Caloric restriction promotes genomic stability by induction of base excision repair and reversal of its age-related decline

DNA Repair

Volumn 2, Issue 3, 2003, Pages 295-307

  Cabelof, Diane C ^a   Yanamadala, Sunitha ^a,c   Raffoul, Julian J ^a   Guo, ZhongMao ^b   Soofi, Abdulsalam ^a,d   Heydari, Ahmad R ^a  

^a WAYNE STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Aging; Base excision repair; Caloric restriction; DNA polymerase ; Mutation frequency

Indexed keywords

2 NITROPROPANE; CARCINOGEN; DIMETHYL SULFATE; DNA DIRECTED DNA POLYMERASE BETA; MESSENGER RNA;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BRAIN; CALORIC RESTRICTION; CANCER PREVENTION; CONTROLLED STUDY; DNA REPAIR; ENZYME ACTIVITY; ENZYME ASSAY; EXCISION REPAIR; FEEDING; GENETIC STABILITY; HORMESIS; LIVER; MALE; MUTATION RATE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; REGULATORY MECHANISM; SPLEEN; TESTIS; UPREGULATION;

AGING; ANIMALS; CALORIC RESTRICTION; DNA; DNA POLYMERASE BETA; DNA REPAIR; MALE; MICE; MICE, INBRED C57BL; MUTAGENS; MUTATION; NITROPARAFFINS; PROPANE; RATS; RATS, INBRED F344; SULFURIC ACID ESTERS; UP-REGULATION;

ANIMALIA; RODENTIA; ZIZIPHUS MAURITIANA;

EID: 0037353433     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1568-7864(02)00219-7     Document Type: Article

References (44)

1. Weindruch R. Dietary restriction, tumors, and aging in rodents. J. Gerontol. 44:1989;67-71.
2. Weindruch R. Effect of caloric restriction on age-associated cancers. Exp. Gerontol. 27:1992;575-581.
3. Manjgaladze M., Chen S., Frame L.T., Seng J.E., Duffy P.H., Feuers R.J., Hart R.W., Leakey J.E. Effects of caloric restriction on rodent drug and carcinogen metabolizing enzymes: implications for mutagenesis and cancer. Mutat. Res. 295:1993;201-222.
4. Haley-Zitlin V., Richardson A. Effect of dietary restriction on DNA repair and DNA damage. Mutat. Res. 295:1993;237-245.
5. Raffoul J.J., Guo Z., Soofi A., Heydari A.R. Caloric restriction and genomic stability. J. Nutr. Health Aging. 3:1999;100-109.
6. Chung M.H., Kasai H., Nishimura S., Yu B.P. Protection of DNA damage by dietary restriction. Free Radic. Biol. Med. 12:1992;523-525.
7. Melov S., Hinerfeld D., Esposito L., Wallace D.C. Multi-organ characterization of mitochondrial genomic rearrangements in ad libitum and caloric restricted mice show striking somatic mitochondrial DNA rearrangements with age. Nucl. Acids Res. 25:1997;974-982.
8. Kang C.M., Kristal B.S., Yu B.P. Age-related mitochondrial DNA deletions: effect of dietary restriction. Free Radic. Biol. Med. 24:1998;148-154.
9. Hamilton M.L., Van Remmen H., Drake J.A., Yang H., Guo Z.M., Kewitt K., Walter C.A., Richardson A. Does oxidative damage to DNA increase with age? Proc. Natl. Acad. Sci. U.S.A. 98:2001;10469-10474.
10. Dempsey J.L., Pfeiffer M., Morley A.A. Effect of dietary restriction on in vivo somatic mutation in mice. Mutat. Res. 291:1993;141-145.
11. Casciano D.A., Chou M., Lyn-Cook L.E., Aidoo A. Calorie restriction modulates chemically induced in vivo somatic mutation frequency. Environ. Mol. Mutagen. 27:1996;162-164.
12. Licastro F., Weindruch R., Davis L.J., Walford R.L. Effect of dietary restriction upon the age-associated decline of lymphocyte DNA repair activity in mice. Age. 11:1988;48-52.
13. Weraarchakul N., Strong R., Wood W.G., Richardson A. The effect of aging and dietary restriction on DNA repair. Exp. Cell. Res. 181:1989;197-204.
14. Lipman J.M., Turturro A., Hart R.W. The influence of dietary restriction on DNA repair in rodents: a preliminary study. Mech. Aging Dev. 48:1989;135-143.
15. Tilley R., Miller S., Srivastava V., Busbee D. Enhanced unscheduled DNA synthesis by secondary cultures of lung cells established from calorically restricted aged rats. Mech. Aging. Dev. 63:1992;165-176.
16. Asakura S., Sawada S., Daimon H., Fukuda T., Ogura K., Yamatsu K., Furihata C. Effects of dietary restriction on induction of unscheduled DNA synthesis (UDS) and replicative DNA synthesis (RDS) in rat liver. Mutat. Res. 322:1994;257-264.
17. Guo Z., Heydari A., Richardson A. Nucleotide excision repair of actively transcribed versus nontranscribed DNA in rat hepatocytes: effect of age and dietary restriction. Exp. Cell. Res. 245:1998;228-238.
18. Singhal R.K., Prasad R., Wilson S.H. DNA polymerase β conducts the gap-filling step in uracil-initiated base excision repair in a bovine testis nuclear extract. J. Biol. Chem. 270:1995;949-957.
19. Klungland A., Lindahl T. Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1). EMBO J. 16:1997;3341-3348.
20. Dianov G.L., Jensen B.R., Kenny M.K., Bohr V.A. Replication protein A stimulates proliferating cell nuclear antigen-dependent repair of abasic sites in DNA by human cell extracts. Biochemistry. 38:1999;1021-11025.
21. Horton J.K., Prasad R., Hou E., Wilson S.H. Protection against methylation-induced cytotoxicity by DNA polymerase beta-dependent long patch base excision repair. J. Biol. Chem. 275:2000;2211-2218.
22. Podlutsky A.J., Dianova I.I., Podust V.N., Bohr V.A., Dianov G.L. Human DNA polymerase beta initiates DNA synthesis during long-patch repair of reduced AP sites in DNA. EMBO J. 20:2001;1477-1482.
23. Srivastava D.K., Vande Berg B.J., Prasad R., Molina J.T., Beard W.A., Tomkinson A.E., Wilson S.H. Mammalian abasic site base excision repair, identification of the reaction sequence and rate-determining steps. J. Biol. Chem. 273:1998;21203-21209.
24. 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. 500:2002;135-145.
25. Cao S.X., Dhahbi J.M., Mote P.L., Spindler S.R. Genomic profiling of short- and long-term caloric restriction effects in the liver of aging mice. Proc. Natl. Acad. Sci. U.S.A. 98:2001;10630-10635.
26. Heydari A.R., You S., Takahashi R., Gutsmann A., Sarge K.D., Richardson A. Effect of caloric restriction on the expression of heat shock protein 70 and the activation of heat shock transcription factor 1. Dev. Genet. 18:1996;114-124.
27. Heydari A.R., Conrad C.C., Richardson A. Expression of heat shock genes in hepatocytes is affected by age and food restriction in rats. J. Nutr. 125:1995;410-418.
28. Heydari A.R., Wu B., Takahashi R., Strong R., Richardson A. Expression of heat shock protein 70 is altered by age and diet at the level of transcription. Mol. Cell. Biol. 13:1993;2909-2918.
29. Walter C.A., Intano G.W., McCarrey J.R., McMahan C.A., Walter R.B. Mutation frequency declines during spermatogenesis in young mice but increases in old mice. Proc. Natl. Acad. Sci. USA. 95:1998;10015-10019.
30. R.R. Sokal, F.J. Rohlf, Biometry, Freeman, New York, 1981, p. 244.
31. Karawya E., Swack J., Albert W., Fedorko J., Minna J.D., Wilson S.H. Identification of a higher molecular weight DNA polymerase alpha catalytic polypeptide in monkey cells by monoclonal antibody. Proc. Natl. Acad. Sci. U.S.A. 81:1984;7777-7781.
32. Tanabe K., Karawya E., Fewell J.W., Kuff E.L., Wislon S.H. DNA polymerase and simian virus 40 infection of resting monkey cells: induction of aphidicolin resistant alpha-polymerase. Nucl. Acids Res. 11:1983;8253-8268.
33. Cabelof D.C., Raffoul J.J., Yanamadala S., Guo Z., Heydari A.R. Induction of DNA polymerase beta-dependent base excision repair in response to oxidative stress in vivo. Carcinogenesis. 23:2002;1419-1425.
34. Prapurna D.R., Rao K.S. Long-term effects of caloric restriction initiated at different ages on DNA polymerases in rat brain. Mech. Aging. Dev. 92:1996;133-142.
35. Cabelof D.C., Guo Z., Raffoul J.J., Ganir C., Richardson A., Heydari A.R. Role of beta-pol-dependent base excision repair in the in vivo processing of damage induced by oxidative and alkylating agents. FASEB J. 15:2001;A401.
36. Sobol R.W., Horton J.K., Kuhn R., Gu H., Singhal R.K., Prasad R., Rajewsky K., Wilson S.H. Requirement of mammalian DNA polymerase-beta in base-excision repair. Nature. 379:1996;183-186.
37. Leakey J.A., Cunny J., Bazasre J., Webb P.J., Feuers R.J., Duffy P.H., Hart R.W. Effects of aging and caloric restriction on hepatic drug metabolizing enzymes in the fisher 344 rat. I. The cytochrome P-450 dependent monooxygenase system. Mech. Aging. Dev. 48:1989;145-155.
38. Shima N., Swiger R.R., Heddle J.A. Dietary restriction during murine development provides protection against MNU-induced mutations. Mutat. Res. 470:2000;189-200.
39. Stuart G.R., Oda Y., de Boer J.G., Glickman B.W. Mutation frequency and specificity with age in liver. Genetics. 154:2000;1291-1300.
40. Zhou J., Ahn J., Wilson S.H., Prives C. A role for p53 in base excision repair. EMBO J. 20:2001;914-923.
41. Offer H., Wolkowicz R., Matas D., Blumenstein S., Livneh Z., Rotter V. Direct involvement of p53 in the base excision repair pathway of the DNA repair machinery. FEBS Lett. 450:1999;197-204.
42. Tyner S.D., Venkatachalam S., Choi J., Jones S., Ghebranious N., Igelmann H., Lu X., Soron G., Cooper B., Brayton C., Hee Park S., Thompson T., Karsenty G., Bradley A., Donehower L.A. p53 mutant mice that display early ageing-associated phenotypes. Nature. 415:2002;45-53.
43. Hursting S.D., Perkins S.N., Phang J.M. Calorie restriction delays spontaneous tumorigenesis in p53-knockout transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 91:1994;7036-7040.
44. Hursting S.D., Perkins S.N., Brown C.C., Haines D.C., Phang J.M. Calorie restriction induces a p53-independent delay of spontaneous carcinogenesis in p53-deficient and wild-type mice. Cancer Res. 57:1997;2843-2846.