Epstein - Barr Virus Transforming Protein LMP-1 Alters B Cells Gene Expression by Promoting Accumulation of the Oncoprotein ΔNp73α

PLoS Pathogens

Volumn 9, Issue 3, 2013, Pages

  Accardi, Rosita ^a   Fathallah, Ikbal ^a   Gruffat, Henri ^b,c,d   Mariggiò, Giuseppe ^a   Le Calvez Kelm, Florence ^a   Voegele, Catherine ^a   Bartosch, Birke ^e   Hernandez Vargas, Hector ^a   McKay, James ^a   Sylla, Bakary S ^a   Manet, Evelyne ^b,c,d   Tommasino, Massimo ^a  

^a INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^b CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^c UNIVERSITÉ DE LYON   (France)

^d UNIVERSITÉ LYON 1   (France)

^e UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LATENT MEMBRANE PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; NOTCH RECEPTOR; ONCOPROTEIN; ONCOPROTEIN DELTA NP73 ALPHA; POLO LIKE KINASE 2; PROTEIN P2; PROTEIN P53; PROTEIN P73; RAS PROTEIN; STRESS ACTIVATED PROTEIN KINASE 1; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; EBV-ASSOCIATED MEMBRANE ANTIGEN, EPSTEIN-BARR VIRUS; MATRIX PROTEIN; MESSENGER RNA; NUCLEAR PROTEIN; TUMOR SUPPRESSOR PROTEIN; TUMOR SUPPRESSOR PROTEIN P73;

APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL SURVIVAL; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; EPIGENETICS; EPSTEIN BARR VIRUS; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LIVER CELL CARCINOMA; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION; UPREGULATION; ANTAGONISTS AND INHIBITORS; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY; PROMOTER REGION; SEQUENCE ANALYSIS; VIROLOGY; VIRUS CELL TRANSFORMATION;

HUMAN HERPESVIRUS 4;

APOPTOSIS; B-LYMPHOCYTES; CELL TRANSFORMATION, VIRAL; DNA-BINDING PROTEINS; DOWN-REGULATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 4, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION; VIRAL MATRIX PROTEINS;

EID: 84876011034     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003186     Document Type: Article

References (72)

1. Kieff E, Rickinson AB (2007) Epstein-Barr Virus and its replication. In: Fields BN, Knipe DM, Howley PM, editors. Fields Virology. Philadelphia: Lippincott-Williams & Wilkins Publishers. pp. 2603-2654.
2. Young LS, Rickinson AB, (2004) Epstein-Barr virus: 40 years on. Nat Rev Cancer 4: 757-768.
3. Babcock GJ, Decker LL, Volk M, Thorley-Lawson DA, (1998) EBV persistence in memory B cells in vivo. Immunity 9: 395-404.
4. Thorley-Lawson DA, (2001) Epstein-Barr virus: exploiting the immune system. Nat Rev Immunol 1: 75-82.
5. Hochberg D, Souza T, Catalina M, Sullivan JL, Luzuriaga K, et al. (2004) Acute infection with Epstein-Barr virus targets and overwhelms the peripheral memory B-cell compartment with resting, latently infected cells. J Virol 78: 5194-5204.
6. Hochberg D, Middeldorp JM, Catalina M, Sullivan JL, Luzuriaga K, et al. (2004) Demonstration of the Burkitt's lymphoma Epstein-Barr virus phenotype in dividing latently infected memory cells in vivo. Proc Natl Acad Sci USA 101: 239-244.
7. Dawson CW, Port RJ, Young LS, (2012) The role of the EBV-encoded latent membrane proteins LMP1 and LMP2 in the pathogenesis of nasopharyngeal carcinoma (NPC). Semin Cancer Biol 22: 144-153.
8. Graham JP, Arcipowski KM, Bishop GA, (2010) Differential B-lymphocyte regulation by CD40 and its viral mimic, latent membrane protein 1. Immunol Rev 237: 226-248.
9. Soni V, Cahir-McFarland E, Kieff E, (2007) LMP1 TRAFficking activates growth and survival pathways. Adv Exp Med Biol 597: 173-187.
10. Cai Q, Guo Y, Xiao B, Banerjee S, Saha A, et al. (2011) Epstein-Barr virus nuclear antigen 3C stabilizes Gemin3 to block p53-mediated apoptosis. PLoS Pathog 7: e1002418.
11. Knight JS, Sharma N, Robertson ES, (2005) Epstein-Barr virus latent antigen 3C can mediate the degradation of the retinoblastoma protein through an SCF cellular ubiquitin ligase. Proc Natl Acad Sci USA 102: 18562-18566.
12. Saha A, Murakami M, Kumar P, Bajaj B, Sims K, et al. (2009) Epstein-Barr virus nuclear antigen 3C augments Mdm2-mediated p53 ubiquitination and degradation by deubiquitinating Mdm2. J Virol 83: 4652-4669.
13. Saha A, Bamidele A, Murakami M, Robertson ES, (2011) EBNA3C attenuates the function of p53 through interaction with inhibitor of growth family proteins 4 and 5. J Virol 85: 2079-2088.
14. Yi F, Saha A, Murakami M, Kumar P, Knight JS, et al. (2009) Epstein-Barr virus nuclear antigen 3C targets p53 and modulates its transcriptional and apoptotic activities. Virology 388: 236-247.
15. Ghittoni R, Accardi R, Hasan U, Gheit T, Sylla B, et al. (2010) The biological properties of E6 and E7 oncoproteins from human papillomaviruses. Virus Genes 40: 1-13.
16. Courtois S, Caron de FC, Hainaut P, (2004) p53 protein variants: structural and functional similarities with p63 and p73 isoforms. Oncogene 23: 631-638.
17. Moll UM, Erster S, Zaika A, (2001) p53, p63 and p73-solos, alliances and feuds among family members. Biochim Biophys Acta 1552: 47-59.
18. Ushiku T, Chong JM, Uozaki H, Hino R, Chang MS, et al. (2007) p73 gene promoter methylation in Epstein-Barr virus-associated gastric carcinoma. Int J Cancer 120: 60-66.
19. Saha A, Lu J, Morizur L, Upadhyay SK, Aj MP, et al. (2012) E2F1 mediated apoptosis induced by the DNA damage response is blocked by EBV nuclear antigen 3C in lymphoblastoid cells. PLoS Pathog 8: e1002573.
20. Accardi R, Dong W, Smet A, Cui R, Hautefeuille A, et al. (2006) Skin human papillomavirus type 38 alters p53 functions by accumulation of deltaNp73. EMBO Rep 7: 334-340.
21. Accardi R, Scalise M, Gheit T, Hussain IS, Yue J, et al. (2011) I{kappa}B Kinase {beta} Promotes Cell Survival by Antagonizing p53 Functions through {Delta}Np73{alpha} Phosphorylation and Stabilization. Mol Cell Biol 31: 2210-2226.
22. Buhlmann S, Pützer BM, (2008) DNp73 a matter of cancer: mechanisms and clinical implications. Biochim Biophys Acta 1785: 207-216.
23. Casciano I, Banelli B, Croce M, Allemanni G, Ferrini S, et al. (2002) Role of methylation in the control of DeltaNp73 expression in neuroblastoma. Cell Death Differ 9: 343-345.
24. Stiewe T, Tuve S, Peter M, Tannapfel A, Elmaagacli AH, et al. (2004) Quantitative TP73 transcript analysis in hepatocellular carcinomas. Clin Cancer Res 10: 626-633.
25. Zaika AI, Slade N, Erster SH, Sansome C, Joseph TW, et al. (2002) DeltaNp73, a dominant-negative inhibitor of wild-type p53 and TAp73, is up-regulated in human tumors. J Exp Med 196: 765-780.
26. Levrero M, De Laurenzi V, Costanzo A, Gong J, Wang JY, et al. (2000) The p53/p63/p73 family of transcription factors: overlapping and distinct functions. J Cell Sci 113 (Pt 10):: 1661-1670.
27. Melino G, De Laurenzi V, Vousden KH, (2002) p73: Friend or foe in tumorigenesis. Nat Rev Cancer 2: 605-615.
28. Brigati C, Banelli B, Casciano I, Di VA, Matis S, et al. (2011) Epigenetic mechanisms regulate DeltaNP73 promoter function in human tonsil B cells. Mol Immunol 48: 408-414.
29. Ueda Y, Hijikata M, Takagi S, Chiba T, Shimotohno K, (1999) New p73 variants with altered C-terminal structures have varied transcriptional activities. Oncogene 18: 4993-4998.
30. Schulz TF, (2009) Cancer and viral infections in immunocompromised individuals. Int J Cancer 125: 1755-1763.
31. Belloni L, Moretti F, Merlo P, Damalas A, Costanzo A, et al. (2006) DNp73alpha protects myogenic cells from apoptosis. Oncogene 25: 3606-3612.
32. Kartasheva NN, Contente A, Lenz-Stoppler C, Roth J, Dobbelstein M, (2002) p53 induces the expression of its antagonist p73 Delta N, establishing an autoregulatory feedback loop. Oncogene 21: 4715-4727.
33. Vossio S, Palescandolo E, Pediconi N, Moretti F, Balsano C, et al. (2002) DN-p73 is activated after DNA damage in a p53-dependent manner to regulate p53-induced cell cycle arrest. Oncogene 21: 3796-3803.
34. Eliopoulos AG, Blake SM, Floettmann JE, Rowe M, Young LS, (1999) Epstein-Barr virus-encoded latent membrane protein 1 activates the JNK pathway through its extreme C terminus via a mechanism involving TRADD and TRAF2. J Virol 73: 1023-1035.
35. Jones EV, Dickman MJ, Whitmarsh AJ, (2007) Regulation of p73-mediated apoptosis by c-Jun N-terminal kinase. Biochem J 405: 617-623.
36. Kieser A, Kilger E, Gires O, Ueffing M, Kolch W, et al. (1997) Epstein-Barr virus latent membrane protein-1 triggers AP-1 activity via the c-Jun N-terminal kinase cascade. EMBO J 16: 6478-6485.
37. Eliopoulos AG, Young LS, (1998) Activation of the cJun N-terminal kinase (JNK) pathway by the Epstein-Barr virus-encoded latent membrane protein 1 (LMP1). Oncogene 16: 1731-1742.
38. Sanchez-Prieto R, Sanchez-Arevalo VJ, Servitja JM, Gutkind JS, (2002) Regulation of p73 by c-Abl through the p38 MAP kinase pathway. Oncogene 21: 974-979.
39. Eliopoulos AG, Gallagher NJ, Blake SM, Dawson CW, Young LS, (1999) Activation of the p38 mitogen-activated protein kinase pathway by Epstein-Barr virus-encoded latent membrane protein 1 coregulates interleukin-6 and interleukin-8 production. J Biol Chem 274: 16085-16096.
40. Schultheiss U, Puschner S, Kremmer E, Mak TW, Engelmann H, Hammerschmidt W, Kieser A, (2001) TRAF6 is a critical mediator of signal transduction by the viral oncogene latent membrane protein 1. EMBO J 20: 5678-5691.
41. Sharma S, Kelly TK, Jones PA, (2010) Epigenetics in cancer. Carcinogenesis 31: 27-36.
42. Paschos K, Allday MJ, (2010) Epigenetic reprogramming of host genes in viral and microbial pathogenesis. Trends Microbiol 18: 439-447.
43. Viré E, Brenner C, Deplus R, Blanchon L, Fraga M, et al. (2006) The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439: 871-874.
44. Testoni B, Schinzari V, Guerrieri F, Gerbal-Chaloin S, Blandino G, et al. (2011) p53-paralog DNp73 oncogene is repressed by IFNalpha/STAT2 through the recruitment of the Ezh2 polycomb group transcriptional repressor. Oncogene 30: 2670-2678.
45. Alberts AS, Geneste O, Treisman R, (1998) Activation of SRF-regulated chromosomal templates by Rho-family GTPases requires a signal that also induces H4 hyperacetylation. Cell 92: 475-487.
46. Tissir F, Ravni A, Achouri Y, Riethmacher D, Meyer G, et al. (2009) DeltaNp73 regulates neuronal survival in vivo. Proc Natl Acad Sci USA 106: 16871-16876.
47. Syed N, Smith P, Sullivan A, Spender LC, Dyer M, et al. (2006) Transcriptional silencing of Polo-like kinase 2 (SNK/PLK2) is a frequent event in B-cell malignancies. Blood 107: 250-256.
48. Salipante SJ, Mealiffe ME, Wechsler J, Krem MM, Liu Y, et al. (2009) Mutations in a gene encoding a midbody kelch protein in familial and sporadic classical Hodgkin lymphoma lead to binucleated cells. Proc Natl Acad Sci USA 106: 14920-14925.
49. Vousden KH, Lane DP, (2007) p53 in health and disease. Nat Rev Mol Cell Biol 8: 275-283.
50. Pise-Masison CA, Brady JN, (2005) Setting the stage for transformation: HTLV-1 Tax inhibition of p53 function. Front BIosci 10: 919-930.
51. Wurm T, Wright DG, Polakowski N, Mesnard JM, Lemasson I, (2012) The HTLV-1-encoded protein HBZ directly inhibits the acetyl transferase activity of p300/CBP. Nucleic Acids Res 40 (13):: 5910-25.
52. Cai Q, Xiao B, Si H, Cervini A, Gao J, et al. (2012) Kaposi's sarcoma herpesvirus upregulates Aurora A expression to promote p53 phosphorylation and ubiquitylation. PLoS Pathog 8: e1002566.
53. Cai QL, Knight JS, Verma SC, Zald P, Robertson ES, (2006) EC5S ubiquitin complex is recruited by KSHV latent antigen LANA for degradation of the VHL and p53 tumor suppressors. PLoS Pathog 2: e116.
54. Friborg J Jr, Kong W, Hottiger MO, Nabel GJ, (1999) p53 inhibition by the LANA protein of KSHV protects against cell death. Nature 402: 889-894.
55. Kutz H, Reisbach G, Schultheiss U, Kieser A, (2008) The c-Jun N-terminal kinase pathway is critical for cell transformation by the latent membrane protein 1 of Epstein-Barr virus. Virology 371: 246-256.
56. Vikhanskaya F, Toh WH, Dulloo I, Wu Q, Boominathan L, et al. (2007) p73 supports cellular growth through c-Jun-dependent AP-1 transactivation. Nat Cell Biol 9: 698-705.
57. Koeppel M, van Heeringen SJ, Kramer D, Smeenk L, Janssen-Megens E, et al. (2011) Crosstalk between c-Jun and TAp73alpha/beta contributes to the apoptosis-survival balance. Nucleic Acids Res 39: 6069-6085.
58. Hyland PL, McDade SS, McCloskey R, Dickson GJ, Arthur K, et al. (2011) Evidence for alteration of EZH2, BMI1, and KDM6A and epigenetic reprogramming in human papillomavirus type 16 E6/E7-expressing keratinocytes. J Virol 85: 10999-11006.
59. Anderton JA, Bose S, Vockerodt M, Vrzalikova K, Wei W, et al. (2011) The H3K27me3 demethylase, KDM6B, is induced by Epstein-Barr virus and over-expressed in Hodgkin's Lymphoma. Oncogene 30: 2037-2043.
60. Cha TL, Zhou BP, Xia W, Wu Y, Yang CC, et al. (2005) Akt-mediated phosphorylation of EZH2 suppresses methylation of lysine 27 in histone H3. Science 310: 306-310.
61. Shair KH, Bendt KM, Edwards RH, Bedford EC, Nielsen JN, et al. (2007) EBV latent membrane protein 1 activates Akt, NFkappaB, and Stat3 in B cell lymphomas. PLoS Pathog 3: e166.
62. Dutton A, Reynolds GM, Dawson CW, Young LS, Murray PG, (2005) Constitutive activation of phosphatidyl-inositide 3 kinase contributes to the survival of Hodgkin's lymphoma cells through a mechanism involving Akt kinase and mTOR. J Pathol 205: 498-506.
63. Morrison JA, Gulley ML, Pathmanathan R, Raab-Traub N, (2004) Differential signaling pathways are activated in the Epstein-Barr virus-associated malignancies nasopharyngeal carcinoma and Hodgkin lymphoma. Cancer Res 64: 5251-5260.
64. Leupin N, Luthi A, Novak U, Grob TJ, Hugli B, et al. (2004) P73 status in B-cell chronic lymphocytic leukaemia. Leuk Lymphoma 45: 1205-1207.
65. Shah N, Sukumar S, (2010) The Hox genes and their roles in oncogenesis. Nat Rev Cancer 10: 361-371.
66. Timms AE, Horwitz MS, (2010) KLHDC8B in Hodgkin lymphoma and possibly twinning. Commun Integr Biol 3: 154-158.
67. Fathallah I, Parroche P, Gruffat H, Zannetti C, Johansson H, et al. (2010) EBV latent membrane protein 1 is a negative regulator of TLR9. J Immunol 185: 6439-6447.
68. Delecluse HJ, Pich D, Hilsendegen T, Baum C, Hammerschmidt W, (1999) A first-generation packaging cell line for Epstein-Barr virus-derived vectors. Proc Natl Acad Sci USA 96: 5188-5193.
69. Lee S, Andrieu C, Saltel F, Destaing O, Auclair J, et al. (2004) IkappaB kinase beta phosphorylates Dok1 serines in response to TNF, IL-1, or gamma radiation. Proc Natl Acad Sci USA 101: 17416-17421.
70. Bartosch B, Cosset FL, (2004) Strategies for retargeted gene delivery using vectors derived from lentiviruses. Curr Gene Ther 4: 427-443.
71. Gong Y, Yue J, Wu X, Wang X, Wen J, et al. (2006) NSPc1 is a cell growth regulator that acts as a transcriptional repressor of p21Waf1/Cip1 via the RARE element. Nucleic Acids Res 34: 6158-6169.
72. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.