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

ABSTRACT: BACKGROUND:Nematode sperm have unique and highly diverged morphology and molecular biology. In particular, nematode sperm contain subcellular vesicles known as membranous organelles that are necessary for male fertility, yet play a still unknown role in overall sperm function. Here we take a novel proteomic approach to characterize the functional protein complement of membranous organelles in two Caenorhabditis species: C. elegans and C. remanei. RESULTS:We identify distinct protein compositions between membranous organelles and the activated sperm body. Two particularly interesting and undescribed gene families-the Nematode-Specific Peptide family, group D and the here designated Nematode-Specific Peptide family, group F-localize to the membranous organelle. Both multigene families are nematode-specific and exhibit patterns of conserved evolution specific to the Caenorhabditis clade. These data suggest gene family dynamics may be a more prevalent mode of evolution than sequence divergence within sperm. Using a CRISPR-based knock-out of the NSPF gene family, we find no evidence of a male fertility effect of these genes, despite their high protein abundance within the membranous organelles. CONCLUSIONS:Our study identifies key components of this unique subcellular sperm component and establishes a path toward revealing their underlying role in reproduction.

SUBMITTER: Kasimatis KR

PROVIDER: S-EPMC6081950 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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

Kasimatis Katja R KR Moerdyk-Schauwecker Megan J MJ Timmermeyer Nadine N Phillips Patrick C PC

BMC genomics 20180807 1

<h4>Background</h4>Nematode sperm have unique and highly diverged morphology and molecular biology. In particular, nematode sperm contain subcellular vesicles known as membranous organelles that are necessary for male fertility, yet play a still unknown role in overall sperm function. Here we take a novel proteomic approach to characterize the functional protein complement of membranous organelles in two Caenorhabditis species: C. elegans and C. remanei.<h4>Results</h4>We identify distinct prote ...[more]

PMID: 30086719

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Project description:PurposeThe advent of proteomics provides new opportunities to investigate the molecular mechanisms underlying male infertility. The selection of relevant targets based on a single analysis is not always feasible, due to the growing number of proteomic studies with conflicting results. Thus, this study aimed to systematically review investigations comparing the sperm proteome of normozoospermic and infertile men to define a panel of proteins with the potential to be used to evaluate sperm quality.Materials and methodsA literature search was conducted on PubMed, Web of Science, and Scopus databases following the PRISMA guidelines. To identify proteins systematically reported, first the studies were divided by condition into four groups (asthenozoospermia, low motility, unexplained infertility, and infertility related to risk factors) and then, all studies were analysed simultaneously (poor sperm quality). To gain molecular insights regarding identified proteins, additional searches were performed within the Human Protein Atlas, Mouse Genome Informatics, UniProt, and PubMed databases.ResultsThirty-two studies were included and divided into 4 sub-analysis groups. A total of 2752 proteins were collected, of which 38, 1, 3 and 2 were indicated as potential markers for asthenozoospermia, low motility, unexplained infertility and infertility related to risk factors, respectively, and 58 for poor sperm quality. Among the identified proteins, ACR, ACRBP, ACRV1, ACTL9, AKAP4, ATG3, CCT2, CFAP276, CFAP52, FAM209A, GGH, HPRT1, LYZL4, PRDX6, PRSS37, REEP6, ROPN1B, SPACA3, SOD1, SPEM1, SPESP1, SPINK2, TEKT5, and ZPBP were highlighted due to their roles in male reproductive tissues, association with infertility phenotypes or participation in specific biological functions in spermatozoa.ConclusionsSperm proteomics allows the identification of protein markers with the potential to overcome limitations in male infertility diagnosis and to understand changes in sperm function at the molecular level. This study provides a reliable list of systematically reported proteins that could be potential targets for further basic and clinical studies.

Dataset Information

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

Publications

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

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