Clinical multidrug resistance in cancer: A multifactorial problem

European Journal of Cancer

Volumn 32, Issue 6, 1996, Pages 912-920

  Lehnert, M ^a  

^a CANTONAL HOSPITAL ST GALLEN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CARMUSTINE; CHLORAMBUCIL; CISPLATIN; CYCLOPHOSPHAMIDE; CYCLOSPORIN; CYTOTOXIC AGENT; DNA TOPOISOMERASE (ATP HYDROLYSING); FLUOROURACIL; GLUTATHIONE; GLYCOPROTEIN P; MELPHALAN; NATURAL PRODUCT; VERAPAMIL;

APOPTOSIS; CANCER CELL; CANCER CHEMOTHERAPY; CANCER RESISTANCE; DOSE CALCULATION; DRUG ACCUMULATION; DRUG DETOXIFICATION; DRUG MECHANISM; DRUG TARGETING; DRUG TRANSPORT; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; REVIEW; TREATMENT OUTCOME;

CELL DEATH; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; NEOPLASMS; P-GLYCOPROTEIN;

EID: 0029929867     PISSN: 09598049     EISSN: None     Source Type: Journal    
DOI: 10.1016/0959-8049(96)00069-X     Document Type: Article

References (137)

1. Biedler JL, Riehm H. Cellular resistance to actinomycin D in Chinese hamster cells in vitro: cross-resistance, radioautographic, and cytogenetic studies. Cancer Res 1970, 30, 1174-1184.
2. Dano K. Cross resistance between vinca alkaloids and anthracyclines in Ehrlich ascites tumour in vitro. Cancer Chemother Rep 1972, 56, 701-708.
3. Ling V, Thompson LH. Reduced permeability in CHO cells as a mechanism of resistance to colchicine. J Cell Physiol 1974, 83, 103-111.
4. Biedler JL. Drug resistance: genotype versus phenotype (Thirty-second G.H.A. Clowes Memorial Award lecture). Cancer Res 1994, 54, 666-678.
5. Juliano RL, Ling V. A surface glycoprotein modulating drug permeability in chinese hamster ovary cell mutants. Biochim Biophys Acta 1976, 455, 152-162.
6. Skovsgaard T. Mechanisms of resistance to daunorubicin in Ehrlich ascites tumour cells. Cancer Res 1978, 38, 1785-1791.
7. Beck WT, Mueller TJ, Tanzer LR. Altered surface membrane glycoprotein in vinca alkaloid-resistant human leukemic lymphoblasts. Cancer Res 1979, 39, 2070-2076.
8. Gros P, Neriah YB, Croop JM, Housman DE. Isolation and expression of a cDNA (mdr) that confers multidrug resistance. Nature 1986, 323, 728-731.
9. Roninson IB, Chin JE, Choi P, et al. Isolation of human mdr DNA sequences amplified in multidrug-resistant KB carcinoma cells. Proc Natl Acad Sci USA 1986, 83, 4538-4542.
10. Gerlach JH, Endicott JA, Juranka PF, et al. Homology between P-glycoprotein and a bacterial haemolysin transport protein suggests a model for multidrug resistance. Nature 1986, 324, 485-489.
11. Chen C, Chin J, Ueda K, et al. Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell 1986, 47, 381-389.
12. Ueda K, Cardarelli C, Gottesman M, Pastan I. Expression of a full-length cDNA for the human MDR1 gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc Natl Acad Sci USA 1987, 84, 3004-3008.
13. Gottesman MM, Pastan I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Ann Rev Biochem 1993, 62, 385-427.
14. Cole SPC, Bhardwaj G, Gerlach JH, et al. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 1992, 258, 1650-1654.
15. Grant CE, Valdimarsson G, Hipfner DR, Almquist KC, Cole SPC, Deeley RG. Overexpression of multidrug resistance-associated protein (MRP) increases resistance to natural product drugs. Cancer Res 1994, 54, 357-361.
16. Zaman GJR, Flens MJ, van Leusden MR, et al. The human multidrug resistance-associated protein MRP is a plasma membrane drug-efflux pump. Proc Natl Acad Sci USA 1994, 91, 8822-8826.
17. Glisson B, Gupta R, Hodges P, Ross W. Cross-resistance to intercalating agents in an epipodophyllotoxin-resistant Chinese hamster ovary cell line: evidence for a common intracellular target. Cancer Res 1986, 46, 1939-1942.
18. Pommier Y, Kerrigan D, Schwartz RE, Swack JA, McCurdy A. Altered DNA topoisomerase II activity in Chinese hamster cells resistant to topoisomerase II inhibitors. Cancer Res 1986, 46, 3075-3081.
19. Beck WT, Cirtain MC, Danks MK, et al. Pharmacological, molecular, and cytogenetic analysis of atypical multidrug-resistant human leukemic cells. Cancer Res 1987, 47, 5455-5460.
20. Deffie AM, Batra JK, Goldenberg GJ. Direct correlation between DNA topoisomerase II activity and cytototoxicity in adriamycin-sensitive and resistant P388 leukemia cell lines. Cancer Res 1989, 49, 58-62.
21. Webb CD, Latham MD, Lock RB, Sullivan DM. Attenuated topoisomerase II content directly correlates with a low level of drug resistance in a chinese hamster ovary cell line. Cancer Res 1991, 51, 6543-6549.
22. Wasserman RA, Wang JC. Mechanistic studies of amsacrine-resistant derivatives of DNA topoisomerase II. J Biol Chem 1994, 269, 20943-20951.
23. Schneider E, Hsiang Y-H, Liu LF. DNA topoisomerases in anticancer drug targets. Adv Pharmacol 1990, 21, 149-183.
24. Peters WHM, Roelofs HMJ. Biochemical characterization of resistance to mitoxantrone and adriamycin in Caco-2 human colon adenocarcinoma cells: a possible role for glutathione S-transferases. Cancer Res 1992, 52, 1886-1890.
25. Meijer C, Mulder NH, Timmer-Bosscha H, Sluiter WJ, Meersma GJ, de Vries EGE. Relationship of cellular glutathione to the cytotoxicity and resistance of seven platinum compounds. Cancer Res 1992, 52, 6885-6889.
26. Hao X-Y, Bergh J, Brodin O, Hellman U, Mannervik B. Acquired resistance to cisplatin and doxorubicin in a small lung cancer cell line is correlated to elevated expression of glutathione-linked detoxification enzymes. Carcinogenesis 1994, 15, 1167-1173.
27. Greenbaum M, Letourneau S, Asar H, Schecter RL, Batist G, Cournoyer D. Retrovirus-mediated gene transfer of rat glutathione S-transferase Yc confers alkylating drug resistance in NIH 3T3 mouse fibroblasts. Cancer Res 1994, 54, 4442-4447.
28. Tew KD. Glutathione-associated enzymes in anticancer drug resistance. Cancer Res 1994, 54, 4313-4320.
29. O'Dwyer PJ, Hamilton TC, Yao K-S, Tew KD, Ozols RF. Modulation of glutathione and related enzymes in reversal of resistance to anticancer drugs. Hematol Oncol Clin North Am 1995, 9, 383-396.
30. r 110,000 vesicular protein in non-P-glycoprotein-mediated multidrug resistance. Cancer Res 1993, 53, 1475-1479.
31. Scheffer GL, Wijngaard PLJ, Flens MJ, et al. The drug resistance-related protein LRP is the human major vault protein. Nature Med 1995, 1, 578-582.
32. Goldstein LJ, Galski H, Fojo A, et al. Expression of a multidrug resistance gene in human cancers. J Natl Cancer Inst 1989, 81, 116-124.
33. Leighton JC, Goldstein LJ. P-glycoprotein in adult solid tumors: expression and prognostic significance. Hematol Oncol Clin North Am 1995, 9, 251-274.
34. Marie J-P. P-glycoprotein in adult hematologic malignancies. Hematol Oncol Clin North Am 1995, 9, 239-250.
35. Arceci RJ. Clinical significance of P-glycoprotein in multidrug resistance malignancies. Blood 1993, 81, 2215-2222.
36. Pirker R, Wallner J, Geisslier K, et al. MDR1 gene expression and treatment outcome in acute myeloid leukemia. J Natl Cancer Inst 1991, 83, 708-712.
37. Chan HSL, Thorner PS, Haddad G, Ling V. Immunohistochemical detection of P-glycoprotein: prognostic correlation in soft tissue sarcoma of childhood. J Clin Oncol 1990, 8, 689-704.
38. Chan HSL, Haddad G, Thorner PS, et al. P-glycoprotein expression as a predictor of the outcome of therapy for neuroblastoma. N Engl J Med 1991, 325, 1608-1614.
39. Verrelle P, Meissonnier F, Fonck Y, et al. Clinical relevance of immunohistochemical detection of multidrug resistance P-glycoprotein in breast carcinoma. J Natl Cancer Inst 1991, 83, 111-116.
40. Baldini N, Scotlandi K, Barbanti-Brodano G, et al. Expression of P-glycoprotein in high-grade osteosarcomas in relation to clinical outcome. N Engl J Med 1995, 333, 1380-1385.
41. Burger H, Nooter K, Zaman GJR et al. Expression of the multidrug resistance-associated protein (MRP) in acute and chronic leukemias. Leukemia 1994, 8, 990-997.
42. Schuurhuis GJ, Broxterman HJ, Ossenkoppele GJ, et al. Functional multidrug resistance phenotype associated with combined overexpression of Pgp/MDR1 and MRP together with 1β-D-arabinoruranosylcytosine sensitivity may predict clinical response to acute myeloid leukemia. Clin Cancer Res 1995, 1, 81-93.
43. Schneider E, Cowan KH, Bader H, et al. Increased expression of the multidrug resistance-associated protein gene in relapsed acute leukemia. Blood 1995, 85, 186-193.
44. Nooter K, Westerman AM, Flens MJ, et al. Expression of the multidrug resistance-associated protein (MRP) gene in human cancers. Clin Cancer Res 1995, 1, 1301-1310.
45. McKenna SL, West RR, Whittaker JA, Padua RA, Holmes JA. Topoisomerase II α expression in acute myeloid leukaemia and its relationship to clinical outcome. Leukemia 1994, 8, 1498-1502.
46. Kaufmann SH, Harp JE, Jones RJ, et al. Topoisomerase II levels and drug sensitivity in adult acute myelogenous leukemia. Blood 1994, 83, 517-530.
47. Beck J, Niethammer D, Gekeler V. High mdrl- and MRP-, but low topoisomerase IIα-gene expression in B-cell chronic lymphocytic leukaemias. Cancer Lett 1994, 86, 135-142.
48. Van der Zee AGJ, de Jong S, Keith N, Hollema H, Boonstra H, de Vries EGE. Quantitative and qualitative aspects of topoisomerase I and IIα and β in untreated and platinum/cyclophosphamide treated malignant ovarian tumors. Cancer Res 1994, 54, 749-755.
49. Albin N, Massaad L, Toussaint C, et al. Main drug-metabolizing enzyme systems in human breast tumors and peritumoral tissues. Cancer Res 1993, 53, 3541-3546.
50. 6-alkylguanine-DNA alkyltransferase as potential indicators of constitutive drug resistance in human colorectal tumors. Cancer Res 1991, 51, 2092-2097.
51. 6-alkyl-guanine-DNA alkyltransferase and P-glycoprotein as indicators of drug resistance in tumor and normal lung of patients with lung cancer. Int J Cancer 1994, 59, 629-636.
52. Klys HS, Whillis D, Howard G, Harrison DJ. Glutathione S-transferase expression in the human testis and testicular germ cell neoplasia. Br J Cancer 1992, 66, 589-593.
53. Van der Zee AGJ, van Ommen B, Meijer C, Hollema H, van Bladeren PJ, de Vries EGE. Glutathione S-transferase activity and isoenzyme composition in benign ovarian tumours, untreated malignant ovarian tumours, and malignant ovarian tumours after platinum/cyclophosphamide chemotherapy. Br J Cancer 1992, 66, 930-936.
54. Mulder TPJ, Verspaget HW, Sier CFM, et al. Glutathione S-transferase π in colorectal tumors is predictive for overall survival. Cancer Res 1995, 55, 2696-2702.
55. Izquierdo MA, van der Zee AGJ, Vermorken JB, et al. Drug resistance-associated marker Lrp for prediction of response to chemotherapy and prognosis in advanced ovarian carcinoma. J Natl Cancer Inst 1995, 87, 1230-1237.
56. Smith CAD, Smith G, Wolf CR. Genetic polymorphisms in xenobiotic metabolism. Eur J Cancer 1993, 30A, 1921-1935.
57. May DG. Genetic differences in drug disposition. J Clin Pharmacol 1994, 34, 881-897.
58. Schinkel AH, Smit JJM, van Tellingen O, et al. Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 1994, 77, 491-502.
59. Sutherland R, Carlson J, Durand R, Yuhas J. Spheroids in cancer research. Cancer Res 1981, 41, 2980-2984.
60. Takemura Y, Kobayashi H, Miyachi H, Hayashi K, Sekiguchi S, Ohnuma T. The influence of tumor cell density on cellular accumulation of doxorubicin or cisplatin in vitro. Cancer Chemother Pharmacol 1991, 27, 417-422.
61. Sutherland RM. Cell and environment interactions in tumor microregions: the multicell spheroid model. Science 1988, 240, 177-184.
62. Rooney M, Kish J, Jacobs J, et al. Improved complete response rate and survival in advanced head and neck cancer after three-course induction therapy with 120-hour 5-FU infusion and cisplatin. Cancer 1985, 55, 1123-1128.
63. Jacobs C, Lyman G, Velez-Garcia E, et al. A phase II randomised study comparing cisplatin and fluorouracil as single agents and in combination for advanced squamous cell carcinoma of the head and neck. J Clin Oncol 1992, 10, 257-263.
64. Forastiere AA, Metch B, Schuller DE, et al. Randomized comparison of cisplatin plus fluorouracil and carboplatin plus fluorouracil versus methotrexate in advanced squamous-cell carcinoma of the head and neck: a South-west Oncology Group study. J Clin Oncol 1992, 10, 1245-1251.
65. Lum BL, Kaubisch S, Yahanda AM, et al. Alteration of etoposide pharmacokinetics and phamacodynamics by cyclosporine in a phase I trial to modulate multidrug resistance. J Clin Oncol 1992, 10, 1635-1642.
66. Bartlett NL, Lum BL, Fisher G, et al. Phase I trial of doxorubicin with cyclosporine as a modulator of multidrug resistance. J Clin Oncol 1994, 12, 835-842.
67. Wilson WH, Jamis-Dow C, Bryant G, et al. Phase I and pharmacokinetic study of the multidrug resistance modulator dexverapamil with EPOCH chemotherapy. J Clin Oncol 1995, 13, 1985-1994.
68. Berg SL, Tocher A, O'Shaughnessy JA, et al. Effect of R-verapamil on the pharmacokinetics of paclitaxel in women with breast cancer. J Clin Oncol 1995, 13, 2039-2042.
69. Sparano JA, Wiernik PH, Leaf A, Dutcher JP. Infusional cyclophosphamide, doxorubicin, and etoposide in relapsed and resistant non-Hodgkin's lymphoma: evidence for a schedule-dependent effect favoring infusional administration of chemotherapy. J Clin Oncol 1993, 11, 1071-1079.
70. Wilson WH, Bryant G, Bates S, et al. EPOCH chemotherapy: toxicity and efficacy in relapsed and refractory non-Hodgkin's lymphoma. J Clin Oncol 1993, 11, 1573-1582.
71. Lai G-M, Chen Y-N, Mickley LA, Fojo AT, Bates SE. P-glycoprotein expression and schedule dependence of adriamycin cytotoxicity in human colon carcinoma cell lines. Int J Cancer 1991, 49, 696-703.
72. Lang A, de Giuli R, Lehnert M. Effects of prolonged drug exposure on P-glycoprotein resistance differ for various cytotoxic agents. Proc Am Soc Clin Oncol 1995, 14, 412 (Abstr).
73. Cass CE, Janowska-Wieczorek A, Lynch MA, Sheinin H, Hindenburg AA, Beck WT. Effect of duration of exposure to verapamil on vincristine activity against multidrug-resistant human leukemic cell lines. Cancer Res 1989, 49, 5798-5804.
74. Perez V, Pierre A, Leonce S, Anstett M, Atassi G. Effect of duration of exposure to S9788, cyclosporin A or verapamil on sensitivity of multidrug resistant cells to vincristine or doxorubicin. Anticancer Res 1993, 13, 985-990.
75. Hindenburg AA, Baker MA, Gleyzer E, Stewart VJ, Case N, Taub RN. Effect of verapamil and other agents on the distribution of anthracyclines and on reversal of drug resistance. Cancer Res 1987, 47, 1421-1425.
76. Hindenburg AA, Gervasoni JE, Krishna S, et al. Intracellular distribution and pharmacokinetics of daunorubicin in anthracycline-sensitive and resistant HL-60 cells. Cancer Res 1989, 49, 4607-4614.
77. Gervasoni JE Jr, Fields SZ, Krishna S, et al. Subcellular distribution of daunorubicin in P-glycoprotein-positive and -negative drug-resistant cell lines using laser-assisted confocal microscropy. Cancer Res 1991, 51, 4955-4963.
78. Schuurhuis GJ, Broxterman HJ, de Lange JHM, et al. Early multidrug resistance, defined by changes in intracellular doxorubicin distribution, independent of P-glycoprotein. Br J Cancer 1991, 64, 857-861.
79. Marquart D, Center MS. Drug transport mechanisms in HL60 cells isolated for resistance to adriamycin: evidence for nuclear drug accumulation and redistribution in resistant cells. Cancer Res 1992, 52, 3157-3163.
80. Coley HM, Amos WB, Twentyman PR, Workman P. Examination by laser scanning confocal fluorescence imaging microscopy of the subcellular localization of anthracyclines in parent and multidrug resistant cell lines. Br J Cancer 1993, 67, 1316-1323.
81. Schuurhuis GJ, van Heijningen THM, Cervantes A, et al. Changes in subcellular doxorubicin distribution and cellular accumulation alone can largely account for doxorubicin resistance in SW-1573 lung cancer and MCF-7 breast cancer multidrug resistant tumour cells. Br J Cancer 1993, 68, 898-908.
82. Breuninger LM, Paul S, Gaughan K, et al. Expression of multidrug resistance-associated protein in NIH/3T3 cells confers multidrug resistance associated with increased drug efflux and altered drug distribution. Cancer Res 1995, 55, 5342-5347.
83. Shao Y, de Giuli R, Wyler B, Lehnen M. Overexpression of MDR1/P-glycoprotein and MRP but not LRP is mutually exclusive in multidrug resistant human myeloma cells selected with doxorubicin. Proc Am Assoc Cancer Res 1995, 36, 337 (Abstr).
84. Dietel M, Arps H, Lage H, Niendorf A. Membrane vesicle formation due to acquired mitoxantrone resistance in human gastric carcinoma cell line EPG85-257. Cancer Res 1990, 50, 6100-6106.
85. Jedlitschky G, Leier I, Buchholz U, Center M, Keppler D. ATP-dependent transport of glutathione S-conjugates by the multidrug resistance-associated protein. Cancer Res 1994, 54, 4833-4836.
86. 4 and structurally related compounds. J Biol Chem 1994, 269, 27807-27810.
87. Müller M, Meijer C, Zaman GJR, et al. Overexpression of the gene encoding the multidrug resistance-associated protein results in increased ATP-dependent glutathione S-conjugate transport. Proc Natl Acad Sci USA 1994, 91, 13033-13037.
88. Zaman GJR, Lankelma J, van Tellingen O, et al. Role of glutathione in the export of compounds from cells by the multidrug-resistance-associated protein. Proc Natl Acad Sci USA 1995, 92, 7690-7694.
89. Versantvoort CHM, Broxterman HJ, Bagrij T, Scheper RJ, Twentyman PR. Regulation by glutathione of drug transport in multidrug-resistant human lung tumour cell lines overexpressing multidrug resistance-associated protein. Br J Cancer 1995, 72, 82-89.
90. Schneider E, Yamazaki H, Sinha BK, Cowan KH. Buthionine sulphoximine-mediated sensitisation of etoposide-resistant human breast cancer MCF7 cells overexpressing the multidrug resistance-associated protein involves increased drug accumulation. Br J Cancer 1995, 71, 738-743.
91. Burden DA, Goldsmith LJ, Sullivan DM. Cell-cycle-dependent phosphorylation and activity of Chinese-hamster ovary topoisomerase II. Biochem J 1993, 293, 297-304.
92. Kimura K, Saijo M, Ui M, Enomoto T. Growth state- and cell cycle-dependent fluctuation in the expression of two forms of DNA topoisomerase II and possible specific modification of the higher molecular weight form in the M phase. J Biol Chem 1994, 269, 1173-1176.
93. Ramachandran C, Mead D, Wellham LL, Sauerteig A, Krishan A. Expression of drug resistance-associated mdr1, GST π, and topoisomerase II genes during cell cycle traverse. Biochem Pharmacol 1995, 49, 545-552.
94. Boege F, Andersen A, Jensen S, Zeidler R, Kreipe H. Proliferation-associated nuclear antigen Ki-S1 is identical with topoisomerase IIα. Delineation of a carboxyl-terminal epitope with peptide antibodies. Am J Pathol 1995, 146, 1302-1308.
95. Twentyman PR. Comparative chemosensitivity of exponential versus plateau-phase cells in both in vitro and in vivo model systems. Cancer Treat Rep 1976, 60, 1719-1722.
96. 6-alkylguanine-DNA-alkyl transferase expression and the presence of double minute chromosomes in alkylating agent selected Chinese hamster cells. Carcinogenesis 1992, 13, 483-487.
97. 6-benzylguanine analogues on sensitivity of human tumor cells to the cytotoxic effects of alkylating agents. Cancer Res 1991, 51, 3367-3372.
98. 6-alkylguanine-DNA-alkyltransferase activity and nitrosourea sensitivity in human cancer cell lines. Br J Cancer 1992, 66, 840-843.
99. 6-alkylguanine-DNA-alkyltransferase and nucleotide excision repair activities in human cells. Cancer Res 1992, 52, 2008-2011.
100. 6-ethylguanine in DNA: relation of chemosensitivity in vitro and treatment outcome. Cancer Res 1994, 54, 4524-4531.
101. Zeng-Rong N, Paterson J, Alpert L, Tsao M-S, Viallet J, Alaoui-Jamali MA. Elevated DNA repair capacity is associated with intrinsic resistance of lung cancer to chemotherapy. Cancer Res 1995, 55, 4760-4764.
102. Fujiwara T, Grimm EA, Mukhopadhyay T, Zhang W-W, Owen-Schaub LB, Roth JA. Induction of chemosensitivity in human lung cancer cells in vivo by adenovirus-mediated transfer of the wild-type p53 gene. Cancer Res 1994, 54, 2287-2291.
103. Fan S, El-Deiry WS, Bae I, et al. p53 gene mutations are associated with decreased sensitivity of human lymphoma cells to DNA damaging agents. Cancer Res 1994, 54, 5824-5830.
104. Lowe SW, Bodis S, McClatchey A, et al. p53 status and the efficacy of cancer therapy in vivo. Science 1994, 266, 807-810.
105. Herzog CE, Zwelling LA, McWatters A, Kleinermann ES. Expression of topoisomerase II, Bcl-2, p53 in three human brain tumor cell lines and their possible relationship to intrinsic resistance to etoposide. Clin Cancer Res 1995, 1, 1391-1397.
106. Lasorella A, Lavarone A, Israel MA. Differentiation of neuro-blastoma enhances Bcl-2 expression and induces alterations in apoptosis and drug resistance. Cancer Res 1995, 55, 4711-4716.
107. Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science 1995, 267, 1456-1462.
108. El Rouby S, Thomas A, Costin D, et al. p53 gene mutation in B-cell chronic lymphocytic leukemia is associated with drug resistance and is independent of MDR1/MDR3 gene expression. Blood 1993, 82, 3452-3459.
109. Wattel E, Preudhomme C, Hecquet B, et al. p53 mutations are associated with resistance to chemotherapy and short survival in hematologic malignancies. Blood 1994, 84, 3148-3157.
110. Gasparini G, Barbareschi M, Doglioni C, et al. Expression of bcl-2 protein predicts efficacy of adjuvant treatments in operable node-positive breast cancer. Clin Cancer Res 1995, 1, 189-198.
111. Zhang W, Kornblau SM, Kobayashi T, Gambel A, Claxton D, Deisseroth AB, High levels of constitutive WAF1/Cip 1 protein are associated with chemoresistance in acute myelogenous leukemia. Clin Cancer Res 1995, 1, 1051-1057.
112. Weinstein RS, Jakate SM, Dominguez JM, et al. Relationship of the expression of the multidrug resistance gene product (P-glycoprotein) in human colon carcinoma to local tumor aggressiveness and lymph node metastasis. Cancer Res 1991, 51, 2720-2726.
113. Tobe SW, Noble-Topham SE, Andrulis IL, Hartwick WJ, Skorecki KL, Earner E. Expression of the multiple drug resistance gene in human renal cell carcinoma depends on tumor histology, grade, and stage. Clin Cancer Res 1995, 1, 1611-1615.
114. Giaccone G, Linn SC, Pinedo HM. Multidrug resistance in breast cancer: mechanisms, strategies. Eur J Cancer 1995, 31A (Suppl. 7), S15-S17.
115. Pinedo HM. Drug resistance. The Joseph Steiner Award Lecture 1995. Int J Cancer (in press).
116. Pinedo HM, Giaccone G. P-glycoprotein - a marker of cancer-cell behavior. N Engl J Med 1995, 333, 1417-1419.
117. Chin K-V, Ueda K, Pastan I, Gottesman MM. Modulation of activity of the promoter of the human MDR1 gene by Ras and p53. Science 1992, 255, 459-462.
118. Chen Y, Chen P-L, Lee W-H. Hot-spot p53 mutants interact specifically with two cellular proteins during progression of the cell cycle. Mol Cell Biol 1994, 14, 6764-6772.
119. Nguyen KT, Liu B, Ueda K, Gottesman MM, Pastan I, Chin K-V. Transactivation of the human multidrug resistance (MDR1) gene promoter by p53 mutants. Oncol Res 1994, 6, 71-77.
120. Lin J, Wu X, Chen J, Chang A, Levine AJ. Functions of the p53 protein in growth regulation and tumor suppression. Cold Spring Harbor Symposia on Quantitative Biology, Vol LIX. The Molecular Genetics of Cancer. Plainview, Cold Spring Harbor Laboratory Press, 1994, 215-223.
121. Goldsmith ME, Gudas JM, Schneider E, Cowan KH. Wild type p53 stimulates expression from the human multidrug resistance promoter in p53-negative cell line. J Biol Chem 1995, 270, 1894-1898.
122. Wosikowski K, Regis JT, Rebey RW, et al. Normal p53 status and function despite the development of drug resistance in human breast cancer cells. Cell Growth & Differ 1995, 6, 1395-1403.
123. Preudhomme C, Lepelley, Vachee A, et al. Relationship between p53 gene mutations and multidrug resistance (MDR1) gene expression in myelodysplastic syndromes. Leukemia 1993, 7, 1888-1890.
124. De Angelis P, Stokke T, Smedshammer L, et al. P-glycoprotein is not expressed in a majority of colorectal carcinomas and is not regulated by mutant p53 in vivo. Br J Cancer 1995, 12, 307-311.
125. Abo J, Inokuchi R, Dan K, Nomura T. p53 and N-ras mutations in two new leukemia cell lines established from a patient with multilineage CD7-positive acute leukemia. Blood 1993, 82, 2829-2836.
126. 4 sub-lines with increasing adriamycin resistance. Int J Cancer 1995, 61, 375-380.
127. Shao Y, Wyler B, Lehnert M, Schneider E, Twentyman PR. RPM1 8226 human myeloma cells develop atypical multidrug resistance when mimicking clinical doxorubicin treatment in vitro. Proc Am Assoc Cancer Res 1994, 35, 362 (Abstr).
128. Volm M, Mattern J, Samsel B. Overexpression of P-glycoprotein and glutathione S-transferase-π in resistant non-small cell lung carcinomas of smokers. Br J Cancer 1991, 64, 700-704.
129. Volm M, Mattern J, Samsel B. Relationship of inherent resistance to doxorubicin, proliferative activity and expression of P-glycoprotein 170, and glutathione S-transferase-π in human lung tumors. Cancer 1992, 70, 764-769.
130. Toffoli G, Frustaci S, Tumiotto L, et al. Expression of MDR1 and GST-π in human soft tissue sarcomas: relation to drug resistance and biological aggressiveness. Ann Oncol 1992, 3, 63-69.
131. 6-alkylguanine-DNA-alkyltransferase and P-glycoprotein in adult patients with leukaemia. Br J Haematol 1993, 85, 103-111.
132. Volm M, Kästel M, Mattern J, Efferth T. Expression of resistance factors (P-glycoprotein, glutathione S-transferase-π, and topoisomerase II) and their interrelationship to proto-oncogene products in renal cell carcinomas. Cancer 1993, 71, 3981-3987.
133. Katagiri A, Tomita Y, Nishiyama T, Kimura M, Sato S. Immunohistochemical detection of P-glycoprotein and GSTP1-1 in testis cancer. Br J Cancer 1993, 68, 125-129.
134. Fidler IJ. Modulation of the organ microenvironment for treatment of cancer metastasis. J Natl Cancer Inst 1995, 87, 1588-1592.
135. Dong Z, Radinsky R, Fan D, et al. Organ-specific modulation of steady state mdr gene expression and drug resistance in murine colon cancer cells. J Natl Cancer Inst 1994, 86, 913-920.
136. Barraco SC, Perry RR, Durm ME, et al. Intratumor variability in prognostic indicators may be the cause of conflicting estimates of patient survival and response to therapy. Cancer Res 1994, 54, 5351-5356.
137. Preisler HD, Venugopal P. Regrowth resistance in cancer: why has it been largely ignored? Cell Prolif 1995, 28, 347-356.