Mediation of Epstein-Barr virus EBNA-LP transcriptional coactivation by Sp100

EMBO Journal

Volumn 24, Issue 20, 2005, Pages 3565-3575

  Ling, Paul D ^a   Peng, Rong Sheng ^a   Nakajima, Ayako ^b   Yu, Jiang H ^b   Tan, Jie ^a   Moses, Stephanie M ^a   Yang, Wei Hong ^b   Zhao, Bo ^c   Kieff, Elliott ^c   Bloch, Kenneth D ^b   Bloch, Donald B ^b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Epstein Barr virus; Gene regulation; Latency; Nuclear bodies; Sp100

Indexed keywords

PROTEIN; PROTEIN EBNA LP; PROTEIN SP100; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; B LYMPHOCYTE; CELL IMMORTALIZATION; CONTROLLED STUDY; EPSTEIN BARR VIRUS; GENE ACTIVATION; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; VIRUS INFECTION;

ANTIGENS, NUCLEAR; AUTOANTIGENS; B-LYMPHOCYTES; CELL NUCLEUS; CELLS, CULTURED; CHROMOSOMAL PROTEINS, NON-HISTONE; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; GENE EXPRESSION REGULATION, VIRAL; HUMANS; NUCLEAR PROTEINS; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE DELETION; TRANSCRIPTION, GENETIC; UP-REGULATION; VIRAL PROTEINS;

HUMAN HERPESVIRUS 4;

EID: 27144522534     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600820     Document Type: Article

References (68)

1. Adamson AL, Kenney S (2001) Epstein-Barr virus immediate-early protein BZLF1 is SUMO-1 modified and disrupts promyelocytic leukemia bodies. J Virol 75: 2388-2399
2. Ahn JH, Hayward GS (1997) The major immediate-early proteins IE1 and IE2 of human cytomegalovirus colocalize with and disrupt PML-associated nuclear bodies at very early times in infected permissive cells. J Virol 71: 4599-4613
3. Allan GJ, Inman GJ, Parker BD, Rowe DT, Farrell PJ (1992) Cell growth effects of Epstein-Barr virus leader protein. J Gen Virol 73: 1547-1551
4. Bell P, Lieberman PM, Maul GG (2000) Lytic but not latent replication of Epstein-Barr virus is associated with PML and induces sequential release of nuclear domain 10 proteins. J Virol 74: 11800-11810
5. Bloch DB, Chiche JD, Orth D, de la Monte SM, Rosenzweig A, Bloch KD (1999) Structural and functional heterogeneity of nuclear bodies. Mol Cell Biol 19: 4423-4430
6. Bloch DB, de la Monte SM, Guigaouri P, Filippov A, Bloch KD (1996) Identification and characterization of a leukocyte-specific component of the nuclear body. J Biol Chem 271: 29198-29204
7. Bloch DB, Nakajima A, Gulick T, Chiche JD, Orth D, de La Monte SM, Bloch KD (2000) Sp110 localizes to the PML-Sp100 nuclear body and may function as a nuclear hormone receptor transcriptional coactivator. Mol Cell Biol 20: 6138-6146
8. Bornkamm GW, Hammerschmidt W (2001) Molecular virology of Epstein-Barr virus. Philos Trans R Soc Lond B Biol Sci 356: 437-459
9. Chelbi-Alix MK, de The H (1999) Herpes virus induced proteasome-dependent degradation of the nuclear bodies-associated PML and Sp100 proteins. Oncogene 18: 935-941
10. Crawford DH (2001) Biology and disease associations of Epstein-Barr virus. Philos Trans R Soc Lond B Biol Sci 356: 461-473
11. Doucas V, Tini M, Egan DA, Evans RM (1999) Modulation of CREB binding protein function by the promyelocytic (PML) oncoprotein suggests a role for nuclear bodies in hormone signaling. Proc Natl Acad Sci USA 96: 2627-2632
12. Dufva M, Olsson M, Rymo L (2001) Epstein-Barr virus nuclear antigen 5 interacts with HAX-1, a possible component of the B-cell receptor signalling pathway. J Gen Virol 82: 1581-1587
13. Eissenberg JC, Elgin SC (2000) The HP1 protein family: getting a grip on chromatin. Curr Opin Genet Dev 10: 204-210
14. Everett RD (2001) DNA viruses and viral proteins that interact with PML nuclear bodies. Oncogene 20: 7266-7273
15. Everett RD, Earnshaw WC, Pluta AF, Sternsdorf T, Ainsztein AM, Carmena M, Ruchaud S, Hsu WL, Orr A (1999) A dynamic connection between centromeres and ND10 proteins. J Cell Sci 112 (Part 20): 3443-3454
16. Floettmann JE, Ward K, Rickinson AB, Rowe M (1996) Cytostatic effect of Epstein-Barr virus latent membrane protein-1 analyzed using tetracycline- regulated expression in B cell lines. Virology 223: 29-40
17. Gu H, Roizman B (2003) The degradation of promyelocytic leukemia and Sp100 proteins by herpes simplex virus 1 is mediated by the ubiquitin- conjugating enzyme UbcH5a. Proc Natl Acad Sci USA 100: 8963-8968
18. Guo A, Salomoni P, Luo J, Shih A, Zhong S, Gu W, Paolo Pandolfi P (2000) The function of PML in p53-dependent apoptosis. Nat Cell Biol 2: 730-736
19. Hagglund R, Roizman B (2004) Role of ICP0 in the strategy of conquest of the host cell by herpes simplex virus 1. J Virol 78: 2169-2178
20. Hammerschmidt W, Sugden B (1989) Genetic analysis of immortalizing functions of Epstein-Barr virus in human B lymphocytes. Nature 340: 393-397
21. Han I, Harada S, Weaver D, Xue Y, Lane W, Orstavik S, Skalhegg B, Kieff E (2001) EBNA-LP associates with cellular proteins including DNA-PK and HA95. J Virol 75: 2475-2481
22. Han I, Xue Y, Harada S, Orstavik S, Skalhegg B, Kieff E (2002) Protein kinase A associates with HA95 and affects transcriptional coactivation by Epstein-Barr virus nuclear proteins. Mol Cell Biol 22: 2136-2146
23. Harada S, Kieff E (1997) Epstein-Barr virus nuclear protein LP stimulates EBNA-2 acidic domain-mediated transcriptional activation. J Virol 71: 6611-6618
24. Hayakawa T, Haraguchi T, Masumoto H, Hiraoka Y (2003) Cell cycle behavior of human HP1 subtypes: distinct molecular domains of HP1 are required for their centromeric localization during interphase and metaphase. J Cell Sci 116: 3327-3338
25. Hodges M, Tissot C, Howe K, Grimwade D, Freemont PS (1998) Structure, organization, and dynamics of promyelocytic leukemia protein nuclear bodies. Am J Hum Genet 63: 297-304
26. Igarashi M, Kawaguchi Y, Hirai K, Mizuno F (2003) Physical interaction of Epstein-Barr virus (EBV) nuclear antigen leader protein (EBNA-LP) with human oestrogen-related receptor 1 (hERR1): hERR1 interacts with a conserved domain of EBNA-LP that is critical for EBV-induced B-cell immortalization. J Gen Virol 84: 319-327
27. Ishov AM, Sotnikov AG, Negorev D, Vladimirova OV, Neff N, Kamitani T, Yeh ET, Strauss III JF, Maul GG (1999) PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J Cell Biol 147: 221-234
28. Jiang WQ, Szekely L, Wendel-Hansen V, Ringertz N, Klein G, Rosen A (1991) Co-localization of the retinoblastoma protein and the Epstein-Barr virus-encoded nuclear antigen EBNA-5. Exp Cell Res 197: 314-318
29. Kashuba E, Mattsson K, Pokrovskaja K, Kiss C, Protopopova M, Ehlin-Henriksson B, Klein G, Szekely L (2003) EBV-encoded EBNA-5 associates with P14ARF in extranucleolar inclusions and prolongs the survival of P14ARF-expressing cells. Int J Cancer 105: 644-653
30. Kawaguchi Y, Nakajima K, Igarashi M, Morita T, Tanaka M, Suzuki M, Yokoyama A, Matsuda G, Kato K, Kanamori M, Hirai K (2000) Interaction of Epstein-Barr virus nuclear antigen leader protein (EBNA-LP) with HS1-associated protein X-1: implication of cytoplasmic function of EBNA-LP. J Virol 74: 10104-10111
31. Kieff E, Rickinson AB (2001) Epstein-Barr virus and its replication. In Virology, Knipe DM, Howley PM (eds), Vol. 2, pp 2511-2573. Philadelphia: Lippencott-Raven Publishers
32. Kitay MK, Rowe DT (1996) Protein-protein interactions between Epstein-Barr virus nuclear antigen-LP and cellular gene products: binding of 70-kilodalton heat shock proteins. Virology 220: 91-99
33. Korioth F, Maul GG, Plachter B, Stamminger T, Frey J (1996) The nuclear domain 10 (ND10) is disrupted by the human cytomegalovirus gene product IE1. Exp Cell Res 229: 155-158
34. Lehming N, Le Saux A, Schuller J, Ptashne M (1998) Chromatin components as part of a putative transcriptional repressing complex. Proc Natl Acad Sci USA 95: 7322-7326
35. Li H, Leo C, Zhu J, Wu X, O'Neil J, Park EJ, Chen JD (2000) Sequestration and inhibition of Daxx-mediated transcriptional repression by PML. Mol Cell Biol 20: 1784-1796
36. Ling PD, Hulls HH (2005) Isolation and immortalization of lymphocytes. In Current Protocols in Molecular Biology, Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Struhl K (eds). New York: John Wiley & Sons Inc
37. Mannick JB, Cohen JI, Birkenbach M, Marchini A, Kieff E (1991) The Epstein-Barr virus nuclear protein encoded by the leader of the EBNA RNAs is important in B-lymphocyte transformation. J Virol 65: 6826-6837
38. Mannick JB, Tong X, Hemnes A, Kieff E (1995) The Epstein-Barr virus nuclear antigen leader protein associates with hsp72/hsc73. J Virol 69: 8169-8172
39. McCann EM, Kelly GL, Rickinson AB, Bell AI (2001) Genetic analysis of the Epstein-Barr virus-coded leader protein EBNA-LP as a co-activator of EBNA2 function. J Gen Virol 82: 3067-3079
40. Melnick A, Licht JD (1999) Deconstructing a disease: RARalpha, its fusion partners, and their roles in the pathogenesis of acute promyelocytic leukemia. Blood 93: 3167-3215
41. Moller A, Sirma H, Hofmann TG, Staege H, Gresko E, Ludi KS, Klimczak E, Droge W, Will H, Schmitz ML (2003) Sp100 is important for the stimulatory effect of homeodomain-interacting protein kinase-2 on p53-dependent gene expression. Oncogene 22: 8731-8737
42. Negorev D, Ishov AM, Maul GG (2001) Evidence for separate ND10-binding and homo-oligomerization domains of Sp100. J Cell Sci 114: 59-68
43. Nicewonger J, Suck G, Bloch D, Swaminathan S (2004) Epstein-Barr virus (EBV) SM protein induces and recruits cellular Sp110b to stabilize mRNAs and enhance EBV lytic gene expression. J Virol 78: 9412-9422
44. Nitsche F, Bell A, Rickinson A (1997) Epstein-Barr virus leader protein enhances EBNA-2-mediated transactivation of latent membrane protein 1 expression: a role for the W1W2 repeat domain. J Virol 71: 6619-6628
45. Pandolfi PP (2001) Oncogenes and tumor suppressors in the molecular pathogenesis of acute promyelocytic leukemia. Hum Mol Genet 10: 769-775
46. Peng CW, Xue Y, Zhao B, Johannsen E, Kieff E, Harada S (2004) Direct interactions between Epstein-Barr virus leader protein LP and the EBNA2 acidic domain underlie coordinate transcriptional regulation. Proc Natl Acad Sci USA 101: 1033-1038
47. Peng R, Gordadze AV, Fuentes Panana EM, Wang F, Zong J, Hayward GS, Tan J, Ling PD (2000a) Sequence and functional analysis of EBNA-LP and EBNA2 proteins from nonhuman primate lymphocryptoviruses. J Virol 74: 379-389
48. Peng R, Tan J, Ling PD (2000b) Conserved regions in the Epstein-Barr virus leader protein define distinct domains required for nuclear localization and transcriptional cooperation with EBNA2. J Virol 74: 9953-9963
49. Peng RS, Moses SC, Tan J, Kremmer E, Ling PD (2005) The Epstein-Barr virus EBNA-LP protein preferentially co-activates EBNA2-mediated stimulation of latent membrane proteins expressed from the viral divergent promoter. J Virol 79: 4492-4505
50. Rickinson AB, Kieff E (2001) Epstein-Barr virus. In Virology, Knipe DM, Howley PM (eds), Vol. 2, pp 2575-2627. Philadelphia: Lippincott-Raven Publishers
51. Sample J, Hummel M, Braun D, Birkenbach M, Kieff E (1986) Nucleotide sequences of mRNAs encoding Epstein-Barr virus nuclear proteins: a probable transcriptional initiation site. Proc Natl Acad Sci USA 83: 5096-5100
52. Seeler JS, Marchio A, Losson R, Desterro JM, Hay RT, Chambon P, Dejean A (2001) Common properties of nuclear body protein SP100 and TIF1alpha chromatin factor: role of SUMO modification. Mol Cell Biol 21: 3314-3324
53. Seeler JS, Marchio A, Sitterlin D, Transy C, Dejean A (1998) Interaction of SP100 with HP1 proteins: a link between the promyelocytic leukemia-associated nuclear bodies and the chromatin compartment. Proc Natl Acad Sci USA 95: 7316-7321
54. Singh PB, Georgatos SD (2002) HP1: facts, open questions, and speculation. J Struct Biol 140: 10-16
55. Speck SH, Pfitzner A, Strominger JL (1986) An Epstein-Barr virus transcript from a latently infected, growth-transformed B-cell line encodes a highly repetitive polypeptide. Proc Natl Acad Sci USA 83: 9298-9302
56. Sternsdorf T, Grotzinger T, Jensen K, Will H (1997) Nuclear dots: actors on many stages. Immunobiology 198: 307-331
57. Sternsdorf T, Guldner HH, Szostecki C, Grotzinger T, Will H (1995) Two nuclear dot-associated proteins, PML and Sp100, are often co-autoimmunogenic in patients with primary biliary cirrhosis. Scand J Immunol 42: 257-268
58. Sternsdorf T, Jensen K, Reich B, Will H (1999) The nuclear dot protein sp100, characterization of domains necessary for dimerization, subcellular localization, and modification by small ubiquitin-like modifiers. J Biol Chem 274: 12555-12566
59. Szekely L, Jiang WQ, Pokrovskaja K, Wiman KG, Klein G, Ringertz N (1995a) 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 76: 2423-2432
60. Szekely L, Pokrovskaja K, Jiang WQ, de The H, Ringertz N, Klein G (1996) The Epstein-Barr virus-encoded nuclear antigen EBNA-5 accumulates in PML-containing bodies. J Virol 70: 2562-2568
61. Szekely L, Pokrovskaja K, Jiang WQ, Selivanova G, Lowbeer M, Ringertz N, Wiman KG, Klein G (1995b) Resting B-cells, EBV-infected B-blasts and established lymphoblastoid cell lines differ in their Rb, p53 and EBNA-5 expression patterns. Oncogene 10: 1869-1874
62. Szekely L, Selivanova G, Magnusson KP, Klein G, Wiman KG (1993) EBNA-5, an Epstein-Barr virus-encoded nuclear antigen, binds to the retinoblastoma and p53 proteins. Proc Natl Acad Sci USA 90: 5455-5459
63. Szostecki C, Guldner HH, Netter HJ, Will H (1990) Isolation and characterization of cDNA encoding a human nuclear antigen predominantly recognized by autoantibodies from patients with primary biliary cirrhosis. J Immunol 145: 4338-4347
64. Szostecki C, Krippner H, Penner E, Bautz FA (1987) Autoimmune sera recognize a 100 kD nuclear protein antigen (sp-100). Clin Exp Immunol 68: 108-116
65. Xie K, Lambie EJ, Snyder M (1993) Nuclear dot antigens may specify transcriptional domains in the nucleus. Mol Cell Biol 13: 6170-6179
66. Yokoyama A, Tanaka M, Matsuda G, Kato K, Kanamori M, Kawasaki H, Hirano H, Kitabayashi I, Ohki M, Hirai K, Kawaguchi Y (2001) Identification of major phosphorylation sites of Epstein-Barr virus nuclear antigen leader protein (EBNA-LP): ability of EBNA-LP to induce latent membrane protein 1 cooperatively with EBNA-2 is regulated by phosphorylation. J Virol 75: 5119-5128
67. Yoo LI, Mooney M, Puglielli MT, Speck SH (1997) B-cell lines immortalized with an Epstein-Barr virus mutant lacking the Cp EBNA2 enhancer are biased toward utilization of the oriP-Proximal EBNA gene promoter Wp1. J Virol 71: 9134-9142
68. Yordy JS, Li R, Sementchenko VI, Pei H, Muise-Helmericks RC, Watson DK (2004) SP100 expression modulates ETS1 transcriptional activity and inhibits cell invasion. Oncogene 23: 6654-6665