Inhibitory ITAMs as novel regulators of immunity

Immunological Reviews

Volumn 232, Issue 1, 2009, Pages 59-71

  Blank, Ulrich ^a   Launay, Pierre ^a   Benhamou, Marc ^a   Monteiro, Renato C ^a  

^a INSERM   (France)

Author keywords

Immunoglobulin A; Immunoreceptors; Inhibitory receptors; Tyrosine based motifs

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD16 ANTIGEN; FC RECEPTOR; IMMUNOGLOBULIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN F(AB) FRAGMENT; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MEMBRANE RECEPTOR; PROTEIN TYROSINE PHOSPHATASE SHP 1; T LYMPHOCYTE RECEPTOR; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 2; UNCLASSIFIED DRUG;

ASTHMA; AUTOIMMUNITY; CELL ACTIVATION; ESCHERICHIA COLI; GLOMERULONEPHRITIS; GUILLAIN BARRE SYNDROME; IDIOPATHIC THROMBOCYTOPENIC PURPURA; IMMUNE RESPONSE; IMMUNORECEPTOR TYROSINE BASED ACTIVATION MOTIF; IMMUNORECEPTOR TYROSINE BASED INHIBITORY MOTIF; IMMUNOREGULATION; IMMUNOTHERAPY; INHIBITORY IMMUNORECEPTOR TYROSINE BASED ACTIVATION MOTIF; KIDNEY DISEASE; MUCOCUTANEOUS LYMPH NODE SYNDROME; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN MOTIF; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; THROMBOCYTOPENIA;

ANIMALS; ANTIGENS, CD; AUTOIMMUNE DISEASES; FEEDBACK, PHYSIOLOGICAL; HUMANS; HYPERSENSITIVITY; IMMUNE EVASION; IMMUNITY; IMMUNOGLOBULIN A; IMMUNOGLOBULINS, INTRAVENOUS; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTORS, FC; SIGNAL TRANSDUCTION; TYROSINE;

EID: 70350406445     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2009.00832.x     Document Type: Review

References (107)

1. Hamerman JA, Lanier LL. Inhibition of immune responses by ITAM-bearing receptors. Sci STKE 2006 320 : re1.
2. Abram CL, Lowell CA. The expanding role for ITAM-based signaling pathways in immune cells. Sci STKE 2007 377 : re2.
3. Veillette A, Latour S, Davidson D. Negative regulation of immunoreceptor signaling. Annu Rev Immunol 2002 20 : 669 707.
4. Daeron M, Lesourne R. Negative signaling in Fc receptor complexes. Adv Immunol 2006 89 : 39 86.
5. Vivier E, Nunes JA, Vely F. Natural killer cell signaling pathways. Science 2004 306 : 1517 1519.
6. Coggeshall KM, Nakamura K, Phee H. How do inhibitory phosphatases work? Mol Immunol 2002 39 : 521 529.
7. Pasquier B, et al. Identification of FcalphaRI as an inhibitory receptor that controls inflammation: dual role of FcRgamma ITAM. Immunity 2005 22 : 31 42.
8. Hamerman JA, Tchao NK, Lowell CA, Lanier LL. Enhanced Toll-like receptor responses in the absence of signaling adaptor DAP12. Nat Immunol 2005 6 : 579 586.
9. Pinheiro da Silva F, et al. CD16 promotes Escherichia coli sepsis through an FcR gamma inhibitory pathway that prevents phagocytosis and facilitates inflammation. Nat Med 2007 13 : 1368 1374.
10. Kanamaru Y, et al. Inhibitory ITAM signaling by Fc alpha RI-FcR gamma chain controls multiple activating responses and prevents renal inflammation. J Immunol 2008 180 : 2669 2678.
11. Pinheiro da Silva F, Aloulou M, Benhamou M, Monteiro RC. Inhibitory ITAMs: a matter of life and death. Trends Immunol 2008 29 : 366 373.
12. Blasius A, Vermi W, Krug A, Facchetti F, Cella M, Colonna M. A cell-surface molecule selectively expressed on murine natural interferon-producing cells that blocks secretion of interferon-alpha. Blood 2004 103 : 4201 4206.
13. Blasius AL, Cella M, Maldonado J, Takai T, Colonna M. Siglec-H is an IPC-specific receptor that modulates type I IFN secretion through DAP12. Blood 2006 107 : 2474 2476.
14. Cao W, et al. Plasmacytoid dendritic cell-specific receptor ILT7-Fc epsilonRI gamma inhibits Toll-like receptor-induced interferon production. J Exp Med 2006 203 : 1399 1405.
15. Hamerman JA, Jarjoura JR, Humphrey MB, Nakamura MC, Seaman WE, Lanier LL. Cutting edge: inhibition of TLR and FcR responses in macrophages by triggering receptor expressed on myeloid cells (TREM)-2 and DAP12. J Immunol 2006 177 : 2051 2055.
16. Takaki R, Watson SR, Lanier LL. DAP12: an adapter protein with dual functionality. Immunol Rev 2006 214 : 118 129.
17. Turnbull IR, McDunn JE, Takai T, Townsend RR, Cobb JP, Colonna M. DAP12 (KARAP) amplifies inflammation and increases mortality from endotoxemia and septic peritonitis. J Exp Med 2005 202 : 363 369.
18. Turnbull IR, et al. Cutting edge: TREM-2 attenuates macrophage activation. J Immunol 2006 177 : 3520 3524.
19. Fuchs A, Cella M, Kondo T, Colonna M. Paradoxic inhibition of human natural interferon-producing cells by the activating receptor NKp44. Blood 2005 106 : 2076 2082.
20. De Magistris MT, et al. Antigen analog-major histocompatibility complexes act as antagonists of the T cell receptor. Cell 1992 68 : 625 634.
21. Sloan-Lancaster J, Evavold BD, Allen PM. Induction of T-cell anergy by altered T-cell-receptor ligand on live antigen-presenting cells. Nature 1993 363 : 156 159.
22. Evavold BD, Allen PM. Separation of IL-4 production from Th cell proliferation by an altered T cell receptor ligand. Science 1991 252 : 1308 1310.
23. Sloan-Lancaster J, Shaw AS, Rothbard JB, Allen PM. Partial T cell signaling: altered phospho-zeta and lack of zap70 recruitment in APL-induced T cell anergy. Cell 1994 79 : 913 922.
24. Dittel BN, Stefanova I, Germain RN, Janeway CA Jr. Cross-antagonism of a T cell clone expressing two distinct T cell receptors. Immunity 1999 11 : 289 298.
25. Robertson JM, Evavold BD. Cutting edge: dueling TCRs: peptide antagonism of CD4+ T cells with dual antigen specificities. J Immunol 1999 163 : 1750 1754.
26. Kersh EN, Shaw AS, Allen PM. Fidelity of T cell activation through multistep T cell receptor zeta phosphorylation. Science 1998 281 : 572 575.
27. Kersh EN, Kersh GJ, Allen PM. Partially phosphorylated T cell receptor zeta molecules can inhibit T cell activation. J Exp Med 1999 190 : 1627 1636.
28. Monroe JG. ITAM-mediated tonic signalling through pre-BCR and BCR complexes. Nat Rev Immunol 2006 6 : 283 294.
29. Kraus M, et al. Interference with immunoglobulin (Ig)alpha immunoreceptor tyrosine-based activation motif (ITAM) phosphorylation modulates or blocks B cell development, depending on the availability of an Igbeta cytoplasmic tail. J Exp Med 2001 194 : 455 469.
30. Kraus M, Saijo K, Torres RM, Rajewsky K. Ig-alpha cytoplasmic truncation renders immature B cells more sensitive to antigen contact. Immunity 1999 11 : 537 545.
31. Furumoto Y, Nunomura S, Terada T, Rivera J, Ra C. The FcepsilonRIbeta immunoreceptor tyrosine-based activation motif exerts inhibitory control on MAPK and IkappaB kinase phosphorylation and mast cell cytokine production. J Biol Chem 2004 279 : 49177 49187.
32. On M, Billingsley JM, Jouvin MH, Kinet JP. Molecular dissection of the FcRbeta signaling amplifier. J Biol Chem 2004 279 : 45782 45790.
33. Bakker AB, Baker E, Sutherland GR, Phillips JH, Lanier LL. Myeloid DAP12-associating lectin (MDL)-1 is a cell surface receptor involved in the activation of myeloid cells. Proc Natl Acad Sci USA 1999 96 : 9792 9796.
34. Launay P, Patry C, Lehuen A, Pasquier B, Blank U, Monteiro RC. Alternative endocytic pathway for immunoglobulin A Fc receptors (CD89) depends on the lack of FcRgamma association and protects against degradation of bound ligand. J Biol Chem 1999 274 : 7216 7225.
35. Monteiro RC, van de Winkel JGJ. IgA Fc receptors. Annu Rev Immunol 2003 21 : 177 204.
36. Olas K, Butterweck H, Teschner W, Schwarz HP, Reipert B. Immunomodulatory properties of human serum immunoglobulin A: anti-inflammatory and pro-inflammatory activities in human monocytes and peripheral blood mononuclear cells. Clin Exp Immunol 2005 140 : 478 490.
37. Van Epps DE, Brown SL. Inhibition of formylmethionyl-leucyl- phenylalanine-stimulated neutrophil chemiluminescence by human immunoglobulin A paraproteins. Infect Immun 1981 34 : 864 870.
38. Van Epps DE, Reed K, Williams RC Jr. Suppression of human PMN bactericidal activity by human IgA paraproteins. Cell Immunol 1978 36 : 363 376.
39. Van Epps DE, Williams RC Jr. Suppression of leukocyte chemotaxis by human IgA myeloma components. J Exp Med 1976 144 : 1227 1242.
40. Wilton JM. Suppression by IgA of IgG-mediated phagocytosis by human polymorphonuclear leucocytes. Clin Exp Immunol 1978 34 : 423 428.
41. Wolf HM, Fischer MB, Puhringer H, Samstag A, Vogel E, Eibl MM. Human serum IgA downregulates the release of inflammatory cytokines (tumor necrosis factor-alpha, interleukin-6) in human monocytes. Blood 1994 83 : 1278 1288.
42. Wines BD, Sardjono CT, Trist HH, Lay CS, Hogarth PM. The interaction of Fc alpha RI with IgA and its implications for ligand binding by immunoreceptors of the leukocyte receptor cluster. J Immunol 2001 166 : 1781 1789.
43. Wurzburg BA, Jardetzky TS. The IgA receptor complex: a two-for-one deal. Nat Struct Biol 2003 10 : 585 587.
44. Bouchon A, Dietrich J, Colonna M. Cutting edge: inflammatory responses can be triggered by TREM-1, a novel receptor expressed on neutrophils and monocytes. J Immunol 2000 164 : 4991 4995.
45. Smith KM, Wu J, Bakker AB, Phillips JH, Lanier LL. Ly-49D and Ly-49H associate with mouse DAP12 and form activating receptors. J Immunol 1998 161 : 7 10.
46. Fukao T, Koyasu S. PI3K and negative regulation of TLR signaling. Trends Immunol 2003 24 : 358 363.
47. Reth M. Antigen receptor tail clue. Nature 1989 338 : 383 384.
48. Fodor S, Jakus Z, Mocsai A. ITAM-based signaling beyond the adaptive immune response. Immunol Lett 2006 104 : 29 37.
49. Underhill DM, Goodridge HS. The many faces of ITAMs. Trends Immunol 2007 28 : 66 73.
50. Bolland S, Ravetch JV. Inhibitory pathways triggered by ITIM-containing receptors. Adv Immunol 1999 72 : 149 177.
51. Held W, Mariuzza RA. Cis interactions of immunoreceptors with MHC and non-MHC ligands. Nat Rev Immunol 2008 8 : 269 278.
52. Fournier EM, et al. Activation of human peripheral IgM+ B cells is transiently inhibited by BCR-independent aggregation of Fc gammaRIIB. J Immunol 2008 181 : 5350 5359.
53. Launay P, Lehuen A, Kawakami T, Blank U, Monteiro RC. IgA Fc receptor (CD89) activation enables coupling to syk and Btk tyrosine kinase pathways: differential signaling after IFN-gamma or phorbol ester stimulation. J Leukoc Biol 1998 63 : 636 642.
54. Kanamaru Y, 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 : 1116 1128.
55. Tiwari N, et al. VAMP-8 segregates mast cell-preformed mediator exocytosis from cytokine trafficking pathways. Blood 2008 111 : 3665 3674.
56. Kilgore NE, Carter JD, Lorenz U, Evavold BD. Cutting edge: dependence of TCR antagonism on Src homology 2 domain-containing protein tyrosine phosphatase activity. J Immunol 2003 170 : 4891 4895.
57. Stefanova I, Hemmer B, Vergelli M, Martin R, Biddison WE, Germain RN. TCR ligand discrimination is enforced by competing ERK positive and SHP-1 negative feedback pathways. Nat Immunol 2003 4 : 248 254.
58. Ganesan LP, Fang H, Marsh CB, Tridandapani S. The protein-tyrosine phosphatase SHP-1 associates with the phosphorylated immunoreceptor tyrosine-based activation motif of Fc gamma RIIa to modulate signaling events in myeloid cells. J Biol Chem 2003 278 : 35710 35717.
59. Kimura T, Zhang J, Sagawa K, Sakaguchi K, Appella E, Siraganian RP. Syk-independent tyrosine phosphorylation and association of the protein tyrosine phosphatases SHP-1 and SHP-2 with the high affinity IgE receptor. J Immunol 1997 159 : 4426 4434. (Pubitemid 127470602)
60. Liang B, et al. Regulatory T cells inhibit dendritic cells by lymphocyte activation gene-3 engagement of MHC class II. J Immunol 2008 180 : 5916 5926.
61. Torigoe C, Inman JK, Metzger H. An unusual mechanism for ligand antagonism. Science 1998 281 : 568 572.
62. Beaufils P, Choquet D, Mamoun RZ, Malissen B. The (YXXL/I)2 signalling motif found in the cytoplasmic segments of the bovine leukaemia virus envelope protein and Epstein-Barr virus latent membrane protein 2A can elicit early and late lymphocyte activation events. EMBO J 1993 12 : 5105 5112.
63. Miller CL, et al. Integral membrane protein 2 of Epstein-Barr virus regulates reactivation from latency through dominant negative effects on protein-tyrosine kinases. Immunity 1995 2 : 155 166.
64. Fukao T, et al. PI3K-mediated negative feedback regulation of IL-12 production in DCs. Nat Immunol 2002 3 : 875 881.
65. Rock J, et al. CD303 (BDCA-2) signals in plasmacytoid dendritic cells via a BCR-like signalosome involving Syk, Slp65 and PLCgamma2. Eur J Immunol 2007 7 : 3564 3575.
66. Kagan JC, Medzhitov R. Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 2006 125 : 943 955.
67. Rodriguez W, et al. C-reactive protein-mediated suppression of nephrotoxic nephritis: role of macrophages, complement, and Fcgamma receptors. J Immunol 2007 178 : 530 538.
68. Sutterwala FS, Noel GJ, Salgame P, Mosser DM. Reversal of proinflammatory responses by ligating the macrophage Fcgamma receptor type I. J Exp Med 1998 188 : 217 222.
69. Lee DJ, et al. LILRA2 activation inhibits dendritic cell differentiation and antigen presentation to T cells. J Immunol 2007 179 : 8128 8136.
70. Kalesnikoff J, et al. Monomeric IgE stimulates signaling pathways in mast cells that lead to cytokine production and cell survival. Immunity 2001 14 : 801 811.
71. Asai K, et al. Regulation of mast cell survival by IgE. Immunity 2001 14 : 791 800.
72. Bryce PJ, Miller ML, Miyajima I, Tsai M, Galli SJ, Oettgen HC. Immune sensitization in the skin is enhanced by antigen-independent effects of IgE. Immunity 2004 20 : 381 392.
73. Kitaura J, et al. Evidence that IgE molecules mediate a spectrum of effects on mast cell survival and activation via aggregation of the FcepsilonRI. Proc Natl Acad Sci USA 2003 100 : 12911 12916.
74. Kerr MA. The structure and function of human IgA. Biochem J 1990 271 : 285 296.
75. Russell MW, Sibley DA, Nikolova EB, Tomana M, Mestecky J. IgA antibody as a non-inflammatory regulator of immunity. Biochem Soc Trans 1997 25 : 466 470.
76. Woof JM, Kerr MA. The function of immunoglobulin A in immunity. J Pathol 2006 208 : 270 282.
77. Corthesy B. Roundtrip ticket for secretory IgA: role in mucosal homeostasis? J Immunol 2007 178 : 27 32.
78. Nikolova EB, Russell MW. Dual function of human IgA antibodies: inhibition of phagocytosis in circulating neutrophils and enhancement of responses in IL-8-stimulated cells. J Leukoc Biol 1995 57 : 875 882.
79. Schaffer FM, Monteiro RC, Volanakis JE, Cooper MD. IgA deficiency. Immunodeficiency Rev 1991 3 : 15 44.
80. Jacob CM, Pastorino AC, Fahl K, Carneiro-Sampaio M, Monteiro RC. Autoimmunity in IgA deficiency: revisiting the role of IgA as a silent housekeeper. J Clin Immunol 2008 28 : S56 S61.
81. Clynes R. Protective mechanisms of IVIG. Curr Opin Immunol 2007 19 : 646 651.
82. Nimmerjahn F, Ravetch JV. Anti-inflammatory actions of intravenous immunoglobulin. Annu Rev Immunol 2008 26 : 513 533.
83. Basta M, et al. F(ab)′2-mediated neutralization of C3a and C5a anaphylatoxins: a novel effector function of immunoglobulins. Nat Med 2003 9 : 431 438.
84. Debre M, et al. Infusion of Fc gamma fragments for treatment of children with acute immune thrombocytopenic purpura. Lancet 1993 342 : 945 949.
85. Kaneko Y, Nimmerjahn F, Ravetch JV. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 2006 313 : 670 673.
86. Samuelsson A, Towers TL, Ravetch JV. Anti-inflammatory activity of IVIG mediated through the inhibitory Fc receptor. Science 2001 291 : 484 486.
87. 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 : 688 692.
88. Park-Min KH, et al. FcgammaRIII-dependent inhibition of interferon-gamma responses mediates suppressive effects of intravenous immune globulin. Immunity 2007 26 : 67 78.
89. Bayry J, et al. Inhibition of maturation and function of dendritic cells by intravenous immunoglobulin. Blood 2003 101 : 758 765.
90. Anthony RM, Wermeling F, Karlsson MC, Ravetch JV. Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc Natl Acad Sci USA 2008 105 : 19571 19578.
91. Araki N, Johnson MT, Swanson JA. A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J Cell Biol 1996 135 : 1249 1260.
92. Guha M, Mackman N. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J Biol Chem 2002 277 : 32124 32132.
93. Hatakeyama M. Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat Rev Cancer 2004 4 : 688 694. (Pubitemid 39215067)
94. Grande SM, Ross SR, Monroe JG. Viral immunoreceptor-associated tyrosine-based activation motifs: potential players in oncogenesis. Future Oncol 2006 2 : 301 310.
95. Barrow AD, Trowsdale J. You say ITAM and I say ITIM, let's call the whole thing off: the ambiguity of immunoreceptor signalling. Eur J Immunol 2006 36 : 1646 1653.
96. Lanier LL. Viral immunoreceptor tyrosine-based activation motif (ITAM)-mediated signaling in cell transformation and cancer. Trends Cell Biol 2006 16 : 388 390.
97. Katz E, et al. MMTV Env encodes an ITAM responsible for transformation of mammary epithelial cells in three-dimensional culture. J Exp Med 2005 201 : 431 439.
98. Scholle F, Bendt KM, Raab-Traub N. Epstein-Barr virus LMP2A transforms epithelial cells, inhibits cell differentiation, and activates Akt. J Virol 2000 74 : 10681 10689.
99. Babcock GJ, Decker LL, Volk M, Thorley-Lawson DA. EBV persistence in memory B cells in vivo. Immunity 1998 9 : 395 404.
100. Thorley-Lawson DA. Epstein-Barr virus: exploiting the immune system. Nat Rev Immunol 2001 1 : 75 82.
101. Turnbull IR, Colonna M. Activating and inhibitory functions of DAP12. Nat Rev Immunol 2007 7 : 155 161.
102. Ivashkiv LB. Cross-regulation of signaling by ITAM-associated receptors. Nat Immunol 2009 10 : 340 347.
103. Kanamaru Y, et al. IgA Fc receptor I signals apoptosis through the FcRgamma ITAM and affects tumor growth. Blood 2007 109 : 203 211.
104. Pearse RN, Kawabe T, Bolland S, Guinamard R, Kurosaki T, Ravetch JV. SHIP recruitment attenuates Fc gamma RIIB-induced B cell apoptosis. Immunity 1999 10 : 753 760.
105. Imbach P, et al. High-dose intravenous gammaglobulin for idiopathic thrombocytopenic purpura in childhood. Lancet 1981 1 : 1228 1231.
106. Fehr J, Hofmann V, Kappeler U. Transient reversal of thrombocytopenia in idiopathic thrombocytopenic purpura by high-dose intravenous gamma globulin. N Engl J Med 1982 306 : 1254 1258.
107. Launay P, et al. Fcalpha receptor (CD89) mediates the development of immunoglobulin A (IgA) nephropathy (Berger's disease). Evidence for pathogenic soluble receptor-Iga complexes in patients and CD89 transgenic mice. J Exp Med 2000 191 : 1999 2009.