Mitochondrial DNA damage is a hallmark of chemically induced and the R6/2 transgenic model of Huntington's disease

DNA Repair

Volumn 8, Issue 1, 2009, Pages 126-136

  Acevedo Torres, Karina ^a   Berríos, Lexsy ^b   Rosario, Nydia ^b   Dufault, Vanessa ^a   Skatchkov, Serguei ^b   Eaton, Misty J ^b   Torres Ramos, Carlos A ^a   Ayala Torres, Sylvette ^a  

^a UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^b UNIVERSIDAD CENTRAL DEL CARIBE   (United States)

Author keywords

3 Nitropropionic acid; Huntington's disease; Mitochondrial DNA repair; R6 2

Indexed keywords

3 NITROPROPIONIC ACID; HUNTINGTIN;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; CORPUS STRIATUM; DNA DAMAGE; HUNTINGTON CHOREA; MALE; MITOCHONDRION; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; TRANSGENIC MOUSE; TRINUCLEOTIDE REPEAT;

ANIMALS; CELL NUCLEUS; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; DNA DAMAGE; DNA, MITOCHONDRIAL; GUANOSINE; HUNTINGTON DISEASE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NITRO COMPOUNDS; PROPIONIC ACIDS;

ANIMALIA; MUS; MUS MUSCULUS;

EID: 56549089781     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2008.09.004     Document Type: Article

References (49)

1. The Huntington's Disease Collaborative Research Group. A novel gene encoding a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72 (1993) 971-983
2. Vonsattel J.P., and DiFiglia M. Huntington disease. J. Neuropathol. Exp. Neurol. 57 (1998) 369-384
3. Browne S.E., Bowling A.C., MacGarvey U., Baik M.J., Berger S.C., Muqit M.M., Bird E.D., and Beal M.F. Oxidative damage and metabolic dysfunction in Huntington's disease: selective vulnerability of the basal ganglia. Ann. Neurol. 41 (1997) 646-653
4. Polidori M.C., Mecocci P., Browne S.E., Senin U., and Beal M.F. Oxidative damage to mitochondrial DNA in Huntington's disease parietal cortex. Neurosci. Lett. 272 (1999) 53-56
5. Bogdanov M.B., Andreassen O.A., Dedeoglu A., Ferrante R.J., and Beal M.F. Increased oxidative damage to DNA in a transgenic mouse model of Huntington's disease. J. Neurochem. 79 (2001) 1246-1249
6. Perez-Severiano F., Rios C., and Segovia J. Striatal oxidative damage parallels the expression of a neurological phenotype in mice transgenic for the mutation of Huntington's disease. Brain Res. 862 (2000) 234-237
7. Brennan W.A., Bird E.D., and Aprille J.R. Regional mitochondrial respiratory activity in Huntington's disease brain. J. Neurochem. 44 (1985) 1948-1950
8. Gu M., Gash M.T., Mann V.M., Javoid-Agid F., Cooper J.M., and Shapira A.H. Mitochondrial defect in Huntington's disease caudate nucleus. Ann. Neurol. 39 (1996) 385-389
9. Tabrizi S.J., Cleeter M., Xuereb J., Taanman J.W., Cooper J.M., and Shapira A.H.V. Biochemical abnormalities and excitotoxicity in Huntington's disease brain. Ann. Neurol. 45 (1999) 25-32
10. Benchoua A., Trioulier Y., Zala D., Gaillard M.-C., Lefort N., Dufour N., Saudou F., Elalouf J.-M., Hirsch E., Hantraye P., Deglon N., and Brouillet E. Involvement of mitochondrial complex II defects in neuronal death produced by N-terminus fragment of mutated huntingtin. Mol. Biol. Cell 17 (2006) 1652-1663
11. Gould D.H. Brain enzyme and clinical alterations induced in rats and mice by nitroaliphatic toxicants. Toxicol. Lett. 27 (1995) 83-89
12. Beal M.F., Brouillet E., Jenkins B., Ferrante R.J., Kowall N.W., Miller J.M., Storey E., Srivastava R., Rosen B.R., and Hyman B.T. Neurochemical and histological characterization of the striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid. J. Neurosci. 13 (1993) 1481-1492
13. Brouillet E., Jenkins B.G., Hyman B.T., Ferrante R.J., Kowall N.W., Srivastava R., Roy D.S., Rosen B.R., and Beal M.F. Age-dependent vulnerability of the striatum to the mitochondrial toxin 3-nitropropionic acid. J. Neurochem. 60 (1993) 356-359
14. Palfi S., Ferrante R.J., Brouillet E., Beal M.F., Dolan R., Guyot M.C., Peschanski M., and Hantraye P. Chronic 3-nitropropionic acid treatment in baboons replicates the cognitive and motor deficits of Huntington's disease. J. Neurosci. 16 (1996) 3019-3025
15. Guyot M.C., Hantraye P., Dolan R., Palfi S., Maziere M., and Brouillet E. Quantifiable bradykinesia, gait abnormalities and Huntington's disease-like striatal lesions in rats chronically treated with 3-nitropropionic acid. Neuroscience 79 (1997) 45-56
16. Huang L.-S., Sun G., Cobessi D., Wang A.C., Shen J.T., Tung E.Y., Anderson V.E., and Berry E.A. 3-nitropropionic acid is a suicide inhibitor of mitochondrial respiration that, upon oxidation by complex II, forms a covalent adduct with a catalytic base arginine in the active site of the enzyme. J. Biol. Chem. 281 (2006) 5965-5972
17. Bogdanov M.B., Ferrante R.J., Kuemmerle S., Klivenyi P., and Beal M.F. Increased vulnerability to 3-nitropropionic acid in an animal model of Huntington's disease. J. Neurochem. 71 (1998) 2642-2644
18. Schulz J.B., Matthews R.T., Henshaw D.R., and Beal M.F. Neuroprotective strategies for treatment of lesions produced by mitochondrial toxins: implications for neurodegenerative diseases. Neuroscience 71 (1996) 1043-1048
19. Pettepher C.C., LeDoux S.P., Bohr V.A., and Wilson G.L. Repair of alkali-labile sites within the mitochondrial DNA of RINr 38 cells after exposure to the nitrosourea streptozotocin. J. Biol. Chem. 266 (1991) 3113-3117
20. Croteau D.L., and Bohr V.A. Repair of oxidative damage to nuclear and mitochondrial DNA in mammalian cells. J. Biol. Chem. 272 (1997) 25409-25412
21. Pinz K.G., and Bogenhagen D.F. Efficient repair of abasic sites in DNA by mitochondrial enzymes. Mol. Cell. Biol. 18 (1998) 1257-1265
22. Chen D., Lan J., Pei W., and Chen J. Detection of DNA base-excision repair activity for oxidative lesions in adult rat brain mitochondria. J. Neurosci. Res. 61 (2000) 225-236
23. Seeberg E., Eide L., and Bjoras M. The base excision repair pathway. Trends Biochem. Sci. 20 (1995) 391-396
24. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., and Ellenberger T. DNA Repair and Mutagenesis (2006), ASM, Washington, DC
25. Mangiarini L., Sathasivam K., Seller M., Cozens B., Harper A., Hetherington C., Lawton M., Trottier Y., Lehrach H., Davies S.W., and Bates G.P. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87 (1996) 493-506
26. Ayala-Torres S., Chen Y., Svoboda T., Rosenblatt J., and Van Houten B. Analysis of gene-specific DNA damage and repair using quantitative PCR. In: Doetchst P. (Ed). Methods: A Companion to Methods in Enzymology (2000), Academic Press
27. Yakes F.M., Chen Y., and Van Houten B. PCR-based assays for the detection and quantitation of DNA damage and repair. In: Pfeifer G.P. (Ed). Technologies for Detection of DNA Damage and Mutations (1996), Plenum Press, New York 169-182
28. Santos J.H., Meyer J.N., Mandavilli B.S., and Van Houten B. Quantitative PCR-based measurement of nuclear and mitochondrial DNA damage and repair in mammalian cells. Methods Mol. Biol. 314 (2006) 183-199
29. Manczak M., Jung Y., Partovi P.S.B., D., and Reddy P.H. Time-course of mitochondrial gene expressions in mice brains: implication for mitochondrial dysfunction, oxidative stredamage, and cytochrome c in aging. J. Neurochem. 92 (2005) 494-504
30. Borlongan C.V., Koutouzis T.K., and Sanberg P.R. 3-Nitropropionic acid animal model and Huntington's disease. Neurosci. Biobehav. Rev. 21 (1997) 289-293
31. Schulz J.B., Henshaw D.R., MacGarvey U., and Beal M.F. Involvement of oxidative stress in 3-nitropropionic acid neurotoxicity. Neurochem. Int. 29 (1996) 167-171
32. Bacsi A., Woodberry M., Widger W., Papaconstantinou J., Mitra S., Peterson J.W., and Boldogh I. Localization of superoxide anion production to mitochondrial electron transport chain in 3-NPA-treated cells. Mitochondrion 6 (2006) 235-244
33. Yakes M.F., and Houten B.v. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Cell Biol. 94 (1997) 514-519
34. Mandavilli B.S., Boldogh I., and Van Houten B. 3-nitropropionic acid-induced hydrogen peroxide, mitochondrial DNA damage, and cell death are attenuated by Bcl-2 overexpression in PC12 cells. Brain Res. Mol. Brain Res. 133 (2005) 215-223
35. Santos J.H., Hunakova L., Chen Y., Bortner C., and Van Houten B. Cell sorting experiments link persistent mitochondrial DNA damage with loss of mitochondrial membrane potential and apoptotic cell death. J. Biol. Chem. 278 (2003) 1728-1734
36. Trushina E., Dyer R.B., Badger J.D., Ure D., Eide L., Tran D.D., Vrieze B.T., Legendre-Guillemin V., McPherson P.S., Mandavilli B.S., Van Houten B., Zeitlin S., McNiven M., Aebersold R., Hayden M., Parisi J.E., Seeberg E., Dragatsis I., Doyle K., Bender A., Chacko C., and McMurray C.T. Mutant huntingtin impairs axonal trafficking in mammalian neurons in vivo and in vitro. Mol. Cell Biol. 24 (2004) 8195-8209
37. Cadet J., and Berger M. Radiation-induced decomposition of the purine bases within DNA and related model compounds. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 47 (1985) 127-143
38. Browne S.E., Bowling A.C., MacGarvey U., Baik M.J., Berger S.C., Muqit M.M.K., Bird E.D., and Beal M.F. Oxidative damage and metabolic dysfunction in Huntington's disease: selective vulnerability of the basal ganglia. Ann. Neurol. 41 (1997) 646-653
39. Mandavilli B.S., Ali S.F., and Van Houten B. DNA damage in brain mitochondria caused by aging and MPTP treatment. Brain Res. 885 (2000) 45-52
40. Kovtun I.V., Liu Y., Bjoras M., Klungland A., Wilson S.H., and McMurray C.T. OGG1 initiates age-dependent CAG trinucleotide expansion in somatic cells. Nature 447 (2007) 447-452
41. Brouillet E., Guyot M.C., Mittoux V., Altairac S., Conde F., Palfi S., and Hantraye P. Partial inhibition of brain succinate dehydrogenase by 3-nitropropionic acid is sufficient to initiate striatal degeneration in rat. J. Neurochem. 70 (1998) 794-805
42. Kim G.W., and Chan P.H. Oxidative stress and neuronal DNA fragmentation mediate age-dependent vulnerability to the mitochondrial toxin, 3-nitropropionic acid, in the mouse striatum. Neurobiol. Dis. 8 (2001) 114-126
43. Chen D., Cao G., Hastings T., Feng Y., Pei W., O'Horo C., and Chen J. Age-dependent decline of DNA repair activity for oxidative lesions in rat brain mitochondria. J. Neurochem. 81 (2002) 1273-1284
44. Intano G.W., Cho E.J., McMahan C.A., and Walter C.A. Age-related base excision repair activity in mouse brain and liver nuclear extracts. J. Gerontol. A Biol. Sci. Med. Sci. 58 (2003) B205-211
45. Imam S.Z., Karahalil B., Hogue B.A., Souza-Pinto N.C., and Bohr V.A. Mitochondrial and nuclear DNA-repair capacity of various brain regions in mouse is altered in an age-dependent manner. Neurobiol. Aging 27 (2006) 1129-1136
46. Klapstein G.J., Fisher R.S., Zanjani H., Cepeda C., Jokel E.S., Chesselet M.-F., Levine M.S., and Electrophysiological. Morphological changes in striatal spiny neurons in R6/2 Huntington's disease transgenic mice. J. Neurophysiol. 86 (2001) 2667-2677
47. Turmaine M., RAza A., Mahal A., Mangiarini L., Bates G., and Davies S. Nonapoptotic neurodegeneration in a transgenic model of Huntington's disease. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 8093-8097
48. Smith K.M., Matson S., Matson W.R., Cormier K., Del Signore S.J., Hagerty S.W., Stack E.C., Ryu H., and Ferrante R.J. Dose ranging and efficacy study of high-dose coenzyme Q10 formulations in Huntington's disease mice. Biochim. Biophys. Acta 1762 (2006) 616-626
49. Tabrizi S.J., Workman J., Hart P.E., Mangiarini L., Mahal A., Bates G., Cooper J.M., and Schapira A.H.V. Mitochondrial dysfunction and free radical damage in the Huntington R6/2 transgenic mouse. Ann. Neurol. 47 (2000) 80-86