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Reproductive Ageing

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Ageing: Lessons from C. elegans

Part of the book series: Healthy Ageing and Longevity ((HAL))

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Abstract

Reproductive senescence is common in many species across great evolutionary distances. Reproductive ageing occurs in mid-adulthood, earlier than most age-related somatic declines manifest. In this chapter, we review the most recent progress in the field of C. elegans reproductive ageing. We first introduce and compare the available methods of measuring reproductive ageing in C. elegans, then summarize the current knowledge of C. elegans reproductive ageing regulation. We also compare and contrast C. elegans and human/mammalian reproductive decline, and illustrate why C. elegans is a good model to study reproductive ageing. Finally, we discuss how the knowledge gained from worm studies may contribute to the understanding of the relationship between reproductive ageing and somatic longevity. With the proper choice of measurements, screen design, and the development of automatic high throughput assays, more exciting discoveries will be made in the C. elegans reproductive ageing field, which will greatly contribute to our understanding of not only how the reproductive system ages, but also how it is coordinated with the ageing of somatic tissues.

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References

  1. Schedl T, Kimble J (1988) fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in C. elegans. Genetics 119(1):43–61

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Hughes SE, Evason K, Xiong C, Kornfeld K (2007) Genetic and pharmacological factors that influence reproductive aging in nematodes. PLoS Genet 3(2):e25. doi:10.1371/journal.pgen.0030025

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Pickett CL, Dietrich N, Chen J, Xiong C, Kornfeld K (2013) Mated progeny production is a biomarker of aging in C. elegans. G3 3(12):2219–2232. doi:10.1534/g3.113.008664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Luo S, Kleemann GA, Ashraf JM, Shaw WM, Murphy CT (2010) TGF-beta and insulin signaling regulate reproductive aging via oocyte and germline quality maintenance. Cell 143(2):299–312. doi:10.1016/j.cell.2010.09.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Hubbard EJ, Greenstein D (2005) Introduction to the germ line. WormBook:1–4. doi:10.1895/wormbook.1.18.1

  6. Ward S, Carrel JS (1979) Fertilization and sperm competition in the nematode C. elegans. Dev Biol 73(2):304–321

    Article  CAS  PubMed  Google Scholar 

  7. Luo S, Shaw WM, Ashraf J, Murphy CT (2009) TGF-beta Sma/Mab signaling mutations uncouple reproductive aging from somatic aging. PLoS Genet 5(12):e1000789. doi:10.1371/journal.pgen.1000789

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Huang C, Xiong C, Kornfeld K (2004) Measurements of age-related changes of physiological processes that predict lifespan of C. elegans. Proc Natl Acad Sci U S A 101(21):8084–8089. doi:10.1073/pnas.0400848101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Mendenhall AR, Wu D, Park SK, Cypser JR, Tedesco PM, Link CD, Phillips PC, Johnson TE (2011) Genetic dissection of late-life fertility in C. elegans. J Gerontol 66(8):842–854. doi:10.1093/gerona/glr089

    Article  Google Scholar 

  10. Sowa JN, Mutlu AS, Xia F, Wang MC (2015) Olfaction modulates reproductive plasticity through neuroendocrine signaling in C. elegans. Curr Biol 25(17):2284–2289. doi:10.1016/j.cub.2015.07.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Wang MC, Oakley HD, Carr CE, Sowa JN, Ruvkun G (2014) Gene pathways that delay C. elegans reproductive senescence. PLoS Genet 10(12):e1004752. doi:10.1371/journal.pgen.1004752

    Article  PubMed  PubMed Central  Google Scholar 

  12. Garigan D, Hsu AL, Fraser AG, Kamath RS, Ahringer J, Kenyon C (2002) Genetic analysis of tissue aging in C. elegans: a role for heat-shock factor and bacterial proliferation. Genetics 161(3):1101–1112

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Andux S, Ellis RE (2008) Apoptosis maintains oocyte quality in aging C. elegans females. PLoS Genet 4(12):e1000295. doi:10.1371/journal.pgen.1000295

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Goudeau J, Aguilaniu H (2010) Carbonylated proteins are eliminated during reproduction in C. elegans. Aging Cell 9(6):991–1003. doi:10.1111/j.1474-9726.2010.00625.x

    Article  CAS  PubMed  Google Scholar 

  15. Hodgkin J, Horvitz HR, Brenner S (1979) Nondisjunction mutants of the nematode C. elegans. Genetics 91(1):67–94

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Gumienny TL, Lambie E, Hartwieg E, Horvitz HR, Hengartner MO (1999) Genetic control of programmed cell death in the C. elegans hermaphrodite germline. Development 126(5):1011–1022

    CAS  PubMed  Google Scholar 

  17. Gartner A, Milstein S, Ahmed S, Hodgkin J, Hengartner MO (2000) A conserved checkpoint pathway mediates DNA damage – induced apoptosis and cell cycle arrest in C. elegans. Mol Cell 5(3):435–443

    Article  CAS  PubMed  Google Scholar 

  18. Kenyon CJ (2010) The genetics of ageing. Nature 464(7288):504–512. doi:10.1038/nature08980

    Article  CAS  PubMed  Google Scholar 

  19. Hodgkin J, Barnes TM (1991) More is not better: brood size and population growth in a self-fertilizing nematode. Proc Biol Sci/Royal Soc 246(1315):19–24. doi:10.1098/rspb.1991.0119

    Article  CAS  Google Scholar 

  20. Lee SJ, Kenyon C (2009) Regulation of the longevity response to temperature by thermosensory neurons in C. elegans. Curr Biol 19(9):715–722. doi:10.1016/j.cub.2009.03.041, S0960-9822(09)00894-X [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Xiao R, Zhang B, Dong Y, Gong J, Xu T, Liu J, Xu XZ (2013) A genetic program promotes C. elegans longevity at cold temperatures via a thermosensitive TRP channel. Cell 152(4):806–817. doi:10.1016/j.cell.2013.01.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Holehan AM, Merry BJ (1985) The control of puberty in the dietary restricted female rat. Mech Ageing Dev 32(2–3):179–191

    Article  CAS  PubMed  Google Scholar 

  23. McShane TM, Wise PM (1996) Life-long moderate caloric restriction prolongs reproductive life span in rats without interrupting estrous cyclicity: effects on the gonadotropin-releasing hormone/luteinizing hormone axis. Biol Reprod 54(1):70–75

    Article  CAS  PubMed  Google Scholar 

  24. Selesniemi K, Lee HJ, Tilly JL (2008) Moderate caloric restriction initiated in rodents during adulthood sustains function of the female reproductive axis into advanced chronological age. Aging Cell 7(5):622–629. doi:10.1111/j.1474-9726.2008.00409.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Chapman T, Partridge L (1996) Female fitness in Drosophila melanogaster: an interaction between the effect of nutrition and of encounter rate with males. Proc Biol Sci/Royal Soc 263(1371):755–759. doi:10.1098/rspb.1996.0113

    Article  CAS  Google Scholar 

  26. Kaeberlein TL, Smith ED, Tsuchiya M, Welton KL, Thomas JH, Fields S, Kennedy BK, Kaeberlein M (2006) Lifespan extension in C. elegans by complete removal of food. Aging Cell 5(6):487–494

    Article  CAS  PubMed  Google Scholar 

  27. Lee GD, Wilson MA, Zhu M, Wolkow CA, de Cabo R, Ingram DK, Zou S (2006) Dietary deprivation extends lifespan in C. elegans. Aging Cell 5(6):515–524. doi:10.1111/j.1474-9726.2006.00241.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Klass MR (1977) Aging in the nematode C. elegans: major biological and environmental factors influencing life span. Mech Ageing Dev 6(6):413–429

    Article  CAS  PubMed  Google Scholar 

  29. Houthoofd K, Braeckman BP, Johnson TE, Vanfleteren JR (2003) Life extension via dietary restriction is independent of the Ins/IGF-1 signalling pathway in C. elegans. Exp Gerontol 38(9):947–954

    Article  CAS  PubMed  Google Scholar 

  30. Bishop NA, Guarente L (2007) Two neurons mediate diet-restriction-induced longevity in C. elegans. Nature 447(7144):545–549

    Article  CAS  PubMed  Google Scholar 

  31. Hosono R, Nishimoto S, Kuno S (1989) Alterations of life span in the nematode C. elegans under monoxenic culture conditions. Exp Gerontol 24(3):251–264

    Article  CAS  PubMed  Google Scholar 

  32. Greer EL, Dowlatshahi D, Banko MR, Villen J, Hoang K, Blanchard D, Gygi SP, Brunet A (2007) An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol 17(19):1646–1656. doi:10.1016/j.cub.2007.08.047, S0960-9822(07)01864-7 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Houthoofd K, Braeckman BP, Lenaerts I, Brys K, De Vreese A, Van Eygen S, Vanfleteren JR (2002) Axenic growth up-regulates mass-specific metabolic rate, stress resistance, and extends life span in C. elegans. Exp Gerontol 37(12):1371–1378

    Article  PubMed  Google Scholar 

  34. Szewczyk NJ, Udranszky IA, Kozak E, Sunga J, Kim SK, Jacobson LA, Conley CA (2006) Delayed development and lifespan extension as features of metabolic lifestyle alteration in C. elegans under dietary restriction. J Exp Biol 209(Pt 20):4129–4139

    Article  CAS  PubMed  Google Scholar 

  35. Honjoh S, Yamamoto T, Uno M, Nishida E (2009) Signalling through RHEB-1 mediates intermittent fasting-induced longevity in C. elegans. Nature 457(7230):726–730

    Article  CAS  PubMed  Google Scholar 

  36. Lakowski B, Hekimi S (1998) The genetics of caloric restriction in C. elegans. Proc Natl Acad Sci U S A 95(22):13091–13096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Avery L (1993) The genetics of feeding in C. elegans. Genetics 133(4):897–917

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Panowski SH, Wolff S, Aguilaniu H, Durieux J, Dillin A (2007) PHA-4/Foxa mediates diet-restriction-induced longevity of C. elegans. Nature 447(7144):550–555

    Article  CAS  PubMed  Google Scholar 

  39. Brenner S (1974) The genetics of C. elegans. Genetics 77(1):71–94

    CAS  PubMed  PubMed Central  Google Scholar 

  40. MacNeil LT, Watson E, Arda HE, Zhu LJ, Walhout AJ (2013) Diet-induced developmental acceleration independent of TOR and insulin in C. elegans. Cell 153(1):240–252. doi:10.1016/j.cell.2013.02.049

    Article  CAS  PubMed  Google Scholar 

  41. Watson E, Macneil LT, Arda HE, Zhu LJ, Walhout AJ (2013) Integration of metabolic and gene regulatory networks modulates the C. elegans dietary response. Cell 153(1):253–266. doi:10.1016/j.cell.2013.02.050

    Article  CAS  PubMed  Google Scholar 

  42. Gracida X, Eckmann CR (2013) Fertility and germline stem cell maintenance under different diets requires nhr-114/HNF4 in C. elegans. Curr Biol 23(7):607–613. doi:10.1016/j.cub.2013.02.034

    Article  CAS  PubMed  Google Scholar 

  43. Chi C, Ronai D, Than MT, Walker CJ, Sewell AK, Han M (2016) Nucleotide levels regulate germline proliferation through modulating GLP-1/Notch signaling in C. elegans. Genes Dev 30(3):307–320. doi:10.1101/gad.275107.115

  44. Luo S, Murphy CT (2011) C. elegans reproductive aging: regulation and underlying mechanisms. Genesis 49(2):53–65. doi:10.1002/dvg.20694

    Article  CAS  PubMed  Google Scholar 

  45. Cassada RC, Russell RL (1975) The dauerlarva, a post-embryonic developmental variant of the nematode C. elegans. Dev Biol 46(2):326–342

    Article  CAS  PubMed  Google Scholar 

  46. Reinke V, Smith HE, Nance J, Wang J, Van Doren C, Begley R, Jones SJ, Davis EB, Scherer S, Ward S, Kim SK (2000) A global profile of germline gene expression in C. elegans. Mol Cell 6(3):605–616

    Google Scholar 

  47. Hall SE, Beverly M, Russ C, Nusbaum C, Sengupta P (2010) A cellular memory of developmental history generates phenotypic diversity in C. elegans. Curr Biol 20(2):149–155. doi:10.1016/j.cub.2009.11.035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Angelo G, Van Gilst MR (2009) Starvation protects germline stem cells and extends reproductive longevity in C. elegans. Science 326(5955):954–958. doi:10.1126/science.1178343, 1178343 [pii]

    Article  CAS  PubMed  Google Scholar 

  49. Fontana L, Partridge L (2015) Promoting health and longevity through diet: from model organisms to humans. Cell 161(1):106–118. doi:10.1016/j.cell.2015.02.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R (1993) A C. elegans mutant that lives twice as long as wild type. Nature 366(6454):461–464

    Google Scholar 

  51. Kimura KD, Tissenbaum HA, Liu Y, Ruvkun G (1997) daf-2, an insulin receptor-like gene that regulates longevity and diapause in C. elegans. Science 277(5328):942–946

    Article  CAS  PubMed  Google Scholar 

  52. Duret L, Guex N, Peitsch MC, Bairoch A (1998) New insulin-like proteins with atypical disulfide bond pattern characterized in C. elegans by comparative sequence analysis and homology modeling. Genome Res 8(4):348–353

    CAS  PubMed  Google Scholar 

  53. Pierce SB, Costa M, Wisotzkey R, Devadhar S, Homburger SA, Buchman AR, Ferguson KC, Heller J, Platt DM, Pasquinelli AA, Liu LX, Doberstein SK, Ruvkun G (2001) Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes Dev 15(6):672–686. doi:10.1101/gad.867301

  54. Li W, Kennedy SG, Ruvkun G (2003) daf-28 encodes a C. elegans insulin superfamily member that is regulated by environmental cues and acts in the DAF-2 signaling pathway. Genes Dev 17(7):844–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Lin K, Dorman JB, Rodan A, Kenyon C (1997) daf-16: an HNF-3/forkhead family member that can function to double the life-span of C. elegans. Science 278(5341):1319–1322

    Article  CAS  PubMed  Google Scholar 

  56. Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, Tissenbaum HA, Ruvkun G (1997) The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389(6654):994–999

    Article  CAS  PubMed  Google Scholar 

  57. Lin K, Hsin H, Libina N, Kenyon C (2001) Regulation of the C. elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nat Genet 28(2):139–145. doi:10.1038/88850

    Article  CAS  PubMed  Google Scholar 

  58. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, Li H, Kenyon C (2003) Genes that act downstream of DAF-16 to influence the lifespan of C. elegans. Nature 424(6946):277–283. doi:10.1038/nature01789

    Article  CAS  PubMed  Google Scholar 

  59. Friedman DB, Johnson TE (1988) A mutation in the age-1 gene in C. elegans lengthens life and reduces hermaphrodite fertility. Genetics 118(1):75–86

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Gems D, Sutton AJ, Sundermeyer ML, Albert PS, King KV, Edgley ML, Larsen PL, Riddle DL (1998) Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in C. elegans. Genetics 150(1):129–155

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Libina N, Berman JR, Kenyon C (2003) Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115(4):489–502

    Article  CAS  PubMed  Google Scholar 

  62. Wolkow CA, Kimura KD, Lee MS, Ruvkun G (2000) Regulation of C. elegans life-span by insulin-like signaling in the nervous system. Science 290(5489):147–150

    Article  CAS  PubMed  Google Scholar 

  63. Dillin A, Crawford DK, Kenyon C (2002) Timing requirements for insulin/IGF-1 signaling in C. elegans. Science 298(5594):830–834

    Google Scholar 

  64. Hsin H, Kenyon C (1999) Signals from the reproductive system regulate the lifespan of C. elegans. Nature 399(6734):362–366

    Google Scholar 

  65. Savage-Dunn C (2005) TGF-beta signaling. WormBook:1–12. doi:10.1895/wormbook.1.22.1

  66. ten Dijke P, Hill CS (2004) New insights into TGF-beta-Smad signalling. Trends Biochem Sci 29(5):265–273. doi:10.1016/j.tibs.2004.03.008

    Article  PubMed  CAS  Google Scholar 

  67. Shaw WM, Luo S, Landis J, Ashraf J, Murphy CT (2007) The C. elegans TGF-beta Dauer pathway regulates longevity via insulin signaling. Curr Biol 17(19):1635–1645. doi:10.1016/j.cub.2007.08.058

  68. Sze JY, Victor M, Loer C, Shi Y, Ruvkun G (2000) Food and metabolic signalling defects in a C. elegans serotonin-synthesis mutant. Nature 403(6769):560–564

    Article  CAS  PubMed  Google Scholar 

  69. Trent C, Tsuing N, Horvitz HR (1983) Egg-laying defective mutants of the nematode C. elegans. Genetics 104(4):619–647

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Schafer WR, Sanchez BM, Kenyon CJ (1996) Genes affecting sensitivity to serotonin in C. elegans. Genetics 143(3):1219–1230

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Lakowski B, Hekimi S (1996) Determination of life-span in C. elegans by four clock genes. Science 272(5264):1010–1013

    Article  CAS  PubMed  Google Scholar 

  72. Feng J, Bussiere F, Hekimi S (2001) Mitochondrial electron transport is a key determinant of life span in C. elegans. Dev Cell 1(5):633–644

    Article  CAS  PubMed  Google Scholar 

  73. Hughes SE, Huang C, Kornfeld K (2011) Identification of mutations that delay somatic or reproductive aging of C. elegans. Genetics 189(1):341–356. doi:10.1534/genetics.111.130450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Evason K, Huang C, Yamben I, Covey DF, Kornfeld K (2005) Anticonvulsant medications extend worm life-span. Science 307(5707):258–262

    Article  CAS  PubMed  Google Scholar 

  75. Collins JJ, Evason K, Pickett CL, Schneider DL, Kornfeld K (2008) The anticonvulsant ethosuximide disrupts sensory function to extend C. elegans lifespan. PLoS Genet 4(10):e1000230. doi:10.1371/journal.pgen.1000230

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Onken B, Driscoll M (2010) Metformin induces a dietary restriction-like state and the oxidative stress response to extend C. elegans Healthspan via AMPK, LKB1, and SKN-1. PLoS One 5(1):e8758. doi:10.1371/journal.pone.0008758

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Li S, Stone HA, Murphy CT (2015) A microfluidic device and automatic counting system for the study of C. elegans reproductive aging. Lab Chip 15(2):524–531. doi:10.1039/c4lc01028k

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. White YA, Woods DC, Takai Y, Ishihara O, Seki H, Tilly JL (2012) Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat Med 18(3):413–421. doi:10.1038/nm.2669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. te Velde ER, Pearson PL (2002) The variability of female reproductive ageing. Hum Reprod Update 8(2):141–154

    Article  Google Scholar 

  80. Blondin P, Coenen K, Sirard MA (1997) The impact of reactive oxygen species on bovine sperm fertilizing ability and oocyte maturation. J Androl 18(4):454–460

    CAS  PubMed  Google Scholar 

  81. Goud P, Goud A, Van Oostveldt P, Van der Elst J, Dhont M (1999) Fertilization abnormalities and pronucleus size asynchrony after intracytoplasmic sperm injection are related to oocyte postmaturity. Fertil Steril 72(2):245–252

    Article  CAS  PubMed  Google Scholar 

  82. Rose AM, Baillie DL (1979) The effect of temperature and parental age on recombination and nondisjunction in C. elegans. Genetics 92(2):409–418

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Tang L, Machacek T, Mamnun YM, Penkner A, Gloggnitzer J, Wegrostek C, Konrat R, Jantsch MF, Loidl J, Jantsch V (2010) Mutations in C. elegans him-19 show meiotic defects that worsen with age. Mol Biol Cell 21(6):885–896. doi:10.1091/mbc.E09-09-0811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Greenstein D (2005) Control of oocyte meiotic maturation and fertilization. WormBook:1–12. doi:10.1895/wormbook.1.53.1

  85. Mehlmann LM (2005) Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130(6):791–799. doi:10.1530/rep.1.00793

    Article  CAS  PubMed  Google Scholar 

  86. Tilly JL, Sinclair DA (2013) Germline energetics, aging, and female infertility. Cell Metab 17(6):838–850. doi:10.1016/j.cmet.2013.05.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Hamatani T, Falco G, Carter MG, Akutsu H, Stagg CA, Sharov AA, Dudekula DB, VanBuren V, Ko MS (2004) Age-associated alteration of gene expression patterns in mouse oocytes. Hum Mol Genet 13(19):2263–2278. doi:10.1093/hmg/ddh241

    Article  CAS  PubMed  Google Scholar 

  88. Steuerwald NM, Bermudez MG, Wells D, Munne S, Cohen J (2007) Maternal age-related differential global expression profiles observed in human oocytes. Reprod Biomed Online 14(6):700–708

    Article  CAS  PubMed  Google Scholar 

  89. Wainer-Katsir K, Zou JY, Linial M (2015) Extended fertility and longevity: the genetic and epigenetic link. Fertil Steril 103(5):1117–1124. doi:10.1016/j.fertnstert.2015.02.008

    Article  PubMed  Google Scholar 

  90. Hosaka T, Biggs WH 3rd, Tieu D, Boyer AD, Varki NM, Cavenee WK, Arden KC (2004) Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc Natl Acad Sci U S A 101(9):2975–2980. doi:10.1073/pnas.0400093101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Pelosi E, Omari S, Michel M, Ding J, Amano T, Forabosco A, Schlessinger D, Ottolenghi C (2013) Constitutively active Foxo3 in oocytes preserves ovarian reserve in mice. Nat Commun 4:1843. doi:10.1038/ncomms2861

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Ong KK, Elks CE, Li S, Zhao JH, Luan J, Andersen LB, Bingham SA, Brage S, Smith GD, Ekelund U, Gillson CJ, Glaser B, Golding J, Hardy R, Khaw KT, Kuh D, Luben R, Marcus M, McGeehin MA, Ness AR, Northstone K, Ring SM, Rubin C, Sims MA, Song K, Strachan DP, Vollenweider P, Waeber G, Waterworth DM, Wong A, Deloukas P, Barroso I, Mooser V, Loos RJ, Wareham NJ (2009) Genetic variation in LIN28B is associated with the timing of puberty. Nat Genet 41(6):729–733. doi:10.1038/ng.382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Broekmans FJ, Knauff EA, te Velde ER, Macklon NS, Fauser BC (2007) Female reproductive ageing: current knowledge and future trends. Trends Endocrinol Metab 18(2):58–65. doi:10.1016/j.tem.2007.01.004

    Article  CAS  PubMed  Google Scholar 

  94. Voorhuis M, Broekmans FJ, Fauser BC, Onland-Moret NC, van der Schouw YT (2011) Genes involved in initial follicle recruitment may be associated with age at menopause. J Clin Endocrinol Metab 96(3):E473–479. doi:10.1210/jc.2010-1799

    Article  CAS  PubMed  Google Scholar 

  95. Al-Edani T, Assou S, Ferrieres A, Bringer Deutsch S, Gala A, Lecellier CH, Ait-Ahmed O, Hamamah S (2014) Female aging alters expression of human cumulus cells genes that are essential for oocyte quality. BioMed Res Int 2014:964614. doi:10.1155/2014/964614

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Shaye DD, Greenwald I (2011) OrthoList: a compendium of C. elegans genes with human orthologs. PLoS One 6(5):e20085. doi:10.1371/journal.pone.0020085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Arantes-Oliveira N, Apfeld J, Dillin A, Kenyon C (2002) Regulation of life-span by germ-line stem cells in C. elegans. Science 295(5554):502–505

    Article  CAS  PubMed  Google Scholar 

  98. Berman JR, Kenyon C (2006) Germ-cell loss extends C. elegans life span through regulation of DAF-16 by kri-1 and lipophilic-hormone signaling. Cell 124(5):1055–1068

    Google Scholar 

  99. Lapierre LR, Gelino S, Melendez A, Hansen M (2011) Autophagy and lipid metabolism coordinately modulate life span in germline-less C. elegans. Curr Biol 21(18):1507–1514. doi:10.1016/j.cub.2011.07.042

  100. Antebi A (2013) Regulation of longevity by the reproductive system. Exp Gerontol 48(7):596–602. doi:10.1016/j.exger.2012.09.009

    Article  CAS  PubMed  Google Scholar 

  101. Kirkwood TB (1977) Evolution of ageing. Nature 270(5635):301–304

    Article  CAS  PubMed  Google Scholar 

  102. Wu D, Tedesco PM, Phillips PC, Johnson TE (2012) Fertility/longevity trade-offs under limiting-male conditions in mating populations of C. elegans. Exp Gerontol 47(10):759–763. doi:10.1016/j.exger.2012.06.010

    Article  PubMed  PubMed Central  Google Scholar 

  103. Gems D, Riddle DL (1996) Longevity in C. elegans reduced by mating but not gamete production. Nature 379(6567):723–725

    Article  CAS  PubMed  Google Scholar 

  104. Shi C, Murphy CT (2014) Mating induces shrinking and death in Caenorhabditis mothers. Science 343(6170):536–540. doi:10.1126/science.1242958

    Article  CAS  PubMed  Google Scholar 

  105. Maures TJ, Booth LN, Benayoun BA, Izrayelit Y, Schroeder FC, Brunet A (2014) Males shorten the life span of C. elegans hermaphrodites via secreted compounds. Science 343(6170):541–544. doi:10.1126/science.1244160

  106. Ghazi A, Henis-Korenblit S, Kenyon C (2009) A transcription elongation factor that links signals from the reproductive system to lifespan extension in C. elegans. PLoS Genet 5(9):e1000639. doi:10.1371/journal.pgen.1000639

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  107. Blagosklonny MV (2006) Aging and immortality: quasi-programmed senescence and its pharmacologic inhibition. Cell Cycle 5(18):2087–2102. doi:10.4161/cc.5.18.3288

    Article  CAS  PubMed  Google Scholar 

  108. DePina AS, Iser WB, Park SS, Maudsley S, Wilson MA, Wolkow CA (2011) Regulation of C. elegans vitellogenesis by DAF-2/IIS through separable transcriptional and posttranscriptional mechanisms. BMC Physiol 11:11. doi:10.1186/1472-6793-11-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Seah NE, de Magalhaes Filho CD, Petrashen AP, Henderson HR, Laguer J, Gonzalez J, Dillin A, Hansen M, Lapierre LR (2016) Autophagy-mediated longevity is modulated by lipoprotein biogenesis. Autophagy 12(2):261–272. doi:10.1080/15548627.2015.1127464

    Article  CAS  PubMed  Google Scholar 

  110. Zimmerman SM, Hinkson IV, Elias JE, Kim SK (2015) Reproductive aging drives protein accumulation in the uterus and limits lifespan in C. elegans. PLoS Genet 11(12):e1005725. doi:10.1371/journal.pgen.1005725

  111. Copes N, Edwards C, Chaput D, Saifee M, Barjuca I, Nelson D, Paraggio A, Saad P, Lipps D, Stevens SM Jr, Bradshaw PC (2015) Metabolome and proteome changes with aging in C. elegans. Exp Gerontol 72:67–84. doi:10.1016/j.exger.2015.09.013

    Article  CAS  PubMed  Google Scholar 

  112. Pickett CL, Kornfeld K (2013) Age-related degeneration of the egg-laying system promotes matricidal hatching in C. elegans. Aging Cell 12(4):544–553. doi:10.1111/acel.12079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Hodgkin J (1983) Male phenotypes and mating efficiency in C. elegans. Genetics 103(1):43–64

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Chasnov JR, Chow KL (2002) Why are there males in the hermaphroditic species C. elegans? Genetics 160(3):983–994

    CAS  PubMed  PubMed Central  Google Scholar 

  115. Kleemann GA, Basolo AL (2007) Facultative decrease in mating resistance in hermaphroditic C. elegans with self-sperm depletion. Anim Behav 74:1339–1347. doi:10.1016/j.anbehav.2007.02.031

    Article  Google Scholar 

  116. Morsci NS, Haas LA, Barr MM (2011) Sperm status regulates sexual attraction in C. elegans. Genetics 189(4):1341–1346. doi:10.1534/genetics.111.133603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Maliha G, Murphy CT (2016) A simple offspring-to-mother size ratio predicts post-reproductive lifespan. bioRxiv. doi: http://dx.doi.org/10.1101/048835

    Google Scholar 

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Authors and Affiliations

  1. LSI Genomics and Department of Molecular Biology, Princeton University, Princeton, NJ, USA

    Cheng Shi & Coleen T. Murphy

  2. Glenn Center for Aging Research, Princeton University, Princeton, NJ, USA

    Coleen T. Murphy

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  1. Cheng Shi
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Correspondence to Coleen T. Murphy .

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  1. Department of Molecular Biology and Genetics, Aarhus University, Aarhus, Denmark

    Anders Olsen

  2. Department of Metabolics & Aging, The Scripps Research Institute - Scripps Florida, Jupiter, Florida, USA

    Matthew S. Gill

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Shi, C., Murphy, C.T. (2017). Reproductive Ageing. In: Olsen, A., Gill, M. (eds) Ageing: Lessons from C. elegans. Healthy Ageing and Longevity. Springer, Cham. https://doi.org/10.1007/978-3-319-44703-2_7

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