Transcriptome analysis of mouse and human sinoatrial node cells reveals a conserved genetic program

Development. 2019 Apr 25;146(8):dev173161. doi: 10.1242/dev.173161.

Abstract

The rate of contraction of the heart relies on proper development and function of the sinoatrial node, which consists of a small heterogeneous cell population, including Tbx3+ pacemaker cells. Here, we have isolated and characterized the Tbx3+ cells from Tbx3+/Venus knock-in mice. We studied electrophysiological parameters during development and found that Venus-labeled cells are genuine Tbx3+ pacemaker cells. We analyzed the transcriptomes of late fetal FACS-purified Tbx3+ sinoatrial nodal cells and Nppb-Katushka+ atrial and ventricular chamber cardiomyocytes, and identified a sinoatrial node-enriched gene program, including key nodal transcription factors, BMP signaling and Smoc2, the disruption of which in mice did not affect heart rhythm. We also obtained the transcriptomes of the sinoatrial node region, including pacemaker and other cell types, and right atrium of human fetuses, and found a gene program including TBX3, SHOX2, ISL1 and HOX family members, and BMP and NOTCH signaling components conserved between human and mouse. We conclude that a conserved gene program characterizes the sinoatrial node region and that the Tbx3+/Venus allele provides a reliable tool for visualizing the sinoatrial node, and studying its development and function.

Keywords: BMP-signaling; Electrophysiology; Human gene expression; Sinoatrial node; Transcriptional profiling; Working myocardium.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium-Binding Proteins / genetics
  • Calcium-Binding Proteins / metabolism
  • Electrocardiography
  • Female
  • Flow Cytometry
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Humans
  • Immunohistochemistry
  • LIM-Homeodomain Proteins / genetics
  • LIM-Homeodomain Proteins / metabolism
  • Mice
  • Mice, Mutant Strains
  • Microscopy, Fluorescence
  • Sinoatrial Node / metabolism*
  • T-Box Domain Proteins / genetics
  • T-Box Domain Proteins / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transcriptome / genetics*

Substances

  • Calcium-Binding Proteins
  • Homeodomain Proteins
  • LIM-Homeodomain Proteins
  • Shox2 protein, mouse
  • Smoc2 protein, mouse
  • T-Box Domain Proteins
  • Tbx3 protein, mouse
  • Transcription Factors
  • insulin gene enhancer binding protein Isl-1