Processing of surfactant protein C requires a type II transmembrane topology directed by juxtamembrane positively charged residues

J Biol Chem. 2003 Nov 28;278(48):47979-86. doi: 10.1074/jbc.M308210200. Epub 2003 Aug 21.

Abstract

Surfactant protein C (SP-C) is a lung-specific protein that is synthesized as a 21-kDa integral membrane propeptide (pro-SP-C) and proteolytically processed to a 3.7-kDa secretory product. Previous studies have shown that palmitoylation of pro-SP-C is dependent on two N-terminal juxtamembrane positively charged residues. We hypothesized that these residues influence modification of pro-SP-C by directing transmembrane orientation. Double substitution mutation of these juxtaposed residues from positive to neutral charged species resulted in complete reversal of transmembrane orientation of pro-SP-C and total abrogation of post-translational processing. Mutation of a single residue resulted in mixed orientation. Protein trafficking studies in A549 cells showed that while the double mutant was retained in the endoplasmic reticulum, single mutants produced a mixed pattern of both endoplasmic reticulum (double mutant-like) and vesicular (wild type-like) expression. Our study demonstrates the crucial role juxtamembrane positively charged residues play in establishing membrane topology and their influence on the trafficking and processing of pro-SP-C. Moreover this study provides a likely precedent for a mechanism in disorders associated with mutations in the membrane-flanking region of integral membrane proteins.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Arginine / chemistry
  • Cell Line, Tumor
  • Cell Membrane / metabolism*
  • DNA, Complementary / metabolism
  • Endopeptidases / chemistry
  • Endoplasmic Reticulum / metabolism
  • Epitopes / chemistry
  • Green Fluorescent Proteins
  • Humans
  • Immunoblotting
  • Immunohistochemistry
  • Luminescent Proteins / metabolism
  • Lysine / chemistry
  • Microscopy, Fluorescence
  • Molecular Sequence Data
  • Mutation
  • Protein Structure, Tertiary
  • Pulmonary Surfactant-Associated Protein C / chemistry
  • Pulmonary Surfactant-Associated Protein C / genetics
  • Pulmonary Surfactant-Associated Protein C / metabolism*
  • Rats

Substances

  • DNA, Complementary
  • Epitopes
  • Luminescent Proteins
  • Pulmonary Surfactant-Associated Protein C
  • Green Fluorescent Proteins
  • Arginine
  • Endopeptidases
  • Lysine