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Inflation-collapse dynamics drive patterning and morphogenesis in intestinal organoids.

Naren P Tallapragada1, Hailey M Cambra1, Tomas Wald2

  • 1Department of Systems Biology, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA.

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Stem cell zones in intestinal organoids self-organize through fission, controlled by ion channels and mechanosensitive Piezo channels. This process involves inflation, driving stem cell differentiation and a unique stretch-responsive cell state.

Keywords:
intestinal stem cellslive imagingmechanobiologyorganoidsself-organizationsize controlstretch-responsive cell

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Area of Science:

  • Developmental Biology
  • Stem Cell Biology
  • Biophysics

Background:

  • Understanding tissue self-organization is crucial for regenerative medicine.
  • Intestinal organoids model stem cell self-organization, forming stem cell zones (SCZs) of consistent size.
  • The mechanisms controlling SCZ size remain largely unknown.

Purpose of the Study:

  • To investigate the processes governing the size of stem cell zones in intestinal organoids.
  • To elucidate the role of mechanical forces and ion channels in SCZ self-organization.
  • To characterize the cellular and molecular responses to mechanical cues during organoid development.

Main Methods:

  • Optimized intestinal organoid culture for long-term, parallel time-lapse imaging.
  • Utilized advanced imaging techniques to observe SCZ dynamics.
  • Employed single-cell transcriptomics to analyze cellular states and gene expression.
  • Investigated the role of ion channels, including Piezo channels, in SCZ formation.

Main Results:

  • SCZs are primarily shaped by fission events, regulated by ion channel-mediated inflation.
  • Mechanosensitive Piezo-family channels are critical regulators of SCZ fission.
  • Organoid inflation induces rapid stem cell differentiation and a stretch-responsive state with significant transcriptional changes, including Piezo1 upregulation.
  • Fission occurs via distinct dynamic modes, differing in budding and differentiation coordination.

Conclusions:

  • The intestinal epithelium possesses an intrinsic capacity for self-organization.
  • SCZ size is actively regulated through a feedback loop involving mechanical state modulation and cellular response.
  • Ion channel activity and mechanosensation are key drivers of tissue self-organization in intestinal organoids.