The aberrant localization of oncogenic kit tyrosine kinase receptor mutants is reversed on specific inhibitory treatment

Molecular Cancer Research

Volumn 7, Issue 9, 2009, Pages 1525-1533

  Bougherara, Houcine ^a   Subra, Frédéric ^a   Crépin, Ronan ^a   Tauc, Patrick ^a   Auclair, Christian ^a   Poul, Marie Alix ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DASATINIB; ENHANCED GREEN FLUORESCENT PROTEIN; IMATINIB; MANNOSE; MUTANT PROTEIN; STEM CELL FACTOR; STEM CELL FACTOR RECEPTOR; TYROSINE KINASE RECEPTOR;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL STIMULATION; CELL SURFACE; CELLULAR DISTRIBUTION; CHIMERA; CHO CELL; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; GENE MUTATION; GLYCOSYLATION; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; CHO CELLS; CLONING, MOLECULAR; CRICETINAE; CRICETULUS; FLOW CYTOMETRY; GLYCOSYLATION; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SPACE; MUTATION; PIPERAZINES; PROTEIN KINASE INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-KIT; PYRIMIDINES; RECOMBINANT FUSION PROTEINS; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; THIAZOLES;

CRICETULUS GRISEUS;

EID: 70349507344     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-09-0138     Document Type: Article

References (56)

1. Yarden Y, Kuang WJ, Yang-Feng T, et al. Human proto-oncogene c-kit: a new cell surface receptor tyrosine kinase for an unidentified ligand. EMBO J 1987;6:3341-3351
2. Roskoski R, Jr. Structure and regulation of Kit protein-tyrosine kinase-the stem cell factor receptor. Biochem Biophys Res Commun 2005;338:1307-1315 (Pubitemid 41608395)
3. Hirota S, Isozaki K, Moriyama Y, et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 1998;279:577-580 (Pubitemid 28067289)
4. Andersson J, Sjogren H, Meis-Kindblom JM, Stenman G, Aman P, Kindblom LG. The complexity of KIT gene mutations and chromosome rearrangements and their clinical correlation in gastrointestinal stromal (pacemaker cell) tumors. Am J Pathol 2002;160:15-22. (Pubitemid 34052260)
5. Strohmeyer T, Reese D, Press M, Ackermann R, Hartmann M, Slamon D. Expression of the c-kit proto-oncogene and its ligand stem cell factor (SCF) in normal and malignant human testicular tissue. J Urol 1995;153:511-515
6. Heinrich MC, Rubin BP, Longley BJ, Fletcher JA. Biology and genetic aspects of gastrointestinal stromal tumors: KIT activation and cytogenetic alterations. Hum Pathol 2002;33:484-495
7. Sekido Y, Obata Y, Ueda R, et al. Preferential expression of c-kit protooncogene transcripts in small cell lung cancer. Cancer Res 1991;51:2416-2419
8. Toyota M, Hinoda Y, Takaoka A, et al. Expression of c-kit and kit ligand in human colon carcinoma cells. Tumour Biol 1993;14:295-302. (Pubitemid 23357718)
9. Beck D, Gross N, Brognara CB, Perruisseau G. Expression of stem cell factor and its receptor by human neuroblastoma cells and tumors. Blood 1995;86:3132-3138
10. Hines SJ, Organ C, Kornstein MJ, Krystal GW. Coexpression of the c-kit and stem cell factor genes in breast carcinomas. Cell Growth Differ 1995;6:769-779
11. Krystal GW, Hines SJ, Organ CP. Autocrine growth of small cell lung cancer mediated by coexpression of c-kit and stem cell factor. Cancer Res 1996;56:370-376 (Pubitemid 26026367)
12. Kitamura Y, Hirotab S. Kit as a human oncogenic tyrosine kinase. Cell Mol Life Sci 2004;61:2924-2931 (Pubitemid 40104590)
13. Orfao A, Garcia-Montero AC, Sanchez L, Escribano L. Recent advances in the understanding of mastocytosis: the role of KIT mutations. Br J Haematol 2007;138:12-30. (Pubitemid 46889785)
14. Mol CD, Lim KB, Sridhar V, et al. Structure of a c-kit product complex reveals the basis for kinase transactivation. J Biol Chem 2003;278:31461-31464 (Pubitemid 37048320)
15. Kitayama H, Kanakura Y, Furitsu T, et al. Constitutively activating mutations of c-kit receptor tyrosine kinase confer factor-independent growth and tumorigenicity of factor-dependent hematopoietic cell lines. Blood 1995;85:790-798
16. Tsujimura T, Hashimoto K, Kitayama H, et al. Activating mutation in the catalytic domain of c-kit elicits hematopoietic transformation by receptor self-association not at the ligand-induced dimerization site. Blood 1999;93:1319-1329 (Pubitemid 29076147)
17. Weinstein IB, Begemann M, Zhou P, et al. Disorders in cell circuitry associated with multistage carcinogenesis: exploitable targets for cancer prevention and therapy. Clin Cancer Res 1997;3:2696-2702 (Pubitemid 28133129)
18. Engelman JA, Settleman J. Acquired resistance to tyrosine kinase inhibitors during cancer therapy. Curr Opin Genet Dev2008;18:73-79
19. Druker BJ, Tamura S, Buchdunger E, et al. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med 1996;2:561-566 (Pubitemid 26151518)
20. Heinrich MC, Griffith DJ, Druker BJ, Wait CL, Ott KA, Zigler AJ. Inhibition of c-kit receptor tyrosine kinase activity by STI 571, a selective tyrosine kinase inhibitor. Blood 2000;96:925-932
21. Joensuu H, Roberts PJ, Sarlomo-Rikala M, et al. Effect of the tyrosine kinase inhibitor STI571 in a patient with a metastatic gastrointestinal stromal tumor. N Engl J Med 2001;344:1052-1056 (Pubitemid 32267975)
22. Cassier PA, Dufresne A, Arifi S, et al. Imatinib mesilate for the treatment of gastrointestinal stromal tumour. Expert Opin Pharmacother 2008;9:1211-1222 (Pubitemid 351721757)
23. Ma Y, Zeng S, Metcalfe DD, et al. The c-KIT mutation causing human mastocytosis is resistant to STI571 and other KIT kinase inhibitors; kinases with enzymatic site mutations show different inhibitor sensitivity profiles than wild-type kinases and those with regulatory-type mutations. Blood 2002;99:1741-1744 (Pubitemid 34533049)
24. Frost MJ, Ferrao PT, Hughes TP, Ashman LK. Juxtamembrane mutant V560GKit is more sensitive to imatinib (STI571) compared with wild-type c-kit whereas the kinase domain mutant D816VKit is resistant. Mol Cancer Ther 2002;1:1115-1124
25. Carter TA, Wodicka LM, Shah NP, et al. Inhibition of drug-resistant mutants of ABL, KIT, EGF receptor kinases. Proc Natl Acad Sci U S A 2005;102:11011-11016
26. Heinrich MC, Corless CL, Blanke CD, et al. Molecular correlates of imatinib resistance in gastrointestinal stromal tumors. J Clin Oncol 2006;24:4764-4774 (Pubitemid 46630941)
27. Schittenhelm MM, Shiraga S, Schroeder A, et al. Dasatinib (BMS-354825), a dual SRC/ABL kinase inhibitor, inhibits the kinase activity of wild-type, juxtamembrane, and activation loop mutant KIT isoforms associated with human malignancies. Cancer Res 2006;66:473-481 (Pubitemid 43166056)
28. Emens LA. Trastuzumab: targeted therapy for the management of HER-2/neu-overexpressing metastatic breast cancer. Am J Ther 2005;12:243-253 (Pubitemid 40825130)
29. Grillo-Lopez AJ. Rituximab (Rituxan/MabThera): the first decade (1993-2003). Expert Rev Anticancer Ther 2003;3:767-779
30. Wilkins DK, Mayer A. Development of antibodies for cancer therapy. Expert Opin Biol Ther 2006;6:787-796
31. Furitsu T, Tsujimura T, Tono T, et al. 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 1993;92:1736-1744 (Pubitemid 23304537)
32. Chian R, Young S, Danilkovitch-Miagkova A, et al. Phosphatidylinositol 3 kinase contributes to the transformation of hematopoietic cells by the D816V c-Kit mutant. Blood 2001;98:1365-1373
33. Moriyama Y, Tsujimura T, Hashimoto K, et al. Role of aspartic acid 814 in the function and expression of c-kit receptor tyrosine kinase. J Biol Chem 1996;271:3347-3350 (Pubitemid 26065636)
34. Crosier PS, Ricciardi ST, Hall LR, Vitas MR, Clark SC, Crosier KE. Expression of isoforms of the human receptor tyrosine kinase c-kit in leukemic cell lines and acute myeloid leukemia. Blood 1993;82:1151-1158
35. Piao X, Curtis JE, Minkin S, Minden MD, Bernstein A. Expression of the Kit and KitA receptor isoforms in human acute myelogenous leukemia. Blood 1994;83:476-481 (Pubitemid 2022486)
36. Ronnstrand L. Signal transduction via the stem cell factor receptor/c-Kit. Cell Mol Life Sci 2004;61:2535-2548 (Pubitemid 39586516)
37. Sun J, Pedersen M, Ronnstrand L. GAB2 is involved in differential pi3-kinase signaling by two splice forms of C-kit. J Biol Chem 2008;283:27444-27451
38. Jahn T, Seipel P, Coutinho S, et al. Analysing c-kit internalization using a functional c-kit-EGFP chimera containing the fluorochrome within the extracellular domain. Oncogene 2002;21:4508-4520 (Pubitemid 34785727)
39. Majumder S, Brown K, Qiu FH, Besmer P. c-kit protein, a transmembrane kinase: identification in tissues and characterization. Mol Cell Biol 1988;8:4896-4903 (Pubitemid 18261564)
40. Lev S, Givol D, Yarden Y. Interkinase domain of kit contains the binding site for phosphatidylinositol 3′ kinase. Proc Natl Acad Sci U S A 1992;89:678-682
41. Serve H, Hsu YC, 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 1994;269:6026-6030 (Pubitemid 24242986)
42. Tsujimura T, Furitsu T, Morimoto M, et al. Ligand-independent activation of c-kit receptor tyrosine kinase in a murine mastocytoma cell line P-815 generated by a point mutation. Blood 1994;83:2619-2626 (Pubitemid 24135855)
43. Tsujimura T, Morimoto M, Hashimoto K, et al. Constitutive activation of c-kit in FMA3 murine mastocytoma cells caused by deletion of seven amino acids at the juxtamembrane domain. Blood 1996;87:273-283 (Pubitemid 26011841)
44. Helenius A, Aebi M. Intracellular functions of N-linked glycans. Science 2001;291:2364-2369
45. Tabone-Eglinger S, Subra F, El Sayadi H, et al. KIT mutations induce intracellular retention and activation of an immature form of the KIT protein in gastrointestinal stromal tumors. Clin Cancer Res 2008;14:2285-2294 (Pubitemid 351551059)
46. Xiang Z, Kreisel F, Cain J, Colson A, Tomasson MH. Neoplasia driven by mutant c-KIT is mediated by intracellular, not plasma membrane, receptor signaling. Mol Cell Biol 2007;27:267-282 (Pubitemid 46013250)
47. Agaram NP, Laquaglia MP, Ustun B, et al. Molecular characterization of pediatric gastrointestinal stromal tumors. Clin Cancer Res 2008;14:3204-3215
48. Sun J, Pedersen M, Ronnstrand L. The D816V mutation of c-Kit circumvents a requirement for Src family kinases in c-Kit signal transduction. J Biol Chem 2009;284:11039-11047
49. Voisset E, Lopez S, Dubreuil P, De Sepulveda P. The tyrosine kinase FES is an essential effector of KITD816V proliferation signal. Blood 2007;110:2593-2599 (Pubitemid 47523183)
50. Koch S, Jacobi A, Ryser M, Ehninger G, Thiede C. Abnormal localization and accumulation of FLT3-ITD, a mutant receptor tyrosine kinase involved in leukemogenesis. Cells Tissues Organs 2008;188:225-235 (Pubitemid 351962245)
51. Schmidt-Arras D, Bohmer SA, Koch S, et al. Anchoring of FLT3 in the endoplasmic reticulum alters signaling quality. Blood 2009;113:3568-3576
52. Clarke ID, Dirks PB. A human brain tumor-derived PDGFR-α deletion mutant is transforming. Oncogene 2003;22:722-733
53. Broudy VC, Lin NL, Buhring HJ, Komatsu N, Kavanagh TJ. Analysis of c-kit receptor dimerization by fluorescence resonance energy transfer. Blood 1998;91:898-906. (Pubitemid 28078292)
54. Theou N, Tabone S, Saffroy R, et al. High expression of both mutant and wild-type alleles of c-kit in gastrointestinal stromal tumors. Biochim Biophys Acta 2004;1688:250-256 (Pubitemid 38438529)
55. Shah NP, Lee FY, Luo R, Jiang Y, Donker M, Akin C. Dasatinib (BMS-354825) inhibits KITD816V, an imatinib-resistant activating mutation that triggers neoplastic growth in most patients with systemic mastocytosis. Blood 2006;108:286-291 (Pubitemid 43990640)
56. Scaltriti M, Verma C, Guzman M, et al. Lapatinib, a HER2 tyrosine kinase inhibitor, induces stabilization and accumulation of HER2 and potentiates trastuzumab-dependent cell cytotoxicity. Oncogene 2009;28:803-814