Saai Suryanarayanan , Dawn S. Chen , Yamei Zuo , Elizabeth J. Gleason , Zhaorong Zhu , Steven W. L'Hernault , Amber Krauchunas , Andrew Singson
{"title":"编码棕榈酰转移酶的秀丽隐杆线虫spe-21基因是精子发生所必需的","authors":"Saai Suryanarayanan , Dawn S. Chen , Yamei Zuo , Elizabeth J. Gleason , Zhaorong Zhu , Steven W. L'Hernault , Amber Krauchunas , Andrew Singson","doi":"10.1016/j.ydbio.2025.08.003","DOIUrl":null,"url":null,"abstract":"<div><div>In most animals, spermatids that are produced must further differentiate into fertilization-competent spermatozoa after completing meiosis. In <em>Caenorhabditis elegans</em>, this process is known as spermiogenesis or spermatid activation and it results in the transformation of round, non-motile spermatids into amoeboid, motile spermatozoa. Spermatid activation in <em>C. elegans</em> is also associated with the fusion of Golgi-derived vesicles called the <u>m</u>embranous <u>o</u>rganelles (MOs) with the plasma membrane. This fusion process is required for producing a fertilization-competent surface on the sperm by placing MO-carried, resident proteins onto the spermatozoon membrane. We have identified, cloned, and characterized the role of <em>spe-21</em>, also designated as <em>dhhc-5,</em> during both hermaphrodite and male spermatid activation. Putative <em>spe-21</em> null mutant worms are severely sub-fertile at all studied growth temperatures. <em>spe-21</em> mutant spermatids fail to activate either <em>in vivo</em> or <em>in vitro</em> after treatment with known chemical activators. We have found that <em>spe-21</em> is necessary for MO fusion and pseudopod formation in spermatids. The <em>spe-21</em> gene encodes a predicted four pass transmembrane protein with a conserved Asp-His-His-Cys (DHHC) tetrapeptide zinc finger motif embedded in a cysteine rich region (DHHC-CRD type zinc finger motif). Generally, proteins with DHHC-CRD motifs catalyze the post-translational addition of palmitate to their protein substrates and are called palmitoyltransferases or <u>p</u>almitoyl<u>a</u>cyl<u>t</u>ransferases (PATs). We also found that mNeonGreen-tagged SPE-21 localizes to the MOs in spermatids. Together, our findings show that SPE-21 is an MO localized palmitoyltransferase required for proper spermatid activation and creation of fertilization-competent spermatozoa.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"527 ","pages":"Pages 77-90"},"PeriodicalIF":2.1000,"publicationDate":"2025-08-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"The Caenorhabditis elegans spe-21 gene that encodes a palmitoyltransferase is necessary for spermiogenesis\",\"authors\":\"Saai Suryanarayanan , Dawn S. Chen , Yamei Zuo , Elizabeth J. Gleason , Zhaorong Zhu , Steven W. L'Hernault , Amber Krauchunas , Andrew Singson\",\"doi\":\"10.1016/j.ydbio.2025.08.003\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<div><div>In most animals, spermatids that are produced must further differentiate into fertilization-competent spermatozoa after completing meiosis. In <em>Caenorhabditis elegans</em>, this process is known as spermiogenesis or spermatid activation and it results in the transformation of round, non-motile spermatids into amoeboid, motile spermatozoa. Spermatid activation in <em>C. elegans</em> is also associated with the fusion of Golgi-derived vesicles called the <u>m</u>embranous <u>o</u>rganelles (MOs) with the plasma membrane. This fusion process is required for producing a fertilization-competent surface on the sperm by placing MO-carried, resident proteins onto the spermatozoon membrane. We have identified, cloned, and characterized the role of <em>spe-21</em>, also designated as <em>dhhc-5,</em> during both hermaphrodite and male spermatid activation. Putative <em>spe-21</em> null mutant worms are severely sub-fertile at all studied growth temperatures. <em>spe-21</em> mutant spermatids fail to activate either <em>in vivo</em> or <em>in vitro</em> after treatment with known chemical activators. We have found that <em>spe-21</em> is necessary for MO fusion and pseudopod formation in spermatids. The <em>spe-21</em> gene encodes a predicted four pass transmembrane protein with a conserved Asp-His-His-Cys (DHHC) tetrapeptide zinc finger motif embedded in a cysteine rich region (DHHC-CRD type zinc finger motif). Generally, proteins with DHHC-CRD motifs catalyze the post-translational addition of palmitate to their protein substrates and are called palmitoyltransferases or <u>p</u>almitoyl<u>a</u>cyl<u>t</u>ransferases (PATs). We also found that mNeonGreen-tagged SPE-21 localizes to the MOs in spermatids. Together, our findings show that SPE-21 is an MO localized palmitoyltransferase required for proper spermatid activation and creation of fertilization-competent spermatozoa.</div></div>\",\"PeriodicalId\":11070,\"journal\":{\"name\":\"Developmental biology\",\"volume\":\"527 \",\"pages\":\"Pages 77-90\"},\"PeriodicalIF\":2.1000,\"publicationDate\":\"2025-08-08\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Developmental biology\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://www.sciencedirect.com/science/article/pii/S0012160625002143\",\"RegionNum\":3,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"DEVELOPMENTAL BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Developmental biology","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0012160625002143","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"DEVELOPMENTAL BIOLOGY","Score":null,"Total":0}
The Caenorhabditis elegans spe-21 gene that encodes a palmitoyltransferase is necessary for spermiogenesis
In most animals, spermatids that are produced must further differentiate into fertilization-competent spermatozoa after completing meiosis. In Caenorhabditis elegans, this process is known as spermiogenesis or spermatid activation and it results in the transformation of round, non-motile spermatids into amoeboid, motile spermatozoa. Spermatid activation in C. elegans is also associated with the fusion of Golgi-derived vesicles called the membranous organelles (MOs) with the plasma membrane. This fusion process is required for producing a fertilization-competent surface on the sperm by placing MO-carried, resident proteins onto the spermatozoon membrane. We have identified, cloned, and characterized the role of spe-21, also designated as dhhc-5, during both hermaphrodite and male spermatid activation. Putative spe-21 null mutant worms are severely sub-fertile at all studied growth temperatures. spe-21 mutant spermatids fail to activate either in vivo or in vitro after treatment with known chemical activators. We have found that spe-21 is necessary for MO fusion and pseudopod formation in spermatids. The spe-21 gene encodes a predicted four pass transmembrane protein with a conserved Asp-His-His-Cys (DHHC) tetrapeptide zinc finger motif embedded in a cysteine rich region (DHHC-CRD type zinc finger motif). Generally, proteins with DHHC-CRD motifs catalyze the post-translational addition of palmitate to their protein substrates and are called palmitoyltransferases or palmitoylacyltransferases (PATs). We also found that mNeonGreen-tagged SPE-21 localizes to the MOs in spermatids. Together, our findings show that SPE-21 is an MO localized palmitoyltransferase required for proper spermatid activation and creation of fertilization-competent spermatozoa.
期刊介绍:
Developmental Biology (DB) publishes original research on mechanisms of development, differentiation, and growth in animals and plants at the molecular, cellular, genetic and evolutionary levels. Areas of particular emphasis include transcriptional control mechanisms, embryonic patterning, cell-cell interactions, growth factors and signal transduction, and regulatory hierarchies in developing plants and animals.