Dramatic fertility decline in aging C. elegans males is associated with mating execution deficits rather than diminished sperm quality

Experimental Gerontology

Volumn 48, Issue 11, 2013, Pages 1156-1166

  Chatterjee, Indrani ^a   Ibanez Ventoso, Carolina ^b   Vijay, Priyanka ^a   Singaravelu, Gunasekaran ^a   Baldi, Christopher ^a   Bair, Julianna ^a   Ng, Susan ^a   Smolyanskaya, Alexandra ^a   Driscoll, Monica ^b   Singson, Andrew ^a  

^a RUTGERS UNIVERSITY   (United States)

^b The State University of New Jersey   (United States)

Author keywords

Aging; C. elegans; Fertility; Males; Sperm

Indexed keywords

INSULIN;

ADULT ANIMAL; AGING; ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; GAMETE; GROWTH PLATE; HERMAPHRODITIC SPECIES; HETEROSIS; LIFESPAN; MALE; MALE FERTILITY; MALE GENITAL TRACT PARAMETERS; MATING SUCCESS; NONHUMAN; PHYSICAL CAPACITY; PRIORITY JOURNAL; PROGENY; REPRODUCTIVE SUCCESS; SENESCENCE; SIGNAL TRANSDUCTION; SPERM QUALITY; SPERMATID; SPERMATOZOON COUNT;

AGING; C. ELEGANS; FERTILITY; MALES; SPERM;

AGING; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CULTURE MEDIA; FEMALE; FERTILITY; GARLIC; GENES, HELMINTH; INSULIN; MALE; MODELS, ANIMAL; MUTATION; RECEPTOR, INSULIN; SEXUAL BEHAVIOR, ANIMAL; SIGNAL TRANSDUCTION; SPERM COUNT; SPERMATOZOA; TRANSCRIPTION FACTORS;

EID: 84883639632     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2013.07.014     Document Type: Article

References (83)

1. Altun Z.F., Herndon L.A., Crocker C., Lints R., Hall D.H. WormAtlas 2002-2012.
2. Anderson J.L., Reynolds R.M., Morran L.T., Tolman-Thompson J., Phillips P.C. Experimental evolution reveals antagonistic pleiotropy in reproductive timing but not life span in Caenorhabditis elegans. J. Gerontol. A Biol. Sci. Med. Sci. 2011, 66:1300-1308.
3. Andux S., Ellis R.E. Apoptosis maintains oocyte quality in aging Caenorhabditis elegans females. PLoS Genet. 2008, 4:e1000295.
4. Arantes-Oliveira N., Apfeld J., Dillin A., Kenyon C. Regulation of life-span by germ-line stem cells in Caenorhabditis elegans. Science 2002, 295:502-505.
5. Balasch J., Gratacós E. Delayed childbearing: effects on fertility and the outcome of pregnancy. Fetal Diagn. Ther. 2011, 29:263-273.
6. Ball Z.B., Barnes R.H., Visscher M.B. The effects of dietary caloric restriction on maturity and senescence, with particular reference to fertility and longevity. Am. J. Physiol. 1947, 150:511-519.
7. Barr M.M., Garcia L.R. Male mating behavior. WormBook 2006, 1-11.
8. Barrios A., Nurrish S., Emmons S.W. Sensory regulation of C. elegans male mate-searching behavior. Curr. Biol. 2008, 18:1865-1871.
9. Berg B.N. Nutrition and longevity in the rat. I. Food intake in relation to size, health and fertility. J. Nutr. 1960, 71:242-254.
10. Berg B.N., Simms H.S. Nutrition and longevity in the rat. II. Longevity and onset of disease with different levels of food intake. J. Nutr. 1960, 71:255-263.
11. Birkhead T.R. Sperm competition: evolution and mechanisms. Curr. Top. Dev. Biol. 1996, 33:103-158.
12. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
13. Casanueva M.O., Burga A., Lehner B. Fitness trade-offs and environmentally induced mutation buffering in isogenic C. elegans. Science 2012, 335:82-85.
14. Cleary-Goldman J., Malone F.D., Vidaver J., Ball R.H., Nyberg D.A., Comstock C.H., Saade G.R., Eddleman K.A., Klugman S., Dugoff L., Timor-Tritsch I.E., Craigo S.D., Carr S.R., Wolfe H.M., Bianchi D.W., D'Alton M., Consortium, F. Impact of maternal age on obstetric outcome. Obstet. Gynecol. 2005, 105:983-990.
15. Collins J.J., Huang C., Hughes S., Kornfeld K. The measurement and analysis of age-related changes in Caenorhabditis elegans. WormBook 2008, 1-21.
16. Croll N.A., Smith J.M., Zuckerman B.M. The aging process of the nematode Caenorhabditis elegans in bacterial and axenic culture. Exp. Aging Res. 1977, 3:175-189.
17. Djahanbakhch O., Ezzati M., Zosmer A. Reproductive ageing in women. J. Pathol. 2007, 211:219-231.
18. Emmons S.W. Male development. WormBook 2005, 1-22.
19. Emmons S.W., Sternberg P.W. Male development and mating behavior. C. elegans II 1997, 295-334. Cold Spring Harbor Laboratory, Cold Spring Harbor. D.L. Riddle, T. Blumenthal, B.J. Meyer, J.R. Priess (Eds.).
20. Garcia L.R., Mehta P., Sternberg P.W. Regulation of distinct muscle behaviors controls the C. elegans male's copulatory spicules during mating. Cell 2001, 107:777-788.
21. Geldziler B.D., Marcello M.R., Shakes D.C., Singson A. The genetics and cell biology of fertilization. Methods Cell Biol. 2011, 106:343-375.
22. Gems D., Riddle D.L. Longevity in Caenorhabditis elegans reduced by mating but not gamete production. Nature 1996, 379:723-725.
23. Gems D., Riddle D.L. Genetic, behavioral and environmental determinants of male longevity in Caenorhabditis elegans. Genetics 2000, 154:1597-1610.
24. Gems D., Sutton A.J., Sundermeyer M.L., Albert P.S., King K.V., Edgley M.L., Larsen P.L., Riddle D.L. Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics 1998, 150:129-155.
25. Ghazi A. Transcriptional networks that mediate signals from reproductive tissues to influence lifespan. Genesis 2013, 51:1-15.
26. Glenn C.F., Chow D.K., David L., Cooke C.A., Gami M.S., Iser W.B., Hanselman K.B., Goldberg I.G., Wolkow C.A. Behavioral deficits during early stages of aging in Caenorhabditis elegans result from locomotory deficits possibly linked to muscle frailty. J. Gerontol. A Biol. Sci. Med. Sci. 2004, 59:1251-1260.
27. Guo X., Navetta A., Gualberto D.G., Garcia L.R. Behavioral decay in aging male C. elegans correlates with increased cell excitability. Neurobiol. Aging 2012, 33. (1483 e5-23).
28. Herndon L.A., Schmeissner P.J., Dudaronek J.M., Brown P.A., Listner K.M., Sakano Y., Paupard M.C., Hall D.H., Driscoll M. Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 2002, 419:808-814.
29. Hosono R., Sato Y., Aizawa S.I., Mitsui Y. Age-dependent changes in mobility and separation of the nematode Caenorhabditis elegans. Exp. Gerontol. 1980, 15:285-289.
30. Hsin H., Kenyon C. Signals from the reproductive system regulate the lifespan of C. elegans. Nature 1999, 399:362-366.
31. Hsu A.L., Murphy C.T., Kenyon C. Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 2003, 300:1142-1145.
32. Huang C., Xiong C., Kornfeld K. Measurements of age-related changes of physiological processes that predict lifespan of Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:8084-8089.
33. Hughes S.E., Evason K., Xiong C., Kornfeld K. Genetic and pharmacological factors that influence reproductive aging in nematodes. PLoS Genet. 2007, 3:e25.
34. Hughes S.E., Huang C., Kornfeld K. Identification of mutations that delay somatic or reproductive aging of Caenorhabditis elegans. Genetics 2011, 189:341-356.
35. Jensen T.K., Carlsen E., Jorgensen N., Berthelsen J.G., Keiding N., Christensen K., Petersen J.H., Knudsen L.B., Skakkebaek N.E. Poor semen quality may contribute to recent decline in fertility rates. Hum. Reprod. 2002, 17:1437-1440.
36. Johnson T.E. Aging can be genetically dissected into component processes using long-lived lines of Caenorhabditis elegans. Proc. Natl Acad. Sci. U. S. A 1987, 84:3777-3781.
37. Johnson T.E., Tedesco P.M., Lithgow G.J. Comparing mutants, selective breeding, and transgenics in the dissection of aging processes of Caenorhabditis elegans. Genetica 1993, 91:65-77.
38. Kaletsky R., Murphy C.T. The role of insulin/IGF-like signaling in C. elegans longevity and aging. Dis. Model Mech. 2010, 3:415-419.
39. Kenyon C.J. The genetics of ageing. Nature 2010, 464:504-512.
40. Kenyon C. A pathway that links reproductive status to lifespan in Caenorhabditis elegans. Ann. N. Y. Acad. Sci. 2010, 1204:156-162.
41. Kenyon C., Chang J., Gensch E., Rudner A., Tabtiang R. A C. elegans mutant that lives twice as long as wild type. Nature 1993, 366:461-464.
42. Kimura K.D., Tissenbaum H.A., Liu Y., Ruvkun G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 1997, 277:942-946.
43. Kirkwood T.B. Evolution of ageing. Nature 1977, 270:301-304.
44. Klass M.R. Aging in the nematode Caenorhabditis elegans: major biological and environmental factors influencing life span. Mech. Ageing Dev. 1977, 6:413-429.
45. Kong A., Frigge M.L., Masson G., Besenbacher S., Sulem P., Magnusson G., Gudjonsson S.A., Sigurdsson A., Jonasdottir A., Wong W.S., Sigurdsson G., Walters G.B., Steinberg S., Helgason H., Thorleifsson G., Gudbjartsson D.F., Helgason A., Magnusson O.T., Thorsteinsdottir U., Stefansson K. Rate of de novo mutations and the importance of father's age to disease risk. Nature 2012, 488:471-475.
46. Lee S.S., Kennedy S., Tolonen A.C., Ruvkun G. DAF-16 target genes that control C. elegans life-span and metabolism. Science 2003, 300:644-647.
47. L'Hernault S.W., Roberts T.M. Cell biology of nematode sperm. Methods Cell Biol. 1995, 48:273-301.
48. L'Hernault S.W., Shakes D.C., Ward S. Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans. Genetics 1988, 120:435-452.
49. Lin K., Dorman J.B., Rodan A., Kenyon C. daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 1997, 278:1319-1322.
50. Lin C.H., Tomioka M., Pereira S., Sellings L., Iino Y., van der Kooy D. Insulin signaling plays a dual role in Caenorhabditis elegans memory acquisition and memory retrieval. J. Neurosci. 2010, 30:8001-8011.
51. Lipton J., Kleemann G., Ghosh R., Lints R., Emmons S.W. Mate searching in Caenorhabditis elegans: a genetic model for sex drive in a simple invertebrate. J. Neurosci. 2004, 24:7427-7434.
52. Liu K.S., Sternberg P.W. Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 1995, 14:79-89.
53. Liu Y., LeBeouf B., Guo X., Correa P.A., Gualberto D.G., Lints R., Garcia L.R. A cholinergic-regulated circuit coordinates the maintenance and bi-stable states of a sensory-motor behavior during Caenorhabditis elegans male copulation. PLoS Genet. 2011, 7:e1001326.
54. Luo S., Shaw W.M., Ashraf J., Murphy C.T. TGF-beta Sma/Mab signaling mutations uncouple reproductive aging from somatic aging. PLoS Genet. 2009, 5:e1000789.
55. Luo S., Kleemann G.A., Ashraf J.M., Shaw W.M., Murphy C.T. TGF-beta and insulin signaling regulate reproductive aging via oocyte and germline quality maintenance. Cell 2010, 143:299-312.
56. McCulloch D., Gems D. Evolution of male longevity bias in nematodes. Aging Cell 2003, 2:165-173.
57. Medawar P.B. An Unsolved Problem of Biology 1952, H.K. Lewis & Co., London.
58. Mendenhall A.R., Wu D., Park S.K., Cypser J.R., Tedesco P.M., Link C.D., Phillips P.C., Johnson T.E. Genetic dissection of late-life fertility in Caenorhabditis elegans. J. Gerontol. A Biol. Sci. Med. Sci. 2011, 66:842-854.
59. Merry B.J., Holehan A.M. Onset of puberty and duration of fertility in rats fed a restricted diet. J. Reprod. Fertil. 1979, 57:253-259.
60. Moller A.P., Mousseau T.A., Rudolfsen G., Balbontin J., Marzal A., Hermosell I., De Lope F. Senescent sperm performance in old male birds. J. Evol. Biol. 2009, 22:334-344.
61. Murakami S., Murakami H. The effects of aging and oxidative stress on learning behavior in C. elegans. Neurobiol. Aging 2005, 26:899-905.
62. Nelson G.A., Ward S. Vesicle fusion, pseudopod extension and amoeboid motility are induced in nematode spermatids by the ionophore monensin. Cell 1980, 19:457-464.
63. Ogg S., Paradis S., Gottlieb S., Patterson G.I., Lee L., Tissenbaum H.A., Ruvkun G. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 1997, 389:994-999.
64. Pan C.L., Peng C.Y., Chen C.H., McIntire S. Genetic analysis of age-dependent defects of the Caenorhabditis elegans touch receptor neurons. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:9274-9279.
65. Partridge L. Some highlights of research on aging with invertebrates, 2010. Aging Cell 2011, 10:5-9.
66. Partridge L., Piper M.D., Mair W. Dietary restriction in Drosophila. Mech. Ageing Dev. 2005, 126:938-950.
67. Powolny A.A., Singh S.V., Melov S., Hubbard A., Fisher A.L. The garlic constituent diallyl trisulfide increases the lifespan of C. elegans via skn-1 activation. Exp. Gerontol. 2011, 46:441-452.
68. Rea S.L., Wu D.Q., Cypser J.R., Vaupel J.W., Johnson T.E. A stress-sensitive reporter predicts longevity in isogenic populations of Caenorhabditis elegans. Nat. Genet. 2005, 37:894-898.
69. Saha S., Barnett A.G., Foldi C., Burne T.H., Eyles D.W., Buka S.L., McGrath J.J. Advanced paternal age is associated with impaired neurocognitive outcomes during infancy and childhood. PLoS Med. 2009, 6:e40.
70. Shakes D., Ward S. Mutations that disrupt the morphogenesis and localization of a sperm-specific organelle in Caenorhabditis elegans. Dev. Biol. 1989, 134:307-316.
71. Silva L.F., Oliveira J.B., Petersen C.G., Mauri A.L., Massaro F.C., Cavagna M., Baruffi R.L., Franco J.G. The effects of male age on sperm analysis by motile sperm organelle morphology examination (MSOME). Reprod. Biol. Endocrinol. 2012, 10:19.
72. Simon J.M., Sternberg P.W. Evidence of a mate-finding cue in the hermaphrodite nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:1598-1603.
73. Singaravelu G., Chatterjee I., Marcello M.R., Singson A. Isolation and in vitro activation of Caenorhabditis elegans sperm. J. Vis. Exp. 2011, 47. pii: 2336. 10.3791/2336.
74. Singson A. Every sperm is sacred: fertilization in Caenorhabditis elegans. Dev. Biol. 2001, 230:101-109.
75. Singson A., Hill K.L., L'Hernault S.W. Sperm competition in the absence of fertilization in Caenorhabditis elegans. Genetics 1999, 152:201-208.
76. Singson A., Hang J.S., Parry J.M. Genes required for the common miracle of fertilization in Caenorhabditis elegans. Int. J. Dev. Biol. 2008, 52:647-656.
77. Tank E.M., Rodgers K.E., Kenyon C. Spontaneous age-related neurite branching in Caenorhabditis elegans. J. Neurosci. 2011, 31:9279-9288.
78. Templado C., Donate A., Giraldo J., Bosch M., Estop A. Advanced age increases chromosome structural abnormalities in human spermatozoa. Eur. J. Hum. Genet. 2011, 19:145-151.
79. Tissenbaum H.A., Ruvkun G. An insulin-like signaling pathway affects both longevity and reproduction in Caenorhabditis elegans. Genetics 1998, 148:703-717.
80. Toth M.L., Melentijevic I., Shah L., Bhatia A., Lu K., Talwar A., Naji H., Ibanez-Ventoso C., Ghose P., Jevince A., Xue J., Herndon L.A., Bhanot G., Rongo C., Hall D.H., Driscoll M. Neurite sprouting and synapse deterioration in the aging Caenorhabditis elegans nervous system. J. Neurosci. 2012, 32:8778-8790.
81. Williams G.C. Pleiotropy, natural selection, and the evolution of senescence. Evolution 1957, 11:398-411.
82. Wu D., Tedesco P.M., Phillips P.C., Johnson T.E. Fertility/longevity trade-offs under limiting-male conditions in mating populations of Caenorhabditis elegans. Exp. Gerontol. 2012, 47:759-763.
83. Zannoni S., L'Hernault S.W., Singson A.W. Dynamic localization of SPE-9 in sperm: a protein required for sperm-oocyte interactions in Caenorhabditis elegans. BMC Dev. Biol. 2003, 3:10.