The EGF-motif-containing protein SPE-36 is a secreted sperm protein required for fertilization in C. elegans

Amber R. Krauchunas; Matthew R. Marcello; A'Maya Looper; Xue Mei; Emily Putiri; Gunasekaran Singaravelu; Iqra I. Ahmed; Andrew Singson

doi:10.1016/j.cub.2023.06.051

The EGF-motif-containing protein SPE-36 is a secreted sperm protein required for fertilization in C. elegans

Amber R. Krauchunas, Matthew R. Marcello, A'Maya Looper, Xue Mei, Emily Putiri, Gunasekaran Singaravelu, Iqra I. Ahmed, Andrew Singson

Waksman Institute of Microbiology

Rutgers, The State University

Research output: Contribution to journal › Article › peer-review

Abstract

Identified through forward genetics, spe-9 was the first gene to be identified in C. elegans as necessary for fertilization.1 Since then, genetic screens in C. elegans have led to the identification of nine additional sperm genes necessary for fertilization (including spe-51 reported by Mei et al.2 and the spe-36 gene reported here).3,4,5,6,7,8,9 This includes spe-45, which encodes an immunoglobulin-containing protein similar to the mammalian protein IZUMO1, and spe-42 and spe-49, which are homologous to vertebrate DCST2 and DCST1, respectively.4,7,8,10,11,12,13 Mutations in any one of these genes result in healthy adult animals that are sterile. Sperm from these mutants have normal morphology, migrate to and maintain their position at the site of fertilization in the reproductive tract, and make contact with eggs but fail to fertilize the eggs. This same phenotype is observed in mammals lacking Izumo1, Spaca6, Tmem95, Sof1, FIMP, or Dcst1 and Dcst2.10,14,15,16,17,18,19 Here we report the discovery of SPE-36 as a sperm-derived secreted protein that is necessary for fertilization. Mutations in the Caenorhabditis elegans spe-36 gene result in a sperm-specific fertilization defect. Sperm from spe-36 mutants look phenotypically normal, are motile, and can migrate to the site of fertilization. However, sperm that do not produce SPE-36 protein cannot fertilize. Surprisingly, spe-36 encodes a secreted EGF-motif-containing protein that functions cell autonomously. The genetic requirement for secreted sperm-derived proteins for fertilization sheds new light on the complex nature of fertilization and represents a paradigm-shifting discovery in the molecular understanding of fertilization.

Original language	American English
Pages (from-to)	3056-3064
Number of pages	9
Journal	Current biology : CB
Volume	33
Issue number	14
DOIs	https://doi.org/10.1016/j.cub.2023.06.051
State	Published - Jul 24 2023

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology
General Agricultural and Biological Sciences

Keywords

C. elegans
fertilization
fertilization synapse
oocyte
secreted protein
spe-36
sperm

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10.1016/j.cub.2023.06.051

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title = "The EGF-motif-containing protein SPE-36 is a secreted sperm protein required for fertilization in C. elegans",

abstract = "Identified through forward genetics, spe-9 was the first gene to be identified in C. elegans as necessary for fertilization.1 Since then, genetic screens in C. elegans have led to the identification of nine additional sperm genes necessary for fertilization (including spe-51 reported by Mei et al.2 and the spe-36 gene reported here).3,4,5,6,7,8,9 This includes spe-45, which encodes an immunoglobulin-containing protein similar to the mammalian protein IZUMO1, and spe-42 and spe-49, which are homologous to vertebrate DCST2 and DCST1, respectively.4,7,8,10,11,12,13 Mutations in any one of these genes result in healthy adult animals that are sterile. Sperm from these mutants have normal morphology, migrate to and maintain their position at the site of fertilization in the reproductive tract, and make contact with eggs but fail to fertilize the eggs. This same phenotype is observed in mammals lacking Izumo1, Spaca6, Tmem95, Sof1, FIMP, or Dcst1 and Dcst2.10,14,15,16,17,18,19 Here we report the discovery of SPE-36 as a sperm-derived secreted protein that is necessary for fertilization. Mutations in the Caenorhabditis elegans spe-36 gene result in a sperm-specific fertilization defect. Sperm from spe-36 mutants look phenotypically normal, are motile, and can migrate to the site of fertilization. However, sperm that do not produce SPE-36 protein cannot fertilize. Surprisingly, spe-36 encodes a secreted EGF-motif-containing protein that functions cell autonomously. The genetic requirement for secreted sperm-derived proteins for fertilization sheds new light on the complex nature of fertilization and represents a paradigm-shifting discovery in the molecular understanding of fertilization.",

keywords = "C. elegans, fertilization, fertilization synapse, oocyte, secreted protein, spe-36, sperm",

author = "Krauchunas, {Amber R.} and Marcello, {Matthew R.} and A'Maya Looper and Xue Mei and Emily Putiri and Gunasekaran Singaravelu and Ahmed, {Iqra I.} and Andrew Singson",

year = "2023",

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doi = "10.1016/j.cub.2023.06.051",

language = "American English",

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journal = "Current biology : CB",

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T1 - The EGF-motif-containing protein SPE-36 is a secreted sperm protein required for fertilization in C. elegans

AU - Krauchunas, Amber R.

AU - Marcello, Matthew R.

AU - Looper, A'Maya

AU - Mei, Xue

AU - Putiri, Emily

AU - Singaravelu, Gunasekaran

AU - Ahmed, Iqra I.

AU - Singson, Andrew

PY - 2023/7/24

Y1 - 2023/7/24

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AB - Identified through forward genetics, spe-9 was the first gene to be identified in C. elegans as necessary for fertilization.1 Since then, genetic screens in C. elegans have led to the identification of nine additional sperm genes necessary for fertilization (including spe-51 reported by Mei et al.2 and the spe-36 gene reported here).3,4,5,6,7,8,9 This includes spe-45, which encodes an immunoglobulin-containing protein similar to the mammalian protein IZUMO1, and spe-42 and spe-49, which are homologous to vertebrate DCST2 and DCST1, respectively.4,7,8,10,11,12,13 Mutations in any one of these genes result in healthy adult animals that are sterile. Sperm from these mutants have normal morphology, migrate to and maintain their position at the site of fertilization in the reproductive tract, and make contact with eggs but fail to fertilize the eggs. This same phenotype is observed in mammals lacking Izumo1, Spaca6, Tmem95, Sof1, FIMP, or Dcst1 and Dcst2.10,14,15,16,17,18,19 Here we report the discovery of SPE-36 as a sperm-derived secreted protein that is necessary for fertilization. Mutations in the Caenorhabditis elegans spe-36 gene result in a sperm-specific fertilization defect. Sperm from spe-36 mutants look phenotypically normal, are motile, and can migrate to the site of fertilization. However, sperm that do not produce SPE-36 protein cannot fertilize. Surprisingly, spe-36 encodes a secreted EGF-motif-containing protein that functions cell autonomously. The genetic requirement for secreted sperm-derived proteins for fertilization sheds new light on the complex nature of fertilization and represents a paradigm-shifting discovery in the molecular understanding of fertilization.

KW - C. elegans

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KW - fertilization synapse

KW - oocyte

KW - secreted protein

KW - spe-36

KW - sperm

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JO - Current biology : CB

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The EGF-motif-containing protein SPE-36 is a secreted sperm protein required for fertilization in C. elegans

Abstract

ASJC Scopus subject areas

Keywords

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