Signal transduction via the stem cell factor receptor/c-Kit

Cellular and Molecular Life Sciences

Volumn 61, Issue 19-20, 2004, Pages 2535-2548

  Ronnstrand L ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

c Kit; Receptor tyrosine kinase; Signal transduction; Src homology 2; Stem cell factor

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 2,3 DIHYDRO 2 OXO 3 (4,5,6,7 TETRAHYDRO 1H INDOL 2 YLMETHYLENE) 1H INDOLE 5 SULFONIC ACID DIMETHYLAMIDE; ADAPTOR PROTEIN; ANTISENSE OLIGONUCLEOTIDE; CALPHOSTIN C; JANUS KINASE; JANUS KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE C INHIBITOR; PROTEIN SH2; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; PROTEIN TYROSINE PHOSPHATASE; RAS PROTEIN; STAT PROTEIN; STEM CELL FACTOR RECEPTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; CELL TYPE; DIMERIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; GASTROINTESTINAL STROMAL TUMOR; GERM CELL; GERM CELL TUMOR; HEMATOPOIETIC STEM CELL; HUMAN; MAST CELL; MELANOCYTE; NONHUMAN; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN; TESTIS CANCER;

ALTERNATIVE SPLICING; ANIMALS; CELL LINE; CELL LINE, TUMOR; DIMERIZATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LIGANDS; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-KIT; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; TYROSINE;

JANUS;

EID: 9744246909     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-004-4189-6     Document Type: Review

References (167)

1. Besmer P., Murphy J. E., George P. C., Qiu F. H., Bergold P. J., Lederman L. et al. (1986) A new acute transforming feline retrovirus and relationship of its oncogene v-kit with the protein kinase gene family. Nature 320: 415-421
2. Yarden Y., Kuang W. J., Yang-Feng T., Coussens L., Munemitsu S., Dull T. J. et al. (1987) Human proto-oncogene c-kit: a new cell surface receptor tyrosine kinase for an unidentified ligand. EMBO J. 6: 3341-3351
3. Chabot B., Stephenson D. A., Chapman V. M., Besmer P. and Bernstein A. (1988) The proto-oncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Nature 335: 88-89
4. Geissler E. N., Ryan M. A. and Housman D. E. (1988) The dominant-white spotting (W) locus of the mouse encodes the c-kit proto-oncogene. Cell 55: 185-192
5. Copeland N. G., Gilbert D. J., Cho B. C., Donovan P. J., Jenkins N. A., Cosman D. et al. (1990) Mast cell growth factor maps near the steel locus on mouse chromosome 10 and is deleted in a number of steel alleles. Cell 63: 175-183
6. Williams D. E., Eisenman J., Baird A., Rauch C., Van Ness K., March C. J. et al. (1990) Identification of a ligand for the c-kit proto-oncogene. Cell 63: 167-174
7. Lev S., Blechman J. M., Givol D. and Yarden Y. (1994) Steel factor and c-kit protooncogene: genetic lessons in signal transduction. Crit. Rev. Oncog. 5: 141-168
8. Reith A. D., Ellis C., Lyman S. D., Anderson D. M., Williams D. E., Bernstein A. et al. (1991) Signal transduction by normal isoforms and W mutant variants of the Kit receptor tyrosine kinase. EMBO J. 10: 2451-2459
9. Crosier P. S., Ricciardi S. T., Hall L. R., Vitas M. R., Clark S. C. and Crosier K. E. (1993) Expression of isoforms of the human receptor tyrosine kinase c-kit in leukemic cell lines and acute myeloid leukemia. Blood 82: 1151-1158
10. Hayashi S., Kunisada T., Ogawa M., Yamaguchi K. and Nishikawa S. (1991) Exon skipping by mutation of an authentic splice site of c-kit gene in W/W mouse. Nucleic Acids Res. 19: 1267-1271
11. Rossi P., Marziali G., Albanesi C., Charlesworth A., Geremia R. and Sorrentino V. (1992) A novel c-kit transcript, potentially encoding a truncated receptor, originates within a kit gene intron in mouse spermatids. Dev. Biol. 152: 203-207
12. Paronetto M. P., Venables J. P., Elliott D. J., Geremia R., Rossi P. and Sette C. (2003) Tr-kit promotes the formation of a multimolecular complex composed by Fyn, PLCgamma1 and Sam68. Oncogene 22: 8707-8715
13. Piao X., Curtis J. E., Minkin S., Minden M. D. and Bernstein A. (1994) Expression of the Kit and KitA receptor isoforms in human acute myelogenous leukemia. Blood 83: 476-481
14. Caruana G., Cambareri A. C. and Ashman L. K. (1999) Isoforms of c-KIT differ in activation of signalling pathways and transformation of NIH3T3 fibroblasts. Oncogene 18: 5573-5581
15. Voytyuk O., Lennartsson J., Mogi A., Caruana G., Courtneidge S., Ashman L. K. et al. (2003) Src family kinases are involved in the differential signaling from two splice forms of c-Kit. J. Biol. Chem. 278: 9159-9166
16. Krystal G. W., Hines S. J. and Organ C. P. (1996) Autocrine growth of small cell lung cancer mediated by coexpression of c-kit and stem cell factor. Cancer Res, 56: 370-376
17. Hines S. J., Litz J. S. and Krystal G. W. (1999) Coexpression of c-kit and stem cell factor in breast cancer results in enhanced sensitivity to members of the EGF family of growth factors. Breast Cancer Res. Treat. 58: 1-10
18. Bellone G., Silvestri S., Artusio E., Tibaudi D., Turletti A., Geuna M. et al. (1997) Growth stimulation of colorectal carcinoma cells via the c-kit receptor is inhibited by TGF-beta 1. J. Cell. Physiol. 172: 1-11
19. Inoue M., Kyo S., Fujita M., Enomoto T. and Kondoh G. (1994) Coexpression of the c-kit receptor and the stem cell factor in gynecological tumors. Cancer Res. 54: 3049-3053
20. Natali P. G., Berlingieri M. T., Nicotra M. R., Fusco A., Santoro E., Bigotti A. et al. (1995) Transformation of thyroid epithelium is associated with loss of c-kit receptor. Cancer Res. 55: 1787-1791
21. Kurosawa K., Miyazawa K., Gotoh A., Katagiri T., Nishimaki J., Ashman L. K. et al. (1996) Immobilized anti-KIT monoclonal antibody induces ligand-independent dimerization and activation of Steel factor receptor: biologic similarity with membrane-bound form of Steel factor rather than its soluble form. Blood 87: 2235-2243
22. Natali P. G., Nicotra M. R., Sures I., Mottolese M., Botti C. and Ullrich A. (1992) Breast cancer is associated with loss of the c-kit oncogene product. Int. J. Cancer 52: 713-717
23. Tsuura Y., Suzuki T., Honma K. and Sano M. (2002) Expression of c-kit protein in proliferative lesions of human breast: sexual difference and close association with phosphotyrosine status. J. Cancer Res. Clin. Oncol. 128: 239-246
24. Longley B. J., Tyrrell L., Lu S. Z., Ma Y. S., Langley K., Ding T. G. et al. (1996) Somatic c-KIT activating mutation in urticaria pigmentosa and aggressive mastocytosis: establishment of clonality in a human mast cell neoplasm. Nat. Genet. 12: 312-314
25. Nagata H., Worobec A. S., Oh C. K., Chowdhury B. A., Tannenbaum S., Suzuki Y. et al. (1995) Identification of a point mutation in the catalytic domain of the protooncogene c-kit in peripheral blood mononuclear cells of patients who have mastocytosis with an associated hematologic disorder. Proc. Natl. Acad. Sci. USA 92: 10560-10564
26. Ning Z. Q., Li J., McGuinness M. and Arceci R. J. (2001) STAT3 activation is required for Asp(816) mutant c-Kit induced tumorigenicity. Oncogene 20: 4528-4536
27. Tian Q., Frierson H. F. Jr, Krystal G. W. and Moskaluk C. A. (1999) Activating c-kit gene mutations in human germ cell tumors. Am. J. Pathol. 154: 1643-1647
28. Hirota S., Isozaki K., Moriyama Y., Hashimoto K., Nishida T., Ishiguro S. et al. (1998) Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 279: 577-580
29. Blume-Jensen P., Claesson-Welsh L., Siegbahn A., Zsebo K. M., Westermark B. and Heldin C. H. (1991) Activation of the human c-kit product by ligand-induced dimerization mediates circular actin reorganization and chemotaxis. EMBO J. 10: 4121-4128
30. Philo J. S., Wen J., Wypych J., Schwartz M. G., Mendiaz E. A. and Langley K. E. (1996) Human stem cell factor dimer forms a complex with two molecules of the extracellular domain of its receptor. Kit. J. Biol. Chem. 271: 6895-6902
31. Lemmon M. A., Pinchasi D., Zhou M., Lax I. and Schlessinger J. (1997) Kit receptor dimerization is driven by bivalent binding of stem cell factor. J. Biol. Chem. 272: 6311-6317
32. Pawson T. (2004) Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116: 191-203
33. Huang E. J., Nocka K. H., Buck J. and Besmer P. (1992) Differential expression and processing of two cell associated forms of the kit-ligand: KL-1 and KL-2. Mol. Biol. Cell 3: 349-362
34. Miyazawa K., Williams D. A., Gotoh A., Nishimaki J., Broxmeyer H. E. and Toyama K. (1995) Membrane-bound Steel factor induces more persistent tyrosine kinase activation and longer life span of c-kit gene-encoded protein than its soluble form. Blood 85: 641-649
35. Kapur R., Chandra S., Cooper R., McCarthy J. and Williams D. A. (2002) Role of p38 and ERK MAP kinase in proliferation of erythroid progenitors in response to stimulation by soluble and membrane isoforms of stem cell factor. Blood 100: 1287-1293
36. Haglund K., Di Fiore P. P. and Dikic I. (2003) Distinct monoubiquitin signals in receptor endocytosis. Trends Biochem. Sci. 28: 598-603
37. Joazeiro C. A., Wing S. S., Huang H., Leverson J. D., Hunter T. and Liu Y. C. (1999) The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science 286: 309-312
38. Yokouchi M., Kondo T., Sanjay A., Houghton A., Yoshimura A., Komiya S. et al. (2001) Src-catalyzed phosphorylation of c-Cbl leads to the interdependent ubiquitination of both proteins. J. Biol. Chem. 276: 35185-35193
39. Sattler M., Salgia R., Shrikhande G., Verma S., Pisick E., Prasad K. V. et al. (1997) Steel factor induces tyrosine phosphorylation of CRKL and binding of CRKL to a complex containing c-kit, phosphatidylinositol 3-kinase, and p120(CBL). J. Biol. Chem. 272: 10248-10253
40. Wisniewski D., Strife A. and Clarkson B. (1996) c-kit ligand stimulates tyrosine phosphorylation of the c-Cbl protein in human hematopoietic cells. Leukemia 10: 1436-1442
41. Wollberg P., Lennartsson J., Gottfridsson E., Yoshimura A. and Rönnstrand L. (2003) The adapter protein APS associates with the multifunctional docking sites Tyr-568 and Tyr-936 in c-Kit. Biochem. J. 370: 1033-1038
42. Broudy V. C., Lin N. L., Liles W. C., Corey S. J., O'Laughlin B., Mou S. et al. (1999) Signaling via Src family kinases is required for normal internalization of the receptor c-Kit. Blood 94: 1979-1986
43. Jalin T., Seipel P., Coutinho S., Urschel S., Schwarz K., Miething C. et al. (2002) Analysing c-kit internalization using a functional c-kit-EGFP chimera containing the fluorochrome within the extracellular domain. Oncogene 21: 4508-4520
44. Blume-Jensen P., Rönnstrand L., Gout I., Waterfield M. D. and Heldin C. H. (1994) Modulation of Kit/stem cell factor receptor-induced signaling by protein kinase C. J. Biol. Chem. 269: 21793-21802
45. Kozawa O., Blume-Jensen P., Heldin C. H. and Rönnstrand L. (1997) Involvement of phosphatidylinositol 3′-kinase in stem-cell-factor-induced phospholipase D activation and arachidonic acid release. Eur. J. Biochem. 248: 149-155
46. Blume-Jensen P., Wernstedt C., Heldin C. H. and Rönnstrand L. (1995) Identification of the major phosphorylation sites for protein kinase C in kit/stem cell factor receptor in vitro and in intact cells. J. Biol. Chem. 270: 14192-14200
47. Blume-Jensen P., Janknecht R. and Hunter T. (1998) The kit receptor promotes cell survival via activation of PI 3-kinase and subsequent Akt-mediated phosphorylation of Bad on Ser136. Curr. Biol. 8: 779-782
48. Yee N. S., Langen H. and Besmer P. (1993) Mechanism of kit ligand, phorbol ester and calcium-induced down-regulation of c-kit receptors in mast cells. J. Biol. Chem. 268: 14189-14201
49. Yee N. S., Hsiau C. W., Serve H., Vosseller K. and Besmer P. (1994) Mechanism of down-regulation of c-kit receptor. Roles of receptor tyrosine kinase, phosphatidylinositol 3′-kinase and protein kinase C. J. Biol. Chem. 269: 31991-31998
50. Wormald S. and Hilton D. J. (2004) Inhibitors of cytokine signal transduction. J. Biol. Chem. 279: 821-824
51. De Sepulveda P., Okkenhaug K., Rose J. L., Hawley R. G., Dubreuil P. and Rottapel R. (1999) Socs1 binds to multiple signalling proteins and suppresses steel factor-dependent proliferation. EMBO J. 18: 904-915
52. Ilangumaran S., Finan D., Raine J. and Rottapel R. (2003) Suppressor of cytokine signaling 1 regulates an endogenous inhibitor of a mast cell protease. J. Biol. Chem. 278: 41871-41880
53. Kozlowski M., Larose L., Lee F., Le D. M., Rottapel R. and Siminovitch K. A. (1998) SHP-1 binds and negatively modulates the c-Kit receptor by interaction with tyrosine 569 in the c-Kit juxtamembrane domain. Mol. Cell. Biol. 18: 2089-2099
54. Yi T. and Ihle J. N. (1993) Association of hematopoietic cell phosphatase with c-Kit after stimulation with c-Kit ligand. Mol. Cell. Biol. 13: 3350-3358
55. Shultz L. D., Schweitzer P. A., Rajan T. V., Yi T., Ihle J. N., Matthews R. J. et al. (1993) Mutations at the murine motheaten locus are within the hematopoietic cell protein-tyrosine phosphatase (Hcph) gene. Cell 73: 1445-1454
56. Lorenz U., Bergemann A. D., Steinberg H. N., Flanagan J. G., Li X., Galli S. J. et al. (1996) Genetic analysis reveals cell type-specific regulation of receptor tyrosine kinase c-Kit by the protein tyrosine phosphatase SHP1. J. Exp. Med. 184: 1111-1126
57. Lewis T. S., Shapiro P. S. and Ahn N. G. (1998) Signal transduction through MAP kinase cascades. Adv. Cancer Res. 74: 49-139
58. Qiu R. G., Chen J., Kirn D., McCormick F. and Symons M. (1995) An essential role for Rac in Ras transformation. Nature 374: 457-459
59. Rodriguez-Viciana P., Warne P. H., Khwaja A., Marte B. M., Pappin D., Das P. et al. (1997) Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeletonby Ras. Cell 89: 457-467
60. Rozakis-Adcock M., McGlade J., Mbamalu G., Pelicci G., Daly R., Li W, et al. (1992) Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature 360: 689-692
61. Lowenstein E. J. Daly R. J., Batzer A. G., Li W., Margolis B., Lammers R. et al. (1992) The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70: 431-442
62. Li W., Nishimura R., Kashishian A., Batzer A. G., Kim W. J., Cooper J. A. et al. (1994) A new function for a phosphotyrosine phosphatase: linking GRB2-Sos to a receptor tyrosine kinase. Mol. Cell. Biol. 14: 509-517
63. Kyriakis J. M., App H., Zhang X. F., Banerjee P., Brautigan D. L., Rapp U. R. et al. (1992) Raf-1 activates MAP kinase-kinase- Nature 358: 417-421
64. Crews C. M. and Erikson R. E. (1992) Purification of a murine protein-tyrosine/threonine kinase that phosphorylates and activates the Erk-1 gene product: relationship to the fission yeast byr1 gene product. Proc. Natl. Acad. Sci. USA 89: 8205-8209
65. Khokhlatchev A. V., Canagarajah B., Wilsbacher J., Robinson M., Atkinson M., Goldsmith E. et al. (1998) Phosphorylation of the MAP kinase ERK2 promotes its homodimerization and nuclear translocation. Cell 93: 605-615
66. Murphy L. O., Smith S., Chen R. H., Fingar D. C. and Blenis J. (2002) Molecular interpretation of ERK signal duration by immediate early gene products. Nat. Cell Biol. 4: 556-564
67. Thömmes K., Lennartsson J., Carlberg M. and Rönnstrand L. (1999) Identification of Tyr-703 and Tyr-936 as the primary association sites for Grb2 and Grb7 in the c-Kit/stem cell factor receptor. Biochem. J. 341 (Pt 1): 211-216
68. Tauchi T., Feng G. S., Marshall M. S., Shen R., Mantel C., Pawson T. et al. (1994) The ubiquitously expressed Syp phosphatase interacts with c-kit and Grb2 in hematopoietic cells. J. Biol. Chem. 269: 25206-25211
69. Tauchi T., Boswell H. S., Leibowitz D. and Broxmeyer H. E. (1994) Coupling between p210bcr-abl and Shc and Grb2 adaptor proteins in hematopoietic cells permits growth factor receptor-independent link to ras activation pathway. J. Exp. Med. 179: 167-175
70. Dorsey J. F., Cunnick J. M., Mane S. M. and Wu J. (2002) Regulation of the Erk2-Elk1 signaling pathway and megakaryocytic differentiation of Bcr-Abl(+) K562 leukemic cells by Gab2. Blood 99: 1388-1397
71. Bondzi C., Litz J., Dent P. and Krystal G. W. (2000) Src family kinase activity is required for Kit-mediated mitogen-activated protein (MAP) kinase activation; however, loss of functional retinoblastoma protein makes MAP kinase activation unnecessary for growth of small cell lung cancer cells. Cell Growth Differ. 11: 305-314
72. Lerrnartsson J., Blume-Jensen P., Hermanson M., Pontén E., Carlberg M. and Rönnstrand L. (1999) Phosphorylation of Shc by Src family kinases is necessary for stem cell factor receptor/c-kit mediated activation of the Ras/MAP kinase pathway and c-fos induction. Oncogene 18: 5546-5553
73. Ueda S., Mizuki M., Ikeda H., Tsujimura T., Matsumura I., Nakano K. et al. (2002) Critical roles of c-Kit tyrosine residues 567 and 719 in stem cell factor-induced chemotaxis: contribution of src family kinase and PI3-kinase on calcium mobilization and cell migration. Blood 99: 3342-3349
74. Timokhina I., Kissel H., Stella G. and Besmer P. (1998) Kit signaling through PI 3-kinase and Src kinase pathways: an essential role for Rac1 and JNK activation in mast cell proliferation. EMBO J. 17: 6250-6262
75. Wandzioch E., Edling C. E., Palmer R. H., Carlsson L. and Hallberg B. (2004) Activation of the MAP-kinase pathway by c-Kit is PI-3-kinase dependent in hematopoietic progenitor/ stem cell lines. Blood 104: 51-57
76. Duckworth B. C. and Cantley L. C. (1997) Conditional inhibition of the mitogen-activated protein kinase cascade by wortmannin. Dependence on signal strength. J. Biol. Chem. 272: 27665-27670
77. Foster F. M., Traer C. J., Abraham S. M. and Fry M. J. (2003) The phosphoinositide (PI) 3-kinase family. J. Cell Sci. 116: 3037-3040
78. Carpenter C. L., Auger K. R., Chanudhuri M., Yoakim M., Schaffhausen B., Shoelson S. et al. (1993) Phosphoinositide 3-kinase is activated by phosphopeptides that bind to the SH2 domains of the 85-kDa subunit. J. Biol. Chem. 268: 9478-9483
79. Ueki K., Fruman D. A., Brachmann S. M., Tseng Y. H., Cantley L. C. and Kahn C. R. (2002) Molecular balance between the regulatory and catalytic subunits of phosphoinositide 3-kinase regulates cell signaling and survival. Mol. Cell. Biol. 22: 965-977
80. Hartley D., Meisner H. and Corvera S. (1995) Specific association of the beta isoform of the p85 subunit of phosphatidylinositol-3 kinase with the proto-oncogene c-cbl. J. Biol. Chem. 270: 18260-18263
81. Lennartsson J., Wernstedt C., Engström U., Hellman U. and Rönnstrand L. (2003) Identification of Tyr900 in the kinase domain of c-Kit as a Src-dependent phosphorylation site mediating interaction with c-Crk. Exp. Cell Res. 288: 110-118
82. Serve H., Yee N. S., Stella G., Sepp-Lorenzino L., Tan J. C. and Besmer P. (1995) Differential roles of PI3-kinase and Kit tyrosine 821 in Kit receptor-mediated proliferation, survival and cell adhesion in mast cells. EMBO J. 14: 473-483
83. Kubota Y., Angelotti T., Niederfellner G., Herbst R. and Ullrich A. (1998) Activation of phosphatidylinositol 3-kinase is necessary for differentiation of FDC-P1 cells following stimulation of type III receptor tyrosine kinases. Cell Growth Differ. 9: 247-256
84. Vosseller K., Stella G., Yee N. S. and Besmer P. (1997) c-kit receptor signaling through its phosphatidylinositide-3′-kinase-binding site and protein kinase C: role in mast cell enhancement of degranulation, adhesion and membrane ruffling. Mol. Biol. Cell 8: 909-922
85. Engström M., Karlsson R. and Jönsson J. I. (2003) Inactivation of the forkhead transcription factor FoxO3 is essential for PKB-mediated survival of hematopoietic progenitor cells by kit ligand. Exp. Hematol. 31: 316-323
86. Chian R., Young S., Danilkovitch-Miagkova A., Rönnstrand L., Leonard E., Ferrao P. et al. (2001) Phosphatidylinositol 3 kinase contributes to the transformation of hematopoietic cells by the DS16V c-Kit mutant. Blood 98: 1365-1373
87. Hashimoto K., Matsumura I., Tsujimura T., Kim D. K., Ogihara H., Ikeda H. et al. (2003) Necessity of tyrosine 719 and phosphatidylinositol 3′-kinase-mediated signal pathway in constitutive activation and oncogenic potential of c-kit receptor tyrosine kinase with the Asp814Val mutation. Blood 101: 1094-1102
88. Blume-Jensen P., Jiang G., Hyman R., Lee K. F., O'Gorman S. and Hunter T. (2000) Kit/stem cell factor receptor-induced activation of phosphatidylinositol 3′-kinase is essential for male fertility. Nat. Genet. 24: 157-162
89. Kissel H., Timokhina I., Hardy M. P., Rothschild G., Tajima Y., Soares V. et al. (2000) Point mutation in kit receptor tyrosine kinase reveals essential roles for kit signaling in spermatogenesis and oogenesis without affecting other kit responses. EMBO J. 19: 1312-1326
90. Nishimura R., Li W., Kashishian A., Mondino A., Zhou M., Cooper J. et al. (1993) Two signaling molecules share a phosphotyrosine-containing binding site in the platelet-derived growth factor receptor. Mol. Cell. Biol. 13: 6889-6896
91. Fukao T., Yamada T., Tanabe M., Terauchi Y., Ota T., Takayama T. et al. (2002) Selective loss of gastrointestinal mast cells and impaired immunity in PI3K-deficient mice. Nat. Immunol. 3: 295-304
92. Tan B. L., Yazicioglu M. N., Ingram D., McCarthy J., Borneo J., Williams D. A. et al. (2003) Genetic evidence for convergence of c-Kit- and alpha4 integrin-mediated signals on class IA PI-3kinase and the Rac pathway in regulating integrin-directed migration in mast cells. Blood 101: 4725-4732
93. Arcaro A., Khanzada U. K., Vanhaesebroeck B., Tetley T. D., Waterfield M. D. and Seckl M. J. (2002) Two distinct phosphoinositide 3-kinases mediate polypeptide growth factor-stimulated PKB activation. EMBO J. 21: 5097-5108
94. Carpenter G. and Ji Q. (1999) Phospholipase C-gamma as a signal-transducing element. Exp. Cell Res. 253: 15-24
95. Berridge M. J., Bootman M. D. and Roderick H. L. (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell. Biol. 4: 517-529
96. Herbst R., Lammers R., Schlessinger J. and Ullrich A. (1991) Substrate phosphorylation specificity of the human c-kit receptor tyrosine kinase. J. Biol. Chem. 266: 19908-19916
97. Herbst R., Shearman M. S., Jallal B., Schlessinger J. and Ullrich A. (1995) Formation of signal transfer complexes between stem cell and platelet-derived growth factor receptors and SH2 domain proteins in vitro. Biochemistry 34: 5971-5979
98. Gommerman J. L., Sittaro D., Klebasz N. Z., Williams D. A. and Berger S. A. (2000) Differential stimulation of c-Kit mutants by membrane-bound and soluble Steel Factor correlates with leukemic potential. Blood 96: 3734-3742
99. Koike T., Hirai K., Morita Y. and Nozawa Y. (1993) Stem cell factor-induced signal transduction in rat mast cells. Activation of phospholipase D but not phosphoinositide-specific phospholipase C in c-kit receptor stimulation. J. Immunol. 151: 359-366
100. Huber M., Helgason C. D., Scheid M. P., Duronio V., Humphries R. K. and Krystal G. (1998) Targeted disruption of SHIP leads to Steel factor-induced degranulation of mast cells. EMBO J. 17: 7311-7319
101. Trieselmann N. Z., Soboloff J. and Berger S. A. (2003) Mast cells stimulated by membrane-bound, but not soluble, steel factor are dependent on phospholipase C activation. Cell. Mol. Life Sci. 60: 759-766
102. Maddens S., Charruyer A., Plo I., Dubreuil P., Berger S., Salles B. et al. (2002) Kit signaling inhibits the sphingomyelin-ceramide pathway through PLC gamma 1: implication in stem cell factor radioprotective effect. Blood 100: 1294-1301
103. Plo I., Lautier D., Casteran N., Dubreuil P., Arock M. and Laurent G. (2001) Kit signaling and negative regulation of daunorubicin-induced apoptosis: role of phospholipase Cgamma. Oncogene 20: 6752-6763
104. Abram C. L. and Courtneidge S. A. (2000) Src family tyrosine kinases and growth factor signaling. Exp. Cell Res. 254: 1-13
105. Krystal G. W., DeBerry C. S., Linnekin D. and Litz J. (1998) Lck associates with and is activated by Kit in a small cell lung cancer cell line: inhibition of SCF-mediated growth by the Src family kinase inhibitor PP1. Cancer Res. 58: 4660-4666
106. Linnekin D., DeBerry C. S. and Mou S. (1997) Lyn associates with the juxtamembrane region of c-Kit and is activated by stem cell factor in hematopoietic cell lines and normal progenitor cells. J. Biol. Chem. 272: 27450-27455
107. Price D. J., Rivnay B., Fu Y., Jiang S., Avraham S. and Avraham H. (1997) Direct association of Csk homologous kinase (CHK) with the diphosphorylated site Tyr568/570 of the activated c-KIT in megakaryocytes. J. Biol. Chem. 272: 5915-5920
108. O'Laughlin-Bunner B., Radosevic N., Taylor M. L., Shivakrapa, DeBerry C., Metcalfe D. D. et al. (2001) Lyn is required for normal stem cell factor-induced proliferation and chemotaxis of primary hematopoietic cells. Blood 98: 343-350
109. Mou S. and Linnekin D. (1999) Lyn is activated during late G1 of stem-cell-factor-induced cell cycle progression in haemopoietic cells. Biochem. J. 342 (Pt 1): 163-170
110. Hong L., Munugalavadla V. and Kapur R. (2004) c-Kit-mediated overlapping and unique functional and biochemical outcomes via diverse signaling pathways. Mol. Cell. Biol. 24: 1401-1410
111. Agosti V., Corbacioglu S., Ehlers I., Waskow C., Sommer G., Berrozpe G. et al. (2004) Critical role for Kit-mediated Src kinase but not PI 3-kinase signaling in Pro T and Pro B cell development. J. Exp. Med. 199: 867-878
112. Jhun B. H., Rivnay B., Price D. and Avraham H. (1995) The MATK tyrosine kinase interacts in a specific and SH2-dependent manner with c-Kit. J. Biol. Chem. 270: 9661-9666
113. Kerr I. M., Costa-Pereira A. P., Lillemeier B. F. and Strobl B. (2003) Of JAKs, STATs, blind watchmakers, jeeps and trains. FEBS Lett. 546: 1-5
114. Brizzi M. F., Zini M. G., Aronica M. G., Blechman J. M., Yarden Y. and Pegoraro L. (1994) Convergence of signaling by interleukin-3, granulocyte-macrophage colony-stimulating factor, and mast cell growth factor on JAK2 tyrosine kinase. J. Biol. Chem. 269: 31680-31684
115. Weiler S. R., Mou S., DeBerry C. S., Keller J. R., Ruscetti F. W., Ferris D. K. et al. (1996) JAK2 is associated with the c-kit proto-oncogene product and is phosphorylated in response to stem cell factor. Blood 87: 3688-3693
116. Radosevic N., Winterstein D., Keller J. R., Neubauer H., Pfeffer K. and Linnekin D. (2004) JAK2 contributes to the intrinsic capacity of primary hematopoietic cells to respond to stem cell factor. Exp. Hematol. 32: 149-156
117. Deberry C., Mou S. and Linnekin D. (1997) Stat1 associates with c-kit and is activated in response to stem cell factor. Biochem. J. 327 (Pt 1): 73-80
118. Brizzi M. F., Dentelli P., Rosso A., Yarden Y. and Pegoraro L. (1999) STAT protein recruitment and activation in c-Kit deletion mutants. J. Biol. Chem. 274: 16965-16972
119. Ryan J. J., Huang H., McReynolds L. J., Shelburne C., Hu-Li J., Huff T. F. et al. (1997) Stem cell factor activates STAT-5 DNA binding in IL-3-derived bone marrow mast cells. Exp. Hematol. 25: 357-362
120. O'Farrell A. M., Ichihara M., Mui A. L. and Miyajima A. (1996) Signaling pathways activated in a unique mast cell line where interleukin-3 supports survival and stem cell factor is required for a proliferative response. Blood 87: 3655-3668
121. Pearson M. A., O'Farrell A. M., Dexter T. M., Whetton A. D., Owen-Lynch P. J. and Heyworth C. M. (1998) Investigation of the molecular mechanisms underlying growth factor synergy: the role of ERK 2 activation in synergy. Growth Factors 15: 293-306
122. Jacobs-Helber S. M., Penta K., Sun Z., Lawson A. and Sawyer S. T. (1997) Distinct signaling from stem cell factor and erythropoietin in HCD57 cells. J. Biol. Chem. 272: 6850-6853
123. Smith C. I., Islam T. C., Mattsson P. T., Mohamed A. J., Nore B. F. and Vihinen M. (2001) The Tec family of cytoplasmic tyrosine kinases: mammalian Btk, Bmx, Itk, Tec. Txk and homologs in other species. Bioessays 23: 436-446
124. Tang B., Mano H., Yi T. and Ihle J. N. (1994) Tec kinase associates with c-kit and is tyrosine phosphorylated and activated following stem cell factor binding. Mol. Cell. Biol. 14: 8432-8437
125. van Dijk T. B., van Den Akker E., Amelsvoort M. P., Mano H., Lowenberg B. and von Lindern M. (2000) Stem cell factor induces phosphatidylinositol 3′-kinase-dependent Lyn/Tec/ Dok-1 complex formation in hematopoietic cells. Blood 96: 3406-3413
126. Liang X., Wisniewski D., Strife A., Shivakrupa, Clarkson B. and Resh M. D. (2002) Phosphatidylinositol 3-kinase and Src family kinases are required for phosphorylation and membrane recruitment of Dok-1 in c-Kit signaling. J. Biol. Chem. 277: 13732-13738
127. Kim L. and Wong T. W. (1995) The cytoplasmic tyrosine kinase FER is associated with the catenin-like substrate pp120 and is activated by growth factors. Mol. Cell. Biol. 15: 4553-4561
128. Craig A. W. and Greer P. A. (2002) Fer kinase is required for sustained p38 kinase activation and maximal chemotaxis of activated mast cells. Mol. Cell. Biol. 22: 6363-6374
129. Masuhara M., Nagao K., Nishikawa M., Sasaki M., Yoshimura A. and Osawa M. (2000) Molecular cloning of murine STAP-1, the stem-cell-specific adaptor protein containing PH and SH2 domains. Biochem. Biophys. Res. Commun. 268: 697-703
130. Pawson T. and Scott J. D. (1997) Signaling through scaffold, anchoring and adaptor proteins. Science 278: 2075-2080
131. Liu S. K., Berry D. M. and McGlade C. J. (2001) The role of Gads in hematopoietic cell signalling. Oncogene 20: 6284-6290
132. Liu S. K. and McGlade C. J. (1998) Gads is a novel SH2 and SH3 domain-containing adaptor protein that binds to tyrosine-phosphorylated Shc Oncogene. 17: 3073-3082
133. Feng G. S., Ouyang Y. B., Hu D. P., Shi Z. Q., Gentz R. and Ni J. (1996) Grap is a novel SH3-SH2-SH3 adaptor protein that couples tyrosine kinases to the Ras pathway. J. Biol. Chem. 271: 12129-12132
134. Ravichandran K. S. (2001) Signaling via Shc family adapter proteins. Oncogene 20: 6322-6330
135. Han D. C., Shen T. L. and Guan J. L. (2001) The Grb7 family proteins: structure, interactions with other signaling molecules and potential cellular functions. Oncogene 20: 6315-6321
136. Jahn T., Seipel P., Urschel S., Peschel C. and Duyster J. (2002) Role for the adaptor protein Grb10 in the activation of Akt. Mol. Cell. Biol. 22: 979-991
137. Iseki M., Takaki S. and Takatsu K. (2000) Molecular cloning of the mouse APS as a member of the Lnk family adaptor proteins. Biochem. Biophys. Res. Commun. 272: 45-54
138. Takaki S., Sauer K., Iritani B. M., Chien S., Ebihara Y., Tsuji K. et al. (2000) Control of B cell production by the adaptor protein Ink. Definition of a conserved family of signal-modulating proteins. Immunity 13: 599-609
139. Yokouchi M., Suzuki R., Masuhara M., Komiya S., Inoue A. and Yoshimura A. (1997) Cloning and characterization of APS, an adaptor molecule containing PH and SH2 domains that is tyrosine phosphorylated upon B-cell receptor stimulation. Oncogene 15: 7-15
140. Wakioka T., Sasaki A., Mitsui K., Yokouchi M., Inoue A., Komiya S. et al. (1999) APS, an adaptor protein containing Pleckstrin homology (PH) and Src homology-2 (SH2) domains, inhibits the JAK-STAT pathway in collaboration with c-Cbl. Leukemia 13: 760-767
141. Yokouchi M., Wakioka T., Sakamoto H., Yasukawa H., Ohtsuka S., Sasaki A. et al. (1999) APS, an adaptor protein containing PH and SH2 domains, is associated with the PDGF receptor and c-Cbl and inhibits PDGF-induced mitogenesis. Oncogene 18: 759-767
142. Hu J., Liu J., Ghirlando R., Saltiel A. R. and Hubbard S. R. (2003) Structural basis for recruitment of the adaptor protein APS to the activated insulin receptor. Mol. Cell. 12: 1379-1389
143. Herbst R., Munemitsu S. and Ullrich A. (1995) Oncogenic activation of v-kit involves deletion of a putative tyrosine-substrate interaction site. Oncogene 10: 369-379
144. Peschard P. and Park M. (2003) Escape from Cbl-mediated downregulation: a recurrent theme for oncogenic deregulation of receptor tyrosine kinases. Cancer Cell 3: 519-523
145. Iseki M., Kubo C., Kwon S. M., Yamaguchi A., Kataoka Y., Yoshida N. et al. (2004) Increased numbers of B-1 cells and enhanced responses against TI-2 antigen in mice lacking APS, an adaptor molecule containing PH and SH2 domains. Mol. Cell. Biol. 24: 2243-2250
146. Kubo-Akashi C., Iseki M., Kwon S. M., Takizawa H., Takatsu K. and Takaki S. (2004) Roles of a conserved family of adaptor proteins, Lnk, SH2-B and APS, for mast cell development, growth and functions: APS-deficiency causes augmented degranulation and reduced actin assembly. Biochem. Biophys. Res. Commun. 315: 356-362
147. Feller S. M. (2001) Crk family adaptors-signalling complex formation and biological roles. Oncogene 20: 6348-6371
148. Prosser S., Sorokina E., Pratt P. and Sorokin A. (2003) CrkIII: a novel and biologically distinct member of the Crk family of adaptor proteins. Oncogene 22: 4799-4806
149. Ellis C., Moran M., McCormick F. and Pawson T. (1990) Phosphorylation of GAP and GAP-associated proteins by transforming and mitogenic tyrosine kinases. Nature 343: 377-381
150. Yamanashi Y., Tamura T., Kanamori T., Yamane H., Nariuchi H., Yamamoto T. et al. (2000) Role of the rasGAP-associated docking protein p62(dok) in negative regulation of B cell receptor-mediated signaling. Genes Dev. 14: 11-16
151. Carpino N., Wisniewski D., Strife A., Marshak D., Kobayashi R., Stillman B. et al. (1997) p62(dok): a constitutively tyrosine-phosphorylated, GAP-associated protein in chronic myelogenous leukemia progenitor cells. Cell 88: 197-204
152. Gu H. and Neel B. G. (2003) The 'Gab' in signal transduction. Trends Cell Biol. 13: 122-130
153. Nishida K., Yoshida Y., Itoh M., Fukada T., Ohtani T., Shirogane T. et al. (1999) Gab-family adapter proteins act downstream of cytokine and growth factor receptors and T- and B-cell antigen receptors. Blood 93: 1809-1816
154. Nishida K., Wang L., Morii E., Park S. J., Narimatsu M., Itoh S. et al. (2002) Requirement of Gab2 for mast cell development and KitL/c-Kit signaling. Blood 99: 1866-1869
155. Neel B. G., Gu H. and Pao L. (2003) The 'Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem. Sci. 28: 284-293
156. Rönnstrand L., Arvidsson A. K., Kallin A., Rorsman C., Hellman U., Engström U. et al. (1999) SHP-2 binds to Tyr763 and Tyr1009 in the PDGF beta-receptor and mediates PDGF-induced activation of the Ras/MAP kinase pathway and chemotaxis. Oncogene 18: 3696-3702
157. Chan R. J., Johnson S. A., Li Y., Yoder M. C. and Feng G. S. (2003) A definitive role of Shp-2 tyrosine phosphatase in mediating embryonic stem cell differentiation and hematopoiesis. Blood 102: 2074-2080
158. Taniguchi Y., London R., Schinkmann K., Jiang S. and Avraham H. (1999) The receptor protein tyrosine phosphatase, PTP-RO, is upregulated during megakaryocyte differentiation and Is associated with the c-Kit receptor. Blood 94: 539-549
159. Perez-Losada J., Sanchez-Martin M., Rodriguez-Garcia A., Sanchez M. L., Orfao A., Flores T. et al. (2002) Zinc-finger transcription factor Slug contributes to the function of the stem cell factor c-kit signaling pathway. Blood 100: 1274-1286
160. Perez-Losada J., Sanchez-Martin M., Perez-Caro M., Perez-Mancera P. A. and Sanchez-Garcia I. (2003) The radioresistance biological function of the SCF/kit signaling pathway is mediated by the zinc-finger transcription factor Slug. Oncogene 22: 4205-4211
161. Hodgkinson C. A., Moore K. J., Nakayama A., Steingrimsson E., Copeland N. G., Jenkins N. A. et al. (1993) Mutations at the mouse microphthalmia locus are associated with defects in a gene encoding a novel basic-helix-loop-helix- zipper protein. Cell 74: 395-404
162. Hughes M. J., Lingrel J. B., Krakowsky J. M. and Anderson K. P. (1993) A helix-loop-helix transcription factor-like gene is located at the mi locus. J. Biol. Chem. 268: 20687-20690
163. Boissy R. E. and Nordlund J. J. (1997) Molecular basis of congenital hypopigmentary disorders in humans: a review. Pigment Cell Res. 10: 12-24
164. Hemesath T. J., Price E. R., Takemoto C., Badalian T. and Fisher D. E. (1998) MAP kinase links the transcription factor Microphthalmia to c-Kit signalling in melanocytes. Nature 391: 298-301
165. Wu M., Hemesath T. J., Takemoto C. M., Horstmann M. A., Wells A. G., Price E. R. et al. (2000) c-Kit triggers dual phosphorylations, which couple activation and degradation of the essential melanocyte factor Mi. Genes Dev. 14: 301-312
166. Weilbaecher K. N., Motyckova G., Huber W. E., Takemoto C. M., Hemesath T. J.. Xu Y. et al. (2001) Linkage of M-CSF signaling to Mitf, TFE3, and the osteoclast defect in Mitf(mi/mi) mice. Mol. Cell. 8: 749-758
167. Price E. R., Ding H. F., Badalian T., Bhattacharya S., Takemoto C., Yao T. P, et al. (1998) Lineage-specific signaling in melanocytes. C-kit stimulation recruits p300/CBP to microphthalmia. J. Biol. Chem. 273: 17983-17986