The DNA polymerase γ Y955C disease variant associated with PEO and parkinsonism mediates the incorporation and translesion synthesis opposite 7,8-dihydro-8-oxo-2′-deoxyguanosine

Human Molecular Genetics

Volumn 16, Issue 22, 2007, Pages 2729-2739

  Graziewicz, Maria A ^a,b   Bienstock, Rachelle J ^a   Copeland, William C ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYGUANINE; DNA DIRECTED DNA POLYMERASE GAMMA; DNA POLYMERASE; GENE PRODUCT; PHENYLALANINE; PROTEIN POLG; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASE PAIRING; CHEMICAL ANALYSIS; CHRONIC PROGRESSIVE EXTERNAL OPHTHALMOPLEGIA; DNA REPLICATION; DNA SYNTHESIS; GENE DELETION; GENE FREQUENCY; GENE INSERTION; GENE MUTATION; GENETIC ANALYSIS; GENETIC VARIABILITY; HUMAN; MOLECULAR MODEL; MUTAGENESIS; NONHUMAN; OXIDATIVE STRESS; PARKINSONISM; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONFORMATION;

DEOXYGUANOSINE; DNA; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; HUMANS; MODELS, MOLECULAR; MUTATION; OPHTHALMOPLEGIA, CHRONIC PROGRESSIVE EXTERNAL; OXIDATIVE STRESS; PARKINSONIAN DISORDERS;

EID: 35548972018     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddm227     Document Type: Article

References (68)

1. Kaguni, L.S. (2004) DNA polymerase gamma, the mitochondrial replicase. Annu. Rev. Biochem., 73, 293-320.
2. Graziewicz, M.A., Longley, M.J. and Copeland, W.C. (2006) DNA polymerase gamma in Mitochondrial DNA Replication and Repair. Chem. Rev., 106, 383-405.
3. Longley, M.J., Graziewicz, M.A., Bienstock, R.J. and Copeland, W.C. (2005) Consequences of mutations in human DNA polymeraseγ. Gene, 354, 125-131.
4. Hudson, G. and Chinnery, P.F. (2006) Mitochondrial DNA polymerase-gamma and human disease. Hum. Mol. Genet., 15 Spec no. 2, R244-R252.
5. DiMauro, S., Davidzon, G. and Hirano, M. (2006) A polymorphic polymerase. Brain, 129, 1637-1639.
6. Van Goethem, G., Dermaut, B., Lofgren, A., Martin, J.J. and Van Broeckhoven, C. (2001) Mutation of POLG is associated with progressive external ophthalmoplegia characterized by mtDNA deletions. Nat. Genet., 28, 211-212.
7. Lamantea, E., Tiranti, V., Bordoni, A., Toscano, A., Bono, F., Servidei, S., Papadimitriou, A., Spelbrink, H., Silvestri, L., Casari, G. et al. (2002) Mutations of mitochondrial DNA polymerase gamma are a frequent cause of autosomal dominant or recessive Progressive External Ophthalmoplegia. Ann. Neurol., 52, 211-219.
8. Luoma, P., Melberg, A., Rinne, J.O., Kaukonen, J.A., Nupponen, N.N., Chalmers, R.M., Oldfors, P.A., Rautakorpi, I., Peltonen, P.L., Majamaa, P.K. et al. (2004) Parkinsonism, premature menopause, and mitochondrial DNA polymerase gamma mutations: Clinical and molecular genetic study Lancet, 364, 875-882.
9. Pagnamenta, A.T., Taanman, J.W., Wilson, C.J., Anderson, N.E., Marotta, R., Duncan, A.J., Bitner-Glindzicz, M., Taylor, R.W., Laskowski, A., Thorburn, D.R. et al. (2006) Dominant inheritance of premature ovarian failure associated with mutant mitochondrial DNA polymerase gamma. Hum. Reprod., 21, 2467-2473.
10. Ponamarev, M.V., Longley, M.J., Nguyen, D., Kunkel, T.A. and Copeland, W.C. (2002) Active site mutation in DNA polymerase gamma associated with progressive external ophthalmoplegia causes error-prone DNA synthesis. J. Biol. Chem., 277, 15225-15228.
11. Graziewicz, M.A., Longley, M.J., Bienstock, R.J., Zeviani, M. and Copeland, W.C. (2004) Structure-function defects of human mitochondrial DNA polymerase in autosomal dominant progressive external ophthalmoplegia. Nat. Struct. Mol. Biol., 11, 770-776.
12. Lewis, W., Day, B.J., Kohler, J.J., Hosseini, S.H., Chan, S.S.L., Green, E., Haase, C.P., Keebaugh, E., Long, R., Ludaway, T. et al. (2007) MtDNA depletion, oxidative stress, cardiomyopathy, and death from transgenic cardiac targeted human mutant polymerase gamma. J. Clin. Invest., 87, 326-335.
13. Stuart, G.R., Santos, J.H., Strand, M.K., Van Houten, B. and Copeland, W.C. (2006) Mitochondrial DNA defects in S. cerevisiae with mutations in DNA polymerase gamma associated with Progressive External Ophthalmolplegia. Hum. Mol. Genet., 15, 363-374.
14. Baruffini, E., Lodi, T., Dallabona, C., Puglisi, A., Zeviani, M. and Ferrero, I. (2006) Genetic and chemical rescue of the Saccharomyces cerevisiae phenotype induced by mitochondrial DNA polymerase mutations associated with progressive external ophthalmoplegia in humans. Hum. Mol. Genet., 15, 2846-2855.
15. Beckman, K.B., Saljoughi, S., Mashiyama, S.T. and Ames, B.N. (2000) A simpler, more robust method for the analysis of 8-oxoguanine in DNA. Free Radic. Biol. Med., 29, 357-367.
16. Beckman, K.B. and Ames, B.N. (1999) Endogenous oxidative damage of mtDNA. Mutat. Res., 424, 51-58.
17. Pinz, K.G., Shibutani, S. and Bogenhagen, D.F. (1995) Action of mitochondrial DNA polymerase gamma at sites of base loss or oxidative damage. J. Biol. Chem., 270, 9202-9206.
18. Hsu, G.W., Ober, M., Carell, T. and Beese, L.S. (2004) Error-prone replication of oxidatively damaged DNA by a high-fidelity DNA polymerase. Nature, 431, 217-221.
19. Krahn, J.M., Beard, W.A., Miller, H., Grollman, A.P. and Wilson, S.H. (2003) Structure of DNA polymerase Beta with the mutagenic DNA lesion 8-oxodeoxyguanine reveals structural insights into its coding potential. Structure (Camb), 11, 121-127.
20. Brieba, L.G., Eichman, B.F., Kokoska, R.J., Doublie, S., Kunkel, T.A. and Ellenberger, T. (2004) Structural basis for the dual coding potential of 8-oxoguanosine by a high-fidelity DNA polymerase. EMBO J., 23, 3452-3461.
21. Furge, L.L. and Guengerich, F.P. (1997) Analysis of nucleotide insertion and extension at 8-oxo-7,8-dihydroguanine by replicative T7 polymerase exo- and human immunodeficiency virus-1 reverse transcriptase using steady-state and pre-steady-state kinetics. Biochemistry, 36 6475-6487.
22. Furge, L.L. and Guengerich, F.P. (1998) Pre-steady-state kinetics of nucleotide insertion following 8-oxo-7,8-dihydroguanine base pair mismatches by bacteriophage T7 DNA polymerase exo. Biochemistry, 37, 3567-3574.
23. Brieba, L.G., Kokoska, R.J., Bebenek, K., Kunkel, T.A. and Ellenberger, T. (2005) A lysine residue in the fingers subdomain of T7 DNA polymerase modulates the miscoding potential of 8-oxo-7,8-dihydroguanosine. Structure (Camb), 13, 1653-1659.
24. Lim, S.E., Ponamarev, M.V., Longley, M.J. and Copeland, W.C. (2003) Structural determinants in human DNA polymerase gamma account for mitochondrial toxicity from nucleoside analogs. J. Mol. Biol., 329, 45-57.
25. Hanes, J.W., Thal, D.M. and Johnson, K.A. (2006) Incorporation and replication of 8-Oxo-deoxyguanosine by the human mitochondrial DNA polymerase. J. Biol. Chem., 281, 36241-36248.
26. Boosalis, M.S., Petruska, J. and Goodman, M.F. (1987) DNA polymerase insertion fidelity. Gel assay for site-specific kinetics. J. Biol. Chem., 262, 14689-14696.
27. Lim, S.E. and Copeland, W.C. (2001) Differential incorporation and removal of antiviral deoxynucleotides by human DNA polymerase gamma. J. Biol. Chem., 276, 23616-23623.
28. Johnson, A.A., Ray, A.S., Hanes, J., Suo, Z., Colacino, J.M., Anderson, K.S. and Johnson, K.A. (2001) Toxicity of antiviral nucleoside analogs and the human mitochondrial DNA polymerase. J. Biol. Chem., 276 40847-40857.
29. Longley, M.J., Nguyen, D., Kunkel, T.A. and Copeland, W.C. (2001) The fidelity of human DNA polymerase gamma with and without exonucleolytic proofreading and the p55 accessory subunit. J Biol. Chem., 276 38555-38562.
30. Kang, D., Nishida, J., Iyama, A., Nakabeppu, Y., Furuichi, M., Fujiwara, T., Sekiguchi, M. and Takeshige, K. (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, 14659-14665.
31. Nakabeppu, Y., Sakumi, K. Sakamoto, K., Tsuchimoto, D., Tsuzuki, T. and Nakatsu, Y. (2006) Mutagenesis and carcinogenesis caused by the oxidation of nucleic acids. Biol. Chem., 387, 373-379.
32. Pavlov, Y.I., Minnick, D.T., Izuta, S. and Kunkel, T.A. (1994) DNA replication fidelity with 8-oxodeoxyguanosine triphosphate. Biochemistry, 33, 4695-4701.
33. Shibutani, S., Takeshita, M. and Grollman, A.P. (1991) Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature, 349, 431-434.
34. Zheng, W., Khrapko, K., Coller, H., Thilly, W.G. and Copeland, W.C. (2006) Origins of human mitochondrial point mutations as DNA polymerase gamma-mediated errors. Mutat. Res., 599, 11-20.
35. Bohr, V.A. (2002) Repair of oxidative DNA damage in nuclear and mitochondrial DNA, and some changes with aging in mammalian cells. Free Radic. Biol. Med., 32, 804-812.
36. O'Rourke, T.W., Doudican, N.A., Mackereth, M.D., Doetsch, P.W. and Shadel, G.S. (2002) Mitochondrial dysfunction due to oxidative mitochondrial DNA damage is reduced through cooperative actions of diverse proteins. Mol. Cell. Biol., 22, 4086-4093.
37. Doudican, N.A., Song, B., Shadel, G.S. and Doetsch, P.W. (2005) Oxidative DNA damage causes mitochondrial genomic instability in Saccharomyces cerevisiae. Mol. Cell. Biol., 25, 5196-5204.
38. Croteau, D.L., Stierum, R.H. and Bohr, V.A. (1999) Mitochondrial DNA repair pathways. Mutat. Res., 434, 137-148.
39. Yamaguchi, H., Kajitani, K., Dan, Y., Furuichi, M., Ohno, M., Sakumi K., Kang, D. and Nakabeppu, Y. (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, 551-563.
40. de Souza-Pinto, N.C., Eide, L., Hogue, B.A., Thybo, T., Stevnsner, T., Seeberg, E., Klungland, A. and Bohr, V.A. (2001) Repair of 8-oxodeoxyguanosine lesions in mitochondrial DNA depends on the oxoguanine dna glycosylase (OGG1) gene and 8-oxoguanine accumulates in the mitochondrial DNA of OGG1-defective mice. Cancer Res., 61 5378-5381.
41. Karahalil, B., de Souza-Pinto, N.C., Parsons, J.L., Elder, R.H. and Bohr, V.A. (2003) Compromised incision of oxidized pyrimidines in liver mitochondria of mice deficient in NTH1 and OGG1 glycosylases. J. Biol. Chem., 278, 33701-33707.
42. Wang, Y., Reddy, S., Beard, W.A., Wilson, S.H. and Schlick, T. (2007) Differing conformational pathways before and after chemistry for insertion of dATP vs. dCTP opposite 8-oxoG in DNA polymerase β. Biophys. J., 92, 3063-3070.
43. Wanrooij, S., Luoma, P., van Goethem, G., van Broeckhoven, C., Suomalainen, A. and Spelbrink, J.N. (2004) Twinkle and POLG defects enhance age-dependent accumulation of mutations in the control region of mtDNA. Nucleic Acids Res., 32, 3053-3064.
44. Mancuso, M., Filosto, M., Oh, S.J. and DiMauro, S. (2004) A novel polymerase gamma mutation in a family with ophthalmoplegia, neuropathy, and Parkinsonism. Arch. Neurol., 61, 1777-1779.
45. Davidzon, G., Greene, P., Mancuso, M., Klos, K.J., Ahlskog, J.E., Hirano, M. and Dimauro, S. (2006) Early-onset familial parkinsonism due to POLG mutations. Ann. Neurol., 59, 859-862.
46. Tiangyou, W., Hudson, G., Ghezzi, D., Ferrari, G., Zeviani, M., Burn, D.J. and Chinnery, P.F. (2006) POLG1 in idiopathic Parkinson disease. Neurology, 67, 1698-1700.
47. DiMauro, S. (1993) Mitochondrial involvement in Parkinson's disease: The controversy continues. Neuolbgy, 43, 2170-2172.
48. Bender, A., Krishnan, K.J., Morris, C.M., Taylor, G.A., Reeve, A.K., Perry, R.H., Jaros, E., Hersheson, J.S., Betts, J., Klopstock, T. et al. (2006) High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nat. Genet., 38 515-517.
49. Kraytsberg, Y., Kudryavtseva, E., McKee, A.C., Geula, C., Kowall, N.W. and Khrapko, K. (2006) Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neurons. Nat. Genet., 38, 518-520.
50. Vyas, I., Heikkila, R.E. and Nicklas, W.J. (1986) Studies on the neurotoxicity of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine: inhibition of NAD-linked substrate oxidation by its metabolite, 1-methyl-4-phenylpyridinium. J. Neurochem., 46, 1501-1507.
51. Greene, J.G., Dingledine, R. and Greenamyer, J.T. (2005) Gene expression profiling of rat midbrain dopamine neurons: Implications for selective vulnerability in parkinsonism. Neurobiol. Dis., 18, 19-31.
52. Nakabeppu, Y., Tsuchimoto, D., Yamaguchi, H. and Saktimi, K. (2007) Oxidative damage in nucleic acids and Parkinson's disease. J. Neurosci. Res., 85, 919-934.
53. Fukae, J., Mizuno, Y. and Hattori, N. (2007) Mitochondrial dysfunction in Parkinson's disease. Mitochondrion, 7, 58-62.
54. Shimura-Miura, H., Hattori, N., Kang, D., Miyako, K., Nakabeppu, Y. and Mizuno, Y. (1999) Increased 8-oxo-dGTPase in the mitochondria of substantia nigral neurons in Parkinson's disease. Ann. Neurol., 46, 920-924.
55. Alam, Z.I., Jenner, A., Daniel, S.E., Lees, A.J., Cairns, N., Marsden, C.D., Jenner, P. and Halliwell, B. (1997) Oxidative DNA damage in the parkinsonian brain: An apparent selective increase in 8-hydroxyguanine levels in substantia nigra. J. Neurochem., 69, 1196-1203.
56. Zhang, J., Perry, G., Smith, M.A., Robertson, D., Olson, S.J., Graham, D.G. and Montine, T.J. (1999) Parkinson's disease is associated with oxidative damage to cytoplasmic DNA and RNA in substantia nigra neurons. Am. J. Pathol., 154, 1423-1429.
57. Shults, C.W., Oakes, D., Kieburtz, K., Beal, M.F.,Haas, R., Plumb, S., Juncos, J.L., Nutt, J., Shoulson, I., Carter, J. et al., (2002) Effects of coenzyme Q10 in early Parkinson disease: Evidence of slowing of the functional decline. Arch. Neurol., 59, 1541-1550.
58. Longley, M.J., Ropp, P.A., Lim, S.E. and Copeland, W.C. (1998) Characterization of the native and recombinant catalytic subunit of human DNA polymerase gamma: Identification of residues critical for exonuclease activity and dideoxymicleotide sensitivity. Biochemistry 37, 10529-10539.
59. Lim, S.E., Longley, M.J. and Copeland, W.C. (1999) The mitochondrial p55 accessory subunit of human DNA polymerase gamma enhances DNA binding, promotes processive DNA synthesis, and confers N-ethylmaleimide resistance. J. Biol. Chem., 274, 38197-38203.
60. Graziewicz, M.A., Sayer, J.M., Jerina, D.M. and Copeland, W.C. (2004) Nucleotide incorporation by human DNA polymerase gamma opposite benzo[a]pyrene and benzo[c]phenanthrene diol epoxide adducts of deoxyguanosine and deoxyadenosine. Nucleic Acids Res., 32, 397-405.
61. Reardon, J.E. and Miller, W.H. (1990) Human immunodeficiency virus reverse transcriptase. Substrate and inhibitor kinetics with thymidine 5′-triphosphate and 3′-azido-3′-deoxythymidine 5′-triphosphate. J. Biol. Chem., 265, 20302-20307.
62. Holm, L. and Sander, C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol., 233, 123-138.
63. Notredame, C., Higgins, D.G. and Heringa, J. (2000) T-Coffee: A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol., 302, 205-217.
64. Hooft, R.W., Vriend, G., Sander, C. and Abola, E.E. (1996) Errors in protein structures. Nature, 381, 272.
65. Rodriguez, R., Chinea, G., Lopez, N., Pons, T. and Vriend, G. (1998) Homology modeling, model and software evaluation: Three related resources. Bioinformatics, 14, 523-528.
66. Sali, A. and Blundell, T.L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol., 234, 779-815.
67. Luthy, R., Bowie, J.U. and Eisenberg, D. (1992) Assessment of protein models with three-dimensional profiles. Nature, 356, 83-85.
68. Shen, M.Y. and Sali, A. (2006) Statistical potential for assessment and prediction of protein structures. Protein Sci., 15, 2507-2524.