A novel immuno-competitive capture mass spectrometry strategy for protein-protein interaction profiling reveals that LATS kinases regulate HCV replication through NS5A phosphorylation

Mol Cell Proteomics. 2014 Nov;13(11):3040-8. doi: 10.1074/mcp.M113.028977. Epub 2014 Jul 20.

Abstract

Mapping protein-protein interactions is essential to fully characterize the biological function of a protein and improve our understanding of diseases. Affinity purification coupled to mass spectrometry (AP-MS) using selective antibodies against a target protein has been commonly applied to study protein complexes. However, one major limitation is a lack of specificity as a substantial part of the proposed binders is due to nonspecific interactions. Here, we describe an innovative immuno-competitive capture mass spectrometry (ICC-MS) method to allow systematic investigation of protein-protein interactions. ICC-MS markedly increases the specificity of classical immunoprecipitation (IP) by introducing a competition step between free and capturing antibody prior to IP. Instead of comparing only one experimental sample with a control, the methodology generates a 12-concentration antibody competition profile. Label-free quantitation followed by a robust statistical analysis of the data is then used to extract the cellular interactome of a protein of interest and to filter out background proteins. We applied this new approach to specifically map the interactome of hepatitis C virus (HCV) nonstructural protein 5A (NS5A) in a cellular HCV replication system and uncovered eight new NS5A-interacting protein candidates along with two previously validated binding partners. Follow-up biological validation experiments revealed that large tumor suppressor homolog 1 and 2 (LATS1 and LATS2, respectively), two closely related human protein kinases, are novel host kinases responsible for NS5A phosphorylation at a highly conserved position required for optimal HCV genome replication. These results are the first illustration of the value of ICC-MS for the analysis of endogenous protein complexes to identify biologically relevant protein-protein interactions with high specificity.

MeSH terms

  • Cell Line
  • DNA Replication / genetics
  • Genome, Viral / genetics
  • Hepacivirus / growth & development*
  • Humans
  • Mass Spectrometry / methods
  • Minor Histocompatibility Antigens
  • Phosphorylation
  • Phosphotransferases (Alcohol Group Acceptor) / genetics
  • Protein Binding
  • Protein Interaction Mapping / methods*
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • Protein Structure, Tertiary
  • Proteome / analysis
  • RNA Interference
  • RNA, Small Interfering
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism*
  • Viral Nonstructural Proteins / metabolism*
  • Virus Replication / genetics
  • Virus Replication / physiology

Substances

  • Minor Histocompatibility Antigens
  • Proteome
  • RNA, Small Interfering
  • Tumor Suppressor Proteins
  • Viral Nonstructural Proteins
  • LATS1 protein, human
  • Phosphotransferases (Alcohol Group Acceptor)
  • LATS2 protein, human
  • phosphatidylinositol phosphate 4-kinase
  • Protein Serine-Threonine Kinases
  • NS-5 protein, hepatitis C virus