Age-related degeneration of the egg-laying system promotes matricidal hatching in Caenorhabditis elegans

Aging Cell. 2013 Aug;12(4):544-53. doi: 10.1111/acel.12079. Epub 2013 May 2.

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.

Keywords: C. elegans; aging; bag of worms; matricidal hatching; reproduction.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Aging / metabolism
  • Aging / physiology*
  • Animals
  • Caenorhabditis elegans / drug effects
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Female
  • Hermaphroditic Organisms / drug effects
  • Hermaphroditic Organisms / genetics
  • Hermaphroditic Organisms / physiology
  • Longevity
  • Male
  • Muscle Contraction
  • Ovum / metabolism*
  • Ovum / physiology
  • Receptors, Nicotinic / genetics
  • Receptors, Nicotinic / metabolism
  • Self-Fertilization
  • Serotonin / pharmacology
  • Species Specificity
  • Survival Analysis
  • Time Factors
  • Vulva / metabolism
  • Vulva / physiology

Substances

  • Caenorhabditis elegans Proteins
  • Eat-2 protein, C elegans
  • Receptors, Nicotinic
  • Serotonin