Negative regulation of pl20gap gtpase promoting activity by p210bcr/abl: Implication for ras-dependent philadelphia chromosome positive cell growth

Journal of Experimental Medicine

Volumn 179, Issue 6, 1994, Pages 1855-1865

  Skorski, Tomasz ^a   Kanakaraj, Palanisamy ^a   Ku, De Hui ^a   Nieborowska Skorska, Malgorzata ^a   Canaani, Eli ^a   Zon, Gerald ^b   Perussia, Bice ^a   Calabretta, Bruno ^a  

^a THOMAS JEFFERSON UNIVERSITY HOSPITAL   (United States)

^b ILLUMINA INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; GUANOSINE TRIPHOSPHATASE; NEUROMODULIN; PROTEIN P21;

ARTICLE; CELL PROLIFERATION; CHRONIC MYELOID LEUKEMIA; DOWN REGULATION; ENZYME ACTIVATION; ENZYME REGULATION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; ONCOGENE C MYB; PHILADELPHIA 1 CHROMOSOME; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

BASE SEQUENCE; CELL DIVISION; CELL LINE; CHROMOSOMES, HUMAN, PAIR 15; CHROMOSOMES, HUMAN, PAIR 17; CHROMOSOMES, HUMAN, PAIR 22; CHROMOSOMES, HUMAN, PAIR 9; FUSION PROTEINS, BCR-ABL; GENE EXPRESSION REGULATION, NEOPLASTIC; GTP PHOSPHOHYDROLASES; GTPASE-ACTIVATING PROTEINS; HOMEOSTASIS; HUMAN; LEUKEMIA, MYELOID, CHRONIC; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDES, ANTISENSE; ONCOGENES; PHILADELPHIA CHROMOSOME; PROTEINS; PROTO-ONCOGENE PROTEIN P21(RAS); PROTO-ONCOGENES; RAS GTPASE-ACTIVATING PROTEINS; SIGNAL TRANSDUCTION; SUPPORT, NON-U.S. GOV'T; SUPPORT, U.S. GOV'T, P.H.S.; TRANSLOCATION (GENETICS); TUMOR CELLS, CULTURED;

EID: 0028263606     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.179.6.1855     Document Type: Article

References (71)

1. Shtivelman, E., B. Lifshitz, R.P. Gale, B.A. Roe, and E. Canaani. 1985. Fused transcript of ahl and her genes in chronic myelogenous leukemia. Nature (Lond.). 315:550.
2. Epner, D.E., and H.P. Koeffler. 1990. Molecular genetics advances in chronic myelogenous leukemia. Ann. Int. Med. 113:3.
3. Clark, S.S., J. McLaughlin, M. Timmonis, A.M. Fendergast, Y. Ben-Neriah, L. Dow, G. Rovera, S.D. Smith, and O.N. Witte. 1988. Expression of a distinctive bcr-abl oncogene in Ph'-positive acute lymphoblastic leukemia (ALL). Science (Wash. DC). 239:775.
4. McLaughlin, J., E. Chianese, and O.N. Witte. 1987. In vitro transformation of immature hematopoietic cells by the P210 BCRJABL oncogene product of the Philadelphia chromosome. Proa Natl. Acad. Sci. USA. 84:6558.
5. Gishizky, M.L, and O.N. Witte. 1992. Initiation of deregulated growth of multipotent progenitor cells by bcr-abl in vitro. Science (Wash. DC). 256:836.
6. KrJMgene of the Philadelphia chromosome. Science (Wash. DC). 247:824.
7. Heisterkamp, N., G. Jenster, J. ten Hoeve, D. Zovich, P.K. Pattengale, and J. Groflen. 1990. Acute leukemia in bcr-abl transgenic mice. Nature (Lond.). 344:251.
8. Elefanty, A.G., I.K. Hariharan, and S. Cory. 1990. bcr-abl, the hallmark of chronic myeloid leukemia in man, induces multiple haemotopoietic neoplasms in mice. EMBO(Eur. Mol. Biol. Organ.) J. 9:1069.
9. Kelliher, M.A., J. McLaughlin, O.N. Witte, and N. Rosenberg. 1990. Induction of a chronic myelogenous leukemia-like syndrome in mice with v-abl and BCRJABL. Proc Natl. Acad. Sci. USA. 87:6649.
10. Szczylik, C., T. Skorski, N.C. Nicolaides, L. Manzella, L. Malaguamera, D. Venturelli, A.M. Gewirtz, and B. Calabretta. 1991. Selective inhibition of leukemia cell proliferation by BCR-BAL antisense oligodeoxynucleotides. Science (Wash. DC). 253:562.
11. 1 leukemia cell growth in mice by bcrJabl antisense oligodeoxynucleotides. Proc Natl. Acad. Sci. USA. In press.
12. Lugo, T.G., A.M. Fendergast, A.J. Muller, and O.N. Witte. 1990. Tyrosine kinase activity and transformation potency of bcr-abl oncogene products. Science (Wash. DC). 247:1079.
13. Fendergast, 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 the ABL SH2 regulatory domain in a non-phosphorotyrosine-dependent manner. Cell. 66:161.
14. Dhut, S., T. Champlin, and B.D. Young. 1990. BCR-ABL and ABL proteins: biochemical characterization and localization. Leukemia. 4:745.
15. Mulcahy, L.S., M.R. Smith, and D.W. Stacey. 1985. Requirement for ms proto-oncogene function during serum-stimulated growth of NIH 3T3 cells. Nature (Lond.). 313:241.
16. Smith, M.R., S.J. DeGudicibus, and D.W. Stacey. 1986. Requirement for c-ras proteins during viral oncogene transformation. Nature (Land.). 320:540.
17. Skorski, T., C. Szczylik, M.Z. Ratajczak, L. Malaguamera, A. Gewirtz, and B. Calabretta. 1992. Growth factor-dependent inhibition of normal hematopoiesis by N-ras antisense oligodeoxynucleotides. J. Exp. Med. 175:743.
18. Bollag, G., and F. McCormick. 1991. Regulators and effectors of ras proteins. Amu. Rev. Cell Biol. 7:601.
19. Downward, J. 1992. Regulatory mechanisms for ras proteins. Bioassays. 14:177.
20. Lowenstein, E.J., R.J. Daly, A.G. Batzer, W. Li, B. Margolis, R. Lammers, A. Ullrich, E.Y. Skolnik, D. Bar-Sag, andj. Schles-singer. 1992. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signalling. Cell. 70:431.
21. Egan, S.E., B.W. Giddings, M.W. Brooks, L. Buday, A.M. Sizeland, and R.A. Weinberg. 1993. Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation. Nature (Lond). 363:45.
22. Fendergast, A.M., L.A. Quilliam, L.D. Cripe, C.H. Bassign, Z. Dal, N. Li, A. Batzer, K.M. Rabun, C.J. Der, J. Schles-singer, and M. Gishizky. 1993. BCR-ABL-induced oncogenesis is mediated by direct interaction with the SH2 domain of the GRB-2 adaptor protein. Cell. 75:175.
23. Ballester, R., D. Marchuk, M. Boguski, A. Saulino, R. Letcher, M. Wigler, and F. Collins. 1990. The NF1 locus encodes a protein functionally related to mammalian GAP and yeast IRA proteins. Cell. 63:851.
24. Martin, G.A., D. Viskochil, G. Bollag, P.C. McCabe, W.J. Crosier, H. Haubruck, L. Conroy, R. Clark, P. O’Connell, R.M. Cawthon, et al. 1990. The GAP-related domain of the neurofibromatosis type 1 gene product interacts with ms p21. Cell. 63:843.
25. Trahey, M., and F. McCormick. 1987. A cytoplasmic protein stimulates normal N-ras p21 GTPase, but does not affect oncogenic mutants. Science (Wash. DC). 238:542.
26. Vogel, U.S., R.A.F. Dixon, M.D. Schaber, R.E. Diehl, M.S. Marshall, E.M. Scolnick, I.S. Sigal, and J.B. Gibbs. 1988. Cloning of bovine GAP and its interaction with oncogenic ras p21. Nature (Lond). 335:90.
27. Muller, A.J., A.M. Pfendergast, M.H. Havlik, L. Puil, T. Pawson, and O.N. Witte. 1992. A limited set of SH2 domains binds BCR through a high-affinity phosphorotyrosine-indepen-dent interaction. Mol. Cell. Biol. 12:5087.
28. Druker, R, K. Okuda, U. Matulonis, R. Saiga, T. Roberts, and J.D. Griffin. 1992. Tyrosine phosphorylation of rasGAP and associated proteins in chronic myelogenous leukemia cell lines. Blood. 79:2215.
29. Ellis, E., M. Moran, F. McCormick, and T. Pawson. 1990. Phosphorylation of GAP and GAP-associated proteins by transforming and mitogenic tyrosine kinases. Nature (Lond.). 343:377.
30. r“‘GTPase-activating protein. Mol. Cell. Biol. 11:1804.
31. Molloy, C.J., D.P. Bottaro, T.P. Fleming, M.S. Marshall, J.B. Gibbs, and S.A. Aaronson. 1989. PDGF induction of tyrosine phosphorylation of GTPase activating protein. Nature (Lond.). 342:711.
32. McCormick, F. 1989. ms GTPase activating protein: signal transmitter and signal terminator. Cell. 56:5.
33. Medema, R.H., W.L. DeLaat, G.A. Martin, F. McCormick, and J.L. Bos. 1992. GTP-ase-activating protein SH2-SH3 domains induce gene expression in a Ras-dependent fashion. Mol. Cell. Biol. 12:3425.
34. Duchesne, M., F. Schweighoffer, F. Parker, F. Clerc, Y. Frobert, M.N. Thang, andB. Tocquye. 1993. Identification ofSFI3 domain of GAP as an essential sequence for Ras-GAP-mediated signalling. Science (Wash. DC). 259:525.
35. Skorski, T., P. Kanakaraj, M. Nieborowska-Skorska, M. Ratajczak, C. Szczylik, G. Zon, R.B. Arlinghaus, A. Gewirtz, B. Ferussia, and B. Calabretta. 1993. pl20 GAP requirement in normal and malignant human hematopoiesis. J. Exp. Med. 178:1923.
36. 1 positive human cell line (BV173). J. Natl. Cancer Inst. 70:447.
37. Lanotte, M., V. Martin-Thouvenin, S. Najman, P. Balerini, F. Valensi, and R. Berger. 1991. NB4, a maturation inducible cell line with t(15;17) marker isolated from a human acute promyelocytic leukemia (M3). Blood. 77:1080.
38. Collins, S.J., R.C. Gallo, and R.E. Gallagher. 1977. Continuous growth and differentiation of human myeloid leukemic cells in suspension culture. Nature (Lond). 270:347.
39. Gluzman, Y. 1981. SV40-transformed simian cells support the replication of early SV40 mutants. Cell 23:175.
40. Shen, Y.M., R.R. Hirschom, W.E. Mercer, E. Surmacz, Y. Tsutsui, K.J. Soprano, and R. Baserga. 1982. Gene transfer: DNA microinjection compared with DNA transfection with a very high efficiency. Mol. Cell. Biol. 2:1145.
41. Shtivelman, E., R Lifshitz, R.P. Gale, B.A. Roe, and E. Canaani. 1986. Alternative splicing of RNAs transcribed from the human ahl gene and from the bcr-abl fused gene. Cell. 47:277-284.
42. Majello, B., L.C. Kenyon, and R. Dalla Favera. 1986. Human c-myb protooncogene: nucleotide sequence of cDNA and organization of the genomic locus. Proc. Natl. Acad. Sci. USA. 83:9636-9640.
43. Capon, D.J., E.Y. Chen, A.D. Levinson, P.H. Seeburg, and D.V. Goeddel. 1983. Complete nucleotide sequences of the T24 human bladder carcinoma oncogene and its normal homologue. Nature (Lond). 302:33.
44. Kahn, S., F. Yamamoto, C. Almoguera, E. Winter, K. Forrester, J. Jordan, and M. Ferucho. 1987. The c-K-ras gene and human cancer. Anticancer Res. 7:639.
45. Hall, A., and R. Brown. 1985. Human N-n*s: cDNA cloning and gene structure. Nucleic Acids Res. 13:5255.
46. Huttner, K.M., J.A. Barbosa, G.A. Scangos, D.D. Pratcheva, and F.H. Ruddle. 1982. DNA-mediated gene transfer without carrier DNA. J. Cell Biol 91:153-156.
47. Clarke, M.F., J.F. Kukowska-Latallo, E. Westin, M. Smith, and E.V. Prochownik. 1988. Constitutive expression of a c-myb cDNA blocks Friend murine erythroleukemia cell differentiation. Mol. Cell. Biol 8:884.
48. Campbell, M.L., W. Li, and R.R Arlinghaus. 1990. P210 BCR-ABL is complexed to pl60 BCR and ph-P53 protein in K562 cells. Oncogene. 5:773.
49. Downward, J., J.D. Graves, P.H. Wame, S. Rayter, and D.A. Cantrell. 1990. Stimulation of p21"“upon T-cell activation. Nature (Lond.). 346:719.
50. Gibbs, J.B., M.S. Marshall, E.M. Scolnick, R.A.F. Dixon, and U.S. Vogel. 1990. Modulation of guanine nucleotides bound to Ras in NIH3T3 cells by oncogenes, growth factors, and the GTPase activating protein (GAP).J. Biol Chem. 265:20437.
51. Bollag, G., and F. McCormick. 1991. Differential regulations of rasGAP and neurofibromatosis gene product activities. Nature (Lond.). 357:576.
52. Brown, D., A. Yu, P. Miller, K. Blake, C. Wei, H.-F. Kung, R.J. Black, P.O.P. Tso, and E.H. Chang. 1989. Modulation of ms expression by anti-sense nonionic deaxynudeotide analogs. Oncogene Research. 4:243.
53. Daaka, Y., and E. Wickstrom. 1990. Target dependence of antisense oligodeoxynucleotide inhibition of c-Ha-ras p21 expression and focus fonnation in T24-transformed NIH 3T3 cells. Oncogene Research. 5:267.
54. Janssen, J.W.G., A.C.M. Steenvoorden, J. Lyons, B. Anger, J.U. Bohlke, J.L. Bos, H. Seliger, and C. Bartram. 1987. RAS gene mutations in acute and chronic myelocytic leukemias, chronic myeloproliferative disorders, myelodysplastic syndromes. Proc Natl. Acad. Sci. USA. 84:9228.
55. Collins, S.J., M. Howard, D.F. Andrews, E. Agura, and J. Radich. 1989. Rare occurrence of N-ras point mutations in Philadelphia chromosome positive chronic myeloid leukemia. Blood. 73:1028.
56. Ahuja, H.G., A. Foti, M. Bar-Eli, and M.J. Cline. 1990. The pattern of mutational involvement of ILAS genes in human hematologic malignancies determined by DNA amplification and direct sequencing. Blood. 75:1684.
57. Lazarus, A.H., K. Kawauchi, M.J. Rapoport, and T.L. Delovitch. 1993. Antigen-induced B lymphocyte activation involves the p21and ras.GAP signaling pathway. J. Exp. Med. 178:1765.
58. Buday, L., and J. Downward. 1993. Epidermal growth factor regulates p21through the fonnation of a complex of receptor, Grb2 adaptor protein, and Sos nucleotide exchange factor. Cell. 73:611.
59. Serth, J., W. Weber, M. Freeh, R.A. Wittinghofe, and A. Pingoud. 1992. Binding the H-ras p21 GTPase activating protein by the activated epidermal growth factor receptor leads to inhibition of the p21 GTPase activity in vitro. Biochemistry. 31:6361.
60. Li, B.-Q., D. Kaplan, H. Rung, and T. Kamata. 1992. Nerve growth factor stimulation of ras-guanine nucleotide exchange factor and GAP activities. Science (Wash. DC). 256:1456.
61. McWhirter, J.R., and TV.J. Wang. 1991. Activation of tyrosine kinase and microfilament-binding functions of c-ahl by ber sequences in bcrJabl fusion proteins. Mol. Cell. Biol. 11:1553.
62. Settleman, J., V. Narasimhan, L.C. Foster, and R.A. Weinberg. 1992. Molecular cloning of cDNAs encoding the GAP-associated protein p!90: implications for a signalling pathway from RAS to the nucleus. Cell. 69:539.
63. Chang, J.H., L.K. Wilson, J.S. Moyers, K. Zhang, and S.J. Parson. 199. Increased levels of p21"“-GTP and enhanced DNA synthesis accompany elevated tyrosyl phosphorylation of GAP-associated proteins, pl90 and p62, in c-scr overexpressors. Oncogene. 8:959.
64. Hall, A. 1990. ms and GAP—Who’s controlling whom? Cell. 61:921.
65. Marshall, M.S., W.S. Hill, S.N. Assunta, U.S. Vogel, M.D. Schaber, E.M. Scolnick, R.A.F. Dixon, I.S. Sigal, and J.B. Gibbs. 1989. A C-terminal domain of GAP is sufficient to stimulate ras p21GTPase activity. EMBO (Eur. Mol Biol Organ.) J. 8:1105.
66. Moran, M.F., C.A. Koch, D. Anderson, C. Ellis, L. England, G.S. Martin, and T. Pawson. 1990. Src homology region 2 domains direct protein-protein interactions in signal transduction. Proc. Natl. Acad. Sci. USA. 87:8622.
67. Adari, H., D.R. Lowy, B.M. Willumsen, C.J. Der, and F. McCormick. 1988. Guanosine triphosphatase activating protein (GAP) interacts with the p21effector binding domain. Science (Wash. DC). 240:518.
68. Wong, G., O. Muller, R. Clarke, L. Conroy, M.F. Moran, P. Folakis, and F. McCormick. 1992. Molecualr cloning and nucleic acid binding properties of the GAP-associated tyrosine phosphoprotein p62. Cell. 69:551.
69. 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 BCRJABL tyrosine kinase oncogene of Philadelphia chromosome-positive human leukemias. Mol. Cell. Biol. 359:153.
70. Hubert, P., P. Debr6, L. Boumsell, and G. Bismuth. 1993. Tyrosine phosphorylation and association with phospholipase Cy-l of the GAP-associated 62-kD protein after CD2 stimulation of Jurkat T cell. J. Exp Med. 178:1587.
71. Settleman, J., C.F. Albright, L.C. Foster, and R. Weinberg. 1992. Association between GTPase activators for Rho and Ras families. Nature (Lond.). 359:153.