Characterization of new potential anticancer drugs designed to overcome glutathione transferase mediated resistance

Molecular Pharmaceutics

Volumn 8, Issue 5, 2011, Pages 1698-1708

  Johansson, Katarina ^a   Ito, Mika ^b,c   Schophuizen, Carolien M S ^a   Mathew Thengumtharayil, Sherin ^a   Heuser, Vanina D ^a   Zhang, Jie ^a   Shimoji, Miyuki ^a   Vahter, Marie ^a   Ang, Wee Han ^d   Dyson, Paul J ^e   Shibata, Aya ^b   Shuto, Satoshi ^c   Ito, Yoshihiro ^b   Abe, Hiroshi ^b   Morgenstern, Ralf ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b Discovery Research Institute   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e EPFL   (Switzerland)

Author keywords

cytostatic drug; drug resistance; glutathione transferase

Indexed keywords

2,4 DINITROBENZENESULFONYL DOXORUBICIN; 4 MONONITROBENZENESULFONYL DOXORUBICIN; ANTINEOPLASTIC AGENT; CISPLATIN; DOXORUBICIN; ETACRYNIC ACID; ETHACRAPLATIN; GLUTATHIONE TRANSFERASE; GLUTATHIONE TRANSFERASE P1; MICROSOMAL GLUTATHIONE TRANSFERASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CLONOGENIC ASSAY; CONCENTRATION RESPONSE; CYTOTOXICITY; DRUG RELEASE; DRUG RESISTANCE; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE; CELL LINE, TUMOR; CISPLATIN; CRICETINAE; CRICETULUS; CYTOSTATIC AGENTS; DOXORUBICIN; DRUG DESIGN; DRUG RESISTANCE, NEOPLASM; ETHACRYNIC ACID; FEMALE; GLUTATHIONE S-TRANSFERASE PI; GLUTATHIONE TRANSFERASE; HUMANS; NEOPLASM PROTEINS; ORGANOPLATINUM COMPOUNDS; PRODRUGS; RATS; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

EID: 80053492515     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp2000692     Document Type: Article

References (59)

1. Simunek, T.; Sterba, M.; Popelova, O.; Adamcova, M.; Hrdina, R.; Gersl, V. Anthracycline-induced cardiotoxicity: overview of studies examining the roles of oxidative stress and free cellular iron Pharmacol. Rep. 2009, 61, 154-71
2. Pabla, N.; Dong, Z. Cisplatin nephrotoxicity: mechanisms and renoprotective strategies Kidney Int. 2008, 73, 994-1007 (Pubitemid 351543900)
3. Rybak, L. P. Mechanisms of cisplatin ototoxicity and progress in otoprotection Curr. Opin. Otolaryngol. Head Neck Surg. 2007, 15, 364-9 (Pubitemid 47373985)
4. McWhinney, S. R.; Goldberg, R. M.; McLeod, H. L. Platinum neurotoxicity pharmacogenetics Mol. Cancer Ther. 2009, 8, 10-6
5. Rautio, J.; Kumpulainen, H.; Heimbach, T.; Oliyai, R.; Oh, D.; Jarvinen, T.; Savolainen, J. Prodrugs: design and clinical applications Nat. Rev. Drug Discovery 2008, 7, 255-70 (Pubitemid 351324639)
6. Sau, A.; Pellizzari Tregno, F.; Valentino, F.; Federici, G.; Caccuri, A. M. Glutathione transferases and development of new principles to overcome drug resistance Arch. Biochem. Biophys. 2010, 500, 116-22
7. Townsend, D. M.; Tew, K. D. The role of glutathione-S-transferase in anti-cancer drug resistance Oncogene 2003, 22, 7369-75
8. Scotlandi, K.; Remondini, D.; Castellani, G.; Manara, M. C.; Nardi, F.; Cantiani, L.; Francesconi, M.; Mercuri, M.; Caccuri, A. M.; Serra, M.; Knuutila, S.; Picci, P. Overcoming resistance to conventional drugs in Ewing sarcoma and identification of molecular predictors of outcome J. Clin. Oncol. 2009, 27, 2209-16
9. Johansson, K.; Ahlen, K.; Rinaldi, R.; Sahlander, K.; Siritantikorn, A.; Morgenstern, R. Microsomal glutathione transferase 1 in anticancer drug resistance Carcinogenesis 2007, 28, 465-70 (Pubitemid 46321864)
10. McIlwain, C. C.; Townsend, D. M.; Tew, K. D. Glutathione S-transferase polymorphisms: cancer incidence and therapy Oncogene 2006, 25, 1639-48
11. Townsend, D.; Tew, K. Cancer drugs, genetic variation and the glutathione-S-transferase gene family Am. J. Pharmacogenomics 2003, 3, 157-72 (Pubitemid 36827674)
12. Hayes, J. D.; 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. 1995, 30, 445-600
13. Morgenstern, R.; DePierre, J. W. Microsomal glutathione transferase, Purification in unactivated form and further characterization of the activation process, substrate specificity and amino acid composition Eur. J. Biochem. 1983, 134, 591-7
14. Zhang, J.; Lou, Y. J. Relationship between activation of microsomal glutathione S-transferase and metabolism behavior of chlorambucil Pharmacol. Res. 2003, 48, 623-30 (Pubitemid 38352781)
15. Zhang, J.; Ye, Z.; Lou, Y. Metabolism of melphalan by rat liver microsomal glutathione S-transferase Chem.-Biol. Interact. 2005, 152, 101-6 (Pubitemid 40517148)
16. Chaib, H.; Cockrell, E. K.; Rubin, M. A.; Macoska, J. A. Profiling and verification of gene expression patterns in normal and malignant human prostate tissues by cDNA microarray analysis Neoplasia 2001, 3, 43-52 (Pubitemid 32201609)
17. Futschik, M.; Jeffs, A.; Pattison, S.; Kasabov, N.; Sullivan, M.; Merrie, A.; Reeve, A. Gene Expression Profiling of Metastatic and Nonmetastatic Colorectal Cancer Cell Lines Genome Lett. 2002, 1, 26-34
18. Lal, A.; Lash, A. E.; Altschul, S. F.; Velculescu, V.; Zhang, L.; McLendon, R. E.; Marra, M. A.; Prange, C.; Morin, P. J.; Polyak, K.; Papadopoulos, N.; Vogelstein, B.; Kinzler, K. W.; Strausberg, R. L.; Riggins, G. J. A public database for gene expression in human cancers Cancer Res. 1999, 59, 5403-7 (Pubitemid 29526444)
19. Linnerth, N. M.; Sirbovan, K.; Moorehead, R. A. Use of a transgenic mouse model to identify markers of human lung tumors Int. J. Cancer 2005, 114, 977-82
20. Tsunoda, T.; Koh, Y.; Koizumi, F.; Tsukiyama, S.; Ueda, H.; Taguchi, F.; Yamaue, H.; Saijo, N.; Nishio, K. Differential gene expression profiles and identification of the genes relevant to clinicopathologic factors in colorectal cancer selected by cDNA array method in combination with principal component analysis Int. J. Oncol. 2003, 23, 49-59
21. Goto, S.; Ihara, Y.; Urata, Y.; Izumi, S.; Abe, K.; Koji, T.; Kondo, T. Doxorubicin-induced DNA intercalation and scavenging by nuclear glutathione S-transferase pi FASEB J. 2001, 15, 2702-14 (Pubitemid 33131096)
22. Burg, D.; Riepsaame, J.; Pont, C.; Mulder, G.; van de Water, B. Peptide-bond modified glutathione conjugate analogs modulate GSTpi function in GSH-conjugation, drug sensitivity and JNK signaling Biochem. Pharmacol. 2006, 71, 268-77 (Pubitemid 41817287)
23. Adler, V.; Yin, Z.; Fuchs, S. Y.; Benezra, M.; Rosario, L.; Tew, K. D.; Pincus, M. R.; Sardana, M.; Henderson, C. J.; Wolf, C. R.; Davis, R. J.; Ronai, Z. Regulation of JNK signaling by GSTp EMBO J. 1999, 18, 1321-34 (Pubitemid 29110316)
24. Raza, A.; Galili, N.; Callander, N.; Ochoa, L.; Piro, L.; Emanuel, P.; Williams, S.; Burris, H., 3rd; Faderl, S.; Estrov, Z.; Curtin, P.; Larson, R. A.; Keck, J. G.; Jones, M.; Meng, L.; Brown, G. L. Phase 1-2a multicenter dose-escalation study of ezatiostat hydrochloride liposomes for injection (Telintra(R), TLK199), a novel glutathione analog prodrug in patients with myelodysplastic syndrome J. Hematol. Oncol. 2009, 2, 20
25. Morgan, A. S.; Sanderson, P. E.; Borch, R. F.; Tew, K. D.; Niitsu, Y.; Takayama, T.; Von Hoff, D. D.; Izbicka, E.; Mangold, G.; Paul, C.; Broberg, U.; Mannervik, B.; Henner, W. D.; Kauvar, L. M. Tumor efficacy and bone marrow-sparing properties of TER286, a cytotoxin activated by glutathione S-transferase Cancer Res. 1998, 58, 2568-75 (Pubitemid 28275427)
26. Tew, K. D. TLK-286: a novel glutathione S-transferase-activated prodrug Expert Opin. Invest. Drugs 2005, 14, 1047-54 (Pubitemid 41131655)
27. Ang, W. H.; Khalaila, I.; Allardyce, C. S.; Juillerat-Jeanneret, L.; Dyson, P. J. Rational design of platinum(IV) compounds to overcome glutathione-S-transferase mediated drug resistance J. Am. Chem. Soc. 2005, 127, 1382-3 (Pubitemid 40204507)
28. Ang, W. H.; Pilet, S.; Scopelliti, R.; Bussy, F.; Juillerat-Jeanneret, L.; Dyson, P. J. Synthesis and characterization of platinum(IV) anticancer drugs with functionalized aromatic carboxylate ligands: influence of the ligands on drug efficacies and uptake J. Med. Chem. 2005, 48, 8060-9 (Pubitemid 41798436)
29. Ploemen, J. H.; van Ommen, B.; van Bladeren, P. J. Inhibition of rat and human glutathione S-transferase isoenzymes by ethacrynic acid and its glutathione conjugate Biochem. Pharmacol. 1990, 40, 1631-5 (Pubitemid 20310584)
30. Molnar, J.; Somberg, J. C. The Clinical Pharmacology of Ethacrynic Acid Am. J. Ther. 2009, 16 (1) 86-92
31. Zhao, Z.; Koeplinger, K. A.; Peterson, T.; Conradi, R. A.; Burton, P. S.; Suarato, A.; Heinrikson, R. L.; Tomasselli, A. G. Mechanism, structure-activity studies, and potential applications of glutathione S-transferase-catalyzed cleavage of sulfonamides Drug Metab. Dispos. 1999, 27, 992-8 (Pubitemid 29409633)
32. Koeplinger, K. A.; Zhao, Z.; Peterson, T.; Leone, J. W.; Schwende, F. S.; Heinrikson, R. L.; Tomasselli, A. G. Activated sulfonamides are cleaved by glutathione-S-transferases Drug Metab. Dispos. 1999, 27, 986-91 (Pubitemid 29409632)
33. van Brakel, R.; Vulders, R. C.; Bokdam, R. J.; Grull, H.; Robillard, M. S. A doxorubicin prodrug activated by the staudinger reaction Bioconjugate Chem. 2008, 19, 714-8 (Pubitemid 351431404)
34. Yoo, H.; Rill, R. L. Single-strand DNA binding of actinomycin D with a chromophore 2-amino to 2-hydroxyl substitution J. Biochem. Mol. Biol. 2003, 36, 305-11 (Pubitemid 36890830)
35. Habig, W. H.; Pabst, M. J.; Jakoby, W. B. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation J. Biol. Chem. 1974, 249, 7130-7139
36. Shibata, A.; Furukawa, K.; Abe, H.; Tsuneda, S.; Ito, Y. Rhodamine-based fluorogenic probe for imaging biological thiol Bioorg. Med. Chem. Lett. 2008, 18, 2246-9 (Pubitemid 351442915)
37. Siritantikorn, A.; Johansson, K.; Ahlen, K.; Rinaldi, R.; Suthiphongchai, T.; Wilairat, P.; Morgenstern, R. Protection of cells from oxidative stress by microsomal glutathione transferase 1 Biochem. Biophys. Res. Commun. 2007, 355, 592-6 (Pubitemid 46282668)
38. Bunting, K. D.; Townsend, A. J. De novo expression of transfected human class 1 aldehyde dehydrogenase (ALDH) causes resistance to oxazaphosphorine anti-cancer alkylating agents in hamster V79 cell lines. Elevated class 1 ALDH activity is closely correlated with reduction in DNA interstrand cross-linking and lethality J. Biol. Chem. 1996, 271, 11884-90
39. Sundberg, K.; Seidel, A.; Mannervik, B.; Jernstrom, B. Detoxication of carcinogenic fjord-region diol epoxides of polycyclic aromatic hydrocarbons by glutathione transferase P1-1 variants and glutathione FEBS Lett. 1998, 438, 206-10 (Pubitemid 28529274)
40. Cogoi, S.; Codognotto, A.; Rapozzi, V.; Meeuwenoord, N.; van der Marel, G.; Xodo, L. E. Transcription inhibition of oncogenic KRAS by a mutation-selective peptide nucleic acid conjugated to the PKKKRKV nuclear localization signal peptide Biochemistry 2005, 44, 10510-9 (Pubitemid 41098228)
41. Alander, J.; Johansson, K.; Heuser, V. D.; Farebo, H.; Jarvliden, J.; Abe, H.; Shibata, A.; Ito, M.; Ito, Y.; Morgenstern, R. Characterization of a new fluorogenic substrate for microsomal glutathione transferase 1 Anal. Biochem. 2009, 390, 52-6
42. Morgenstern, R. Microsomal glutathione transferase 1 Methods Enzymol. 2005, 401, 136-46 (Pubitemid 43052390)
43. Hegazy, U. M.; Mannervik, B.; Stenberg, G. Functional role of the lock and key motif at the subunit interface of glutathione transferase p1-1 J. Biol. Chem. 2004, 279, 9586-96 (Pubitemid 38296027)
44. Mosmann, T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays J. Immunol. Methods 1983, 65, 55-63 (Pubitemid 14203433)
45. Lu, D.; Liu, J. X.; Endo, T.; Zhou, H.; Yao, S.; Willert, K.; Schmidt-Wolf, I. G.; Kipps, T. J.; Carson, D. A. Ethacrynic acid exhibits selective toxicity to chronic lymphocytic leukemia cells by inhibition of the Wnt/beta-catenin pathway PLoS One 2009, 4, e8294
46. Nath, N.; Vassell, R.; Chattopadhyay, M.; Kogan, M.; Kashfi, K. Nitro-aspirin inhibits MCF-7 breast cancer cell growth: effects on COX-2 expression and Wnt/beta-catenin/TCF-4 signaling Biochem. Pharmacol. 2009, 78, 1298-304
47. Scotlandi, K.; Remondini, D.; Castellani, G.; Manara, M. C.; Nardi, F.; Cantiani, L.; Francesconi, M.; Mercuri, M.; Caccuri, A. M.; Serra, M.; Knuutila, S.; Picci, P. Overcoming resistance to conventional drugs in Ewing sarcoma and identification of molecular predictors of outcome J. Clin. Oncol. 2009, 27, 2209-16
48. Kamada, K.; Goto, S.; Okunaga, T.; Ihara, Y.; Tsuji, K.; Kawai, Y.; Uchida, K.; Osawa, T.; Matsuo, T.; Nagata, I.; Kondo, T. Nuclear glutathione S-transferase pi prevents apoptosis by reducing the oxidative stress-induced formation of exocyclic DNA products Free Radical Biol. Med. 2004, 37, 1875-84 (Pubitemid 39441071)
49. Goto, S.; Kawakatsu, M.; Izumi, S.; Urata, Y.; Kageyama, K.; Ihara, Y.; Koji, T.; Kondo, T. Glutathione S-transferase pi localizes in mitochondria and protects against oxidative stress Free Radical Biol. Med. 2009, 46, 1392-403
50. Goto, S.; Iida, T.; Cho, S.; Oka, M.; Kohno, S.; Kondo, T. Overexpression of glutathione S-transferase pi enhances the adduct formation of cisplatin with glutathione in human cancer cells Free Radical Res. 1999, 31, 549-58
51. Lacreta, F. P.; Brennan, J. M.; Nash, S. L.; Comis, R. L.; Tew, K. D.; ODwyer, P. J. Pharmakokinetics and bioavailability study of ethacrynic acid as a modulator of drug resistance in patients with cancer J. Pharmacol. Exp. Ther. 1994, 270, 1186-91 (Pubitemid 24315238)
52. ODwyer, P. J.; LaCreta, F.; Nash, S.; Tinsley, P. W.; Schilder, R.; Clapper, M. L.; Tew, K. D.; Panting, L.; Litwin, S.; Comis, R. L. Phase I study of thiotepa in combination with the glutathione transferase inhibitor ethacrynic acid Cancer Res. 1991, 51, 6059-65
53. Townsend, D. M.; Tew, K. D.; He, L.; King, J. B.; Hanigan, M. H. Role of glutathione S-transferase Pi in cisplatin-induced nephrotoxicity Biomed. Pharmacother. 2009, 63, 79-85
54. Byun, S. S.; Kim, S. W.; Choi, H.; Lee, C.; Lee, E. Augmentation of cisplatin sensitivity in cisplatin-resistant human bladder cancer cells by modulating glutathione concentrations and glutathione-related enzyme activities BJU Int. 2005, 95, 1086-90 (Pubitemid 40655712)
55. Mosialou, E.; Morgenstern, R. Inhibition studies on rat liver microsomal glutathione transferase Chem.-Biol. Interact. 1990, 74, 275-80 (Pubitemid 20158186)
56. Morgenstern, R.; Lundqvist, G.; Andersson, G.; Balk, L.; DePierre, J. W. The distribution of microsomal glutathione transferase among different organelles, different organs and different organisms Biochem. Pharmacol. 1984, 33, 3609-14 (Pubitemid 15220938)
57. Axarli, I.; Labrou, N. E.; Petrou, C.; Rassias, N.; Cordopatis, P.; Clonis, Y. D. Sulphonamide-based bombesin prodrug analogues for glutathione transferase, useful in targeted cancer chemotherapy Eur. J. Med. Chem. 2009, 44, 2009-16
58. Morgenstern, R.; Lundqvist, G.; Hancock, V.; DePierre, J. W. Studies on the activity and activation of rat liver microsomal glutathione transferase, in particular with a substrate analogue series J. Biol. Chem. 1988, 263, 6671-5
59. Morgenstern, R. A simple alternate substrate test can help determine the aqueous or bilayer location of binding sites for hydrophobic ligands/substrates on membrane proteins Chem. Res. Toxicol. 1998, 11, 703-7 (Pubitemid 28285596)