Extracellular Ca2+ Is Required for Fertilization in the African Clawed Frog, Xenopus laevis
The necessity of extracellular Ca2+ for fertilization and early embryonic development in the African clawed frog, Xenopus laevis, is controversial. Ca2+ entry into X. laevis sperm is reportedly required for the acrosome reaction, yet fertilization and embryonic development have been documented to oc...
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| description | The necessity of extracellular Ca2+ for fertilization and early embryonic development in the African clawed frog, Xenopus laevis, is controversial. Ca2+ entry into X. laevis sperm is reportedly required for the acrosome reaction, yet fertilization and embryonic development have been documented to occur in high concentrations of the Ca2+ chelator BAPTA. Here we sought to resolve this controversy.
Using the appearance of cleavage furrows as an indicator of embryonic development, we found that X. laevis eggs inseminated in a solution lacking added divalent cations developed normally. By contrast, eggs inseminated in millimolar concentrations of BAPTA or EGTA failed to develop. Transferring embryos to varying solutions after sperm addition, we found that extracellular Ca2+ is specifically required for events occurring within the first 30 minutes after sperm addition, but not after. We found that the fluorescently stained sperm were not able to penetrate the envelope of eggs inseminated in high BAPTA, whereas several had penetrated the vitelline envelope of eggs inseminated without a Ca2+ chelator, or with BAPTA and saturating CaCl2. Together these results indicate that fertilization does not occur in high concentrations of Ca2+ chelators. Finally, we found that the jelly coat includes >5 mM of readily diffusible Ca2+.
Taken together, these data are consistent with requirement of extracellular Ca2+ for fertilization. Based on our findings, we hypothesize that the jelly coat surrounding the egg acts as a reserve of readily available Ca2+ ions to foster fertilization in changing extracellular milieu. |
| doi_str_mv | 10.1371/journal.pone.0170405 |
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Using the appearance of cleavage furrows as an indicator of embryonic development, we found that X. laevis eggs inseminated in a solution lacking added divalent cations developed normally. By contrast, eggs inseminated in millimolar concentrations of BAPTA or EGTA failed to develop. Transferring embryos to varying solutions after sperm addition, we found that extracellular Ca2+ is specifically required for events occurring within the first 30 minutes after sperm addition, but not after. We found that the fluorescently stained sperm were not able to penetrate the envelope of eggs inseminated in high BAPTA, whereas several had penetrated the vitelline envelope of eggs inseminated without a Ca2+ chelator, or with BAPTA and saturating CaCl2. Together these results indicate that fertilization does not occur in high concentrations of Ca2+ chelators. Finally, we found that the jelly coat includes >5 mM of readily diffusible Ca2+.
Taken together, these data are consistent with requirement of extracellular Ca2+ for fertilization. Based on our findings, we hypothesize that the jelly coat surrounding the egg acts as a reserve of readily available Ca2+ ions to foster fertilization in changing extracellular milieu.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0170405</identifier><identifier>PMID: 28114360</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acrosome reaction ; Amphibians ; Animals ; Anura ; Biology and Life Sciences ; Calcium (extracellular) ; Calcium - metabolism ; Calcium chloride ; Calcium influx ; Cations ; Chelating agents ; Chelating Agents - chemistry ; Divalent cations ; Eggs ; Embryogenesis ; Embryonic growth stage ; Embryos ; Female ; Fertilization ; Furrows ; Male ; Mammals ; Motility ; Physiology ; Research and Analysis Methods ; Sperm ; Sperm-Ovum Interactions ; Xenopus laevis ; Xenopus laevis - embryology ; Xenopus laevis - physiology</subject><ispartof>PloS one, 2017, Vol.12 (1), p.e0170405-e0170405</ispartof><rights>2017 Wozniak 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>2017 Wozniak et al 2017 Wozniak et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c489t-266780ec306da85c86881f04f5ef234bc58500bc044d190e689b7cd75f2b8da13</citedby><cites>FETCH-LOGICAL-c489t-266780ec306da85c86881f04f5ef234bc58500bc044d190e689b7cd75f2b8da13</cites><orcidid>0000-0003-2724-1325</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/PMC5256882/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5256882/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,729,782,786,866,887,2106,2932,4028,23875,27932,27933,27934,53800,53802</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28114360$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Klymkowsky, Michael</contributor><creatorcontrib>Wozniak, Katherine L</creatorcontrib><creatorcontrib>Mayfield, Brianna L</creatorcontrib><creatorcontrib>Duray, Alexis M</creatorcontrib><creatorcontrib>Tembo, Maiwase</creatorcontrib><creatorcontrib>Beleny, David O</creatorcontrib><creatorcontrib>Napolitano, Marc A</creatorcontrib><creatorcontrib>Sauer, Monica L</creatorcontrib><creatorcontrib>Wisner, Bennett W</creatorcontrib><creatorcontrib>Carlson, Anne E</creatorcontrib><title>Extracellular Ca2+ Is Required for Fertilization in the African Clawed Frog, Xenopus laevis</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The necessity of extracellular Ca2+ for fertilization and early embryonic development in the African clawed frog, Xenopus laevis, is controversial. Ca2+ entry into X. laevis sperm is reportedly required for the acrosome reaction, yet fertilization and embryonic development have been documented to occur in high concentrations of the Ca2+ chelator BAPTA. Here we sought to resolve this controversy.
Using the appearance of cleavage furrows as an indicator of embryonic development, we found that X. laevis eggs inseminated in a solution lacking added divalent cations developed normally. By contrast, eggs inseminated in millimolar concentrations of BAPTA or EGTA failed to develop. Transferring embryos to varying solutions after sperm addition, we found that extracellular Ca2+ is specifically required for events occurring within the first 30 minutes after sperm addition, but not after. We found that the fluorescently stained sperm were not able to penetrate the envelope of eggs inseminated in high BAPTA, whereas several had penetrated the vitelline envelope of eggs inseminated without a Ca2+ chelator, or with BAPTA and saturating CaCl2. Together these results indicate that fertilization does not occur in high concentrations of Ca2+ chelators. Finally, we found that the jelly coat includes >5 mM of readily diffusible Ca2+.
Taken together, these data are consistent with requirement of extracellular Ca2+ for fertilization. Based on our findings, we hypothesize that the jelly coat surrounding the egg acts as a reserve of readily available Ca2+ ions to foster fertilization in changing extracellular milieu.</description><subject>Acrosome reaction</subject><subject>Amphibians</subject><subject>Animals</subject><subject>Anura</subject><subject>Biology and Life Sciences</subject><subject>Calcium (extracellular)</subject><subject>Calcium - metabolism</subject><subject>Calcium chloride</subject><subject>Calcium influx</subject><subject>Cations</subject><subject>Chelating agents</subject><subject>Chelating Agents - chemistry</subject><subject>Divalent cations</subject><subject>Eggs</subject><subject>Embryogenesis</subject><subject>Embryonic growth stage</subject><subject>Embryos</subject><subject>Female</subject><subject>Fertilization</subject><subject>Furrows</subject><subject>Male</subject><subject>Mammals</subject><subject>Motility</subject><subject>Physiology</subject><subject>Research and Analysis Methods</subject><subject>Sperm</subject><subject>Sperm-Ovum Interactions</subject><subject>Xenopus laevis</subject><subject>Xenopus laevis - 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metabolism</topic><topic>Calcium chloride</topic><topic>Calcium influx</topic><topic>Cations</topic><topic>Chelating agents</topic><topic>Chelating Agents - chemistry</topic><topic>Divalent cations</topic><topic>Eggs</topic><topic>Embryogenesis</topic><topic>Embryonic growth stage</topic><topic>Embryos</topic><topic>Female</topic><topic>Fertilization</topic><topic>Furrows</topic><topic>Male</topic><topic>Mammals</topic><topic>Motility</topic><topic>Physiology</topic><topic>Research and Analysis Methods</topic><topic>Sperm</topic><topic>Sperm-Ovum Interactions</topic><topic>Xenopus laevis</topic><topic>Xenopus laevis - embryology</topic><topic>Xenopus laevis - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wozniak, Katherine L</creatorcontrib><creatorcontrib>Mayfield, Brianna L</creatorcontrib><creatorcontrib>Duray, Alexis M</creatorcontrib><creatorcontrib>Tembo, Maiwase</creatorcontrib><creatorcontrib>Beleny, David O</creatorcontrib><creatorcontrib>Napolitano, Marc A</creatorcontrib><creatorcontrib>Sauer, Monica L</creatorcontrib><creatorcontrib>Wisner, Bennett W</creatorcontrib><creatorcontrib>Carlson, Anne E</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>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</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>Public Health Database</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>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</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>Environmental Sciences and Pollution Management</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>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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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>Wozniak, Katherine L</au><au>Mayfield, Brianna L</au><au>Duray, Alexis M</au><au>Tembo, Maiwase</au><au>Beleny, David O</au><au>Napolitano, Marc A</au><au>Sauer, Monica L</au><au>Wisner, Bennett W</au><au>Carlson, Anne E</au><au>Klymkowsky, Michael</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Extracellular Ca2+ Is Required for Fertilization in the African Clawed Frog, Xenopus laevis</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2017</date><risdate>2017</risdate><volume>12</volume><issue>1</issue><spage>e0170405</spage><epage>e0170405</epage><pages>e0170405-e0170405</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The necessity of extracellular Ca2+ for fertilization and early embryonic development in the African clawed frog, Xenopus laevis, is controversial. Ca2+ entry into X. laevis sperm is reportedly required for the acrosome reaction, yet fertilization and embryonic development have been documented to occur in high concentrations of the Ca2+ chelator BAPTA. Here we sought to resolve this controversy.
Using the appearance of cleavage furrows as an indicator of embryonic development, we found that X. laevis eggs inseminated in a solution lacking added divalent cations developed normally. By contrast, eggs inseminated in millimolar concentrations of BAPTA or EGTA failed to develop. Transferring embryos to varying solutions after sperm addition, we found that extracellular Ca2+ is specifically required for events occurring within the first 30 minutes after sperm addition, but not after. We found that the fluorescently stained sperm were not able to penetrate the envelope of eggs inseminated in high BAPTA, whereas several had penetrated the vitelline envelope of eggs inseminated without a Ca2+ chelator, or with BAPTA and saturating CaCl2. Together these results indicate that fertilization does not occur in high concentrations of Ca2+ chelators. Finally, we found that the jelly coat includes >5 mM of readily diffusible Ca2+.
Taken together, these data are consistent with requirement of extracellular Ca2+ for fertilization. Based on our findings, we hypothesize that the jelly coat surrounding the egg acts as a reserve of readily available Ca2+ ions to foster fertilization in changing extracellular milieu.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28114360</pmid><doi>10.1371/journal.pone.0170405</doi><orcidid>https://orcid.org/0000-0003-2724-1325</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Acrosome reaction Amphibians Animals Anura Biology and Life Sciences Calcium (extracellular) Calcium - metabolism Calcium chloride Calcium influx Cations Chelating agents Chelating Agents - chemistry Divalent cations Eggs Embryogenesis Embryonic growth stage Embryos Female Fertilization Furrows Male Mammals Motility Physiology Research and Analysis Methods Sperm Sperm-Ovum Interactions Xenopus laevis Xenopus laevis - embryology Xenopus laevis - physiology |
| title | Extracellular Ca2+ Is Required for Fertilization in the African Clawed Frog, Xenopus laevis |
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