A role for oxidized DNA precursors in Huntington's disease-like striatal neurodegeneration

PLoS Genetics

Volumn 4, Issue 11, 2008, Pages

  De Luca, Gabriele ^a   Russo, Maria Teresa ^a   Degan, Paolo ^b   Tiveron, Cecilia ^c   Zijno, Andrea ^a   Meccia, Ettore ^a   Ventura, Ilenia ^a   Mattei, Elisabetta ^d   Nakabeppu, Yusaku ^e   Crescenzi, Marco ^a   Pepponi, Rita ^a   Pèzzola, Antonella ^a   Popoli, Patrizia ^a   Bignami, Margherita ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^d CNR   (Italy)

^e KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROPROPIONIC ACID; 8 HYDROXYGUANINE; GUANINE DERIVATIVE; HYDROLASE; NUCLEIC ACID PRECURSOR; NUCLEOSIDE TRIPHOSPHATE; OXIDIZING AGENT; 3-NITROPROPIONIC ACID; 8 OXO 7 HYDRODEOXYGUANOSINE; 8 OXODGTPASE; 8-HYDROXYGUANINE; 8-OXO-7-HYDRODEOXYGUANOSINE; 8-OXODGTPASE; COMPLEMENTARY DNA; DEOXYGUANOSINE; DRUG DERIVATIVE; GUANINE; HUNTINGTON PROTEIN, MOUSE; NERVE PROTEIN; NITRO DERIVATIVE; NUCLEAR PROTEIN; PHOSPHATASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROPIONIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DEATH; DYSTONIA; FEMALE; FIBROBLAST; GAIT DISORDER; GENE EXPRESSION; GENETIC MODEL; HEXOSE MONOPHOSPHATE SHUNT; HUNTINGTON CHOREA; MOUSE; NERVE DEGENERATION; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; STEM CELL; TRANSGENIC MOUSE; WEIGHT REDUCTION; WILD TYPE; ANIMAL; ANIMAL EMBRYO; DEGENERATIVE DISEASE; DNA DAMAGE; GENETICS; HUMAN; METABOLISM; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS;

MUS; MUS MUSCULUS;

ANIMALS; CORPUS STRIATUM; DEOXYGUANOSINE; DNA DAMAGE; DNA REPAIR ENZYMES; DNA, COMPLEMENTARY; EMBRYO, MAMMALIAN; FIBROBLASTS; GUANINE; HUMANS; HUNTINGTON DISEASE; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURODEGENERATIVE DISEASES; NITRO COMPOUNDS; NUCLEAR PROTEINS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHOSPHORIC MONOESTER HYDROLASES; PROPIONIC ACIDS; STEM CELLS;

EID: 57149107147     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000266     Document Type: Article

References (43)

1. Russo MT, De Luca G, Degan P, Parlanti E, Dogliotti E, et al. (2004) 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: 4411-4.
2. Xie Y, Yang H, Cunanan C, Okamoto K, Shibata D, et al. (2004) 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: 3096-3102.
3. Rass U, Ahel I, West SC (2007) Defective DNA repair and neurodegenerative disease. Cell 130: 991-1004.
4. Browne SE, Bowling AC, MacGarvey U, Baik MJ, Berger SC, et al. (1997) Oxidative damage and metabolic dysfunction in Huntington's disease: selective vulnerability of the basal ganglia. Ann Neurol 41: 646-53.
5. Polidori MC, Mecocci P, Browne SE, Senin U, Beal MF (1999) Oxidative damage to mitochondrial DNA in Huntington's disease parietal cortex. Neurosci Lett 272: 53-6.
6. Bogdanov MB, Andreassen OA, Dedeoglu A, Ferrante RJ, Beal MF (2001) Increased oxidative damage to DNA in a transgenic mouse model of Huntington's disease. J Neurochem 79: 1246-9.
7. Nakabeppu Y, Tsuchimoto D, Yamaguchi H, Sakumi K (2007) Oxidative damage in nucleic acids and Parkinson's disease. J Neurosci Res 85: 919-34.
8. Ferrante RJ, Browne SE, Shinobu LA, Bowling AC, Baik MJ, et al. (1997) Evidence of increased oxidative damage in both sporadic and familial amyotrophic lateral sclerosis. J Neurochem 69: 2064-74.
9. Kikuchi H, Furuta A, Nishioka K, Suzuki SO, Nakabeppu Y, et al. (2002) Impairment of mitochondrial DNA repair enzymes against accumulation of 8-oxo-guanine in the spinal motor neurons of amyotrophic lateral sclerosis. Acta Neuropathol (Berl) 103: 408-14.
10. Barnes DE, Lindahl T (2004) Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annu Rev Genet 38: 445-76.
11. Tuo J, Jaruga P, Rodriguez H, Bohr VA, Dizdaroglu M (2003) Primary fibroblasts of Cockayne syndrome patients are defective in cellular repair of 8-hydroxyguanine and 8-hydroxyadenine resulting from oxidative stress. Faseb J 17: 668-74.
12. de Waard H, de Wit J, Andressoo JO, van Oostrom CT, Riis B, et al. (2004) Different effects of CSA and CSB deficiency on sensitivity to oxidative DNA damage. Mol Cell Biol 24: 7941-8.
13. D'Errico M, Parlanti E, Teson M, Degan P, Lemma T, et al. (2007) The role of CSA in the response to oxidative DNA damage in human cells. Oncogene 26: 4336-43.
14. Ishibashi T, Hayakawa H, Sekiguchi M (2003) A novel mechanism for preventing mutations caused by oxidation of guanine nucleotides. EMBO Rep 4: 479-83.
15. Sakumi K, Furuichi M, Tsuzuki T, Kakuma T, Kawabata S, et al. (1993) Cloning and expression of cDNA for a human enzyme that hydrolyzes 8-oxo-dGTP, a mutagenic substrate for DNA synthesis. J Biol Chem 268: 23524-30.
16. Fujikawa K, Kamiya H, Yakushiji H, Fujii Y, Nakabeppu Y, et al. (1999) The oxidized forms of dATP are substrates for the human MutT homologue, the hMTH1 protein. J Biol Chem 274: 18201-5.
17. Hayakawa H, Hofer A, Thelander L, Kitajima S, Cai Y, et al. (1999) Metabolic fate of oxidized guanine ribonucleotides in mammalian cells. Biochemistry 38: 3610-4.
18. Tsuzuki T, Egashira A, Igarashi H, Iwakuma T, Nakatsuru Y, et al. (2001) Spontaneous tumorigenesis in mice defective in the MTH1 gene encoding 8-oxo-dGTPase. Proc Natl Acad Sci U S A 98: 11456-11461.
19. Yamaguchi K, Kajitani H, Dan Y, Furuichi M, Ohno M, et al. (2006) MTH1, an oxidized purine nucleoside triphosphatase, protects the dopamine neurons from oxidative damage in nucleic acids caused by 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine. Cell Death Differ 13: 551-63.
20. The Huntington's Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72: 971-83.
21. Brouillet E, Condé F, Beal MF, Hantraye P (1999) Replicating Huntington's disease phenotype in experimental animals. Prog Neurobiol 59: 427-68.
22. Trettel F, Rigamonti D, Hilditch-Maguire P, Wheeler VC, Sharp AH, et al. (2000) Dominant phenotypes produced by the HD mutation in STHdh(Q111) striatal cells. Hum Mol Genet 9: 2799-809.
23. Kang D, Nishida J, Iyama A, Nakabeppu Y, Furuichi M, et al. (1995) Intracellular localization of 8-oxo-dGTPase in human cells, with special reference to the role of the enzyme in mitochondria. J Biol Chem 270: 14659-65.
24. Russo MT, Blasi MF, Chiera F, Fortini P, Degan P, et al. (2004) The oxidized deoxynucleoside triphosphate pool is a significant contributor to genetic instability in mismatch repair-deficient cells. Mol Cell Biol 24: 465-74.
25. Hofer T, Seo AY, Prudencio M, Leeuwenburgh C (2006) A method to determine RNA and DNA oxidation simultaneously by HPLC-ECD: greater RNA than DNA oxidation in rat liver after doxorubicin administration. Biol Chem 387: 103-11.
26. Hofer T, Badouard C, Bajak E, Ravanat JL, Mattsson A, et al. (2005) Hydrogen peroxide causes greater oxidation in cellular RNA than in DNA. Biol Chem 386: 333-7.
27. Kawanishi S, Murata M (2006) Mechanism of DNA damage induced by bromate differs from general types of oxidative stress. Toxicology 221: 172-178.
28. Bus JS, Gibson JE (1984) Paraquat: model for oxidant-initiated toxicity. Environ Health Perspect 55: 37-46.
29. Waddell WJ, Marlowe C (1980) Tissue and cellular disposition of paraquat in mice. Toxicol Appl Pharmacol 56: 127-140.
30. Tokunaga I, Kubo S, Mikasa H, et al. (1997) Determination of 8-hydroxydeoxyguanosine formation in rat organs: assessment of paraquat-evoked oxidative DNA damage. Biochem Mol Biol Int 43: 73-77.
31. Blum D, Galas MC, Gall D, Cuvelier L, Schiffmann SN (2002) Striatal and cortical neurochemical changes induced by chronic metabolic compromise in the 3-nitropropionic model of Huntington's disease. Neurobiol Dis 10: 410-26.
32. Rigamonti D, Bauer JH, De-Fraja C, Conti L, Sipione S, et al. (2000) Wild-type huntingtin protects from apoptosis upstream of caspase-3. J Neurosci 20: 3705-13.
33. Ruan Q, Lesort M, MacDonald ME, Johnson GV (2004) Striatal cells from mutant huntingtin knock-in mice are selectively vulnerable to mitochondrial complex II inhibitor-induced cell death through a non-apoptotic pathway. Hum Mol Genet 13: 669-81.
34. Gray JP, Heck DE, Mishin V, et al. (2007) Paraquat increases cyanide-insensitive respiration in murine lung epithelial cells by activating an NAD(P)H:paraquat oxidoreductase: identification of the enzyme as thioredoxin reductase. J Biol Chem 282: 7939-7949.
35. Kajitani K, Yamaguchi H, Dan Y, Furuichi M, Kang D, et al. (2006) MTH1, an oxidized purine nucleoside triphosphatase, suppresses the accumulation of oxidative damage of nucleic acids in the hippocampal microglia during kainite-induced excitotoxicity. J Neurosci 26: 1688-98.
36. Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443: 787-95.
37. Shimura-Miura H, Hattori N, Kang D, Miyako K, Nakabeppu Y, et al. (1999) Increased 8-oxo-dGTPase in the mitochondria of substantia nigral neurons in Parkinson's disease. Ann Neurol 46: 920-4.
38. Arai T, Fukae J, Hatano T, Kubo S, Ohtsubo T, et al. (2006) Up-regulation of hMUTYH, a DNA repair enzyme, in the mitochondria of substantia nigra in Parkinson's disease. Acta Neuropathol 112: 139-45.
39. Fukae J, Takanashi M, Kubo S, Nishioka K, Nakabeppu Y, et al. (2005) Expression of 8-oxoguanine DNA glycosylase (OGG1) in Parkinson's disease and related neurodegenerative disorders. Acta Neuropathol (Berl) 109: 256-62.
40. Kovtun IV, Liu Y, Bjoras M, Klungland A, Wilson SH, et al. (2007) OGG1 initiates age-dependent CAG trinucleotide expansion in somatic cells. Nature 447: 447-52.
41. Nunomura A, Moreira PI, Takeda A, Smith MA, Perry G (2007) Oxidative RNA damage and in neurodegeneration. Curr Med Chem 14: 2968-75.
42. Ishibashi T, Hayakawa H, Ito R, Miyazawa M, Yamagata Y, et al. (2005) Mammalian enzymes for preventing transcriptional errors caused by oxidative damage. Nucleic Acids Res 33: 3779-84.
43. Taddei F, Hayakawa H, Bouton LF, Cirinesi AM, Matic I, et al. (1997) Counteraction by MutT protein of transcriptional errors caused by oxidative damage. Science 278: 128-130.