The serum- and glucocorticoid-inducible kinase 1 (SGK1) influences platelet calcium signaling and function by regulation of Orai1 expression in megakaryocytes

Blood. 2012 Jan 5;119(1):251-61. doi: 10.1182/blood-2011-06-359976. Epub 2011 Oct 26.

Abstract

Platelets are activated on increase of cytosolic Ca2+ activity ([Ca2+](i)), accomplished by store-operated Ca2+ entry (SOCE) involving the pore-forming ion channel subunit Orai1. Here, we show, for the first time, that the serum- and glucocorticoid-inducible kinase 1 (SGK1) is expressed in platelets and megakaryocytes. SOCE and agonist-induced [Ca2+](i) increase are significantly blunted in platelets from SGK1 knockout mice (sgk1(-/-)). Similarly, Ca2+ -dependent degranulation, integrin α(IIb)β3 activation, phosphatidylserine exposure, aggregation, and in vitro thrombus formation were significantly impaired in sgk1(-/-) platelets, whereas tail bleeding time was not significantly enhanced. Platelet and megakaryocyte Orai1 transcript levels and membrane protein abundance were significantly reduced in sgk1(-/-) mice. In human megakaryoblastic cells (MEG-01), transfection with constitutively active (S422D)SGK1 but not with inactive (K127N)SGK1 significantly enhanced Orai1 expression and SOCE, while effects reversed by the SGK1 inhibitor GSK650394 (1μM). Transfection of MEG-01 cells with (S422D)SGK1 significantly increased phosphorylation of IκB kinase α/β and IκBα resulting in nuclear translocation of NF-κB subunit p65. Treatment of (S422D)SGK1-transfected MEG-01 cells with the IκB kinase inhibitor BMS-345541 (10μM) abolished SGK1-induced increase of Orai1 expression and SOCE. The present observations unravel SGK1 as novel regulator of platelet function, effective at least in part by NF-κB-dependent transcriptional up-regulation of Orai1 in megakaryocytes and increasing platelet SOCE.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bleeding Time
  • Blood Platelets / metabolism*
  • Blotting, Western
  • Calcium / metabolism*
  • Calcium Channels / genetics
  • Calcium Channels / metabolism*
  • Calcium Signaling*
  • Cells, Cultured
  • Female
  • Flow Cytometry
  • Fluorescent Antibody Technique
  • Humans
  • Immediate-Early Proteins / physiology*
  • Immunoenzyme Techniques
  • Leukemia, Megakaryoblastic, Acute / metabolism
  • Leukemia, Megakaryoblastic, Acute / pathology
  • Male
  • Megakaryocytes / cytology
  • Megakaryocytes / metabolism*
  • Mice
  • Mice, Knockout
  • NF-kappa B / genetics
  • NF-kappa B / metabolism
  • ORAI1 Protein
  • Phosphorylation
  • Platelet Aggregation
  • Protein Serine-Threonine Kinases / physiology*
  • RNA, Messenger / genetics
  • Reverse Transcriptase Polymerase Chain Reaction
  • Thrombosis / etiology
  • Thrombosis / metabolism
  • Thrombosis / pathology

Substances

  • Calcium Channels
  • Immediate-Early Proteins
  • NF-kappa B
  • ORAI1 Protein
  • Orai1 protein, mouse
  • RNA, Messenger
  • Protein Serine-Threonine Kinases
  • serum-glucocorticoid regulated kinase
  • Calcium