Donor-specific phenotypic variation in hiPSC cardiomyocyte-derived exosomes impacts endothelial cell function

Am J Physiol Heart Circ Physiol. 2021 Mar 1;320(3):H954-H968. doi: 10.1152/ajpheart.00463.2020. Epub 2021 Jan 8.

Abstract

Exosomes are an important mechanism of cell-cell interaction in the cardiovascular system, both in maintaining homeostasis and in stress response. Interindividual differences that alter content in exosomes may play a role in cardiovascular disease pathology. To study the effect of interindividual cardiomyocyte (CM) variation, we characterized exosomal content in phenotypically diverse human induced pluripotent stem cell-derived CMs (hiPSC-CMs). Cell lines were generated from six participants in the HyperGEN cohort: three with left ventricular hypertrophy (LVH) and three with normal left ventricular mass (LVM). Sequence analysis of the intracellular and exosomal RNA populations showed distinct expression pattern differences between hiPSC-CM lines derived from individuals with LVH and those with normal LVM. Functional analysis of hiPSC-endothelial cells (hiPSC-ECs) treated with exosomes from both hiPSC-CM groups showed significant variation in response, including differences in tube formation, migration, and proliferation. Overall, treatment of hiPSC-ECs with exosomes resulted in significant expression changes associated with angiogenesis and endothelial cell vasculogenesis. However, the hiPSC-ECs treated with exosomes from the LVH-affected donors exhibited significantly increased proliferation but decreased tube formation and migration, suggesting angiogenic dysregulation.NEW & NOTEWORTHY The intracellular RNA and the miRNA content in exosomes are significantly different in hiPSC-CMs derived from LVH-affected individuals compared with those from unaffected individuals. Treatment of endothelial cells with these exosomes functionally affects cellular phenotypes in a donor-specific manner. These findings provide novel insight into underlying mechanisms of hypertrophic cell signaling between different cell types. With a growing interest in stem cells and exosomes for cardiovascular therapeutic use, this also provides information important for regenerative medicine.

Keywords: cardiomyocyte hypertrophy; exosomes; human induced pluripotent stem cells; intercellular communication; miRNA.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural

MeSH terms

  • Adult
  • Aged
  • Case-Control Studies
  • Cell Differentiation*
  • Cell Movement
  • Cell Proliferation
  • Cell Separation
  • Cells, Cultured
  • Exosomes / genetics
  • Exosomes / metabolism*
  • Exosomes / ultrastructure
  • Female
  • Gene Expression Regulation
  • Humans
  • Hypertrophy, Left Ventricular / genetics
  • Hypertrophy, Left Ventricular / metabolism*
  • Hypertrophy, Left Ventricular / pathology
  • Induced Pluripotent Stem Cells / metabolism*
  • Induced Pluripotent Stem Cells / ultrastructure
  • Male
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Middle Aged
  • Myocytes, Cardiac / metabolism*
  • Myocytes, Cardiac / ultrastructure
  • Neovascularization, Physiologic* / genetics
  • Phenotype
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Signal Transduction
  • Tissue Donors*
  • Transcriptome

Substances

  • MicroRNAs
  • RNA, Messenger