Agarose microgel culture delineates lumenogenesis in naive and primed human pluripotent stem cells

Stem Cell Reports. 2021 May 11;16(5):1347-1362. doi: 10.1016/j.stemcr.2021.04.009.

Abstract

Human periimplantation development requires the transformation of the naive pluripotent epiblast into a polarized epithelium. Lumenogenesis plays a critical role in this process, as the epiblast undergoes rosette formation and lumen expansion to form the amniotic cavity. Here, we present a high-throughput in vitro model for epiblast morphogenesis. We established a microfluidic workflow to encapsulate human pluripotent stem cells (hPSCs) into monodisperse agarose microgels. Strikingly, hPSCs self-organized into polarized epiblast spheroids that could be maintained in self-renewing and differentiating conditions. Encapsulated primed hPSCs required Rho-associated kinase inhibition, in contrast to naive hPSCs. We applied microgel suspension culture to examine the lumen-forming capacity of hPSCs and reveal an increase in lumenogenesis during the naive-to-primed transition. Finally, we demonstrate the feasibility of co-encapsulating cell types across different lineages and species. Our work provides a foundation for stem cell-based embryo models to interrogate the critical components of human epiblast self-organization and morphogenesis.

Keywords: epiblast; epiblast spheroid; human development; lumenogenesis; microfluidic platform; microgel suspension culture; naive pluripotency; primed pluripotency; self-organization.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Culture Techniques*
  • Cell Differentiation / drug effects
  • Cell Lineage / drug effects
  • Cell Survival / drug effects
  • Cells, Immobilized / cytology
  • Cells, Immobilized / drug effects
  • Germ Layers / cytology
  • Humans
  • Induced Pluripotent Stem Cells / cytology*
  • Induced Pluripotent Stem Cells / drug effects
  • Induced Pluripotent Stem Cells / metabolism
  • Microgels / chemistry*
  • Morphogenesis* / drug effects
  • Protein Kinase Inhibitors / pharmacology
  • Sepharose / pharmacology*
  • Spheroids, Cellular / cytology
  • Spheroids, Cellular / drug effects
  • rho-Associated Kinases / antagonists & inhibitors
  • rho-Associated Kinases / metabolism

Substances

  • Microgels
  • Protein Kinase Inhibitors
  • Sepharose
  • rho-Associated Kinases