Regulation of the c-Abl and Bcr–Abl tyrosine kinases (original) (raw)

• Hanks, S. K. Genomic analysis of the eukaryotic protein kinase superfamily: a perspective. Genome Biol. 4, 111 (2003).
  Article PubMed PubMed Central Google Scholar
• Pendergast, A. M. The Abl family kinases: mechanisms of regulation and signaling. Adv. Cancer Res. 85, 51–100 (2002). An extremely comprehensive review article covering, in particular, all aspects of Abl signalling mechanisms and cellular functions.
  Article CAS PubMed Google Scholar
• Woodring, P. J., Hunter, T. & Wang, J. Y. Regulation of F-actin-dependent processes by the Abl family of tyrosine kinases. J. Cell Sci. 116, 2613–2626 (2003).
  Article CAS PubMed Google Scholar
• Smith, J. M. & Mayer, B. J. Abl: mechanisms of regulation and activation. Front. Biosci. 7, d31–d42 (2002).
  Article CAS PubMed Google Scholar
• Advani, A. S. & Pendergast, A. M. Bcr–Abl variants: biological and clinical aspects. Leuk. Res. 26, 713–720 (2002).
  Article CAS PubMed Google Scholar
• Druker, B. J. et al. Chronic myelogenous leukemia. Hematology (Am. Soc. Hematol. Educ. Program) 87–112 (2001).
• Van Etten, R. A. Cycling, stressed-out and nervous: cellular functions of c-Abl. Trends Cell Biol. 9, 179–186 (1999).
  Article CAS PubMed Google Scholar
• Abelson, H. T. & Rabstein, L. S. Lymphosarcoma: virus-induced thymic-independent disease in mice. Cancer Res. 30, 2213–2222 (1970). The historic paper describing the identification of v-Abl from Moloney murine leukaemia virus.
  CAS PubMed Google Scholar
• Abelson, H. T. & Rabstein, L. S. Influence of prednisolone on Moloney leukemogenic virus in BALB-c mice. Cancer Res. 30, 2208–2212 (1970).
  CAS 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. 3, 773–779 (1983).
  Article CAS PubMed PubMed Central Google Scholar
• Raitano, A. B., Whang, Y. E. & Sawyers, C. L. Signal transduction by wild-type and leukemogenic Abl proteins. Biochim. Biophys. Acta 1333, F201–F216 (1997).
  CAS 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 247, 824–830 (1990).
  Article CAS PubMed Google Scholar
• Goldman, J. M. & Melo, J. V. Chronic myeloid leukemia — advances in biology and new approaches to treatment. N. Engl. J. Med. 349, 1451–1464 (2003).
  Article CAS PubMed Google Scholar
• McWhirter, J. R., Galasso, D. L. & Wang, J. Y. A coiled-coil oligomerization domain of Bcr is essential for the transforming function of Bcr–Abl oncoproteins. Mol. Cell. Biol. 13, 7587–7595 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, X., Subrahmanyam, R., Wong, R., Gross, A. W. & Ren, R. The NH(2)-terminal coiled-coil domain and tyrosine 177 play important roles in induction of a myeloproliferative disease in mice by Bcr–Abl. Mol. Cell. Biol. 21, 840–853 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Zhao, X., Ghaffari, S., Lodish, H., Malashkevich, V. N. & Kim, P. S. Structure of the Bcr–Abl oncoprotein oligomerization domain. Nature Struct. Biol. 7, 117–120 (2002).
  Google Scholar
• Smith, K. M. & Van Etten, R. A. Activation of c-Abl kinase activity and transformation by a chemical inducer of dimerization. J. Biol. Chem. 276, 24372–24379 (2001).
  Article CAS PubMed Google Scholar
• Superti-Furga, G. & Courtneidge, S. A. Structure-function relationships in Src family and related protein tyrosine kinases. Bioessays 17, 321–330 (1995).
  Article CAS PubMed Google Scholar
• Smith, C. I. et al. The Tec family of cytoplasmic tyrosine kinases: mammalian Btk, Bmx, Itk, Tec, Txk and homologs in other species. Bioessays 23, 436–446 (2001).
  Article CAS PubMed Google Scholar
• Feller, S. M., Knudsen, B. & Hanafusa, H. c-Abl kinase regulates the protein binding activity of c-Crk. EMBO J. 13, 2341–2351 (1994).
  Article CAS PubMed PubMed Central Google Scholar
• Smith, J. M., Katz, S. & Mayer, B. J. Activation of the abl tyrosine kinase in vivo by src homology 3 domains from the src homology 2/Src homology 3 adaptor Nck. J. Biol. Chem. 274, 27956–27962 (1999).
  Article CAS PubMed Google Scholar
• Shafman, T. et al. Interaction between ATM protein and c-Abl in response to DNA damage. Nature 387, 520–523 (1997).
  Article CAS PubMed Google Scholar
• Goga, A., et al. p53 dependent growth suppression by the c-Abl nuclear tyrosine kinase. Oncogene 11, 791–799 (1995).
  CAS PubMed Google Scholar
• Welch, P. J. & Wang, J. Y. J. 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).
  Article CAS PubMed Google Scholar
• Baskaran, R., Chiang, G. G. & Wang, J. Y. Identification of a binding site in c-Abl tyrosine kinase for the C-terminal repeated domain of RNA polymerase II. Mol. Cell. Biol. 16, 3361–3369 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• David-Cordonnier, M. H. et al. The DNA-binding domain of human c-Abl tyrosine kinase promotes the interaction of a HMG chromosomal protein with DNA. Nucleic Acids Res. 27, 2265–2270 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Van Etten, R. A. et al. The COOH terminus of the c-Abl tyrosine kinase contains distinct F- and G-actin binding domains with bundling activity. J. Cell Biol. 124, 325–340 (1994).
  Article CAS PubMed Google Scholar
• Van Etten, R. A., Jackson, P. & Baltimore, D. The mouse type IV c-abl gene product is a nuclear protein, and activation of transforming ability is associated with cytoplasmic localization. Cell 58, 669–678 (1989).
  Article CAS PubMed Google Scholar
• Taagepera, S. et al. Nuclear-cytoplasmic shuttling of C-ABL tyrosine kinase. Proc. Natl Acad. Sci. USA 95, 7457–7462 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Goga, A. et al. Oncogenic activation of c-ABL by mutation within its last exon. Mol. Cell. Biol. 13, 4967–4975 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Pluk, H., Dorey, K. & Superti-Furga, G. Autoinhibition of c-Abl. Cell 108, 247–259 (2002).
  Article CAS PubMed Google Scholar
• Nagar, B. et al. Structural basis for the autoinhibition of c-Abl tyrosine kinase. Cell 112, 859–871 (2003).
  Article CAS PubMed Google Scholar
• Harrison, S. C. Variation on an Src-like theme. Cell 112, 737–740 (2003).
  Article CAS PubMed Google Scholar
• Courtneidge, S. A. Cancer: escape from inhibition. Nature 422, 827–828 (2003).
  Article CAS PubMed Google Scholar
• Xu, W., Harrison, S. C. & Eck, M. J. Three-dimensional structure of the tyrosine kinase c-Src. Nature 385, 595–601 (1997).
  Article CAS PubMed Google Scholar
• Sicheri, F., Moarefi, I. & Kuriyan, J. Crystal structure of the Src family tyrosine kinase Hck. Nature 385, 602–609 (1997).
  Article CAS PubMed Google Scholar
• Williams, J. C. et al. The 2.35 Å crystal structure of the inactivated form of chicken Src: a dynamic molecule with multiple regulatory interactions. J. Mol. Biol. 274, 757–775 (1997).
  Article CAS PubMed Google Scholar
• Barilá, D. & Superti-Furga, G. An intramolecular SH3-domain interaction regulates c-Abl activity. Nature Genet. 18, 280–282 (1998). The article that first suggested c-Abl to be regulated by an intramolecular interaction involving the SH3 domain, the SH2–kinase linker and the small lobe. The structural model proposed, which includes a unique salt-bridge between the SH3 domain and the small lobe, is basically identical to the structure of regulated c-Abl determined five years later.
  Article PubMed Google Scholar
• Young, M. A., Gonfloni, S., Superti-Furga, G., Roux, B. & Kuriyan, J. Dynamic coupling between the SH2 and SH3 domains of c-Src and Hck underlies their inactivation by C-terminal tyrosine phosphorylation. Cell 105, 115–126 (2001).
  Article CAS PubMed Google Scholar
• Hantschel, O. et al. A myristoyl/phosphotyrosine switch regulates c-Abl. Cell 112, 845–857 (2003). References 32 and 40 show the structure of regulated c-Abl, its autoinhibition mechanism, binding of the myristoyl group to the kinase domain, SH2 domain occlusion, activation by phosphotyrosine and conformational dependence for STI-571 binding.
  Article CAS PubMed Google Scholar
• Barilá, D. et al. A nuclear tyrosine phosphorylation circuit: c-Jun as an activator and substrate of c-Abl and JNK. EMBO J. 19, 273–281 (2000).
  Article PubMed PubMed Central Google Scholar
• Juang, J. L. & Hoffmann, F. M. Drosophila Abelson interacting protein (dAbi) is a positive regulator of Abelson tyrosine kinase activity. Oncogene 18, 5138–5147 (1999).
  Article CAS PubMed Google Scholar
• Lewis, J. M. & Schwartz, M. A. Integrins regulate the association and phosphorylation of paxillin by c-Abl. J. Biol. Chem. 273, 14225–14230 (1998).
  Article CAS PubMed Google Scholar
• Miyoshi-Akiyama, T., Aleman, L. M., Smith, J. M., Adler, C. E. & Mayer, B. J. Regulation of Cbl phosphorylation by the Abl tyrosine kinase and the Nck SH2/SH3 adaptor. Oncogene 20, 4058–4069 (2001).
  Article CAS PubMed Google Scholar
• Roig, J., Tuazon, P. T., Zipfel, P. A., Pendergast, A. M. & Traugh, J. A. Functional interaction between c-Abl and the p21-activated protein kinase γ-PAK. Proc. Natl Acad. Sci. USA 97, 14346–14351 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Zukerberg, L. R. et al. Cables links Cdk5 and c-Abl and facilitates Cdk5 tyrosine phosphorylation, kinase upregulation, and neurite outgrowth. Neuron 26, 633–646 (2000).
  Article CAS PubMed Google Scholar
• Schindler, T. et al. Structural mechanism for STI-571 inhibition of abelson tyrosine kinase. Science 289, 1938–1942 (2000). Showed the structural basis for STI-571 inhibition and the first structure of the Abl kinase domain.
  Article CAS PubMed Google Scholar
• Nagar, B. et al. Crystal structures of the kinase domain of c-Abl in complex with the small molecule inhibitors PD173955 and imatinib (STI-571). Cancer Res. 62, 4236–4243 (2002).
  CAS PubMed Google Scholar
• Huse, M. & Kuriyan, J. The conformational plasticity of protein kinases. Cell 109, 275–282 (2002). A hallmark review for readers interested in the structural basis for the diverse mechanisms of protein kinase inhibition.
  Article CAS PubMed Google Scholar
• Yamaguchi, H. & Hendrickson, W. A. Structural basis for activation of human lymphocyte kinase Lck upon tyrosine phosphorylation. Nature 384, 484–489 (1996).
  Article CAS PubMed Google Scholar
• Franz, W. M., Berger, P. & Wang, J. Y. J. Deletion of an N-terminal regulatory domain of the c-Abl tyrosine kinase activates its oncogenic potential. EMBO J. 8, 137–147 (1989).
  Article CAS PubMed PubMed Central Google Scholar
• Daley, G. Q., Van Etten, R. A., Jackson, P. K., Bernards, A. & Baltimore, D. Nonmyristoylated Abl proteins transform a factor-dependent hematopoietic cell line. Mol. Cell. Biol. 12, 1864–1871 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• Brasher, B. B. & Van Etten, R. A. c-Abl has high intrinsic tyrosine kinase activity that is stimulated by mutation of the src homology 3 domain and by autophosphorylation at two distinct regulatory tyrosines. J. Biol. Chem. 275, 35631–35637 (2000).
  Article CAS PubMed Google Scholar
• Dorey, K. et al. Phosphorylation and structure-based functional studies reveal a positive and a negative role for the activation loop of the c-Abl tyrosine kinase. Oncogene 20, 8075–8084 (2001).
  Article CAS PubMed Google Scholar
• Jackson, P. & Baltimore, D. N-terminal mutations activate the leukemogenic potential of the myristoylated form of c-Abl. EMBO J. 8, 449–456 (1989).
  Article CAS PubMed PubMed Central Google Scholar
• Van Etten, R. A., Debnath, J., Zhou, H. & Casasnovas, J. M. Introduction of a loss-of-function point mutation from the SH3 region of the Caenorhabditis elegans Sem-5 gene activates the transforming ability of c-Abl in vivo and abolishes binding of proline-rich ligands in vitro. Oncogene 10, 1977–1988 (1995).
  CAS PubMed Google Scholar
• Reynolds, F. H. Jr., Oroszlan, S. & Stephenson, J. R. Abelson murine leukemia virus P120: identification and characterization of tyrosine phosphorylation sites. J. Virol. 44, 1097–1101 (1982).
  CAS PubMed PubMed Central Google Scholar
• Plattner, R., Kadlec, L., DeMali, K. A., Kazlauskas, A. & Pendergast, A. M. c-Abl is activated by growth factors and src family kinases and has a role in the cellular response to PDGF. Genes Dev. 13, 2400–2411 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Furstoss, O. et al. c-Abl is an effector of Src for growth factor-induced c-myc expression and DNA synthesis. EMBO J. 21, 514–524 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Tanis, K. Q., Veach, D., Duewel, H. S., Bornmann, W. G. & Koleske, A. J. Two distinct phosphorylation pathways have additive effects on Abl family kinase activation. Mol. Cell. Biol. 23, 3884–3896 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Steen, H., Fernandez, M., Ghaffari, S., Pandey, A. & Mann, M. Phosphotyrosine mapping in Bcr/Abl oncoprotein using phosphotyrosine-specific immonium ion scanning. Mol. Cell Proteomics 2, 138–145 (2003).
  Article CAS PubMed Google Scholar
• Salomon, A. R. et al. Profiling of tyrosine phosphorylation pathways in human cells using mass spectrometry. Proc. Natl Acad. Sci. USA 100, 443–448 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Pendergast, A. M. et al. BCR–ABL-induced oncogenesis is mediated by direct interaction with the SH2 domain of the GRB-2 adaptor protein. Cell 75, 175–185 (1993).
  Article CAS PubMed Google Scholar
• Gould, K. L. & Nurse, P. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature 342, 39–45 (1989).
  Article CAS PubMed Google Scholar
• McGowan, C. H. & Russell, P. Human Wee1 kinase inhibits cell division by phosphorylating p34cdc2 exclusively on Tyr15. EMBO J. 12, 75–85 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Roumiantsev, S. et al. Clinical resistance to the kinase inhibitor STI-571 in chronic myeloid leukemia by mutation of Tyr-253 in the Abl kinase domain P-loop. Proc. Natl Acad. Sci. USA 99, 10700–10705 (2002). Contains the first evidence for a correlation between regulatory mutations and drug resistance.
  Article CAS PubMed PubMed Central Google Scholar
• Azam, M., Latek, R. R. & Daley, G. Q. Mechanisms of autoinhibition and STI-571/Imatinib resistance revealed by mutagenesis of BCR–ABL. Cell 112, 831–843 (2003). This groundbreaking paper changed the view of how Bcr–Abl functions, and will guide Abl researchers for the following years.
  Article CAS PubMed Google Scholar
• Allen, P. B. & Wiedemann, L. M. An activating mutation in the ATP binding site of the ABL kinase domain. J. Biol. Chem. 271, 19585–19591 (1996).
  Article CAS PubMed Google Scholar
• Brasher, B. B., Roumiantsev, S. & Van Etten, R. A. Mutational analysis of the regulatory function of the c-Abl Src homology 3 domain. Oncogene 20, 7744–7752 (2001).
  Article CAS PubMed Google Scholar
• Musacchio, A., Wilmanns, M. & Saraste, M. Structure and function of the SH3 domain. Prog. Biophys. Mol. Biol. 61, 283–297 (1994).
  Article CAS PubMed Google Scholar
• Zhou, H. X. How often does the myristoylated N-terminal latch of c-Abl come off? FEBS Lett. 552, 160–162 (2003).
  Article CAS PubMed Google Scholar
• Wright, P. E. & Dyson, H. J. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J. Mol. Biol. 293, 321–331 (1999).
  Article CAS PubMed Google Scholar
• Smith, K. M., Yacobi, R. & Van Etten, R. A. Autoinhibition of Bcr–Abl through its SH3 domain. Mol. Cell 12, 27–37 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Plattner, R. et al. A new link between the c-Abl tyrosine kinase and phosphoinositide signalling through PLC-γ1. Nature Cell Biol. 5, 309–319 (2003).
  Article CAS PubMed Google Scholar
• Plattner, R. & Pendergast, A. M. Activation and signaling of the Abl tyrosine kinase: bidirectional link with phosphoinositide signaling. Cell Cycle 2, 273–274 (2003).
  Article CAS PubMed Google Scholar
• Van Etten, R. A. c-Abl regulation: a tail of two lipids. Curr. Biol. 13, R608–R610 (2003).
  Article CAS PubMed Google Scholar
• Woodring, P. J., Hunter, T. & Wang, J. Y. Inhibition of c-Abl tyrosine kinase activity by filamentous actin. J. Biol. Chem. 276, 27104–27110 (2001).
  Article CAS PubMed Google Scholar
• Woodring, P. J. et al. Modulation of the F-actin cytoskeleton by c-Abl tyrosine kinase in cell spreading and neurite extension. J. Cell Biol. 156, 879–892 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Wen, S. -T. & Van Etten, R. A. The PAG gene product, a stress-induced protein with antioxidant properties, is an Abl SH3-binding protein and a physiological inhibitor of c-Abl tyrosine kinase activity. Genes Dev. 11, 2456–2467 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Neumann, C. A. et al. Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature 424, 561–565 (2003).
  Article CAS PubMed Google Scholar
• Baskaran, R. et al. Ataxia telangiectasia mutant protein activates c-Abl tyrosine kinase in response to ionizing radiation. Nature 387, 516–519 (1997).
  Article CAS PubMed Google Scholar
• Kharbanda, S. et al. Functional interaction between DNA-PK and c-Abl in response to DNA damage. Nature 386, 732–735 (1997).
  Article CAS PubMed Google Scholar
• Bhatnagar, R. S. et al. Structure of N-myristoyltransferase with bound myristoylCoA and peptide substrate analogs. Nature Struct. Biol. 5, 1091–1097 (1998).
  Article CAS PubMed Google Scholar
• Farazi, T. A., Waksman, G. & Gordon, J. I. The biology and enzymology of protein N–myristoylation. J. Biol. Chem. 276, 39501–39504 (2001).
  Article CAS PubMed Google Scholar
• Resh, M. D. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim. Biophys. Acta 1451, 1–16 (1999). An extremely interesting review discussing the different mechanisms and functions of protein myristoylation and palmitoylation.
  Article CAS PubMed Google Scholar
• Resh, M. D. Myristylation and palmitylation of Src family members: the fats of the matter. Cell 76, 411–413 (1994).
  Article CAS PubMed Google Scholar
• Nicholson, D. W. Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ. 6, 1028–1042 (1999).
  Article CAS PubMed Google Scholar
• Manning, G., Whyte, D. B., Martinez, R., Hunter, T. & Sudarsanam, S. The protein kinase complement of the human genome. Science 298, 1912–1934 (2002).
  Article CAS PubMed Google Scholar
• Cox, S., Radzio-Andzelm, E. & Taylor, S. S. Domain movements in protein kinases. Curr. Opin. Struct. Biol. 4, 893–901 (1994).
  Article CAS PubMed Google Scholar
• Buchdunger, E. et al. Inhibition of the Abl protein-tyrosine kinase in vitro and in vivo by a 2-phenylaminopyrimidine derivative. Cancer Res. 56, 100–104 (1996). First report about the selective inhibition of Abl and PDGF-R by STI-571.
  CAS PubMed Google Scholar
• Druker, B. J. et al. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr–Abl positive cells. Nature Med. 2, 561–566 (1996).
  Article CAS PubMed Google Scholar
• Druker, B. J. et al. Efficacy and safety of a specific inhibitor of the BCR–ABL tyrosine kinase in chronic myeloid leukemia. N. Engl. J. Med. 344, 1031–1037 (2001).
  Article CAS PubMed Google Scholar
• Heinrich, M. C. et al. Inhibition of c-kit receptor tyrosine kinase activity by STI-571, a selective tyrosine kinase inhibitor. Blood 96, 925–932 (2000).
  CAS PubMed Google Scholar
• Heinrich, M. C. et al. PDGFRA activating mutations in gastrointestinal stromal tumors. Science 299, 708–710 (2003).
  Article CAS PubMed Google Scholar
• Hochhaus, A. et al. Molecular and chromosomal mechanisms of resistance to imatinib (STI571) therapy. Leukemia 16, 2190–2196 (2002).
  Article CAS PubMed Google Scholar
• Mayer, B. J. SH3 domains: complexity in moderation. J. Cell Sci. 114, 1253–1263 (2001).
  CAS PubMed Google Scholar
• Pawson, T., Gish, G. D. & Nash, P. SH2 domains, interaction modules and cellular wiring. Trends Cell Biol. 11, 504–511 (2001).
  Article CAS PubMed Google Scholar
• Lemmon, M. A. Phosphoinositide recognition domains. Traffic 4, 201–213 (2003).
  Article CAS PubMed Google Scholar
• DeLano, W. L. The PyMOL Molecular Graphics System. The PyMOL homepage. <http://pymol.sourceforge.net.> (2002).
  Google Scholar