Human Pathology
Volume 38, Issue 2 , Pages 220-227 , February 2007

Expression of glutathione S-transferase π and glutathione synthase correlates with survival in early stage non–small cell carcinomas of the lung

  • Timothy C. Allen, MD, JD

      Affiliations

    • The University of Texas Health Center at Tyler, Tyler, TX 75708, USA
    • ,
  • Laura A. Granville, MD

      Affiliations

    • Baylor College of Medicine, Houston, TX 77030, USA
    • ,
  • Philip T. Cagle, MD

      Affiliations

    • Weill Cornell Medical College and The Methodist Hospital, Houston, TX 77030, USA
    • Corresponding Author InformationCorresponding author. Department of Pathology, The Methodist Hospital, Houston, TX 77030, USA.
    • ,
  • Abida Haque, MD

      Affiliations

    • Weill Cornell Medical College and The Methodist Hospital, Houston, TX 77030, USA
    • ,
  • Dani S. Zander, MD

      Affiliations

    • University of Texas Health Science Center at Houston Medical School, Houston, TX 77030, USA
    • ,
  • Roberto Barrios, MD

      Affiliations

    • Weill Cornell Medical College and The Methodist Hospital, Houston, TX 77030, USA

Received 2 March 2006 ,Revised 30 June 2006 ,Accepted 3 July 2006.

References 

  1. Rushmore TH, Pickett CB. Glutathione S-transferases, structure, regulation, and therapeutic implications. J Biol Chem. 1993;268:11475–11478
  2. Armstrong RN. Glutathione S-transferases: structure and mechanism of an archetypical detoxication enzyme. Adv Enzymol Relat Areas Mol Biol. 1994;69:1–44
  3. Lu SC. Regulation of hepatic glutathione synthesis: current concepts and controversies. FASEB J. 1999;13:1169–1183
  4. Ketterer B. A bird's eye view of the glutathione transferase field. Chem Biol Interact. 2001;138:27–42
  5. Chwals WJ. Regulation of the cellular and physiological effects of glutamine. Mini Rev Med Chem. 2004;4:833–838
  6. Townsend DM, Findlay VL, Tew KD. Glutathione S-transferases as regulators of kinase pathways and anticancer drug targets. Methods Enzymol. 2005;401:287–307
  7. Zappacosta B, Persichilli S, Minucci A, et al. Effect of cigarette smoke extract on the polymorphonuclear leukocytes chemiluminescence: influence of a filter containing glutathione. Luminescence. 2005;20:73–75
  8. Fidan F, Unlu M, Kiken T, et al. Oxidant-antioxidant status and pulmonary function in welding workers. J Occup Health. 2005;47:286–292
  9. Burg D, Mulder GJ. Glutathione conjugates and their synthetic derivatives as inhibitors of glutathione-dependent enzymes involved in cancer and drug resistance. Drug Metab Rev. 2002;34:821–863
  10. Ohtake Y, Yabuuchi S. Molecular cloning of the gamma-glutamylcysteine synthetase gene of Saccharomyces cerevisiae. Yeast. 1991;7:953–961
  11. Gushima H, Yasuda S, Soeda E, Yokota M, Kondo M, Kimura A. Complete nucleotide sequence of the E. coli glutathione synthetase Gsh-II. Nucleic Acids Res. 1984;12:9299–9307
  12. Anderson ME. Glutathione: an overview of biosynthesis and modulation. Chem Biol Interact 1998;24:111-112:1-14.
  13. Armstrong RN. Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem Res Toxicol. 1997;10:2–18
  14. Hayes JD, Pulford DJ. 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 Bio. 1995;30:445–600
  15. Norppa H. Cytogenetic biomarkers and genetic polymorphisms. Toxicology Letters. 2004;149:309–334
  16. Miller DP, Neuberg D, de Vivo I, et al. Smoking and the risk of lung cancer: susceptibility with GSTP1 polymorphisms. Epidemiology. 2003;14:545–551
  17. Russo AL, Thiagalingam A, Pan H, et al. Differential DNA hypermethylation of critical genes mediates the stage-specific tobacco smoke-induced neoplastic progression of lung cancer. Clin Cancer Res. 2005;11:2466–2470
  18. Cote ML, Kardia SL, Wenzlaff AS, Land SJ, Schwartz AG. Combinations of glutathione S-transferase genotypes and risk of early-onset lung cancer in Caucasians and African Americans: a population-based study. Carcinogenesis. 2005;26:1158
  19. Townsend DM, Tew KD. The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene. 2003;22:7369–7375
  20. Cullen KJ, Newkirk KA, Schumaker LM, et al. Glutathione S-transferase pi amplification is associated with cisplatin resistance in head and neck squamous cell carcinoma lines and primary tumors. Cancer Res. 2003;63:8097–8102
  21. Nishimura T, Newkirk K, Sessions R, et al. Immunohistochemical staining for glutathione S-transferase predicts response to platinum based chemotherapy in head and neck cancer. Clin Cancer Res. 1996;2:1238–1243
  22. Shiga H, Heath EI, Rasmussen AA, et al. Prognostic value of p53, glutathione S-transferase π and thymidylate synthase for neoadjuvant cisplatin-based chemotherapy in head and neck cancer. Clin Cancer Res. 1999;5:4097–4104
  23. Tew KD. Glutathione-associated enzymes in anticancer drug resistance. Cancer Res. 1994;54:4313–4320
  24. Shen H, Kauvar L, Tew KD. Importance of glutathione and associated enzymes in drug response. Oncol Res. 1997;9:295–302
  25. Duvoix A, Schmitz M, Schnekenburger M, et al. Transcriptional regulation of glutathione S-transferase P1-1 in human leukemia. Biofactors. 2003;17:131–138
  26. Cookson MS, Reuter VE, Linkov I, Fair WR. Glutathione S-transferase pi class expression by immunohistochemistry in benign and malignant prostate tissue. J Urol. 1995;47:271–330
  27. Inoue T, Ishida T, Sugio K, et al. Glutathione S-transferase pi is a powerful indicator in chemotherapy of human lung squamous-cell carcinoma. Respiration. 1995;62:23–27
  28. Sauerbrey A, Zintl F, Volm M. P-glycoprotein and glutathione S transferase π in childhood acute lymphoblastic leukemia. Br J Cancer. 1994;70:1144–1149
  29. Toffoli G, Frustaci S, Tumiotto L, et al. Expression of MDR1 and GST-pi in human soft tissue sarcomas: relation to drug resistance and biological aggressiveness. Ann Oncol. 1992;3:63–69
  30. Monden N, Abe S, Sutoh I, et al. Prognostic significance of the expressions of metallothionein, glutathione-S-transferase-pi, and P-glycoprotein in curatively resected gastric cancer. Oncology. 1997;54:391–399
  31. Nakagawa K, Saijo N, Tsuchida S, et al. Glutathione-S-transferase pi as a determinant of drug resistance in transfectant cell lines. J Biol Chem. 1990;265:4296–4301
  32. Hao XY, Bergh J, Brodin O, et al. Acquired-resistance to cisplatin and doxorubicin in a small-cell lung-cancer cell-line is correlated to elevated expression of glutathione-linked detoxification enzymes. Carcinogenesis. 1994;15:1167–1173
  33. Harbottle A, Daly AK, Atherton K, Campbell FC. Role of glutathione S-transferase pi, p-glycoprotein and multidrug resistance-associated protein 1 in acquired doxorubicin resistance. Int J Cancer. 2001;92:777–783
  34. Morrow JA. Combined expression of multidrug resistance protein (MRP) and glutathione S-transferase-pi (GSTP1-1) in MCF7 cells and high level resistance to the cytotoxicities of ethacrynic acid but not oxazaphosphorines or cisplatin. Biochem Pharmacol. 1998;56:1013–1021
  35. Moscow JA. Elevation of π class glutathione transferase activity in human breast cancer cells by transfection of the GSTπ gene and its effect on sensitivity to toxins. Mol Pharmacol. 1989;36:22–28
  36. Masanek U. Messenger RNA expression of resistance proteins and related factors in human ovarian carcinoma cell lines resistant to doxorubicin, taxol and cisplatin. Anticancer Drugs. 1997;8:189–198
  37. Puchalski RB, Fahl WE. Expression of recombinant glutathione S-transferase π, Ya, or Yb1 confers resistance to alkylating agents. Med Sci. 1990;87:2443–2447
  38. Lung. In: American Joint Committee on Cancer: AJCC cancer staging manual. 5th ed.. Philadelphia (Pa): Lippincott-Raven Publishers; 1997;p. 127–137
  39. Chen X, Carystinos GD, Batist G. Potential for selective modulation of glutathione in cancer chemotherapy. Chem Biol Interact 1998;111-112:263-75.
  40. Geroni C, Marchini S, Cozzi P, et al. Brostallicin, a novel anticancer agent whose activity is enhanced upon binding to glutathione. Cancer Res. 2002;62:2332–2336
  41. Tew KD. TLK-286: a novel glutathione S-tranferase–activated prodrug. Expert Opin Investig Drugs. 2005;14:1047–1054
  42. Huang J, Tan PH, Thiyagarajan J, Bay BH. Prognostic significance of glutathione S-transferase-pi in invasive breast cancer. Mod Pathol. 2003;16:558–565
  43. Katahira T, Takayama T, Miyanishi K, et al. Plasma glutathione S-Transferase P1-1 as a prognostic factor in patients with advanced non-Hodgkin's lymphoma (stages III and IV). Clin Cancer Res. 2004;10:7934–7940
  44. Su F, HU X, Jia W, et al. Glutathione S-transferase pi indicates chemotherapy resistance in breast cancer. J Surg Res. 2003;113:102–108
  45. Ribrag V, Koscielny S, Carpiuc I, et al. Prognostic value of GST-pi expression in diffuse large B-cell lymphomas. Leukemia. 2003;17:972–977
  46. Bennaceur-Griscelli A, Bosq J, Koscielny S, et al. High level of glutathione-S-transferase pi expression in mantle cell lymphomas. Clin Cancer Res. 2004;10:3029–3034
  47. Hirano T, Kato H, Maeda M, et al. Identification of postoperative adjuvant chemotherapy responders in non–small cell lung cancer by novel biomarker. Int J Cancer. 2005;117:460–468
  48. Kamada K, Goto S, Okunaga T, et al. Nuclear glutathione S-transferase π prevents apoptosis by reducing the oxidative stress-induced formation of exocyclic DNA products. Free Radic Biol Med. 2004;37:1875–1884
  49. Shiratori Y, Soma Y, Maruyama H, et al. Immunohistochemical detection of the placental form of glutathione S-transferase in dysplastic and neoplastic human uterine cervix lesions. Cancer Res. 1987;47:6806–6809
  50. Ali-Osman F, Brunner JM, Kutluk TM, et al. Prognostic significance of glutathione S-transferase π expression and subcellular localization in human gliomas. Clin Cancer Res. 1997;3:2253–2261
  51. Goto S, Kamada K, Hoh Y, et al. Significance of nuclear glutathione S-transferase pi in resistance to anti-cancer drugs. Jpn J Cancer Res. 2002;93:1047–1056
  52. Soh Y, Goto S, Kitajima M, et al. Nuclear localization of glutathione S-tranferase pi is an evaluation factor for drug resistance in gynaecologic cancers. Clin Oncol (R Coll Radiol). 2005;17:264–270
  53. Calatozzolo C, Gelati M, Cuisani E, et al. Expression of drug resistance proteins Pgp, MRP1, MRP3, MRP5, and GST-π in human glioma. J Neuro-oncology. 2005;74:113–121
  54. Chan QKY, Khoo US, Chan KYK, et al. Promoter methylation and differential expression of π-class glutathione S-transferase in endometrial carcinoma. J Mol Diagn. 2005;7:8–16
  55. Bradender J, Lord RV, Wickramasinghe K, et al. Glutathione S-transferase-pi expression is downregulated in patients with Barrett's esophagus and esophageal adenocarcinoma. J Gastrointest Surg. 2002;6:359–367
  56. Lu C, Spitz MR, Zhao H, et al. Association between glutathione S-transferase pi polymorphisms and survival in patients with advanced nonsmall cell lung carcinomas. Cancer. 2006;106:441–447
  57. Rothnie A, Callaghan R, Deeley RG, Cole SPC. Role of GSH in estrone sulfate binding and translocation by the multidrug resistance protein 1 (MRP1/ABCC1). J Biol Chem. 2006;281:13906–13914
  58. Loe DW, Almquist KC, Deeley RG, Cole SPC. Multidrug resistance protein (MRP)–mediated transport of leukotriene C4 and chemotherapeutic agents in membrane vesicles. Demonstration of glutathione-dependent vincristine transport. J Biol Chem. 1996;271:9675–9682
  59. Qian YM, Song WC, Cui H, et al. Glutathione stimulates sulfated estrogen transport by multidrug resistance protein 1. J Biol Chem. 2001;276:6404–6411
  60. Rappa G, Lrico A, Glavell RA, Sartorelli AC. Evidence that the multidrug resistance protein (MRP) functions as a co-transporter of glutathione and natural product toxins. Cancer Res. 1997;57:5232–5237
  61. Loe DW, Deeley RG, Cole SPC. Characterization of vincristine transport by the M9r0 190,000 multidrug resistance protein (MRP): evidence for cotransport with reduced glutathione. Cancer Res. 1998;58:5130–5136
  62. Renes J, de Vries EGE, Hienhuis EF, et al. ATP- and glutathione-dependent transport of chemotherapeutic drugs by the multidrug resistance protein MRP1. Br J Pharm. 1999;126:681–688
  63. Leslie EM, Ito K, Upadhyaya P, et al. Transport of the beta-O-glucuronide conjugate of the tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol (NNAL) by the multidrug resistance protein 1 (MRP1). Requirement for glutathione or a non–sulfur-containing analog. J Biol Chem. 2001;276:27846–27854
  64. Peklak-Scott C, Townsend AJ, Morrow CS. Dynamics of glutathione conjugation and conjugate efflux in detoxification of the carcinogen, 4-nitroquinoline 1-oxide: contributions of glutathione, glutathione S-tranferase, and MRP1. Biochemistry. 2005;44:4426–4433
  65. Morrow CS, Peklak-Scott C, Bishwokarma B, et al. Multidrug resistance protein 1 (MRP1, ABCC1) mediates resistance to mitoxantrone via glutathione-dependent drug efflux. Mol Pharmacol. 2006;69:1499–1505
  66. Estrela JM, Ortega A, Obrador E. Glutathione in cancer biology and therapy. Crit Rev Clin Lab Sci. 2006;43:143–181
  67. Honda T, Coppola S, Ghibelli L, et al. GSH depletion enhances adenoviral bax-induced apoptosis in lung cancer cells. Cancer Gene Ther. 2004;11:249–255

PII: S0046-8177(06)00419-9

doi: 10.1016/j.humpath.2006.07.006

Human Pathology
Volume 38, Issue 2 , Pages 220-227 , February 2007

Article Tools

* Image Usage & Resolution