Activating mutation in the catalytic domain of C-kit elicits hematopoietic transformation by receptor self-association not at the ligand- induced dimerization site

Blood

Volumn 93, Issue 4, 1999, Pages 1319-1329

  Tsujimura, Tohru ^b   Hashimoto, Koji ^b   Kitayama, Hitoshi ^b   Ikeda, Hirokazu ^b   Sugahara, Hiroyuki ^b   Matsumura, Itaru ^b   Kaisho, Tsuneyasu ^b   Terada, Nobuyuki ^b   Kitamura, Yukihiko ^b   Kanakura, Yuzuru ^a  

^a OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

STEM CELL FACTOR;

ARTICLE; CARCINOGENICITY; DIMERIZATION; GROWTH REGULATION; HEMATOLOGIC DISEASE; HEMATOPOIESIS; HUMAN; HUMAN CELL; LIGAND BINDING; ONCOGENE C KIT; PRIORITY JOURNAL; PROTO ONCOGENE;

EID: 0033557589     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood.v93.4.1319     Document Type: Article

References (55)

1. Qiu F, Ray P, Brown K, Barker PE, Jhanwar S, Ruddle FH, Besmer P: Primary structure of c-kit: Relationship with the CSF-1/ PDGF receptor kinase family - Oncogenic activation of v-kit involves deletion of extracellular domain and C terminus. EMBO J 7:1003, 1988
2. Yarden Y, Kuang WJ, Yang-Feng T, Coussens L, Munemitsu S, Dull TJ, Chen E, Schlessinger J, Francke U, Ullrich A: Human proto-oncogene c-kit: A new cell surface receptor tyrosine kinase for an unidentified ligand. EMBO J 6:3341, 1987
3. Yarden Y, Ullrich A: Growth factor receptor tyrosine kinase. Annu Rev Biochem 57:443, 1988
4. Ullrich A, Schlessinger J: Signal transduction by receptors with tyrosine kinase activity. Cell 61:203, 1990
5. Fantl WJ, Johnson DE, Williams LT: Signalling by receptor tyrosine kinases. Annu Rev Biochem 62:453, 1993
6. Reith AD, Bernstein A: Molecular biology of the W and Steel Loci, in Davis KE, Tilghman S (eds): Genes and Phenotypes, vol 3. New York, NY, Cold Spring Harbor Laboratory, 1991, p 105
7. Zsebo KM, Williams DA, Geissler EN, Broudy VC, Martin FH, Atkins HL, Hsu RY, Birkett NC, Okino KH, Murdock DC, Jacobson FW, Langley KE, Smith KA, Takeishi T, Cattanach BM, Galli SJ, Suggs SV: Stem cell factor is encoded at the Sl locus of the mouse and is the ligand for the c-kit tyrosine kinase receptor. Cell 63:213, 1990
8. Williams DE, Eisenman J, Baird A, Rauch C, Ness KV, March CJ, Park LS, Martin U, Mochizuki DY, Boswell HS, Burgess GS, Cosman D, Lyman SD: Identification of ligand for the c-kit proto-oncogene. Cell 63:167, 1990
9. Huang E, Nocka K, Beier DR, Chu TY, Buck J, Lahm HW, Wellner D, Leder P, Besmer P: The hematopoietic growth factor KL is encoded by the Sl locus and is the ligand of the c-kit receptor, the gene product of the W locus. Cell 63:225, 1990
10. Flanagan JG, Leder P: The kit ligand: A cell surface molecule altered in steel mutant fibroblasts. Cell 63:185, 1990
11. Rottapel R, Reedijk M, Williams DE, Lyman SD, Anderson DM, Pawson T, Bernstein A: The steel/W transduction pathway: Kit autophosphorylation and its association with a unique subset of cytoplasmic signaling proteins is induced by the steel factor. Mol Cell Biol 11:3043, 1991
12. Reith AD, Ellis C, Lyman SD, Anderson DM, Williams DE, Bernstein A, Pawson T: Signal transduction by normal isoforms and W mutant variants of the Kit receptor tyrosine kinase. EMBO J 10:2451, 1991
13. Lev S, Givol D, Yarden Y: Interkinase domain of kit contains the binding site for phosphatidylinositol 3' kinase. Proc Natl Acad Sci USA 89:678, 1992
14. Yi T, Ihle JN: Association of hematopoietic cell phosphatase with c-Kit after stimulation with c-Kit ligand. Mol Cell Biol 13:3350, 1993
15. Serve H, Hsu Y-C, Besmer P: Tyrosine residue 719 of the c-kit receptor is essential for binding of the P85 subunit of phosphatidylinositol (PI) 3-kinase and for c-kit-associated PI 3-kinase activity in COS-1 cells. J Biol Chem 269:6026, 1994
16. Huizinga JD, Thuneberg L, Klffippel M, Malysz J, Mikkelsen HB, Bernstein A: W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature 373:347, 1995
17. Furitsu T, Tsujimura T, Tono T, Ikeda H, Kitayama H, Koshimizu U, Sugahara H, Butterfield JH, Ashman LK, Kanayama Y, Matsuzawa Y, Kitamura Y, Kanakura Y: Identification of mutations in the coding sequence of the proto-oncogene c-kit in a human mast cell leukemia cell line causing ligand-independent activation of c-kit product. J Clin Invest 92:1736, 1993
18. Tsujimura T, Furitsu T, Morimoto M, Kanayama Y, Nomura S, Matsuzawa Y, Kitamura Y, Kanakura Y: Substitution of an aspartic acid results in constitutive activation of c-kit receptor tyrosine kinase in a rat tumor mast cell line RBL-2H3. Int Arch Allergy Immunol 106:377, 1995
19. Tsujimura T, Furitsu T, Morimoto M, Isozaki K, Nomura S, Matsuzawa Y, Kitamura Y, Kanakura Y: Ligand-independent activation of c-kit receptor tyrosine kinase in a murine mastocytoma cell line P-815 generated by a point mutation. Blood 83:2619, 1994
20. Tsujimura T, Morimoto M, Hashimoto K, Moriyama Y, Kitayama H, Matsuzawa Y, Kitamura Y, Kanakura Y: Constitutive activation of c-kit in FMA3 murine mastocytoma cells caused by deletion of seven amino acids at the juxtamembrane domain. Blood 87:273, 1996
21. Kitayama H, Kanakura Y, Furitsu T, Tsujimura T, Oritani K, Ikeda H, Sugahara H, Mitsui H, Kanayama Y, Kitamura Y, Matsuzawa Y: Constitutively activating mutations of c-kit receptor tyrosine kinase confer factor-independent growth and tumorigenicity of factor-dependent hematopoietic cell lines. Blood 85:790, 1995
22. Hashimoto K, Tsujimura T, Moriyama Y, Yamatodani A, Kimura M, Tohya K, Morimoto M, Kitayama H, Kanakura Y, Kitamura Y: Transforming and differentiation-inducing potentials of constitutively activated c-kit mutant genes in the IC-2 murine interleukin-3 - dependent mast cell line. Am J Pathol 148:189, 1996
23. Kitayama H, Tsujimura T, Matsumura I, Oritani K, Ikeda H, Ishikawa J, Okabe M, Suzuki M, Yamamura K-I, Matsuzawa Y, Kitamura Y, Kanakura Y: Neoplastic transformation of normal hematopoietic cells by constitutively activating mutations of c-kit receptor tyrosine kinase. Blood 88:995, 1996
24. Nagata H, Worobec AS, Oh CK, Chowdhury BA, Tannenbaum S, Suzuki Y, Metcalfe DD: 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, 1995
25. Longley BJ, Tyrrell L, Lu S-Z, Ma Y-S, Langley K, Ding T, Duffy T, Jacobs P, Tang LH, Modlin I: Somatic c-KIT activating mutation in urticaria pigmentosa and aggressive mastocytosis: Establishment of clonality in a human mast cell neoplasm. Nat Genet 12:312, 1996
26. Ferrao P, Gonda TJ, Ashman LK: Expression of constitutively activated human c-kit in myb transformed early myeloid cells leads to factor independence, histiocytic differentiation, and tumorigenicity. Blood 90:4539, 1997
27. Hirota S, Isozaki K, Moriyama Y, Hashimoto K, Nishida T, Ishiguro S, Kawano K, Hanada M, Kurata A, Takeda M, Tunio GM, Matsuzawa Y, Kanakura Y, Shinomura Y, Kitamura Y: Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 279:577, 1998
28. Schlessinger J, Ullrich A: Growth factor signaling by receptor tyrosine kinase. Neuron 9:383, 1992
29. Blechman JM, Yarden Y: Structural aspects of receptor dimerization: c-Kit as an example. Ann NY Acad Sci 766:344, 1995
30. Lev S, Yarden Y, Givol D: A recombinant ectodomain of the receptor for the stem cell factor (SCF) retains ligand-induced receptor dimerization and antagonizes SCF-stimulated cellular responses. J Biol Chem 267:10866, 1992
31. Lev S, Blechman JM, Nishikawa S-I, Givol D, Yarden Y: Interspecies molecular chimeras of Kit help define the binding site of the stem cell factor. Mol Cell Biol 13:2224, 1993
32. Blechman JM, Lev S, Barg J, Eisenstein M, Vaks B, Vogel Z, Givol D, Yarden Y: The fourth immunoglobulin domain of the stem cell factor receptor couples ligand binding to signal transduction. Cell 80:101, 1995
33. Ogawa M, Matsuzaki Y, Nishikawa S, Hayashi S-I, Kunisada T, Nakauchi H, Nishikawa S-I: Expression and function of c-kit in hematopoietic progenitor cells. J Exp Med 174:63, 1991
34. Coussens L, Van Beveren C, Smith D, Chen E, Mitchell RL, Isacke CM, Verma IM, Ullrich A: Structural alteration of viral homologue of receptor proto-oncogene fms at carboxyl terminus. Nature 320:277, 1986
35. Roussel MF, Dull TJ, Rettenmier CW, Ralph P, Ullrich A, Sherr CJ: Transforming potential of the c-fms proto-oncogene (CSF-1 receptor). Nature 325:549, 1987
36. Reith AD, Rottapel R, Giddens E, Brady C, Forrester L, Bernstein A: W mutant mice with mild or severe developmental defects contain distinct point mutations in the kinase domain of the c-kit receptor. Genes Dev 4:390, 1990
37. Graham FL, Smith J, Russell WC, Nairn R: Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol 36:59, 1977
38. 42 spotting phenotype results from a missense mutation in the c-kit receptor kinase. Science 247:209, 1990
39. Mizushima S, Nagata S: pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res 18:5322, 1990
40. Moriyama Y, Tsujimura T, Hashimoto K, Morimoto M, Kitayama H, Matsuzawa Y, Kitamura Y, Kanakura Y: Role of aspartic acid 814 in the function and expression of c-kit receptor tyrosine kinase. J Biol Chem 271:3347, 1996
41. Tsujimura T, Koshimizu U, Katoh H, Isozaki K, Kanakura Y, Tono T, Adachi S, Kasugai T, Tei H, Nishimune Y, Nomura S, Kitamura Y: Mast cell number in the skin of heterozygotes reflects the molecular nature of c-kit mutation. Blood 81:2530, 1993
42. Kanakura Y, Druker B, Cannistra SA, Furukawa Y, Torimoto Y, Griffin JD: Signal transduction of the human granulocyte-macrophage colony-stimulating factor and interleukin-3 receptors involves tyrosine phosphorylation of a common set of cytoplasmic proteins. Blood 76:706, 1990
43. Majumder S, Brown K, Qiu FH, Besmer P: c-kit protein, a transmembrane kinase: Identification in tissues and characterization. Mol Cell Biol 8:4896, 1988
44. Tsujimura T, Morii E, Nozaki M, Hashimoto K, Moriyama Y, Takebayashi K, Kondo T, Kanakura Y, Kitamura Y: Involvement of transcription factor encoded by the mi locus in the expression of c-kit receptor tyrosine kinase in cultured mast cells of mice. Blood 88:1225, 1996
45. Tsujimura T, Hashimoto K, Morii E, Tunio GM, Tsujino K, Kondo T, Kanakura Y, Kitamura Y: Involvement of transcription factor encoded by the mouse mi locus (MITF) in apoptosis of cultured mast cells induced by removal of interleukin-3. Am J Pathol 151:1043, 1997
46. Lemmon MA, Pinchasi D, Zhou M, Lax I, Schlessinger J: Kit receptor dimerization is driven by bivalent binding of stem cell factor. J Biol Chem 272:6311, 1997
47. Khazaie K, Dull TJ, Graf T, Schlessinger J, Ullrich A, Beug H, Vennström B: Truncation of the human EGF receptor leads to differential transforming potentials in primary avian fibroblasts and erthroblasts. EMBO J 7:3061, 1988
48. Uren A, Yu JC, Karcaaltincaba M, Pierce JH, Heidaran MA: Oncogenic activation of the αPDGFR defines a domain that negatively regulates receptor dimerization. Oncogene 14:157, 1997
49. Besmer P, Murphy JE, George PC, Qiu F, Bergold PJ, Lederman L, Snyder HW, Brodeur D, Zuckerman EE, Hardy WD: A new acute transforming feline retrovirus and relationship of its oncogene v-kit with the protein kinase gene family. Nature 320:415, 1986
50. Herbst R, Munemitsu S, Ullrich A: Oncogenic activation of v-kit involves deletion of a putative tyrosine-substrate interaction site. Oncogene 10:369, 1995
51. c-neu and epidermal growth factor receptor tyrosine kinase: Oligomerization of kinase domains. Proc Natl Acad Sci USA 93:6252, 1996
52. Piao X, Paulson R, van der Geer P, Pawson T, Bernstein A: Oncogenic mutation in the Kit receptor tyrosine kinase alters substrate specificity and induces degradation of the protein tyrosine phosphatase SHP-1. Proc Natl Acad Sci USA 93:14665, 1996
53. Klingmffiller U, Lorenz U, Cantley LC, Neel BG, Lodish HF: Specific recruitment of SH-PTP1 to the erythropoietin receptor causes inactivation of JAK2 and termination of proliferative signals. Cell 80:729, 1995
54. Yi T, Mui AL, Krystal G, Ihle JN: Hematopoietic cell phosphatase associates with the interleukin-3 (IL-3) receptor β chain and down-regulates IL-3 - induced tyrosine phosphorylation and mitogenesis. Mol Cell Biol 13:7577, 1993
55. Paulson RF, Vesely S, Siminovitch KA, Bernstein A: Signalling by the W/Kit receptor tyrosine kinase is negatively regulated in vivo by the protein tyrosine phosphatase Shp1. Nat Genet 13:309, 1996