Transcription factor ISL1 is essential for pacemaker development and function

J Clin Invest. 2015 Aug 3;125(8):3256-68. doi: 10.1172/JCI68257. Epub 2015 Jul 20.

Abstract

The sinoatrial node (SAN) maintains a rhythmic heartbeat; therefore, a better understanding of factors that drive SAN development and function is crucial to generation of potential therapies, such as biological pacemakers, for sinus arrhythmias. Here, we determined that the LIM homeodomain transcription factor ISL1 plays a key role in survival, proliferation, and function of pacemaker cells throughout development. Analysis of several Isl1 mutant mouse lines, including animals harboring an SAN-specific Isl1 deletion, revealed that ISL1 within SAN is a requirement for early embryonic viability. RNA-sequencing (RNA-seq) analyses of FACS-purified cells from ISL1-deficient SANs revealed that a number of genes critical for SAN function, including those encoding transcription factors and ion channels, were downstream of ISL1. Chromatin immunoprecipitation assays performed with anti-ISL1 antibodies and chromatin extracts from FACS-purified SAN cells demonstrated that ISL1 directly binds genomic regions within several genes required for normal pacemaker function, including subunits of the L-type calcium channel, Ank2, and Tbx3. Other genes implicated in abnormal heart rhythm in humans were also direct ISL1 targets. Together, our results demonstrate that ISL1 regulates approximately one-third of SAN-specific genes, indicate that a combination of ISL1 and other SAN transcription factors could be utilized to generate pacemaker cells, and suggest ISL1 mutations may underlie sick sinus syndrome.

Publication types

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

MeSH terms

  • Animals
  • Ankyrins / genetics
  • Ankyrins / metabolism
  • Cell Proliferation / physiology*
  • Cell Survival
  • Chromatin / genetics
  • Chromatin / metabolism
  • Gene Deletion
  • Gene Expression Regulation, Developmental / physiology*
  • LIM-Homeodomain Proteins / genetics
  • LIM-Homeodomain Proteins / metabolism*
  • Mice
  • Mice, Transgenic
  • Myocardial Contraction / physiology*
  • Protein Binding
  • Sick Sinus Syndrome / embryology
  • Sick Sinus Syndrome / genetics
  • Sick Sinus Syndrome / pathology
  • Sinoatrial Node / cytology
  • Sinoatrial Node / embryology*
  • T-Box Domain Proteins / genetics
  • T-Box Domain Proteins / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • Ank2 protein, mouse
  • Ankyrins
  • Chromatin
  • LIM-Homeodomain Proteins
  • T-Box Domain Proteins
  • Tbx3 protein, mouse
  • Transcription Factors
  • insulin gene enhancer binding protein Isl-1