Skip to main content
Top
Published in: Reproductive Medicine and Biology 4/2015

01-10-2015 | Review Article

Oocyte aging underlies female reproductive aging: biological mechanisms and therapeutic strategies

Authors: Hideki Igarashi, Toshifumi Takahashi, Satoru Nagase

Published in: Reproductive Medicine and Biology | Issue 4/2015

Login to get access

Abstract

In recent years, postponement of marriage and childbearing in women of reproductive age has led to an increase in the incidence of age-related infertility. The reproductive aging process in women is assumed to occur due to a decrease in both the quantity and quality of the oocytes, with the ultimate result being a decline in fecundity. This age-related decline in fecundity is strongly dependent on oocyte quality, which is critical for fertilization and subsequent embryo development. Aged oocytes display increased chromosomal abnormality and dysfunction of cellular organelles, both of which factor into oocyte quality. In particular, mitochondrial dysfunction has been suggested as a major contributor to the reduction in oocyte quality as well as to chromosomal abnormalities in aged oocytes and embryos. Participation of oxidative stress in the oocyte aging process has been proposed because oxidative stress has the capacity to induce mitochondrial dysfunction and directly damage many intracellular components of the oocytes such as lipids, protein, and DNA. In an attempt to improve mitochondrial function in aged oocytes, several therapeutic strategies have been investigated using both animal models and assisted reproductive technology. Here, we review the biological mechanisms and present status of therapeutic strategies in the female reproductive aging field and indicate possible future therapeutic strategies.
Literature
1.
go back to reference te Velde ER, Pearson PL. The variability of female reproductive ageing. Hum Reprod Update. 2002;8:141–54.CrossRef te Velde ER, Pearson PL. The variability of female reproductive ageing. Hum Reprod Update. 2002;8:141–54.CrossRef
2.
go back to reference Broekmans FJ, Knauff EA, te Velde ER, Macklon NS, Fauser BC. Female reproductive ageing: current knowledge and future trends. Trends Endocrinol Metab. 2007;18:58–65.CrossRefPubMed Broekmans FJ, Knauff EA, te Velde ER, Macklon NS, Fauser BC. Female reproductive ageing: current knowledge and future trends. Trends Endocrinol Metab. 2007;18:58–65.CrossRefPubMed
3.
go back to reference Baird DT, Collins J, Egozcue J, Evers LH, Gianaroli L, Leridon H, Sunde A, Templeton A, Van Steirteghem A, Cohen J, Crosignani PG, Devroey P, et al. Fertility and ageing. Hum Reprod Update. 2005;11:261–76.CrossRefPubMed Baird DT, Collins J, Egozcue J, Evers LH, Gianaroli L, Leridon H, Sunde A, Templeton A, Van Steirteghem A, Cohen J, Crosignani PG, Devroey P, et al. Fertility and ageing. Hum Reprod Update. 2005;11:261–76.CrossRefPubMed
4.
go back to reference Mac Dougall K, Beyene Y, Nachtigall RD. Age shock: misperceptions of the impact of age on fertility before and after IVF in women who conceived after age 40. Hum Reprod. 2013;28:350–6.CrossRef Mac Dougall K, Beyene Y, Nachtigall RD. Age shock: misperceptions of the impact of age on fertility before and after IVF in women who conceived after age 40. Hum Reprod. 2013;28:350–6.CrossRef
5.
go back to reference Takeshima K, Saito H, Nakaza A, Kuwahara A, Ishihara O, Irahara M, Hirahara H, Yoshimura Y, Sakumoto T. Efficacy, safety, and trends in assisted reproductive technology in Japan—analysis of four-year data from the national registry system. J Assist Reprod Genet. 2014;31:477–84.PubMedCentralCrossRefPubMed Takeshima K, Saito H, Nakaza A, Kuwahara A, Ishihara O, Irahara M, Hirahara H, Yoshimura Y, Sakumoto T. Efficacy, safety, and trends in assisted reproductive technology in Japan—analysis of four-year data from the national registry system. J Assist Reprod Genet. 2014;31:477–84.PubMedCentralCrossRefPubMed
6.
go back to reference Ferraretti AP, Goossens V, Kupka M, Bhattacharya S, de Mouzon J, Castilla JA, Erb K, Korsak V, Nyboe Andersen A, European IVFMCftESoHR, Embryology. Assisted reproductive technology in Europe, 2009: results generated from European registers by ESHRE. Hum Reprod. 2013;28:2318–31.CrossRefPubMed Ferraretti AP, Goossens V, Kupka M, Bhattacharya S, de Mouzon J, Castilla JA, Erb K, Korsak V, Nyboe Andersen A, European IVFMCftESoHR, Embryology. Assisted reproductive technology in Europe, 2009: results generated from European registers by ESHRE. Hum Reprod. 2013;28:2318–31.CrossRefPubMed
7.
go back to reference van Noord-Zaadstra BM, Looman CW, Alsbach H, Habbema JD, te Velde ER, Karbaat J. Delaying childbearing: effect of age on fecundity and outcome of pregnancy. BMJ. 1991;302:1361–5.PubMedCentralCrossRefPubMed van Noord-Zaadstra BM, Looman CW, Alsbach H, Habbema JD, te Velde ER, Karbaat J. Delaying childbearing: effect of age on fecundity and outcome of pregnancy. BMJ. 1991;302:1361–5.PubMedCentralCrossRefPubMed
8.
go back to reference Menken J, Trussell J, Larsen U. Age and infertility. Science. 1986;233:1389–94.PubMed Menken J, Trussell J, Larsen U. Age and infertility. Science. 1986;233:1389–94.PubMed
9.
go back to reference Toner JP, Grainger DA, Frazier LM. Clinical outcomes among recipients of donated eggs: an analysis of the U.S. National Experience, 1996-1998. Fertil Steril. 2002;78:1038–45.CrossRefPubMed Toner JP, Grainger DA, Frazier LM. Clinical outcomes among recipients of donated eggs: an analysis of the U.S. National Experience, 1996-1998. Fertil Steril. 2002;78:1038–45.CrossRefPubMed
10.
go back to reference Spandorfer SD, Bendikson K, Dragisic K, Schattman G, Davis OK, Rosenwaks Z. Outcome of in vitro fertilization in women 45 years and older who use autologous oocytes. Fertil Steril. 2007;87:74–6.CrossRefPubMed Spandorfer SD, Bendikson K, Dragisic K, Schattman G, Davis OK, Rosenwaks Z. Outcome of in vitro fertilization in women 45 years and older who use autologous oocytes. Fertil Steril. 2007;87:74–6.CrossRefPubMed
12.
go back to reference Sunderam S, Kissin DM, Crawford S, Anderson JE, Folger SG, Jamieson DJ, Barfield WD. Assisted reproductive technology surveillance—United States, 2010. MMWR Surveill Summ. 2013;62:1–24.PubMed Sunderam S, Kissin DM, Crawford S, Anderson JE, Folger SG, Jamieson DJ, Barfield WD. Assisted reproductive technology surveillance—United States, 2010. MMWR Surveill Summ. 2013;62:1–24.PubMed
13.
go back to reference Sunderam S, Kissin DM, Flowers L, Anderson JE, Folger SG, Jamieson DJ, Barfield WD. Assisted reproductive technology surveillance—United States, 2009. MMWR Surveill Summ. 2012;61:1–23.PubMed Sunderam S, Kissin DM, Flowers L, Anderson JE, Folger SG, Jamieson DJ, Barfield WD. Assisted reproductive technology surveillance—United States, 2009. MMWR Surveill Summ. 2012;61:1–23.PubMed
14.
go back to reference American College of. O, Gynecologists Committee on Gynecologic P, Practice C. Female age-related fertility decline. Committee Opinion No. 589. Fertil Steril. 2014;101:633–4.CrossRef American College of. O, Gynecologists Committee on Gynecologic P, Practice C. Female age-related fertility decline. Committee Opinion No. 589. Fertil Steril. 2014;101:633–4.CrossRef
15.
go back to reference Klinkert ER. Clinical significance and management of poor response in IVF. Thesis Utrecht University. 2005. Klinkert ER. Clinical significance and management of poor response in IVF. Thesis Utrecht University. 2005.
16.
go back to reference Miao YL, Kikuchi K, Sun QY, Schatten H. Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum Reprod Update. 2009;15:573–85.CrossRefPubMed Miao YL, Kikuchi K, Sun QY, Schatten H. Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Hum Reprod Update. 2009;15:573–85.CrossRefPubMed
17.
go back to reference Van Blerkom J. Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion. 2011;11:797–813.CrossRefPubMed Van Blerkom J. Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion. 2011;11:797–813.CrossRefPubMed
18.
go back to reference Eichenlaub-Ritter U, Vogt E, Yin H, Gosden R. Spindles, mitochondria and redox potential in ageing oocytes. Reprod Biomed Online. 2004;8:45–58.CrossRefPubMed Eichenlaub-Ritter U, Vogt E, Yin H, Gosden R. Spindles, mitochondria and redox potential in ageing oocytes. Reprod Biomed Online. 2004;8:45–58.CrossRefPubMed
19.
go back to reference Duncan FE, Hornick JE, Lampson MA, Schultz RM, Shea LD, Woodruff TK. Chromosome cohesion decreases in human eggs with advanced maternal age. Aging Cell. 2012;11:1121–4.PubMedCentralCrossRefPubMed Duncan FE, Hornick JE, Lampson MA, Schultz RM, Shea LD, Woodruff TK. Chromosome cohesion decreases in human eggs with advanced maternal age. Aging Cell. 2012;11:1121–4.PubMedCentralCrossRefPubMed
20.
go back to reference Bentov Y, Yavorska T, Esfandiari N, Jurisicova A, Casper RF. The contribution of mitochondrial function to reproductive aging. J Assist Reprod Genet. 2011;28:773–83.PubMedCentralCrossRefPubMed Bentov Y, Yavorska T, Esfandiari N, Jurisicova A, Casper RF. The contribution of mitochondrial function to reproductive aging. J Assist Reprod Genet. 2011;28:773–83.PubMedCentralCrossRefPubMed
21.
go back to reference Eichenlaub-Ritter U, Wieczorek M, Luke S, Seidel T. Age related changes in mitochondrial function and new approaches to study redox regulation in mammalian oocytes in response to age or maturation conditions. Mitochondrion. 2011;11:783–96.CrossRefPubMed Eichenlaub-Ritter U, Wieczorek M, Luke S, Seidel T. Age related changes in mitochondrial function and new approaches to study redox regulation in mammalian oocytes in response to age or maturation conditions. Mitochondrion. 2011;11:783–96.CrossRefPubMed
22.
go back to reference Lord T, Aitken RJ. Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction. 2013;146:R217–27.CrossRefPubMed Lord T, Aitken RJ. Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction. 2013;146:R217–27.CrossRefPubMed
23.
go back to reference Miyazaki S. Thirty years of calcium signals at fertilization. Semin Cell Dev Biol. 2006;17:233–43.CrossRefPubMed Miyazaki S. Thirty years of calcium signals at fertilization. Semin Cell Dev Biol. 2006;17:233–43.CrossRefPubMed
25.
go back to reference Ducibella T, Schultz RM, Ozil JP. Role of calcium signals in early development. Semin Cell Dev Biol. 2006;17:324–32.CrossRefPubMed Ducibella T, Schultz RM, Ozil JP. Role of calcium signals in early development. Semin Cell Dev Biol. 2006;17:324–32.CrossRefPubMed
26.
go back to reference Ozil JP, Huneau D. Activation of rabbit oocytes: the impact of the Ca2+ signal regime on development. Development. 2001;128:917–28.PubMed Ozil JP, Huneau D. Activation of rabbit oocytes: the impact of the Ca2+ signal regime on development. Development. 2001;128:917–28.PubMed
27.
go back to reference Ozil JP, Banrezes B, Toth S, Pan H, Schultz RM. Ca2 + oscillatory pattern in fertilized mouse eggs affects gene expression and development to term. Dev Biol. 2006;300:534–44.CrossRefPubMed Ozil JP, Banrezes B, Toth S, Pan H, Schultz RM. Ca2 + oscillatory pattern in fertilized mouse eggs affects gene expression and development to term. Dev Biol. 2006;300:534–44.CrossRefPubMed
28.
go back to reference Igarashi H, Knott JG, Schultz RM, Williams CJ. Alterations of PLCbeta1 in mouse eggs change calcium oscillatory behavior following fertilization. Dev Biol. 2007;312:321–30.PubMedCentralCrossRefPubMed Igarashi H, Knott JG, Schultz RM, Williams CJ. Alterations of PLCbeta1 in mouse eggs change calcium oscillatory behavior following fertilization. Dev Biol. 2007;312:321–30.PubMedCentralCrossRefPubMed
29.
go back to reference Takahashi T, Igarashi H, Amita M, Hara S, Matsuo K, Kurachi H. Molecular mechanism of poor embryo development in postovulatory aged oocytes: mini review. J Obstet Gynaecol Res. 2013;39:1431–9.PubMed Takahashi T, Igarashi H, Amita M, Hara S, Matsuo K, Kurachi H. Molecular mechanism of poor embryo development in postovulatory aged oocytes: mini review. J Obstet Gynaecol Res. 2013;39:1431–9.PubMed
30.
go back to reference Fissore RA, Kurokawa M, Knott J, Zhang M, Smyth J. Mechanisms underlying oocyte activation and postovulatory ageing. Reproduction. 2002;124:745–54.CrossRefPubMed Fissore RA, Kurokawa M, Knott J, Zhang M, Smyth J. Mechanisms underlying oocyte activation and postovulatory ageing. Reproduction. 2002;124:745–54.CrossRefPubMed
31.
go back to reference Igarashi H, Takahashi E, Hiroi M, Doi K. Aging-related changes in calcium oscillations in fertilized mouse oocytes. Mol Reprod Dev. 1997;48:383–90.CrossRefPubMed Igarashi H, Takahashi E, Hiroi M, Doi K. Aging-related changes in calcium oscillations in fertilized mouse oocytes. Mol Reprod Dev. 1997;48:383–90.CrossRefPubMed
32.
go back to reference Takahashi T, Saito H, Hiroi M, Doi K. Effects of aging on inositol 1,4,5-triphosphate-induced Ca(2+) release in unfertilized mouse oocytes. Mol Reprod Dev. 2000;55:299–306.CrossRefPubMed Takahashi T, Saito H, Hiroi M, Doi K. Effects of aging on inositol 1,4,5-triphosphate-induced Ca(2+) release in unfertilized mouse oocytes. Mol Reprod Dev. 2000;55:299–306.CrossRefPubMed
33.
go back to reference Jones KT, Whittingham DG. A comparison of sperm- and IP3-induced Ca2 + release in activated and aging mouse oocytes. Dev Biol. 1996;178:229–37.CrossRefPubMed Jones KT, Whittingham DG. A comparison of sperm- and IP3-induced Ca2 + release in activated and aging mouse oocytes. Dev Biol. 1996;178:229–37.CrossRefPubMed
34.
go back to reference Gordo AC, Rodrigues P, Kurokawa M, Jellerette T, Exley GE, Warner C, Fissore R. Intracellular calcium oscillations signal apoptosis rather than activation in in vitro aged mouse eggs. Biol Reprod. 2002;66:1828–37.CrossRefPubMed Gordo AC, Rodrigues P, Kurokawa M, Jellerette T, Exley GE, Warner C, Fissore R. Intracellular calcium oscillations signal apoptosis rather than activation in in vitro aged mouse eggs. Biol Reprod. 2002;66:1828–37.CrossRefPubMed
35.
36.
37.
go back to reference Schon EA, Kim SH, Ferreira JC, Magalhaes P, Grace M, Warburton D, Gross SJ. Chromosomal non-disjunction in human oocytes: is there a mitochondrial connection? Hum Reprod. 2000;15(Suppl 2):160–72.CrossRefPubMed Schon EA, Kim SH, Ferreira JC, Magalhaes P, Grace M, Warburton D, Gross SJ. Chromosomal non-disjunction in human oocytes: is there a mitochondrial connection? Hum Reprod. 2000;15(Suppl 2):160–72.CrossRefPubMed
38.
go back to reference Desler C, Munch-Petersen B, Stevnsner T, Matsui S, Kulawiec M, Singh KK, Rasmussen LJ. Mitochondria as determinant of nucleotide pools and chromosomal stability. Mutat Res. 2007;625:112–24.CrossRefPubMed Desler C, Munch-Petersen B, Stevnsner T, Matsui S, Kulawiec M, Singh KK, Rasmussen LJ. Mitochondria as determinant of nucleotide pools and chromosomal stability. Mutat Res. 2007;625:112–24.CrossRefPubMed
39.
go back to reference Acton BM. Alterations in mitochondrial membrane potential during preimplantation stages of mouse and human embryo development. Mol Hum Reprod. 2004;10:23–32.CrossRefPubMed Acton BM. Alterations in mitochondrial membrane potential during preimplantation stages of mouse and human embryo development. Mol Hum Reprod. 2004;10:23–32.CrossRefPubMed
40.
go back to reference Van Blerkom J, Davis PW, Lee J. ATP content of human oocytes and developmental potential and outcome after in vitro fertilization and embryo transfer. Hum Reprod. 1995;10:415–24.PubMed Van Blerkom J, Davis PW, Lee J. ATP content of human oocytes and developmental potential and outcome after in vitro fertilization and embryo transfer. Hum Reprod. 1995;10:415–24.PubMed
41.
go back to reference Simsek-Duran F, Li F, Ford W, Swanson RJ, Jones HW Jr, Castora FJ. Age-associated metabolic and morphologic changes in mitochondria of individual mouse and hamster oocytes. PLoS ONE. 2013;8:e64955.PubMedCentralCrossRefPubMed Simsek-Duran F, Li F, Ford W, Swanson RJ, Jones HW Jr, Castora FJ. Age-associated metabolic and morphologic changes in mitochondria of individual mouse and hamster oocytes. PLoS ONE. 2013;8:e64955.PubMedCentralCrossRefPubMed
42.
go back to reference Sato D, Itami N, Tasaki H, Takeo S, Kuwayama T, Iwata H. Relationship between mitochondrial DNA copy number and SIRT1 expression in porcine oocytes. PLoS ONE. 2014;9:e94488.PubMedCentralCrossRefPubMed Sato D, Itami N, Tasaki H, Takeo S, Kuwayama T, Iwata H. Relationship between mitochondrial DNA copy number and SIRT1 expression in porcine oocytes. PLoS ONE. 2014;9:e94488.PubMedCentralCrossRefPubMed
43.
go back to reference Igarashi H, Takahashi T, Takahashi E, Tezuka N, Nakahara K, Takahashi K, Kurachi H. Aged mouse oocytes fail to readjust intracellular adenosine triphosphates at fertilization. Biol Reprod. 2005;72:1256–61.CrossRefPubMed Igarashi H, Takahashi T, Takahashi E, Tezuka N, Nakahara K, Takahashi K, Kurachi H. Aged mouse oocytes fail to readjust intracellular adenosine triphosphates at fertilization. Biol Reprod. 2005;72:1256–61.CrossRefPubMed
44.
go back to reference Van Blerkom J, Davis P, Alexander S. Differential mitochondrial distribution in human pronuclear embryos leads to disproportionate inheritance between blastomeres: relationship to microtubular organization. ATP content and competence. Hum Reprod. 2000;15:2621–33.CrossRefPubMed Van Blerkom J, Davis P, Alexander S. Differential mitochondrial distribution in human pronuclear embryos leads to disproportionate inheritance between blastomeres: relationship to microtubular organization. ATP content and competence. Hum Reprod. 2000;15:2621–33.CrossRefPubMed
45.
go back to reference May-Panloup P, Chretien MF, Malthiery Y, Reynier P. Mitochondrial DNA in the oocyte and the developing embryo. Curr Top Dev Biol. 2007;77:51–83.CrossRefPubMed May-Panloup P, Chretien MF, Malthiery Y, Reynier P. Mitochondrial DNA in the oocyte and the developing embryo. Curr Top Dev Biol. 2007;77:51–83.CrossRefPubMed
46.
go back to reference Barritt JA, Cohen J, Brenner CA. Mitochondrial DNA point mutation in human oocytes is associated with maternal age. Reprod Biomed Online. 2000;1:96–100.CrossRefPubMed Barritt JA, Cohen J, Brenner CA. Mitochondrial DNA point mutation in human oocytes is associated with maternal age. Reprod Biomed Online. 2000;1:96–100.CrossRefPubMed
47.
go back to reference Yesodi V, Yaron Y, Lessing JB, Amit A, Ben-Yosef D. The mitochondrial DNA mutation (deltamtDNA5286) in human oocytes: correlation with age and IVF outcome. J Assist Reprod Genet. 2002;19:60–6.PubMedCentralCrossRefPubMed Yesodi V, Yaron Y, Lessing JB, Amit A, Ben-Yosef D. The mitochondrial DNA mutation (deltamtDNA5286) in human oocytes: correlation with age and IVF outcome. J Assist Reprod Genet. 2002;19:60–6.PubMedCentralCrossRefPubMed
48.
go back to reference Reynier P, May-Panloup P, Chretien MF, Morgan CJ, Jean M, Savagner F, Barriere P, Malthiery Y. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol Hum Reprod. 2001;7:425–9.CrossRefPubMed Reynier P, May-Panloup P, Chretien MF, Morgan CJ, Jean M, Savagner F, Barriere P, Malthiery Y. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol Hum Reprod. 2001;7:425–9.CrossRefPubMed
49.
go back to reference Keefe DL, Niven-Fairchild T, Powell S, Buradagunta S. Mitochondrial deoxyribonucleic acid deletions in oocytes and reproductive aging in women. Fertil Steril. 1995;64:577–83.PubMed Keefe DL, Niven-Fairchild T, Powell S, Buradagunta S. Mitochondrial deoxyribonucleic acid deletions in oocytes and reproductive aging in women. Fertil Steril. 1995;64:577–83.PubMed
50.
go back to reference Ramalingam M, Kim SJ. Reactive oxygen/nitrogen species and their functional correlations in neurodegenerative diseases. J Neural Transm. 2012;119:891–910.CrossRefPubMed Ramalingam M, Kim SJ. Reactive oxygen/nitrogen species and their functional correlations in neurodegenerative diseases. J Neural Transm. 2012;119:891–910.CrossRefPubMed
51.
go back to reference Tarin JJ. Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol Hum Reprod. 1996;2:717–24.CrossRefPubMed Tarin JJ. Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol Hum Reprod. 1996;2:717–24.CrossRefPubMed
52.
go back to reference Takahashi T, Takahashi E, Igarashi H, Tezuka N, Kurachi H. Impact of oxidative stress in aged mouse oocytes on calcium oscillations at fertilization. Mol Reprod Dev. 2003;66:143–52.CrossRefPubMed Takahashi T, Takahashi E, Igarashi H, Tezuka N, Kurachi H. Impact of oxidative stress in aged mouse oocytes on calcium oscillations at fertilization. Mol Reprod Dev. 2003;66:143–52.CrossRefPubMed
53.
go back to reference Thouas GA, Trounson AO, Jones GM. Effect of female age on mouse oocyte developmental competence following mitochondrial injury. Biol Reprod. 2005;73:366–73.CrossRefPubMed Thouas GA, Trounson AO, Jones GM. Effect of female age on mouse oocyte developmental competence following mitochondrial injury. Biol Reprod. 2005;73:366–73.CrossRefPubMed
54.
go back to reference Seino T, Saito H, Kaneko T, Takahashi T, Kawachiya S, Kurachi H. Eight-hydroxy-2′-deoxyguanosine in granulosa cells is correlated with the quality of oocytes and embryos in an in vitro fertilization-embryo transfer program. Fertil Steril. 2002;77:1184–90.CrossRefPubMed Seino T, Saito H, Kaneko T, Takahashi T, Kawachiya S, Kurachi H. Eight-hydroxy-2′-deoxyguanosine in granulosa cells is correlated with the quality of oocytes and embryos in an in vitro fertilization-embryo transfer program. Fertil Steril. 2002;77:1184–90.CrossRefPubMed
55.
go back to reference Hamatani T, Falco G, Carter MG, Akutsu H, Stagg CA, Sharov AA, Dudekula DB, VanBuren V, Ko MS. Age-associated alteration of gene expression patterns in mouse oocytes. Hum Mol Genet. 2004;13:2263–78.CrossRefPubMed Hamatani T, Falco G, Carter MG, Akutsu H, Stagg CA, Sharov AA, Dudekula DB, VanBuren V, Ko MS. Age-associated alteration of gene expression patterns in mouse oocytes. Hum Mol Genet. 2004;13:2263–78.CrossRefPubMed
56.
go back to reference Miyamoto K, Sato EF, Kasahara E, Jikumaru M, Hiramoto K, Tabata H, Katsuragi M, Odo S, Utsumi K, Inoue M. Effect of oxidative stress during repeated ovulation on the structure and functions of the ovary, oocytes, and their mitochondria. Free Radic Biol Med. 2010;49:674–81.CrossRefPubMed Miyamoto K, Sato EF, Kasahara E, Jikumaru M, Hiramoto K, Tabata H, Katsuragi M, Odo S, Utsumi K, Inoue M. Effect of oxidative stress during repeated ovulation on the structure and functions of the ovary, oocytes, and their mitochondria. Free Radic Biol Med. 2010;49:674–81.CrossRefPubMed
57.
go back to reference Tarin JJ, Perez-Albala S, Cano A. Oral antioxidants counteract the negative effects of female aging on oocyte quantity and quality in the mouse. Mol Reprod Dev. 2002;61:385–97.CrossRefPubMed Tarin JJ, Perez-Albala S, Cano A. Oral antioxidants counteract the negative effects of female aging on oocyte quantity and quality in the mouse. Mol Reprod Dev. 2002;61:385–97.CrossRefPubMed
58.
go back to reference Carlomagno G, Nordio M, Chiu TT, Unfer V. Contribution of myo-inositol and melatonin to human reproduction. Eur J Obstet Gynecol Reprod Biol. 2011;159:267–72.CrossRefPubMed Carlomagno G, Nordio M, Chiu TT, Unfer V. Contribution of myo-inositol and melatonin to human reproduction. Eur J Obstet Gynecol Reprod Biol. 2011;159:267–72.CrossRefPubMed
59.
go back to reference Brzezinski A, Seibel MM, Lynch HJ, Deng MH, Wurtman RJ. Melatonin in human preovulatory follicular fluid. J Clin Endocrinol Metab. 1987;64:865–7.CrossRefPubMed Brzezinski A, Seibel MM, Lynch HJ, Deng MH, Wurtman RJ. Melatonin in human preovulatory follicular fluid. J Clin Endocrinol Metab. 1987;64:865–7.CrossRefPubMed
60.
go back to reference Tamura H, Takasaki A, Taketani T, Tanabe M, Kizuka F, Lee L, Tamura I, Maekawa R, Asada H, Yamagata Y, Sugino N. Melatonin as a free radical scavenger in the ovarian follicle. Endocr J. 2013;60:1–13.CrossRefPubMed Tamura H, Takasaki A, Taketani T, Tanabe M, Kizuka F, Lee L, Tamura I, Maekawa R, Asada H, Yamagata Y, Sugino N. Melatonin as a free radical scavenger in the ovarian follicle. Endocr J. 2013;60:1–13.CrossRefPubMed
61.
go back to reference Unfer V, Raffone E, Rizzo P, Buffo S. Effect of a supplementation with myo-inositol plus melatonin on oocyte quality in women who failed to conceive in previous in vitro fertilization cycles for poor oocyte quality: a prospective, longitudinal, cohort study. Gynecol Endocrinol. 2011;27:857–61.CrossRefPubMed Unfer V, Raffone E, Rizzo P, Buffo S. Effect of a supplementation with myo-inositol plus melatonin on oocyte quality in women who failed to conceive in previous in vitro fertilization cycles for poor oocyte quality: a prospective, longitudinal, cohort study. Gynecol Endocrinol. 2011;27:857–61.CrossRefPubMed
62.
go back to reference Seko LM, Moroni RM, Leitao VM, Teixeira DM, Nastri CO, Martins WP. Melatonin supplementation during controlled ovarian stimulation for women undergoing assisted reproductive technology: systematic review and meta-analysis of randomized controlled trials. Fertil Steril. 2014;101(154–61):e4.PubMed Seko LM, Moroni RM, Leitao VM, Teixeira DM, Nastri CO, Martins WP. Melatonin supplementation during controlled ovarian stimulation for women undergoing assisted reproductive technology: systematic review and meta-analysis of randomized controlled trials. Fertil Steril. 2014;101(154–61):e4.PubMed
63.
go back to reference Showell MG, Brown J, Clarke J, Hart RJ. Antioxidants for female subfertility. Cochrane Database Syst Rev 2013; 8:Cd007807 Showell MG, Brown J, Clarke J, Hart RJ. Antioxidants for female subfertility. Cochrane Database Syst Rev 2013; 8:Cd007807
64.
go back to reference Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, Zipkin RE, Chung P, Kisielewski A, Zhang LL, Scherer B, Sinclair DA. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature. 2003;425:191–6.CrossRefPubMed Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, Zipkin RE, Chung P, Kisielewski A, Zhang LL, Scherer B, Sinclair DA. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature. 2003;425:191–6.CrossRefPubMed
66.
go back to reference Baur JA, Sinclair DA. Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov. 2006;5:493–506.CrossRefPubMed Baur JA, Sinclair DA. Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov. 2006;5:493–506.CrossRefPubMed
67.
go back to reference Price NL, Gomes AP, Ling AJ, Duarte FV, Martin-Montalvo A, North BJ, Agarwal B, Ye L, Ramadori G, Teodoro JS, Hubbard BP, Varela AT, et al. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab. 2012;15:675–90.PubMedCentralCrossRefPubMed Price NL, Gomes AP, Ling AJ, Duarte FV, Martin-Montalvo A, North BJ, Agarwal B, Ye L, Ramadori G, Teodoro JS, Hubbard BP, Varela AT, et al. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab. 2012;15:675–90.PubMedCentralCrossRefPubMed
68.
go back to reference Takeo S, Sato D, Kimura K, Monji Y, Kuwayama T, Kawahara-Miki R, Iwata H. Resveratrol improves the mitochondrial function and fertilization outcome of bovine oocytes. J Reprod Dev. 2014;60:92–9.PubMedCentralCrossRefPubMed Takeo S, Sato D, Kimura K, Monji Y, Kuwayama T, Kawahara-Miki R, Iwata H. Resveratrol improves the mitochondrial function and fertilization outcome of bovine oocytes. J Reprod Dev. 2014;60:92–9.PubMedCentralCrossRefPubMed
69.
go back to reference Robb EL, Page MM, Wiens BE, Stuart JA. Molecular mechanisms of oxidative stress resistance induced by resveratrol: specific and progressive induction of MnSOD. Biochem Biophys Res Commun. 2008;367:406–12.CrossRefPubMed Robb EL, Page MM, Wiens BE, Stuart JA. Molecular mechanisms of oxidative stress resistance induced by resveratrol: specific and progressive induction of MnSOD. Biochem Biophys Res Commun. 2008;367:406–12.CrossRefPubMed
70.
go back to reference Liu Y, He XQ, Huang X, Ding L, Xu L, Shen YT, Zhang F, Zhu MB, Xu BH, Qi ZQ, Wang HL. Resveratrol protects mouse oocytes from methylglyoxal-induced oxidative damage. PLoS ONE. 2013;8:e77960.PubMedCentralCrossRefPubMed Liu Y, He XQ, Huang X, Ding L, Xu L, Shen YT, Zhang F, Zhu MB, Xu BH, Qi ZQ, Wang HL. Resveratrol protects mouse oocytes from methylglyoxal-induced oxidative damage. PLoS ONE. 2013;8:e77960.PubMedCentralCrossRefPubMed
71.
go back to reference Guarente L, Franklin H. Epstein Lecture: sirtuins, aging, and medicine. N Engl J Med. 2011;364:2235–44.CrossRefPubMed Guarente L, Franklin H. Epstein Lecture: sirtuins, aging, and medicine. N Engl J Med. 2011;364:2235–44.CrossRefPubMed
72.
go back to reference Lin J, Handschin C, Spiegelman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 2005;1:361–70.CrossRefPubMed Lin J, Handschin C, Spiegelman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 2005;1:361–70.CrossRefPubMed
73.
go back to reference Liu M, Yin Y, Ye X, Zeng M, Zhao Q, Keefe DL, Liu L. Resveratrol protects against age-associated infertility in mice. Hum Reprod. 2013;28:707–17.CrossRefPubMed Liu M, Yin Y, Ye X, Zeng M, Zhao Q, Keefe DL, Liu L. Resveratrol protects against age-associated infertility in mice. Hum Reprod. 2013;28:707–17.CrossRefPubMed
75.
go back to reference Park S, Mori R, Shimokawa I. Do sirtuins promote mammalian longevity? A critical review on its relevance to the longevity effect induced by calorie restriction. Mol Cells. 2013;35:474–80.PubMedCentralCrossRefPubMed Park S, Mori R, Shimokawa I. Do sirtuins promote mammalian longevity? A critical review on its relevance to the longevity effect induced by calorie restriction. Mol Cells. 2013;35:474–80.PubMedCentralCrossRefPubMed
77.
go back to reference Liu C, Lin JD. PGC-1 coactivators in the control of energy metabolism. Acta Biochim Biophys Sin (Shanghai). 2011;43:248–57.CrossRef Liu C, Lin JD. PGC-1 coactivators in the control of energy metabolism. Acta Biochim Biophys Sin (Shanghai). 2011;43:248–57.CrossRef
78.
go back to reference Daitoku H, Sakamaki J, Fukamizu A. Regulation of FoxO transcription factors by acetylation and protein–protein interactions. Biochim Biophys Acta. 2011;1813:1954–60.CrossRefPubMed Daitoku H, Sakamaki J, Fukamizu A. Regulation of FoxO transcription factors by acetylation and protein–protein interactions. Biochim Biophys Acta. 2011;1813:1954–60.CrossRefPubMed
79.
go back to reference Corton JC, Brown-Borg HM. Peroxisome proliferator-activated receptor gamma coactivator 1 in caloric restriction and other models of longevity. J Gerontol A Biol Sci Med Sci. 2005;60:1494–509.CrossRefPubMed Corton JC, Brown-Borg HM. Peroxisome proliferator-activated receptor gamma coactivator 1 in caloric restriction and other models of longevity. J Gerontol A Biol Sci Med Sci. 2005;60:1494–509.CrossRefPubMed
80.
go back to reference Selesniemi K, Lee HJ, Muhlhauser A, Tilly JL. Prevention of maternal aging-associated oocyte aneuploidy and meiotic spindle defects in mice by dietary and genetic strategies. Proc Natl Acad Sci USA. 2011;108:12319–24.PubMedCentralCrossRefPubMed Selesniemi K, Lee HJ, Muhlhauser A, Tilly JL. Prevention of maternal aging-associated oocyte aneuploidy and meiotic spindle defects in mice by dietary and genetic strategies. Proc Natl Acad Sci USA. 2011;108:12319–24.PubMedCentralCrossRefPubMed
81.
go back to reference Xiang Y, Xu J, Li L, Lin X, Chen X, Zhang X, Fu Y, Luo L. Calorie restriction increases primordial follicle reserve in mature female chemotherapy-treated rats. Gene. 2012;493:77–82.CrossRefPubMed Xiang Y, Xu J, Li L, Lin X, Chen X, Zhang X, Fu Y, Luo L. Calorie restriction increases primordial follicle reserve in mature female chemotherapy-treated rats. Gene. 2012;493:77–82.CrossRefPubMed
82.
go back to reference Selesniemi K, Lee HJ, Tilly JL. Moderate caloric restriction initiated in rodents during adulthood sustains function of the female reproductive axis into advanced chronological age. Aging Cell. 2008;7:622–9.PubMedCentralCrossRefPubMed Selesniemi K, Lee HJ, Tilly JL. Moderate caloric restriction initiated in rodents during adulthood sustains function of the female reproductive axis into advanced chronological age. Aging Cell. 2008;7:622–9.PubMedCentralCrossRefPubMed
83.
go back to reference Luzzo KM, Wang Q, Purcell SH, Chi M, Jimenez PT, Grindler N, Schedl T, Moley KH. High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects. PLoS ONE. 2012;7:e49217.PubMedCentralCrossRefPubMed Luzzo KM, Wang Q, Purcell SH, Chi M, Jimenez PT, Grindler N, Schedl T, Moley KH. High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects. PLoS ONE. 2012;7:e49217.PubMedCentralCrossRefPubMed
84.
go back to reference Cohen J, Scott R, Alikani M, Schimmel T, Munne S, Levron J, Wu L, Brenner C, Warner C, Willadsen S. Ooplasmic transfer in mature human oocytes. Mol Hum Reprod. 1998;4:269–80.CrossRefPubMed Cohen J, Scott R, Alikani M, Schimmel T, Munne S, Levron J, Wu L, Brenner C, Warner C, Willadsen S. Ooplasmic transfer in mature human oocytes. Mol Hum Reprod. 1998;4:269–80.CrossRefPubMed
85.
go back to reference Brenner CA, Barritt JA, Willadsen S, Cohen J. Mitochondrial DNA heteroplasmy after human ooplasmic transplantation. Fertil Steril. 2000;74:573–8.CrossRefPubMed Brenner CA, Barritt JA, Willadsen S, Cohen J. Mitochondrial DNA heteroplasmy after human ooplasmic transplantation. Fertil Steril. 2000;74:573–8.CrossRefPubMed
86.
go back to reference Barritt JA, Brenner CA, Malter HE, Cohen J. Mitochondria in human offspring derived from ooplasmic transplantation. Hum Reprod. 2001;16:513–6.CrossRefPubMed Barritt JA, Brenner CA, Malter HE, Cohen J. Mitochondria in human offspring derived from ooplasmic transplantation. Hum Reprod. 2001;16:513–6.CrossRefPubMed
88.
go back to reference Perez GI, Trbovich AM, Gosden RG, Tilly JL. Mitochondria and the death of oocytes. Nature. 2000;403:500–1.CrossRefPubMed Perez GI, Trbovich AM, Gosden RG, Tilly JL. Mitochondria and the death of oocytes. Nature. 2000;403:500–1.CrossRefPubMed
89.
go back to reference Woods DC, White YA, Tilly JL. Purification of oogonial stem cells from adult mouse and human ovaries: an assessment of the literature and a view toward the future. Reprod Sci. 2013;20:7–15.PubMedCentralCrossRefPubMed Woods DC, White YA, Tilly JL. Purification of oogonial stem cells from adult mouse and human ovaries: an assessment of the literature and a view toward the future. Reprod Sci. 2013;20:7–15.PubMedCentralCrossRefPubMed
90.
go back to reference Woods DC, Tilly JL. Isolation, characterization and propagation of mitotically active germ cells from adult mouse and human ovaries. Nat Protoc. 2013;8:966–88.CrossRefPubMed Woods DC, Tilly JL. Isolation, characterization and propagation of mitotically active germ cells from adult mouse and human ovaries. Nat Protoc. 2013;8:966–88.CrossRefPubMed
Metadata
Title
Oocyte aging underlies female reproductive aging: biological mechanisms and therapeutic strategies
Authors
Hideki Igarashi
Toshifumi Takahashi
Satoru Nagase
Publication date
01-10-2015
Publisher
Springer Japan
Published in
Reproductive Medicine and Biology / Issue 4/2015
Print ISSN: 1445-5781
Electronic ISSN: 1447-0578
DOI
https://doi.org/10.1007/s12522-015-0209-5

Other articles of this Issue 4/2015

Reproductive Medicine and Biology 4/2015 Go to the issue