Resistance to chemotherapy in cancer: A complex and integrated cellular response

Pharmacology

Volumn 81, Issue 4, 2008, Pages 275-300

  Mellor, Howard R ^a   Callaghan, Richard ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Anticancer drugs; Cancer chemotherapy; Drug resistance; Multidrug resistance; Pharmacodynamic resistance; Pharmacokinetic resistance

Indexed keywords

ANTHRACYCLINE; BLEOMYCIN; CARBOPLATIN; CARMUSTINE; CISPLATIN; CYCLOPHOSPHAMIDE; DAUNORUBICIN; DJ 927; DOCETAXEL; DOXORUBICIN; ELACRIDAR; EPIRUBICIN; FLUOROURACIL; GEMCITABINE; HYCAMPTIN; IDARUBICIN; IFOSFAMIDE; IRINOTECAN; LOMEGUATRIB; METHOTREXATE; MITOMYCIN C; NAVELBINE; OXALIPLATIN; TEMOZOLOMIDE; TIRAPAZAMINE; TOPOTECAN; UNINDEXED DRUG; VINBLASTINE; VINCRISTINE; VINDESINE; VINFLUNINE; VINLEUROSINE;

ACUTE LYMPHOCYTIC LEUKEMIA; ADENOCARCINOMA; ALKYLATION; APOPTOSIS; BREAST CANCER; CANCER CELL; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CANCER SURVIVAL; CLINICAL TRIAL; COLON CANCER; COLORECTAL CANCER; COMBINATION CHEMOTHERAPY; DNA ALKYLATION; DNA DAMAGE; DNA METHYLATION; DNA REPAIR; DRUG ABSORPTION; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG MECHANISM; DRUG SENSITIVITY; DRUG TARGETING; DRUG TRANSFORMATION; DRUG TRANSPORT; ESOPHAGUS CANCER; GLIOBLASTOMA; GLIOMA; HODGKIN DISEASE; HUMAN; HYPOXIA; LUNG CANCER; LYMPHOMA; MELANOMA; MULTIDRUG RESISTANCE; MULTIPLE MYELOMA; NONHODGKIN LYMPHOMA; NONHUMAN; OSTEOSARCOMA; OVARY CANCER; PANCREAS CANCER; PH; PRIORITY JOURNAL; PROSTATE CANCER; REVIEW; SQUAMOUS CELL CARCINOMA; TESTIS CANCER; TREATMENT FAILURE; UROGENITAL TRACT TUMOR;

ANIMALS; ANTINEOPLASTIC AGENTS; DRUG RESISTANCE, NEOPLASM; HUMANS; NEOPLASMS; PHENOTYPE;

EID: 43449133278     PISSN: 00317012     EISSN: None     Source Type: Journal    
DOI: 10.1159/000115967     Document Type: Review

References (281)

1. Giaccia AJ, Kastan MB: The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev 1998;12:2973-2983.
2. Haupt S, Berger M, Goldberg Z, Haupt Y: Apoptosis - the p53 network. J Cell Sci 2003;116:4077-4085.
3. Lohrum MA, Vousden KH: Regulation and activation of p53 and its family members. Cell Death Differ 1999;6:1162-1168.
4. Post LE: Selectively replicating adenoviruses for cancer therapy: an update on clinical development. Curr Opin Invest Drugs 2002;3:1768-1772.
5. Wen SF, Mahavni V, Quijano E, Shinoda J, Grace M, Musco-Hobkinson ML, Yang TY, Chen Y, Runnenbaum I, Horowitz J, Maneval D, Hutchins B, Buller R: Assessment of p53 gene transfer and biological activities in a clinical study of adenovirus-p53 gene therapy for recurrent ovarian cancer. Cancer Gene Ther 2003;10:224-238.
6. Ferreira CG, Tolis C, Giaccone G: p53 and chemosensitivity. Ann Oncol 1999;10:1011-1021.
7. Bassing CH, Alt FW: The cellular response to general and programmed DNA double strand breaks. DNA Repair (Amst) 2004;3:781-796.
8. Madhusudan S, Middleton MR: The emerging role of DNA repair proteins as predictive, prognostic and therapeutic targets in cancer. Cancer Treat Rev 2005;31:603-617.
9. Lord RV, Brabender J, Gandara D, Alberola V, Camps C, Domine M, Cardenal F, Sanchez JM, Gumerlock PH, Taron M, Sanchez JJ, Danenberg KD, Danenberg PV, Rosell R: 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.
10. Rosell R, Taron M, Barnadas A, Scagliotti G, Sarries C, Roig B: Nucleotide excision repair pathways involved in cisplatin resistance in non-small-cell lung cancer. Cancer Control 2003;10:297-305.
11. Jiricny J: The multifaceted mismatch-repair system. Nat Rev Mol Cell Biol 2006;7:335-346.
12. Fedier A, Fink D: Mutations in DNA mismatch repair genes: implications for DNA damage signaling and drug sensitivity (review). Int J Oncol 2004;24:1039-1047.
13. Pors K, Patterson LH: DNA Mismatch repair deficiency, resistance to cancer chemotherapy and the development of hypersensitive agents. Curr Top Med Chem 2005;5:1133.
14. Trivedi RN, Almeida KH, Fornsaglio JL, Schamus S, Sobol RW: The role of base excision repair in the sensitivity and resistance to temozolomide-mediated cell death. Cancer Res 2005;65:6394-6400.
15. Liu L, Gerson SL: Therapeutic impact of methoxyamine: blocking repair of abasic sites in the base excision repair pathway. Curr Opin Invest Drugs 2004;5:623-627.
16. Hail N Jr, Carter BZ, Konopleva M, Andreeff M: Apoptosis effector mechanisms: a requiem performed in different keys. Apoptosis 2006;11:889-904.
17. Kerr JF: History of the events leading to the formulation of the apoptosis concept. Toxicology 2002;181-182:471-474.
18. Majno G, Joris I: Apoptosis, oncosis, and necrosis: an overview of cell death. Am J Pathol 1995;146:3-15.
19. Deng X, Kornblau SM, Ruvolo PP, May WS Jr: Regulation of Bcl2 phosphorylation and potential significance for leukemic cell chemoresistance. J Natl Cancer Inst Monogr 2001:30-37.
20. Sjostrom J, Blomqvist C, von Boguslawski K, Bengtsson NO, Mjaaland I, Malmstrom P, Ostenstadt B, Wist E, Valvere V, Takayama S, Reed JC, Saksela E: The predictive value of bcl-2, bax, bcl-xL, bag-1, fas, and fasL for chemotherapy response in advanced breast cancer. Clin Cancer Res 2002;8:811-816.
21. Ghaneh P, Kawesha A, Evans JD, Neoptolemos JP: Molecular prognostic markers in pancreatic cancer. J Hepatobiliary Pancreat Surg 2002;9:1-11.
22. Mrozek A, Petrowsky H, Sturm I, Kraus J, Hermann S, Hauptmann S, Lorenz M, Dorken B, Daniel PT: Combined p53/Bax mutation results in extremely poor prognosis in gastric carcinoma with low microsatellite instability. Cell Death Differ 2003;10:461-467.
23. Oliveira C, Seruca R, Seixas M, Sobrinho-Simoes M: The clinicopathological features of gastric carcinomas with microsatellite instability may be mediated by mutations of different 'target genes': a study of the TGFbeta RII, IGFII R, and BAX genes. Am J Pathol 1998;153:1211-1219.
24. Baylin SB, Herman JG, Graff JR, Vertino PM, Issa JP: Alterations in DNA methylation: a fundamental aspect of neoplasia. Adv Cancer Res 1998;72:141-196.
25. Herman JG, Baylin SB: Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003;349:2042-2054.
26. Teitz T, Lahti JM, Kidd VJ: Aggressive childhood neuroblastomas do not express caspase-8: an important component of programmed cell death. J Mol Med 2001;79:428-436.
27. Issa JP: DNA methylation as a therapeutic target in cancer. Clin Cancer Res 2007;13:1634-1637.
28. Fulda S, Kufer MU, Meyer E, van Valen F, Dockhorn-Dworniczak B, Debatin KM: Sensitization for death receptor- or drug-induced apoptosis by re-expression of caspase-8 through demethylation or gene transfer. Oncogene 2001;20:5865-5877.
29. Soejima H, Zhao W, Mukai T: Epigenetic silencing of the MGMT gene in cancer. Biochem Cell Biol 2005;83:429-437.
30. Giles GI, Sharma RP: Topoisomerase enzymes as therapeutic targets for cancer chemotherapy. Med Chem 2005;1:383-394.
31. Martincic D, Hande KR: Topoisomerase II inhibitors. Cancer Chemother Biol Response Modif 2005;22:101-121.
32. Pommier Y: Topoisomerase I inhibitors: camptothecins and beyond. Nat Rev Cancer 2006;6:789-802.
33. Baldwin EL, Osheroff N: Etoposide, topoisomerase II and cancer. Curr Med Chem Anticancer Agents 2005;5:363-372.
34. Mathijssen RH, Loos WJ, Verweij J, Sparreboom A: Pharmacology of topoisomerase I inhibitors irinotecan (CPT-11) and topotecan. Curr Cancer Drug Targets 2002;2:103-123.
35. Warburg O: On the origin of cancer cells. Science 1956;123:309-314.
36. Griffiths JR: Are cancer cells acidic? Br J Cancer 1991;64:425-427.
37. Negendank W: Studies of human tumors by MRS: a review. NMR Biomed 1992;5:303-324.
38. Wike-Hooley JL, Haveman J, Reinhold HS: The relevance of tumour pH to the treatment of malignant disease. Radiother Oncol 1984;2:343-366.
39. Roos A: Weak acids, weak bases and intracellular pH. Respir Physiol 1978;33:27-30.
40. Hasuda K, Lee C, Tannock IF: Antitumor activity of nigericin and 5-(N-ethyl-N-isopropyl) amiloride: an approach to therapy based on cellular acidification and the inhibition of regulation of intracellular pH. Oncol Res 1994;6:259-268.
41. Raghunand N, He X, van Sluis R, Mahoney B, Baggett B, Taylor CW, Paine-Murrieta G, Roe D, Bhujwalla ZM, Gillies RJ: Enhancement of chemotherapy by manipulation of tumour pH. Br J Cancer 1999;80:1005-1011.
42. Sahin AA, Ro JY, el-Naggar AK, Wilson PL, Teague K, Blick M, Ayala AG: Tumor proliferative fraction in solid malignant neoplasms: a comparative study of Ki-67 immunostaining and flow cytometric determinations. Am J Clin Pathol 1991;96:512-519.
43. Demirel D, Laucirica R, Fishman A, Owens RG, Grey MM, Kaplan AL, Ramzy I: Ovarian tumors of low malignant potential: correlation of DNA index and S-phase fraction with histopathologic grade and clinical outcome. Cancer 1996;77:1494-1500.
44. Ikonen JT, Ojala A, Salenius JP, Mattila J, Riekkinen H, Wigren T: DNA flow cytometry in surgically treated lung cancer - prognostic significance. Scand Cardiovasc J 1999;33:228-233.
45. Sahin AA, Ro JY, Brown RW, Ordonez NG, Cleary KR, el-Naggar AK, Wilson P, Ayala AG: Assessment of Ki-67-derived tumor proliferative activity in colorectal adenocarcinomas. Mod Pathol 1994;7:17-22.
46. Blain SW, Scher HI, Cordon-Cardo C, Koff A: p27 as a target for cancer therapeutics. Cancer Cell 2003;3:111-115.
47. Deshmukh P, Ramsey L, Garewal HS: Ki-67 labeling index is a more reliable measure of solid tumor proliferative activity than tritiated thymidine labeling. Am J Clin Pathol 1990;94:192-195.
48. 1/S transition through regulation of p27 expression. J Biol Chem 2001;276:7919-7926.
49. Scholzen T, Gerdes J: The Ki-67 protein: from the known and the unknown. J Cell Physiol 2000;182:311-322.
50. Mellor HR, Ferguson DJ, Callaghan R: A model of quiescent tumour microregions for evaluating multicellular resistance to chemotherapeutic drugs. Br J Cancer 2005;93:302-309.
51. Dang CV, Semenza GL: Oncogenic alterations of metabolism. Trends Biochem Sci 1999;24:68-72.
52. Harris AL: Hypoxia - a key regulatory factor in tumour growth. Nat Rev Cancer 2002;2:38-47.
53. Maxwell PH, Dachs GU, Gleadle JM, Nicholls LG, Harris AL, Stratford IJ, Hankinson O, Pugh CW, Ratcliffe PJ: Hypoxia-inducible factor-1 modulates gene expression in solid tumors and influences both angiogenesis and tumor growth. Proc Natl Acad Sci USA 1997;94:8104-8109.
54. Semenza GL: Expression of hypoxia-inducible factor 1: mechanisms and consequences. Biochem Pharmacol 2000;59:47-53.
55. Shannon AM, Bouchier-Hayes DJ, Condron CM, Toomey D: Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies. Cancer Treat Rev 2003;29:297-307.
56. Lluis JM, Morales A, Blasco C, Colell A, Mari M, Garcia-Ruiz C, Fernandez-Checa JC: Critical role of mitochondrial glutathione in the survival of hepatocytes during hypoxia. J Biol Chem 2005;280:3224-3232.
57. Mansfield KD, Simon MC, Keith B: Hypoxic reduction in cellular glutathione levels requires mitochondrial reactive oxygen species. J Appl Physiol 2004;97:1358-1366.
58. Murphy BJ, Laderoute KR, Chin RJ, Sutherland RM: Metallothionein IIA is up-regulated by hypoxia in human A431 squamous carcinoma cells. Cancer Res 1994;54:5808-5810.
59. Wilson TR, Longley DB, Johnston PG: Chemoresistance in solid tumours. Ann Oncol 2006;17(suppl 10):x315-324.
60. Bjornaes I, Rofstad EK: Transvascular and interstitial transport of a 19 kDa linear molecule in human melanoma xenografts measured by contrast-enhanced magnetic resonance imaging. J Magn Reson Imaging 2001;14:608-616.
61. Graff BA, Kvinnsland Y, Skretting A, Rofstad EK: Intratumour heterogeneity in the uptake of macromolecular therapeutic agents in human melanoma xenografts. Br J Cancer 2003;88:291-297.
62. Jain RK: Delivery of molecular medicine to solid tumors: lessons from in vivo imaging of gene expression and function. J Control Release 2001;74:7-25.
63. Heldin CH, Rubin K, Pietras K, Ostman A: High interstitial fluid pressure - an obstacle in cancer therapy. Nat Rev Cancer 2004;4:806-813.
64. Modok S, Scott R, Alderden RA, Hall MD, Mellor HR, Bohic S, Roose T, Hambley TW, Callaghan R: Transport kinetics of four- and six-coordinate platinum compounds in the multicell layer tumour model. Br J Cancer 2007;97:194-200.
65. Juliano RL, Ling V: A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Biophys Acta 1976;455:152-162.
66. Gottesman MM, Fojo T, Bates SE: Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2002;2:48-58.
67. Cole SP, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, Stewart AJ, Kurz EU, Duncan AM, Deeley RG: Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 1992;258:1650-1654.
68. Miyake K, Mickley L, Litman T, Zhan Z, Robey R, Cristensen B, Brangi M, Greenberger L, Dean M, Fojo T, Bates SE: Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: demonstration of homology to ABC transport genes. Cancer Res 1999;59:8-13.
69. Ross DD, Yang W, Abruzzo LV, Dalton WS, Schneider E, Lage H, Dietel M, Greenberger L, Cole SP, Doyle LA: Atypical multidrug resistance: breast cancer resistance protein messenger RNA expression in mitoxantrone-selected cell lines. J Natl Cancer Inst 1999;91:429-433.
70. Hall MD, Mellor HR, Callaghan R, Hambley TW: Basis for design and development of platinum(IV) anticancer complexes. J Med Chem 2007;50:3403-3411.
71. Jansen BA, Brouwer J, Reedijk J: Glutathione induces cellular resistance against cationic dinuclear platinum anticancer drugs. J Inorg Biochem 2002;89:197-202.
72. Hagrman D, Goodisman J, Dabrowiak JC, Souid AK: Kinetic study on the reaction of cisplatin with metallothionein. Drug Metab Dispos 2003;31:916-923.
73. Hishikawa Y, Abe S, Kinugasa S, Yoshimura H, Monden N, Igarashi M, Tachibana M, Nagasue N: Overexpression of metallothionein correlates with chemoresistance to cisplatin and prognosis in esophageal cancer. Oncology 1997;54:342-347.
74. Surowiak P, Materna V, Kaplenko I, Spaczynski M, Dietel M, Lage H, Zabel M: Augmented expression of metallothionein and glutathione S-transferase pi as unfavourable prognostic factors in cisplatin-treated ovarian cancer patients. Virchows Arch 2005;447:626-633.
75. Surowiak P, Materna V, Maciejczyk A, Pudelko M, Markwitz E, Spaczynski M, Dietel M, Zabel M, Lage H: Nuclear metallothionein expression correlates with cisplatin resistance of ovarian cancer cells and poor clinical outcome. Virchows Arch 2007;450:279-285.
76. Dhaini HR, Thomas DG, Giordano TJ, Johnson TD, Biermann JS, Leu K, Hollenberg PF, Baker LH: Cytochrome P450 CYP3A4/5 expression as a biomarker of outcome in osteosarcoma. J Clin Oncol 2003;21:2481-2485.
77. Downie D, McFadyen MC, Rooney PH, Cruickshank ME, Parkin DE, Miller ID, Telfer C, Melvin WT, Murray GI: Profiling cytochrome P450 expression in ovarian cancer: identification of prognostic markers. Clin Cancer Res 2005;11:7369-7375.
78. Gharavi N, El-Kadi AO: Expression of cytochrome P450 in lung tumor. Curr Drug Metab 2004;5:203-210.
79. Miyoshi Y, Taguchi T, Kim SJ, Tamaki Y, Noguchi S: Prediction of response to docetaxel by immunohistochemical analysis of CYP3A4 expression in human breast cancers. Breast Cancer 2005;12:11-15.
80. Wu MH, Yan B, Humerickhouse R, Dolan ME: Irinotecan activation by human carboxylesterases in colorectal adenocarcinoma cells. Clin Cancer Res 2002;8:2696-2700.
81. Kojima A, Hackett NR, Crystal RG: Reversal of CPT-11 resistance of lung cancer cells by adenovirus-mediated gene transfer of the human carboxylesterase cDNA. Cancer Res 1998;58:4368-4374.
82. Kojima A, Hackett NR, Ohwada A, Crystal RG: In vivo human carboxylesterase cDNA gene transfer to activate the prodrug CPT-11 for local treatment of solid tumors. J Clin Invest 1998;101:1789-1796.
83. Matherly LH: Molecular and cellular biology of the human reduced folate carrier. Prog Nucleic Acid Res Mol Biol 2001;67:131-162.
84. Chaney SG, Sancar A: DNA repair: enzymatic mechanisms and relevance to drug response. J Natl Cancer Inst 1996;88:1346-1360.
85. Hurley LH: DNA and its associated processes as targets for cancer therapy. Nat Rev Cancer 2002;2:188-200.
86. Drablos F, Feyzi E, Aas PA, Vaagbo CB, Kavli B, Bratlie MS, Pena-Diaz J, Otterlei M, Slupphaug G, Krokan HE: Alkylation damage in DNA and RNA-repair mechanisms and medical significance. DNA Repair (Amst) 2004;3:1389-1407.
87. Krokan HE, Standal R, Slupphaug G: DNA glycosylases in the base excision repair of DNA. Biochem J 1997;325(Pt 1):1-16.
88. Plosky B, Samson L, Engelward BP, Gold B, Schlaen B, Millas T, Magnotti M, Schor J, Scicchitano DA: Base excision repair and nucleotide excision repair contribute to the removal of N-methylpurines from active genes. DNA Repair (Amst) 2002;1:683-696.
89. Mitra S, Kaina B: Regulation of repair of alkylation damage in mammalian genomes. Prog Nucleic Acid Res Mol Biol 1993;44:109-142.
90. 6-methylguanine-DNA methyltransferase in pediatric primary brain tumors: relation to patient and tumor characteristics. Clin Cancer Res 2001;7:613-619.
91. 6-methylguanine-DNA methyltransferase in human normal and malignant lung tissues. Cancer Invest 1993;11:258-263.
92. 6-methylguanine-DNA methyltransferase in the resistance of pancreatic tumors to DNA alkylating agents. Cancer Res 1997;57:5360-5368.
93. 6-alkylguanine DNA-alkyltransferase in human liver and melanoma. Br J Cancer 1992;66:355-360.
94. 6-alkylguanine-DNA alkyltransferase expression in normal and malignant human colon. Clin Cancer Res 1996;2:577-584.
95. Belanich M, Pastor M, Randall T, Guerra D, Kibitel J, Alas L, Li B, Citron M, Wasserman P, White A, Eyre H, Jaeckle K, Schulman S, Rector D, Prados M, Coons S, Shapiro W, Yarosh D: Retrospective study of the correlation between the DNA repair protein alkyltransferase and survival of brain tumor patients treated with carmustine. Cancer Res 1996;56:783-788.
96. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, Mirimanoff RO, Cairncross JG, Janzer RC, Stupp R: MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005;352:997-1003.
97. Esteller M, Garcia-Foncillas J, Andion E, Goodman SN, Hidalgo OF, Vanaclocha V, Baylin SB, Herman JG: Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med 2000;343:1350-1354.
98. Paz MF, Yaya-Tur R, Rojas-Marcos I, Reynes G, Pollan M, Aguirre-Cruz L, Garcia-Lopez JL, Piquer J, Safont MJ, Balana C, Sanchez-Cespedes M, Garcia-Villanueva M, Arribas L, Esteller M: CpG island hypermethylation of the DNA repair enzyme methyltransferase predicts response to temozolomide in primary gliomas. Clin Cancer Res 2004;10:4933-4938.
99. 6-alkylguanines increases sensitivity to the cytotoxic effects of alkylating agents. Biochem Biophys Res Commun 1985;132:178-185.
100. 6-methylguanine as a free base. Cancer Res 1986;46:1663-1668.
101. 6- methylguanine. Cancer Chemother Pharmacol 1989;25:103-108.
102. 6- benzylguanine provides a means to evaluate the role of this protein in protection against carcinogenic and therapeutic alkylating agents. Proc Natl Acad Sci USA 1990;87:5368-5372.
103. 6-benzylguanine. Biochemistry 1993;32:11998-12006.
104. 6-benzylguanine and carmustine in patients with advanced soft tissue sarcoma. Cancer Chemother Pharmacol 2006;58:634-639.
105. 6-(4-bromothenyl)guanine improves the therapeutic index of temozolomide against A375M melanoma xenografts. Int J Cancer 2000;85:248-252.
106. 6-(4-bromothenyl)guanine on different temozolomide schedules in a human melanoma xenograft model. Int J Cancer 2002;100:615-617.
107. 6 -alkylguanine-DNA-alkyltransferase: phase I safety, pharmacodynamic, and pharmacokinetic trial and evaluation in combination with temozolomide in patients with advanced solid tumors. Clin Cancer Res 2006;12:1577-1584.
108. Zhang J, Tian Q, Chan SY, Duan W, Zhou S: Insights into oxazaphosphorine resistance and possible approaches to its circumvention. Drug Resist Updat 2005;8:271-297.
109. Chen CS, Lin JT, Goss KA, He YA, Halpert JR, Waxman DJ: Activation of the anticancer prodrugs cyclophosphamide and ifosfamide: identification of cytochrome P450 2B enzymes and site-specific mutants with improved enzyme kinetics. Mol Pharmacol 2004;65:1278-1285.
110. Qiu R, Kalhorn TF, Slattery JT: ABCC2-mediated biliary transport of 4-glutathionylcyclophosphamide and its contribution to elimination of 4-hydroxycyclophosphamide in rat. J Pharmacol Exp Ther 2004;308:1204-1212.
111. Tian Q, Zhang J, Tan TM, Chan E, Duan W, Chan SY, Boelsterli UA, Ho PC, Yang H, Bian JS, Huang M, Zhu YZ, Xiong W, Li X, Zhou S: Human multidrug resistance associated protein 4 confers resistance to camptothecins. Pharm Res 2005;22:1837-1853.
112. Burger H, Foekens JA, Look MP, Meijervan Gelder ME, Klijn JG, Wiemer EA, Stoter G, Nooter K: RNA expression of breast cancer resistance protein, lung resistance-related protein, multidrug resistance-associated proteins 1 and 2, and multidrug resistance gene 1 in breast cancer: correlation with chemotherapeutic response. Clin Cancer Res 2003;9:827-836.
113. Filipits M, Pohl G, Rudas M, Dietze O, Lax S, Grill R, Pirker R, Zielinski CC, Hausmaninger H, Kubista E, Samonigg H, Jakesz R: Clinical role of multidrug resistance protein 1 expression in chemotherapy resistance in early-stage breast cancer: the Austrian Breast and Colorectal Cancer Study Group. J Clin Oncol 2005;23:1161-1168.
114. Tanner B, Hengstler JG, Dietrich B, Henrich M, Steinberg P, Weikel W, Meinert R, Kaina B, Oesch F, Knapstein PG: Glutathione, glutathione S-transferase alpha and pi, and aldehyde dehydrogenase content in relationship to drug resistance in ovarian cancer. Gynecol Oncol 1997;65:54-62.
115. Vester U, Kranz B, Zimmermann S, Buscher R, Hoyer PF: The response to cyclophosphamide in steroid-sensitive nephrotic syndrome is influenced by polymorphic expression of glutathion-S-transferases-M1 and -P1. Pediatr Nephrol 2005;20:478-481.
116. Sladek NE, Kollander R, Sreerama L, Kiang DT: Cellular levels of aldehyde dehydrogenases (ALDH1A1 and ALDH3A1) as predictors of therapeutic responses to cyclophosphamide-based chemotherapy of breast cancer: a retrospective study. Rational individualization of oxazaphosphorine-based cancer chemotherapeutic regimens. Cancer Chemother Pharmacol 2002;49:309-321.
117. Sreerama L, Rekha GK, Sladek NE: Phenolic antioxidant-induced overexpression of class-3 aldehyde dehydrogenase and oxazaphosphorine-specific resistance. Biochem Pharmacol 1995;49:669-675.
118. 6-methylguanine-DNA methyl transferase gene expression and prognosis in breast carcinoma. Int J Oncol 2002;21:1125-1131.
119. 6-alkylguanine-DNA alkyltransferase. Cancer Chemother Pharmacol 1999;43:80-85.
120. Jamieson ER, Lippard SJ: Structure, recognition, and processing of cisplatin-DNA adducts. Chem Rev 1999;99:2467-2498.
121. Dabholkar M, Bostick-Bruton F, Weber C, Bohr VA, Egwuagu C, Reed E: ERCC1 and ERCC2 expression in malignant tissues from ovarian cancer patients. J Natl Cancer Inst 1992;84:1512-1517.
122. Dabholkar M, Vionnet J, Bostick-Bruton F, Yu JJ, Reed E: Messenger RNA levels of XPAC and ERCC1 in ovarian cancer tissue correlate with response to platinum-based chemotherapy. J Clin Invest 1994;94:703-708.
123. Reed E, Dabholkar M, Thornton K, Thompson C, Yu JJ, Bostick-Bruton F: Evidence for the appearance of mRNAs of nucleotide excision repair genes, in human ovarian cancer tissues. Oncol Rep 2000;7:1123-1128.
124. Scartozzi M, Franciosi V, Campanini N, Benedetti G, Barbieri F, Rossi G, Berardi R, Camisa R, Silva RR, Santinelli A, Ardizzoni A, Crino L, Rindi G, Cascinu S: Mismatch repair system (MMR) status correlates with response and survival in non-small cell lung cancer (NSCLC) patients. Lung Cancer 2006;53:103-109.
125. 2/M arrest requires a full complement of the mismatch repair protein hMLH1. Embo J 2003;22:2245-2254.
126. di Pietro M, Marra G, Cejka P, Stojic L, Menigatti M, Cattaruzza MS, Jiricny J: Mismatch repair-dependent transcriptome changes in human cells treated with the methylating agent N-methyl-n′-nitro-N-nitrosoguanidine. Cancer Res 2003;63:8158-8166.
127. Ikeda K, Sakai K, Yamamoto R, Hareyama H, Tsumura N, Watari H, Shimizu M, Minakami H, Sakuragi N: Multivariate analysis for prognostic significance of histologic subtype, GST-pi, MDR-1, and p53 in stages II-IV ovarian cancer. Int J Gynecol Cancer 2003;13:776-784.
128. Siu LL, Banerjee D, Khurana RJ, Pan X, Pflueger R, Tannock IF, Moore MJ: The prognostic role of p53, metallothionein, P-glycoprotein, and MIB-1 in muscle-invasive urothelial transitional cell carcinoma. Clin Cancer Res 1998;4:559-565.
129. Arts HJ, Katsaros D, de Vries EG, Massobrio M, Genta F, Danese S, Arisio R, Scheper RJ, Kool M, Scheffer GL, Willemse PH, van der Zee AG, Suurmeijer AJ: Drug resistance-associated markers P-glycoprotein, multidrug resistance-associated protein 1, multidrug resistance-associated protein 2, and lung resistance protein as prognostic factors in ovarian carcinoma. Clin Cancer Res 1999;5:2798-2805.
130. Komatsu M, Sumizawa T, Mutoh M, Chen ZS, Terada K, Furukawa T, Yang XL, Gao H, Miura N, Sugiyama T, Akiyama S: Copper-transporting P-type adenosine triphosphatase (ATP7B) is associated with cisplatin resistance. Cancer Res 2000;60:1312-1316.
131. Choi MK, Kim DD: Platinum transporters and drug resistance. Arch Pharm Res 2006;29:1067-1073.
132. 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.
133. Nakayama K, Kanzaki A, Terada K, Mutoh M, Ogawa K, Sugiyama T, Takenoshita S, Itoh K, Yaegashi N, Miyazaki K, Neamati N, Takebayashi Y: Prognostic value of the Cutransporting ATPase in ovarian carcinoma patients receiving cisplatin-based chemotherapy. Clin Cancer Res 2004;10:2804-2811.
134. Ohbu M, Ogawa K, Konno S, Kanzaki A, Terada K, Sugiyama T, Takebayashi Y: Copper-transporting P-type adenosine triphosphatase (ATP7B) is expressed in human gastric carcinoma. Cancer Lett 2003;189:33-38.
135. Kanzaki A, Toi M, Neamati N, Miyashita H, Oubu M, Nakayama K, Bando H, Ogawa K, Mutoh M, Mori S, Terada K, Sugiyama T, Fukumoto M, Takebayashi Y: Copper-transporting P-type adenosine triphosphatase (ATP7B) is expressed in human breast carcinoma. Jpn J Cancer Res 2002;93:70-77.
136. Aida T, Takebayashi Y, Shimizu T, Okamura C, Higasimoto M, Kanzaki A, Nakayama K, Terada K, Sugiyama T, Miyazaki K, Ito K, Takenoshita S, Yaegashi N: Expression of copper-transporting P-type adenosine triphosphatase (ATP7B) as a prognostic factor in human endometrial carcinoma. Gynecol Oncol 2005;97:41-45.
137. Kaina B, Lohrer H, Karin M, Herrlich P: Overexpressed human metallothionein IIA gene protects Chinese hamster ovary cells from killing by alkylating agents. Proc Natl Acad Sci USA 1990;87:2710-2714.
138. Dziegiel P, Forgacz J, Suder E, Surowiak P, Kornafel J, Zabel M: Prognostic significance of metallothionein expression in correlation with Ki-67 expression in adenocarcinomas of large intestine. Histol Histopathol 2003;18:401-407.
139. McCluggage WG, Strand K, Abdulkadir A: Immunohistochemical localization of metallothionein in benign and malignant epithelial ovarian tumors. Int J Gynecol Cancer 2002;12:62-65.
140. Surowiak P, Dziegiel P, Matkowski R, Kornafel J, Wojnar A, Zabe M: Immunocytochemical evaluation of metallothionein (MT) expression in myoepithelial cells of ductal mammary carcinoma and its relation to survival time: analysis of 7-year course of the disease. Folia Histochem Cytobiol 2002;40:199-200.
141. Satoh T, Nishida M, Tsunoda H, Kubo T: Expression of glutathione S-transferase pi (GST-pi) in human malignant ovarian tumors. Eur J Obstet Gynecol Reprod Biol 2001;96:202-208.
142. Cullen KJ, Newkirk KA, Schumaker LM, Aldosari N, Rone JD, Haddad BR: Glutathione S-transferase pi amplification is associated with cisplatin resistance in head and neck squamous cell carcinoma cell lines and primary tumors. Cancer Res 2003;63:8097-8102.
143. Mayr D, Pannekamp U, Baretton GB, Gropp M, Meier W, Flens MJ, Scheper R, Diebold J: Immunohistochemical analysis of drug resistance-associated proteins in ovarian carcinomas. Pathol Res Pract 2000;196:469-475.
144. Schuijer M, Berns EM: TP53 and ovarian cancer. Hum Mutat 2003;21:285-291.
145. Fraser M, Leung B, Jahani-Asl A, Yan X, Thompson WE, Tsang BK: Chemoresistance in human ovarian cancer: the role of apoptotic regulators. Reprod Biol Endocrinol 2003;1:66.
146. Mabuchi S, Ohmichi M, Nishio Y, Hayasaka T, Kimura A, Ohta T, Saito M, Kawagoe J, Takahashi K, Yada-Hashimoto N, Sakata M, Motoyama T, Kurachi H, Tasaka K, Murata Y: Inhibition of NFkappaB increases the efficacy of cisplatin in in vitro and in vivo ovarian cancer models. J Biol Chem 2004;279:23477-23485.
147. Mansouri A, Ridgway LD, Korapati AL, Zhang Q, Tian L, Wang Y, Siddik ZH, Mills GB, Claret FX: Sustained activation of JNK/p38 MAPK pathways in response to cisplatin leads to Fas ligand induction and cell death in ovarian carcinoma cells. J Biol Chem 2003;278:19245-19256.
148. Niedner H, Christen R, Lin X, Kondo A, Howell SB: Identification of genes that mediate sensitivity to cisplatin. Mol Pharmacol 2001;60:1153-1160.
149. Schimmer AD, Welsh K, Pinilla C, Wang Z, Krajewska M, Bonneau MJ, Pedersen IM, Kitada S, Scott FL, Bailly-Maitre B, Glinsky G, Scudiero D, Sausville E, Salvesen G, Nefzi A, Ostresh JM, Houghten RA, Reed JC: Small-molecule antagonists of apoptosis suppressor XIAP exhibit broad antitumor activity. Cancer Cell 2004;5:25-35.
150. Jordan MA, Wendell K, Gardiner S, Derry WB, Copp H, Wilson L: Mitotic block induced in HeLa cells by low concentrations of paclitaxel (Taxol) results in abnormal mitotic exit and apoptotic cell death. Cancer Res 1996;56:816-825.
151. Schiff PB, Horwitz SB: Taxol stabilizes microtubules in mouse fibroblast cells. Proc Natl Acad Sci USA 1980;77:1561-1565.
152. Rowinsky EK, Donehower RC: Paclitaxel (taxol). N Engl J Med 1995;332:1004-1014.
153. Snyder JP, Nettles JH, Cornett B, Downing KH, Nogales E: The binding conformation of Taxol in beta-tubulin: a model based on electron crystallographic density. Proc Natl Acad Sci USA 2001;98:5312-5316.
154. Rowinsky EK, Tolcher AW: Antimicrotubule agents; in Devita VT Jr, Hellman S, Rosenberg SA (eds): Cancer Principles and Practice. Philadelphia, Lippincott, Williams & Wilkins, 2001, pp 431-452.
155. Figgitt DP, Wiseman LR: Docetaxel: an update of its use in advanced breast cancer. Drugs 2000;59:621-651.
156. Wiseman LR, Spencer CM: Paclitaxel: an update of its use in the treatment of metastatic breast cancer and ovarian and other gynaecological cancers. Drugs Aging 1998;12:305-334.
157. Henderson IC, Berry DA, Demetri GD, Cirrincione CT, Goldstein LJ, Martino S, Ingle JN, Cooper MR, Hayes DF, Tkaczuk KH, Fleming G, Holland JF, Duggan DB, Carpenter JT, Frei E 3rd, Schilsky RL, Wood WC, Muss HB, Norton L: Improved outcomes from adding sequential paclitaxel but not from escalating doxorubicin dose in an adjuvant chemotherapy regimen for patients with node-positive primary breast cancer. J Clin Oncol 2003;21:976-983.
158. Piccart MJ, Lohrisch C, Duchateau L, Buyse M: Taxanes in the adjuvant treatment of breast cancer: why not yet? J Natl Cancer Inst Monogr 2001:88-95.
159. Jones SE, Savin MA, Holmes FA, O'Shaughnessy JA, Blum JL, Vukelja S, Mc-Intyre KJ, Pippen JE, Bordelon JH, Kirby R, Sandbach J, Hyman WJ, Khandelwal
160. Noguchi S: Predictive factors for response to docetaxel in human breast cancers. Cancer Sci 2006;97:813-820.
161. Hopper-Borge E, Chen ZS, Shchaveleva I, Belinsky MG, Kruh GD: Analysis of the drug resistance profile of multidrug resistance protein 7 (ABCC10): resistance to docetaxel. Cancer Res 2004;64:4927-4930.
162. Lecureur V, Sun D, Hargrove P, Schuetz EG, Kim RB, Lan LB, Schuetz JD: Cloning and expression of murine sister of P-glycoprotein reveals a more discriminating transporter than MDR1/P-glycoprotein. Mol Pharmacol 2000;57:24-35.
163. Hill BT, Whelan RD, Shellard SA, McClean S, Hosking LK: Differential cytotoxic effects of docetaxel in a range of mammalian tumor cell lines and certain drug resistant sublines in vitro. Invest New Drugs 1994;12:169-182.
164. Le LH, Moore MJ, Siu LL, Oza AM, MacLean M, Fisher B, Chaudhary A, de Alwis DP, Slapak C, Seymour L: Phase I study of the multidrug resistance inhibitor zosuquidar administered in combination with vinorelbine in patients with advanced solid tumours. Cancer Chemother Pharmacol 2005;56:154-160.
165. Engels FK, Sparreboom A, Mathot RA, Verweij J: Potential for improvement of docetaxel-based chemotherapy: a pharmacological review. Br J Cancer 2005;93:173-177.
166. Modok S, Mellor HR, Callaghan R: Modulation of multidrug resistance efflux pump activity to overcome chemoresistance in cancer. Curr Opin Pharmacol 2006;6:350-354.
167. Kemper EM, Verheij M, Boogerd W, Beijnen JH, van Tellingen O: Improved penetration of docetaxel into the brain by coadministration of inhibitors of P-glycoprotein. Eur J Cancer 2004;40:1269-1274.
168. Gokmen-Polar Y, Escuin D, Walls CD, Soule SE, Wang Y, Sanders KL, Lavallee TM, Wang M, Guenther BD, Giannakakou P, Sledge GW Jr: Beta-tubulin mutations are associated with resistance to 2-methoxyestradiol in MDA-MB-435 cancer cells. Cancer Res 2005;65:9406-9414.
169. Hari M, Loganzo F, Annable T, Tan X, Musto S, Morilla DB, Nettles JH, Snyder JP, Greenberger LM: Paclitaxel-resistant cells have a mutation in the paclitaxel-binding region of beta-tubulin (Asp26Glu) and less stable microtubules. Mol Cancer Ther 2006;5:270-278.
170. Shalli K, Brown I, Heys SD, Schofield AC: Alterations of beta-tubulin isotypes in breast cancer cells resistant to docetaxel. Faseb J 2005;19:1299-1301.
171. Diaz JF, Menendez M, Andreu JM: Thermodynamics of ligand-induced assembly of tubulin. Biochemistry 1993;32:10067-10077.
172. Sale S, Sung R, Shen P, Yu K, Wang Y, Duran GE, Kim JH, Fojo T, Oefner PJ, Sikic BI: Conservation of the class I beta-tubulin gene in human populations and lack of mutations in lung cancers and paclitaxel-resistant ovarian cancers. Mol Cancer Ther 2002;1:215-225.
173. Kelley MJ, Li S, Harpole DH: Genetic analysis of the beta-tubulin gene, TUBB, in non-small-cell lung cancer. J Natl Cancer Inst 2001;93:1886-1888.
174. Maeno K, Ito K, Hama Y, Shingu K, Kimura M, Sano M, Nakagomi H, Tsuchiya S, Fujimori M: Mutation of the class I beta-tubulin gene does not predict response to paclitaxel for breast cancer. Cancer Lett 2003;198:89-97.
175. Shionoya M, Jimbo T, Kitagawa M, Soga T, Tohgo A: DJ-927, a novel oral taxane, overcomes P-glycoprotein-mediated multidrug resistance in vitro and in vivo. Cancer Sci 2003;94:459-466.
176. Hill BT: Vinflunine, a second generation novel vinca alkaloid with a distinctive pharmacological profile, now in clinical development and prospects for future mitotic blockers. Curr Pharm Des 2001;7:1199-1212.
177. Jordan MA, Thrower D, Wilson L: Mechanism of inhibition of cell proliferation by Vinca alkaloids. Cancer Res 1991;51:2212-2222.
178. Barnett CJ, Cullinan GJ, Gerzon K, Hoying RC, Jones WE, Newlon WM, Poore GA, Robison RL, Sweeney MJ, Todd GC, Dyke RW, Nelson RL: Structure-activity relationships of dimeric Catharanthus alkaloids. 1. Deacetylvinblastine amide (vindesine) sulfate. J Med Chem 1978;21:88-96.
179. Johnson IS, Armstrong JG, Gorman M, Burnett JP Jr: The vinca alkaloids: a new class of oncolytic agents. Cancer Res 1963;23:1390-1427.
180. Jordan MA, Himes RH, Wilson L: Comparison of the effects of vinblastine, vincristine, vindesine, and vinepidine on microtubule dynamics and cell proliferation in vitro. Cancer Res 1985;45:2741-2747.
181. Mullin K, Houghton PJ, Houghton JA, Horowitz ME: Studies with 4′-deoxyepivincristine (vinepidine), a semisynthetic vinca alkaloid. Biochem Pharmacol 1985;34:1975-1979.
182. Fischer JR, Drings P: Role of vindesine in induction chemotherapy in locally advanced non-small-cell lung cancer. J Cancer Res Clin Oncol 1998;124:4-9.
183. Gralla RJ: Preoperative and adjuvant chemotherapy in non-small cell lung cancer. Semin Oncol 1988;15:8-12.
184. Martini N, Kris MG, Flehinger BJ, Gralla RJ, Bains MS, Burt ME, Heelan R, McCormack PM, Pisters KM, Rigas JR, et al: Preoperative chemotherapy for stage IIIa (N2) lung cancer: the Sloan-Kettering experience with 136 patients. Ann Thorac Surg 1993;55:1365-1373, discussion 1373-1364.
185. Djuanda I, Depenbrock H, Peter R, Block T, Pohlmann G, Rastetter J, Hanauske AR: Efficacy of 5′-nor-anhydrovinblastine (vinorelbine), against freshly explanted clonogenic human tumor cells in vitro. Invest New Drugs 1996;14:153-159.
186. Photiou A, Sheikh MN, Bafaloukos D, Retsas S: Antiproliferative activity of vinorelbine (Navelbine) against six human melanoma cell lines. J Cancer Res Clin Oncol 1992;118:249-254.
187. Bunn PA Jr, Kelly K: New chemotherapeutic agents prolong survival and improve quality of life in non-small cell lung cancer: a review of the literature and future directions. Clin Cancer Res 1998;4:1087-1100.
188. Gregory RK, Smith IE: Vinorelbine - a clinical review. Br J Cancer 2000;82:1907-1913.
189. Johnson SA, Harper P, Hortobagyi GN, Pouillart P: Vinorelbine: an overview. Cancer Treat Rev 1996;22:127-142.
190. Depierre A, Lemarie E, Dabouis G, Garnier G, Jacoulet P, Dalphin JC: A phase II study of Navelbine (vinorelbine) in the treatment of non-small-cell lung cancer. Am J Clin Oncol 1991;14:115-119.
191. Wozniak AJ, Crowley JJ, Balcerzak SP, Weiss GR, Spiridonidis CH, Baker LH, Albain KS, Kelly K, Taylor SA, Gandara DR, Livingston RB: Randomized trial comparing cisplatin with cisplatin plus vinorelbine in the treatment of advanced non-small-cell lung cancer: a Southwest Oncology Group study. J Clin Oncol 1998;16:2459-2465.
192. Kourousis C, Androulakis N, Kakolyris S, Souglakos J, Maltezakis G, Metaxaris G, Chalkiadakis G, Samonis G, Vlachonikolis J, Georgoulias V: First-line treatment of advanced nonsmall cell lung carcinoma with docetaxel and vinorelbine. Cancer 1998;83:2083-2090.
193. Romero A, Rabinovich MG, Vallejo CT, Perez JE, Rodriguez R, Cuevas MA, Machiavelli M, Lacava JA, Langhi M, Romero Acuna L, et al: Vinorelbine as first-line chemotherapy for metastatic breast carcinoma. J Clin Oncol 1994;12:336-341.
194. Aapro MS, Harper P, Johnson SA, Vermorken JB: Developments in cytotoxic chemotherapy: advances in treatment utilising vinorelbine. Crit Rev Oncol Hematol 2001;40:251-263.
195. Goa KL, Faulds D: Vinorelbine: a review of its pharmacological properties and clinical use in cancer chemotherapy. Drugs Aging 1994;5:200-234.
196. Campone M, Cortes-Funes H, Vorobiof D, Martin M, Slabber CF, Ciruelos E, Bourbouloux E, Mendiola C, Delgado FM, Colin C, Aslanis V, Fumoleau P: Vinflunine: a new active drug for second-line treatment of advanced breast cancer. Results of a phase II and pharmacokinetic study in patients progressing after first-line anthracycline/taxane-based chemotherapy. Br J Cancer 2006;95:1161-1166.
197. Kruczynski A, Hill BT: Vinflunine, the latest Vinca alkaloid in clinical development: a review of its preclinical anticancer properties. Crit Rev Oncol Hematol 2001;40:159-173.
198. Ngan VK, Bellman K, Hill BT, Wilson L, Jordan MA: Mechanism of mitotic block and inhibition of cell proliferation by the semisynthetic Vinca alkaloids vinorelbine and its newer derivative vinflunine. Mol Pharmacol 2001;60:225-232.
199. Ngan VK, Bellman K, Panda D, Hill BT, Jordan MA, Wilson L: Novel actions of the antitumor drugs vinflunine and vinorelbine on microtubules. Cancer Res 2000;60:5045-5051.
200. Bennouna J, Fumoleau P, Armand JP, Raymond E, Campone M, Delgado FM, Puozzo C, Marty M: Phase I and pharmacokinetic study of the new vinca alkaloid vinflunine administered as a 10-min infusion every 3 weeks in patients with advanced solid tumours. Ann Oncol 2003;14:630-637.
201. Gottesman MM, Pastan I: Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem 1993;62:385-427.
202. Hill BT: Differing patterns of cross-resistance resulting from exposures to specific antitumour drugs or to radiation in vitro. Cytotechnology 1993;12:265-288.
203. Murren JR, Hait WN: Why haven't we cured multidrug-resistant tumors? Oncol Res 1992;4:1-6.
204. Etievant C, Barret JM, Kruczynski A, Perrin D, Hill BT: Vinflunine (20′,20′-difluoro-3′,4′-dihydrovinorelbine), a novel Vinca alkaloid, which participates in P-glycoprotein (Pgp)-mediated multidrug resistance in vivo and in vitro. Invest New Drugs 1998;16:3-17.
205. Etievant C, Kruczynski A, Barret JM, Tait AS, Kavallaris M, Hill BT: Markedly diminished drug resistance-inducing properties of vinflunine (20′,20′-difluoro-3′,4′-dihydrovinorelbine) relative to vinorelbine, identified in murine and human tumour cells in vivo and in vitro. Cancer Chemother Pharmacol 2001;48:62-70.
206. Pui CH: Childhood leukemias. N Engl J Med 1995;332:1618-1630.
207. Walling J: From methotrexate to pemetrexed and beyond: a review of the pharmacodynamic and clinical properties of antifolates. Invest New Drugs 2006;24:37-77.
208. McGuire JJ, Hsieh P, Coward JK, Bertino JR: Enzymatic synthesis of folylpolyglutamates: characterization of the reaction and its products. J Biol Chem 1980;255:5776-5788.
209. Yao R, Schneider E, Ryan TJ, Galivan J: Human gamma-glutamyl hydrolase: cloning and characterization of the enzyme expressed in vitro. Proc Natl Acad Sci USA 1996;93:10134-10138.
210. Li WW, Waltham M, Tong W, Schweitzer BI, Bertino JR: Increased activity of gamma-glutamyl hydrolase in human sarcoma cell lines: a novel mechanism of intrinsic resistance to methotrexate (MTX). Adv Exp Med Biol 1993;338:635-638.
211. Cole PD, Kamen BA, Gorlick R, Banerjee D, Smith AK, Magill E, Bertino JR: Effects of overexpression of gamma-glutamyl hydrolase on methotrexate metabolism and resistance. Cancer Res 2001;61:4599-4604.
212. Rhee MS, Wang Y, Nair MG, Galivan J: Acquisition of resistance to antifolates caused by enhanced gamma-glutamyl hydrolase activity. Cancer Res 1993;53:2227-2230.
213. Yao R, Rhee MS, Galivan J: Effects of gamma-glutamyl hydrolase on folyl and antifolylpolyglutamates in cultured H35 hepatoma cells. Mol Pharmacol 1995;48:505-511.
214. Alt FW, Kellems RE, Bertino JR, Schimke RT: Selective multiplication of dihydrofolate reductase genes in methotrexate-resistant variants of cultured murine cells. J Biol Chem 1978;253:1357-1370.
215. McIvor RS, Simonsen CC: Isolation and characterization of a variant dihydrofolate reductase cDNA from methotrexate-resistant murine L5178Y cells. Nucleic Acids Res 1990;18:7025-7032.
216. Melera PW, Davide JP, Hession CA, Scotto KW: Phenotypic expression in Escherichia coli and nucleotide sequence of two Chinese hamster lung cell cDNAs encoding different dihydrofolate reductases. Mol Cell Biol 1984;4:38-48.
217. Melera PW, Davide JP, Oen H: Antifolate-resistant Chinese hamster cells: molecular basis for the biochemical and structural heterogeneity among dihydrofolate reductases produced by drug-sensitive and drug-resistant cell lines. J Biol Chem 1988;263:1978-1990.
218. Simonsen CC, Levinson AD: Isolation and expression of an altered mouse dihydrofolate reductase cDNA. Proc Natl Acad Sci USA 1983;80:2495-2499.
219. Assaraf YG: Molecular basis of antifolate resistance. Cancer Metastasis Rev 2007;26:153-181.
220. Spears CP: Clinical resistance to antimetabolites. Hematol Oncol Clin North Am 1995;9:397-413.
221. Longo GS, Gorlick R, Tong WP, Lin S, Steinherz P, Bertino JR: Gamma-glutamyl hydrolase and folylpolyglutamate synthetase activities predict polyglutamylation of methotrexate in acute leukemias. Oncol Res 1997;9:259-263.
222. Rots MG, Pieters R, Peters GJ, Noordhuis P, van Zantwijk CH, Kaspers GJ, Hahlen K, Creutzig U, Veerman AJ, Jansen G: Role of folylpolyglutamate synthetase and folylpolyglutamate hydrolase in methotrexate accumulation and polyglutamylation in childhood leukemia. Blood 1999;93:1677-1683.
223. Whitehead VM, Vuchich MJ, Lauer SJ, Mahoney D, Carroll AJ, Shuster JJ, Esseltine DW, Payment C, Look AT, Akabutu J, et al: Accumulation of high levels of methotrexate polyglutamates in lymphoblasts from children with hyperdiploid (greater than 50 chromosomes) B-lineage acute lymphoblastic leukemia: a Pediatric Oncology Group study. Blood 1992;80:1316-1323.
224. Li WW, Lin JT, Tong WP, Trippett TM, Brennan MF, Bertino JR: Mechanisms of natural resistance to antifolates in human soft tissue sarcomas. Cancer Res 1992;52:1434-1438.
225. Trippett T, Schlemmer S, Elisseyeff Y, Goker E, Wachter M, Steinherz P, Tan C, Berman E, Wright JE, Rosowsky A, et al: Defective transport as a mechanism of acquired resistance to methotrexate in patients with acute lymphocytic leukemia. Blood 1992;80:1158-1162.
226. Goker E, Waltham M, Kheradpour A, Trippett T, Mazumdar M, Elisseyeff Y, Schnieders B, Steinherz P, Tan C, Berman E, et al: Amplification of the dihydrofolate reductase gene is a mechanism of acquired resistance to methotrexate in patients with acute lymphoblastic leukemia and is correlated with p53 gene mutations. Blood 1995;86:677-684.
227. Yang R, Sowers R, Mazza B, Healey JH, Huvos A, Grier H, Bernstein M, Beardsley GP, Krailo MD, Devidas M, Bertino JR, Meyers PA, Gorlick R: Sequence alterations in the reduced folate carrier are observed in osteosarcoma tumor samples. Clin Cancer Res 2003;9:837-844.
228. Gorlick R, Goker E, Trippett T, Steinherz P, Elisseyeff Y, Mazumdar M, Flintoff WF, Bertino JR: Defective transport is a common mechanism of acquired methotrexate resistance in acute lymphocytic leukemia and is associated with decreased reduced folate carrier expression. Blood 1997;89:1013-1018.
229. Ifergan I, Meller I, Issakov J, Assaraf YG: Reduced folate carrier protein expression in osteosarcoma: implications for the prediction of tumor chemosensitivity. Cancer 2003;98:1958-1966.
230. Matherly LH, Taub JW, Wong SC, Simpson PM, Ekizian R, Buck S, Williamson M, Amylon M, Pullen J, Camitta B, Ravindranath Y: Increased frequency of expression of elevated dihydrofolate reductase in T-cell versus B-precursor acute lymphoblastic leukemia in children. Blood 1997;90:578-589.
231. Midgley R, Kerr D: Colorectal cancer. Lancet 1999;353:391-399.
232. Copur S, Aiba K, Drake JC, Allegra CJ, Chu E: Thymidylate synthase gene amplification in human colon cancer cell lines resistant to 5-fluorouracil. Biochem Pharmacol 1995;49:1419-1426.
233. Johnston PG, Drake JC, Trepel J, Allegra CJ: Immunological quantitation of thymidylate synthase using the monoclonal antibody TS 106 in 5-fluorouracil-sensitive and -resistant human cancer cell lines. Cancer Res 1992;52:4306-4312.
234. Peters GJ, Backus HH, Freemantle S, van Triest B, Codacci-Pisanelli G, van der Wilt CL, Smid K, Lunec J, Calvert AH, Marsh S, McLeod HL, Bloemena E, Meijer S, Jansen G, van Groeningen CJ, Pinedo HM: Induction of thymidylate synthase as a 5-fluorouracil resistance mechanism. Biochim Biophys Acta 2002;1587:194-205.
235. Matsuyama R, Togo S, Shimizu D, Momiyama N, Ishikawa T, Ichikawa Y, Endo I, Kunisaki C, Suzuki H, Hayasizaki Y, Shimada H: Predicting 5-fluorouracil chemosensitivity of liver metastases from colorectal cancer using primary tumor specimens: three-gene expression model predicts clinical response. Int J Cancer 2006;119:406-413.
236. Ciaparrone M, Quirino M, Schinzari G, Zannoni G, Corsi DC, Vecchio FM, Cassano A, La Torre G, Barone C: Predictive role of thymidylate synthase, dihydropyrimidine dehydrogenase and thymidine phosphorylase expression in colorectal cancer patients receiving adjuvant 5-fluorouracil. Oncology 2006;70:366-377.
237. Lassmann S, Hennig M, Rosenberg R, Nahrig J, Schreglmann J, Krause F, Poignee-Heger M, Nekarda H, Hofler H, Werner M: Thymidine phosphorylase, dihydropyrimidine dehydrogenase and thymidylate synthase mRNA expression in primary colorectal tumors - correlation to tumor histopathology and clinical follow-up. Int J Colorectal Dis 2006;21:238-247.
238. Giovannetti E, Del Tacca M, Mey V, Funel N, Nannizzi S, Ricci S, Orlandini C, Boggi U, Campani D, Del Chiaro M, Iannopollo M, Bevilacqua G, Mosca F, Danesi R: Transcription analysis of human equilibrative nucleoside transporter-1 predicts survival in pancreas cancer patients treated with gemcitabine. Cancer Res 2006;66:3928-3935.
239. Bergman AM, Eijk PP, Ruiz van Haperen VW, Smid K, Veerman G, Hubeek I, van den Ijssel P, Ylstra B, Peters GJ: In vivo induction of resistance to gemcitabine results in increased expression of ribonucleotide reductase subunit M1 as the major determinant. Cancer Res 2005;65:9510-9516.
240. Nakahira S, Nakamori S, Tsujie M, Takahashi Y, Okami J, Yoshioka S, Yamasaki M, Marubashi S, Takemasa I, Miyamoto A, Takeda Y, Nagano H, Dono K, Umeshita K, Sakon M, Monden M: Involvement of ribonucleotide reductase M1 subunit overexpression in gemcitabine resistance of human pancreatic cancer. Int J Cancer 2007;120:1355-1363.
241. Nakano Y, Tanno S, Koizumi K, Nishikawa T, Nakamura K, Minoguchi M, Izawa T, Mizukami Y, Okumura T, Kohgo Y: Gemcitabine chemoresistance and molecular markers associated with gemcitabine transport and metabolism in human pancreatic cancer cells. Br J Cancer 2007;96:457-463.
242. Smid K, Bergman AM, Eijk PP, Veerman G, van Haperen VW, van den Ijssel P, Ylstra B, Peters GJ: Micro-array analysis of resistance for gemcitabine results in increased expression of ribonucleotide reductase subunits. Nucleosides Nucleotides Nucleic Acids 2006;25:1001-1007.
243. Wang JC: Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 2002;3:430-440.
244. Wall ME, Wani MC: Camptothecin and taxol: discovery to clinic - thirteenth Bruce F. Cain Memorial Award Lecture. Cancer Res 1995;55:753-760.
245. Hsiang YH, Hertzberg R, Hecht S, Liu LF: Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I. J Biol Chem 1985;260:14873-14878.
246. Wall ME, Wani MC, Cook CE, Palmer KH, McPhail HT, Sim GA: Plant antitumour agents. 1. The isolation and structure of camptothecin, a novel alkaloidal leukemia and tumour inhibitor from Camptotheca acuminata. J Am Chem Soc 1966;88:3888-3890.
247. Gottlieb JA, Guarino AM, Call JB, Oliverio VT, Block JB: Preliminary pharmacologic and clinical evaluation of camptothecin sodium (NSC-100880). Cancer Chemother Rep 1970;54:461-470.
248. Hsiang YH, Liu LF: Identification of mammalian DNA topoisomerase I as an intracellular target of the anticancer drug camptothecin. Cancer Res 1988;48:1722-1726.
249. Gerrits CJ, de Jonge MJ, Schellens JH, Stoter G, Verweij J: Topoisomerase I inhibitors: the relevance of prolonged exposure for present clinical development. Br J Cancer 1997;76:952-962.
250. Tsao YP, Russo A, Nyamuswa G, Silber R, Liu LF: Interaction between replication forks and topoisomerase I-DNA cleavable complexes: studies in a cell-free SV40 DNA replication system. Cancer Res 1993;53:5908-5914.
251. Armstrong DK, Spriggs D, Levin J, Poulin R, Lane S: Hematologic safety and tolerability of topotecan in recurrent ovarian cancer and small cell lung cancer: an integrated analysis. Oncologist 2005;10:686-694.
252. Kawahara M: Irinotecan in the treatment of small cell lung cancer: a review of patient safety considerations. Expert Opin Drug Saf 2006;5:303-312.
253. Hautefaye P, Cimetiere B, Pierre A, Leonce S, Hickman J, Laine W, Bailly C, Lavielle G: Synthesis and pharmacological evaluation of novel non-lactone analogues of camptothecin. Bioorg Med Chem Lett 2003;13:2731-2735.
254. ten Bokkel Huinink W, Gore M, Carmichael J, Gordon A, Malfetano J, Hudson I, Broom C, Scarabelli C, Davidson N, Spanczynski M, Bolis G, Malmstrom H, Coleman R, Fields SC, Heron JF: Topotecan versus paclitaxel for the treatment of recurrent epithelial ovarian cancer. J Clin Oncol 1997;15:2183-2193.
255. Garcia-Carbonero R, Supko JG: Current perspectives on the clinical experience, pharmacology, and continued development of the camptothecins. Clin Cancer Res 2002;8:641-661.
256. von Pawel J, Schiller JH, Shepherd FA, Fields SZ, Kleisbauer JP, Chrysson NG, Stewart DJ, Clark PI, Palmer MC, Depierre A, Carmichael J, Krebs JB, Ross G, Lane SR, Gralla R: Topotecan versus cyclophosphamide, doxorubicin, and vincristine for the treatment of recurrent small-cell lung cancer. J Clin Oncol 1999;17:658-667.
257. Beran M, Kantarjian H, O'Brien S, Koller C, al-Bitar M, Arbuck S, Pierce S, Moore M, Abbruzzese JL, Andreeff M, Keating M, Estey E: Topotecan, a topoisomerase I inhibitor, is active in the treatment of myelodysplastic syndrome and chronic myelomonocytic leukemia. Blood 1996;88:2473-2479.
258. Levine EG, Cirrincione CT, Szatrowski TP, Canellos G, Norton L, Henderson IC: Phase II trial of topotecan in advanced breast cancer: a Cancer and Leukemia Group B study. Am J Clin Oncol 1999;22:218-222.
259. Perez-Soler R, Fossella FV, Glisson BS, Lee JS, Murphy WK, Shin DM, Kemp BL, Lee JJ, Kane J, Robinson RA, Lippman SM, Kurie JM, Huber MH, Raber MN, Hong WK: Phase II study of topotecan in patients with advanced non-small-cell lung cancer previously untreated with chemotherapy. J Clin Oncol 1996;14:503-513.
260. Rowinsky EK, Baker SD, Burks K, O'Reilly S, Donehower RC, Grochow LB: High-dose topotecan with granulocyte-colony stimulating factor in fluoropyrimidine-refractory colorectal cancer: a phase II and pharmacodynamic study. Ann Oncol 1998;9:173-180.
261. Rougier P, Bugat R, Douillard JY, Culine S, Suc E, Brunet P, Becouarn Y, Ychou M, Marty M, Extra JM, Bonneterre J, Adenis A, Seitz JF, Ganem G, Namer M, Conroy T, Negrier S, Merrouche Y, Burki F, Mousseau M, Herait P, Mahjoubi M: Phase II study of irinotecan in the treatment of advanced colorectal cancer in chemotherapy-naive patients and patients pretreated with fluorouracil-based chemotherapy. J Clin Oncol 1997;15:251-260.
262. Douillard JY, Cunningham D, Roth AD, Navarro M, James RD, Karasek P, Jandik P, Iveson T, Carmichael J, Alakl M, Gruia G, Awad L, Rougier P: Irinotecan combined with fluorouracil compared with fluorouracil alone as first-line treatment for metastatic colorectal cancer: a multicentre randomised trial. Lancet 2000;355:1041-1047.
263. Hoki Y, Fujimori A, Pommier Y: Differential cytotoxicity of clinically important camptothecin derivatives in P-glycoprotein-overexpressing cell lines. Cancer Chemother Pharmacol 1997;40:433-438.
264. van Ark-Otte J, Kedde MA, van der Vijgh WJ, Dingemans AM, Jansen WJ, Pinedo HM, Boven E, Giaccone G: Determinants of CPT-11 and SN-38 activities in human lung cancer cells. Br J Cancer 1998;77:2171-2176.
265. Danks MK, Garrett KE, Marion RC, Whipple DO: Subcellular redistribution of DNA topoisomerase I in anaplastic astrocytoma cells treated with topotecan. Cancer Res 1996;56:1664-1673.
266. Eng WK, McCabe FL, Tan KB, Mattern MR, Hofmann GA, Woessner RD, Hertzberg RP, Johnson RK: Development of a stable camptothecin-resistant subline of P388 leukemia with reduced topoisomerase I content. Mol Pharmacol 1990;38:471-480.
267. Tan KB, Mattern MR, Eng WK, McCabe FL, Johnson RK: Nonproductive rearrangement of DNA topoisomerase I and II genes: correlation with resistance to topoisomerase inhibitors. J Natl Cancer Inst 1989;81:1732-1735.
268. Horenstein MS, Vander Heide RS, L'Ecuyer TJ: Molecular basis of anthracycline-induced cardiotoxicity and its prevention. Mol Genet Metab 2000;71:436-444.
269. Trock BJ, Leonessa F, Clarke R: Multidrug resistance in breast cancer: a meta-analysis of MDR1/gp170 expression and its possible functional significance. J Natl Cancer Inst 1997;89:917-931.
270. Marie JP, Zhou DC, Gurbuxani S, Legrand O, Zittoun R: MDR1/P-glycoprotein in haematological neoplasms. Eur J Cancer 1996;32A:1034-1038.
271. Wunder JS, Bull SB, Aneliunas V, Lee PD, Davis AM, Beauchamp CP, Conrad EU, Grimer RJ, Healey JH, Rock MJ, Bell RS, Andrulis IL: MDR1 gene expression and outcome in osteosarcoma: a prospective, multicenter study. J Clin Oncol 2000;18:2685-2694.
272. Giaccone G, Gazdar AF, Beck H, Zunino F, Capranico G: Multidrug sensitivity phenotype of human lung cancer cells associated with topoisomerase II expression. Cancer Res 1992;52:1666-1674.
273. Danks MK, Warmoth MR, Friche E, Granzen B, Bugg BY, Harker WG, Zwelling LA, Futscher BW, Suttle DP, Beck WT: Single-strand conformational polymorphism analysis of the M r 170,000 isozyme of DNA topoisomerase II in human tumor cells. Cancer Res 1993;53:1373-1379.
274. Matsumoto Y, Takano H, Nagao S, Fojo T: Altered topoisomerase IIalpha and multidrug resistance-associated protein levels during drug selection: adaptations to increasing drug pressure. Jpn J Cancer Res 2001;92:968-974.
275. Koshiyama M, Fujii H, Kinezaki M, Morita Y, Nanno H, Yoshida M: Immunohistochemical expression of topoisomerase IIalpha (Topo IIalpha) and multidrug resistance-associated protein (MRP), plus chemosensitivity testing, as chemotherapeutic indices of ovarian and endometrial carcinomas. Anticancer Res 2001;21:2925-2932.
276. Koshiyama M, Fujii H, Kinezaki M, Yoshida M: Correlation between Topo II alpha expression and chemosensitivity testing for Topo II-targeting drugs in gynaecological carcinomas. Anticancer Res 2001;21:905-910.
277. Dingemans AC, van Ark-Otte J, Span S, Scagliotti GV, van der Valk P, Postmus PE, Giaccone G: Topoisomerase IIalpha and other drug resistance markers in advanced non-small cell lung cancer. Lung Cancer 2001;32:117-128.
278. Kubo A, Yoshikawa A, Hirashima T, Masuda N, Takada M, Takahara J, Fukuoka M, Nakagawa K: Point mutations of the topoisomerase IIalpha gene in patients with small cell lung cancer treated with etoposide. Cancer Res 1996;56:1232-1236.
279. Tinari N, Lattanzio R, Natoli C, Cianchetti E, Angelucci D, Ricevuto E, Ficorella C, Marchetti P, Alberti S, Piantelli M, Iacobelli S: Changes of topoisomerase IIalpha expression in breast tumors after neoadjuvant chemotherapy predicts relapse-free survival. Clin Cancer Res 2006;12:1501-1506.
280. Jarvinen TA, Holli K, Kuukasjarvi T, Isola JJ: Predictive value of topoisomerase IIalpha and other prognostic factors for epirubicin chemotherapy in advanced breast cancer. Br J Cancer 1998;77:2267-2273.
281. Di Leo A, Isola J: Topoisomerase II alpha as a marker predicting the efficacy of anthracyclines in breast cancer: are we at the end of the beginning? Clin Breast Cancer 2003;4:179-186.