Phosphoinositide substrates of myotubularin affect voltage-activated Ca2+ release in skeletal muscle
Skeletal muscle excitation–contraction (E–C) coupling is altered in several models of phosphatidylinositol phosphate (PtdIns P ) phosphatase deficiency and ryanodine receptor activity measured in vitro was reported to be affected by certain PtdIns P s, thus prompting investigation of the physiologic...
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| Veröffentlicht in: | Pflügers Archiv 2014-05, Vol.466 (5), p.973-985 |
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| creator | González Rodríguez, Estela Lefebvre, Romain Bodnár, Dóra Legrand, Claude Szentesi, Peter Vincze, János Poulard, Karine Bertrand-Michel, Justine Csernoch, Laszlo Buj-Bello, Anna Jacquemond, Vincent |
| description | Skeletal muscle excitation–contraction (E–C) coupling is altered in several models of phosphatidylinositol phosphate (PtdIns
P
) phosphatase deficiency and ryanodine receptor activity measured in vitro was reported to be affected by certain PtdIns
P
s, thus prompting investigation of the physiological role of PtdIns
P
s in E–C coupling. We measured intracellular Ca
2+
transients in voltage-clamped mouse muscle fibres microinjected with a solution containing a PtdIns
P
substrate (PtdIns(3,5)
P
2
or PtdIns(3)
P
) or product (PtdIns(5)
P
or PtdIns) of the myotubularin phosphatase MTM1. No significant change was observed in the presence of either PtdIns(5)
P
or PtdIns but peak SR Ca
2+
release was depressed by ~30% and 50% in fibres injected with PtdIns(3,5)
P
2
and PtdIns(3)
P
, respectively, with no concurrent alteration in the membrane current signals associated with the DHPR function as well as in the voltage dependence of Ca
2+
release inactivation. In permeabilized muscle fibres, the frequency of spontaneous Ca
2+
release events was depressed in the presence of the three tested phosphorylated forms of PtdIns
P
with PtdIns(3,5)
P
2
being the most effective, leading to an almost complete disappearance of Ca
2+
release events. Results support the possibility that pathological accumulation of MTM1 substrates may acutely depress ryanodine receptor-mediated Ca
2+
release. Overexpression of a mCherry-tagged form of MTM1 in muscle fibres revealed a striated pattern consistent with the triadic area. Ca
2+
release remained although unaffected by MTM1 overexpression and was also unaffected by the PtdIns-3-kinase inhibitor LY2940002, suggesting that the 3-phosphorylated PtdIns lipids active on voltage-activated Ca
2+
release are inherently maintained at a low level, inefficient on Ca
2+
release in normal conditions. |
| doi_str_mv | 10.1007/s00424-013-1346-5 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_hal_p</sourceid><recordid>TN_cdi_hal_primary_oai_HAL_hal_04481702v1</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1534466839</sourcerecordid><originalsourceid>FETCH-LOGICAL-c417t-874d749cec4e868d4ed9f33c75f78721de8f698813648cf4877eddb91cfd8e773</originalsourceid><addsrcrecordid>eNp9kU9vEzEQxa0K1KaFD8AF-QhCLv6XtfdYRYUiRSoHOFuOPW62eNfB9kbqt8fRtj1ymtHM773Dewh9YPSaUaq-Fkoll4QyQZiQHVmfoRWTghPeTm_QilLBSKc6fYEuS3mklHKp-Tm64JJyrqhcIf9zn8phn4YplaEOHnCZd6VmW6HgFPD4lOq8m6PNw4RtCOAqPqZY7QMQ6-pwbKDHG8u_4AwRbAHcwPKn7dVGPM7FRXiH3gYbC7x_nlfo97fbX5s7sr3__mNzsyVOMlWJVtIr2TtwEnSnvQTfByGcWgelFWcedOh6rZnopHZBaqXA-13PXPAalBJX6PPiu7fRHPIw2vxkkh3M3c3WnG5USs0U5UfW2E8Le8jp7wylmnEoDmK0E6S5GLYWUnadFn1D2YK6nErJEF69GTWnIsxShGmpm1MRZt00H5_t590I_lXxknwD-AKU9poeIJvHNOepxfMf139TP5Os</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1534466839</pqid></control><display><type>article</type><title>Phosphoinositide substrates of myotubularin affect voltage-activated Ca2+ release in skeletal muscle</title><source>MEDLINE</source><source>SpringerNature Journals</source><creator>González Rodríguez, Estela ; Lefebvre, Romain ; Bodnár, Dóra ; Legrand, Claude ; Szentesi, Peter ; Vincze, János ; Poulard, Karine ; Bertrand-Michel, Justine ; Csernoch, Laszlo ; Buj-Bello, Anna ; Jacquemond, Vincent</creator><creatorcontrib>González Rodríguez, Estela ; Lefebvre, Romain ; Bodnár, Dóra ; Legrand, Claude ; Szentesi, Peter ; Vincze, János ; Poulard, Karine ; Bertrand-Michel, Justine ; Csernoch, Laszlo ; Buj-Bello, Anna ; Jacquemond, Vincent</creatorcontrib><description>Skeletal muscle excitation–contraction (E–C) coupling is altered in several models of phosphatidylinositol phosphate (PtdIns
P
) phosphatase deficiency and ryanodine receptor activity measured in vitro was reported to be affected by certain PtdIns
P
s, thus prompting investigation of the physiological role of PtdIns
P
s in E–C coupling. We measured intracellular Ca
2+
transients in voltage-clamped mouse muscle fibres microinjected with a solution containing a PtdIns
P
substrate (PtdIns(3,5)
P
2
or PtdIns(3)
P
) or product (PtdIns(5)
P
or PtdIns) of the myotubularin phosphatase MTM1. No significant change was observed in the presence of either PtdIns(5)
P
or PtdIns but peak SR Ca
2+
release was depressed by ~30% and 50% in fibres injected with PtdIns(3,5)
P
2
and PtdIns(3)
P
, respectively, with no concurrent alteration in the membrane current signals associated with the DHPR function as well as in the voltage dependence of Ca
2+
release inactivation. In permeabilized muscle fibres, the frequency of spontaneous Ca
2+
release events was depressed in the presence of the three tested phosphorylated forms of PtdIns
P
with PtdIns(3,5)
P
2
being the most effective, leading to an almost complete disappearance of Ca
2+
release events. Results support the possibility that pathological accumulation of MTM1 substrates may acutely depress ryanodine receptor-mediated Ca
2+
release. Overexpression of a mCherry-tagged form of MTM1 in muscle fibres revealed a striated pattern consistent with the triadic area. Ca
2+
release remained although unaffected by MTM1 overexpression and was also unaffected by the PtdIns-3-kinase inhibitor LY2940002, suggesting that the 3-phosphorylated PtdIns lipids active on voltage-activated Ca
2+
release are inherently maintained at a low level, inefficient on Ca
2+
release in normal conditions.</description><identifier>ISSN: 0031-6768</identifier><identifier>EISSN: 1432-2013</identifier><identifier>DOI: 10.1007/s00424-013-1346-5</identifier><identifier>PMID: 24022704</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Action Potentials ; Animals ; Biomedical and Life Sciences ; Biomedicine ; Calcium - metabolism ; Calcium Channels - metabolism ; Cell Biology ; Excitation Contraction Coupling ; Human Physiology ; Life Sciences ; Mice ; Molecular Medicine ; Muscle Fibers, Skeletal - metabolism ; Muscle Fibers, Skeletal - physiology ; Muscle Physiology ; Neurosciences ; Phosphatidylinositol Phosphates - metabolism ; Protein Tyrosine Phosphatases, Non-Receptor - genetics ; Protein Tyrosine Phosphatases, Non-Receptor - metabolism ; Receptors</subject><ispartof>Pflügers Archiv, 2014-05, Vol.466 (5), p.973-985</ispartof><rights>Springer-Verlag Berlin Heidelberg 2013</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c417t-874d749cec4e868d4ed9f33c75f78721de8f698813648cf4877eddb91cfd8e773</citedby><cites>FETCH-LOGICAL-c417t-874d749cec4e868d4ed9f33c75f78721de8f698813648cf4877eddb91cfd8e773</cites><orcidid>0000-0002-1098-3798</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00424-013-1346-5$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00424-013-1346-5$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24022704$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04481702$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>González Rodríguez, Estela</creatorcontrib><creatorcontrib>Lefebvre, Romain</creatorcontrib><creatorcontrib>Bodnár, Dóra</creatorcontrib><creatorcontrib>Legrand, Claude</creatorcontrib><creatorcontrib>Szentesi, Peter</creatorcontrib><creatorcontrib>Vincze, János</creatorcontrib><creatorcontrib>Poulard, Karine</creatorcontrib><creatorcontrib>Bertrand-Michel, Justine</creatorcontrib><creatorcontrib>Csernoch, Laszlo</creatorcontrib><creatorcontrib>Buj-Bello, Anna</creatorcontrib><creatorcontrib>Jacquemond, Vincent</creatorcontrib><title>Phosphoinositide substrates of myotubularin affect voltage-activated Ca2+ release in skeletal muscle</title><title>Pflügers Archiv</title><addtitle>Pflugers Arch - Eur J Physiol</addtitle><addtitle>Pflugers Arch</addtitle><description>Skeletal muscle excitation–contraction (E–C) coupling is altered in several models of phosphatidylinositol phosphate (PtdIns
P
) phosphatase deficiency and ryanodine receptor activity measured in vitro was reported to be affected by certain PtdIns
P
s, thus prompting investigation of the physiological role of PtdIns
P
s in E–C coupling. We measured intracellular Ca
2+
transients in voltage-clamped mouse muscle fibres microinjected with a solution containing a PtdIns
P
substrate (PtdIns(3,5)
P
2
or PtdIns(3)
P
) or product (PtdIns(5)
P
or PtdIns) of the myotubularin phosphatase MTM1. No significant change was observed in the presence of either PtdIns(5)
P
or PtdIns but peak SR Ca
2+
release was depressed by ~30% and 50% in fibres injected with PtdIns(3,5)
P
2
and PtdIns(3)
P
, respectively, with no concurrent alteration in the membrane current signals associated with the DHPR function as well as in the voltage dependence of Ca
2+
release inactivation. In permeabilized muscle fibres, the frequency of spontaneous Ca
2+
release events was depressed in the presence of the three tested phosphorylated forms of PtdIns
P
with PtdIns(3,5)
P
2
being the most effective, leading to an almost complete disappearance of Ca
2+
release events. Results support the possibility that pathological accumulation of MTM1 substrates may acutely depress ryanodine receptor-mediated Ca
2+
release. Overexpression of a mCherry-tagged form of MTM1 in muscle fibres revealed a striated pattern consistent with the triadic area. Ca
2+
release remained although unaffected by MTM1 overexpression and was also unaffected by the PtdIns-3-kinase inhibitor LY2940002, suggesting that the 3-phosphorylated PtdIns lipids active on voltage-activated Ca
2+
release are inherently maintained at a low level, inefficient on Ca
2+
release in normal conditions.</description><subject>Action Potentials</subject><subject>Animals</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Calcium - metabolism</subject><subject>Calcium Channels - metabolism</subject><subject>Cell Biology</subject><subject>Excitation Contraction Coupling</subject><subject>Human Physiology</subject><subject>Life Sciences</subject><subject>Mice</subject><subject>Molecular Medicine</subject><subject>Muscle Fibers, Skeletal - metabolism</subject><subject>Muscle Fibers, Skeletal - physiology</subject><subject>Muscle Physiology</subject><subject>Neurosciences</subject><subject>Phosphatidylinositol Phosphates - metabolism</subject><subject>Protein Tyrosine Phosphatases, Non-Receptor - genetics</subject><subject>Protein Tyrosine Phosphatases, Non-Receptor - metabolism</subject><subject>Receptors</subject><issn>0031-6768</issn><issn>1432-2013</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kU9vEzEQxa0K1KaFD8AF-QhCLv6XtfdYRYUiRSoHOFuOPW62eNfB9kbqt8fRtj1ymtHM773Dewh9YPSaUaq-Fkoll4QyQZiQHVmfoRWTghPeTm_QilLBSKc6fYEuS3mklHKp-Tm64JJyrqhcIf9zn8phn4YplaEOHnCZd6VmW6HgFPD4lOq8m6PNw4RtCOAqPqZY7QMQ6-pwbKDHG8u_4AwRbAHcwPKn7dVGPM7FRXiH3gYbC7x_nlfo97fbX5s7sr3__mNzsyVOMlWJVtIr2TtwEnSnvQTfByGcWgelFWcedOh6rZnopHZBaqXA-13PXPAalBJX6PPiu7fRHPIw2vxkkh3M3c3WnG5USs0U5UfW2E8Le8jp7wylmnEoDmK0E6S5GLYWUnadFn1D2YK6nErJEF69GTWnIsxShGmpm1MRZt00H5_t590I_lXxknwD-AKU9poeIJvHNOepxfMf139TP5Os</recordid><startdate>20140501</startdate><enddate>20140501</enddate><creator>González Rodríguez, Estela</creator><creator>Lefebvre, Romain</creator><creator>Bodnár, Dóra</creator><creator>Legrand, Claude</creator><creator>Szentesi, Peter</creator><creator>Vincze, János</creator><creator>Poulard, Karine</creator><creator>Bertrand-Michel, Justine</creator><creator>Csernoch, Laszlo</creator><creator>Buj-Bello, Anna</creator><creator>Jacquemond, Vincent</creator><general>Springer Berlin Heidelberg</general><general>Springer Verlag</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>1XC</scope><orcidid>https://orcid.org/0000-0002-1098-3798</orcidid></search><sort><creationdate>20140501</creationdate><title>Phosphoinositide substrates of myotubularin affect voltage-activated Ca2+ release in skeletal muscle</title><author>González Rodríguez, Estela ; Lefebvre, Romain ; Bodnár, Dóra ; Legrand, Claude ; Szentesi, Peter ; Vincze, János ; Poulard, Karine ; Bertrand-Michel, Justine ; Csernoch, Laszlo ; Buj-Bello, Anna ; Jacquemond, Vincent</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c417t-874d749cec4e868d4ed9f33c75f78721de8f698813648cf4877eddb91cfd8e773</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Action Potentials</topic><topic>Animals</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Calcium - metabolism</topic><topic>Calcium Channels - metabolism</topic><topic>Cell Biology</topic><topic>Excitation Contraction Coupling</topic><topic>Human Physiology</topic><topic>Life Sciences</topic><topic>Mice</topic><topic>Molecular Medicine</topic><topic>Muscle Fibers, Skeletal - metabolism</topic><topic>Muscle Fibers, Skeletal - physiology</topic><topic>Muscle Physiology</topic><topic>Neurosciences</topic><topic>Phosphatidylinositol Phosphates - metabolism</topic><topic>Protein Tyrosine Phosphatases, Non-Receptor - genetics</topic><topic>Protein Tyrosine Phosphatases, Non-Receptor - metabolism</topic><topic>Receptors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>González Rodríguez, Estela</creatorcontrib><creatorcontrib>Lefebvre, Romain</creatorcontrib><creatorcontrib>Bodnár, Dóra</creatorcontrib><creatorcontrib>Legrand, Claude</creatorcontrib><creatorcontrib>Szentesi, Peter</creatorcontrib><creatorcontrib>Vincze, János</creatorcontrib><creatorcontrib>Poulard, Karine</creatorcontrib><creatorcontrib>Bertrand-Michel, Justine</creatorcontrib><creatorcontrib>Csernoch, Laszlo</creatorcontrib><creatorcontrib>Buj-Bello, Anna</creatorcontrib><creatorcontrib>Jacquemond, Vincent</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>Hyper Article en Ligne (HAL)</collection><jtitle>Pflügers Archiv</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>González Rodríguez, Estela</au><au>Lefebvre, Romain</au><au>Bodnár, Dóra</au><au>Legrand, Claude</au><au>Szentesi, Peter</au><au>Vincze, János</au><au>Poulard, Karine</au><au>Bertrand-Michel, Justine</au><au>Csernoch, Laszlo</au><au>Buj-Bello, Anna</au><au>Jacquemond, Vincent</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Phosphoinositide substrates of myotubularin affect voltage-activated Ca2+ release in skeletal muscle</atitle><jtitle>Pflügers Archiv</jtitle><stitle>Pflugers Arch - Eur J Physiol</stitle><addtitle>Pflugers Arch</addtitle><date>2014-05-01</date><risdate>2014</risdate><volume>466</volume><issue>5</issue><spage>973</spage><epage>985</epage><pages>973-985</pages><issn>0031-6768</issn><eissn>1432-2013</eissn><abstract>Skeletal muscle excitation–contraction (E–C) coupling is altered in several models of phosphatidylinositol phosphate (PtdIns
P
) phosphatase deficiency and ryanodine receptor activity measured in vitro was reported to be affected by certain PtdIns
P
s, thus prompting investigation of the physiological role of PtdIns
P
s in E–C coupling. We measured intracellular Ca
2+
transients in voltage-clamped mouse muscle fibres microinjected with a solution containing a PtdIns
P
substrate (PtdIns(3,5)
P
2
or PtdIns(3)
P
) or product (PtdIns(5)
P
or PtdIns) of the myotubularin phosphatase MTM1. No significant change was observed in the presence of either PtdIns(5)
P
or PtdIns but peak SR Ca
2+
release was depressed by ~30% and 50% in fibres injected with PtdIns(3,5)
P
2
and PtdIns(3)
P
, respectively, with no concurrent alteration in the membrane current signals associated with the DHPR function as well as in the voltage dependence of Ca
2+
release inactivation. In permeabilized muscle fibres, the frequency of spontaneous Ca
2+
release events was depressed in the presence of the three tested phosphorylated forms of PtdIns
P
with PtdIns(3,5)
P
2
being the most effective, leading to an almost complete disappearance of Ca
2+
release events. Results support the possibility that pathological accumulation of MTM1 substrates may acutely depress ryanodine receptor-mediated Ca
2+
release. Overexpression of a mCherry-tagged form of MTM1 in muscle fibres revealed a striated pattern consistent with the triadic area. Ca
2+
release remained although unaffected by MTM1 overexpression and was also unaffected by the PtdIns-3-kinase inhibitor LY2940002, suggesting that the 3-phosphorylated PtdIns lipids active on voltage-activated Ca
2+
release are inherently maintained at a low level, inefficient on Ca
2+
release in normal conditions.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>24022704</pmid><doi>10.1007/s00424-013-1346-5</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-1098-3798</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0031-6768 |
| ispartof | Pflügers Archiv, 2014-05, Vol.466 (5), p.973-985 |
| issn | 0031-6768 1432-2013 |
| language | eng |
| recordid | cdi_hal_primary_oai_HAL_hal_04481702v1 |
| source | MEDLINE; SpringerNature Journals |
| subjects | Action Potentials Animals Biomedical and Life Sciences Biomedicine Calcium - metabolism Calcium Channels - metabolism Cell Biology Excitation Contraction Coupling Human Physiology Life Sciences Mice Molecular Medicine Muscle Fibers, Skeletal - metabolism Muscle Fibers, Skeletal - physiology Muscle Physiology Neurosciences Phosphatidylinositol Phosphates - metabolism Protein Tyrosine Phosphatases, Non-Receptor - genetics Protein Tyrosine Phosphatases, Non-Receptor - metabolism Receptors |
| title | Phosphoinositide substrates of myotubularin affect voltage-activated Ca2+ release in skeletal muscle |
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