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Meiosis progression and donor age affect expression profile of DNA repair genes in bovine oocytes

Published online by Cambridge University Press:  14 May 2013

S. Bilotto ,
R. Boni ,
G.L. Russo  and
M.B. Lioi
S. Bilotto
Affiliation:
Department of Sciences, University of Basilicata, 85100 Potenza, Italy. Institute of Food Sciences, National Research Council, 83100 Avellino, Italy.
R. Boni*
Affiliation:
University of Basilicata, Via dell'Ateneo Lucano, 10–85100–Potenza, Italy.
G.L. Russo
Affiliation:
Institute of Food Sciences, National Research Council, 83100 Avellino, Italy.
M.B. Lioi
Affiliation:
Department of Sciences, University of Basilicata, 85100 Potenza, Italy.
*
All correspondence to: Raffaele Boni. University of Basilicata, Via dell'Ateneo Lucano, 10–85100–Potenza, Italy. Tel: +39 0971 205017. Fax: +39 0971 205099. e-mail: [email protected]
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Summary

Several genetic and physiological factors increase the risk of DNA damage in mammalian oocytes. Two critical events are: (i) meiosis progression, from maturation to fertilization, due to extensive chromatin remodelling during genome decondensation; and (ii) aging, which is associated with a progressive oxidative stress. In this work, we studied the transcriptional patterns of three genes, RAD51, APEX-1 and MLH1, involved in DNA repair mechanisms. The analyses were performed by real-time quantitative PCR (RT-qPCR) in immature and in vitro matured oocytes collected from 17 ± 3-month-old heifers and 94 ± 20-month-old cows. Batches of 30–50 oocytes for each group (three replicates) were collected from ovarian follicles of slaughtered animals. The oocytes were freed from cumulus cells at the time of follicle removal, or after in vitro maturation (IVM) carried out in M199 supplemented with 10% fetal calf serum, 10 IU luteinising hormone (LH)/ml, 0.1 IU follicle-stimulating hormone (FSH)/ml and 1 μg 17β-oestradiol/ml. Total RNA was extracted by Trizol method. The expression of bovine GAPDH gene was used as the internal standard, while primers for bovine RAD51, APEX-1 and MLH1 genes were designed from DNA sequences retrieved from GenBank. Results obtained indicate a clear up-regulation of RAD51, APEX-1 and MLH1 genes after IVM, ranging between two- and four-fold compared with germinal vesicle (GV) oocytes. However, only RAD51 showed a significant transcript increase between the immature oocytes collected from young or old individuals. This finding highlights RAD51 as a candidate gene marker for discriminating bovine immature oocytes in relation to the donor age.

Keywords

APEX-1BovineDNA repair genesIVMMLH1OocyteRAD5
Type
Research Article
Information
Zygote , Volume 23 , Issue 1 , February 2015 , pp. 11 - 18
Copyright
Copyright © Cambridge University Press 2013 

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References

Baerwald, A.R., Adams, G.P. & Pierson, R.A. (2003). Characterization of ovarian follicular wave dynamics in women. Biol. Reprod. 69, 1023–31.Google Scholar
Bernstein, H., Byerly, H.C., Hopf, F.A. & Michod, R.E. (1985). Genetic damage, mutation, and the evolution of sex. Science 229, 1277–81.Google Scholar
Bertram, C. & Hass, R. (2008). Cellular responses to reactive oxygen species-induced DNA damage and aging. Biol. Chem. 389, 211–20.Google Scholar
Bessho, T., Roy, R., Yamamoto, K., Kasai, H., Nishimura, S., Tano, K. & Mitra, S. (1993). Repair of 8-hydroxyguanine in DNA by mammalian N-methylpurine-DNA glycosylase. Proc. Natl. Acad. Sci. USA 90, 8901–4.Google Scholar
Best, B.P. (2009). Nuclear DNA damage as a direct cause of aging. Rejuvenation Res. 12, 199–208.Google Scholar
Boni, R., Cuomo, A. & Tosti, E. (2002). Developmental potential in bovine oocytes is related to cumulus–oocyte complex grade, calcium current activity, and calcium stores. Biol. Reprod. 66, 836–42.Google Scholar
Cortopassi, G.A. & Wang, E. (1996). There is substantial agreement among interspecies estimates of DNA repair activity. Mech. Ageing Dev. 91, 211–8.CrossRefGoogle ScholarPubMed
Cui, X.S., Li, X.Y., Yin, X.J., Kong, I.K., Kang, J.J. & Kim, N.H. (2007). Maternal gene transcription in mouse oocytes: genes implicated in oocyte maturation and fertilization. J. Reprod. Dev. 53, 405–18.Google Scholar
Darwash, A.O., Lamming, G.E. & Woolliams, J.A. (1997) Estimation of genetic variation in the interval from calving to postpartum ovulation of dairy cows. J. Dairy Sci. 80, 1227–34.Google Scholar
de Boer, J., Andressoo, J.O., de Wit, J., Huijmans, J., Beems, R.B., van Steeg, H., Weeda, G., van der Horst, G.T., van Leeuwen, W., Themmen, A.P., Meradji, M. & Hoeijmakers, J.H. (2002). Premature aging in mice deficient in DNA repair and transcription. Science 296, 1276–9.Google Scholar
Dumollard, R., Carroll, J., Duchen, M.R., Campbell, K. & Swann, K. (2009). Mitochondrial function and redox state in mammalian embryos. Semin. Cell. Dev. Biol. 20. 346–53.CrossRefGoogle ScholarPubMed
Edelmann, W., Cohen, P.E., Kane, M., Lau, K., Morrow, B., Bennett, S., Umar, A., Kunkel, T., Cattoretti, G., Chaganti, R., Pollard, J.W., Kolodner, R.D. & Kucherlapati, R. (1996). Meiotic pachytene arrest in MLH1-deficient mice. Cell 85, 1125–34.Google Scholar
El-Mouatassim, S., Bilotto, S., Russo, G.L., Tosti, E. & Menezo, Y. (2007). APEX/Ref-1 (apurinic/apyrimidic endonuclease DNA-repair gene) expression in human and ascidian (Ciona intestinalis) gametes and embryos. Mol. Hum. Reprod. 13, 549–56.Google Scholar
Erickson, B.H., Reynolds, R.A. & Murphree, R.L. (1976). Ovarian characteristics and reproductive performance of the aged cow. Biol. Reprod. 15, 555–60.Google Scholar
Espejel, S., Klatt, P., Ménissier-de Murcia, J., Martín-Caballero, J., Flores, J.M., Taccioli, G., de Murcia, G. & Blasco, M.A. (2004). Impact of telomerase ablation on organismal viability, aging, and tumorigenesis in mice lacking the DNA repair proteins PARP-1, Ku86, or DNA-PKcs. J. Cell Biol. 167, 627–638.Google Scholar
Grube, K. & Bürkle, A. (1992). Poly(ADP-ribose) polymerase activity in mononuclear leukocytes of 13 mammalian species correlates with species-specific life span. Proc. Natl. Acad. Sci. USA 89, 11759–63.Google Scholar
Harman, D. (2006). Aging: overview. Ann. N. Y. Acad. Sci. 928, 1–21.Google Scholar
Hart, R.W. & Setlow, R.B. (1974). Correlation between deoxyribonucleic acid excision-repair and life-span in a number of mammalian species. Proc. Natl. Acad. Sci. USA 71, 2169–73.CrossRefGoogle Scholar
Hsieh, P. (2001). Molecular mechanisms of DNA mismatch repair. Mutat. Res. 486, 71–87.Google Scholar
Hunter, N. & Borts, R.H. (1997). Mlh1 is unique among mismatch repair proteins in its ability to promote crossing-over during meiosis. Genes Dev. 11, 1573–82.Google Scholar
Jaroudi, S. & SenGupta, , , S. (2007). DNA repair in mammalian embryos. Mutat. Res. 635, 53–77.Google Scholar
Kan, R., Sun, X., Kolas, N.K., Avdievich, E., Kneitz, B., Edelmann, W. & Cohen, P.E. (2008). Comparative analysis of meiotic progression in female mice bearing mutations in genes of the DNA mismatch repair pathway. Biol. Reprod. 78, 462–71.Google Scholar
Kelley, M.R. & Parsons, S.H. (2001). Redox regulation of the DNA repair function of the human AP endonuclease Ape1/ref-1. Antioxid. Redox Signal. 3, 671–83.Google Scholar
Kujjo, L.L., Laine, T., Pereira, R.J., Kagawa, W., Kurumizaka, H., Yokoyama, S. & Perez, G.I. (2010). Enhancing survival of mouse oocytes following chemotherapy or aging by targeting Bax and Rad51. PLoS One 5, e9204.Google Scholar
Kujjo, L.L., Ronningen, R., Ross, P., Pereira, R.J., Rodriguez, R., Beyhan, Z., Goissis, M.D., Baumann, T., Kagawa, W., Camsari, C., Smith, G.W., Kurumizaka, H., Yokoyama, S., Cibelli, J.B. & Perez, G.I. (2012). RAD51 plays a crucial role in halting cell death program induced by ionizing radiation in bovine oocytes. Biol. Reprod. 86, 76, 1–11.Google Scholar
Leal, C., Mamo, S., Fair, T. & Lonergan, P. (2012). Gene expression in bovine oocytes and cumulus cells after meiotic inhibition with the cyclin-dependent kinase inhibitor butyrolactone I. Reprod. Domest. Anim. 47, 615–24.CrossRefGoogle ScholarPubMed
Malhi, P.S., Adams, G.P. & Singh, J. (2005). Bovine model for the study of reproductive aging in women: follicular, luteal, and endocrine characteristics. Biol. Reprod. 73, 45–53.CrossRefGoogle Scholar
Malhi, P.S., Adams, G.P., Pierson, R.A. & Singh, J. (2006). Bovine model of reproductive aging: response to ovarian synchronization and superstimulation. Theriogenology 66, 1257–66.CrossRefGoogle ScholarPubMed
Malhi, P.S., Adams, G.P., Mapletoft, R.J. & Singh, J. (2007). Oocyte developmental competence in a bovine model of reproductive aging. Reproduction 134, 233–9.Google Scholar
Mamo, S., Carter, F., Lonergan, P., Leal, C.L., Al Naib, A., McGettigan, P., Mehta, J.P., Evans, A.C. & Fair, T. (2011). Sequential analysis of global gene expression profiles in immature and in vitro matured bovine oocytes: potential molecular markers of oocyte maturation. BMC Genomics 12, 151.Google Scholar
Maynard, S., Schurman, S.H., Harboe, C., de Souza-Pinto, N.C. & Bohr, V.A. (2009). Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis 30, 2–10.Google Scholar
Memili, E., Dominko, T. & First, N.L. (1998). Onset of transcription in bovine oocytes and preimplantation embryos. Mol. Reprod. Dev. 51, 36–41.Google Scholar
Ménézo, Y., Dale, B. & Cohen, M. (2010). DNA damage and repair in human oocytes and embryos: a review. Zygote 18, 357–65.Google Scholar
Ozturk, S. & Demir, N. (2011). DNA repair mechanisms in mammalian germ cells. Histol. Histopathol. 26, 505–17.Google ScholarPubMed
Paciolla, M., Boni, R., Fusco, F., Pescatore, A., Poeta, L., Ursini, M.V., Lioi, M.B. & Miano, M.G. (2011). Nuclear factor-kappa-B-inhibitor alpha (NFKBIA) is a developmental marker of NF-κB/p65 activation during in vitro oocyte maturation and early embryogenesis. Hum. Reprod. 26, 1191–201.Google Scholar
Paynton, B.V., Rempel, R. & Bachvarova, R. (1988). Changes in state of adenylation and time course of degradation of maternal mRNAs during oocyte maturation and early embryonic development in the mouse. Dev. Biol. 129, 304–14.Google Scholar
Perez, G.I., Acton, B.M., Jurisicova, A., Perkins, G.A., White, A., Brown, J., Trbovich, A.M., Kim, M.R., Fissore, R., Xu, J., Ahmady, A., D'Estaing, S.G., Li, H., Kagawa, W., Kurumizaka, H., Yokoyama, S., Okada, H., Mak, T.W., Ellisman, M.H., Casper, R.F. & Tilly, J.L. (2007). Genetic variance modifies apoptosis susceptibility in mature oocytes via alterations in DNA repair capacity and mitochondrial ultrastructure. Cell Death Differ. 14, 524–33.Google Scholar
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.Google Scholar
Russo, G.L., Bilotto, S. & Silvestre, F. (2011). Meiotic regulation by maturating promoting factor and cytostatic factor in the oocyte. In Oocyte Maturation and Fertilization: A Long History for a Short Event (eds. Tosti, E. & Boni, R.), pp. 80–92. Dubai, Bentham Science Publisher Ltd.Google Scholar
Russo, G.L., Wilding, M., Marino, M. & Dale, B. (1998). Ins and outs of meiosis in ascidians. Semin. Cell. Dev. Biol. 9, 559–67.Google Scholar
Sage, J.M., Gildemeister, O.S. & Knight, K.L. (2010). Discovery of a novel function for human Rad51 maintenance of the mitochondrial genome. J. Biol. Chem. 285, 18984–90.CrossRefGoogle ScholarPubMed
Schumacher, B., Garinis, G.A. & Hoeijmakers, J.H. (2008). Age to survive: DNA damage and aging. Trends Genet. 24, 77–85.Google Scholar
Somfai, T, Imai, K, Kaneda, M, Akagi, S, Watanabe, S, Haraguchi, S, Mizutani, E, Dang-Nguyen, TQ, Inaba, Y, Geshi, M, Nagai, T.J. (2011). The effect of ovary storage and in vitro maturation on mRNA levels in bovine oocytes; a possible impact of maternal ATP1A1 on blastocyst development in slaughterhouse-derived oocytes. J. Reprod Dev. 57, 723–30.Google Scholar
Su, Y.Q., Sugiura, K., Woo, Y., Wigglesworth, K., Kamdar, S., Affourtit, J. & Eppig, J.J. (2007). Selective degradation of transcripts during meiotic maturation of mouse oocytes. Dev. Biol. 302, 104–17.Google Scholar
Tomek, W., Torner, H. & Kanitz, W. (2002). Comparative analysis of protein synthesis, transcription and cytoplasmic polyadenylation of mRNA during maturation of bovine oocytes in vitro. Reprod. Domest. Anim. 37, 86–91.Google Scholar
Vallée, M., Robert, C., Méthot, S., Palin, M.F. & Sirard, M.A. (2006). Cross-species hybridizations on a multi-species cDNA microarray to identify evolutionarily conserved genes expressed in oocytes. BMC Genomics 7, 113.Google Scholar
Van Blerkom, J. (2011). Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion 11, 797–813.Google Scholar
Wood, R.D., Mitchell, M., Sgouros, J. & Lindahl, T. (2001). Human DNA repair genes. Science 291, 1284–9.CrossRefGoogle ScholarPubMed
Yamamoto, T., Iwata, H., Goto, H., Shiratuki, S., Tanaka, H., Monji, Y. & Kuwayama, T. (2010). Effect of maternal age on the developmental competence and progression of nuclear maturation in bovine oocytes. Mol. Reprod. Dev. 77, 595–604.CrossRefGoogle ScholarPubMed
Zheng, P., Schramm, R.D. & Latham, K.E. (2005). Developmental regulation and in vitro culture effects on expression of dna repair and cell cycle checkpoint control genes in rhesus monkey oocytes and embryos. Biol. Reprod. 72, 1359–69.Google Scholar