Mapping of a serine-rich domain essential for the transcriptional, antiapoptotic, and transforming activities of the v-Rel oncoprotein

Molecular and Cellular Biology

Volumn 19, Issue 1, 1999, Pages 307-316

  Chen, Cailin ^a   Agnès, François ^a,e   Gélinas, Céline ^a,b,c,d  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

^d CABM   (United States)

^e Centre de Biologie du Developpement Toulouse   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ONCOPROTEIN; SERINE; TRANSFORMING GROWTH FACTOR;

AMINO ACID SUBSTITUTION; ARTICLE; CELL DEATH; CELL PROLIFERATION; CELL TRANSFORMATION; GENE ACTIVATION; GENE MAPPING; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; RETICULOENDOTHELIOSIS; TRANSACTIVATION; TRANSCRIPTION REGULATION;

EID: 0032908349     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.1.307     Document Type: Article

References (87)

1. Baeuerle, P. A., and D. Baltimore. 1989. A 65-kD subunit of active NF-κB is required for inhibition of NF-κB by IκB. Genes Dev. 3:1689-1698.
2. Baeuerle, P. A., and T. Henkel. 1994. Function and activity of NF-κB in the immune system. Annu. Rev. Immunol. 12:141-179.
3. Baldwin, A. S., Jr. 1996. The NF-κB and IκB proteins: new discoveries and insights. Annu. Rev. Immunol. 14:649-681.
4. Ballard, D. W., W. H. Walker, S. Doerre, P. Sista, J. A. Molitor, E. P. Dixon, N. J. Pefler, M. Hannink, and W. C. Greene. 1990 The v-rel oncogene encodes a κB enhancer binding protein that inhibits NF-κB function. Cell 63:803-814.
5. Beug, H., H. Muller, G. Doederlein, and T. Graf. 1981. Hematopoietic cells transformed in vitro by REV-T avian reticuloendotheliosis virus express characteristics of very immature lymphoid cells. Virology 115:295-309.
6. Bhat, G., and H. M. Temin. 1990. Mutational analysis of v-rel, the oncogene of reticuloendotheliosis virus strain T. Oncogene 5:625-634.
7. Boehmelt, G., J. Madruga, P. Dorfler, K. Briegel, H. Schwartz, P. J. Enrietto, and M. Zenke. 1995. Dendritic cell progenitor is transformed by a conditional v-Rel estrogen receptor fusion protein V-RelER. Cell 80:341-352.
8. Bose, H. R., Jr. 1992. The Rel family: models for transcriptional regulation and oncogenic transformation. Biochim. Biophys. Acta 1114:1-17.
9. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
10. Bushdid, P., D. Brantley, F. Yull, G. Blaeuer, L. Hoffman, L. Niswander, and L. Kerr. 1998. Inhibition of NF-κB activity results in disruption of the apical ectodermal ridge and aberrant limb morphogenesis. Nature 392:615-618.
11. Capobianco, A. J., D. Chang, G. Mosialos, and T. D. Gilmore. 1992. p105, the NF-κB p50 precursor protein, is one of the cellular proteins complexed with the v-Rel oncoprotein in transformed chicken spleen cells. J. Virol. 66:3758-3767.
12. c-rel is a cytoplasmic protein in chicken embryo fibroblasts. Oncogene 5:257-265.
13. Carrasco, D., C. A. Risso, K. Dorfman, and R. Bravo. 1996. The v-rel oncogene promotes malignant T-cell leukemia/lymphoma in transgenic mice. EMBO J. 15:3640-3650.
14. Chen, C., and C. Gélinas. Unpublished data.
15. Chen, C., and H. Okayama. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745-2752.
16. Davis, J. N., W. Bargmann, and H. R. Bose, Jr. 1990. Identification of protein complexes containing the c-rel proto-oncogene product in avian hematopoietic cells. Oncogene 5:1109-1115.
17. IκB-B inhibition of DNA binding by rel proteins. Mol. Cell. Biol. 13:1769-1778.
18. Dougherty, J. P., and H. M. Temin. 1986. High mutation rate of a spleen necrosis virus-based retrovirus vector. Mol. Cell. Biol. 6:4387-4395.
19. Dougherty, J. P., R. Wisniewski, S. Yang, B. W. Rhode, and H. M. Temin. 1989. New retrovirus helper cells with almost no nucleotide sequence homology to retrovirus vectors. J. Virol. 63:3209-3212.
20. Franklin, R. B., R. L. Maldonado, and H. R. Bose. 1974. Isolation and characterization of reticuloendotheliosis virus transformed bone marrow cells. Intervirology 3:342-352.
21. Garson, K., H. Percival, and Y. C. Kang. 1990. The N-terminal env-derived amino acids of v-Rel are required for full transforming activity. Virology 177:106-115.
22. Gélinas, C., and H. M. Temin. 1988. The v-rel oncogene encodes a cell-specific transcriptional activator of certain promoters. Oncogene 3:349-355.
23. Gilmore, T. D. Personal communication.
24. Gilmore, T. D., M. Koedood, K. A. Piffat, and D. W. White. 1996. Rel/NF-κB/IκB proteins and cancer. Oncogene 13:1367-1378.
25. Gilmore, T. D., and H. M. Temin. 1986. Different localization of the product of the v-rel oncogene in chicken fibroblasts and spleen cells correlates with transformation by Rev-T. Cell 44:791-800.
26. Gilmore, T. D., D. W. White, S. Sarkar, and S. Sif. 1995. Malignant transformation of cells by the v-Rel oncoprotein, p. 109-128. In G. M. Cooper, R. Greenberg Temin, and B. Sugden (ed.). The DNA provirus: Howard Temin's scientific legacy. American Society for Microbiology. Washington, D.C.
27. Gossen, M., and H. Bujard. 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA 89:5547-5551.
28. Greenblatt, J. 1992. Riding high on the TATA box. Nature 360:15-17.
29. Guermah, M., S. Malik, and R. G. Roeder. 1998. Involvement of TFIID and USA components in transcriptional activation of the human immunodeficiency virus promoter by NF-κB and Sp1. Mol. Cell. Biol. 18:3234-3244.
30. Hahn, S. 1993. Structure(?) and function of acidic transcription activators. Cell 72:481-483.
31. Hrdličková, R., J. Nehyba, and E. H. Humphries. 1994. In vivo evolution of c-rel oncogenic potential. J. Virol. 68:2371-2382.
32. Inoue, J.-I., L. D. Kerr, L. J. Ransone, E. Bengal, T. Hunter, and I. M. Verma. 1991. c-rel activates but v-rel suppresses transcription from κB sites. Proc. Natl. Acad. Sci. USA 88:3715-3719.
33. Ishikawa, H., M. Asano, T. Kanda, S. Kumar, C. Gélinas, and Y. Ito. 1993. Two novel functions associated with the Rel oncoproteins: DNA replication and cell-specific transcriptional activation. Oncogene 8:2889-2896.
34. Kamens, J., P. Richardson, G. Mosialos, R. Brent, and T. Gilmore. 1990. Oncogenic transformation by v-Rel requires an amino-terminal activation domain. Mol. Cell. Biol. 10:2840-2847.
35. Kanegae, Y., A. Tavares, J. Belmonte, and I. Verma. 1998. Role of Rel/ NF-κB transcription factors during the outgrowth of the vertebrate limb. Nature 392:611-614.
36. Karin, M. 1994. Signal transduction from the cell surface to the nucleus through the phosphorylation of transcription factors. Curr. Opin. Cell Biol. 6:415-424.
37. Kochel, T., J. F. Mushinski, and N. R. Rice. 1991. The v-rel and c-rel proteins exist in high molecular weight complexes in avian and murine cells. Oncogene 6:615-626.
38. Kralova, J., A. Liss, W. Bargmann, and H. Bose. 1998. AP-1 factors play an important role in transformation induced by the v-rel oncogene. Mol. Cell. Biol. 18:2997-3009.
39. Kralova, J., J. D. Schatzle, W. Bargmann, and H. R. Bose, Jr. 1994. Transformation of avian fibroblasts overexpressing the c-rel proto-oncogene and a variant of c-rel lacking 40 C-terminal amino acids. J. Virol. 68:2073-2083.
40. Kumar, S., A. B. Rabson, and C. Gélinas. 1992. The RxxRxRxxC motif conserved in all Rel/κB proteins is essential for the DNA-binding activity and redox regulation of the v-Rel oncoprotein. Mol. Cell. Biol. 12:3094-3106.
41. Lewis, R. B., J. McClure, B. Rup, D. W. Niesel, R. F. Garry, J. D. Hoelzer, K. Nazerian, and H. R. Bose, Jr. 1981. Avian reticuloendotheliosis virus: identification of the hematopoietic target cell for transformation. Cell 25: 421-431.
42. Lillie, J. W., and M. R. Green. 1989. Transcription activation by the adenovirus E1A protein. Nature 338:39-44.
43. Luque, I., and C. Gélinas. 1997. Rel/NF-κB and IκB factors in oncogenesis. Semin. Cancer Biol. 8:103-111.
44. Maniatis, T. 1997. Catalysis by a multiprotein IkappaB kinase complex. Science 278:818-819.
45. McDonnell, P. C., S. Kumar, A. B. Rabson, and C. Gélinas. 1992. Transcriptional activity of Rel family proteins. Oncogene 7:163-170.
46. Miyamoto, S., and I. M. Verma. 1995. Rel/NF-κB/IκB story. Adv. Cancer Res. 66:255-293.
47. Morrison, L. E., G. Boehmelt, and P. J. Enrietto. 1992. Mutations in the rel-homology domain alter the biochemical properties of v-Rel and render it transformation defective in chicken fibroblasts. Oncogene 7:1137-1147.
48. Morrison, L. E., N. Kabrun, S. Mudri, M. J. Hayman, and P. J. Enrietto. 1989. Viral Rel and cellular Rel associate with cellular proteins in transformed and normal cells. Oncogene 4:677-683.
49. Mosialos, G., and T. D. Gilmore. 1993. v-Rel and c-Rel are differentially affected by mutations at a consensus protein kinase recognition sequence. Oncogene 8:721-730.
50. c-rel.. Mol. Cell. Biol. 11:5867-5877.
51. Nakayama, K., H. Shimizu, K. Mitomo, T. Watanabe, S.-I. Okamoto, and K.-I. Yamamoto. 1992. A lymphoid cell-specific nuclear factor containing c-Rel-like proteins preferentially interacts with interleukin-6 κB-related motifs whose activities are repressed in lymphoid cells. Mol. Cell. Biol. 12:1736-1746.
52. Naumann, M., and C. Scheidereit. 1994. Activation of NF-κB in vivo is regulated by multiple phosphorylations. EMBO J. 13:4597-4607.
53. Nehyba, J., R. Hrdličková, and H. R. Bose, Jr. 1997. Differences in κB DNA-binding properties of v-Rel and c-Rel are the result of oncogenic mutations in three distinct functional regions of the Rel protein. Oncogene 14:2881-2897.
54. Neiman, P. E., S. J. Thomas, and G. Loring. 1991. Induction of apoptosis during normal and neoplastic B-cell development in the bursa of Fabricius. Proc. Natl. Acad. Sci. USA 88:5857-5861.
55. Perkins, N. D., L. K. Felzien, J. C. Betts, K. Leung, D. H. Beach, and G. J. Nabel. 1997. Regulation of NF-κB by cyclin-dependent kinases associated with the p300 coactivator. Science 275:523-527.
56. Ptashne, M., and A. Gann. 1997. Transcriptional activation by recruitment. Nature 386:569-577.
57. Resnitzky, D., M. Gossen, H. Bujard, and S. I. Reed. 1994. Acceleration of the G1/S-phase transition by expression of cyclins D1 and E with an inducible system. Mol. Cell. Biol. 14:1669-1679.
58. Richardson, P. M., and T. D. Gilmore. 1991. v-Rel is an inactive member of the Rel family of transcriptional activating proteins. J. Virol. 65:3122-3130.
59. Sarkar, S., and T. D. Gilmore. 1993. Transformation by the v-Rel oncoprotein requires sequences carboxy-terminal to the Rel homology domain. Oncogene 8:2245-2252.
60. Schmitz, M. L., G. Stelzer, H. Altmann, M. Meisterernst, and P. A. Baeuerle. 1995. Interaction of the COOH-terminal transactivation domain of p65 NF-κB with TATA-binding protein, transcription factor IIB, and coactivators. J. Biol. Chem. 270:7219-7226.
61. Shibuya, T., I. Chen, A. Howatson, and T. W. Mak. 1982. Morphological, immunological, and biochemical analyses of chicken spleen cells transformed in vitro by reticuloendotheliosis virus strain T. Cancer Res. 42:2722-2728.
62. Sif, S., and T. D. Gilmore. 1993. NF-κB p100 is one of the high-molecular-weight proteins complexed with the v-Rel oncoprotein in transformed chicken spleen cells. J. Virol. 67:7612-7617.
63. v-rel, the transforming protein of reticuloendotheliosis virus, is complexed with at least four other proteins in transformed chicken lymphoid cells. J. Virol. 62:4730-4736.
64. Smardova, J., A. Walker, L. E. Morrison, N. Kabrun, and P. J. Enrietto. 1995. The role of the carboxy terminus of v-Rel in transformation and activation of endogenous gene expression. Oncogene 10:2017-2026.
65. Stephens, R. M., N. R. Rice, R. R. Hiebsch, H. R. Bose, and R. V. Gilden. 1983. Nucleotide sequence of v-rel: the oncogene of reticuloendotheliosis virus. Proc. Natl. Acad. Sci. USA 80:6229-6233.
66. Tanaka, M., and W. Herr. 1990. Differential transcriptional activation by Oct-1 and Oct-2: interdependent activation domains induce Oct-2 phosphorylation. Cell 60:375-386.
67. Tanaka, M., J.-S. Lai, and W. Herr. 1992. Promoter-selective activation domains in Oct-1 and Oct-2 direct differential activation of an snRNA and mRNA promoter. Cell 68:755-767.
68. Thanos, D., and T. Maniatis. 1995. NF-κB: a lesson in family values. Cell 80:529-532.
69. Theilen, G., R. Zeigel, and M. Tweihaus. 1966. Biological studies with RE virus (strain T) that induces reticuloendotheliosis in turkeys, chickens, and Japanese quails. J. Natl. Cancer Inst. 37:747-749.
70. Tung, H. Y. L., W. Bargmann, M. Y. Lim, and H. R. Bose. 1988. The v-rel oncogene product is complexed to a 40-kDa phosphoprotein in transformed lymphoid cells. Proc. Natl. Acad. Sci. USA 85:2479-2483.
71. Verma, I. M., and J. Stevenson. 1997. IkappaB kinase: beginning, not the end. Proc. Natl. Acad. Sci. USA 94:11758-11760.
72. Verma, I. M., J. K. Stevenson, E. M. Schwarz, D. Van Antwerp, and S. Miyamoto. 1995. Rel/NF-κB/IκB family: intimate tales of association and dissociation. Genes Dev. 9:2723-2735.
73. Walker, W. H., B. Stein, P. A. Ganchi, J. A. Hoffman, P. A. Kaufman, D. W. Ballard, M. Hannink, and W. C. Greene. 1992. The v-rel oncogene: insights into the mechanism of transcriptional activation, repression, and transformation. J. Virol. 66:5018-5029.
74. Watanabe, S., and H. M. Temin. 1983. Construction of a helper cell line for avian reticuloendotheliosis virus cloning vectors. Mol. Cell. Biol. 3:2241-2249.
75. White, D. W., A. Roy, and T. D. Gilmore. 1995. The v-Rel oncoprotein blocks apoptosis and proteolysis of IκB-α in transformed chicken spleen cells. Oncogene 10:857-868.
76. White, E., P. Sabbatini, M. Debbas, W. S. M. Wold, D. I. Kusher, and L. R. Gooding. 1992. The 19-kilodalton adenovirus E1B transforming protein inhibits programmed cell death and prevents cytolysis by tumor necrosis factor α. Mol. Cell. Biol. 12:2570-2580.
77. Wilhelmsen, K. C., K. Eggelton, and H. M. Temin. 1984. Nucleic acid sequences of the oncogene v-rel in reticuloendotheliosis virus strain T and its cellular homolog, the proto-oncogene c-rel. J. Virol. 52:172-182.
78. Wong, T. C., and M. M. C. Lai. 1981. Avian reticuloendotheliosis virus contains a new class of oncogene of turkey origin. Virology 111:289-293.
79. Xu, X., and C. Gélinas. 1995. The v-Rel oncoprotein complexes with new Rel- and RelA-related proteins in transformed cells. Virology 207:362-368.
80. Xu, X., and C. Gélinas. 1997. A mutant Rel homology domain promotes transcription by p50/NF-κB1. Oncogene 14:1521-1530.
81. Xu, X., and C. Gélinas. Unpublished data.
82. Xu, X., C. Prorock, H. Ishikawa, E. Maldonado, Y. Ito, and C. Gélinas. 1993. Functional interaction of the v-Rel and c-Rel oncoproteins with the TATA-binding protein and association with transcription factor IIB. Mol. Cell. Biol. 13:6733-6741.
83. Zhang, J., and A. Winoto. 1996. A mouse Fas-associated protein with homology to the human Mort1/FADD protein is essential for Fas-mediated apoptosis. Mol. Cell. Biol. 16:2756-2763.
84. Zhong, H., H. SuYang, H. Erdjument-Bromage, P. Tempst, and S. Ghosh. 1997. The transcriptional activity of NF-κB is regulated by the IκB-associated PKAc subunit through a cyclic AMP-independent mechanism. Cell 89:413-424.
85. Zhong, H., R. Voll, and S. Ghosh. 1998. Phosphorylation of NF-κB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol. Cell 1:661-671.
86. Zong, W.-X., M. Farrell, J. Bash, and C. Gélinas. 1997. v-Rel prevents apoptosis in transformed lymphoid cells and blocks TNFα-induced cell death. Oncogene 15:971-980.
87. Zong, W.-X., J. Bash, and C. Gélinas. 1998. Rel blocks both anti-Fas- and TNFα-induced apoptosis and an intact Rel transactivation domain is essential for this effect. Cell Death Differ. 5:963-972.