The cytostatic function of c-Abl is controlled by multiple nuclear localization signals and requires the p53 and Rb tumor suppressor gene products

EMBO Journal

Volumn 15, Issue 7, 1996, Pages 1583-1595

  Wen, Shih Te ^a   Jackson, Peter K ^a   Van Etten, Richard A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Abelson murine leukemia virus; p53; Retinoblastoma protein; Tyrosine kinase

Indexed keywords

PROTEIN P53; PROTEIN TYROSINE KINASE; RETINOBLASTOMA PROTEIN;

ABELSON MURINE LEUKEMIA ONCOVIRUS; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; DNA DAMAGE; FIBROBLAST; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN DNA BINDING; TUMOR SUPPRESSOR GENE;

ABELSON MURINE LEUKEMIA VIRUS; ANIMALIA; MURINAE; MURINE LEUKEMIA ONCOVIRUS; MURINE LEUKEMIA VIRUS; ONCOVIRINAE;

EID: 0029879676     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00503.x     Document Type: Article

References (83)

1. cdc2 kinase motif. Oncogene, 5, 423-426.
2. Baskaran, R., Dahmus, M.E. and Wang, J.Y.J. (1993) Tyrosme phosphorylation of mammalian RNA polymerase II carboxyterminal domain. Proc. Natl Acad. Sci. USA, 90, 11167-11171.
3. Ben-Neriah, Y., Bernards, A., Paskind, M., Daley, G.Q. and Baltimore, D. (1986) Alternative 5′ exons in c-abl mRNA. Cell, 44, 577-586.
4. Birchenall-Roberts, M.C. et al. (1995) Nuclear localization of v-Abl leads to complex formation with cyclic AMP response element (CRE)-binding protein and transactivation through CRE motifs. Mol. Cell. Biol., 15, 6088-6099.
5. Daley, G.Q., Van Etten, R.A., Jackson, PK., Bernards, A. and Baltimore, D. (1992) Non-myristoylated Abl proteins transform a factor-dependent hematopoietic cell line. Mol. Cell. Biol., 12, 1864-1871.
6. Damel, R., Cai, Y., Wong, P.M.C. and Chung, S.-W. (1995) Deregulation of c-abl mediated cell growth after retroviral transfer and expression of antisense sequences. Oncogene, 10, 1607-1614.
7. CIPI/WAFI undergo normal development, but are defective in G1 checkpoint control Cell, 82, 675-684.
8. Dikbtein, R., Heffetz, D., Ben-Neriah, Y. and Shaul, Y. (1992) c-Abl has a sequence-specific enhancer binding activity. Cell, 69, 751-757.
9. Dingwall, C. and Laskey, R.A. (1991) Nuclear targeting sequences - a consensus? Trends Biol. Sci., 16, 478-481.
10. Dingwall, C., Sharnick, S.V. and Laskey, R.A. (1982) A polypeptide domain that specifies migration of nucleoplasmin into the nucleus. Cell, 30, 449-458.
11. Dingwall, C., Robbins, J., Dilworth, S.M., Roberts, B. and Richardson, W.D. (1988) The nucleoplasmin nuclear location sequence is larger and more complex than that of SV-40 large T antigen. J. Cell Biol., 107, 841-849.
12. Dulic, V., Kaufmann, W.K., Wilson, S.J., Tlsty, T.D., Lees, S., Harper, J.W., Elledge, S.J. and Reed, S.I. (1994) p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell, 76, 1013-1023.
13. Engelman, A. and Rosenberg, N. (1987) Isolation of temperature-sensitive Abelson virus mutants by site-directed mutasenesis. Proc. Natl Acad. Sci. USA, 84, 8021-8025.
14. Frangioni, J.V. and Neel, B.G. (1993) Use of a general purpose mammalian expression vector for studying intracellular protein targeting: identification of critical residues in the nuclear lamin A/C nuclear localization signal. J. Cell Sci., 105, 481-488.
15. Franz, W.M., Berger, P. and Wang, J.Y.J. (1989) Deletion of an N-terminal regulatory domain of the c-abl tyrosine kinase activates its oncogenic potential. EMBO J., 8, 137-147.
16. Goff, S.P., Tabin, C.J., Wang, J.Y.-J., Weinberg, R. and Baltimore, D. (1982) Transfection of fibroblasts by cloned Abelson murine leukemia virus DNA and recovery of transmissible virus by recombination with helper virus. J. Virol., 41, 271-285.
17. Goga, A., McLaughlin, J., Pendergast, A.M., Parmar, K., Muller, A., Rosenberg, N. and Witte, O.N. (1993) Oncogenic activation of c-ABL by mutation within its last exon. Mol. Cell. Biol., 13, 4967-1975.
18. Goga, A., Liu, X., Hambuch, T.M., Senechal, K., Major, E., Berk, A.J., Witte, O.N. and Sawyers, C.L. (1995) p53 dependent growth suppression by the c-Abl nuclear tyrosine kinase. Oncogene, 11, 791-799.
19. Hall, M.N., Craik, C. and Hiraoka, Y. (1990) Homeodomain of yeast repressor α2 contains a nuclear localization signal Proc. Natl Acad. Sci. USA, 87, 6954-6958.
20. Hirano, Y., Yamato, K. and Tsuchida, N. (1995) A temperature sensitive mutant of the human p53, Vall38, arrests rat cell growth without induced expression of cip1/waf1/sdi1 after temperature shift-down. Oncogene, 10, 1879-1885.
21. Hu, Q., Dyson, N. and Harlow, E. (1990) The regions of the retinoblastoma protein needed for binding to adenovirus E1A or SV40 large T antigen are common sites for mutations. EMBO J., 9, 1147-1155.
22. Huang, T.-S., Duyster, J. and Wang, J.Y.J. (1995) Biological response to phorbol ester determined by alternative G1 pathways. Proc. Natl Acad. Sci. USA, 92, 4793-4797.
23. Jacks, T., Fazeli, A., Schmitt, E.M., Bronson, R.T., Goodell, M.A. and Weinberg, R.A. (1992) Effects of an Rb mutation in the mouse. Nature, 359, 295-300.
24. Jackson, P. and Baltimore, D. (1989) N-terminal mutations activate the leukemogenic potential of the myristoylaled form of c-abl. EMBO J., 8, 449-456.
25. Jackson, P., Baltimore, D. and Picard, D. (1993a) Hormone-conditional transformation by fusion proteins of c-Abl and its transforming variants. EMBO J., 12, 2809-2819.
26. Jackson, P.K., Paskind, M. and Baltimore, D. (1993b) Mutation of a phenylalanine conserved in SH3-containing tyrosine kinases activates the transforming ability of c-Abl. Oncogene, 8, 1943-1956.
27. Kalderon, D., Roberts, B.L., Richardson, W.D. and Smith, A.E. (1984) A short ammo acid sequence able to specify nuclear location. Cell, 39, 499-509.
28. Kharbanda, S., Ren, R., Pandey, P., Shafman, T.D., Feller, S.M., Weichselbaum, R.R. and Kufe, D.W (1995) Acivation of the c-Abl tyrosine kinase in the stress response to DNA-damaging agents Nature, 376, 785-788.
29. Kipreos, E.T. and Wang, J.Y.J. (1990) Differential phosphorylation of c-Abl in cell cycle determined by cdc2 kinase and phosphatase activity. Science, 248, 217-220.
30. Kipreos, E.T. and Wang, J.Y.J. (1992) Cell cycle-regulated binding of c-Abl tyrosine kinase to DNA. Science, 256, 382-385.
31. Kipreos, E., Lee, G.J. and Wang, J.Y.J. (1987) Isolation of temperature-sensitive tyrosine kinase mutants of v-abl oncogene by screening with antibodies for phosphotyrosine. Proc. Natl Acad. Sci. USA, 84, 1345-1349
32. Kruh, G.D., Perego, R., Miki, T. and Aaronson, S.A. (1990) The complete coding sequence of arg defines the Abelson subfamily of cytoplasmic tyrosine kinases. Proc. Natl Acad. Sci USA, 87, 5802-5806.
33. Kunkel, T.A. (1985) Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl Acad. Sci. USA, 82, 488-492.
34. Lowe, S.H., Schmitt, E.M., Smith, S.W., Osborne, B.A. and Jacks, T. (1993) p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature, 362, 847-849.
35. Lyons, R.H., Ferguson, B.Q. and Rosenberg, M. (1987) Pentapeptide nuclear localization signal in adenovirus E1A. Mol. Cell. Biol., 7, 2451-2456.
36. Mattioni, T., Jackson, P.K., Behini-Hooft van Huijsduinnen, O. and Picard, D. (1995) Cell cycle arrest by tyrosine kinase Abl involves altered early mitogenic response. Oncogene, 10, 1325-1333.
37. Mayer, B.J., Jackson, P.K , Van Etten, R.A. and Baltimore, D. (1992) Point mutations in the abl SH2 domain coordinately impair phosphotyrosine binding in vitro and transforming activity in vivo. Mol. Cell. Biol., 12, 609-618.
38. McWhirter, J.R. and Wang, J.Y.J. (1991) Activation of tyrosine kinase and nucrofilament-binding functions of c-abl by bcr sequences in bcr/abl fusion proteins. Mol. Cell. Biol., 11, 1785-1792.
39. McWhirter, J.R. and Wang, J.Y.J (1993) An actin-binding function contributes to transformation by the Ber-Ab1 oncoprotein of the Philadelphia chromosome-positive leukemias. EMBO J., 12, 1533-1546.
40. Michalovitz, D., Halevy, O. and Oren, M. (1990) Conditional inhibition of transformation and of cell proliferation by a temperature-sensitive mutant of p53. Cell, 62, 671-680
41. Muller, R., Slamon, D.J, Tremblay, J.M., Cline, M.J. and Verma, I.M. (1982) Differential expression of cellular oncogenes during pre-and postnatal development of the mouse Nature, 299, 640-644.
42. Munger, K., Werness, B.A., Dyson, N., Phelps, W.C., Harlow, E and Howley, P.M. (1989) Complex formation of human papilloma virus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J., 8, 4099-4105.
43. Nevins, J.R. (1992) E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science, 258, 424-429.
44. Oppi, C., Shore, S.K. and Reddy, E.P. (1987) Nucleotide sequence of testis-derived c-abl cDNAs: implications for testis-specific transcription and abl oncogene activation. Proc. Natl Acad. Sci. USA, 84, 8200-8204.
45. Papadopoulos, P., Ridge, S A. Boucher, C.A., Stocking, C and Wiedemann, L.M. (1995) The novel activation of ABL by fusion to an ets-related gene, TEL. Cancer Res., 55, 34-38.
46. Pawson, T. and Schlessinger, J (1993) SH2 and SH3 domains Curr. Biol., 3, 434-441.
47. Pear, W.S., Nolan, G.P., Scott, M.L. and Baltimore, D. (1993) Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl Acad. Sci. USA, 90, 8392-8396
48. Pendergast, A.M, Traugh, J.A. and Witte, O.N. (1987) Normal cellular and transformation-associated abl proteins share common sites for protein kinase C phosphorylation. Mol. Cell, Biol., 7, 4280-4289.
49. Pendergast, A.M., Muller, A.J., Havlik, M.H., Clark, R., McCormick, F and Witte, O.N. (1991) Evidence for regulation of the human ABL tyrosine kinase by a cellular inhibitor. Proc. Natl Acad. Sci. USA, 88, 5927-5931
50. Picard, D. and Yamamoto, K.R. (1987) Two signals mediate hormone-dependent nuclear localization of the glucocorticoid receptor. EMBO J., 6, 3333-3340.
51. Reddy, E P., Smith, M.J. and Srinivasan, A. (1983) Nucleotide sequence of Abelson murine leukemia virus genome: structural similarity of its transforming gene product to other one gene products with tyrosine-specific kinase activity. Proc. Natl Acad. Sci. USA, 80, 3623-3627.
52. Ren.R., Zheng, S.Y. and Baltimore, D. (1994) Abl protein-tyrosine kinase selects the Crk adapter as a substrate using SH3-binding sites. Genes Dev., 8, 783-795.
53. Renshaw, M.W., Capozza, M.A. and Wang, J.Y.J. (1988) Differential expression of type-specific c-abl mRNAs in mouse tissues and cell lines. Mol. Cell, Biol., 8, 4547-4551.
54. Renshaw, M.W., Kipreos, E.T., Albrecht, M.R. and Wang, J.Y.J. (1992) Oncogenic v-Abl tyrosine kinase can inhibit or stimulate growth. depending on the cell context. EMBO J., 11, 3941-3951.
55. Richardson, W.D., Roberts, B.L. and Smith, A.E. (1986) Nuclear location signals in polyoma virus large-T. Cell, 44, 77-85.
56. Robbins, J., Dilworth, S.M., Laskey, R.A. and Dingwall, C. (1991) Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence Cell, 64, 615-623.
57. Rosenberg, N.E., Clark, D.R. and Witte, O.N. (1980) Abelson murine leukemia virus mutants deficient in kinase activity and lymphoid cell transformation. J. Virol., 36, 563-568.
58. Scinchez, I., Hughes, R.T., Mayer, B.J., Yee, K., Woodgett, J.R., Avruch, A, Kyriakis, J.M. and Zon, L.I. (1994) Role of SAPK/ERK kinase-1 in the stress-activated pathway regulating transcription factor c-Jun. Nature, 372, 794-798.
59. Sawyers, C.L., Callahan, W. and Witte, O N (1992) Dominant negative myc blocks transformation by ABL oncogenes. Cell, 70, 901-910
60. Sawyers, C.L., McLaughlin, J.L , Goga, A., Havlik, M. and Witte, O. (1994) The nuclear tyrosine kinase c-Abl negatively regulates cell growth. Cell, 77, 121-131.
61. Sawyers, C.L., McLaughlin, J. and Witte, O.N. (1995) Genetic requirement for Ras in the transformation of fibroblasts and hematopoietic cells by the Bcr-Abl oncogene. J. Exp. Med., 181, 307-313.
62. Scheffner, M., Werness, B.A., Huibregtse, J.M., Levine, A.J. and Howley, PM. (1990) The E6 oncoprotein of human papilloma virus types 16 and 18 promotes the degradation of p53. Cell, 63, 1129-1136.
63. ml mutation show poor viability and depletion of selected B and T cell populations. Cell, 65, 1165-1176.
64. Sherr, C.J (1994) G1 phase progression: cycling on cue Cell, 79 551-555
65. Shtivelman, E., Lifshitz, B., Gale, R.P. and Canaam, E. (1985) Fused transcript of abl and ber genes in chronic myelogenous leukaemia. Nature, 315, 550-554.
66. Slebos, R.J.C., Lee, M.H., Plunkett, B.S., Kessis, T.D. Williams, B.O., Jacks, T., Hedrick, L., Kastan, M.B. and Cho, K.R (1994) p53-dependent G1 arrest involves pRB-related proteins and is disrupted by the human papillomavirus 16 E7 oncoprotein. Proc. Natl Acad. Sci. USA, 91, 5320-5324.
67. Smith, M.R., DeGudicibus, S.J. and Stacey, D.W. (1986) Requirement for c-ras proteins during viral oncogene transformation Nature, 320, 540-543.
68. Stacey, D.W., Roudebush, M., Day, R., Mosser, S.D., Gibbs, J.B. and Feig, L.A. (1991) Dominant inhibitory Ras mutants demonstrate the requirement for Ras activity in the action of tyrosine kinase oncogenes. Oncogene, 6, 2297-2304.
69. Stam, K., Heisterkamp, N, Grosveld, G., De Klein, A., Verma, R.S., Coleman, M., Dosik, H. and Groffen, J. (1985) Evidence of a new chimeric bcr/c-abl mRNA in patients with chronic myelocytic leukemia and the Philadelphia chromosome. N. Engl. J. Med., 313, 1429-1433
70. Tybulewicz, V.L.J., Crawford, C.E., Jackson, P.K. and Mulligan, R.C. (1991) Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl protooncogene. Cell, 65, 1153-1164.
71. Underwood, M.R. and Fried, H.M. (1990) Characterization of nuclear localizing sequences derived from yeast ribosomal protein L29. EMBO J., 9, 91-99.
72. Vandromme, M., Cavadore, J.-C., Bonnieu, A., Froeschle, A., Lamb, N. and Fernandez, A. (1995) Two nuclear localization signals present m the basic-helix 1 domains of MyoD promote its active nuclear translocation and can function independently. Proc. Natl Acad. Sci. USA, 92, 4646-4650.
73. Van Etten, R.A., Jackson, P. and Baltimore, D. (1989) 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.
74. Van Etten, R.A., Jackson, P.K., Baltimore, D., Sanders, M.C., Matsudaira, P.T and Janmey, P.A. (1994) The C-terminus of the c-Abl tyrosine kinase contains distinct F- and G-actin binding domains with bundling activity. J. Cell Biol., 124, 325-340.
75. Van Etten, R.A., Debnath, J., Zhou, H. and Casasnovas, J.M. (1995) 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.
76. Vousden, K.H., Vojtesek, B., Fisher, C and Lane, D (1993) HPV-16 E7 or adenovirus E1A can overcome the growth arrest of cells immortalized with a temperature-sensitive p53. Oncogene, 8, 1697-1702.
77. Waga, S., Hannon, G.J., Beach, D. and Stillman, B. (1994) The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature, 369, 574-578.
78. Watanabe, S.M. and Witte, O N. (1983) Site-directed deletions of Abelson murine leukemia virus define 3′ sequences essential for transformation and lethality. J. Virol., 45, 1028-1036.
79. Welch, P.J. and Wang, J.Y.J (1993) A C-terminal protein-binding domain in the retinoblastoma protein regulates nuclear c-Abl tyrosine kinase in the cell cycle. Cell, 75, 779-790.
80. Wetzler, M., Talpaz, M., Van Etten, R.A., Hirsch-Ginsberg, C., Beran, M. and Kurzrock, R. (1993) Subcellular localization of Bcr, Abl, and Bcr-Abl proteins in normal and leukemic cells and correlation of expression with myeloid differentiation. J. Clin. Invest., 92, 1925-1939.
81. Wilson, I.A., Niman, H L., Houghten, R.A , Cherenson, A.R., Connolly, M.L and Lerner, R.A. (1984) The structure of an antigenic determinant in a protein. Cell, 37, 767-778.
82. Zacksenhaus, E., Bremner, R., Phillips, R A. and Gallie, B.L. (1993) A bipartite nuclear localization signal in the retinoblastoma gene product and its importance for biological activity. Mol. Cell. Biol., 13, 4588-4599.
83. Ziegler, S.F, Whitlock, C.A., Goff, S P., Gifford, A. and Witte, O.N. (1981) Lethal effect of the Abelson murine leukemia virus transforming gene product. Cell, 27, 477-486.