IgG1 and IVIg induce inhibitory ITAM signaling through FcγRIII controlling inflammatory responses

Blood

Volumn 119, Issue 13, 2012, Pages 3084-3096

  Aloulou, Meryem ^a,b   Mkaddem, Sanae Ben ^a,b   Biarnes Pelicot, Martine ^a,b   Boussetta, Tarek ^a,b   Souchet, Hervé ^a,b   Rossato, Elisabetta ^a,b   Benhamou, Marc ^a,b   Crestani, Bruno ^a,b,c   Zhu, Zhou ^d   Blank, Ulrich ^a,b   Launay, Pierre ^a,b   Monteiro, Renato C ^a,b,c  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c BICHAT HOSPITAL   (France)

^d JOHNS HOPKINS ASTHMA AND ALLERGY CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; FC GAMMA RIII ANTIBODY; IMMUNOGLOBULIN F(AB')2 FRAGMENT; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNORECEPTOR TYROSINE BASED ACTIVATION MOTIF; INHIBITOR PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN TYROSINE PHOSPHATASE SHP 1; REACTIVE OXYGEN METABOLITE; RECEPTOR ANTIBODY; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CALCIUM SIGNALING; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG RECEPTOR BINDING; DRUG TARGETING; ENDOCYTOSIS; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOREGULATION; IN VIVO STUDY; MONOCYTE; MOUSE; NEPHRITIS; NONHUMAN; NORMAL HUMAN; OXIDATIVE STRESS; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN MOTIF; SIGNAL TRANSDUCTION; URETER OBSTRUCTION;

EID: 84859364858     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-08-376046     Document Type: Article

References (50)

1. Nimmerjahn F, Ravetch JV. Anti-inflammatory actions of intravenous immunoglobulin. Annu Rev Immunol. 2008;26:513-533. (Pubitemid 351600384)
2. Tha-In T, Bayry J, Metselaar HJ, Kaveri SV, Kwekkeboom J. Modulation of the cellular immune system by intravenous immunoglobulin. Trends Immunol. 2008;29(12):608-615.
3. Crow AR, Song S, Siragam V, Lazarus AH. Mechanisms of action of intravenous immunoglobulin in the treatment of immune thrombocytopenia. Pediatr Blood Cancer. 2006;47(5 suppl): 710-713. (Pubitemid 44360037)
4. Bussel JB. Another interaction of the FcR system with IVIG. Thromb Haemost. 2002;88(6):890-891. (Pubitemid 36018771)
5. Negi VS, Elluru S, Siberil S, et al. Intravenous immunoglobulin: an update on the clinical use and mechanisms of action. J Clin Immunol. 2007; 27(3):233-245. (Pubitemid 46790823)
6. Anthony RM, Kobayashi T,Wermeling F, Ravetch JV. Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway. Nature. 2011; 475(7354):110-113.
7. Nimmerjahn F, Ravetch JV. Fcgamma receptors as regulators of immune responses. Nat Rev Immunol. 2008;8(1):34-47.
8. 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(3): 1165-1170. (Pubitemid 24256631)
9. Ghazizadeh S, Bolen JB, Fleit HB. Physical and functional association of Src-related protein tyrosine kinases with Fc gamma RII in monocytic THP-1 cells. J Biol Chem. 1994;269(12):8878-8884.
10. Hazenbos WL, Gessner JE, Hofhuis FM, et al. Impaired IgG-dependent anaphylaxis and Arthus reaction in Fc gamma RIII (CD16) deficient mice. Immunity. 1996;5(2):181-188. (Pubitemid 26301094)
11. Meyer D, Schiller C, Westermann J, et al. FcgammaRIII (CD16)-deficient mice show IgG isotype-dependent protection to experimental autoimmune hemolytic anemia. Blood. 1998;92(11): 3997-4002. (Pubitemid 28544311)
12. Nimmerjahn F, Ravetch JV. Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science. 2005;310(5753):1510-1512. (Pubitemid 41746349)
13. Vivier E, Daeron M. Immunoreceptor tyrosine-based inhibition motifs. Immunol Today. 1997; 18(6):286-291. (Pubitemid 27261448)
14. Siragam V, Crow AR, Brinc D, Song S, Freedman J, Lazarus AH. Intravenous immunoglobulin ameliorates ITP via activating Fc gamma receptors on dendritic cells. Nat Med. 2006;12(6):688-692. (Pubitemid 43865239)
15. Park-Min KH, Serbina NV, Yang W, et al. FcgammaRIII-dependent inhibition of interferongamma responses mediates suppressive effects of intravenous immune globulin. Immunity. 2007; 26(1):67-78. (Pubitemid 46127754)
16. Araujo LM, Chauvineau A, Zhu R, et al. Cutting edge: intravenous Ig inhibits invariant NKT cell-mediated allergic airway inflammation through FcgammaRIIIA-dependent mechanisms. J Immunol. 2011;186(6):3289-3293.
17. Hamerman JA, Lanier LL. Inhibition of immune responses by ITAM-bearing receptors. Sci STKE. 2006;2006(320):re1.
18. Blank U, Launay P, Benhamou M, Monteiro RC. Inhibitory ITAMs as novel regulators of immunity. Immunol Rev. 2009;232(1):59-71.
19. Ivashkiv LB. Cross-regulation of signaling by ITAM-associated receptors. Nat Immunol. 2009; 10(4):340-347.
20. Pasquier B, Launay P, Kanamaru Y, et al. Identification of FcalphaRI as an inhibitory receptor that controls inflammation: dual role of FcRgamma ITAM. Immunity. 2005;22(1):31-42. (Pubitemid 40143449)
21. Kanamaru Y, Pfirsch S, Aloulou M, et al. Inhibitory ITAM signaling by Fc alpha RI-FcR gamma chain controls multiple activating responses and prevents renal inflammation. J Immunol. 2008; 180(4):2669-2678.
22. Pfirsch-Maisonnas S, Aloulou M, Xu T, et al. Inhibitory ITAM signaling traps activating receptors with the phosphatase SHP-1 to form polarized "inhibisome" clusters. Sci Signal. 2011;4(169): ra24.
23. Pinheiro da Silva F, Aloulou M, Skurnik D, et al. CD16 promotes Escherichia coli sepsis through an FcR gamma inhibitory pathway that prevents phagocytosis and facilitates inflammation. Nat Med. 2007;13(11):1368-1374. (Pubitemid 350073597)
24. Takai T, Ono M, Hikida M, Ohmori H, Ravetch JV. Augmented humoral and anaphylactic responses in Fc gamma RII-deficient mice. Nature. 1996; 379(6563):346-349. (Pubitemid 26033077)
25. Takai T, Li M, Sylvestre D, Clynes R, Ravetch JV. FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell. 1994;76(3):519-529. (Pubitemid 24064172)
26. Zhang L, Oh SY, Wu X, et al. SHP-1 deficient mast cells are hyperresponsive to stimulation and critical in initiating allergic inflammation in the lung. J Immunol. 2010;184(3):1180-1190.
27. Shultz LD, Schweitzer PA, Rajan TV, et al. Mutations at the murine motheaten locus are within the hematopoietic cell protein-tyrosine phosphatase (Hcph) gene. Cell. 1993;73(7):1445-1454. (Pubitemid 23201156)
28. Nishiya T, DeFranco AL. Ligand-regulated chimeric receptor approach reveals distinctive subcellular localization and signaling properties of the Toll-like receptors. J Biol Chem. 2004;279(18): 19008-19017. (Pubitemid 38623331)
29. Unkeless JC. Characterization of a monoclonal antibody directed against mouse macrophage and lymphocyte Fc receptors. J Exp Med. 1979; 150(3):580-596. (Pubitemid 9250687)
30. Fleit HB, Wright SD, Unkeless JC. Human neutrophil Fc gamma receptor distribution and structure. Proc Natl Acad Sci U S A. 1982;79(10):3275-3279. (Pubitemid 12008389)
31. Silvain C, Patry C, Launay P, LehuenA, Monteiro RC. Altered expression of monocyte IgA Fc receptors is associated with defective endocytosis in patients with alcoholic cirrhosis. Potential role for IFNgamma. J Immunol. 1995;155(3):1606-1618.
32. Liu FT, Bohn JW, Ferry EL, et al. Monoclonal dinitrophenyl- specific murine IgE antibody: preparation, isolation, and characterization. J Immunol. 1980;124(6):2728-2737. (Pubitemid 10116046)
33. Monteiro RC, Cooper MD, Kubagawa H. Molecular heterogeneity of Fc alpha receptors detected by receptor-specific monoclonal antibodies. J Immunol. 1992;148(6):1764-1770.
34. van der Laan LJ, Dopp EA, Haworth R, et al. Regulation and functional involvement of macrophage scavenger receptor MARCO in clearance of bacteria in vivo. J Immunol. 1999;162(2):939-947. (Pubitemid 29035419)
35. Roa M, Paumet F, Le Mao J, David B, Blank U. Involvement of the ras-like GTPase rab3d in RBL-2H3 mast cell exocytosis following stimulation via high affinity IgE receptors (Fc epsilonRI). J Immunol. 1997;159(6):2815-2823. (Pubitemid 127681303)
36. Inazaki K, Kanamaru Y, Kojima Y, et al. Smad3 deficiency attenuates renal fibrosis, inflammation, and apoptosis after unilateral ureteral obstruction. Kidney Int. 2004;66(2):597-604. (Pubitemid 38982001)
37. Kanamaru Y, Arcos-Fajardo M, Moura IC, et al. Fc alpha receptor I activation induces leukocyte recruitment and promotes aggravation of glomerulonephritis through the FcR gamma adaptor. Eur J Immunol. 2007;37(4):1116-1128. (Pubitemid 46925347)
38. Bowdish DM, Gordon S. Conserved domains of the class A scavenger receptors: evolution and function. Immunol Rev. 2009;227(1):19-31.
39. Fournier EM, Siberil S, Costes A, et al. Activation of human peripheral IgM+ B cells is transiently inhibited by BCR-independent aggregation of Fc gammaRIIB. J Immunol. 2008;181(8):5350-5359.
40. Clynes R. Protective mechanisms of IVIG. Curr Opin Immunol. 2007;19(6):646-651. (Pubitemid 350236813)
41. Nimmerjahn F, Ravetch JV. Fcgamma receptors: old friends and new family members. Immunity. 2006;24(1):19-28. (Pubitemid 43077197)
42. Doerner AM, Chen LY, Ye RD, Yong J, Huang S, Pan ZK. Cell type-specific release of matrix-metallo-proteinase-9 by bacterial chemoattractant in human blood phagocytic leukocytes. Int J Clin Exp Med. 2011;4(1):67-73.
43. Boussetta T, Gougerot-Pocidalo MA, Hayem G, et al. The prolyl isomerase Pin1 acts as a novel molecular switch for TNF-alpha-induced priming of the NADPH oxidase in human neutrophils. Blood. 2010;116(26):5795-5802.
44. Mohr FC, Fewtrell C. IgE receptor-mediated depolarization of rat basophilic leukemia cells measured with the fluorescent probe bis-oxonol. J Immunol. 1987;138(5):1564-1570. (Pubitemid 17029458)
45. Woof JM, Burton DR. Human antibody-Fc receptor interactions illuminated by crystal structures. Nat Rev Immunol. 2004;4(2):89-99. (Pubitemid 38209203)
46. Pinheiro da Silva F, Aloulou M, Benhamou M, Monteiro RC. Inhibitory ITAMs: a matter of life and death. Trends Immunol. 2008;29(8):366-373.
47. Long EO. Negative signaling by inhibitory receptors: the NK cell paradigm. Immunol Rev. 2008; 224:70-84.
48. Zhang Z, Shen K, Lu W, Cole PA. The role of C-terminal tyrosine phosphorylation in the regulation of SHP-1 explored via expressed protein ligation. J Biol Chem. 2003;278(7):4668-4674. (Pubitemid 36800966)
49. Bruhns P, Iannascoli B, England P, et al. Specificity and affinity of human Fcgamma receptors and their polymorphic variants for human IgG subclasses. Blood. 2009;113(16):3716-3725.
50. Spalter SH, Kaveri SV, Bonnin E, Mani JC, Cartron JP, Kazatchkine MD. Normal human serum contains natural antibodies reactive with autologous ABO blood group antigens. Blood. 1999; 93(12):4418-4424. (Pubitemid 29279285)