Involvement of Bruton's tyrosine kinase in FcεRI-dependent mast cell degranulation and cytokine production

Journal of Experimental Medicine

Volumn 187, Issue 8, 1998, Pages 1235-1247

  Hata, Daisuke ^a   Kawakami, Yuko ^a   Inagaki, Naoki ^b   Lantz, Chris S ^c   Kitamura, Toshio ^d   Khan, Wasif N ^e   Maeda Yamamoto, Mari ^a   Miura, Toru ^a   Han, Wei ^a   Hartman, Stephen E ^a   Yao, Libo ^a   Nagai, Hiroichi ^b   Goldfeld, Anne E ^f   Alt, Frederick W ^e   Galli, Stephen J ^c   Witte, Owen N ^g   Kawakami, Toshiaki ^a  

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

^b GIFU PHARMACEUTICAL UNIVERSITY   (Japan)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF TOKYO   (Japan)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f DANA FARBER CANCER INSTITUTE   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; CYTOKINE; FC RECEPTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN E ANTIBODY; INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 6; MONOCLONAL ANTIBODY; MUTANT PROTEIN; RECOMBINANT STEM CELL FACTOR; RNA; TUMOR NECROSIS FACTOR ALPHA; TYROSINE KINASE RECEPTOR;

ALLERGY; ANIMAL CELL; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; GENE TRANSFER; HISTAMINE RELEASE; MAST CELL DEGRANULATION; MOUSE; NONHUMAN; PASSIVE SKIN ANAPHYLAXIS; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; RETROVIRUS; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANIMALS; BONE MARROW CELLS; CELL DEGRANULATION; CYTOKINES; GENE EXPRESSION REGULATION; HISTAMINE RELEASE; MAST CELLS; MICE; MICE, MUTANT STRAINS; MODELS, BIOLOGICAL; PASSIVE CUTANEOUS ANAPHYLAXIS; PROTEIN-TYROSINE KINASES; RECEPTORS, IGE; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 0032550335     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.187.8.1235     Document Type: Article

References (90)

1. Galli, S.J. 1993. New concepts about the mast cell. N. Engl. J. Med. 328:257-265.
2. Beaven, M.A., and H. Metzger. 1993. Signal transduction by Fc receptors: the Fc∈RI case. Immunol. Today. 14:222-226.
3. Ravetch, J.V., and J.-P. Kinet. 1991. Fc receptors. Annu. Rev. Immunol. 9:457-492.
4. Reth, M. 1989. Antigen receptor tail clue. Nature. 338:383-384.
5. Cambier, J.C. 1995. New nomenclature for the Reth Motif (or ARH1/TAM/ARAM/YXXL). Immunol. Today. 16:110.
6. Benhamou, M., J.S. Gutkind, K.C. Robbins, and R.P. Siraganian. 1990. Tyrosine phosphorylation coupled to IgE receptor-mediated signal transduction and histamine release. Proc. Natl. Acad. Sci. USA. 87:5327-5330.
7. Kawakami, T., N. Inagaki, M. Takei, H. Fukamachi, K.M. Coggeshall, K. Ishizaka, and T. Ishizaka. 1992. Tyrosine phosphorylation is required for mast cell activation by Fc∈RI cross-linking. J. Immunol. 148:3513-3519.
8. Stephen, V., M. Benhamou, J.S. Gutkind, K.C. Robbins, and R.P. Siraganian. 1992. Fc∈RI-induced protein tyrosine phosphorylation of pp72 in rat basophilic leukemia cells (RBL-2H3). Evidence for a novel signal transduction pathway unrelated to G protein activation and phosphatidylinositol hydrolysis. J. Biol. Chem. 267:5434-5441.
9. Hibbs, M.L., D.M. Tarlinton, J. Armes, D. Grail, G. Hodgson, R. Maglitto, S.A. Stacker, and A.R. Dunn. 1995. Multiple defects in the immune system of Lyn-defective mice, culminating in autoimmune disease. Cell. 83:301-311.
10. Rivera, V., and J.S. Brugge. 1995. Clustering of Syk is sufficient to induce tyrosine phosphorylation and release of allergic mediators from rat basophilic leukemia cells. Mol. Cell. Biol. 15:1582-1590.
11. Zhang, J., E.H. Berenstein, R.L. Evans, and R.P. Siraganian. 1996. 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. 184:71-79.
12. Jouvin, M.-H., M. Adamczewski, R. Numerof, O. Letourneur, A. Valle, and J.-P. Kinet. 1994. Differential control of the tyrosine kinases Lyn and Syk by the two signaling chains of the high affinity immunoglobulin E receptor. J. Biol. Chem. 269:5918-5925.
13. Kihara, H., and R.P. Siraganian. 1994. Src homlogy 2 domains of Syk and Lyn bind to tyrosine-phosphorylated subunits of the high affinity IgE receptor. J. Biol. Chem. 269: 22427-22432.
14. Rowley, R.B., A.L. Burkhardt, H.-G. Chao, G.R. Matsueda, and J.B. Bolen. 1995. Syk protein-tyrosine kinase is regulated by tyrosine-phosphorylated Igα/Igβ immunoreceptor tyrosine activation motif binding and autophosphorylation. J. Biol. Chem. 270:11590-11594.
15. Shiue, L., M.J. Zoller, and J.S. Brugge. 1995. Syk is activated by phosphotyrosine-containing peptides representing the tyrosine-based activation motifs of the high affinity receptor for IgE. J. Biol. Chem. 270:10498-10502.
16. Yamada, N., Y. Kawakami, H. Kimura, H. Fukamachi, G. Baier, A. Altman, T. Kato, Y. Inagaki, and T. Kawakami. 1993. Structure and expression of novel protein tyrosine kinases, Emb and Emt, in hematopoietic cells. Biochem. Biophys. Res. Commun. 192:231-240.
17. Tang, B., H. Mano, H., T. Yi, and J.N. Ihle. 1994. Tec kinase associates with c-kit and is tyrosine phosphorylated and activated following stem cell factor binding. Mol. Cell. Biol. 14:8432-8437.
18. Kawakami, Y., L. Yao, S. Tsukada, O.N. Witte, and T. Kawakami. 1994. Tyrosine phosphorylation and activation of Bruton tyrosine kinase upon Fc∈RI cross-linking. Mol. Cell. Biol. 14:5108-5113.
19. Kawakami, Y., L. Yao, M. Tashiro, S. Gibson, G.B. Mills, and T. Kawakami. 1995. Activation and interaction with protein kinase C of a cytoplasmic tyrosine kinase, Itk/Tsk/ Emt, upon Fc∈RI cross-linking on mast cells. J. Immunol. 155:3556-3562.
20. Eiseman, E., and J.B. Bolen. 1992. Engagement of the high-affinity IgE receptor activates src protein-related tyrosine kinases. Nature. 355:78-80.
21. Hutchcroft, J.E., R.L. Geahlen, G.G. Deanin, and J.M. Oliver. 1992. Fc∈RI-mediated tyrosine phosphorylation and activation of the 72-kDa protein-tyrosine kinase, PTK72, in RBL-2H3 rat tumor mast cells. Proc. Natl. Acad. Sci. USA. 89:9107-9111.
22. syk in high affinity IgE receptor signaling. Identification as a component of pp72 and association with the receptor γ chain after receptor aggregation. J. Biol. Chem. 268:23318-23324.
23. Tsukada, S., D. Saffran, D.J. Rawlings, O. Parolini, R.C. Allen, I. Klisak, R.S. Sparkes, H. Kubagawa, T. Mohandas, S. Quan, et al. 1993. Deficient expression of a B cell cytoplasmic tyrosine kinase in human X-linked agammaglobulinemia. Cell. 72:279-290.
24. Vetrie, D., I. Vorechovsky, P. Sideras, J. Holland, A. Davies, F. Flinter, L. Hammarstrom, C. Kinnon, R. Levinsky, M. Bobrow, et al. 1993. The gene involved in X-linked agammaglobulinemia is a member of the src family of protein-tyrosine kinases. Nature. 361:226-233.
25. Thomas, J.D., P. Sideras, C.I.E. Smith, I. Vorechovsky, V. Chapman, and W.E. Paul. 1993. Colocalization of X-linked agammaglobulinemia and X-linked immunodeficiency genes. Science. 261:355-358.
26. Rawlings, D.J., D.C. Saffran, S. Tsukada, D.A. Largaespada, J.C. Grimaldi, L. Cohen, R.N. Mohr, J.F. Bazan, M. Howard, N.G. Copeland, et al. 1993. Mutation of unique region of Bruton's tyrosine kinase in immunodieficient XID mice. Science. 261:358-361.
27. Aoki, Y., K.J. Isselbacher, and S. Pillai. 1994. Bruton tyrosine kinase is tyrosine phosphorylated and activated in pre-B lymphocytes and receptor-ligated B cells. Proc. Natl. Acad. Sci. USA. 91:10606-10609.
28. Saouaf, S.J., S. Mahajan, R.B. Rowley, S.A. Kut, J. Fargnoll, A.L. Burkhardt, S. Tsukada, O.N. Witte, and J.B. Bolen. 1994. Temporal differences in the activation of three classes of non-transmembrane protein tyrosine kinases following B-cell antigen receptor surface engagement. Proc. Natl. Acad. Sci. USA. 91:9524-9528.
29. de Weers, M., G.S. Brouns, S. Hinshelwood, C. Kinnon, R.K.B. Schuurman, R.W. Hendriks, and J. Borst. 1994. B-cell antigen receptor stimulation activates the human Bruton's tyrosine kinase, which is deficient in X-linked agammaglobulinemia. J. Biol. Chem. 269:23857-23860.
30. Santos-Argumedo, L., F.E. Lund, A.W. Heath, N. Solvason, W.W. Mu, J.C. Grimaldi, R.M.E. Parkhouse, and M. Howard. 1995. CD38 unresponsiveness of xid B cells implicates Bruton's tyrosine kinase (btk) as a regulator of CD38 induced signal transduction. Int. Immunol. 7:163-170.
31. Yamashita, Y., K. Miyake, Y. Kikuchi, K. Takatsu, S. Noda, and A. Kosugi. 1995. A monoclonal antibody against a murine CD38 homologue delivers a signal to B cells for prolongation of survival and production against apoptosis in vitro: unresponsiveness of X-linked immunodeficient B cells. Immunology. 85:248-255.
32. Hasbold, J., and G.G.B. Klaus. 1994. B cells from CBA/N mice do not proliferate following ligation of CD40. Eur. J. Immunol. 24:152-157.
33. Sato, S., T. Katagiri, S. Takaki, Y. Kikuchi, Y. Hitoshi, S. Yonehara, S. Tsukada, D. Kitamura, T. Watanabe, O.N. Witte, and K. Takatsu. 1994. IL-5 receptor-mediated tyrosine phosphorylation of SH2/SH3-containing proteins and activation of Bruton's tyrosine and Janus 2 kinases. J. Exp. Med. 180:2101-2111.
34. Matsuda, T., M. Takahashi-Tezuka, T. Fukuda, Y. Okuyama, Y. Fujitani, S. Tsukada, H. Mano, H. Hirai, O.N. Witte, and T. Hirano. 1995. Association and activation of Btk and Tec tyrosine kinases by gp130, a signal transducer of the interleukin-6 family of cytokines. Blood. 85:627-633.
35. Go, N.F., B.E. Castle, R. Barrett, R. Kastelein, W. Dang, T.R. Mosmann, K.W. Moor, and M. Howard. 1990. Interleukin 10, a novel B cell stimulatory factor: unresponsiveness of X-chromosome-linked immunodeficiency B cells. J. Exp. Med. 172:1625-1631.
36. August, A., S. Gibson, Y. Kawakami, T. Kawakami, G.B. Mills, and B. Dupont. 1994. CD28 is associated with and induces the immediate tyrosine phosphorylation and activation of the Tec family kinase ITK/EMT in the human Jurkat leukemic T-cell line, Proc. Natl. Acad. Sci. USA. 91:9347-9351.
37. Gibson S., A. August, Y. Kawakami, T. Kawakami, B. Dupont, and G.B. Mills. 1996. The EMT/ITK/TSK (EMT) tyrosine kinase is activated during TCR signaling. J. Immunol. 156:2716-2722.
38. Liao, X.C., and D.R. Littman. 1995. Altered T cell receptor signaling and disrupted T cell development in mice lacking Itk. Immunity. 3:757-769.
39. Khan, W.N., F.W. Alt, R.M. Gerstein, B.A. Malynn, I. Larsson, G. Rathbun, L. Davidson, S. Mueller, A.B. Kantor, L.A. Herzenberg, et al. 1995. Defective B cell development and function in Btk-deficient mice. Immunity. 3:283-299.
40. Kerner, J.D., M.W. Appleby, R.N. Mohr, S. Chien, D.J. Rawlings, C.R. Maliszewski, O.N. Witte, and R.M. Perlmutter. 1995. Impaired expansion of mouse B cell progenitors lacking Btk. Immunity. 3:301-312.
41. Inagaki, N., S. Goto, H. Nagai, and A. Koda. 1986. Homologous passive cutaneous anaphylaxis in various strains of mice. Int. Arch. Allergy Appl. Immunol. 81:58-62.
42. Nagai, H., T. Sakurai, N. Inagaki, and H. Mori. 1995. An immunopharmacological study of the biphasic allergic skin reaction. Biol. Pharm. Bull. 18:239-245.
43. Yao, L., Y. Kawakami, and T. Kawakami. 1994. The pleckstrin homology domain of Btk tyrosine kinase interacts with protein kinase C. Proc. Natl. Acad. Sci. USA. 91:9175-9179.
44. Gibson, S., B. Leung, J.A. Squire, M. Hill, N. Arima, P. Gross, D. Hogg, and G.B. Mills. 1993. Identification, cloning, and characterization of a novel human T-cell-specific tyrosine kinase located at the hematopoietin complex on chromosome 5q. Blood. 83:1561-1572.
45. Horton, R.M., H.D. Hunt, S.N. Ho, J.K. Pullen, and L.R. Pease. 1989. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene. 77:61-68.
46. Omshi, M., S. Kinoshita, Y. Morikawa, A. Shibuya, J. Phillips, L.L. Lanier, D.M. Gorman, G.P. Nolan, A. Miyajima, and T. Kitamura. 1996. Applications of retrovirus-mediated expression cloning. Exp. Hematol. 24:324-329.
47. Pear, W.S., G.P. Nolan, M.L. Scott, and D. Baltimore. 1993. Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. USA. 90:8392-8396.
48. Siraganian, R.P. 1974. An automated continuous-flow system for the extraction and fluorometric analysis of histamine. Anal. Biochem. 57:383-394.
49. Tsuruta, L., H.-J. Lee, E.S. Masuda, N. Koyano-Nakagawa, N. Arai, K. Arai, and T. Yokota. 1995. Cyclic AMP inhibits expresssion of the IL-2 gene through the nuclear factor of activated T cells (NF-AT) site, and transfection of NF-AT cDNAs abrogates the sensitivity of EL-4 cells to cyclic AMP. J. Immunol. 154:5255-5264.
50. Deng, T., and M. Karin. 1994. c-Fos transcriptional activity stimulated by H-Ras-activated protein kinase distinct from JNK and ERK. Nature. 371:171-175.
51. Wershil, B.K., Z.-S. Wang, J.R. Gordon, and S.J. Galli. 1991. Recruitment of neutrophils during IgE-dependent cutaneous late phase reactions in the mouse is mast cell-dependent. Partial inhibition of the reaction with antiserum against tumor necrosis factor-α. J. Clin. Invest. 87:446-453.
52. Inagaki, N., S. Goto, M. Yamasaki, H. Nagai, and A. Koda. 1986. Studies on vascular permeability increasing factors involved in 48-hour homologous PCA in the mouse ear. Int. Arch. Allergy Appl. Immunol. 80:285-290.
53. Kriegler, M., C. Perez, K. DeFay, I. Albert, and S.D. Lu. 1988. A novel form of TNF/cachectin is a cell surface cytotoxic transmembrane protein: ramifications for the complex physiology of TNF. Cell. 53:45-53.
54. Shaw, J.-P., P.J. Utz, D.B. Durand, J.J. Toole, E.A. Emmel, and G.R. Crabtree. 1988. Identification of a putative regulator of early T cell activation genes. Science. 241:202-205.
55. Rooney, J.W., Y.-L. Sun, L.H. Glimcher, and T. Hoey. 1995. Novel NFAT sites that mediate activation of the interleukin-2 promoter in response to T-cell receptor stimulation. Mol. Cell. Biol. 15:6299-6310.
56. Goldfeld, A.E., P.G. McCaffrey, J.L. Strominger, and A. Rao. 1993. Identification of a novel cyclosporin-sensitive element in the human tumor necrosis factor α gene promoter. J. Exp. Med. 178:1365-1379.
57. Tsai, E.Y., J. Jain, P.A. Pesavento, A. Rao, and A.E. Goldfeld. 1996. Tumor necrosis factor alpha gene regulation in activated T cells involves ATF-2/Jun and NFATp. Mol. Cell. Biol. 16:459-467.
58. Tsai, E.Y., J. Yie, D. Thanos, and A.E. Goldfeld. 1996. Cell-type-specific regulation of the human tumor necrosis factor alpha gene in B cells and T cells by NFATp and ATF-2/ JUN. Mol. Cell. Biol. 16:5232-5244.
59. Kawakami, Y., T. Miura, R. Bissonnette, D. Hata, W.N. Khan, T. Kitamura, M. Maeda-Yamamoto, S.E. Hartman, L. Yao, F.W. Alt, and T. Kawakami. 1997. Bruton's tyrosine kinase regulates apoptosis and JNK/SAPK kinase activity. Proc. Natl. Acad. Sci. USA. 94:3938-3942.
60. Li, T., S. Tsukada, A. Satterthwaite, M.H. Havlik, H. Park, K. Takatsu, and O.N. Witte. 1995. Activation of Bruton's tyrosine kinase (BTK) by a point mutation in its pleckstrin homology (PH) domain. Immunity. 2:1-20.
61. Clark, S.G., M.J. Stern, and H.R. Horvitz. 1992. C. elegans cell-signalling gene sem-5 encodes a protein with SH2 and SH3 domains. Nature. 356:340-344.
62. Conley, M.E., O. Parolini, J. Rohrer, and D. Campana. 1994. X-linked agammaglobulinemia: new approaches to old questions based on the identification of the defective gene. Immunol. Rev. 138:5-21.
63. Scher, I. 1982. The CBA/N mouse strain: an experimental model illustrating the influence of X chromosome on immunity. Adv. Immunol. 33:1-71.
64. Harlan, J.E., P.J. Hajduk, H.S. Yoon, and S.W. Fesik. 1994. Pleckstrin homology domains bind to phosphatidylinositol-4,5-bisphosphate. Nature. 371:168-170.
65. Salim, K., M.J. Bottomley, E. Querfurth, M.J. Zvelebil, I. Gout, R. Scaife, R.L. Margolis, R. Gigg, C.I.E. Smith, P.C. Driscoll, et al. 1996. Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. EMBO (Eur. Mol. Biol. Organ.) J. 15:6241-6250.
66. Fukuda, M., T. Kojima, H. Kabayama, and K. Mikoshiba. 1996. Mutation of the pleckstrin homology domain of Bruton's tyrosine kinase in immunodeficiency impaired inositol 1,3,4,5-terakisphosphate binding capacity. J. Biol. Chem. 271: 30303-30306.
67. Touhara, K., J. Inglese, J.A. Pitcher, G. Shaw, and R.J. Lefkowitz. 1994. Binding of G protein βγ-subunits to pleckstrin homology domains. Biol. Chem. 269:10217-10220.
68. Wang, D.-S., R. Shaw, J.C. Winkelmann, and G. Shaw. 1994. Binding of PH domains of β-adrenergic receptor kinase and β-spectrin to WD40/β-transducin repeat containing regions of the β-subunit of trimeric G-proteins. Biochem. Biophys. Res. Commun. 203:29-35.
69. Yang, W., and S. Desiderio. 1997. BAP-135, a target for Bruton's tyrosine kinase in response to B cell receptor engagement. Proc. Natl. Acad. Sci. USA. 94:604-609.
70. Cheng, G., Z.-S. Ye, and D. Baltimore. 1994. Binding of Bruton's tyrosine kinase to Fyn, Lyn, or Hck through a Src homology 3 domain-mediated interaction. Proc. Natl. Acad. Sci. USA. 91:8152-8155.
71. Yang, W., S.N. Malek, and S. Desiderio. 1995. An SH3-binding site conserved in Bruton's tyrosine kinase and related tyrosine kinases mediates specific protein interactions in vitro and in vivo. J. Biol. Chem. 270:20832-20840.
72. Cory, G.O.C., R.C. Lovering, S. Hinshelwood, L. MacCarthy-Morrogh, R.J. Levinsky, and G. Kinnon. 1995. The protein product of the c-cbl protooncogene is phosphorylated after B cell receptor stimulation and binds the SH3 domain of Bruton's tyrosine kinase. J. Exp. Med. 182:611-615.
73. Lindsten, T., C.H. June, J.A. Ledbetter, G. Stella, and C.B. Thompson. 1989. Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway. Science. 244:339-343.
74. Caput, D., B. Beutler, K. Hartog, R. Thayer, S. Brown-Shimer, and A. Cerami. 1986. Identification of a common nucleotide sequence in the 3′-untranslated region of mRNA molecules specifying inflammatory mediators. Proc. Natl. Acad. Sci. USA. 83:1670-1674.
75. Beutler, B., N. Krochin, I.W. Milsark, C. Luedke, and A. Cerami. 1986. Control of cachectin (tumor necrosis factor) synthesis: mechanisms of endotoxin resistance. Science. 232: 977-980.
76. Han, J., T. Brown, and B. Beutler. 1990. Endotoxin-responsive sequences control cachectin/tumor necrosis factor biosynthesis at the translational level. J. Exp. Med. 171:465-475.
77. Goldfeld, A.E., E.Y. Tsai, R. Kincaid, P.J. Belshaw, S.L. Schreiber, J.L. Strominger, and A. Rao. 1994. Calcineurin mediates human tumor necrosis factor α gene induction in stimulated T and B cells. J. Exp. Med. 180:763-768.
78. ras links Fc∈RI to NF-AT family member in mast cells. The AP3-like factor in this cell type is an NF-AT family member. J. Immunol. 155:4963-1970.
79. Jain, J., P.G. McCaffrey, Z. Miner, T.K. Kerppola, J.N. Lamben, G.L. Verdine, T. Curran, and A. Rao. 1993. The T-cell transcription factor NFATp is a substrate for calcineurin and interacts with Fos and Jun. Nature. 365:352-355.
80. Rawlings, D.J., A.M. Scharenberg, H. Park, M.I. Wahl, S. Lin, R.M. Kato, A.-C. Fluckiger, O.N. Witte, and J.-P. Kinet. 1996. Activation of BTK by a phosphorylation mechanism initiated by SRC family kinases. Science. 271:822-825.
81. Park, H., M.I. Wahl, D.E.H. Afar, C.W. Turck, D.J. Rawlings, C. Tam, A.M. Scharenberg, J.-P. Kinet, and O.N. Witte. 1996. Regulation of Btk function by a major autophosphorylation site within the SH3 domain. Immunity. 4: 515-525.
82. Takata, M., and T. Kurosaki. 1996. A role for Bruton's tyrosine kinase in B cell antigen receptor-mediated activation of phospholipase C-γ2. J. Exp. Med. 184:31-40.
83. Nishizuka, Y. 1984. The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature. 308: 693-698.
84. Rao, A. 1994. NF-ATp: a transcription factor required for the co-ordinate induction of several cytokine genes. Immunol. Today. 15:274-281.
85. 2 pathway by Fc∈RI is not shared by a G protein-coupled receptor. J. Biol. Chem. 270:10960-10967.
86. Gupta, S., D. Campbell, B. Derijard, and R.J. Davis. 1995. Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science. 267:389-393.
87. Livingstone, C., G. Patel, and N. Jones. 1995. ATF-2 contains a phosphorylation-dependent transcriptional activation domain. EMBO (Eur. Mol. Biol. Organ.) J. 14:1785-1797.
88. van Dam, H., D. Wilhelm, I. Herr, A. Steffen, P. Herrlich, and P. Angel. 1995. ATF-2 is preferentially activated by stress-activated protein kinases to mediate c-jun induction in response to genotoxic agents. EMBO (Eur. Mol. Biol. Organ.) J. 14:1798-1811.
89. Lev, S., D. Givol, and Y. Yarden. 1991. A specific combination of substrates is involved in signal transduction by the kit-encoded receptor. EMBO (Eur. Mol. Biol. Organ.) J. 10: 647-654.
90. Reith, A.D., C. Ellis, S.D. Lyman, D.M. Anderson, D.E. Williams, A. Bernstein, and T. Pawson. 1991. Signal transduction by normal isoforms and W mutant variants of the Kit receptor tyrosine kinase. EMBO (Eur. Mol. Biol. Organ.) J. 10:2451-2459.