Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1995 Jan;69(1):403–413. doi: 10.1128/jvi.69.1.403-413.1995

The relocalization of v-Rel from the nucleus to the cytoplasm coincides with induction of expression of Ikba and nfkb1 and stabilization of I kappa B-alpha.

R Hrdlicková 1, J Nehyba 1, A Roy 1, E H Humphries 1, H R Bose Jr 1
PMCID: PMC188588  PMID: 7983736

Abstract

The v-Rel oncogene induces the expression of major histocompatibility complex class I and II proteins and the interleukin-2 receptor more efficiently than does c-Rel (R. Hrdlicková, J. Nehyba, and E. H. Humphries, J. Virol. 68:308-319, 1994). The kinetics with which these immunoregulatory receptors are induced in B- and T-lymphoid cell lines and chicken embryo fibroblast cultures expressing c-Rel or v-Rel have been examined. v-Rel induced the expression of major histocompatibility complex classes I and II and interleukin-2 receptor more efficiently than did c-Rel at later times after infection. In all three cell types, this increased efficiency was accompanied by a shift in the majority of v-Rel from the nucleus of the cytoplasm. The concomitant relocalization of v-Rel was also demonstrated during the in vitro transformation of spleen cells. The translocation coincided with increased steady-state levels of I kappa B-alpha. Coninfection by retroviral vectors expressing v-Rel, I kappa B-alpha, or NF-kappa B1 demonstrated that either I kappa B-alpha can contribute to the shift of v-Rel to the cytoplasmic compartment. The induction of nfkb1 and Ikba mRNA and the stabilization of I kappa B-alpha by v-Rel were shown to be responsible for these effects. In comparison with c-Rel, the expression of v-Rel was associated with lower levels of transcription of these genes. However, the ability of v-Rel to stabilize I kappa B-alpha remained unchanged. The ability of v-Rel to stabilize I kappa B-alpha but poorly induce Ikba mRNA expression relative to c-Rel may play a role in regulating gene expression, thereby leading to transformation.

Full Text

The Full Text of this article is available as a PDF (1.0 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abbadie C., Kabrun N., Bouali F., Smardova J., Stéhelin D., Vandenbunder B., Enrietto P. J. High levels of c-rel expression are associated with programmed cell death in the developing avian embryo and in bone marrow cells in vitro. Cell. 1993 Dec 3;75(5):899–912. doi: 10.1016/0092-8674(93)90534-w. [DOI] [PubMed] [Google Scholar]
  2. Akiyama Y., Kato S. Two cell lines from lymphomas of Marek's disease. Biken J. 1974 Sep;17(3):105–116. [PubMed] [Google Scholar]
  3. Baba T. W., Giroir B. P., Humphries E. H. Cell lines derived from avian lymphomas exhibit two distinct phenotypes. Virology. 1985 Jul 15;144(1):139–151. doi: 10.1016/0042-6822(85)90312-5. [DOI] [PubMed] [Google Scholar]
  4. Barth C. F., Ewert D. L., Olson W. C., Humphries E. H. Reticuloendotheliosis virus REV-T(REV-A)-induced neoplasia: development of tumors within the T-lymphoid and myeloid lineages. J Virol. 1990 Dec;64(12):6054–6062. doi: 10.1128/jvi.64.12.6054-6062.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beg A. A., Ruben S. M., Scheinman R. I., Haskill S., Rosen C. A., Baldwin A. S., Jr I kappa B interacts with the nuclear localization sequences of the subunits of NF-kappa B: a mechanism for cytoplasmic retention. Genes Dev. 1992 Oct;6(10):1899–1913. doi: 10.1101/gad.6.10.1899. [DOI] [PubMed] [Google Scholar]
  6. Bhat G. V., Temin H. M. Mutational analysis of v-rel, the oncogene of reticuloendotheliosis virus strain T. Oncogene. 1990 May;5(5):625–634. [PubMed] [Google Scholar]
  7. Bose H. R., Jr The Rel family: models for transcriptional regulation and oncogenic transformation. Biochim Biophys Acta. 1992 Sep 14;1114(1):1–17. doi: 10.1016/0304-419x(92)90002-g. [DOI] [PubMed] [Google Scholar]
  8. Bressler P., Brown K., Timmer W., Bours V., Siebenlist U., Fauci A. S. Mutational analysis of the p50 subunit of NF-kappa B and inhibition of NF-kappa B activity by trans-dominant p50 mutants. J Virol. 1993 Jan;67(1):288–293. doi: 10.1128/jvi.67.1.288-293.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brown K., Park S., Kanno T., Franzoso G., Siebenlist U. Mutual regulation of the transcriptional activator NF-kappa B and its inhibitor, I kappa B-alpha. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2532–2536. doi: 10.1073/pnas.90.6.2532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bull P., Morley K. L., Hoekstra M. F., Hunter T., Verma I. M. The mouse c-rel protein has an N-terminal regulatory domain and a C-terminal transcriptional transactivation domain. Mol Cell Biol. 1990 Oct;10(10):5473–5485. doi: 10.1128/mcb.10.10.5473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Capobianco A. J., Chang D., Mosialos G., Gilmore T. D. p105, the NF-kappa B p50 precursor protein, is one of the cellular proteins complexed with the v-Rel oncoprotein in transformed chicken spleen cells. J Virol. 1992 Jun;66(6):3758–3767. doi: 10.1128/jvi.66.6.3758-3767.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Capobianco A. J., Gilmore T. D. Repression of the chicken c-rel promoter by vRel in chicken embryo fibroblasts is not mediated through a consensus NF-kappa B binding site. Oncogene. 1991 Dec;6(12):2203–2210. [PubMed] [Google Scholar]
  13. Capobianco A. J., Simmons D. L., Gilmore T. D. Cloning and expression of a chicken c-rel cDNA: unlike p59v-rel, p68c-rel is a cytoplasmic protein in chicken embryo fibroblasts. Oncogene. 1990 Mar;5(3):257–265. [PubMed] [Google Scholar]
  14. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol. 1987 Aug;7(8):2745–2752. doi: 10.1128/mcb.7.8.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Chen I. S., Temin H. M. Substitution of 5' helper virus sequences into non-rel portion of reticuloendotheliosis virus strain T suppresses transformation of chicken spleen cells. Cell. 1982 Nov;31(1):111–120. doi: 10.1016/0092-8674(82)90410-x. [DOI] [PubMed] [Google Scholar]
  16. Chiao P. J., Miyamoto S., Verma I. M. Autoregulation of I kappa B alpha activity. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):28–32. doi: 10.1073/pnas.91.1.28. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  18. Cogswell P. C., Scheinman R. I., Baldwin A. S., Jr Promoter of the human NF-kappa B p50/p105 gene. Regulation by NF-kappa B subunits and by c-REL. J Immunol. 1993 Apr 1;150(7):2794–2804. [PubMed] [Google Scholar]
  19. Crone M., Simonsen M., Skjødt K., Linnet K., Olsson L. Mouse monoclonal antibodies to class I and class II antigens of the chicken MHC. Evidence for at least two class I products of the B complex. Immunogenetics. 1985;21(2):181–187. doi: 10.1007/BF00364870. [DOI] [PubMed] [Google Scholar]
  20. Davis N., Bargmann W., Lim M. Y., Bose H., Jr Avian reticuloendotheliosis virus-transformed lymphoid cells contain multiple pp59v-rel complexes. J Virol. 1990 Feb;64(2):584–591. doi: 10.1128/jvi.64.2.584-591.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Davis N., Ghosh S., Simmons D. L., Tempst P., Liou H. C., Baltimore D., Bose H. R., Jr Rel-associated pp40: an inhibitor of the rel family of transcription factors. Science. 1991 Sep 13;253(5025):1268–1271. doi: 10.1126/science.1891714. [DOI] [PubMed] [Google Scholar]
  22. Diehl J. A., McKinsey T. A., Hannink M. Differential pp40I kappa B-beta inhibition of DNA binding by rel proteins. Mol Cell Biol. 1993 Mar;13(3):1769–1778. doi: 10.1128/mcb.13.3.1769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Dobrzanski P., Ryseck R. P., Bravo R. Both N- and C-terminal domains of RelB are required for full transactivation: role of the N-terminal leucine zipper-like motif. Mol Cell Biol. 1993 Mar;13(3):1572–1582. doi: 10.1128/mcb.13.3.1572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Dougherty J. P., Temin H. M. High mutation rate of a spleen necrosis virus-based retrovirus vector. Mol Cell Biol. 1986 Dec;6(12):4387–4395. doi: 10.1128/mcb.6.12.4387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Evans R. B., Gottlieb P. D., Bose H. R., Jr Identification of a rel-related protein in the nucleus during the S phase of the cell cycle. Mol Cell Biol. 1993 Oct;13(10):6147–6156. doi: 10.1128/mcb.13.10.6147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Fan C. M., Maniatis T. Generation of p50 subunit of NF-kappa B by processing of p105 through an ATP-dependent pathway. Nature. 1991 Dec 5;354(6352):395–398. doi: 10.1038/354395a0. [DOI] [PubMed] [Google Scholar]
  27. Franzoso G., Bours V., Park S., Tomita-Yamaguchi M., Kelly K., Siebenlist U. The candidate oncoprotein Bcl-3 is an antagonist of p50/NF-kappa B-mediated inhibition. Nature. 1992 Sep 24;359(6393):339–342. doi: 10.1038/359339a0. [DOI] [PubMed] [Google Scholar]
  28. Geisler R., Bergmann A., Hiromi Y., Nüsslein-Volhard C. cactus, a gene involved in dorsoventral pattern formation of Drosophila, is related to the I kappa B gene family of vertebrates. Cell. 1992 Nov 13;71(4):613–621. doi: 10.1016/0092-8674(92)90595-4. [DOI] [PubMed] [Google Scholar]
  29. Ghosh S., Baltimore D. Activation in vitro of NF-kappa B by phosphorylation of its inhibitor I kappa B. Nature. 1990 Apr 12;344(6267):678–682. doi: 10.1038/344678a0. [DOI] [PubMed] [Google Scholar]
  30. Ghosh S., Gifford A. M., Riviere L. R., Tempst P., Nolan G. P., Baltimore D. Cloning of the p50 DNA binding subunit of NF-kappa B: homology to rel and dorsal. Cell. 1990 Sep 7;62(5):1019–1029. doi: 10.1016/0092-8674(90)90276-k. [DOI] [PubMed] [Google Scholar]
  31. Gilmore T. D., Temin H. M. v-rel oncoproteins in the nucleus and in the cytoplasm transform chicken spleen cells. J Virol. 1988 Mar;62(3):703–714. doi: 10.1128/jvi.62.3.703-714.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Grilli M., Chiu J. J., Lenardo M. J. NF-kappa B and Rel: participants in a multiform transcriptional regulatory system. Int Rev Cytol. 1993;143:1–62. doi: 10.1016/s0074-7696(08)61873-2. [DOI] [PubMed] [Google Scholar]
  33. Hannink M., Temin H. M. Structure and autoregulation of the c-rel promoter. Oncogene. 1990 Dec;5(12):1843–1850. [PubMed] [Google Scholar]
  34. Hannink M., Temin H. M. Transactivation of gene expression by nuclear and cytoplasmic rel proteins. Mol Cell Biol. 1989 Oct;9(10):4323–4336. doi: 10.1128/mcb.9.10.4323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Haskill S., Beg A. A., Tompkins S. M., Morris J. S., Yurochko A. D., Sampson-Johannes A., Mondal K., Ralph P., Baldwin A. S., Jr Characterization of an immediate-early gene induced in adherent monocytes that encodes I kappa B-like activity. Cell. 1991 Jun 28;65(7):1281–1289. doi: 10.1016/0092-8674(91)90022-q. [DOI] [PubMed] [Google Scholar]
  36. Hatada E. N., Nieters A., Wulczyn F. G., Naumann M., Meyer R., Nucifora G., McKeithan T. W., Scheidereit C. The ankyrin repeat domains of the NF-kappa B precursor p105 and the protooncogene bcl-3 act as specific inhibitors of NF-kappa B DNA binding. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2489–2493. doi: 10.1073/pnas.89.6.2489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Henkel T., Machleidt T., Alkalay I., Krönke M., Ben-Neriah Y., Baeuerle P. A. Rapid proteolysis of I kappa B-alpha is necessary for activation of transcription factor NF-kappa B. Nature. 1993 Sep 9;365(6442):182–185. doi: 10.1038/365182a0. [DOI] [PubMed] [Google Scholar]
  38. Henkel T., Zabel U., van Zee K., Müller J. M., Fanning E., Baeuerle P. A. Intramolecular masking of the nuclear location signal and dimerization domain in the precursor for the p50 NF-kappa B subunit. Cell. 1992 Mar 20;68(6):1121–1133. doi: 10.1016/0092-8674(92)90083-o. [DOI] [PubMed] [Google Scholar]
  39. Herzog N. K., Bose H. R., Jr Expression of the oncogene of avian reticuloendotheliosis virus in Escherichia coli and identification of the transforming protein in reticuloendotheliosis virus T-transformed cells. Proc Natl Acad Sci U S A. 1986 Feb;83(3):812–816. doi: 10.1073/pnas.83.3.812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Hrdlicková R., Nehyba J., Humphries E. H. In vivo evolution of c-rel oncogenic potential. J Virol. 1994 Apr;68(4):2371–2382. doi: 10.1128/jvi.68.4.2371-2382.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Hrdlicková R., Nehyba J., Humphries E. H. v-rel induces expression of three avian immunoregulatory surface receptors more efficiently than c-rel. J Virol. 1994 Jan;68(1):308–319. doi: 10.1128/jvi.68.1.308-319.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Inoue J., Kerr L. D., Kakizuka A., Verma I. M. I kappa B gamma, a 70 kd protein identical to the C-terminal half of p110 NF-kappa B: a new member of the I kappa B family. Cell. 1992 Mar 20;68(6):1109–1120. doi: 10.1016/0092-8674(92)90082-n. [DOI] [PubMed] [Google Scholar]
  43. Inoue J., Kerr L. D., Rashid D., Davis N., Bose H. R., Jr, Verma I. M. Direct association of pp40/I kappa B beta with rel/NF-kappa B transcription factors: role of ankyrin repeats in the inhibition of DNA binding activity. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4333–4337. doi: 10.1073/pnas.89.10.4333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Inoue J., Takahara T., Akizawa T., Hino O. Bcl-3, a member of the I kappa B proteins, has distinct specificity towards the Rel family of proteins. Oncogene. 1993 Aug;8(8):2067–2073. [PubMed] [Google Scholar]
  45. Isoda K., Roth S., Nüsslein-Volhard C. The functional domains of the Drosophila morphogen dorsal: evidence from the analysis of mutants. Genes Dev. 1992 Apr;6(4):619–630. doi: 10.1101/gad.6.4.619. [DOI] [PubMed] [Google Scholar]
  46. Kamens J., Richardson P., Mosialos G., Brent R., Gilmore T. Oncogenic transformation by vrel requires an amino-terminal activation domain. Mol Cell Biol. 1990 Jun;10(6):2840–2847. doi: 10.1128/mcb.10.6.2840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Kerr L. D., Duckett C. S., Wamsley P., Zhang Q., Chiao P., Nabel G., McKeithan T. W., Baeuerle P. A., Verma I. M. The proto-oncogene bcl-3 encodes an I kappa B protein. Genes Dev. 1992 Dec;6(12A):2352–2363. doi: 10.1101/gad.6.12a.2352. [DOI] [PubMed] [Google Scholar]
  48. Kerr L. D., Inoue J., Davis N., Link E., Baeuerle P. A., Bose H. R., Jr, Verma I. M. The rel-associated pp40 protein prevents DNA binding of Rel and NF-kappa B: relationship with I kappa B beta and regulation by phosphorylation. Genes Dev. 1991 Aug;5(8):1464–1476. doi: 10.1101/gad.5.8.1464. [DOI] [PubMed] [Google Scholar]
  49. Kidd S. Characterization of the Drosophila cactus locus and analysis of interactions between cactus and dorsal proteins. Cell. 1992 Nov 13;71(4):623–635. doi: 10.1016/0092-8674(92)90596-5. [DOI] [PubMed] [Google Scholar]
  50. Kieran M., Blank V., Logeat F., Vandekerckhove J., Lottspeich F., Le Bail O., Urban M. B., Kourilsky P., Baeuerle P. A., Israël A. The DNA binding subunit of NF-kappa B is identical to factor KBF1 and homologous to the rel oncogene product. Cell. 1990 Sep 7;62(5):1007–1018. doi: 10.1016/0092-8674(90)90275-j. [DOI] [PubMed] [Google Scholar]
  51. Kralova J., Schatzle J. D., Bargmann W., Bose H. R., Jr Transformation of avian fibroblasts overexpressing the c-rel proto-oncogene and a variant of c-rel lacking 40 C-terminal amino acids. J Virol. 1994 Apr;68(4):2073–2083. doi: 10.1128/jvi.68.4.2073-2083.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Le Bail O., Schmidt-Ullrich R., Israël A. Promoter analysis of the gene encoding the I kappa B-alpha/MAD3 inhibitor of NF-kappa B: positive regulation by members of the rel/NF-kappa B family. EMBO J. 1993 Dec 15;12(13):5043–5049. doi: 10.1002/j.1460-2075.1993.tb06197.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Lee T. H., Tempelis C. H. Characterization of a receptor on activated chicken T cells. Dev Comp Immunol. 1991 Fall;15(4):329–339. doi: 10.1016/0145-305x(91)90025-t. [DOI] [PubMed] [Google Scholar]
  54. Link E., Kerr L. D., Schreck R., Zabel U., Verma I., Baeuerle P. A. Purified I kappa B-beta is inactivated upon dephosphorylation. J Biol Chem. 1992 Jan 5;267(1):239–246. [PubMed] [Google Scholar]
  55. Liou H. C., Baltimore D. Regulation of the NF-kappa B/rel transcription factor and I kappa B inhibitor system. Curr Opin Cell Biol. 1993 Jun;5(3):477–487. doi: 10.1016/0955-0674(93)90014-h. [DOI] [PubMed] [Google Scholar]
  56. Liou H. C., Nolan G. P., Ghosh S., Fujita T., Baltimore D. The NF-kappa B p50 precursor, p105, contains an internal I kappa B-like inhibitor that preferentially inhibits p50. EMBO J. 1992 Aug;11(8):3003–3009. doi: 10.1002/j.1460-2075.1992.tb05370.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Logeat F., Israël N., Ten R., Blank V., Le Bail O., Kourilsky P., Israël A. Inhibition of transcription factors belonging to the rel/NF-kappa B family by a transdominant negative mutant. EMBO J. 1991 Jul;10(7):1827–1832. doi: 10.1002/j.1460-2075.1991.tb07708.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Lu D., Thompson J. D., Gorski G. K., Rice N. R., Mayer M. G., Yunis J. J. Alterations at the rel locus in human lymphoma. Oncogene. 1991 Jul;6(7):1235–1241. [PubMed] [Google Scholar]
  59. Mercurio F., Didonato J., Rosette C., Karin M. Molecular cloning and characterization of a novel Rel/NF-kappa B family member displaying structural and functional homology to NF-kappa B p50/p105. DNA Cell Biol. 1992 Sep;11(7):523–537. doi: 10.1089/dna.1992.11.523. [DOI] [PubMed] [Google Scholar]
  60. Miyamoto S., Chiao P. J., Verma I. M. Enhanced I kappa B alpha degradation is responsible for constitutive NF-kappa B activity in mature murine B-cell lines. Mol Cell Biol. 1994 May;14(5):3276–3282. doi: 10.1128/mcb.14.5.3276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Moore B. E., Bose H. R., Jr Expression of the v-rel oncogene in reticuloendotheliosis virus-transformed fibroblasts. Virology. 1988 Feb;162(2):377–387. doi: 10.1016/0042-6822(88)90478-3. [DOI] [PubMed] [Google Scholar]
  62. Morrison L. E., Boehmelt G., Enrietto P. J. Mutations in the rel-homology domain alter the biochemical properties of v-rel and render it transformation defective in chicken embryo fibroblasts. Oncogene. 1992 Jun;7(6):1137–1147. [PubMed] [Google Scholar]
  63. Morrison L. E., Kabrun N., Mudri S., Hayman M. J., Enrietto P. J. Viral rel and cellular rel associate with cellular proteins in transformed and normal cells. Oncogene. 1989 Jun;4(6):677–683. [PubMed] [Google Scholar]
  64. Møller L. B., Kaufman J., Verland S., Salomonsen J., Avila D., Lambris J. D., Skjødt K. Variations in the cytoplasmic region account for the heterogeneity of the chicken MHC class I (B-F) molecules. Immunogenetics. 1991;34(2):110–120. doi: 10.1007/BF00211423. [DOI] [PubMed] [Google Scholar]
  65. Narayanan R., Klement J. F., Ruben S. M., Higgins K. A., Rosen C. A. Identification of a naturally occurring transforming variant of the p65 subunit of NF-kappa B. Science. 1992 Apr 17;256(5055):367–370. doi: 10.1126/science.256.5055.367. [DOI] [PubMed] [Google Scholar]
  66. Nehyba J., Hrdlicková R., Humphries E. H. Evolution of the oncogenic potential of v-rel: rel-induced expression of immunoregulatory receptors correlates with tumor development and in vitro transformation. J Virol. 1994 Apr;68(4):2039–2050. doi: 10.1128/jvi.68.4.2039-2050.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Neri A., Chang C. C., Lombardi L., Salina M., Corradini P., Maiolo A. T., Chaganti R. S., Dalla-Favera R. B cell lymphoma-associated chromosomal translocation involves candidate oncogene lyt-10, homologous to NF-kappa B p50. Cell. 1991 Dec 20;67(6):1075–1087. doi: 10.1016/0092-8674(91)90285-7. [DOI] [PubMed] [Google Scholar]
  68. Neumann M., Tsapos K., Scheppler J. A., Ross J., Franza B. R., Jr Identification of complex formation between two intracellular tyrosine kinase substrates: human c-Rel and the p105 precursor of p50 NF-kappa B. Oncogene. 1992 Nov;7(11):2095–2104. [PubMed] [Google Scholar]
  69. Ohno H., Takimoto G., McKeithan T. W. The candidate proto-oncogene bcl-3 is related to genes implicated in cell lineage determination and cell cycle control. Cell. 1990 Mar 23;60(6):991–997. doi: 10.1016/0092-8674(90)90347-h. [DOI] [PubMed] [Google Scholar]
  70. Rice N. R., Ernst M. K. In vivo control of NF-kappa B activation by I kappa B alpha. EMBO J. 1993 Dec;12(12):4685–4695. doi: 10.1002/j.1460-2075.1993.tb06157.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Rice N. R., MacKichan M. L., Israël A. The precursor of NF-kappa B p50 has I kappa B-like functions. Cell. 1992 Oct 16;71(2):243–253. doi: 10.1016/0092-8674(92)90353-e. [DOI] [PubMed] [Google Scholar]
  72. Richardson P. M., Gilmore T. D. vRel is an inactive member of the Rel family of transcriptional activating proteins. J Virol. 1991 Jun;65(6):3122–3130. doi: 10.1128/jvi.65.6.3122-3130.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Sarkar S., Gilmore T. D. Transformation by the vRel oncoprotein requires sequences carboxy-terminal to the Rel homology domain. Oncogene. 1993 Aug;8(8):2245–2252. [PubMed] [Google Scholar]
  74. Schmitz M. L., Baeuerle P. A. The p65 subunit is responsible for the strong transcription activating potential of NF-kappa B. EMBO J. 1991 Dec;10(12):3805–3817. doi: 10.1002/j.1460-2075.1991.tb04950.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Schreck R., Rieber P., Baeuerle P. A. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J. 1991 Aug;10(8):2247–2258. doi: 10.1002/j.1460-2075.1991.tb07761.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Scott M. L., Fujita T., Liou H. C., Nolan G. P., Baltimore D. The p65 subunit of NF-kappa B regulates I kappa B by two distinct mechanisms. Genes Dev. 1993 Jul;7(7A):1266–1276. doi: 10.1101/gad.7.7a.1266. [DOI] [PubMed] [Google Scholar]
  77. Sif S., Gilmore T. D. NF-kappa B p100 is one of the high-molecular-weight proteins complexed with the v-Rel oncoprotein in transformed chicken spleen cells. J Virol. 1993 Dec;67(12):7612–7617. doi: 10.1128/jvi.67.12.7612-7617.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Simek S. L., Stephens R. M., Rice N. R. Localization of the v-rel protein in reticuloendotheliosis virus strain T-transformed lymphoid cells. J Virol. 1986 Jul;59(1):120–126. doi: 10.1128/jvi.59.1.120-126.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Stoker A. W., Bissell M. J. Quantitative immunocytochemical assay for infectious avian retroviruses. J Gen Virol. 1987 Sep;68(Pt 9):2481–2485. doi: 10.1099/0022-1317-68-9-2481. [DOI] [PubMed] [Google Scholar]
  80. Storms R. W., Bose H. R., Jr Alterations within pp59v-rel-containing protein complexes following the stimulation of REV-T-transformed lymphoid cells with zinc. Virology. 1992 Jun;188(2):765–777. doi: 10.1016/0042-6822(92)90531-s. [DOI] [PubMed] [Google Scholar]
  81. Sun S. C., Ganchi P. A., Ballard D. W., Greene W. C. NF-kappa B controls expression of inhibitor I kappa B alpha: evidence for an inducible autoregulatory pathway. Science. 1993 Mar 26;259(5103):1912–1915. doi: 10.1126/science.8096091. [DOI] [PubMed] [Google Scholar]
  82. Ten R. M., Paya C. V., Israël N., Le Bail O., Mattei M. G., Virelizier J. L., Kourilsky P., Israël A. The characterization of the promoter of the gene encoding the p50 subunit of NF-kappa B indicates that it participates in its own regulation. EMBO J. 1992 Jan;11(1):195–203. doi: 10.1002/j.1460-2075.1992.tb05042.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Tewari M., Dobrzanski P., Mohn K. L., Cressman D. E., Hsu J. C., Bravo R., Taub R. Rapid induction in regenerating liver of RL/IF-1 (an I kappa B that inhibits NF-kappa B, RelB-p50, and c-Rel-p50) and PHF, a novel kappa B site-binding complex. Mol Cell Biol. 1992 Jun;12(6):2898–2908. doi: 10.1128/mcb.12.6.2898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Thisse C., Perrin-Schmitt F., Stoetzel C., Thisse B. Sequence-specific transactivation of the Drosophila twist gene by the dorsal gene product. Cell. 1991 Jun 28;65(7):1191–1201. doi: 10.1016/0092-8674(91)90014-p. [DOI] [PubMed] [Google Scholar]
  85. Turnbull P. C., Snoeyenbos G. H. Experimental salmonellosis in the chicken. 2. Fate of a temperature-sensitive filamentous mutant. Avian Dis. 1974 Apr-Jun;18(2):178–185. [PubMed] [Google Scholar]
  86. White D. W., Gilmore T. D. Temperature-sensitive transforming mutants of the v-rel oncogene. J Virol. 1993 Nov;67(11):6876–6881. doi: 10.1128/jvi.67.11.6876-6881.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Wilhelmsen K. C., Eggleton K., Temin H. M. Nucleic acid sequences of the oncogene v-rel in reticuloendotheliosis virus strain T and its cellular homolog, the proto-oncogene c-rel. J Virol. 1984 Oct;52(1):172–182. doi: 10.1128/jvi.52.1.172-182.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Xu Y. X., Pitcovski J., Peterson L., Auffray C., Bourlet Y., Gerndt B. M., Nordskog A. W., Lamont S. J., Warner C. M. Isolation and characterization of three class II MHC genomic clones from the chicken. J Immunol. 1989 Mar 15;142(6):2122–2132. [PubMed] [Google Scholar]
  89. Zabel U., Baeuerle P. A. Purified human I kappa B can rapidly dissociate the complex of the NF-kappa B transcription factor with its cognate DNA. Cell. 1990 Apr 20;61(2):255–265. doi: 10.1016/0092-8674(90)90806-p. [DOI] [PubMed] [Google Scholar]
  90. Zabel U., Henkel T., Silva M. S., Baeuerle P. A. Nuclear uptake control of NF-kappa B by MAD-3, an I kappa B protein present in the nucleus. EMBO J. 1993 Jan;12(1):201–211. doi: 10.1002/j.1460-2075.1993.tb05646.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. de Martin R., Vanhove B., Cheng Q., Hofer E., Csizmadia V., Winkler H., Bach F. H. Cytokine-inducible expression in endothelial cells of an I kappa B alpha-like gene is regulated by NF kappa B. EMBO J. 1993 Jul;12(7):2773–2779. doi: 10.1002/j.1460-2075.1993.tb05938.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. van Krieken J. H., McKeithan T. W., Raghoebier S., Medeiros L. J., Kluin P. M., Raffeld M. Chromosomal translocation t(14;19) as indicated by bcl-3 rearrangement is a rare phenomenon in non-Hodgkin's lymphoma and chronic lymphocytic leukemia: a molecular genetic analysis of 176 cases. Leukemia. 1990 Dec;4(12):811–812. [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES