Disease-linked mutations in factor H reveal pivotal role of cofactor activity in self-surface-selective regulation of complement activation

J Biol Chem. 2017 Aug 11;292(32):13345-13360. doi: 10.1074/jbc.M117.795088. Epub 2017 Jun 21.

Abstract

Spontaneous activation enables the complement system to respond very rapidly to diverse threats. This activation is efficiently suppressed by complement factor H (CFH) on self-surfaces but not on foreign surfaces. The surface selectivity of CFH, a soluble protein containing 20 complement-control protein modules (CCPs 1-20), may be compromised by disease-linked mutations. However, which of the several functions of CFH drives this self-surface selectivity remains unknown. To address this, we expressed human CFH mutants in Pichia pastoris We found that recombinant I62-CFH (protective against age-related macular degeneration) and V62-CFH functioned equivalently, matching or outperforming plasma-derived CFH, whereas R53H-CFH, linked to atypical hemolytic uremic syndrome (aHUS), was defective in C3bBb decay-accelerating activity (DAA) and factor I cofactor activity (CA). The aHUS-linked CCP 19 mutant D1119G-CFH had virtually no CA on (self-like) sheep erythrocytes (ES) but retained DAA. The aHUS-linked CCP 20 mutant S1191L/V1197A-CFH (LA-CFH) had dramatically reduced CA on ES but was less compromised in DAA. D1119G-CFH and LA-CFH both performed poorly at preventing complement-mediated hemolysis of ES PspCN, a CFH-binding Streptococcus pneumoniae protein domain, binds CFH tightly and increases accessibility of CCPs 19 and 20. PspCN did not improve the DAA of any CFH variant on ES Conversely, PspCN boosted the CA, on ES, of I62-CFH, R53H-CFH, and LA-CFH and also enhanced hemolysis protection by I62-CFH and LA-CFH. We conclude that CCPs 19 and 20 are critical for efficient CA on self-surfaces but less important for DAA. Exposing CCPs 19 and 20 with PspCN and thus enhancing CA on self-surfaces may reverse deficiencies of some CFH variants.

Keywords: CCP module; Streptococcus; complement system; erythrocyte; innate immunity; kidney; multiple domain; mutagenesis; recombinant protein expression; surface plasmon resonance (SPR).

Publication types

  • Comparative Study

MeSH terms

  • Amino Acid Substitution
  • Animals
  • Atypical Hemolytic Uremic Syndrome / genetics*
  • Atypical Hemolytic Uremic Syndrome / metabolism
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Binding Sites
  • Complement Activation*
  • Complement C3 Convertase, Alternative Pathway / chemistry
  • Complement C3 Convertase, Alternative Pathway / genetics
  • Complement C3 Convertase, Alternative Pathway / metabolism
  • Complement C3d / chemistry
  • Complement C3d / genetics
  • Complement C3d / metabolism
  • Complement Factor H / chemistry
  • Complement Factor H / genetics
  • Complement Factor H / metabolism
  • Complement Factor I / chemistry
  • Complement Factor I / genetics
  • Complement Factor I / metabolism
  • Erythrocytes / chemistry
  • Hemolysis
  • Humans
  • Immobilized Proteins / chemistry
  • Immobilized Proteins / genetics
  • Immobilized Proteins / metabolism
  • Macular Degeneration / genetics*
  • Macular Degeneration / metabolism
  • Mutation*
  • Peptide Fragments / chemistry
  • Peptide Fragments / genetics
  • Peptide Fragments / metabolism
  • Protein Interaction Domains and Motifs
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / metabolism
  • Sheep, Domestic
  • Solubility
  • Streptococcus pneumoniae / metabolism
  • Surface Properties

Substances

  • Bacterial Proteins
  • CFH protein, human
  • Immobilized Proteins
  • Peptide Fragments
  • Recombinant Fusion Proteins
  • Complement C3d
  • Complement Factor H
  • CFI protein, human
  • Complement Factor I
  • Complement C3 Convertase, Alternative Pathway