Presenilin/gamma-secretase-mediated cleavage regulates association of leukocyte-common antigen-related (LAR) receptor tyrosine phosphatase with beta-catenin

J Biol Chem. 2007 Mar 23;282(12):9063-72. doi: 10.1074/jbc.M611324200. Epub 2007 Jan 26.

Abstract

Leukocyte-common antigen-related (LAR) receptor tyrosine phosphatase regulates cell adhesion and formation of functional synapses and neuronal networks. Here we report that LAR is sequentially cleaved by alpha- and presenilin (PS)/gamma-secretases, which also affect signaling and/or degradation of type-I membrane proteins including the Alzheimer disease-related beta-amyloid precursor protein. Similar to the previously characterized PS/gamma-secretase substrates, inhibition of gamma-secretase activity resulted in elevated LAR C-terminal fragment (LAR-CTF) levels in stably LAR-overexpressing Chinese hamster ovary (CHO) cells, human neuroglioma cells, and mouse cortical neurons endogenously expressing LAR. Furthermore, LAR-CTF levels increased in cells lacking functional PS, indicating that gamma-secretase-mediated cleavage of LAR was PS-dependent. Inhibition of alpha-secretase activity by TAPI-1 treatment blocked LAR-CTF accumulation, demonstrating that prior ectodomain shedding was prerequisite for PS/gamma-secretase-mediated cleavage of LAR. Moreover, we identified the product of PS/gamma-secretase cleavage, LAR intracellular domain (LICD), both in vitro and in cells overexpressing full-length (FL) LAR or LAR-CTFs. LAR localizes to cadherin-beta-catenin-based cellular junctions. Assembly and disassembly of these junctions are regulated by tyrosine phosphorylation. We found that endogenous tyrosine-phosphorylated beta-catenin coimmunoprecipitated with LAR in CHO cells. However, when PS/gamma-secretase activity was inhibited, the association between LAR and beta-catenin significantly diminished. In addition to cell adhesion, beta-catenin is involved in transcriptional regulation. We observed that LICD significantly decreased transcription of cyclin D1, one of the beta-catenin target genes. Thus, our results show that PS/gamma-secretase-mediated cleavage of LAR controls LAR-beta-catenin interaction, suggesting an essential role for PS/gamma-secretase in the regulation of LAR signaling.

Publication types

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

MeSH terms

  • Amyloid Precursor Protein Secretases / metabolism*
  • Animals
  • CHO Cells
  • Cell Membrane / metabolism
  • Cell Nucleus / metabolism
  • Cricetinae
  • Cricetulus
  • Cyclin D1 / chemistry
  • Cytoskeleton / metabolism
  • Humans
  • Mice
  • Presenilins / metabolism
  • Presenilins / physiology*
  • Protein Tyrosine Phosphatases / metabolism*
  • Receptor-Like Protein Tyrosine Phosphatases, Class 4
  • Receptors, Cell Surface / metabolism*
  • Signal Transduction
  • beta Catenin / metabolism*

Substances

  • Presenilins
  • Receptors, Cell Surface
  • beta Catenin
  • Cyclin D1
  • PTPRA protein, human
  • Protein Tyrosine Phosphatases
  • Ptpra protein, mouse
  • Receptor-Like Protein Tyrosine Phosphatases, Class 4
  • Amyloid Precursor Protein Secretases