Abstract
Chronic myelogenous leukemia (CML) is characterized by a translocation involving the c-abl protein-tyrosine kinase gene. A chimeric mRNA is formed containing sequences from a chromosome 22 gene (bcr) at its 5' end and all but the variable exon 1 of c-abl sequence. The product of this mRNA, p210bcr-abl, has constitutively high protein-tyrosine kinase activity. We examined K562 cells and other lines established from CML patients for the presence of phosphotyrosine (P-Tyr)-containing proteins which might be p210bcr-abl substrates. Two-dimensional gel separation of 32P-labeled proteins followed by phosphoamino acid analysis of 25 phosphoproteins, which comprised the major alkali-stable phosphoproteins, indicated that three related proteins of 41 kDa are the most prominent P-Tyr-containing proteins detected by this method. The 41-kDa phosphoproteins are found in two other CML lines that we examined but not in lines of similar lineage isolated from patients with distinct leukemic disease. A protein that comigrates with the major form of pp41 (pp41A) and contains P-Tyr is also found in murine fibroblasts and B-lymphoid cells transformed by Abelson murine leukemia virus, which encodes the v-abl protein, and in platelet-derived growth factor-treated fibroblasts, in which it has been described previously. We analyzed three pairs of Epstein-Barr virus-immortalized B-cell lines from individual CML patients and found that only the lines in which active p210bcr-abl was present contained detectable pp41. We also performed immunoblotting with anti-P-Tyr antibodies on the same CML cell lines and detected at least four other putative substrates of p210bcr-abl, which were undetected with use of the two-dimensional gel technique.
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- Bartram C. R., de Klein A., Hagemeijer A., van Agthoven T., Geurts van Kessel A., Bootsma D., Grosveld G., Ferguson-Smith M. A., Davies T., Stone M. Translocation of c-ab1 oncogene correlates with the presence of a Philadelphia chromosome in chronic myelocytic leukaemia. Nature. 1983 Nov 17;306(5940):277–280. doi: 10.1038/306277a0. [DOI] [PubMed] [Google Scholar]
- Ben-Neriah Y., Bernards A., Paskind M., Daley G. Q., Baltimore D. Alternative 5' exons in c-abl mRNA. Cell. 1986 Feb 28;44(4):577–586. doi: 10.1016/0092-8674(86)90267-9. [DOI] [PubMed] [Google Scholar]
- Ben-Neriah Y., Daley G. Q., Mes-Masson A. M., Witte O. N., Baltimore D. The chronic myelogenous leukemia-specific P210 protein is the product of the bcr/abl hybrid gene. Science. 1986 Jul 11;233(4760):212–214. doi: 10.1126/science.3460176. [DOI] [PubMed] [Google Scholar]
- Benz E. J., Jr, Murnane M. J., Tonkonow B. L., Berman B. W., Mazur E. M., Cavallesco C., Jenko T., Snyder E. L., Forget B. G., Hoffman R. Embryonic-fetal erythroid characteristics of a human leukemic cell line. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3509–3513. doi: 10.1073/pnas.77.6.3509. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boulton T. G., Nye S. H., Robbins D. J., Ip N. Y., Radziejewska E., Morgenbesser S. D., DePinho R. A., Panayotatos N., Cobb M. H., Yancopoulos G. D. ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell. 1991 May 17;65(4):663–675. doi: 10.1016/0092-8674(91)90098-j. [DOI] [PubMed] [Google Scholar]
- Boulton T. G., Yancopoulos G. D., Gregory J. S., Slaughter C., Moomaw C., Hsu J., Cobb M. H. An insulin-stimulated protein kinase similar to yeast kinases involved in cell cycle control. Science. 1990 Jul 6;249(4964):64–67. doi: 10.1126/science.2164259. [DOI] [PubMed] [Google Scholar]
- Boyle W. J., van der Geer P., Hunter T. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 1991;201:110–149. doi: 10.1016/0076-6879(91)01013-r. [DOI] [PubMed] [Google Scholar]
- Chan L. C., Karhi K. K., Rayter S. I., Heisterkamp N., Eridani S., Powles R., Lawler S. D., Groffen J., Foulkes J. G., Greaves M. F. A novel abl protein expressed in Philadelphia chromosome positive acute lymphoblastic leukaemia. Nature. 1987 Feb 12;325(6105):635–637. doi: 10.1038/325635a0. [DOI] [PubMed] [Google Scholar]
- Clark S. S., Crist W. M., Witte O. N. Molecular pathogenesis of Ph-positive leukemias. Annu Rev Med. 1989;40:113–122. doi: 10.1146/annurev.me.40.020189.000553. [DOI] [PubMed] [Google Scholar]
- Clark S. S., McLaughlin J., Crist W. M., Champlin R., Witte O. N. Unique forms of the abl tyrosine kinase distinguish Ph1-positive CML from Ph1-positive ALL. Science. 1987 Jan 2;235(4784):85–88. doi: 10.1126/science.3541203. [DOI] [PubMed] [Google Scholar]
- Cleveland D. W., Fischer S. G., Kirschner M. W., Laemmli U. K. Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem. 1977 Feb 10;252(3):1102–1106. [PubMed] [Google Scholar]
- Collins S. J., Groudine M. T. Rearrangement and amplification of c-abl sequences in the human chronic myelogenous leukemia cell line K-562. Proc Natl Acad Sci U S A. 1983 Aug;80(15):4813–4817. doi: 10.1073/pnas.80.15.4813. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Collins S. J., Kubonishi I., Miyoshi I., Groudine M. T. Altered transcription of the c-abl oncogene in K-562 and other chronic myelogenous leukemia cells. Science. 1984 Jul 6;225(4657):72–74. doi: 10.1126/science.6587568. [DOI] [PubMed] [Google Scholar]
- Cooper J. A., Bowen-Pope D. F., Raines E., Ross R., Hunter T. Similar effects of platelet-derived growth factor and epidermal growth factor on the phosphorylation of tyrosine in cellular proteins. Cell. 1982 Nov;31(1):263–273. doi: 10.1016/0092-8674(82)90426-3. [DOI] [PubMed] [Google Scholar]
- Cooper J. A., Hunter T. Changes in protein phosphorylation in Rous sarcoma virus-transformed chicken embryo cells. Mol Cell Biol. 1981 Feb;1(2):165–178. doi: 10.1128/mcb.1.2.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cooper J. A., Hunter T. Major substrate for growth factor-activated protein-tyrosine kinases is a low-abundance protein. Mol Cell Biol. 1985 Nov;5(11):3304–3309. doi: 10.1128/mcb.5.11.3304. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Daley G. Q., Baltimore D. Transformation of an interleukin 3-dependent hematopoietic cell line by the chronic myelogenous leukemia-specific P210bcr/abl protein. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9312–9316. doi: 10.1073/pnas.85.23.9312. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Daley G. Q., McLaughlin J., Witte O. N., Baltimore D. The CML-specific P210 bcr/abl protein, unlike v-abl, does not transform NIH/3T3 fibroblasts. Science. 1987 Jul 31;237(4814):532–535. doi: 10.1126/science.2440107. [DOI] [PubMed] [Google Scholar]
- Daley G. Q., Van Etten R. A., Baltimore D. Induction of chronic myelogenous leukemia in mice by the P210bcr/abl gene of the Philadelphia chromosome. Science. 1990 Feb 16;247(4944):824–830. doi: 10.1126/science.2406902. [DOI] [PubMed] [Google Scholar]
- Davis R. L., Konopka J. B., Witte O. N. Activation of the c-abl oncogene by viral transduction or chromosomal translocation generates altered c-abl proteins with similar in vitro kinase properties. Mol Cell Biol. 1985 Jan;5(1):204–213. doi: 10.1128/mcb.5.1.204. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Elefanty A. G., Hariharan I. K., Cory S. bcr-abl, the hallmark of chronic myeloid leukaemia in man, induces multiple haemopoietic neoplasms in mice. EMBO J. 1990 Apr;9(4):1069–1078. doi: 10.1002/j.1460-2075.1990.tb08212.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ellis C., Moran M., McCormick F., Pawson T. Phosphorylation of GAP and GAP-associated proteins by transforming and mitogenic tyrosine kinases. Nature. 1990 Jan 25;343(6256):377–381. doi: 10.1038/343377a0. [DOI] [PubMed] [Google Scholar]
- Evans J. P., Wickremasinghe R. G., Hoffbrand A. V. Detection of tyrosine protein kinase substrates in fresh leukemia cells and normal blood cells using an immunoblotting technique. Leukemia. 1987 Nov;1(11):782–785. [PubMed] [Google Scholar]
- Evans J. P., Wickremasinghe R. G., Hoffbrand A. V. Tyrosine protein kinase substrates in Philadelphia-positive human chronic granulocytic leukemia derived cell lines (K562 and BV173): detection by using an immunoblotting technique. Leukemia. 1987 Jun;1(6):524–525. [PubMed] [Google Scholar]
- Ferrell J. E., Jr, Martin G. S. Identification of a 42-kilodalton phosphotyrosyl protein as a serine(threonine) protein kinase by renaturation. Mol Cell Biol. 1990 Jun;10(6):3020–3026. doi: 10.1128/mcb.10.6.3020. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fialkow P. J., Jacobson R. J., Papayannopoulou T. Chronic myelocytic leukemia: clonal origin in a stem cell common to the granulocyte, erythrocyte, platelet and monocyte/macrophage. Am J Med. 1977 Jul;63(1):125–130. doi: 10.1016/0002-9343(77)90124-3. [DOI] [PubMed] [Google Scholar]
- Fialkow P. J., Martin P. J., Najfeld V., Penfold G. K., Jacobson R. J., Hansen J. A. Evidence for a multistep pathogenesis of chronic myelogenous leukemia. Blood. 1981 Jul;58(1):158–163. [PubMed] [Google Scholar]
- Franz W. M., Berger P., Wang J. Y. Deletion of an N-terminal regulatory domain of the c-abl tyrosine kinase activates its oncogenic potential. EMBO J. 1989 Jan;8(1):137–147. doi: 10.1002/j.1460-2075.1989.tb03358.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Garrels J. I. Two dimensional gel electrophoresis and computer analysis of proteins synthesized by clonal cell lines. J Biol Chem. 1979 Aug 25;254(16):7961–7977. [PubMed] [Google Scholar]
- Glenney J. R., Jr, Zokas L. Novel tyrosine kinase substrates from Rous sarcoma virus-transformed cells are present in the membrane skeleton. J Cell Biol. 1989 Jun;108(6):2401–2408. doi: 10.1083/jcb.108.6.2401. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Groffen J., Stephenson J. R., Heisterkamp N., de Klein A., Bartram C. R., Grosveld G. Philadelphia chromosomal breakpoints are clustered within a limited region, bcr, on chromosome 22. Cell. 1984 Jan;36(1):93–99. doi: 10.1016/0092-8674(84)90077-1. [DOI] [PubMed] [Google Scholar]
- Hariharan I. K., Adams J. M., Cory S. bcr-abl oncogene renders myeloid cell line factor independent: potential autocrine mechanism in chronic myeloid leukemia. Oncogene Res. 1988;3(4):387–399. [PubMed] [Google Scholar]
- Heisterkamp N., Stam K., Groffen J., de Klein A., Grosveld G. Structural organization of the bcr gene and its role in the Ph' translocation. 1985 Jun 27-Jul 3Nature. 315(6022):758–761. doi: 10.1038/315758a0. [DOI] [PubMed] [Google Scholar]
- Heisterkamp N., Stephenson J. R., Groffen J., Hansen P. F., de Klein A., Bartram C. R., Grosveld G. Localization of the c-ab1 oncogene adjacent to a translocation break point in chronic myelocytic leukaemia. Nature. 1983 Nov 17;306(5940):239–242. doi: 10.1038/306239a0. [DOI] [PubMed] [Google Scholar]
- Hermans A., Heisterkamp N., von Linden M., van Baal S., Meijer D., van der Plas D., Wiedemann L. M., Groffen J., Bootsma D., Grosveld G. Unique fusion of bcr and c-abl genes in Philadelphia chromosome positive acute lymphoblastic leukemia. Cell. 1987 Oct 9;51(1):33–40. doi: 10.1016/0092-8674(87)90007-9. [DOI] [PubMed] [Google Scholar]
- Huhn R. D., Posner M. R., Rayter S. I., Foulkes J. G., Frackelton A. R., Jr Cell lines and peripheral blood leukocytes derived from individuals with chronic myelogenous leukemia display virtually identical proteins phosphorylated on tyrosine residues. Proc Natl Acad Sci U S A. 1987 Jul;84(13):4408–4412. doi: 10.1073/pnas.84.13.4408. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hunter T. Protein modification: phosphorylation on tyrosine residues. Curr Opin Cell Biol. 1989 Dec;1(6):1168–1181. doi: 10.1016/s0955-0674(89)80068-7. [DOI] [PubMed] [Google Scholar]
- Hunter T. The Ca2+/phospholipid-binding proteins of the submembraneous skeleton. Adv Exp Med Biol. 1988;234:169–193. doi: 10.1007/978-1-4757-1980-2_12. [DOI] [PubMed] [Google Scholar]
- Isacke C. M., Trowbridge I. S., Hunter T. Modulation of p36 phosphorylation in human cells: studies using anti-p36 monoclonal antibodies. Mol Cell Biol. 1986 Jul;6(7):2745–2751. doi: 10.1128/mcb.6.7.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jackson P., Baltimore D. N-terminal mutations activate the leukemogenic potential of the myristoylated form of c-abl. EMBO J. 1989 Feb;8(2):449–456. doi: 10.1002/j.1460-2075.1989.tb03397.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kamps M. P., Sefton B. M. Identification of multiple novel polypeptide substrates of the v-src, v-yes, v-fps, v-ros, and v-erb-B oncogenic tyrosine protein kinases utilizing antisera against phosphotyrosine. Oncogene. 1988 Apr;2(4):305–315. [PubMed] [Google Scholar]
- Kazlauskas A., Cooper J. A. Protein kinase C mediates platelet-derived growth factor-induced tyrosine phosphorylation of p42. J Cell Biol. 1988 Apr;106(4):1395–1402. doi: 10.1083/jcb.106.4.1395. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kelliher M. A., McLaughlin J., Witte O. N., Rosenberg N. Induction of a chronic myelogenous leukemia-like syndrome in mice with v-abl and BCR/ABL. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6649–6653. doi: 10.1073/pnas.87.17.6649. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kloetzer W., Kurzrock R., Smith L., Talpaz M., Spiller M., Gutterman J., Arlinghaus R. The human cellular abl gene product in the chronic myelogenous leukemia cell line K562 has an associated tyrosine protein kinase activity. Virology. 1985 Jan 30;140(2):230–238. doi: 10.1016/0042-6822(85)90361-7. [DOI] [PubMed] [Google Scholar]
- Koch C. A., Anderson D., Moran M. F., Ellis C., Pawson T. SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins. Science. 1991 May 3;252(5006):668–674. doi: 10.1126/science.1708916. [DOI] [PubMed] [Google Scholar]
- Koeffler H. P., Golde D. W. Acute myelogenous leukemia: a human cell line responsive to colony-stimulating activity. Science. 1978 Jun 9;200(4346):1153–1154. doi: 10.1126/science.306682. [DOI] [PubMed] [Google Scholar]
- Konopka J. B., Watanabe S. M., Witte O. N. An alteration of the human c-abl protein in K562 leukemia cells unmasks associated tyrosine kinase activity. Cell. 1984 Jul;37(3):1035–1042. doi: 10.1016/0092-8674(84)90438-0. [DOI] [PubMed] [Google Scholar]
- Konopka J. B., Witte O. N. Detection of c-abl tyrosine kinase activity in vitro permits direct comparison of normal and altered abl gene products. Mol Cell Biol. 1985 Nov;5(11):3116–3123. doi: 10.1128/mcb.5.11.3116. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kurzrock R., Shtalrid M., Romero P., Kloetzer W. S., Talpas M., Trujillo J. M., Blick M., Beran M., Gutterman J. U. A novel c-abl protein product in Philadelphia-positive acute lymphoblastic leukaemia. Nature. 1987 Feb 12;325(6105):631–635. doi: 10.1038/325631a0. [DOI] [PubMed] [Google Scholar]
- Lozzio C. B., Lozzio B. B. Human chronic myelogenous leukemia cell-line with positive Philadelphia chromosome. Blood. 1975 Mar;45(3):321–334. [PubMed] [Google Scholar]
- Lugo T. G., Pendergast A. M., Muller A. J., Witte O. N. Tyrosine kinase activity and transformation potency of bcr-abl oncogene products. Science. 1990 Mar 2;247(4946):1079–1082. doi: 10.1126/science.2408149. [DOI] [PubMed] [Google Scholar]
- Lugo T. G., Witte O. N. The BCR-ABL oncogene transforms Rat-1 cells and cooperates with v-myc. Mol Cell Biol. 1989 Mar;9(3):1263–1270. doi: 10.1128/mcb.9.3.1263. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MacDonald I., Levy J., Pawson T. Expression of the mammalian c-fes protein in hematopoietic cells and identification of a distinct fes-related protein. Mol Cell Biol. 1985 Oct;5(10):2543–2551. doi: 10.1128/mcb.5.10.2543. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Martin P. J., Najfeld V., Hansen J. A., Penfold G. K., Jacobson R. J., Fialkow P. J. Involvement of the B-lymphoid system in chronic myelogenous leukaemia. Nature. 1980 Sep 4;287(5777):49–50. doi: 10.1038/287049a0. [DOI] [PubMed] [Google Scholar]
- Martin P., Papayannopoulou T. HEL cells: a new human erythroleukemia cell line with spontaneous and induced globin expression. Science. 1982 Jun 11;216(4551):1233–1235. doi: 10.1126/science.6177045. [DOI] [PubMed] [Google Scholar]
- McLaughlin J., Chianese E., Witte O. N. Alternative forms of the BCR-ABL oncogene have quantitatively different potencies for stimulation of immature lymphoid cells. Mol Cell Biol. 1989 May;9(5):1866–1874. doi: 10.1128/mcb.9.5.1866. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McLaughlin J., Chianese E., Witte O. N. 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. 1987 Sep;84(18):6558–6562. doi: 10.1073/pnas.84.18.6558. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McWhirter J. R., Wang J. Y. Activation of tyrosinase kinase and microfilament-binding functions of c-abl by bcr sequences in bcr/abl fusion proteins. Mol Cell Biol. 1991 Mar;11(3):1553–1565. doi: 10.1128/mcb.11.3.1553. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Muller A. J., Young J. C., Pendergast A. M., Pondel M., Landau N. R., Littman D. R., Witte O. N. BCR first exon sequences specifically activate the BCR/ABL tyrosine kinase oncogene of Philadelphia chromosome-positive human leukemias. Mol Cell Biol. 1991 Apr;11(4):1785–1792. doi: 10.1128/mcb.11.4.1785. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Müller R., Slamon D. J., Tremblay J. M., Cline M. J., Verma I. M. Differential expression of cellular oncogenes during pre- and postnatal development of the mouse. Nature. 1982 Oct 14;299(5884):640–644. doi: 10.1038/299640a0. [DOI] [PubMed] [Google Scholar]
- NOWELL P. C., HUNGERFORD D. A. Chromosome studies on normal and leukemic human leukocytes. J Natl Cancer Inst. 1960 Jul;25:85–109. [PubMed] [Google Scholar]
- Naldini L., Stacchini A., Cirillo D. M., Aglietta M., Gavosto F., Comoglio P. M. Phosphotyrosine antibodies identify the p210c-abl tyrosine kinase and proteins phosphorylated on tyrosine in human chronic myelogenous leukemia cells. Mol Cell Biol. 1986 May;6(5):1803–1811. doi: 10.1128/mcb.6.5.1803. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nitta M., Kato Y., Strife A., Wachter M., Fried J., Perez A., Jhanwar S., Duigou-Osterndorf R., Chaganti R. S., Clarkson B. Incidence of involvement of the B and T lymphocyte lineages in chronic myelogenous leukemia. Blood. 1985 Nov;66(5):1053–1061. [PubMed] [Google Scholar]
- Ogawa R., Ohtsuka M., Watanabe Y. Complement-mediated lysis of K562 human leukemic cells by antibodies to phosphotyrosine and identification of cell surface proteins phosphorylated on tyrosine. Cancer Res. 1986 May;46(5):2507–2510. [PubMed] [Google Scholar]
- Payne D. M., Rossomando A. J., Martino P., Erickson A. K., Her J. H., Shabanowitz J., Hunt D. F., Weber M. J., Sturgill T. W. Identification of the regulatory phosphorylation sites in pp42/mitogen-activated protein kinase (MAP kinase). EMBO J. 1991 Apr;10(4):885–892. doi: 10.1002/j.1460-2075.1991.tb08021.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pendergast A. M., Muller A. J., Havlik M. H., Clark R., McCormick F., Witte O. N. Evidence for regulation of the human ABL tyrosine kinase by a cellular inhibitor. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5927–5931. doi: 10.1073/pnas.88.13.5927. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pendergast A. M., Muller A. J., Havlik M. H., Maru Y., Witte O. N. BCR sequences essential for transformation by the BCR-ABL oncogene bind to the ABL SH2 regulatory domain in a non-phosphotyrosine-dependent manner. Cell. 1991 Jul 12;66(1):161–171. doi: 10.1016/0092-8674(91)90148-r. [DOI] [PubMed] [Google Scholar]
- Posada J., Sanghera J., Pelech S., Aebersold R., Cooper J. A. Tyrosine phosphorylation and activation of homologous protein kinases during oocyte maturation and mitogenic activation of fibroblasts. Mol Cell Biol. 1991 May;11(5):2517–2528. doi: 10.1128/mcb.11.5.2517. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ramakrishnan L., Rosenberg N. abl genes. Biochim Biophys Acta. 1989 Dec 17;989(2):209–224. doi: 10.1016/0304-419x(89)90043-7. [DOI] [PubMed] [Google Scholar]
- Richardson J. M., Morla A. O., Wang J. Y. Reduction in protein tyrosine phosphorylation during differentiation of human leukemia cell line K-562. Cancer Res. 1987 Aug 1;47(15):4066–4070. [PubMed] [Google Scholar]
- Rosenberg N., Witte O. N. The viral and cellular forms of the Abelson (abl) oncogene. Adv Virus Res. 1988;35:39–81. doi: 10.1016/s0065-3527(08)60708-3. [DOI] [PubMed] [Google Scholar]
- Rossomando A. J., Payne D. M., Weber M. J., Sturgill T. W. Evidence that pp42, a major tyrosine kinase target protein, is a mitogen-activated serine/threonine protein kinase. Proc Natl Acad Sci U S A. 1989 Sep;86(18):6940–6943. doi: 10.1073/pnas.86.18.6940. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rowley J. D. Letter: A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature. 1973 Jun 1;243(5405):290–293. doi: 10.1038/243290a0. [DOI] [PubMed] [Google Scholar]
- Sherr C. J. Colony-stimulating factor-1 receptor. Blood. 1990 Jan 1;75(1):1–12. [PubMed] [Google Scholar]
- Shtivelman E., Lifshitz B., Gale R. P., Canaani E. Fused transcript of abl and bcr genes in chronic myelogenous leukaemia. Nature. 1985 Jun 13;315(6020):550–554. doi: 10.1038/315550a0. [DOI] [PubMed] [Google Scholar]
- Shtivelman E., Lifshitz B., Gale R. P., Roe B. A., Canaani E. Alternative splicing of RNAs transcribed from the human abl gene and from the bcr-abl fused gene. Cell. 1986 Oct 24;47(2):277–284. doi: 10.1016/0092-8674(86)90450-2. [DOI] [PubMed] [Google Scholar]
- Strife A., Lambek C., Wisniewski D., Wachter M., Gulati S. C., Clarkson B. D. Discordant maturation as the primary biological defect in chronic myelogenous leukemia. Cancer Res. 1988 Feb 15;48(4):1035–1041. [PubMed] [Google Scholar]
- Szczylik C., Skorski T., Nicolaides N. C., Manzella L., Malaguarnera L., Venturelli D., Gewirtz A. M., Calabretta B. Selective inhibition of leukemia cell proliferation by BCR-ABL antisense oligodeoxynucleotides. Science. 1991 Aug 2;253(5019):562–565. doi: 10.1126/science.1857987. [DOI] [PubMed] [Google Scholar]
- Walker L. C., Ganesan T. S., Dhut S., Gibbons B., Lister T. A., Rothbard J., Young B. D. Novel chimaeric protein expressed in Philadelphia positive acute lymphoblastic leukaemia. 1987 Oct 29-Nov 4Nature. 329(6142):851–853. doi: 10.1038/329851a0. [DOI] [PubMed] [Google Scholar]
- Wang J. Y., Baltimore D. Cellular RNA homologous to the Abelson murine leukemia virus transforming gene: expression and relationship to the viral sequence. Mol Cell Biol. 1983 May;3(5):773–779. doi: 10.1128/mcb.3.5.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang J. Y., Ledley F., Goff S., Lee R., Groner Y., Baltimore D. The mouse c-abl locus: molecular cloning and characterization. Cell. 1984 Feb;36(2):349–356. doi: 10.1016/0092-8674(84)90228-9. [DOI] [PubMed] [Google Scholar]
- Young J. C., Gishizky M. L., Witte O. N. Hyperexpression of interleukin-7 is not necessary or sufficient for transformation of a pre-B lymphoid cell line. Mol Cell Biol. 1991 Feb;11(2):854–863. doi: 10.1128/mcb.11.2.854. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Young J. C., Witte O. N. Selective transformation of primitive lymphoid cells by the BCR/ABL oncogene expressed in long-term lymphoid or myeloid cultures. Mol Cell Biol. 1988 Oct;8(10):4079–4087. doi: 10.1128/mcb.8.10.4079. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Klein A., van Kessel A. G., Grosveld G., Bartram C. R., Hagemeijer A., Bootsma D., Spurr N. K., Heisterkamp N., Groffen J., Stephenson J. R. A cellular oncogene is translocated to the Philadelphia chromosome in chronic myelocytic leukaemia. Nature. 1982 Dec 23;300(5894):765–767. doi: 10.1038/300765a0. [DOI] [PubMed] [Google Scholar]