Sulfotyrosine-Mediated Recognition of Human Thrombin by a Tsetse Fly Anticoagulant Mimics Physiological Substrates

Bárbara Calisto, Jorge Ripoll-Rozada, L.J. Dowman, Charlotte Franck, Stijn Agten, Benjamin L Parker, Rita Carvalho Veloso, Nuno Vale, Paula Gomes, Daniele de Sanctis, R.J. Payne, P.J.B. Pereira*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Despite possessing only 32 residues, the tsetse thrombin inhibitor (TTI) is among the most potent anticoagulants described, with sub-picomolar inhibitory activity against thrombin. Unexpectedly, TTI isolated from the fly is 2000-fold more active and 180 Da heavier than synthetic and recombinant variants. We predicted the presence of a tyrosine O-sulfate post-translational modification of TTI, prompting us to investigate the effect of the modification on anticoagulant activity. A combination of chemical synthesis and functional assays was used to reveal that sulfation significantly improved the inhibitory activity of TTI against thrombin. Using X-ray crystallography, we show that the N-terminal sulfated segment of TTI binds the basic exosite II of thrombin, establishing interactions similar to those of physiologic substrates, while the C-terminal segment abolishes the catalytic activity of thrombin. This non-canonical mode of inhibition, coupled with its potency and small size, makes TTI an attractive scaffold for the design of novel antithrombotics.

Original languageEnglish
Pages (from-to)26-33.e8
Number of pages16
JournalCell Chemical Biology
Volume28
Issue number1
DOIs
Publication statusPublished - 21 Jan 2021
Externally publishedYes

Keywords

  • TYROSINE SULFATION SITES
  • CRYSTAL-STRUCTURE
  • ALPHA-THROMBIN
  • FACTOR-V
  • ACTIVATION
  • FIBRINOGEN
  • BEAMLINE
  • COMPLEX
  • IDENTIFICATION
  • SULFOPROTEINS
  • Alpha-thrombin
  • Activation
  • Identification
  • Crystal-structure
  • Factor-v
  • Complex
  • Tyrosine sulfation sites
  • Fibrinogen
  • Beamline
  • Sulfoproteins

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