Metal ion fluxes controlling amphibian fertilization
Mammalian oocytes undergo major changes in zinc content and localization to be fertilized, the most striking being the rapid exocytosis of over 10 billion zinc ions in what are known as zinc sparks. Here, we report that fertilization of amphibian Xenopus laevis eggs also initiates a zinc spark that...
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| Veröffentlicht in: | Nature chemistry 2021-07, Vol.13 (7), p.683-691 |
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| creator | Seeler, John F. Sharma, Ajay Zaluzec, Nestor J. Bleher, Reiner Lai, Barry Schultz, Emma G. Hoffman, Brian M. LaBonne, Carole Woodruff, Teresa K. O’Halloran, Thomas V. |
| description | Mammalian oocytes undergo major changes in zinc content and localization to be fertilized, the most striking being the rapid exocytosis of over 10 billion zinc ions in what are known as zinc sparks. Here, we report that fertilization of amphibian
Xenopus laevis
eggs also initiates a zinc spark that progresses across the cell surface in coordination with dynamic calcium waves. This zinc exocytosis is accompanied by a newly recognized loss of intracellular manganese. Synchrotron-based X-ray fluorescence and analytical electron microscopy reveal that zinc and manganese are sequestered in a system of cortical granules that are abundant at the animal pole. Through electron–nuclear double-resonance studies, we rule out Mn
2+
complexation with phosphate or nitrogenous ligands in intact eggs, but the data are consistent with a carboxylate coordination environment. Our observations suggest that zinc and manganese fluxes are a conserved feature of fertilization in vertebrates and that they function as part of a physiological block to polyspermy.
Zinc fluxes have now been shown to be essential in the fertilization of amphibian eggs. Furthermore, manganese(
ii
), which is initially bound to low-molecular-weight carboxylates, is stored and released with zinc from cortical vesicles following fertilization. This rapid metal ion release blocks the otherwise fatal entry of a second sperm. |
| doi_str_mv | 10.1038/s41557-021-00705-2 |
| format | Article |
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Xenopus laevis
eggs also initiates a zinc spark that progresses across the cell surface in coordination with dynamic calcium waves. This zinc exocytosis is accompanied by a newly recognized loss of intracellular manganese. Synchrotron-based X-ray fluorescence and analytical electron microscopy reveal that zinc and manganese are sequestered in a system of cortical granules that are abundant at the animal pole. Through electron–nuclear double-resonance studies, we rule out Mn
2+
complexation with phosphate or nitrogenous ligands in intact eggs, but the data are consistent with a carboxylate coordination environment. Our observations suggest that zinc and manganese fluxes are a conserved feature of fertilization in vertebrates and that they function as part of a physiological block to polyspermy.
Zinc fluxes have now been shown to be essential in the fertilization of amphibian eggs. Furthermore, manganese(
ii
), which is initially bound to low-molecular-weight carboxylates, is stored and released with zinc from cortical vesicles following fertilization. This rapid metal ion release blocks the otherwise fatal entry of a second sperm.</description><identifier>ISSN: 1755-4330</identifier><identifier>ISSN: 1755-4349</identifier><identifier>EISSN: 1755-4349</identifier><identifier>DOI: 10.1038/s41557-021-00705-2</identifier><identifier>PMID: 34155376</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/1647/328/1649 ; 631/1647/328/1978 ; 631/1647/334/1874/761 ; 631/45/321 ; 631/45/49 ; Analytical Chemistry ; Animals ; Biochemistry ; Calcium signalling ; Carboxylates ; Cell surface ; Chemistry ; Chemistry and Materials Science ; Chemistry/Food Science ; Coordination ; Eggs ; Electron microscopy ; Embryo, Nonmammalian - metabolism ; Embryo, Nonmammalian - ultrastructure ; Exocytosis ; Exocytosis - physiology ; Fertilization ; Fertilization - drug effects ; Fertilization - physiology ; Gametocytes ; Inorganic Chemistry ; Ion flux ; Localization ; Manganese ; Metal ions ; Metals, Heavy - metabolism ; Metals, Heavy - pharmacology ; Oocytes ; Organic Chemistry ; Ovum - drug effects ; Ovum - metabolism ; Ovum - ultrastructure ; Physical Chemistry ; Synchrotrons ; Vertebrates ; X-ray fluorescence ; Xenopus laevis - metabolism ; Zinc</subject><ispartof>Nature chemistry, 2021-07, Vol.13 (7), p.683-691</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2021</rights><rights>The Author(s), under exclusive licence to Springer Nature Limited 2021.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c474t-9b71d7fd907832edb395f37a4d92aebe583836ff4dc453352a1b6b3e859124303</citedby><cites>FETCH-LOGICAL-c474t-9b71d7fd907832edb395f37a4d92aebe583836ff4dc453352a1b6b3e859124303</cites><orcidid>0000-0001-8732-5059 ; 0000-0002-1197-3399 ; 0000-0002-4857-3487 ; 0000-0003-0962-797X ; 0000-0001-5580-6202</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34155376$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Seeler, John F.</creatorcontrib><creatorcontrib>Sharma, Ajay</creatorcontrib><creatorcontrib>Zaluzec, Nestor J.</creatorcontrib><creatorcontrib>Bleher, Reiner</creatorcontrib><creatorcontrib>Lai, Barry</creatorcontrib><creatorcontrib>Schultz, Emma G.</creatorcontrib><creatorcontrib>Hoffman, Brian M.</creatorcontrib><creatorcontrib>LaBonne, Carole</creatorcontrib><creatorcontrib>Woodruff, Teresa K.</creatorcontrib><creatorcontrib>O’Halloran, Thomas V.</creatorcontrib><title>Metal ion fluxes controlling amphibian fertilization</title><title>Nature chemistry</title><addtitle>Nat. Chem</addtitle><addtitle>Nat Chem</addtitle><description>Mammalian oocytes undergo major changes in zinc content and localization to be fertilized, the most striking being the rapid exocytosis of over 10 billion zinc ions in what are known as zinc sparks. Here, we report that fertilization of amphibian
Xenopus laevis
eggs also initiates a zinc spark that progresses across the cell surface in coordination with dynamic calcium waves. This zinc exocytosis is accompanied by a newly recognized loss of intracellular manganese. Synchrotron-based X-ray fluorescence and analytical electron microscopy reveal that zinc and manganese are sequestered in a system of cortical granules that are abundant at the animal pole. Through electron–nuclear double-resonance studies, we rule out Mn
2+
complexation with phosphate or nitrogenous ligands in intact eggs, but the data are consistent with a carboxylate coordination environment. Our observations suggest that zinc and manganese fluxes are a conserved feature of fertilization in vertebrates and that they function as part of a physiological block to polyspermy.
Zinc fluxes have now been shown to be essential in the fertilization of amphibian eggs. Furthermore, manganese(
ii
), which is initially bound to low-molecular-weight carboxylates, is stored and released with zinc from cortical vesicles following fertilization. This rapid metal ion release blocks the otherwise fatal entry of a second sperm.</description><subject>631/1647/328/1649</subject><subject>631/1647/328/1978</subject><subject>631/1647/334/1874/761</subject><subject>631/45/321</subject><subject>631/45/49</subject><subject>Analytical Chemistry</subject><subject>Animals</subject><subject>Biochemistry</subject><subject>Calcium signalling</subject><subject>Carboxylates</subject><subject>Cell surface</subject><subject>Chemistry</subject><subject>Chemistry and Materials Science</subject><subject>Chemistry/Food Science</subject><subject>Coordination</subject><subject>Eggs</subject><subject>Electron microscopy</subject><subject>Embryo, Nonmammalian - metabolism</subject><subject>Embryo, Nonmammalian - ultrastructure</subject><subject>Exocytosis</subject><subject>Exocytosis - physiology</subject><subject>Fertilization</subject><subject>Fertilization - drug effects</subject><subject>Fertilization - physiology</subject><subject>Gametocytes</subject><subject>Inorganic Chemistry</subject><subject>Ion flux</subject><subject>Localization</subject><subject>Manganese</subject><subject>Metal ions</subject><subject>Metals, Heavy - metabolism</subject><subject>Metals, Heavy - pharmacology</subject><subject>Oocytes</subject><subject>Organic Chemistry</subject><subject>Ovum - drug effects</subject><subject>Ovum - metabolism</subject><subject>Ovum - ultrastructure</subject><subject>Physical Chemistry</subject><subject>Synchrotrons</subject><subject>Vertebrates</subject><subject>X-ray fluorescence</subject><subject>Xenopus laevis - metabolism</subject><subject>Zinc</subject><issn>1755-4330</issn><issn>1755-4349</issn><issn>1755-4349</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kTtPwzAUhS0EolD4AwyoEgtLwPa142RBQhUvqYgFZstJnNaVGxc7QcCvx6GlPAYmWzrfOb7XB6Ejgs8Ihuw8MMK5SDAlCcYC84RuoT0iOE8YsHx7cwc8QPshzDFOOZB0Fw2gd4JI9xC7162yI-OaUW27Vx1GpWta76w1zXSkFsuZKYyKovatseZdtRE9QDu1skEfrs8herq-ehzfJpOHm7vx5SQpmWBtkheCVKKuciwyoLoqIOc1CMWqnCpdaJ5BBmlds6pkHIBTRYq0AJ3xnFAGGIboYpW77IqFrkodJ1NWLr1ZKP8mnTLyt9KYmZy6F5kxwYXgMeB0HeDdc6dDKxcmlNpa1WjXBUk5iz8hIO3Rkz_o3HW-iev1VCpyTHIWKbqiSu9C8LreDEOw7EuRq1JkLEV-liJpNB3_XGNj-WohArACQpSaqfbfb_8T-wHjgpdt</recordid><startdate>20210701</startdate><enddate>20210701</enddate><creator>Seeler, John F.</creator><creator>Sharma, Ajay</creator><creator>Zaluzec, Nestor J.</creator><creator>Bleher, Reiner</creator><creator>Lai, Barry</creator><creator>Schultz, Emma G.</creator><creator>Hoffman, Brian M.</creator><creator>LaBonne, Carole</creator><creator>Woodruff, Teresa K.</creator><creator>O’Halloran, Thomas V.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><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>3V.</scope><scope>7QR</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PDBOC</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-8732-5059</orcidid><orcidid>https://orcid.org/0000-0002-1197-3399</orcidid><orcidid>https://orcid.org/0000-0002-4857-3487</orcidid><orcidid>https://orcid.org/0000-0003-0962-797X</orcidid><orcidid>https://orcid.org/0000-0001-5580-6202</orcidid></search><sort><creationdate>20210701</creationdate><title>Metal ion fluxes controlling amphibian fertilization</title><author>Seeler, John F. ; Sharma, Ajay ; Zaluzec, Nestor J. ; Bleher, Reiner ; Lai, Barry ; Schultz, Emma G. ; Hoffman, Brian M. ; LaBonne, Carole ; Woodruff, Teresa K. ; O’Halloran, Thomas V.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c474t-9b71d7fd907832edb395f37a4d92aebe583836ff4dc453352a1b6b3e859124303</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>631/1647/328/1649</topic><topic>631/1647/328/1978</topic><topic>631/1647/334/1874/761</topic><topic>631/45/321</topic><topic>631/45/49</topic><topic>Analytical Chemistry</topic><topic>Animals</topic><topic>Biochemistry</topic><topic>Calcium signalling</topic><topic>Carboxylates</topic><topic>Cell surface</topic><topic>Chemistry</topic><topic>Chemistry and Materials Science</topic><topic>Chemistry/Food Science</topic><topic>Coordination</topic><topic>Eggs</topic><topic>Electron microscopy</topic><topic>Embryo, Nonmammalian - metabolism</topic><topic>Embryo, Nonmammalian - ultrastructure</topic><topic>Exocytosis</topic><topic>Exocytosis - physiology</topic><topic>Fertilization</topic><topic>Fertilization - drug effects</topic><topic>Fertilization - physiology</topic><topic>Gametocytes</topic><topic>Inorganic Chemistry</topic><topic>Ion flux</topic><topic>Localization</topic><topic>Manganese</topic><topic>Metal ions</topic><topic>Metals, Heavy - metabolism</topic><topic>Metals, Heavy - pharmacology</topic><topic>Oocytes</topic><topic>Organic Chemistry</topic><topic>Ovum - drug effects</topic><topic>Ovum - metabolism</topic><topic>Ovum - ultrastructure</topic><topic>Physical Chemistry</topic><topic>Synchrotrons</topic><topic>Vertebrates</topic><topic>X-ray fluorescence</topic><topic>Xenopus laevis - metabolism</topic><topic>Zinc</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Seeler, John F.</creatorcontrib><creatorcontrib>Sharma, Ajay</creatorcontrib><creatorcontrib>Zaluzec, Nestor J.</creatorcontrib><creatorcontrib>Bleher, Reiner</creatorcontrib><creatorcontrib>Lai, Barry</creatorcontrib><creatorcontrib>Schultz, Emma G.</creatorcontrib><creatorcontrib>Hoffman, Brian M.</creatorcontrib><creatorcontrib>LaBonne, Carole</creatorcontrib><creatorcontrib>Woodruff, Teresa K.</creatorcontrib><creatorcontrib>O’Halloran, Thomas V.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Chemoreception Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Materials Science Collection</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nature chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Seeler, John F.</au><au>Sharma, Ajay</au><au>Zaluzec, Nestor J.</au><au>Bleher, Reiner</au><au>Lai, Barry</au><au>Schultz, Emma G.</au><au>Hoffman, Brian M.</au><au>LaBonne, Carole</au><au>Woodruff, Teresa K.</au><au>O’Halloran, Thomas V.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Metal ion fluxes controlling amphibian fertilization</atitle><jtitle>Nature chemistry</jtitle><stitle>Nat. Chem</stitle><addtitle>Nat Chem</addtitle><date>2021-07-01</date><risdate>2021</risdate><volume>13</volume><issue>7</issue><spage>683</spage><epage>691</epage><pages>683-691</pages><issn>1755-4330</issn><issn>1755-4349</issn><eissn>1755-4349</eissn><abstract>Mammalian oocytes undergo major changes in zinc content and localization to be fertilized, the most striking being the rapid exocytosis of over 10 billion zinc ions in what are known as zinc sparks. Here, we report that fertilization of amphibian
Xenopus laevis
eggs also initiates a zinc spark that progresses across the cell surface in coordination with dynamic calcium waves. This zinc exocytosis is accompanied by a newly recognized loss of intracellular manganese. Synchrotron-based X-ray fluorescence and analytical electron microscopy reveal that zinc and manganese are sequestered in a system of cortical granules that are abundant at the animal pole. Through electron–nuclear double-resonance studies, we rule out Mn
2+
complexation with phosphate or nitrogenous ligands in intact eggs, but the data are consistent with a carboxylate coordination environment. Our observations suggest that zinc and manganese fluxes are a conserved feature of fertilization in vertebrates and that they function as part of a physiological block to polyspermy.
Zinc fluxes have now been shown to be essential in the fertilization of amphibian eggs. Furthermore, manganese(
ii
), which is initially bound to low-molecular-weight carboxylates, is stored and released with zinc from cortical vesicles following fertilization. This rapid metal ion release blocks the otherwise fatal entry of a second sperm.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>34155376</pmid><doi>10.1038/s41557-021-00705-2</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0001-8732-5059</orcidid><orcidid>https://orcid.org/0000-0002-1197-3399</orcidid><orcidid>https://orcid.org/0000-0002-4857-3487</orcidid><orcidid>https://orcid.org/0000-0003-0962-797X</orcidid><orcidid>https://orcid.org/0000-0001-5580-6202</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | 631/1647/328/1649 631/1647/328/1978 631/1647/334/1874/761 631/45/321 631/45/49 Analytical Chemistry Animals Biochemistry Calcium signalling Carboxylates Cell surface Chemistry Chemistry and Materials Science Chemistry/Food Science Coordination Eggs Electron microscopy Embryo, Nonmammalian - metabolism Embryo, Nonmammalian - ultrastructure Exocytosis Exocytosis - physiology Fertilization Fertilization - drug effects Fertilization - physiology Gametocytes Inorganic Chemistry Ion flux Localization Manganese Metal ions Metals, Heavy - metabolism Metals, Heavy - pharmacology Oocytes Organic Chemistry Ovum - drug effects Ovum - metabolism Ovum - ultrastructure Physical Chemistry Synchrotrons Vertebrates X-ray fluorescence Xenopus laevis - metabolism Zinc |
| title | Metal ion fluxes controlling amphibian fertilization |
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