Redox regulation by TXNRD3 during epididymal maturation underlies capacitation-associated mitochondrial activity and sperm motility in mice
During epididymal transit, redox remodeling protects mammalian spermatozoa, preparing them for survival in the subsequent journey to fertilization. However, molecular mechanisms of redox regulation in sperm development and maturation remain largely elusive. In this study, we report that thioredoxin-...
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Veröffentlicht in: | The Journal of biological chemistry 2022-07, Vol.298 (7), p.102077-102077, Article 102077 |
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creator | Wang, Huafeng Dou, Qianhui Jeong, Kyung Jo Choi, Jungmin Gladyshev, Vadim N. Chung, Jean-Ju |
description | During epididymal transit, redox remodeling protects mammalian spermatozoa, preparing them for survival in the subsequent journey to fertilization. However, molecular mechanisms of redox regulation in sperm development and maturation remain largely elusive. In this study, we report that thioredoxin-glutathione reductase (TXNRD3), a thioredoxin reductase family member particularly abundant in elongating spermatids at the site of mitochondrial sheath formation, regulates redox homeostasis to support male fertility. Using Txnrd3−/− mice, our biochemical, ultrastructural, and live cell imaging analyses revealed impairments in sperm morphology and motility under conditions of TXNRD3 deficiency. We find that mitochondria develop more defined cristae during capacitation in wildtype sperm. Furthermore, we show that absence of TXNRD3 alters thiol redox status in both the head and tail during sperm maturation and capacitation, resulting in defective mitochondrial ultrastructure and activity under capacitating conditions. These findings provide insights into molecular mechanisms of redox homeostasis and bioenergetics during sperm maturation, capacitation, and fertilization. |
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However, molecular mechanisms of redox regulation in sperm development and maturation remain largely elusive. In this study, we report that thioredoxin-glutathione reductase (TXNRD3), a thioredoxin reductase family member particularly abundant in elongating spermatids at the site of mitochondrial sheath formation, regulates redox homeostasis to support male fertility. Using Txnrd3−/− mice, our biochemical, ultrastructural, and live cell imaging analyses revealed impairments in sperm morphology and motility under conditions of TXNRD3 deficiency. We find that mitochondria develop more defined cristae during capacitation in wildtype sperm. Furthermore, we show that absence of TXNRD3 alters thiol redox status in both the head and tail during sperm maturation and capacitation, resulting in defective mitochondrial ultrastructure and activity under capacitating conditions. These findings provide insights into molecular mechanisms of redox homeostasis and bioenergetics during sperm maturation, capacitation, and fertilization.</description><identifier>ISSN: 0021-9258</identifier><identifier>EISSN: 1083-351X</identifier><identifier>DOI: 10.1016/j.jbc.2022.102077</identifier><identifier>PMID: 35643315</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Epididymis ; Male ; male fertility ; Mammals ; Mice ; Mitochondria - metabolism ; mitochondrial function ; Oxidation-Reduction ; redox homeostasis ; Semen ; Sperm Capacitation - genetics ; Sperm Motility - physiology ; Spermatozoa - metabolism ; thioredoxin glutathione reductase ; Thioredoxin-Disulfide Reductase - metabolism ; TXNRD3 ; ultrastructure</subject><ispartof>The Journal of biological chemistry, 2022-07, Vol.298 (7), p.102077-102077, Article 102077</ispartof><rights>2022 The Authors</rights><rights>Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.</rights><rights>2022 The Authors 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c451t-d542a1cd1a735fdd0fb9c2c509bf3ae16432bd8d2745564744dbfd6d1f3031a23</citedby><cites>FETCH-LOGICAL-c451t-d542a1cd1a735fdd0fb9c2c509bf3ae16432bd8d2745564744dbfd6d1f3031a23</cites><orcidid>0000-0001-5210-9962 ; 0000-0002-7326-4379 ; 0000-0002-8614-0973 ; 0000-0001-8018-1355</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9218152/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9218152/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35643315$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Huafeng</creatorcontrib><creatorcontrib>Dou, Qianhui</creatorcontrib><creatorcontrib>Jeong, Kyung Jo</creatorcontrib><creatorcontrib>Choi, Jungmin</creatorcontrib><creatorcontrib>Gladyshev, Vadim N.</creatorcontrib><creatorcontrib>Chung, Jean-Ju</creatorcontrib><title>Redox regulation by TXNRD3 during epididymal maturation underlies capacitation-associated mitochondrial activity and sperm motility in mice</title><title>The Journal of biological chemistry</title><addtitle>J Biol Chem</addtitle><description>During epididymal transit, redox remodeling protects mammalian spermatozoa, preparing them for survival in the subsequent journey to fertilization. However, molecular mechanisms of redox regulation in sperm development and maturation remain largely elusive. In this study, we report that thioredoxin-glutathione reductase (TXNRD3), a thioredoxin reductase family member particularly abundant in elongating spermatids at the site of mitochondrial sheath formation, regulates redox homeostasis to support male fertility. Using Txnrd3−/− mice, our biochemical, ultrastructural, and live cell imaging analyses revealed impairments in sperm morphology and motility under conditions of TXNRD3 deficiency. We find that mitochondria develop more defined cristae during capacitation in wildtype sperm. Furthermore, we show that absence of TXNRD3 alters thiol redox status in both the head and tail during sperm maturation and capacitation, resulting in defective mitochondrial ultrastructure and activity under capacitating conditions. These findings provide insights into molecular mechanisms of redox homeostasis and bioenergetics during sperm maturation, capacitation, and fertilization.</description><subject>Animals</subject><subject>Epididymis</subject><subject>Male</subject><subject>male fertility</subject><subject>Mammals</subject><subject>Mice</subject><subject>Mitochondria - metabolism</subject><subject>mitochondrial function</subject><subject>Oxidation-Reduction</subject><subject>redox homeostasis</subject><subject>Semen</subject><subject>Sperm Capacitation - genetics</subject><subject>Sperm Motility - physiology</subject><subject>Spermatozoa - metabolism</subject><subject>thioredoxin glutathione reductase</subject><subject>Thioredoxin-Disulfide Reductase - metabolism</subject><subject>TXNRD3</subject><subject>ultrastructure</subject><issn>0021-9258</issn><issn>1083-351X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kcuKFDEUhoMoTjv6AG4kSzfV5lJXBEHGKwwKwwizC6nkVM9pqpIySTX2M_jSpq1x0I3ZhJx8_39y8hPynLMtZ7x-td_ue7MVTIh8FqxpHpANZ60sZMVvHpINY4IXnajaM_Ikxj3Lq-z4Y3Imq7qUklcb8vMKrP9BA-yWUSf0jvZHen3z5eqdpHYJ6HYUZrRoj5Me6aTTElZscRbCiBCp0bM2mH6XCx2jN6gTWDph8ubWOxswS7VJeMB0pNpZGmcIE518wvFUQpdhA0_Jo0GPEZ7d7efk24f31xefisuvHz9fvL0sTFnxVNiqFJoby3Ujq8FaNvSdEaZiXT9IDTyPJnrbWtGUVZ6zKUvbD7a2fJBMci3kOXmz-s5LP4E14FLQo5oDTjocldeo_r1xeKt2_qA6wVtenQxe3hkE_32BmNSE0cA4agd-iUrUjZC8bWqWUb6iJvgYAwz3bThTpxDVXuUQ1SlEtYaYNS_-ft-94k9qGXi9ApB_6YAQVDQIzoDFACYp6_E_9r8A75mxnA</recordid><startdate>20220701</startdate><enddate>20220701</enddate><creator>Wang, Huafeng</creator><creator>Dou, Qianhui</creator><creator>Jeong, Kyung Jo</creator><creator>Choi, Jungmin</creator><creator>Gladyshev, Vadim N.</creator><creator>Chung, Jean-Ju</creator><general>Elsevier Inc</general><general>American Society for Biochemistry and Molecular Biology</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-5210-9962</orcidid><orcidid>https://orcid.org/0000-0002-7326-4379</orcidid><orcidid>https://orcid.org/0000-0002-8614-0973</orcidid><orcidid>https://orcid.org/0000-0001-8018-1355</orcidid></search><sort><creationdate>20220701</creationdate><title>Redox regulation by TXNRD3 during epididymal maturation underlies capacitation-associated mitochondrial activity and sperm motility in mice</title><author>Wang, Huafeng ; Dou, Qianhui ; Jeong, Kyung Jo ; Choi, Jungmin ; Gladyshev, Vadim N. ; Chung, Jean-Ju</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c451t-d542a1cd1a735fdd0fb9c2c509bf3ae16432bd8d2745564744dbfd6d1f3031a23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Animals</topic><topic>Epididymis</topic><topic>Male</topic><topic>male fertility</topic><topic>Mammals</topic><topic>Mice</topic><topic>Mitochondria - metabolism</topic><topic>mitochondrial function</topic><topic>Oxidation-Reduction</topic><topic>redox homeostasis</topic><topic>Semen</topic><topic>Sperm Capacitation - genetics</topic><topic>Sperm Motility - physiology</topic><topic>Spermatozoa - metabolism</topic><topic>thioredoxin glutathione reductase</topic><topic>Thioredoxin-Disulfide Reductase - metabolism</topic><topic>TXNRD3</topic><topic>ultrastructure</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Huafeng</creatorcontrib><creatorcontrib>Dou, Qianhui</creatorcontrib><creatorcontrib>Jeong, Kyung Jo</creatorcontrib><creatorcontrib>Choi, Jungmin</creatorcontrib><creatorcontrib>Gladyshev, Vadim N.</creatorcontrib><creatorcontrib>Chung, Jean-Ju</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of biological chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Huafeng</au><au>Dou, Qianhui</au><au>Jeong, Kyung Jo</au><au>Choi, Jungmin</au><au>Gladyshev, Vadim N.</au><au>Chung, Jean-Ju</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Redox regulation by TXNRD3 during epididymal maturation underlies capacitation-associated mitochondrial activity and sperm motility in mice</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2022-07-01</date><risdate>2022</risdate><volume>298</volume><issue>7</issue><spage>102077</spage><epage>102077</epage><pages>102077-102077</pages><artnum>102077</artnum><issn>0021-9258</issn><eissn>1083-351X</eissn><abstract>During epididymal transit, redox remodeling protects mammalian spermatozoa, preparing them for survival in the subsequent journey to fertilization. However, molecular mechanisms of redox regulation in sperm development and maturation remain largely elusive. In this study, we report that thioredoxin-glutathione reductase (TXNRD3), a thioredoxin reductase family member particularly abundant in elongating spermatids at the site of mitochondrial sheath formation, regulates redox homeostasis to support male fertility. Using Txnrd3−/− mice, our biochemical, ultrastructural, and live cell imaging analyses revealed impairments in sperm morphology and motility under conditions of TXNRD3 deficiency. We find that mitochondria develop more defined cristae during capacitation in wildtype sperm. Furthermore, we show that absence of TXNRD3 alters thiol redox status in both the head and tail during sperm maturation and capacitation, resulting in defective mitochondrial ultrastructure and activity under capacitating conditions. 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subjects | Animals Epididymis Male male fertility Mammals Mice Mitochondria - metabolism mitochondrial function Oxidation-Reduction redox homeostasis Semen Sperm Capacitation - genetics Sperm Motility - physiology Spermatozoa - metabolism thioredoxin glutathione reductase Thioredoxin-Disulfide Reductase - metabolism TXNRD3 ultrastructure |
title | Redox regulation by TXNRD3 during epididymal maturation underlies capacitation-associated mitochondrial activity and sperm motility in mice |
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