Age- and tissue-specific changes in mitochondrial and nuclear DNA base excision repair activity in mice: Susceptibility of skeletal muscles to oxidative injury

Mechanisms of Ageing and Development

Volumn 131, Issue 5, 2010, Pages 330-337

  Szczesny, Bartosz ^a   Tann, Anne W ^a   Mitra, Sankar ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Aging; Base excision repair; Mitochondria; Oxidative stress; Sarcopenia

Indexed keywords

CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; MANGANESE SUPEROXIDE DISMUTASE;

AGING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; ENZYME LOCALIZATION; EXCISION REPAIR; HEART; KIDNEY; MALE; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; PROTEIN EXPRESSION; QUADRICEPS FEMORIS MUSCLE; SKELETAL MUSCLE;

AGING; ANIMALS; CELL NUCLEUS; CITRATE (SI)-SYNTHASE; DNA REPAIR; DNA, MITOCHONDRIAL; MALE; MICE; MICE, INBRED BALB C; MUSCLE, SKELETAL; OXIDATIVE STRESS; SUPEROXIDE DISMUTASE;

ANIMALIA; MUS;

EID: 77953036663     PISSN: 00476374     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mad.2010.03.009     Document Type: Article

References (53)

1. Akbari M., Otterlei M., Pena-Diaz J., Aas P.A., Kavli B., Liabakk N.B., Hagen L., Imai K., Durandy A., Slupphaug G., Krokan H.E. Repair of U/G and U/A in DNA by UNG2-associated repair complexes takes place predominantly by short-patch repair both in proliferating and growth-arrested cells. Nucleic Acids Res. 2004, 32:5486-5498.
2. Akbari M., Visnes T., Krokan H.E., Otterlei M. Mitochondrial base excision repair of uracil and AP sites takes place by single-nucleotide insertion and long-patch DNA synthesis. DNA Repair (Amst.) 2008, 7:605-616.
3. Almeida K.H., Sobol R.W. A unified view of base excision repair: lesion-dependent protein complexes regulated by post-translational modification. DNA Repair (Amst.) 2007, 6:695-711.
4. Cabelof D.C., Raffoul J.J., Yanamadala S., Ganir C., Guo Z., Heydari A.R. Attenuation of DNA polymerase beta-dependent base excision repair and increased DMS-induced mutagenicity in aged mice. Mutat. Res. 2002, 500:135-145.
5. Carrillo M.C., Kanai S., Sato Y., Kitani K. Age-related changes in antioxidant enzyme activities are region and organ, as well as sex, selective in the rat. Mech. Ageing Dev. 1992, 65:187-198.
6. Chabi B., Ljubicic V., Menzies K.J., Huang J.H., Saleem A., Hood D.A. Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell 2008, 7:2-12.
7. Charge S.B., Brack A.S., Hughes S.M. Aging-related satellite cell differentiation defect occurs prematurely after Ski-induced muscle hypertrophy. Am. J. Physiol. Cell Physiol. 2002, 283:C1228-C1241.
8. Choksi K.B., Nuss J.E., Deford J.H., Papaconstantinou J. Age-related alterations in oxidatively damaged proteins of mouse skeletal muscle mitochondrial electron transport chain complexes. Free Radic. Biol. Med. 2008, 45:826-838.
9. Chua W.C., Liu L., Mansfield K.J., Vaux K.J., Moore K.H., Millard R.J., Burcher E. Age-related changes of P2X(1) receptor mRNA in the bladder detrusor from men with and without bladder outlet obstruction. Exp. Gerontol. 2007, 42:686-692.
10. Cristiano F., de Haan J.B., Iannello R.C., Kola I. Changes in the levels of enzymes which modulate the antioxidant balance occur during aging and correlate with cellular damage. Mech. Ageing Dev. 1995, 80:93-105.
11. de Souza-Pinto N.C., Harris C.C., Bohr V.A. p53 functions in the incorporation step in DNA base excision repair in mouse liver mitochondria. Oncogene 2004, 23:6559-6568.
12. Fan Z., Beresford P.J., Zhang D., Xu Z., Novina C.D., Yoshida A., Pommier Y., Lieberman J. Cleaving the oxidative repair protein Ape1 enhances cell death mediated by granzyme A. Nat. Immunol. 2003, 4:145-153.
13. Fortini P., Dogliotti E. Base damage and single-strand break repair: mechanisms and functional significance of short- and long-patch repair subpathways. DNA Repair (Amst.) 2007, 6:398-409.
14. Frosina G., Fortini P., Rossi O., Carrozzino F., Raspaglio G., Cox L.S., Lane D.P., Abbondandolo A., Dogliotti E. Two pathways for base excision repair in mammalian cells. J. Biol. Chem. 1996, 271:9573-9578.
15. Goodrick C.L. Life-span and the inheritance of longevity of inbred mice. J. Gerontol. 1975, 30:257-263.
16. Gordon D.M., Wang J., Amutha B., Pain D. Self-association and precursor protein binding of Saccharomyces cerevisiae Tom40p, the core component of the protein translocation channel of the mitochondrial outer membrane. Biochem. J. 2001, 356:207-215.
17. Hawke T.J., Garry D.J. Myogenic satellite cells: physiology to molecular biology. J. Appl. Physiol. 2001, 91:534-551.
18. Hayakawa M., Torii K., Sugiyama S., Tanaka M., Ozawa T. Age-associated accumulation of 8-hydroxydeoxyguanosine in mitochondrial DNA of human diaphragm. Biochem. Biophys. Res. Commun. 1991, 179:1023-1029.
19. Hegde M.L., Hazra T.K., Mitra S. Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells. Cell Res. 2008, 18:27-47.
20. Herbst A., Pak J.W., McKenzie D., Bua E., Bassiouni M., Aiken J.M. Accumulation of mitochondrial DNA deletion mutations in aged muscle fibers: evidence for a causal role in muscle fiber loss. J. Gerontol. A: Biol. Sci. Med. Sci. 2007, 62:235-245.
21. Hiona A., Leeuwenburgh C. The role of mitochondrial DNA mutations in aging and sarcopenia: implications for the mitochondrial vicious cycle theory of aging. Exp. Gerontol. 2008, 43:24-33.
22. Holloszy J.O., Oscai L.B., Don I.J., Mole P.A. Mitochondrial citric acid cycle and related enzymes: adaptive response to exercise. Biochem. Biophys. Res. Commun. 1970, 40:1368-1373.
23. Hughes V.A., Frontera W.R., Roubenoff R., Evans W.J., Singh M.A. Longitudinal changes in body composition in older men and women: role of body weight change and physical activity. Am. J. Clin. Nutr. 2002, 76:473-481.
24. Imam S.Z., Karahalil B., Hogue B.A., Souza-Pinto N.C., Bohr V.A. Mitochondrial and nuclear DNA-repair capacity of various brain regions in mouse is altered in an age-dependent manner. Neurobiol. Aging 2006, 27:1129-1136.
25. Intano G.W., Cho E.J., McMahan C.A., Walter C.A. Age-related base excision repair activity in mouse brain and liver nuclear extracts. J. Gerontol. A: Biol. Sci. Med. Sci. 2003, 58:205-211.
26. Izumi T., Mitra S. Deletion analysis of human AP-endonuclease: minimum sequence required for the endonuclease activity. Carcinogenesis 1998, 19:525-527.
27. Karahalil B., Hogue B.A., de Souza-Pinto N.C., Bohr V.A. Base excision repair capacity in mitochondria and nuclei: tissue-specific variations. FASEB J. 2002, 16:1895-1902.
28. Katayama M., Tanaka M., Yamamoto H., Ohbayashi T., Nimura Y., Ozawa T. Deleted mitochondrial DNA in the skeletal muscle of aged individuals. Biochem. Int. 1991, 25:47-56.
29. Kowaltowski A.J., de Souza-Pinto N.C., Castilho R.F., Vercesi A.E. Mitochondria and reactive oxygen species. Free Radic. Biol. Med. 2009, 47:333-343.
30. Lee C.M., Chung S.S., Kaczkowski J.M., Weindruch R., Aiken J.M. Multiple mitochondrial DNA deletions associated with age in skeletal muscle of rhesus monkeys. J. Gerontol. 1993, 48:B201-B205.
31. Liu P., Qian L., Sung J.S., de Souza-Pinto N.C., Zheng L., Bogenhagen D.F., Bohr V.A., Wilson D.M., Shen B., Demple B. Removal of oxidative DNA damage via FEN1-dependent long-patch base excision repair in human cell mitochondria. Mol. Cell. Biol. 2008, 28:4975-4987.
32. Marzetti E., Leeuwenburgh C. Skeletal muscle apoptosis, sarcopenia and frailty at old age. Exp. Gerontol. 2006, 41:1234-1238.
33. Moore D.H., Michael H., Tritt R., Parsons S.H., Kelley M.R. Alterations in the expression of the DNA repair/redox enzyme APE/ref-1 in epithelial ovarian cancers. Clin. Cancer Res. 2000, 6:602-609.
34. Muradian K.K., Utko N.A., Fraifeld V., Mozzhukhina T.G., Pishel I.N., Litoshenko A.Y. Superoxide dismutase, catalase and glutathione peroxidase activities in the liver of young and old mice: linear regression and correlation. Arch. Gerontol. Geriatr. 2002, 35:205-214.
35. Nadal-Ginard B., Kajstura J., Leri A., Anversa P. Myocyte death, growth, and regeneration in cardiac hypertrophy and failure. Circ. Res. 2003, 92:139-150.
36. Nakamura J., Swenberg J.A. Endogenous apurinic/apyrimidinic sites in genomic DNA of mammalian tissues. Cancer Res. 1999, 59:2522-2526.
37. Narciso L., Fortini P., Pajalunga D., Franchitto A., Liu P., Degan P., Frechet M., Demple B., Crescenzi M., Dogliotti E. Terminally differentiated muscle cells are defective in base excision DNA repair and hypersensitive to oxygen injury. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:17010-17015.
38. Pinz K.G., Bogenhagen D.F. Efficient repair of abasic sites in DNA by mitochondrial enzymes. Mol. Cell. Biol. 1998, 18:1257-1265.
39. Radak Z., Apor P., Pucsok J., Berkes I., Ogonovszky H., Pavlik G., Nakamoto H., Goto S. Marathon running alters the DNA base excision repair in human skeletal muscle. Life Sci. 2003, 72:1627-1633.
40. Radak Z., Kumagai S., Nakamoto H., Goto S. 8-Oxoguanosine and uracil repair of nuclear and mitochondrial DNA in red and white skeletal muscle of exercise-trained old rats. J. Appl. Physiol. 2007, 102:1696-1701.
41. Ramana C.V., Boldogh I., Izumi T., Mitra S. Activation of apurinic/apyrimidinic endonuclease in human cells by reactive oxygen species and its correlation with their adaptive response to genotoxicity of free radicals. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:5061-5066.
42. Raue U., Slivka D., Jemiolo B., Hollon C., Trappe S. Proteolytic gene expression differs at rest and after resistance exercise between young and old women. J. Gerontol. A: Biol. Sci. Med. Sci. 2007, 62:1407-1412.
43. Rikans L.E., Moore D.R., Snowden C.D. Sex-dependent differences in the effects of aging on antioxidant defense mechanisms of rat liver. Biochim. Biophys. Acta 1991, 1074:195-200.
44. Schulke N., Sepuri N.B., Gordon D.M., Saxena S., Dancis A., Pain D. A multisubunit complex of outer and inner mitochondrial membrane protein translocases stabilized in vivo by translocation intermediates. J. Biol. Chem. 1999, 274:22847-22854.
45. Short K.R., Bigelow M.L., Kahl J., Singh R., Coenen-Schimke J., Raghavakaimal S., Nair K.S. Decline in skeletal muscle mitochondrial function with aging in humans. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:5618-5623.
46. Sinitsyna O., Krysanova Z., Ishchenko A., Dikalova A.E., Stolyarov S., Kolosova N., Vasunina E., Nevinsky G. Age-associated changes in oxidative damage and the activity of antioxidant enzymes in rats with inherited overgeneration of free radicals. J. Cell. Mol. Med. 2006, 10:206-215.
47. Stierum R.H., Dianov G.L., Bohr V.A. Single-nucleotide patch base excision repair of uracil in DNA by mitochondrial protein extracts. Nucleic Acids Res. 1999, 27:3712-3719.
48. Sung J.S., Demple B. Roles of base excision repair subpathways in correcting oxidized abasic sites in DNA. FEBS J. 2006, 273:1620-1629.
49. Szczesny B., Bhakat K.K., Mitra S., Boldogh I. Age-dependent modulation of DNA repair enzymes by covalent modification and subcellular distribution. Mech. Ageing Dev. 2004, 125:755-765.
50. Szczesny B., Hazra T.K., Papaconstantinou J., Mitra S., Boldogh I. Age-dependent deficiency in import of mitochondrial DNA glycosylases required for repair of oxidatively damaged bases. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:10670-10675.
51. Szczesny B., Mitra S. Effect of aging on intracellular distribution of abasic (AP) endonuclease 1 in the mouse liver. Mech. Ageing Dev. 2005, 126:1071-1078.
52. Szczesny B., Tann A.W., Longley M.J., Copeland W.C., Mitra S. Long patch base excision repair in mammalian mitochondrial genomes. J. Biol. Chem. 2008, 283:26349-26356.
53. Touchberry C.D., Wacker M.J., Richmond S.R., Whitman S.A., Godard M.P. Age-related changes in relative expression of real-time PCR housekeeping genes in human skeletal muscle. J. Biomol. Tech. 2006, 17:157-162.