Coordinated Proliferation and Differentiation of Human-Induced Pluripotent Stem Cell-Derived Cardiac Progenitor Cells Depend on Bone Morphogenetic Protein Signaling Regulation by GREMLIN 2

Stem Cells Dev. 2017 May 1;26(9):678-693. doi: 10.1089/scd.2016.0226. Epub 2017 Mar 20.

Abstract

Heart development depends on coordinated proliferation and differentiation of cardiac progenitor cells (CPCs), but how the two processes are synchronized is not well understood. Here, we show that the secreted Bone Morphogenetic Protein (BMP) antagonist GREMLIN 2 (GREM2) is induced in CPCs shortly after cardiac mesoderm specification during differentiation of human pluripotent stem cells. GREM2 expression follows cardiac lineage differentiation independently of the differentiation method used, or the origin of the pluripotent stem cells, suggesting that GREM2 is linked to cardiogenesis. Addition of GREM2 protein strongly increases cardiomyocyte output compared to established procardiogenic differentiation methods. Our data show that inhibition of canonical BMP signaling by GREM2 is necessary to promote proliferation of CPCs. However, canonical BMP signaling inhibition alone is not sufficient to induce cardiac differentiation, which depends on subsequent JNK pathway activation specifically by GREM2. These findings may have broader implications in the design of approaches to orchestrate growth and differentiation of pluripotent stem cell-derived lineages that depend on precise regulation of BMP signaling.

Keywords: BMP signaling; GREMLIN 2; cardiomyocyte differentiation; human pluripotent stem cells.

MeSH terms

  • Bone Morphogenetic Proteins / genetics*
  • Bone Morphogenetic Proteins / metabolism
  • Bone Morphogenetic Proteins / pharmacology
  • Cell Differentiation / drug effects
  • Cell Differentiation / genetics*
  • Cell Line
  • Cell Proliferation / drug effects
  • Cell Proliferation / genetics*
  • Cells, Cultured
  • Cytokines
  • Gene Expression Profiling
  • Gene Expression Regulation, Developmental
  • Humans
  • Induced Pluripotent Stem Cells / cytology
  • Induced Pluripotent Stem Cells / drug effects
  • Induced Pluripotent Stem Cells / metabolism*
  • Intercellular Signaling Peptides and Proteins / genetics*
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Intercellular Signaling Peptides and Proteins / pharmacology
  • Myocardium / cytology
  • Myocardium / metabolism
  • Myocytes, Cardiac / cytology
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism
  • Organogenesis / genetics
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Stem Cells / cytology
  • Stem Cells / drug effects
  • Stem Cells / metabolism*

Substances

  • Bone Morphogenetic Proteins
  • Cytokines
  • GREM2 protein, human
  • Intercellular Signaling Peptides and Proteins