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      A Novel Glucagon-Related Peptide (GCRP) and Its Receptor GCRPR Account for Coevolution of Their Family Members in Vertebrates

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          Abstract

          The glucagon (GCG) peptide family consists of GCG, glucagon-like peptide 1 (GLP1), and GLP2, which are derived from a common GCG precursor, and the glucose-dependent insulinotropic polypeptide (GIP). These peptides interact with cognate receptors, GCGR, GLP1R, GLP2R, and GIPR, which belong to the secretin-like G protein-coupled receptor (GPCR) family. We used bioinformatics to identify genes encoding a novel GCG-related peptide (GCRP) and its cognate receptor, GCRPR. The GCRP and GCRPR genes were found in representative tetrapod taxa such as anole lizard, chicken, and Xenopus, and in teleosts including medaka, fugu, tetraodon, and stickleback. However, they were not present in mammals and zebrafish. Phylogenetic and genome synteny analyses showed that GCRP emerged through two rounds of whole genome duplication (2R) during early vertebrate evolution. GCRPR appears to have arisen by local tandem gene duplications from a common ancestor of GCRPR, GCGR, and GLP2R after 2R. Biochemical ligand-receptor interaction analyses revealed that GCRP had the highest affinity for GCRPR in comparison to other GCGR family members. Stimulation of chicken, Xenopus, and medaka GCRPRs activated Gα s-mediated signaling. In contrast to chicken and Xenopus GCRPRs, medaka GCRPR also induced Gα q/11-mediated signaling. Chimeric peptides and receptors showed that the K 16M 17K 18 and G 16Q 17A 18 motifs in GCRP and GLP1, respectively, may at least in part contribute to specific recognition of their cognate receptors through interaction with the receptor core domain. In conclusion, we present novel data demonstrating that GCRP and GCRPR evolved through gene/genome duplications followed by specific modifications that conferred selective recognition to this ligand-receptor pair.

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          Author and article information

          Contributors
          Role: Editor
          Journal
          PLoS One
          PLoS ONE
          plos
          plosone
          PLoS ONE
          Public Library of Science (San Francisco, USA )
          1932-6203
          2013
          11 June 2013
          : 8
          : 6
          Affiliations
          [1 ]Laboratory of G-protein Coupled Receptors, Graduate School of Medicine Korea University, Seoul, Republic of Korea
          [2 ]Mammal Research Institute, Department of Zoology & Entomology, University of Pretoria, Hatfield, South Africa
          [3 ]Medical Research Council Receptor Biology Unit, University of Cape Town, Observatory 7925, South Africa
          [4 ]Centre for Integrative Physiology, University of Edinburgh, Edinburgh, Scotland
          Van Andel Research Institute, United States of America
          Author notes

          Competing Interests: The authors have declared that no competing interests exist.

          Conceived and designed the experiments: CRP MJM RPM JIH JYS. Performed the experiments: CRP MJM SP DKK EBC. Analyzed the data: CRP MJM JIH JYS. Contributed reagents/materials/analysis tools: JIH JYS. Wrote the paper: RPM JIH JYS.

          Article
          PONE-D-13-13774
          10.1371/journal.pone.0065420
          3679108
          23776481

          This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

          Page count
          Pages: 13
          Funding
          This work was supported by grants from the Brain Research Program (2011–0019205), Basic Research Program (2010–0022054) and Korea-South Africa Collaboration Program (2012K1A3A1A09033014) of the National Research Foundation of Korea and the National Research Foundation of South Africa. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
          Categories
          Research Article
          Biology
          Biochemistry
          Neurochemistry
          Neurochemicals
          Neuropeptides
          Biomacromolecule-Ligand Interactions
          Computational Biology
          Genomics
          Genome Evolution
          Evolutionary Biology
          Evolutionary Systematics
          Phylogenetics
          Genomics
          Genome Evolution
          Molecular Cell Biology
          Signal Transduction
          Membrane Receptor Signaling
          Hormone Receptor Signaling
          Mathematics
          Statistics
          Biostatistics

          Uncategorized

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