Neurosensory Perception of Environmental Cues Modulates Sperm Motility Critical for Fertilization

McKnight, Katherine; Hoang, Hieu D.; Prasain, Jeevan K.; Brown, Naoko; Vibbert, Jack; Hollister, Kyle A.; Moore, Ray; Ragains, Justin R.; Reese, Jeff; Miller, Michael A.

doi:10.1126/science.1250598

Cited by 48 publications

(90 citation statements)

References 34 publications

(39 reference statements)

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“…srb-13 , 12 , 16(xmDf2) sperm are slow and reverse course frequently (Table 1). These motility defects are consistent with failure to respond effectively to prostaglandins, which stimulate sperm velocity and prevent reversals (Table 1) [22, 24]. When sperm competitiveness was evaluated, we found that srb-13 , 12 , 16(xmDf2) sperm are less competitive at fertilization than control and srb-13(xm1) sperm (S3C and S3D Fig).…”

Section: Resultssupporting

confidence: 70%

Chemosensory and hyperoxia circuits in C. elegans males influence sperm navigational capacity

Hoang

Miller

2017

PLoS Biol

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The sperm’s crucial function is to locate and fuse with a mature oocyte. Under laboratory conditions, Caenorhabditis elegans sperm are very efficient at navigating the hermaphrodite reproductive tract and locating oocytes. Here, we identify chemosensory and oxygen-sensing circuits that affect the sperm’s navigational capacity. Multiple Serpentine Receptor B (SRB) chemosensory receptors regulate Gα pathways in gustatory sensory neurons that extend cilia through the male nose. SRB signaling is necessary and sufficient in these sensory neurons to influence sperm motility parameters. The neuropeptide Y pathway acts together with SRB-13 to antagonize negative effects of the GCY-35 hyperoxia sensor on spermatogenesis. SRB chemoreceptors are not essential for sperm navigation under low oxygen conditions that C. elegans prefers. In ambient oxygen environments, SRB-13 signaling impacts gene expression during spermatogenesis and the sperm’s mitochondria, thereby increasing migration velocity and inhibiting reversals within the hermaphrodite uterus. The SRB-13 transcriptome is highly enriched in genes implicated in pathogen defense, many of which are expressed in diverse tissues. We show that the critical time period for SRB-13 signaling is prior to spermatocyte differentiation. Our results support the model that young C. elegans males sense external environment and oxygen tension, triggering long-lasting downstream signaling events with effects on the sperm’s mitochondria and navigational capacity. Environmental exposures early in male life may alter sperm function and fertility.

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Section: Resultssupporting

confidence: 70%

Chemosensory and hyperoxia circuits in C. elegans males influence sperm navigational capacity

Hoang

Miller

2017

PLoS Biol

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“…It remains an important goal to understand which components of sperm guidance may be conserved across species and which evolve species-specific roles. Recent work also shows that chemosensory cues from the external environment encountered by females and hermaphrodites, as well as their starvation state, can modulate female production of sperm chemoattractants that they secrete in their reproductive tract (KUBAGAWA et al 2006;MCKNIGHT et al 2014). Exogenous factors experienced by males also can influence sperm migration ability (HOANG AND MILLER 2017).…”

Section: Caenorhabditismentioning

confidence: 99%

Genetic contributions to ectopic sperm cell migration inCaenorhabditisnematodes

Ting

Tsai

Cutter

2018

Preprint

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Reproductive barriers involving gametic incompatibilities can act to enhance population divergence and promote the persistence of species boundaries. Observing gametic interactions in internal fertilizing organisms, however, presents a considerable practical challenge to characterizing mechanisms of such gametic isolation. Here we exploit the transparency of Caenorhabditis nematodes to investigate gametic isolation mediated by sperm that can migrate to ectopic locations, with this sperm invasion capable of inducing female sterility and premature death. As a step toward identifying genetic factors and mechanisms associated with female susceptibility to sperm invasion, we characterized a panel of 25 C. elegans genetic mutants to test for effects on the incidence and severity of sperm invasion in both conspecific and interspecies matings. We found genetic perturbations to contribute to distinct patterns of susceptibility that identify ovulation dynamics and sperm guidance cues as modulators of ectopic sperm migration incidence and severity. Genotypes confer distinctive phenotypic sensitivities to the sperm from conspecific C. elegans males versus heterospecific C. nigoni males, implicating evolution of functional divergence in the history of these species for components of spermreproductive tract interactions. Sexually-antagonistic co-evolution within species that drives divergent trait and molecular evolution between species provides a working model to explain mismatched species-specific gametic interactions that promote or mitigate ectopic sperm migration. Article SummaryHere we exploit the transparency of C. elegans roundworms to investigate reproductive barriers between species resulting from sperm-cell invasion into ectopic tissues, causing female sterility and premature death. We quantify female sensitivity to sperm invasion from conspecific and interspecific matings in a panel of 25 C. elegans genetic mutants, to demonstrate how ovulation dynamics and sperm guidance cues act as modulators of ectopic sperm-cell migration incidence and severity. We observe both conserved and divergent responses to different species, implicating evolution of functional divergence for components of sperm-reproductive tract interactions consistent with the outcome of sexually-antagonistic co-evolution.

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“…Therefore, when genes involved in the synthesis are mutated, spermatozoa become partly defective in their relocation from the uterus into the spermatheca. [18][19][20] These phenotypes seem similar to those of spe-9 and spe-45 mutants, resulting in the incomplete sperm recruitment into the spermatheca. Currently the sperm prostaglandin-receptor(s) is not known, but SPE-9 and/or SPE-45 could function in the prostaglandin binding to spermatozoa and/or subsequent sperm reaction(s).…”

Section: Introductionmentioning

confidence: 52%

Gamete interactions require transmembranous immunoglobulin-like proteins with conserved roles during evolution

Nishimura

L’Hernault

2016

Worm

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C. elegans spe-9 class genes are male germline-enriched in their expression and indispensable during sperm-oocyte fusion. Identification of mammalian orthologs that exhibit similar functions to these C. elegans genes has been a challenge. The mouse Izumo1 gene encodes a sperm-specific, immunoglobulin (Ig)-like transmembrane (TM) protein that is required for gamete fusion. We recently identified the C. elegans spe-45 gene, which shows male germline-enriched expression and encodes an Ig-like TM protein. spe-45 mutant worms produced otherwise normal spermatozoa that cannot fuse with oocytes, causing essentially the same phenotype as that seen in the Izumo1-knockout mice. By counting the number of self-sperm in the spermatheca of spe-45 hermaphrodites, it was found that this gene might be involved in sperm guidance from the uterus into the spermatheca, as well as gamete fusion. Moreover, we discovered that SPE-45 and IZUMO1 share certain functions for gamete fusion, which are presumably related to binding with cis-and/or trans-partners. Intriguingly, various organisms have Ig-like TM proteins that act during gamete interactions, indicating the wide-spread utility of Ig-like domains during fertilization.

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Neurosensory Perception of Environmental Cues Modulates Sperm Motility Critical for Fertilization

Cited by 48 publications

References 34 publications

Chemosensory and hyperoxia circuits in C. elegans males influence sperm navigational capacity

Chemosensory and hyperoxia circuits in C. elegans males influence sperm navigational capacity

Genetic contributions to ectopic sperm cell migration inCaenorhabditisnematodes

Gamete interactions require transmembranous immunoglobulin-like proteins with conserved roles during evolution

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