Glutathione S-transferase P1 (GSTP1) directly influences platinum drug chemosensitivity in ovarian tumour cell lines

British Journal of Cancer

Volumn 111, Issue 6, 2014, Pages 1150-1158

  Sawers, L ^a   Ferguson, M J ^a   Ihrig, B R ^a   Young, H C ^a   Chakravarty, P ^b   Wolf, C R ^a   Smith, G ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

chemosensitivity; drug resistance; glutathione; GSTP1; personalised medicine; platinum

Indexed keywords

CARBOPLATIN; CISPLATIN; DOXORUBICIN; GEMCITABINE; GLUTATHIONE; GLUTATHIONE TRANSFERASE P1; PACLITAXEL; SHORT HAIRPIN RNA; TOPOTECAN; ANTINEOPLASTIC AGENT;

ARTICLE; CELL CYCLE ASSAY; CELL CYCLE PROGRESSION; CELL INVASION; CELL MIGRATION; CHEMOSENSITIVITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DATA ANALYSIS SOFTWARE; DRUG METABOLISM; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GENE DELETION; GENE EXPRESSION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; IC50; MTT ASSAY; OVARY TUMOR; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; CELL CYCLE; CELL MOTION; DRUG EFFECT; DRUG RESISTANCE; GENETICS; IC 50; METABOLISM; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CARBOPLATIN; CELL CYCLE; CELL LINE, TUMOR; CELL MOVEMENT; CISPLATIN; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; GLUTATHIONE S-TRANSFERASE PI; HUMANS; INHIBITORY CONCENTRATION 50; OVARIAN NEOPLASMS;

EID: 84908370913     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2014.386     Document Type: Article

References (61)

1. Adler V, Yin Z, Fuchs SY, Benezra M, Rosario L, Tew KD, Pincus MR, Sardana M, Henderson CJ, Wolf CR, Davis RJ, Ronai Z (1999) Regulation of JNK signaling by GSTp. EMBO J 18(5): 1321-1334.
2. Ahokas JT, Davies C, Ravenscroft PJ, Emmerson BT (1984) Inhibition of soluble glutathione S-transferase by diuretic drugs. Biochem Pharmacol 33(12): 1929-1932.
3. Ali-Osman F, Akande O, Antoun G, Mao JX, Buolamwini J (1997) Molecular cloning, characterization, and expression in Escherichia coli of full-length cDNAs of three human glutathione S-transferase Pi gene variants. Evidence for differential catalytic activity of the encoded proteins. J Biol Chem 272(15): 10004-10012.
4. Anathy V, Roberson E, Cunniff B, Nolin JD, Hoffman S, Spiess P, Guala AS, Lahue KG, Goldman D, Flemer S, van der Vliet A, Heintz NH, Budd RC, Tew KD, Janssen-Heininger YM (2012) Oxidative processing of latent Fas in the endoplasmic reticulum controls the strength of apoptosis. Mol Cell Biol 32(17): 3464-3478.
5. Ban N, Takahashi Y, Takayama T, Kura T, Katahira T, Sakamaki S, Niitsu Y (1996) Transfection of glutathione S-transferase (GST)-pi antisense complementary DNA increases the sensitivity of a colon cancer cell line to adriamycin, cisplatin, melphalan, and etoposide. Cancer Res 56(15): 3577-3582.
6. Behrens BC, Hamilton TC, Masuda H, Grotzinger KR, Whang-Peng J, Louie KG, Knutsen T, McKoy WM, Young RC, Ozols RF (1987) Characterization of a cis-diamminedichloroplatinum(II)-resistant human ovarian cancer cell line and its use in evaluation of platinum analogues. Cancer Res 47(2): 414-418.
7. Black SM, Beggs JD, Hayes JD, Bartoszek A, Muramatsu M, Sakai M, Wolf CR (1990) Expression of human glutathione S-transferases in Saccharomyces cerevisiae confers resistance to the anticancer drugs adriamycin and chlorambucil. Biochem J 268(2): 309-315.
8. Black SM, Wolf CR (1991) The role of glutathione-dependent enzymes in drug resistance. Pharmacol Ther 51(1): 139-154.
9. Board PG (1981) Biochemical genetics of glutathione-S-transferase in man. Am J Hum Genet 33(1): 36-43.
10. Boss EA, Peters WH, Roelofs HM, Boonstra H, Steegers EA, Massuger LF (2001) Glutathione S-transferases P1-1 and A1-1 in ovarian cyst fluids. Eur J Gynaecol Oncol 22(6): 427-432.
11. Chen J, Hurford M, Mekan S, Simpkins H (2013) Downregulation of glutathione transferase pi sensitizes lymphoma/leukaemia cells to platinum-based chemotherapy. Br J Haematol 162(1): 135-137.
12. Chen J, Solomides C, Simpkins H (2014) Sensitization of mesothelioma cells to platinum-based chemotherapy by GSTpi knockdown. Biochem Biophys Res Commun 447(1): 77-82.
13. Cheng G, Zhu H, Sun L (2000) [The expression of multiple drug resistance associated genes in ovarian cancer]. Zhonghua fu chan ke za zhi 35(2): 87-90.
14. De Luca A, Pellizzari Tregno F, Sau A, Pastore A, Palumbo C, Alama A, Cicconi R, Federici G, Caccuri AM (2013) Glutathione S-transferase P1-1 as a target for mesothelioma treatment. Cancer Sci 104(2): 223-230.
15. Dourado DF, Fernandes PA, Ramos MJ, Mannervik B (2013) Mechanism of glutathione transferase P1-1-catalyzed activation of the prodrug canfosfamide (TLK286, TELCYTA). Biochemistry 52(45): 8069-8078.
16. Eastman A (1987) The formation, isolation and characterization of DNA adducts produced by anticancer platinum complexes. Pharmacol Ther 34(2): 155-166.
17. Elsby R, Kitteringham NR, Goldring CE, Lovatt CA, Chamberlain M, Henderson CJ, Wolf CR, Park BK (2003) Increased constitutive c-Jun N-terminal kinase signaling in mice lacking glutathione S-transferase Pi. J Biol Chem 278(25): 22243-22249.
18. Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O, Castedo M, Kroemer G (2012) Molecular mechanisms of cisplatin resistance. Oncogene 31(15): 1869-1883.
19. Hagrman D, Goodisman J, Souid AK (2004) Kinetic study on the reactions of platinum drugs with glutathione. J Pharmacol Exp Ther 308(2): 658-666.
20. Harries LW, Stubbins MJ, Forman D, Howard GC, Wolf CR (1997) Identification of genetic polymorphisms at the glutathione S-transferase Pi locus and association with susceptibility to bladder, testicular and prostate cancer. Carcinogenesis 18(4): 641-644.
21. Hayes JD, Pulford DJ (1995) 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(6): 445-600.
22. Henderson CJ, Smith AG, Ure J, Brown K, Bacon EJ, Wolf CR (1998) Increased skin tumorigenesis in mice lacking pi class glutathione S-transferases. Proc Natl Acad Sci USA 95(9): 5275-5280.
23. Ishimoto TM, Ali-Osman F (2002) Allelic variants of the human glutathione S-transferase P1 gene confer differential cytoprotection against anticancer agents in Escherichia coli. Pharmacogenetics 12(7): 543-553.
24. Kase H, Kodama S, Nagai E, Tanaka K (1998) Glutathione S-transferase pi immunostaining of cisplatin-resistant ovarian cancer cells in ascites. Acta Cytologica 42(6): 1397-1402.
25. Kolwijck E, Zusterzeel PL, Roelofs HM, Hendriks JC, Peters WH, Massuger LF (2009) GSTP1-1 in ovarian cyst fluid and disease outcome of patients with ovarian cancer. Cancer Epidemiol Biomarkers Prev 18(8): 2176-2181.
26. Konecny G, Crohns C, Pegram M, Felber M, Lude S, Kurbacher C, Cree IA, Hepp H, Untch M (2000) Correlation of drug response with the ATP tumorchemosensitivity assay in primary FIGO stage III ovarian cancer. Gynecol Oncol 77(2): 258-263.
27. Kotoh S, Naito S, Yokomizo A, Kohno K, Kuwano M, Kumazawa J (1997) Enhanced expression of gamma-glutamylcysteine synthetase and glutathione S-transferase genes in cisplatin-resistant bladder cancer cells with multidrug resistance phenotype. J Urol 157(3): 1054-1058.
28. Kristensen GB, Trope C (1997) Epithelial ovarian carcinoma. Lancet 349(9045): 113-117.
29. Kuroda H, Sugimoto T, Ueda K, Tsuchida S, Horii Y, Inazawa J, Sato K, Sawada T (1991) Different drug sensitivity in two neuroblastoma cell lines established from the same patient before and after chemotherapy. Int J Cancer 47(5): 732-737.
30. Lewis AD, Hayes JD, Wolf CR (1988) Glutathione and glutathione-dependent enzymes in ovarian adenocarcinoma cell lines derived from a patient before and after the onset of drug resistance: intrinsic differences and cell cycle effects. Carcinogenesis 9(7): 1283-1287.
31. Li L, Luan Y, Wang G, Tang B, Li D, Zhang W, Li X, Zhao J, Ding H, Reed E, Li QQ (2004) Development and characterization of five cell models for chemoresistance studies of human ovarian carcinoma. Int J Mol Med 14(2): 257-264.
32. Lyttle MH, Satyam A, Hocker MD, Bauer KE, Caldwell CG, Hui HC, Morgan AS, Mergia A, Kauvar LM (1994) Glutathione-S-transferase activates novel alkylating agents. J Med Chem 37(10): 1501-1507.
33. McLellan LI, Wolf CR (1999) Glutathione and glutathione-dependent enzymes in cancer drug resistance. Drug Resist Updates 2(3): 153-164.
34. Mizutani Y, Bonavida B, Koishihara Y, Akamatsu K, Ohsugi Y, Yoshida O (1995) Sensitization of human renal cell carcinoma cells to cisdiamminedichloroplatinum( II) by anti-interleukin 6 monoclonal antibody or anti-interleukin 6 receptor monoclonal antibody. Cancer Res 55(3): 590-596.
35. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65(1-2): 55-63.
36. Parekh H, Simpkins H (1996) Cross-resistance and collateral sensitivity to natural product drugs in cisplatin-sensitive and -resistant rat lymphoma and human ovarian carcinoma cells. Cancer Chemother Pharmacol 37(5): 457-462.
37. Peklak-Scott C, Smitherman PK, Townsend AJ, Morrow CS (2008) Role of glutathione S-transferase P1-1 in the cellular detoxification of cisplatin. Mol Cancer Ther 7(10): 3247-3255.
38. Ricci G, De Maria F, Antonini G, Turella P, Bullo A, Stella L, Filomeni G, Federici G, Caccuri AM (2005) 7-Nitro-2,1,3-benzoxadiazole derivatives, a new class of suicide inhibitors for glutathione S-transferases. Mechanism of action of potential anticancer drugs. J Biol Chem 280(28): 26397-26405.
39. Rosario LA, OBrien ML, Henderson CJ, Wolf CR, Tew KD (2000) Cellular response to a glutathione S-transferase P1-1 activated prodrug. Mol Pharmacol 58(1): 167-174.
40. Sachse C, Smith G, Wilkie MJ, Barrett JH, Waxman R, Sullivan F, Forman D, Bishop DT, Wolf CR. Colorectal Cancer Study G (2002) A pharmacogenetic study to investigate the role of dietary carcinogens in the etiology of colorectal cancer. Carcinogenesis 23(11): 1839-1849.
41. Saip P, Tuzlali S, Demir K, Sakar B, Yavuz E, Berkman S, Bengisu E, Topuz E (2005) Value of glutathion-S transferase pi as a prognostic factor in epithelial ovarian carcinoma. Eur J Gynaecol Oncol 26(1): 90-94.
42. Satoh K, Kitahara A, Soma Y, Inaba Y, Hatayama I, Sato K (1985) Purification, induction, and distribution of placental glutathione transferase: a new marker enzyme for preneoplastic cells in the rat chemical hepatocarcinogenesis. Proc Natl Acad Sci USA 82(12): 3964-3968.
43. Scambia G, Testa U, Benedetti Panici P, Foti E, Martucci R, Gadducci A, Perillo A, Facchini V, Peschle C, Mancuso S (1995) Prognostic significance of interleukin 6 serum levels in patients with ovarian cancer. Br J Cancer 71(2): 354-356.
44. Shea TC, Kelley SL, Henner WD (1988) Identification of an anionic form of glutathione transferase present in many human tumors and human tumor cell lines. Cancer Res 48(3): 527-533.
45. Smith G, Ng MT, Shepherd L, Herrington CS, Gourley C, Ferguson MJ, Wolf CR (2012) Individuality in FGF1 expression significantly influences platinum resistance and progression-free survival in ovarian cancer. Br J Cancer 107(8): 1327-1336.
46. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
47. Sun KH, Chang KH, Clawson S, Ghosh S, Mirzaei H, Regnier F, Shah K (2011) Glutathione-S-transferase P1 is a critical regulator of Cdk5 kinase activity. J Neurochem 118(5): 902-914.
48. Surowiak P, Materna V, Kaplenko I, Spaczynski M, Dietel M, Lage H, Zabel M (2005) Augmented expression of metallothionein and glutathione S-transferase pi as unfavourable prognostic factors in cisplatin-treated ovarian cancer patients. Virchows Arch 447(3): 626-633.
49. Tew KD (1994) Glutathione-associated enzymes in anticancer drug resistance. Cancer Res 54(16): 4313-4320.
50. Townsend DM, Shen H, Staros AL, Gate L, Tew KD (2002) Efficacy of a glutathione S-transferase pi-activated prodrug in platinum-resistant ovarian cancer cells. Mol Cancer Ther 1(12): 1089-1095.
51. Tozawa K, Oshima T, Kobayashi T, Yamamoto N, Hayashi C, Matsumoto T, Miwa H (2008) Oxaliplatin in treatment of the cisplatin-resistant MKN45 cell line of gastric cancer. Anticancer Res 28(4B): 2087-2092.
52. Turella P, Cerella C, Filomeni G, Bullo A, De Maria F, Ghibelli L, Ciriolo MR, Cianfriglia M, Mattei M, Federici G, Ricci G, Caccuri AM (2005) Proapoptotic activity of new glutathione S-transferase inhibitors. Cancer Res 65(9): 3751-3761.
53. Vaughan S, Coward JI, Bast RC, Berchuck A, Berek JS, Brenton JD, Coukos G, Crum CC, Drapkin R, Etemadmoghadam D, Friedlander M, Gabra H, Kaye SB, Lord CJ, Lengyel E, Levine DA, McNeish IA, Menon U, Mills GB, Nephew KP, Oza AM, Sood AK, Stronach EA, Walczak H, Bowtell DD, Balkwill FR (2011) Rethinking ovarian cancer: recommendations for improving outcomes. Nat Rev Cancer 11(10): 719-725.
54. Wang Y, Niu XL, Qu Y, Wu J, Zhu YQ, Sun WJ, Li LZ (2010) Autocrine production of interleukin-6 confers cisplatin and paclitaxel resistance in ovarian cancer cells. Cancer Lett 295(1): 110-123.
55. Wang YY, Teicher BA, Shea TC, Holden SA, Rosbe KW, al-Achi A, Henner WD (1989) Cross-resistance and glutathione-S-transferase-pi levels among four human melanoma cell lines selected for alkylating agent resistance. Cancer Res 49(22): 6185-6192.
56. Wu Y, Fan Y, Xue B, Luo L, Shen J, Zhang S, Jiang Y, Yin Z (2006) Human glutathione S-transferase P1-1 interacts with TRAF2 and regulates TRAF2-ASK1 signals. Oncogene 25(42): 5787-5800.
57. Yanagie H, Hisa T, Ogata A, Miyazaki A, Nonaka Y, Nishihira T, Osada I, Sairennji T, Sugiyama H, Furuya Y, Kidani Y, Takamoto S, Takahashi H, Eriguchi M (2009) Improvement of sensitivity to platinum compound with siRNA knockdown of upregulated genes in platinum complexresistant ovarian cancer cells in vitro. Biomed Pharmacother 63(8): 553-560.
58. Yang JX, Luo Y, Qiu HM, Tang WX (2009) Characterization and resistance mechanisms of cisplatin-resistant human hepatocellular carcinoma cell line. Saudi Med J 30(1): 35-40.
59. Yin Z, Ivanov VN, Habelhah H, Tew K, Ronai Z (2000) Glutathione S-transferase p elicits protection against H2O2-induced cell death via coordinated regulation of stress kinases. Cancer Res 60(15): 4053-4057.
60. Zhang X, Zhu J, Xing R, Tie Y, Fu H, Zheng X, Yu B (2012) miR-513a-3p sensitizes human lung adenocarcinoma cells to chemotherapy by targeting GSTP1. Lung Cancer 77(3): 488-494.
61. Zimniak P, Nanduri B, Pikula S, Bandorowicz-Pikula J, Singhal SS, Srivastava SK, Awasthi S, Awasthi YC (1994) Naturally occurring human glutathione S-transferase GSTP1-1 isoforms with isoleucine and valine in position 104 differ in enzymic properties. Eur J Biochem 224(3): 893-899.