The activity of D-raf in Torso signal transduction is altered by serine substitution, N-terminal deletion, and membrane targeting

Developmental Biology

Volumn 175, Issue 2, 1996, Pages 191-204

  Baek, Kwang Hyun ^a   Fabian, John R ^b   Sprenger, Frank ^c   Morrison, Deborah K ^b   Ambrosio, Linda ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; PROTEIN SERINE THREONINE KINASE; RAF PROTEIN; SERINE;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME STRUCTURE; FEMALE; MALE; MEMBRANE BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 0029943160     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1996.0107     Document Type: Article

References (85)

1. Ambrosio, L., Mahowald, A. P., and Perrimon, N. (1989a). Requirement of the Drosophila rafhomologue for torso function. Nature 342, 288-291.
2. Ambrosio, L., Mahowald, A. P., and Perrimon, N. (1989b). l(1)pole hole is required maternally for pattern formation in the terminal regions of the embryo. Development 106, 145-158.
3. Ashburner, M. (1989). "Drosophila: A Laboratory Handbook." Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
4. Baek, K.-H., and Ambrosio, L. (1994). An efficient method for microinjection of mRNA into Drosophila embryos. BioTechniques 17, 1024-1026.
5. Biggs, W. H., III, Zavitz, K. H., Dickson, B., van der Straten, A., Brunner, D., Hafen, E., and Zipursky, S. L. (1994). The Drosophila rolled locus encodes a MAP kinase required in the sevenless signal transduction pathway. EMBO J. 13, 1628-1635.
6. Biggs, W. H., III, and Zipursky, S. L. (1992). Primary structure, expression, and signal-dependent tyrosine phosphorylation of a Drosophila homolog of extracellular signal-regulated kinase. Proc. Natl. Acad. Sci. USA 89, 6295-6299.
7. Bonner, T. I., Kerby, S. B., Gunnell, M. A., Mark, G. E., and Rapp, U. R. (1985). Structure and biological activity of human homologs of the raf/mil oncogene. Mol. Cell. Biol. 5, 1400-1407.
8. Brand, A., and Perrimon, N. (1994). Raf acts downstream of the EGF receptor to determine dorsoventral polarity during Drosophila oogenesis. Genes Dev. 8, 629-639.
9. Brönner, G., and Jäckle, H. (1991). Control and function of the terminal gap gene activity in the posterior pole region of the Drosophila embryo. Mech. Dev. 35, 205-211.
10. Bruder, J. T., Heidecker, G., and Rapp, U. R. (1992). Serum-, TPA-, and Ras-induced expression from Ap-1/Ets-driven promoters requires Raf-1 kinase. Genes Dev. 6, 545-556.
11. Brunner, S., Oellers, N., Szabad, J., Biggs, W. H., II, and Zipursky, S. L. (1994). A gain-of-function mutation in Drosophila MAP kinase activates multiple receptor tyrosine kinase signaling pathways. Cell 76, 875-888.
12. Campos-Ortega, J. A., and Hartenstein, V. (1985). "The Embryonic Development of Drosophila melangaster." Springer-Verlag, New York/Berlin.
13. Casanova, J., Furriols, M., McCormick, C. A., and Struhl, G. (1995). Similarities between trunk and spätzle, putative extracellular ligands specifying body patternin Drosophila. Genes Dev. 9, 2539-2544.
14. Casanova, J., and Struhl, G. (1989). Localized surface activity of torso, a receptor tyrosine kinase, specifies terminal body pattern in Drosophila. Genes Dev. 3, 2025-2038.
15. Choi, K.-Y., Satterberg, B., Lyons, D. M., and Elion, E. A. (1994). Ste 5 tethers mutipleprotein kinases in the MAP kinase cascade required for mating in S. cerevisiae. Cell 78, 499-512.
16. Chou, T. B., and Perrimon, N. (1992). Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila embryogenesis. Genetics 131, 643-653.
17. Cleghon, V., and Morrison, D. K. (1994). Raf-1 interacts with Fyn and Src in a non-phosphotyrosine-dependent manner. J. Biol. Chem. 269, 17749-17755.
18. Degelmann, A., Hardy, P. A., Perrimon, N., and Mahowald, A. P. (1986). Developmental analysis of the torso-like phenotype in Drosophila produced by a maternal effect locus. Dev. Biol. 115, 479-489.
19. Dent, P., Jelinek, T., Morrison, D. K., Weber, M. J., and Sturgill, T. W. (1995). Reversal of Raf-1 activation by purified and membrane-associated protein phosphatases. Science 268, 1902-1906.
20. Dickson, B., Sprenger, D., Morrisin, D. K., and Hafen, E. (1992). Raf functions downstream of Ras1 in the sevenless signal transduction pathway. Nature 360, 600-603.
21. Fabian, J. R., Morrison, D. K., and Daar, I. O. (1993). Requirement for Raf and MAP kinase function during the meiotic maturation of Xenopus oocytes. J. Cell. Biol. 122, 645-652.
22. Fabian, J. R., Vojtek, A. B., Cooper, J. A., and Morrison, D. K. (1994). A single amino acid change in Raf-1 inhibits Ras binding and alters Raf-1 function. Proc. Natl. Acad. Sci. USA 91, 5982-5986.
23. Fantl, W. J., Muslin, A. J., Kikuchi, A., Martin, J. A., MacNicol, A. M., Gross, R. W., and Williams, L. T. (1994). Activation of Raf-1 by 14-3-3 proteins. Nature 371, 612-614.
24. Foe, V. E., and Alberts, B. M. (1983). Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J. Cell Sci. 61, 31-70.
25. Freed, E., Symons, M., MacDonald, S. G., McCormick, F., and Ruggieri, R. (1994). Binding of 14-3-3 proteins to the protein kinase Raf and effects on its activation .Science 265, 1713-1716.
26. Fu, H., Xia, K., Pallas, D. C., Cui, C., Conroy, K., Narsimhan, R. P., Mamon, H., Collier, R., and Roberts, T. M. (1994). Interaction of the protein kinase Raf-1 with 14-3-3 proteins. Science 266, 126-129.
27. Heidecker, G., Huleihel, M., Cleveland, J. L., Kolch, W., Beck, T. W., Lloyd, P., Pawson, T., and Rapp, U. R. (1990). Mutational activation of c-raf-1 and definition of the minimal transforming sequence. Mol. Cell. Biol. 10, 2503-2512.
28. Henkemeyer, M., West, S. R., Gertler, F. B., and Hoffmann, F. M. (1990). A novel tyrosine kinase-independent function of Drosophila abl correlates with proper subcellular localization. Cell 63, 949-960.
29. Henkemeyer, M. J., Bennett, R. L., Gertler, F. B., and Hoffman, F. M. (1988). DNA sequence structure, and tyrosine kinase activity of the Drosophila Abelson proto-oncogene homolog. Mol. Cell. Biol. 8, 843-853.
30. Hou, X. S., Chou, T.-B., Melnick, M. B., and Perrimon, N. (1995). The torso receptor kinase can activate Raf in a Ras-independent pathway. Cell 81, 63-71.
31. Hsu, J.-C., and Perrimon, N. (1994). A temperature-sensitive MEK mutation demonstrates the conservation of the signaling pathways activated by receptor tyrosine kinase. Genes Dev. 8, 2176-2187.
32. Huang, W., Alessandrini, A., Crews, C. M., and Erikson, R. L. (1993). Raf-1 forms a stable complex with Mek1 and activates Mek1 by serine phosphorylation. Proc. Natl. Acad. Sci. USA 90, 10947-10951.
33. Irie, K., Gotoh, Y., Yashar, B. M., Errede, B., Nishida, E., and Matsumoto, K. (1994). Stimulatory effects of yeast and mammalian 14-3-3 proteins on the Raf proteinkinase. Science 265, 1716-1719.
34. Jelinek, T., Catling, A. D., Reuter, C. W. M., Moodie, S. A., Wolfman, A., and Weber, M. J. (1994). RAS and RAF-1 form a signalling complex with MEK-1 but not MEK-2. Mol. Cell. Biol. 14, 8212-8218.
35. Klinger, M. (1990). The organization of the antero-posterior axis. Semin. Cell Biol. 1, 151-160.
36. Kolch, W. G., Heidecker, G., Kochs, G., Hummel, R., Vahidi, H., Mischak, G., Finkenseller, D., Marme, D., and Rapp, U. R. (1993). Protien kinase C activates Raf-1 by direct phosphorylation. Nature 364, 249-252.
37. Krantz, J. E., Satterburg, B., and Elion, E. A. (1994). The MAP kinases Fus3 associates with and phosphorylates the upstream signaling component Ste5. Genes Dev. 8, 313-327.
38. Kunkel, T. A., Roberts, J. D., and Zakour, R. A. (1987). Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154, 367-382.
39. Leevers, S. J., Paterson, H. F., and Marshall, C. J. (1994). Requirement for Ras in Raf activation is overcome by targeting Raf to the plasma membrane. Nature 369, 411-414.
40. Lindsley, D. L., and Zimm, G. G. (1992). "The Genome of Drosophila Melanogaster." Academic Press, San Diego.
41. ras, an essential component of torso signaling in Drosophila. Genes Dev. 7, 621-632.
42. Lu, X., Perkins, L. A., and Perrimon, N. (1993b). The torso pathway in Drosophila: A model system to study receptor tyrosine kinase signal transduction. Development Suppl., 47-56.
43. Lu, X., Melnick, M. B., Hsu, J.-C., and Perrimon, N. (1994). Genetic and molecular analyses of mutations involved in Drosophila raf signal transduction. EMBO J. 13, 2592-2599.
44. Mark, G. E., MacIntyre, R. J., Digan, M. E., Ambrosio, L., and Perrimon, N. (1987). Drosophila melanogaster homolog of the raf oncogene. Mol. Cell. Biol. 7, 2134-2140.
45. Marshall, C. J. (1995). Specificity of receptor tyrosine kinase signaling: Transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 179-185.
46. Martin, J.-R., Raibaud, A., and Ollo, R. (1994). Terminal pattern elements in Drosophila embryo induced by the torso-like protein. Nature 367, 741-745.
47. Melnick, M. B., Perkins, L. A., Lee, M., Ambrosio, L., and Perrimon, N. (1993). Developmental and molecular characterization of mutations in the Drosophila-raf serine/threonine protein kinase. Development 118, 127-138.
48. Michaud, N. R., Fabian, J. R., Mathes, K. D., and Morrison, D. K. (1995). 14-3-3 is not essential for Raf-1 function: Identification of Raf-1 proteins that are biologically activated in a 14-3-3 and Ras-independent manner. Mol. Cell. Biol. 15, 3390-3397.
49. ras GMPPNP is dependent on B-Raf. Mol. Cell. Biol. 14, 7153-7162.
50. Moodie, S. A., Willumsen, B. M., Weber, M. J., and Wolfman, A. (1993). Complexes of Ras-GTP with Raf-1 and mitogen-activated protein kinase kinase. Science 260, 1658-1661.
51. Morrison, D. K. (1994). 14-3-3: Modulators of signaling proteins? Science 266, 56-57.
52. Morrison, D. K., Heidecker, G., Rapp, U. R., and Copeland, T. D. (1993). Identification of the major phosphorylation sites of the Raf-1 kinase. J. Biol. Chem. 268, 17309-17316.
53. Morrison, D. K., Kaplan, D. R., Excobedo, J. A., Rapp, U. R., Roberts, T. M., and Williams, L. T. (1989). Direct activation of the serine/ threonine kinase activity of Raf-1 through tyrosine phosphorylation by the PDGF β-receptor. Cell 58, 649-657.
54. Morrison, D. K., Kaplan, D. R., Rapp, U. R., and Roberts, T. M. (1988). Signal transduction from membrane to cytoplasm: Growth factors and membrane-bound oncogene products increase Raf-1 phosphorylation and associated protein kinase activity. Proc. Natl. Acad. Sci. USA 85, 8855-8859.
55. Nishida, Y., Hata, M., Ayaki, T., Ryo, M., Yamagata, M., Shimizu, K., and Nishizuka, Y. (1988). Proliferation of both somatic and germ cells is affected in the Drosophila mutants of raf protooncogene. EMBO J. 7, 775-781.
56. Nüsslein-Volhard, C. (1991). Determination of the embryonic areas of Drosophila. Development Suppl., 1-10.
57. Perrimon, N. (1993). The torso receptor protein-tyrosine kinase signaling pathway: An endless story. Cell 74, 219-222.
58. Perrimon, N., Mohler, D., Engstrom, L., and Mahowald, A. P. (1986). X-linked female sterile loci in Drosophila melanogaster. Genetics 113, 695-712.
59. Pignoni, F., Baldarelli, R., Steingrimmson, E., Diaz, R. J., Patapoutian, A., Merriam, J. R., and Lengyel, J. A. (1990). The Drosophila gene tailless is expressed at the embryonic termini and is a member of the steroid receptor superfamily. Cell 62, 151-163.
60. Pignoni, F., Stengrimsson, E., and Lengel, J. A. (1992). bicoid and the terminal system activates tailless expression in the early Drosophila embryo. Development 115, 239-251.
61. Pumiglia, K., Chow, Y.-H., Fabian, J., Morrison, D. K., Decker, S., and Jove, R. (1995). Raf-1 N-terminal sequences necessary for Ras-Raf interaction and signal transduction. Mol. Cell. Biol. 15, 398-406.
62. Rapp, U. R., Heidecker, G., Huleihel, M., Cleveland, J. L., Choi, T., Pawson, T., Ihle, J. N., and Anderson, W. B. (1988). raf family serine/threonine protein kinases in mitogen signal transduction. Cold Spring Harbor Symp. Quant. Biol. 53, 173-184.
63. Roberts, D. B. (1986). Basic Drosophila care and techniques. In "Drosophila: A Practical Approach." IRL Press, New York.
64. Samuels, M. L., Weber, J. M., Bishop, J. M., and McMahon, M. (1993). Conditional transformation of cells and rapid activation of the mitogen-activated protein kinase cascade by an estradiol-dependent human Raf-1 protein kinase. Mol. Cell.Biol. 13, 6241-6252.
65. Savant-Bhonsale, S., and Montell, D. J. (1993). torso-like encodes the localized determinant of Drosophila terminal pattern formation. Genes Dev. 7, 2548-2555.
66. Sprenger, F., and Nüsslein-Volhard, C. (1992). Torso receptor activity is regulated by a diffusible ligand produced at the extracellular terminal regions of the Drosophila egg. Cell 71, 987-1001.
67. Sprenger, F., Trosclair, M. M., and Morrison, D. K. (1993). Biochemical analysis of torso and D-raf during Drosophila embryogenesis: Implications for terminal signal transduction. Mol. Cell. Biol. 13, 1163-1172.
68. St. Johnston, D., and Nüsslein-Volhard, C. (1992). The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201-219.
69. Stancato, L. F., Chow, Y.-H., Hutchinson, K. A., Perdew, G. H., Jove, R., and Pratt, W. B. (1993). Raf exists in a native heterocomplex with hsp90 and p50 that can be reconstituted in a cell-free system. J. Biol. Chem. 268, 21711-21716.
70. Stanton, V. P., Jr., Nichols, D. W., Laudano, A. P., and Coper, G. M. (1989). Definition of the human raf amino-terminal regulatory region by deletion mutagenesis. Mol. Cell. Biol. 9, 639-647.
71. Stevens, L. M., Frohnhofer, H. G., Klinger, M., and Nüsslein-Volhard, C. (1990). Localized requirement for torso-like expression in follicle cells for development of terminal anlagen of the Drosophila embryo. Nature 346, 660-663.
72. Stokoe, D., MacDonald, S. G., Cadwallader, K., Symons, M., and Hancock, J. F. (1994). Activation of Raf as a result of recruitment to the plasma membrane. Science 264, 1463-1467.
73. Summers, M. D., and Smith, G. E. (1987). "A Manual of Methods for Baculovirus Vector and Insect Cell Culture Procedures." Texas Agricultural Experiment Station, College Station,TX.
74. Tsuda, L., Inoue, Y. H., Yoo, M.-A., Mizuno, M., Hata, M., Lim, Y.-M., Adachi-Yamada, T., Ryo, H., Masamune, Y., and Nishida, Y. (1993). A protein kinase similar to MAP kinase activator acts downstream of the Raf kinase in Drosophila. Cell 72, 407-414.
75. Van Aelst, L., Barr, M., Marcus, S., Polverino, A., and Wigler, M. (1993). Complex formation between RAS and RAF and other protein kinases. Proc. Natl. Acad. Sci. USA 90, 6213-6217.
76. van der Greer, P., Hunter, T., and Linderberg, R. A. (1994). Receptor protein-tyrosine kinases and their signal transduction pathways. Annu. Rev. Cell. Biol. 10, 251-338.
77. van der Meer, J. M. (1977). Optical clean and permanent whole mount preparation for phase-contrast microscopy of cuticular structures of insect larvae. DrosophilaInf. Service 52, 160.
78. Vieira, J., and Messing, J. (1987). Production of single-stranded plasmid DNA. Methods Enzymol. 153, 3-11.
79. Vojtek, A. B., Hollenberg, S. M., and Cooper, J. A. (1993). Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 74, 205-214.
80. Warne, P. H., Viciana, P. R., and Downard, J. (1993). Direct interaction of Ras and the amino-terminal region of Raf-1 in vitro. Nature 364, 352-355.
81. Wartmann, M., and Davis, R. J. (1994). The native structure of the activated Raf protein kinase is a membrane-bound multi-subunit complex. J. Biol. Chem. 269, 6695-6701.
82. Weigel, D., Jürgens, G., Küttner, F., Seifert, E., and Jäckle, H. (1989). The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell 57, 645-658.
83. Weischaus, E., and Nüsslein-Volhard, C. (1986). Looking at embryos. In "Drosophila: A Practical Approach." IRL Press, New York.
84. v-src are required, but neither alone is sufficient, to activate the Raf-1 kinase. Proc. Natl. Acad. Sci. USA 89, 2922-2926.
85. rasprotein binds to the amino-terminal regulatory domain of c-Raf-1. Nature 364, 308-313.