The Src family kinase Hck regulates mast cell activation by suppressing an inhibitory Src family kinase Lyn

Blood

Volumn 110, Issue 7, 2007, Pages 2511-2519

  Hong, Hong ^a   Kitaura, Jiro ^a   Xiao, Wenbin ^a   Horejsi, Vaclav ^b   Ra, Chisei ^c   Lowell, Clifford A ^d   Kawakami, Yuko ^a   Kawakami, Toshiaki ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^c NIHON UNIVERSITY   (Japan)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; HEMATOPOIETIC CELL KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN; PROTEIN GAB2; PROTEIN KINASE B; PROTEIN KINASE BTK; PROTEIN KINASE LYN; PROTEIN KINASE SYK; PROTEIN TYROSINE KINASE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; IMMUNOREGULATION; IMMUNOSTIMULATION; MAST CELL; MAST CELL DEGRANULATION; MICROTUBULE ASSEMBLY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL PROLIFERATION; CYTOKINES; ENZYME ACTIVATION; GENES, TUMOR SUPPRESSOR; GRB2 ADAPTOR PROTEIN; MAST CELLS; MICE; MICE, KNOCKOUT; MICROTUBULES; NUCLEAR PROTEINS; PHENOTYPE; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-HCK; RECEPTORS, IGE; SRC-FAMILY KINASES; UP-REGULATION;

EID: 34948882787     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2007-01-066092     Document Type: Article

References (64)

1. Kinet JP. The high-affinity IgE receptor (Fc epsilon RI): from physiology to pathology. Annu Rev Immunol. 1999;17:931-972.
2. Turner H, Kinet JP. Signalling through the high-affinity IgE receptor Fc epsilonRI. Nature. 1999;402:B24-30.
3. Eiseman E, Bolen JB. Engagement of the high-affinity IgE receptor activates src protein-related tyrosine kinases. Nature. 1992;355:78-80.
4. 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.
5. Kawakami T, Galli SJ. Regulation of mast-cell and basophil function and survival by IgE. Nat Rev Immunol. 2002;2:773-786.
6. Gilfillan AM, Tkaczyk C. Integrated signalling pathways for mast-cell activation. Nat Rev Immunol. 2006;6:218-230.
7. Rivera J, Gilfillan AM. Molecular regulation of mast cell activation. J Allergy Clin Immunol. 2006;117:1214-1226.
8. Parravicini V, Gadina M, Kovarova M, et al. Fyn kinase initiates complementary signals required for IgE-dependent mast cell degranulation. Nat Immunol. 2002;3:741-748.
9. Nishida K, Yamasaki S, Ito Y, et al. Fc{epsilon}RI-mediated mast cell degranulation requires calcium-independent microtubule-dependent translocation of granules to the plasma membrane. J Cell Biol. 2005;170:115-126.
10. Kawakami Y, Kitaura J, Satterthwaite AB, et al. Redundant and opposing functions of two tyrosine kinases, Btk and Lyn, in mast cell activation. J Immunol. 2000;165:1210-1219.
11. Hernandez-Hansen V, Smith AJ, Surviladze Z, et al. Dysregulated FcepsilonRI signaling and altered Fyn and SHIP activities in Lyn-deficient mast cells. J Immunol. 2004;173:100-112.
12. Odom S, Gomez G, Kovarova M, et al. Negative regulation of immunoglobulin E-dependent allergic responses by Lyn kinase. J Exp Med. 2004;199:1491-1502.
13. Xu Y, Harder KW, Huntington ND, Hibbs ML, Tarlinton DM. Lyn tyrosine kinase: accentuating the positive and the negative. Immunity. 2005;22:9-18.
14. Tolar P, Draberova L, Tolarova H, Draber P. Positive and negative regulation of Fc epsilon receptor I-mediated signaling events by Lyn kinase Cterminal tyrosine phosphorylation. Eur J Immunol. 2004;34:1136-1145.
15. 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.
16. Dombrowicz D, Lin S, Flamand V, Brini AT, Koller BH, Kinet JP. Allergy-associated FcRbeta is a molecular amplifier of IgE- and IgG-mediated in vivo responses. Immunity. 1998;8:517-529.
17. Hiraoka S, Furumoto Y, Koseki H, et al. Fc receptor beta subunit is required for full activation of mast cells through Fc receptor engagement. Int Immunol. 1999;11:199-207.
18. Donnadieu E, Jouvin MH, Kinet JP. A second amplifier function for the allergy-associated Fc(epsilon) RI-beta subunit. Immunity. 2000;12:515-523.
19. On M, Billingsley JM, Jouvin MH, Kinet JP. Molecular dissection of the FcRbeta signaling amplifier. J Biol Chem. 2004;279:45782-45790.
20. 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.
21. Costello PS, Turner M, Walters AE, 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.
22. 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.
23. Xiao W, Nishimoto H, Hong H, et al. Positive and negative regulation of mast cell activation by Lyn via the FcepsilonRI. J Immunol. 2005;175:6885-6892.
24. Gimborn K, Lessmann E, Kuppig S, Krystal G, Huber M. SHIP down-regulates FcepsilonR1-induced degranulation at supraoptimal IgE or antigen levels. J Immunol. 2005;174:507-516.
25. Leitges M, Gimborn K, Elis W, et al. Protein kinase C-delta is a negative regulator of antigen-induced mast cell degranulation. Mol Cell Biol. 2002;22:3970-3980.
26. Magro AM, Alexander A. Histamine release: in vitro studies of the inhibitory region of the dose-response curve. J Immunol. 1974;112:1762-1765.
27. Robertson D, Holowka D, Baird B. Cross-linking of immunoglobulin E-receptor complexes induces their interaction with the cytoskeleton of rat basophilic leukemia cells. J Immunol. 1986;136:4565-4572.
28. Ortega E, Schweitzer-Stenner R, Pecht I. Possible orientational constraints determine secretory signals induced by aggregation of IgE receptors on mast cells. Embo J. 1988;7:4101-4109.
29. Chan VW, Meng F, Soriano P, DeFranco AL, Lowell CA. Characterization of the B lymphocyte populations in Lyn-deficient mice and the role of Lyn in signal initiation and down-regulation. Immunity. 1997;7:69-81.
30. Lowell CA, Soriano P, Varmus HE. Functional overlap in the src gene family: inactivation of hck and fgr impairs natural immunity. Genes Dev. 1994;8:387-398.
31. Yu CC, Yen TS, Lowell CA, DeFranco AL. Lupus-like kidney disease in mice deficient in the Src family tyrosine kinases Lyn and Fyn. Curr Biol. 2001;11:34-38.
32. Kitaura J, Song J, Tsai M, 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.
33. Nishimoto H, Lee SW, Hong H, et al. Costimulation of mast cells by 4-1BB, a member of the tumor necrosis factor receptor superfamily, with the high-affinity IgE receptor. Blood. 2005;106:4241-4248.
34. Kawakami Y, Kitaura J, Yao L, et al. A Ras activation pathway dependent on Syk phosphorylation of protein kinase C. Proc Natl Acad Sci USA. 2003;100:9470-9475.
35. Ozawa K, Szallasi Z, Kazanietz MG, et al. Ca(2+)-dependent and Ca(2+)-independent isozymes of protein kinase C mediate exocytosis in antigen-stimulated rat basophilic RBL-2H3 cells. Reconstitution of secretory responses with Ca2+ and purified isozymes in washed permeabilized cells. J Biol Chem. 1993;268:1749-1756.
36. Saitoh S, Arudchandran R, Manetz TS, et al. LAT is essential for Fc(epsilon)RI-mediated mast cell activation. Immunity. 2000;12:525-535.
37. Brdicka T, Pavlistova D, Leo A, et al. Phosphoprotein associated with glycosphingolipid-enriched microdomains (PAG), a novel ubiquitously expressed transmembrane adaptor protein, binds the protein tyrosine kinase csk and is involved in regulation of T cell activation. J Exp Med. 2000;191:1591-1604.
38. Kawabuchi M, Satomi Y, Takao T, et al. Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature. 2000;404:999-1003.
39. Volná P, Lebduska P, Draberova L, et al. Negative regulation of mast cell signaling and function by the adaptor LAB/NTAL. J Exp Med. 2004;200:1001-1013.
40. Nada S, Okada M, MacAuley A, Cooper JA, Nakagawa H. Cloning of a complementary DNA for a protein-tyrosine kinase that specifically phosphorylates a negative regulatory site of p60c-src. Nature. 1991;351:69-72.
41. Huber M, Helgason CD, Damen JE, Liu L, Humphries RK, Krystal G. The src homology 2-containing inositol phosphatase (SHIP) is the gatekeeper of mast cell degranulation. Proc Natl Acad Sci USA. 1998;95:11330-11335.
42. Jones N, Dumont DJ. Recruitment of Dok-R to the EGF receptor through its PTB domain is required for attenuation of Erk MAP kinase activation. Curr Biol. 1999;9:1057-1060.
43. Nelms K, Snow AL, Hu-Li J, Paul WE. FRIP, a hematopoietic cell-specific rasGAP-interacting protein phosphorylated in response to cytokine stimulation. Immunity. 1998;9:13-24.
44. Hata D, Kawakami Y, Inagaki N, et al. Involvement of Bruton's tyrosine kinase in FcepsilonRI-dependent mast cell degranulation and cytokine production. J Exp Med. 1998;187:1235-1247.
45. 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.
46. Park H, Wahl MI, Afar DE, et al. Regulation of Btk function by a major autophosphorylation site within the SH3 domain. Immunity. 1996;4:515-525.
47. Kawakami Y, Kitaura J, Hartman SE, Lowell CA, Siraganian RP, Kawakami T. Regulation of protein kinase CbetaI by two protein-tyrosine kinases, Btk and Syk. Proc Natl Acad Sci USA. 2000;97:7423-7428.
48. Song JS, Haleem-Smith H, Arudchandran R, et al. Tyrosine phosphorylation of Vav stimulates IL-6 production in mast cells by a Rac/c-Jun N-terminal kinase-dependent pathway. J Immunol. 1999;163:802-810.
49. 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.
50. Chayama K, Papst PJ, Garrington TP, et al. Role of MEKK2-MEK5 in the regulation of TNF-alpha gene expression and MEKK2-MKK7 in the activation of c-Jun N-terminal kinase in mast cells. Proc Natl Acad Sci USA. 2001;98:4599-4604.
51. Kalesnikoff J, Baur N, Leitges M, et al. SHIP negatively regulates IgE + antigen-induced IL-6 production in mast cells by inhibiting NF-kappa B activity. J Immunol. 2002;168:4737-4746.
52. Zandi E, Rothwarf DM, Delhase M, Hayakawa M, Karin M. The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation. Cell. 1997;91:243-252.
53. Gilmore TD. The Rel/NF-kappaB signal transduction pathway: introduction. Oncogene. 1999;18:6842-6844.
54. Hernandez-Hansen V, Mackay GA, Lowell CA, Wilson BS, Oliver JM. The Src kinase Lyn is a negative regulator of mast cell proliferation. J Leukoc Biol. 2004;75:143-151.
55. Kmiecik TE, Shalloway D. Activation and suppression of pp60c-src transforming ability by mutation of its primary sites of tyrosine phosphorylation. Cell. 1987;49:65-73.
56. Piwnica-Worms H, Saunders KB, Roberts TM, Smith AE, Cheng SH. Tyrosine phosphorylation regulates the biochemical and biological properties of pp60c-src. Cell. 1987;49:75-82.
57. Ernst M, Inglese M, Scholz GM, et al. Constitutive activation of the SRC family kinase Hck results in spontaneous pulmonary inflammation and an enhanced innate immune response. J Exp Med. 2002;196:589-604.
58. Yu M, Lowell CA, Neel BG, Gu H. Scaffolding adapter Grb2-associated binder 2 requires Syk to transmit signals from FcεRI. J Immunol. 2006;176:2421-2429.
59. Field KA, Holowka D, Baird B. Fc epsilon RI-mediated recruitment of p53/56lyn to detergent-resistant membrane domains accompanies cellular signaling. Proc Natl Acad Sci USA. 1995;92:9201-9205.
60. Field KA, Holowka D, Baird B. Compartmentalized activation of the high affinity immunoglobulin E receptor within membrane domains. J Biol Chem. 1997;272:4276-4280.
61. Field KA, Holowka D, Baird B. Structural aspects of the association of FcepsilonRI with detergent-resistant membranes. J Biol Chem. 1999;274:1753-1758.
62. Wilson BS, Pfeiffer JR, Oliver JM. Observing FcepsilonRI signaling from the inside of the mast cell membrane. J Cell Biol. 2000;149:1131-1142.
63. Wilson BS, Pfeiffer JR, Surviladze Z, Gaudet EA, Oliver JM. High resolution mapping of mast cell membranes reveals primary and secondary domains of FcεRI and LAT. J Cell Biol. 2001;154:645-658.
64. Gomez G, Gonzalez-Espinosa C, Odom S, 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.