Inhibition of germinal centre apoptotic programmes by Epstein-Barr virus

Advances in Hematology

Volumn 2011, Issue , 2011, Pages

  Spender, Lindsay C ^a   Inman, Gareth J ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; BCL2 RELATED PROTEIN A1; BH3 PROTEIN; BIM PROTEIN; BREAKPOINT CLUSTER REGION PROTEIN; CASPASE 3; CASPASE 9; CD4 ANTIGEN; DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEIN; FAS ANTIGEN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; FLICE INHIBITORY PROTEIN; INTERLEUKIN 4; MICRORNA; PROTEIN; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN BIK; PROTEIN P53; PUMA PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANTIBODY RESPONSE; APOPTOSIS; B LYMPHOCYTE; CELL SURVIVAL; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; GERMINAL CENTER; HUMAN; LATENT VIRUS INFECTION; LYMPHOCYTE DIFFERENTIATION; MEMORY CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; VIRUS CELL INTERACTION; VIRUS GENE;

EID: 84855278480     PISSN: 16879104     EISSN: 16879112     Source Type: Journal    
DOI: 10.1155/2011/829525     Document Type: Review

References (90)

1. Miyashita E. M., Yang B., Babcock G. J., Thorley-Lawson D. A., Identification of the site of Epstein-Barr virus persistence in vivo as a resting B cell Journal of Virology 1997 71 7 4882 4891 (Pubitemid 27258155)
2. Joseph A. M., Babcock G. J., Thorley-Lawson D. A., Cells expressing the Epstein-Barr virus growth program are present in and restricted to the naive B-cell subset of healthy tonsils Journal of Virology 2000 74 21 9964 9971
3. Kalla M., Hammerschmidt W., Human B cells on their route to latent infectionearly but transient expression of lytic genes of Epstein-Barr virus. European Journal of Cell Biology. In press
4. Sinclair A. J., Palmero I., Peters G., Farrell P. J., EBNA-2 and EBNA-LP cooperate to cause G0 to G1 transition during immortalization of resting human B lymphocytes by Epstein-Barr virus The EMBO Journal 1994 13 14 3321 3328 (Pubitemid 24226947)
5. Kaiser C., Laux G., Eick D., Jochner N., Bornkamm G. W., Kempkes B., The proto-oncogene c-myc is a direct target gene of Epstein-Barr virus nuclear antigen 2 Journal of Virology 1999 73 5 4481 4484 (Pubitemid 29189900)
6. Spender L. C., Cornish G. H., Rowland B., Kempkes B., Farrell P. J., Direct and indirect regulation of cytokine and cell cycle proteins by EBNA-2 during Epstein-Barr virus infection Journal of Virology 2001 75 8 3537 3546 (Pubitemid 32246363)
7. Kurth J., Spieker T., Wustrow J., Strickler J. G., Hansmann M. L., Rajewsky K., Kppers R., EBV-infected B cells in infectious mononucleosis: viral strategies for spreading in the B cell compartment and establishing latency Immunity 2000 13 4 485 495
8. Pope J. H., Scott W., Moss D. J., Human lymphoid cell transformation by Epstein Barr virus Nature New Biology 1973 246 153 140 141
9. Siemer D., Kurth J., Lang S., Lehnerdt G., Stanelle J., Kppers R., EBV transformation overrides gene expression patterns of B cell differentiation stages Molecular Immunology 2008 45 11 3133 3141
10. Thorley-Lawson D. A., Epstein-Barr virus: exploiting the immune system Nature Reviews Immunology 2001 1 1 75 82 (Pubitemid 33741978)
11. Roughan J. E., Thorley-Lawson D. A., The intersection of Epstein-Barr virus with the germinal center Journal of Virology 2009 83 8 3968 3976
12. Roughan J. E., Torgbor C., Thorley-Lawson D. A., Germinal center B cells latently infected with Epstein-Barr virus proliferate extensively but do not increase in number Journal of Virology 2010 84 2 1158 1168
13. Souza T. A., Stollar B. D., Sullivan J. L., Luzuriaga K., Thorley-Lawson D. A., Influence of EBV on the peripheral blood memory B cell compartment Journal of Immunology 2007 179 5 3153 3160
14. Souza T. A., Stollar B. D., Sullivan J. L., Luzuriaga K., Thorley-Lawson D. A., Peripheral B cells latently infected with Epstein-Barr virus display molecular hallmarks of classical antigen-selected memory B cells Proceedings of the National Academy of Sciences of the United States of America 2005 102 50 18093 18098 (Pubitemid 41798507)
15. MacLennan I. C. M., Germinal centers Annual Review of Immunology 1994 12 117 139 (Pubitemid 24140411)
16. Allen C. D. C., Okada T., Tang H. L., Cyster J. G., Imaging of germinal center selection events during affinity maturation Science 2007 315 5811 528 531 (Pubitemid 46175759)
17. Allen C. D. C., Okada T., Cyster J. G., Germinal-center organization and cellular dynamics Immunity 2007 27 2 190 202 (Pubitemid 47284923)
18. Spender L. C., O'Brien D. I., Simpson D., Dutt D., Gregory C. D., Allday M. J., Clark L. J., Inman G. J., TGF- induces apoptosis in human B cells by transcriptional regulation of BIK and BCL-XL Cell Death and Differentiation 2009 16 4 593 602
19. Inman G. J., Allday M. J., Apoptosis induced by TGF- 1 in Burkitt's lymphoma cells is caspase 8 dependent but is death receptor independent Journal of Immunology 2000 165 5 2500 2510 (Pubitemid 30660695)
20. Briere F., Defrance T., Vanbervliet B., Bridon J. M., Durand I., Rousset F., Banchereau J., Transforming growth factor beta (TGF ) directs IgA1 and IgA2 switching in human naive B cells Advances in Experimental Medicine and Biology 1995 371 21 26
21. Cazac B. B., Roes J., TGF- receptor controls B cell responsiveness and induction of IgA in vivo Immunity 2000 13 4 443 451
22. Borsutzky S., Cazac B. B., Roes J., Guzmn C. A., TGF- receptor signaling is critical for mucosal IgA responses Journal of Immunology 2004 173 5 3305 3309 (Pubitemid 39142039)
23. Fahmi H., Cochet C., Hmama Z., Opolon P., Joab I., 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 Journal of Virology 2000 74 13 5810 5818 (Pubitemid 30412948)
24. Liang C. L., Chen J. L., Hsu Y. P. P., Ou J. T., Chang Y. S., Epstein-Barr virus BZLF1 gene is activated by transforming growth factor- through cooperativity of smads and c-Jun/c-Fos proteins The Journal of Biological Chemistry 2002 277 26 23345 23357 (Pubitemid 34952165)
25. Iempridee T., Transforming growth factor-{beta}-induced reactivation of epstein-barr virus involves multiple smad-binding elements cooperatively activating expression of the latent-lytic switch BZLF1 gene The Journal of Virology 2011 85 15 7836 7848
26. Inman G. J., Binnié U. K., Parker G. A., Farrell P. J., Allday M. J., Activators of the Epstein-Barr virus lytic program concomitantly induce apoptosis, but lytic gene expression protects from cell death Journal of Virology 2001 75 5 2400 2410 (Pubitemid 32147578)
27. Kalla M., Schmeinck A., Bergbauer M., Pich D., Hammerschmidt W., AP-1 homolog BZLF1 of Epstein-Barr virus has two essential functions dependent on the epigenetic state of the viral genome Proceedings of the National Academy of Sciences of the United States of America 2010 107 2 850 855
28. Shi Y., Massagué J., Mechanisms of TGF- signaling from cell membrane to the nucleus Cell 2003 113 6 685 700 (Pubitemid 36724933)
29. Derynck R., Zhang Y. E., Smad-dependent and Smad-independent pathways in TGF- family signalling Nature 2003 425 6958 577 584 (Pubitemid 37280136)
30. Massagué J., Seoane J., Wotton D., Smad transcription factors Genes and Development 2005 19 23 2783 2810 (Pubitemid 41739965)
31. Letai A., Bassik M. C., Walensky L. D., Sorcinelli M. D., Weiler S., Korsmeyer S. J., Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics Cancer Cell 2002 2 3 183 192 (Pubitemid 41043974)
32. Kim H., Rafiuddin-Shah M., Tu H. C., Jeffers J. R., Zambetti G. P., Hsieh J. J. D., Cheng E. H. Y., Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies Nature Cell Biology 2006 8 12 1348 1358 (Pubitemid 44835109)
33. Gallenne T., Gautier F., Oliver L., Hervouet E., Nol B., Hickman J. A., Geneste O., Cartron P. F., Vallette F. M., Manon S., Juin P., Bax activation by the BH3-only protein Puma promotes cell dependence on antiapoptotic Bcl-2 family members Journal of Cell Biology 2009 185 2 279 290
34. Chen L., Willis S. N., Wei A., Smith B. J., Fletcher J. I., Hinds M. G., Colman P. M., Day C. L., Adams J. M., Huang D. C. S., Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function Molecular Cell 2005 17 3 393 403 (Pubitemid 40193310)
35. Certo M., Moore V. D. G., Nishino M., Wei G., Korsmeyer S., Armstrong S. A., Letai A., Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members Cancer Cell 2006 9 5 351 365 (Pubitemid 43668734)
36. Willis S. N., Fletcher J. I., Kaufmann T., Van Delft M. F., Chen L., Czabotar P. E., Ierino H., Lee E. F., Fairlie W. D., Bouillet P., Strasser A., Kluck R. M., Adams J. M., Huang D. C. S., Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak Science 2007 315 5813 856 859
37. Spender L. C., Inman G. J., Targeting the BCL-2 family in malignancies of germinal centre origin Expert opinion on therapeutic targets 2009 13 12 1459 1472
38. Hennino A., Bérard M., Krammer P. H., Defrance T., FLICE-inhibitory protein is a key regulator of germinal center B cell apoptosis Journal of Experimental Medicine 2001 193 4 447 458 (Pubitemid 32524476)
39. van Eijk M., Medema J. P., de Groot C., Cutting edge: cellular Fas-associated death domain-like IL-1-converting enzyme-inhibitory protein protects germinal center B cells from apoptosis during germinal center reactions Journal of Immunology 2001 166 11 6473 6476 (Pubitemid 32467183)
40. van Eijk M., Defrance T., Hennino A., de Groot C., Death-receptor contribution to the germinal-center reaction Trends in Immunology 2001 22 12 677 682 (Pubitemid 34008604)
41. Miller C. L., Burkhardt A. L., Lee J. H., Stealey B., Longnecker R., Bolen J. B., Kieff E., Integral membrane protein 2 of Epstein-Barr virus regulates reactivation from latency through dominant negative effects on protein-tyrosine kinases Immunity 1995 2 2 155 166
42. Caldwell R. G., Wilson J. B., Anderson S. J., Longnecker R., Epstein-Barr virus LMP2A drives B cell development and survival in the absence of normal B cell receptor signals Immunity 1998 9 3 405 411 (Pubitemid 28462761)
43. Mancao C., Altmann M., Jungnickel B., Hammerschmidt W., Rescue of crippled germinal center B cells from apoptosis by Epstein-Barr virus Blood 2005 106 13 4339 4344 (Pubitemid 41775945)
44. Bechtel D., Kurth J., Unkel C., Kppers R., Transformation of BCR-deficient germinal-center B cells by EBV supports a major role of the virus in the pathogenesis of Hodgkin and posttransplantation lymphomas Blood 2005 106 13 4345 4350 (Pubitemid 41775946)
45. Casola S., Otipoby K. L., Alimzhanov M., Humme S., Uyttersprot N., Kutok J. L., Carroll M. C., Rajewsky K., B cell receptor signal strength determines B cell fate Nature Immunology 2004 5 3 317 327 (Pubitemid 38332129)
46. Swanson-Mungerson M. A., Caldwell R. G., Bultema R., Longnecker R., Epstein-Barr virus LMP2A alters in vivo and in vitro models of B-cell anergy, but not deletion, in response to autoantigen Journal of Virology 2005 79 12 7355 7362 (Pubitemid 40756771)
47. Miller C. L., Lee J. H., Kieff E., Burkhardt A. L., Bolen J. B., Longnecker R., Epstein-Barr virus protein LMP2A regulates reactivation from latency by negatively regulating tyrosine kinases involved in sIg-mediated signal transduction Infectious Agents and Disease 1994 3 2-3 128 136 (Pubitemid 24280991)
48. Swanson-Mungerson M., Bultema R., Longnecker R., Epstein-Barr virus LMP2A imposes sensitivity to apoptosis Journal of General Virology 2010 91 9 2197 2202
49. Kenney J. L., Guinness M. E., Reiss M., Lacy J., Antisense to the Epstein-Barr virus (EBV)-encoded latent membrane protein 1 (LMP-1) sensitizes EBV-immortalized B cells to transforming growth factor-beta and chemotherapeutic agents International Journal of Cancer 2001 91 1 89 98
50. Inman G. J., Allday M. J., Resistance to TGF- 1 correlates with a reduction of TGF- type II receptor expression in Burkitt's lymphoma and Epstein-Barr virus-transformed B lymphoblastoid cell lines Journal of General Virology 2000 81, part 6 1567 1578 (Pubitemid 30342904)
51. Mori N., Morishita M., Tsukazaki T., Yamamoto N., Repression of SMAD-dependent transforming growth factor- signaling by Epstein-Barr virus latent membrane protein 1 through nuclear factor- B International Journal of Cancer 2003 105 5 661 668 (Pubitemid 36687734)
52. Flavell J. R., Baumforth K. R. N., Wood V. H. J., Davies G. L., Wei W., Reynolds G. M., Morgan S., Boyce A., Kelly G. L., Young L. S., Murray P. G., Down-regulation of the TGF-beta target gene, PTPRK, by the Epstein-Barr virus-encoded EBNA1 contributes to the growth and survival of Hodgkin lymphoma cells Blood 2008 111 1 292 301
53. Wood V. H. J., O'Neil J. D., Wei W., Stewart S. E., Dawson C. W., Young L. S., Epstein-Barr virus-encoded EBNA1 regulates cellular gene transcription and modulates the STAT1 and TGF signaling pathways Oncogene 2007 26 28 4135 4147 (Pubitemid 46920177)
54. Fukuda M., Kurosaki H., Sairenji T., Loss of functional transforming growth factor (TGF)- type II receptor results in insensitivity to TGF- -mediated apoptosis and Epstein-Barr virus reactivation Journal of Medical Virology 2006 78 11 1456 1464 (Pubitemid 44533876)
55. Horndasch M., Raschke E. E., Bommer G., Schuhmacher M., Dumont E., Kuklik-Roos C., Eick D., Kempkes B., Epstein-Barr virus antagonizes the antiproliferative activity of transforming growth factor- but does not abolish its signaling International Journal of Cancer 2002 101 5 442 447
56. Kang Y., Chen C. R., Massagué J., A self-enabling TGF response coupled to stress signaling: smad engages stress response factor ATF3 for Id1 repression in epithelial cells Molecular Cell 2003 11 4 915 926 (Pubitemid 36566314)
57. Lo A. K. F., Dawson C. W., Lo K. W., Yu Y., Young L. S., Upregulation of Id1 by Epstein-Barr Virus-encoded LMP1 confers resistance to TGF -mediated growth inhibition Molecular Cancer 2010 9, article 155
58. Spender L. C., Inman G. J., TGF- induces growth arrest in burkitt lymphoma cells via transcriptional repression of E2F-1 The Journal of Biological Chemistry 2009 284 3 1435 1442
59. George N. M., Evans J. J. D., Luo X., A three-helix homo-oligomerization domain containing BH3 and BH1 is responsible for the apoptotic activity of Bax Genes and Development 2007 21 15 1937 1948 (Pubitemid 47204932)
60. Grimm T., Schneider S., Naschberger E., Huber J., Guenzi E., Kieser A., Reitmeir P., Schulz T. F., Morris C. A., Strzl M., EBV latent membrane protein-1 protects B cells from apoptosis by inhibition of BAX Blood 2005 105 8 3263 3269
61. Altmann M., Hammerschmidt W., Epstein-barr virus provides a new paradigm: a requirement for the immediate inhibition of apoptosis PLoS Biology 2005 3 12, article e404
62. Kvansakul M., Wei A. H., Fletcher J. I., Willis S. N., Chen L., Roberts A. W., Huang D. C.S., Colman P. M., Structural basis for apoptosis inhibition by Epstein-Barr virus bhrf1 PLoS Pathogens 2010 6 12
63. Pegman P. M., Smith S. M., D'Souza B. N., Loughran S. T., Maier S., Kempkes B., Cahill P. A., Simmons M. J., Gélinas C., Walls D., Epstein-Barr virus nuclear antigen 2 trans-activates the cellular antiapoptotic bfl-1 gene by a CBF1/RBPJ -dependent pathway Journal of Virology 2006 80 16 8133 8144 (Pubitemid 44182313)
64. D'Souza B., Rowe M., Walls D., The bfl-1 gene is transcriptionally upregulated by the Epstein-Barr virus LMP1, and its expression promotes the survival of a Burkitt's lymphoma cell line Journal of Virology 2000 74 14 6652 6658 (Pubitemid 30429836)
65. Henderson S., Rowe M., Gregory C., Croom-Carter D., Wang F., Longnecker R., Kieff E., Rickinson A., Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death Cell 1991 65 7 1107 1115 (Pubitemid 121001325)
66. Wang S., Rowe M., Lundgren E., Expression of the Epstein Barr virus transforming protein LMP1 causes a rapid and transient stimulation of the Bcl-2 homologue Mcl-1 levels in B- cell lines Cancer Research 1996 56 20 4610 4613 (Pubitemid 26338058)
67. Portis T., Longnecker R., Epstein-Barr virus (EBV) LMP2A mediates B-lymphocyte survival through constitutive activation of the Ras/PI3K/Akt pathway Oncogene 2004 23 53 8619 8628 (Pubitemid 39576469)
68. Choy E. Y. W., Siu K. L., Kok K. H., Lung R. W. M., Tsang C. M., To K. F., Kwong D. L. W., Tsao S. W., Jin D. Y., An Epstein-Barr virus-encoded microRNA targets PUMA to promote host cell survival Journal of Experimental Medicine 2008 205 11 2551 2560
69. Linnstaedt S. D., Gottwein E., Skalsky R. L., Luftig M. A., Cullen B. R., Virally induced cellular microRNA miR-155 plays a key role in B-cell immortalization by Epstein-Barr virus Journal of Virology 2010 84 22 11670 11678
70. Boyd J. M., Gallo G. J., Elangovan B., Houghton A. B., Malstrom S., Avery B. J., Ebb R. G., Subramanian T., Chittenden T., Lutz R. J., Chinnadurai G., Bik, a novel death-inducing protein shares a distinct sequence motif with Bcl-2 family proteins and interacts with viral and cellular survival-promoting proteins Oncogene 1995 11 9 1921 1928
71. Shimazu T., Degenhardt K., Nur-E-Kamal A., Zhang J., Yoshida T., Zhang Y., Mathew R., White E., Inouye M., NBK/BIK antagonizes MCL-1 and BCL-XL and activates BAK-mediated apoptosis in response to protein synthesis inhibition Genes and Development 2007 21 8 929 941 (Pubitemid 46625642)
72. Rowe M., Glaunsinger B., Van Leeuwen D., Zuo J., Sweetman D., Ganem D., Middeldorp J., Wiertz E. J. H. J., Ressing M. E., Host shutoff during productive Epstein-Barr virus infection is mediated by BGLF5 and may contribute to immune evasion Proceedings of the National Academy of Sciences of the United States of America 2007 104 9 3366 3371 (Pubitemid 46364165)
73. Mebratu Y. A., Dickey B. F., Evans C., Tesfaigzi Y., The BH3-only protein Bik/Blk/Nbk inhibits nuclear translocation of activated ERK1/2 to mediate IFN -induced cell death Journal of Cell Biology 2008 183 3 429 439
74. Clybouw C., Mchichi B., Mouhamad S., Auffredou M. T., Bourgeade M. F., Sharma S., Leca G., Vazquez A., EBV infection of human B lymphocytes leads to down-regulation of bim expression: relationship to resistance to apoptosis Journal of Immunology 2005 175 5 2968 2973 (Pubitemid 41170514)
75. Anderton E., Yee J., Smith P., Crook T., White R. E., Allday M. J., Two Epstein-Barr virus (EBV) oncoproteins cooperate to repress expression of the proapoptotic tumour-suppressor Bim: clues to the pathogenesis of Burkitt's lymphoma Oncogene 2008 27 4 421 433
76. Paschos K., Smith P., Anderton E., Middeldorp J. M., White R. E., Allday M. J., Epstein-Barr virus latency in B cells leads to epigenetic repression and CpG methylation of the tumour suppressor gene Bim PLoS Pathogens 2009 5 6
77. Bieging K. T., Swanson-Mungerson M., Amick A. C., Longnecker R., Epstein-Barr virus in Burkitt's lymphoma: a role for latent membrane protein 2A Cell Cycle 2010 9 5 901 908
78. Egle A., Harris A. W., Bouillet P., Cory S., Bim is a suppressor of Myc-induced mouse B cell leukemia Proceedings of the National Academy of Sciences of the United States of America 2004 101 16 6164 6169 (Pubitemid 38520545)
79. Skalska L., White R. E., Franz M., Ruhmann M., Allday M. J., Epigenetic repression of p16INK4A by latent epstein-barr virus requires the interaction of EBNA3A and EBNA3C with CtBP PLoS Pathogens 2010 6 6
80. Maruo S., Zhao B., Johannsen E., Kieff E., Zou J., Takada K., Epstein-Barr virus nuclear antigens 3C and 3A maintain lymphoblastoid cell growth by repressing p16INK4A and p14ARF expression Proceedings of the National Academy of Sciences of the United States of America 2011 108 5 1919 1924
81. Oussaief L., Hippocrate A., Clybouw C., Rampanou A., Ramirez V., Desgranges C., Vazquez A., Khelifa R., Joab I., Activation of the lytic program of the Epstein-Barr virus in Burkitt's lymphoma cells leads to a two steps downregulation of expression of the proapoptotic protein BimEL, one of which is EBV-late-gene expression dependent Virology 2009 387 1 41 49
82. Hannon G. J., RNA interference Nature 2002 418 6894 244 251 (Pubitemid 34773784)
83. Seto E., Moosmann A., Grmminger S., Walz N., Grundhoff A., Hammerschmidt W., Micro RNAS of epstein-barr virus promote cell cycle progression and prevent apoptosis of primary human B cells PLoS Pathogens 2010 6 8 69 70
84. Allday M. J., Sinclair A., Parker G., Crawford D. H., Farrell P. J., Epstein-Barr virus efficiently immortalizes human B cells without neutralizing the function of p53 The EMBO Journal 1995 14 7 1382 1391
85. O'Nions J., Turner A., Craig R., Allday M. J., Epstein-Barr virus selectively deregulates DNA damage responses in normal B cells but has no detectable effect on regulation of the tumor suppressor p53 Journal of Virology 2006 80 24 12408 12413 (Pubitemid 44904393)
86. Saha A., Murakami M., Kumar P., Bajaj B., Sims K., Robertson E. S., Epstein-Barr virus nuclear antigen 3C augments Mdm2-mediated p53 ubiquitination and degradation by deubiquitinating Mdm2 Journal of Virology 2009 83 9 4652 4669
87. Kashuba E., Yurchenko M., Yenamandra S. P., Snopok B., Szekely L., Bercovich B., Ciechanover A., Klein G., Epstein-Barr virus-encoded EBNA-5 forms trimolecular protein complexes with MDM2 and p53 and inhibits the transactivating function of p53 International Journal of Cancer 2011 128 4 817 825
88. Sato Y., Shirata N., Kudoh A., Iwahori S., Nakayama S., Murata T., Isomura H., Nishiyama Y., Tsurumi T., Expression of Epstein-Barr virus BZLF1 immediate-early protein induces p53 degradation independent of MDM2, leading to repression of p53-mediated transcription Virology 2009 388 1 204 211
89. Vereide D. T., Sugden B., Lymphomas differ in their dependence on Epstein-Barr virus Blood 2011 117 6 1977 1985
90. Bultema R., Longnecker R., Swanson-Mungerson M., Epstein-Barr virus LMP2A accelerates MYC-induced lymphomagenesis Oncogene 2009 28 11 1471 1476