EPB41L5 controls podocyte extracellular matrix assembly by adhesome-dependent force transmission

Cell Rep. 2021 Mar 23;34(12):108883. doi: 10.1016/j.celrep.2021.108883.

Abstract

The integrity of the kidney filtration barrier essentially relies on the balanced interplay of podocytes and the glomerular basement membrane (GBM). Here, we show by analysis of in vitro and in vivo models that a loss of the podocyte-specific FERM-domain protein EPB41L5 results in impaired extracellular matrix (ECM) assembly. By using quantitative proteomics analysis of the secretome and matrisome, we demonstrate a shift in ECM composition characterized by diminished deposition of core GBM components, such as LAMA5. Integrin adhesome proteomics reveals that EPB41L5 recruits PDLIM5 and ACTN4 to integrin adhesion complexes (IACs). Consecutively, EPB41L5 knockout podocytes show insufficient maturation of integrin adhesion sites, which translates into impaired force transmission and ECM assembly. These observations build the framework for a model in which EPB41L5 functions as a cell-type-specific regulator of the podocyte adhesome and controls a localized adaptive module in order to prevent podocyte detachment and thereby ensures GBM integrity.

Keywords: ECM; EPB41L5; GBM; IAC; PDLIM5; extracellular matrix; focal adhesion; glomerular basement membrane; matrisome; podocyte.

Publication types

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

MeSH terms

  • Actinin / metabolism
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Basement Membrane / metabolism
  • Basement Membrane / ultrastructure
  • Biomechanical Phenomena
  • Cattle
  • Cell Adhesion
  • Cytoskeletal Proteins / chemistry
  • Cytoskeletal Proteins / metabolism*
  • Disease Models, Animal
  • Extracellular Matrix / metabolism*
  • HEK293 Cells
  • Humans
  • Integrins / metabolism
  • Male
  • Membrane Proteins / chemistry
  • Membrane Proteins / metabolism*
  • Mice
  • Microfilament Proteins / metabolism
  • Podocytes / metabolism*
  • Podocytes / ultrastructure
  • Protein Domains
  • Secretome

Substances

  • Actn4 protein, mouse
  • Adaptor Proteins, Signal Transducing
  • Cytoskeletal Proteins
  • ENH protein, mouse
  • EPB41L5 protein, human
  • EPB41L5 protein, mouse
  • Integrins
  • Membrane Proteins
  • Microfilament Proteins
  • Actinin