A flanking gene problem leads to the discovery of a Gprc5b splice variant predominantly expressed in C57Bl/6J mouse brain and in maturing neurons

PLoS One. 2010 Apr 26;5(4):e10351. doi: 10.1371/journal.pone.0010351.

Abstract

Background: Gprc5b, a retinoic acid-inducible orphan G protein-coupled receptor (GPCR), is a member of the group C metabotropic glutamate receptor family proteins possibly involved in non-canonical Wnt signaling. Many GPCR transcripts are alternatively spliced, which diversifies this class of proteins in their cell- and tissue-specific signaling, regulatory and/or pharmacological properties. We previously generated p97FE65 isoform-specific knockout mice that showed learning/memory deficits. In this study, we further characterized the 97FE65 null mice using cDNA microarray and RT-PCR analyses.

Methodology/principal findings: We discovered a novel brain-specific C-terminal splice variant of Gprc5b, Gprc5b_v2, which was differentially expressed in p97FE65 wild type and null mouse brains. The null mice were generated in 129/Sv ES cells, and backcrossed to C57Bl/6J for ten generations. We found that expression of Gprc5b_v2 mRNA in the brains of p97FE65 null mice was dramatically down-regulated (more than 20 fold) compared to their wild type littermates. However, expression profiles of Gprc5b variants and SNP analysis surrounding the FE65 locus suggest that the down-regulation is unlikely due to the altered FE65 function, but rather is caused by gene retention from the 129/Sv ES cells. Consistently, in contrast to ubiquitously expressed Gprc5b_v1, Gprc5b_v2 was predominantly expressed in the brain tissues of C57Bl/6J mice. The alternative splicing of the 3' terminal exon also altered the protein coding sequences, giving rise to the characteristic C-termini. Levels of Gprc5b_v2 mRNA were increased during neuronal maturation, paralleling the expression of synaptic proteins. Overexpression of both Gprc5b variants stimulated neurite-like outgrowth in a neuroblastoma cell line.

Conclusions/significance: Our results suggest that Gprc5b-v2 may play a role during brain maturation and in matured brain, possibly through the regulation of neuronal morphology and protein-protein interaction. This study also highlights the fact that unexpected gene retention following repeated backcrosses can lead to important biological consequences.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Brain / growth & development
  • Brain / metabolism*
  • Brain Chemistry
  • Gene Expression Profiling
  • Inbreeding
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neurons / chemistry*
  • Neurons / metabolism
  • Polymorphism, Single Nucleotide
  • Protein Isoforms
  • RNA, Messenger / analysis
  • Receptors, G-Protein-Coupled / analysis*
  • Receptors, G-Protein-Coupled / genetics*

Substances

  • GPRC5B protein, human
  • Protein Isoforms
  • RNA, Messenger
  • Receptors, G-Protein-Coupled