Myocilin mutations causing glaucoma inhibit the intracellular endoproteolytic cleavage of myocilin between amino acids Arg226 and Ile227

J Biol Chem. 2005 Jun 3;280(22):21043-51. doi: 10.1074/jbc.M501340200. Epub 2005 Mar 28.

Abstract

Myocilin is a secreted glycoprotein of unknown function that is ubiquitously expressed in many human organs, including the eye. Mutations in this protein produce glaucoma, a leading cause of blindness worldwide. To explore the biological role of myocilin and the pathogenesis of glaucoma, we have analyzed the expression of recombinant wild type and four representative pathogenic myocilin mutations (E323K, Q368X, P370L, and D380A) in transiently transfected cell lines derived from ocular and nonocular tissues. We found that wild type myocilin undergoes an intracellular endoproteolytic processing at the C terminus of Arg226. This cleavage predicts the production of two fragments, one of 35 kDa containing the C-terminal olfactomedin-like domain, and another of 20 kDa containing the N-terminal leucine zipper-like domain. Here we have analyzed the 35-kDa processed fragment, and we have found that it is co-secreted with the nonprocessed protein. Western immunoblot analyses showed that human aqueous humor and some ocular tissues also contain the processed 35-kDa myocilin, indicating that the endoproteolytic cleavage occurs in vivo. Mutant myocilins accumulated in the endoplasmic reticulum of transfected cells as insoluble aggregates. Interestingly, the four pathogenic myocilins inhibited the endoproteolytic processing with varying efficiency. Furthermore, the mutation P370L, which produces the most severe glaucoma phenotype, also elicited the most potent endoproteolytic cleavage inhibition. We propose that the endoproteolytic processing might regulate the activity of myocilin and that the inhibition of the processing by pathogenic mutations impairs the normal role of myocilin.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Arginine / chemistry
  • Blotting, Western
  • Brefeldin A / pharmacology
  • COS Cells
  • Cattle
  • Cell Line
  • Computational Biology
  • Culture Media / pharmacology
  • Cytoskeletal Proteins / chemistry
  • Cytoskeletal Proteins / genetics*
  • Extracellular Matrix Proteins / chemistry
  • Eye Proteins / chemistry
  • Eye Proteins / genetics*
  • Glaucoma / metabolism*
  • Glycoproteins / chemistry
  • Glycoproteins / genetics*
  • Green Fluorescent Proteins / metabolism
  • Humans
  • Isoleucine / chemistry
  • Leucine / chemistry
  • Microscopy, Fluorescence
  • Molecular Sequence Data
  • Mutation*
  • Peptides / chemistry
  • Phenotype
  • Protein Structure, Tertiary
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
  • Transfection

Substances

  • Culture Media
  • Cytoskeletal Proteins
  • Extracellular Matrix Proteins
  • Eye Proteins
  • Glycoproteins
  • Peptides
  • olfactomedin
  • trabecular meshwork-induced glucocorticoid response protein
  • Isoleucine
  • Green Fluorescent Proteins
  • Brefeldin A
  • Arginine
  • Leucine