Accelerated clinical course of prion disease in mice compromised in repair of oxidative DNA damage

Free Radical Biology and Medicine

Volumn 68, Issue , 2014, Pages 1-7

  Jalland, Clara M O ^a   Benestad, Sylvie L ^b   Ersdal, Cecilie ^a   Scheffler, Katja ^c   Suganthan, Rajikala ^d   Nakabeppu, Yusaku ^e   Eide, Lars ^c   Bjørås, Magnar ^d   Tranulis, Michael A ^a  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b NORWEGIAN VETERINARY INSTITUTE   (Norway)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

^d UNIVERSITY OF OSLO   (Norway)

^e KYUSHU UNIVERSITY   (Japan)

Author keywords

DNA damage; DNA repair; Free radicals; Neurodegeneration; Prion disease; Reactive oxygen species

Indexed keywords

8 HYDROXYGUANINE; ADENINE; DNA BASE; DNA GLYCOSYLASE MUTY; OGG1 PROTEIN; PROTEIN; PROTEINASE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DNA DAMAGE; DNA REPAIR; EXCISION REPAIR; FEMALE; MOUSE; NEUROTOXICITY; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRION; PRION DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCRAPIE; WESTERN BLOTTING;

MUS;

DNA DAMAGE; DNA REPAIR; FREE RADICALS; NEURODEGENERATION; PRION DISEASE; REACTIVE OXYGEN SPECIES;

ANIMALS; DISEASE MODELS, ANIMAL; DNA DAMAGE; DNA GLYCOSYLASES; DNA REPAIR; GUANINE; HUMANS; MICE; MICE, KNOCKOUT; OXIDATIVE STRESS; PRION DISEASES; PRIONS; REACTIVE OXYGEN SPECIES; SCRAPIE;

EID: 84890475430     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.11.013     Document Type: Article

References (45)

1. B. Dalhus, J.K. Laerdahl, P.H. Backe, and M. Bjoras DNA base repair - recognition and initiation of catalysis FEMS Microbiol. Rev. 33 2009 1044 1078
2. M.L. Hegde, T.K. Hazra, and S. Mitra Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells Cell Res 18 2008 27 47
3. S. Shibutani, M. Takeshita, and A.P. Grollman Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG Nature 349 1991 431 434 (Pubitemid 21926107)
4. H. Aburatani, Y. Hippo, T. Ishida, R. Takashima, C. Matsuba, and T. Kodama Cloning and characterization of mammalian 8-hydroxyguanine-specific DNA glycosylase/apurinic, apyrimidinic lyase, a functional mutM homologue Cancer Res 57 1997 2151 2156 (Pubitemid 27247031)
5. M. Bjoras, L. Luna, B. Johnsen, E. Hoff, T. Haug, and T. Rognes Opposite base-dependent reactions of a human base excision repair enzyme on DNA containing 7,8-dihydro-8-oxoguanine and abasic sites EMBO J 16 1997 6314 6322 (Pubitemid 27458351)
6. R. Lu, H.M. Nash, and G.L. Verdine A mammalian DNA repair enzyme that excises oxidatively damaged guanines maps to a locus frequently lost in lung cancer Curr. Biol 7 1997 397 407 (Pubitemid 27274793)
7. J.P. Radicella, C. Dherin, C. Desmaze, M.S. Fox, and S. Boiteux Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae Proc. Natl. Acad. Sci. USA 94 1997 8010 8015 (Pubitemid 27343767)
8. T. Roldan-Arjona, Y.F. Wei, K.C. Carter, A. Klungland, C. Anselmino, and R.P. Wang Molecular cloning and functional expression of a human cDNA encoding the antimutator enzyme 8-hydroxyguanine-DNA glycosylase Proc. Natl. Acad. Sci. USA 94 1997 8016 8020 (Pubitemid 27343768)
9. T.A. Rosenquist, D.O. Zharkov, and A.P. Grollman Cloning and characterization of a mammalian 8-oxoguanine DNA glycosylase Proc. Natl. Acad. Sci. USA 94 1997 7429 7434 (Pubitemid 27345332)
10. M.M. Slupska, C. Baikalov, W.M. Luther, J.H. Chiang, Y.F. Wei, and J.H. Miller Cloning and sequencing a human homolog (hMYH) of the Escherichia coli mutY gene whose function is required for the repair of oxidative DNA damage J. Bacteriol 178 1996 3885 3892 (Pubitemid 26227206)
11. T. Ohtsubo, K. Nishioka, Y. Imaiso, S. Iwai, H. Shimokawa, and H. Oda Identification of human MutY homolog (hMYH) as a repair enzyme for 2-hydroxyadenine in DNA and detection of multiple forms of hMYH located in nuclei and mitochondria Nucleic Acids Res 28 2000 1355 1364 (Pubitemid 30142678)
12. M.T. Russo, L.G. De, P. Degan, E. Parlanti, E. Dogliotti, and D.E. Barnes Accumulation of the oxidative base lesion 8-hydroxyguanine in DNA of tumor-prone mice defective in both the Myh and Ogg1 DNA glycosylases Cancer Res 64 2004 4411 4414 (Pubitemid 38856910)
13. K. Sakamoto, Y. Tominaga, K. Yamauchi, Y. Nakatsu, K. Sakumi, and K. Yoshiyama MUTYH-null mice are susceptible to spontaneous and oxidative stress induced intestinal tumorigenesis Cancer Res 67 2007 6599 6604 (Pubitemid 47105504)
14. S. Jones, P. Emmerson, J. Maynard, J.M. Best, S. Jordan, and G.T. Williams Biallelic germline mutations in MYH predispose to multiple colorectal adenoma and somatic G:C→T:A mutations Hum. Mol. Genet 11 2002 2961 2967
15. S. Jones, S. Lambert, G.T. Williams, J.M. Best, J.R. Sampson, and J.P. Cheadle Increased frequency of the k-ras G12C mutation in MYH polyposis colorectal adenomas Br. J. Cancer 90 2004 1591 1593 (Pubitemid 38648243)
16. A. Aguzzi, and C. Haass Games played by rogue proteins in prion disorders and Alzheimer's disease Science 302 2003 814 818 (Pubitemid 37339613)
17. Y. Christen Oxidative stress and Alzheimer disease Am. J. Clin. Nutr. 71 2000 621S 629S (Pubitemid 30061247)
18. N. Ahmed, U. Ahmed, P.J. Thornalley, K. Hager, G. Fleischer, and G. Munch Protein glycation, oxidation and nitration adduct residues and free adducts of cerebrospinal fluid in Alzheimer's disease and link to cognitive impairment J. Neurochem 92 2005 255 263 (Pubitemid 40194017)
19. K.S. Montine, E. Reich, M.D. Neely, K.R. Sidell, S.J. Olson, and W.R. Markesbery Distribution of reducible 4-hydroxynonenal adduct immunoreactivity in Alzheimer disease is associated with APOE genotype J. Neuropathol. Exp. Neurol. 57 1998 415 425 (Pubitemid 28237325)
20. W.R. Markesbery Oxidative stress hypothesis in Alzheimer's disease Free Radic. Biol. Med. 23 1997 134 147 (Pubitemid 27217017)
21. J. Wang, S. Xiong, C. Xie, W.R. Markesbery, and M.A. Lovell Increased oxidative damage in nuclear and mitochondrial DNA in Alzheimer's disease J. Neurochem 93 2005 953 962 (Pubitemid 40695754)
22. C. Haass, and D.J. Selkoe Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide Nat. Rev. Mol. Cell. Biol. 8 2007 101 112 (Pubitemid 46432529)
23. X. Huang, C.S. Atwood, M.A. Hartshorn, G. Multhaup, L.E. Goldstein, and R.C. Scarpa The A beta peptide of Alzheimer's disease directly produces hydrogen peroxide through metal ion reduction Biochemistry 38 1999 7609 7616 (Pubitemid 29289332)
24. 2 J. Biol. Chem 277 2002 40302 40308 (Pubitemid 35215603)
25. S.D. Yan, and D.M. Stern Mitochondrial dysfunction and Alzheimer's disease: role of amyloid-beta peptide alcohol dehydrogenase (ABAD) Int. J. Exp. Pathol. 86 2005 161 171 (Pubitemid 40813912)
26. M. Guentchev, S.L. Siedlak, C. Jarius, F. Tagliavini, R.J. Castellani, and G. Perry Oxidative damage to nucleic acids in human prion disease Neurobiol. Dis. 9 2002 275 281 (Pubitemid 34442076)
27. M.W. Brazier, V. Lewis, G.D. Ciccotosto, G.M. Klug, V.A. Lawson, and R. Cappai Correlative studies support lipid peroxidation is linked to PrP(res) propagation as an early primary pathogenic event in prion disease Brain Res. Bull 68 2006 346 354 (Pubitemid 41827717)
28. D.R. Brown, W.J. Schulz-Schaeffer, B. Schmidt, and H.A. Kretzschmar Prion protein-deficient cells show altered response to oxidative stress due to decreased SOD-1 activity Exp. Neurol 146 1997 104 112 (Pubitemid 27319724)
29. D.R. Brown, R.S. Nicholas, and L. Canevari Lack of prion protein expression results in a neuronal phenotype sensitive to stress J. Neurosci. Res 67 2002 211 224 (Pubitemid 34052040)
30. F. Klamt, F. Dal-Pizzol, ML Conte da Frota Jr., R. Walz, M.E. Andrades, and E.G. da Silva Imbalance of antioxidant defense in mice lacking cellular prion protein Free Radic. Biol. Med 30 2001 1137 1144 (Pubitemid 32441839)
31. N.F. McLennan, P.M. Brennan, A. McNeill, I. Davies, A. Fotheringham, and K.A. Rennison Prion protein accumulation and neuroprotection in hypoxic brain damage Am. J. Pathol. 165 2004 227 235 (Pubitemid 38821830)
32. C.L. Haigh, A.R. McGlade, V. Lewis, C.L. Masters, V.A. Lawson, and S.J. Collins Acute exposure to prion infection induces transient oxidative stress progressing to be cumulatively deleterious with chronic propagation in vitro Free Radic. Biol. Med 51 2011 594 608
33. M.K. Sandberg, H. Al-Doujaily, B. Sharps, A.R. Clarke, and J. Collinge Prion propagation and toxicity in vivo occur in two distinct mechanistic phases Nature 470 2011 540 542
34. S. Hirano, Y. Tominaga, A. Ichinoe, Y. Ushijima, D. Tsuchimoto, and Y. Honda-Ohnishi Mutator phenotype of MUTYH-null mouse embryonic stem cells J. Biol. Chem 278 2003 38121 38124 (Pubitemid 37221699)
35. Y. Nakabeppu, D. Tsuchimoto, A. Ichinoe, M. Ohno, Y. Ide, and S. Hirano Biological significance of the defense mechanisms against oxidative damage in nucleic acids caused by reactive oxygen species: from mitochondria to nuclei Ann. N. Y. Acad. Sci 1011 2004 101 111 (Pubitemid 38608396)
36. Y. Xie, H. Yang, C. Cunanan, K. Okamoto, D. Shibata, and J. Pan Deficiencies in mouse Myh and Ogg1 result in tumor predisposition and G to T mutations in codon 12 of the K-ras oncogene in lung tumors Cancer Res 64 2004 3096 3102 (Pubitemid 38581409)
37. M.E. Bruce, P.A. McBride, and C.F. Farquhar Precise targeting of the pathology of the sialoglycoprotein, PrP, and vacuolar degeneration in mouse scrapie Neurosci. Lett. 102 1989 1 6 (Pubitemid 19163144)
38. H. Fraser, and A.G. Dickinson The sequential development of the brain lesion of scrapie in three strains of mice J. Comp. Pathol 78 1968 301 311
39. L. Gonzalez, S. Martin, I. Begara-McGorum, N. Hunter, F. Houston, and M. Simmons Effects of agent strain and host genotype on PrP accumulation in the brain of sheep naturally and experimentally affected with scrapie J. Comp. Pathol 126 2002 17 29
40. V. Selvaraju, M. Joshi, S. Suresh, J.A. Sanchez, N. Maulik, and G. Maulik Diabetes, oxidative stress, molecular mechanism, and cardiovascular disease - an overview Toxicol. Mech. Methods 22 2012 330 335
41. X. Wang, and E.K. Michaelis Selective neuronal vulnerability to oxidative stress in the brain Front. Aging Neurosci 2 2010 12
42. A.D. Steele, G. Hutter, W.S. Jackson, F.L. Heppner, A.W. Borkowski, and O.D. King Heat shock factor 1 regulates lifespan as distinct from disease onset in prion disease Proc. Natl. Acad. Sci. USA 105 2008 13626 13631
43. J. Tatzelt, J. Zuo, R. Voellmy, M. Scott, U. Hartl, and S.B. Prusiner Scrapie prions selectively modify the stress response in neuroblastoma cells Proc. Natl. Acad. Sci. USA 92 1995 2944 2948
44. S. Akhtar, J. Grizenkova, A. Wenborn, H. Hummerich, M.M. Fernandez de, and S. Brandner Sod1 deficiency reduces incubation time in mouse models of prion disease PLoS One 8 2013 e54454
45. G. Tamguney, K. Giles, D.V. Glidden, P. Lessard, H. Wille, and P. Tremblay Genes contributing to prion pathogenesis J. Gen. Virol. 89 2008 1777 1788