Recombination signal binding protein for Ig-κJ region regulates juxtaglomerular cell phenotype by activating the myo-endocrine program and suppressing ectopic gene expression

J Am Soc Nephrol. 2015 Jan;26(1):67-80. doi: 10.1681/ASN.2013101045. Epub 2014 Jun 5.

Abstract

Recombination signal binding protein for Ig-κJ region (RBP-J), the major downstream effector of Notch signaling, is necessary to maintain the number of renin-positive juxtaglomerular cells and the plasticity of arteriolar smooth muscle cells to re-express renin when homeostasis is threatened. We hypothesized that RBP-J controls a repertoire of genes that defines the phenotype of the renin cell. Mice bearing a bacterial artificial chromosome reporter with a mutated RBP-J binding site in the renin promoter had markedly reduced reporter expression at the basal state and in response to a homeostatic challenge. Mice with conditional deletion of RBP-J in renin cells had decreased expression of endocrine (renin and Akr1b7) and smooth muscle (Acta2, Myh11, Cnn1, and Smtn) genes and regulators of smooth muscle expression (miR-145, SRF, Nfatc4, and Crip1). To determine whether RBP-J deletion decreased the endowment of renin cells, we traced the fate of these cells in RBP-J conditional deletion mice. Notably, the lineage staining patterns in mutant and control kidneys were identical, although mutant kidneys had fewer or no renin-expressing cells in the juxtaglomerular apparatus. Microarray analysis of mutant arterioles revealed upregulation of genes usually expressed in hematopoietic cells. Thus, these results suggest that RBP-J maintains the identity of the renin cell by not only activating genes characteristic of the myo-endocrine phenotype but also, preventing ectopic gene expression and adoption of an aberrant phenotype, which could have severe consequences for the control of homeostasis.

Keywords: cell fate; hematopoiesis; juxtaglomerular cell; renin; smooth muscle.

Publication types

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

MeSH terms

  • Animals
  • Binding Sites
  • Cell Communication
  • Cell Lineage
  • Cell Proliferation
  • Chromosomes, Artificial, Bacterial
  • Gene Deletion
  • Gene Expression Regulation*
  • Genes, Reporter
  • Hematopoietic Stem Cells / cytology
  • Immunoglobulin J Recombination Signal Sequence-Binding Protein / metabolism*
  • Juxtaglomerular Apparatus / metabolism*
  • Kidney / blood supply
  • Kidney / metabolism
  • Mice
  • Mice, Knockout
  • Microcirculation
  • Mutation
  • Myocytes, Smooth Muscle / cytology
  • Oligonucleotide Array Sequence Analysis
  • Phenotype
  • Promoter Regions, Genetic
  • Renin / genetics

Substances

  • Immunoglobulin J Recombination Signal Sequence-Binding Protein
  • Rbpj protein, mouse
  • Renin