An interaction between OTULIN and SCRIB uncovers roles for linear ubiquitination in planar cell polarity

Dis Model Mech. 2023 Aug 1;16(8):dmm049762. doi: 10.1242/dmm.049762. Epub 2023 Aug 17.

Abstract

Planar cell polarity (PCP) plays critical roles in developmental and homeostatic processes. Membrane presentation of PCP complexes containing Van Gogh-like (VANGL) transmembrane proteins is central to PCP and can be directed by the scaffold protein scribble (SCRIB). The role atypical linear ubiquitin (Met1-Ub) chains might play in PCP is unknown. Here, HEK293 cell-based interactomic analyses of the Met1-Ub deubiquitinase OTULIN revealed that OTULIN can interact with SCRIB. Moreover, Met1-Ub chains associated with VANGL2 and PRICKLE1, but not SCRIB, can direct VANGL2 surface presentation. Mouse embryos lacking Otulin showed variable neural tube malformations, including rare open neural tubes, a deficit associated with PCP disruption in mice. In Madin-Darby canine kidney cells, in which the enrichment of VANGL2-GFP proteins at cell-cell contacts represents activated PCP complexes, endogenous OTULIN was recruited to these sites. In the human MDA-MB-231 breast cancer cell model, OTULIN loss caused deficits in Wnt5a-induced filopodia extension and trafficking of transfected HA-VANGL2. Taken together, these findings support a role for linear (de)ubiquitination in PCP signaling. The association of Met1-Ub chains with PCP complex components offers new opportunities for integrating PCP signaling with OTULIN-dependent immune and inflammatory pathways.

Keywords: Linear ubiquitin; Linear ubiquitin assembly complex; Mouse genetics; OTULIN; Planar cell polarity; Scribble.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Polarity*
  • Dogs
  • Endopeptidases* / metabolism
  • Female
  • HEK293 Cells
  • Humans
  • MDA-MB-231 Cells
  • Madin Darby Canine Kidney Cells
  • Membrane Proteins* / metabolism
  • Mice
  • Ubiquitin
  • Ubiquitination

Substances

  • Ubiquitin
  • OTULIN protein, human
  • SCRIB protein, human
  • Endopeptidases
  • Membrane Proteins