Abstract
Marek's disease virus (MDV) is one of the most oncogenic herpesviruses and induces T lymphomas in chickens within weeks after infection. Only a limited number of viral transcripts are detected in MDV tumor samples and cell lines. One of the major transcripts encodes MEQ, a 339-amino-acid bZIP protein which is homologous to the Jun/Fos family of transcription factors. The C-terminal half of MEQ contains proline-rich repeats and, when fused to the DNA-binding domain of a yeast transcription factor, Gal4 (residues 1 to 147), exhibits transactivation function. MEQ can dimerize with itself and with c-Jun. The MEQ-c-Jun heterodimers bind to an AP-1-like enhancer within the MEQ promoter region with greater affinity than do homodimers of either protein, and they transactivate MEQ expression. Here we show that MEQ is expressed in the nucleus but, interestingly, with a predominant fraction in the nucleoli and coiled bodies. This makes MEQ the first bZIP protein to be identified in the nucleoli. MEQ contains two stretches of basic residues, designated basic region 1 (BR1) and basic region 2 (BR2). Using a series of deletion mutants, we have mapped the primary nuclear localization signal (NLS) and the sole nucleolar localization signal (NoLS) to the BR2 region. BR1 was shown to provide an auxiliary signal in nuclear translocation. To demonstrate that BR2 is an authentic NoLS, BR2 was fused to cytoplasmic v-Raf (delta gag) kinase. The BR2-Raf fusion protein was observed to migrate into the nucleoplasm and the nucleolus. The BR2 region can be further divided into two long arginine-lysine stretches, BR2N and BR2C, which are separated by the five amino acids Asn-Arg-Asp-Ala-Ala (NRDAA). We provide evidence that the requirement for nuclear translocation is less stringent than that for nucleolar translocation, as either BR2N or BR2C alone is sufficient to translocate the cytoplasmic v-Raf (delta gag) into the nucleus, but only in combination can they translocate v-Raf (delta gag) into the nucleolus. Our studies demonstrate that MEQ is both a nuclear and nucleolar protein, adding MEQ to the growing list of transactivators which localize to the nucleolus.
Full Text
The Full Text of this article is available as a PDF (400.8 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Adachi Y., Copeland T. D., Hatanaka M., Oroszlan S. Nucleolar targeting signal of Rex protein of human T-cell leukemia virus type I specifically binds to nucleolar shuttle protein B-23. J Biol Chem. 1993 Jul 5;268(19):13930–13934. [PubMed] [Google Scholar]
- Alfieri C., Birkenbach M., Kieff E. Early events in Epstein-Barr virus infection of human B lymphocytes. Virology. 1991 Apr;181(2):595–608. doi: 10.1016/0042-6822(91)90893-g. [DOI] [PubMed] [Google Scholar]
- Boulikas T. Nuclear localization signals (NLS). Crit Rev Eukaryot Gene Expr. 1993;3(3):193–227. [PubMed] [Google Scholar]
- Boulikas T. Putative nuclear localization signals (NLS) in protein transcription factors. J Cell Biochem. 1994 May;55(1):32–58. doi: 10.1002/jcb.240550106. [DOI] [PubMed] [Google Scholar]
- Bradley G., Lancz G., Tanaka A., Nonoyama M. Loss of Marek's disease virus tumorigenicity is associated with truncation of RNAs transcribed within BamHI-H. J Virol. 1989 Oct;63(10):4129–4135. doi: 10.1128/jvi.63.10.4129-4135.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burd C. G., Dreyfuss G. Conserved structures and diversity of functions of RNA-binding proteins. Science. 1994 Jul 29;265(5172):615–621. doi: 10.1126/science.8036511. [DOI] [PubMed] [Google Scholar]
- Call K. M., Glaser T., Ito C. Y., Buckler A. J., Pelletier J., Haber D. A., Rose E. A., Kral A., Yeger H., Lewis W. H. Isolation and characterization of a zinc finger polypeptide gene at the human chromosome 11 Wilms' tumor locus. Cell. 1990 Feb 9;60(3):509–520. doi: 10.1016/0092-8674(90)90601-a. [DOI] [PubMed] [Google Scholar]
- Calnek B. W. Marek's disease--a model for herpesvirus oncology. Crit Rev Microbiol. 1986;12(4):293–320. doi: 10.3109/10408418509104432. [DOI] [PubMed] [Google Scholar]
- Carvalho T., Seeler J. S., Ohman K., Jordan P., Pettersson U., Akusjärvi G., Carmo-Fonseca M., Dejean A. Targeting of adenovirus E1A and E4-ORF3 proteins to nuclear matrix-associated PML bodies. J Cell Biol. 1995 Oct;131(1):45–56. doi: 10.1083/jcb.131.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cavanaugh A. H., Hempel W. M., Taylor L. J., Rogalsky V., Todorov G., Rothblum L. I. Activity of RNA polymerase I transcription factor UBF blocked by Rb gene product. Nature. 1995 Mar 9;374(6518):177–180. doi: 10.1038/374177a0. [DOI] [PubMed] [Google Scholar]
- Cheng Y. Q., Lee L. F., Smith E. J., Witter R. L. An enzyme-linked immunosorbent assay for the detection of antibodies to Marek's disease virus. Avian Dis. 1984 Oct-Dec;28(4):900–911. [PubMed] [Google Scholar]
- Coleman N. A., Peeples M. E. The matrix protein of Newcastle disease virus localizes to the nucleus via a bipartite nuclear localization signal. Virology. 1993 Aug;195(2):596–607. doi: 10.1006/viro.1993.1411. [DOI] [PubMed] [Google Scholar]
- Corsetti M. T., Levi G., Lancia F., Sanseverino L., Ferrini S., Boncinelli E., Corte G. Nucleolar localisation of three Hox homeoproteins. J Cell Sci. 1995 Jan;108(Pt 1):187–193. doi: 10.1242/jcs.108.1.187. [DOI] [PubMed] [Google Scholar]
- Dang C. V., Lee W. M. Identification of the human c-myc protein nuclear translocation signal. Mol Cell Biol. 1988 Oct;8(10):4048–4054. doi: 10.1128/mcb.8.10.4048. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dang C. V., Lee W. M. Nuclear and nucleolar targeting sequences of c-erb-A, c-myb, N-myc, p53, HSP70, and HIV tat proteins. J Biol Chem. 1989 Oct 25;264(30):18019–18023. [PubMed] [Google Scholar]
- Dawson M. J., Trapani J. A. The interferon-inducible autoantigen, IFI 16: localization to the nucleolus and identification of a DNA-binding domain. Biochem Biophys Res Commun. 1995 Sep 5;214(1):152–162. doi: 10.1006/bbrc.1995.2269. [DOI] [PubMed] [Google Scholar]
- Delling U., Roy S., Sumner-Smith M., Barnett R., Reid L., Rosen C. A., Sonenberg N. The number of positively charged amino acids in the basic domain of Tat is critical for trans-activation and complex formation with TAR RNA. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6234–6238. doi: 10.1073/pnas.88.14.6234. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Diaz J. J., Dodon M. D., Schaerer-Uthurralt N., Simonin D., Kindbeiter K., Gazzolo L., Madjar J. J. Post-transcriptional transactivation of human retroviral envelope glycoprotein expression by herpes simplex virus Us11 protein. Nature. 1996 Jan 18;379(6562):273–277. doi: 10.1038/379273a0. [DOI] [PubMed] [Google Scholar]
- Dundr M., Leno G. H., Hammarskjöld M. L., Rekosh D., Helga-Maria C., Olson M. O. The roles of nucleolar structure and function in the subcellular location of the HIV-1 Rev protein. J Cell Sci. 1995 Aug;108(Pt 8):2811–2823. doi: 10.1242/jcs.108.8.2811. [DOI] [PubMed] [Google Scholar]
- Everett R. D., Maul G. G. HSV-1 IE protein Vmw110 causes redistribution of PML. EMBO J. 1994 Nov 1;13(21):5062–5069. doi: 10.1002/j.1460-2075.1994.tb06835.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Falkner F. G., Fuerst T. R., Moss B. Use of vaccinia virus vectors to study the synthesis, intracellular localization, and action of the human immunodeficiency virus trans-activator protein. Virology. 1988 Jun;164(2):450–457. doi: 10.1016/0042-6822(88)90559-4. [DOI] [PubMed] [Google Scholar]
- Fankhauser C., Izaurralde E., Adachi Y., Wingfield P., Laemmli U. K. Specific complex of human immunodeficiency virus type 1 rev and nucleolar B23 proteins: dissociation by the Rev response element. Mol Cell Biol. 1991 May;11(5):2567–2575. doi: 10.1128/mcb.11.5.2567. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Favre D., Studer E., Michel M. R. Two nucleolar targeting signals present in the N-terminal part of Semliki Forest virus capsid protein. Arch Virol. 1994;137(1-2):149–155. doi: 10.1007/BF01311181. [DOI] [PubMed] [Google Scholar]
- Feldherr C. M. Nucleocytoplasmic exchanges during cell division. J Cell Biol. 1966 Oct;31(1):199–203. doi: 10.1083/jcb.31.1.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fontoura B. M., Sorokina E. A., David E., Carroll R. B. p53 is covalently linked to 5.8S rRNA. Mol Cell Biol. 1992 Nov;12(11):5145–5151. doi: 10.1128/mcb.12.11.5145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Garcia-Bustos J., Heitman J., Hall M. N. Nuclear protein localization. Biochim Biophys Acta. 1991 Mar 7;1071(1):83–101. doi: 10.1016/0304-4157(91)90013-m. [DOI] [PubMed] [Google Scholar]
- Guo B., Odgren P. R., van Wijnen A. J., Last T. J., Nickerson J., Penman S., Lian J. B., Stein J. L., Stein G. S. The nuclear matrix protein NMP-1 is the transcription factor YY1. Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10526–10530. doi: 10.1073/pnas.92.23.10526. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hammerschmidt W., Sugden B. Genetic analysis of immortalizing functions of Epstein-Barr virus in human B lymphocytes. Nature. 1989 Aug 3;340(6232):393–397. doi: 10.1038/340393a0. [DOI] [PubMed] [Google Scholar]
- Hammes S. R., Greene W. C. Multiple arginine residues within the basic domain of HTLV-I Rex are required for specific RNA binding and function. Virology. 1993 Mar;193(1):41–49. doi: 10.1006/viro.1993.1101. [DOI] [PubMed] [Google Scholar]
- Hatanaka M. Discovery of the nucleolar targeting signal. Bioessays. 1990 Mar;12(3):143–148. doi: 10.1002/bies.950120310. [DOI] [PubMed] [Google Scholar]
- Hatton T., Zhou S., Standring D. N. RNA- and DNA-binding activities in hepatitis B virus capsid protein: a model for their roles in viral replication. J Virol. 1992 Sep;66(9):5232–5241. doi: 10.1128/jvi.66.9.5232-5241.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hauber J., Malim M. H., Cullen B. R. Mutational analysis of the conserved basic domain of human immunodeficiency virus tat protein. J Virol. 1989 Mar;63(3):1181–1187. doi: 10.1128/jvi.63.3.1181-1187.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Henderson J. E., Amizuka N., Warshawsky H., Biasotto D., Lanske B. M., Goltzman D., Karaplis A. C. Nucleolar localization of parathyroid hormone-related peptide enhances survival of chondrocytes under conditions that promote apoptotic cell death. Mol Cell Biol. 1995 Aug;15(8):4064–4075. doi: 10.1128/mcb.15.8.4064. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hsu T., King D. L., LaBonne C., Kafatos F. C. A Drosophila single-strand DNA/RNA-binding factor contains a high-mobility-group box and is enriched in the nucleolus. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6488–6492. doi: 10.1073/pnas.90.14.6488. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones D., Lee L., Liu J. L., Kung H. J., Tillotson J. K. Marek disease virus encodes a basic-leucine zipper gene resembling the fos/jun oncogenes that is highly expressed in lymphoblastoid tumors. Proc Natl Acad Sci U S A. 1992 May 1;89(9):4042–4046. doi: 10.1073/pnas.89.9.4042. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jordan P., Mannervik M., Tora L., Carmo-Fonseca M. In vivo evidence that TATA-binding protein/SL1 colocalizes with UBF and RNA polymerase I when rRNA synthesis is either active or inactive. J Cell Biol. 1996 Apr;133(2):225–234. doi: 10.1083/jcb.133.2.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kalland K. H., Szilvay A. M., Langhoff E., Haukenes G. Subcellular distribution of human immunodeficiency virus type 1 Rev and colocalization of Rev with RNA splicing factors in a speckled pattern in the nucleoplasm. J Virol. 1994 Mar;68(3):1475–1485. doi: 10.1128/jvi.68.3.1475-1485.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kato S., Hirai K. Marek's disease virus. Adv Virus Res. 1985;30:225–277. doi: 10.1016/s0065-3527(08)60452-2. [DOI] [PubMed] [Google Scholar]
- Kiefer P., Dickson C. Nucleolar association of fibroblast growth factor 3 via specific sequence motifs has inhibitory effects on cell growth. Mol Cell Biol. 1995 Aug;15(8):4364–4374. doi: 10.1128/mcb.15.8.4364. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kubota S., Siomi H., Satoh T., Endo S., Maki M., Hatanaka M. Functional similarity of HIV-I rev and HTLV-I rex proteins: identification of a new nucleolar-targeting signal in rev protein. Biochem Biophys Res Commun. 1989 Aug 15;162(3):963–970. doi: 10.1016/0006-291x(89)90767-5. [DOI] [PubMed] [Google Scholar]
- Larsson S. H., Charlieu J. P., Miyagawa K., Engelkamp D., Rassoulzadegan M., Ross A., Cuzin F., van Heyningen V., Hastie N. D. Subnuclear localization of WT1 in splicing or transcription factor domains is regulated by alternative splicing. Cell. 1995 May 5;81(3):391–401. doi: 10.1016/0092-8674(95)90392-5. [DOI] [PubMed] [Google Scholar]
- Lazinski D., Grzadzielska E., Das A. Sequence-specific recognition of RNA hairpins by bacteriophage antiterminators requires a conserved arginine-rich motif. Cell. 1989 Oct 6;59(1):207–218. doi: 10.1016/0092-8674(89)90882-9. [DOI] [PubMed] [Google Scholar]
- Lee C. Z., Lin J. H., Chao M., McKnight K., Lai M. M. RNA-binding activity of hepatitis delta antigen involves two arginine-rich motifs and is required for hepatitis delta virus RNA replication. J Virol. 1993 Apr;67(4):2221–2227. doi: 10.1128/jvi.67.4.2221-2227.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee L. F., Liu X., Witter R. L. Monoclonal antibodies with specificity for three different serotypes of Marek's disease viruses in chickens. J Immunol. 1983 Feb;130(2):1003–1006. [PubMed] [Google Scholar]
- Leopardi R., Roizman B. Functional interaction and colocalization of the herpes simplex virus 1 major regulatory protein ICP4 with EAP, a nucleolar-ribosomal protein. Proc Natl Acad Sci U S A. 1996 May 14;93(10):4572–4576. doi: 10.1073/pnas.93.10.4572. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lutz P., Puvion-Dutilleul F., Lutz Y., Kedinger C. Nucleoplasmic and nucleolar distribution of the adenovirus IVa2 gene product. J Virol. 1996 Jun;70(6):3449–3460. doi: 10.1128/jvi.70.6.3449-3460.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MacLean C. A., Rixon F. J., Marsden H. S. The products of gene US11 of herpes simplex virus type 1 are DNA-binding and localize to the nucleoli of infected cells. J Gen Virol. 1987 Jul;68(Pt 7):1921–1937. doi: 10.1099/0022-1317-68-7-1921. [DOI] [PubMed] [Google Scholar]
- Malim M. H., Böhnlein S., Hauber J., Cullen B. R. Functional dissection of the HIV-1 Rev trans-activator--derivation of a trans-dominant repressor of Rev function. Cell. 1989 Jul 14;58(1):205–214. doi: 10.1016/0092-8674(89)90416-9. [DOI] [PubMed] [Google Scholar]
- Marasco W. A., Szilvay A. M., Kalland K. H., Helland D. G., Reyes H. M., Walter R. J. Spatial association of HIV-1 tat protein and the nucleolar transport protein B23 in stably transfected Jurkat T-cells. Arch Virol. 1994;139(1-2):133–154. doi: 10.1007/BF01309460. [DOI] [PubMed] [Google Scholar]
- Marechal V., Elenbaas B., Piette J., Nicolas J. C., Levine A. J. The ribosomal L5 protein is associated with mdm-2 and mdm-2-p53 complexes. Mol Cell Biol. 1994 Nov;14(11):7414–7420. doi: 10.1128/mcb.14.11.7414. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matera A. G., Frey M. R., Margelot K., Wolin S. L. A perinucleolar compartment contains several RNA polymerase III transcripts as well as the polypyrimidine tract-binding protein, hnRNP I. J Cell Biol. 1995 Jun;129(5):1181–1193. doi: 10.1083/jcb.129.5.1181. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mears W. E., Lam V., Rice S. A. Identification of nuclear and nucleolar localization signals in the herpes simplex virus regulatory protein ICP27. J Virol. 1995 Feb;69(2):935–947. doi: 10.1128/jvi.69.2.935-947.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morgenstern J. P., Land H. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 1990 Jun 25;18(12):3587–3596. doi: 10.1093/nar/18.12.3587. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ochs R. L., Lischwe M. A., Spohn W. H., Busch H. Fibrillarin: a new protein of the nucleolus identified by autoimmune sera. Biol Cell. 1985;54(2):123–133. doi: 10.1111/j.1768-322x.1985.tb00387.x. [DOI] [PubMed] [Google Scholar]
- Paine P. L., Moore L. C., Horowitz S. B. Nuclear envelope permeability. Nature. 1975 Mar 13;254(5496):109–114. doi: 10.1038/254109a0. [DOI] [PubMed] [Google Scholar]
- Pelham H. R. Hsp70 accelerates the recovery of nucleolar morphology after heat shock. EMBO J. 1984 Dec 20;3(13):3095–3100. doi: 10.1002/j.1460-2075.1984.tb02264.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Perkins A., Cochrane A. W., Ruben S. M., Rosen C. A. Structural and functional characterization of the human immunodeficiency virus rev protein. J Acquir Immune Defic Syndr. 1989;2(3):256–263. [PubMed] [Google Scholar]
- Phelan A., Carmo-Fonseca M., McLaughlan J., Lamond A. I., Clements J. B. A herpes simplex virus type 1 immediate-early gene product, IE63, regulates small nuclear ribonucleoprotein distribution. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9056–9060. doi: 10.1073/pnas.90.19.9056. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Qian Z., Brunovskis P., Lee L., Vogt P. K., Kung H. J. Novel DNA binding specificities of a putative herpesvirus bZIP oncoprotein. J Virol. 1996 Oct;70(10):7161–7170. doi: 10.1128/jvi.70.10.7161-7170.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Qian Z., Brunovskis P., Rauscher F., 3rd, Lee L., Kung H. J. Transactivation activity of Meq, a Marek's disease herpesvirus bZIP protein persistently expressed in latently infected transformed T cells. J Virol. 1995 Jul;69(7):4037–4044. doi: 10.1128/jvi.69.7.4037-4044.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Raska I., Ochs R. L., Andrade L. E., Chan E. K., Burlingame R., Peebles C., Gruol D., Tan E. M. Association between the nucleolus and the coiled body. J Struct Biol. 1990 Jul-Sep;104(1-3):120–127. doi: 10.1016/1047-8477(90)90066-l. [DOI] [PubMed] [Google Scholar]
- Roussel P., André C., Comai L., Hernandez-Verdun D. The rDNA transcription machinery is assembled during mitosis in active NORs and absent in inactive NORs. J Cell Biol. 1996 Apr;133(2):235–246. doi: 10.1083/jcb.133.2.235. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sacher R., Ahlquist P. Effects of deletions in the N-terminal basic arm of brome mosaic virus coat protein on RNA packaging and systemic infection. J Virol. 1989 Nov;63(11):4545–4552. doi: 10.1128/jvi.63.11.4545-4552.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Samad A., Carroll R. B. The tumor suppressor p53 is bound to RNA by a stable covalent linkage. Mol Cell Biol. 1991 Mar;11(3):1598–1606. doi: 10.1128/mcb.11.3.1598. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schat K. A., Buckmaster A., Ross L. J. Partial transcription map of Marek's disease herpesvirus in lytically infected cells and lymphoblastoid cell lines. Int J Cancer. 1989 Jul 15;44(1):101–109. doi: 10.1002/ijc.2910440119. [DOI] [PubMed] [Google Scholar]
- Semmes O. J., Jeang K. T. Localization of human T-cell leukemia virus type 1 tax to subnuclear compartments that overlap with interchromatin speckles. J Virol. 1996 Sep;70(9):6347–6357. doi: 10.1128/jvi.70.9.6347-6357.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Siomi H., Shida H., Nam S. H., Nosaka T., Maki M., Hatanaka M. Sequence requirements for nucleolar localization of human T cell leukemia virus type I pX protein, which regulates viral RNA processing. Cell. 1988 Oct 21;55(2):197–209. doi: 10.1016/0092-8674(88)90043-8. [DOI] [PubMed] [Google Scholar]
- Strouboulis J., Wolffe A. P. Functional compartmentalization of the nucleus. J Cell Sci. 1996 Aug;109(Pt 8):1991–2000. doi: 10.1242/jcs.109.8.1991. [DOI] [PubMed] [Google Scholar]
- Su L., Hershberger R. J., Weissman I. L. LYAR, a novel nucleolar protein with zinc finger DNA-binding motifs, is involved in cell growth regulation. Genes Dev. 1993 May;7(5):735–748. doi: 10.1101/gad.7.5.735. [DOI] [PubMed] [Google Scholar]
- Sugaya K., Bradley G., Nonoyama M., Tanaka A. Latent transcripts of Marek's disease virus are clustered in the short and long repeat regions. J Virol. 1990 Dec;64(12):5773–5782. doi: 10.1128/jvi.64.12.5773-5782.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Szebeni A., Herrera J. E., Olson M. O. Interaction of nucleolar protein B23 with peptides related to nuclear localization signals. Biochemistry. 1995 Jun 27;34(25):8037–8042. doi: 10.1021/bi00025a009. [DOI] [PubMed] [Google Scholar]
- Szekely L., Jiang W. Q., Pokrovskaja K., Wiman K. G., Klein G., Ringertz N. Reversible nucleolar translocation of Epstein-Barr virus-encoded EBNA-5 and hsp70 proteins after exposure to heat shock or cell density congestion. J Gen Virol. 1995 Oct;76(Pt 10):2423–2432. doi: 10.1099/0022-1317-76-10-2423. [DOI] [PubMed] [Google Scholar]
- Szekely L., Pokrovskaja K., Jiang W. Q., de The H., Ringertz N., Klein G. The Epstein-Barr virus-encoded nuclear antigen EBNA-5 accumulates in PML-containing bodies. J Virol. 1996 Apr;70(4):2562–2568. doi: 10.1128/jvi.70.4.2562-2568.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Valdez B. C., Perlaky L., Henning D., Saijo Y., Chan P. K., Busch H. Identification of the nuclear and nucleolar localization signals of the protein p120. Interaction with translocation protein B23. J Biol Chem. 1994 Sep 23;269(38):23776–23783. [PubMed] [Google Scholar]
- Waseem N. H., Lane D. P. Monoclonal antibody analysis of the proliferating cell nuclear antigen (PCNA). Structural conservation and the detection of a nucleolar form. J Cell Sci. 1990 May;96(Pt 1):121–129. doi: 10.1242/jcs.96.1.121. [DOI] [PubMed] [Google Scholar]
- Xie Q., Anderson A. S., Morgan R. W. Marek's disease virus (MDV) ICP4, pp38, and meq genes are involved in the maintenance of transformation of MDCC-MSB1 MDV-transformed lymphoblastoid cells. J Virol. 1996 Feb;70(2):1125–1131. doi: 10.1128/jvi.70.2.1125-1131.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yanagida N., Ogawa R., Li Y., Lee L. F., Nazerian K. Recombinant fowlpox viruses expressing the glycoprotein B homolog and the pp38 gene of Marek's disease virus. J Virol. 1992 Mar;66(3):1402–1408. doi: 10.1128/jvi.66.3.1402-1408.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zapp M. L., Hope T. J., Parslow T. G., Green M. R. Oligomerization and RNA binding domains of the type 1 human immunodeficiency virus Rev protein: a dual function for an arginine-rich binding motif. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7734–7738. doi: 10.1073/pnas.88.17.7734. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhao L. J., Padmanabhan R. Nuclear transport of adenovirus DNA polymerase is facilitated by interaction with preterminal protein. Cell. 1988 Dec 23;55(6):1005–1015. doi: 10.1016/0092-8674(88)90245-0. [DOI] [PubMed] [Google Scholar]