Molecular determinants of nephron vascular specialization in the kidney

Nat Commun. 2019 Dec 13;10(1):5705. doi: 10.1038/s41467-019-12872-5.

Abstract

Although kidney parenchymal tissue can be generated in vitro, reconstructing the complex vasculature of the kidney remains a daunting task. The molecular pathways that specify and sustain functional, phenotypic and structural heterogeneity of the kidney vasculature are unknown. Here, we employ high-throughput bulk and single-cell RNA sequencing of the non-lymphatic endothelial cells (ECs) of the kidney to identify the molecular pathways that dictate vascular zonation from embryos to adulthood. We show that the kidney manifests vascular-specific signatures expressing defined transcription factors, ion channels, solute transporters, and angiocrine factors choreographing kidney functions. Notably, the ontology of the glomerulus coincides with induction of unique transcription factors, including Tbx3, Gata5, Prdm1, and Pbx1. Deletion of Tbx3 in ECs results in glomerular hypoplasia, microaneurysms and regressed fenestrations leading to fibrosis in subsets of glomeruli. Deciphering the molecular determinants of kidney vascular signatures lays the foundation for rebuilding nephrons and uncovering the pathogenesis of kidney disorders.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Capillaries / cytology
  • Capillaries / growth & development*
  • Capillaries / metabolism
  • Cells, Cultured
  • Embryo, Mammalian
  • Endothelial Cells / metabolism*
  • Endothelium, Vascular / cytology
  • Endothelium, Vascular / growth & development
  • Endothelium, Vascular / metabolism*
  • GATA5 Transcription Factor / genetics
  • GATA5 Transcription Factor / metabolism
  • Gene Expression Profiling
  • Gene Expression Regulation, Developmental*
  • Humans
  • Kidney Glomerulus / blood supply*
  • Kidney Glomerulus / growth & development
  • Kidney Glomerulus / metabolism
  • Male
  • Mice
  • Mice, Transgenic
  • Positive Regulatory Domain I-Binding Factor 1 / genetics
  • Positive Regulatory Domain I-Binding Factor 1 / metabolism
  • Pre-B-Cell Leukemia Transcription Factor 1 / genetics
  • Pre-B-Cell Leukemia Transcription Factor 1 / metabolism
  • Primary Cell Culture
  • RNA-Seq
  • Single-Cell Analysis
  • T-Box Domain Proteins / genetics
  • T-Box Domain Proteins / metabolism

Substances

  • GATA5 Transcription Factor
  • Gata5 protein, mouse
  • Pbx1 protein, mouse
  • Prdm1 protein, mouse
  • Pre-B-Cell Leukemia Transcription Factor 1
  • T-Box Domain Proteins
  • Tbx3 protein, mouse
  • Positive Regulatory Domain I-Binding Factor 1