Proteomic and evolutionary analyses of sperm activation identify uncharacterized genes in Caenorhabditis nematodes

Kasimatis, Katja R; Moerdyk-Schauwecker, Megan; Timmermeyer, Nadine; Phillips, Patrick C.

doi:10.1186/s12864-018-4980-7

Cited by 3 publications

(21 citation statements)

References 52 publications

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“…Microarray analysis found 430 genes with enriched expression in male soma, which was about one-third the number of genes with spermatogenesis enrichment in that study (Reinke et al 2004). Lower throughput proteomics analysis further supports the presence and abundance of a subset of these genes (Kasimatis et al 2018b). These male-biased genes are enriched for membrane and kinase/ phosphatase gene ontology terms (Reinke et al 2004;Thomas et al 2012).…”

Section: Genomic Persistence Of Male-related Genesmentioning

confidence: 55%

“…The PLG-1 mucin protein also gets transferred during copulation to form a copulatory plug on the vulva, which partially inhibits subsequent male mating attempts, and may aid in sperm retention in the uterus (Barker 1994;Palopoli et al 2008). The sperm themselves secrete some proteins via specialized vesicles upon activation (Kasimatis et al 2018b), and secretion of MSP is important in triggering ovulation (Miller et al 2001), although it is not clear whether any of these proteins play an important part in sperm competition. Interestingly, the SWM-1 sperm activation protein is actually produced by muscle cells before it migrates to the gonad (Chavez et al 2018) and gut-derived compounds migrate to the female germline for use by oocytes to secrete prostaglandins as sperm chemoattractant (Kubagawa et al 2006), suggesting that proteins important for mediating sexual conflict could be recruited from tissues spread across the bodies of both males and hermaphrodites/females.…”

Section: Evolution Of Sperm Competitionmentioning

confidence: 99%

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Males, Outcrossing, and Sexual Selection in Caenorhabditis Nematodes

2019

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Males of Caenorhabditis elegans provide a crucial practical tool in the laboratory, but, as the rarer and more finicky sex, have not enjoyed the same depth of research attention as hermaphrodites. Males, however, have attracted the attention of evolutionary biologists who are exploiting the C. elegans system to test longstanding hypotheses about sexual selection, sexual conflict, transitions in reproductive mode, and genome evolution, as well as to make new discoveries about Caenorhabditis organismal biology. Here, we review the evolutionary concepts and data informed by study of males of C. elegans and other Caenorhabditis. We give special attention to the important role of sperm cells as a mediator of inter-male competition and male–female conflict that has led to drastic trait divergence across species, despite exceptional phenotypic conservation in many other morphological features. We discuss the evolutionary forces important in the origins of reproductive mode transitions from males being common (gonochorism: females and males) to rare (androdioecy: hermaphrodites and males) and the factors that modulate male frequency in extant androdioecious populations, including the potential influence of selective interference, host–pathogen coevolution, and mutation accumulation. Further, we summarize the consequences of males being common vs rare for adaptation and for trait divergence, trait degradation, and trait dimorphism between the sexes, as well as for molecular evolution of the genome, at both micro-evolutionary and macro-evolutionary timescales. We conclude that C. elegans male biology remains underexploited and that future studies leveraging its extensive experimental resources are poised to discover novel biology and to inform profound questions about animal function and evolution.

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Section: Genomic Persistence Of Male-related Genesmentioning

confidence: 55%

Section: Evolution Of Sperm Competitionmentioning

confidence: 99%

Males, Outcrossing, and Sexual Selection in Caenorhabditis Nematodes

2019

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“…3) and uterus (Fig. 4) was unexpected given that the NSPFs were previously characterized as being associated with sperm MOs (Kasimatis et al 2018) and that mRNA expression data indicated that all three nspf genes are expressed in the gonad only (Kruse et al 2016). One potential reason for the non-overlapping localization patterns could be an artifact of our experimental set-up.…”

Section: Discussionmentioning

confidence: 91%

“…Previous fecundity data were replotted using the data available in Kasimatis et al (2018) Additional File 9.…”

Section: Fertility Assaysmentioning

confidence: 99%

“…Consequently, we hypothesize that these MO fusions provide a novel contribution to the seminal fluid proteome. Characterization of the MO proteome identified the Nematode-Specific Peptide family, group F (NSPF) as the second most abundant set of proteins in the MO (Kasimatis et al, 2018). Kasimatis et al (2018) additionally showed that the NSPF genes are conserved in both sequence identity and synteny across the genus.…”

Section: Introductionmentioning

confidence: 99%

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A novel sperm-derived seminal fluid protein inCaenorhabditisnematodes

Kasimatis

Rehaluk

Rowe

et al. 2022

Preprint

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Post-insemination molecular interactions involving sperm are an ideal system for linking genotype, phenotype, and fitness. Nematode sperm contain subcellular vesicles known as membranous organelles (MOs) that fuse with the cell membrane upon sperm activation to release their soluble contents into the extracellular space. The second most abundant protein group in the MOs is the conserved Nematode-Specific Peptide family, group F (NSPF) gene family. We hypothesize that these proteins contribute to seminal fluid upon MO fusion and are part of post-insemination reproductive tract dynamics. We used experimental evolution to compete the wildtype allele against a deletion allele in 10 replicate populations. We calculated a significant mean selective disadvantage of 0.1% for the deletion allele, which indicated that the NSPF genes are an evolutionarily important component of male reproductive success. This conclusion was reinforced by qualitative trends from lower powered single-generation male fertility assays. We then characterized the functional location of NSPF proteins during fertilization using whole- worm immunostaining of a His-tagged nspf-1 transgene. Throughout male development, we found that NSPF presence and abundance was correlated with reproductive maturity in males, localizing to the seminal vesicle during L4 and to the spicules throughout adulthood. We confirmed that NSPF proteins are transferred to females during mating and hypothesize that proteins adhere to the spicules during transfer. NSPF proteins localize to the vulva and uterus lumen when transferred to mated females and in unmated adult hermaphrodites. These results suggest that the uterine localization of the NSPF proteins is likely a functional property of both male-derived sperm and self-sperm and not simply incidental to the point of transfer during mating. Our study demonstrates that nematodes use a novel mechanism for generating seminal fluid proteins and shows that the highly abundant NSPF proteins likely have a female-beneficial fitness effect.

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The expression, function, and utilization of Protamine1: a literature review

Ren¹,

Chen²,

Tian³

et al. 2021

Transl Cancer Res TCR

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Objective Protamine 1 (PRM1) is specific in sperm and plays essential roles in fertilization, also a member of cancer testis antigen (CTA) family. This study aims to summarize the expression and function of PRM1 in spermatogenesis, and to broaden the current knowledge and inspire future development of PRM1-based therapeutic strategies in cancer treatment and nanomedicine. Background The protamine proteins, are characterized by an arginine-rich core and cysteine residues. Humans express two types of protamine: PRM1 and PRM2. The abnormal expression or proportion of PRM1 and PRM2 is known to be associated with subfertility and infertility, especially for PRM1 which is highly evolutionary conserved in mammalians and expressed in all vertebrates. Biological functions of PRM1 have been unveiled in diverse cellular processes, such as tumorigenesis, somatic cell nucleus transfer, and drug delivery systems. Moreover, PRM1 is identified as a CTA in chronic leukemia (CLL) and colorectal cancer (CRC). Methods Literature was obtained using PubMed and the keywords protamine 1, PRM1, or P1, from January 1, 1980, through July 20, 2021. We also collect the additional evidence through screening references of articles identified through the PubMed searches. Conclusions PRM1 is well-studied in male infertility, and further researches and attempts to develop PRM1 as novel tumor marker, as well as drug delivery vector, will be of important clinical significance.

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Proteomic and evolutionary analyses of sperm activation identify uncharacterized genes in Caenorhabditis nematodes

Cited by 3 publications

References 52 publications

Males, Outcrossing, and Sexual Selection in Caenorhabditis Nematodes

Males, Outcrossing, and Sexual Selection in Caenorhabditis Nematodes

A novel sperm-derived seminal fluid protein inCaenorhabditisnematodes

The expression, function, and utilization of Protamine1: a literature review

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