Id1 interacts and stabilizes the Epstein-Barr virus latent membrane protein 1 (LMP1) in nasopharyngeal epithelial cells

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Hau, Pok Man ^a   Tsang, Chi Man ^a   Yip, Yim Ling ^a   Huen, Michael S Y ^b   Tsao, Sai Wah ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; INHIBITOR OF DIFFERENTIATION 1; LATENT MEMBRANE PROTEIN 1; MESSENGER RNA; PROTEASOME; EBV ASSOCIATED MEMBRANE ANTIGEN, EPSTEIN BARR VIRUS; EBV-ASSOCIATED MEMBRANE ANTIGEN, EPSTEIN-BARR VIRUS; ID1 PROTEIN, HUMAN; MATRIX PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CANCER CELL CULTURE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EPITHELIUM CELL; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INCUBATION TIME; INHIBITION KINETICS; NASOPHARYNX CARCINOMA; NOSE MUCOSA; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STABILITY; RNA TRANSCRIPTION; UBIQUITINATION; CELL LINE; CELL STRAIN HEK293; EPSTEIN BARR VIRUS INFECTION; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; NASOPHARYNX TUMOR; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELL LINE; VIROLOGY; WESTERN BLOTTING;

HUMAN HERPESVIRUS 4;

BLOTTING, WESTERN; CELL LINE; CELL LINE, TUMOR; EPSTEIN-BARR VIRUS INFECTIONS; FLUORESCENT ANTIBODY TECHNIQUE; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; INHIBITOR OF DIFFERENTIATION PROTEIN 1; NASOPHARYNGEAL NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UBIQUITINATION; VIRAL MATRIX PROTEINS;

EID: 79959295164     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021176     Document Type: Article

References (47)

1. Epstein MA, Achong BG, Barr YM, (1964) Virus Particles in Cultured Lymphoblasts from Burkitt's Lymphoma. Lancet 1: 702-703.
2. Young LS, Rickinson AB, (2004) Epstein-Barr virus: 40 years on. Nat Rev Cancer 4: 757-768.
3. Lam N, Sugden B, (2003) LMP1, a viral relative of the TNF receptor family, signals principally from intracellular compartments. EMBO J 22: 3027-3038.
4. Rothenberger S, Rousseaux M, Knecht H, Bender FC, Legler DF, et al. (2002) Association of the Epstein-Barr virus latent membrane protein 1 with lipid rafts is mediated through its N-terminal region. Cell Mol Life Sci 59: 171-180.
5. Soni V, Cahir-McFarland E, Kieff E, (2007) LMP1 TRAFficking activates growth and survival pathways. Adv Exp Med Biol 597: 173-187.
6. Brooks L, Yao QY, Rickinson AB, Young LS, (1992) Epstein-Barr virus latent gene transcription in nasopharyngeal carcinoma cells: coexpression of EBNA1, LMP1, and LMP2 transcripts. J Virol 66: 2689-2697.
7. Cheung ST, Huang DP, Hui AB, Lo KW, Ko CW, et al. (1999) Nasopharyngeal carcinoma cell line (C666-1) consistently harbouring Epstein-Barr virus. Int J Cancer 83: 121-126.
8. Chen H, Hutt-Fletcher L, Cao L, Hayward SD, (2003) A positive autoregulatory loop of LMP1 expression and STAT activation in epithelial cells latently infected with Epstein-Barr virus. J Virol 77: 4139-4148.
9. Johansson P, Jansson A, Ruetschi U, Rymo L, (2010) The p38 signaling pathway upregulates expression of the Epstein-Barr virus LMP1 oncogene. J Virol 84: 2787-2797.
10. Goormachtigh G, Ouk TS, Mougel A, Tranchand-Bunel D, Masy E, et al. (2006) Autoactivation of the Epstein-Barr virus oncogenic protein LMP1 during type II latency through opposite roles of the NF-kappaB and JNK signaling pathways. J Virol 80: 7382-7393.
11. Demetriades C, Mosialos G, (2009) The LMP1 promoter can be transactivated directly by NF-kappaB. J Virol 83: 5269-5277.
12. Johansson P, Jansson A, Ruetschi U, Rymo L, (2009) Nuclear factor-kappaB binds to the Epstein-Barr Virus LMP1 promoter and upregulates its expression. J Virol 83: 1393-1401.
13. Lo AK, To KF, Lo KW, Lung RW, Hui JW, et al. (2007) Modulation of LMP1 protein expression by EBV-encoded microRNAs. Proc Natl Acad Sci U S A 104: 16164-16169.
14. Aviel S, Winberg G, Massucci M, Ciechanover A, (2000) Degradation of the epstein-barr virus latent membrane protein 1 (LMP1) by the ubiquitin-proteasome pathway. Targeting via ubiquitination of the N-terminal residue. J Biol Chem 275: 23491-23499.
15. Benezra R, Davis RL, Lassar A, Tapscott S, Thayer M, et al. (1990) Id: a negative regulator of helix-loop-helix DNA binding proteins. Control of terminal myogenic differentiation. Ann N Y Acad Sci 599: 1-11.
16. Perk J, Iavarone A, Benezra R, (2005) Id family of helix-loop-helix proteins in cancer. Nat Rev Cancer 5: 603-614.
17. Li HM, Zhuang ZH, Wang Q, Pang JC, Wang XH, et al. (2004) Epstein-Barr virus latent membrane protein 1 (LMP1) upregulates Id1 expression in nasopharyngeal epithelial cells. Oncogene 23: 4488-4494.
18. Everly DN Jr, Mainou BA, Raab-Traub N, (2008) The ID proteins contribute to the growth of rodent fibroblasts during LMP1-mediated transformation. Virology 376: 258-269.
19. Everly DN Jr, Mainou BA, Raab-Traub N, (2004) Induction of Id1 and Id3 by latent membrane protein 1 of Epstein-Barr virus and regulation of p27/Kip and cyclin-dependent kinase 2 in rodent fibroblast transformation. J Virol 78: 13470-13478.
20. Tsang CM, Zhang G, Seto E, Takada K, Deng W, et al. (2010) Epstein-Barr virus infection in immortalized nasopharyngeal epithelial cells: Regulation of infection and phenotypic characterization. Int J Cancer 127: 1570-1583.
21. Lui VW, Wong EY, Ho Y, Hong B, Wong SC, et al. (2009) STAT3 activation contributes directly to Epstein-Barr virus-mediated invasiveness of nasopharyngeal cancer cells in vitro. Int J Cancer 125: 1884-1893.
22. Kwok WK, Pang JC, Lo KW, Ng HK, (2009) Role of the RARRES1 gene in nasopharyngeal carcinoma. Cancer Genet Cytogenet 194: 58-64.
23. Tsang CM, Zhang G, Seto E, Takada K, Deng W, et al. (2010) Epstein-Barr virus infection in immortalized nasopharyngeal epithelial cells: Regulation of infection and phenotypic characterization. Int J Cancer.
24. Yao KT, Zhang HY, Zhu HC, Wang FX, Li GY, et al. (1990) Establishment and characterization of two epithelial tumor cell lines (HNE-1 and HONE-1) latently infected with Epstein-Barr virus and derived from nasopharyngeal carcinomas. Int J Cancer 45: 83-89.
25. Sizhong Z, Xiukung G, Yi Z, (1983) Cytogenetic studies on an epithelial cell line derived from poorly differentiated nasopharyngeal carcinoma. Int J Cancer 31: 587-590.
26. Huang DP, Ho JH, Poon YF, Chew EC, Saw D, et al. (1980) Establishment of a cell line (NPC/HK1) from a differentiated squamous carcinoma of the nasopharynx. Int J Cancer 26: 127-132.
27. Barranco SC, Townsend CM Jr, Casartelli C, Macik BG, Burger NL, et al. (1983) Establishment and characterization of an in vitro model system for human adenocarcinoma of the stomach. Cancer Res 43: 1703-1709.
28. Takada K, Horinouchi K, Ono Y, Aya T, Osato T, et al. (1991) An Epstein-Barr virus-producer line Akata: establishment of the cell line and analysis of viral DNA. Virus Genes 5: 147-156.
29. Hu LF, Chen F, Zhen QF, Zhang YW, Luo Y, et al. (1995) Differences in the growth pattern and clinical course of EBV-LMP1 expressing and non-expressing nasopharyngeal carcinomas. Eur J Cancer 31A: 658-660.
30. Hila L, Farah F, Ayari H, Ferjaoui M, Dehria W, et al. (2009) Epidemiological study, immunohistochemistry and in situ hybridization studies of nasopharyngeal carcinomas: a Tunisian report. Pathol Biol (Paris) 57: 427-429.
31. Lo AK, Lo KW, Tsao SW, Wong HL, Hui JW, et al. (2006) Epstein-Barr virus infection alters cellular signal cascades in human nasopharyngeal epithelial cells. Neoplasia 8: 173-180.
32. Hicke L, (1997) Ubiquitin-dependent internalization and down-regulation of plasma membrane proteins. FASEB J 11: 1215-1226.
33. Miskimins WK, Shimizu N, (1982) Dual pathways for epidermal growth factor processing after receptor-mediated endocytosis. J Cell Physiol 112: 327-338.
34. Man C, Rosa J, Yip YL, Cheung AL, Kwong YL, et al. (2008) Id1 overexpression induces tetraploidization and multiple abnormal mitotic phenotypes by modulating aurora A. Mol Biol Cell 19: 2389-2401.
35. Kim AH, Puram SV, Bilimoria PM, Ikeuchi Y, Keough S, et al. (2009) A centrosomal Cdc20-APC pathway controls dendrite morphogenesis in postmitotic neurons. Cell 136: 322-336.
36. Manthey C, Mern DS, Gutmann A, Zielinski AJ, Herz C, et al. (2010) Elevated endogenous expression of the dominant negative basic helix-loop-helix protein ID1 correlates with significant centrosome abnormalities in human tumor cells. BMC Cell Biol 11: 2.
37. Lasorella A, Stegmuller J, Guardavaccaro D, Liu G, Carro MS, et al. (2006) Degradation of Id2 by the anaphase-promoting complex couples cell cycle exit and axonal growth. Nature 442: 471-474.
38. Hasskarl J, Mern DS, Munger K, (2008) Interference of the dominant negative helix-loop-helix protein ID1 with the proteasomal subunit S5A causes centrosomal abnormalities. Oncogene 27: 1657-1664.
39. Rothenberger S, Burns K, Rousseaux M, Tschopp J, Bron C, (2003) Ubiquitination of the Epstein-Barr virus-encoded latent membrane protein 1 depends on the integrity of the TRAF binding site. Oncogene 22: 5614-5618.
40. Lo AK, Dawson CW, Lo KW, Yu Y, Young LS, (2010) Upregulation of Id1 by Epstein-Barr Virus-encoded LMP1 confers resistance to TGFbeta-mediated growth inhibition. Mol Cancer 9: 155.
41. Panchanathan R, Shen H, Zhang X, Ho SM, Choubey D, (2010) Mutually positive regulatory feedback loop between interferons and estrogen receptor-alpha in mice: implications for sex bias in autoimmunity. PLoS One 5: e10868.
42. Rocca A, Viale G, Gelber RD, Bottiglieri L, Gelber S, et al. (2008) Pathologic complete remission rate after cisplatin-based primary chemotherapy in breast cancer: correlation with p63 expression. Cancer Chemother Pharmacol 61: 965-971.
43. Anand G, Yin X, Shahidi AK, Grove L, Prochownik EV, (1997) Novel regulation of the helix-loop-helix protein Id1 by S5a, a subunit of the 26 S proteasome. J Biol Chem 272: 19140-19151.
44. Ikeda M, Ikeda A, Longnecker R, (2001) PY motifs of Epstein-Barr virus LMP2A regulate protein stability and phosphorylation of LMP2A-associated proteins. J Virol 75: 5711-5718.
45. Tang W, Pavlish OA, Spiegelman VS, Parkhitko AA, Fuchs SY, (2003) Interaction of Epstein-Barr virus latent membrane protein 1 with SCFHOS/beta-TrCP E3 ubiquitin ligase regulates extent of NF-kappaB activation. J Biol Chem 278: 48942-48949.
46. Glaser R, Zhang HY, Yao KT, Zhu HC, Wang FX, et al. (1989) Two epithelial tumor cell lines (HNE-1 and HONE-1) latently infected with Epstein-Barr virus that were derived from nasopharyngeal carcinomas. Proc Natl Acad Sci U S A 86: 9524-9528.
47. Li HM, Man C, Jin Y, Deng W, Yip YL, et al. (2006) Molecular and cytogenetic changes involved in the immortalization of nasopharyngeal epithelial cells by telomerase. Int J Cancer 119: 1567-1576.