Sphingomyelin Synthase 1 Is Essential for Male Fertility in Mice
Sphingolipids and the derived gangliosides have critical functions in spermatogenesis, thus mutations in genes involved in sphingolipid biogenesis are often associated with male infertility. We have generated a transgenic mouse line carrying an insertion in the sphingomyelin synthase gene Sms1, the...
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| creator | Wittmann, Anke Grimm, Marcus O W Scherthan, Harry Horsch, Marion Beckers, Johannes Fuchs, Helmut Gailus-Durner, Valerie Hrabě de Angelis, Martin Ford, Steven J Burton, Neal C Razansky, Daniel Trümbach, Dietrich Aichler, Michaela Walch, Axel Karl Calzada-Wack, Julia Neff, Frauke Wurst, Wolfgang Hartmann, Tobias Floss, Thomas |
| description | Sphingolipids and the derived gangliosides have critical functions in spermatogenesis, thus mutations in genes involved in sphingolipid biogenesis are often associated with male infertility. We have generated a transgenic mouse line carrying an insertion in the sphingomyelin synthase gene Sms1, the enzyme which generates sphingomyelin species in the Golgi apparatus. We describe the spermatogenesis defect of Sms1-/- mice, which is characterized by sloughing of spermatocytes and spermatids, causing progressive infertility of male homozygotes. Lipid profiling revealed a reduction in several long chain unsaturated phosphatidylcholins, lysophosphatidylcholins and sphingolipids in the testes of mutants. Multi-Spectral Optoacoustic Tomography indicated blood-testis barrier dysfunction. A supplementary diet of the essential omega-3 docosahexaenoic acid and eicosapentaenoic acid diminished germ cell sloughing from the seminiferous epithelium and restored spermatogenesis and fertility in 50% of previously infertile mutants. Our findings indicate that SMS1 has a wider than anticipated role in testis polyunsaturated fatty acid homeostasis and for male fertility. |
| doi_str_mv | 10.1371/journal.pone.0164298 |
| format | Article |
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We have generated a transgenic mouse line carrying an insertion in the sphingomyelin synthase gene Sms1, the enzyme which generates sphingomyelin species in the Golgi apparatus. We describe the spermatogenesis defect of Sms1-/- mice, which is characterized by sloughing of spermatocytes and spermatids, causing progressive infertility of male homozygotes. Lipid profiling revealed a reduction in several long chain unsaturated phosphatidylcholins, lysophosphatidylcholins and sphingolipids in the testes of mutants. Multi-Spectral Optoacoustic Tomography indicated blood-testis barrier dysfunction. A supplementary diet of the essential omega-3 docosahexaenoic acid and eicosapentaenoic acid diminished germ cell sloughing from the seminiferous epithelium and restored spermatogenesis and fertility in 50% of previously infertile mutants. Our findings indicate that SMS1 has a wider than anticipated role in testis polyunsaturated fatty acid homeostasis and for male fertility.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0164298</identifier><identifier>PMID: 27788151</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Aging - physiology ; Alternative Splicing ; Animals ; Apoptosis ; Biology and Life Sciences ; Docosahexaenoic acid ; Eicosapentaenoic acid ; Enzymes ; Epididymis - drug effects ; Epididymis - metabolism ; Epithelium ; Evolution ; Fatty acids ; Fatty Acids, Omega-3 - biosynthesis ; Fatty Acids, Omega-3 - pharmacology ; Fertility ; Fertility - drug effects ; Gangliosides ; Genetic aspects ; Golgi apparatus ; Homeostasis ; Homozygotes ; Infertility ; Infertility, Male - enzymology ; Lipid Metabolism - drug effects ; Lipids ; Male ; Medical imaging ; Medicine and Health Sciences ; Mice ; Mutagenesis, Insertional ; Mutants ; Mutation ; Omega 3 fatty acids ; Pathology ; Plasma ; Polyunsaturated fatty acids ; Promoter Regions, Genetic - genetics ; Proteins ; Research and Analysis Methods ; Rodents ; Spermatids ; Spermatocytes ; Spermatogenesis ; Spermatogenesis - drug effects ; Sphingolipids ; Sphingomyelin ; Testes ; Testis - drug effects ; Testis - metabolism ; Transferases (Other Substituted Phosphate Groups) - genetics ; Transferases (Other Substituted Phosphate Groups) - metabolism ; Transgenic mice ; Unsaturated fatty acids</subject><ispartof>PloS one, 2016-10, Vol.11 (10), p.e0164298-e0164298</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Wittmann et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2016 Wittmann et al 2016 Wittmann et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c725t-f7e53b3883de798d93009f529fc90f1b81beda4c14f563294ee4541fbe2c60183</citedby><cites>FETCH-LOGICAL-c725t-f7e53b3883de798d93009f529fc90f1b81beda4c14f563294ee4541fbe2c60183</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5082796/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5082796/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27788151$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wittmann, Anke</creatorcontrib><creatorcontrib>Grimm, Marcus O W</creatorcontrib><creatorcontrib>Scherthan, Harry</creatorcontrib><creatorcontrib>Horsch, Marion</creatorcontrib><creatorcontrib>Beckers, Johannes</creatorcontrib><creatorcontrib>Fuchs, Helmut</creatorcontrib><creatorcontrib>Gailus-Durner, Valerie</creatorcontrib><creatorcontrib>Hrabě de Angelis, Martin</creatorcontrib><creatorcontrib>Ford, Steven J</creatorcontrib><creatorcontrib>Burton, Neal C</creatorcontrib><creatorcontrib>Razansky, Daniel</creatorcontrib><creatorcontrib>Trümbach, Dietrich</creatorcontrib><creatorcontrib>Aichler, Michaela</creatorcontrib><creatorcontrib>Walch, Axel Karl</creatorcontrib><creatorcontrib>Calzada-Wack, Julia</creatorcontrib><creatorcontrib>Neff, Frauke</creatorcontrib><creatorcontrib>Wurst, Wolfgang</creatorcontrib><creatorcontrib>Hartmann, Tobias</creatorcontrib><creatorcontrib>Floss, Thomas</creatorcontrib><title>Sphingomyelin Synthase 1 Is Essential for Male Fertility in Mice</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Sphingolipids and the derived gangliosides have critical functions in spermatogenesis, thus mutations in genes involved in sphingolipid biogenesis are often associated with male infertility. We have generated a transgenic mouse line carrying an insertion in the sphingomyelin synthase gene Sms1, the enzyme which generates sphingomyelin species in the Golgi apparatus. We describe the spermatogenesis defect of Sms1-/- mice, which is characterized by sloughing of spermatocytes and spermatids, causing progressive infertility of male homozygotes. Lipid profiling revealed a reduction in several long chain unsaturated phosphatidylcholins, lysophosphatidylcholins and sphingolipids in the testes of mutants. Multi-Spectral Optoacoustic Tomography indicated blood-testis barrier dysfunction. A supplementary diet of the essential omega-3 docosahexaenoic acid and eicosapentaenoic acid diminished germ cell sloughing from the seminiferous epithelium and restored spermatogenesis and fertility in 50% of previously infertile mutants. Our findings indicate that SMS1 has a wider than anticipated role in testis polyunsaturated fatty acid homeostasis and for male fertility.</description><subject>Aging - physiology</subject><subject>Alternative Splicing</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Biology and Life Sciences</subject><subject>Docosahexaenoic acid</subject><subject>Eicosapentaenoic acid</subject><subject>Enzymes</subject><subject>Epididymis - drug effects</subject><subject>Epididymis - metabolism</subject><subject>Epithelium</subject><subject>Evolution</subject><subject>Fatty acids</subject><subject>Fatty Acids, Omega-3 - biosynthesis</subject><subject>Fatty Acids, Omega-3 - pharmacology</subject><subject>Fertility</subject><subject>Fertility - drug effects</subject><subject>Gangliosides</subject><subject>Genetic aspects</subject><subject>Golgi apparatus</subject><subject>Homeostasis</subject><subject>Homozygotes</subject><subject>Infertility</subject><subject>Infertility, Male - enzymology</subject><subject>Lipid Metabolism - drug effects</subject><subject>Lipids</subject><subject>Male</subject><subject>Medical imaging</subject><subject>Medicine and Health Sciences</subject><subject>Mice</subject><subject>Mutagenesis, Insertional</subject><subject>Mutants</subject><subject>Mutation</subject><subject>Omega 3 fatty acids</subject><subject>Pathology</subject><subject>Plasma</subject><subject>Polyunsaturated fatty acids</subject><subject>Promoter Regions, Genetic - genetics</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>Rodents</subject><subject>Spermatids</subject><subject>Spermatocytes</subject><subject>Spermatogenesis</subject><subject>Spermatogenesis - drug effects</subject><subject>Sphingolipids</subject><subject>Sphingomyelin</subject><subject>Testes</subject><subject>Testis - drug effects</subject><subject>Testis - metabolism</subject><subject>Transferases (Other Substituted Phosphate Groups) - genetics</subject><subject>Transferases (Other Substituted Phosphate Groups) - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wittmann, Anke</au><au>Grimm, Marcus O W</au><au>Scherthan, Harry</au><au>Horsch, Marion</au><au>Beckers, Johannes</au><au>Fuchs, Helmut</au><au>Gailus-Durner, Valerie</au><au>Hrabě de Angelis, Martin</au><au>Ford, Steven J</au><au>Burton, Neal C</au><au>Razansky, Daniel</au><au>Trümbach, Dietrich</au><au>Aichler, Michaela</au><au>Walch, Axel Karl</au><au>Calzada-Wack, Julia</au><au>Neff, Frauke</au><au>Wurst, Wolfgang</au><au>Hartmann, Tobias</au><au>Floss, Thomas</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Sphingomyelin Synthase 1 Is Essential for Male Fertility in Mice</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-10-27</date><risdate>2016</risdate><volume>11</volume><issue>10</issue><spage>e0164298</spage><epage>e0164298</epage><pages>e0164298-e0164298</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Sphingolipids and the derived gangliosides have critical functions in spermatogenesis, thus mutations in genes involved in sphingolipid biogenesis are often associated with male infertility. We have generated a transgenic mouse line carrying an insertion in the sphingomyelin synthase gene Sms1, the enzyme which generates sphingomyelin species in the Golgi apparatus. We describe the spermatogenesis defect of Sms1-/- mice, which is characterized by sloughing of spermatocytes and spermatids, causing progressive infertility of male homozygotes. Lipid profiling revealed a reduction in several long chain unsaturated phosphatidylcholins, lysophosphatidylcholins and sphingolipids in the testes of mutants. Multi-Spectral Optoacoustic Tomography indicated blood-testis barrier dysfunction. A supplementary diet of the essential omega-3 docosahexaenoic acid and eicosapentaenoic acid diminished germ cell sloughing from the seminiferous epithelium and restored spermatogenesis and fertility in 50% of previously infertile mutants. Our findings indicate that SMS1 has a wider than anticipated role in testis polyunsaturated fatty acid homeostasis and for male fertility.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27788151</pmid><doi>10.1371/journal.pone.0164298</doi><tpages>e0164298</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2016-10, Vol.11 (10), p.e0164298-e0164298 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1833129968 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Aging - physiology Alternative Splicing Animals Apoptosis Biology and Life Sciences Docosahexaenoic acid Eicosapentaenoic acid Enzymes Epididymis - drug effects Epididymis - metabolism Epithelium Evolution Fatty acids Fatty Acids, Omega-3 - biosynthesis Fatty Acids, Omega-3 - pharmacology Fertility Fertility - drug effects Gangliosides Genetic aspects Golgi apparatus Homeostasis Homozygotes Infertility Infertility, Male - enzymology Lipid Metabolism - drug effects Lipids Male Medical imaging Medicine and Health Sciences Mice Mutagenesis, Insertional Mutants Mutation Omega 3 fatty acids Pathology Plasma Polyunsaturated fatty acids Promoter Regions, Genetic - genetics Proteins Research and Analysis Methods Rodents Spermatids Spermatocytes Spermatogenesis Spermatogenesis - drug effects Sphingolipids Sphingomyelin Testes Testis - drug effects Testis - metabolism Transferases (Other Substituted Phosphate Groups) - genetics Transferases (Other Substituted Phosphate Groups) - metabolism Transgenic mice Unsaturated fatty acids |
| title | Sphingomyelin Synthase 1 Is Essential for Male Fertility in Mice |
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