MutT Homolog-1 Attenuates Oxidative DNA Damage and Delays Photoreceptor Cell Death in Inherited Retinal Degeneration

American Journal of Pathology

Volumn 181, Issue 4, 2012, Pages 1378-1386

  Murakami, Yusuke ^a   Ikeda, Yasuhiro ^a,b   Yoshida, Noriko ^a   Notomi, Shoji ^a   Hisatomi, Toshio ^a   Oka, Sugako ^b   De Luca, Gabriele ^c   Yonemitsu, Yoshikazu ^b   Bignami, Margherita ^c   Nakabeppu, Yusaku ^b   Ishibashi, Tatsuro ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; MUTT HOMOLOG 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NUCLEIC ACID BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CLINICAL ARTICLE; CONTROLLED STUDY; DNA DAMAGE; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHOTORECEPTOR CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINITIS PIGMENTOSA; SINGLE STRANDED DNA BREAK; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS INDUCING FACTOR; CALPAIN; CELL DEATH; CELL NUCLEUS; DISEASE MODELS, ANIMAL; DNA BREAKS, SINGLE-STRANDED; DNA DAMAGE; DNA REPAIR ENZYMES; ENZYME ACTIVATION; HUMANS; INHERITANCE PATTERNS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OXIDATION-REDUCTION; PHOSPHORIC MONOESTER HYDROLASES; PHOTORECEPTOR CELLS, VERTEBRATE; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN TRANSPORT; RATS; RETINAL DEGENERATION; RETINITIS PIGMENTOSA; SIGNAL TRANSDUCTION;

EID: 84866491686     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.06.026     Document Type: Article

References (47)

1. D.T. Hartong, E.L. Berson, T.P. Dryja Retinitis pigmentosa Lancet 368 2006 1795 1809 (Pubitemid 44739028)
2. K. Komeima, B.S. Rogers, L. Lu, P.A. Campochiaro Antioxidants reduce cone cell death in a model of retinitis pigmentosa Proc Natl Acad Sci U S A 103 2006 11300 11305 (Pubitemid 44159928)
3. K. Komeima, B.S. Rogers, P.A. Campochiaro Antioxidants slow photoreceptor cell death in mouse models of retinitis pigmentosa J Cell Physiol 213 2007 809 815 (Pubitemid 350058275)
4. Z.Z. Chong, F. Li, K. Maiese Oxidative stress in the brain: novel cellular targets that govern survival during neurodegenerative disease Prog Neurobiol 75 2005 207 246 (Pubitemid 40693131)
5. A.M. Mackey, N. Sanvicens, G. Groeger, F. Doonan, D. Wallace, T.G. Cotter Redox survival signalling in retina-derived 661W cells Cell Death Differ 15 2008 1291 1303 (Pubitemid 351984758)
6. J. Chen, K. Jin, M. Chen, W. Pei, K. Kawaguchi, D.A. Greenberg, R.P. Simon Early detection of DNA strand breaks in the brain after transient focal ischemia: implications for the role of DNA damage in apoptosis and neuronal cell death J Neurochem 69 1997 232 245 (Pubitemid 27274177)
7. M. Guillet, S. Boiteux Endogenous DNA abasic sites cause cell death in the absence of Apn1. Apn2 and Rad1/Rad10 in Saccharomyces cerevisiae EMBO J 21 2002 2833 2841 (Pubitemid 34619399)
8. J. Zhang, G. Perry, M.A. Smith, D. Robertson, S.J. Olson, D.G. Graham, T.J. Montine Parkinson's disease is associated with oxidative damage to cytoplasmic DNA and RNA in substantia nigra neurons Am J Pathol 154 1999 1423 1429 (Pubitemid 29226437)
9. A. Nunomura, G. Perry, G. Aliev, K. Hirai, A. Takeda, E.K. Balraj, P.K. Jones, H. Ghanbari, T. Wataya, S. Shimohama, S. Chiba, C.S. Atwood, R.B. Petersen, M.A. Smith Oxidative damage is the earliest event in Alzheimer disease J Neuropathol Exp Neurol 60 2001 759 767 (Pubitemid 32678256)
10. S. Boiteux, J.P. Radicella The human OGG1 gene: structure, functions, and its implication in the process of carcinogenesis Arch Biochem Biophys 377 2000 1 8 (Pubitemid 30257280)
11. H. Maki, M. Sekiguchi MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis Nature 355 1992 273 275
12. K. Sakumi, M. Furuichi, T. Tsuzuki, T. Kakuma, S. Kawabata, H. Maki, M. Sekiguchi Cloning and expression of cDNA for a human enzyme that hydrolyzes 8-oxo-dGTP, a mutagenic substrate for DNA synthesis J Biol Chem 268 1993 23524 23530 (Pubitemid 23328081)
13. H. Yamaguchi, K. Kajitani, Y. Dan, M. Furuichi, M. Ohno, K. Sakumi, D. Kang, Y. Nakabeppu 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 2006 551 563
14. G. De Luca, M.T. Russo, P. Degan, C. Tiveron, A. Zijno, E. Meccia, I. Ventura, E. Mattei, Y. Nakabeppu, M. Crescenzi, R. Pepponi, A. Pezzola, P. Popoli, M. Bignami A role for oxidized DNA precursors in Huntington's disease-like striatal neurodegeneration PLoS Genet 4 2008 e1000266
15. T. Murakami, M. Akimoto, S. Ooto, T. Suzuki, H. Ikeda, N. Kawagoe, M. Takahashi, N. Yoshimura Association between abnormal autofluorescence and photoreceptor disorganization in retinitis pigmentosa Am J Ophthalmol 145 2008 687 694
16. M. Hayakawa, K. Fujiki, A. Kanai Multicenter genetic study of retinitis pigmentosa in Japan, I: genetic heterogeneity in typical retinitis pigmentosa Jpn J Ophthalmol 41 1997 1 6 (Pubitemid 27220141)
17. K. Tsuruya, M. Furuichi, Y. Tominaga, M. Shinozaki, M. Tokumoto, T. Yoshimitsu, K. Fukuda, H. Kanai, H. Hirakata, M. Iida, Y. Nakabeppu Accumulation of 8-oxoguanine in the cellular DNA and the alteration of the OGG1 expression during ischemia-reperfusion injury in the rat kidney DNA Repair (Amst) 2 2003 211 229 (Pubitemid 36071506)
18. Y. Murakami, Y. Ikeda, Y. Yonemitsu, M. Onimaru, K. Nakagawa, R. Kohno, M. Miyazaki, T. Hisatomi, M. Nakamura, T. Yabe, M. Hasegawa, T. Ishibashi, K. Sueishi Inhibition of nuclear translocation of apoptosis-inducing factor is an essential mechanism of the neuroprotective activity of pigment epithelium-derived factor in a rat model of retinal degeneration Am J Pathol 173 2008 1326 1338
19. B. Chang, N.L. Hawes, R.E. Hurd, M.T. Davisson, S. Nusinowitz, J.R. Heckenlively Retinal degeneration mutants in the mouse Vision Res 42 2002 517 525 (Pubitemid 34169709)
20. J.J. Pang, S.L. Boye, A. Kumar, A. Dinculescu, W. Deng, J. Li, Q. Li, A. Rani, T.C. Foster, B. Chang, N.L. Hawes, J.H. Boatright, W.W. Hauswirth AAV-mediated gene therapy for retinal degeneration in the rd10 mouse containing a recessive PDEbeta mutation Invest Ophthalmol Vis Sci 49 2008 4278 4283
21. H. Kasai, S. Nishimura Hydroxylation of deoxyguanosine at the C-8 position by ascorbic acid and other reducing agents Nucleic Acids Res 12 1984 2137 2145
22. P.M. D'Cruz, D. Yasumura, J. Weir, M.T. Matthes, H. Abderrahim, M.M. LaVail, D. Vollrath Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat Hum Mol Genet 9 2000 645 651 (Pubitemid 30154023)
23. A. Gal, Y. Li, D.A. Thompson, J. Weir, U. Orth, S.G. Jacobson, E. Apfelstedt-Sylla, D. Vollrath Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa Nat Genet 26 2000 270 271
24. M.K. Shigenaga, C.J. Gimeno, B.N. Ames Urinary 8-hydroxy-2′- deoxyguanosine as a biological marker of in vivo oxidative DNA damage Proc Natl Acad Sci U S A 86 1989 9697 9701 (Pubitemid 20030700)
25. S. Sato, Y. Mizuno, N. Hattori Urinary 8-hydroxydeoxyguanosine levels as a biomarker for progression of Parkinson disease Neurology 64 2005 1081 1083 (Pubitemid 40388471)
26. T. Shiihara, M. Kato, T. Ichiyama, Y. Takahashi, N. Tanuma, R. Miyata, K. Hayasaka Acute encephalopathy with refractory status epilepticus: bilateral mesial temporal and claustral lesions, associated with a peripheral marker of oxidative DNA damage J Neurol Sci 250 2006 159 161 (Pubitemid 44665931)
27. S. Oka, M. Ohno, D. Tsuchimoto, K. Sakumi, M. Furuichi, Y. Nakabeppu Two distinct pathways of cell death triggered by oxidative damage to nuclear and mitochondrial DNAs EMBO J 27 2008 421 432 (Pubitemid 351161663)
28. S.W. Yu, H. Wang, M.F. Poitras, C. Coombs, W.J. Bowers, H.J. Federoff, G.G. Poirier, T.M. Dawson, V.L. Dawson Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor Science 297 2002 259 263 (Pubitemid 34761289)
29. F. Paquet-Durand, J. Silva, T. Talukdar, L.E. Johnson, S. Azadi, T. van Veen, M. Ueffing, S.M. Hauck, P.A. Ekstrom Excessive activation of poly(ADP-ribose) polymerase contributes to inherited photoreceptor degeneration in the retinal degeneration 1 mouse J Neurosci 27 2007 10311 10319 (Pubitemid 47450474)
30. D. Sanges, A. Comitato, R. Tammaro, V. Marigo Apoptosis in retinal degeneration involves cross-talk between apoptosis-inducing factor (AIF) and caspase-12 and is blocked by calpain inhibitors Proc Natl Acad Sci U S A 103 2006 17366 17371 (Pubitemid 44788975)
31. S. Mizukoshi, M. Nakazawa, K. Sato, T. Ozaki, T. Metoki, S. Ishiguro Activation of mitochondrial calpain and release of apoptosis-inducing factor from mitochondria in RCS rat retinal degeneration Exp Eye Res 91 2010 353 361
32. K. Takahashi, A.A. Pieper, S.E. Croul, J. Zhang, S.H. Snyder, J.H. Greenberg Post-treatment with an inhibitor of poly(ADP-ribose) polymerase attenuates cerebral damage in focal ischemia Brain Res 829 1999 46 54 (Pubitemid 29251683)
33. M. Kawamura, W. Nakajima, A. Ishida, A. Ohmura, S. Miura, G. Takada Calpain inhibitor MDL 28170 protects hypoxic-ischemic brain injury in neonatal rats by inhibition of both apoptosis and necrosis Brain Res 1037 2005 59 69 (Pubitemid 40372099)
34. S.A. Susin, H.K. Lorenzo, N. Zamzami, I. Marzo, B.E. Snow, G.M. Brothers, J. Mangion, E. Jacotot, P. Costantini, M. Loeffler, N. Larochette, D.R. Goodlett, R. Aebersold, D.P. Siderovski, J.M. Penninger, G. Kroemer Molecular characterization of mitochondrial apoptosis-inducing factor Nature 397 1999 441 446
35. S.W. Yu, S.A. Andrabi, H. vWang, N.S. Kim, G.G. Poirier, T.M. Dawson, V.L. Dawson Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death Proc Natl Acad Sci U S A 103 2006 18314 18319 (Pubitemid 44871655)
36. M.E. McLaughlin, M.A. Sandberg, E.L. Berson, T.P. Dryja Recessive mutations in the gene encoding the beta-subunit of rod phosphodiesterase in patients with retinitis pigmentosa Nat Genet 4 1993 130 134 (Pubitemid 23179094)
37. G.Q. Chang, Y. Hao, F. Wong Apoptosis: final common pathway of photoreceptor death in rd, rds, and rhodopsin mutant mice Neuron 11 1993 595 605 (Pubitemid 23321770)
38. H. Kikuchi, A. Furuta, K. Nishioka, S.O. Suzuki, Y. Nakabeppu, T. Iwaki Impairment of mitochondrial DNA repair enzymes against accumulation of 8-oxo-guanine in the spinal motor neurons of amyotrophic lateral sclerosis Acta Neuropathol 103 2002 408 414 (Pubitemid 36097036)
39. S.B. Laughlin, R.R. de Ruyter van Steveninck, J.C. Anderson The metabolic cost of neural information Nat Neurosci 1 1998 36 41 (Pubitemid 128652639)
40. R. Takeya, H. Sumimoto Molecular mechanism for activation of superoxide-producing NADPH oxidases Mol Cells 16 2003 271 277 (Pubitemid 41582851)
41. M. Haruta, R.A. Bush, S. Kjellstrom, C. Vijayasarathy, Y. Zeng, Y.Z. Le, P.A. Sieving Depleting Rac1 in mouse rod photoreceptors protects them from photo-oxidative stress without affecting their structure or function Proc Natl Acad Sci U S A 106 2009 9397 9402
42. H. Kamiya, H. Kasai Formation of 2-hydroxydeoxyadenosine triphosphate, an oxidatively damaged nucleotide, and its incorporation by DNA polymerases Steady-state kinetics of the incorporation J Biol Chem 270 1995 19446 19450
43. Y. Nakabeppu, S. Oka, Z. Sheng, D. Tsuchimoto, K. Sakumi Programmed cell death triggered by nucleotide pool damage and its prevention by MutT homolog-1 (MTH1) with oxidized purine nucleoside triphosphatase Mutat Res 703 2010 51 58
44. M. Akimoto, H. Cheng, D. Zhu, J.A. Brzezinski, R. Khanna, E. Filippova, E.C. Oh, Y. Jing, J.L. Linares, M. Brooks, S. Zareparsi, A.J. Mears, A. Hero, vT. Glaser, A. Swaroop Targeting of GFP to newborn rods by Nrl promoter and temporal expression profiling of flow-sorted photoreceptors Proc Natl Acad Sci U S A 103 2006 3890 3895 (Pubitemid 43376651)
45. I.I. Kruman, R.P. Wersto, F. Cardozo-Pelaez, L. Smilenov, S.L. Chan, F.J. Chrest, R. Emokpae Jr, M. Gorospe, M.P. Mattson Cell cycle activation linked to neuronal cell death initiated by DNA damage Neuron 41 2004 549 561 (Pubitemid 38253067)
46. T.M. Kauppinen, R.A. Swanson The role of poly(ADP-ribose) polymerase-1 in CNS disease Neuroscience 145 2007 1267 1272 (Pubitemid 46602734)
47. D. Martin-Oliva, R.M. Ferrer-Martin, A.M. Santos, M.C. Carrasco, A. Sierra, J.L. Marin-Teva, R. Calvente, J. Navascues, M.A. Cuadros Simultaneous cell death and upregulation of poly(ADP-ribose) polymerase-1 expression in early postnatal mouse retina Invest Ophthalmol Vis Sci 52 2011 7445 7454