Aging results in differential regulation of DNA repair pathways in pachytene: Spermatocytes in the Brown Norway rat

Biology of Reproduction

Volumn 85, Issue 6, 2011, Pages 1269-1278

  Pau, Catriona ^a   Nagano, Makoto ^a   Robaire, Bernard ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Aging; Gene expression; Oxidative stress; Spermatocyte

Indexed keywords

8 HYDROXYDEOXYGUANOSINE;

AGED; AGING; ANIMAL CELL; ARTICLE; BROWN NORWAY RAT; CELL ISOLATION; CONTROLLED STUDY; DNA REPAIR; EXCISION REPAIR; GENE EXPRESSION; IMMUNOREACTIVITY; MALE; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PACHYTENE; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPERMATID; SPERMATOCYTE; UPREGULATION;

AGING; ANIMALS; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION; MALE; PACHYTENE STAGE; RATS; RATS, INBRED BN; SPERMATIDS; SPERMATOCYTES;

RATTUS NORVEGICUS;

EID: 84855400137     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.094219     Document Type: Article

References (52)

1. Molina RI, Martini AC, Tissera A, Olmedo J, Senestrari D, Fiol de Cuneo M, Ruiz RD. Semen quality and aging: analysis of 9.168 samples in Cordoba. Argentina. Arch Esp Urol 2010, 63: 214-222.
2. Cardona Maya W, Berdugo J, Cadavid Jaramillo A. The effects of male age on semen parameters: analysis of 1364 men attending an andrology center. Aging Male 2009, 12: 100-103.
3. Kidd SA, Eskenazi B, Wyrobek AJ. Effects of male age on semen quality and fertility: a review of the literature. Fertil Steril 2001, 75: 237-248.
4. Syntin P, Robaire B. Sperm structural and motility changes during aging in the Brown Norway rat. J Androl 2001, 22: 235-244.
5. Ford WC, North K, Taylor H, Farrow A, Hull MG, Golding J. Increasing paternal age is associated with delayed conception in a large population of fertile couples: evidence for declining fecundity in older men. The ALSPAC Study Team (Avon Longitudinal Study of Pregnancy and Childhood). Hum Reprod 2000, 15: 1703-1708.
6. Hassan MA, Killick SR. Effect of male age on fertility: evidence for the decline in male fertility with increasing age. Fertil Steril 2003, 79(suppl 3): 1520-1527.
7. Klonoff-Cohen HS, Natarajan L. The effect of advancing paternal age on pregnancy and live birth rates in couples undergoing in vitro fertilization or gamete intrafallopian transfer. Am J Obstet Gynecol 2004, 191: 507-514.
8. Baarends WM, van der Laan R, Grootegoed JA. DNA repair mechanisms and gametogenesis. Reproduction 2001, 121: 31-39.
9. Aitken RJ, De Iuliis GN. Origins and consequences of DNA damage in male germ cells. Reprod Biomed Online 2007, 14: 727-733.
10. Fisher HM, Aitken RJ. Comparative analysis of the ability of precursor germ cells and epididymal spermatozoa to generate reactive oxygen metabolites. J Exp Zool 1997, 277: 390-400.
11. Schoneich C. Reactive oxygen species and biological aging: a mechanistic approach. Exp Gerontol 1999, 34: 19-34.
12. Bauche F, Fouchard M, Jegou B. Antioxidant system in rat testicular cells. FEBS Lett 1994, 349: 392-396.
13. Vazquez-Memije ME, Capin R, Tolosa A, El-Hafidi M. Analysis of ageassociated changes in mitochondrial free radical generation by rat testis. Mol Cell Biochem 2008, 307: 23-30.
14. Weir CP, Robaire B. Spermatozoa have decreased antioxidant enzymatic capacity and increased reactive oxygen species production during aging in the Brown Norway rat. J Androl 2007, 28: 229-240.
15. Aitken RJ, Clarkson JS. Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J Reprod Fertil 1987, 81: 459-469.
16. Aitken RJ, Gordon E, Harkiss D, Twigg JP, Milne P, Jennings Z, Irvine DS. Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol Reprod 1998, 59: 1037-1046.
17. Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993, 362: 709-715.
18. Wang C, Leung A, Sinha-Hikim AP. Reproductive aging in the male Brown Norway rat: a model for the human. Endocrinology 1993; 133: 2773-2781.
19. Wright WW, Fiore C, Zirkin BR. The effect of aging on the seminiferous epithelium of the brown Norway rat. J Androl 1993, 14: 110-117.
20. Bellve AR, Cavicchia JC, Millette CA, O'Brien DA, Bhatnagar YM, Dym M. Spermatogenic cells of the prepubertal mouse, isolation and morphological characterization. J Cell Biol 1977, 74: 68-85.
21. Aguilar-Mahecha A, Hales BF, Robaire B. Expression of stress response genes in germ cells during spermatogenesis. Biol Reprod 2001, 65: 119-127.
22. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4: 249-264.
23. Bieber AM, Marcon L, Hales BF, Robaire B. Effects of chemotherapeutic agents for testicular cancer on the male rat reproductive system, spermatozoa, and fertility. J Androl 2006, 27: 189-200.
24. Saunders PT, Sharpe RM, Williams K, Macpherson S, Urquart H, Irvine DS, Millar MR. Differential expression of oestrogen receptor alpha and beta proteins in the testes and male reproductive system of human and non-human primates. Mol Hum Reprod 2001, 7: 227-236.
25. Brasnjevic I, Hof PR, Steinbusch HW, Schmitz C. Accumulation of nuclear DNA damage or neuron loss: molecular basis for a new approach to understanding selective neuronal vulnerability in neurodegenerative diseases. DNA Repair (Amst) 2008, 7: 1087-1097.
26. Moller P, Lohr M, Folkmann JK, Mikkelsen L, Loft S. Aging and oxidatively damaged nuclear DNA in animal organs. Free Radic Biol Med 2010, 48: 1275-1285.
27. Essers J, Vermeulen W, Houtsmuller AB. DNA damage repair: anytime, anywhere? Curr Opin Cell Biol 2006, 18: 240-246.
28. Almeida KH, Sobol RW. A unified view of base excision repair: lesiondependent protein complexes regulated by post-translational modification. DNA Repair (Amst) 2007, 6: 695-711.
29. Zharkov DO. Base excision DNA repair. Cell Mol Life Sci 2008; 65: 1544-1565.
30. Intano GW, McMahan CA, Walter RB, McCarrey JR, Walter CA. Mixed spermatogenic germ cell nuclear extracts exhibit high base excision repair activity. Nucleic Acids Res 2001, 29: 1366-1372.
31. Intano GW, McMahan CA, McCarrey JR, Walter RB, McKenna AE, Matsumoto Y, MacInnes MA, Chen DJ, Walter CA. Base excision repair is limited by different proteins in male germ cell nuclear extracts prepared from young and old mice. Mol Cell Biol 2002, 22: 2410-2418.
32. Cabelof DC, Raffoul JJ, Yanamadala S, Ganir C, Guo Z, Heydari AR. Attenuation of DNA polymerase beta-dependent base excision repair and increased DMS-induced mutagenicity in aged mice. Mutat Res 2002; 500: 135-145.
33. El-Domyati MM, Al-Din AB, Barakat MT, El-Fakahany HM, Xu J, Sakkas D. Deoxyribonucleic acid repair and apoptosis in testicular germ cells of aging fertile men: the role of the poly(adenosine diphosphateribosyl) ation pathway. Fertil Steril 2009, 91: 2221-2229.
34. Hsu GW, Ober M, Carell T, Beese LS. Error-prone replication of oxidatively damaged DNA by a high-fidelity DNA polymerase. Nature 2004, 431: 217-221.
35. Neeley WL, Essigmann JM. Mechanisms of formation, genotoxicity, and mutation of guanine oxidation products. Chem Res Toxicol 2006, 19: 491-505.
36. Walter CA, Intano GW, McCarrey JR, McMahan CA, Walter RB. Mutation frequency declines during spermatogenesis in young mice but increases in old mice. Proc Natl Acad Sci U S A 1998, 95: 10015-10019.
37. Walter CA, Intano GW, McMahan CA, Kelner K, McCarrey JR, Walter RB. Mutation spectral changes in spermatogenic cells obtained from old mice. DNA Repair (Amst) 2004, 3: 495-504.
38. Schmid TE, Eskenazi B, Baumgartner A, Marchetti F, Young S, Weldon R, Anderson D, Wyrobek AJ. The effects of male age on sperm DNA damage in healthy non-smokers. Hum Reprod 2007, 22: 180-187.
39. Zubkova EV, Robaire B. Effects of ageing on spermatozoal chromatin and its sensitivity to in vivo and in vitro oxidative challenge in the Brown Norway rat. Hum Reprod 2006, 21: 2901-2910.
40. Wyrobek AJ, Eskenazi B, Young S, Arnheim N, Tiemann-Boege I, Jabs EW, Glaser RL, Pearson FS, Evenson D. Advancing age has differential effects on DNA damage, chromatin integrity, gene mutations, and aneuploidies in sperm. Proc Natl Acad Sci U S A 2006, 103: 9601-9606.
41. Sugasawa K, Ng JM, Masutani C, Iwai S, van der Spek PJ, Eker AP, Hanaoka F, Bootsma D, Hoeijmakers JH. Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol Cell 1998, 2: 223-232.
42. Tanaka K, Miura N, Satokata I, Miyamoto I, Yoshida MC, Satoh Y, Kondo S, Yasui A, Okayama H, Okada Y. Analysis of a human DNA excision repair gene involved in group A xeroderma pigmentosum and containing a zinc-finger domain. Nature 1990, 348: 73-76.
43. Miyamoto I, Miura N, Niwa H, Miyazaki J, Tanaka K. Mutational analysis of the structure and function of the xeroderma pigmentosum group A complementing protein: identification of essential domains for nuclear localization and DNA excision repair. J Biol Chem 1992, 267: 12182-12187.
44. de Laat WL, Appeldoorn E, Sugasawa K, Weterings E, Jaspers NG, Hoeijmakers JH. DNA-binding polarity of human replication protein A positions nucleases in nucleotide excision repair. Genes Dev 1998; 12: 2598-2609.
45. Gorbunova V, Seluanov A, Mao Z, Hine C. Changes in DNA repair during aging. Nucleic Acids Res 2007, 35: 7466-7474.
46. Gillette TG, Yu S, Zhou Z, Waters R, Johnston SA, Reed SH. Distinct functions of the ubiquitin-proteasome pathway influence nucleotide excision repair. EMBO J 2006, 25: 2529-2538.
47. Reed SH, Gillette TG. Nucleotide excision repair and the ubiquitin proteasome pathway-do all roads lead to Rome? DNA Repair (Amst) 2007, 6: 149-156.
48. Niedernhofer LJ, Odijk H, Budzowska M, van Drunen E, Maas A, Theil AF, de Wit J, Jaspers NG, Beverloo HB, Hoeijmakers JH, Kanaar R. The structure-specific endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-link-induced double-strand breaks. Mol Cell Biol 2004; 24: 5776-5787.
49. Wang QE, Zhu Q, Wani G, El-Mahdy MA, Li J, Wani AA. DNA repair factor XPC is modified by SUMO-1 and ubiquitin following UV irradiation. Nucleic Acids Res 2005, 33: 4023-4034.
50. Xu G, Spivak G, Mitchell DL, Mori T, McCarrey JR, McMahan CA, Walter RB, Hanawalt PC, Walter CA. Nucleotide excision repair activity varies among murine spermatogenic cell types. Biol Reprod 2005; 73: 123-130.
51. Wang C, Sinha Hikim AP, Lue YH, Leung A, Baravarian S, Swerdloff RS. Reproductive aging in the Brown Norway rat is characterized by accelerated germ cell apoptosis and is not altered by luteinizing hormone replacement. J Androl 1999, 20: 509-518.
52. Steger K. Transcriptional and translational regulation of gene expression in haploid spermatids. Anat Embryol (Berl) 1999, 199: 471-487.