Zinc deficiency reduces fertility in C. elegans hermaphrodites and disrupts oogenesis and meiotic progression

Comp Biochem Physiol C Toxicol Pharmacol. 2017 Jan:191:203-209. doi: 10.1016/j.cbpc.2016.09.006. Epub 2016 Sep 20.

Abstract

Zinc is necessary for successful gametogenesis in mammals; however the role of zinc in the gonad function of non-mammalian species has not been investigated. The genetic tractability, short generation time, and hermaphroditic reproduction of the nematode C. elegans offer distinct advantages for the study of impaired gametogenesis as a result of zinc deficiency. However the phenotypic reproductive effects arising from zinc restriction have not been established in this model. We therefore examined the effect of zinc deficiency on C. elegans reproduction by exposing worms to the zinc chelator N,N,N',N'-tetrakis (2-pyridylmethyl)ethane-1,2-diamine (TPEN). Treatment began at the early larval stage and continued until reproductive senescence. TPEN treatment reduced the total number of progeny produced by C. elegans hermaphrodites compared with control subjects, with the largest difference in output observed 48h after larval stage 4. At this time-point, zinc deficient worms displayed fewer embryos in the uterus and disorganized oocyte development when observed under DIC microscopy. DAPI staining revealed impaired oogenesis and chromosome dynamics with an expanded region of pachytene stage oocytes extending into the proximal arm of the gonad. This phenotype was not seen in control or zinc-rescue subjects. This study demonstrates that reproduction in C. elegans is sensitive to environmental perturbations in zinc, indicating that this is a good model for future studies in zinc-mediated subfertility. Aberrant oocyte development and disruption of the pachytene-diplotene transition indicate that oogenesis in particular is affected by zinc deficiency in this model.

Keywords: C. elegans; Fertility; Oogenesis; Zinc.

MeSH terms

  • Animals
  • Caenorhabditis elegans / drug effects
  • Caenorhabditis elegans / embryology
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Chelating Agents / pharmacology
  • Embryo, Nonmammalian / drug effects
  • Embryo, Nonmammalian / metabolism
  • Ethylamines / pharmacology
  • Female
  • Fertility
  • Hermaphroditic Organisms* / drug effects
  • Meiosis* / drug effects
  • Oocytes / drug effects
  • Oocytes / metabolism*
  • Oocytes / pathology
  • Oogenesis* / drug effects
  • Pyridines / pharmacology
  • Time Factors
  • Zinc / deficiency*

Substances

  • Chelating Agents
  • Ethylamines
  • N,N,N',N'-tetrakis(2-pyridylmethyl)ethane-1,2-diamine
  • Pyridines
  • Zinc