δ-Conotoxin SuVIA suggests an evolutionary link between ancestral predator defence and the origin of fish-hunting behaviour in carnivorous cone snails.
Identifieur interne : 002B43 ( PubMed/Corpus ); précédent : 002B42; suivant : 002B44δ-Conotoxin SuVIA suggests an evolutionary link between ancestral predator defence and the origin of fish-hunting behaviour in carnivorous cone snails.
Auteurs : Ai-Hua Jin ; Mathilde R. Israel ; Marco C. Inserra ; Jennifer J. Smith ; Richard J. Lewis ; Paul F. Alewood ; Irina Vetter ; Sébastien DutertreSource :
- Proceedings. Biological sciences [ 1471-2954 ] ; 2015.
English descriptors
- KwdEn :
- MESH :
- chemical , genetics : Conotoxins.
- chemical , metabolism : Conotoxins.
- chemical , pharmacology : Conotoxins.
- genetics : Conus Snail.
- physiology : Conus Snail, Mice.
- Amino Acid Sequence, Animals, Biological Evolution, Male, Mice, Inbred C57BL, Pain, Predatory Behavior, Sequence Alignment.
Abstract
Some venomous cone snails feed on small fishes using an immobilizing combination of synergistic venom peptides that target Kv and Nav channels. As part of this envenomation strategy, δ-conotoxins are potent ichtyotoxins that enhance Nav channel function. δ-Conotoxins belong to an ancient and widely distributed gene superfamily, but any evolutionary link from ancestral worm-eating cone snails to modern piscivorous species has not been elucidated. Here, we report the discovery of SuVIA, a potent vertebrate-active δ-conotoxin characterized from a vermivorous cone snail (Conus suturatus). SuVIA is equipotent at hNaV1.3, hNaV1.4 and hNaV1.6 with EC50s in the low nanomolar range. SuVIA also increased peak hNaV1.7 current by approximately 75% and shifted the voltage-dependence of activation to more hyperpolarized potentials from -15 mV to -25 mV, with little effect on the voltage-dependence of inactivation. Interestingly, the proximal venom gland expression and pain-inducing effect of SuVIA in mammals suggest that δ-conotoxins in vermivorous cone snails play a defensive role against higher order vertebrates. We propose that δ-conotoxins originally evolved in ancestral vermivorous cones to defend against larger predators including fishes have been repurposed to facilitate a shift to piscivorous behaviour, suggesting an unexpected underlying mechanism for this remarkable evolutionary transition.
DOI: 10.1098/rspb.2015.0817
PubMed: 26156767
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pubmed:26156767Le document en format XML
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Inserra</name><affiliation><nlm:affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia The School of Pharmacy, The University of Queensland, Woolloongabba, Queensland 4102, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Smith, Jennifer J" sort="Smith, Jennifer J" uniqKey="Smith J" first="Jennifer J" last="Smith">Jennifer J. Smith</name><affiliation><nlm:affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Lewis, Richard J" sort="Lewis, Richard J" uniqKey="Lewis R" first="Richard J" last="Lewis">Richard J. 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Israel</name><affiliation><nlm:affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Inserra, Marco C" sort="Inserra, Marco C" uniqKey="Inserra M" first="Marco C" last="Inserra">Marco C. Inserra</name><affiliation><nlm:affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia The School of Pharmacy, The University of Queensland, Woolloongabba, Queensland 4102, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Smith, Jennifer J" sort="Smith, Jennifer J" uniqKey="Smith J" first="Jennifer J" last="Smith">Jennifer J. Smith</name><affiliation><nlm:affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Lewis, Richard J" sort="Lewis, Richard J" uniqKey="Lewis R" first="Richard J" last="Lewis">Richard J. Lewis</name><affiliation><nlm:affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Alewood, Paul F" sort="Alewood, Paul F" uniqKey="Alewood P" first="Paul F" last="Alewood">Paul F. Alewood</name><affiliation><nlm:affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Vetter, Irina" sort="Vetter, Irina" uniqKey="Vetter I" first="Irina" last="Vetter">Irina Vetter</name><affiliation><nlm:affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia The School of Pharmacy, The University of Queensland, Woolloongabba, Queensland 4102, Australia i.vetter@uq.edu.au.</nlm:affiliation></affiliation></author><author><name sortKey="Dutertre, Sebastien" sort="Dutertre, Sebastien" uniqKey="Dutertre S" first="Sébastien" last="Dutertre">Sébastien Dutertre</name><affiliation><nlm:affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia Institut des Biomolécules Max Mousseron, UMR 5247, Université Montpellier - CNRS, Place Eugène Bataillon, Montpellier Cedex 5 34095, France sebastien.dutertre@univ-montp2.fr.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Proceedings. Biological sciences</title><idno type="eISSN">1471-2954</idno><imprint><date when="2015" type="published">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Amino Acid Sequence</term><term>Animals</term><term>Biological Evolution</term><term>Conotoxins (genetics)</term><term>Conotoxins (metabolism)</term><term>Conotoxins (pharmacology)</term><term>Conus Snail (genetics)</term><term>Conus Snail (physiology)</term><term>Male</term><term>Mice (physiology)</term><term>Mice, Inbred C57BL</term><term>Pain</term><term>Predatory Behavior</term><term>Sequence Alignment</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Conotoxins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Conotoxins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Conotoxins</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Conus Snail</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Conus Snail</term><term>Mice</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Amino Acid Sequence</term><term>Animals</term><term>Biological Evolution</term><term>Male</term><term>Mice, Inbred C57BL</term><term>Pain</term><term>Predatory Behavior</term><term>Sequence Alignment</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Some venomous cone snails feed on small fishes using an immobilizing combination of synergistic venom peptides that target Kv and Nav channels. As part of this envenomation strategy, δ-conotoxins are potent ichtyotoxins that enhance Nav channel function. δ-Conotoxins belong to an ancient and widely distributed gene superfamily, but any evolutionary link from ancestral worm-eating cone snails to modern piscivorous species has not been elucidated. Here, we report the discovery of SuVIA, a potent vertebrate-active δ-conotoxin characterized from a vermivorous cone snail (Conus suturatus). SuVIA is equipotent at hNaV1.3, hNaV1.4 and hNaV1.6 with EC50s in the low nanomolar range. SuVIA also increased peak hNaV1.7 current by approximately 75% and shifted the voltage-dependence of activation to more hyperpolarized potentials from -15 mV to -25 mV, with little effect on the voltage-dependence of inactivation. Interestingly, the proximal venom gland expression and pain-inducing effect of SuVIA in mammals suggest that δ-conotoxins in vermivorous cone snails play a defensive role against higher order vertebrates. We propose that δ-conotoxins originally evolved in ancestral vermivorous cones to defend against larger predators including fishes have been repurposed to facilitate a shift to piscivorous behaviour, suggesting an unexpected underlying mechanism for this remarkable evolutionary transition.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">26156767</PMID><DateCreated><Year>2015</Year><Month>07</Month><Day>09</Day></DateCreated><DateCompleted><Year>2016</Year><Month>04</Month><Day>14</Day></DateCompleted><DateRevised><Year>2016</Year><Month>10</Month><Day>18</Day></DateRevised><Article PubModel="Print"><Journal><ISSN IssnType="Electronic">1471-2954</ISSN><JournalIssue CitedMedium="Internet"><Volume>282</Volume><Issue>1811</Issue><PubDate><Year>2015</Year><Month>Jul</Month><Day>22</Day></PubDate></JournalIssue><Title>Proceedings. Biological sciences</Title><ISOAbbreviation>Proc. Biol. Sci.</ISOAbbreviation></Journal><ArticleTitle>δ-Conotoxin SuVIA suggests an evolutionary link between ancestral predator defence and the origin of fish-hunting behaviour in carnivorous cone snails.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1098/rspb.2015.0817</ELocationID><ELocationID EIdType="pii" ValidYN="Y">20150817</ELocationID><Abstract><AbstractText>Some venomous cone snails feed on small fishes using an immobilizing combination of synergistic venom peptides that target Kv and Nav channels. As part of this envenomation strategy, δ-conotoxins are potent ichtyotoxins that enhance Nav channel function. δ-Conotoxins belong to an ancient and widely distributed gene superfamily, but any evolutionary link from ancestral worm-eating cone snails to modern piscivorous species has not been elucidated. Here, we report the discovery of SuVIA, a potent vertebrate-active δ-conotoxin characterized from a vermivorous cone snail (Conus suturatus). SuVIA is equipotent at hNaV1.3, hNaV1.4 and hNaV1.6 with EC50s in the low nanomolar range. SuVIA also increased peak hNaV1.7 current by approximately 75% and shifted the voltage-dependence of activation to more hyperpolarized potentials from -15 mV to -25 mV, with little effect on the voltage-dependence of inactivation. Interestingly, the proximal venom gland expression and pain-inducing effect of SuVIA in mammals suggest that δ-conotoxins in vermivorous cone snails play a defensive role against higher order vertebrates. We propose that δ-conotoxins originally evolved in ancestral vermivorous cones to defend against larger predators including fishes have been repurposed to facilitate a shift to piscivorous behaviour, suggesting an unexpected underlying mechanism for this remarkable evolutionary transition.</AbstractText><CopyrightInformation>© 2015 The Author(s) Published by the Royal Society. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Jin</LastName><ForeName>Ai-Hua</ForeName><Initials>AH</Initials><AffiliationInfo><Affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Israel</LastName><ForeName>Mathilde R</ForeName><Initials>MR</Initials><AffiliationInfo><Affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Inserra</LastName><ForeName>Marco C</ForeName><Initials>MC</Initials><AffiliationInfo><Affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia The School of Pharmacy, The University of Queensland, Woolloongabba, Queensland 4102, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Smith</LastName><ForeName>Jennifer J</ForeName><Initials>JJ</Initials><AffiliationInfo><Affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lewis</LastName><ForeName>Richard J</ForeName><Initials>RJ</Initials><AffiliationInfo><Affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Alewood</LastName><ForeName>Paul F</ForeName><Initials>PF</Initials><AffiliationInfo><Affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vetter</LastName><ForeName>Irina</ForeName><Initials>I</Initials><AffiliationInfo><Affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia The School of Pharmacy, The University of Queensland, Woolloongabba, Queensland 4102, Australia i.vetter@uq.edu.au.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dutertre</LastName><ForeName>Sébastien</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>The Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia Institut des Biomolécules Max Mousseron, UMR 5247, Université Montpellier - CNRS, Place Eugène Bataillon, Montpellier Cedex 5 34095, France sebastien.dutertre@univ-montp2.fr.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research 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Version="1">24131469</PMID></CommentsCorrections></CommentsCorrectionsList><MeshHeadingList><MeshHeading><DescriptorName UI="D000595" MajorTopicYN="N">Amino Acid Sequence</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005075" MajorTopicYN="Y">Biological Evolution</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D020916" MajorTopicYN="N">Conotoxins</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName><QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D052078" MajorTopicYN="N">Conus Snail</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008297" MajorTopicYN="N">Male</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D051379" MajorTopicYN="N">Mice</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008810" MajorTopicYN="N">Mice, Inbred C57BL</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010146" MajorTopicYN="Y">Pain</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D011235" MajorTopicYN="Y">Predatory Behavior</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D016415" MajorTopicYN="N">Sequence Alignment</DescriptorName></MeshHeading></MeshHeadingList><OtherID Source="NLM">PMC4528551</OtherID><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">conotoxin</Keyword><Keyword MajorTopicYN="N">defence</Keyword><Keyword MajorTopicYN="N">molecular evolution</Keyword><Keyword MajorTopicYN="N">predation</Keyword><Keyword 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