Role of glutathione S-transferases in the resistance of human colon cancer cell lines to doxorubicin

Cancer Research

Volumn 58, Issue 5, 1998, Pages 947-955

  Beaumont, Peter O ^a   Moore, Malcolm J ^a,b   Ahmad, Kamran ^a   Payne, Michelle M ^a   Lee, Chunja ^a   Riddick, David S ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; ETACRYNIC ACID; GLUTATHIONE DERIVATIVE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; GLYCOPROTEIN P;

ARTICLE; CATALYSIS; COLON CANCER; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG RESISTANCE; HUMAN; HUMAN CELL; PRIORITY JOURNAL;

ANTIBIOTICS, ANTINEOPLASTIC; CACO-2 CELLS; DOXORUBICIN; DRUG RESISTANCE, MICROBIAL; DRUG RESISTANCE, NEOPLASM; GLUTATHIONE TRANSFERASE; HUMANS;

EID: 0032031001     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (76)

1. Booser, D. J., and Hortobagyi, G. N. Anthracycline antibiotics in cancer therapy: focus on drug resistance. Drugs, 47: 223-258, 1994.
2. Nielsen, D., Maare, C., and Skovsgaard, T. Cellular resistance to anthracyclines. Gen. Pharmacol., 27: 251-255, 1996.
3. Bellamy, W. T. P-glycoproteins and multidrug resistance. Annu. Rev. Pharmacol. Toxicol., 36: 161-183, 1996.
4. Lautier, D., Canitrot, Y., Deeley, R. G., and Cole, S. P. C. Multidrug resistance mediated by the multidrug resistance protein (MRP) gene. Biochem. Pharmacol., 52: 967-977, 1996.
5. Tew, K. D. Glutathione-associated enzymes in anticancer drug resistance. Cancer Res., 54: 4313-4320, 1994.
6. Hayes, J. D., and Pulford, D. J. The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit. Rev. Biochem. Mol. Biol., 30: 445-600, 1995.
7. Chen, A. Y., and Liu, L. F. DNA topoisomerases: essential enzymes and lethal targets. Annu. Rev. Pharmacol. Toxicol., 34: 191-218, 1994.
8. Chancy, S. G., and Sancar, A. DNA repair: enzymatic mechanisms and relevance to drug response. J. Natl. Cancer Inst., 88: 1346-1360, 1996.
9. Ranganathan, S., and Tew, K. D. Immunohistochemical localization of glutathione S-transferases α, μ and π in normal tissue and carcinomas from human colon. Carcinogenesis (Lond.), 12: 2383-2387, 1991.
10. Moorghen, M., Cairns, J., Forrester, L. M., Hayes, J. D., Hall, A., Cattan, A. R., Wolf, C. R., and Harris, A. L. Enhanced expression of glutathione S-transferases in colorectal carcinoma compared to non-neoplastic mucosa. Carcinogenesis (Lond.), 12: 13-17, 1991.
11. Peters, W. H. M., Boon, C. E. W., Roelofs, H. M. J., Wobbes, T., Nagengast, F. M., and Kremers, P. G. Expression of drug-metabolizing enzymes and P-170 glycoprotein in colorectal carcinoma and normal mucosa. Gastroenterology, 103: 448-455, 1992.
12. Chao, C. C-K., Huang, Y-T., Ma, C. M., Chou, W-Y., and Lin-Chao, S. Overexpression of glutathione S-transferase and elevation of thiol pools in a multidrug-resistant human colon cancer cell line. Mol. Pharmacol., 41: 69-75, 1992.
13. Lai, G-M., Moscow, J. A., Alvarez, M. G., Fojo, A. T., and Bates, S. E. Contribution of glutathione and glutathione-dependent enzymes in the reversal of adriamycin resistance in colon carcinoma cell lines. Int. J. Cancer, 49: 688-695, 1991.
14. Peters, W. H. M., and Roelofs, H. M. J. Biochemical characterization of resistance to mitoxantrone and adriamycin in Caco-2 human colon adenocarcinoma cells: a possible role for glutathione S-transferases. Cancer Res., 52: 1886-1890, 1992.
15. Tew, K. D., Monks, A., Barone, L., Rosser, D., Akerman, G., Montali, J. A., Wheatley, J. B., and Schmidt, D. E., Jr. Glutathione-associated enzymes in the human cell lines of the National Cancer Institute drug screening program. Mol. Pharmacol., 50: 149-159, 1996.
16. Nakagawa, K., Saijo, N., Tsuchida, S., Sakai, M., Tsunokawa, Y., Yokota, J., Muramatsu, M., Sato, K., Terada, M., and Tew, K. D. Glutathione S-transferase π as a determinant of drug resistance in transfectant cell lines. J. Biol. Chem., 265: 4296-4301, 1990.
17. He, N. G., Singhal, S. S., Srivastava, S. K., Zimniak, P., Awasthi, Y. C., and Awasthi, S. Transfection of a 4-hydroxynonenal metabolizing glutathione S-transferase isozyme, mouse GSTA4-4, confers doxorubicin resistance to Chinese hamster ovary cells. Arch. Biochem. Biophys., 333: 214-220, 1996.
18. Moscow, J. A., Townsend, A. J., and Cowan, K. H. Elevation of π class glutathione S-transferase activity in human breast cancer cells by transfection of the GST π gene and its effect on sensitivity to toxins. Mol. Pharmacol., 36: 22-28, 1989.
19. Kisara, S., Furusawa, S., Murata, R., Ogata, M., Hikichi, N., Takayanagi, Y., and Sasaki, K. I. Combined effects of buthionine sulfoximine and cepharamhine on cytotoxic activity of doxorubicin to multidrug-resistant cells. Oncol. Res., 7: 191-200, 1995.
20. Kisara, S., Furusawa, S., Takayanagi, Y., and Sasaki, K. Effect of glutathione depletion by buthionine sulfoximine on doxorubicin toxicity in mice. Res. Commun. Mol. Pathol. Pharmacol., 89: 401-410, 1995.
21. Ban, N., Takahashi, Y., Takayama, T., Kura, T., Katahira, T., Sakamaki, S., and Niitsu, Y. Transfection of glutathione S-transferase (GST)-π antisense complementary DNA increases the sensitivity of a colon cancer cell line to adriamycin, cisplatin, melphalan, and eloposide. Cancer Res., 56: 3577-3582, 1996.
22. Nagoumey, R. A., Messenger, J. C., Kem D. H., and Weisenthal, L. M. Enhancement of anthracycline and alkylator cytotoxicity by ethacrynic acid in primary cultures of human tissues. Cancer Chemother. Pharmacol., 26: 318-322, 1990.
23. Tew, K. D., Bomber, A. M., and Hoffman, S. J. Ethacrynic acid and piriprost as enhancers of cytotoxicity in drug resistant and sensitive cell lines. Cancer Res., 48: 3622-3625, 1988.
24. Xu, B. H., and Singh, S. V. Effect of buthionine sulfoximine and ethacrynic acid on cytotoxic activity of mitomycin C analogues BMY 25282 and BMY 25067. Cancer Res., 52: 6666-6670, 1992.
25. Ciaccio, P. J., Shen, H. X., Jaiswal, A. K., Lyttle, M. H., and Tew, K. D. Modulation of detoxification gene expression in human colon HT29 cells by glutathione S-transferase inhibitors. Mol. Pharmacol., 48: 639-647, 1995.
26. O'Dwyer, P. J., LaCreta, F. P., Nash, S., Tinsley, P. W., Schilder, R., Clapper, M. L., Tew, K. D., Panting, L., Litwin, S., Comis, R. L., and Ozols, R. F. Phase I study of thiotepa in combination with the glutathione S transferase inhibitor ethacrynic acid. Cancer Res., 51: 6059-6065, 1991.
27. Ouwerkerk-Mahadevan, S., van Boom, J. H., Dreef-Tromp, M. C., Ploemen, J. H. T. M., Meyer, D. J., and Mulder, G. J. Glutathione analogues as novel inhibitors of rat and human glutathione S-transferase isoenzymes, as well as of glutathione conjugation in isolated rat hepatocytes and in the rat in vivo. Biochem. J., 308: 283-290, 1995.
28. Flatgaard, J. E., Bauer, K. E., and Kauvar, L. M. Isozyme specificity of novel glutathione S-transferase inhibitors. Cancer Chemother. Pharmacol., 33: 63-70, 1993.
29. Lyttle, M. H., Hocker, M. D., Hui, H. C., Caldwell, C. G., Aaron, D. T., Engqvist-Goldstein, A., Flatgaard, J. E., and Bauer, K. E. Isozyme-specific glutathione S-transferase inhibitors: design and synthesis. J. Med. Chem., 37: 189-194, 1994.
30. Morgan, A. S., Ciaccio, P. J., Tew, K. D., and Kauvar, L. N. Isozyme-specific glutathione S-transferase inhibitors potentiate drug sensitivity in cultured human tumor cell lines. Cancer Chemother. Pharmacol., 37: 363-370, 1996.
31. Gibbs, J. P., Czerwinski, M., and Slattery, J. T. Busulfan-glutathione conjugation catalyzed by human liver cytosolic glutathione S-transferases. Cancer Res., 56: 3678-3681, 1996.
32. Hall, A. G., Matheson, E., Hickson, I. D., Foster, S. A., and Hogarth, L. Purification of an α class glutathione S-transferase from melphalan-resistant Chinese hamster ovary cells and demonstration of its ability to catalyze melphalan-glutathione adduct formation. Cancer Res., 54: 3369-3372, 1994.
33. Doroshow, J. H., Akman, S., Chu, F-F., and Esworthy, S. Role of the glutathione-glutathione peroxidase cycle in the cytotoxicity of the anticancer quinones. Pharmacol. & Ther., 47: 359-370, 1990.
34. Singhal, S. S., Saxena, M., Ahmad, H., Awasthi, S., Haque, A. K., and Awasthi, Y. C. Glutathione S-transferases of human lung: characterization and evaluation of the protective role of the α-class isozymes against lipid peroxidation. Arch. Biochem. Biophys., 299: 232-241, 1992.
35. Alin, P., Danielson, U. H., and Mannervik, B. 4-Hydroxyalk-2-enals are substrates for glutathione S-transferases. FEBS Lett., 179: 267-270, 1985.
36. Grant, C. E., Valdimarsson, G., Hipfner, D. R., Almquist, K. C., Cole, S. P. C., and Deeley, R. G. Overexpression of multidrug resistance-associated protein (MRP) increases resistance to natural product drugs. Cancer Res., 54: 357-361, 1994.
37. Zaman, G. J. R., Flens, M. J., Vanleusden, M. R., Dehaas, M., Mulder, H. S., Lankelma, J., Pinedo, H. M., Scheper, R. J., Baas, F., Broxterman, H. J., and Borst, P. The human multidrug resistance-associated protein MRP is a plasma membrane drug-efflux pump. Proc. Natl. Acad. Sci. USA, 91: 8822-8826, 1994.
38. Jedlitschky, G., Leier, I., Buchholz, U., Bamouin, K., Kurz, G., and Keppler, D. Transport of glutathione, glucuronate, and sulfate conjugates by the MRP gene-encoded conjugate export pump. Cancer Res., 56: 988-994, 1996.
39. Paul, S., Breuninger, L. M., Tew, K. D., Shen, H. X., and Kruh, G. D. ATP-dependent uptake of natural product cytotoxic drugs by membrane vesicles establishes MRP as a broad specificity transporter. Proc. Natl. Acad. Sci. USA, 93: 6929-6934, 1996.
40. 4, and structurally related conjugates. J. Biol. Chem., 269: 27807-27810, 1994.
41. 4 and chemotherapeutic agents in membrane vesicles: demonstration of glutathione-dependent vincristine transport. J. Biol. Chem., 271: 9675-9682, 1996.
42. Alley, M. C., Scudiero, D. A., Monks, A., Hursey, M. L., Czerwinski, M. J., Fine, D. L., Abbott, B. J., Mayo, J. G., Shoemaker, R. H., and Boyd, M. R. Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay. Cancer Res., 48: 589-601, 1988.
43. Harper, P. A., Prokipcak, R. D., Bush, L. E., Golas, C. L., and Okey, A. B. Detection and characterization of the Ah-receptor for 2,3,7,8-tetrachlorodibenzo-p-dioxin in the human colon adenocarcinoma cell line LS180. Arch. Biochem. Biophys., 290: 27-36, 1991.
44. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72: 248-254, 1976.
45. Habig, W. H., Pabst, M. J., and Jakoby, W. B. Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. J. Biol. Chem., 249: 7130-7139, 1974.
46. Lawrence, R. A., and Burk, R. F. Glutathione peroxidase activity in selenium-deficient rat liver. Biochem. Biophys. Res. Commun., 71: 952-958, 1976.
47. Comstock, K. E., Widersten, M., Hao, X. Y., Henner, W. D., and Mannervik, B. A comparison of the enzymatic and physicochemical properties of human glutathione transferase M4-4 and three other human μ class enzymes. Arch. Biochem. Biophys., 311: 487-495, 1994.
48. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.), 227: 680-685, 1970.
49. Towbin, H., Staehelin, T., and Gordon, J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA, 76: 4350-4354, 1979.
50. Chomczynski, P., and Sacchi, N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162: 156-159, 1987.
51. Sambrook, J., Fritsch, E. F., and Maniatis, T. Molecular Cloning: A Laboratory Manual, Ed. 2. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1989.
52. a subunit cDNA. Biochem. Biophys. Res Commun., 141: 229-237, 1986.
53. Rhoads, D. M., Zarlengo, R. P., and Tu, C-P. D. The basic glutathione S-transferases from human livers are products of separate genes. Biochem. Biophys. Res. Commun., 145: 474-481, 1987.
54. Waxman, D. J., Sundseth, S. S., Srivastava, P. K., and Lapenson, D. P. Gene-specific oligonucleotide probes for α, μ, and π, and microsomal rat glutathione S-transferases: analysis of liver transferase expression and its modulation by hepatic enzyme inducers and platinum anticancer drugs. Cancer Res., 52: 5797-5802, 1992.
55. b subunit cDNA. Nucleic Acids Res., 16: 8541-8554, 1988.
56. Vorachek, W. R., Pearson, W. R., and Rule, G. S. Cloning, expression, and characterization of a class-μ. glutathione transferase from human muscle, the product of the GST4 locus. Proc. Natl. Acad. Sci. USA, 88: 4443-4447, 1991.
57. Campbell, E., Takahashi, Y., Abramovitz, M., Peretz, M., and Listowsky, I. A distinct human testis and brain μ.-class glutathione S-transferase: molecular cloning and characterization of a form present in individuals lacking hepatic type μ isoenzymes. J. Biol. Chem., 265: 9188-9193, 1990.
58. Board, P. G., Webb, G. C., and Coggan, M. Isolation of a cDNA clone and localization of the human glutathione S-transferase 3 genes to chromosome bands 11q13 and 12q13-14. Ann. Hum. Genet., 53: 205-213, 1989.
59. Waxman, D. J. Rat hepatic P450IIA and P450IIC subfamily expression using catalytic, immunochemical, and molecular probes. Methods Enzymol., 206: 249-267, 1991.
60. Ginzburg, I., Behar, L., Givol, D., and Littauer, U. Z. The nucleotide sequence of rat α-tubulin: 3′-end characteristics, and evolutionary conservation. Nucleic Acids Res., 9: 2691-2697, 1981.
61. Mannervik, B., Alin, P., Guthenberg, C., Jensson, H., Tahir, M. K., Warholm, M., and Jornvall, H. Identification of three classes of cytosolic glutathione transferase common to several mammalian species: correlation between structural data and enzymatic properties. Proc. Natl. Acad. Sci. USA, 82: 7202-7206, 1985.
62. Flens, M. J., Zaman, G. J. R., Vandervalk, P., Izquierdo, M. A., Schroeijers, A. B., Scheffer, G. L., Vandergroep, P., Dehaas, M., Meijer, C. J. L. M., and Scheper, R. J. Tissue distribution of the multidrug resistance protein. Am. J. Pathol., 148: 1237-1247, 1996.
63. Kruh, G. D., Gaughan, K. T., Godwin, A., and Chan, A. Expression pattern of MRP in human tissues and adult solid tumor cell lines. J. Natl. Cancer Inst., 87: 1256-1258, 1995.
64. Kuo, M. T., Bao, J-J., Curley, S. A., Ikeguchi, M., Johnston, D. A., and Ishikawa, T. Frequent coordinated overexpression of the MRP/GS-X pump and γ-glutamylcysteine synthetase genes in human colorectal cancers. Cancer Res., 56: 3642-3644, 1996.
65. Chuman, Y., Sumizawa, T., Takebayashi, Y., Niwa, K., Yamada, K., Haraguchi, M., Furukawa, T., Akiyama, S., and Aikou, T. Expression of the multidrug-resistance-associated protein (MRP) gene in human colorectal, gastric and non-small-cell lung carcinomas. Int. J. Cancer, 66: 274-279, 1996.
66. Filipits, M., Suchomel, R. W., Dekan, G., Stiglbauer, W., Haider, K., Depisch. D., and Pirker, R. Expression of the multidrug resistance-associated protein (MRP) gene in colorectal carcinomas. Br. J. Cancer. 75: 208-212, 1997.
67. Tomonaga, M., Oka, M., Narasaki, F., Fukuda, M., Nakano, R., Takatani, H., Ikeda, K., Terashi, K., Matsuo, I., Soda, H., Cowan, K. H., and Kohno, S. The multidrug resistance-associated protein gene confers drug resistance in human gastric and colon cancers. Jpn. J. Cancer Res., 87: 1263-1270, 1996.
68. DeAngelis, P., Stokke, T., Smedshammer, L., Lothe, R. A., Lehne, G., Chen, Y., and Clausen, O. P. F. P-glycoprotein is not expressed in a majority of colorectal carcinomas and is not regulated by mutant p53 in vivo. Br. J. Cancer, 72: 307-311, 1995.
69. Ikeguchi, M., Shirai, H., Kaibara, N., and lto, H. Expression of P-glycoprotein in the normal colorectal epithelium and in colorectal carcinoma. Int. J. Oncol., 7: 319-324, 1995.
70. Linn, S. C., and Giaccone, G. MDR1/P-glycoprotein expression in colorectal cancer. Eur. J. Cancer, 31A: 1291-1294, 1995.
71. Kramer, R., Weber, T. K., Morse, B., Arceci, R., Staniunas, R., Steele Jr. G., and Summerhayes, I. C. Constitutive expression of multidrug resistance in human colorectal tumors, and cell lines. Br. J. Cancer, 67, 959-968, 1993.
72. Alvarez, M., Paull, K., Monks, A., Hose, C., Lee, J. S., Weinstein, J., Grever, M., Bates, S., and Fojo, T. Generation of a drug resistance profile by quantitation of mdr-1/P-glycoprotein in the cell lines of the National Cancer Institute anticancer drug screen. J. Clin. Invest., 95: 2205-2214, 1995.
73. Hosoya, K., Kim, K. J., and Lee, V. H. L. Age-dependent expression of P-glycoprotein gp170 in Caco-2 cell monolayers. Pharm. Res. (NY), 13: 885-890, 1996.
74. Tew, K. D., Houghton, P. J., and Houghton, J. A. Preclinical and Clinical Modulation of Anticancer Drugs. Boca Raton, FL: CRC Press, 1993.
75. Mulders, T. M. T., Keizer, H. J., Breimer, D. D., and Mulder, G. J. In vivo characterization and modulation of the glutathione/glutathione S-transferase system in cancer patients. Drug Metab. Rev., 27: 191-229, 1995.
76. Berridge, M. V., and Tan, A. S. Characterization of the cellular reduction of MTT: subcellular localisation, substrate dependence and involvement of mitochondrial electron transport in MTT reduction. Arch. Biochem. Biophys., 303: 474-482, 1993.