The involvement of Bcr in leukemias with the Philadelphia chromosome

Critical Reviews in Oncogenesis

Volumn 9, Issue 1, 1998, Pages 1-18

  Arlinghaus, Ralph B ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Bcr protein; Bcr serine threonine kinase inhibition; Bcr Abl oncoprotein; C Abl; Chronic phase CML; Inhibition of Bcr Abl; Philadelphia chromosome; Signal transduction

Indexed keywords

BCR ABL PROTEIN; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; RAS PROTEIN;

AUTOPHOSPHORYLATION; CELL DEATH; CHRONIC MYELOID LEUKEMIA; ENZYME ACTIVITY; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE FUSION; GROWTH INHIBITION; MITOGENESIS; ONCOGENE; ONCOGENE RAS; PHILADELPHIA 1 CHROMOSOME; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

EID: 0031720660     PISSN: 08939675     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevOncog.v9.i1.10     Document Type: Review

References (97)

1. Annamalai, A. E. and R. F. Colman: Reaction of the adenine nucleotide analogue 5′-p-fluorosulfonylbenzoyl adenosine at distinct tyrosine and cysteine residues of rabbit muscle pyruvate kinase. J. Biol. Chem., 256:10276-10283(1981).
2. Beran, M., P. Pisa, S. O'Brien, R. Kurzrock, M. Siciliano, A. Cork, B. S. Andersson, V. Kohli, and H. Kantarjian: Biological properties and growth in SCID mice of a new myelogenous leukemia cell line (KBM-5) derived from chronic myelogenous leukemia in blast phase. Cancer Res., 53:3603-3610 (1993).
3. Baskaran, R., L. D. Wood, L. L. Whitaker, C. E. Canman, S. E. Morgan, Y. Wu, C. Barlow, D. Baltimore, A. Wynshaw-Boris, and M. B. Kastam: Ataxia telangiectasia mutant protein activates c-Abl tyrosine kinase in response to ionizing radiation. Nature, 387:516-519 (1997).
4. Bedi, A., B. A. Zehnbauer, J. P. Barber, S. J. Sharkis, and R. J. Jones. Inhibition of Apoptosis by BCR-ABL in chronic myeloid leukemia. Blood, 83:2038-2044 (1994).
5. Braselmann, S. and McCormick: BCR and RAF form a complex in vivo via 14-3-3 proteins. EMBO J., 14:4839-4848 (1995).
6. Buday, L. and J. Downward: Epidermal growth factor regulates p21ras through the formation of a complex of receptor Grb2 adapter protein, and Sos nucleotide exchange factor. Cell, 73:611-620 (1993).
7. Cambier, N., R. Chopra, A. Strasser, D. Metcalf, and A. G. Eleganty: BCR-ABL activates pathways mediating cytokine independence and protection against apoptosis in murine hematopoietic cells in a dose-dependent manner. Oncogene, 16:335-348 (1998).
8. Campbell, M. L., W. Li, and R. B. Arlinghaus: P210 BCR-ABL is complexed to P160 BCR and ph-P53 proteins in K562 cells. Oncogene, 5:773-776 (1990).
9. Carlesso, N., D. A. Frank, and J. D. Griffin: Tyrosyl phosphorylation and DNA binding activity of signal transducers and activators of transcription (STAT) proteins in hematopoietic cell lines transformed by Bcr/Abl. J. Exp. Med., 183:811-820 (1996).
10. Carpino, N., D. Wisniewski, A. Strife, D. Marshak, R. Kobayashi, B. Stillman, and B. Clarkson: p62 dok: a constitutively tyrosine-phosphorylated GAP-associated proteins in chronic myelogenous leukemia progenitor cells. Cell, 88:197-204 (1997).
11. Chan, L. C., K. K. Karhi, S. I. Rayter, N. Heisterkamp, S. Eridani, R. Powles, S. D. Lawler, J. Groffen, J. G. Foulkes, M. L. Greaves, and L. Wiedemann: A novel abl protein expressed in Philadelphia chromosome positive acute lymphoblastic leukemia. Nature, 325:635-642 (1987).
12. Chissoe, S. L., A. Bodenteich, Y. F. Wang, Y. P. Wang, D. Burian, S. W. Clifton, J. Crabtree, A. Freeman, K. Iyer, L. Jian, Y. Ma, H-J. McLaury, H-Q. Pan, O. H. Sarhan, S. Toth, Z. Wang, G. Zhang, N. Heisterkamp, J. Groffen, and B. A. Roe: Sequence and analysis of the human ABL gene, the BCR gene, and regions involved in the Philadelphia chromosomal translocation. Genomics, 27:67-82 (1995).
13. Chuang, T-H, X. Xu, V. Kaartinen, N. Heisterkamp, J. Groffen, and G. M. Bokoch: Abr and Bcr are multifunctional regulators of the Rho GTP-binding protein family. Proc. Natl. Acad. Sci. U.S.A., 92:10282-10286 (1995).
14. Chung, S-W., R. Daniel, B. Y. Wong, and P. M. C. Wong: The ABL genes in normal and abnormal cell development. Crit. Rev. Oncogen., 7:33-48 (1996).
15. Clark, S. S., J. McLaughlin, W. M. Crist, R. Champlin, and O. N. Witte: Unique forms of the abl tyrosine kinase distinguish Ph-positive CML from Ph-positive ALL. Science, 235:85-87 (1987).
16. Cortez, D., L. Kadlec, and A. M. Pendergast: Structural and signaling requirements for BCR-ABL-mediated transformation and inhibition of apoptosis. Mol. Cell. Biol., 15:5531-5541 (1995).
17. Cortez, D., G. Reuther, and A. M. Pendergast: The Bcr-Abl tyrosine kinase activates mitogenic signaling pathways and stimulates G1-to-S phase transition in hematopoietic cells. Oncogene, 15:2333-2342 (1997).
18. Croce, C. M., K. Huebner, M. Isobe, E. Fainstein, B. Lifshitz, E. Shtivelman, and E. Canaani: Mapping of four distinct bcr-related loci to chromosome region 22q11: order of bcr loci relative to chronic myelogenous leukemia and acute lymphoblastic leukemia breakpoints. Proc. Natl. Acad. Sci., U.S.A., 84:7174-7179 (1987).
19. Dai, Z. and A. M. Pendergast: Abl-2, a novel SH3-containing protein interacts with the c-ABL tyrosine kinase and modultes c-ABL transforming activity. Genes Dev., 9:2583-2597 (1995).
20. Daley, G. Q., R. A. Van Etten, and D. Baltimore: Induction of chronic myelogenous leukemia in mice by the P210bcr-abl gene of the Philadelphia chromosome. Science, 247:824-830 (1990).
21. Datta, S. R., H. Dudek, X. Tao, S. Masters, H. Fu, Y. Gotoh, and M. E. Greenberg. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell, 91:231-241 (1997).
22. deJong, R, J. ten Hoeve, N. Heisterkamp, and J. Groffen: Tyrosine 207 in CRKL is the BCR/ABL phosphorylation site. Oncogene, 11:507-513 (1996).
23. rac. Nature, 351:400-403 (1991).
24. Ford, J. C., F. Al-Khodairy, E. Fotou, K. S. Sheldrick, D. J. F. Griffiths, and A. M. Carr: 14-3-3 protein homologs required for the DNA damage checkpoint in fission yeast. Science, 265:533-535 (1994).
25. Gale, W. N., D. Kaplan, E. J. Lowenstein, J. Schlessinger, and D. Bar-Sagi: Grb2 mediates the EGF-dependent activation of guanine nucleotide exchange on Ras. Nature, 363:88-92 (1993).
26. Goga, A., J. McLaughlin, D. E. H., Afar, D. C. Saffran, and O. N. Witte: Alternative signals to RAS for hematopoietic transformation by the BCR-ABL oncogene. Cell, 42:983-988 (1995).
27. Guo, J. Q., C. F. Hirsch-Ginsberg, Y. M. Xian, S. A. Stass, R. E. Champlin, S. A. Giralt, K. B. McCredie, M. L. Campbell, and R. B. Arlinghaus: Acute lymphoid leukemia molecular phenotype in a patient with benign-phase chronic myelogenous leukemia. Hematol. Pathol., 7:91-106 (1993).
28. Guo, J. Q., J. Lian, A. Glassman, M. Talpaz, H. Kantarjian, A. B. Deisseroth, and R. B. Arlinghaus: Comparison of Bcr-Abl protein expression and Philadelphia chromosome analysis in chronic myelogenous leukemia patients. Am. J. Clin. Pathol., 106:442-448 (1996).
29. Guo, J. Q., J. Y. Lian, Y. M. Xian, M-S. Lee, A. B. Deisseroth, S. A. Stass, R. E. Champlin, M. Talpaz, J. Y. J. Wang, and R. B. Arlinghaus: BCR-ABL protein expression in peripheral blood cells of chronic myelogenous leukemia patients undergoing therapy. Blood, 83:3629-3637 (1994).
30. Guo, J. Q., J. Y. J. Wang, and R. B. Arlinghaus: Detection of BCR-ABL proteins in blood cells of benign phase chronic myelogenous leukemia patients. Cancer Res., 51:3048-3051 (1991).
31. Hanks, S. K., A. M. Quinn, and T. Hunter: The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science, 241:42-52 (1988).
32. Heisterkamp, N., G. Jenster, H. ten Hoeve, D. Zovich, P. K. Pattengale, and J. Groffen: Acute leukaemia in bcr/abl transgenic mice. Nature, 334:251-258 (1990).
33. Hermans, A., N. Heisterkamp, M. von Lindern, S. van Baal, D. Meijer, D. van der Plas, L. M. Wiedemann, J. Groffen, D. Bootsma, and G. Grosveld: Unique fusion of bcr and c-abl genes in Philadelphia chromosome positive acute lymphoblastic leukemia. Cell, 51:33-37 (1987).
34. Hochhaus, A., A. Reiter, H. Skladmy, J. V. Melo, C. Sick, U. Berger, J. Q. Guo, R. B. Arlinghaus, R. Hehlmann, J. M. Goldman, an N. C. P. Cross: A novel BCR-ABL fusion gene (e6a2) in a patient with Philadelphia chromosome negative chronic myelogenous leukemia. Blood, 88:2236-2240 (1996).
35. Hunter, T. Oncoprotein networks. Cell, 88:333-346 (1997).
36. Kantarjian, H. M., A. B. Deisseroth, R. Kurzrock, Z. Estrov, and M. Talpaz: Chronic myelogenous leukemia; a concise update. Blood, 82:691-703 (1993).
37. Kloetzer, W., R. Kurzrock L. Smith, M. Talpaz, M. Spiller, J. Gutterman, and R. Arlinghaus: The human cellular abl gene product in the chronic myelogenous leukemia cell line has an associated tyrosine protein kinase activity. Virology, 140:230-238 (1985).
38. Konopka, J. B., S. M. Watanabe, and O. N. Witte: An alteration of the human c-abl protein in K562 leukemia cells unmasks associated tyrosine kinase activity. Cell, 37:1035-1042 (1984).
39. Kurzrock, R., M. Shtalrid, P. Romero, W. S. Kloetzer, M. Talpaz, J. M. Trujillo, M. Blick, M. Beran, and J. U. Gutterman: A novel c-abl protein in Philadelphia positive acute lymphoblstic leukemia. Nature, 325:631-635 (1987).
40. Lewis, J. M., R. Baskaran, S. Taagepera, M. A. Schwartz, and J. Y. J. Wang: Integrin regulation of c-Abl tyrosine kinase activity and cytoplasmic-nuclear transport. Proc. Natl. Acad. Sci. U.S.A., 93:15174-15179 (1996).
41. Li, J. and T. E. Smithgall. Co-expression with BCR induces activation of the FES tyrosine kinase and phosphorylation of specific N-terminal BCR tyrosine kinase. J. Biol. Chem., 271:32920-32936 (1996).
42. Li, W., O. Dreazen, W. Kloetzer, R. P. Gale, and R. B. Arlinghaus. Characterization of bcr gene products in hematopoietic cells. Oncogene, 4:127-138 (1989).
43. Liu, J., M. Campbell, J. Q. Guo, D. Lu, Y. M. Xian, B. S. Andersson, and R. B. Arlinghaus: BCR-ABL tyrosine kinase is autophosphorylated or transphosphorylates P160 BCR on tyrosine predominantly within the first BCR exon. Oncogene, 8:101-109 (1993).
44. Liu, J., Y. Wu, and R. B. Arlinghaus: Sequences within the first exon of BCR inhibit the activated tyrosine kinase of c-Abl and the Bcr-Abl oncoprotein. Cancer Res., 56:5120-5124 (1996a).
45. Liu, J., Y. Wu, D. Lu, L. Haataja, N. Heisterkamp, J. Groffen, and R. B. Arlinghaus: Inhibition of Bcr serine kinase by tyrosine phosphorylation. Mol. Cell. Biol., 16:998-1003 (1996b).
46. Lu, D., J. Liu, M. Campbell, J. G. Guo, N. Heisterkamp, J. Groffen, E. Canaani, and R. B. Arlinghaus: Tyrosine phosphorylation of P160 BCR by P210 BCR-ABL. Blood, 82:1257-1262 (1993).
47. Lugo, T. G., A. M. Pendergast, A. J. Muller, and O. N. Witte: Tyrosine kinase activity and transformation potency of bcr-abl oncogene products. Science, 247:1079-1082 (1990).
48. Lugo, T. G. and O. N. Witte: The BCR/ABL oncogene transforms Rat-1 cells and cooperates with v-myc. Mol. Cell. Biol., 9:1263-1270 (1989).
49. Ma, G., D. Lu, Y. Wu, J. Liu, and R. B. Arlinghaus: Bcr phosphorylated on tyr177 binds Grb2. Oncogene, 14:2367-2372 (1997).
50. Maguer-Satta, V., S. Burl, L. Liu, J. Damen, H. Chahine, G. Krystal, A. Eaves, and C. Eaves: BCR-ABL accelerates C2-ceramide-induced apoptosis. Oncogene, 16:237-248 (1998).
51. Maru, Y. and O. N. Witte: The BCR gene encodes a novel serine/threonine kinase activity within a single exon. Cell, 67:459-468 (1991).
52. McGahon, A. J., W. K. Nishioka, S. J. Martin, and A. Mahboubi: Regulation of the Fas apoptotic cell death pathway by Abl. J. Biol. Chem., 270:22625-22631 (1995).
53. McLaughlin, J., E. Chianese, and O. N. Witte: In vitro transformation of immature hematopoietic cells by the P210 BCR/ABL oncogene product of the Philadelphia chromosome. Proc. Natl. Acad. Sci. U.S.A., 84:6558-6562 (1987).
54. McLaughlin, J., E. Chianese, and O. N. Witte: Alternative forms of the BCR-ABL oncogene have quantitatively different potencies for stimulation of immature lymphoid cells. Mol. Cell. Biol., 9:1866-1869 (1989).
55. McWhirter, J. R., D. L. Galasso, and J. Y. J. Wang: A coiled-coil oligomerization domain of Bcr is essential for the transforming function of Bcr-Abl oncoproteins. Mol. Cell. Biol., 13:7587-7595 (1993).
56. McWhirter, J. R. and J. Y. J. Wang: Activation of tyrosine kinase and microfilament-binding functions of c-abl by bcr sequences in bcr/abl fusion proteins. Mol. Cell. Biol., 11:7587-7595, (1991).
57. McWhirter, J. R. and J. Y. J. Wang: Effect of Bcr sequences on the cellular function of the Bcr-Abl oncoprotein. Oncogene, 15:1625-1634 (1997).
58. Melo, J. V.: The diversity of BCR-ABL fusion proteins and their relationship to leukemia phenotype. Blood, 88:2375-2384 (1996).
59. Muller, A. J., A. M. Pendergast, M. H. Havlik, L. Puil, T. Pawson, and O. N. Witte: A limited set of SH2 domains binds Bcr through a high-affinity phosphotyrosine-independent interaction. Mol. Cell. Biol, 12:5087-5083 (1992).
60. Muller, A. J., J. C. Young, A. M. Pendergast, M. Pondel, R. N. Landau, D. R. Littman, and O. N. Witte: BCR first exon sequences specifically activate the BCR/ABL tyrosine kinase oncogene of Philadelphia chromosome-positive human leukemias. Mol. Cell. Biol., 11:1785-1789 (1991).
61. Musacchio, A., T. Gibson, P. Rice, J. Thompson, and M. Saraste: The PH domain: a common piece in the structural patchwork of signaling proteins. Trends Biochem. Sci., 18:343-348 (1993).
62. Nowell, P. C. and D. A. Hungerford: Chromosome studies on normal and leukemic human leukocytes. J. Natl. Cancer Inst., 25:85-109 (1960).
63. Olivier, J. P., T. Raabe, M. Henkemeyer, B. Dickson, G. Mabalamu, B. Margolis, J. Schlessinger, E. Hafen, and T. Pawson: A Drosophila SH2-SH3 adaptor protein implicated in coupling the seven less tyrosine kinase to an activator of Ras guanine nucleotide exchange, Sos. Cell, 73:179-191 (1993).
64. Pear, W. S., J. Miller, L. W. Xu, B. Soffer, R. Ren, X. M. Long, J. Aster, R. Bronson, and D. Baltimore: Murine models for studying the pathogenesis of chronic myelogenous leukemia. Blood, 90(Suppl. 1): 393 (1997).
65. Pendergast, A. M., L. A. Quilliam., L. D. Cripe, C. H. Bassing, Z. Dai, N. Li, A. Batzer, K. M. Rabun, C. J. Der, J. Schlessinger, and M. L. Gishizky: BCR-ABL-induced oncogenesis is mediated by direct interaction with the SH2 domain of the GRB2 adaptor protein. Cell, 75:175-185 (1993).
66. Pendergast, A. M., A. J. Muller, M. H. Havlik, Y. Maru, and O. N. Witte: BCR sequences essential for transformation by the BCR-ABL oncogene bind to the ABL SH2 regulatory domain in a nonphosphotyrosine-dependent manner. Cell, 66:161-171 (1991).
67. Puil, L., J. Liu, G. Gish, G. Mbamalu, D. Bowtell, P. G. Pelicci, R. Arlinghaus, and T. Pawson: BCR-ABL oncoproteins bind directly to activators of the Ras signaling pathway. EMBO J., 13:764-773 (1994).
68. Raitano, A. B., J. R. Halpern, T. M. Hambuch, and C. L. Sawyers: The Bcr-Abl leukemia oncogene activates Jun kinase and requires Jun for transformation. Proc. Natl. Acad. Sci. U.S.A., 92:11746-11750 (1995).
69. Renshaw, M. W., J. R. McWhirter, and J. Y. J. Wang: The human leukemia oncogene bcr-abl abrogates the anchorage requirement but not the growth factor requirement for proliferation. Mol. Cell. Biol., 15:1286-1293 (1995).
70. Reuther, G. W., H. Fu, L. D. Cripe, R. J. Collier, and A. M. Pendergast: Association of the protein kinases c-Bcr and Bcr-Abl with proteins of the 14-3-3 family. Science, 266:129-133 (1994).
71. Ron, D., M. Zannini, M. Lewis, R. B. Wickner, L. T. Hunt, G. Graziani, S. R. Tronick, S. A. Aaronson, and A. Eva: A region of proto-dbl essential for its transforming activity shows sequence similarity to a yeast cell cycle gene, CDC24, and the human breakpoint cluster gene Bcr. The New Biol., 3:372-375 (1991).
72. Rowley, J. D.: A new consistent chromosomal abnormality in chronic myelogenous leukemia identified by quinacrine fluorescence and giemsa staining. Nature, 243:290-293 (1973).
73. Salcini, A. E., J. McGlade, G. Pelicci, I. Nicoletti, T. Pawson, and P. G. Pelicci: Formation of Shc-Grb2 complexes is necessary to induce neoplastic transformation by overexpression of Shc proteins. Oncogene, 9:2827-2836 (1994).
74. BCR/ABL. Oncogene, 11:1149-1155 (1995).
75. Sattler, M., R. Salgia, K. Okuda, N. Uemura, M. A. Durstin, E. Pisick, G. Xu, J-L. Li, K. V. Prasad, and J. D. Griffin: The protooncogene product p120CBL and the adaptor proteins CRKL and c-CRK link c-ABL, p190BCR/ABL and p210BCR/ ABL to the phosphatidylinositol-3′ kinase pathway. Oncogene, 12:839-846 (1996).
76. Sawyers, C. L., W. Callahan, and O. N. Witte: Dominant negative MYC blocks transformation by ABL oncogenes. Cell, 70:901-910 (1992).
77. Seong, D., H. Kantarjian, J. Ro, and M. Siciliano: Hypermetaphase FISH for quantitative monitoring of Ph-positive cells in patients with CML during treatment. Blood, 86:2343-2349 (1995).
78. Shtivelman, E., B. Lifshitz, R. P. Gale, and E. Canaani: Fused transcripts of abl and bcr genes in chronic myelogenous leukemia. Nature, 315:550-554 (1985).
79. Shtivelman, E., B. Lifshitz, R. P. Gale, B. A. Roe, and E. Canaani: Alternative splicing of RNAs transcribed from the human abl gene and from the bcr-abl fused gene. Cell, 47:277-284 (1986).
80. Shuai, K., J. Halpern, J. ten Hoeve, X. Rao, and C. L. Sawyers: Constitutive activation of STATS by the BCR-ABL oncogene in chronic myelogenous leukemia. Oncogene, 13:247-254 (1996).
81. Sirard C., P. Laneuville, and J. E. Dick: Expression of bcr-abl abrogates factor-dependent growth of human hematopoietic MO7E cells by an autocrine mechanism. Blood, 83:1575-1585 (1994).
82. Skorski, T., A. Bellacosa, M. Nieborowska-Skorska, M. Majewski, R. Martinez, J. K. Choi, R. Trotta, P. Wlodarski, D. Perrotti, T. O. Chan, M. A. Wasik, P. N. Tsichlis, and B. Calabretta: Transformation of hematopoietic cells by BCR/ABL requires activation of a P1-3k/Akt-dependent. EMBO J., 16:6151-6161 (1997).
83. + leukemia. Blood, 84:1731-1736 (1994a).
84. ten Hoeve, J., V. Kaartinen, T. Fioretos, L. Haataja, J.-W. Voncken, N. Heisterkamp, and J. Groffen: Cellular interactions of CRKL, an SH2-SH3 adaptor protein. Cancer Res., 54:2563-2567 (1994b).
85. ten Hoeve, J., C. Morris, N. Heisterkamp, and J. Groffen: Isolation and chromosomal localization of CRKL, a human crk-like gene. Oncogene, 8:2469-2474 (1993).
86. Timmons, M. S. and O. N. Witte: Structural characterization of the BCR gene product. Oncogene, 4:559-562 (1989).
87. Tomich, J. M., C. Marti, and R. F. Colman: Modification of two essential cysteines in rabbit muscle pyruvate kinase by the guanine nucleotide analogue 5′[p-(fluorosulfonyl)benzoyl] guanosine. Biochemistry, 20:6711-6720 (1981).
88. Van Etten, R. A.: Malignant transformation by Abl and Bcr-Abl: In: Oncogenes and Tumor Suppressor Genes in Human Malignancies. (C. C. Benz and E. T. Liu, Eds.) 167-192. Kluwer Academic Publishers, Norwood, MA (1992).
89. Voncken, J. W., H. van Schaick, V. Kaartinen, K. Deemer, T. Coates, B. Landing, P. Pattengale, O. Dorseuil, G. M. Bokoch, J. Groffen, and N. Heisterkamp: Increased neutrophil respiratory burst in bcr-null mutants. Cell, 80:719-728 (1995).
90. Welch, P. J. and J. Y. J. Wang: A C-terminal protein-binding domain in the retinoblastoma protein regulates nuclear c-Abl tyrosine kinase in the cell cycle. Cell, 75:779-790 (1993).
91. Welch, P. J. and J. Y. J. Wang: Abrogation of retinoblastoma protein function by c-Abl through tyrosine kinase-dependent and -independent mechanisms. Mol. Cell. Biol., 15:5542-5551 (1995).
92. Wen, S-T. and R. A. Van Etten: The PAG gene product, a stress-induced protein with antioxidant properaties, is an Abl SH3-binding protein and a physiological inhibitor of c-Abl tyrosine kinase activity. Genes Dev., 11:2456-246 (1997).
93. Wisniewski, D., A. Strife, E. Berman, and B. Clarkson: c-kit ligand stimulates tyrosine phosphorylation of a similar pattern of phosphotyrosyl proteins in primary primitive normal hematopoietic progenitors that are constitutively phosphorylated in comparable primitive progenitors in chronic phase chronic myelogenous leukemia. Leukemia, 10:229-237 (1996).
94. Wilson-Rawls, J., S. Xie, J. Liu, P. Laneuville, and R. B. Arlinghaus: P210 Bcr-Abl interacts with the interleukin-3 receptor c subunit and constitutively induces its tyrosine phosphorylation. Cancer Res., 56:3426-3430 (1996).
95. Wu, Y., J. Liu, and R. B. Arlinghaus: Requirement of two specific tyrosine residues for the catalytic activity of Bcr serine/threonine kinase. Oncogene, 16:141-146 (1998).
96. Yuan, Z-M., Huang, Whang, Sawyers, R. Weichselbaum, S. Kharbanda, and D. Kufe: Role for c-Abl tyrosine kinase in growth arrest response to DNA damage. Nature, 382:272-274 (1996).
97. Zhu, J. and S. K. Shore: c-ABL tyrosine kinase activity is regulated by association with a novel SH3-domain-binding domain. Mol. Cell. Biol., 16:7054-7062 (1996).