Expression and Characterization of Gly-317 Variants of Factor IX Causing Variable Bleeding in Hemophilia B Patients

Biochemistry. 2015 Jun 23;54(24):3814-21. doi: 10.1021/acs.biochem.5b00270. Epub 2015 Jun 10.

Abstract

We recently identified two hemophilia B patients who carried Gly-317 to Arg (FIX-G317R) or Gly-317 to Glu (FIX-G317E) substitutions in their FIX gene. The former mutation caused severe and the latter moderate bleeding in afflicted patients. To understand the molecular basis for the variable clinical manifestation of Gly-317 mutations, we prepared recombinant G317R and G317E derivatives of FIX and compared their kinetic properties to those of recombinant wild-type FIX in appropriate assay systems. Both physiological activators, factor XIa and extrinsic Tenase (factor VIIa-tissue factor), activated both zymogen variants with an ∼1.5-fold elevated K(m); however, extrinsic Tenase activated FIX-G317E with an ∼2-fold improved k(cat). By contrast to zymogen activation, the catalytic activities of both FIXa-G317R and FIXa-G317E enzymes toward the natural substrate, factor X, were dramatically (>4 orders of magnitude) impaired, but their apparent affinity for interaction with factor VIIIa was only slightly (<2-fold) decreased. Further studies revealed that the reactivity of FIXa-G317R and FIXa-G317E with antithrombin has been impaired 10- and 13-fold, respectively, in the absence and 166- and 500-fold, respectively, in the presence of pentasaccharide. As expected, the clotting activities of FIX variants could not be measured by the aPTT assay. These results implicate a critical role for Gly-317 in maintaining normal catalytic function for FIX/FIXa in the clotting cascade. The results further suggest that improved k(cat) of FIX-G317E activation in the extrinsic pathway together with dramatically impaired reactivity of FIXa-G317E with antithrombin may account for the less severe bleeding phenotype of a hemophilia B patient carrying the FIX-G317E mutation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Substitution
  • Cysteine Endopeptidases / metabolism
  • Enzyme Activation
  • Enzyme Precursors / genetics
  • Enzyme Precursors / metabolism*
  • Factor IX / genetics
  • Factor IX / metabolism*
  • Factor VIIIa / metabolism
  • Factor X / metabolism
  • Factor XIa / metabolism
  • Glycine / chemistry*
  • HEK293 Cells
  • Hemophilia B / genetics*
  • Hemophilia B / metabolism
  • Hemophilia B / physiopathology
  • Hemorrhage / etiology*
  • Humans
  • Kinetics
  • Male
  • Mutagenesis, Site-Directed
  • Mutant Proteins / metabolism*
  • Mutation*
  • Neoplasm Proteins / metabolism
  • Recombinant Proteins / metabolism
  • Severity of Illness Index

Substances

  • Enzyme Precursors
  • Mutant Proteins
  • Neoplasm Proteins
  • Recombinant Proteins
  • Factor VIIIa
  • Factor IX
  • Factor X
  • Factor XIa
  • Cysteine Endopeptidases
  • cancer procoagulant
  • Glycine