Drug Resistance Updates
Volume 12, Issue 6 , Pages 148-152 , December 2009

Novel strategies for reversing platinum resistance

  • Mian M.K. Shahzad

      Affiliations

    • Department of Gynecologic Oncology, U.T.M.D. Anderson Cancer Center, 1155 Herman Pressler, Unit 1362, Houston, TX 77030, United States
    • Department of Obstetrics and Gynecology, Baylor College of Medicine, 1709 Dryden Road, Houston, TX 77030, United States
  • ,
  • Gabriel Lopez-Berestein

      Affiliations

    • Department of Experimental Therapeutics, U.T.M.D. Anderson Cancer Center, 1155 Holcombe Blvd, Houston, TX 77030, United States
    • Department of Cancer Biology, U.T.M.D. Anderson Cancer Center, 1155 Herman Pressler, Unit 1362, Houston, TX 77030, United States
    • Center for RNA Interference and Non-coding RNA, U.T.M.D. Anderson Cancer Center, 1155 Herman Pressler, Unit 1362, Houston, TX 77030, United States
  • ,
  • Anil K. Sood

      Affiliations

    • Department of Gynecologic Oncology, U.T.M.D. Anderson Cancer Center, 1155 Herman Pressler, Unit 1362, Houston, TX 77030, United States
    • Department of Cancer Biology, U.T.M.D. Anderson Cancer Center, 1155 Herman Pressler, Unit 1362, Houston, TX 77030, United States
    • Center for RNA Interference and Non-coding RNA, U.T.M.D. Anderson Cancer Center, 1155 Herman Pressler, Unit 1362, Houston, TX 77030, United States
    • Corresponding Author InformationCorresponding author at: Departments of Gynecologic Oncology and Cancer Biology, University of Texas M.D. Anderson Cancer Center, 1155 Herman Pressler, Unit 1362, Houston, TX 77030, United States. Tel.: +1 713 745 5266; fax: +1 713 792 7586.

Received 31 August 2009 ,Revised 8 September 2009 ,Accepted 9 September 2009.

References 

  1. Agarwal R, Kaye SB. Ovarian cancer: strategies for overcoming resistance to chemotherapy. Nat. Rev. Cancer. 2003;3:502–516
  2. Ame JC, Spenlehauer C, de Murcia G. The PARP superfamily. Bioessays. 2004;26:882–893
  3. Anand S, Penrhyn-Lowe S, Venkitaraman AR. AURORA-A amplification overrides the mitotic spindle assembly checkpoint, inducing resistance to Taxol. Cancer Cell. 2003;3:51–62
  4. Arbitrario, J.P, Belmont, B.J., Evanchik, M.J., Flanagan, W.M., Funcini, R.V., Hansen, S.K., Harris, S.O., Hashash, A., Hoch, U., Hogan, N.J., Howlett, A.R., Jacobs, J.W., Lam, J.W., Ritchie, S.C., Romanowski, M.J., Silverman, J.A., Stockett, D.E., Teague, J.N., Zimmerman, M.K., Taverna, P., 2009. SNS-314, a pan-Aurora kinase inhibitor, shows potent anti-tumor activity and dosing flexibility in vivo. Cancer Chemother. Pharmacol., doi:10.1007/s00280-009-1076-8.
  5. Beauchamp, M.C., Knafo, A., Yasmeen, A., Carboni, J.M., Gottardis, M.M., Pollak, M.N., Gotlieb, W.H., 2009. BSM-536924 sensitizes human epithalial ovarian cancer cells to the PARP inhibitor, 3-amniobenzamide. Gynecol. Oncol., doi:10.1016/j.ygyno.2009.07.009.
  6. Borst P, Rottenberg S, Jonkers J. How do real tumors become resistant to platinum?. Cell Cycle. 2008;7:1353–1359
  7. Brabec V, Kasparkova J. Modifications of DNA by platinum complexes. Relation to resistance of tumors to platinum antitumor drugs. Drug Resist. Updat. 2005;8:131–146
  8. Carvajal RD, Tse A, Schwartz GK. Aurora kinases: new targets for cancer therapy. Clin. Cancer Res. 2006;12:6869–6875
  9. Chen HY, Shao CJ, Chen FR, Kwan AL, Chen ZP. Role of ERCC1 promoter hypermethylation in drug resistance to cisplatin in human gliomas. Int. J. Cancer. 2009;
  10. Dantzer F, de La Rubia G, Menissier-De Murcia J, Hostomsky Z, de Murcia G, Schreiber V. Base excision repair is impaired in mammalian cells lacking poly(ADP-ribose) polymerase-1. Biochemistry. 2000;39:7559–7569
  11. Ferry KV, Hamilton TC, Johnson SW. Increased nucleotide excision repair in cisplatin-resistant ovarian cancer cells: role of ERCC1-XPF. Biochem. Pharmacol. 2000;60:1305–1313
  12. Fojo T, Bates S. Strategies for reversing drug resistance. Oncogene. 2003;22:7512–7523
  13. Fong PC, Boss DS, Yap TA, Tutt A, Wu P, Mergui-Roelvink M, et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. New Engl. J. Med. 2009;361:123–134
  14. Gottlieb JA, Drewinko B. Review of the current clinical status of platinum coordination complexes in cancer chemotherapy. Cancer Chemother. Rep. 1975;59:621–628
  15. Halder J, Kamat AA, Landen CN, Han LY, Lutgendorf SK, Lin YG, et al. Focal adhesion kinase targeting using in vivo short interfering RNA delivery in neutral liposomes for ovarian carcinoma therapy. Clin. Cancer Res. 2006;12:4916–4924
  16. Harrington EA, Bebbington D, Moore J, Rasmussen RK, Ajose-Adeogun AO, Nakayama T, et al. VX-680, a potent and selective small-molecule inhibitor of the Aurora kinases, suppresses tumor growth in vivo. Nat. Med. 2004;10:262–267
  17. Hata T, Furukawa T, Sunamura M, Egawa S, Motoi F, Ohmura N, et al. RNA interference targeting aurora kinase a suppresses tumor growth and enhances the taxane chemosensitivity in human pancreatic cancer cells. Cancer Res. 2005;65:2899–2905
  18. Hay T, Mathews JR, Pietzka L, Lau A, Cranston A, Nygren AO, et al. Poly(ADP-ribose) polymerase-1 inhibitor treatment regresses autochthonous Brca2/p53-mutant mammary tumors in vivo and delays tumor relapse in combination with carboplatin. Cancer Res. 2009;69:3850–3855
  19. Hazlehurst LA, Dalton WS. Mechanisms associated with cell adhesion mediated drug resistance (CAM-DR) in hematopoietic malignancies. Cancer Metastasis Rev. 2001;20:43–50
  20. Higashimoto M, Kanzaki A, Shimakawa T, Konno S, Naritaka Y, Nitta Y, et al. Expression of copper-transporting P-type adenosine triphosphatase in human esophageal carcinoma. Int. J. Mol. Med. 2003;11:337–341
  21. Hoeijmakers JH. Genome maintenance mechanisms for preventing cancer. Nature. 2001;411:366–374
  22. Jackson SP. Detecting, signalling and repairing DNA double-strand breaks. Biochem. Soc. Trans. 2001;29:655–661
  23. Kang S, Ju W, Kim JW, Park NH, Song YS, Kim SC, et al. Association between excision repair cross-complementation group 1 polymorphism and clinical outcome of platinum-based chemotherapy in patients with epithelial ovarian cancer. Exp. Mol. Med. 2006;38:320–324
  24. Kanzaki A, Toi M, Neamati N, Miyashita H, Oubu M, Nakayama K, et al. Copper-transporting P-type adenosine triphosphatase (ATP7B) is expressed in human breast carcinoma. Jpn. J. Cancer Res. 2002;93:70–77
  25. Kartalou M, Essigmann JM. Mechanisms of resistance to cisplatin. Mutat. Res. 2001;478:23–43
  26. Katano K, Kondo A, Safaei S, Holzer A, Samimi G, Mishima M, et al. Acquisition of resistance to cisplatin is accompanied by changes in the cellular pharmacology of copper. Cancer Res. 2002;62:6559–6565
  27. Katano K, Safaei R, Samimi G, Holzer A, Rochdi M, Howell SB. The copper export pump ATP7B modulates the cellular pharmacology of carboplatin in ovarian carcinoma cells. Mol. Pharmacol. 2003;64:466–473
  28. Katano K, Safaei R, Samimi G, Holzer A, Tomioka M, Goodman M, et al. Confocal microscopic analysis of the interaction between cisplatin and the copper transporter ATP7B in human ovarian carcinoma cells. Clin. Cancer Res. 2004;10:4578–4588
  29. Katayama H, Brinkley WR, Sen S. The Aurora kinases: role in cell transformation and tumorigenesis. Cancer Metastasis Rev. 2003;22:451–464
  30. Keen N, Taylor S. Aurora-kinase inhibitors as anticancer agents. Nat. Rev. Cancer. 2004;4:927–936
  31. Kiat LS, Hui KM, Gopalan G. Aurora-A kinase interacting protein (AIP), a novel negative regulator of human Aurora-A kinase. J. Biol. Chem. 2002;277:45558–45565
  32. Landen CN, Chavez-Reyes A, Bucana C, Schmandt R, Deavers MT, Lopez-Berestein G, et al. Therapeutic EphA2 gene targeting in vivo using neutral liposomal small interfering RNA delivery. Cancer Res. 2005;65:6910–6918
  33. Landen CN, Lin YG, Immaneni A, Deavers MT, Merritt WM, Spannuth WA, et al. Overexpression of the centrosomal protein Aurora-A kinase is associated with poor prognosis in epithelial ovarian cancer patients. Clin. Cancer Res. 2007;13:4098–4104
  34. Leonhardt K, Gebhardt R, Mössner J, Lutsenko S, Huster D. Funtional interactions of Cu-ATPase ATP7B with cisplatin and the role of ATP7B in the resistance to the drug. J. Biol. Chem. 2009;284:7793–7802
  35. Lin YG, Immaneni A, Merritt WM, Mangala LS, Kim SW, Shahzad MM, et al. Targeting aurora kinase with MK-0457 inhibits ovarian cancer growth. Clin. Cancer Res. 2008;14:5437–5446
  36. Lindahl T. Instability and decay of the primary structure of DNA. Nature. 1993;362:709–715
  37. Lord RV, Brabender J, Gandara D, Alberola V, Camps C, Domine M, et al. Low ERCC1 expression correlates with prolonged survival after cisplatin plus gemcitabine chemotherapy in non-small cell lung cancer. Clin. Cancer Res. 2002;8:2286–2291
  38. Lutsenko S, Barnes NL, Bartee MY, Dmitriev OY. Function and regulation of human copper-transporting ATPases. Physiol. Rev. 2007;87:1011–1046
  39. Mangala LS, Zuzel V, Schmandt R, Leshane ES, Halder JB, Armaiz-Pena GN, et al. Therapeutic targeting of ATP7B in ovarian carcinoma. Clin. Cancer Res. 2009;15:3770–3780
  40. McGuire WP, Hoskins WJ, Brady MF, Kucera PR, Partridge EE, Look KY, et al. Cyclophosphamide and cisplatin compared with paclitaxel and cisplatin in patients with stage III and stage IV ovarian cancer. New Engl. J. Med. 1996;334:1–6
  41. McLaughlin, J., Markovtsov, V., Li, H., Wong, S., Gelman, M., Zhu, Y., Franci,C., Lang, D., W., Pali, E., Lasaga, J., Low, C., Zhao, F., Chang, B., Gururaja, T.L., Xu, W., Baluom, M., Sweeny, D., Carrol, D., Sran, A., Thota, S., Parmer, M., Romane, A., Clemens, G., Grossbard, E., Qu, K., Jenkins, T., Kinoshita, T., Taylor, V., Holland, S.J., Argade, A., Singh, R., Pine, P., Payan, D.G., Hitoshi, Y., 2009. Preclinical characterization of Aurora kinase inhibitor R763/AS703569 identified through an image-based phenotypic screen. J Cancer Res. Clin. Oncol., doi:10.1007/s00432-009-0641-1.
  42. Meads MB, Gatenby RA, Dalton WS. Environment-mediated drug resistance: a major contributor to minimal residual disease. Nat. Rev. Cancer. 2009;9:665–674
  43. Miyashita H, Uchida T, Mori S, Echigo S, Motegi K. Expression status of Pin1 and cyclins in oral squamous cell carcinoma: Pin1 correlates with Cyclin D1 mRNA expression and clinical significance of cyclins. Oncol. Rep. 2003;10:1045–1048
  44. Morin PJ. Drug resistance and the microenvironment: nature and nurture. Drug Resist. Updat. 2003;6:169–172
  45. Nakayama K, Kanzaki A, Terada K, Mutoh M, Ogawa K, Sugiyama T, et al. Prognostic value of the Cu-transporting ATPase in ovarian carcinoma patients receiving cisplatin-based chemotherapy. Clin. Cancer Res. 2004;10:2804–2811
  46. Ohbu M, Ogawa K, Konno S, Kanzaki A, Terada K, Sugiyama T, et al. Copper-transporting P-type adenosine triphosphatase (ATP7B) is expressed in human gastric carcinoma. Cancer Lett. 2003;189:33–38
  47. Ooi CE, Rabinovich E, Dancis A, Bonifacino JS, Klausner RD. Copper-dependent degradation of the Saccharomyces cerevisiae plasma membrane copper transporter Ctr1p in the apparent absence of endocytosis. EMBO J. 1996;15:3515–3523
  48. Ozols RF, Young RC. Chemotherapy of ovarian cancer. Semin. Oncol. 1984;11:251–263
  49. Pan S, Cheng L, White JT, Lu W, Utleg AG, Yan X, et al. Quantitative proteomics analysis integrated with microarray data reveals that extracellular matrix proteins, catenins, and p53 binding protein 1 are important for chemotherapy response in ovarian cancers. OMICS. 2009;13:345–354
  50. Perez RP. Cellular and molecular determinants of cisplatin resistance. Eur. J. Cancer. 1998;34:1535–1542
  51. Pinto AL, Lippard SJ. Binding of the antitumor drug cis-diamminedichloroplatinum(II) (cisplatin) to DNA. Biochim. Biophys. Acta. 1985;780:167–180
  52. Qian Y, Tiffany-Castiglioni E, Harris ED. Copper transport and kinetics in cultured C6 rat glioma cells. Am. J. Physiol. 1995;269:C892–C898
  53. Rabik CA, Dolan ME. Molecular mechanisms of resistance and toxicity associated with platinating agents. Cancer Treat. Rev. 2007;33:9–23
  54. Reed E, Yu JJ, Davies A, Gannon J, Armentrout SL. Clear cell tumors have higher mRNA levels of ERCC1 and XPB than other histological types of epithelial ovarian cancer. Clin. Cancer Res. 2003;9:5299–5305
  55. Richardson A, Kaye SB. Drug resistance in ovarian cancer: the emerging importance of gene transcription and spatio-temporal regulation of resistance. Drug Resist. Updat. 2005;8:311–321
  56. Rosenberg B, Vancamp L, Krigas T. Inhibition of cell division in Escherichia Coli by electrolysis products from a platinum electrode. Nature. 1965;205:698–699
  57. Rosenberg B, VanCamp L, Trosko JE, Mansour VH. Platinum compounds: a new class of potent antitumour agents. Nature. 1969;222:385–386
  58. Rottenberg S, Jaspers JE, Kersbergen A, van der Burg E, Nygren AO, Zander SA, et al. High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugs. Proc. Natl. Acad. Sci. USA. 2008;105:17079–17084
  59. Sakai W, Swisher EM, Jacquemont C, Chandramohan KV, Couch FJ, Langdon SP, et al. Functional restoration of BRCA2 protein by secobdary mutatuions in BRCA2-mutated ovarian carcinoma. Cancer Res. 2009;69:6381–6386
  60. Sakai W, Swisher EM, Karlan BY, Agarwal MK, Higgins J, Friedman C, et al. Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature. 2008;451:1116–1120
  61. Samimi G, Safaei R, Katano K, Holzer AK, Rochdi M, Tomioka M, et al. Increased expression of the copper efflux transporter ATP7A mediates resistance to cisplatin, carboplatin, and oxaliplatin in ovarian cancer cells. Clin. Cancer Res. 2004;10:4661–4669
  62. Selvakumaran M, Pisarcik DA, Bao R, Yeung AT, Hamilton TC. Enhanced cisplatin cytotoxicity by disturbing the nucleotide excision repair pathway in ovarian cancer cell lines. Cancer Res. 2003;63:1311–1316
  63. Sethi T, Rintoul RC, Moore SM, MacKinnon AC, Salter D, Choo C, et al. Extracellular matrix proteins protect small cell lung cancer cells against apoptosis: a mechanism for small cell lung cancer growth and drug resistance in vivo. Nat. Med. 1999;5:662–668
  64. Sherman-Baust CA, Weeraratna AT, Rangel LB, Pizer ES, Cho KR, Schwartz DR, et al. Remodeling of the extracellular matrix through overexpression of collagen VI contributes to cisplatin resistance in ovarian cancer cells. Cancer Cell. 2003;3:377–386
  65. Shiotsu Y, Kiyoi H, Ishikawa Y, Tanizaki R, Shimizu M, Umehara H, et al. KW-2449, a novel multikinase inhibitor, suppresses the growth of leukemia cells with FLT3 mutations or T3151-mutated BCR/ABL translocation. Blood. 2009;114:1607–1617
  66. Shirota Y, Stoehlmacher J, Brabender J, Xiong YP, Uetake H, Danenberg KD, et al. ERCC1 and thymidylate synthase mRNA levels predict survival for colorectal cancer patients receiving combination oxaliplatin and fluorouracil chemotherapy. J. Clin. Oncol. 2001;19:4298–4304
  67. Sood AK, Buller RE. Drug resistance in ovarian cancer: from the laboratory to the clinic. Obstet. Gynecol. 1998;92:312–319
  68. Steffensen KD, Waldstrom M, Jakobsen A. The relationship of platinum resistance and ERCC1 protein expression in epithelial ovarian cancer. Int. J. Gynecol. Cancer. 2009;19:820–825
  69. Stewart DJ. Mechanisms of resistance to cisplatin and carboplatin. Crit. Rev. Oncol. Hematol. 2007;63:12–31
  70. Stordal B, Davey R. A systematic review of genes involved in the inverse resistance relationship between cisplatin and paclitaxel chemotherapy: Role of BRCA1. Current Cancer Drug Targets. 2009;9:354–365
  71. Sugeno H, Takebayashi Y, Higashimoto M, Ogura Y, Shibukawa G, Kanzaki A, et al. Expression of copper-transporting P-type adenosine triphosphatase (ATP7B) in human hepatocellular carcinoma. Anticancer Res. 2004;24:1045–1048
  72. Sun C, Chan F, Briassouli P, Linardopoulos S. Aurora kinase inhibition downregulates NF-kappaB and sensitises tumour cells to chemotherapeutic agents. Biochem. Biophys. Res. Commun. 2007;352:220–225
  73. Swisher EM, Sakai W, Karlan BY, Wurz K, Urban N, Taniguchi T. Secondary BRCA1 mutations in BRCA1-mutated ovarian carcinomas with platinum resistance. Cancer Res. 2008;68:2581–2586
  74. Van Hensbergen Y, Broxterman HJ, Rana S, van Diest PJ, Duyndam MC, Hoekman K, et al. Reduced growth, increased vasccular area, and reduced response to cisplatin in CD13-overexpressing human ovarian cancer xenografts. Clin. Cancer Res. 2004;10:1180–1191
  75. Vasey PA. Resistance to chemotherapy in advanced ovarian cancer: mechanisms and current strategies. Br. J. Cancer. 2003;89(Suppl. 3):S23–S28
  76. Yang H, He L, Kruk P, Nicosia SV, Cheng JQ. Aurora-A induces cell survival and chemoresistance by activation of Akt through a p53-dependent manner in ovarian cancer cells. Int. J. Cancer. 2006;119:2304–2312

PII: S1368-7646(09)00050-8

doi: 10.1016/j.drup.2009.09.001

Drug Resistance Updates
Volume 12, Issue 6 , Pages 148-152 , December 2009