The Sperm TRP-3 Channel Mediates the Onset of a Ca 2+ Wave in the Fertilized C. elegans Oocyte

Abstract

Sperm induce Ca(2+) waves in the fertilized egg by introducing soluble factors or by surface interactions, which activate egg Ca(2+) channels. Involvement of sperm Ca(2+) channels is predicted by the conduit model; however, this model has not been validated. In Caenorhabditis elegans, the sperm-specific TRP family Ca(2+) channel TRP-3 mediates sperm-oocyte fusion. Here, using high-speed in vivo imaging and image analyses, we show that sperm induce an immediate local Ca(2+) rise followed by a Ca(2+) wave in fertilized C. elegans oocytes. Oocytes fertilized by rare trp-3 escaper sperm showed a lack of local rise and a delay in onset of the Ca(2+) wave. Sperm Ca(2+) imaging suggests that the local rise is not due to the bolus introduction of stored Ca(2+). These results suggest that, along with its primary function in sperm-oocyte fusion, TRP-3 induces Ca(2+) waves in fertilized oocytes, consistent with the conduit model.

TRPM7 and Ca V 3.2 channels mediate Ca 2+ influx required for egg activation at fertilization

“…It is unlikely that new channels are derived from cortical granule membranes, because cortical granule exocytosis occurs normally following ICSI (34,35); yet ICSI eggs do not display the stop-restart Ca 2+ oscillation pattern. A possible source, however, is the sperm plasma membrane, which has several types of Ca 2+ -permeable channels that could function in the newly formed zygote; this phenomenon occurs in Caenorhabditis elegans (38). Lastly, the new channels could come from fusion of egg intracellular vesicles other than cortical granules, with the caveat that this fusion event must be dependent on a signal that originates as a result of sperm-egg fusion.…”

DrosophilaTrpm mediates calcium influx during egg activation

“…This apparent conservation in mechanisms in egg activation involving orthologous Trpm channels in a protostome (Drosophila) and a deuterostome (mouse) prompts us to wonder whether Trpm-mediated calcium influx is a very ancient and basal aspect of egg activation, with other more variable aspects such as sperm-triggered calcium rises being more derived, if better known, features. It is interesting in this light that a sperm-delivered TRP channel (TRP-3) has also been reported to mediate calcium influx and a calcium rise in another protostome, C. elegans (38).…”

Mechanisms that prevent catastrophic interactions between paternal chromosomes and the oocyte meiotic spindle

“…The germinal vesicle in the -1 oocyte first migrates away from the spermatheca in a kinesin-1 dependent manner [34,35] to assume a cortical position far from the spermatheca (Figure 2(A)). The spermathecal valve proximal to the oocyte then dilates to allow egg entry into the spermatheca and fertilization occurs at the point on the oocyte surface that first enters the spermathecal valve [8]. The site of fertilization is thus on the opposite side of the zygote from the germinal vesicle.…”

“…The exact point during female meiosis when fertilization occurs varies between species. Fertilization occurs during metaphase II in vertebrates [4], during metaphase I in ascidians [5], Drosophila [3], starfish [2], some molluscs [6] and the annelid Chaetopterus [7], during prometaphase I in C. elegans [8,9] and during late prophase in Urechis [10] and other molluscs [11]. Thus the egg must tolerate the presence of sperm-derived chromosomes while actively trying to reduce its ploidy for time periods ranging from 35 minutes in C. elegans [9] to 2 hours in mouse [12].…”