Novel mutations in RASGRP2, which encodes CalDAG-GEFI, abrogate Rap1 activation, causing platelet dysfunction

Blood. 2016 Sep 1;128(9):1282-9. doi: 10.1182/blood-2015-11-683102. Epub 2016 May 27.

Abstract

In addition to mutations in ITG2B or ITGB3 genes that cause defective αIIbβ3 expression and/or function in Glanzmann's thrombasthenia patients, platelet dysfunction can be a result of genetic variability in proteins that mediate inside-out activation of αIIbβ3 The RASGRP2 gene is strongly expressed in platelets and neutrophils, where its encoded protein CalDAG-GEFI facilitates the activation of Rap1 and subsequent activation of integrins. We used next-generation sequencing (NGS) and whole-exome sequencing (WES) to identify 2 novel function-disrupting mutations in RASGRP2 that account for bleeding diathesis and platelet dysfunction in 2 unrelated families. By using a panel of 71 genes, we identified a homozygous change (c.1142C>T) in exon 10 of RASGRP2 in a 9-year-old child of Chinese origin (family 1). This variant led to a p.Ser381Phe substitution in the CDC25 catalytic domain of CalDAG-GEFI. In 2 Spanish siblings from family 2, WES identified a nonsense homozygous variation (c.337C>T) (p.Arg113X) in exon 5 of RASGRP2 CalDAG-GEFI expression was markedly reduced in platelets from all patients, and by using a novel in vitro assay, we found that the nucleotide exchange activity was dramatically reduced in CalDAG-GEFI p.Ser381Phe. Platelets from homozygous patients exhibited agonist-specific defects in αIIbβ3 integrin activation and aggregation. In contrast, α- and δ-granule secretion, platelet spreading, and clot retraction were not markedly affected. Integrin activation in the patients' neutrophils was also impaired. These patients are the first cases of a CalDAG-GEFI deficiency due to homozygous RASGRP2 mutations that are linked to defects in both leukocyte and platelet integrin activation.

Publication types

  • Case Reports
  • Clinical Trial
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Substitution
  • Blood Platelets / metabolism*
  • Blood Platelets / pathology
  • Child
  • Enzyme Activation / genetics
  • Exons*
  • Female
  • Guanine Nucleotide Exchange Factors* / genetics
  • Guanine Nucleotide Exchange Factors* / metabolism
  • High-Throughput Nucleotide Sequencing
  • Humans
  • Integrin beta3 / genetics
  • Integrin beta3 / metabolism
  • Male
  • Middle Aged
  • Mutation, Missense*
  • Platelet Activation / genetics*
  • Platelet Membrane Glycoprotein IIb / genetics
  • Platelet Membrane Glycoprotein IIb / metabolism
  • Secretory Vesicles / genetics
  • Secretory Vesicles / metabolism
  • Thrombasthenia* / genetics
  • Thrombasthenia* / metabolism
  • Thrombasthenia* / pathology
  • rap1 GTP-Binding Proteins / metabolism*

Substances

  • Guanine Nucleotide Exchange Factors
  • ITGB3 protein, human
  • Integrin beta3
  • Platelet Membrane Glycoprotein IIb
  • RASGRP2 protein, human
  • rap1 GTP-Binding Proteins