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Cited by 38Reproductive Biology and FertilitySperm and Testicular FunctionGenetics, Aging, and Longevity in Model Organisms

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Reproductive aging: biological pathways and potential interventive strategies

Liu, Yuanyuan, Gao, Jinmin·2023·Journal of Genetics and Genomics
DOI 10.1016/j.jgg.2022.07.002
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Abstract

Reproductive aging is a natural process conserved across species and is well-known in females. It shows age-related follicle depletion and reduction of oocyte quality, eventually causing reproductive senescence and menopause. Although reproductive aging in males is not well noticed as in females, it also causes infertility and has deleterious consequences on the offspring. Various factors have been suggested to contribute to reproductive aging, including oxidative stress, mitochondrial defects, telomere shortening, meiotic chromosome segregation errors and genetic alterations. With the increasing trend of pregnancy age, it is particularly crucial to find interventions to preserve or extend human fertility. Studies in humans and model organisms have provided insights into the biological pathways associated with reproductive aging, and a series of potential interventive strategies have been tested. Here, we review factors affecting reproductive aging in females and males and summarize interventive strategies that may help delay or rescue the aging phenotypes of reproduction.

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Research works printed but not linked: 95

  1. Agarwal, 2012, The effects of oxidative stress on female reproduction: a review, Reprod. Biol. Endocrinol., 10, 49, 10.1186/1477-7827-10-49 · DOI
  2. Astolfi, 1999, Risks of preterm delivery and association with maternal age, birth order, and fetal gender, Hum. Reprod., 14, 2891, 10.1093/humrep/14.11.2891 · DOI
  3. Aston, 2012, Divergence of sperm and leukocyte age-dependent telomere dynamics: implications for male-driven evolution of telomere length in humans, Mol. Hum. Reprod., 18, 517, 10.1093/molehr/gas028 · DOI
  4. Belloc, 2008, Effect of maternal and paternal age on pregnancy and miscarriage rates after intrauterine insemination, Reprod. Biomed. Online, 17, 392, 10.1016/S1472-6483(10)60223-4 · DOI
  5. Ben-Meir, 2015, Coenzyme Q10 restores oocyte mitochondrial function and fertility during reproductive aging, Aging Cell, 14, 887, 10.1111/acel.12368 · DOI
  6. Ben-Meir, 2019, Co-enzyme Q10 supplementation rescues cumulus cells dysfunction in a maternal aging model, Antioxidants, 8, 58, 10.3390/antiox8030058 · DOI
  7. Bertoldo, 2020, NAD+ repletion rescues female fertility during reproductive aging, Cell Rep., 30, 1670, 10.1016/j.celrep.2020.01.058 · DOI
  8. Blengini, 2021, Age-dependent integrity of the meiotic spindle assembly checkpoint in females requires aurora kinase B, Aging Cell, 20, 10.1111/acel.13489 · DOI
  9. Broekmans, 2004, Antral follicle counts are related to age at natural fertility loss and age at menopause, Menopause, 11, 607, 10.1097/01.GME.0000123643.76105.27 · DOI
  10. Burkhardt, 2016, Chromosome cohesion established by Rec8-cohesin in fetal oocytes is maintained without detectable turnover in oocytes arrested for months in mice, Curr. Biol., 26, 678, 10.1016/j.cub.2015.12.073 · DOI
  11. Chatzidaki, 2021, Ovulation suppression protects against chromosomal abnormalities in mouse eggs at advanced maternal age, Curr. Biol., 31, 4038, 10.1016/j.cub.2021.06.076 · DOI
  12. Chen, 2018, Effect of stem cell transplantation of premature ovarian failure in animal models and patients: a meta-analysis and case report, Exp. Ther. Med., 15, 4105
  13. Cheng, 2017, Age-related loss of cohesion: causes and effects, Int. J. Mol. Sci., 18, 1578, 10.3390/ijms18071578 · DOI
  14. Chiang, 2010, Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes, Curr. Biol., 20, 1522, 10.1016/j.cub.2010.06.069 · DOI
  15. Chin, 2014, The metabolite α-ketoglutarate extends lifespan by inhibiting ATP synthase and TOR, Nature, 510, 397, 10.1038/nature13264 · DOI
  16. Christodoulaki, 2021, Prospects of germline nuclear transfer in women with diminished ovarian reserve, Front. Endocrinol., 12, 10.3389/fendo.2021.635370 · DOI
  17. Cioppi, 2021, Genetics of Aazoospermia, Int. J. Mol. Sci., 22, 3264, 10.3390/ijms22063264 · DOI
  18. Colella, 2021, Ovarian aging: role of pituitary-ovarian axis hormones and ncRNAs in regulating ovarian mitochondrial activity, Front. Endocrinol., 12, 10.3389/fendo.2021.791071 · DOI
  19. Crawford, 2015, Age-related infertility, Obstet. Gynecol. Clin. N. Am., 42, 15, 10.1016/j.ogc.2014.09.005 · DOI
  20. Cui, 2016, Protective effect of resveratrol on spermatozoa function in male infertility induced by excess weight and obesity, Mol. Med. Rep., 14, 4659, 10.3892/mmr.2016.5840 · DOI
  21. Darmishonnejad, 2019, Evaluation of sperm telomere length in infertile men with failed/low fertilization after intracytoplasmic sperm injection, Reprod. Biomed. Online, 38, 579, 10.1016/j.rbmo.2018.12.022 · DOI
  22. Day, 2015, Large-scale genomic analyses link reproductive aging to hypothalamic signaling, breast cancer susceptibility and BRCA1-mediated DNA repair, Nat. Genet., 47, 1294, 10.1038/ng.3412 · DOI · Paper page
  23. Dechanet, 2011, Effects of cigarette smoking on reproduction, Hum. Reprod. Update, 17, 76, 10.1093/humupd/dmq033 · DOI
  24. Douhard, 2020, Sons accelerate maternal aging in a wild mammal, Proc. Natl. Acad. Sci. U. S. A., 117, 4850, 10.1073/pnas.1914654117 · DOI
  25. Duncan, 2012, Chromosome cohesion decreases in human eggs with advanced maternal age, Aging Cell, 11, 1121, 10.1111/j.1474-9726.2012.00866.x · DOI
  26. Ergenoglu, 2015, Effects of resveratrol on ovarian morphology, plasma anti-mullerian hormone, IGF-1 levels, and oxidative stress parameters in a rat model of polycystic ovary syndrome, Reprod. Sci., 22, 942, 10.1177/1933719115570900 · DOI
  27. Faid, 2015, Resveratrol alleviates diabetes-induced testicular dysfunction by inhibiting oxidative stress and c-Jun N-terminal kinase signaling in rats, Toxicol. Appl. Pharmacol., 289, 482, 10.1016/j.taap.2015.10.012 · DOI
  28. Fitzgerald, 1998, Aging and reproductive potential in women, Yale J. Biol. Med., 71, 367
  29. Fricke, 2019, Male reproductive ageing: a tale of the whole ejaculate, Reproduction, 158, R219, 10.1530/REP-18-0579 · DOI
  30. Ghosh, 2010, Telomere length is associated with types of chromosome 21 nondisjunction: a new insight into the maternal age effect on Down syndrome birth, Hum. Genet., 127, 403, 10.1007/s00439-009-0785-8 · DOI
  31. Ghosh, 2009, Etiology of down syndrome: evidence for consistent association among altered meiotic recombination, nondisjunction, and maternal age across populations, Am. J. Med. Genet., 149A, 1415, 10.1002/ajmg.a.32932 · DOI
  32. Gruhn, 2019, Chromosome errors in human eggs shape natural fertility over reproductive life span, Science, 365, 1466, 10.1126/science.aav7321 · DOI
  33. Hu, 2020, Melatonin application in assisted reproductive technology: a systematic review and meta-analysis of randomized trials, Front. Endocrinol., 11, 160, 10.3389/fendo.2020.00160 · DOI
  34. Hurt, 2006, Does the number of sons born affect long-term mortality of parents? A cohort study in rural Bangladesh, Proc. Biol. Sci., 273, 149
  35. Hvide, 2021, Parental age and birth defects: a sibling study, Eur. J. Epidemiol., 36, 849, 10.1007/s10654-021-00734-8 · DOI
  36. Itami, 2015, Resveratrol improves the quality of pig oocytes derived from early antral follicles through sirtuin 1 activation, Theriogenology, 83, 1360, 10.1016/j.theriogenology.2015.01.029 · DOI
  37. Jiao, 2018, Molecular genetics of premature ovarian insufficiency, Trends Endocrinol. Metabol., 29, 795, 10.1016/j.tem.2018.07.002 · DOI
  38. Johnson, 1984, Quantification of the human sertoli cell population: its distribution, relation to germ cell numbers, and age-related decline, Biol. Reprod., 31, 785, 10.1095/biolreprod31.4.785 · DOI
  39. Juan, 2005, Trans-resveratrol, a natural antioxidant from grapes, increases sperm output in healthy rats, J. Nutr., 135, 757, 10.1093/jn/135.4.757 · DOI
  40. Keefe, 2005, Telomere length predicts embryo fragmentation after in vitro fertilization in women--toward a telomere theory of reproductive aging in women, Am. J. Obstet. Gynecol., 192, 1256, 10.1016/j.ajog.2005.01.036 · DOI
  41. Kordowitzki, 2020, The effect of rapamycin on bovine oocyte maturation success and metaphase telomere length maintenance, Aging (Albany NY), 12, 7576, 10.18632/aging.103126 · DOI
  42. Labarta, 2019, Mitochondria as a tool for oocyte rejuvenation, Fertil. Steril., 111, 219, 10.1016/j.fertnstert.2018.10.036 · DOI
  43. Leisegang, 2017, Redox regulation of fertility in aging male and the role of antioxidants: a savior or stressor, Curr. Pharmaceut. Des., 23, 4438, 10.2174/1381612822666161019150241 · DOI
  44. Liu, 2012, Delay in oocyte aging in mice by the antioxidant N-acetyl-L-cysteine (NAC), Hum. Reprod., 27, 1411, 10.1093/humrep/des019 · DOI
  45. Liu, 2002, Requirement of functional telomeres for metaphase chromosome alignments and integrity of meiotic spindles, EMBO Rep., 3, 230, 10.1093/embo-reports/kvf055 · DOI
  46. Liu, 2004, Irregular telomeres impair meiotic synapsis and recombination in mice, Proc. Natl. Acad. Sci. U. S. A., 101, 6496, 10.1073/pnas.0400755101 · DOI
  47. Liu, 2013, Resveratrol protects against age-associated infertility in mice, Hum. Reprod., 28, 707, 10.1093/humrep/des437 · DOI
  48. Liu, 2018, Resveratrol improves in vitro maturation of oocytes in aged mice and humans, Fertil. Steril., 109, 900, 10.1016/j.fertnstert.2018.01.020 · DOI
  49. Liu, 2022, The effects of human umbilical cord mesenchymal stem cell transplantation on female fertility restoration in mice, Curr. Gene Ther., 22, 319, 10.2174/1566523221666211014165341 · DOI
  50. Liu, 2013, Resveratrol protects mouse oocytes from methylglyoxal-induced oxidative damage, PLoS ONE, 8
  51. Ma, 2015, Sirt1 protects pig oocyte against in vitro aging, Anim. Sci. J., 86, 826, 10.1111/asj.12360 · DOI
  52. Mahmoud, 2003, Testicular volume in relation to hormonal indices of gonadal function in community-dwelling elderly men, J. Clin. Endocrinol. Metab., 88, 179, 10.1210/jc.2002-020408 · DOI
  53. Matzkin, 2021, Hallmarks of testicular aging: the challenge of anti-inflammatory and antioxidant therapies using natural and/or pharmacological compounds to improve the physiopathological status of the aged male gonad, Cells, 10, 3114, 10.3390/cells10113114 · DOI
  54. McIntosh, 1995, Paternal age and the risk of birth defects in offspring, Epidemiology, 6, 282, 10.1097/00001648-199505000-00016 · DOI
  55. Merriman, 2012, Effect of aging on superovulation efficiency, aneuploidy rates, and sister chromatid cohesion in mice aged up to 15 months, Biol. Reprod., 86, 49, 10.1095/biolreprod.111.095711 · DOI
  56. Miller, 2011, Meta-analysis of paternal age and schizophrenia risk in male versus female offspring, Schizophr. Bull., 37, 1039, 10.1093/schbul/sbq011 · DOI
  57. Miller, 2022, Pregnancy, preeclampsia and maternal aging: from epidemiology to functional genomics, Ageing Res. Rev., 73, 10.1016/j.arr.2021.101535 · DOI
  58. Minamoto, 2020, Pregnancy by assisted reproductive technology is associated with shorter telomere length in neonates, Int. J. Mol. Sci., 21, 9688, 10.3390/ijms21249688 · DOI
  59. Næss, 2017, Offspring sex and parental health and mortality, Sci. Rep., 7, 5285, 10.1038/s41598-017-05161-y · DOI
  60. Nagaoka, 2011, Oocyte-specific differences in cell-cycle control create an innate susceptibility to meiotic errors, Curr. Biol., 21, 651, 10.1016/j.cub.2011.03.003 · DOI
  61. Niu, 2020, Melatonin enhances mitochondrial biogenesis and protects against rotenone-induced mitochondrial deficiency in early porcine embryos, J. Pineal Res., 68, 10.1111/jpi.12627 · DOI
  62. Orrenius, 2007, Mitochondrial oxidative stress: implications for cell death, Annu. Rev. Pharmacol. Toxicol., 47, 143, 10.1146/annurev.pharmtox.47.120505.105122 · DOI
  63. Pan, 2021, Effects and mechanisms of mUCMSCs on ovarian structure and function in naturally ageing C57 mice, J. Ovarian Res., 14, 133, 10.1186/s13048-021-00854-5 · DOI
  64. Perkins, 2016, Oxidative stress in oocytes during midprophase induces premature loss of cohesion and chromosome segregation errors, Proc. Natl. Acad. Sci. U. S. A., 113, E6823, 10.1073/pnas.1612047113 · DOI
  65. Pines, 2011, Male menopause: is it a real clinical syndrome?, Climacteric, 14, 15, 10.3109/13697137.2010.507442 · DOI
  66. Pittenger, 2019, Mesenchymal stem cell perspective: cell biology to clinical progress, NPJ. Regen. Med., 4, 22, 10.1038/s41536-019-0083-6 · DOI · Paper page
  67. Riris, 2014, Digital multiplexed mRNA analysis of functionally important genes in single human oocytes and correlation of changes in transcript levels with oocyte protein expression, Fertil. Steril., 101, 857, 10.1016/j.fertnstert.2013.11.125 · DOI
  68. Ruth, 2021, Genetic insights into biological mechanisms governing human ovarian ageing, Nature, 596, 393, 10.1038/s41586-021-03779-7 · DOI
  69. Salvatore, 2021, Human adipose-derived stromal cells transplantation prolongs reproductive lifespan on mouse models of mild and severe premature ovarian insufficiency, Stem Cell Res. Ther., 12, 537, 10.1186/s13287-021-02590-5 · DOI
  70. Sasaki, 2019, Impact of oxidative stress on age-associated decline in oocyte developmental competence, Front. Endocrinol., 10, 811, 10.3389/fendo.2019.00811 · DOI
  71. Schmidt, 2009, Female mice delay reproductive aging in males, Biol. Reprod., 80, 1009, 10.1095/biolreprod.108.073619 · DOI
  72. Selesniemi, 2008, Moderate caloric restriction initiated in rodents during adulthood sustains function of the female reproductive axis into advanced chronological age, Aging Cell, 7, 622, 10.1111/j.1474-9726.2008.00409.x · DOI
  73. Sherman, 1994, Non-disjunction of chromosome 21 in maternal meiosis I: evidence for a maternal age-dependent mechanism involving reduced recombination, Hum. Mol. Genet., 3, 1529, 10.1093/hmg/3.9.1529 · DOI
  74. Stone, 2013, Age thresholds for changes in semen parameters in men, Fertil. Steril., 100, 952, 10.1016/j.fertnstert.2013.05.046 · DOI
  75. Tamura, 2008, Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate, J. Pineal Res., 44, 280, 10.1111/j.1600-079X.2007.00524.x · DOI
  76. Trifunovic, 2004, Premature ageing in mice expressing defective mitochondrial DNA polymerase, Nature, 429, 417, 10.1038/nature02517 · DOI · Paper page
  77. Wang, 2021, NAMPT reduction-induced NAD+ insufficiency contributes to the compromised oocyte quality from obese mice, Aging Cell, 20, 10.1111/acel.13496 · DOI
  78. Wang, 2021, The effect of oxidative stress on the chicken ovary: involvement of microbiota and melatonin interventions, Antioxidants, 10, 1422, 10.3390/antiox10091422 · DOI
  79. Wang, 2006, The mTOR pathway in the control of protein synthesis, Physiology, 21, 362, 10.1152/physiol.00024.2006 · DOI · Paper page
  80. Webster, 2017, Mechanisms of aneuploidy in human eggs, Trends Cell Biol., 27, 55, 10.1016/j.tcb.2016.09.002 · DOI
  81. Weichhart, 2018, mTOR as regulator of lifespan, aging, and cellular senescence: a mini-review, Gerontology, 64, 127, 10.1159/000484629 · DOI · Paper page
  82. Weiss, 2009, Inflammation in reproductive disorders, Reprod. Sci., 16, 216, 10.1177/1933719108330087 · DOI
  83. Winship, 2018, The importance of DNA repair for maintaining oocyte quality in response to anti-cancer treatments, environmental toxins and maternal ageing, Hum. Reprod. Update, 24, 119, 10.1093/humupd/dmy002 · DOI
  84. Xie, 2021, Melatonin ameliorates ovarian dysfunction by regulating autophagy in PCOS via the PI3K-Akt pathway, Reproduction, 162, 73
  85. Yamada-Fukunaga, 2013, Age-associated telomere shortening in mouse oocytes, Reprod. Biol. Endocrinol., 11, 108, 10.1186/1477-7827-11-108 · DOI
  86. Yang, 2020, Mitochondrial DNA mutation exacerbates female reproductive aging via impairment of the NADH/NAD+ redox, Aging Cell, 19, 10.1111/acel.13206 · DOI
  87. Yang, 2020, Increasing ovarian NAD+ levels improve mitochondrial functions and reverse ovarian aging, Free Radic. Biol. Med., 156, 1, 10.1016/j.freeradbiomed.2020.05.003 · DOI
  88. Yi, 2020, Melatonin ameliorates excessive PINK1/Parkin-mediated mitophagy by enhancing SIRT1 expression in granulosa cells of PCOS, Am. J. Physiol. Endocrinol. Metab., 319, E91, 10.1152/ajpendo.00006.2020 · DOI
  89. Yorino, 2020, Rapamycin treatment maintains developmental potential of oocytes in mice and follicle reserve in human cortical fragments grafted into immune-deficient mice, Mol. Cell. Endocrinol., 504
  90. Zhang, 2021, Mitochondrial transfer from induced pluripotent stem cells rescues developmental potential of in vitro fertilized embryos from aging females, Biol. Reprod., 104, 1114, 10.1093/biolre/ioab009 · DOI
  91. Zhang, 2022, Alterations in synaptonemal complex coding genes and human infertility, Int. J. Biol. Sci., 18, 1933, 10.7150/ijbs.67843 · DOI
  92. Zhang, 2019, Melatonin regulates the activities of ovary and delays the fertility decline in female animals via MT1/AMPK pathway, J. Pineal Res., 66, 10.1111/jpi.12550 · DOI
  93. Zhang, 2013, Rapamycin preserves the follicle pool reserve and prolongs the ovarian lifespan of female rats via modulating mTOR activation and sirtuin expression, Gene, 523, 82, 10.1016/j.gene.2013.03.039 · DOI
  94. Zhang, 2021, α-ketoglutarate delays age-related fertility decline in mammals, Aging Cell, 20, 10.1111/acel.13291 · DOI
  95. Zhu, 2005, Paternal age and preterm birth, Epidemiology, 16, 259, 10.1097/01.ede.0000152526.63279.da · DOI

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Metadata

Authors
Liu, Y., & Gao, J.
Affiliations
Shandong Normal University (CN)
Corresponding author
Gao, Jinmin
ORCID
Venue
Journal of Genetics and Genomics
Publisher
Elsevier BV
Published
2023-03
Volume
50
Issue
3
Pages
141-150
ISSN
  • 1873-5533 (ISSN-L)
  • 1673-8527
DOI
10.1016/j.jgg.2022.07.002
OpenAlex
W4285405294
Cited by
38
References
4
Citations by year
2026: 14 · 2025: 12 · 2024: 7 · 2023: 4
FWCI
1.15
Type
journal article
Language
en
Open access
closed
Licence
Locations
  • Journal of genetics and genomics/Journal of Genetics and Genomics (publishedVersion)
  • PubMed (publishedVersion)
Funders
National Natural Science Foundation of China (31871360, 32022018)
Topics
  • Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
  • Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Keywords
reproductive aging, male reproductive aging, follicle depletion, oocyte quality, menopause, male infertility, oxidative stress, mitochondrial dysfunction, telomere shortening, advanced maternal age, fertility preservation
MeSH terms
Aging, Female, Humans, Infertility, Male, Maternal Age, Oocytes, Pregnancy, Reproduction

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