STIM1 is essential for Fc{γ}receptor activation and autoimmune inflammation

Blood

Volumn 113, Issue 5, 2009, Pages 1097-1104

  Braun, Attila ^a   Gessner, J Engelbert ^b   David, Varga Szabo ^a   Syed, Shahzad N ^b   Konrad, Stephanie ^b   Stegner, David ^a   Vögtle, Timo ^a   Schmidt, Reinhold E ^b   Nieswandt, Bernhard ^a,c  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; FC RECEPTOR; IMMUNOGLOBULIN G; CALCIUM; MEMBRANE PROTEIN; STIM1 PROTEIN, MOUSE;

ALLERGIC PNEUMONITIS; ANAPHYLAXIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNE HEMOLYTIC ANEMIA; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FEMALE; FLOW CYTOMETRY; GENE; IMMUNE COMPLEX DISEASE; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; STROMAL INTERACTION MOLECULE 1 GENE; THROMBOCYTOPENIA; ANIMAL; ANTIGEN ANTIBODY COMPLEX; GENETICS; HUMAN; IMMUNOLOGY; INFLAMMATION; MALE; MOUSE MUTANT; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGEN-ANTIBODY COMPLEX; AUTOANTIBODIES; AUTOIMMUNE DISEASES; CALCIUM; FEMALE; HUMANS; IMMUNOGLOBULIN G; INFLAMMATION; MACROPHAGES; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; PHAGOCYTOSIS; RECEPTORS, IGG; SIGNAL TRANSDUCTION;

EID: 60849115836     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-05-158477     Document Type: Article

References (60)

1. Takai T, Li M, Sylvestre D, Clynes R, Ravetch JV. FcRγchain deletion results in pleiotrophic effector cell defects. Cell. 1994;76:519-529.
2. Schmidt RE, Gessner JE. Fc receptors and their interaction with complement in autoimmunity. Immunol Lett. 2005;100:56-67.
3. Nimmerjahn F, Ravetch JV. Fcγreceptors as regulators of immune responses. Nat Rev Immunol. 2008;8:34-47.
4. Wang AV, Scholl PR, Geha RS. Physical and functional association of the high affinity immunoglobulin G receptor (Fc gamma RI) with the kinases Hck and Lyn. J Exp Med. 1994;180:1165-1170.
5. Takai T. Roles of Fc receptors in autoimmunity. Nat Rev Immunol. 2002;2:580-592.
6. Nimmerjahn F, Bruhns P, Horiuchi K, Ravetch JV. FcγRIV: a novel FcR with distinct IgG subclass specificity. Immunity. 2005;23:41-51.
7. Kiener PA, Rankin BM, Burkhardt AL, et al. Cross-linking of Fcγreceptor I (FcγRI) and receptor II (FcγRII) on monocytic cells activates a signal transduction pathway common to both Fc receptors that involves the stimulation of p72 Syk protein tyrosine kinase. J Biol Chem. 1993;268: 24442-24448.
8. Rankin BM, Yocum SA, Mittler RS, Kiener PA. Stimulation of tyrosine phosphorylation and calcium mobilization by Fcγreceptor cross-linking. Regulation by the phosphotyrosine phosphatase CD45. J Immunol. 1993;150:605-616.
9. 2+]i flux by distinct regions of an Fc receptor. Science. 1991;254:1785-1788.
10. Liao F, Shin HS, Rhee SG. Tyrosine phosphorylation of phospholipase C-γ-1 induced by crosslinking of the high-affinity or low-affinity Fc receptor for IgG in U937 cells. Proc Natl Acad Sci U S A. 1992;89:3659-3663.
11. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol. 2003;4:517-529.
12. Feske S. Calcium signalling in lymphocyte activation and disease. Nat Rev Immunol. 2007;7:690-702.
13. Bird GS, Aziz O, Lievremont JP, et al. Mechanisms of phospholipase C-regulated calcium entry. Curr Mol Med. 2004;4:291-301.
14. 2+channel function. J Cell Biol. 2005;169:435-445.
15. 2+ influx. Curr Biol. 2005;15:1235-1241.
16. 2+ store to the plasma membrane. Nature. 2005;437:902-905.
17. Peinelt C, Vig M, Koomoa DL, et al. Amplification of CRAC current by STIM1 and CRACM1 (Orai1). Nat Cell Biol. 2006;8:771-773.
18. 2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J Cell Biol. 2006;174:803-813.
19. 2+ store depletion. Proc Natl Acad Sci U S A. 2007;104:9301-9306.
20. Xu P, Lu J, Li Z, et al. Aggregation of STIM1 underneath the plasma membrane induces clustering of Orai1. Biochem Biophys Res Commun. 2006;350:969-976.
21. 2+ entry: local activation of CRAC channels by STIM1 at ERplasma membrane junctions. J Cell Biol. 2006; 174:815-825.
22. Feske S, Gwack Y, Prakriya M, et al. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature. 2006;441:179-185.
23. Vig M, Dehaven WI, Bird GS, et al. Defective mast cell effector functions in mice lacking the CRACM1 pore subunit of store-operated calcium release-activated calcium channels. Nat Immunol. 2008;9:89-96.
24. Huang GN, Zeng W, Kim JY, et al. STIM1 carboxyl-terminus activates native SOC, I(crac) and TRPC1 channels. Nat Cell Biol. 2006;8:1003-1010.
25. Oh-Hora M, Yamashita M, Hogan PG, et al. Dual functions for the endoplasmic reticulum calcium sensors STIM1 and STIM2 in T cell activation and tolerance. Nat Immunol. 2008;9:432-443.
26. Baba Y, Nishida K, Fujii Y, et al. Essential function for the calcium sensor STIM1 in mast cell activation and anaphylactic responses. Nat Immunol. 2008;9:81-88.
27. Semenova SB, Kiselev KI, Mozhaeva GN. Lowconductivity calcium channels in the macrophage plasma membrane: activation by inositol-1,4,5-triphosphate. Neurosci Behav Physiol. 1999;29: 339-345.
28. Del Corno M, Liu QH, Schols D, et al. HIV-1 gp120 and chemokine activation of Pyk2 and mitogen-activated protein kinases in primary macrophages mediated by calcium-dependent, pertussis toxin-insensitive chemokine receptor signaling. Blood. 2001;98:2909-2916.
29. 2+ and protein kinase C-dependent signaling pathway for nuclear factor-αB activation, inducible nitric-oxide synthase expression, and tumor necrosis factor-γ production in lipopolysaccharide-stimulated rat peritoneal macrophages. J Biol Chem. 2006;281: 31337-31347.
30. 2+-dependent signaling by TLR2. J Immunol. 2006;177:1330-1337.
31. Hishikawa T, Cheung JY, Yelamarty RV, Knutson DW. Calcium transients during Fc receptor-mediated and nonspecific phagocytosis by murine peritoneal macrophages. J Cell Biol. 1991;115: 59-66.
32. Greenberg S, el Khoury J, di Virgilio F, Kaplan EM, Silverstein SC. Ca(2+)-independent F-actin assembly and disassembly during Fc receptormediated phagocytosis in mouse macrophages. J Cell Biol. 1991;113:757-767.
33. McNeil PL, Swanson JA, Wright SD, Silverstein SC, Taylor DL. Fc-receptor-mediated phagocytosis occurs in macrophages without an increase in average [Ca++]i. J Cell Biol. 1986;102:1586-1592.
34. Varga-Szabo D, Braun A, Kleinschnitz C, et al. The ER calcium sensor STIM1 is an essential mediator of arterial thrombosis and ischemic brain infarction. J Exp Med. 2008;205:1583-1591.
35. Holmes KL, Palfree RG, Hammerling U, Morse HC III. Alleles of the Ly-17 alloantigen define polymorphisms of the murine IgG Fc receptor. Proc Natl Acad Sci U S A. 1985;82:7706-7710.
36. Schiller C, Janssen-Graalfs I, Baumann U, et al. Mouse FcγRII is a negative regulator of FcγRIII in IgG immune complex-triggered inflammation but not in autoantibody-induced hemolysis. Eur J Immunol. 2000;30:481-490.
37. Shibata T, Berney T, Reininger L, et al. Monoclonal anti-erythrocyte autoantibodies derived from NZB mice cause autoimmune hemolytic anemia by two distinct pathogenic mechanisms. Int Immunol. 1990;2:1133-1141.
38. Shushakova N, Skokowa J, Schulman J, et al. C5a anaphylatoxin is a major regulator of activating versus inhibitory FcγRs in immune complexinduced lung disease. J Clin Invest. 2002;110: 1823-1830.
39. Baumann U, Kohl J, Tschernig T, et al. A codominant role of Fcγ RI/III and C5aR in the reverse Arthus reaction. J Immunol. 2000;164:1065-1070.
40. Nieswandt B, Bergmeier W, Rackebrandt K, Gessner JE, Zirngibl H. Identification of critical antigen-specific mechanisms in the development of immune thrombocytopenic purpura in mice. Blood. 2000;96:2520-2527.
41. Hirano M, Davis RS, Fine WD, et al. IgEb immune complexes activate macrophages through FcγRIV binding. Nat Immunol. 2007;8:762-771.
42. Meyer D, Schiller C, Westermann J, et al. FcγRIII (CD16)-deficient mice show IgG isotype-dependent protection to experimental autoimmune hemolytic anemia. Blood. 1998;92:3997-4002.
43. Kumar V, Ali SR, Konrad S, et al. Cell-derived anaphylatoxins as key mediators of antibody-dependent type II autoimmunity in mice. J Clin Invest. 2006;116:512-520.
44. Chouchakova N, Skokowa J, Baumann U, et al. Fcγ RIII-mediated production of TNF-α induces immune complex alveolitis independently of CXC chemokine generation. J Immunol. 2001;166: 5193-5200.
45. Baumann U, Chouchakova N, Gewecke B, et al. Distinct tissue site-specific requirements of mast cells and complement components C3/C5a receptor in IgG immune complex-induced injury of skin and lung. J Immunol. 2001;167:1022-1027.
46. Skokowa J, Ali SR, Felda O, et al. Macrophages induce the inflammatory response in the pulmonary Arthus reaction through G alpha i2 activation that controls C5aR and Fc receptor cooperation. J Immunol. 2005;174:3041-3050.
47. He R, Reid DM, Jones CE, Shulman NR. Spectrum of Ig classes, specificities, and titers of serum antiglycoproteins in chronic idiopathic thrombocytopenic purpura. Blood. 1994;83:1024-1032.
48. Woods Jr., VL, McMillan R. Platelet autoantigens in chronic ITP. Br J Haematol. 1984;57:1-4.
49. Beardsley DS, Ertem M. Platelet autoantibodies in immune thrombocytopenic purpura. Transfus Sci. 1998;19:237-244.
50. Webster ML, Sayeh E, Crow M, et al. Relative efficacy of intravenous immunoglobulin G in ameliorating thrombocytopenia induced by antiplatelet GPIIbIIIa versus GPIbαantibodies. Blood. 2006; 108:943-946.
51. Nieswandt B, Bergmeier W, Schulte V, et al. Targeting of platelet integrin αIIbγ3 determines systemic reaction and bleeding in murine thrombocytopenia regulated by activating and inhibitory FcαR. Int Immunol. 2003;15:341-349.
52. Nieswandt B, Echtenacher B, Wachs FP, et al. Acute systemic reaction and lung alterations induced by an antiplatelet integrin gpIIb/IIIa antibody in mice. Blood. 1999;94:684-693.
53. Grosse J, Braun A, Varga-Szabo D, et al. An EF hand mutation in Stim1 causes premature platelet activation and bleeding in mice. J Clin Invest. 2007;117:3540-3550.
54. Putney Jr., JW. Recent breakthroughs in the molecular mechanism of capacitative calcium entry (with thoughts on how we got here). Cell Calcium. 2007;42:103-110.
55. Parvez S, Beck A, Peinelt C, et al. STIM2 protein mediates distinct store-dependent and store-independent modes of CRAC channel activation. FASEB J. 2008;22:752-761.
56. Gehrs BC, Friedberg RC. Autoimmune hemolytic anemia. Am J Hematol. 2002;69:258-271.
57. Semple JW, Freedman J. Autoimmune pathogenesis and autoimmune hemolytic anemia. Semin Hematol. 2005;42:122-130.
58. Coopamah MD, Garvey MB, Freedman J, Semple JW. Cellular immune mechanisms in autoimmune thrombocytopenic purpura: an update. Transfus Med Rev. 2003;17:69-80.
59. Nardi M, Tomlinson S, Greco MA, Karpatkin S. Complement-independent, peroxide-induced antibody lysis of platelets in HIV-1-related immune thrombocytopenia. Cell. 2001;106:551-561.
60. Huber-Lang M, Younkin EM, Sarma JV, et al. Generation of C5a by phagocytic cells. Am J Pathol. 2002;161:1849-1859.