Kidney organoids recapitulate human basement membrane assembly in health and disease

Elife. 2022 Jan 25:11:e73486. doi: 10.7554/eLife.73486.

Abstract

Basement membranes (BMs) are complex macromolecular networks underlying all continuous layers of cells. Essential components include collagen IV and laminins, which are affected by human genetic variants leading to a range of debilitating conditions including kidney, muscle, and cerebrovascular phenotypes. We investigated the dynamics of BM assembly in human pluripotent stem cell-derived kidney organoids. We resolved their global BM composition and discovered a conserved temporal sequence in BM assembly that paralleled mammalian fetal kidneys. We identified the emergence of key BM isoforms, which were altered by a pathogenic variant in COL4A5. Integrating organoid, fetal, and adult kidney proteomes, we found dynamic regulation of BM composition through development to adulthood, and with single-cell transcriptomic analysis we mapped the cellular origins of BM components. Overall, we define the complex and dynamic nature of kidney organoid BM assembly and provide a platform for understanding its wider relevance in human development and disease.

Keywords: basement membrane; extracellular matrix; fetal kidney; glomerular development; human; kidney organoid; mouse; regenerative medicine; stem cells.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Basement Membrane / pathology*
  • Basement Membrane / physiology*
  • Biopsy
  • Cell Culture Techniques, Three Dimensional / methods
  • Cell Line
  • Child, Preschool
  • Collagen Type IV / genetics
  • Extracellular Matrix Proteins / genetics
  • Female
  • Humans
  • Kidney / pathology
  • Kidney / physiology*
  • Kidney Diseases / genetics
  • Kidney Diseases / pathology*
  • Male
  • Mice
  • Organoids / physiology*
  • Pluripotent Stem Cells / physiology
  • Proteomics / methods

Substances

  • COL4A5 protein, human
  • Collagen Type IV
  • Extracellular Matrix Proteins

Associated data

  • GEO/GSE114802
  • figshare/10.6084/m9.figshare.c.5429628