Sulfiredoxin-1 Attenuates Oxidative Stress via Nrf2/ARE Pathway and 2-Cys Prdxs After Oxygen-Glucose Deprivation in Astrocytes

Journal of Molecular Neuroscience

Volumn 55, Issue 4, 2015, Pages 941-950

  Zhou, Yang ^a   Duan, Song ^a   Zhou, Yunchuan ^a   Yu, Shanshan ^a   Wu, Jingxian ^a   Wu, Xiaoying ^a   Zhao, Jing ^a   Zhao, Yong ^a  

^a CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

2 Cys Prdxs; Astrocytes; Nrf2 ARE pathway; OGD; Oxidative stress; Sulfiredoxin 1

Indexed keywords

ANTIOXIDANT; CYSTEINE; GLUCOSE; GLUTATHIONE; LACTATE DEHYDROGENASE; OXYGEN; PEROXIREDOXIN 3; SULFIREDOXIN 1; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; GA BINDING PROTEIN; OXIDOREDUCTASE; PEROXIREDOXIN; SRXN1 PROTEIN, RAT; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; ASTROCYTE; BINDING SITE; BRAIN ISCHEMIA; CELL DAMAGE; CELL PROLIFERATION ASSAY; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; GEL MOBILITY SHIFT ASSAY; GENE SILENCING; GENETIC TRANSFECTION; HYPOXIA; IMMUNOBLOTTING; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; OXYGEN GLUCOSE DEPRIVATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REPERFUSION INJURY; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CELL HYPOXIA; DEFICIENCY; GENETICS; METABOLISM; WISTAR RAT;

ANIMALS; ANTIOXIDANT RESPONSE ELEMENTS; ASTROCYTES; CELL HYPOXIA; GA-BINDING PROTEIN TRANSCRIPTION FACTOR; GLUCOSE; GLUTATHIONE; OXIDATIVE STRESS; OXIDOREDUCTASES ACTING ON SULFUR GROUP DONORS; OXYGEN; PEROXIREDOXINS; RATS; RATS, WISTAR; SUPEROXIDE DISMUTASE;

EID: 84925541204     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-014-0449-6     Document Type: Article

References (57)

1. Alfieri A, Srivastava S, Siow RC, Modo M, Fraser PA, Mann GE (2011) Targeting the Nrf2-Keap1 antioxidant defence pathway for neurovascular protection in stroke. J Physiol 589:4125–4136
2. Bae SH, Sung SH, Lee HE, Kang HT, Lee SK, Oh SY, Woo HA, Kil IS, Rhee SG (2012) Peroxiredoxin III and sulfiredoxin together protect mice from pyrazole-induced oxidative liver injury. Antioxid Redox Signal 17:1351–1361
3. Baek JY, Han SH, Sung SH, Lee HE, Y-m K, Noh YH, Bae SH, Rhee SG, Chang T-S (2012) Sulfiredoxin protein is critical for redox balance and survival of cells exposed to low steady-state levels of H2O2. J Biol Chem 287:81–89
4. Barreto G, White RE, Ouyang Y, Xu L, Giffard RG (2011) Astrocytes: targets for neuroprotection in stroke. Cent Nerv Syst Agents Med Chem 11:164–173
5. Biteau B, Labarre J, Toledano MB (2003) ATP-dependent reduction of cysteine–sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425:980–984
6. Blackwood EM, Kadonaga JT (1998) Going the distance: a current view of enhancer action. Science 281:60–63
7. Botia B, Seyer D, Ravni A, Benard M, Falluel-Morel A, Cosette P, Jouenne T, Fournier A, Vaudry H, Gonzalez BJ, Vaudry D (2008) Peroxiredoxin 2 is involved in the neuroprotective effects of PACAP in cultured cerebellar granule neurons. J Mol Neurosci 36:61–72
8. Bruno V, Goldberg M, Dugan L, Giffard R, Choi D (1994) Neuroprotective effect of hypothermia in cortical cultures exposed to oxygen‐glucose deprivation or excitatory amino acids. J Neurochem 63:1398–1406
9. Calkins MJ, Jakel RJ, Johnson DA, Chan K, Kan YW, Johnson JA (2005) Protection from mitochondrial complex II inhibition in vitro and in vivo by Nrf2-mediated transcription. Proc Natl Acad Sci U S A 102:244–249
10. Chang T-S, Jeong W, Woo HA, Lee SM, Park S, Rhee SG (2004) Characterization of mammalian sulfiredoxin and its reactivation of hyperoxidized peroxiredoxin through reduction of cysteine sulfinic acid in the active site to cysteine. J Biol Chem 279:50994–51001
11. Coyle JT, Puttfarcken P (1993) Oxidative stress, glutamate, and neurodegenerative disorders. Science 262:689–695
12. Cullinan SB, Gordan JD, Jin J, Harper JW, Diehl JA (2004) The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase. Mol Cell Biol 24:8477–8486
13. Danbolt NC (1994) The high affinity uptake system for excitatory amino acids in the brain. Prog Neurobiol 44:377–396
14. Fang J, Nakamura T, Cho D-H, Gu Z, Lipton SA (2007) S-nitrosylation of peroxiredoxin 2 promotes oxidative stress-induced neuronal cell death in Parkinson’s disease. Proc Natl Acad Sci 104:18742–18747
15. Favreau L, Pickett C (1991) Transcriptional regulation of the rat NAD (P) H: quinone reductase gene. Identification of regulatory elements controlling basal level expression and inducible expression by planar aromatic compounds and phenolic antioxidants. J Biol Chem 266:4556–4561
16. Friling RS, Bergelson S, Daniel V (1992) Two adjacent AP-1-like binding sites form the electrophile-responsive element of the murine glutathione S-transferase Ya subunit gene. Proc Natl Acad Sci 89:668–672
17. Goldberg MP, Choi DW (1993) Combined oxygen and glucose deprivation in cortical cell culture: calcium-dependent and calcium-independent mechanisms of neuronal injury. J Neurosci 13:3510–3524
18. Halliwell B (1992). Reactive oxygen species and the central nervous system. Free Radicals in the Brain, Springer: 21–40.
19. Hattori F and Oikawa S (2007). Peroxiredoxins in the central nervous system. Peroxiredoxin Systems, Springer: 357–374.
20. Heneka MT, Rodriguez JJ, Verkhratsky A (2010) Neuroglia in neurodegeneration. Brain Res Rev 63:189–211
21. Hu J, Castets F, Guevara JL, Van Eldik LJ (1996) S100 beta stimulates inducible nitric oxide synthase activity and mRNA levels in rat cortical astrocytes. J Biol Chem 271:2543–2547
22. Inamdar NM, Ahn YI, Alam J (1996) The heme-responsive element of the mouse heme oxygenase-1 gene is an extended AP-1 binding site that resembles the recognition sequences for MAF and NF-E2 transcription factors. Biochem Biophys Res Commun 221:570–576
23. Jakel RJ, Townsend JA, Kraft AD, Johnson JA (2007) Nrf2-mediated protection against 6-hydroxydopamine. Brain Res 1144:192–201
24. Jing X, Ren D, Wei X, Shi H, Zhang X, Perez RG, Lou H and Lou H (2013) Eriodictyol-7-O- glucoside activates Nrf2 and protects against cerebral ischemic injury. Toxicol Appl Pharmacol
25. Johnson DA, Andrews GK, Xu W, Johnson JA (2002) Activation of the antioxidant response element in primary cortical neuronal cultures derived from transgenic reporter mice. J Neurochem 81:1233–1241
26. Jowsey IR, Jiang Q, Itoh K, Yamamoto M, Hayes JD (2003) Expression of the aflatoxin B1-8, 9-epoxide-metabolizing murine glutathione S-transferase A3 subunit is regulated by the Nrf2 transcription factor through an antioxidant response element. Mol Pharmacol 64:1018–1028
27. Kim Y-J, Ahn J-Y, Liang P, Ip C, Zhang Y, Park Y-M (2007) Human prx1 gene is a target of Nrf2 and is up-regulated by hypoxia/reoxygenation: implication to tumor biology. Cancer Res 67:546–554
28. Knoops B, Goemaere J, Van der Eecken V, Declercq J-P (2011) Peroxiredoxin 5: structure, mechanism, and function of the mammalian atypical 2-Cys peroxiredoxin. Antioxid Redox Signal 15:817–829
29. Kraft AD, Johnson DA, Johnson JA (2004) Nuclear factor E2-related factor 2-dependent antioxidant response element activation by tert-butylhydroquinone and sulforaphane occurring preferentially in astrocytes conditions neurons against oxidative insult. J Neurosci 24:1101–1112
30. Lee JM, Calkins MJ, Chan K, Kan YW, Johnson JA (2003) Identification of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis. J Biol Chem 278:12029–12038
31. Li Q, Yu S, Wu J, Zou Y, Zhao Y (2013) Sulfiredoxin-1 protects PC12 cells against oxidative stress induced by hydrogen peroxide. J Neurosci Res 91:861–870
32. Lipton P (1999) Ischemic cell death in brain neurons. Physiol Rev 79:1431–1568
33. −ΔΔCT method. Methods 25:402–408
34. Mulcahy RT, Wartman MA, Bailey HH, Gipp JJ (1997) Constitutive and beta-naphthoflavone-induced expression of the human gamma-glutamylcysteine synthetase heavy subunit gene is regulated by a distal antioxidant response element/TRE sequence. J Biol Chem 272:7445–7454
35. Nguyen T, Sherratt PJ, Pickett CB (2003) Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol 43:233–260
36. Nioi P, McMahon M, Itoh K, Yamamoto M, Hayes J (2003) Identification of a novel Nrf2-regulated antioxidant response element (ARE) in the mouse NAD (P) H: quinone oxidoreductase 1 gene: reassessment of the ARE consensus sequence. Biochem J 374:337–348
37. Olanow C (1993) A radical hypothesis for neurodegeneration. Trends Neurosci 16:439–444
38. Parpura V, Heneka MT, Montana V, Oliet SH, Schousboe A, Haydon PG, Stout RF Jr, Spray DC, Reichenbach A, Pannicke T, Pekny M, Pekna M, Zorec R, Verkhratsky A (2012) Glial cells in (patho) physiology. J Neurochem 121:4–27
39. Poole LB, Nelson KJ (2008) Discovering mechanisms of signaling-mediated cysteine oxidation. Curr Opin Chem Biol 12:18–24
40. Rhee SG, Woo HA (2011) Multiple functions of peroxiredoxins: peroxidases, sensors and regulators of the intracellular messenger H2O2, and protein chaperones. Antioxid Redox Signal 15:781–794
41. Rhee SG, Kang SW, Jeong W, Chang TS, Yang KS, Woo HA (2005) Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr Opin Cell Biol 17:183–189
42. Rhee S, Jeong W, Chang T, Woo H (2007) Sulfiredoxin, the cysteine sulfinic acid reductase specific to 2-Cys peroxiredoxin: its discovery, mechanism of action, and biological significance. Kidney Int 72:S3–S8
43. Rushmore TH, King RG, Paulson KE, Pickett CB (1990) Regulation of glutathione S-transferase Ya subunit gene expression: identification of a unique xenobiotic-responsive element controlling inducible expression by planar aromatic compounds. Proc Natl Acad Sci 87:3826–3830
44. Shih AY, Johnson DA, Wong G, Kraft AD, Jiang L, Erb H, Johnson JA, Murphy TH (2003) Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress. J Neurosci 23:3394–3406
45. Singh A, Rangasamy T, Thimmulappa RK, Lee H, Osburn WO, Brigelius-Flohé R, Kensler TW, Yamamoto M, Biswal S (2006) Glutathione peroxidase 2, the major cigarette smoke-inducible isoform of GPX in lungs, is regulated by Nrf2. Am J Respir Cell Mol Biol 35:639
46. Smith-Pearson PS, Kooshki M, Spitz DR, Poole LB, Zhao W, Robbins ME (2008) Decreasing peroxiredoxin II expression decreases glutathione, alters cell cycle distribution, and sensitizes glioma cells to ionizing radiation and H2O2. Free Radic Biol Med 45:1178–1189
47. Son TG, Camandola S, Arumugam TV, Cutler RG, Telljohann RS, Mughal MR, Moore TA, Luo W, Yu QS, Johnson DA, Johnson JA, Greig NH, Mattson MP (2010) Plumbagin, a novel Nrf2/ARE activator, protects against cerebral ischemia. J Neurochem 112:1316–1326
48. Soriano FX, Léveillé F, Papadia S, Higgins LG, Varley J, Baxter P, Hayes JD, Hardingham GE (2008) Induction of sulfiredoxin expression and reduction of peroxiredoxin hyperoxidation by the neuroprotective Nrf2 activator 3H‐1, 2‐dithiole‐3‐thione. J Neurochem 107:533–543
49. Swanson RA, Ying W, Kauppinen TM (2004) Astrocyte influences on ischemic neuronal death. Curr Mol Med 4:193–205
50. Tavender T, Sheppard A, Bulleid N (2008) Peroxiredoxin IV is an endoplasmic reticulum-localized enzyme forming oligomeric complexes in human cells. Biochem J 411:191–199
51. Tsuji Y, Ayaki H, Whitman SP, Morrow CS, Torti SV, Torti FM (2000) Coordinate transcriptional and translational regulation of ferritin in response to oxidative stress. Mol Cell Biol 20:5818–5827
52. Wasserman WW, Fahl WE (1997) Comprehensive analysis of proteins which interact with the antioxidant responsive element: correlation of ARE-BP-1 with the chemoprotective induction response. Arch Biochem Biophys 344:387–396
53. Winyard PG, Moody CJ, Jacob C (2005) Oxidative activation of antioxidant defence. Trends Biochem Sci 30:453–461
54. Woo HA, Jeong W, Chang TS, Park KJ, Park SJ, Yang JS, Rhee SG (2005) Reduction of cysteine sulfinic acid by sulfiredoxin is specific to 2-cys peroxiredoxins. J Biol Chem 280:3125–3128
55. Wood ZA, Schröder E, Robin Harris J, Poole LB (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 28:32–40
56. Yu AC, Liu RY, Zhang Y, Sun HR, Qin LY, Lau LT, Wu BY, Hui HK, Heung MY, Han JS (2007) Glial cell line-derived neurotrophic factor protects astrocytes from staurosporine- and ischemia-induced apoptosis. J Neurosci Res 85:3457–3464
57. Zimmerman BJ, Grisham MB, Granger DN (1990) Role of oxidants in ischemia/reperfusion-induced granulocyte infiltration. Am J Physiol Gastrointest Liver Physiol 258:G185–G190