Role of the P2 residue of human alpha 1-antitrypsin in determining target protease specificity

PLoS One. 2017 Sep 18;12(9):e0185074. doi: 10.1371/journal.pone.0185074. eCollection 2017.

Abstract

Alpha 1-antitrypsin (A1AT) is a serine protease inhibitor that mainly inhibits neutrophil elastase in the lungs. A variant of A1AT at the P1 position with methionine 358 to arginine (A1AT-Pittsburgh) is a rapid inhibitor of thrombin with greatly diminished anti-elastase activity. The P2 residue (position 357) of A1AT-Pittsburgh has been shown to play an important role in interactions with thrombin and kallikrein, but the role of P2 residue in wild-type A1AT has largely been unraveled. Here, we investigated the effects of P2 proline substitutions in wild-type A1AT on interactions with porcine pancreatic elastase (PPE) and human neutrophil elastase (HNE). The mutant A1AT proteins (P357A, P357D, P357K, P357L, P357N, P357S, and P357W) were less efficient than the wild-type A1AT at inhibiting PPE and HNE. Among the mutants, P357D did not form a complex with PPE, whereas P357L, P357N, and P357W showed significantly reduced complex formation with PPE. Surprisingly, mass spectrometry analysis revealed that P357D had two cleavage sites after the P9 alanine and the P3 isoleucine residues. Our results indicate that the size and negative charge of the R group of the P2 residue influence the interaction with elastases. Specifically, the negative charge at the P2 residue is disfavored and the resulting conformational changes in the reactive center loop upon interaction with PPE lead to cleavage at new sites. Overall, the results of this study demonstrate a previously unknown role for P2 residue in determining inhibitory specificity of A1AT.

MeSH terms

  • Amino Acid Substitution
  • Animals
  • Humans
  • Leukocyte Elastase / chemistry*
  • Leukocyte Elastase / metabolism
  • Mutation, Missense
  • Swine
  • alpha 1-Antitrypsin / chemistry*
  • alpha 1-Antitrypsin / genetics
  • alpha 1-Antitrypsin / metabolism

Substances

  • SERPINA1 protein, human
  • alpha 1-Antitrypsin
  • Leukocyte Elastase

Grants and funding

Alteogen Inc. provided support in the form of salaries for authors [H-SC, J-SK, SML, and SJP] and research materials/instruments but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the 'author contributions' section.