S-Glutathionylation of Keap1: A new role for glutathione S-transferase pi in neuronal protection

FEBS Letters

Volumn 590, Issue 10, 2016, Pages 1455-1466

  Carvalho, Andreia Neves ^a   Marques, Carla ^b   Guedes, Rita C ^a,c   Castro Caldas, Margarida ^a,d   Rodrigues, Elsa ^a,c   Van Horssen, Jack ^e   Gama, Maria João ^a,c  

^a RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF LISBON   (Portugal)

^d UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^e VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Glutathione S Transferase pi; Nrf2 Keap1 pathway; S glutathionylation

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; GLUTATHIONE TRANSFERASE P1; KELCH LIKE ECH ASSOCIATED PROTEIN 1; TRANSCRIPTION FACTOR NRF2; GLUTATHIONE; GSTP1 PROTEIN, MOUSE; KEAP1 PROTEIN, MOUSE; NFE2L2 PROTEIN, MOUSE; PROTEIN BINDING;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; COMPUTER MODEL; CONTROLLED STUDY; IN VIVO STUDY; MALE; MOUSE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; S GLUTATHIONYLATION; TRANSCRIPTION INITIATION; ANIMAL; BRAIN; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR DOCKING; MOLECULAR MODEL; PHYSIOLOGICAL FEEDBACK;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ANIMALS; BRAIN; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; GLUTATHIONE; GLUTATHIONE S-TRANSFERASE PI; KELCH-LIKE ECH-ASSOCIATED PROTEIN 1; MICE; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PROTEIN BINDING;

EID: 84965157697     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1002/1873-3468.12177     Document Type: Article

References (53)

1. Dauer W, and, Przedborski S, (2003) Parkinson's disease: mechanisms and models. Neuron 39, 889-909.
2. Exner N, Lutz AK, Haass C, and, Winklhofer KF, (2012) Mitochondrial dysfunction in Parkinson's disease: molecular mechanisms and pathophysiological consequences. EMBO J 31, 3038-3062.
3. Jenner P, (2003) Oxidative stress in Parkinson's disease. Ann Neurol 53 (Suppl 3), S26-S36; discussion S36-8.
4. McGeer PL, and, McGeer EG, (2008) Glial reactions in Parkinson's disease. Mov Disord 23, 474-483.
5. Moore DJ, West AB, Dawson VL, and, Dawson TM, (2005) Molecular pathophysiology of Parkinson's disease. Annu Rev Neurosci 28, 57-87.
6. de Vries HE, Witte M, Hondius D, Rozemuller AJ, Drukarch B, Hoozemans J, and, van Horssen J, (2008) Nrf2-induced antioxidant protection: a promising target to counteract ROS-mediated damage in neurodegenerative disease? Free Radic Biol Med 45, 1375-1383.
7. Lee JM, and, Johnson JA, (2004) An important role of Nrf2-ARE pathway in the cellular defense mechanism. J Biochem Mol Biol 37, 139-143.
8. Nguyen T, Nioi P, and, Pickett CB, (2009) The Nrf2-ARE signaling pathway and its activation by oxidative stress. J Biol Chem 284, 13291-13295.
9. Kensler TW, Wakabayashi N, and, Biswal S, (2007) Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47, 89-116.
10. Kobayashi A, Kang MI, Okawa H, Ohtsuji M, Zenke Y, Chiba T, Igarashi K, and, Yamamoto M, (2004) Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol Cell Biol 24, 7130-7139.
11. Kobayashi A, Kang MI, Watai Y, Tong KI, Shibata T, Uchida K, and, Yamamoto M, (2006) Oxidative and electrophilic stresses activate Nrf2 through inhibition of ubiquitination activity of Keap1. Mol Cell Biol 26, 221-229.
12. Hayes JD, Flanagan JU, and, Jowsey IR, (2005) Glutathione transferases. Annu Rev Pharmacol Toxicol 45, 51-88.
13. Ikeda H, Serria MS, Kakizaki I, Hatayama I, Satoh K, Tsuchida S, Muramatsu M, Nishi S, and, Sakai M, (2002) Activation of mouse Pi-class glutathione S-transferase gene by Nrf2(NF-E2-related factor 2) and androgen. Biochem J 364, 563-570.
14. Ketterer B, (2001) A bird's eye view of the glutathione transferase field. Chem Biol Interact 138, 27-42.
15. Baez S, Segura-Aguilar J, Widersten M, Johansson AS, and, Mannervik B, (1997) Glutathione transferases catalyse the detoxication of oxidized metabolites (o-quinones) of catecholamines and may serve as an antioxidant system preventing degenerative cellular processes. Biochem J 324 (Pt 1), 25-28.
16. Tew KD, and, Ronai Z, (1999) GST function in drug and stress response. Drug Resist Updat 2, 143-147.
17. Adler V, Yin Z, Fuchs SY, Benezra M, Rosario L, Tew KD, Pincus MR, Sardana M, Henderson CJ, Wolf CR, et al,. (1999) Regulation of JNK signaling by GSTp. EMBO J 18, 1321-1334.
18. Castro-Caldas M, Carvalho AN, Rodrigues E, Henderson C, Wolf CR, and, Gama MJ, (2012) Glutathione S-transferase pi mediates MPTP-induced c-Jun N-terminal kinase activation in the nigrostriatal pathway. Mol Neurobiol 45, 466-477.
19. Elsby R, Kitteringham NR, Goldring CE, Lovatt CA, Chamberlain M, Henderson CJ, Wolf CR, and, Park BK, (2003) Increased constitutive c-Jun N-terminal kinase signaling in mice lacking glutathione S-transferase Pi. J Biol Chem 278, 22243-22249.
20. Wang T, Arifoglu P, Ronai Z, and, Tew KD, (2001) Glutathione S-transferase P1-1 (GSTP1-1) inhibits c-Jun N-terminal kinase (JNK1) signaling through interaction with the C terminus. J Biol Chem 276, 20999-21003.
21. Klatt P, and, Lamas S, (2000) Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur J Biochem 267, 4928-4944.
22. Manevich Y, Feinstein SI, and, Fisher AB, (2004) Activation of the antioxidant enzyme 1-CYS peroxiredoxin requires glutathionylation mediated by heterodimerization with pi GST. Proc Natl Acad Sci USA 101, 3780-3785.
23. Tew KD, (2007) Redox in redux: emergent roles for glutathione S-transferase P (GSTP) in regulation of cell signaling and S-glutathionylation. Biochem Pharmacol 73, 1257-1269.
24. Townsend DM, Manevich Y, He L, Hutchens S, Pazoles CJ, and, Tew KD, (2009) Novel role for glutathione S-transferase pi. Regulator of protein S-Glutathionylation following oxidative and nitrosative stress. J Biol Chem 284, 436-445.
25. Wetzelberger K, Baba SP, Thirunavukkarasu M, Ho YS, Maulik N, Barski OA, Conklin DJ, and, Bhatnagar A, (2010) Postischemic deactivation of cardiac aldose reductase: role of glutathione S-transferase P and glutaredoxin in regeneration of reduced thiols from sulfenic acids. J Biol Chem 285, 26135-26148.
26. Dalle-Donne I, Milzani A, Gagliano N, Colombo R, Giustarini D, and, Rossi R, (2008) Molecular mechanisms and potential clinical significance of S-glutathionylation. Antioxid Redox Signal 10, 445-473.
27. Townsend DM, (2007) S-glutathionylation: indicator of cell stress and regulator of the unfolded protein response. Mol Interv 7, 313-324.
28. Zhang X, Zhao X, and, Ma Z, (2010) PYDDT, a novel phase 2 enzymes inducer, activates Keap1-Nrf2 pathway via depleting the cellular level of glutathione. Toxicol Lett 199, 93-101.
29. Dinkova-Kostova AT, Holtzclaw WD, Cole RN, Itoh K, Wakabayashi N, Katoh Y, Yamamoto M, and, Talalay P, (2002) Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc Natl Acad Sci USA 99, 11908-11913.
30. Rachakonda G, Xiong Y, Sekhar KR, Stamer SL, Liebler DC, and, Freeman ML, (2008) Covalent modification at Cys151 dissociates the electrophile sensor Keap1 from the ubiquitin ligase CUL3. Chem Res Toxicol 21, 705-710.
31. Gambhir L, Checker R, Thoh M, Patwardhan RS, Sharma D, Kumar M, and, Sandur SK, (2014) 1,4-Naphthoquinone, a pro-oxidant, suppresses immune responses via KEAP-1 glutathionylation. Biochem Pharmacol 88, 95-105.
32. Castro-Caldas M, Neves Carvalho A, Peixeiro I, Rodrigues E, Lechner MC, and, Gama MJ, (2009) GSTpi expression in MPTP-induced dopaminergic neurodegeneration of C57BL/6 mouse midbrain and striatum. J Mol Neurosci 38, 114-127.
33. Carvalho AN, Marques C, Rodrigues E, Henderson CJ, Wolf CR, Pereira P, and, Gama MJ, (2013) Ubiquitin-proteasome system impairment and MPTP-induced oxidative stress in the brain of C57BL/6 wild-type and GSTP knockout mice. Mol Neurobiol 47, 662-672.
34. Henderson CJ, Smith AG, Ure J, Brown K, Bacon EJ, and, Wolf CR, (1998) Increased skin tumorigenesis in mice lacking pi class glutathione S-transferases. Proc Natl Acad Sci USA 95, 5275-5280.
35. Szasz G, (1974) New substrates for measuring gamma-glutamyl transpeptidase activity. Z Klin Chem Klin Biochem 12, 228.
36. Levrand S, Pesse B, Feihl F, Waeber B, Pacher P, Rolli J, Schaller MD, and, Liaudet L, (2005) Peroxynitrite is a potent inhibitor of NF-{kappa}B activation triggered by inflammatory stimuli in cardiac and endothelial cell lines. J Biol Chem 280, 34878-34887.
37. Jones G, Willett P, Glen RC, Leach AR, and, Taylor R, (1997) Development and validation of a genetic algorithm for flexible docking. J Mol Biol 267, 727-748.
38. Lo SC, Li X, Henzl MT, Beamer LJ, and, Hannink M, (2006) Structure of the Keap1:Nrf2 interface provides mechanistic insight into Nrf2 signaling. EMBO J 25, 3605-3617.
39. Przedborski S, Tieu K, Perier C, and, Vila M, (2004) MPTP as a mitochondrial neurotoxic model of Parkinson's disease. J Bioenerg Biomembr 36, 375-379.
40. Saporito MS, Brown EM, Miller MS, and, Carswell S, (1999) CEP-1347/KT-7515, an inhibitor of c-jun N-terminal kinase activation, attenuates the 1-methyl-4-phenyl tetrahydropyridine-mediated loss of nigrostriatal dopaminergic neurons In vivo. J Pharmacol Exp Ther 288, 421-427.
41. Sian J, Dexter DT, Lees AJ, Daniel S, Agid Y, Javoy-Agid F, Jenner P, and, Marsden CD, (1994) Alterations in glutathione levels in Parkinson's disease and other neurodegenerative disorders affecting basal ganglia. Ann Neurol 36, 348-355.
42. Sian J, Dexter DT, Lees AJ, Daniel S, Jenner P, and, Marsden CD, (1994) Glutathione-related enzymes in brain in Parkinson's disease. Ann Neurol 36, 356-361.
43. Ghezzi P, Bonetto V, and, Fratelli M, (2005) Thiol-disulfide balance: from the concept of oxidative stress to that of redox regulation. Antioxid Redox Signal 7, 964-972.
44. Maher P, (2006) Redox control of neural function: background, mechanisms, and significance. Antioxid Redox Signal 8, 1941-1970.
45. Barker JE, Heales SJ, Cassidy A, Bolanos JP, Land JM, and, Clark JB, (1996) Depletion of brain glutathione results in a decrease of glutathione reductase activity; an enzyme susceptible to oxidative damage. Brain Res 716, 118-122.
46. Circu ML, Stringer S, Rhoads CA, Moyer MP, and, Aw TY, (2009) The role of GSH efflux in staurosporine-induced apoptosis in colonic epithelial cells. Biochem Pharmacol 77, 76-85.
47. Franco R, and, Cidlowski JA, (2012) Glutathione efflux and cell death. Antioxid Redox Signal 17, 1694-1713.
48. Dringen R, and, Hirrlinger J, (2003) Glutathione pathways in the brain. Biol Chem 384, 505-516.
49. Ghezzi P, (2005) Regulation of protein function by glutathionylation. Free Radic Res 39, 573-580.
50. Mieyal JJ, Gallogly MM, Qanungo S, Sabens EA, and, Shelton MD, (2008) Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxid Redox Signal 10, 1941-1988.
51. Burton NC, Kensler TW, and, Guilarte TR, (2006) In vivo modulation of the Parkinsonian phenotype by Nrf2. Neurotoxicology 27, 1094-1100.
52. Chen PC, Vargas MR, Pani AK, Smeyne RJ, Johnson DA, Kan YW, and, Johnson JA, (2009) Nrf2-mediated neuroprotection in the MPTP mouse model of Parkinson's disease: critical role for the astrocyte. Proc Natl Acad Sci USA 106, 2933-2938.
53. Jazwa A, Rojo AI, Innamorato NG, Hesse M, Fernandez-Ruiz J, and, Cuadrado A, (2011) Pharmacological targeting of the transcription factor Nrf2 at the basal ganglia provides disease modifying therapy for experimental parkinsonism. Antioxid Redox Signal 14, 2347-2360.