The nuclear and adherent junction complex component protein ubinuclein negatively regulates the productive cycle of Epstein-Barr Virus in epithelial cells

Journal of Virology

Volumn 85, Issue 2, 2011, Pages 784-794

  Gruffat, Henri ^a,b   Lupo, Julien ^c,d   Morand, Patrice ^c,d   Boyer, Véronique ^c   Manet, Evelyne ^a,b  

^a UNIVERSITÉ DE LYON   (France)

^b University Lyon i   (France)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^d GRENOBLE UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; IMMEDIATE EARLY PROTEIN BZLF1; SHORT HAIRPIN RNA; UBINUCLEIN; UNCLASSIFIED DRUG; VIRUS DNA;

ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; DOWN REGULATION; EPITHELIUM CELL; EPSTEIN BARR VIRUS; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; TIGHT JUNCTION; VIRUS PARTICLE;

CELL LINE; CHROMATIN IMMUNOPRECIPITATION; DNA, VIRAL; EPITHELIAL CELLS; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; HERPESVIRUS 4, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; PROTEIN BINDING; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

EQUUS SUBG. HIPPOTIGRIS; HUMAN HERPESVIRUS 4;

EID: 78650655864     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01397-10     Document Type: Article

References (70)

1. Adamson, A. L., D. Darr, E. Holley-Guthrie, R. A. Johnson, A. Mauser, J. Swenson, and S. Kenney. 2000. Epstein-Barr virus immediate-early proteins BZLF1 and BRLF1 activate the ATF2 transcription factor by increasing the levels of phosphorylated p38 and c-Jun N-terminal kinases. J. Virol. 74:1224-1233.
2. Aho, S., M. Buisson, T. Pajunen, Y. W. Ryoo, J. F. Giot, H. Gruffat, A.Sergeant, and J. Uitto. 2000. Ubinuclein, a novel nuclear protein interacting with cellular and viral transcription factors. J. Cell Biol. 148:1165-1176.
3. Aho, S., J. Lupo, P. A. Coly, A. Sabine, M. Castellazzi, P. Morand, A. Sergeant, E. Manet, V. Boyer, and H. Gruffat. 2009. Characterization of the ubinuclein protein as a new member of the nuclear and adhesion complex components (NACos). Biol. Cell 101:319-334.
4. Babcock, G. J., L. L. Decker, M. Volk, and D. A. Thorley-Lawson. 1998. EBV persistence in memory B cells in vivo. Immunity 9:395-404.
5. Balaji, S., L. M. Iyer, and L. Aravind. 2009. HPC2 and ubinuclein define a novel family of histone chaperones conserved throughout eukaryotes. Mol. Biosyst. 5:269-275.
6. Balda, M. S., and K. Matter. 2009. Tight junctions and the regulation of gene expression. Biochim. Biophys. Acta 1788:761-767.
7. Banumathy, G., N. Somaiah, R. Zhang, Y. Tang, J. Hoffmann, M. Andrake, H. Ceulemans, D. Schultz, R. Marmorstein, and P. D. Adams. 2009. Human UBN1 is an ortholog of yeast Hpc2p and has an essential role in the HIRA/ ASF1a chromatin-remodeling pathway in senescent cells. Mol. Cell. Biol. 29:758-770.
8. Becker, J., U. Leser, M. Marschall, A. Langford, W. Jilg, H. Gelderblom, P. Reichart, and H. Wolf. 1991. Expression of proteins encoded by Epstein- Barr virus trans-activator genes depends on the differentiation of epithelial cells in oral hairy leukoplakia. Proc. Natl. Acad. Sci. U. S. A. 88:8332-8336.
9. Betanzos, A., M. Huerta, E. Lopez-Bayghen, E. Azuara, J. Amerena, and L. Gonzalez-Mariscal. 2004. The tight junction protein ZO-2 associates with Jun, Fos and C/EBP transcription factors in epithelial cells. Exp. Cell Res. 292:51-66.
10. Bhende, P. M., S. J. Dickerson, X. Sun, W. H. Feng, and S. C. Kenney. 2007. X-box-binding protein 1 activates lytic Epstein-Barr virus gene expression in combination with protein kinase D. J. Virol. 81:7363-7370.
11. Bhende, P. M., W. T. Seaman, H. J. Delecluse, and S. C. Kenney. 2004. The EBV lytic switch protein, Z, preferentially binds to and activates the methylated viral genome. Nat. Genet. 36:1099-1104.
12. Chang, Y.-N., D. L.-Y. Dong, G. S. Hayward, and D. Hayward. 1990. The Epstein-Barr virus Zta transactivator: a member of the bZIP family with unique DNA-binding specificity and a dimerization domain that lacks the characteristic heptad leucine zipper motif. J. Virol. 64:3358-3369.
13. Chevallier-Greco, A., H. Gruffat, E. Manet, A. Calender, and A. Sergeant. 1989. The Epstein-Barr virus (EBV) DR enhancer contains two functionally different domains: domain A is constitutive and cell specific, domain B is transactivated by the EBV early protein R. J. Virol. 63:615-623.
14. Chevallier-Greco, A., E. Manet, P. Chavrier, C. Mosnier, J. Daillie, and A. Sergeant. 1986. Both Epstein-Barr virus (EBV) encoded trans-acting factors, EB1 and EB2, are required to activate transcription from an EBV early promoter. EMBO J. 5:3243-3249.
15. Countryman, J., and G. Miller. 1985. Activation of expression of latent Epstein-Barr herpesvirus after gene transfer with a small cloned subfragment of heterogeneous viral DNA. Proc. Natl. Acad. Sci. U. S. A. 82:4085-4089.
16. Crawford, D. H., and I. Ando. 1986. EB virus induction is associated with B-cell maturation. Immunology 59:405-409.
17. Delecluse, H. J., T. Hilsendegen, D. Pich, R. Zeidler, and W. Hammerschmidt. 1998. Propagation and recovery of intact, infectious Epstein-Barr virus from prokaryotic to human cells. Proc. Natl. Acad. Sci. U. S. A. 95:8245-8250.
18. Dickerson, S. J., Y. Xing, A. R. Robinson, W. T. Seaman, H. Gruffat, and S. C. Kenney. 2009. Methylation-dependent binding of the Epstein-Barr virus BZLF1 protein to viral promoters. PLoS Pathog. 5:e1000356.
19. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
20. Fahmi, H., C. Cochet, Z. Hmama, P. Opolon, and I. Joab. 2000. Transforming growth factor beta 1 stimulates expression of the Epstein-Barr virus BZLF1 immediate-early gene product ZEBRA by an indirect mechanism which requires the MAPK kinase pathway. J. Virol. 74:5810-5818.
21. Farrell, P. J., D. T. Rowe, C. M. Rooney, and T. Kouzarides. 1989. Epstein-Barr virus BZLF1 trans-activator specifically binds to a consensus AP-1 site and is related to c-fos. EMBO J. 8:127-132.
22. Feng, W. H., R. J. Kraus, S. J. Dickerson, H. J. Lim, R. J. Jones, X. Yu, J. E. Mertz, and S. C. Kenney. 2007. ZEB1 and c-Jun levels contribute to the establishment of highly lytic Epstein-Barr virus infection in gastric AGS cells. J. Virol. 81:10113-10122.
23. Grogan, E., H. Jenson, J. Countryman, L. Heston, L. Gradoville, and G. Miller. 1987. Transfection of a rearranged viral DNA fragment, WZhet, stably converts latent Epstein-Barr viral infection to productive infection in lymphoid cells. Proc. Natl. Acad. Sci. U. S. A. 84:1332-1336.
24. Gruffat, H., J. Batisse, D. Pich, B. Neuhierl, E. Manet, W. Hammerschmidt, and A. Sergeant. 2002. Epstein-Barr virus mRNA export factor EB2 is essential for production of infectious virus. J. Virol. 76:9635-9644.
25. Gruffat, H., E. Manet, A. Rigolet, and A. Sergeant. 1990. The enhancer factor R of Epstein-Barr virus (EBV) is a sequence-specific DNA binding protein. Nucleic Acids Res. 18:6835-6843.
26. Gruffat, H., E. Manet, and A. Sergeant. 2002. MEF2-mediated recruitment of class II HDAC at the EBV immediate early gene BZLF1 links latency and chromatin remodeling. EMBO Rep. 3:141-146.
27. Gruffat, H., and A. Sergeant. 1994. Characterization of the DNA-binding site repertoire for the Epstein-Barr virus transcription factor R. Nucleic Acids Res. 22:1172-1178.
28. Hadinoto, V., M. Shapiro, C. C. Sun, and D. A. Thorley-Lawson. 2009. The dynamics of EBV shedding implicate a central role for epithelial cells in amplifying viral output. PLoS Pathog. 5:e1000496.
29. Hardwick, J. M., P. M. Lieberman, and S. D. Hayward. 1988. A new Epstein-Barr virus transactivator, R, induces expression of a cytoplasmic early antigen. J. Virol. 62:2274-2284.
30. Henle, W. 1972. Role of Epstein-Barr virus in infectious mononucleosis and malignant lymphomas in man. Fed. Proc. 31:1674.
31. Hiriart, E., G. Farjot, H. Gruffat, M. V. Nguyen, A. Sergeant, and E. Manet. 2003. A novel nuclear export signal and a REF interaction domain both promote mRNA export by the Epstein-Barr virus EB2 protein. J. Biol. Chem. 278:335-342.
32. Hochberg, D., J. M. Middeldorp, M. Catalina, J. L. Sullivan, K. Luzuriaga, and D. A. Thorley-Lawson. 2004. Demonstration of the Burkitt's lymphoma Epstein-Barr virus phenotype in dividing latently infected memory cells in vivo. Proc. Natl. Acad. Sci. U. S. A. 101:239-244.
33. Hong, G. K., M. L. Gulley, W. H. Feng, H. J. Delecluse, E. Holley-Guthrie, and S. C. Kenney. 2005. Epstein-Barr virus lytic infection contributes to lymphoproliferative disease in a SCID mouse model. J. Virol. 79:13993-14003.
34. Huang, J., G. Liao, H. Chen, F. Y. Wu, L. Hutt-Fletcher, G. S. Hayward, and S. D. Hayward. 2006. Contribution of C/EBP proteins to Epstein-Barr virus lytic gene expression and replication in epithelial cells. J. Virol. 80:1098-1109.
35. Israel, B. F., and S. C. Kenney. 2005. EBV lytic infection. Robertson ES, Philadelphia, PA.
36. Jaramillo, B. E., A. Ponce, J. Moreno, A. Betanzos, M. Huerta, E. Lopez- Bayghen, and L. Gonzalez-Mariscal. 2004. Characterization of the tight junction protein ZO-2 localized at the nucleus of epithelial cells. Exp. Cell Res. 297:247-258. (Pubitemid 38759577)
37. Jones, R. J., S. Dickerson, P. M. Bhende, H. J. Delecluse, and S. C. Kenney. 2007. Epstein-Barr virus lytic infection induces retinoic acid-responsive genes through induction of a retinol-metabolizing enzyme, DHRS9. J. Biol. Chem. 282:8317-8324.
38. Kavanagh, E., M. Buchert, A. Tsapara, A. Choquet, M. S. Balda, F. Hollande, and K. Matter. 2006. Functional interaction between the ZO-1-interacting transcription factor ZONAB/DbpA and the RNA processing factor symplekin. J. Cell Sci. 119:5098-5105.
39. Laichalk, L. L., and D. A. Thorley-Lawson. 2005. Terminal differentiation into plasma cells initiates the replicative cycle of Epstein-Barr virus in vivo. J. Virol. 79:1296-1307.
40. Mahot, S., A. Sergeant, E. Drouet, and H. Gruffat. 2003. A novel function for the Epstein-Barr virus transcription factor EB1/Zta: induction of transcription of the hIL-10 gene. J. Gen. Virol. 84:965-974.
41. Manet, E., C. Allera, H. Gruffat, I. Mikaelian, A. Rigolet, and A. Sergeant. 1993. The acidic activation domain of the Epstein-Barr virus transcription factor R interacts in vitro with both TBP and TFIIB and is cell-specifically potentiated by a proline-rich region. Gene Expr. 3:49-59.
42. Matter, K., and M. S. Balda. 2007. Epithelial tight junctions, gene expression and nucleo-junctional interplay. J. Cell Sci. 120:1505-1511.
43. Matter, K., and M. S. Balda. 2003. Signalling to and from tight junctions. Nat. Rev. Mol. Cell Biol. 4:225-236.
44. Mikaelian, I., E. Drouet, V. Marechal, G. Denoyel, J. C. Nicolas, and A. Sergeant. 1993. The DNA-binding domain of two bZIP transcription factors, the Epstein-Barr virus switch gene product EB1 and Jun, is a bipartite nuclear targeting sequence. J. Virol. 67:734-742.
45. Neuhierl, B., R. Feederle, W. Hammerschmidt, and H. J. Delecluse. 2002.Glycoprotein gp110 of Epstein-Barr virus determines viral tropism and efficiency of infection. Proc. Natl. Acad. Sci. U. S. A. 99:15036-15041.
46. Niedobitek, G., A. Agathanggelou, H. Herbst, L. Whitehead, D. H. Wright, and L. S. Young. 1997. Epstein-Barr virus (EBV) infection in infectious mononucleosis: virus latency, replication and phenotype of EBV-infected cells. J. Pathol. 182:151-159.
47. Niedobitek, G., A. Agathanggelou, N. Steven, and L. S. Young. 2000. Epstein- Barr virus (EBV) in infectious mononucleosis: detection of the virus in tonsillar B lymphocytes but not in desquamated oropharyngeal epithelial cells. Mol. Pathol. 53:37-42.
48. Orlando, V., H. Strutt, and R. Paro. 1997. Analysis of chromatin structure by in vivo formaldehyde cross-linking. Methods 11:205-214.
49. Petosa, C., P. Morand, F. Baudin, M. Moulin, J. B. Artero, and C. W. Muller. 2006. Structural basis of lytic cycle activation by the Epstein-Barr virus ZEBRA protein. Mol. Cell 21:565-572.
50. Rickinson, A. B., J. E. Jarvis, D. H. Crawford, and M. A. Epstein. 1974. Observations on the type of infection by Epstein-Barr virus in pe ripheral lymphoid cells of patients with infectious mononucleosis. Int. J. Cancer. 14:704-715.
51. Santaguida, M., K. Schepers, B. King, A. J. Sabnis, E. C. Forsberg, J. L. Attema, B. S. Braun, and E. Passegue. 2009. JunB protects against myeloid malignancies by limiting hematopoietic stem cell proliferation and differentiation without affecting self-renewal. Cancer Cell 15:341-352.
52. Schepers, A., D. Pich, J. Mankertz, and W. Hammerschmidt. 1993. cis-acting elements in the lytic origin of DNA replication of Epstein-Barr virus. J. Virol. 67:4237-4245.
53. Sista, N. D., C. Barry, K. Sampson, and J. Pagano. 1995. Physical and functional interaction of the Epstein-Barr virus BZLF1 transactivator with the retinoic acid receptors RAR alpha and RXR alpha. Nucleic Acids Res. 23:1729-1736.
54. Sista, N. D., J. S. Pagano, W. Liao, and S. Kenney. 1993. Retinoic acid is a negative regulator of the Epstein-Barr virus protein (BZLF1) that mediates disruption of latent infection. Proc. Natl. Acad. Sci. U. S. A. 90:3894-3898.
55. Speck, S. H., T. Chatila, and E. Flemington. 1997. Reactivation of the Epstein-Barr virus: regulation and function of the BZLF1 gene. Trends Microbiol. 5:399-405.
56. Tagami, H., D. Ray-Gallet, G. Almouzni, and Y. Nakatani. 2004. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116:51-61. (Pubitemid 38156183)
57. Takada, K., and Y. Ono. 1989. Synchronous and sequential activation of latently infected Epstein-Barr virus genomes. J. Virol. 63:445-449.
58. Thompson, M. P., and R. Kurzrock. 2004. Epstein-Barr virus and cancer. Clin. Cancer Res. 10:803-821.
59. Thorley-Lawson, D. A. 2001. Epstein-Barr virus: exploiting the immune system. Nat. Rev. Immunol. 1:75-82.
60. Thorley-Lawson, D. A., and M. J. Allday. 2008. The curious case of the tumour virus: 50 years of Burkitt's lymphoma. Nat. Rev. Microbiol. 6:913-924.
61. Thorley-Lawson, D. A., and A. Gross. 2004. Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N. Engl. J. Med. 350:1328-1337.
62. Urier, G., M. Buisson, P. Chambard, and A. Sergeant. 1989. The Epstein-Barr virus early protein EB1 activates transcription from different responsive elements including AP-1 binding sites. EMBO J. 8:1447-1453.
63. Waltzer, L., P. Y. Bourillot, A. Sergeant, and E. Manet. 1995. RBP-J. κrepression activity is mediated by a co-repressor and antagonized by the Epstein-Barr virus transcription factor EBNA2. Nucleic Acids Res. 23:4939-4945.
64. Waltzer, L., M. Perricaudet, A. Sergeant, and E. Manet. 1996. Epstein-Barr virus EBNA3A and EBNA3C proteins both repress RBP-J. κ-EBNA2-activated transcription by inhibiting the binding of RBP-J. κ to DNA. J. Virol. 70:5909-5915.
65. Wu, F. Y., H. Chen, S. E. Wang, C. M. ApRhys, G. Liao, M. Fujimuro, C. J. Farrell, J. Huang, S. D. Hayward, and G. S. Hayward. 2003. CCAAT/ enhancer binding protein alpha interacts with ZTA and mediates ZTAinduced p21(CIP-1) accumulation and G(1) cell cycle arrest during the Epstein-Barr virus lytic cycle. J. Virol. 77:1481-1500.
66. Yang-Yen, H. F., X. K. Zhang, G. Graupner, M. Tzukerman, B. Sakamoto, M. Karin, and M. Pfahl. 1991. Antagonism between retinoic acid receptors and AP-1: implications for tumor promotion and inflammation. New Biol. 3:1206-1219.
67. Young, L. S., R. Lau, M. Rowe, G. Niedobitek, G. Packham, F. Shanahan, D. T. Rowe, D. Greenspan, J. S. Greenspan, A. B. Rickinson, et al. 1991. Differentiation-associated expression of the Epstein-Barr virus BZLF1 transactivator protein in oral hairy leukoplakia. J. Virol. 65:2868-2874.
68. Zalani, S., E. Holley-Guthrie, and S. Kenney. 1996. Epstein-Barr viral latency is disrupted by the immediate-early BRLF1 protein through a cellspecific mechanism. Proc. Natl. Acad. Sci. U. S. A. 93:9194-9199.
69. Zhang, J. X., H. L. Chen, Y. S. Zong, K. H. Chan, J. Nicholls, J. M. Middeldorp, J. S. Sham, B. E. Griffin, and M. H. Ng. 1998. Epstein-Barr virus expression within keratinizing nasopharyngeal carcinoma. J. Med. Virol. 55:227-233. (Pubitemid 28270768)
70. Zur Hausen, H., F. J. O'Neil, U. K. Freese, and E. Hecker. 1978. Persisting oncogenic herpesvirus induced by the tumor promoter TPA. Nature 27:373-375