Protein-protein interaction and not glycosylation determines the binding selectivity of heterodimers between the calcitonin receptor-like receptor and the receptor activity-modifying proteins

J Biol Chem. 2001 Aug 3;276(31):29575-81. doi: 10.1074/jbc.M102722200. Epub 2001 May 31.

Abstract

The receptor activity-modifying proteins (RAMPs) and the calcitonin receptor-like receptor (CRLR) are both required to generate adrenomedullin (AM) and calcitonin gene-related peptide (CGRP) receptors. A mature, fully glycosylated, form of CRLR was associated with (125)I-CGRP binding, upon co-expression of RAMP1 and CRLR. In contrast, RAMP2 and -3 promoted the expression of smaller, core-glycosylated, CRLR forms, which were linked to AM receptor pharmacology. Since core glycosylation is classically a trademark of immature proteins, we tested the hypothesis that the core-glycosylated CRLR forms the AM receptor. Although significant amounts of core-glycosylated CRLR were produced upon co-expression with RAMP2 or -3, cross-linking experiments revealed that (125)I-AM only bound to the fully glycosylated forms. Similarly, (125)I-CGRP selectively recognized the mature CRLR species upon co-expression with RAMP1, indicating that the glycosylation does not determine ligand-binding selectivity. Our results also show that the three RAMPs lie close to the peptide binding pocket within the CRLR-RAMP heterodimers, since (125)I-AM and (125)I-CGRP were incorporated in RAMP2, -3, and -1, respectively. Cross-linking also stabilized the peptide-CRLR-RAMP ternary complexes, with the expected ligand selectivity, indicating that the fully processed heterodimers represent the functional receptors. Overall, the data indicate that direct protein-protein interactions dictate the pharmacological properties of the CRLR-RAMP complexes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Binding Sites
  • Calcitonin Gene-Related Peptide / metabolism*
  • Calcitonin Receptor-Like Protein
  • Cell Line
  • Cell Membrane / metabolism
  • Conserved Sequence
  • Dimerization
  • Glycosylation
  • Humans
  • Intracellular Signaling Peptides and Proteins
  • Iodine Radioisotopes
  • Kinetics
  • Membrane Proteins / chemistry
  • Membrane Proteins / genetics*
  • Membrane Proteins / metabolism*
  • Protein Isoforms / chemistry
  • Protein Isoforms / metabolism
  • Receptor Activity-Modifying Protein 1
  • Receptor Activity-Modifying Protein 2
  • Receptor Activity-Modifying Proteins
  • Receptors, Calcitonin / chemistry*
  • Receptors, Calcitonin / metabolism*
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Substrate Specificity
  • Transfection

Substances

  • CALCRL protein, human
  • Calcitonin Receptor-Like Protein
  • Intracellular Signaling Peptides and Proteins
  • Iodine Radioisotopes
  • Membrane Proteins
  • Protein Isoforms
  • RAMP1 protein, human
  • RAMP2 protein, human
  • Receptor Activity-Modifying Protein 1
  • Receptor Activity-Modifying Protein 2
  • Receptor Activity-Modifying Proteins
  • Receptors, Calcitonin
  • Recombinant Fusion Proteins
  • Recombinant Proteins
  • Calcitonin Gene-Related Peptide