Developments in Burkitt's lymphoma: Novel cooperations in oncogenic MYC signaling

Cancer Management and Research

Volumn 6, Issue 1, 2014, Pages 27-38

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

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

AKT; Burkitt's lymphoma; C MYC; Epstein Barr virus; MTOR; PI3 kinase

Indexed keywords

2 (4 HYDROXYPHENYL) 4 MORPHOLINOPYRIDO[3',2':4,5]FURO[3,2 D]PYRIMIDINE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; 8 [4 (1 AMINOCYCLOBUTYL)PHENYL] 9 PHENYL 1,2,4 TRIAZOLO[3,4 F][1,6]NAPHTHYRIDIN 3(2H) ONE; BIM PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAX; PROTEIN P53;

AMINO ACID SUBSTITUTION; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BURKITT LYMPHOMA; CARCINOGENESIS; DISEASE ASSOCIATION; ENZYME ACTIVITY; EPSTEIN BARR VIRUS INFECTION; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; HERPES VIRUS INFECTION; HUMAN; MALARIA; MOLECULAR PATHOLOGY; NONHUMAN; ONCOGENE C MYC; ONCOGENE MYC; PROTEIN STABILITY; REVIEW; SIGNAL TRANSDUCTION; STRESS;

EID: 84892397073     PISSN: None     EISSN: 11791322     Source Type: Journal    
DOI: 10.2147/CMAR.S37745     Document Type: Review

References (119)

1. Burkitt D. A sarcoma involving the jaws in African children. Br J Surg. 1958; 46(197): 218-223.
2. Crawford DH. Biology and disease associations of Epstein-Barr virus. Philos Trans R Soc Lond B Biol Sci. 2001; 356(1408): 461-473.
3. Dalla-Favera R, Bregni M, Erikson J, Patterson D, Gallo RC, Croce CM. Human c-myc onc gene is located on the region of chromosome 8 that is translocated in Burkitt lymphoma cells. Proc Natl Acad Sci U S A. 1982; 79(24): 7824-7827.
4. Taub R, Kirsch I, Morton C, et al. Translocation of the c-myc gene into the immunoglobulin heavy chain locus in human Burkitt lymphoma and murine plasmacytoma cells. Proc Natl Acad Sci U S A. 1982; 79(24): 7837-7841.
5. Moormann AM, Snider CJ, Chelimo K. The company malaria keeps: how co-infection with Epstein-Barr virus leads to endemic Burkitt lymphoma. Curr Opin Infect Dis. 2011; 24(5): 435-441.
6. Spender LC, Inman GJ. Inhibition of germinal centre apoptotic programmes by epstein-barr virus. Adv Hematol. 2011; 2011: 829525.
7. Chang TC, Yu D, Lee YS, et al. Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet. 2008; 40(1): 43-50.
8. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature. 2005; 435(7043): 839-843.
9. Blackwell TK, Kretzner L, Blackwood EM, Eisenman RN, Weintraub H. Sequence-specific DNA binding by the c-Myc protein. Science. 1990; 250(4984): 1149-1151.
10. Blackwell TK, Huang J, Ma A, et al. Binding of myc proteins to canonical and noncanonical DNA sequences. Mol Cell Biol. 1993; 13(9): 5216-5224.
11. Lüscher B. MAD1 and its life as a MYC antagonist: an update. Eur J Cell Biol. 2012; 91(6-7): 506-514.
12. Taub R, Moulding C, Battey J, et al. Activation and somatic mutation of the translocated c-myc gene in burkitt lymphoma cells. Cell. 1984; 36(2): 339-348.
13. ar-Rushdi A, Nishikura K, Erikson J, Watt R, Rovera G, Croce CM. Differential expression of the translocated and the untranslocated c-myc oncogene in Burkitt lymphoma. Science. 1983; 222(4622): 390-393.
14. Hayday AC, Gillies SD, Saito H, et al. Activation of a translocated human c-myc gene by an enhancer in the immunoglobulin heavy-chain locus. Nature. 1984; 307(5949): 334-340.
15. Johnston LA, Prober DA, Edgar BA, Eisenman RN, Gallant P. Drosophila myc regulates cellular growth during development. Cell. 1999; 98(6): 779-790.
16. Grewal SS, Li L, Orian A, Eisenman RN, Edgar BA. Myc-dependent regulation of ribosomal RNA synthesis during Drosophila development. Nat Cell Biol. 2005; 7(3): 295-302.
17. Bouchard C, Stellar P, Eilers M. Control of cell proliferation by Myc. Trends Cell Biol. 1998; 8(5): 202-206.
18. Park SS, Kim JS, Tessarollo L, et al. Insertion of c-Myc into Igh induces B-cell and plasma-cell neoplasms in mice. Cancer Res. 2005; 65(4): 1306-1315.
19. Yin X, Giap C, Lazo JS, Prochownik EV. Low molecular weight inhibitors of Myc-Max interaction and function. Oncogene. 2003; 22(40): 6151-6159.
20. Gomez-Curet I, Perkins RS, Bennett R, Feidler KL, Dunn SP, Krueger LJ. c-Myc inhibition negatively impacts lymphoma growth. J Pediatr Surg. 2006; 41(1): 207-211; discussion 207-211.
21. Sampson VB, Rong NH, Han J, et al. MicroRNA let-7a down-regulates MYC and reverts MYC-induced growth in Burkitt lymphoma cells. Cancer Res. 2007; 67(20): 9762-9770.
22. Spender LC, Inman GJ. Phosphoinositide 3-kinase/AKT/mTORC1/2 signaling determines sensitivity of Burkitt's lymphoma cells to BH3 mimetics. Mol Cancer Res. 2012; 10(3): 347-359.
23. Schuhmacher M, Staege MS, Pajic A, et al. Control of cell growth by c-Myc in the absence of cell division. Curr Biol. 1999; 9(21): 1255-1258.
24. Schlosser I, Hölzel M, Hoffmann R, et al. Dissection of transcriptional programmes in response to serum and c-Myc in a human B-cell line. Oncogene. 2005; 24(3): 520-524.
25. Marinkovic D, Marinkovic T, Mahr B, Hess J, Wirth T. Reversible lymphomagenesis in conditionally c-MYC expressing mice. Int J Cancer. 2004; 110(3): 336-342.
26. Schuhmacher M, Kohlhuber F, Hölzel M, et al. The transcriptional program of a human B cell line in response to Myc. Nucleic Acids Res. 2001; 29(2): 397-406.
27. Ji H, Wu G, Zhan X, et al. Cell-type independent MYC target genes reveal a primordial signature involved in biomass accumulation. PLoS One. 2011; 6(10): e26057.
28. Lin CY, Lovén J, Rahl PB, et al. Transcriptional amplification in tumor cells with elevated c-Myc. Cell. 2012; 151(1): 56-67.
29. Li Z, Van Calcar S, Qu C, Cavenee WK, Zhang MQ, Ren B. A global transcriptional regulatory role for c-Myc in Burkitt's lymphoma cells. Proc Natl Acad Sci U S A. 2003; 100(14): 8164-8169.
30. Seitz V, Butzhammer P, Hirsch B, et al. Deep sequencing of MYC DNA-binding sites in Burkitt lymphoma. PLoS One. 2011; 6(11): e26837.
31. Fan J, Zeller K, Chen YC, et al. Time-dependent c-Myc transactomes mapped by Array-based nuclear run-on reveal transcriptional modules in human B cells. PLoS One. 2010; 5(3): e9691.
32. Love C, Sun Z, Jima D, et al. The genetic landscape of mutations in Burkitt lymphoma. Nat Genet. 2012; 44(12): 1321-1325.
33. Hann SR, Eisenman RN. Proteins encoded by the human c-myc oncogene: differential expression in neoplastic cells. Mol Cell Biol. 1984; 4(11): 2486-2497.
34. Sakamuro D, Prendergast GC. New Myc-interacting proteins: a second Myc network emerges. Oncogene. 1999; 18(19): 2942-2954.
35. Kuttler F, Amé P, Clark H, et al. c-myc box II mutations in Burkitt's lymphoma-derived alleles reduce cell-transformation activity and lower response to broad apoptotic stimuli. Oncogene. 2001; 20(42): 6084-6094.
36. Sears R, Nuckolls F, Haura E, Taya Y, Tamai K, Nevins JR. Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability. Genes Dev. 2000; 14(19): 2501-2514.
37. Salghetti SE, Kim SY, Tansey WP. Destruction of Myc by ubiquitin-mediated proteolysis: cancer-associated and transforming mutations stabilize Myc. EMBO J. 1999; 18(3): 717-726.
38. Gregory MA, Hann SR. c-Myc proteolysis by the ubiquitin-proteasome pathway: stabilization of c-Myc in Burkitt's lymphoma cells. Mol Cell Biol. 2000; 20(7): 2423-2435.
39. Bahram F, von der Lehr N, Cetinkaya C, Larsson LG. c-Myc hot spot mutations in lymphomas result in inefficient ubiquitination and decreased proteasome-mediated turnover. Blood. 2000; 95(6): 2104-2110.
40. Hoang AT, Lutterbach B, Lewis BC, et al. A link between increased transforming activity of lymphoma-derived MYC mutant alleles, their defective regulation by p107, and altered phosphorylation of the c-Myc transactivation domain. Mol Cell Biol. 1995; 15(8): 4031-4042.
41. Bouchard C, Lee S, Paulus-Hock V, Loddenkemper C, Eilers M, Schmitt CA. FoxO transcription factors suppress Myc-driven lymphomagenesis via direct activation of Arf. Genes Dev. 2007; 21(21): 2775-2787.
42. Eischen CM, Weber JD, Roussel MF, Sherr CJ, Cleveland JL. Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes Dev. 1999; 13(20): 2658-2669.
43. Post SM, Quintás-Cardama A, Terzian T, Smith C, Eischen CM, Lozano G. p53-dependent senescence delays Emu-myc-induced B-cell lymphomagenesis. Oncogene. 2010; 29(9): 1260-1269.
44. Farrell PJ, Allan GJ, Shanahan F, Vousden KH, Crook T. p53 is frequently mutated in Burkitt's lymphoma cell lines. EMBO J. 1991; 10(10): 2879-2887.
45. Vousden KH, Crook T, Farrell PJ. Biological activities of p53 mutants in Burkitt's lymphoma cells. J Gen Virol. 1993; 74(Pt 5): 803-810.
46. Leventaki V, Rodic V, Tripp SR, et al. TP53 pathway analysis in paediatric Burkitt lymphoma reveals increased MDM4 expression as the only TP53 pathway abnormality detected in a subset of cases. Br J Haematol. 2012; 158(6): 763-771.
47. Lindström MS, Klangby U, Wiman KG. p14ARF homozygous deletion or MDM2 overexpression in Burkitt lymphoma lines carrying wild type p53. Oncogene. 2001; 20(17): 2171-2177.
48. Pujals A, Renouf B, Robert A, Chelouah S, Hollville E, Wiels J. Treatment with a BH3 mimetic overcomes the resistance of latency III EBV (+) cells to p53-mediated apoptosis. Cell Death Dis. 2011; 2: e184.
49. Egle A, Harris AW, Bouillet P, Cory S. Bim is a suppressor of Myc-induced mouse B cell leukemia. Proc Natl Acad Sci U S A. 2004; 101(16): 6164-6169.
50. Dang CV, O'Donnell KA, Juopperi T. The great MYC escape in tumorigenesis. Cancer Cell. 2005; 8(3): 177-178.
51. Hemann MT, Bric A, Teruya-Feldstein J, et al. Evasion of the p53 tumour surveillance network by tumour-derived MYC mutants. Nature. 2005; 436(7052): 807-811.
52. Eischen CM, Roussel MF, Korsmeyer SJ, Cleveland JL. Bax loss impairs Myc-induced apoptosis and circumvents the selection of p53 mutations during Myc-mediated lymphomagenesis. Mol Cell Biol. 2001; 21(22): 7653-7662.
53. Paschos K, Smith P, Anderton E, Middeldorp JM, White RE, Allday MJ. Epstein-barr virus latency in B cells leads to epigenetic repression and CpG methylation of the tumour suppressor gene Bim. PLoS Pathog. 2009; 5(6): e1000492.
54. Richter-Larrea JA, Robles EF, Fresquet V, et al. Reversion of epigenetically mediated BIM silencing overcomes chemoresistance in Burkitt lymphoma. Blood. 2010; 116(14): 2531-2542.
55. Erlacher M, Labi V, Manzl C, et al. Puma cooperates with Bim, the rate-limiting BH3-only protein in cell death during lymphocyte development, in apoptosis induction. J Exp Med. 2006; 203(13): 2939-2951.
56. Garrison SP, Jeffers JR, Yang C, et al. Selection against PUMA gene expression in Myc-driven B-cell lymphomagenesis. Mol Cell Biol. 2008; 28(17): 5391-5402.
57. Spender LC, Carter MJ, O'Brien DI, et al. Transforming growth factor-β directly induces p53-up-regulated modulator of apoptosis (PUMA) during the rapid induction of apoptosis in myc-driven B-cell lymphomas. J Biol Chem. 2013; 288(7): 5198-5209.
58. Spender LC, O'Brien DI, Simpson D, et al. TGF-beta induces apoptosis in human B cells by transcriptional regulation of BIK and BCL-XL. Cell Death Differ. 2009; 16(4): 593-602.
59. Sander S, Calado DP, Srinivasan L, et al. Synergy between PI3K signaling and MYC in Burkitt lymphomagenesis. Cancer Cell. 2012; 22(2): 167-179.
60. Rohn JL, Hueber AO, McCarthy NJ, et al. The opposing roles of the Akt and c-Myc signalling pathways in survival from CD95-mediated apoptosis. Oncogene. 1998; 17(22): 2811-2818.
61. Zhao JJ, Gjoerup OV, Subramanian RR, et al. Human mammary epithelial cell transformation through the activation of phosphatidylinositol 3-kinase. Cancer Cell. 2003; 3(5): 483-495.
62. Kumar A, Marqués M, Carrera AC. Phosphoinositide 3-kinase activation in late G1 is required for c-Myc stabilization and S phase entry. Mol Cell Biol. 2006; 26(23): 9116-9125.
63. Han SS, Yun H, Son DJ, et al. NF-kappaB/STAT3/PI3K signaling crosstalk in iMyc E mu B lymphoma. Mol Cancer. 2010; 9: 97.
64. Bouchard C, Marquardt J, Brás A, Medema RH, Eilers M. Myc-induced proliferation and transformation require Akt-mediated phosphorylation of FoxO proteins. EMBO J. 2004; 23(14): 2830-2840.
65. Curnock AP, Knox KA. LY294002-mediated inhibition of phosphatidylinositol 3-kinase activity triggers growth inhibition and apoptosis in CD40-triggered Ramos-Burkitt lymphoma B cells. Cell Immunol. 1998; 187(2): 77-87.
66. Brennan P, Mehl AM, Jones M, Rowe M. Phosphatidylinositol 3-kinase is essential for the proliferation of lymphoblastoid cells. Oncogene. 2002; 21(8): 1263-1271.
67. Peled JU, Yu JJ, Venkatesh J, et al. Requirement for cyclin D3 in germinal center formation and function. Cell Res. 2010; 20(6): 631-646.
68. Cato MH, Chintalapati SK, Yau IW, Omori SA, Rickert RC. Cyclin D3 is selectively required for proliferative expansion of germinal center B cells. Mol Cell Biol. 2011; 31(1): 127-137.
69. Møller MB, Nielsen O, Pedersen NT. Cyclin D3 expression in non-Hodgkin lymphoma. Correlation with other cell cycle regulators and clinical features. Am J Clin Pathol. 2001; 115(3): 404-412.
70. Schmitz R, Young RM, Ceribelli M, et al. Burkitt lymphoma pathogenesis and therapeutic targets from structural and functional genomics. Nature. 2012; 490(7418): 116-120.
71. Goldfarb AN, Flores JP, Lewandowska K. Involvement of the E2A basic helix-loop-helix protein in immunoglobulin heavy chain class switching. Mol Immunol. 1996; 33(11-12): 947-956.
72. Richter J, Schlesner M, Hoffmann S, et al; ICGC MMML-Seq Project. Recurrent mutation of the ID3 gene in Burkitt lymphoma identified by integrated genome, exome and transcriptome sequencing. Nat Genet. 2012; 44(12): 1316-1320.
73. Spender LC, Lucchesi W, Bodelon G, et al. Cell target genes of Epstein-Barr virus transcription factor EBNA-2: induction of the p55alpha regulatory subunit of PI3-kinase and its role in survival of EREB2. 5 cells. J Gen Virol. 2006; 87(Pt 10): 2859-2867.
74. Schild C, Wirth M, Reichert M, Schmid RM, Saur D, Schneider G. PI3K signaling maintains c-myc expression to regulate transcription of E2F1 in pancreatic cancer cells. Mol Carcinog. 2009; 48(12): 1149-1158.
75. van Weeren PC, de Bruyn KM, de Vries-Smits AM, van Lint J, Burgering BM. Essential role for protein kinase B (PKB) in insulin-induced glycogen synthase kinase 3 inactivation. Characterization of dominant-negative mutant of PKB. J Biol Chem. 1998; 273(21): 13150-13156.
76. Amente S, Zhang J, Lavadera ML, Lania L, Avvedimento EV, Majello B. Myc and PI3K/AKT signaling cooperatively repress FOXO3a-dependent PUMA and GADD45a gene expression. Nucleic Acids Res. 2011; 39(22): 9498-9507.
77. Ashcroft M, Ludwig RL, Woods DB, et al. Phosphorylation of HDM2 by Akt. Oncogene. 2002; 21(13): 1955-1962.
78. Cardone MH, Roy N, Stennicke HR, et al. Regulation of cell death protease caspase-9 by phosphorylation. Science. 1998; 282(5392): 1318-1321.
79. Devlin JR, Hannan KM, Ng PY, et al. AKT signalling is required for ribosomal RNA synthesis and progression of Eμ-Myc B-cell lymphoma in vivo. FEBS J. Epub January 19, 2013.
80. Hsieh AC, Costa M, Zollo O, et al. Genetic dissection of the oncogenic mTOR pathway reveals druggable addiction to translational control via 4EBP-eIF4E. Cancer Cell. 2010; 17(3): 249-261.
81. Dowling RJ, Topisirovic I, Alain T, et al. mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science. 2010; 328(5982): 1172-1176.
82. Feldman ME, Apsel B, Uotila A, et al. Active-site inhibitors of mTOR target rapamycin-resistant outputs of mTORC1 and mTORC2. PLoS Biol. 2009; 7(2): e38.
83. Thoreen CC, Sabatini DM. Rapamycin inhibits mTORC1, but not completely. Autophagy. 2009; 5(5): 725-726.
84. Zhu J, Blenis J, Yuan J. Activation of PI3K/Akt and MAPK pathways regulates Myc-mediated transcription by phosphorylating and promoting the degradation of Mad1. Proc Natl Acad Sci U S A. 2008; 105(18): 6584-6589.
85. Li S, Takasu T, Perlman DM, et al. Translation factor eIF4E rescues cells from Myc-dependent apoptosis by inhibiting cytochrome c release. J Biol Chem. 2003; 278(5): 3015-3022.
86. Mills JR, Hippo Y, Robert F, et al. mTORC1 promotes survival through translational control of Mcl-1. Proc Natl Acad Sci U S A. 2008; 105(31): 10853-10858.
87. Wall M, Poortinga G, Stanley KL, et al. The mTORC1 inhibitor everolimus prevents and treats Eμ-Myc lymphoma by restoring oncogene-induced senescence. Cancer Discov. 2013; 3(1): 82-95.
88. Grespi F, Soratroi C, Krumschnabel G, et al. BH3-only protein Bmf mediates apoptosis upon inhibition of CAP-dependent protein synthesis. Cell Death Differ. 2010; 17(11): 1672-1683.
89. Shortt J, Martin BP, Newbold A, et al. Combined inhibition of PI3K-related DNA damage response kinases and mTORC1 induces apoptosis in MYC-driven B-cell lymphomas. Blood. 2013; 121(15): 2964-2974.
90. Pourdehnad M, Truitt ML, Siddiqi IN, Ducker GS, Shokat KM, Ruggero D. Myc and mTOR converge on a common node in protein synthesis control that confers synthetic lethality in Myc-driven cancers. Proc Natl Acad Sci U S A. 2013; 110(29): 11988-11993.
91. Allday MJ. How does Epstein-Barr virus (EBV) complement the activation of Myc in the pathogenesis of Burkitt's lymphoma? Semin Cancer Biol. 2009; 19(6): 366-376.
92. Sinclair AJ, Palmero I, Peters G, Farrell PJ. EBNA-2 and EBNA-LP cooperate to cause G0 to G1 transition during immortalization of resting human B lymphocytes by Epstein-Barr virus. EMBO J. 1994; 13(14): 3321-3328.
93. Kaiser C, Laux G, Eick D, Jochner N, Bornkamm GW, Kempkes B. The proto-oncogene c-myc is a direct target gene of Epstein-Barr virus nuclear antigen 2. J Virol. 1999; 73(5): 4481-4484.
94. Spender LC, Cornish GH, Rowland B, Kempkes B, Farrell PJ. Direct and indirect regulation of cytokine and cell cycle proteins by EBNA-2 during Epstein-Barr virus infection. J Virol. 2001; 75(8): 3537-3546.
95. Rosato P, Anastasiadou E, Garg N, et al. Differential regulation of miR-21 and miR-146a by Epstein-Barr virus-encoded EBNA2. Leukemia. 2012; 26(11): 2343-2352.
96. 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.
97. Mancao C, Hammerschmidt W. Epstein-Barr virus latent membrane protein 2A is a B-cell receptor mimic and essential for B-cell survival. Blood. 2007; 110(10): 3715-3721.
98. Swanson-Mungerson MA, Caldwell RG, 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. J Virol. 2005; 79(12): 7355-7362.
99. Gires O, Zimber-Strobl U, Gonnella R, et al. Latent membrane protein 1 of Epstein-Barr virus mimics a constitutively active receptor molecule. EMBO J. 1997; 16(20): 6131-6140.
100. Wang D, Liebowitz D, Kieff E. An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells. Cell. 1985; 43(3 Pt 2): 831-840.
101. Izumi KM, Kieff ED. The Epstein-Barr virus oncogene product latent membrane protein 1 engages the tumor necrosis factor receptor-associated death domain protein to mediate B lymphocyte growth transformation and activate NF-kappaB. Proc Natl Acad Sci U S A. 1997; 94(23): 12592-12597.
102. Roberts ML, Cooper NR. Activation of a ras-MAPK-dependent pathway by Epstein-Barr virus latent membrane protein 1 is essential for cellular transformation. Virology. 1998; 240(1): 93-99.
103. Eliopoulos AG, Young LS. Activation of the cJun N-terminal kinase (JNK) pathway by the Epstein-Barr virus-encoded latent membrane protein 1 (LMP1). Oncogene. 1998; 16(13): 1731-1742.
104. Dawson CW, Tramountanis G, Eliopoulos AG, Young LS. Epstein-Barr virus latent membrane protein 1 (LMP1) activates the phosphatidylinositol 3-kinase/Akt pathway to promote cell survival and induce actin filament remodeling. J Biol Chem. 2003; 278(6): 3694-3704.
105. Mainou BA, Everly DN Jr, Raab-Traub N. Epstein-Barr virus latent membrane protein 1 CTAR1 mediates rodent and human fibroblast transformation through activation of PI3K. Oncogene. 2005; 24(46): 6917-6924.
106. 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 Res. 1996; 56(20): 4610-4613.
107. Pegman PM, Smith SM, D'Souza BN, et al. Epstein-Barr virus nuclear antigen 2 trans-activates the cellular antiapoptotic bfl-1 gene by a CBF1/RBPJ kappa-dependent pathway. J Virol. 2006; 80(16): 8133-8144.
108. Clybouw C, McHichi B, Mouhamad S, et al. EBV infection of human B lymphocytes leads to down-regulation of Bim expression: relationship to resistance to apoptosis. J Immunol. 2005; 175(5): 2968-2973.
109. Anderton E, Yee J, Smith P, Crook T, White RE, Allday MJ. 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.
110. 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. Proc Natl Acad Sci U S A. 2011; 108(5): 1919-1924.
111. Saha A, Murakami M, Kumar P, Bajaj B, Sims K, Robertson ES. Epstein-Barr virus nuclear antigen 3C augments Mdm2-mediated p53 ubiquitination and degradation by deubiquitinating Mdm2. J Virol. 2009; 83(9): 4652-4669.
112. Sato Y, Shirata N, Kudoh A, et al. 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.
113. Kashuba E, Yurchenko M, Yenamandra SP, et al. Epstein-Barr virus-encoded EBNA-5 forms trimolecular protein complexes with MDM2 and p53 and inhibits the transactivating function of p53. Int J Cancer. 2011; 128(4): 817-825.
114. Pokrovskaja K, Ehlin-Henriksson B, Bartkova J, et al. Phenotype-related differences in the expression of D-type cyclins in human B cell-derived lines. Cell Growth Differ. 1996; 7(12): 1723-1732.
115. Mataraza JM, Tumang JR, Gumina MR, Gurdak SM, Rothstein TL, Chiles TC. Disruption of cyclin D3 blocks proliferation of normal B-1a cells, but loss of cyclin D3 is compensated by cyclin D2 in cyclin D3-deficient mice. J Immunol. 2006; 177(2): 787-795.
116. Brady G, Macarthur GJ, Farrell PJ. Epstein-Barr virus and Burkitt lymphoma. Postgrad Med J. 2008; 84(993): 372-377.
117. Rickinson AB, Young LS, Rowe M. Influence of the Epstein-Barr virus nuclear antigen EBNA2 on the growth phenotype of virus-transformed B cells. J Virol. 1987; 61(5): 1310-1317.
118. Lucchesi W, Brady G, Dittrich-Breiholz O, Kracht M, Russ R, Farrell PJ. Differential gene regulation by Epstein-Barr virus type 1 and type 2 EBNA2. J Virol. 2008; 82(15): 7456-7466.
119. Aitken C, Sengupta SK, Aedes C, Moss DJ, Sculley TB. Heterogeneity within the Epstein-Barr virus nuclear antigen 2 gene in different strains of Epstein-Barr virus. J Gen Virol. 1994; 75(Pt 1): 95-100.