Resistance mechanisms and their regulation in lung cancer

Critical Reviews in Oncogenesis

Volumn 7, Issue 3-4, 1996, Pages 227-244

  Volm, Manfred ^a   Mattern, Jürgen ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Cell cycle proteins; Lung cancer; Protooncogenes; Resistance related proteins; Tumor suppressor genes

Indexed keywords

6 O ALKYLGUANINE DNA ALKYLTRANSFERASE; DIHYDROFOLATE REDUCTASE; DNA TOPOISOMERASE (ATP HYDROLYSING); GLUTATHIONE; GLYCOPROTEIN P; HEAT SHOCK PROTEIN; METALLOTHIONEIN; THYMIDYLATE SYNTHASE;

HISTOPATHOLOGY; HUMAN; LUNG BIOPSY; LUNG CANCER; PROTEIN DETERMINATION; PROTO ONCOGENE; REVIEW; TUMOR SUPPRESSOR GENE;

EID: 0030390492     PISSN: 08939675     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevOncog.v7.i3-4.50     Document Type: Review

References (176)

1. Abe, Y., M. Nakamura, E. Ota, Y. Ozeki, S. Tamai, H. Inoue, Y. Ueyama, T. Ogata, and N. Tamaoki: Expression of the multidrug resistance gene (mdr1) in non-small cell lung cancer. Jpn. J. Cancer Res., 85:536-541 (1994).
2. Alama, A., M. Constantini, L. Repetto, P. F. Conte, J. Serrano, A. Nicolin, F. Barbieri, A. Ardizzoni, and P. Bruzzi: Thymidine labeling index as prognostic factor in resected non-small cell lung cancer. Eur. J. Cancer, 26:622-625 (1990).
3. Angel, P. and M. Karin: The role of jun, fos and the AP-1 complex in cell proliferation and transformation. Biochim. Biophys. Acta, 1072:129-157 (1991).
4. Angeletti, C. A., M. Lucchi, G. Fontanini, A. Mussi, A. Chella, A. Ribechini, S. Vignati, and G. Bevilaqua: Prognostic significance of tumoral angiogenesis in completely resected late stage lung carcinoma (stage III A-N2). Cancer, 78:409-415 (1996).
5. Antilla, S., A. Hirvonen, H. Vainio, K. Husgafvel-Pursiainen, J. D. Hayes, and B. Ketterer: Immunohistochemical localization of glutathione S- transferases in human lung. Cancer Res., 53:5643-5648 (1993).
6. Arai, T., T. Kuroishi, Y. Saito, Y. Kurita, T. Naruke, M. Kaneko, and the Japanese Lung Cancer Screening Research Group: Tumor doubling time and prognosis in lung cancer patients: evaluation from chest films and clinical follow-up study. Jpn. J. Clin. Oncol., 24:199-204 (1994).
7. Awasthi, Y. C., S. V. Singh, H. Ahmad, and P. C. Moller: Immunobistochemical evidence for the expression of GST1, GST2, and GST3 gene loci for glutathione S-transferase in human lung. Lung, 165:323-332 (1987).
8. Bookstein, R., J. Y. Shew, P. L. Chen, P. Scully, and W. H. Lee: Suppression of tumorigenicity of human prostate carcinoma cells by replacing a mutated Rb gene. Science, 247:712-715 (1990).
9. Bradley, G., P. F. Juranka, and V. Ling: Mechanisms of multidrug resistance. Biochim. Biophys. Acta, 948:87-128 (1988).
10. Brent, T. P., P. J. Houghton, and J. A. Houghton: O6-alkyguanine-DNA alkyltransferase activity correlates with the therapeutic response of human rhabdomyosarcoma xenografts to 1-(2-chloroethyl)-3-(trans-4-methyl-cyclohexyl)-1-nitrosourea. Proc. Natl. Acad. Sci. U.S.A., 82:2985-2989 (1985).
11. Bukh, A., H. Martinez-Valdez, S. J. Freedman, M. H. Freedman, and A. Cohen: The expression of c-fos, c-jun and c-myc genes is regulated by heat shock in human lymphoid cells. J. Immunol., 144:4835-4840 (1990).
12. Burt, R. K., S. Garfield, K. Johnson, and S. Thorgeirsson: Transformation of rat liver epithelial cells with v-H-ras or v-H-raf causes expression of MDR1, glutathione S-transferase-π, and increased resistance to cytotoxic chemicals. Carcinogenesis, 9:2329-2332 (1988).
13. Carmichael, J., J. B. Mitchel, W. G. De Graff, J. Gamson, A. F. Gazdar, B. E. Johnson, E. Glatstein, and J. D. Minna: Chemosensitivity testing of human lung cancer cell lines using the MTT assay. Br. J. Cancer, 57:540-547 (1985).
14. Carmichael, J., J. B. Mitchell, N. Friedman, A. F. Gazdar, and A. Russo: Glutathione and related enzyme activity in human lung cancer cell lines. Br. J. Cancer, 58:437-440 (1988).
15. Chambers, T. C., E. M. Me Avoy, J. W. Jakobs, and G. Eilon: Protein kinase C phosphorylates P-glycoprotein in multidrug resistant human KB carcinoma cells. J. Biol. Chem., 265:7679-7686 (1990).
16. Chin, J. L., D. Banerjee, S. A. Kadhim, T. E. Kontozoglou, P. J. Chauvin, and M. G. Cherian: Metallothionein in testicular germ cell tumors and drug resistance. Cancer, 72:3029-3035 (1993).
17. Chu, E., J. C. Drake, D. M. Koeller, S. Zinn, C. A. Jamis-Dow, G. C. Yeh, and C. J. Allegra: Induction of thymidylate synthase associated with multidrug resistance in human breast and colon cancer cell lines. Mol. Pharmacol., 39:136-143 (1991).
18. Chu, E., D. M. Voeller, K. L. Jones, T. Takechi, G. F. Maley, F. Maley, S. Segal, and C. J. Allegra: Identification of a thymidylate synthase ribonucleoprotein complex in human colon cancer cells. Mol. Cell. Biol., 14:207-213 (1994).
19. Ciocca, D. R., S. A. W. Fuqua, S. Lock-Lim, D. O. Toft, W. J. Welch, and W. L. McGuire: Response of human breast cancer cells to heat shock and chemotherapeutic drugs. Cancer Res., 52:3648-3654 (1992).
20. Ciocca, D. R., G. M. Clark, A. K. Taudon, S. A. W. Fuqua, W. J. Welch, and W. L. McGuire: Heat shock protein hsp 70 in patients with axillary lymph node-negative breast cancer: Prognostic implications. J. Natl. Cancer. Inst, 85:570-574 (1993).
21. Citron, M., R. Decker, S. Chen, S. Schneider, M. Graver, L. Kleynerman, L. B. Kahn, A. White, M. Schoenhaus, and D. Yarosh: O6-methylguanine-DNA methyltransferase in human normal and tumor tissue from brain, lung, and ovary. Cancer Res., 51:4131-4134 (1991).
22. Citron, M., M. Schoenhaus, M. Graver, M. Hoffman, M. Lewis, P. Wasserman, M. Niederland, L. Kahn, A. White, and D. Yarosh: O6-methylguanine-DNA methyltransferase in human normal and malignant lung tissues. Cancer Invest., 11:258-263 (1993).
23. Clapper, M. L., S. J. Hoffman, N. Carp, P. Watts, L. M. Seestaller, J. L. Weese, and K. D. Tew: Contribution of patient history to the glutathione S-transferase activity of human lung, breast and colon tissue. Carcinogenesis, 12:1957-1961 (1991).
24. Cole, S. P., E. R. Chanda, F. P. Dicke, J. H. Gerlach, and S. E. L. Mirski: Non-P-glycoprotein-mediated multidrug resistance in a small cell lung cancer cell line: evidence for decreased susceptibility to drug-induced DNA damage and reduced levels of topoisomerase II. Cancer Res., 51:3345-3352 (1991).
25. Cole, S. P. C., G. Bhardwaj, J. H. Gerlach, J. E. Mackie, C. E. Grant, K. C. Almquist, A. J. Stewart, E. U. Kurz, A. M. V. Duncan, and R. G. Deeley: Overexpression of a transporter gene in a multidrag-resistant human lung cancer cell line. Science, 258:1650-1654 (1992).
26. Cordon-Cardo, C.: Mutation of cell cycle regulators. Biological and clinical implications for human neoplasia (review). Am. J. Pathol., 147:545-560 (1995).
27. Craft, P.S. and A. L. Harris: Clinical prognostic significance of tumour angiogenesis. Ann. Oncol., 5:305-311 (1994).
28. D'Arpa, P. and L. F. Liu: Topoisomerase-targeting antitumor drugs. Biochim. Biophys. Acta, 989:163-177 (1989).
29. De Vries, E. G. E., C. Meijer, N. H. Mulder, and P. E. Postmus: In vitro chemosensitivity of human lung cancer for vindesine. Eur. J. Cancer, 23:55-60 (1987).
30. Di Ilio, C., G. Del Boccio, A. Aceto, R. Casaccia, F. Mucilli, and G. Federici: Elevation of glutathione transferase activity in human lung tumor. Carcinogenesis, 9:335-340 (1988).
31. Dingemans, A. M. C., J. van Ark-Otte, P. van der Valk, R. M. Apolinario, R. J. Scheper, P. E. Postmus, and G. Giaccone: Expression of the human major vault protein LRP inTiuman lung cancer samples and normal lung tissues. Ann. Oncol., 7:625-630 (1996).
32. Dolan, M. E., A. E. Pegg, R. C. Moschel, and G. B. Grindey: Effect of O6-benzylguanine on the sensitivity of human colon tumor xenografts to 1,3-bis (2-chloroethyl)-1-nitrosourea (BCNU). Biochem. Pharmacol., 46:285-290 (1993).
33. Drewinko, B., M. Patchen, L. Y. Yang, and B. Barlogie: Differential killing efficacy of twenty antitumor drugs on proliferating and nonproliferating human tumor cells. Cancer Res., 41:2328-2333 (1981).
34. Drin, I. B. Schoket, S. Kostic, and I. Vincze: Smoking-related increase in O6-alkylguanine-DNA alkyltransferase activity in human lung tissue. Carcinogenesis, 15:1535-1539 (1994).
35. Dutta, A., R. Chandra, L. Leiter, and S. Lester: Cyclins as marker of tumor proliferation: Immunocytochemical studies in breast cancer. Proc. Natl. Acad. Sci. U.S.A., 92:5386-5390 (1995).
36. Efferth, T. and M. Volm: Antibody-directed therapy of multidrug-resistant tumor cells. Med. Oncol. Tumor Pharmacother., 9:11-19 (1992a).
37. Efferth, T. and M. Volm: Immunocytochemical detection of oncoproteins in animal and human tumor lines with acquired or inherent multidrug resistance. Cancer Detection & Prevention, 16:237-243 (1992b).
38. Efferth, T. and M. Volm: Modulation of P-glycoprotein-mediated multidrug resistance by monoclonal antibodies, immunotoxins or antisense oligodeoxynucleotides in kidney carcinoma and normal kidney cells. Oncology, 50:2107-2115 (1992c).
39. Efferth, T., B. Lathan, and M. Volm: Selective growth-inhibition of multidrug-resistant CHO-cells by the monoclonal antibody 265/F4. Br. J. Cancer, 64:87-89 (1991).
40. Eijdems, E. W. H. M., M. De Haas, A. J. Timmermann, G. P. Van der Schans, E. Kamst, J. De Nooij, G. C. B. Astaldi-Ricotti, P. Borst, and F. Baas: Reduced topoisomerase I activity in multidrug-resistant human non-small cell lung cancer Cell lines. Br. J. Cancer, 71:40-47 (1995).
41. Fan, S., M. L. Smith, D. J., Rivet, D. Duba, Q. Zhan, K. W. Kohn, A. J. Fornace, and P. M. O'Connor: Disruption of p53 function sensitizes breast cancer MCF7 cells to cisplatin and pentoxifylline. Cancer Res., 55:1649-1654 (1995).
42. Fine, P. L., J. A. Patel, and B. A. Chabner: Phorbol esters induce multidrug resistance in human breast cancer cells. Proc. Natl. Acad. Sci. U.S.A., 65:582-586 (1988).
43. Fitzgerald, D. J., M. G. Willingham, C. O. Cardarelli, T. Tsuruo, T. Hamada, M. M. Gottesman and I. Pastan: A monoclonal antibody-Pseudomonas exotoxin conjugate that specifically kills multidrug-resistant cells. Proc. Natl. Acad. Sci. U.S.A., 84:4288-4292 (1987).
44. Fojo, A. T., K. Ueda, D. J. Slamon, D. G. Poplack, M. M. Gottesman, and I. Pastan: Expression of multidrug-resistance gene in human tumors and tissues. Proc. Natl. Acad. Sci. U.S.A., 84:265-269 (1987).
45. Fontanini, G., D. Bigini, S. Vignati, F. Basalo, A. Mussi, M. Lucchi, S. Chine, C. A. Angeletti, A. L. Harris, and G. Bevilaqua: Microvessel counts predicts metastatic disease and survival in non-small cell lung cancer. J. Pathol, 177:57-63 (1995).
46. Fraire, A.E.:Pathology of Lung Cancer. In: Comprehensive Textbook of Thoracic Oncology, Aisner et al., Eds., Williams and Wilkins, Baltimore, 1996.
47. Fujiwara, T., E. A. Grimm, T. Mukhopadhyay, W.-W. Zhang, L. B. Owen-Schaub, and J. A. Roth: Induction of chemosensitivity in human lung cancer cells in vivo by adenovirus-mediated transfer of the wild-type p53 gene. Cancer Res., 54:2287-2291 (1994).
48. Fuqua, S. A. W., S. Oestenreich, S. G. Hilsenbeck, D. D. von Hoff, J. Eckhardt, and C. K. Osborne: Heat shock proteins and drug resistance. Breast Cancer Res. Treat., 32:67-71 (1994).
49. Gewirtz, D. A.: DNA damage, gene expression, growth arrest and cell death. Oncol. Res., 5:397-408 (1993).
50. Giaccone, G., A. F. Gazdar, H. Beck, F. Zunino, and G. Capranico: Multidrug sensitivity phenotype of human lung cancer cells associated with topoisomerase II expression. Cancer Res., 52:1666-1674 (1992).
51. Goldstein, L. J., H. Galski, A. Fojo, M. Willingham, S. L. Lai, A. Gazdar, R. Pirker, A. Green, W. Crist, G. M. Brodeur, M. Lieber, J. Cossman, M. M. Gottesman, and I. Pastan: Expression of a multidrug resistance gene in human cancers. J. Natl. Cancer Inst., 81:116-124 (1989).
52. Gottesman, M. M., and I. Pastan: The multidrug transporter, a double-edged sword. J. Biol. Chem., 263:12163-12166 (1988).
53. Gros, P., Y. B. Neriah, J. M. Croop, and D. E. Housman: Isolation and expression of a complementary DNA that confers multidrug resistance. Nature, 323:728-731 (1986).
54. Hamburger, A. W. and S. E. Salmon: Primary bioassay of human tumor stem cells. Science, 197:461-463 (1977).
55. Hamer, D. H.: Metallothionein. Ann. Rev. Biochem., 55:913-951 (1986).
56. Harbour, J. W., S. L. Lai, J. Whang-Penk, A. F. Gazdar, J. D. Minna, and F. J. Kaye: Abnormalities in structure and expression of the retinoblastoma gene in SCLC. Science, 241:353-357 (1988).
57. Harpole, D. H., W. G. Richards, J. E. Herndon, and D. J. Sugarbaker: Angiogenesis and molecular biologic substaging in patients with stage I non-small cell lung cancer. Ann. Thorac. Surg., 61:1470-1476 (1996).
58. Hart, B. A., G. W. Voss, and P. M. Vacek: Metallothionein in human lung carcinoma. Cancer Lett., 75:121-128 (1993).
59. Herzog, C. E., J. B. Trepel, L. A. Mickley, S. E. Bates, and A. T. Fojo: Various methods of analysis of mdrl/P-glycoprotein in human colon cancer cell lines. J. Natl. Cancer Inst., 84:711-716 (1992).
60. Hickman, J. A.: Apoptosis induced by anticancer drugs. Cancer Metast. Rev., 11:121-139 (1992).
61. 2 predicts survival in advanced cancer of the uterine cervix. Radiother. Oncol., 26:45-50 (1993).
62. Horton, J. K., K. N. Thimmaiah, J. A. Houghton, M. E. Horowitz, and P. J. Houghton: Modulation by verapamil of vincristine pharmacokinetics and toxicity in mice bearing human tumor xenografts. Biochem. Pharmacol., 38:1727-1736 (1989).
63. Huot, J., H. Lambert, G. Roy, and J. Landry: A typical multidrug-resistance conferred by expression of the human HSP 27 heat shock gene in Chinese hamster cells. Eur. J. Pharmacol., 183:1632-1633 (1990).
64. Huot, J., G. Roy, H. Lambert, P. Chretien, and J. Landry: Increased survival after treatments with anticancer agents of Chinese hamster cells expressing the human M,. 27,000 heat shock protein. Cancer Res., 51:245-252 (1991).
65. Johnston, P. G., H. J. Lenz, C. G. Leichman, K. D. Danenberg, C. J. Allegra, P. V. Danenberg, and L. Leichman: Thymidylate synthase gene and protein expression correlate and are associated with response to 5-fluorouracil in human colorectal and gastric tumors. Cancer Res., 55:1407-1412 (1995).
66. Kaina, B., G. Fritz, S. Mitra, and T. Coquerelle: Transfection and expression of human O6-methylguanine-DNA methyltransferase (MGMT) cDNA in Chinese hamster cells: the role of MGMT in protection against the genotoxic effects of alkylating agents. Carcinogenesis, 12:1857-1867 (1991).
67. Kasahara, K., Y. Fujiwara, K. Nishio, T. Ohmori, Y. Sugimoto, K. Komiya, T. Matsuda, and N. Saijo: Metallothionein content correlates with the sensitivity of human small cell lung cancer cell lines to cisplatin. Cancer Res., 51:3237-3242 (1991).
68. Kasahara, K., Y. Fujiwara, Y. Sugimoto, K. Nishio, T. Tamura, T. Matsuda, and N. Saijo: Determinants of response to the DNA topoisomerase II inhibitors doxorubicin and etoposide in human lung cancer cell lines. J. Natl Cancer Inst., 84:113-118 (1992).
69. Kelley, S. L., A. Basu, B. A. Teicher, M. P. Hacker, D. H. Hamer, and J. S. Lazo: Overexpression of metallothionein confers resistance to anticancer drugs. Science, 241:1813-1815 (1988).
70. Kastan, M. B., O. Onkyekwere, D. Sidransky, B. Vogelstein, and R. W. Craig: Participation of p53 protein in the cellular response to DNA damage. Cancer Res., 51:6304-6311 (1991).
71. Keith, F. J., D. A. Bradbury, Y. M. Zhu, and N. H. Russel: Inhibition of bcl-2 with antisense oligonucleotides induces apoptosis and increases the sensitivity of AML blasts to Ara-C. Leukemia, 9:131-138 (1995).
72. Kolch, W., G. Martiny-Baron, A. Kieser, and D. Marme: Regulation of the expression of the VEGF/VPS and its receptors: role in tumor angiogenesis. Breast Cancer Res. Treat., 36:139-155 (1995).
73. Koomägi, R., J. Mattern, and M. Volm: Up-regulation of resistance-related proteins in human lung tumors with poor vascularization. Carcinogenesis, 16:2129-2133 (1995).
74. Lai, S. L., L. J. Goldstein, M. M. Gottesman, I. Pastan, C. M. Tsai, B. E. Johnson, J. L. Mulshine, D. C. Ihde, K. Kayser, and A. Gazdar: MDR1 gene expression in lung cancer. J. Natl. Cancer Inst., 81:1144-1150 (1989).
75. Li, G. C.: Heat shock proteins: role in thermotolerance, drug resistance, and relationship to DNA topoisomerases. NCI Monogr., 4:99-103 (1987).
76. Linsenmeyer, M. E., S. Jefferson, M. Wolf, J. P. Matthews, P. G. Board, and D. M. Woodcock: Levels of expression of the mdr1 gene and glutathione S-transferase genes 2 and 3 and response to chemotherapy in multiple myeloma. Br. J. Cancer, 65:471-475 (1992).
77. Lowe, S. W., H. E. Ruley, T. Jacks, and D. E. Housman: p53 dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell, 74:957-967 (1993).
78. Macchiarini, P., G. Fontanini, M. J. Hardin, F. Squartini, and C. A. Angeletti: Relation of neovascularisation to metastasis of non-small cell lung cancer. Lancet, 340:145-146 (1992).
79. 2+1 in induction of c-fos, c-jun and c-myc mRNA in rat PTE after oxidative stress. FASEB J., 6:919-924 (1992).
80. Margolis, B., S. G. Rhee, S. Felder, M. Mervic, R. Lyall, A. Levitzki, A. Ullrich, A. Zilberstein, and J. Schlesinger: EGF induces tyrosine phosphorylation of phospholipase C-II: A potential mechanism for EGF receptor signaling. Cell, 57:1101-1107 (1989).
81. Masanek, U., E. W. Pommerenke, J. Mattern, and M. Volm: Resistance proteins in human kidney, breast, ovarian and lung carcinoma. A comparative analysis. Oncol. Rep., 2:41-44 (1995).
82. Mattern, J. and M. Volm: Clinical relevance of predictive tests for cancer chemotherapy. Cancer Treat. Rev., 9:267-298 (1982).
83. Mattern, J. and M. Volm: Increased resistance to doxorubicin in human non-small cell lung carcinomas with metallothionein expression. Int. J. Oncol., 1:687-689 (1992).
84. Mattern, J., K. Wayss, and M. Volm: Effect of five antineoplastic agents on tumor xenografts with different growth rates. J. Natl. Cancer Inst., 72:1335-1339 (1984).
85. Mattern, J., M. Bak, E. W. Hahn, and M. Volm: Human tumor xenografts as model for drug testing. Cancer Met. Rev., 7:263-284 (1988).
86. McLeod, H. L., F. Douglas, M. Oates, R. P. Symond, D. Prakash, A. G. J. Van der Zee, S. B. Kaye, R. Brown, and W. N. Keith: Topoisomerase I and II activity in human breast, cervix, lung and colon cancer. Int. J. Cancer, 59:607-611 (1994).
87. Millward, M. J., B. M. J. Cantwell, N. C. Munro, A. Robinson, P. A. Corris, and A. L. Harris: Oral verapamil with chemotherapy for advanced non-small cell lung cancer: a randomised study. Br. J. Cancer, 67:1031-1035 (1993).
88. Milroy, R. on behalf of the West of Scotland Lung Cancer Research Group, and the Aberdeen Oncology Group: a randomized clinical study of verapamil in addition to combination chemotherapy in small cell lung cancer. Br. J. Cancer, 68:813-818 (1993).
89. Mittnacht, S. and R. A. Weinberg: G1/S phosphorylation of the retinoblastoma protein is associated with an altered affinity for the nuclear compartment. Cell, 65:381-393 (1991).
90. Morrow, C. S., K. H. Cowan, and M. E. Goldsmith: Structure of the human genomic glutathione S-transferase-π gene. Gene, 75:3-11 (1989).
91. Moseley, P. L., S. J. York, and X. Jork: Bleomycin induces the HSP-70 heat shock promoter in cultured cells. Am. J. Resp. Cell. Mol. Biol., 1:89-93 (1989).
92. Muggia, F. M.: Cell kinetic studies in patients with lung cancer. Oncology, 30:353-361 (1974).
93. Mulder, T. P. J., H. W. Verspaget, C. F. M. Sier, H. M. J. Roelof, S. Ganesn, G. Griffioen, and W. H. M. Peters: Glutathione S-transferase-π in colorectal tumors is predictive for overall survival. Cancer Res., 55:2696-2702 (1995).
94. Murphy, D., A. T. McGown, D. Growther, A. Mander, and B. W. Fox: Metallothionein levels in ovarian tumours before and after chemotherapy. Br. J. Cancer, 63:711-714 (1991).
95. Nakagawa, K., N. Saijo, S. Tsuchidas, M. Sakai, Y. Tsunokawa, J. Yokota, M. Muramatsu, K. Sato, M. Tereda, and K. D. Tew: Glutathione S-transferase-π as a determinant of drug resistance in transfectant cell lines. J. Biol Chem., 265:4296-4301 (1990).
96. Nevins, J.R.: E2F: a link between the Rb tumor suppressor protein and viral oncoprotein. Science, 258:424-429 (1992).
97. Nooter, K., F. T. Bosman, H. Burger, K. E. van Wingerden, M. J. Flens, R. J. Scheper, R. G. Oostrum, A. W. M. Boersma, A. van der Gaast, and G. Stoter: Expression of the multidrug resistance associated protein (MRP) gene in primary non-small cell lung cancer. Ann. Oncol., 7:75-81 (1996).
98. O'Brian, C. A., D. Fan, N. E. Ward, C. Seid, and I. J. Fidler: Level of protein kinase C correlated directly with resistance to adriamycin in murine fibrosarcoma cells. FEBS Lett., 246:78-82 (1989).
99. O'Dwyer, P. J., K. S. Yao, P. Ford, A. K. Godwin, and M. Clayton: Effects of hypoxia on detoxicating enzyme activity and expression in HT29 colon adenocarcinoma cells. Cancer Res., 54:3082-3987 (1994).
100. Oberli-Schrämmli, A. E., F. Joncourt, M. Stadler, H. J. Altermatt, K. Buser, H. B. Ris, U. Schmid, and T. Cerny : Parallel assessment of glutathione-based detoxifying enzymes, O6-alkylguanine-DNA alkyltransferase and P-glycoprotein as indicators of drug resistance in tumor and normal lung of patients with lung cancer. Int. J. Cancer; 59:629-636 (1994).
101. Oesterreich, S., C. N. Weng, M. Qui, S. G. Hilsenbeck, C. K. Osborne, and S. A. W. Fuqua: The small heat shock protein hsp 27 is correlated with growth and drug resistance in human breast cancer cell lines. Cancer Res., 53:4443-4448 (1993).
102. Oefner, D., H. Maier, B. Riedmann, T. Bammer, A. Rumer, G. Winde, W. Böcker, B. Jasan, and K. W. Schmid: Immunohistochemical metallothionein expression in colorectal adenocarcinoma: correlation with tumor stage and patient survival. Virch. Arch., 425:491-497 (1994).
103. Ohta, Y., Y. Watanabe, M. Oda, Y. Hayashi, Y. Endo, and T. Sasaki: Vascular endothelial growth factor-121mRNA expression and neomicrovessel density in primary lung cancer. Oncol. Rep., 3:713-717 (1996).
104. Paterlini, P., J. F. Flejou, M. S. De Mitri, E. Pisi, D. Franco, and C. Brechet: Structure and expression of the cyclin A gene in human primary liver cancer. Correlation with low cytometric parameters. J. Hepatol., 13:47-52 (1995).
105. Pearson, J. W., W. E. Fogler, K. Volker, N. Usui, S. K. Goldenberg, E. Grays, C. W. Riggs, K. Komschlies, R. H. Wiltrout, T. Tsuruo, I. Pastan, M. M. Gottesman, and D. L. Longo: Reversal of drug resistance in a human colon cancer xenograft expressing MDR1 complementary DNA by in vivo administration of MRK-16 monoclonal antibody. J. Natl. Cancer Inst, 83:1386-1391 (1991).
106. Pegg, A. E.: Mammalian O6-alkylguanine-DNA alkyltransferase: Regulation and importance in response to alkylating carcinogenic and therapeutic agents. Cancer Res., 50:6119-6129 (1990).
107. Pestalozzi, B. C., C. J. McGinn, T. J. Kinsella, J. C. Drake, M. C. Glennon, C. J. Allegra, and P. G. Johnston: Increased thymidylate synthase protein levels are principally associated with proliferation but not cell cycle phase in asynchronous human cancer cells. Br. J. Cancer, 71:1151-1157 (1995).
108. Posada, J. A., E. M. Me Keegan, K. F. Worthington, M. J. Morin, S. Jahen, and T. R. Tritton: Human multidrug resistance KB cells overexpress protein kinase C: involvement in drug resistance. Cancer Commun., 1:285-292 (1989).
109. Radosevich, J. A., P. G. Robinson, L. S. Rittmann-Grauer, B. Wilson, J. P. Leung, M. L. Maminta, W. Warren, S. Rosen, and V. E. Gould: Immunohistochemical analysis of pulmonary and pleural tumors with the monoclonal antibody HYB-612 directed against the multidrug resistance (MDR-1) gene product, P-glycoprotein. Tumor Biol., 10:252-257 (1989).
110. Reed, J. C.: Bel 2: Prevention of apoptosis as a mechanism of drug resistance. Hematol. Oncol. Clin. North Am., 9:451-473 (1995).
111. Reed, J. C., S. Kitada, S. Takayama, and T. Miyashita: Regulation of chemoresistance by the bcl-2 oncoprotein in non-Hodgkin's lymphoma and lymphocytic leukemia cell lines. Ann. Oncol., 5:61-65 (1994).
112. Reissmann, P. T., H. Koga, R. Takahashi, R. A. Figlin, E. C. Holmes, S. Piantadosi, C. Cordon-Cardo, and D. J. Slamon: Inactivation of the retinoblastoma susceptibility gene in non-small cell lung cancer. Oncogene, 8:1913-1919 (1993).
113. Rice, G. C., C. Hoy, and R. T. Schimke: Transient hypoxia enhances the frequency of dihydrofolate reductase gene amplification in Chinese hamster ovary cells. Proc. Natl. Acad. Sci. (Wash.), 83:5978-5982 (1986).
114. Richardson, G. E. and B. E. Johnson: The biology of lung cancer. Semin. Oncol., 20:105-127 (1993).
115. Ritke, M. K., J. M. Rusnak, J. S. Lazo, W. P. Allan, C. Dive, S. Heer, and J. C. Yalowich: Differential induction of etoposide-mediated apoptosis in human leukemia HL-60 and K562 cells. Mol Pharmacol., 46:605-611 (1994).
116. Rivoltini, L., M. P. Colombo, R. Supino, D. Ballinari, T. Tsuruo, and G. Parmiam: Modulation of multidrug resistance by verapamil or mdrl antisense oligodeoxy-nucleotide does not change the high susceptibility to lymphokine-activated killers in mdr-resistant human carcinoma (LoVo) line. Int. J. Cancer, 46:727-732 (1990).
117. Ruckdeschel, J. C., D. N. Carney, H. K. Oie, E. K. Russel, and A. F. Gazdar: In vitro chemosensitivity of human lung cancer cell lines. Cancer Treat. Rep., 71:697-704 (1987).
118. Safran, H., T. King, H. Choy, A. Collerkeri, H. Kwakwa, F. Lopez, B. Cole, J. Myers, J. Tarpey, and A. Rosmarin: p53 mutations do not predict response to Paclitaxel/ Radiation for non-small cell lung carcinoma. Cancer, 78:1203-1210 (1996).
119. Sahyoun, N., M. Wolf, J. Besterman, T. S. Hsiele, M. Sander, H. Le Vine IH, K. J. Chang, and E. Cuatrecasas: Protein kinase C phosphorylates topoisomerase II. Topoisomerase activation and its possible role in phorbol ester-induced differentiation of HL-60 cells. Proc. Natl. Acad. Sci. U.S.A., 83:1603-1607 (1986).
120. Sassone-Corsi, P., H. W. Lamph, M. Kamps, and I. M. Verma: Fos-associated cellular p39 is related to nuclear transcription factor AP-1. Cell, 54:553-563 (1988).
121. Scanlon, K. J. and M. Kashani-Sabet: Elevated expression of thymidylate synthase cycle genes in cisplatin-resistant human ovarian carcinoma A 2780 cells. Proc. Natl. Acad. Sci. U.S.A., 85:650-653 (1988).
122. Scanlon, K. J., M. Kashani-Sabet, H. Miyachi, L. C. Sowers, and J. Rossi: Molecular basis of cisplatin resistance in human carcinomas: model systems and patients. Anticancer Res., 9:1301-1312 (1989).
123. Scanlon, K. J., L. Jiao, W. Wang, T. Tone, J. J. Rossi, and M. Kashani-Sabet: Ribozyme-mediated cleavage of c-fos mRNA reduces gene expression of DNA synthesis enzymes andmetallothionein. Proc. Natl. Acad. Sci. U.S.A., 88:10591-10595 (1991).
124. Schardt, C., S. Kasimir-Bauer, A. Harstrick, J. M. Huesker, R. Nettersheim, W. Stellberg, M. R. Nowrousian, B. Opalka, M. E. Scheulen, and S. Suber: Differential mRNA expression of heat shock proteins hsp 27, hsp 60 and hsp 70 in cisplatin and doxorubicin resistant cell lines and regulation by topoisomerase II inhibitors. Proc. Am. Assoc. Cancer Res., 36:20 (1995).
125. Scheper, R. J., H. J. Broxterman, G. L. Scheffer, P. Kaaijk, W. S. Dalton, T. H. M. Van Heijningen, C. K. Van Kalken, M. L. Slovak, E. G. E. De Vries, P. Van der Kalk, C. J. L. M. Meijer, and H. M. Pinedo: Overexpression of a Mr 110,000 vesicular protein in non-P-glycoprotein-mediated multidrug resistance. Cancer Res., 53:1475-1479 (1993).
126. Schimke, R. T.: Gene amplification in cultured cells. Cell, 37:705-713 (1984).
127. Sharma, R., S. S. Singhal, S. K. Srivastava, K. K. Bajpai, E. P. Frenkel, and S. Awasthi: Glutathione and glutathionelinked enzymes in human small cell lung cancer cell lines. Cancer Lett., 75:111-119 (1993).
128. Sherr, C. J.: Mammalian GI cyclins. Cell, 73:1059-1065 (1993).
129. Shimizu, E., A. Coxon, G. A. Otterson, S. M. Steinberg, R. A. Kratzke, Y. W. Kim, J. Fedorko, H. Oie, B. E. Johnson, J. L. Mulshine, J. D. Minna, A. F. Gazdar, and F. J. Kaye: RB protein status and clinical correlation from 171 cell lines representing lung cancer, extrapulmonary small cell carcinoma, and mesothelioma. Oncogene, 9:2441-2448 (1994).
130. Shin, H. J. C., J. S. Lee, W. K. Hong, and D. M. Shin: Study of multidrug resistance (mdr1) gene in non-small cell lung cancer. Anticancer Res., 12:367-370 (1992).
131. Smith, M. J. and E. V. Prochownik: Inhibition of c-jun causes reversible proliferation arrest and withdrawal from the cell cycle. Blood, 79:2107-2115 (1992).
132. Stammler, G. and M. Volm: Apoptosis in non-small cell lung cancer as related to drug resistance and prognosis. Apoptosis, 1:95-99 (1996).
133. Stammler, G., A. Sauerbrey, and M. Volm: Messenger RNA expression of resistance factors-and their correlation to the proliferative activity in childhood acute lymphoblastic leukemia. Cancer Lett., 89:129-135 (1995).
134. ++-phospholipid-dependent protein kinase (protein kinase C). Biochim. Biophys. Res. Commun., 162:903-907 (1989).
135. Teeter, L. D., T. Eckersberg, Y. Tsai, and M. T. Kuo: Analysis of the Chinese hamster P-glycoprotein/multidrug resistance gene pgp1 reveals that the AP-1 site is essential for full promoter activity. Cell Growth Differ., 2:429-437 (1991).
136. Teicher, B. A.: Hypoxia and drug resistance. Cancer Metast. Rev., 13:139-168 (1994).
137. Tritton, T. R. : Cell surface actions of adriamycin. Pharmacol. Ther., 49:293-309 (1991).
138. Tsai, C. M., K. T. Chang, L. H. Wu, J. Y. Chen, A. F. Gazdar, T. Mitsudomi, M. H. Chen, and R. P. Perng: Correlation between intrinsic chemoresistance and HER-2/neu gene expression, p53 gene mutations, and cell proliferation characteristics in non-small cell lung cancer cell lines. Cancer Res., 56:206-209 (1996).
139. Tsuruo, T., H. Hamada, S. Sato, and Y. Heike: Inhibition of multidrug-resistant human tumor growth in athymic mice by anti-P-glycoprotein monoclonal antibodies. Jpn. J. Cancer Res., 80:627-631 (1989).
140. Twentyman, P. R., N. E. Fox, K. A. Wright, and N. M. Bleehen: Derivation and preliminary characterisation of adriamycin resistant lines of human lung cancer cells. Br. J. Cancer, 53:529-537 (1986).
141. Valeriote, F. and L. Van Putten: Proliferation-dependent cytotoxicity of anticancer agents: areview. Cancer Res., 3:2619-2630 (1975).
142. Volm, M.: P-glycoprotein associated expression of c-fos and c-jun products in human lung carcinomas. Anticancer Res., 13:375-378 (1993).
143. Volm, M., and J. Mattern: Elevated expression of thymidylate synthase in doxorubicin-resistant non-small cell lung carciomas. Anticancer Res., 12:2293-2296 (1992a).
144. Volm, M. and J. Mattern: Expression of topoisomerase II, catalase, metallothionein and thymidylate synthase in human squamous cell lung carcinomas and their correlation with doxorubicin resistance and with patients' smoking habits. Carcinogenesis, 13:1947-1950 (1992b).
145. Volm, M. and J. Mattern: Detection of multiple mechanisms in untreated human lung cancer. Onkologie, 16:189-194 (1993).
146. Volm, M. and J. Mattern: Increased expression of Bcl-2 in drug-resistant squamous cell lung carcinomas. Int. J. Oncol., 7:1333-1338 (1995).
147. Volm, M. and E. W. Pommerenke: Associated expression of protein kinase C with resistance to doxorubicin in human lung cancer. Anticancer Res., 15:463-466 (1995).
148. Volm, M., K. Wayss, M. Kaufmann, and J. Mattern: Pretherapeutic detection of tumor resistance and the results of tumour chemotherapy. Eur. J. Cancer, 15:983-993 (1979).
149. Volm, M., J. Mattern, J. Spnka, M. Vogt-Schaden, and K. Wayss: DNA distribution in non-small cell lung carcinomas and its relationship to clinical behavior. Cytometry, 6:348-356 (1985 a).
150. Volm, M., P. Drings, J. Mattem, J. Sonka, I. Vogt-Moykopf, and K. Wayss: Prognostic significance of DNA patterns and resistance-predictive tests in non-small cell lung carcinoma. Cancer, 56:1396-1403 (1985b).
151. Volm, M., P. Drings, E. W. Hahn, and J. Mattern: Prediction of the clinical chemotherapeutic response of stage III lung adenocarcinoma patients by an in vitro short term test. Br. J. Cancer, 57:198-200 (1988a).
152. Volm, M., E. W. Hahn, J. Mattern, T. Müller, I. Vogt-Moykopf, and E. Weber: Five-year follow-up study of independent clinical and flow cytometric prognostic factors for the survival of patients with nonsmall cell lung carcinomas. Cancer Res., 48:2923-2928 (1988b).
153. Volm, M., J. Mattern, and B. Samsel: Overexpression of P-glycoprotein and glutathione S-transferase-π in resistant non-small cell lung carcinomas of smokers. Br. J. Cancer, 64:700-704 (1991a).
154. Volm, M., E. W. Pommerenke, T. Efferth, H. Löhrke, and J. Mattern: Circumvention of multi-drug resistance in human kidney and kidney carcinoma in vitro. Cancer, 67:2484-2489 (1991b).
155. Volm, M., J. Mattern, and B. Samsel: Relationship of inherent resistance to doxorubicin, proliferative activity and expression of P-glycoprotein 170, and glutathione S-transferase-π in human lung tumors. Cancer, 70:764-769, (1992a).
156. Volm, M., J. Mattern, T. Efferth, and E. W. Pommerenke: Expression of several resistance mechanisms in untreated human kidney and lung carcinomas. Anticancer Res., 12:1063-1068 (1992b).
157. Volm, M., M. Kästel, J. Mattern, and T. Efferth: Expression of resistance factors (P-glycoprotein, glutathione 5-transferase-π, and topoisomerase II) and their interrelationship to protooncogene products in renal cell carcinoma. Cancer, 71:3981-3987 (1993).
158. Volm, M., R. Koomägi, and J. Mattern: Prognostic significance of proliferating cell nuclear antigen (PCNA) in adenocarcinoma of the lung. Int. J. Oncol, 6:359-362 (1995a).
159. 0-associated cell cycle protein, in childhood acute lymphoblastic leukemia. Int. J. Cancer (Pred. Oncol.), 64:166-170 (1995b).
160. Volm, M., R. Koomägi, J. Mattern, and G. Stammler: Heat shock (hsp 70) and resistance proteins in nonsmall cell lung carcinomas. Cancer Letters, 95:195-200 (1995c).
161. Volm, M., J. Mattem, and G. Stammler: Up-regulation of heat shock protein 70 in adenocarcinomas of the lung in smokers. Anticancer Res., 15:2607-2610 (1995d).
162. Volm, M., R. Koomägi, and J. Mattern: Interrelationship between microvessel density, expression of VEGF and resistance to doxorubicin in non-small cell lung carcinoma. Anticancer Res., 16:213-218 (1996).
163. Volm, M., R. Koomägi, and J. Mattern: Prognostic value of vascular endothelial growth factor and its receptor flt-1 in squamous cell lung cancer. Int. J. Cancer (Pred. Oncol.), 74:64-68 (1997a).
164. Volm, M., R. Koomägi, J. Mattern, and G. Stammler: Angiogenic growth factors and their receptors in non-small cell lung carcinomas and their relationships to drug response in vitro. Anticancer Res. 17:99-104 (1997b).
165. Volm, M., R. Koomägi, J. Mattern, and G. Stammler: Cyclin A is associated with an unfavourable outcome in patients with non-small cell lung carcinomas. Br. J. Cancer (in press 1997c).
166. Wang, Y., B. A. Teicher, T. C: Shea, S. A. Holden, K. W. Rosbe, A. Al-Achi, and W. D. Hennen Cross-resistance and glutathione S-transferase-π levels among four human melanoma cell lines selected for alkylating agent resistance. Cancer Res., 49:6185-6192 (1989).
167. Washtien, W. L.: Thymidylate synthase levels as a factor in 5-fluorodeoxyuridine and methotrexate cytotoxicity in gastrointestinal tumor cells. Mol. Pharmacol., 21:723-728 (1982).
168. Weidner, N., J. P. Semple, W. R. Welch, and J. Folkman: Tumor angiogenesis and metastasis-correlation in invasive breast carcinomas. N. Engl. J. Med., 324:1-8 (1991).
169. Weisenthal, L. M., J. A. Marsden, P. L. Dill, and C. K. Macaluso: A novel dye exclusion method for testing in vitro chemosensitivity of human tumors. Cancer Res., 43:749-757 (1983).
170. Whelan, R. D. H., L. K. Hosking, A. J. Townsend, K. H. Cowan, and B. T. Hill: Differential increases in glutathione S-transferase activities in a range of multidrug-resistant human tumor cell lines. Cancer Commun., 1:359-365 (1989).
171. Xia, C. L., I. G. Cowell, K. H. Dixon, S. E. Pemble, B. Ketterer, and J. B. Taylor: Glutathione S-transferase-π. Its minimal promoter and downstream cis-acting element. Biochim. Biophys. Res. Commun., 176:233-240 (1991).
172. Xu, H. J., S. X. Hu, P. T. Cagle, G. E. Moore, and W. F. Benedict: Absence of retinoblastoma protein expression in primary non-small cell lung carcinomas. Cancer Res., 51:2735-2739 (1991).
173. Yamazaki, K., S. Abe, H. Takekawa, N. Sukoh, N. Watanabe, S. Ogura, I. Nakajima, H. Isoba, K. Inoue, and Y. Kawakamy: Tumor angiogenesis in human lung carcinoma. Cancer, 74:2245-2250 (1994).
174. Yu, G., S. Ahmad, A. Aquino, C. R. Fairchild, J. B. Trepel, S. Ohno, K. Suzuki, T. Tsuruo, K. H. Cowan, and R. I. Glazer: Transfection with protein kinase C confers multidrug resistance to MCF-7 cells expressing P-glycoprotein. Cancer Commun., 3:181-189 (1991).
175. Yuan, A., P. C. Yang, C. J. Yu, C. Lee, Y. T. Yao, C. Chen, L. N. Lee, S. A. Kuo, and K. T. Luh: Tumor angiogenesis correlates with histologic type and metastasis in nonsmall cell lung cancer. Am. J. Respir. Crit. Care Med., 152: 2157-2162 (1995).
176. Zijlstra, J. G., S. De Jongs, E. G. E. De Vries, and N. H. Mulder: Topoisomerases, new targets in cancer chemotherapy. Med. Oncol. Tumor Pharmacother., 7: 11-18 (1990).