Control of the Low Voltage-Activated Calcium Channel of Mouse Sperm by Egg ZP3 and by Membrane Hyperpolarization during Capacitation
Sperm adhesion to egg zonae pellucidae initiates sperm acrosome reactions, an exocytotic event that is an early step during fertilization. Previously, it was suggested that zona pellucida-evoked Ca2+ entry into sperm through low voltage-activated Ca2+ channels is an essential step in acrosome reacti...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 1999-06, Vol.96 (12), p.6757-6762 |
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| container_title | Proceedings of the National Academy of Sciences - PNAS |
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| creator | Arnoult, Christophe Kazam, Imrana G. Visconti, Pablo E. Kopf, Gregory S. Villaz, Michel Florman, Harvey M. |
| description | Sperm adhesion to egg zonae pellucidae initiates sperm acrosome reactions, an exocytotic event that is an early step during fertilization. Previously, it was suggested that zona pellucida-evoked Ca2+ entry into sperm through low voltage-activated Ca2+ channels is an essential step in acrosome reactions, based on the inhibitory effects of Ca2+ channel antagonists. However, analysis of this channel is limited by the inability to apply electrophysiological methods directly to sperm. In this report, optical methods of determining membrane potential and internal Ca2+ levels were used to demonstrate that (i) contact with zonae pellucidae activates a transient Ca2+ response in sperm that has a time course and antagonist sensitivity anticipated of low voltage-activated Ca2+ channels; (ii) these channels are unavailable for opening in uncapacitated sperm because of voltage-dependent, steady state inactivation; (iii) membrane hyperpolarization during sperm capacitation is sufficient to recruit channels into a closed state, from which they are available for opening during fertilization; and (iv) channel conductance state may be a factor in determines the efficacy with which channel antagonists inhibit fertilization. This study provides evidence for the activation of sperm Ca2+ channels during gamete adhesion and offers a mechanism that may account for aspects of the regulation of sperm fertility during capacitation through the control of channel availability. Finally, these results suggest that channel conductance state may be a central feature in the design of channel antagonists that inhibit sperm function. |
| doi_str_mv | 10.1073/pnas.96.12.6757 |
| format | Article |
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Previously, it was suggested that zona pellucida-evoked Ca2+ entry into sperm through low voltage-activated Ca2+ channels is an essential step in acrosome reactions, based on the inhibitory effects of Ca2+ channel antagonists. However, analysis of this channel is limited by the inability to apply electrophysiological methods directly to sperm. In this report, optical methods of determining membrane potential and internal Ca2+ levels were used to demonstrate that (i) contact with zonae pellucidae activates a transient Ca2+ response in sperm that has a time course and antagonist sensitivity anticipated of low voltage-activated Ca2+ channels; (ii) these channels are unavailable for opening in uncapacitated sperm because of voltage-dependent, steady state inactivation; (iii) membrane hyperpolarization during sperm capacitation is sufficient to recruit channels into a closed state, from which they are available for opening during fertilization; and (iv) channel conductance state may be a factor in determines the efficacy with which channel antagonists inhibit fertilization. This study provides evidence for the activation of sperm Ca2+ channels during gamete adhesion and offers a mechanism that may account for aspects of the regulation of sperm fertility during capacitation through the control of channel availability. Finally, these results suggest that channel conductance state may be a central feature in the design of channel antagonists that inhibit sperm function.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.96.12.6757</identifier><identifier>PMID: 10359785</identifier><language>eng</language><publisher>United States: National Academy of Sciences of the United States of America</publisher><subject>Acrosome reaction ; Acrosomes ; Animal reproduction ; Animals ; Biological Sciences ; Calcium ; Calcium Channels - physiology ; capacitation ; Cell biology ; Cells ; Cellular biology ; Egg Proteins - analysis ; Egg Proteins - pharmacology ; Exocytosis ; Female ; Fertilization ; Fluorescence ; Inhibitory concentration 50 ; Ion Channel Gating - drug effects ; Male ; Membrane Glycoproteins - analysis ; Membrane Glycoproteins - pharmacology ; Membrane Glycoproteins - physiology ; Membrane Potentials - drug effects ; Membranes ; Mice ; Ova ; Receptors, Cell Surface ; Rodents ; Sperm Capacitation - physiology ; Sperm-Ovum Interactions - physiology ; Spermatozoa ; Spermatozoa - physiology ; Zona Pellucida ; Zona Pellucida Glycoproteins</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 1999-06, Vol.96 (12), p.6757-6762</ispartof><rights>Copyright 1933-1999 The National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Jun 8, 1999</rights><rights>Copyright © 1999, The National Academy of Sciences 1999</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c585t-38ad4ac713072bd864ab0427ba41be70a593f8a0041690899bbe8188461af9df3</citedby><cites>FETCH-LOGICAL-c585t-38ad4ac713072bd864ab0427ba41be70a593f8a0041690899bbe8188461af9df3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/96/12.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/47954$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/47954$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,315,729,782,786,805,887,27931,27932,53798,53800,58024,58257</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/10359785$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Arnoult, Christophe</creatorcontrib><creatorcontrib>Kazam, Imrana G.</creatorcontrib><creatorcontrib>Visconti, Pablo E.</creatorcontrib><creatorcontrib>Kopf, Gregory S.</creatorcontrib><creatorcontrib>Villaz, Michel</creatorcontrib><creatorcontrib>Florman, Harvey M.</creatorcontrib><title>Control of the Low Voltage-Activated Calcium Channel of Mouse Sperm by Egg ZP3 and by Membrane Hyperpolarization during Capacitation</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Sperm adhesion to egg zonae pellucidae initiates sperm acrosome reactions, an exocytotic event that is an early step during fertilization. Previously, it was suggested that zona pellucida-evoked Ca2+ entry into sperm through low voltage-activated Ca2+ channels is an essential step in acrosome reactions, based on the inhibitory effects of Ca2+ channel antagonists. However, analysis of this channel is limited by the inability to apply electrophysiological methods directly to sperm. In this report, optical methods of determining membrane potential and internal Ca2+ levels were used to demonstrate that (i) contact with zonae pellucidae activates a transient Ca2+ response in sperm that has a time course and antagonist sensitivity anticipated of low voltage-activated Ca2+ channels; (ii) these channels are unavailable for opening in uncapacitated sperm because of voltage-dependent, steady state inactivation; (iii) membrane hyperpolarization during sperm capacitation is sufficient to recruit channels into a closed state, from which they are available for opening during fertilization; and (iv) channel conductance state may be a factor in determines the efficacy with which channel antagonists inhibit fertilization. This study provides evidence for the activation of sperm Ca2+ channels during gamete adhesion and offers a mechanism that may account for aspects of the regulation of sperm fertility during capacitation through the control of channel availability. Finally, these results suggest that channel conductance state may be a central feature in the design of channel antagonists that inhibit sperm function.</description><subject>Acrosome reaction</subject><subject>Acrosomes</subject><subject>Animal reproduction</subject><subject>Animals</subject><subject>Biological Sciences</subject><subject>Calcium</subject><subject>Calcium Channels - physiology</subject><subject>capacitation</subject><subject>Cell biology</subject><subject>Cells</subject><subject>Cellular biology</subject><subject>Egg Proteins - analysis</subject><subject>Egg Proteins - pharmacology</subject><subject>Exocytosis</subject><subject>Female</subject><subject>Fertilization</subject><subject>Fluorescence</subject><subject>Inhibitory concentration 50</subject><subject>Ion Channel Gating - drug effects</subject><subject>Male</subject><subject>Membrane Glycoproteins - analysis</subject><subject>Membrane Glycoproteins - pharmacology</subject><subject>Membrane Glycoproteins - physiology</subject><subject>Membrane Potentials - drug effects</subject><subject>Membranes</subject><subject>Mice</subject><subject>Ova</subject><subject>Receptors, Cell Surface</subject><subject>Rodents</subject><subject>Sperm Capacitation - physiology</subject><subject>Sperm-Ovum Interactions - physiology</subject><subject>Spermatozoa</subject><subject>Spermatozoa - physiology</subject><subject>Zona Pellucida</subject><subject>Zona Pellucida Glycoproteins</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1999</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFks2P0zAQxS0EYkvhjMQBWRzglK4dO_6QuKyiXRapK5D4OHCxJonTpkri4DjLljN_OO62LAUhcbLs-b2neeNB6CklC0okOx16GBdaLGi6EDKT99CMEk0TwTW5j2aEpDJRPOUn6NE4bgghOlPkITqhhGVaqmyGfuSuD9612NU4rC1eum_4s2sDrGxyVobmGoKtcA5t2UwdztfQ9_YWvnLTaPGHwfoOF1t8vlrhL-8Zhr7aXa9sV3joLb7cRmJwLfjmO4TG9biafNOvouUAZRNu3x6jBzW0o31yOOfo08X5x_wyWb578zY_WyZlprKQMAUVh1JSRmRaVEpwKAhPZQGcFlYSyDSrFRDCqdBEaV0UVlGluKBQ66pmc_R67ztMRWer0sbo0JrBNx34rXHQmD8rfbM2K3dtUqqVivKXB7l3Xyc7BtM1Y2nbNgaN0zBCK5pKTf4LUskEZzHHHL34C9y4yfdxBiYllPFUCxGh0z1UejeO3tZ3DVNidltgdltgtDA0NbstiIrnxzmP-P23R-DVAdgpf5V_O5h6attgb8KR1b_JCDzbA5sxOH9HcKkzzn4CqSHQSQ</recordid><startdate>19990608</startdate><enddate>19990608</enddate><creator>Arnoult, Christophe</creator><creator>Kazam, Imrana G.</creator><creator>Visconti, Pablo E.</creator><creator>Kopf, Gregory S.</creator><creator>Villaz, Michel</creator><creator>Florman, Harvey M.</creator><general>National Academy of Sciences of the United States of America</general><general>National Acad Sciences</general><general>National Academy of Sciences</general><general>The National Academy of Sciences</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>19990608</creationdate><title>Control of the Low Voltage-Activated Calcium Channel of Mouse Sperm by Egg ZP3 and by Membrane Hyperpolarization during Capacitation</title><author>Arnoult, Christophe ; 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Previously, it was suggested that zona pellucida-evoked Ca2+ entry into sperm through low voltage-activated Ca2+ channels is an essential step in acrosome reactions, based on the inhibitory effects of Ca2+ channel antagonists. However, analysis of this channel is limited by the inability to apply electrophysiological methods directly to sperm. In this report, optical methods of determining membrane potential and internal Ca2+ levels were used to demonstrate that (i) contact with zonae pellucidae activates a transient Ca2+ response in sperm that has a time course and antagonist sensitivity anticipated of low voltage-activated Ca2+ channels; (ii) these channels are unavailable for opening in uncapacitated sperm because of voltage-dependent, steady state inactivation; (iii) membrane hyperpolarization during sperm capacitation is sufficient to recruit channels into a closed state, from which they are available for opening during fertilization; and (iv) channel conductance state may be a factor in determines the efficacy with which channel antagonists inhibit fertilization. This study provides evidence for the activation of sperm Ca2+ channels during gamete adhesion and offers a mechanism that may account for aspects of the regulation of sperm fertility during capacitation through the control of channel availability. Finally, these results suggest that channel conductance state may be a central feature in the design of channel antagonists that inhibit sperm function.</abstract><cop>United States</cop><pub>National Academy of Sciences of the United States of America</pub><pmid>10359785</pmid><doi>10.1073/pnas.96.12.6757</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Acrosome reaction Acrosomes Animal reproduction Animals Biological Sciences Calcium Calcium Channels - physiology capacitation Cell biology Cells Cellular biology Egg Proteins - analysis Egg Proteins - pharmacology Exocytosis Female Fertilization Fluorescence Inhibitory concentration 50 Ion Channel Gating - drug effects Male Membrane Glycoproteins - analysis Membrane Glycoproteins - pharmacology Membrane Glycoproteins - physiology Membrane Potentials - drug effects Membranes Mice Ova Receptors, Cell Surface Rodents Sperm Capacitation - physiology Sperm-Ovum Interactions - physiology Spermatozoa Spermatozoa - physiology Zona Pellucida Zona Pellucida Glycoproteins |
| title | Control of the Low Voltage-Activated Calcium Channel of Mouse Sperm by Egg ZP3 and by Membrane Hyperpolarization during Capacitation |
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