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Evidence for Conservation of the Calcitonin Superfamily and Activity-regulating Mechanisms in the Basal Chordate Branchiostoma floridae: INSIGHTS INTO THE MOLECULAR AND FUNCTIONAL EVOLUTION IN CHORDATES

J Biol Chem. 2016 Jan 29;291(5):2345-56. doi: 10.1074/jbc.M115.664003. Epub 2015 Dec 7.

Abstract

The calcitonin (CT)/CT gene-related peptide (CGRP) family is conserved in vertebrates. The activities of this peptide family are regulated by a combination of two receptors, namely the calcitonin receptor (CTR) and the CTR-like receptor (CLR), and three receptor activity-modifying proteins (RAMPs). Furthermore, RAMPs act as escort proteins by translocating CLR to the cell membrane. Recently, CT/CGRP family peptides have been identified or inferred in several invertebrates. However, the molecular characteristics and relevant functions of the CTR/CLR and RAMPs in invertebrates remain unclear. In this study, we identified three CT/CGRP family peptides (Bf-CTFPs), one CTR/CLR-like receptor (Bf-CTFP-R), and three RAMP-like proteins (Bf-RAMP-LPs) in the basal chordate amphioxus (Branchiostoma floridae). The Bf-CTFPs were shown to possess an N-terminal circular region typical of the CT/CGRP family and a C-terminal Pro-NH2. The Bf-CTFP genes were expressed in the central nervous system and in endocrine cells of the midgut, indicating that Bf-CTFPs serve as brain and/or gut peptides. Cell surface expression of the Bf-CTFP-R was enhanced by co-expression with each Bf-RAMP-LP. Furthermore, Bf-CTFPs activated Bf-CTFP-R·Bf-RAMP-LP complexes, resulting in cAMP accumulation. These results confirmed that Bf-RAMP-LPs, like vertebrate RAMPs, are prerequisites for the function and translocation of the Bf-CTFP-R. The relative potencies of the three peptides at each receptor were similar. Bf-CTFP2 was a potent ligand at all receptors in cAMP assays. Bf-RAMP-LP effects on ligand potency order were distinct to vertebrate CGRP/adrenomedullin/amylin receptors. To the best of our knowledge, this is the first molecular and functional characterization of an authentic invertebrate CT/CGRP family receptor and RAMPs.

Keywords: G protein-coupled receptor (GPCR); amphioxus; calcitonin; chordate; molecular evolution; protein evolution; receptor activity-modifying protein; receptor modification; receptor regulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adrenomedullin / metabolism
  • Amino Acid Sequence
  • Animals
  • COS Cells
  • Calcitonin / genetics*
  • Calcitonin / metabolism*
  • Calcitonin Gene-Related Peptide / metabolism
  • Calcitonin Receptor-Like Protein / metabolism
  • Cell Membrane / metabolism
  • Central Nervous System / metabolism
  • Chlorocebus aethiops
  • Chordata
  • Cloning, Molecular
  • Cyclic AMP / metabolism
  • Evolution, Molecular*
  • Flow Cytometry
  • Gene Expression Regulation*
  • HEK293 Cells
  • Humans
  • Intestinal Mucosa / metabolism
  • Islet Amyloid Polypeptide / metabolism
  • Lancelets / metabolism*
  • Molecular Sequence Data
  • Multigene Family*
  • Open Reading Frames
  • Phylogeny
  • Protein Structure, Tertiary
  • Receptor Activity-Modifying Proteins / metabolism
  • Receptors, Calcitonin / metabolism
  • Sequence Homology, Amino Acid

Substances

  • Calcitonin Receptor-Like Protein
  • Islet Amyloid Polypeptide
  • Receptor Activity-Modifying Proteins
  • Receptors, Calcitonin
  • Adrenomedullin
  • Calcitonin
  • Cyclic AMP
  • Calcitonin Gene-Related Peptide