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The Kunming mouse: as a model for age-related decline in female fertility in human

Published online by Cambridge University Press:  21 March 2013

Long-Bo Cui ,
Xue-Ying Zhou ,
Zhen-Jun Zhao ,
Qian Li ,
Xiu-Ying Huang  and
Fang-Zhen Sun
Long-Bo Cui*
Affiliation:
School of Life Sciences, Yantai University, Yantai 264005, P.R. China. or Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100080, P.R. China.
Xue-Ying Zhou
Affiliation:
School of Life Sciences, Yantai University, Yantai 264005, P.R. China.
Zhen-Jun Zhao
Affiliation:
School of Life Sciences, Yantai University, Yantai 264005, P.R. China.
Qian Li
Affiliation:
School of Life Sciences, Yantai University, Yantai 264005, P.R. China.
Xiu-Ying Huang
Affiliation:
Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100080, P. R. China.
Fang-Zhen Sun*
Affiliation:
School of Life Sciences, Yantai University, Yantai 264005, P.R. China. or Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100080, P.R. China.
*
All correspondence to: Long-Bo Cui. School of Life Sciences, Yantai University, Yantai 264005, P.R. China. Tel: +86 535 6903162. e-mail: lbcui@163.com. or Fang-Zhen Sun. Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100080, P.R. China. Tel: +86 10 64807677. e-mail: fzsun@genetics.ac.cn
All correspondence to: Long-Bo Cui. School of Life Sciences, Yantai University, Yantai 264005, P.R. China. Tel: +86 535 6903162. e-mail: lbcui@163.com. or Fang-Zhen Sun. Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100080, P.R. China. Tel: +86 10 64807677. e-mail: fzsun@genetics.ac.cn
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Summary

To ascertain whether the Kunming (KM) mouse is an available model for age-related decline in female fertility in human or not, oocytes from young (6–8 weeks), middle-aged (9 months) and aged (12 months) female mice were compared with respect to number of oocytes, frequency of in-vitro maturation (IVM) and in-vitro fertilization (IVF), and meiotic chromosome segregation and alignment. The mean number of pups born per mouse decreased significantly from the young to the middle-aged and the aged mice. The mean number of ovarian follicles, ovarian germinal vesicle oocytes and ovulated MII oocytes decreased significantly with maternal age. The rate of IVM in oocytes from young mice (73.9%) was less significantly than that in oocytes from middle-aged and aged mice (86.1% and 84.4%, respectively). Immunocytochemical analysis showed that ageing caused a significantly higher rate (49.3%) of chromosome misalignment than that (15.7%) of the young mice. The presence of premature chromatids was also significantly higher in MII oocytes of aged mice as compared with young mice (37.8 versus 8.3%). Pronuclear formation was delayed in oocytes of middle-aged and aged females (35.5 and 42.3% respectively in 5 h of IVF) as compared with young mice (88.1%). The study suggests that KM mouse exhibits an age-related decline in female fertility. Significant reduction of germinal vesicle (GV) and MII oocytes and significant increase of metaphase chromosome misalignment and premature chromatid segregation after meiotic maturation of oocytes, similar to human, presumably contribute to the decline in aged KM mice.

Keywords

AgeFertilityHumanMouse
Type
Research Article
Information
Zygote , Volume 21 , Issue 4 , November 2013 , pp. 367 - 376
Copyright
Copyright © Cambridge University Press 2013 

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References

Angell, R.R. (1997). First meiotic-division nondisjunction in human oocytes. Am. J. Hum. Genet. 61, 23–32.CrossRefGoogle ScholarPubMed
Battaglia, D.E., Goodwin, P., Klein, N.A. & Soules, M.R. (1996). Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum. Reprod. 11, 2217–22.CrossRefGoogle ScholarPubMed
Cui, L.B., Huang, X.Y. & Sun, F.Z. (2005). Transfer of germinal vesicle to ooplasm of young mice could not rescue ageing-associated chromosome misalignment in meiosis of oocytes from aged mice. Hum. Reprod. 20, 1624–31.CrossRefGoogle Scholar
Eichenlaub-Ritter, U. (1998). Genetics of oocyte ageing. Maturitas 30, 143–69.CrossRefGoogle ScholarPubMed
Eichenlaub-Ritter, U. & Boll, I. (1989). Nocodazole sensitivity, age-related aneuploidy, and alterations in the cell cycle during maturation of mouse oocytes. Cytogenet. Cell Genet. 52, 170–6.CrossRefGoogle ScholarPubMed
Eppig, J.J. & O'Brien, M. (1995). In-vitro maturation and fertilization of oocytes isolated from aged mice: a strategy to rescue valuable genetic resources. J. Assist. Reprod. Genet. 12, 269–73.CrossRefGoogle ScholarPubMed
Fabricant, J.D. & Schneider, E.L. (1978). Studies of the genetic and immunologic components of the maternal age effect. Dev. Biol. 66, 337–43.CrossRefGoogle ScholarPubMed
Faddy, M.J., Gosden, R.G., Gougeon, A., Richardson, S.J. & Nelson, J.F. (1992). Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause. Hum. Reprod. 7, 1342–7.CrossRefGoogle ScholarPubMed
Fitzgerald, C.Zimon, A.E. & Jones, E.E. (1998). Ageing and reproductive potential in women. Yale J. Biol. Med. 71, 367–81.Google ScholarPubMed
Fujino, Y., Ozaki, K., Yamamasu, S., Ito, F., Matsuoka, I., Hayashi, E., Nakamura, H., Ogita, S., Sato, E. & Inoue, M. (1996). DNA fragmentation of oocytes in aged mice. Hum. Reprod. 11, 1480–3.CrossRefGoogle ScholarPubMed
Golbus, M.S. (1981). The influence of strain, maternal age, and method of maturation on mouse oocyte aneuploidy. Cytogenet. Cell Genet. 31, 84–90.CrossRefGoogle ScholarPubMed
Gosden, R.G. (1975). Ovarian support of pregnancy in ageing inbred mice. J. Reprod. Fertil. 42, 423–30.CrossRefGoogle ScholarPubMed
Hansmann, I. & Pabst, B. (1992). Nondisjunction by failures in the molecular control of oocyte maturation. Ann. Anat. 174, 485–90.CrossRefGoogle ScholarPubMed
Hodges, C.A., Revenkova, E., Jessberger, R., Hassold, T.J. & Hunt, P.A. (2005). SMC1beta-deficient female mice provide evidence that cohesins are a missing link in age-related nondisjunction. Nat. Genet. 37,1351–5.CrossRefGoogle ScholarPubMed
Hogan, B., Constantini, F. & Lacey, E. (1986). In: Manipulating the Mouse Embryo, A Laboratory Manual (Nagy, A., Gertsenstein, M., Vintersten, K. & Behringer, R.R., eds). New York: Cold Spring Harbor Laboratory, pp. 107–9.Google Scholar
Ishikawa, H. & Endo, A. (1996). Prolongation of duration of ovulation in ageing mice. J. Reprod. Fertil. 108, 167–70.CrossRefGoogle ScholarPubMed
Lamb, N.E., Yu, K., Shaffer, J., Feingold, E. & Sherman, S.L. (2005). Association between maternal age and meiotic recombination for trisomy 21. Am. J. Hum. Genet. 76, 91–9.CrossRefGoogle ScholarPubMed
Lim, A.S.T. & Tsakok, F.H. (1997). Age-related decline in fertility: a link to degenerative oocytes? Fertil. Steril. 68, 265–71.CrossRefGoogle ScholarPubMed
Liu, L. & Keefe, D.L. (2002). Ageing-associated aberration in meiosis of oocytes from senescence-accelerated mice. Hum. Reprod. 17, 2678–85.CrossRefGoogle ScholarPubMed
Liu, L. & Keefe, D.L. (2004). Nuclear origin of ageing-associated meiotic defects in senescence-accelerated mice. Biol. Reprod. 71, 1724–9.CrossRefGoogle Scholar
Liu, L. & Keefe, D.L. (2008). Defective cohesin is associated with age-dependent misaligned chromosomes in oocytes. Reprod. Biomed. Online 16, 103–12.CrossRefGoogle ScholarPubMed
Martin, R.H. (2008). Meiotic errors in human oogenesis and spermatogenesis. Reprod. Biomed. Online 16, 523–31.CrossRefGoogle ScholarPubMed
Navot, D., Bergh, P.A., Williams, M.A., Garrisi, G.J., Guzman, I., Sandler, B. & Grunfeld, L. (1991). Poor oocytes quality rather than implantation failure as a cause of age-related decline in female fertility. Lancet 337, 1375–7.CrossRefGoogle ScholarPubMed
Oehninger, S.et al (1995). Intracytoplasmic sperm injection: achievement of high pregnancy rats in couples with severe male factor infertility is dependent primarily upon female and not male factors. Fertil. Steril. 64, 977–81.CrossRefGoogle Scholar
Pan, H., Ma, P., Zhu, W. & Schultz, R.M. (2008). Age-associated increase in aneuploidy and changes in gene expression in mouse eggs. Dev. Biol. 316, 397–407.CrossRefGoogle ScholarPubMed
Pellestor, F., Andréo, B., Arnal, F., Humeau, C. & Demaille, J. (2002). Mechanisms of non-disjunction in human female meiosis: the co-existence of two modes of malsegregation evidenced by the karyotyping of 1397 in-vitro unfertilized oocytes. Hum. Reprod. 17, 2134–45.CrossRefGoogle ScholarPubMed
Pellestor, F.Andréo, B., Arnal, F., Humeau, C. & Demaille, J. (2003). Maternal aging and chromosomal abnormalities: new data drawn from in-vitro unfertilized human oocytes. Hum. Genet. 112, 195–203.CrossRefGoogle ScholarPubMed
Sakurada, K., Omoe, K. & Endo, A. (1994). Increased incidence of unpartnered single chromatids in metaphase II oocytes in 39 X (XO) mice. Experientia 50, 502–5.CrossRefGoogle ScholarPubMed
Sakurada, K., Ishikawa, H. & Endo, A. (1996). Cytogenetic effects of advanced maternal age and delayed fertilization on first-cleavage mouse embryos. Cytogenet. Cell. Genet. 72, 46–9.CrossRefGoogle ScholarPubMed
Steuerwald, N.M., Bermúdez, M.G., Wells, D., Munné, S. & Cohen, J. (2007). Maternal age-related differential global expression profiles observed in human oocytes. Reprod. Biomed. Online 14, 700–8.CrossRefGoogle ScholarPubMed
Szamatowicz, M. & Grochowski, D. (1998). Fertility and infertility in aging women. Gynecol. Endocrinol. 12, 407–13.CrossRefGoogle ScholarPubMed
Tarin, J.J., Pérez-Albalá, S. & Cano, A. (2001). Cellular and morphological traits of oocytes retrieved from ageing mice after exogenous ovarian stimulation. Biol. Reprod. 65, 141–50.CrossRefGoogle ScholarPubMed
Tarin, J.J., Pérez-Albalá, S. & Cano, A. (2002). Oral antioxidants counteract the negative effects of female ageing on oocyte quantity and quality in the mouse. Mol. Reprod. Dev. 61, 385–97.CrossRefGoogle ScholarPubMed
Tarkowski, A.K. (1966). An air-drying method for chromosome preparations from mouse eggs. Cytogenetics 5, 394–400.CrossRefGoogle Scholar
Vialard, F., Petit, C., Bergerem, M., Gomes, G.M., Martek-Petit, V., Lombroso, R., Ville, Y., Gerard, H. & Selva, J. (2006). Evidence of a high proportion of premature unbalanced separation of sister chromatids in the first polar bodies of women of advanced age. Hum. Reprod. 21, 1172–8.CrossRefGoogle ScholarPubMed
Vogt, E., Kirsch-Volders, M., Parry, J. & Eichenlaub-Ritter, U. (2008). Spindle formation, chromosome segregation and the spindle checkpoint in mammalian oocytes and susceptibility to meiotic error. Mutat. Res. 651, 14–29.CrossRefGoogle ScholarPubMed
Volarcik, K., Sheean, L., Goldfarb, J., Woods, L., Abdul-Karim, F.W. & Hunt, P. (1998). The meiotic competence of in-vitro matured human oocytes is influenced by donor age: evidence that folliculogenesis is compromised in the reproductively aged ovary. Hum. Reprod. 13, 154–60.CrossRefGoogle ScholarPubMed
Wu, J., Zhang, L. & Wang, X. (2000). Maturation and apoptosis of human oocytes in vitro are age-related. Fertil. Steril. 74, 1137–41.CrossRefGoogle ScholarPubMed
Zuccotti, M., Boiani, M., Garagna, S. & Redi, C.A. (1998). Analysis of aneuploidy rate in antral and ovulated mouse oocytes during female ageing. Mol. Reprod. Dev. 50, 305–12.3.0.CO;2-N>CrossRefGoogle Scholar