoma cell lines pre-exposed in vitro to either x-irradiation or cisplatin. Int. J. Cancer 40(5), 681-686 (1987). (Pubitemid 18003860)
61. Ahn H, Lee E, Kim K, Lee C. Effect of glutathione and its related enzymes on chemosensitivity of renal cell carcinoma and bladder carcinoma cell lines. J. Urol. 151(1), 263-267 (1994). (Pubitemid 24046986)
62. Masters JR, Thomas R, Hall AG et al. Sensitivity of testis tumour cells to chemotherapeutic drugs: Role of detoxifying pathways. Eur. J. Cancer 32A(7), 1248-1253 (1996). (Pubitemid 26231811)
63. Xu BH, Gupta V, Singh SV. Characterization of a human bladder cancer cell line selected for resistance to mitomycin C. Int. J. Cancer 58(5), 686-692 (1994). (Pubitemid 24279432)
64. Yokomizo A, Ono M, Nanri H et al. Cellular levels of thioredoxin associated with drug sensitivity to cisplatin, mitomycin C, doxorubicin, and etoposide. Cancer Res. 55(19), 4293-4296 (1995).
65. Takahara PM, Rosenzweig AC, Frederick CA, Lippard SJ. Crystal structure of double-stranded DNA containing the major adduct of the anticancer drug cisplatin. Nature 377(6550), 649-652 (1995).
66. Welsh C, Day R, McGurk C, Masters JR, Wood RD, Koberle B. Reduced levels of XPA, ERCC1 and XPF DNA repair proteins in testis tumor cell lines. Int. J. Cancer 110(3), 352-361 (2004). (Pubitemid 38649885)
67. Nouspikel T. DNA repair in mammalian cells: Nucleotide excision repair: Variations on versatility. Cell. Mol. Life Sci. 66(6), 994-1009 (2009).
68. Arora S, Kothandapani A, Tillison K, Kalman-Maltese V, Patrick SM. Downregulation of XPF-ERCC1 enhances cisplatin efficacy in cancer cells. DNA Repair (Amst.) 9(7), 745-753 (2010).
69. Ferry KV, Hamilton TC, Johnson SW. Increased nucleotide excision repair in cisplatin-resistant ovarian cancer cells: Role of ERCC1-XPF. Biochem. Pharmacol. 60(9), 1305-1313 (2000).
70. Bessho T, Sancar A, Thompson LH, Thelen MP. Reconstitution of human excision nuclease with recombinant XPF-ERCC1 complex. J. Biol. Chem. 272(6), 3833-3837 (1997). (Pubitemid 27066894)
71. Niedernhofer LJ, Odijk H, Budzowska M et al. The structure-specific endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-link-induced double-strand breaks. Mol. Cell. Biol. 24(13), 5776-5787 (2004). (Pubitemid 38787963)
72. Kawashima A, Nakayama M, Kakuta Y et al. Excision repair cross-complementing group 1 may predict the efficacy of chemoradiation therapy for muscle-invasive bladder cancer. Clin. Cancer Res. 17(8), 2561-2569 (2011).
73. Wang G, Chuang L, Zhang X et al. The initiative role of XPC protein in cisplatin DNA damaging treatment-mediated cell cycle regulation. Nucleic Acids Res. 32(7), 2231-2240 (2004). (Pubitemid 38854777)
74. Chen Z, Yang J, Wang G, Song B, Li J, Xu Z. Attenuated expression of xeroderma pigmentosum group C is associated with critical events in human bladder cancer carcinogenesis and progression. Cancer Res. 67(10), 4578-4585 (2007). (Pubitemid 46910162)
75. Xu XS, Wang L, Abrams J, Wang G. Histone deacetylases (HDACs) in XPC gene silencing and bladder cancer. J. Hematol. Oncol. 4, 17 (2011).
76. Aebi S, Kurdi-Haidar B, Gordon R et al. Loss of DNA mismatch repair in acquired resistance to cisplatin. Cancer Res. 56(13), 3087-3090 (1996). (Pubitemid 26199755)
77. Martin LP, Hamilton TC, Schilder RJ. Platinum resistance: The role of DNA repair pathways. Clin. Cancer Res. 14(5), 1291-1295 (2008). (Pubitemid 351413906)
78. Catto JW, Xinarianos G, Burton JL, Meuth M, Hamdy FC. Differential expression of hMLH1 and hMSH2 is related to bladder cancer grade, stage and prognosis but not microsatellite instability. Int. J. Cancer 105(4), 484-490 (2003). (Pubitemid 36578551)
79. Abuzeid WM, Jiang X, Shi G et al. Molecular disruption of RAD50 sensitizes human tumor cells to cisplatin-based chemotherapy. J. Clin. Invest. 119(7), 1974-1985 (2009). . Describes the use of a dominant negative RAD50 to disrupt MRE11/Rad50/Nbs1 complex formation with associated increase in cisplatin sensitivity.
80. Barry MA, Behnke CA, Eastman A. Activation of programmed cell death (apoptosis) by cisplatin, other anticancer drugs, toxins and hyperthermia. Biochem. Pharmacol. 40(10), 2353-2362 (1990). (Pubitemid 20373997)
81. Shimizu S, Narita M, Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome C by the mitochondrial channel VDAC. Nature 399(6735), 483-487 (1999). (Pubitemid 29258855)
82. Hong JH, Lee E, Hong J, Shin YJ, Ahn H. Antisense Bcl2 oligonucleotide in cisplatin-resistant bladder cancer cell lines. BJU Int. 90(1), 113-117 (2002).
83. Cho HJ, Kim JK, Kim KD et al. Upregulation of Bcl-2 is associated with cisplatin-resistance via inhibition of Bax translocation in human bladder cancer cells. Cancer Lett. 237(1), 56-66 (2006).
84. Cooke PW, James ND, Ganesan R, Burton A, Young LS, Wallace DM. Bcl-2 expression identifies patients with advanced bladder cancer treated by radiotherapy who benefit from neoadjuvant chemotherapy. BJU Int. 85(7), 829-835 (2000). (Pubitemid 30242786)
85. Miyake H, Hanada N, Nakamura H et al. Overexpression of Bcl-2 in bladder cancer cells inhibits apoptosis induced by cisplatin and adenoviral-mediated p53 gene transfer. Oncogene 16(7), 933-943 (1998). (Pubitemid 28102597)
86. Srinivasula SM, Hegde R, Saleh A et al. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 410(6824), 112-116 (2001). (Pubitemid 32225846)
87. Mizutani Y, Katsuoka Y, Bonavida B. Prognostic significance of second mitochondria-derived activator of caspase (Smac/DIABLO) expression in bladder cancer and target for therapy. Int. J. Oncol. 37(2), 503-508 (2010).
88. Bolenz C, Becker A, Trojan L et al. Optimizing chemotherapy for transitional cell carcinoma by application of bcl-2 and bcl-xL antisense oligodeoxynucleotides. Urol. Oncol. 25(6), 476-482 (2007). (Pubitemid 350151900)
89. Kim JK, Kim KD, Lee E et al. Up-regulation of Bfl-1/A1 via NF-kappaB activation in cisplatin-resistant human bladder cancer cell line. Cancer Lett. 212(1), 61-70 (2004). (Pubitemid 38887721)
90. Li J, Viallet J, Haura EB. A small molecule pan-Bcl-2 family inhibitor, GX15-070, induces apoptosis and enhances cisplatin-induced apoptosis in non-small cell lung cancer cells. Cancer Chemother. Pharmacol. 61(3), 525-534 (2008). (Pubitemid 350275989)
91. Arisan ED, Kutuk O, Tezil T, Bodur C, Telci D, Basaga H. Small inhibitor of Bcl-2, HA14-1, selectively enhanced the apoptotic effect of cisplatin by modulating Bcl-2 family members in MDA-MB-231 breast cancer cells. Breast Cancer Res. Treat. 119(2), 271-281 (2010).
92. Slaton JW, Benedict WF, Dinney CP. p53 in bladder cancer: Mechanism of action, prognostic value, and target for therapy. Urology 57(5), 852-859 (2001). (Pubitemid 32405300)
93. Branch P, Masson M, Aquilina G, Bignami M, Karran P. Spontaneous development of drug resistance: Mismatch repair and p53 defects in resistance to cisplatin in human tumor cells. Oncogene 19(28), 3138-3145 (2000). (Pubitemid 30455925)
94. Koberle B, Tomicic MT, Usanova S, Kaina B. Cisplatin resistance: Preclinical findings and clinical implications. Biochim. Biophys. Acta. 1806(2), 172-182 (2010).
95. Shirakawa T, Sasaki R, Gardner TA et al. Drug-resistant human bladder-cancer cells are more sensitive to adenovirus-mediated wild-type p53 gene therapy compared to drug-sensitive cells. Int. J. Cancer 94(2), 282-289 (2001). (Pubitemid 32911425)
96. Pagliaro LC, Keyhani A, Liu B, Perrotte P, Wilson D, Dinney CP. Adenoviral p53 gene transfer in human bladder cancer cell lines: Cytotoxicity and synergy with cisplatin. Urol. Oncol. 21(6), 456-462 (2003). (Pubitemid 38542722)
97. Cote RJ, Esrig D, Groshen S, Jones PA, Skinner DG. p53 and treatment of bladder cancer. Nature 385(6612), 123-125 (1997).
98. Qureshi KN, Griffiths TR, Robinson MC et al. TP53 accumulation predicts improved survival in patients resistant to systemic cisplatin-based chemotherapy for muscle-invasive bladder cancer. Clin. Cancer Res. 5(11), 3500-3507 (1999).
99. Stadler WM, Lerner SP, Groshen S et al. Phase III study of molecularly targeted adjuvant therapy in locally advanced urothelial cancer of the bladder based on p53 status. J. Clin. Oncol. 29(25), 3443-3449 (2011).
100. Tsunoda T, Koga H, Yokomizo A et al. Inositol 1,4,5-trisphosphate (IP3) receptor type 1 (IP3R1) modulates the acquisition of cisplatin resistance in bladder cancer cell lines. Oncogene 24(8), 1396-1402 (2005). (Pubitemid 40343119)
101. Shiota M, Tsunoda T, Song Y et al. Enhanced S100 calcium-binding protein P expression sensitizes human bladder cancer cells to cisplatin. BJU Int. 107(7), 1148-1153 (2011).
102. Fulda S, Debatin KM. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 25(34), 4798-4811 (2006). (Pubitemid 44187627)
103. Walczak H, Miller RE, Ariail K et al. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med. 5(2), 157-163 (1999). (Pubitemid 29068521)
104. Mizutani Y, Yoshida O, Bonavida B. Sensitization of human bladder cancer cells to Fas-mediated cytotoxicity by cis-diamminedichloroplatinum (II). J. Urol. 160(2), 561-570 (1998). (Pubitemid 29476735)
105. Mizutani Y, Nakao M, Ogawa O, Yoshida O, Bonavida B, Miki T. Enhanced sensitivity of bladder cancer cells to tumor necrosis factor related apoptosis inducing ligand mediated apoptosis by cisplatin and carboplatin. J. Urol. 165(1), 263-270 (2001).
106. Wu XX, Kakehi Y. Enhancement of lexatumumab-induced apoptosis in human solid cancer cells by cisplatin in caspase-dependent manner. Clin. Cancer Res. 15(6), 2039-2047 (2009).
107. Winograd-Katz SE, Levitzki A. Cisplatin induces PKB/Akt activation and p38(MAPK) phosphorylation of the EGF receptor. Oncogene 25(56), 7381-7390 (2006). (Pubitemid 44853429)
108. Liccardi G, Hartley JA, Hochhauser D. EGFR nuclear translocation modulates DNA repair following cisplatin and ionizing radiation treatment. Cancer Res. 71(3), 1103-1114 (2011).
109. Li Y, Yang X, Su LJ, Flaig TW. VEGFR and EGFR inhibition increases epithelial cellular characteristics and chemotherapy sensitivity in mesenchymal bladder cancer cells. Oncol. Rep. 24(4), 1019-1028 (2010).
110. Flaig TW, Su LJ, Mccoach C et al. Dual epidermal growth factor receptor and vascular endothelial growth factor receptor inhibition with vandetanib sensitizes bladder cancer cells to cisplatin in a dose- and sequence-dependent manner. BJU Int. 103(12), 1729-1737 (2009).
111. Li F, Yang W, Guo D, Hu Z, Xu H, Ye Z. LRIG1 combined with cisplatin enhances bladder cancer lesions via a novel pathway. Oncol. Rep. 25(6), 1629-1637 (2011).
112. Cappellen D, De Oliveira C, Ricol D et al. Frequent activating mutations of FGFR3 in human bladder and cervix carcinomas. Nat. Genet. 23(1), 18-20 (1999).
113. Tomlinson DC, Lamont FR, Shnyder SD, Knowles MA. Fibroblast growth factor receptor 1 promotes proliferation and survival via activation of the mitogen-activated protein kinase pathway in bladder cancer. Cancer Res. 69(11), 4613-4620 (2009).
114. Miyake H, Hara I, Gohji K, Yoshimura K, Arakawa S, Kamidono S. Expression of basic fibroblast growth factor is associated with resistance to cisplatin in a human bladder cancer cell line. Cancer Lett. 123(2), 121-126 (1998). (Pubitemid 28064088)
115. Pardo OE, Latigo J, Jeffery RE et al. The fibroblast growth factor receptor inhibitor PD173074 blocks small cell lung cancer growth in vitro and in vivo. Cancer Res. 69(22), 8645-8651 (2009).
116. Burt RK, Garfield S, Johnson K, Thorgeirsson SS. Transformation of rat liver epithelial cells with v-H-Ras or v-raf causes expression of MDR-1, glutathione-S-transferase-P and increased resistance to cytotoxic chemicals. Carcinogenesis 9(12), 2329-2332 (1988). (Pubitemid 19001341)
117. Sklar MD. The Ras oncogenes increase the intrinsic resistance of NIH 3T3 cells to ionizing radiation. Science 239(4840), 645-647 (1988). (Pubitemid 18066229)
118. Wood DP Jr, Anderson AE, Fair R, Chaganti RS. Ras oncogene point mutations in bladder cancer resistant to cisplatin. Urol. Res. 20(4), 313-316 (1992).
119. Theodorescu D, Connors KM, Groce A, Hoffman RM, Kerbel RS. Lack of influence of c-Ha-Ras expression on the drug sensitivity of human bladder cancer histocultured in three-dimensions. Anti Cancer Res. 13(4), 941-946 (1993). (Pubitemid 23247442)
120. Kompier LC, Lurkin I, van der Aa MN, van Rhijn BW, van der Kwast TH, Zwarthoff EC. FGFR3, HRAS, KRAS, NRAS and PIK3CA mutations in bladder cancer and their potential as biomarkers for surveillance and therapy. PLoS One 5(11), e13821 (2010).
121. Yoon CY, Park MJ, Lee JS et al. The histone deacetylase inhibitor trichostatin A synergistically resensitizes a cisplatin resistant human bladder cancer cell line. J. Urol. 185(3), 1102-1111 (2011). .. Evidence of epigenetic involvement in the regulation of cisplatin resistance in bladder cancer.
122. Yang H, Kong W, He L et al. MicroRNA expression profiling in human ovarian cancer: MiR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Res. 68(2), 425-433 (2008). (Pubitemid 351380068)
123. Zhu W, Xu H, Zhu D et al. miR-200bc/429 cluster modulates multidrug resistance of human cancer cell lines by targeting BCL2 and XIAP. Cancer Chemother. Pharmacol. doi:10.1007/s00280-011-1752-3 (2011) (Epub ahead of print).
124. Wiklund ED, Bramsen JB, Hulf T et al. Coordinated epigenetic repression of the miR-200 family and miR-205 in invasive bladder cancer. Int. J. Cancer 128(6), 1327-1334 (2011).
125. Dudziec E, Miah S, Choudhry HM et al. Hypermethylation of CpG islands and shores around specific microRNAs and mirtrons is associated with the phenotype and presence of bladder cancer. Clin. Cancer Res. 17(6), 1287-1296 (2011).
126. Plumb JA, Strathdee G, Sludden J, Kaye SB, Brown R. Reversal of drug resistance in human tumor xenografts by 2́-deoxy-5-azacytidine-induced demethylation of the hMLH1 gene promoter. Cancer Res. 60(21), 6039-6044 (2000).
127. Steele N, Finn P, Brown R, Plumb JA. Combined inhibition of DNA methylation and histone acetylation enhances gene re-expression and drug sensitivity in vivo. Br. J. Cancer 100(5), 758-763 (2009).
128. Yates DR, Rehman I, Meuth M, Cross SS, Hamdy FC, Catto JW. Methylational urinalysis: A prospective study of bladder cancer patients and age stratified benign controls. Oncogene 25(13), 1984-1988 (2006).
129. Yates DR, Rehman I, Abbod MF et al. Promoter hypermethylation identifies progression risk in bladder cancer. Clin. Cancer Res. 13(7), 2046-2053 (2007). (Pubitemid 46649871)