The mammalian skeletal muscle DHPR has larger Ca(2+) conductance and is phylogenetically ancient to the early ray-finned fish sterlet (Acipenser ruthenus).
Identifieur interne : 000032 ( PubMed/Curation ); précédent : 000031; suivant : 000033The mammalian skeletal muscle DHPR has larger Ca(2+) conductance and is phylogenetically ancient to the early ray-finned fish sterlet (Acipenser ruthenus).
Auteurs : Kai Schrötter [Autriche] ; Anamika Dayal [Autriche] ; Manfred Grabner [Autriche]Source :
- Cell calcium [ 1532-1991 ] ; 2016.
Abstract
The L-type Ca(2+) channel or dihydropyridine receptor (DHPR) in vertebrate skeletal muscle is responsible for sensing sarcolemmal depolarizations and transducing this signal to the sarcoplasmic Ca(2+) release channel RyR1 via conformational coupling to initiate muscle contraction. During this excitation-contraction (EC) coupling process there is a slow Ca(2+) current through the mammalian DHPR which is fully missing in euteleost fishes. In contrast to ancestral evolutionary stages where skeletal muscle EC coupling is still depended on Ca(2+)-induced Ca(2+)-release (CICR), it is possible that the DHPR Ca(2+) conductivity during mammalian (conformational) EC coupling was retained as an evolutionary remnant (vestigiality). Here, we wanted to test the hypothesis that due to the lack of evolutionary pressure in post-CICR species skeletal muscle DHPR Ca(2+) conductivity gradually reduced as evolution progressed. Interestingly, we identified that the DHPR of the early ray-finned fish sterlet (Acipenser ruthenus) is phylogenetically positioned above the mammalian rabbit DHPR which retained robust Ca(2+) conductivity, but below the euteleost zebrafish DHPR which completely lost Ca(2+) conductivity. Remarkably, our results revealed that sterlet DHPR still retained the Ca(2+) conductivity but currents are significantly reduced compared to rabbit. This decrease is due to lower DHPR membrane expression similar to zebrafish, as well as due to reduced channel open probability (Po). In both these fish species the lower DHPR expression density is partially compensated by higher efficacy of DHPR-RyR1 coupling. The complete loss of Po in zebrafish and other euteleost species was presumably based on the teleost specific 3rd round of genome duplication (Ts3R). Ts3R headed into the appearance of two skeletal muscle DHPR isoforms which finally, together with the radiation of the euteleost clade, fully lost the Po.
DOI: 10.1016/j.ceca.2016.10.002
PubMed: 27793347
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Electronic address: manfred.grabner@i-med.ac.at.</nlm:affiliation><country xml:lang="fr">Autriche</country><wicri:regionArea>Department of Medical Genetics, Molecular and Clinical Pharmacology, Division of Biochemical Pharmacology, Medical University of Innsbruck, Peter Mayr Strasse 1, A-6020, Innsbruck</wicri:regionArea></affiliation></author></analytic><series><title level="j">Cell calcium</title><idno type="eISSN">1532-1991</idno><imprint><date when="2016" type="published">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The L-type Ca(2+) channel or dihydropyridine receptor (DHPR) in vertebrate skeletal muscle is responsible for sensing sarcolemmal depolarizations and transducing this signal to the sarcoplasmic Ca(2+) release channel RyR1 via conformational coupling to initiate muscle contraction. During this excitation-contraction (EC) coupling process there is a slow Ca(2+) current through the mammalian DHPR which is fully missing in euteleost fishes. In contrast to ancestral evolutionary stages where skeletal muscle EC coupling is still depended on Ca(2+)-induced Ca(2+)-release (CICR), it is possible that the DHPR Ca(2+) conductivity during mammalian (conformational) EC coupling was retained as an evolutionary remnant (vestigiality). Here, we wanted to test the hypothesis that due to the lack of evolutionary pressure in post-CICR species skeletal muscle DHPR Ca(2+) conductivity gradually reduced as evolution progressed. Interestingly, we identified that the DHPR of the early ray-finned fish sterlet (Acipenser ruthenus) is phylogenetically positioned above the mammalian rabbit DHPR which retained robust Ca(2+) conductivity, but below the euteleost zebrafish DHPR which completely lost Ca(2+) conductivity. Remarkably, our results revealed that sterlet DHPR still retained the Ca(2+) conductivity but currents are significantly reduced compared to rabbit. This decrease is due to lower DHPR membrane expression similar to zebrafish, as well as due to reduced channel open probability (Po). In both these fish species the lower DHPR expression density is partially compensated by higher efficacy of DHPR-RyR1 coupling. The complete loss of Po in zebrafish and other euteleost species was presumably based on the teleost specific 3rd round of genome duplication (Ts3R). Ts3R headed into the appearance of two skeletal muscle DHPR isoforms which finally, together with the radiation of the euteleost clade, fully lost the Po.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">27793347</PMID><DateCreated><Year>2016</Year><Month>10</Month><Day>29</Day></DateCreated><DateRevised><Year>2016</Year><Month>10</Month><Day>30</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1532-1991</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2016</Year><Month>Oct</Month><Day>23</Day></PubDate></JournalIssue><Title>Cell calcium</Title><ISOAbbreviation>Cell Calcium</ISOAbbreviation></Journal><ArticleTitle>The mammalian skeletal muscle DHPR has larger Ca(2+) conductance and is phylogenetically ancient to the early ray-finned fish sterlet (Acipenser ruthenus).</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">S0143-4160(16)30163-4</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.ceca.2016.10.002</ELocationID><Abstract><AbstractText NlmCategory="UNASSIGNED">The L-type Ca(2+) channel or dihydropyridine receptor (DHPR) in vertebrate skeletal muscle is responsible for sensing sarcolemmal depolarizations and transducing this signal to the sarcoplasmic Ca(2+) release channel RyR1 via conformational coupling to initiate muscle contraction. During this excitation-contraction (EC) coupling process there is a slow Ca(2+) current through the mammalian DHPR which is fully missing in euteleost fishes. In contrast to ancestral evolutionary stages where skeletal muscle EC coupling is still depended on Ca(2+)-induced Ca(2+)-release (CICR), it is possible that the DHPR Ca(2+) conductivity during mammalian (conformational) EC coupling was retained as an evolutionary remnant (vestigiality). Here, we wanted to test the hypothesis that due to the lack of evolutionary pressure in post-CICR species skeletal muscle DHPR Ca(2+) conductivity gradually reduced as evolution progressed. Interestingly, we identified that the DHPR of the early ray-finned fish sterlet (Acipenser ruthenus) is phylogenetically positioned above the mammalian rabbit DHPR which retained robust Ca(2+) conductivity, but below the euteleost zebrafish DHPR which completely lost Ca(2+) conductivity. Remarkably, our results revealed that sterlet DHPR still retained the Ca(2+) conductivity but currents are significantly reduced compared to rabbit. This decrease is due to lower DHPR membrane expression similar to zebrafish, as well as due to reduced channel open probability (Po). In both these fish species the lower DHPR expression density is partially compensated by higher efficacy of DHPR-RyR1 coupling. The complete loss of Po in zebrafish and other euteleost species was presumably based on the teleost specific 3rd round of genome duplication (Ts3R). Ts3R headed into the appearance of two skeletal muscle DHPR isoforms which finally, together with the radiation of the euteleost clade, fully lost the Po.</AbstractText><CopyrightInformation>Copyright © 2016 The Authors. Published by Elsevier Ltd.. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Schrötter</LastName><ForeName>Kai</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Department of Medical Genetics, Molecular and Clinical Pharmacology, Division of Biochemical Pharmacology, Medical University of Innsbruck, Peter Mayr Strasse 1, A-6020, Innsbruck, Austria.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dayal</LastName><ForeName>Anamika</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Medical Genetics, Molecular and Clinical Pharmacology, Division of Biochemical Pharmacology, Medical University of Innsbruck, Peter Mayr Strasse 1, A-6020, Innsbruck, Austria.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Grabner</LastName><ForeName>Manfred</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Department of Medical Genetics, Molecular and Clinical Pharmacology, Division of Biochemical Pharmacology, Medical University of Innsbruck, Peter Mayr Strasse 1, A-6020, Innsbruck, Austria. Electronic address: manfred.grabner@i-med.ac.at.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2016</Year><Month>10</Month><Day>23</Day></ArticleDate></Article><MedlineJournalInfo><Country>Netherlands</Country><MedlineTA>Cell Calcium</MedlineTA><NlmUniqueID>8006226</NlmUniqueID><ISSNLinking>0143-4160</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Calcium influx evolution</Keyword><Keyword MajorTopicYN="N">Excitation-contraction coupling</Keyword><Keyword MajorTopicYN="N">L-Type calcium channel</Keyword><Keyword MajorTopicYN="N">Skeletal muscle</Keyword><Keyword MajorTopicYN="N">Sterlet DHPR</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2016</Year><Month>09</Month><Day>15</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2016</Year><Month>10</Month><Day>21</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2016</Year><Month>10</Month><Day>21</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2016</Year><Month>10</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2016</Year><Month>10</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2016</Year><Month>10</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">27793347</ArticleId><ArticleId IdType="pii">S0143-4160(16)30163-4</ArticleId><ArticleId IdType="doi">10.1016/j.ceca.2016.10.002</ArticleId></ArticleIdList></PubmedData></pubmed></record>Pour manipuler ce document sous Unix (Dilib)
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