Preferential activation by galanin 1-15 fragment of the GalR1 protomer of a GalR1-GalR2 heteroreceptor complex

Biochem Biophys Res Commun. 2014 Sep 26;452(3):347-53. doi: 10.1016/j.bbrc.2014.08.061. Epub 2014 Aug 22.

Abstract

The three cloned galanin receptors show a higher affinity for galanin than for galanin N-terminal fragments. Galanin fragment (1-15) binding sites were discovered in the rat Central Nervous System, especially in dorsal hippocampus, indicating a relevant role of galanin fragments in central galanin communication. The hypothesis was introduced that these N-terminal galanin fragment preferring sites are formed through the formation of GalR1-GalR2 heteromers which may play a significant role in mediating galanin fragment (1-15) signaling. In HEK293T cells evidence for the existence of GalR1-GalR2 heteroreceptor complexes were obtained with proximity ligation and BRET(2) assays. PLA positive blobs representing GalR1-GalR2 heteroreceptor complexes were also observed in the raphe-hippocampal system. In CRE luciferase reporter gene assays, galanin (1-15) was more potent than galanin (1-29) in inhibiting the forskolin-induced increase of luciferase activity in GalR1-GalR2 transfected cells. The inhibition of CREB by 50nM of galanin (1-15) and of galanin (1-29) was fully counteracted by the non-selective galanin antagonist M35 and the selective GalR2 antagonist M871. These results suggested that the orthosteric agonist binding site of GalR1 protomer may have an increased affinity for the galanin (1-15) vs galanin (1-29) which can lead to its demonstrated increase in potency to inhibit CREB vs galanin (1-29). In contrast, in NFAT reporter gene assays galanin (1-29) shows a higher efficacy than galanin (1-15) in increasing Gq/11 mediated signaling over the GalR2 of these heteroreceptor complexes. This disbalance in the signaling of the GalR1-GalR2 heteroreceptor complexes induced by galanin (1-15) may contribute to depression-like actions since GalR1 agonists produce such effects.

Keywords: Allosteric receptor–receptor interactions; GalR1–GalR2 heteromers; Galanin; Heteroreceptor complexes; In situ Proximity Ligation Assay; N-terminal galanin fragment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Allosteric Regulation
  • Animals
  • Bradykinin / analogs & derivatives
  • Bradykinin / pharmacology
  • Brain Mapping
  • CREB-Binding Protein / antagonists & inhibitors
  • CREB-Binding Protein / genetics
  • CREB-Binding Protein / metabolism
  • Galactolipids / pharmacology
  • Galanin / metabolism
  • Galanin / pharmacology*
  • Gene Expression Regulation
  • Genes, Reporter
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • HEK293 Cells
  • Hippocampus / cytology
  • Hippocampus / drug effects
  • Hippocampus / metabolism*
  • Humans
  • Neurons / cytology
  • Neurons / drug effects
  • Neurons / metabolism*
  • Peptide Fragments / metabolism
  • Peptide Fragments / pharmacology*
  • Promoter Regions, Genetic
  • Protein Multimerization
  • Rats
  • Receptor, Galanin, Type 1 / agonists
  • Receptor, Galanin, Type 1 / chemistry
  • Receptor, Galanin, Type 1 / genetics
  • Receptor, Galanin, Type 1 / metabolism*
  • Receptor, Galanin, Type 2 / chemistry
  • Receptor, Galanin, Type 2 / genetics
  • Receptor, Galanin, Type 2 / metabolism*
  • Signal Transduction

Substances

  • Galactolipids
  • Peptide Fragments
  • Receptor, Galanin, Type 1
  • Receptor, Galanin, Type 2
  • galanin (1-15)
  • galanin-(1-13)-bradykinin-(2-9)-amide
  • Green Fluorescent Proteins
  • Galanin
  • CREB-Binding Protein
  • CREBBP protein, human
  • Bradykinin