Defective secretion of recombinant fragments of fibrillin-1: implications of protein misfolding for the pathogenesis of Marfan syndrome and related disorders

Hum Mol Genet. 2003 Apr 1;12(7):727-37. doi: 10.1093/hmg/ddg081.

Abstract

Fibrillin-1 is a large modular glycoprotein that assembles to form 10-12 nm microfibrils in the extracellular matrix. Mutations in the fibrillin-1 gene (FBN1) cause Marfan syndrome and related connective tissue disorders (fibrillinopathies) that show autosomal dominant inheritance. The pathogenic mechanism is thought to be a dominant negative effect of a mutant protein on microfibril assembly, although direct evidence is lacking. A significant group of disease-causing FBN1 mutations are cysteine substitutions within EGF domains that are predicted to cause misfolding by removal of disulphide bonds that stabilize the native domain fold. We have studied three missense mutations (C1117Y, C1129Y and G1127S) to investigate the effect of misfolding on the trafficking of fibrillin-1 from fibroblast cells. We demonstrate that both C1117Y and C1129Y, expressed as recombinant fragments of fibrillin-1, are retained and accumulate within the cell. Both undergo core glycosylation but lack the complex glycosylation observed in the secreted wild-type fragment, suggesting retention in the endoplasmic reticulum (ER). In addition, co-immunoprecipitation experiments show association with the ER chaperone calreticulin, but not calnexin, 78 kDa glucose-regulated protein (Grp78/BiP) or protein disulfide isomerase. In contrast, G1127S, which causes a moderate change in the EGF domain fold, shows a pattern of glycosylation and trafficking profile indistinguishable from the wild-type fragment. Since expression of the recombinant fragments does not disrupt the secretion of endogenous fibrillin-1 by the cell, we propose that G1127S causes disease via an extracellular dominant negative effect. In contrast, the observed ER retention of C1117Y and C1129Y suggests that disease associated with these missense mutations is caused either by an intracellular dominant negative effect or haploinsufficiency.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Blotting, Western
  • Calreticulin / chemistry
  • Cell Line
  • Cloning, Molecular
  • Culture Media, Conditioned / pharmacology
  • DNA / chemistry
  • Endoplasmic Reticulum / metabolism
  • Endoplasmic Reticulum Chaperone BiP
  • Fibrillin-1
  • Fibrillins
  • Fibroblasts / metabolism
  • Genes, Dominant
  • Glucose / chemistry
  • Glycosylation
  • Humans
  • Marfan Syndrome / genetics*
  • Microfilament Proteins / chemistry*
  • Microfilament Proteins / metabolism*
  • Molecular Sequence Data
  • Mutation
  • Mutation, Missense
  • Precipitin Tests
  • Protein Folding
  • Protein Structure, Tertiary
  • RNA, Messenger / metabolism
  • Recombinant Proteins / chemistry*
  • Transfection

Substances

  • Calreticulin
  • Culture Media, Conditioned
  • Endoplasmic Reticulum Chaperone BiP
  • FBN1 protein, human
  • Fibrillin-1
  • Fibrillins
  • HSPA5 protein, human
  • Microfilament Proteins
  • RNA, Messenger
  • Recombinant Proteins
  • DNA
  • Glucose