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International Journal of Hepatology
Volume 2012 (2012), Article ID 137676, 11 pages
http://dx.doi.org/10.1155/2012/137676
Review Article

Regulation of Signal Transduction by Glutathione Transferases

Inserm, UMR991, Foie, Métabolismes et Cancer, CHU Pontchaillou, 35033 Rennes, France

Received 9 July 2012; Revised 13 September 2012; Accepted 13 September 2012

Academic Editor: Pascal Loyer

Copyright © 2012 Julie Pajaud et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. D. Hayes, J. U. Flanagan, and I. R. Jowsey, “Glutathione transferases,” Annual Review of Pharmacology and Toxicology, vol. 45, pp. 51–88, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. J. D. Hayes and D. J. Pulford, “The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance,” Critical Reviews in Biochemistry and Molecular Biology, vol. 30, no. 6, pp. 445–600, 1995. View at Google Scholar · View at Scopus
  3. S. Dwivedi, A. Sharma, B. Patrick, R. Sharma, and Y. C. Awasthi, “Role of 4-hydroxynonenal and its metabolites in signaling,” Redox Report, vol. 12, no. 1-2, pp. 4–10, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. G. Leonarduzzi, F. Robbesyn, and G. Poli, “Signaling kinases modulated by 4-hydroxynonenal,” Free Radical Biology and Medicine, vol. 37, no. 11, pp. 1694–1702, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. V. Adler, Z. Yin, S. Y. Fuchs et al., “Regulation of JNK signaling by GSTp,” The EMBO Journal, vol. 18, no. 5, pp. 1321–1334, 1999. View at Google Scholar · View at Scopus
  6. M. A. Yusuf, T. Chuang, G. J. Bhat, and K. S. Srivenugopal, “Cys-141 glutathionylation of human p53: studies using specific polyclonal antibodies in cancer samples and cell lines,” Free Radical Biology and Medicine, vol. 49, no. 5, pp. 908–917, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Fratelli, H. Demol, M. Puype et al., “Identification of proteins undergoing glutathionylation in oxidatively stressed hepatocytes and hepatoma cells,” Proteomics, vol. 3, no. 7, pp. 1154–1161, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. Y. Suryo Rahmanto, D. S. Kalinowski, D. J. Lane et al., “Nitrogen monoxide (NO) storage and transport by dinitrosyl-dithiol-iron complexes: long-lived NO that is trafficked by interacting proteins,” The Journal of Biological Chemistry, vol. 287, no. 10, pp. 6960–6968, 2012. View at Google Scholar
  9. J. Z. Pedersen, F. De Maria, P. Turella et al., “Glutathione transferases sequester toxic dinitrosyl-iron complexes in cells: a protection mechanism against excess nitric oxide,” The Journal of Biological Chemistry, vol. 282, no. 9, pp. 6364–6371, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. P. V. Usatyuk and V. Natarajan, “Role of mitogen-activated protein kinases in 4-hydroxy-2-nonenal-induced actin remodeling and barrier function in endothelial cells,” The Journal of Biological Chemistry, vol. 279, no. 12, pp. 11789–11797, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. J. Z. Cheng, S. S. Singhal, M. Saini et al., “Effects of mGST A4 transfection on 4-hydroxynonenal-mediated apoptosis and differentiation of K562 human erythroleukemia cells,” Archives of Biochemistry and Biophysics, vol. 372, no. 1, pp. 29–36, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. C. Awasthi, R. Sharma, J. Z. Cheng et al., “Role of 4-hydroxynonenal in stress-mediated apoptosis signaling,” Molecular Aspects of Medicine, vol. 24, no. 4-5, pp. 219–230, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. N. Zarkovic, Z. Ilic, M. Jurin, R. J. Schaur, H. Puhl, and H. Esterbauer, “Stimulation of HeLa cell growth by physiological concentrations of 4-hydroxynonenal,” Cell Biochemistry and Function, vol. 11, no. 4, pp. 279–286, 1993. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Pizzimenti, G. Barrera, M. U. Dianzani, and S. Brüsselbach, “Inhibition of D1, D2, and A cyclin expression in HL-60 cells by the lipid peroxydation product 4-hydroxynonenal,” Free Radical Biology and Medicine, vol. 26, no. 11-12, pp. 1578–1586, 1999. View at Publisher · View at Google Scholar · View at Scopus
  15. G. Barrera, S. Pizzimenti, S. Laurora, E. Moroni, B. Giglioni, and M. U. Dianzani, “4-Hydroxynonenal affects pRb/E2F pathway in HL-60 human leukemic cells,” Biochemical and Biophysical Research Communications, vol. 295, no. 2, pp. 267–275, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. G. Barrera, S. Pizzimenti, S. Laurora, F. Briatore, C. Toaldo, and M. U. Dianzani, “4-Hydroxynonenal and cell cycle,” BioFactors, vol. 24, no. 1–4, pp. 151–157, 2005. View at Google Scholar · View at Scopus
  17. A. Matsuzawa and H. Ichijo, “Stress-responsive protein kinases in redox-regulated apoptosis signaling,” Antioxidants and Redox Signaling, vol. 7, no. 3-4, pp. 472–481, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. S. W. Luckey and D. R. Petersen, “Metabolism of 4-hydroxynonenal by rat Kupffer cells,” Archives of Biochemistry and Biophysics, vol. 389, no. 1, pp. 77–83, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. J. F. Reichard, V. Vasiliou, and D. R. Petersen, “Characterization of 4-hydroxy-2-nonenal metabolism in stellate cell lines derived from normal and cirrhotic rat liver,” Biochimica et Biophysica Acta, vol. 1487, no. 2-3, pp. 222–232, 2000. View at Publisher · View at Google Scholar · View at Scopus
  20. N. G. He, S. S. Singhal, S. K. Srivastava, P. Zimniak, Y. C. Awasthi, and S. Awasthi, “Transfection of a 4-hydroxynonenal metabolizing glutathione S-transferase isozyme, mouse GSTA4-4, confers doxorubicin resistance to Chinese hamster ovary cells,” Archives of Biochemistry and Biophysics, vol. 333, no. 1, pp. 214–220, 1996. View at Publisher · View at Google Scholar · View at Scopus
  21. P. G. Board, “Identification of cDNAs encoding two human Alpha class glutathione transferases (GSTA3 and GSTA4) and the heterologous expression of GSTA4-4,” Biochemical Journal, vol. 330, part 2, pp. 827–831, 1998. View at Google Scholar · View at Scopus
  22. F. Desmots, M. Rissel, D. Gilot et al., “Pro-inflammatory cytokines tumor necrosis factor α and interleukin-6 and survival factor epidermal growth factor positively regulate the murine GSTA4 enzyme in hepatocytes,” The Journal of Biological Chemistry, vol. 277, no. 20, pp. 17892–17900, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. E. H. Kim and Y. J. Surh, “15-Deoxy-Δ12,14-prostaglandin J2 as a potential endogenous regulator of redox-sensitive transcription factors,” Biochemical Pharmacology, vol. 72, no. 11, pp. 1516–1528, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. E. H. Kim and Y. J. Surh, “The role of 15-deoxy-Δ12,14-prostaglandin J2, an endogenous ligand of peroxisome proliferator-activated receptor γ, in tumor angiogenesis,” Biochemical Pharmacology, vol. 76, no. 11, pp. 1544–1553, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Yu, L. Qiao, L. Zimmermann et al., “Troglitazone inhibits tumor growth in hepatocellular carcinoma in vitro and in vivo,” Hepatology, vol. 43, no. 1, pp. 134–143, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Shen et al., “PPARgamma inhibits hepatocellular carcinoma metastases in vitro and in mice,” British Journal of Cancer, vol. 106, no. 9, pp. 1486–1494, 2012. View at Google Scholar
  27. J. G. Jiang, C. Johnson, and R. Zarnegar, “Peroxisome proliferator-activated receptor γ-mediated transcriptional up-regulation of the hepatocyte growth factor gene promoter via a novel composite cis-acting element,” The Journal of Biological Chemistry, vol. 276, no. 27, pp. 25049–25056, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. K. Yanagawa, “The antiproliferative effect of HGF on hepatoma cells involves induction of apoptosis with increase in intracellular polyamine concentration levels,” Oncology Reports, vol. 5, no. 1, pp. 185–190, 1998. View at Google Scholar · View at Scopus
  29. J. Shim, B. H. Kim, Y. I. Kim et al., “The peroxisome proliferator-activated receptor γ ligands, pioglitazone and 15-deoxy-Δ12,14-prostaglandin J2, have antineoplastic effects against hepatitis B virus-associated hepatocellular carcinoma cells,” International Journal of Oncology, vol. 36, no. 1, pp. 223–231, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Cheng, H. Nakamura, H. Imanishi et al., “Peroxisome proliferator-activated receptor γ ligands, 15-deoxy-Δ12,14-prostaglandin J2, and ciglitazone, induce growth inhibition and cell cycle arrest in hepatic oval cells,” Biochemical and Biophysical Research Communications, vol. 322, no. 2, pp. 458–464, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. Y. Yamamoto, T. Ono, D. K. Dhar et al., “Role of peroxisome proliferator-activated receptor-gamma (PPARγ) during liver regeneration in rats,” Journal of Gastroenterology and Hepatology, vol. 23, no. 6, pp. 930–937, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. D. S. Straus et al., “deoxy-delta 12, 14-prostaglandin J2 inhibits multiple steps in the NF-kappa B signaling pathway,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 9, pp. 4844–4849, 2000. View at Google Scholar
  33. N. D. Perkins, “The diverse and complex roles of NF-kappaB subunits in cancer,” Nature Reviews Cancer, vol. 12, no. 2, pp. 121–132, 2012. View at Google Scholar
  34. N. D. Perkins and T. D. Gilmore, “Good cop, bad cop: the different faces of NF-κB,” Cell Death and Differentiation, vol. 13, no. 5, pp. 759–772, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. E. A. Klein, C. Yang, M. G. Kazanietz, and R. K. Assoian, “NFκB-independent signaling to the cyclin D1 gene by Rac,” Cell Cycle, vol. 6, no. 9, pp. 1115–1121, 2007. View at Google Scholar · View at Scopus
  36. N. Fausto, “Liver regeneration,” Journal of Hepatology, vol. 32, supplement 1, pp. 19–31, 2000. View at Google Scholar · View at Scopus
  37. A. Rossi, P. Kapahi, G. Natoli et al., “Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IκB kinase,” Nature, vol. 403, no. 6765, pp. 103–108, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Okano, K. Shiraki, H. Inoue et al., “The PPARgamma ligand, 15-Deoxy-Delta12, 14-PGJ2, regulates apoptosis-related protein expression in cholangio cell carcinoma cells,” International Journal of Molecular Medicine, vol. 12, no. 6, pp. 867–870, 2003. View at Google Scholar
  39. I. R. Jowsey, S. A. Smith, and J. D. Hayes, “Expression of the murine glutathione S-transferase α3 (GSTA3) subunit is markedly induced during adipocyte differentiation: activation of the GSTA3 gene promoter by the pro-adipogenic eicosanoid 15-deoxy-Δ 12,14-prostaglandin J2,” Biochemical and Biophysical Research Communications, vol. 312, no. 4, pp. 1226–1235, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Itoh, M. Mochizuki, Y. Ishii et al., “Transcription Factor Nrf2 Regulates Inflammation by Mediating the Effect of 15-Deoxy-Δ12,14-Prostaglandin J2,” Molecular and Cellular Biology, vol. 24, no. 1, pp. 36–45, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. M. McMahon, K. Itoh, M. Yamamoto, and J. D. Hayes, “Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression,” The Journal of Biological Chemistry, vol. 278, no. 24, pp. 21592–21600, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. T. A. Beyer, W. Xu, D. Teupser et al., “Impaired liver regeneration in Nrf2 knockout mice: role of ROS-mediated insulin/IGF-1 resistance,” The EMBO Journal, vol. 27, no. 1, pp. 212–223, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. T. A. Beyer and S. Werner, “The cytoprotective Nrf2 transcription factor controls insulin receptor signaling in the regenerating liver,” Cell Cycle, vol. 7, no. 7, pp. 874–878, 2008. View at Google Scholar · View at Scopus
  44. J. U. Flanagan and M. L. Smythe, “Sigma-class glutathione transferases,” Drug Metabolism Reviews, vol. 43, no. 2, pp. 194–214, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. J. J. P. Bogaards, J. C. Venekamp, and P. J. Van Bladeren, “Stereoselective conjugation of prostaglandin A2 and prostaglandin J2 with glutathione, catalyzed by the human glutathione S-transferases A1-1, A2-2, M1a-1a, and P1-1,” Chemical Research in Toxicology, vol. 10, no. 3, pp. 310–317, 1997. View at Publisher · View at Google Scholar · View at Scopus
  46. E. M. Brunoldi, G. Zanoni, G. Vidari et al., “Cyclopentenone prostaglandin, 15-deoxy-Δ12,14-PGJ2, is metabolized by HepG2 cells via conjugation with glutathione,” Chemical Research in Toxicology, vol. 20, no. 10, pp. 1528–1535, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Gayarre, M. I. Avellano, F. J. Sánchez-Gómez, M. J. Carrasco, F. J. Cañada, and D. Pérez-Sala, “Modification of proteins by cyclopentenone prostaglandins is differentially modulated by GSH in vitro,” Annals of the New York Academy of Sciences, vol. 1096, pp. 78–85, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. Y. Kawamoto, Y. Nakamura, Y. Naito et al., “Cyclopentenone prostaglandins as potential inducers of phase II detoxification enzymes. 15-deoxy-δ prostaglandin J2-induced expression of glutathione S-transferases,” The Journal of Biological Chemistry, vol. 275, no. 15, pp. 11291–11299, 2000. View at Publisher · View at Google Scholar · View at Scopus
  49. F. J. Sánchez-Gómez, J. Gayarre, M. I. Avellano, and D. Pérez-Sala, “Direct evidence for the covalent modification of glutathione-S-transferase P1-1 by electrophilic prostaglandins: implications for enzyme inactivation and cell survival,” Archives of Biochemistry and Biophysics, vol. 457, no. 2, pp. 150–159, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. C. M. Paumi, P. K. Smitherman, A. J. Townsend, and C. S. Morrow, “Glutathione S-transferases (GSTs) inhibit transcriptional activation by the peroxisomal proliferator-activated receptor γ (PPARγ) ligand, 15-deoxy-Δ12,14prostaglandin J2 (15-d-PGJ 2),” Biochemistry, vol. 43, no. 8, pp. 2345–2352, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Wang, P. Arifoglu, Z. Ronai, and K. D. Tew, “Glutathione S-transferase P1-1 (GSTP1-1) inhibits c-Jun N-terminal kinase (JNK1) signaling through interaction with the C terminus,” The Journal of Biological Chemistry, vol. 276, no. 24, pp. 20999–21003, 2001. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Bernardini, F. Bernassola, C. Cortese et al., “Modulation of GST P1-1 activity by polymerization during apoptosis,” Journal of Cellular Biochemistry, vol. 77, no. 4, pp. 645–653, 2000. View at Google Scholar
  53. S. Gildenhuys, L. A. Wallace, J. P. Burke, D. Balchin, Y. Sayed, and H. W. Dirr, “Class Pi glutathione transferase unfolds via a dimeric and not monomeric intermediate: functional implications for an unstable monomer,” Biochemistry, vol. 49, no. 24, pp. 5074–5081, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. S. I. Holley, A. A. Fryer, J. W. Haycock, S. E. W. Grubb, R. C. Strange, and P. R. Hoban, “Differential effects of glutathione S-transferase pi (GSTP1) haplotypes on cell proliferation and apoptosis,” Carcinogenesis, vol. 28, no. 11, pp. 2268–2273, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. A. F. Thévenin, C. L. Zony, B. J. Bahnson, and R. F. Colman, “GST pi modulates JNK activity through a direct interaction with JNK substrate, ATF2,” Protein Science, vol. 20, no. 5, pp. 834–848, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. R. Elsby, N. R. Kitteringham, C. E. Goldring et al., “Increased constitutive c-Jun N-terminal kinase signaling in mice lacking glutathione S-transferase Pi,” The Journal of Biological Chemistry, vol. 278, no. 25, pp. 22243–22249, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Castro-Caldas, A. N. Carvalho, E. Rodrigues et al., “Glutathione S-transferase pi mediates MPTP-induced c-Jun N-terminal kinase activation in the nigrostriatal pathway,” Molecular Neurobiology, vol. 45, no. 3, pp. 466–477, 2012. View at Google Scholar
  58. L. Romero, K. Andrews, L. Ng, K. O'Rourke, A. Maslen, and G. Kirby, “Human GSTA1-1 reduces c-Jun N-terminal kinase signalling and apoptosis in Caco-2 cells,” Biochemical Journal, vol. 400, no. 1, pp. 135–141, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. F. Desmots, P. Loyer, M. Rissel, A. Guillouzo, and F. Morel, “Activation of C-Jun N-terminal kinase is required for glutathione transferase A4 induction during oxidative stress, not during cell proliferation, in mouse hepatocytes,” FEBS Letters, vol. 579, no. 25, pp. 5691–5696, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. S. G. Cho, Y. H. Lee, H. S. Park et al., “S-transferase mu modulates the stress-activated signals by suppressing apoptosis signal-regulating kinase,” The Journal of Biological Chemistry, vol. 276, no. 16, pp. 12749–12755, 2001. View at Publisher · View at Google Scholar · View at Scopus
  61. S. Dorion, H. Lambert, and J. Landry, “Activation of the p38 signaling pathway by heat shock involves the dissociation of glutathione S-transferase Mu from Ask1,” The Journal of Biological Chemistry, vol. 277, no. 34, pp. 30792–30797, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. D. Gilot, P. Loyer, A. Corlu et al., “Liver protection from apoptosis requires both blockage of initiator caspase activities and inhibition of ASK1/JNK pathway via glutathione S-transferase regulation,” The Journal of Biological Chemistry, vol. 277, no. 51, pp. 49220–49229, 2002. View at Publisher · View at Google Scholar · View at Scopus
  63. Y. Wu, Y. Fan, B. Xue et al., “Human glutathione S-transferase P1-1 interacts with TRAF2 and regulates TRAF2-ASK1 signals,” Oncogene, vol. 25, no. 42, pp. 5787–5800, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Ishisaki, H. Hayashi, S. Suzuki et al., “Glutathione S-transferase Pi is a dopamine-inducible suppressor of dopamine-induced apoptosis in PC12 cells,” Journal of Neurochemistry, vol. 77, no. 5, pp. 1362–1371, 2001. View at Publisher · View at Google Scholar · View at Scopus
  65. Y. Yang, J. Z. Cheng, S. S. Singhal et al., “Role of glutathione S-transferases in protection against lipid peroxidation: overexpression of hGSTA2-2 in K562 cells protects against hydrogen peroxide-induced apoptosis and inhibits JNK and caspase 3 activation,” The Journal of Biological Chemistry, vol. 276, no. 22, pp. 19220–19230, 2001. View at Publisher · View at Google Scholar · View at Scopus
  66. S. Piaggi, C. Raggi, A. Corti et al., “Glutathione transferase omega 1-1 (GSTO1-1) plays an anti-apoptotic role in cell resistance to cisplatin toxicity,” Carcinogenesis, vol. 31, no. 5, pp. 804–811, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. Z. Yin, V. N. Ivanov, H. Habelhah, K. Tew, and Z. Ronai, “Glutathione S-Transferase p elicits protection against H2O2-induced cell death via coordinated regulation of stress kinases1,” Cancer Research, vol. 60, no. 15, pp. 4053–4057, 2000. View at Google Scholar · View at Scopus
  68. D. M. Townsend, Y. Manevich, L. He, S. Hutchens, C. J. Pazoles, and K. D. Tew, “Novel role for glutathione S-transferase π regulator of protein S-glutathionylation following oxidative and nitrosative stress,” The Journal of Biological Chemistry, vol. 284, no. 1, pp. 436–445, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. L. A. Ralat, Y. Manevich, A. B. Fisher, and R. F. Colman, “Direct evidence for the formation of a complex between 1-cysteine peroxiredoxin and glutathione S-transferase π with activity changes in both enzymes,” Biochemistry, vol. 45, no. 2, pp. 360–372, 2006. View at Publisher · View at Google Scholar · View at Scopus
  70. L. A. Ralat, S. A. Misquitta, Y. Manevich, A. B. Fisher, and R. F. Colman, “Characterization of the complex of glutathione S-transferase pi and 1-cysteine peroxiredoxin,” Archives of Biochemistry and Biophysics, vol. 474, no. 1, pp. 109–118, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. D. R. Richardson and H. C. Lok, “The nitric oxide-iron interplay in mammalian cells: transport and storage of dinitrosyl iron complexes,” Biochimica et Biophysica Acta, vol. 1780, no. 4, pp. 638–651, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. F. De Maria, J. Z. Pedersen, A. M. Caccuri et al., “The specific interaction of dinitrosyl-diglutathionyl-iron complex, a natural NO carrier, with the glutathione transferase superfamily: suggestion for an evolutionary pressure in the direction of the storage of nitric oxide,” The Journal of Biological Chemistry, vol. 278, no. 43, pp. 42283–42293, 2003. View at Publisher · View at Google Scholar · View at Scopus
  73. E. Cesareo, L. J. Parker, J. Z. Pedersen et al., “Nitrosylation of human glutathione transferase P1-1 with dinitrosyl diglutathionyl iron complex in vitro and in vivo,” The Journal of Biological Chemistry, vol. 280, no. 51, pp. 42172–42180, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. H. C. Lok, Y. Suryo Rahmanto, C. L. Hawkins et al., “Nitric oxide storage and transport in cells are mediated by glutathione S-transferase P1-1 and multidrug resistance protein 1 via dinitrosyl iron complexes,” The Journal of Biological Chemistry, vol. 287, no. 1, pp. 607–618, 2012. View at Google Scholar
  75. K. J. Cullen, K. A. Newkirk, L. M. Schumaker, N. Aldosari, J. D. Rone, and B. R. Haddad, “Glutathione S-transferase pi amplification is associated with cisplatin resistance in head and neck squamous cell carcinoma cell lines and primary tumors,” Cancer Research, vol. 63, no. 23, pp. 8097–8102, 2003. View at Google Scholar · View at Scopus
  76. H. A. A. M. Dirven, B. Van Ommen, and P. J. Van Bladeren, “Involvement of human glutathione S-transferase isoenzymes in the conjugation of cyclophosphamide metabolites with glutathione,” Cancer Research, vol. 54, no. 23, pp. 6215–6220, 1994. View at Google Scholar · View at Scopus
  77. C. Peklak-Scott, P. K. Smitherman, A. J. Townsend, and C. S. Morrow, “Role of glutathione S-transferase P1-1 in the cellular detoxification of cisplatin,” Molecular Cancer Therapeutics, vol. 7, no. 10, pp. 3247–3255, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. V. Adler and M. R. Pincus, “Effector peptides from glutathione-S-transferase-pi affect the activation of jun by jun-N-terminal kinase,” Annals of Clinical and Laboratory Science, vol. 34, no. 1, pp. 35–46, 2004. View at Google Scholar · View at Scopus
  79. D. Burg, J. Riepsaame, C. Pont, G. Mulder, and B. Van De Water, “Peptide-bond modified glutathione conjugate analogs modulate GSTπ function in GSH-conjugation, drug sensitivity and JNK signaling,” Biochemical Pharmacology, vol. 71, no. 3, pp. 268–277, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. L. Chie, V. Adler, F. K. Friedman, D. Chung, and M. R. Pincus, “An effector peptide from glutathione-S-transferase-pi strongly and selectively blocks mitotic signaling by oncogenic ras-p21,” Protein Journal, vol. 23, no. 3, pp. 235–238, 2004. View at Publisher · View at Google Scholar · View at Scopus