Inhibition of the Raf-1 kinase by cyclic AMP agonists causes apoptosis of v-abl-transformed cells

Molecular and Cellular Biology

Volumn 17, Issue 6, 1997, Pages 3229-3241

  Weissinger, Eva M ^a   Eissner, Günther ^a   Grammer, Christine ^a   Fackler, Susanne ^a   Haefner, Burkhard ^a   Yoon, Luke S ^b   Lu, Kimberly S ^b   Bazarov, Alex ^b   Sedivy, John M ^b,c   Mischak, Harald ^a   Kolch, Walter ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; 5,6 DICHLOROBENZIMIDAZOLE RIBOSIDE; 8 BROMO CYCLIC AMP; 8 CHLOROADENOSINE 3',5' PHOSPHATE; BCR ABL PROTEIN; BUCLADESINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DERIVATIVE; CYTIDINE TRIPHOSPHATE; ESTROGEN; FORSKOLIN; MITOGEN ACTIVATED PROTEIN KINASE; MYC PROTEIN; PHOSPHOROTHIOIC ACID DERIVATIVE; PROTEIN TYROSINE KINASE INHIBITOR; RAF PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL STRAIN 3T3; CELL STRAIN COS1; CELL SURVIVAL; CELL TRANSFORMATION; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; ENZYME INHIBITION; ETIOLOGY; GENE EXPRESSION; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TEMPERATURE SENSITIVE MUTANT;

EID: 0030947318     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.6.3229     Document Type: Article

References (102)

1. Ally, S., T. Clair, D. Katsaros, G. Tortora, H. Yokozaki, R. A. Finch, T. L. Avery, and Y. S. Cho Chung. 1989. Inhibition of growth and modulation of gene expression in human lung carcinoma in athymic mice by site-selective 8-Cl-cyclic adenosine monophosphate. Cancer Res. 49:5650-5655.
2. Arcinas, M., K. C. Sizer, and L. M. Boxer. 1994. Activation of c-myc expression by c-Abl is independent of both the DNA binding function of c-Abl and the c-myc EP site. J. Biol. Chem. 269:21919-21924.
3. c-src in mitosis. Mol. Cell. Biol. 13:1464-1470.
4. Burgering, B. M., G. J. Pronk, P. C. van Weeren, P. Chardin, and J. L. Bos. 1993. cAMP antagonizes p21ras-directed activation of extracellular signal-regulated kinase 2 and phosphorylation of mSos nucleotide exchange factor. EMBO J. 12:4211-4220.
5. Buscher, D., R. A. Hipskind, S. Krautwald, T. Reimann, and M. Baccarini. 1995. Ras-dependent and -independent pathways target the mitogen-activated protein kinase network in macrophages. Mol. Cell. Biol. 15:466-475.
6. Carroll, M. P., and W. S. May. 1994. Protein kinase C-mediated serine phosphorylation directly activates Raf-1 in murine hematopoietic cells. J. Biol. Chem. 269:1249-1256.
7. Chapman, R. S., A. D. Whetton, and C. Dive. 1994. The suppression of drug-induced apoptosis by activation of v-ABL protein tyrosine kinase. Cancer Res. 54:5131-5137.
8. Cleveland, J. L., M. Dean, N. Rosenberg, J. Y. J. Wang, and U. R. Rapp. 1989. Tyrosine kinase oncogenes abrogate interleukin-3 dependence of murine myeloid cells through signaling pathways involving c-myc: conditional regulation of c-myc transcription by temperature-sensitive v-abl. Mol. Cell. Biol. 9:5685-5695.
9. Cleveland, J. L., H. W. Jansen, K. Bister, T. N. Fredrickson, H. C. Morse, J. N. Ihle, and U. R. Rapp. 1986. Interaction between Raf and Myc oncogenes in transformation in vivo and in vitro. J. Cell. Biochem. 30:195-218.
10. Cleveland, J. L., J. Troppmair, G. Packham, D. S. Askew, P. Lloyd, M. Gonzalez Garcia, G. Nunez, J. N. Ihle, and U. R. Rapp. 1994. v-raf suppresses apoptosis and promotes growth of interleukin-3-dependent myeloid cells. Oncogene 9:2217-2226.
11. Cook, S. J., and F. McCormick. 1993. Inhibition by cAMP of Ras-dependent activation of Raf. Science 262:1069-1072.
12. Cortez, D., L. Kadlec, and A. M. Pendergast. 1995. Structural and signaling requirements for BCR-ABL-mediated transformation and inhibition of apoptosis. Mol. Cell. Biol. 15:5531-5541.
13. Cotter, T. G., S. V. Lennon, J. M. Glynn, and D. R. Green. 1992. Microfilament-disrupting agents prevent the formation of apoptotic bodies in tumor cells undergoing apoptosis. Cancer Res. 52:997-1005. (Erratum, 52:3512.)
14. Cowley, S., H. Paterson, P. Kemp, and C. J. Marshall. 1994. Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 77:841-852.
15. Cruz Reyes, J., and J. R. Tata. 1995. Cloning, characterization and expression of two Xenopus bcl-2-like cell-survival genes. Gene 158:171-179.
16. Curran, T., and B. R. Franza. 1988. Fos and Jun: the AP-1 connection. Cell 55:395-397.
17. Darzynkiewicz, Z., S. Bruno, G. Del Bino, W. Gorczyca, M. A. Hotz, P. Lassota, and F. Traganos. 1992. Features of apoptotic cells measured by flow cytometry. Cytometry 13:795-808.
18. Daum, G., I. Eisenmann-Tappe, H.-W. Fries, J. Troppmair, and U. R. Rapp. 1994. The ins and outs of Raf kinases. Trends Biochem. Sci. 19:474-480.
19. Dudley, D. T., L. Pang, S. J. Decker, A. J. Bridges, and A. R. Saltiel. 1995. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA 92:7686-7689.
20. 2 phase if ts Kirsten sarcoma virus-infected NRK cells are to proliferate in serum-free medium. Mol. Cell. Biol. 7:444-449.
21. Eilers, M., D. Picard, K. R. Yamamoto, and J. M. Bishop. 1989. Chimaeras of myc oncoprotein and steroid receptors cause hormone-dependent transformation of cells. Nature 340:66-68.
22. Eissner, G., F. Kohlhuber, M. Grell, M. Ueffing, P. Scheurich, A. Hieke, G. Multhoff, G. W. Bornkamm, and E. Holler. 1995. Critical involvement of transmembrane tumor necrosis factor-α in endothelial programmed cell death mediated by ionizing radiation and bacterial endotoxin. Blood 86: 4184-4193.
23. Evan, G. I., and T. D. Littlewood. 1993. The role of c-myc in cell growth. Curr. Opin. Genet. Dev. 3:44-49.
24. Evan, G. I., A. H. Wyllie, C. S. Gilbert, T. D. Littlewood, H. Land, M. Brooks, C. M. Waters, L. Z. Penn, and D. C. Hancock. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69:119-128.
25. Evans, C. A., P. J. Owen Lynch, A. D. Whetton, and C. Dive. 1993. Activation of the Abelson tyrosine kinase activity is associated with suppression of apoptosis in hemopoietic cells. Cancer Res. 53:1735-1738.
26. Fabian, J. R., I. O. Daar, and D. K. Morrison. 1993. Critical tyrosine residues regulate the enzymatic and biological activity of Raf-1 kinase. Mol. Cell. Biol. 13:7170-7179.
27. Feig, L. A., and B. Schaffhausen. 1994. The hunt for Ras targets. Nature 370:508-509.
28. 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.
29. Feller, S. M., B. Knudsen, and H. Hanafusa. 1995. Cellular proteins binding to the first Src homology 3 (SH3) domain of the proto-oncogene product c-Crk indicate Crk-specific signaling pathways. Oncogene 10:1465-1473.
30. Fraker, P. J., L. E. King, D. Lill Elghanian, and W. G. Telford. 1995. Quantification of apoptotic events in pure and heterogeneous populations of cells using the flow cytometer. Methods Cell Biol. 46:57-76.
31. Fujita, M., and H. Shiku. 1995. Differences in sensitivity to induction of apoptosis among rat fibroblast cells transformed by HTLV-I tax gene or cellular nuclear oncogenes. Oncogene 11:15-20.
32. Fumagalli, S., N. F. Totty, J. J. Hsuan, and S. A. Courtneidge. 1994. A target for Src in mitosis. Nature 368:871-874.
33. Gardner, A. M., R. R. Vaillancourt, and G. L. Johnson. 1993. Activation of mitogen-activated protein kinase/extracellular signal regulated kinase kinase by G protein and tyrosine kinase oncoproteins. J. Biol. Chem. 268: 17896-17901.
34. TCF by MAP kinase stimulates ternary complex formation at c-fos promoter. Nature 358:414-417.
35. Goga, A., J. McLaughlin, D. E. Afar, D. C. Saffran, and O. N. Witte. 1995. Alternative signals to RAS for hematopoietic transformation by the BCR-ABL oncogene. Cell 82:981-988.
36. Graves, L. M., K. E. Bornfeldt, E. W. Raines, B. C. Potts, S. G. Macdonald, R. Ross, and E. G. Krebs. 1993. Protein kinase A antagonizes platelet-derived growth factor-induced signaling by mitogen-activated protein kinase in human arterial smooth muscle cells. Proc. Natl. Acad. Sci. USA 90:10300-10304.
37. Green, D. R., A. Mahboubi, W. Nishioka, S. Oja, F. Echeverri, Y. Shi, J. Glynn, Y. Yang, J. Ashwell, and R. Bissonnette. 1994. Promotion and inhibition of activation-induced apoptosis in T-cell hybridomas by oncogenes and related signals. Immunol. Rev. 142:321-342.
38. Häfner, S., H. S. Adler, H. Mischak, P. Janosch, G. Heidecker, A. Wolfman, S. Pippig, M. Lohse, M. Ueffing, and W. Kolch. 1994. Mechanism of inhibition of Raf-1 by protein kinase A. Mol. Cell. Biol. 14:6696-6703.
39. Heidecker, G., M. Huleihel, J. L. Cleveland, W. Kolch, T. W. Beck, P. Lloyd, T. Pawson, and U. R. Rapp. 1990. Mutational activation of c-raf-1 and definition of the minimal transforming sequence. Mol. Cell. Biol. 10:2503-2512.
40. ras-mitogen-activated protein kinase pathway in fibroblasts. J. Biol. Chem. 269:3534-3538.
41. Jaiswal, R. K., E. Weissinger, W. Kolch, and G. E. Landreth. 1996. Nerve growth factor-mediated activation of the mitogen-activated protein (MAP) kinase cascade involves a signaling complex containing B-Raf and HSP90. J. Biol. Chem. 271:23626-23629.
42. Jelinek, T., P. Dent, T. W. Sturgill, and M. J. Weber. 1996. Ras-induced activation of Raf-1 is dependent on tyrosine phosphorylation. Mol. Cell. Biol. 16:1027-1034.
43. Johnson, G. L., A. M. Gardner, C. Lange Carter, N. X. Qian, M. Russell, and S. Winitz. 1994. How does the G protein, Gi2, transduce mitogenic signals? J. Cell. Biochem. 54:415-422.
44. Kabarowski, J. H., P. B. Allen, and L. M. Wiedemann. 1994. A temperature sensitive p210 BCR-ABL mutant defines the primary consequences of BCR-ABL tyrosine kinase expression in growth factor dependent cells. EMBO J. 13:5887-5895.
45. Kan, O., S. A. Baldwin, and A. D. Whetton. 1994. Apoptosis is regulated by the rate of glucose transport in an interleukin 3 dependent cell line. J. Exp. Med. 180:917-923.
46. Karnitz, L. M., L. A. Burns, S. L. Sutor, J. Blenis, and R. T. Abraham. 1995. Interleukin-2 triggers a novel phosphatidylinositol 3-kinase-dependent MEK activation pathway. Mol. Cell. Biol. 15:3049-3057.
47. Kato, J. Y., M. Matsuoka, K. Polyak, J. Massague, and C. J. Sherr. 1994. Cyclic AMP-induced G1 phase arrest mediated by an inhibitor (p27Kip1) of cyclin-dependent kinase 4 activation. Cell 79:487-496.
48. Kauffmann-Zeh, A., P. Rodriguez-Viciana, E. Ulrich, C. Gilbert, P. Coffer, J. Downward, and G. Evan. 1997. Suppression of c-myc-induced apoptosis by Ras signalling through PI(3)K and PKB. Nature 385:544-548.
49. Kizaka Kondoh, S., and H. Okayama. 1993. Raf-1 is not a major upstream regulator of MAP kinases in rat fibroblasts. FEBS Lett. 336:255-258.
50. Kolch, W., R. H. Bassin, and U. R. Rapp. 1992. Raf function is required for proliferation of NIH 3T3 cells and transformation by non-nuclear oncogenes, p. 208-212. In R. Neth et al. (ed.), Modern trends in human leukemia IX: new results in clinical & biological research including pediatric oncology. Springer-Verlag, Berlin, Germany.
51. Kolch, W., J. L. Cleveland, and U. R. Rapp. 1990. Role of oncogenes in the abrogation of growth factor requirements of hemopoietic cells. Crit. Rev. Cancer 2:279-303.
52. Kolch, W., G. Heidecker, G. Kochs, R. Hummel, H. Vahidi, H. Mischak, G. Finkenzeller, D. Marme, and U. R. Rapp. 1993. PKCα activates Raf-1 by direct phosphorylation. Nature 364:249-251.
53. Kolch, W., G. Heidecker, J. Troppmair, K. Yanagihara, R. H. Bassin, and U. R. Rapp. 1993. Raf revertant cells resist transformation by non-nuclear oncogenes and are deficient in the induction of early response genes by TPA and serum. Oncogene 8:361-370.
54. Kortenjann, M., O. Thomae, and P. E. Shaw. 1994. Inhibition of v-raf-dependent c-fos expression and transformation by a kinase-defective mutant of the mitogen-activated protein kinase Erk2. Mol. Cell. Biol. 14:4815-4824.
55. Krautwald, S., D. Büscher, P. Dent, K. Ruthenberg, and M. Baccarini. 1995. Suppression of growth factor-mediated MAP kinase activation by v-raf in macrophages: a putative role for the MKP-1 phosphatase. Oncogene 10:1187-1192.
56. Kurzrock, R., J. U. Gutterman, and M. Talpaz. 1988. The molecular genetics of Philadelphia chromosome-positive leukemias. N. Engl. J. Med. 319:990-998.
57. Largaespada, D. A., D. A. Kaehler, H. Mishak, E. Weissinger, M. Potter, J. F. Mushinski, and R. Risser. 1992. A retrovirus that expresses v-abl and c-myc oncogenes rapidly induces plasmacytomas. Oncogene 7:811-819.
58. Leevers, S. J., H. F. Paterson, and C. J. Marshall. 1994. Requirement for Ras in Raf activation is overcome by targeting Raf to the plasma membrane. Nature 369:411-114.
59. Lovric, J., and K. Moelling. 1996. Activation of Mil/Raf protein kinases in mitotic cells. Oncogene 12:1109-1116.
60. Marais, R., Y. Light, H. F. Paterson, and C. J. Marshall. 1995. Ras recruits Raf-1 to the plasma membrane for activation by tyrosine phosphorylation. EMBO J. 14:3136-3145.
61. Marshall, C. J. 1994. MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr. Opin. Genet. Dev. 4:82-89.
62. Matsuda, M., Y. Hashimoto, K. Muroya, H. Hasegawa, T. Kurata, S. Tanaka, S. Nakamura, and S. Hattori. 1994. CRK protein binds to two guanine nucleotide-releasing proteins for the Ras family and modulates nerve growth factor-induced activation of Ras in PC12 cells. Mol. Cell. Biol. 14:5495-5500.
63. McCormick, F. 1993. Signal transduction. How receptors turn Ras on. Nature 363:15-16.
64. Miller, A. D., D. G. Miller, J. V. Garcia, and C. M. Lynch. 1993. Use of retroviral vectors for gene transfer and expression. Methods Enzymol. 217: 581-599.
65. Mischak, H., T. Seitz, P. Janosch, M. Eulitz, H. Steen, M. Schellerer, A. Philipp, and W. Kolch. 1996. Negative regulation of Raf-1 by phosphorylation of serine 621. Mol. Cell. Biol. 16:5409-5418.
66. Mitra, G., M. Weber, and D. Stacey. 1993. Multiple pathways for activation of MAP kinases. Cell. Mol. Biol. Res. 39:517-523.
67. Moodie, S. A., M. Paris, E. Villafranca, P. Kirshmeier, B. M. Willumsen, and A. Wolfman. 1995. Different structural requirements within the switch II region of the Ras protein for interaction with specific downstream targets. Oncogene 11:447-454.
68. Moodie, S. A., and A. Wolfman. 1994. The 3 Rs of life: Ras, Raf and growth regulation. Trends Genet. 10:44-48.
69. Owen Lynch, P. J., A. K. Wong, and A. D. Whetton. 1995. v-Abl-mediated apoptotic suppression is associated with SHC phosphorylation without concomitant mitogen-activated protein kinase activation. J. Biol. Chem. 270: 5956-5962.
70. Pendergast, A. M., L. A. Quilliam, L. D. Cripe, C. H. Bassing, Z. Dai, N. Li, A. Batzer, K. M. Rabun, C. J. Der, J. Schlessinger et al. 1993. BCR-ABL-induced oncogenesis is mediated by direct interaction with the SH2 domain of the GRB-2 adaptor protein. Cell 75:175-185.
71. Prouty, S. M., K. D. Hanson, A. L. Boyle, J. R. Brown, M. Shichiri, M. R. Follansbee, W. Kang, and J. M. Sedivy. 1993. A cell culture model system for genetic analyses of the cell cycle by targeted homologous recombination. Oncogene 8:899-907.
72. Rapp, U. R., J. L. Cleveland, S. M. Storm, T. W. Beck, and M. Huleihel. 1986. Transformation by rat and myc oncogenes. Int. Symp. Princess Takamatsu Cancer Res. Fund 17:55-74.
73. Rapp, U. R., J. Troppmair, T. Beck, and M. J. Birrer. 1994. Transformation by Raf and other oncogenes renders cells differentially sensitive to growth inhibition by a dominant negative c-jun mutant. Oncogene 9:3493-3498.
74. 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.
75. Renshaw, M., E. Kipreos, M. Albrecht, and J. Wang. 1992. Oncogenic v-Abl tyrosine kinase can inhibit or stimulate growth, depending on the cell context. EMBO J. 11:3941-3951.
76. Renshaw, M. W., J. R. McWhirter, and J. Y. J. Wang. 1995. The human leukemia oncogene bcr-abl abrogates the anchorage requirement but not the growth factor requirement for proliferation. Mol. Cell. Biol. 15:1286-1293.
77. Reuter, C. W. M., A. D. Catling, T. Jelinek, and M. J. Weber. 1995. Biochemical analysis of MEK activation in NIH3T3 fibroblasts. Identification of B-Raf and other activators. J. Biol. Chem. 270:7644-7655.
78. Roche, S., S. Fumagalli, and S. A. Courtneidge. 1995. Requirement for Src family protein tyrosine kinases in G2 for fibroblast cell division. Science 269:1567-1569.
79. Rosenberg, N., and O. N. Witte. 1988. The viral and cellular forms of the Abelson (abl) oncogene. Adv. Virus Res. 35:39-81.
80. Russell, M., S. Winitz, and G. L. Johnson. 1994. Acetylcholine muscarinic m1 receptor regulation of cyclic AMP synthesis controls growth factor stimulation of Raf activity. Mol. Cell. Biol. 14:2343-2351.
81. BCR/ABL to the pnosphatidylinositol-3′ kinase pathway. Oncogene 12:839-846.
82. Sawyers, C. L. 1993. The role of myc in transformation by BCR-ABL. Leuk. Lymphoma 11(Suppl. 1):45-46.
83. Sawyers, C. L., W. Callahan, and O. N. Witte. 1992. Dominant negative MYC blocks transformation by ABL oncogenes. Cell 70:901-910.
84. Sawyers, C. L., J. McLaughlin, and O. N. Witte. 1995. Genetic requirement for Ras in the transformation of fibroblasts and hematopoietic cells by the Bcr-Abl oncogene. J. Exp. Med. 181:307-313.
85. Seth, A., S. Gupta, and R. J. Davis. 1993. Cell cycle regulation of the c-Myc transcriptional activation domain. Mol. Cell. Biol. 13:4125-4136.
86. Sherr, C. J., and J. M. Roberts. 1995. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9:1149-1163.
87. Sozeri, O., K. Vollmer, M. Liyanage, D. Frith, G. Kour, G. E. Mark, and S. Stabel. 1992. Activation of the c-Raf protein kinase by protein kinase C phosphorylation. Oncogene 7:2259-2262.
88. Stanton, L. W., R. Watt, and K. B. Marcu. 1983. Translocation, breakage and truncated transcripts of the c-myc oncogene in murine plasmacytomas. Nature 303:401-406.
89. Stokoe, D., S. G. Macdonald, K. Cadwallader, M. Symons, and J. F. Hancock. 1994. Activation of Raf as a result of recruitment to the plasma membrane. Science 264:1463-1467.
90. Sun, X. M., R. T. Snowden, D. N. Skilleter, D. Dinsdale, M. G. Ormerod, and G. M. Cohen. 1992. A flow-cytometric method for the separation and quantitation of normal and apoptotic thymocytes. Anal. Biochem. 204:351-356.
91. Svetson, B. R., X. Kong, and J. C. Lawrence, Jr. 1993. Increasing cAMP attenuates activation of mitogen-activated protein kinase. Proc. Natl. Acad. Sci. USA 990:10305-10309.
92. Tauchi, T., and H. E. Broxmeyer. 1995. BCR/ABL signal transduction. Int. J. Hematol. 61:105-112.
93. Taylor, S. J., and D. Shalloway. 1994. An RNA-binding protein associated with Src through its SH2 and SH3 domains in mitosis. Nature 368:867-871.
94. Thompson, P. A., J. A. Ledbetter, U. R. Rapp, and J. B. Bolen. 1991. The Raf-1 serine-threonine kinase is a substrate for the p56lck protein tyrosine kinase in human T-cells. Cell Growth Differ. 2:609-617.
95. Troppmair, J., J. T. Bruder, H. Munoz, P. A. Lloyd, J. Kyriakis, P. Banerjee, J. Avruch, and U. R. Rapp. 1994. Mitogen-activated protein kinase/extracellular signal-regulated protein kinase activation by oncogenes, serum, and 12-O-tetradecanoylphorbol-13-acetate requires Raf and is necessary for transformation. J. Biol. Chem. 269:7030-7035.
96. Varticovski, L., G. Q. Daley, P. Jackson, D. Baltimore, and L. C. Cantley. 1991. Activation of phosphatidylinositol 3-kinase in cells expressing abl oncogene variants. Mol. Cell. Biol. 11:1107-1113.
97. Wang, H.-G., U. R. Rapp, and J. C. Reed. 1996. Bcl-2 targets the protein kinase Raf-1 to mitochondria. Cell 87:629-638.
98. Williams, N. G., and T. M. Roberts. 1994. Signal transduction pathways involving the Raf proto-oncogene. Cancer Metastasis Rev. 13:105-116.
99. Williams, N. G., T. M. Roberts, and P. Li. 1992. Both p21ras and pp60v-src are required, but neither alone is sufficient, to activate the Raf-1 kinase. Proc. Natl. Acad. Sci. USA 89:2922-2926.
100. Wong, K.-K., X. Zou, K. T. Merrell, A. J. Patel, K. B. Marcu, S. Chellappan, and K. Calame. 1995. v-Abl activates c-myc transcription through the E2F site. Mol. Cell. Biol. 15:6535-6544.
101. Wu, J., P. Dent, T. Jelinek, A. Wolfman, M. J. Weber, and T. W. Sturgill. 1993. Inhibition of the EGF-activated MAP kinase signaling pathway by adenosine 3′,5′-monophosphate. Science 262:1065-1069.
102. Zha, J., H. Harada, E. Yang, J. Jockel, and S. J. Korsmeyer. 1996. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not bcl-xl. Cell 87:619-628.