Fibrillin-1 mgΔ(lpn) Marfan syndrome mutation associates with preserved proteostasis and bypass of a protein disulfide isomerase-dependent quality checkpoint

Int J Biochem Cell Biol. 2016 Feb:71:81-91. doi: 10.1016/j.biocel.2015.12.009. Epub 2015 Dec 21.

Abstract

Fibrillin-1 mutations promote Marfan syndrome (MFS) via complex yet unclear pathways. The roles of endoplasmic reticulum (ER) and the major ER redox chaperone protein disulfide isomerase-A1 in the processing of normal and mutated fibrillin-1 and ensuing protein secretion and/or intracellular retention are unclear. Our results in mouse embryonic fibroblasts bearing the exon-skipping mgΔ(lox-P-neo) (mgΔ(lpn)) mutation, which associates in vivo with MFS and in vitro with disrupted microfibrils, indicate a preserved ER-dependent proteostasis or redox homeostasis. Rather, mutated fibrillin-1 is secreted normally through Golgi-dependent pathways and is not intracellularly retained. Similar results occurred for the C1039G point mutation. In parallel, we provide evidence that PDIA1 physically interacts with fibrillin-1 in the ER. Moreover, siRNA against PDIA1 augmented fibrillin-1 secretion rates in wild-type cells. However, fibrillin-1 with the mgΔ(lpn) mutation bypassed PDI checkpoint delay, while the C1039G mutation did not. This heretofore undisclosed PDIA1-mediated mechanism may be important to control the extracellular availability of function-competent fibrillin-1, an important determinant of disease phenotype. Moreover, our results may reveal a novel, holdase-like, PDI function associated with ER protein quality control.

Keywords: Endoplasmic reticulum stress; Fibrillin-1; Marfan syndrome; Oxidative folding; Protein disulfide isomerase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Endoplasmic Reticulum / metabolism
  • Fibrillin-1
  • Fibrillins
  • Gene Silencing
  • Homeostasis / genetics*
  • Marfan Syndrome / genetics*
  • Mice
  • Microfibrils / metabolism
  • Microfilament Proteins / genetics*
  • Mutation*
  • Phenotype
  • Protein Disulfide-Isomerases / deficiency
  • Protein Disulfide-Isomerases / genetics
  • Protein Disulfide-Isomerases / metabolism*

Substances

  • Fbn1 protein, mouse
  • Fibrillin-1
  • Fibrillins
  • Microfilament Proteins
  • Protein Disulfide-Isomerases