Germline energetics, aging, and female infertility

Cell Metabolism

Volumn 17, Issue 6, 2013, Pages 838-850

  Tilly, Jonathan L ^a,b   Sinclair, David A ^b,c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MITOCHONDRIAL DNA; PHOSPHATIDYLINOSITOL 3 KINASE; SIRTUIN 1; SOMATOMEDIN C;

AGING; APOPTOSIS; CALCIUM CELL LEVEL; CELL ENERGY; CHROMOSOME ABERRATION; CHROMOSOME SEGREGATION; DIET RESTRICTION; EMBRYO DEVELOPMENT; ENERGY YIELD; FEMALE FERTILITY; FEMALE GENITAL SYSTEM; FEMALE INFERTILITY; FERTILIZATION IN VITRO; GENE SILENCING; GERM CELL; GERM LINE; HUMAN; LONGEVITY; MEIOSIS; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL GENOME; MITOCHONDRIAL RESPIRATION; NONHUMAN; NUTRIENT AVAILABILITY; OOCYTE; OOCYTE DEVELOPMENT; OOCYTE DONATION; OOCYTE MATURATION; OVARIAN RESERVE; OVARY FUNCTION; OVARY INSUFFICIENCY; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; REPRODUCTION; REVIEW; SPERMATOZOON MOTILITY; SPERMATOZOON PENETRATION;

AGING; ANIMALS; CALORIC RESTRICTION; FEMALE; GERM CELLS; HUMANS; INFERTILITY, FEMALE; MENOPAUSE; MICE; MITOCHONDRIA; OOCYTES; OOGENESIS; OVARY; RATS; STEM CELLS;

MAMMALIA;

EID: 84878785222     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2013.05.007     Document Type: Review

References (158)

1. B.M. Acton, I. Lai, X. Shang, A. Jurisicova, and R.F. Casper Neutral mitochondrial heteroplasmy alters physiological function in mice Biol. Reprod. 77 2007 569 576
2. R.J. Aitken Free radicals, lipid peroxidation and sperm function Reprod. Fertil. Dev. 7 1995 659 668
3. G. Angelo, and M.R. Van Gilst Starvation protects germline stem cells and extends reproductive longevity in C. elegans Science 326 2009 954 958
4. S. Bahadorani, J. Cho, T. Lo, H. Contreras, H.O. Lawal, D.E. Krantz, T.J. Bradley, and D.W. Walker Neuronal expression of a single-subunit yeast NADH-ubiquinone oxidoreductase (Ndi1) extends Drosophila lifespan Aging Cell 9 2010 191 202
5. J.A. Barritt, C.A. Brenner, H.E. Malter, and J. Cohen Mitochondria in human offspring derived from ooplasmic transplantation Hum. Reprod. 16 2001 513 516
6. G.W. Bates Body weight control practice as a cause of infertility Clin. Obstet. Gynecol. 28 1985 632 644
7. J.A. Baur, K.J. Pearson, N.L. Price, H.A. Jamieson, C. Lerin, A. Kalra, V.V. Prabhu, J.S. Allard, G. Lopez-Lluch, and K. Lewis Resveratrol improves health and survival of mice on a high-calorie diet Nature 444 2006 337 342
8. C.A. Benadiva, I. Kligman, and S. Munné Aneuploidy 16 in human embryos increases significantly with maternal age Fertil. Steril. 66 1996 248 255
9. Y. Bentov, N. Esfandiari, E. Burstein, and R.F. Casper The use of mitochondrial nutrients to improve the outcome of infertility treatment in older patients Fertil. Steril. 93 2010 272 275
10. Y. Bentov, T. Yavorska, N. Esfandiari, A. Jurisicova, and R.F. Casper The contribution of mitochondrial function to reproductive aging J. Assist. Reprod. Genet. 28 2011 773 783
11. N.A. Bishop, and L. Guarente Two neurons mediate diet-restriction-induced longevity in C. elegans Nature 447 2007 545 549
12. C.A. Blum, J.L. Ellis, C. Loh, P.Y. Ng, R.B. Perni, and R.L. Stein SIRT1 modulation as a novel approach to the treatment of diseases of aging J. Med. Chem. 54 2011 417 432
13. C.A. Brenner, Y.M. Wolny, J.A. Barritt, D.W. Matt, S. Munné, and J. Cohen Mitochondrial DNA deletion in human oocytes and embryos Mol. Hum. Reprod. 4 1998 887 892
14. C.A. Brenner, J.A. Barritt, S. Willadsen, and J. Cohen Mitochondrial DNA heteroplasmy after human ooplasmic transplantation Fertil. Steril. 74 2000 573 578
15. D.T. Brown, D.C. Samuels, E.M. Michael, D.M. Turnbull, and P.F. Chinnery Random genetic drift determines the level of mutant mtDNA in human primary oocytes Am. J. Hum. Genet. 68 2001 533 536
16. H. Buckler The menopause transition: endocrine changes and clinical symptoms J. Br. Menopause Soc. 11 2005 61 65
17. C. Cantó, and J. Auwerx PGC-1α, SIRT1 and AMPK, an energy sensing network that controls energy expenditure Curr. Opin. Lipidol. 20 2009 98 105
18. + metabolism and SIRT1 activity Nature 458 2009 1056 1060
19. F.M. Cerqueira, F.R. Laurindo, and A.J. Kowaltowski Mild mitochondrial uncoupling and calorie restriction increase fasting eNOS, akt and mitochondrial biogenesis PLoS ONE 6 2011 e18433 10.1371/journal.pone.0018433
20. T. Chiba, T. Tsuchiya, T. Komatsu, R. Mori, H. Hayashi, and I. Shimokawa Development of calorie restriction mimetics as therapeutics for obesity, diabetes, inflammatory and neurodegenerative diseases Curr. Genomics 11 2010 562 567
21. J. Cho, J.H. Hur, and D.W. Walker The role of mitochondria in Drosophila aging Exp. Gerontol. 46 2011 331 334
22. A.E. Civitarese, S. Carling, L.K. Heilbronn, M.H. Hulver, B. Ukropcova, W.A. Deutsch, S.R. Smith, E. Ravussin CALERIE Pennington Team Calorie restriction increases muscle mitochondrial biogenesis in healthy humans PLoS Med. 4 2007 e76 10.1371/journal.pmed.0040076
23. J. Cohen, R. Scott, T. Schimmel, J. Levron, and S. Willadsen Birth of infant after transfer of anucleate donor oocyte cytoplasm into recipient eggs Lancet 350 1997 186 187
24. J. Cohen, R. Scott, M. Alikani, T. Schimmel, S. Munné, J. Levron, L. Wu, C.A. Brenner, C. Warner, and S. Willadsen Ooplasmic transfer in mature human oocytes Mol. Hum. Reprod. 4 1998 269 280
25. J. Cummins Mitochondrial DNA in mammalian reproduction Rev. Reprod. 3 1998 172 182
26. + and is a causative event in the death of myocytes in postischemic reperfusion of the heart J. Biol. Chem. 276 2001 2571 2575
27. F. Di Lisa, N. Kaludercic, A. Carpi, R. Menabò, and M. Giorgio Mitochondria and vascular pathology Pharmacol. Rep. 61 2009 123 130
28. 2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production Development 131 2004 3057 3067
29. R. Dumollard, M. Duchen, and J. Carroll The role of mitochondrial function in the oocyte and embryo Curr. Top. Dev. Biol. 77 2007 21 49
30. H.E. Duran, F. Simsek-Duran, S.C. Oehninger, H.W. Jones Jr., and F.J. Castora The association of reproductive senescence with mitochondrial quantity, function, and DNA integrity in human oocytes at different stages of maturation Fertil. Steril. 96 2011 384 388
31. J. Durieux, S. Wolff, and A. Dillin The cell-non-autonomous nature of electron transport chain-mediated longevity Cell 144 2011 79 91
32. U. Eichenlaub-Ritter, E. Vogt, H. Yin, and R. Gosden Spindles, mitochondria and redox potential in ageing oocytes Reprod. Biomed. Online 8 2004 45 58
33. S.H. El Shourbagy, E.C. Spikings, M. Freitas, and J.C. St John Mitochondria directly influence fertilisation outcome in the pig Reproduction 131 2006 233 245
34. M.J. Faddy, R.G. Gosden, A. Gougeon, S.J. Richardson, and J.F. Nelson Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause Hum. Reprod. 7 1992 1342 1346
35. J.N. Feige, M. Lagouge, C. Canto, A. Strehle, S.M. Houten, J.C. Milne, P.D. Lambert, C. Mataki, P.J. Elliott, and J. Auwerx Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation Cell Metab. 8 2008 347 358
36. M. Ferguson, R.J. Mockett, Y. Shen, W.C. Orr, and R.S. Sohal Age-associated decline in mitochondrial respiration and electron transport in Drosophila melanogaster Biochem. J. 390 2005 501 511
37. T. Flatt, K.J. Min, C. D'Alterio, E. Villa-Cuesta, J. Cumbers, R. Lehmann, D.L. Jones, and M. Tatar Drosophila germ-line modulation of insulin signaling and lifespan Proc. Natl. Acad. Sci. USA 105 2008 6368 6373
38. J.A. Funk, S. Odejinmi, and R.G. Schnellmann SRT1720 induces mitochondrial biogenesis and rescues mitochondrial function after oxidant injury in renal proximal tubule cells J. Pharmacol. Exp. Ther. 333 2010 593 601
39. M.E. Gaulden Maternal age effect: the enigma of Down syndrome and other trisomic conditions Mutat. Res. 296 1992 69 88
40. Z. Gerhart-Hines, J.T. Rodgers, O. Bare, C. Lerin, S.H. Kim, R. Mostoslavsky, F.W. Alt, Z. Wu, and P. Puigserver Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1α EMBO J. 26 2007 1913 1923
41. R.E. Giles, H. Blanc, H.M. Cann, and D.C. Wallace Maternal inheritance of human mitochondrial DNA Proc. Natl. Acad. Sci. USA 77 1980 6715 6719
42. R.G. Gosden, S.C. Laing, L.S. Felicio, J.F. Nelson, and C.E. Finch Imminent oocyte exhaustion and reduced follicular recruitment mark the transition to acyclicity in aging C57BL/6J mice Biol. Reprod. 28 1983 255 260
43. A. Gougeon Regulation of ovarian follicular development in primates: facts and hypotheses Endocr. Rev. 17 1996 121 155
44. R.C. Grandison, M.D. Piper, and L. Partridge Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila Nature 462 2009 1061 1064
45. L. Guarente Mitochondria - a nexus for aging, calorie restriction, and sirtuins? Cell 132 2008 171 176
46. A.V. Hafner, J. Dai, A.P. Gomes, C.Y. Xiao, C.M. Palmeira, A. Rosenzweig, and D.A. Sinclair Regulation of the mPTP by SIRT3-mediated deacetylation of CypD at lysine 166 suppresses age-related cardiac hypertrophy Aging (Albany NY) 2 2010 914 923
47. C.R. Hancock, D.H. Han, K. Higashida, S.H. Kim, and J.O. Holloszy Does calorie restriction induce mitochondrial biogenesis? A reevaluation FASEB J. 25 2011 785 791
48. A.J. Harvey, T.C. Gibson, T.M. Quebedeaux, and C.A. Brenner Impact of assisted reproductive technologies: a mitochondrial perspective of cytoplasmic transplantation Curr. Top. Dev. Biol. 77 2007 229 249
49. T. Hassold, and D. Chiu Maternal age-specific rates of numerical chromosome abnormalities with special reference to trisomy Hum. Genet. 70 1985 11 17
50. T. Hassold, and P. Hunt Maternal age and chromosomally abnormal pregnancies: what we know and what we wish we knew Curr. Opin. Pediatr. 21 2009 703 708
51. H. Hsin, and C. Kenyon Signals from the reproductive system regulate the lifespan of C. elegans Nature 399 1999 362 366
52. P.A. Hunt The control of mammalian female meiosis: factors that influence chromosome segregation J. Assist. Reprod. Genet. 15 1998 246 252
53. C.A. Hutchison 3rd, J.E. Newbold, S.S. Potter, and M.H. Edgell Maternal inheritance of mammalian mitochondrial DNA Nature 251 1974 536 538
54. H. Igarashi, E. Takahashi, M. Hiroi, and K. Doi Aging-related changes in calcium oscillations in fertilized mouse oocytes Mol. Reprod. Dev. 48 1997 383 390
55. H. Igarashi, T. Takahashi, E. Takahashi, N. Tezuka, K. Nakahara, K. Takahashi, and H. Kurachi Aged mouse oocytes fail to readjust intracellular adenosine triphosphates at fertilization Biol. Reprod. 72 2005 1256 1261
56. R.P. Jansen Germline passage of mitochondria: quantitative considerations and possible embryological sequelae Hum. Reprod. 15 Suppl 2 2000 112 128
57. R.P. Jansen, and G.J. Burton Mitochondrial dysfunction in reproduction Mitochondrion 4 2004 577 600
58. R.P. Jansen, and K. de Boer The bottleneck: mitochondrial imperatives in oogenesis and ovarian follicular fate Mol. Cell. Endocrinol. 145 1998 81 88
59. H. Jasper, and D.L. Jones Metabolic regulation of stem cell behavior and implications for aging Cell Metab. 12 2010 561 565
60. J.C. Jiang, E. Jaruga, M.V. Repnevskaya, and S.M. Jazwinski An intervention resembling caloric restriction prolongs life span and retards aging in yeast FASEB J. 14 2000 2135 2137
61. D.L. Johannsen, and E. Ravussin The role of mitochondria in health and disease Curr. Opin. Pharmacol. 9 2009 780 786
62. J. Johnson, J. Canning, T. Kaneko, J.K. Pru, and J.L. Tilly Germline stem cells and follicular renewal in the postnatal mammalian ovary Nature 428 2004 145 150
63. H. Kaneda, J. Hayashi, S. Takahama, C. Taya, K.F. Lindahl, and H. Yonekawa Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis Proc. Natl. Acad. Sci. USA 92 1995 4542 4546
64. S. Kao, H.T. Chao, and Y.H. Wei Mitochondrial deoxyribonucleic acid 4977-bp deletion is associated with diminished fertility and motility of human sperm Biol. Reprod. 52 1995 729 736
65. S.D. Katewa, and P. Kapahi Role of TOR signaling in aging and related biological processes in Drosophila melanogaster Exp. Gerontol. 46 2011 382 390
66. Y. Kawamura, Y. Uchijima, N. Horike, K. Tonami, K. Nishiyama, T. Amano, T. Asano, Y. Kurihara, and H. Kurihara Sirt3 protects in vitro-fertilized mouse preimplantation embryos against oxidative stress-induced p53-mediated developmental arrest J. Clin. Invest. 120 2010 2817 2828
67. D. Kirilly, and T. Xie The Drosophila ovary: an active stem cell community Cell Res. 17 2007 15 25
68. T.B. Kirkwood Immortality of the germ-line versus disposability of the soma Basic Life Sci. 42 1987 209 218
69. T.B. Kirkwood Understanding the odd science of aging Cell 120 2005 437 447
70. T.B. Kirkwood, and R. Holliday The evolution of ageing and longevity Proc. R. Soc. Lond. B Biol. Sci. 205 1979 531 546
71. A.J. Klar, S. Fogel, and K. Macleod MAR1 - a regulator of the HMa and HMα loci in Saccharomyces cerevisiae Genetics 93 1979 37 50
72. J. Klein, and M.V. Sauer Oocyte donation Best Pract. Res. Clin. Obstet. Gynaecol. 16 2002 277 291
73. M. Lagouge, C. Argmann, Z. Gerhart-Hines, H. Meziane, C. Lerin, F. Daussin, N. Messadeq, J. Milne, P. Lambert, and P. Elliott Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1α Cell 127 2006 1109 1122
74. S.E. Lanzendorf, J.F. Mayer, J. Toner, S. Oehninger, D.S. Saffan, and S. Muasher Pregnancy following transfer of ooplasm from cryopreserved-thawed donor oocytes into recipient oocytes Fertil. Steril. 71 1999 575 577
75. N.G. Larsson, J. Wang, H. Wilhelmsson, A. Oldfors, P. Rustin, M. Lewandoski, G.S. Barsh, and D.A. Clayton Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice Nat. Genet. 18 1998 231 236
76. S.E. Lee, S.C. Sun, H.Y. Choi, S.J. Uhm, and N.H. Kim mTOR is required for asymmetric division through small GTPases in mouse oocytes Mol. Reprod. Dev. 79 2012 356 366
77. J. Li, K. Kawamura, Y. Cheng, S. Liu, C. Klein, S. Liu, E.K. Duan, and A.J. Hsueh Activation of dormant ovarian follicles to generate mature eggs Proc. Natl. Acad. Sci. USA 107 2010 10280 10284
78. M.T. Lin, and M.F. Beal Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases Nature 443 2006 787 795
79. S. Lintern-Moore, and A.V. Everitt The effect of restricted food intake on the size and composition of the ovarian follicle population in the Wistar rat Biol. Reprod. 19 1978 688 691
80. L. Liu, J. Zhu, P.R. Brink, P.S. Glass, and M.J. Rebecchi Age-associated differences in the inhibition of mitochondrial permeability transition pore opening by cyclosporine A Acta Anaesthesiol. Scand. 55 2011 622 630
81. G. López-Lluch, N. Hunt, B. Jones, M. Zhu, H. Jamieson, S. Hilmer, M.V. Cascajo, J. Allard, D.K. Ingram, P. Navas, and R. de Cabo Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency Proc. Natl. Acad. Sci. USA 103 2006 1768 1773
82. G. López-Lluch, P.M. Irusta, P. Navas, and R. de Cabo Mitochondrial biogenesis and healthy aging Exp. Gerontol. 43 2008 813 819
83. L.L. Luo, X.C. Chen, Y.C. Fu, J.J. Xu, L. Li, X.H. Lin, Y.F. Xiang, and X.M. Zhang The effects of caloric restriction and a high-fat diet on ovarian lifespan and the expression of SIRT1 and SIRT6 proteins in rats Aging Clin. Exp. Res. 24 2012 125 133
84. T.J. Matthews, and B.E. Hamilton Delayed childbearing: more women are having their first child later in life NCHS Data Brief. 21 2009 1 8
85. M.M. Matzuk, K.H. Burns, M.M. Viveiros, and J.J. Eppig Intercellular communication in the mammalian ovary: oocytes carry the conversation Science 296 2002 2178 2180
86. C.J. McLeod, L. Wang, C. Wong, and D.L. Jones Stem cell dynamics in response to nutrient availability Curr. Biol. 20 2010 2100 2105
87. R.K. Minor, J.A. Baur, A.P. Gomes, T.M. Ward, A. Csiszar, E. Mercken, K. Abdelmohsen, Y. Shin, C. Canto, and M. Scheibye-Knudsen SRT1720 improves survival and healthspan of obese mice Sci. Rep. 1 2011 70 10.1038/srep00070
88. P.M. Motta, S.A. Nottola, S. Makabe, and R. Heyn Mitochondrial morphology in human fetal and adult female germ cells Hum. Reprod. 15 Suppl 2 2000 129 147
89. J. Müller-Höcker, S. Schäfer, S. Weis, C. Münscher, and T. Strowitzki Morphological-cytochemical and molecular genetic analyses of mitochondria in isolated human oocytes in the reproductive age Mol. Hum. Reprod. 2 1996 951 958
90. S. Munné, and J. Cohen Chromosome abnormalities in human embryos Hum. Reprod. Update 4 1998 842 855
91. S. Munné, M. Alikani, G. Tomkin, J. Grifo, and J. Cohen Embryo morphology, developmental rates, and maternal age are correlated with chromosome abnormalities Fertil. Steril. 64 1995 382 391
92. S. Nakamura, K. Kobayashi, T. Nishimura, S. Higashijima, and M. Tanaka Identification of germline stem cells in the ovary of the teleost medaka Science 328 2010 1561 1563
93. D. Navot, P.A. Bergh, M.A. Williams, G.J. Garrisi, I. Guzman, B. Sandler, and L. Grunfeld Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility Lancet 337 1991 1375 1377
94. J.F. Nelson, R.G. Gosden, and L.S. Felicio Effect of dietary restriction on estrous cyclicity and follicular reserves in aging C57BL/6J mice Biol. Reprod. 32 1985 515 522
95. M. Orisaka, K. Tajima, B.K. Tsang, and F. Kotsuji Oocyte-granulosa-theca cell interactions during preantral follicular development J. Ovarian Res. 2 2009 9 10.1186/1757-2215-2-9
96. T.B. Osborne, L.B. Mendel, and E.L. Ferry The effect of retardation of growth upon the breeding period and duration of life of rats Science 45 1917 294 295
97. J. Pacchiarotti, C. Maki, T. Ramos, J. Marh, K. Howerton, J. Wong, J. Pham, S. Anorve, Y.C. Chow, and F. Izadyar Differentiation potential of germ line stem cells derived from the postnatal mouse ovary Differentiation 79 2010 159 170
98. C.S. Palmer, L.D. Osellame, D. Stojanovski, and M.T. Ryan The regulation of mitochondrial morphology: intricate mechanisms and dynamic machinery Cell. Signal. 23 2011 1534 1545
99. R.J. Paulson, R. Boostanfar, P. Saadat, E. Mor, D.E. Tourgeman, C.C. Slater, M.M. Francis, and J.K. Jain Pregnancy in the sixth decade of life: obstetric outcomes in women of advanced reproductive age JAMA 288 2002 2320 2323
100. G.I. Perez, A.M. Trbovich, R.G. Gosden, and J.L. Tilly Mitochondria and the death of oocytes Nature 403 2000 500 501
101. L. Pikó, and L. Matsumoto Number of mitochondria and some properties of mitochondrial DNA in the mouse egg Dev. Biol. 49 1976 1 10
102. L. Pikó, and K.D. Taylor Amounts of mitochondrial DNA and abundance of some mitochondrial gene transcripts in early mouse embryos Dev. Biol. 123 1987 364 374
103. K. Powell Going against the grain PLoS Biol. 5 2007 e338 10.1371/journal.pbio.0050338
104. J.C. Prior Perimenopause: the complex endocrinology of the menopausal transition Endocr. Rev. 19 1998 397 428
105. P. Reddy, L. Liu, D. Adhikari, K. Jagarlamudi, S. Rajareddy, Y. Shen, C. Du, W. Tang, T. Hämäläinen, and S.L. Peng Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool Science 319 2008 611 613
106. M. Rera, S. Bahadorani, J. Cho, C.L. Koehler, M. Ulgherait, J.H. Hur, W.S. Ansari, T. Lo Jr., D.L. Jones, and D.W. Walker Modulation of longevity and tissue homeostasis by the Drosophila PGC-1 homolog Cell Metab. 14 2011 623 634
107. P. Reynier, M.F. Chrétien, F. Savagner, G. Larcher, V. Rohmer, P. Barrière, and Y. Malthièry Long PCR analysis of human gamete mtDNA suggests defective mitochondrial maintenance in spermatozoa and supports the bottleneck theory for oocytes Biochem. Biophys. Res. Commun. 252 1998 373 377
108. P. Reynier, P. May-Panloup, M.F. Chrétien, C.J. Morgan, M. Jean, F. Savagner, P. Barrière, and Y. Malthièry Mitochondrial DNA content affects the fertilizability of human oocytes Mol. Hum. Reprod. 7 2001 425 429
109. S.J. Richardson, V. Senikas, and J.F. Nelson Follicular depletion during the menopausal transition: evidence for accelerated loss and ultimate exhaustion J. Clin. Endocrinol. Metab. 65 1987 1231 1237
110. E. Ruiz-Pesini, A.C. Lapeña, C. Díez, E. Alvarez, J.A. Enríquez, and M.J. López-Pérez Seminal quality correlates with mitochondrial functionality Clin. Chim. Acta 300 2000 97 105
111. T.A. Santos, S. El Shourbagy, and J.C. St John Mitochondrial content reflects oocyte variability and fertilization outcome Fertil. Steril. 85 2006 584 591
112. A.H. Sathananthan, and A.O. Trounson Mitochondrial morphology during preimplantational human embryogenesis Hum. Reprod. 15 Suppl 2 2000 148 159
113. M.V. Sauer, R.J. Paulson, and R.A. Lobo Reversing the natural decline in human fertility. An extended clinical trial of oocyte donation to women of advanced reproductive age JAMA 268 1992 1275 1279
114. M.V. Sauer, R.J. Paulson, and R.A. Lobo Pregnancy in women 50 or more years of age: outcomes of 22 consecutively established pregnancies from oocyte donation Fertil. Steril. 64 1995 111 115
115. E.A. Schon, S.H. Kim, J.C. Ferreira, P. Magalhães, M. Grace, D. Warburton, and S.J. Gross Chromosomal non-disjunction in human oocytes: is there a mitochondrial connection? Hum. Reprod. 15 Suppl 2 2000 160 172
116. K. Selesniemi, H.J. Lee, and J.L. Tilly Moderate caloric restriction initiated in rodents during adulthood sustains function of the female reproductive axis into advanced chronological age Aging Cell 7 2008 622 629
117. K. Selesniemi, H.-J. Lee, A. Muhlhauser, and J.L. Tilly Prevention of maternal aging-associated oocyte aneuploidy and meiotic spindle defects in mice by dietary and genetic strategies Proc. Natl. Acad. Sci. USA 108 2011 12319 12324
118. D.P. Shanley, and T.B. Kirkwood Calorie restriction and aging: a life-history analysis Evolution 54 2000 740 750
119. M.S. Sharpley, C. Marciniak, K. Eckel-Mahan, M. McManus, M. Crimi, K. Waymire, C.S. Lin, S. Masubuchi, N. Friend, and M. Koike Heteroplasmy of mouse mtDNA is genetically unstable and results in altered behavior and cognition Cell 151 2012 333 343
120. K.R. Short, M.L. Bigelow, J. Kahl, R. Singh, J. Coenen-Schimke, S. Raghavakaimal, and K.S. Nair Decline in skeletal muscle mitochondrial function with aging in humans Proc. Natl. Acad. Sci. USA 102 2005 5618 5623
121. E.C. Spikings, J. Alderson, and J.C. St John Transmission of mitochondrial DNA following assisted reproduction and nuclear transfer Hum. Reprod. Update 12 2006 401 415
122. E.C. Spikings, J. Alderson, and J.C. St John Regulated mitochondrial DNA replication during oocyte maturation is essential for successful porcine embryonic development Biol. Reprod. 76 2007 327 335
123. J.C. St John, R.P. Jokhi, and C.L. Barratt Men with oligoasthenoteratozoospermia harbour higher numbers of multiple mitochondrial DNA deletions in their spermatozoa, but individual deletions are not indicative of overall aetiology Mol. Hum. Reprod. 7 2001 103 111
124. P. Sutovsky, R.D. Moreno, J. Ramalho-Santos, T. Dominko, C. Simerly, and G. Schatten Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos Biol. Reprod. 63 2000 582 590
125. P. Sutovsky, K. Van Leyen, T. McCauley, B.N. Day, and M. Sutovsky Degradation of paternal mitochondria after fertilization: implications for heteroplasmy, assisted reproductive technologies and mtDNA inheritance Reprod. Biomed. Online 8 2004 24 33
126. M. Suwa, T. Egashira, H. Nakano, H. Sasaki, and S. Kumagai Metformin increases the PGC-1α protein and oxidative enzyme activities possibly via AMPK phosphorylation in skeletal muscle in vivo J. Appl. Physiol. 101 2006 1685 1692
127. J.J. Tarín, S. Pérez-Albalá, and A. Cano Oral antioxidants counteract the negative effects of female aging on oocyte quantity and quality in the mouse Mol. Reprod. Dev. 61 2002 385 397
128. J.J. Tarín, S. Pérez-Albalá, J.F. Pertusa, and A. Cano Oral administration of pharmacological doses of vitamins C and E reduces reproductive fitness and impairs the ovarian and uterine functions of female mice Theriogenology 57 2002 1539 1550
129. J.L. Tilly Commuting the death sentence: how oocytes strive to survive Nat. Rev. Mol. Cell Biol. 2 2001 838 848
130. J.L. Tilly, Y. Niikura, and B.R. Rueda The current status of evidence for and against postnatal oogenesis in mammals: a case of ovarian optimism versus pessimism? Biol. Reprod. 80 2009 2 12
131. S. Törnroth-Horsefield, and R. Neutze Opening and closing the metabolite gate Proc. Natl. Acad. Sci. USA 105 2008 19565 19566
132. J. Van Blerkom Developmental failure in human reproduction associated with preovulatory oogenesis and preimplantation embryogenesis J. Van Blerkom, P. Motta, Ultrastructure of Human Gametogenesis and and Embryogenesis 1989 Kluwer Academic Publishers Boston 125 180
133. J. Van Blerkom Morphodynamics of nuclear and cytoplasmic reorganization during the resumption of arrested meiosis in the mouse oocyte Prog. Clin. Biol. Res. 294 1989 33 51
134. J. Van Blerkom Development of human embryos to the hatched blastocyst stage in the presence or absence of a monolayer of Vero cells Hum. Reprod. 8 1993 1525 1539
135. J. Van Blerkom Mitochondria as regulatory forces in oocytes, preimplantation embryos and stem cells Reprod. Biomed. Online 16 2008 553 569
136. J. Van Blerkom Mitochondrial function in the human oocyte and embryo and their role in developmental competence Mitochondrion 11 2011 797 813
137. J. Van Blerkom, and P. Motta The Cellular Basis of Mammalian Reproduction 1979 Urban and Schwarzenberg Munich
138. J. Van Blerkom, C. Manes, and J.C. Daniel Jr. Development of preimplantation rabbit embryos in vivo and in vitro. I. An ultrastructural comparison Dev. Biol. 35 1973 262 282
139. J. Van Blerkom, P.W. Davis, and J. Lee ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer Hum. Reprod. 10 1995 415 424
140. J. Van Blerkom, J. Sinclair, and P. Davis Mitochondrial transfer between oocytes: potential applications of mitochondrial donation and the issue of heteroplasmy Hum. Reprod. 13 1O 1998 2857 2868
141. A.D. van Diepeningen, S.M. Slakhorst, A.B. Koopmanschap, G.J. Ikink, A.J. Debets, and R.F. Hoekstra Calorie restriction in the filamentous fungus Podospora anserina Exp. Gerontol. 45 2010 516 524
142. S.J. Ventura Trends and variations in first births to older women, United States, 1970-86 Vital Health Stat. 21 47 1989 1 27
143. M.B. Visscher, J.T. King, and Y.C. Lee Further studies on influence of age and diet upon reproductive senescence in strain A female mice Am. J. Physiol. 170 1952 72 76
144. A.D. Vitullo, and J.P. Ozil Repetitive calcium stimuli drive meiotic resumption and pronuclear development during mouse oocyte activation Dev. Biol. 151 1992 128 136
145. T. Wai, D. Teoli, and E.A. Shoubridge The mitochondrial DNA genetic bottleneck results from replication of a subpopulation of genomes Nat. Genet. 40 2008 1484 1488
146. T. Wai, A. Ao, X. Zhang, D. Cyr, D. Dufort, and E.A. Shoubridge The role of mitochondrial DNA copy number in mammalian fertility Biol. Reprod. 83 2010 52 62
147. D.C. Wallace A mitochondrial paradigm for degenerative diseases and ageing Novartis Found. Symp. 235 2001 247 263 discussion 263-266
148. Y.A.R. White, D.C. Woods, Y. Takai, O. Ishihara, H. Seki, and J.L. Tilly Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women Nat. Med. 18 2012 413 421
149. J.G. Wood, B. Rogina, S. Lavu, K. Howitz, S.L. Helfand, M. Tatar, and D. Sinclair Sirtuin activators mimic caloric restriction and delay ageing in metazoans Nature 430 2004 686 689
150. D.C. Woods, and J.L. Tilly Oogonial stem cells: a source for autologous germline mitochondria Reprod. Sci. 20 2013 7 15
151. D.C. Woods, Y.A.R. White, and J.L. Tilly Purification of oogonial stem cells from adult mouse and human ovaries: an assessment of the literature and a view toward the future Reprod. Sci. 20 2013 7 15
152. Y.-C. Yi, M.-J. Chen, J.Y.-P. Ho, H.-F. Guu, and E.-S. Ho Mitochondria transfer can enhance the murine embryo development J. Assist. Reprod. Genet. 24 2007 445 449
153. P. Zheng, R. Vassena, and K.E. Latham Effects of in vitro oocyte maturation and embryo culture on the expression of glucose transporters, glucose metabolism and insulin signaling genes in rhesus monkey oocytes and preimplantation embryos Mol. Hum. Reprod. 13 2007 361 371
154. W. Zheng, N. Gorre, Y. Shen, T. Noda, W. Ogawa, E. Lundin, and K. Liu Maternal phosphatidylinositol 3-kinase signalling is crucial for embryonic genome activation and preimplantation embryogenesis EMBO Rep. 11 2010 890 895
155. B.M. Zid, A.N. Rogers, S.D. Katewa, M.A. Vargas, M.C. Kolipinski, T.A. Lu, S. Benzer, and P. Kapahi 4E-BP extends lifespan upon dietary restriction by enhancing mitochondrial activity in Drosophila Cell 139 2009 149 160
156. Zoon, K.C. (2001). Human cells used in therapy involving the transfer of genetic material by means other than the union of gamete nuclei. U.S. Food and Drug Administration, http://www.fda.gov/BiologicsBloodVaccines/ SafetyAvailability/ucm105852.htm.
157. K. Zou, Z. Yuan, Z. Yang, H. Luo, K. Sun, L. Zhou, J. Xiang, L. Shi, Q. Yu, and Y. Zhang Production of offspring from a germline stem cell line derived from neonatal ovaries Nat. Cell Biol. 11 2009 631 636
158. S. Zuckerman The number of oocytes in the mature ovary Recent Prog. Horm. Res. 6 1951 63 108