Abl-interactor-1, a novel SH3 protein binding to the carboxy-terminal portion of the Abl protein, suppresses v-abl transforming activity

Genes and Development

Volumn 9, Issue 21, 1995, Pages 2583-2597

  Shi, Yanggu ^b   Ålin, Kimona ^b   Goff, Stephen P ^b  

^a New York Presbyterian Columbia University Medical Center   (United States)

^b NONE

Author keywords

Abelson; leukemia; SH3 domain; tyrosine kinase

Indexed keywords

MESSENGER RNA; ONCOPROTEIN; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CARBOXY TERMINAL SEQUENCE; CHROMOSOME 2; ENZYME ACTIVITY; ENZYME REGULATION; GENE EXPRESSION REGULATION; GENE LOCATION; LEUKEMIA CELL; LYMPHOCYTE TRANSFORMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

ABELSON LEUKEMIA VIRUS; ANIMALIA;

EID: 0028844631     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.9.21.2583     Document Type: Article

References (83)

1. Abelson, H.T. and L.S. Rabstein. 1970a. Influence of prednisolone on Moloney leukemogenic virus in BALB/c mice. Cancer Res. 30: 2208-2212.
2. _. 1970b. Lymphosarcoma: Virus-induced thymic-independent disease in mice. Cancer Res. 30: 2213-2222.
3. Alt, F., N. Rosenberg, S. Lewis, E. Thomas, and D. Baltimore. 1981. Organization and reorganization of immunoglobulin genes in Abelson murine leukemia virus-transformed cells: Rearrangement of heavy but not light chain genes. Cell 27: 391-400.
4. Ausubel, F.M., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl. 1987. Current protocols in molecular biology. John Wiley/Greene, New York.
5. Baskaran, R., M.E. Dahmus, and J.Y. Wang. 1993. Tyrosine phosphorylation of mammalian RNA polymerase II carboxyl-terminal domain. Proc. Natl. Acad. Sci. 90: 11167-11171.
6. Bergold, P.J., J.A. Blumenthal, E.D. Andrea, H.W. Snyder, L. Lederman, A. Silverstone, H. Nguyen, and P. Besmer. 1987. Nucleic acid sequence and oncogenic properties of the HZ2 Feline sarcoma virus v-abl insert. J. Virol. 61: 1193-1202.
7. Blatt, C. and L. Sachs. 1988. Deletion of a homeobox gene in myeloid leukemias with a deletion in chromosome 2. Biochem. Biophys. Res. Commun. 156: 1265-1268.
8. Breier, G., G.R. Dressler, and P. Gruss. 1988. Primary structure and developmental expression pattern of Hox3.1, a member of the murine Hox3 homeobox gene cluster. EMBO J. 7: 1329-1336.
9. Chen, C. and H. Okayama. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7: 2745-2752.
10. Chen, Y.Y. and N. Rosenberg. 1992. Lymphoid cells transformed by Abelson virus require the v-abl tyrosine kinase only during early G1. Proc. Natl. Acad. Sci. 89: 6683-6687.
11. Chen, Y.Y., L.C. Wang, M.S. Huang, and N. Rosenberg. 1994. An active v-abl protein tyrosine kinase blocks immunoglobulin light-chain gene rearrangement. Genes & Dev. 8: 688-697.
12. Cicchetti, P., B.J. Mayer, G. Thiel, and D. Baltimore. 1992. Identification of a protein that binds to the SH3 region of Abl and is similar to Bcr and GAP-Rho. Science 257: 803-806.
13. Clark, S.G., M.J. Stern, and H.R. Horvitz. 1992. C. elegans cell-signalling gene sem-5 encodes a protein with SH2 and SH3 domains. Nature 356: 340-344.
14. Cohen, G.B., R. Ren, and D. Baltimore. 1995. Modular binding domains in signal transduction proteins. Cell 80: 237-248.
15. Dai, Z. and A.M. Pendergast. 1995. Aip-1, a novel SH3-containing nuclear protein is a substrate of the c-abl tyrosine kinase (this issue).
16. de Klein, A., A.G. van Kellel, G. Grosveld, C.R. Bartram, A. Hagemeijer, D. Bootsma, N.K. Spurr, N. Heisterkamp, J. Groffen, and J.R. Stephenson. 1982. A cellular oncogene is translocated to the Philadelphia chromosome in chronic myelocytic leukemia. Nature 300: 765-767.
17. Dunaief, J.L., B.E. Strober, S. Guha, P.A. Khavari, K. Alin, J. Luban, M. Begemann, G.R. Crabtree, and S.P. Goff. 1993. The retinoblastoma gene product and BRG1 form a complex and cooperate to induced cell cycle arrest. Cell 79: 119-130.
18. Feller, S.M., B. Knudsen, and H. Hanafusa. 1994. c-Abl kinase regulates the protein binding activity of c-Crk. EMBO J. 13: 2341-2351.
19. Fields, S. and O. Song. 1989. A novel genetic system to detect protein-protein interactions. Nature 340: 245-246.
20. Franz, W.M., P. Berger, and J.Y.J. Wang. 1989. Deletion of an N-terminal regulatory domain of the c-abl tyrosine kinase activates its oncogenic potential. EMBO J. 8: 137-147.
21. Goff, S.P., E. Gilboa, O.N. Witte, and D. Baltimore. 1980. Structure of the Abelson murine leukemia virus genome and the homologous cellular gene: Studies with cloned viral DNA. Cell 22: 777-786.
22. Goff, S.P., P. Traktman, and D. Baltimore. 1981a. Isolation and properties of Moloney murine leukemia virus mutants: use of a rapid assay for release of virion reverse transcriptase. J. Virol. 38: 239-248.
23. Goff, S.P., O.N. Witte, E. Gilboa, N. Rosenberg, and D. Baltimore. 1981b. Genome structure of Abelson murine leukemia virus variants: Proviruses in fibroblasts and lymphoid cells. J. Virol. 38: 460-468.
24. Goga, A., J. McLaughlin, A.M. Pendergast, K. Parmar, A. Muller, N. Rosenberg, and O.N. Witte. 1993. Oncogenic activation of c-ABL by mutation within its last exon. Mol. Cell. Biol. 13: 4967-4975.
25. Hanes, S.D. and R. Brent. 1989. DNA specificity of the bicoid activator protein is determined by homeodomain recognition helix residue 9. Cell 57: 1275-1283.
26. Hevezi, P., K. Alin, R. Rees-Jones, and S.P. Goff. 1992. Bone marrow-transforming activity of linker insertion mutants of Abelson murine leukemia virus. Oncogene 7: 2323-2328.
27. Hevezi, P., K. Alin, and S.P. Goff. 1993. Transforming activity and tissue tropism of hybrid retroviral genomes containing portions of the v-abl and v-src oncogenes. Oncogene 8: 2413-2423.
28. Jackson, P. and D. Baltimore. 1989. N-terminal mutations activate the leukemogenic potential of the myristylated form of c-abl. EMBO J. 8: 449-456.
29. Jackson, P.K., M. Paskind, and D. Baltimore. 1993. Mutation of a phenylalanine conserved in SH3-containing tyrosine kinases activates the transforming ability of c-Abl. Oncogene 8: 1943-1956.
30. Jackson, S.H., H.L. Malech, C.A. Kozak, K.J. Lomax, J.I. Gallin, and S.M. Holland. 1994. Cloning and functional expression of the mouse homologue of p47phox. Immunogenetics 39: 272-275.
31. Kalpana, G.V., S. Marmon, W. Wang, G.R. Crabtree, and S.P. Goff. 1994. Binding and stimulation of HIV-1 integrase by a human homolog of yeast transcription factor SNF5. Science 266: 2002-2006.
32. Katzav, S., D. Martin-Zanca, and M. Barbacid. 1989. Vav, a novel human oncogene derived from a locus ubiquitously expressed in hematopoietic cells. EMBO J. 8: 2283-2290.
33. Kerr, L.D. 1994. Arrested development: understanding v-abl. BioEssays 16: 453-455.
34. Kipreos, E.T. and J.Y.J. Wang. 1992. Cell cycle-regulated binding of c-abl tyrosine kinase to DNA. Science 256: 382-385.
35. Klug, C.A., S.J. Gerety, P.C. Shah, Y.Y. Chen, N.R. Rice, N. Rosenberg, and H. Singh. 1994. The v-abl tyrosine kinase negatively regulates NF-κ-B/Rel factors and blocks Kgene transcription in pre-B lymphocytes. Genes &. Dev. 8: 678-687.
36. Koch, C.A., D. Anderson, M.F. Moran, C. Ellis, and T. Pawson. 1991. SH2 and SH3 domains: Elements that control interactions of cytoplasmic signalling proteins. Science 252: 668-674.
37. Kruh, G.D., R. Perego, T. Miki, and S.A. Aaronson. 1990. The complete coding sequence of arg defines the abelson subfamily of cytoplasmic tyrosine kinases. Proc. Natl. Acad. Sci. 87: 5802-5806.
38. Lai, Z.-C. and G.M. Rubin. 1992. Negative control of photoreceptor development in Drosophila by the product of the yan gene, an ETS domain protein. Cell 70: 609-620.
39. Lehmann, J.M., G. Riethmuller, and J.P. Johnson. 1990. Nck, a melanoma cDNA encoding a cytoplasmic protein consisting of the src homology units SH2 and SH3. Nucleic Acids Res. 18: 1048.
40. Lowenstein, E.J., R.J. Daley, A.G. Batzer, W. Li, B. Margolis, R. Lammers, A. Ullrich, E.Y. Skolnik, D. Bar-Sagi, and J. Schlessinger. 1992. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to Ras signalling. Cell 70: 431-442.
41. Luban, J., K. Alin, K. Bossolt, T. Humaran, and S. Goff. 1992. Genetic assay for multimerization of retroviral gag polyproteins. J. Virol. 66: 5157-5160.
42. Maniatis, T., E.F. Fristch, and J. Sambrook. 1982. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
43. Matuoka, K., M. Shibata, A. Yamakawa, and T. Takenawa. 1992. Cloning of ASH, a ubiquitous protein composed of one src homology region (SH)2 and two SH3 domains, from human and rat cDNA libraries. Proc. Natl. Acad. Sci. 89: 9015-9019.
44. Mayer, B.J. and D. Baltimore. 1994. Mutagenic analysis of the roles of SH2 and SH3 domains in regulation of the Abl tyrosine kinase. Mol. Cell. Biol. 14: 2883-2894.
45. Mayer, B.J., P.K. Jackson, and D. Baltimore. 1991. The noncatalytic src homology region 2 segment of abl tyrosine kinase binds to tyrosine-phosphorylated cellular proteins with high affinity. Proc. Natl. Acad. Sci. 88: 627-631.
46. Mayer, B.J., P.K. Jackson, R.A. Van Etten, and D. Baltimore. 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.
47. Mazo, A.M., D.-H. Huang, B.A. Mozer, and I.B. Dawid. 1990. The trithorax gene, a trans-acting regulator of the bithorax complex in Drosophila, encodes a protein with zinc-binding domains. Proc. Natl. Acad. Sci. 87: 2112-2116.
48. McWhirter, J.R. and J.Y. Wang. 1993. An actin-binding function contributes to transformation by the Bcr-Abl oncoprotein of Philadelphia chromosome-positive human leukemias. EMBO J. 12: 1533-1546.
49. Miglarese, M.R., J. Mannion-Henderson, H. Wu, J.T. Parsons, and T.P. Bender. 1994. The protein tyrosine kinase substrate cortactin is differentially expressed in murine B lymphoid tumors. Oncogene 9: 1989-1997.
50. Muller, A.J., J.C. Young, A.M. Pendergast, M. Pondel, N.R. Landau, D.R. Littman, and O.N. Witte. 1991. BCR first exon sequences specifically activate the BCR/ABL tyrosine kinase oncogene of Philadelphia chromosome-positive human leukemias. Mol. Cell. Biol. 11: 1785-1792.
51. Murtagh, K., G. Skladany, J. Hoag, and N. Rosenberg. 1986. Abelson murine leukemia virus variants with increased oncogenic potential. J. Virol. 60: 599-606.
52. Nichols, G.L., M.A. Raines, J.C. Vera, L. Lacomis, P. Tempst, and D.W. Golde. 1994. Identification of CRKL as the constitutively phosphorylated 39-kD tyrosine phosphoprotein in chronic myelogenous leukemia cells. Blood 84: 2912-2918.
53. Parmar, K., R.C. Huebner, and N. Rosenberg. 1991. Carboxyl-terminal determinants of Abelson protein important for lymphoma induction. J. Virol. 65: 6478-6485.
54. Pawson, T. 1992. SH2 and SH3 domains. Curr. Opin. Struct. Biol. 2: 432-437.
55. Pendergast, A.M., A.J. Muller, M.H. Havlik, Y. Maru, and O.N. Witte. 1991. BCR sequences essential for transformation by the BCR-ABL oncogene bind to the ABL SH2 regulatory domain in a non-phosphotyrosine-dependent manner. Cell 66: 161-171.
56. Prywes, R., J.G. Foulkes, N. Rosenberg, and D. Baltimore. 1983. Sequences of the A-MuLV protein required for fibroblast and lymphoid cell transformation. Cell 34: 569-579.
57. Reddy, B.A., M. Kloc, and L.D. Etkin. 1992. The cloning and characterization of a localized maternal transcript in Xenopus laevis whose zygotic counterpart is detected in the CNS. Mech. Dev. 39: 143-150.
58. Ren, R., B.J. Mayer, P. Cicchetti, and D. Baltimore. 1993. Identification of a 10-amino acid proline-rich SH3 binding site. Science 259: 1157-1161.
59. Ren, R., Z.S. Ye, and D. Baltimore. 1994. Abl protein-tyrosine kinase selects the Crk adapter as a substrate using SH3-binding sites. Genes & Dev. 8: 783-795.
60. Renshaw, M.W., E.T. Kipreos, M.R. Albrecht, and J.Y.J. Wang. 1992. Oncogenic v-abl tyrosine kinase can inhibit or stimulate growth, depending on the cell context. EMBO J. 11: 3941-3951.
61. Renucci, A., V. Zappavigna, J. Zakany, J.C. Izpisua-Bemonte, K. Burki, and D. Deboule. 1992. Comparison of mouse and human Hox4.4 complexes defines conserved sequences involved in the regulation of Hox4.4. EMBO J. 11: 1459-1468.
62. Rogers, S., R. Wells, and M. Rechsteiner. 1986. Amino acid sequences common to rapidly degraded proteins: The PEST hypothesis. Science 234: 364-368.
63. Rosenberg, N. 1994. Abl-mediated transformation, immunoglobulin gene rearrangements and arrest of B lymphocyte differentiation. Semin. Cancer Biol. 5: 95-102.
64. Rosenberg, N. and O.N. Witte. 1980. Abelson leukemia virus mutants with alterations in virus-specific P120 molecule. J. Virol. 33: 340-348.
65. Rosenberg, N., D. Baltimore, and C.D. Scher. 1975. In vitro transformation of lymphoid cells by Abelson murine leukemia virus. Proc. Natl. Acad. Sci. 72: 1932-1936.
66. Rosenberg, N.E., D.R. Clark, and O.N. Witte. 1980. Abelson murine leukemia virus mutants deficient in kinase activity and lymphoid cell transformation. J. Virol. 36: 766-774.
67. Rowe, L.B., J.H. Nadeau, R. Turner, W.N. Frankel, V.A. Letts, J.T. Eppig, M.S.H. Ko, S.J. Thurston, and E.H. Birkenmeier. 1994. Maps from two interspecific backcross DNA panels available as a community genetic mapping reserve. Mamm. Genome 5: 253-274.
68. Rowley, J.D. 1993. Rearrangements involving chromosome band 11Q23 in acute leukaemia. Semin. Cancer Biol. 4: 377-385.
69. Salama, S., K. Hendricks, and J. Thorner. 1994. G1 cyclin degradation: The PEST motif of yeast cln2 is necessary but not sufficient for rapid protein turnover. Mol. Cell. Biol. 14: 7953-7966.
70. Sawyers, C.L. 1993. The role of myc in transformation by BCR-ABL. Leuk. Lymphoma 1: 45-46.
71. Sawyers, C.L., W. Callahan, and O.N. Witte. 1992. Dominant negative MYC blocks transformation by ABL oncogenes. Cell 70: 901-910.
72. Scher, C.D. and R. Siegler. 1975. Direct transformation of 3T3 cells by Abelson murine leukemia virus. Nature 253: 729-731.
73. Schuuring, E., E. Verhoeven, S. Litvinuv, and R.J.A.M. Michalides. 1993. The product of the EMS1 gene, amplified and overexpressed in human carcinomas, is homologous to a v-src substrate and is located in cell-substratum contact sites. Mol. Cell. Biol. 13: 2891-2898.
74. Schwartz, D.E., R. Tizard and W. Gilbert. 1983. Nucleotide sequence of Rous sarcoma virus. Cell 32: 853-869.
75. Schwartzberg, P.L., A.M. Stall, J.D. Hardin, K.S. Bowdish, T. Humaran, S. Boast, M.L. Harbison, E.J. Robertson, and S.P. Goff. 1991. Mice homozygous for the ablm1 mutation show poor viability and depletion of selected B and T cell populations. Cell 65: 1165-1175.
76. Tanaka, M. and W. Herr. 1990. Differential transcriptional activation by Oct-1 and Oct-2: Interdependent activation domains induce Oct-2 phophorylation. Cell 60: 375-386.
77. Tybulewicz, V.L.J., C.E. Crawford, P.K. Jackson, R.T. Bronson, and R.C. Mulligan. 1991. Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl protooncogene. Cell 65: 1153-1163.
78. Van Etten, R.A., P. Jackson, and D. Baltimore. 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.
79. Van Etten, R.A., P.K. Jackson, D. Baltimore, M.C. Sanders, P.T. Matsudaira, and P.A. Janmey. 1994. 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.
80. Wang, J.Y.J. 1993. Abl tyrosine kinase in signal transduction and cell-cycle regulation. Curr. Opin. Genet. Dev. 3: 35-43.
81. Watanabe, S.M. and O.N. Witte. 1983. Site-directed deletions of Abelson murine leukemia virus define 3′ sequences essential for transformation and lethality. J. Virol. 45: 1028-1036.
82. Welch, P.J. and J.Y. Wang. 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.
83. Zeigler, S.F., C.A. Whitlock, S.P. Goff, A. Gifford, and O.N. Witte. 1981. Lethal effect of the Abelson murine leukemia virus transforming product. Cell 27: 477-486.