Dominant activating RAC2 mutation with lymphopenia, immunodeficiency, and cytoskeletal defects

Amy P. Hsu*, Agnes Donkó, Megan E. Arrington, Muthulekha Swamydas, Danielle Fink, Arundhoti Das, Omar Escobedo, Vincent Bonagura, Paul Szabolcs, Harry N. Steinberg, Jenna Bergerson, Amanda Skoskiewicz, Melanie Mala Makhija, Joie Davis, Ladan Foruraghi, Cindy Palmer, Ramsay L Fuleihan, Joseph A. Church, Avinash Bhandoola, Michail S. LionakisSharon Campbell, Thomas L. Leto, Douglas B. Kuhns, Steven M. Holland

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

40 Scopus citations

Abstract

Ras-related C3 botulinum toxin substrate 2 (RAC2), through interactions with reduced NAD phosphate oxidase component p67phox, activates neutrophil superoxide production, whereas interactions with p21-activated kinase are necessary for fMLF-induced actin remodeling. We identified 3 patients with de novo RAC2[E62K] mutations resulting in severe T- and B-cell lymphopenia, myeloid dysfunction, and recurrent respiratory infections. Neutrophils from RAC2[E62K] patients exhibited excessive superoxide production, impaired fMLF-directed chemotaxis, and abnormal macropinocytosis. Cell lines transfected with RAC2[E62K] displayed characteristics of active guanosine triphosphate (GTP)-bound RAC2 including enhanced superoxide production and increased membrane ruffling. Biochemical studies demonstrated that RAC2[E62K] retains intrinsic GTP hydrolysis; however, GTPase-activating protein failed to accelerate hydrolysis resulting in prolonged active GTP-bound RAC2. Rac2+/E62K mice phenocopy the T- and B-cell lymphopenia, increased neutrophil F-actin, and excessive superoxide production seen in patients. This gain-of-function mutation highlights a specific, nonredundant role for RAC2 in hematopoietic cells that discriminates RAC2 from the related, ubiquitous RAC1.

Original languageEnglish (US)
Pages (from-to)1977-1988
Number of pages12
JournalBlood
Volume133
Issue number18
DOIs
StatePublished - May 2 2019

ASJC Scopus subject areas

  • Hematology
  • Biochemistry
  • Cell Biology
  • Immunology

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