Receptor Activity-modifying Proteins 2 and 3 Generate Adrenomedullin Receptor Subtypes with Distinct Molecular Properties*
Identifieur interne : 000762 ( Pmc/Curation ); précédent : 000761; suivant : 000763Receptor Activity-modifying Proteins 2 and 3 Generate Adrenomedullin Receptor Subtypes with Distinct Molecular Properties*
Auteurs : Harriet A. Watkins ; Madhuri Chakravarthy ; Rekhati S. Abhayawardana ; Joseph J. Gingell ; Michael Garelja ; Meenakshi Pardamwar ; James M. W. R. Mcelhinney ; Alex Lathbridge ; Arran Constantine ; Paul W. R. Harris ; Tsz-Ying Yuen ; Margaret A. Brimble ; James Barwell ; David R. Poyner ; Michael J. Woolley ; Alex C. Conner ; Augen A. Pioszak ; Christopher A. Reynolds ; Debbie L. HaySource :
- The Journal of Biological Chemistry [ 0021-9258 ] ; 2016.
Abstract
Adrenomedullin (AM) is a peptide hormone with numerous effects in the vascular systems. AM signals through the AM1 and AM2 receptors formed by the obligate heterodimerization of a G protein-coupled receptor, the calcitonin receptor-like receptor (CLR), and receptor activity-modifying proteins 2 and 3 (RAMP2 and RAMP3), respectively. These different CLR-RAMP interactions yield discrete receptor pharmacology and physiological effects. The effective design of therapeutics that target the individual AM receptors is dependent on understanding the molecular details of the effects of RAMPs on CLR. To understand the role of RAMP2 and -3 on the activation and conformation of the CLR subunit of AM receptors, we mutated 68 individual amino acids in the juxtamembrane region of CLR, a key region for activation of AM receptors, and determined the effects on cAMP signaling. Sixteen CLR mutations had differential effects between the AM1 and AM2 receptors. Accompanying this, independent molecular modeling of the full-length AM-bound AM1 and AM2 receptors predicted differences in the binding pocket and differences in the electrostatic potential of the two AM receptors. Druggability analysis indicated unique features that could be used to develop selective small molecule ligands for each receptor. The interaction of RAMP2 or RAMP3 with CLR induces conformational variation in the juxtamembrane region, yielding distinct binding pockets, probably via an allosteric mechanism. These subtype-specific differences have implications for the design of therapeutics aimed at specific AM receptors and for understanding the mechanisms by which accessory proteins affect G protein-coupled receptor function.
Url:
DOI: 10.1074/jbc.M115.688218
PubMed: 27013657
PubMed Central: 4882435
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Receptor Activity-modifying Proteins 2 and 3 Generate Adrenomedullin Receptor Subtypes with Distinct Molecular Properties<xref ref-type="fn" rid="FN1">*</xref>
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<series><title level="j">The Journal of Biological Chemistry</title>
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<front><div type="abstract" xml:lang="en"><p>Adrenomedullin (AM) is a peptide hormone with numerous effects in the vascular systems. AM signals through the AM<sub>1</sub>
and AM<sub>2</sub>
receptors formed by the obligate heterodimerization of a G protein-coupled receptor, the calcitonin receptor-like receptor (CLR), and receptor activity-modifying proteins 2 and 3 (RAMP2 and RAMP3), respectively. These different CLR-RAMP interactions yield discrete receptor pharmacology and physiological effects. The effective design of therapeutics that target the individual AM receptors is dependent on understanding the molecular details of the effects of RAMPs on CLR. To understand the role of RAMP2 and -3 on the activation and conformation of the CLR subunit of AM receptors, we mutated 68 individual amino acids in the juxtamembrane region of CLR, a key region for activation of AM receptors, and determined the effects on cAMP signaling. Sixteen CLR mutations had differential effects between the AM<sub>1</sub>
and AM<sub>2</sub>
receptors. Accompanying this, independent molecular modeling of the full-length AM-bound AM<sub>1</sub>
and AM<sub>2</sub>
receptors predicted differences in the binding pocket and differences in the electrostatic potential of the two AM receptors. Druggability analysis indicated unique features that could be used to develop selective small molecule ligands for each receptor. The interaction of RAMP2 or RAMP3 with CLR induces conformational variation in the juxtamembrane region, yielding distinct binding pockets, probably via an allosteric mechanism. These subtype-specific differences have implications for the design of therapeutics aimed at specific AM receptors and for understanding the mechanisms by which accessory proteins affect G protein-coupled receptor function.</p>
</div>
</front>
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</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Biol Chem</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Biol. Chem</journal-id>
<journal-id journal-id-type="hwp">jbc</journal-id>
<journal-id journal-id-type="pmc">jbc</journal-id>
<journal-id journal-id-type="publisher-id">JBC</journal-id>
<journal-title-group><journal-title>The Journal of Biological Chemistry</journal-title>
</journal-title-group>
<issn pub-type="ppub">0021-9258</issn>
<issn pub-type="epub">1083-351X</issn>
<publisher><publisher-name>American Society for Biochemistry and Molecular Biology</publisher-name>
<publisher-loc>11200 Rockville Pike, Suite 302, Rockville, MD 20852-3110, U.S.A.</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27013657</article-id>
<article-id pub-id-type="pmc">4882435</article-id>
<article-id pub-id-type="publisher-id">M115.688218</article-id>
<article-id pub-id-type="doi">10.1074/jbc.M115.688218</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Signal Transduction</subject>
</subj-group>
</article-categories>
<title-group><article-title>Receptor Activity-modifying Proteins 2 and 3 Generate Adrenomedullin Receptor Subtypes with Distinct Molecular Properties<xref ref-type="fn" rid="FN1">*</xref>
<xref ref-type="fn" rid="FN2"><sup><inline-graphic xlink:href="sbox.jpg"></inline-graphic>
</sup>
</xref>
</article-title>
<alt-title alt-title-type="short">RAMP Effects on Adrenomedullin Receptors</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Watkins</surname>
<given-names>Harriet A.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
<xref ref-type="author-notes" rid="FN3"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chakravarthy</surname>
<given-names>Madhuri</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Abhayawardana</surname>
<given-names>Rekhati S.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gingell</surname>
<given-names>Joseph J.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Garelja</surname>
<given-names>Michael</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pardamwar</surname>
<given-names>Meenakshi</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>¶</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>McElhinney</surname>
<given-names>James M. W. R.</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>¶</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lathbridge</surname>
<given-names>Alex</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>¶</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Constantine</surname>
<given-names>Arran</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>¶</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Harris</surname>
<given-names>Paul W. R.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>‖</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yuen</surname>
<given-names>Tsz-Ying</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>‖</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Brimble</surname>
<given-names>Margaret A.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>‖</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Barwell</surname>
<given-names>James</given-names>
</name>
<xref ref-type="aff" rid="aff5">**</xref>
<xref ref-type="author-notes" rid="FN4"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Poyner</surname>
<given-names>David R.</given-names>
</name>
<xref ref-type="aff" rid="aff5">**</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Woolley</surname>
<given-names>Michael J.</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>‡‡</sup>
</xref>
<xref ref-type="author-notes" rid="FN5"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Conner</surname>
<given-names>Alex C.</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>‡‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pioszak</surname>
<given-names>Augen A.</given-names>
</name>
<xref ref-type="aff" rid="aff7"><sup>§§</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Reynolds</surname>
<given-names>Christopher A.</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>¶</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0002-9558-5122</contrib-id>
<name><surname>Hay</surname>
<given-names>Debbie L.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>‡</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>§</sup>
</xref>
<xref ref-type="author-notes" rid="FN3"><sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor2"><sup>5</sup>
</xref>
</contrib>
<aff id="aff1">From the<label>‡</label>
School of Biological Sciences,</aff>
<aff id="aff2">the<label>§</label>
Maurice Wilkins Centre for Molecular Biodiscovery, and</aff>
<aff id="aff3">the<label>‖</label>
School of Chemical Sciences, University of Auckland, Auckland 1010, New Zealand,</aff>
<aff id="aff4">the<label>¶</label>
School of Biological Sciences, University of Essex, Wivenhoe Park, Colchester CO4 3SQ, United Kingdom,</aff>
<aff id="aff5">the<label>**</label>
School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham B4 7ET, United Kingdom,</aff>
<aff id="aff6">the<label>‡‡</label>
School of Clinical and Experimental Medicine, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom,</aff>
<aff id="aff7">the<label>§§</label>
Department of Biochemistry and Molecular Biology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma 73104</aff>
</contrib-group>
<author-notes><corresp id="cor1"><label>4</label>
To whom correspondence may be addressed: <addr-line>School of Biological Sciences, University of Essex, Wivenhoe Park, Colchester CO4 3SQ, United Kingdom.</addr-line>
E-mail: <email>reync@essex.ac.uk</email>
.</corresp>
<corresp id="cor2"><label>5</label>
To whom correspondence may be addressed: <addr-line>School of Biological Sciences, University of Auckland, Auckland 1010, New Zealand.</addr-line>
E-mail: <email>dl.hay@auckland.ac.nz</email>
.</corresp>
<fn fn-type="supported-by" id="FN3"><label>1</label>
<p>Supported by the National Heart Foundation of New Zealand, the Maurice and Phyllis Paykel Trust, and the Maurice Wilkins Centre for Molecular Biodiscovery.</p>
</fn>
<fn fn-type="supported-by" id="FN4"><label>2</label>
<p>Supported by British Heart Foundation Grant FS/05/054.</p>
</fn>
<fn fn-type="supported-by" id="FN5"><label>3</label>
<p>Supported by British Heart Foundation Grant PG/12/59/29795.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>27</day>
<month>5</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="epub"><day>24</day>
<month>3</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>24</day>
<month>3</month>
<year>2016</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
. </pmc-comment>
<volume>291</volume>
<issue>22</issue>
<fpage>11657</fpage>
<lpage>11675</lpage>
<history><date date-type="received"><day>3</day>
<month>9</month>
<year>2015</year>
</date>
<date date-type="rev-recd"><day>20</day>
<month>3</month>
<year>2016</year>
</date>
</history>
<permissions><copyright-statement>© 2016 by The American Society for Biochemistry and Molecular Biology, Inc.</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>The American Society for Biochemistry and Molecular Biology, Inc.</copyright-holder>
<license license-type="open-access"><license-p><italic>Author's Choice</italic>
—Final version free via <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0">Creative Commons CC-BY license</ext-link>
.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="zbc02216011657.pdf"></self-uri>
<abstract><p>Adrenomedullin (AM) is a peptide hormone with numerous effects in the vascular systems. AM signals through the AM<sub>1</sub>
and AM<sub>2</sub>
receptors formed by the obligate heterodimerization of a G protein-coupled receptor, the calcitonin receptor-like receptor (CLR), and receptor activity-modifying proteins 2 and 3 (RAMP2 and RAMP3), respectively. These different CLR-RAMP interactions yield discrete receptor pharmacology and physiological effects. The effective design of therapeutics that target the individual AM receptors is dependent on understanding the molecular details of the effects of RAMPs on CLR. To understand the role of RAMP2 and -3 on the activation and conformation of the CLR subunit of AM receptors, we mutated 68 individual amino acids in the juxtamembrane region of CLR, a key region for activation of AM receptors, and determined the effects on cAMP signaling. Sixteen CLR mutations had differential effects between the AM<sub>1</sub>
and AM<sub>2</sub>
receptors. Accompanying this, independent molecular modeling of the full-length AM-bound AM<sub>1</sub>
and AM<sub>2</sub>
receptors predicted differences in the binding pocket and differences in the electrostatic potential of the two AM receptors. Druggability analysis indicated unique features that could be used to develop selective small molecule ligands for each receptor. The interaction of RAMP2 or RAMP3 with CLR induces conformational variation in the juxtamembrane region, yielding distinct binding pockets, probably via an allosteric mechanism. These subtype-specific differences have implications for the design of therapeutics aimed at specific AM receptors and for understanding the mechanisms by which accessory proteins affect G protein-coupled receptor function.</p>
</abstract>
<kwd-group><kwd>allosteric regulation</kwd>
<kwd>cardiovascular disease</kwd>
<kwd>conformational change</kwd>
<kwd>G protein-coupled receptor (GPCR)</kwd>
<kwd>molecular modeling</kwd>
<kwd>GPCR</kwd>
<kwd>RAMP</kwd>
<kwd>adrenomedullin</kwd>
<kwd>extracellular loops</kwd>
<kwd>receptor activity-modifying protein</kwd>
</kwd-group>
<funding-group><award-group id="award1"><funding-source>Biotechnology and Biological Sciences Research Council
<named-content content-type="funder-id">http://dx.doi.org/10.13039/501100000268</named-content>
</funding-source>
<award-id>BB/M006883/1</award-id>
<award-id>BB/M007529/1</award-id>
<award-id>BB/M000176/1</award-id>
</award-group>
<award-group id="award2"><funding-source>British Heart Foundation
<named-content content-type="funder-id">http://dx.doi.org/10.13039/501100000274</named-content>
</funding-source>
<award-id>FS/05/054</award-id>
<award-id>PG/12/59/29795</award-id>
</award-group>
<award-group id="award3"><funding-source>National Heart Foundation of New Zealand
<named-content content-type="funder-id">http://dx.doi.org/10.13039/501100001516</named-content>
</funding-source>
</award-group>
<award-group id="award4"><funding-source>Maurice Wilkins Centre for Molecular Biodiscovery</funding-source>
</award-group>
<award-group id="award5"><funding-source>Maurice and Phyllis Paykel Trust
<named-content content-type="funder-id">http://dx.doi.org/10.13039/501100001518</named-content>
</funding-source>
</award-group>
</funding-group>
</article-meta>
</front>
</pmc>
</record>
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