Expression of Nrf2 and its downstream gene targets in hibernating 13-lined ground squirrels, Spermophilus tridecemlineatus

Molecular and Cellular Biochemistry

Volumn 312, Issue 1-2, 2008, Pages 121-129

  Pier Jr , Morin ^a   Ni, Zhouli ^a   McMullen, David C ^a   Storey, Kenneth B ^a  

^a CARLETON UNIVERSITY   (Canada)

Author keywords

Aflatoxin aldehyde reductase; Antioxidant defense; Heart; Heme oxygenase; Ischemia resistance; NF E2 related factor 2; Oxidative stress; Superoxide dismutase; Torpor arousalcycle

Indexed keywords

AFLATOXIN ALDEHYDE; ALDEHYDE; COMPLEMENTARY DNA; COPPER ZINC SUPEROXIDE DISMUTASE; HEME OXYGENASE 1; MESSENGER RNA; PROLINE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BODY TEMPERATURE; COMPARATIVE GENE MAPPING; CONTROLLED STUDY; GENE EXPRESSION; GENE TARGETING; HEART; HIBERNATION; HUMAN; IMMUNOBLOTTING; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; REGULATORY MECHANISM; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SLEEP WAKING CYCLE; SPECIES DIFFERENCE; SQUIRREL;

AMINO ACID SEQUENCE; ANIMALS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION; HEART; HIBERNATION; MOLECULAR SEQUENCE DATA; MYOCARDIUM; NF-E2-RELATED FACTOR 2; SCIURIDAE; SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA; MAMMALIA; SCIURIDAE; SPERMOPHILUS; SPERMOPHILUS TRIDECEMLINEATUS;

EID: 42149160644     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-008-9727-3     Document Type: Article

References (41)

1. Wang LCH, Lee TF (1996) Torpor and hibernation in mammals: Metabolic, physiological and biochemical adaptations. In: Fregley MJ, Blatteis CM (eds) Handbook of physiology: Environmental physiology. Oxford University Press, Oxford, pp 507-532
2. Storey KB (2003) Mammalian hibernation: Transcriptional and translational controls. Adv Exp Med Biol 543:21-38
3. Storey KB, Storey JM (2007) Putting life on 'pause' - molecular regulation of hypometabolism. J Exp Biol 210:1700-1714
4. Ma YL, Zhu X, Rivera PM, Tøien Ø, Barnes BM, LaManna JC, Smith MA, Drew KL (2005) Absence of cellular stress in brain after hypoxia induced by arousal from hibernation in Arctic ground squirrels. Am J Physiol 289:R1297-R1306
5. Lee YJ, Hallenbeck JM (2006) Insights into cytoprotection from ground squirrel hibernation, a natural model of tolerance to profound brain oligaemia. Biochem Soc Trans 34:1295-1298
6. Frank CL (1992) The influence of dietary fatty acids on hibernation by golden-mantled ground squirrels (Spermophilus lateralis). Physiol Zool 65:906-920
7. Gunstone FD (1996) Fatty acid and lipid chemistry. Aspen Publishers, Maryland
8. Stewart D, Killeen E, Naquin R, Alam S, Alam J (2003) Degradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmium. J Biol Chem 278:2396-2402
9. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, Yamamoto M (1999) Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 13:76-86
10. Venugopal R, Jaiswal AK (1996) Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:qUinone oxidoreductase1 gene. Proc Natl Acad Sci USA 93:14960-14965
11. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I, Yamamoto M, Nabeshima YI (1997) An Nrf2/ small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Comm 236:313-322
12. He CH, Gong P, Hu B, Stewart D, Choi ME, Choi AM, Alam J (2001) Identification of activating transcription factor 4 (ATF4) as an Nrf2-interacting protein. Implication for heme oxygenase-1 gene regulation. J Biol Chem 276:20858-20865
13. Kim IC, Masutani H, Yamaguchi Y, Itoh K, Yamamoto M, Yodoi J (2001) Hemin-induced activation of the thioredoxin gene by Nrf2. A differential regulation of the antioxidant responsive element by a switch of its binding factors. J Biol Chem 276:18399-18406
14. Chanas SA, Jiang Q, McMahon M, McWalter GK, McLellan LI, Elcombe CR, Henderson CJ, Wolf CR, Moffat GJ, Itoh K, Yamamoto M, Hayes JD (2002) Loss of the Nrf2 transcription factor causes a marked reduction in constitutive and inducible expression of the glutathione S-transferase Gsta1, Gsta2, Gstm1, Gstm2, Gstm3 and Gstm4 genes in the livers of male and female mice. Biochem J 365:405-416
15. Park EY, Rho HM (2002) The transcriptional activation of the human copper/zinc superoxide dismutase gene by 2,3,7,8-tetrachlorodibenzo-p-dioxin through two different regulator sites, the antioxidant responsive element and xenobiotic responsive element. Mol Cell Biochem 240:47-55
16. Alam J, Stewart D, Touchard C, Boinapally S, Choi AMK, Cook JL (1999) Nrf2, a cap'n'collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 274:26071-26078
17. Ellis EM, Hayes JD (1995) Substrate specificity of an aflatoxin-metabolizing aldehyde reductase. Biochem J 312:535-541
18. Ellis EM, Slattery CM, Hayes JD (2003) Characterization of the rat aflatoxin B1 aldehyde reductase gene, AKR7A1. Structure and chromosomal localization of AKR7A1 as well as identification of antioxidant response elements in the gene promoter. Carcinogenesis 24:727-737
19. Lee YJ, Miyake SI, Wakita H, McMullen DC, Azuma Y, Auh S, Hallenbeck JM (2006) Protein SUMOylation is massively increased in hibernation torpor and is critical for the cytoprotection provided by ischemic preconditioning and hypothermia in SHSY5Y cells. J Cereb Blood Flow Metabol 27:950-962
20. Morin P Jr, Storey KB (2005) Cloning and expression of hypoxia-inducible factor 1α from the hibernating ground squirrel, Spermophilus tridecemlineatus. Biochim Biophys Acta 1729:32-40
21. Carey HV, Frank CL, Seifert JP (2000) Hibernation induces oxidative stress and activation of NK-kappaB in ground squirrel intestine. J Comp Physiol B 170:551-559
22. +-ATPase in the red blood cells of the hibernating black bear. Life Sci 71:153-161
23. Buzadzic B, Spasic M, Saicic ZS, Radojicic R, Petrovic VM, Halliwell B (1990) Antioxidant defenses in the ground squirrel Citellus citellus. 2. The effect of hibernation. Free Radic Biol Med 9:407-413
24. Eddy SF, McNally JD, Storey KB (2005) Up-regulation of a thioredoxin peroxidase-like protein, proliferation associated gene, in hibernating bats. Arch Biochem Biophys 435:101-111
25. Morin P Jr, Storey KB (2007) Antioxidant defense in hibernation: Cloning and expression of peroxiredoxins from hibernating ground squirrels, Spermophilus tridecemlineatus. Arch Biochem Biophys 461:59-65
26. Ohta H, Okamoto I, Hanaya T, Arai S, Ohta T, Fukuda S (2006) Enhanced antioxidant defense due to extracellular catalase activity in Syrian hamster during arousal from hibernation. Comp Biochem Physiol C 143:484-491
27. Okamoto I, Kayano T, Hanaya T, Arai S, Ikeda M, Kurimoto M (2006) Up-regulation of an extracellular superoxide dismutase-like activity in hibernating hamsters subjected to oxidative stress in mid- to late arousal from torpor. Comp Biochem Physiol C 144:47-56
28. Drew KL, Toien O, Rivera PM, Smith MA, Perry G, Rice ME (2002) Role of the antioxidant ascorbate in hibernation and warming from hibernation. Comp Biochem Physiol C 133:483-492
29. Osborne PG, Hashimoto M (2006) Brain antioxidant levels in hamsters during hibernation, arousal and cenothermia. Behav Brain Res 168:208-214
30. Chan K, Kan YW (1999) Nrf2 is essential for protection against acute pulmonary injury in mice. Proc Natl Acad Sci USA 96:12731-12736
31. Cho HY, Jedlicka AE, Reddy SP, Kensler TW, Yamamoto M, Zhang LY, Kleeberger SR (2002) Role of NRF2 in protection against hyperoxic lung injury in mice. Am J Respir Cell Mol Biol 26:175-182
32. Katoh Y, Itoh K, Yoshida E, Miyagishi M, Fukamizu A, Yamamoto M (2001) Two domains of Nrf2 cooperatively bind CBP, a CREB binding protein, and synergistically activate transcription. Genes Cells 6:857-868
33. Shen G, Hebbar V, Nair S, Xu C, Li W, Lin W, Keum YS, Han J, Gallo MA, Kong AN (2004) Regulation of Nrf2 transactivation domain activity. The differential effects of mitogen-activated protein kinase cascades and synergistic stimulatory effect of Raf and CREB-binding protein. J Biol Chem 279:23052-23060
34. Papaiahgari S, Kleeberger SR, Cho HY, Kalvakolanu DV, Reddy SP (2004) NADPH oxidase and ERK signaling regulates hyperoxia-induced Nrf2-ARE transcriptional response in pulmonary epithelial cells. J Biol Chem 279:42302-42312
35. Pi J, Qu W, Reece JM, Kumagai Y, Waalkes MP (2003) Transcription factor Nrf2 activation by inorganic arsenic in cultured keratinocytes: involvement of hydrogen peroxide. Exp Cell Res 290:234-245
36. Qiang W, Cahill JM, Liu J, Kuang X, Liu N, Scofield VL, Voorhees JR, Reid AJ, Yan M, Lynn WS, Wong PK (2004) Activation of transcription factor Nrf-2 and its downstream targets in response to moloney murine leukemia virus ts1-induced thiol depletion and oxidative stress in astrocytes. J Virol 78:11926-11938
37. Tenhunen R, Marver HS, Schmid R (1968) The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 61:748-755
38. Lee PJ, Jiang BH, Chin BY, Iyer NV, Alam J, Semenza GL, Choi AMK (1997) Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J Biol Chem 272:5375-5381
39. Wang P, Chen H, Qin H, Sankarapandi S, Becher MW, Wong PC, Zweier JL (1998) Overexpression of human copper,zinc-superoxide dismutase (SOD1) prevents postischemic injury. Proc Natl Acad Sci USA 95:4556-4560
40. Hermes-Lima M, Storey JM, Storey KB (1998) Antioxidant defenses and metabolic depression. The hypothesis of preparation for oxidative stress in land snails. Comp Biochem Physiol B Biochem Mol Biol 120:437-448
41. Kim YJ, Ahn JY, Liang P, Ip C, Zhang Y, Park YM (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