Prolonged Calcitonin Receptor Signaling by Salmon, but Not Human Calcitonin, Reveals Ligand Bias
Identifieur interne : 003595 ( Main/Exploration ); précédent : 003594; suivant : 003596Prolonged Calcitonin Receptor Signaling by Salmon, but Not Human Calcitonin, Reveals Ligand Bias
Auteurs : Kim Vietz Andreassen [Danemark] ; Sara Toftegaard Hjuler [Danemark] ; Sebastian G. Furness [Australie] ; Patrick M. Sexton [Australie] ; Arthur Christopoulos [Australie] ; Olivier Nosjean [France] ; Morten Asser Karsdal [Danemark] ; Kim Henriksen [Danemark]Source :
- PLoS ONE [ 1932-6203 ] ; 2014.
Descripteurs français
- KwdFr :
- AMP cyclique (métabolisme), Animaux, Arrestines (génétique), Arrestines (métabolisme), Calcitonine (génétique), Calcitonine (métabolisme), Facteurs temps, Humains, Ligands, Lignée cellulaire, Récepteurs à la calcitonine (génétique), Récepteurs à la calcitonine (métabolisme), Régulation de l'expression des gènes, Saumon, Spécificité d'espèce, Transduction du signal (génétique), Transgènes, Transport de protéines, bêta-Arrestines.
- MESH :
- génétique : Arrestines, Calcitonine, Récepteurs à la calcitonine, Transduction du signal.
- métabolisme : AMP cyclique, Arrestines, Calcitonine, Récepteurs à la calcitonine.
- Animaux, Facteurs temps, Humains, Ligands, Lignée cellulaire, Régulation de l'expression des gènes, Saumon, Spécificité d'espèce, Transgènes, Transport de protéines, bêta-Arrestines.
English descriptors
- KwdEn :
- Animals, Arrestins (genetics), Arrestins (metabolism), Calcitonin (genetics), Calcitonin (metabolism), Cell Line, Cyclic AMP (metabolism), Gene Expression Regulation, Humans, Ligands, Protein Transport, Receptors, Calcitonin (genetics), Receptors, Calcitonin (metabolism), Salmon, Signal Transduction (genetics), Species Specificity, Time Factors, Transgenes, beta-Arrestins.
- MESH :
- chemical , genetics : Arrestins, Calcitonin, Receptors, Calcitonin.
- chemical , metabolism : Arrestins, Calcitonin, Cyclic AMP, Receptors, Calcitonin.
- genetics : Signal Transduction.
- Animals, Cell Line, Gene Expression Regulation, Humans, Ligands, Protein Transport, Salmon, Species Specificity, Time Factors, Transgenes, beta-Arrestins.
Abstract
Salmon calcitonin (sCT) and human calcitonin (hCT) are pharmacologically distinct. However, the reason for the differences is unclear. Here we analyze the differences between sCT and hCT on the human calcitonin receptor (CT(a)R) with respect to activation of cAMP signaling, β-arrestin recruitment, ligand binding kinetics and internalization. The study was conducted using mammalian cell lines heterologously expressing the human CT(a) receptor. CT(a)R downstream signaling was investigated with dose response profiles for cAMP production and β-arrestin recruitment for sCT and hCT during short term (<2 hours) and prolonged (up to 72 hours) stimulation. CT(a)R kinetics and internalization was investigated with radio-labeled sCT and hCT ligands on cultured cells and isolated membrane preparations from the same cell line. We found that sCT and hCT are equipotent during short-term stimulations with differences manifesting themselves only during long-term stimulation with sCT inducing a prolonged activation up to 72 hours, while hCT loses activity markedly earlier. The prolonged sCT stimulation of both cAMP accumulation and β-arrestin recruitment was attenuated, but not abrogated by acid wash, suggesting a role for sCT activated internalized receptors. We have demonstrated a novel phenomenon, namely that two distinct CT(a)R downstream signaling activation patterns are activated by two related ligands, thereby highlighting qualitatively different signaling responses in vitro that could have implications for sCT use in vivo.
Url:
DOI: 10.1371/journal.pone.0092042
PubMed: 24643196
PubMed Central: 3958426
Affiliations:
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Monash Institute of Pharmaceutical Sciences, Monash University, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation></author><author><name sortKey="Nosjean, Olivier" sort="Nosjean, Olivier" uniqKey="Nosjean O" first="Olivier" last="Nosjean">Olivier Nosjean</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>Institut de Recherches Servier, Croissy-sur-Seine, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut de Recherches Servier, Croissy-sur-Seine</wicri:regionArea><wicri:noRegion>Croissy-sur-Seine</wicri:noRegion><wicri:noRegion>Croissy-sur-Seine</wicri:noRegion></affiliation></author><author><name sortKey="Karsdal, Morten Asser" sort="Karsdal, Morten Asser" uniqKey="Karsdal M" first="Morten Asser" last="Karsdal">Morten Asser Karsdal</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Nordic Bioscience A/S, Herlev, Denmark</addr-line></nlm:aff><country xml:lang="fr">Danemark</country><wicri:regionArea>Nordic Bioscience A/S, Herlev</wicri:regionArea><wicri:noRegion>Herlev</wicri:noRegion></affiliation></author><author><name sortKey="Henriksen, Kim" sort="Henriksen, Kim" uniqKey="Henriksen K" first="Kim" last="Henriksen">Kim Henriksen</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Nordic Bioscience A/S, Herlev, Denmark</addr-line></nlm:aff><country xml:lang="fr">Danemark</country><wicri:regionArea>Nordic Bioscience A/S, Herlev</wicri:regionArea><wicri:noRegion>Herlev</wicri:noRegion></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Arrestins (genetics)</term><term>Arrestins (metabolism)</term><term>Calcitonin (genetics)</term><term>Calcitonin (metabolism)</term><term>Cell Line</term><term>Cyclic AMP (metabolism)</term><term>Gene Expression Regulation</term><term>Humans</term><term>Ligands</term><term>Protein Transport</term><term>Receptors, Calcitonin (genetics)</term><term>Receptors, Calcitonin (metabolism)</term><term>Salmon</term><term>Signal Transduction (genetics)</term><term>Species Specificity</term><term>Time Factors</term><term>Transgenes</term><term>beta-Arrestins</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>AMP cyclique (métabolisme)</term><term>Animaux</term><term>Arrestines (génétique)</term><term>Arrestines (métabolisme)</term><term>Calcitonine (génétique)</term><term>Calcitonine (métabolisme)</term><term>Facteurs temps</term><term>Humains</term><term>Ligands</term><term>Lignée cellulaire</term><term>Récepteurs à la calcitonine (génétique)</term><term>Récepteurs à la calcitonine (métabolisme)</term><term>Régulation de l'expression des gènes</term><term>Saumon</term><term>Spécificité d'espèce</term><term>Transduction du signal (génétique)</term><term>Transgènes</term><term>Transport de protéines</term><term>bêta-Arrestines</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Arrestins</term><term>Calcitonin</term><term>Receptors, Calcitonin</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Arrestins</term><term>Calcitonin</term><term>Cyclic AMP</term><term>Receptors, Calcitonin</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Signal Transduction</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Arrestines</term><term>Calcitonine</term><term>Récepteurs à la calcitonine</term><term>Transduction du signal</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>AMP cyclique</term><term>Arrestines</term><term>Calcitonine</term><term>Récepteurs à la calcitonine</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Cell Line</term><term>Gene Expression Regulation</term><term>Humans</term><term>Ligands</term><term>Protein Transport</term><term>Salmon</term><term>Species Specificity</term><term>Time Factors</term><term>Transgenes</term><term>beta-Arrestins</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Animaux</term><term>Facteurs temps</term><term>Humains</term><term>Ligands</term><term>Lignée cellulaire</term><term>Régulation de l'expression des gènes</term><term>Saumon</term><term>Spécificité d'espèce</term><term>Transgènes</term><term>Transport de protéines</term><term>bêta-Arrestines</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Salmon calcitonin (sCT) and human calcitonin (hCT) are pharmacologically distinct. However, the reason for the differences is unclear. Here we analyze the differences between sCT and hCT on the human calcitonin receptor (CT<sub>(a)</sub>R) with respect to activation of cAMP signaling, β-arrestin recruitment, ligand binding kinetics and internalization. The study was conducted using mammalian cell lines heterologously expressing the human CT<sub>(a)</sub> receptor. CT<sub>(a)</sub>R downstream signaling was investigated with dose response profiles for cAMP production and β-arrestin recruitment for sCT and hCT during short term (<2 hours) and prolonged (up to 72 hours) stimulation. CT<sub>(a)</sub>R kinetics and internalization was investigated with radio-labeled sCT and hCT ligands on cultured cells and isolated membrane preparations from the same cell line. We found that sCT and hCT are equipotent during short-term stimulations with differences manifesting themselves only during long-term stimulation with sCT inducing a prolonged activation up to 72 hours, while hCT loses activity markedly earlier. The prolonged sCT stimulation of both cAMP accumulation and β-arrestin recruitment was attenuated, but not abrogated by acid wash, suggesting a role for sCT activated internalized receptors. We have demonstrated a novel phenomenon, namely that two distinct CT<sub>(a)</sub>R downstream signaling activation patterns are activated by two related ligands, thereby highlighting qualitatively different signaling responses in vitro that could have implications for sCT use in vivo.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Pham, Vi" uniqKey="Pham V">VI Pham</name></author><author><name sortKey="Sexton, Pm" uniqKey="Sexton P">PM Sexton</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Poyner, Dr" uniqKey="Poyner D">DR Poyner</name></author><author><name sortKey="Sexton, Pm" uniqKey="Sexton P">PM Sexton</name></author><author><name sortKey="Marshall, I" uniqKey="Marshall I">I Marshall</name></author><author><name sortKey="Smith, Dm" uniqKey="Smith D">DM Smith</name></author><author><name sortKey="Quirion, R" uniqKey="Quirion R">R Quirion</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sexton, Pm" uniqKey="Sexton P">PM Sexton</name></author><author><name sortKey="Findlay, Dm" uniqKey="Findlay D">DM Findlay</name></author><author><name sortKey="Martin, Tj" uniqKey="Martin T">TJ Martin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chakraborty, M" uniqKey="Chakraborty M">M Chakraborty</name></author><author><name sortKey="Chatterjee, D" uniqKey="Chatterjee D">D Chatterjee</name></author><author><name sortKey="Kellokumpu, S" uniqKey="Kellokumpu S">S Kellokumpu</name></author><author><name sortKey="Rasmussen, H" uniqKey="Rasmussen H">H Rasmussen</name></author><author><name sortKey="Baron, R" uniqKey="Baron R">R Baron</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Su, Y" uniqKey="Su Y">Y Su</name></author><author><name sortKey="Chakraborty, M" uniqKey="Chakraborty M">M Chakraborty</name></author><author><name sortKey="Nathanson, Mh" uniqKey="Nathanson M">MH Nathanson</name></author><author><name sortKey="Baron, R" uniqKey="Baron R">R Baron</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chen, Y" uniqKey="Chen Y">Y Chen</name></author><author><name sortKey="Shyu, Jf" uniqKey="Shyu J">JF Shyu</name></author><author><name sortKey="Santhanagopal, A" uniqKey="Santhanagopal A">A Santhanagopal</name></author><author><name sortKey="Inoue, D" uniqKey="Inoue D">D Inoue</name></author><author><name sortKey="David, Jp" uniqKey="David J">JP David</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chakraborty, M" uniqKey="Chakraborty M">M Chakraborty</name></author><author><name sortKey="Chatterjee, D" uniqKey="Chatterjee D">D Chatterjee</name></author><author><name sortKey="Gorelick, Fs" uniqKey="Gorelick F">FS Gorelick</name></author><author><name sortKey="Baron, R" uniqKey="Baron R">R 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Morton</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dong, M" uniqKey="Dong M">M Dong</name></author><author><name sortKey="Pinon, Di" uniqKey="Pinon D">DI Pinon</name></author><author><name sortKey="Cox, Rf" uniqKey="Cox R">RF Cox</name></author><author><name sortKey="Miller, Lj" uniqKey="Miller L">LJ Miller</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dong, M" uniqKey="Dong M">M Dong</name></author><author><name sortKey="Pinon, Di" uniqKey="Pinon D">DI Pinon</name></author><author><name sortKey="Cox, Rf" uniqKey="Cox R">RF Cox</name></author><author><name sortKey="Miller, Lj" uniqKey="Miller L">LJ Miller</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chambers, Tj" uniqKey="Chambers T">TJ Chambers</name></author><author><name sortKey="Chambers, Jc" uniqKey="Chambers J">JC Chambers</name></author><author><name sortKey="Symonds, J" uniqKey="Symonds J">J Symonds</name></author><author><name sortKey="Darby, Ja" uniqKey="Darby J">JA Darby</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>Australie</li><li>Danemark</li><li>France</li></country></list><tree><country name="Danemark"><noRegion><name sortKey="Andreassen, Kim Vietz" sort="Andreassen, Kim Vietz" uniqKey="Andreassen K" first="Kim Vietz" last="Andreassen">Kim Vietz Andreassen</name></noRegion><name sortKey="Henriksen, Kim" sort="Henriksen, Kim" uniqKey="Henriksen K" first="Kim" last="Henriksen">Kim Henriksen</name><name sortKey="Hjuler, Sara Toftegaard" sort="Hjuler, Sara Toftegaard" uniqKey="Hjuler S" first="Sara Toftegaard" last="Hjuler">Sara Toftegaard Hjuler</name><name sortKey="Karsdal, Morten Asser" sort="Karsdal, Morten Asser" uniqKey="Karsdal M" first="Morten Asser" last="Karsdal">Morten Asser Karsdal</name></country><country name="Australie"><noRegion><name sortKey="Furness, Sebastian G" sort="Furness, Sebastian G" uniqKey="Furness S" first="Sebastian G." last="Furness">Sebastian G. Furness</name></noRegion><name sortKey="Christopoulos, Arthur" sort="Christopoulos, Arthur" uniqKey="Christopoulos A" first="Arthur" last="Christopoulos">Arthur Christopoulos</name><name sortKey="Sexton, Patrick M" sort="Sexton, Patrick M" uniqKey="Sexton P" first="Patrick M." last="Sexton">Patrick M. Sexton</name></country><country name="France"><noRegion><name sortKey="Nosjean, Olivier" sort="Nosjean, Olivier" uniqKey="Nosjean O" first="Olivier" last="Nosjean">Olivier Nosjean</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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