Viral oncoprotein LMP1 disrupts p53-induced cell cycle arrest and apoptosis through modulating K63-linked ubiquitination of p53

Cell Cycle

Volumn 11, Issue 12, 2012, Pages 2327-2336

  Li, Lili ^a,b,c   Li, Wei ^a,b   Xiao, Lanbo ^a,b   Xu, Juan ^a,b   Chen, Xue ^a,b   Tang, Min ^a,b   Dong, Zigang ^d   Tao, Qian ^c   Cao, Ya ^a,b  

^a Central South University   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Epstein Barr virus; K63; LMP1; p53; Ubiquitination

Indexed keywords

LATENT MEMBRANE PROTEIN 1; PROTEIN MDM2; PROTEIN P53; SERINE; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2;

APOPTOSIS; ARTICLE; BIOLOGICAL FUNCTIONS; BREAST ADENOCARCINOMA; CELL CYCLE ARREST; CONTROLLED STUDY; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; NASOPHARYNX CARCINOMA; NONHUMAN; OSTEOSARCOMA; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TUMOR CELL; UBIQUITINATION;

HUMAN HERPESVIRUS 4; PYRONIA TITHONUS;

EID: 84862891080     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.20771     Document Type: Article

References (58)

1. Moody CA, Laimins LA. Human papillomavirus oncoproteins: pathways to transformation. Nat Rev Cancer 2010; 10:550-60; PMID:20592731; http://dx.doi.org/10.1038/nrc2886.
2. Pipas JM, Levine AJ. Role of T antigen interactions with p53 in tumorigenesis. Semin Cancer Biol 2001; 11:23-30; PMID:11243896; http://dx.doi.org/10.1006/scbi.2000.0343.
3. Thomas M, Pim D, Banks L. The role of the E6-p53 interaction in the molecular pathogenesis of HPV. Oncogene 1999; 18:7690-700; PMID:10618709; http://dx.doi.org/10.1038/sj.onc.1202953.
4. O'Neill FJ, Hu Y, Chen T, Carney H. Identification of p53 unbound to T-antigen in human cells transformed by simian virus 40 T-antigen. Oncogene 1997; 14:955- 65; PMID:9050995; http://dx.doi.org/10.1038/sj.onc.1200913.
5. Kohli M, Jorgensen TJ. Lack of dependence on p53 for DNA double strand break repair of episomal vectors in human lymphoblasts. Biochem Biophys Res Commun 1999; 264:702-8; PMID:10543995; http://dx.doi.org/10.1006/bbrc.1999.1575.
6. Deppert W, Haug M. Evidence for free and metabolically stable p53 protein in nuclear subfractions of simian virus 40-transformed cells. Mol Cell Biol 1986; 6:2233-40; PMID:3023923.
7. Hermannstädter A, Ziegler C, Kühl M, Deppert W, Tolstonog GV. Wild-type p53 enhances efficiency of simian virus 40 large-T-antigen-induced cellular transformation. J Virol 2009; 83:10106- 18; PMID:19625393; http://dx.doi.org/10.1128/JVI.00174-09.
8. Bieging KT, Swanson-Mungerson M, Amick AC, Longnecker R. Epstein-Barr virus in Burkitt's lymphoma: a role for latent membrane protein 2A. Cell Cycle 2010; 9:901-8; PMID:20160479; http://dx.doi.org/10.4161/cc.9.5.10840.
9. Löber C, Lenz-Stöppler C, Dobbelstein M. Adenovirus E1-transformed cells grow despite the continuous presence of transcriptionally active p53. J Gen Virol 2002; 83:2047-57; PMID:12124469.
10. Koch P, Gatfield J, Löber C, Hobom U, Lenz-Stöppler C, Roth J, et al. Efficient replication of adenovirus despite the overexpression of active and nondegradable p53. Cancer Res 2001; 61:5941-7; PMID:11479237.
11. Hess RD, Brandner G. DNA damage-inducible p53 activity in SV40-transformed cells. Oncogene 1997; 15:2501-4; PMID:9395246; http://dx.doi.org/10.1038/sj.onc.1201404.
12. Li L, Zhou S, Chen X, Guo L, Li Z, Hu D, et al. The activation of p53 mediated by Epstein-Barr virus latent membrane protein 1 in SV40 large T-antigen transformed cells. FEBS Lett 2008; 582:755-62; PMID:18242176; http://dx.doi.org/10.1016/j.febslet.2008.01.031.
13. Scheffner M, Huibregtse JM, Vierstra RD, Howley PM. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 1993; 75:495-505; PMID:8221889; http:// dx.doi.org/10.1016/0092- 8674(93)90384-3.
14. Querido E, Blanchette P, Yan Q, Kamura T, Morrison M, Boivin D, et al. Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev 2001; 15:3104-17; PMID:11731475; http://dx.doi.org/10.1101/gad.926401.
15. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 1990; 63:1129-36; PMID:2175676; http://dx.doi.org/10. 1016/0092-8674(90)90409-8.
16. Mukhopadhyay D, Riezman H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 2007; 315:201-5; PMID:17218518; http://dx.doi.org/10.1126/science.1127085.
17. Haglund K, Dikic I. Ubiquitylation and cell signaling. EMBO J 2005; 24:3353-9; PMID:16148945; http:// dx.doi.org/10.1038/sj.emboj.7600808.
18. Fuchs SY, Adler V, Buschmann T, Wu X, Ronai Z. Mdm2 association with p53 targets its ubiquitination. Oncogene 1998; 17:2543-7; PMID:9824166; http://dx.doi.org/10.1038/sj.onc.1202200.
19. Fang S, Jensen JP, Ludwig RL, Vousden KH, Weissman AM. Mdm2 is a RING finger-dependent ubiquitin protein ligase for itself and p53. J Biol Chem 2000; 275:8945-51; PMID:10722742; http://dx.doi.org/10.1074/jbc.275.12.8945.
20. Lee JT, Gu W. The multiple levels of regulation by p53 ubiquitination. Cell Death Differ 2010; 17:86- 92; PMID:19543236; http://dx.doi.org/10.1038/cdd. 2009.77.
21. Tao Q, Young LS, Woodman CB, Murray PG. Epstein-Barr virus (EBV) and its associated human cancers - genetics, epigenetics, pathobiology and novel therapeutics. Front Biosci 2006; 11:2672-713; PMID:16720343; http://dx.doi.org/10.2741/2000.
22. Young LS, Rickinson AB. Epstein-Barr virus: 40 years on. Nat Rev Cancer 2004; 4:757-68; PMID:15510157; http://dx.doi.org/10.1038/nrc1452.
23. Mauser A, Saito S, Appella E, Anderson CW, Seaman WT, Kenney S. The Epstein-Barr virus immediateearly protein BZLF1 regulates p53 function through multiple mechanisms. J Virol 2002; 76:12503-12; PMID:12438576; http://dx.doi.org/10.1128/ JVI.76.24.12503-12.2002.
24. Sato Y, Tsurumi T. Noise cancellation: viral fine tuning of the cellular environment for its own genome replication. PLoS Pathog 2010; 6:1001158; PMID:21187893; http://dx.doi.org/10.1371/journal.ppat.1001158.
25. Sato Y, Shirata N, Murata T, Nakasu S, Kudoh A, Iwahori S, et al. Transient increases in p53-responsible gene expression at early stages of Epstein-Barr virus productive replication. Cell Cycle 2010; 9:807- 14; PMID:20139729; http://dx.doi.org/10.4161/cc.9.4.10675.
26. Sato Y, Kamura T, Shirata N, Murata T, Kudoh A, Iwahori S, et al. Degradation of phosphorylated p53 by viral protein-ECS E3 ligase complex. PLoS Pathog 2009; 5:1000530; PMID:19649319; http://dx.doi. org/10.1371/journal.ppat. 1000530.
27. Morris MA, Dawson CW, Young LS. Role of the Epstein-Barr virus-encoded latent membrane protein-1, LMP1, in the pathogenesis of nasopharyngeal carcinoma. Future Oncol 2009; 5:811-25; PMID:19663731; http://dx.doi.org/10. 2217/fon.09.53.
28. Hu D, Zheng H, Liu H, Li M, Ren W, Liao W, et al. Immunoglobulin expression and its biological significance in cancer cells. Cell Mol Immunol 2008; 5:319- 24; PMID:18954554; http://dx.doi.org/10.1038/cmi.2008.39.
29. Sun Y, Dong Z, Nakamura K, Colburn NH. Dosage-dependent dominance over wild-type p53 of a mutant p53 isolated from nasopharyngeal carcinoma. FASEB J 1993; 7:944-50; PMID:8344492.
30. Spruck CH, 3rd, Tsai YC, Huang DP, Yang AS, Rideout WM, 3rd, Gonzalez-Zulueta M, et al. Absence of p53 gene mutations in primary nasopharyngeal carcinomas. Cancer Res 1992; 52:4787-90; PMID:1511442.
31. Sun Y, Hegamyer G, Cheng YJ, Hildesheim A, Chen JY, Chen IH, et al. An infrequent point mutation of the p53 gene in human nasopharyngeal carcinoma. Proc Natl Acad Sci USA 1992; 89:6516- 20; PMID:1631151; http://dx.doi.org/10. 1073/ pnas.89.14.6516.
32. Shao JY, Ernberg I, Biberfeld P, Heiden T, Zeng YX, Hu LF. Epstein-Barr virus LMP1 status in relation to apoptosis, p53 expression and leucocyte infiltration in nasopharyngeal carcinoma. Anticancer Res 2004; 24:2309-18; PMID:15330177.
33. Cheung FM, Pang SW, Yau TK, Chow SK, Lo KW. Nasopharyngeal intraepithelial lesion: latent Epstein-Barr virus infection with malignant potential. Histopathology 2004; 45:171-9; PMID:15279636; http://dx.doi.org/10. 1111/j.1365-2559.2004.01935.x.
34. Murono S, Yoshizaki T, Park CS, Furukawa M. Association of Epstein-Barr virus infection with p53 protein accumulation but not bcl-2 protein in nasopharyngeal carcinoma. Histopathology 1999; 34:432-8; PMID:10231418; http://dx.doi.org/10.1046/j.1365- 2559.1999.00625.x.
35. Li L, Guo L, Tao Y, Zhou S, Wang Z, Luo W, et al. Latent membrane protein 1 of Epstein-Barr virus regulates p53 phosphorylation through MAP kinases. Cancer Lett 2007; 255:219-31; PMID:17582679; http://dx.doi.org/10.1016/j.canlet. 2007.04.014.
36. Liao W, Tang M, Yin L. EBV latent membrane protein 1 induces p53 expression via NFkappaB in nasopharyngeal carcinoma. Zhonghua Zhong Liu Za Zhi 2001; 23:199-201; PMID:11783085.
37. Nigro JM, Baker SJ, Preisinger AC, Jessup JM, Hostetter R, Cleary K, et al. Mutations in the p53 gene occur in diverse human tumour types. Nature 1989; 342:705-8; PMID:2531845; http://dx.doi. org/10.1038/342705a0.
38. Hollstein M, Sidransky D, Vogelstein B, Harris CC. p53 mutations in human cancers. Science 1991; 253:49-53; PMID:1905840; http://dx.doi.org/10.1126/ science.1905840.
39. Deppert W, Steinmayer T, Richter W. Cooperation of SV40 large T antigen and the cellular protein p53 in maintenance of cell transformation. Oncogene 1989; 4:1103-10; PMID:2674854.
40. 1/S cell cycle progression in nasopharyngeal carcinoma. Int J Mol Med 2012; 29:574-80; PMID:22266808.
41. Saridakis V, Sheng Y, Sarkari F, Holowaty MN, Shire K, Nguyen T, et al. Structure of the p53 binding domain of HAUSP/USP7 bound to Epstein-Barr nuclear antigen 1 implications for EBV-mediated immortalization. Mol Cell 2005; 18:25-36; PMID:15808506; http://dx.doi.org/10.1016/j.molcel.2005.02.029.
42. Inuzuka H, Fukushima H, Shaik S, Wei W. Novel insights into the molecular mechanisms governing Mdm2 ubiquitination and destruction. Oncotarget 2010; 1:685-90; PMID:21317463.
43. Bosanac I, Wertz IE, Pan B, Yu C, Kusam S, Lam C, et al. Ubiquitin binding to A20 ZnF4 is required for modulation of NFκB signaling. Mol Cell 2010; 40:548-57; PMID:21095585; http://dx.doi.org/10.1016/j.molcel.2010.10.009.
44. Shembade N, Ma A, Harhaj EW. Inhibition of NFkappaB signaling by A20 through disruption of ubiquitin enzyme complexes. Science 2010; 327:1135- 9; PMID:20185725; http://dx.doi.org/10.1126/science. 1182364.
45. Tauriello DV, Haegebarth A, Kuper I, Edelmann MJ, Henraat M, Canninga-van Dijk MR, et al. Loss of the tumor suppressor CYLD enhances Wnt/beta-catenin signaling through K63-linked ubiquitination of Dvl. Mol Cell 2010; 37:607-19; PMID:20227366; http://dx.doi.org/10.1016/j.molcel.2010.01.035.
46. Fukuyo Y, Kitamura T, Inoue M, Horikoshi NT, Higashikubo R, Hunt CR, et al. Phosphorylation-dependent Lys63-linked polyubiquitination of Daxx is essential for sustained TNFalpha-induced ASK1 activation. Cancer Res 2009; 69:7512-7; PMID:19789334; http://dx.doi.org/10.1158/0008-5472.CAN-09-2148.
47. Kayagaki N, Phung Q, Chan S, Chaudhari R, Quan C, O'Rourke KM, et al. DUBA: a deubiquitinase that regulates type I interferon production. Science 2007; 318:1628-32; PMID:17991829; http://dx.doi.org/10.1126/science.1145918.
48. Bouwmeester T, Bauch A, Ruffner H, Angrand PO, Bergamini G, Croughton K, et al. A physical and functional map of the human TNFalpha/NFkappaB signal transduction pathway. Nat Cell Biol 2004; 6:97- 105; PMID:14743216; http://dx.doi.org/10.1038/ncb1086.
49. Deng L, Wang C, Spencer E, Yang L, Braun A, You J, et al. Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 2000; 103:351-61; PMID:11057907; http://dx.doi.org/10.1016/S0092-8674(00)00126-4.
50. Huye LE, Ning S, Kelliher M, Pagano JS. Interferon regulatory factor 7 is activated by a viral oncoprotein through RIP-dependent ubiquitination. Mol Cell Biol 2007; 27:2910-8; PMID:17296724; http://dx.doi.org/10.1128/MCB.02256-06.
51. Ning S, Campos AD, Darnay BG, Bentz GL, Pagano JS. TRAF6 and the three C-terminal lysine sites on IRF7 are required for its ubiquitination-mediated activation by the tumor necrosis factor receptor family member latent membrane protein 1. Mol Cell Biol 2008; 28:6536-46; PMID:18710948; http://dx.doi.org/10. 1128/MCB.00785-08.
52. Neznanov N, Komarov AP, Neznanova L, Stanhope- Baker P, Gudkov AV. Proteotoxic stress targeted therapy (PSTT): induction of protein misfolding enhances the antitumor effect of the proteasome inhibitor bortezomib. Oncotarget 2011; 2:209-21; PMID:21444945.
53. Zhang Q, Gutsch D, Kenney S. Functional and physical interaction between p53 and BZLF1: implications for Epstein-Barr virus latency. Mol Cell Biol 1994; 14:1929-38; PMID:8114724.
54. Rodriguez A, Armstrong M, Dwyer D, Flemington E. Genetic dissection of cell growth arrest functions mediated by the Epstein-Barr virus lytic gene product, Zta. J Virol 1999; 73:9029-38; PMID:10516009.
55. Sinclair A, Yarranton S, Schelcher C. DNA damage response pathways triggered by viral replication. Expert Rev Mol Med 2006; 8:1-11; PMID:16515730; http://dx.doi.org/10.1017/S1462399406010544.
56. Tsao SW, Wang X, Liu Y, Cheung YC, Feng H, Zheng Z, et al. Establishment of two immortalized nasopharyngeal epithelial cell lines using SV40 large T and HPV16E6/E7 viral oncogenes. Biochim Biophys Acta 2002; 1590:150-8; PMID:12063178; http://dx.doi.org/10.1016/S0167-4889(02)00208-2.
57. Lo AK, Liu Y, Wang XH, Huang DP, Yuen PW, Wong YC, et al. Alterations of biologic properties and gene expression in nasopharyngeal epithelial cells by the Epstein-Barr virus-encoded latent membrane protein 1. Lab Invest 2003; 83:697-709; PMID:12746479.
58. Zhao BX, Chen HZ, Lei NZ, Li GD, Zhao WX, Zhan YY, et al. p53 mediates the negative regulation of MDM2 by orphan receptor TR3. EMBO J 2006; 25:5703-15; PMID:17139261; http://dx.doi.org/10.1038/sj.emboj.7601435.