XRCC1 haploinsufficiency in mice has little effect on aging, but adversely modifies exposure-dependent susceptibility

Nucleic Acids Research

Volumn 39, Issue 18, 2011, Pages 7994-8002

  McNeill, Daniel R ^a   Lin, Ping Chang ^a   Miller, Marshall G ^b   Pistell, Paul J ^c   De Souza Pinto, Nadja C ^d   Fishbein, Kenneth W ^a   Spencer, Richard G ^a   Liu, Yie ^e   Pettan Brewer, Christina ^e   Ladiges, Warren C ^a   Wilson, David M ^a,b  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b TUFTS UNIVERSITY   (United States)

^c TOWSON UNIVERSITY   (United States)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

^e UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZOXYMETHANE; SCAFFOLD PROTEIN; XRCC1 PROTEIN; ALKYLATING AGENT; DNA BINDING PROTEIN; MUTAGENIC AGENT; X-RAY REPAIR CROSS COMPLEMENTING PROTEIN 1;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BLOOD CHEMISTRY; BODY WEIGHT; BRAIN SIZE; C57BL 6 MOUSE; CELL TYPE; CHROMOSOME; COLON TUMOR; CONTROLLED STUDY; DEVELOPMENT; DEVELOPMENTAL DISORDER; DISEASE PREDISPOSITION; DNA DAMAGE; DNA REPAIR; ENDODERM; ENVIRONMENTAL FACTOR; FEMALE; GENOTOXICITY; HAPLOINSUFFICIENCY; HETEROZYGOTE; LIFE EXPECTANCY; LIFESPAN; LIPID COMPOSITION; LIVER TOXICITY; LONGEVITY; MALE; MAMMAL; MESODERM; MOUSE; NONHUMAN; OXIDATION; PATHOGENESIS; PHENOTYPE; PRECANCER; PRIORITY JOURNAL; RUPTURE; SINGLE STRANDED DNA BREAK; TELOMERE; ANIMAL; ANIMAL BEHAVIOR; BONE MARROW CELL; BRAIN; C57BL MOUSE; CELL SURVIVAL; DRUG EFFECT; GENETICS; GENOMIC INSTABILITY; HISTOLOGY; METABOLISM; PATHOLOGY; TOXIC HEPATITIS;

ANIMALIA; MAMMALIA; MUS;

AGING; ALKYLATING AGENTS; ANIMALS; BEHAVIOR, ANIMAL; BODY WEIGHT; BONE MARROW CELLS; BRAIN; CELL SURVIVAL; DISEASE SUSCEPTIBILITY; DNA-BINDING PROTEINS; DRUG-INDUCED LIVER INJURY; FEMALE; GENOMIC INSTABILITY; HAPLOINSUFFICIENCY; MALE; MICE; MICE, INBRED C57BL; MUTAGENS;

EID: 80054053350     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr280     Document Type: Article

References (36)

1. Lindahl, T. (1993) Instability and decay of the primary structure of DNA. Nature, 362, 709-715. (Pubitemid 23125973)
2. Hoeijmakers, J.H. (2001) Genome maintenance mechanisms for preventing cancer. Nature, 411, 366-374. (Pubitemid 32467046)
3. Kulkarni, A. and Wilson, D.M. III (2008) The involvement of DNA-damage and-repair defects in neurological dysfunction. Am. J. Hum. Genet., 82, 539-566. (Pubitemid 351726119)
4. Wilson, D.M. III, Bohr, V.A. and McKinnon, P.J. (2008) DNA damage, DNA repair, ageing and age-related disease. Mech. Ageing Dev., 129, 349-352.
5. Wilson, D.M. III and Bohr, V.A. (2007) The mechanics of base excision repair, and its relationship to aging and disease. DNA Repair, 6, 544-559. (Pubitemid 46357056)
6. Tomkinson, A.E., Vijayakumar, S., Pascal, J.M. and Ellenberger, T. (2006) DNA ligases: structure, reaction mechanism, and function. Chem. Rev., 106, 687-699.
7. Caldecott, K.W. (2003) XRCC1 and DNA strand break repair. DNA Repair, 2, 955-969. (Pubitemid 37088158)
8. Lakshmipathy, U. and Campbell, C. (2000) Mitochondrial DNA ligase III function is independent of Xrcc1. Nucleic Acids Res., 28, 3880-3886.
9. Wilson, D.M. III (2007) Processing of nonconventional DNA strand break ends. Environ. Mol. Mutagen., 48, 772-782.
10. Caldecott, K.W. (2008) Single-strand break repair and genetic disease. Nat. Rev. Genet., 9, 619-631.
11. Shen, J., Gilmore, E.C., Marshall, C.A., Haddadin, M., Reynolds, J.J., Eyaid, W., Bodell, A., Barry, B., Gleason, D., Allen, K. et al. (2010) Mutations in PNKP cause microcephaly, seizures and defects in DNA repair. Nat. Genet., 42, 245-249.
12. Takashima, H., Boerkoel, C.F., John, J., Saifi, G.M., Salih, M.A., Armstrong, D., Mao, Y., Quiocho, F.A., Roa, B.B., Nakagawa, M. et al. (2002) Mutation of TDP1, encoding a topoisomerase I-dependent DNA damage repair enzyme, in spinocerebellar ataxia with axonal neuropathy. Nat. Genet., 32, 267-272.
13. Date, H., Onodera, O., Tanaka, H., Iwabuchi, K., Uekawa, K., Igarashi, S., Koike, R., Hiroi, T., Yuasa, T., Awaya, Y. et al. (2001) Early-onset ataxia with ocular motor apraxia and hypoalbuminemia is caused by mutations in a new HIT superfamily gene. Nat. Genet., 29, 184-188. (Pubitemid 32952656)
14. Moreira, M.C., Barbot, C., Tachi, N., Kozuka, N., Uchida, E., Gibson, T., Mendonca, P., Costa, M., Barros, J., Yanagisawa, T. et al. (2001) The gene mutated in ataxia-ocular apraxia 1 encodes the new HIT/Zn-finger protein aprataxin. Nat. Genet., 29, 189-193. (Pubitemid 32952657)
15. Kulkarni, A., McNeill, D.R., Gleichmann, M., Mattson, M.P. and Wilson, D.M. III (2008) XRCC1 protects against the lethality of induced oxidative DNA damage in nondividing neural cells. Nucleic Acids Res., 36, 5111-5121.
16. Lee, Y., Katyal, S., Li, Y., El-Khamisy, S.F., Russell, H.R., Caldecott, K.W. and McKinnon, P.J. (2009) The genesis of cerebellar interneurons and the prevention of neural DNA damage require XRCC1. Nat. Neurosci., 12, 973-980.
17. Ladiges, W.C. (2006) Mouse models of XRCC1 DNA repair polymorphisms and cancer. Oncogene, 25, 1612-1619.
18. Thompson, L.H. and West, M.G. (2000) XRCC1 keeps DNA from getting stranded. Mutat. Res., 459, 1-18. (Pubitemid 30085463)
19. Wilson, D.M. III and Thompson, L.H. (2007) Molecular mechanisms of sister-chromatid exchange. Mutat. Res., 616, 11-23. (Pubitemid 46198860)
20. Tebbs, R.S., Flannery, M.L., Meneses, J.J., Hartmann, A., Tucker, J.D., Thompson, L.H., Cleaver, J.E. and Pedersen, R.A. (1999) Requirement for the Xrcc1 DNA base excision repair gene during early mouse development. Dev. Biol., 208, 513-529. (Pubitemid 29184008)
21. Tkac, I., Starcuk, Z., Choi, I.Y. and Gruetter, R. (1999) In vivo H-1 NMR spectroscopy of rat brain at 1 ms echo time. Magn. Res. Med., 41, 649-656. (Pubitemid 29205710)
22. Rasband, W.S. and Image, J. U. S. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/(1997-2011).
23. Zijlmans, J.M., Martens, U.M., Poon, S.S., Raap, A.K., Tanke, H.J., Ward, R.K. and Lansdorp, P.M. (1997) Telomeres in the mouse have large inter-chromosomal variations in the number of T2AG3 repeats. Proc. Natl Acad. Sci. USA, 94, 7423-7428. (Pubitemid 27345331)
24. Jiang, J., Zhang, X., Yang, H. and Wang, W. (2009) Polymorphisms of DNA repair genes: ADPRT, XRCC1, and XPD and cancer risk in genetic epidemiology. Methods Mol. Biol., 471, 305-333.
25. Berquist, B.R., Singh, D.K., Fan, J., Kim, D., Gillenwater, E., Kulkarni, A., Bohr, V.A., Ackerman, E.J., Tomkinson, A.E. and Wilson, D.M. III (2010) Functional capacity of XRCC1 protein variants identified in DNA repair-deficient Chinese hamster ovary cell lines and the human population. Nucleic Acids Res., 38, 5023-5035.
26. Vartanian, V., Lowell, B., Minko, I.G., Wood, T.G., Ceci, J.D., George, S., Ballinger, S.W., Corless, C.L., McCullough, A.K. and Lloyd, R.S. (2006) The metabolic syndrome resulting from a knockout of the NEIL1 DNA glycosylase. Proc. Natl Acad. Sci. USA, 103, 1864-1869. (Pubitemid 43228784)
27. Enns, L.C., Morton, J.F., Mangalindan, R.S., McKnight, G.S., Schwartz, M.W., Kaeberlein, M.R., Kennedy, B.K., Rabinovitch, P.S. and Ladiges, W.C. (2009) Attenuation of age-related metabolic dysfunction in mice with a targeted disruption of the Cbeta subunit of protein kinase A. J. Gerontol. A Biol. Sci. Med. Sci., 64, 1221-1231.
28. Chen, J. and Huang, X.F. (2009) The signal pathways in azoxymethane-induced colon cancer and preventive implications. Cancer Biol. Ther., 8, 1313-1317.
29. Wilson, D.M. III, Kim, D., Berquist, B.R. and Sigurdson, A.J. (2010) Variation in base excision repair capacity. Mutat. Res., [Epub ahead of print].
30. Wilson, D.M. III and Thompson, L.H. (1997) Life without DNA repair. Proc. Natl Acad. Sci. USA, 94, 12754-12757. (Pubitemid 27518420)
31. McKinnon, P.J. (2009) DNA repair deficiency and neurological disease. Nat. Rev. Neurosci., 10, 100-112.
32. Fujimura, M., Morita-Fujimura, Y., Sugawara, T. and Chan, P.H. (1999) Early decrease of XRCC1, a DNA base excision repair protein, may contribute to DNA fragmentation after transient focal cerebral ischemia in mice. Stroke, 30, 2456-2462.
33. Li, N., Wu, H., Yang, S. and Chen, D. (2007) Ischemic preconditioning induces XRCC1, DNA polymerase-beta, and DNA ligase III and correlates with enhanced base excision repair. DNA Repair, 6, 1297-1306. (Pubitemid 47238684)
34. Dutra, A.V., Lin, H.F., Juo, S.H., Mohrenweiser, H., Sen, S. and Grewal, R.P. (2006) Analysis of the XRCC1 gene as a modifier of the cerebral response in ischemic stroke. BMC Med. Genet., 7, 78.
35. Mahabir, S., Abnet, C.C., Qiao, Y.L., Ratnasinghe, L.D., Dawsey, S.M., Dong, Z.W., Taylor, P.R. and Mark, S.D. (2007) A prospective study of polymorphisms of DNA repair genes XRCC1, XPD23 and APE/ref-1 and risk of stroke in Linxian, China. J. Epidemiol. Community Health, 61, 737-741. (Pubitemid 47122075)
36. Tebbs, R.S., Thompson, L.H. and Cleaver, J.E. (2003) Rescue of Xrcc1 knockout mouse embryo lethality by transgene-complementation. DNA Repair, 2, 1405-1417. (Pubitemid 37464817)