title: Age-related degeneration of the egg-laying system promotes matricidal hatching in Caenorhabditis elegans.
abstract: The identification and characterization of age-related degenerative changes is a critical goal because it can elucidate mechanisms of aging biology and contribute to understanding interventions that promote longevity. Here, we document a novel, age-related degenerative change in C. elegans hermaphrodites, an important model system for the genetic analysis of longevity. Matricidal hatching--intra-uterine hatching of progeny that causes maternal death--displayed an age-related increase in frequency and affected ~70% of mated, wild-type hermaphrodites. The timing and incidence of matricidal hatching were largely independent of the levels of early and total progeny production and the duration of male exposure. Thus, matricidal hatching appears to reflect intrinsic age-related degeneration of the egg-laying system rather than use-dependent damage accumulation. Consistent with this model, mutations that extend longevity by causing dietary restriction significantly delayed matricidal hatching, indicating age-related degeneration of the egg-laying system is controlled by nutrient availability. To identify the underlying tissue defect, we analyzed serotonin signaling that triggers vulval muscle contractions. Mated hermaphrodites displayed an age-related decline in the ability to lay eggs in response to exogenous serotonin, indicating that vulval muscles and/or a further downstream function that is necessary for egg laying degenerate in an age-related manner. By characterizing a new, age-related degenerative event displayed by C. elegans hermaphrodites, these studies contribute to understanding a frequent cause of death in mated hermaphrodites and establish a model of age-related reproductive complications that may be relevant to the birthing process in other animals such as humans.
authors.affiliation: Department of Developmental Biology, Washington University School of Medicine, 660 South Euclid Ave., Campus Box 8103, St. Louis, MO 63110, USA.
authors.forename: Christopher L
authors.initials: CL
authors.lastname: Pickett
authors.forename: Kerry
authors.initials: K
authors.lastname: Kornfeld
mesh_terms: D000375:Aging / Q000378:metabolism / Q000502:physiology*; D000818:Animals; D017173:Caenorhabditis elegans / Q000187:drug effects / Q000235:genetics / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism; D005260:Female; D057850:Hermaphroditic Organisms / Q000187:drug effects / Q000235:genetics / Q000502:physiology; D008136:Longevity; D008297:Male; D009119:Muscle Contraction; D010063:Ovum / Q000378:metabolism* / Q000502:physiology; D011978:Receptors, Nicotinic / Q000235:genetics / Q000378:metabolism; D057945:Self-Fertilization; D012701:Serotonin / Q000494:pharmacology; D013045:Species Specificity; D016019:Survival Analysis; D013997:Time Factors; D014844:Vulva / Q000378:metabolism / Q000502:physiology
chemical_list: D029742:Caenorhabditis elegans Proteins; C487508:Eat-2 protein, C elegans; D011978:Receptors, Nicotinic; D012701:Serotonin
keywords: C. elegans; aging; bag of worms; matricidal hatching; reproduction
references.citation: WormBook. 2005 Dec 14;:1-7
references.pmid: 18050396
references.citation: Genetics. 1985 May;110(1):17-72
references.pmid: 3996896
references.citation: Aging Cell. 2003 Jun;2(3):165-73
references.pmid: 12882409
references.citation: Curr Biol. 2006 Feb 7;16(3):252-63
references.pmid: 16461278
references.citation: Proc Natl Acad Sci U S A. 1998 Oct 27;95(22):13091-6
references.pmid: 9789046
references.citation: Curr Biol. 2007 Oct 9;17(19):1635-45
references.pmid: 17900898
references.citation: Nat Genet. 2009 Jun;41(6):637-8
references.pmid: 19471299
references.citation: WormBook. 2008 Jan 24;:1-21
references.pmid: 18381800
references.citation: Science. 1982 May 28;216(4549):1012-4
references.pmid: 6805073
references.citation: Nature. 2002 Oct 24;419(6909):808-14
references.pmid: 12397350
references.citation: Curr Biol. 2008 Oct 14;18(19):1445-55
references.pmid: 18818084
references.citation: Obstet Gynecol. 2005 May;105(5 Pt 1):983-90
references.pmid: 15863534
references.citation: Science. 1982 Nov 5;218(4572):578-80
references.pmid: 6896933
references.citation: Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):790-4
references.pmid: 8570636
references.citation: Genetics. 1998 Sep;150(1):129-55
references.pmid: 9725835
references.citation: Hum Genet. 1982;60(2):101-21
references.pmid: 7042533
references.citation: PLoS Genet. 2007 Feb 16;3(2):e25
references.pmid: 17305431
references.citation: Nature. 1993 Dec 2;366(6454):461-4
references.pmid: 8247153
references.citation: PLoS Genet. 2009 Dec;5(12):e1000789
references.pmid: 20041217
references.citation: PLoS Genet. 2008 Dec;4(12):e1000295
references.pmid: 19057674
references.citation: Nature. 1997 Oct 30;389(6654):994-9
references.pmid: 9353126
references.citation: J Neurosci. 1995 Oct;15(10):6975-85
references.pmid: 7472454
references.citation: Dev Biol. 1979 Dec;73(2):304-21
references.pmid: 499670
references.citation: Nature. 1996 Feb 22;379(6567):723-5
references.pmid: 8602217
references.citation: Proc Natl Acad Sci U S A. 2004 May 25;101(21):8084-9
references.pmid: 15141086
references.citation: J Parasitol. 1999 Dec;85(6):1053-64
references.pmid: 10647037
references.citation: Genetics. 1974 May;77(1):71-94
references.pmid: 4366476
references.citation: J Nematol. 2004 Jun;36(2):107-13
references.pmid: 19262794
references.citation: WormBook. 2006 Jun 19;:1-11
references.pmid: 18050467
references.citation: WormBook. 2005 Dec 28;:1-12
references.pmid: 18050412
references.citation: Genetics. 1993 Apr;133(4):897-917
references.pmid: 8462849
references.citation: Nature. 2000 Feb 3;403(6769):560-4
references.pmid: 10676966
references.citation: Science. 1997 Aug 15;277(5328):942-6
references.pmid: 9252323
references.citation: Science. 1996 May 17;272(5264):1010-3
references.pmid: 8638122
references.citation: Genetics. 1983 Aug;104(4):619-47
references.pmid: 11813735
references.citation: Development. 2000 Dec;127(24):5265-76
references.pmid: 11076749
references.citation: Dev Cell. 2001 Nov;1(5):633-44
references.pmid: 11709184
references.citation: PLoS Genet. 2008 Oct;4(10):e1000230
references.pmid: 18949032
references.citation: Genetics. 1988 Jan;118(1):75-86
references.pmid: 8608934
references.citation: J Gerontol A Biol Sci Med Sci. 2011 Aug;66(8):842-54
references.pmid: 21622982