Zinc availability during germline development impacts embryo viability in Caenorhabditis elegans

Abstract

Zinc is an essential metal that serves as a cofactor in a variety of cellular processes, including meiotic maturation. Cellular control of zinc uptake, availability and efflux is closely linked to meiotic progression in rodent and primate reproduction where large fluctuations in zinc levels are critical at several steps in the oocyte-to-embryo transition. Despite these well-documented roles of zinc fluxes during meiosis, only a few of the genes encoding key zinc receptors, membrane-spanning transporters, and downstream signaling pathway factors have been identified to date. Furthermore, little is known about analogous roles for zinc fluxes in the context of a whole organism. Here, we evaluate whether zinc availability regulates germline development and oocyte viability in the nematode Caenorhabditis elegans, an experimentally flexible model organism. We find that similar to mammals, mild zinc limitation in C. elegans profoundly impacts the reproductive axis: the brood size is significantly reduced under conditions of zinc limitation where other physiological functions are not perturbed. Zinc limitation in this organism has a more pronounced impact on oocytes than sperm and this leads to the decrease in viable embryo production. Moreover, acute zinc limitation of isolated zygotes prevents extrusion of the second polar body during meiosis and leads to aneuploid embryos. Thus, the zinc-dependent steps in C. elegans gametogenesis roughly parallel those described in meiotic-to-mitotic transitions in mammals.

In utero and peripubertal metals exposure in relation to reproductive hormones and sexual maturation and progression among boys in Mexico City

“…Few cross-sectional studies on boys and girls also reported a significant positive relationship between serum or plasma zinc concentrations and stages of sexual maturation [101][102][103][104], as well as reproductive hormones (testosterone). Zn is an essential trace metal and is fundamental for the development of the male reproductive system [105,106]. Studies on various animals described the role of Zn in advancing male puberty, through increased testicular activity, testosterone production, metabolism, and growth, primarily via activated the hypothalamus and the pituitary functions [107][108][109][110][111][112].…”

Assessing the Viability and Degeneration of the Medically Important Filarial Nematodes

“…Using C. elegans as the type model [20] is useful but filarial worms and other parasitic nematodes are considerably more complex and are likely to have different and unique characteristics. This kind of research is difficult to maintain in the present world where research funding is difficult to acquire, but nevertheless, the acquisition of more detailed information in this subject would undoubtedly be highly valuable.…”

Role of Zinc (Zn) in Human Reproduction: A Journey from Initial Spermatogenesis to Childbirth

“…Zn spark is treated as a novel biomarker of the mammalian quality of embryos and other aspects of developmental potential. In terms of flux, little research has been done on Zn ions and their implications [ 60 ]. The proton extrusion mechanism plays a key parameter in capacitation.…”