Loading…
A Ca2+-induced Ca2+ release mechanism involved in asynchronous exocytosis at frog motor nerve terminals
The extent to which Ca2+-induced Ca2+ release (CICR) affects transmitter release is unknown. Continuous nerve stimulation (20-50 Hz) caused slow transient increases in miniature end-plate potential (MEPP) frequency (MEPP-hump) and intracellular free Ca2+ ([Ca2+]i) in presynaptic terminals (Ca2+-hump...
Saved in:
| Published in: | The Journal of general physiology 1998-11, Vol.112 (5), p.593-609 |
|---|---|
| Main Authors: | , , , , , |
| Format: | Article |
| Language: | English |
| Subjects: | |
| Citations: | Items that this one cites Items that cite this one |
| Online Access: | Get full text |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| cited_by | cdi_FETCH-LOGICAL-c380t-943a5bf2e6bfea674eedd13f9c2aacbf842d210c880d252dd59e5c10d4fef8c53 |
|---|---|
| cites | cdi_FETCH-LOGICAL-c380t-943a5bf2e6bfea674eedd13f9c2aacbf842d210c880d252dd59e5c10d4fef8c53 |
| container_end_page | 609 |
| container_issue | 5 |
| container_start_page | 593 |
| container_title | The Journal of general physiology |
| container_volume | 112 |
| creator | Narita, K Akita, T Osanai, M Shirasaki, T Kijima, H Kuba, K |
| description | The extent to which Ca2+-induced Ca2+ release (CICR) affects transmitter release is unknown. Continuous nerve stimulation (20-50 Hz) caused slow transient increases in miniature end-plate potential (MEPP) frequency (MEPP-hump) and intracellular free Ca2+ ([Ca2+]i) in presynaptic terminals (Ca2+-hump) in frog skeletal muscles over a period of minutes in a low Ca2+, high Mg2+ solution. Mn2+ quenched Indo-1 and Fura-2 fluorescence, thus indicating that stimulation was accompanied by opening of voltage-dependent Ca2+ channels. MEPP-hump depended on extracellular Ca2+ (0.05-0.2 mM) and stimulation frequency. Both the Ca2+- and MEPP-humps were blocked by 8-(N, N-diethylamino)octyl3,4,5-trimethoxybenzoate hydrochloride (TMB-8), ryanodine, and thapsigargin, but enhanced by CN-. Thus, Ca2+-hump is generated by the activation of CICR via ryanodine receptors by Ca2+ entry, producing MEPP-hump. A short interruption of tetanus ( |
| doi_str_mv | 10.1085/jgp.112.5.593 |
| format | article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_2229444</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>70049591</sourcerecordid><originalsourceid>FETCH-LOGICAL-c380t-943a5bf2e6bfea674eedd13f9c2aacbf842d210c880d252dd59e5c10d4fef8c53</originalsourceid><addsrcrecordid>eNpVkUFrGzEQhUVJSF2nxx4LOuUS1pG0ki1dCsYkTcHQS3IWsjSyZXYlV1qb-N9HiU1o5vIY5vFmhg-hH5RMKJHibrveTShlEzERqv2CRlRw0sxmXF6gESGMNZQp8RV9K2VLaglGrtCVkmSqpnKE1nO8MOy2CdHtLbj3BmfowBTAPdiNiaH0OMRD6g51HiI25RjtJqeY9gXDS7LHIZVQsBmwz2mN-zSkjCPkA-ABch-i6co1uvRV4PtZx-j54f5p8dgs__7-s5gvG9tKMjSKt0asPIPpyoOZzjiAc7T1yjJj7MpLzhyjxEpJHBPMOaFAWEoc9-ClFe0Y_Trl7varHpyFOGTT6V0OvclHnUzQnycxbPQ6HTRjTHHOa8DNOSCnf3sog-5DsdB1JkJ9WM8I4UooWo3NyWhzKiWD_1hCiX4joysZXclooSuZ6v_5_2Uf7jOK9hWLiI1L</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>70049591</pqid></control><display><type>article</type><title>A Ca2+-induced Ca2+ release mechanism involved in asynchronous exocytosis at frog motor nerve terminals</title><creator>Narita, K ; Akita, T ; Osanai, M ; Shirasaki, T ; Kijima, H ; Kuba, K</creator><creatorcontrib>Narita, K ; Akita, T ; Osanai, M ; Shirasaki, T ; Kijima, H ; Kuba, K</creatorcontrib><description>The extent to which Ca2+-induced Ca2+ release (CICR) affects transmitter release is unknown. Continuous nerve stimulation (20-50 Hz) caused slow transient increases in miniature end-plate potential (MEPP) frequency (MEPP-hump) and intracellular free Ca2+ ([Ca2+]i) in presynaptic terminals (Ca2+-hump) in frog skeletal muscles over a period of minutes in a low Ca2+, high Mg2+ solution. Mn2+ quenched Indo-1 and Fura-2 fluorescence, thus indicating that stimulation was accompanied by opening of voltage-dependent Ca2+ channels. MEPP-hump depended on extracellular Ca2+ (0.05-0.2 mM) and stimulation frequency. Both the Ca2+- and MEPP-humps were blocked by 8-(N, N-diethylamino)octyl3,4,5-trimethoxybenzoate hydrochloride (TMB-8), ryanodine, and thapsigargin, but enhanced by CN-. Thus, Ca2+-hump is generated by the activation of CICR via ryanodine receptors by Ca2+ entry, producing MEPP-hump. A short interruption of tetanus (<1 min) during MEPP-hump quickly reduced MEPP frequency to a level attained under the effect of TMB-8 or thapsigargin, while resuming tetanus swiftly raised MEPP frequency to the previous or higher level. Thus, the steady/equilibrium condition balancing CICR and Ca2+ clearance occurs in nerve terminals with slow changes toward a greater activation of CICR (priming) during the rising phase of MEPP-hump and toward a smaller activation during the decay phase. A short pause applied after the end of MEPP- or Ca2+-hump affected little MEPP frequency or [Ca2+]i, but caused a quick increase (faster than MEPP- or Ca2+-hump) after the pause, whose magnitude increased with an increase in pause duration (<1 min), suggesting that Ca2+ entry-dependent inactivation, but not depriming process, explains the decay of the humps. The depriming process was seen by giving a much longer pause (>1 min). Thus, ryanodine receptors in frog motor nerve terminals are endowed with Ca2+ entry-dependent slow priming and fast inactivation mechanisms, as well as Ca2+ entry-dependent activation, and involved in asynchronous exocytosis. Physiological significance of CICR in presynaptic terminals was discussed.</description><identifier>ISSN: 0022-1295</identifier><identifier>EISSN: 1540-7748</identifier><identifier>DOI: 10.1085/jgp.112.5.593</identifier><identifier>PMID: 9806968</identifier><language>eng</language><publisher>United States: The Rockefeller University Press</publisher><subject>Action Potentials - physiology ; Animals ; Calcium - metabolism ; Calcium - pharmacology ; Calcium Channel Blockers - pharmacology ; Chelating Agents - pharmacology ; Egtazic Acid - analogs & derivatives ; Egtazic Acid - pharmacology ; Evoked Potentials, Motor - drug effects ; Evoked Potentials, Motor - physiology ; Exocytosis - drug effects ; Exocytosis - physiology ; Fluorescent Dyes ; Gallic Acid - analogs & derivatives ; Gallic Acid - pharmacology ; Ion Channel Gating - drug effects ; Ion Channel Gating - physiology ; Magnesium - pharmacology ; Motor Neurons - chemistry ; Motor Neurons - cytology ; Motor Neurons - metabolism ; Neurotransmitter Agents - metabolism ; Presynaptic Terminals - chemistry ; Presynaptic Terminals - drug effects ; Presynaptic Terminals - metabolism ; Ranidae ; Ryanodine Receptor Calcium Release Channel - metabolism ; Time Factors</subject><ispartof>The Journal of general physiology, 1998-11, Vol.112 (5), p.593-609</ispartof><rights>1998</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c380t-943a5bf2e6bfea674eedd13f9c2aacbf842d210c880d252dd59e5c10d4fef8c53</citedby><cites>FETCH-LOGICAL-c380t-943a5bf2e6bfea674eedd13f9c2aacbf842d210c880d252dd59e5c10d4fef8c53</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>780,885</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/9806968$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Narita, K</creatorcontrib><creatorcontrib>Akita, T</creatorcontrib><creatorcontrib>Osanai, M</creatorcontrib><creatorcontrib>Shirasaki, T</creatorcontrib><creatorcontrib>Kijima, H</creatorcontrib><creatorcontrib>Kuba, K</creatorcontrib><title>A Ca2+-induced Ca2+ release mechanism involved in asynchronous exocytosis at frog motor nerve terminals</title><title>The Journal of general physiology</title><addtitle>J Gen Physiol</addtitle><description>The extent to which Ca2+-induced Ca2+ release (CICR) affects transmitter release is unknown. Continuous nerve stimulation (20-50 Hz) caused slow transient increases in miniature end-plate potential (MEPP) frequency (MEPP-hump) and intracellular free Ca2+ ([Ca2+]i) in presynaptic terminals (Ca2+-hump) in frog skeletal muscles over a period of minutes in a low Ca2+, high Mg2+ solution. Mn2+ quenched Indo-1 and Fura-2 fluorescence, thus indicating that stimulation was accompanied by opening of voltage-dependent Ca2+ channels. MEPP-hump depended on extracellular Ca2+ (0.05-0.2 mM) and stimulation frequency. Both the Ca2+- and MEPP-humps were blocked by 8-(N, N-diethylamino)octyl3,4,5-trimethoxybenzoate hydrochloride (TMB-8), ryanodine, and thapsigargin, but enhanced by CN-. Thus, Ca2+-hump is generated by the activation of CICR via ryanodine receptors by Ca2+ entry, producing MEPP-hump. A short interruption of tetanus (<1 min) during MEPP-hump quickly reduced MEPP frequency to a level attained under the effect of TMB-8 or thapsigargin, while resuming tetanus swiftly raised MEPP frequency to the previous or higher level. Thus, the steady/equilibrium condition balancing CICR and Ca2+ clearance occurs in nerve terminals with slow changes toward a greater activation of CICR (priming) during the rising phase of MEPP-hump and toward a smaller activation during the decay phase. A short pause applied after the end of MEPP- or Ca2+-hump affected little MEPP frequency or [Ca2+]i, but caused a quick increase (faster than MEPP- or Ca2+-hump) after the pause, whose magnitude increased with an increase in pause duration (<1 min), suggesting that Ca2+ entry-dependent inactivation, but not depriming process, explains the decay of the humps. The depriming process was seen by giving a much longer pause (>1 min). Thus, ryanodine receptors in frog motor nerve terminals are endowed with Ca2+ entry-dependent slow priming and fast inactivation mechanisms, as well as Ca2+ entry-dependent activation, and involved in asynchronous exocytosis. Physiological significance of CICR in presynaptic terminals was discussed.</description><subject>Action Potentials - physiology</subject><subject>Animals</subject><subject>Calcium - metabolism</subject><subject>Calcium - pharmacology</subject><subject>Calcium Channel Blockers - pharmacology</subject><subject>Chelating Agents - pharmacology</subject><subject>Egtazic Acid - analogs & derivatives</subject><subject>Egtazic Acid - pharmacology</subject><subject>Evoked Potentials, Motor - drug effects</subject><subject>Evoked Potentials, Motor - physiology</subject><subject>Exocytosis - drug effects</subject><subject>Exocytosis - physiology</subject><subject>Fluorescent Dyes</subject><subject>Gallic Acid - analogs & derivatives</subject><subject>Gallic Acid - pharmacology</subject><subject>Ion Channel Gating - drug effects</subject><subject>Ion Channel Gating - physiology</subject><subject>Magnesium - pharmacology</subject><subject>Motor Neurons - chemistry</subject><subject>Motor Neurons - cytology</subject><subject>Motor Neurons - metabolism</subject><subject>Neurotransmitter Agents - metabolism</subject><subject>Presynaptic Terminals - chemistry</subject><subject>Presynaptic Terminals - drug effects</subject><subject>Presynaptic Terminals - metabolism</subject><subject>Ranidae</subject><subject>Ryanodine Receptor Calcium Release Channel - metabolism</subject><subject>Time Factors</subject><issn>0022-1295</issn><issn>1540-7748</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1998</creationdate><recordtype>article</recordtype><recordid>eNpVkUFrGzEQhUVJSF2nxx4LOuUS1pG0ki1dCsYkTcHQS3IWsjSyZXYlV1qb-N9HiU1o5vIY5vFmhg-hH5RMKJHibrveTShlEzERqv2CRlRw0sxmXF6gESGMNZQp8RV9K2VLaglGrtCVkmSqpnKE1nO8MOy2CdHtLbj3BmfowBTAPdiNiaH0OMRD6g51HiI25RjtJqeY9gXDS7LHIZVQsBmwz2mN-zSkjCPkA-ABch-i6co1uvRV4PtZx-j54f5p8dgs__7-s5gvG9tKMjSKt0asPIPpyoOZzjiAc7T1yjJj7MpLzhyjxEpJHBPMOaFAWEoc9-ClFe0Y_Trl7varHpyFOGTT6V0OvclHnUzQnycxbPQ6HTRjTHHOa8DNOSCnf3sog-5DsdB1JkJ9WM8I4UooWo3NyWhzKiWD_1hCiX4joysZXclooSuZ6v_5_2Uf7jOK9hWLiI1L</recordid><startdate>199811</startdate><enddate>199811</enddate><creator>Narita, K</creator><creator>Akita, T</creator><creator>Osanai, M</creator><creator>Shirasaki, T</creator><creator>Kijima, H</creator><creator>Kuba, K</creator><general>The Rockefeller University Press</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>199811</creationdate><title>A Ca2+-induced Ca2+ release mechanism involved in asynchronous exocytosis at frog motor nerve terminals</title><author>Narita, K ; Akita, T ; Osanai, M ; Shirasaki, T ; Kijima, H ; Kuba, K</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c380t-943a5bf2e6bfea674eedd13f9c2aacbf842d210c880d252dd59e5c10d4fef8c53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1998</creationdate><topic>Action Potentials - physiology</topic><topic>Animals</topic><topic>Calcium - metabolism</topic><topic>Calcium - pharmacology</topic><topic>Calcium Channel Blockers - pharmacology</topic><topic>Chelating Agents - pharmacology</topic><topic>Egtazic Acid - analogs & derivatives</topic><topic>Egtazic Acid - pharmacology</topic><topic>Evoked Potentials, Motor - drug effects</topic><topic>Evoked Potentials, Motor - physiology</topic><topic>Exocytosis - drug effects</topic><topic>Exocytosis - physiology</topic><topic>Fluorescent Dyes</topic><topic>Gallic Acid - analogs & derivatives</topic><topic>Gallic Acid - pharmacology</topic><topic>Ion Channel Gating - drug effects</topic><topic>Ion Channel Gating - physiology</topic><topic>Magnesium - pharmacology</topic><topic>Motor Neurons - chemistry</topic><topic>Motor Neurons - cytology</topic><topic>Motor Neurons - metabolism</topic><topic>Neurotransmitter Agents - metabolism</topic><topic>Presynaptic Terminals - chemistry</topic><topic>Presynaptic Terminals - drug effects</topic><topic>Presynaptic Terminals - metabolism</topic><topic>Ranidae</topic><topic>Ryanodine Receptor Calcium Release Channel - metabolism</topic><topic>Time Factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Narita, K</creatorcontrib><creatorcontrib>Akita, T</creatorcontrib><creatorcontrib>Osanai, M</creatorcontrib><creatorcontrib>Shirasaki, T</creatorcontrib><creatorcontrib>Kijima, H</creatorcontrib><creatorcontrib>Kuba, K</creatorcontrib><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 general physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Narita, K</au><au>Akita, T</au><au>Osanai, M</au><au>Shirasaki, T</au><au>Kijima, H</au><au>Kuba, K</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Ca2+-induced Ca2+ release mechanism involved in asynchronous exocytosis at frog motor nerve terminals</atitle><jtitle>The Journal of general physiology</jtitle><addtitle>J Gen Physiol</addtitle><date>1998-11</date><risdate>1998</risdate><volume>112</volume><issue>5</issue><spage>593</spage><epage>609</epage><pages>593-609</pages><issn>0022-1295</issn><eissn>1540-7748</eissn><abstract>The extent to which Ca2+-induced Ca2+ release (CICR) affects transmitter release is unknown. Continuous nerve stimulation (20-50 Hz) caused slow transient increases in miniature end-plate potential (MEPP) frequency (MEPP-hump) and intracellular free Ca2+ ([Ca2+]i) in presynaptic terminals (Ca2+-hump) in frog skeletal muscles over a period of minutes in a low Ca2+, high Mg2+ solution. Mn2+ quenched Indo-1 and Fura-2 fluorescence, thus indicating that stimulation was accompanied by opening of voltage-dependent Ca2+ channels. MEPP-hump depended on extracellular Ca2+ (0.05-0.2 mM) and stimulation frequency. Both the Ca2+- and MEPP-humps were blocked by 8-(N, N-diethylamino)octyl3,4,5-trimethoxybenzoate hydrochloride (TMB-8), ryanodine, and thapsigargin, but enhanced by CN-. Thus, Ca2+-hump is generated by the activation of CICR via ryanodine receptors by Ca2+ entry, producing MEPP-hump. A short interruption of tetanus (<1 min) during MEPP-hump quickly reduced MEPP frequency to a level attained under the effect of TMB-8 or thapsigargin, while resuming tetanus swiftly raised MEPP frequency to the previous or higher level. Thus, the steady/equilibrium condition balancing CICR and Ca2+ clearance occurs in nerve terminals with slow changes toward a greater activation of CICR (priming) during the rising phase of MEPP-hump and toward a smaller activation during the decay phase. A short pause applied after the end of MEPP- or Ca2+-hump affected little MEPP frequency or [Ca2+]i, but caused a quick increase (faster than MEPP- or Ca2+-hump) after the pause, whose magnitude increased with an increase in pause duration (<1 min), suggesting that Ca2+ entry-dependent inactivation, but not depriming process, explains the decay of the humps. The depriming process was seen by giving a much longer pause (>1 min). Thus, ryanodine receptors in frog motor nerve terminals are endowed with Ca2+ entry-dependent slow priming and fast inactivation mechanisms, as well as Ca2+ entry-dependent activation, and involved in asynchronous exocytosis. Physiological significance of CICR in presynaptic terminals was discussed.</abstract><cop>United States</cop><pub>The Rockefeller University Press</pub><pmid>9806968</pmid><doi>10.1085/jgp.112.5.593</doi><tpages>17</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0022-1295 |
| ispartof | The Journal of general physiology, 1998-11, Vol.112 (5), p.593-609 |
| issn | 0022-1295 1540-7748 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_2229444 |
| source | |
| subjects | Action Potentials - physiology Animals Calcium - metabolism Calcium - pharmacology Calcium Channel Blockers - pharmacology Chelating Agents - pharmacology Egtazic Acid - analogs & derivatives Egtazic Acid - pharmacology Evoked Potentials, Motor - drug effects Evoked Potentials, Motor - physiology Exocytosis - drug effects Exocytosis - physiology Fluorescent Dyes Gallic Acid - analogs & derivatives Gallic Acid - pharmacology Ion Channel Gating - drug effects Ion Channel Gating - physiology Magnesium - pharmacology Motor Neurons - chemistry Motor Neurons - cytology Motor Neurons - metabolism Neurotransmitter Agents - metabolism Presynaptic Terminals - chemistry Presynaptic Terminals - drug effects Presynaptic Terminals - metabolism Ranidae Ryanodine Receptor Calcium Release Channel - metabolism Time Factors |
| title | A Ca2+-induced Ca2+ release mechanism involved in asynchronous exocytosis at frog motor nerve terminals |
| url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-25T04%3A28%3A36IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=A%20Ca2+-induced%20Ca2+%20release%20mechanism%20involved%20in%20asynchronous%20exocytosis%20at%20frog%20motor%20nerve%20terminals&rft.jtitle=The%20Journal%20of%20general%20physiology&rft.au=Narita,%20K&rft.date=1998-11&rft.volume=112&rft.issue=5&rft.spage=593&rft.epage=609&rft.pages=593-609&rft.issn=0022-1295&rft.eissn=1540-7748&rft_id=info:doi/10.1085/jgp.112.5.593&rft_dat=%3Cproquest_pubme%3E70049591%3C/proquest_pubme%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c380t-943a5bf2e6bfea674eedd13f9c2aacbf842d210c880d252dd59e5c10d4fef8c53%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=70049591&rft_id=info:pmid/9806968&rfr_iscdi=true |