Increased TIMP-3 expression alters the cellular secretome through dual inhibition of the metalloprotease ADAM10 and ligand-binding of the LRP-1 receptor

Sci Rep. 2018 Oct 2;8(1):14697. doi: 10.1038/s41598-018-32910-4.

Abstract

The tissue inhibitor of metalloproteinases-3 (TIMP-3) is a major regulator of extracellular matrix turnover and protein shedding by inhibiting different classes of metalloproteinases, including disintegrin metalloproteinases (ADAMs). Tissue bioavailability of TIMP-3 is regulated by the endocytic receptor low-density-lipoprotein receptor-related protein-1 (LRP-1). TIMP-3 plays protective roles in disease. Thus, different approaches have been developed aiming to increase TIMP-3 bioavailability, yet overall effects of increased TIMP-3 in vivo have not been investigated. Herein, by using unbiased mass-spectrometry we demonstrate that TIMP-3-overexpression in HEK293 cells has a dual effect on shedding of transmembrane proteins and turnover of soluble proteins. Several membrane proteins showing reduced shedding are known as ADAM10 substrates, suggesting that exogenous TIMP-3 preferentially inhibits ADAM10 in HEK293 cells. Additionally identified shed membrane proteins may be novel ADAM10 substrate candidates. TIMP-3-overexpression also increased extracellular levels of several soluble proteins, including TIMP-1, MIF and SPARC. Levels of these proteins similarly increased upon LRP-1 inactivation, suggesting that TIMP-3 increases soluble protein levels by competing for their binding to LRP-1 and their subsequent internalization. In conclusion, our study reveals that increased levels of TIMP-3 induce substantial modifications in the cellular secretome and that TIMP-3-based therapies may potentially provoke undesired, dysregulated functions of ADAM10 and LRP-1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADAM10 Protein / metabolism*
  • Amyloid Precursor Protein Secretases / metabolism*
  • Cell Membrane / metabolism*
  • Extracellular Matrix / metabolism
  • HEK293 Cells
  • Humans
  • Ligands
  • Low Density Lipoprotein Receptor-Related Protein-1 / metabolism*
  • Mass Spectrometry
  • Membrane Proteins / metabolism*
  • Protein Transport / physiology
  • Proteomics
  • Secretory Pathway / physiology*
  • Tissue Inhibitor of Metalloproteinase-3 / metabolism*

Substances

  • LDLR-related protein 1A, human
  • Ligands
  • Low Density Lipoprotein Receptor-Related Protein-1
  • Membrane Proteins
  • TIMP3 protein, human
  • Tissue Inhibitor of Metalloproteinase-3
  • Amyloid Precursor Protein Secretases
  • ADAM10 Protein
  • ADAM10 protein, human