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Conserved NPPB+ Border Zone Switches From MEF2- to AP-1-Driven Gene Program.

Karel van Duijvenboden1, Dennis E M de Bakker2, Joyce C K Man1

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Summary

Surviving heart cells near an infarct activate a stress program, including B-type natriuretic peptide (Nppb) expression, crucial for preventing heart failure. This response is conserved in humans.

Keywords:
border zoneepigenomicsmyocardial infarctionmyocardiumsequence analysis, RNAtranscription

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Area of Science:

  • Cardiology
  • Molecular Biology
  • Genomics

Background:

  • The postinfarction border zone contains surviving cardiomyocytes with unique microenvironmental fluctuations.
  • These border zone cardiomyocytes are increasingly recognized for their role in cardiac regeneration.

Purpose of the Study:

  • To define the unique transcriptional and regulatory properties of border zone cardiomyocytes.
  • To identify and validate novel molecular markers in the postinfarction border zone.

Main Methods:

  • Utilized transgenic reporter mice to identify Nppb-positive border zones post-myocardial infarction.
  • Performed RNA-sequencing on remote, border, and infarct zones, and purified cardiomyocyte nuclei.
  • Validated candidate genes in ischemic human hearts and assessed chromatin accessibility via ATAC-sequencing.

Main Results:

  • Identified a transcriptionally distinct border zone with a strong stress-response program, including downregulation of oxidative phosphorylation and fatty acid metabolism.
  • Discovered conserved border zone markers in human hearts, including NPPB, ANKRD1, DES, UCHL1, JUN, and FOXP1.
  • Demonstrated that Nppb-deficient mice exhibit lethal heart failure post-infarction, highlighting Nppb's critical role.

Conclusions:

  • Border zone cardiomyocytes shift from a homeostatic MEF2-driven program to an AP-1-driven injury-induced program.
  • This conserved transcriptional switch includes Nppb expression, essential for preventing acute postinfarct heart failure.