Cooperation of adapter molecules in proximal signaling cascades during allergic inflammation

Immunological Reviews

Volumn 232, Issue 1, 2009, Pages 99-114

  Kambayashi, Taku ^a   Larosa, David F ^b   Silverman, Michael A ^c   Koretzky, Gary A ^a,b,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Adapter molecules; Allergy; Cell signaling; Fc RI; Mast cell; TLR

Indexed keywords

ADAPTOR PROTEIN; HIGH AFFINITY IMMUNOGLOBULIN E BINDING RECEPTOR; IMMUNOGLOBULIN E RECEPTOR; LAT PROTEIN; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C GAMMA1; PHOSPHOLIPASE C GAMMA2; PROTEIN KINASE FYN; PROTEIN KINASE LYN; PROTEIN KINASE SYK; PROTEIN LAX; PROTEIN NTAL; PROTEIN TYROSINE KINASE; SRC HOMOLOGY 2 DOMAIN CONTAINING LEUKOCYTE PROTEIN OF 76 KDA; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ALLERGIC DISEASE; ALLERGIC INFLAMMATION; AMINO TERMINAL SEQUENCE; CELL ACTIVATION; CELL FUNCTION; COMPLEX FORMATION; DEGRANULATION; ENZYME ACTIVATION; HUMAN; MAST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEFICIENCY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; HUMANS; HYPERSENSITIVITY; MAST CELLS; PROTEIN MULTIMERIZATION; RECEPTOR CROSS-TALK; RECEPTORS, IGE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 70350402356     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2009.00825.x     Document Type: Review

References (135)

1. Kitamura Y. Heterogeneity of mast cells and phenotypic change between subpopulations. Annu Rev Immunol 1989 7 : 59 76.
2. Galli SJ, Maurer M, Lantz CS. Mast cells as sentinels of innate immunity. Curr Opin Immunol 1999 11 : 53 59.
3. Marshall JS. Mast-cell responses to pathogens. Nat Rev Immunol 2004 4 : 787 799.
4. Kulczycki A Jr., Metzger H. The interaction of IgE with rat basophilic leukemia cells. II. Quantitative aspects of the binding reaction. J Exp Med 1974 140 : 1676 1695.
5. Hines C. The diverse effects of mast cell mediators. Clin Rev Allergy Immunol 2002 22 : 149 160.
6. Gilfillan AM, Tkaczyk C. Integrated signalling pathways for mast-cell activation. Nat Rev Immunol 2006 6 : 218 230.
7. Ra C, Jouvin MH, Kinet JP. Complete structure of the mouse mast cell receptor for IgE (Fc epsilon RI) and surface expression of chimeric receptors (rat-mouse-human) on transfected cells. J Biol Chem 1989 264 : 15323 15327.
8. Blank U, Ra C, Miller L, White K, Metzger H, Kinet JP. Complete structure and expression in transfected cells of high affinity IgE receptor. Nature 1989 337 : 187 189.
9. Hakimi J, Seals C, Kondas JA, Pettine L, Danho W, Kochan J. The alpha subunit of the human IgE receptor (FcERI) is sufficient for high affinity IgE binding. J Biol Chem 1990 265 : 22079 22081.
10. Sakurai D, et al. Fc epsilon RI gamma-ITAM is differentially required for mast cell function in vivo. J Immunol 2004 172 : 2374 2381.
11. 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.
12. Gounni AS, Lamkhioued B, Koussih L, Ra C, Renzi PM, Hamid Q. Human neutrophils express the high-affinity receptor for immunoglobulin E (Fc epsilon RI): role in asthma. FASEB J 2001 15 : 940 949.
13. Gounni AS, et al. High-affinity IgE receptor on eosinophils is involved in defence against parasites. Nature 1994 367 : 183 186.
14. Maurer D, et al. Fc epsilon receptor I on dendritic cells delivers IgE-bound multivalent antigens into a cathepsin S-dependent pathway of MHC class II presentation. J Immunol 1998 161 : 2731 2739.
15. Donnadieu E, Jouvin MH, Kinet JP. A second amplifier function for the allergy-associated Fc(epsilon)RI-beta subunit. Immunity 2000 12 : 515 523.
16. Hiraoka S, et al. Fc receptor beta subunit is required for full activation of mast cells through Fc receptor engagement. Int Immunol 1999 11 : 199 207.
17. Hartman ML, Lin SY, Jouvin MH, Kinet JP. Role of the extracellular domain of Fc epsilon RI alpha in intracellular processing and surface expression of the high affinity receptor for IgE Fc epsilon RI. Mol Immunol 2008 45 : 2307 2311.
18. Lin S, Cicala C, Scharenberg AM, Kinet JP. The Fc(epsilon)RIbeta subunit functions as an amplifier of Fc(epsilon)RIgamma-mediated cell activation signals. Cell 1996 85 : 985 995.
19. Pribluda VS, Pribluda C, Metzger H. Transphosphorylation as the mechanism by which the high-affinity receptor for IgE is phosphorylated upon aggregation. Proc Natl Acad Sci USA 1994 91 : 11246 11250.
20. Jouvin MH, Adamczewski M, Numerof R, Letourneur O, Valle A, Kinet JP. Differential control of the tyrosine kinases Lyn and Syk by the two signaling chains of the high affinity immunoglobulin E receptor. J Biol Chem 1994 269 : 5918 5925.
21. Kimura T, Kihara H, Bhattacharyya S, Sakamoto H, Appella E, Siraganian RP. Downstream signaling molecules bind to different phosphorylated immunoreceptor tyrosine-based activation motif (ITAM) peptides of the high affinity IgE receptor. J Biol Chem 1996 271 : 27962 27968.
22. Shiue L, et al. Interaction of p72syk with the gamma and beta subunits of the high-affinity receptor for immunoglobulin E, Fc epsilon RI. Mol Cell Biol 1995 15 : 272 281.
23. Zhang J, Berenstein EH, Evans RL, Siraganian RP. Transfection of Syk protein tyrosine kinase reconstitutes high affinity IgE receptor-mediated degranulation in a Syk-negative variant of rat basophilic leukemia RBL-2H3 cells. J Exp Med 1996 184 : 71 79. (Pubitemid 26247216)
24. Costello PS, et al. Critical role for the tyrosine kinase Syk in signalling through the high affinity IgE receptor of mast cells. Oncogene 1996 13 : 2595 2605.
25. Zhang J, Berenstein E, Siraganian RP. Phosphorylation of Tyr342 in the linker region of Syk is critical for Fc epsilon RI signaling in mast cells. Mol Cell Biol 2002 22 : 8144 8154.
26. Saitoh S, et al. LAT is essential for Fc(epsilon)RI-mediated mast cell activation. Immunity 2000 12 : 525 535.
27. Saitoh S, et al. The four distal tyrosines are required for LAT-dependent signaling in FcepsilonRI-mediated mast cell activation. J Exp Med 2003 198 : 831 843.
28. Malbec O, et al. Linker for activation of T cells integrates positive and negative signaling in mast cells. J Immunol 2004 173 : 5086 5094.
29. Yablonski D, Kadlecek T, Weiss A. Identification of a phospholipase C-gamma1 (PLC-gamma1) SH3 domain-binding site in SLP-76 required for T-cell receptor-mediated activation of PLC-gamma1 and NFAT. Mol Cell Biol 2001 21 : 4208 4218.
30. Liu SK, Fang N, Koretzky GA, McGlade CJ. The hematopoietic-specific adaptor protein gads functions in T-cell signaling via interactions with the SLP-76 and LAT adaptors. Curr Biol 1999 9 : 67 75.
31. Liu Q, Berry D, Nash P, Pawson T, McGlade CJ, Li SS. Structural basis for specific binding of the Gads SH3 domain to an RxxK motif-containing SLP-76 peptide: a novel mode of peptide recognition. Mol Cell 2003 11 : 471 481.
32. Ishiai M, Kurosaki M, Inabe K, Chan AC, Sugamura K, Kurosaki T. Involvement of LAT, Gads, and Grb2 in compartmentation of SLP-76 to the plasma membrane. J Exp Med 2000 192 : 847 856.
33. Pivniouk VI, Martin TR, Lu-Kuo JM, Katz HR, Oettgen HC, Geha RS. SLP-76 deficiency impairs signaling via the high-affinity IgE receptor in mast cells. J Clin Invest 1999 103 : 1737 1743.
34. Fang N, Koretzky GA. SLP-76 and Vav function in separate, but overlapping pathways to augment interleukin-2 promoter activity. J Biol Chem 1999 274 : 16206 16212.
35. Motto D, Ross S, Wu J, Hendricks-Taylor L, Koretzky G. Implication of the GRB2-associated phosphoprotein SLP-76 in T cell receptor-mediated interleukin 2 production. J Exp Med 1996 183 : 1937 1943.
36. Su YW, Zhang Y, Schweikert J, Koretzky GA, Reth M, Wienands J. Interaction of SLP adaptors with the SH2 domain of Tec family kinases. Eur J Immunol 1999 29 : 3702 3711.
37. Zeng R, et al. SLP-76 coordinates Nck-dependent Wiskott-Aldrich syndrome protein recruitment with Vav-1/Cdc42-dependent Wiskott-Aldrich syndrome protein activation at the T cell-APC contact site. J Immunol 2003 171 : 1360 1368.
38. Finkelstein LD, Schwartzberg PL. Tec kinases: shaping T-cell activation through actin. Trends Cell Biol 2004 14 : 443 451.
39. Kim YJ, Sekiya F, Poulin B, Bae YS, Rhee SG. Mechanism of B-cell receptor-induced phosphorylation and activation of phospholipase C-gamma2. Mol Cell Biol 2004 24 : 9986 9999.
40. Takata M, Kurosaki T. A role for Bruton's tyrosine kinase in B cell antigen receptor-mediated activation of phospholipase C-gamma 2. J Exp Med 1996 184 : 31 40.
41. Kawakami Y, et al. Bruton's tyrosine kinase regulates apoptosis and JNK/SAPK kinase activity. Proc Natl Acad Sci USA 1997 94 : 3938 3942.
42. Kettner A, et al. Structural requirements of SLP-76 in signaling via the high-affinity immunoglobulin E receptor (Fc epsilon RI) in mast cells. Mol Cell Biol 2003 23 : 2395 2406. (Pubitemid 36351021)
43. Wu JN, Jordan MS, Silverman MA, Peterson EJ, Koretzky GA. Differential requirement for adapter proteins Src homology 2 domain-containing leukocyte phosphoprotein of 76 kDa and adhesion- and degranulation-promoting adapter protein in FcepsilonRI signaling and mast cell function. J Immunol 2004 172 : 6768 6774.
44. Jordan MS, Singer AL, Koretzky GA. Adaptors as central mediators of signal transduction in immune cells. Nat Immunol 2003 4 : 110 116.
45. Finco TS, Kadlecek T, Zhang W, Samelson LE, Weiss A. LAT is required for TCR-mediated activation of PLCgamma1 and the Ras pathway. Immunity 1998 9 : 617 626.
46. Singer AL, et al. Roles of the proline-rich domain in SLP-76 subcellular localization and T cell function. J Biol Chem 2004 279 : 15481 15490.
47. Law CL, Chandran KA, Sidorenko SP, Clark EA. Phospholipase C-gamma1 interacts with conserved phosphotyrosyl residues in the linker region of Syk and is a substrate for Syk. Mol Cell Biol 1996 16 : 1305 1315.
48. Hoth M, Penner R. Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 1992 355 : 353 356.
49. Ebinu JO, et al. RasGRP links T-cell receptor signaling to Ras. Blood 2000 95 : 3199 3203.
50. Liu Y, Zhu M, Nishida K, Hirano T, Zhang W. An essential role for RasGRP1 in mast cell function and IgE-mediated allergic response. J Exp Med 2007 204 : 93 103.
51. Wilde JI, Watson SP. Regulation of phospholipase C gamma isoforms in haematopoietic cells: why one, not the other? Cell Signal 2001 13 : 691 701.
52. Wen R, Jou ST, Chen Y, Hoffmeyer A, Wang D. Phospholipase C gamma 2 is essential for specific functions of Fc epsilon R and Fc gamma R. J Immunol 2002 169 : 6743 6752.
53. Ji QS, et al. Essential role of the tyrosine kinase substrate phospholipase C-gamma1 in mammalian growth and development. Proc Natl Acad Sci USA 1997 94 : 2999 3003.
54. Boerth NJ, Sadler JJ, Bauer DE, Clements JL, Gheith SM, Koretzky GA. Recruitment of SLP-76 to the membrane and glycolipid-enriched membrane microdomains replaces the requirement for linker for activation of T cells in T cell receptor signaling. J Exp Med 2000 192 : 1047 1058.
55. Bezman NA, Baker RG, Lenox LE, Jordan MS, Koretzky GA. Cutting edge: rescue of pre-TCR but not mature TCR signaling in mice expressing membrane-targeted SLP-76. J Immunol 2009 182 : 5183 5187.
56. Liou J, et al. HPK1 is activated by lymphocyte antigen receptors and negatively regulates AP-1. Immunity 2000 12 : 399 408.
57. Wu J, Motto DG, Koretzky GA, Weiss A. Vav and SLP-76 interact and functionally cooperate in IL-2 gene activation. Immunity 1996 4 : 593 602.
58. Wunderlich L, Farago A, Downward J, Buday L. Association of Nck with tyrosine-phosphorylated SLP-76 in activated T lymphocytes. Eur J Immunol 1999 29 : 1068 1075.
59. Bubeck Wardenburg J, et al. Regulation of PAK activation and the T cell cytoskeleton by the linker protein SLP-76. Immunity 1998 9 : 607 616.
60. Bunnell SC, Diehn M, Yaffe MB, Findell PR, Cantley LC, Berg LJ. Biochemical interactions integrating Itk with the T cell receptor-initiated signaling cascade. J Biol Chem 2000 275 : 2219 2230.
61. Jordan MS, et al. Complementation in trans of altered thymocyte development in mice expressing mutant forms of the adaptor molecule SLP76. Immunity 2008 28 : 359 369.
62. Hata D, et al. Involvement of Bruton's tyrosine kinase in Fcepsilon RI-dependent mast cell degranulation and cytokine production. J Exp Med 1998 187 : 1235 1247.
63. Hata D, Kitaura J, Hartman SE, Kawakami Y, Yokota T, Kawakami T. Bruton's tyrosine kinase-mediated interleukin-2 gene activation in mast cells. Dependence on the c-Jun N-terminal kinase activation pathway. J Biol Chem 1998 273 : 10979 10987.
64. Manetz TS, Gonzalez-Espinosa C, Arudchandran R, Xirasagar S, Tybulewicz V, Rivera J. Vav1 regulates phospholipase cgamma activation and calcium responses in mast cells. Mol Cell Biol 2001 21 : 3763 3774.
65. Silverman MA, Shoag J, Wu J, Koretzky GA. Disruption of SLP-76 interaction with Gads inhibits dynamic clustering of SLP-76 and FcepsilonRI signaling in mast cells. Mol Cell Biol 2006 26 : 1826 1838.
66. Wilson BS, Pfeiffer JR, Surviladze Z, Gaudet EA, Oliver JM. High resolution mapping of mast cell membranes reveals primary and secondary domains of Fc(epsilon)RI and LAT. J Cell Biol 2001 154 : 645 658.
67. Houtman JC, et al. Oligomerization of signaling complexes by the multipoint binding of GRB2 to both LAT and SOS1. Nat Struct Mol Biol 2006 13 : 798 805.
68. Nag A, Monine MI, Faeder JR, Goldstein B. Aggregation of membrane proteins by cytosolic cross-linkers: theory and simulation of the LAT-Grb2-SOS1 system. Biophys J 2009 96 : 2604 2623.
69. Qiao F, Bowie JU. The many faces of SAM. Sci STKE 2005 2005 : re7.
70. Shen S, et al. The importance of Src homology 2 domain-containing leukocyte phosphoprotein of 76 kilodaltons sterile-alpha motif domain in thymic selection and T-cell activation. Blood 2009 114 : 74 84.
71. Thanos CD, Goodwill KE, Bowie JU. Oligomeric structure of the human EphB2 receptor SAM domain. Science 1999 283 : 833 836.
72. Bezman NA, et al. Requirements of SLP76 tyrosines in ITAM and integrin receptor signaling and in platelet function in vivo. J Exp Med 2008 205 : 1775 1788.
73. Yamasaki S, et al. Selective impairment of FcepsilonRI-mediated allergic reaction in Gads-deficient mice. Int Immunol 2008 20 : 1289 1297.
74. Zhu M, Liu Y, Koonpaew S, Granillo O, Zhang W. Positive and negative regulation of FcepsilonRI-mediated signaling by the adaptor protein LAB/NTAL. J Exp Med 2004 200 : 991 1000.
75. Brdicka T, et al. Non-T cell activation linker (NTAL): a transmembrane adaptor protein involved in immunoreceptor signaling. J Exp Med 2002 196 : 1617 1626.
76. Iwaki S, Jensen BM, Gilfillan AM. Ntal/Lab/Lat2 Int J Biochem Cell Biol 2007 39 : 868 873.
77. Volna P, et al. Negative regulation of mast cell signaling and function by the adaptor LAB/NTAL. J Exp Med 2004 200 : 1001 1013.
78. Janssen E, Zhu M, Zhang W, Koonpaew S. LAB: a new membrane-associated adaptor molecule in B cell activation. Nat Immunol 2003 4 : 117 123.
79. Janssen E, Zhu M, Craven B, Zhang W. Linker for activation of B cells: a functional equivalent of a mutant linker for activation of T cells deficient in phospholipase C-gamma1 binding. J Immunol 2004 172 : 6810 6819.
80. Iwaki S, et al. Kit- and Fc epsilonRI-induced differential phosphorylation of the transmembrane adaptor molecule NTAL/LAB/LAT2 allows flexibility in its scaffolding function in mast cells. Cell Signal 2008 20 : 195 205.
81. Parravicini V, et al. Fyn kinase initiates complementary signals required for IgE-dependent mast cell degranulation. Nat Immunol 2002 3 : 741 748.
82. Zhu M, Rhee I, Liu Y, Zhang W. Negative regulation of Fc epsilonRI-mediated signaling and mast cell function by the adaptor protein LAX. J Biol Chem 2006 281 : 18408 18413.
83. Zhu M, et al. Negative regulation of lymphocyte activation by the adaptor protein LAX. J Immunol 2005 174 : 5612 5619.
84. 2+ mobilization, but not degranulation, in lyn-deficient bone marrow-derived mast cells. J Immunol 1997 158 : 2350 2355.
85. Hibbs ML, et al. Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell 1995 83 : 301 311.
86. Odom S, et al. Negative regulation of immunoglobulin E-dependent allergic responses by Lyn kinase. J Exp Med 2004 199 : 1491 1502.
87. Hernandez-Hansen V, et al. Dysregulated FcepsilonRI signaling and altered Fyn and SHIP activities in Lyn-deficient mast cells. J Immunol 2004 173 : 100 112.
88. Kimura T, Sakamoto H, Appella E, Siraganian RP. The negative signaling molecule SH2 domain-containing inositol-polyphosphate 5-phosphatase (SHIP) binds to the tyrosine-phosphorylated beta subunit of the high affinity IgE receptor. J Biol Chem 1997 272 : 13991 13996.
89. Xiao W, et al. Positive and negative regulation of mast cell activation by Lyn via the FcepsilonRI. J Immunol 2005 175 : 6885 6892.
90. Yamashita Y, et al. Cutting edge: genetic variation influences Fc epsilonRI-induced mast cell activation and allergic responses. J Immunol 2007 179 : 740 743.
91. Roget K, Malissen M, Malbec O, Malissen B, Daeron M. Non-T cell activation linker promotes mast cell survival by dampening the recruitment of SHIP1 by linker for activation of T cells. J Immunol 2008 180 : 3689 3698.
92. 2+ mobilization in antigen-stimulated mast cells. J Leukoc Biol 1999 65 : 321 329.
93. Barker SA, et al. Wortmannin blocks lipid and protein kinase activities associated with PI 3-kinase and inhibits a subset of responses induced by Fc epsilon R1 cross-linking. Mol Biol Cell 1995 6 : 1145 1158.
94. Ishizuka T, et al. Mitogen-activated protein kinase activation through Fc epsilon receptor I and stem cell factor receptor is differentially regulated by phosphatidylinositol 3-kinase and calcineurin in mouse bone marrow-derived mast cells. J Immunol 1999 162 : 2087 2094.
95. Pelletier C, et al. Specific signaling pathways in the regulation of TNF-alpha mRNA synthesis and TNF-alpha secretion in RBL-2H3 mast cells stimulated through the high affinity IgE receptor. Inflamm Res 1998 47 : 493 500.
96. Kitaura J, Asai K, Maeda-Yamamoto M, Kawakami Y, Kikkawa U, Kawakami T. Akt-dependent cytokine production in mast cells. J Exp Med 2000 192 : 729 740.
97. Gu H, et al. New role for Shc in activation of the phosphatidylinositol 3-kinase/Akt pathway. Mol Cell Biol 2000 20 : 7109 7120.
98. Gu H, et al. Essential role for Gab2 in the allergic response. Nature 2001 412 : 186 190.
99. Yu M, Lowell CA, Neel BG, Gu H. Scaffolding adapter Grb2-associated binder 2 requires Syk to transmit signals from FcepsilonRI. J Immunol 2006 176 : 2421 2429.
100. Simon M, Vanes L, Geahlen RL, Tybulewicz VL. Distinct roles for the linker region tyrosines of Syk in FcepsilonRI signaling in primary mast cells. J Biol Chem 2005 280 : 4510 4517.
101. Turner H, Kinet JP. Signalling through the high-affinity IgE receptor Fc epsilonRI. Nature 1999 402 : B24 B30.
102. Hirasawa N, Santini F, Beaven M. Activation of the mitogen-activated protein kinase/cytosolic phospholipase A2 pathway in a rat mast cell line. Indications of different pathways for release of arachidonic acid and secretory granules. J Immunol 1995 154 : 5391 5402.
103. Borsch-Haubold AG, et al. Phosphorylation of cytosolic phospholipase A2 in platelets is mediated by multiple stress-activated protein kinase pathways. Eur J Biochem 1999 265 : 195 203.
104. Boudreau RT, Hoskin DW, Lin TJ. Phosphatase inhibition potentiates IL-6 production by mast cells in response to FcepsilonRI-mediated activation: involvement of p38 MAPK. J Leukoc Biol 2004 76 : 1075 1081.
105. Ishizuka T, et al. Mast cell tumor necrosis factor alpha production is regulated by MEK kinases. Proc Natl Acad Sci USA 1997 94 : 6358 6363.
106. Gomez G, et al. Impaired FcepsilonRI-dependent gene expression and defective eicosanoid and cytokine production as a consequence of Fyn deficiency in mast cells. J Immunol 2005 175 : 7602 7610.
107. Yamasaki S, et al. LAT and NTAL mediate immunoglobulin E-induced sustained extracellular signal-regulated kinase activation critical for mast cell survival. Mol Cell Biol 2007 27 : 4406 4415.
108. Yamasaki S, et al. Zinc is a novel intracellular second messenger. J Cell Biol 2007 177 : 637 645.
109. Nishida K, et al. Zinc transporter Znt5/Slc30a5 is required for the mast cell-mediated delayed-type allergic reaction but not the immediate-type reaction. J Exp Med 2009 206 : 1351 1364.
110. Kawakami Y, et al. A Ras activation pathway dependent on Syk phosphorylation of protein kinase C. Proc Natl Acad Sci USA 2003 100 : 9470 9575.
111. Downward J, Graves JD, Warne PH, Rayter S, Cantrell DA. Stimulation of p21ras upon T-cell activation. Nature 1990 346 : 719 723.
112. Siegel JN, Klausner RD, Rapp UR, Samelson LE. T cell antigen receptor engagement stimulates c-raf phosphorylation and induces c-raf-associated kinase activity via a protein kinase C-dependent pathway. J Biol Chem 1990 265 : 18472 18480.
113. Kuehn HS, Gilfillan AM. G protein-coupled receptors and the modification of FcepsilonRI-mediated mast cell activation. Immunol Lett 2007 113 : 59 69.
114. Gilfillan AM, Rivera J. The tyrosine kinase network regulating mast cell activation. Immunol Rev 2009 228 : 149 169.
115. Okayama Y, Kawakami T. Development, migration, and survival of mast cells. Immunol Res 2006 34 : 97 115.
116. Hundley TR, Gilfillan AM, Tkaczyk C, Andrade MV, Metcalfe DD, Beaven MA. Kit and FcepsilonRI mediate unique and convergent signals for release of inflammatory mediators from human mast cells. Blood 2004 104 : 2410 2417.
117. Miyazaki D, Nakamura T, Toda M, Cheung-Chau KW, Richardson RM, Ono SJ. Macrophage inflammatory protein-1alpha as a costimulatory signal for mast cell-mediated immediate hypersensitivity reactions. J Clin Invest 2005 115 : 434 442.
118. Laffargue M, et al. Phosphoinositide 3-kinase gamma is an essential amplifier of mast cell function. Immunity 2002 16 : 441 451.
119. Nigo YI, et al. Regulation of allergic airway inflammation through Toll-like receptor 4-mediated modification of mast cell function. Proc Natl Acad Sci USA 2006 103 : 2286 2291.
120. Supajatura V, Ushio H, Nakao A, Okumura K, Ra C, Ogawa H. Protective roles of mast cells against enterobacterial infection are mediated by Toll-like receptor 4. J Immunol 2001 167 : 2250 2256.
121. Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol 2004 5 : 987 995.
122. Slack JL, et al. Identification of two major sites in the type I interleukin-1 receptor cytoplasmic region responsible for coupling to pro-inflammatory signaling pathways. J Biol Chem 2000 275 : 4670 4678.
123. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004 4 : 499 511.
124. Kulka M, Alexopoulou L, Flavell RA, Metcalfe DD. Activation of mast cells by double-stranded RNA: evidence for activation through Toll-like receptor 3. J Allergy Clin Immunol 2004 114 : 174 182.
125. Matsushima H, Yamada N, Matsue H, Shimada S. TLR3-, TLR7-, and TLR9-mediated production of proinflammatory cytokines and chemokines from murine connective tissue type skin-derived mast cells but not from bone marrow-derived mast cells. J Immunol 2004 173 : 531 541.
126. Mrabet-Dahbi S, Metz M, Dudeck A, Zuberbier T, Maurer M. Murine mast cells secrete a unique profile of cytokines and prostaglandins in response to distinct TLR2 ligands. Exp Dermatol 2009 18 : 437 444.
127. 2+ mobilization and G protein usage on regulation of Toll-like receptor function in human and murine mast cells. Immunology 2006 119 : 412 420.
128. Qiao H, Andrade MV, Lisboa FA, Morgan K, Beaven MA. FcepsilonR1 and toll-like receptors mediate synergistic signals to markedly augment production of inflammatory cytokines in murine mast cells. Blood 2006 107 : 610 618.
129. McCurdy JD, Lin TJ, Marshall JS. Toll-like receptor 4-mediated activation of murine mast cells. J Leukoc Biol 2001 70 : 977 984.
130. Ali K, et al. Essential role for the p110delta phosphoinositide 3-kinase in the allergic response. Nature 2004 431 : 1007 1011.
131. Hazeki K, Nigorikawa K, Hazeki O. Role of phosphoinositide 3-kinase in innate immunity. Biol Pharm Bull 2007 30 : 1617 1623.
132. Arbibe L, et al. Toll-like receptor 2-mediated NF-kappa B activation requires a Rac1-dependent pathway. Nat Immunol 2000 1 : 533 540.
133. + T cells and enables CpG oligodeoxynucleotide- mediated costimulation. Immunity 2006 25 : 783 793.
134. Li X, Tupper JC, Bannerman DD, Winn RK, Rhodes CJ, Harlan JM. Phosphoinositide 3 kinase mediates Toll-like receptor 4-induced activation of NF-kappa B in endothelial cells. Infect Immun 2003 71 : 4414 4420.
135. Rhee SH, Kim H, Moyer MP, Pothoulakis C. Role of MyD88 in phosphatidylinositol 3-kinase activation by flagellin/toll-like receptor 5 engagement in colonic epithelial cells. J Biol Chem 2006 281 : 18560 18568.