Oxr1 is essential for protection against oxidative stress-induced neurodegeneration

PLoS Genetics

Volumn 7, Issue 10, 2011, Pages

  Oliver, Peter L ^a   Finelli, Mattéa J ^a   Edwards, Benjamin ^a   Bitoun, Emmanuelle ^a   Butts, Darcy L ^a   Becker, Esther B E ^a   Cheeseman, Michael T ^b   Davies, Ben ^c   Davies, Kay E ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MEDICAL RESEARCH COUNCIL   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; ISOPROTEIN; NERVE PROTEIN; OXIDATION RESISTANCE 1 PROTEIN; PEROXIDE; UNCLASSIFIED DRUG; NEUROPEPTIDE RECEPTOR; OX1 PROTEIN, MOUSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CEREBELLUM DEGENERATION; CONTROLLED STUDY; DNA DAMAGE; ESSENTIAL GENE; GENE DELETION; GENE FUNCTION; GENE OVEREXPRESSION; GENE STRUCTURE; GENETIC ASSOCIATION; GRANULE CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION RESISTANCE 1 GENE; OXIDATIVE STRESS; PHENOTYPE; PROTEIN FUNCTION; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; C3H MOUSE; CEREBELLUM; DEGENERATIVE DISEASE; DISEASE MODEL; GENETICS; HUMAN; METABOLISM; MOUSE MUTANT; PATHOLOGY;

MUS;

ANIMALS; CEREBELLUM; CYSTEINE; DISEASE MODELS, ANIMAL; HUMANS; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, MUTANT STRAINS; NEURODEGENERATIVE DISEASES; NEURONS; OXIDATIVE STRESS; RECEPTORS, NEUROPEPTIDE; SEQUENCE DELETION;

EID: 80055074330     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002338     Document Type: Article

References (50)

1. Ott M, Gogvadze V, Orrenius S, Zhivotovsky B, (2007) Mitochondria, oxidative stress and cell death. Apoptosis 12: 913-922.
2. Calabrese V, Cornelius C, Mancuso C, Pennisi G, Calafato S, et al. (2008) Cellular stress response: a novel target for chemoprevention and nutritional neuroprotection in aging, neurodegenerative disorders and longevity. Neurochem Res 33: 2444-2471.
3. Fernandez-Checa JC, Fernandez A, Morales A, Mari M, Garcia-Ruiz C, et al. (2010) Oxidative stress and altered mitochondrial function in neurodegenerative diseases: lessons from mouse models. CNS Neurol Disord Drug Targets 9: 439-454.
4. Yant LJ, Ran Q, Rao L, Van Remmen H, Shibatani T, et al. (2003) The selenoprotein GPX4 is essential for mouse development and protects from radiation and oxidative damage insults. Free Radic Biol Med 34: 496-502.
5. Nonn L, Williams RR, Erickson RP, Powis G, (2003) The absence of mitochondrial thioredoxin 2 causes massive apoptosis, exencephaly, and early embryonic lethality in homozygous mice. Mol Cell Biol 23: 916-922.
6. Lebovitz RM, Zhang H, Vogel H, Cartwright J Jr, Dionne L, et al. (1996) Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc Natl Acad Sci U S A 93: 9782-9787.
7. DiMauro S, Schon EA, (2008) Mitochondrial disorders in the nervous system. Annu Rev Neurosci 31: 91-123.
8. Lin MT, Beal MF, (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443: 787-795.
9. Chong ZZ, Li F, Maiese K, (2005) Oxidative stress in the brain: novel cellular targets that govern survival during neurodegenerative disease. Prog Neurobiol 75: 207-246.
10. Andersen JK, (2004) Oxidative stress in neurodegeneration: cause or consequence? Nat Med 10 (Suppl): S18-25.
11. Moreira PI, Zhu X, Wang X, Lee HG, Nunomura A, et al. (2010) Mitochondria: a therapeutic target in neurodegeneration. Biochim Biophys Acta 1802: 212-220.
12. Volkert MR, Elliott NA, Housman DE, (2000) Functional genomics reveals a family of eukaryotic oxidation protection genes. Proc Natl Acad Sci U S A 97: 14530-14535.
13. Elliott NA, Volkert MR, (2004) Stress induction and mitochondrial localization of Oxr1 proteins in yeast and humans. Mol Cell Biol 24: 3180-3187.
14. Durand M, Kolpak A, Farrell T, Elliott NA, Shao W, et al. (2007) The OXR domain defines a conserved family of eukaryotic oxidation resistance proteins. BMC Cell Biol 8: 13.
15. Shkolnik K, Ben-Dor S, Galiani D, Hourvitz A, Dekel N, (2008) Molecular characterization and bioinformatics analysis of Ncoa7B, a novel ovulation-associated and reproduction system-specific Ncoa7 isoform. Reproduction 135: 321-333.
16. Falace A, Filipello F, La Padula V, Vanni N, Madia F, et al. (2010) TBC1D24, an ARF6-interacting protein, is mutated in familial infantile myoclonic epilepsy. Am J Hum Genet 87: 365-370.
17. Doerks T, Copley RR, Schultz J, Ponting CP, Bork P, (2002) Systematic identification of novel protein domain families associated with nuclear functions. Genome Res 12: 47-56.
18. Natoli R, Provis J, Valter K, Stone J, (2008) Expression and role of the early-response gene Oxr1 in the hyperoxia-challenged mouse retina. Invest Ophthalmol Vis Sci 49: 4561-4567.
19. Chung SH, Calafiore M, Plane JM, Pleasure DE, Deng W, (2011) Apoptosis inducing factor deficiency causes reduced mitofusion 1 expression and patterned Purkinje cell degeneration. Neurobiol Dis 41: 445-457.
20. Heintz N, Zoghbi HY, (2000) Insights from mouse models into the molecular basis of neurodegeneration. Annu Rev Physiol 62: 779-802.
21. Frank TC, Nunley MC, Sons HD, Ramon R, Abbott LC, (2003) Fluoro-jade identification of cerebellar granule cell and purkinje cell death in the alpha1A calcium ion channel mutant mouse, leaner. Neuroscience 118: 667-680.
22. Maricich SM, Soha J, Trenkner E, Herrup K, (1997) Failed cell migration and death of purkinje cells and deep nuclear neurons in the weaver cerebellum. J Neurosci 17: 3675-3683.
23. Arai A, Spencer JA, Olson EN, (2002) STARS, a striated muscle activator of Rho signaling and serum response factor-dependent transcription. J Biol Chem 277: 24453-24459.
24. Fischer H, Zhang XU, O'Brien KP, Kylsten P, Engvall E, (2001) C7, a novel nucleolar protein, is the mouse homologue of the Drosophila late puff product L82 and an isoform of human OXR1. Biochem Biophys Res Commun 281: 795-803.
25. Stadtman ER, Levine RL, (2003) Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 25: 207-218.
26. Fabisiak JP, Sedlov A, Kagan VE, (2002) Quantification of oxidative/nitrosative modification of CYS(34) in human serum albumin using a fluorescence-based SDS-PAGE assay. Antioxid Redox Signal 4: 855-865.
27. Wilson MA, (2011) The role of cysteine oxidation in DJ-1 function and dysfunction. Antioxid Redox Signal 15: 111-122.
28. Andres-Mateos E, Perier C, Zhang L, Blanchard-Fillion B, Greco TM, et al. (2007) DJ-1 gene deletion reveals that DJ-1 is an atypical peroxiredoxin-like peroxidase. Proc Natl Acad Sci U S A 104: 14807-14812.
29. Ogusucu R, Rettori D, Munhoz DC, Netto LE, Augusto O, (2007) Reactions of yeast thioredoxin peroxidases I and II with hydrogen peroxide and peroxynitrite: rate constants by competitive kinetics. Free Radic Biol Med 42: 326-334.
30. Guipponi M, Li QX, Hyde L, Beissbarth T, Smyth GK, et al. (2010) SAGE analysis of genes differentially expressed in presymptomatic TgSOD1G93A transgenic mice identified cellular processes involved in early stage of ALS pathology. J Mol Neurosci 41: 172-182.
31. Acevedo-Arozena A, Kalmar B, Essa S, Ricketts T, Joyce P, et al. (2011) A comprehensive assessment of the SOD1G93A low-copy transgenic mouse, which models human amyotrophic lateral sclerosis. Dis Model Mech.
32. Massaad CA, Washington TM, Pautler RG, Klann E, (2009) Overexpression of SOD-2 reduces hippocampal superoxide and prevents memory deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 106: 13576-13581.
33. Klein JA, Longo-Guess CM, Rossmann MP, Seburn KL, Hurd RE, et al. (2002) The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 419: 367-374.
34. El Ghouzzi V, Csaba Z, Olivier P, Lelouvier B, Schwendimann L, et al. (2007) Apoptosis-inducing factor deficiency induces early mitochondrial degeneration in brain followed by progressive multifocal neuropathology. J Neuropathol Exp Neurol 66: 838-847.
35. Wang X, Zaidi A, Pal R, Garrett AS, Braceras R, et al. (2009) Genomic and biochemical approaches in the discovery of mechanisms for selective neuronal vulnerability to oxidative stress. BMC Neurosci 10: 12.
36. Wang X, Michaelis EK, (2010) Selective neuronal vulnerability to oxidative stress in the brain. Front Aging Neurosci 2: 12.
37. Barber SC, Shaw PJ, (2010) Oxidative stress in ALS: key role in motor neuron injury and therapeutic target. Free Radic Biol Med 48: 629-641.
38. Perrin FE, Boisset G, Docquier M, Schaad O, Descombes P, et al. (2005) No widespread induction of cell death genes occurs in pure motoneurons in an amyotrophic lateral sclerosis mouse model. Hum Mol Genet 14: 3309-3320.
39. Ferraiuolo L, Heath PR, Holden H, Kasher P, Kirby J, et al. (2007) Microarray analysis of the cellular pathways involved in the adaptation to and progression of motor neuron injury in the SOD1 G93A mouse model of familial ALS. J Neurosci 27: 9201-9219.
40. Radi R, Beckman JS, Bush KM, Freeman BA, (1991) Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J Biol Chem 266: 4244-4250.
41. Peskin AV, Low FM, Paton LN, Maghzal GJ, Hampton MB, et al. (2007) The high reactivity of peroxiredoxin 2 with H(2)O(2) is not reflected in its reaction with other oxidants and thiol reagents. J Biol Chem 282: 11885-11892.
42. Dunford HB, (1999) Heme Peroxidases: Wiley-VCH, Weinheim, Germany.
43. Fomenko DE, Marino SM, Gladyshev VN, (2008) Functional diversity of cysteine residues in proteins and unique features of catalytic redox-active cysteines in thiol oxidoreductases. Mol Cells 26: 228-235.
44. Brandes N, Schmitt S, Jakob U, (2009) Thiol-based redox switches in eukaryotic proteins. Antioxid Redox Signal 11: 997-1014.
45. Jaramillo-Gutierrez G, Molina-Cruz A, Kumar S, Barillas-Mury C, (2010) The Anopheles gambiae oxidation resistance 1 (OXR1) gene regulates expression of enzymes that detoxify reactive oxygen species. PLoS ONE 5: e11168 doi:10.1371/journal.pone.0011168.
46. Stamper C, Siegel A, Liang WS, Pearson JV, Stephan DA, et al. (2008) Neuronal gene expression correlates of Parkinson's disease with dementia. Mov Disord 23: 1588-1595.
47. Poduri A, Lowenstein D, (2011) Epilepsy genetics-past, present, and future. Curr Opin Genet Dev 21: 325-332.
48. Isaacs AM, Oliver PL, Jones EL, Jeans A, Potter A, et al. (2003) A mutation in Af4 is predicted to cause cerebellar ataxia and cataracts in the robotic mouse. J Neurosci 23: 1631-1637.
49. Suraweera A, Becherel OJ, Chen P, Rundle N, Woods R, et al. (2007) Senataxin, defective in ataxia oculomotor apraxia type 2, is involved in the defense against oxidative DNA damage. J Cell Biol 177: 969-979.
50. Bilimoria PMaB A, (2008) Cold Spring Harb. Protoc.; 2008; doi:10.1101/pdb.prot5107.