Epstein-Barr virus and Burkitt lymphoma

Chinese Journal of Cancer

Volumn 33, Issue 12, 2014, Pages 609-619

  Rowe, Martin ^a   Fitzsimmons, Leah ^a   Bell, Andrew I ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Burkitt lymphoma; C MYC; Epstein Barr virus; Malaria; Tumor virus

Indexed keywords

B LYMPHOCYTE; BURKITT LYMPHOMA; EPSTEIN BARR VIRUS; GENE TRANSLOCATION; HUMAN; VIROLOGY;

B-LYMPHOCYTES; BURKITT LYMPHOMA; HERPESVIRUS 4, HUMAN; HUMANS; TRANSLOCATION, GENETIC;

EID: 84909967046     PISSN: None     EISSN: 1944446X     Source Type: Journal    
DOI: 10.5732/cjc.014.10190     Document Type: Review

References (159)

1. [1] De-The G. The epidemiology of Burkitt’s lymphoma: evidence for a causal association with Epstein-Barr virus. Epidemiol Rev, 1979,1:32-54.
2. [2] Magrath I. Epidemiology: clues to the pathogenesis of Burkitt lymphoma. Br J Haematol, 2012,156:744-756.
3. [3] Henle G, Henle W. Immunofluorescence in cells derived from Burkitt’s lymphoma. J Bacteriol, 1966,91:1248-1256.
4. [4] Henle G, Henle W, Clifford P, et al. Antibodies to Epstein-Barr virus in Burkitt's lymphoma and control groups. J Natl Cancer Inst, 1969,43:1147-1157.
5. [5] Klein G, Clifford P, Henle G, et al. EBV-associated serological patterns in a Burkitt lymphoma patient during regression and recurrence. Int J Cancer, 1969,4:416-421.
6. [6] Geser A, Lenoir GM, Anvret M, et al. Epstein-Barr virus markers in a series of Burkitt's lymphomas from the West Nile District, Uganda. Eur J Cancer Clin Oncol, 1983,19:1393-1404.
7. [7] Geser A, de The G, Lenoir G, et al. Final case reporting from the Ugandan prospective study of the relationship between EBV and Burkitt's lymphoma. Int J Cancer, 1982,29:397-400.
8. [8] Zur Hausen H, Schulte-Holthausen H, Klein G, et al. EBV DNA in biopsies of Burkitt tumours and anaplastic carcinomas of the nasopharynx. Nature, 1970,228:1056-1058.
9. [9] Lindahl T, Klein G, Reedman BM, et al. Relationship between Epstein-Barr virus (EBV) DNA and the EBV-determined nuclear antigen (EBNA) in Burkitt lymphoma biopsies and other lymphoproliferative malignancies. Int J Cancer, 1974,13:764-772.
10. [10] Reedman BM, Klein G. Cellular localization of an Epstein-Barr virus (EBV)-associated complement-fixing antigen in producer and nonproducer lymphoblastoid cell lines. Int J Cancer, 1973,11:499-520.
11. [11] Henle W, Diehl V, Kohn G, et al. Herpes-type virus and chromosome marker in normal leukocytes after growth with irradiated Burkitt cells. Science, 1967,157:1064-1065.
12. [12] Pope JH, Horne MK, Scott W. Transformation of foetal human leukocytes in vitro by filtrates of a human leukaemic cell line containing herpes-like virus. Int J Cancer, 1968,3:857-866.
13. [13] IARC/WHO. Epstein-Barr Virus and Kaposi’s Sarcoma Herpesvirus/Human Herpesvirus 8. 1997/01/01. IARC, 1997.
14. [14] Delecluse HJ, Hammerschmidt W. The genetic approach to the Epstein-Barr virus: from basic virology to gene therapy. Mol Pathol, 2000,53:270-279.
15. [15] Kieff E, Rickinson AB. Epstein-Barr virus and its replication. Knipe DM, Howley PM (eds). Fields Virology. 5th Edition. Philadelphia, USA: Lippincott, Williams & Wilkins, 2007:2603-2654.
16. [16] Masucci MG, Torsteindottir S, Colombani J, et al. Down-regulation of class I HLA antigens and of the Epstein-Barr virus-encoded latent membrane protein in Burkitt lymphoma lines. Proc Natl Acad Sci U S A, 1987,84:4567-4571.
17. [17] Rowe DT, Rowe M, Evan GI, et al. Restricted expression of EBV latent genes and T-lymphocyte-detected membrane antigen in Burkitt's lymphoma cells. EMBO J, 1986,5:2599-2607.
18. [18] Rowe M, Rowe DT, Gregory CD, et al. Differences in B cell growth phenotype reflect novel patterns of Epstein-Barr virus latent gene expression in Burkitt's lymphoma cells. EMBO J, 1987,6:2743-2751.
19. [19] Amoroso R, Fitzsimmons L, Thomas WA, et al. Quantitative studies of Epstein-Barr virus-encoded microRNAs provide novel insights into their regulation. J Virol, 2011,85:996-1010.
20. [20] Burkitt D. A "tumour safari" in East and Central Africa. Br J Cancer, 1962,16:379-386.
21. [21] Burkitt D. A children's cancer dependent on climatic factors. Nature, 1962,194:232-234.
22. [22] Dalldorf G, Linsell CA, Barnhart FE, et al. An epidemiologic approach to the lymphomas of African children and Burkitt's sacroma of the jaws. Perspect Biol Med, 1964,7:435-449.
23. [23] Kafuko GW, Burkitt DP. Burkitt's lymphoma and malaria. Int J Cancer, 1970,6:1-9.
24. [24] Geser A, Brubaker G, Draper CC. Effect of a malaria suppression program on the incidence of African Burkitt's lymphoma. Am J Epidemiol, 1989,129:740-752.
25. [25] Carpenter LM, Newton R, Casabonne D, et al. Antibodies against malaria and Epstein-Barr virus in childhood Burkitt lymphoma: a case-control study in Uganda. Int J Cancer, 2008,122:1319-1323.
26. [26] Mutalima N, Molyneux E, Jaffe H, et al. Associations between Burkitt lymphoma among children in Malawi and infection with HIV, EBV and malaria: results from a case-control study. PLoS One, 2008,3:e2505.
27. [27] Rochford R, Cannon MJ, Moormann AM. Endemic Burkitt‘s lymphoma: a polymicrobial disease? Nat Rev Microbiol, 2005,3:182-187.
28. [28] Manolov G, Manolova Y. Marker band in one chromosome 14 from Burkitt lymphomas. Nature, 1972,237:33-34.
29. [29] Dalla-Favera R, Bregni M, Erikson J, et al. Human c-myc oncogene is located on the region of chromosome 8 that is translocated in Burkitt lymphoma cells. Proc Natl Acad Sci U S A, 1982,79:7824-7827.
30. [30] 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, 1982,79:7837-7841.
31. [31] OConor GT, Rappaport H, Smith EB. Childhood lymphoma resembling “Burkitt Tumor” in the United States. Cancer, 1965,18:411-417.
32. [32] OConor GT, Davies JN. Malignant tumors in African children. With special reference to malignant lymphoma. J Pediatr, 1960,56:526-535.
33. [33] OConor GT. Significant aspects of childhood lymphoma in Africa. Cancer Res, 1963,23:1514-1518.
34. [34] Leoncini L, Raphaël M, Stein H, et al. Burkitt lymphoma. Swedlow SH, Campo E, Harris NL, et al. (eds). WHO classification of tumours of haematopoietic and lymphoid tissues. 4th edition. Lyon, France: International Agency for Research on Cancer, 2008.
35. [35] Mbulaiteye SM, Pullarkat ST, Nathwani BN, et al. Epstein-Barr virus patterns in US Burkitt lymphoma tumors from the SEER residual tissue repository during 1979-2009. APMIS, 2014,122:5-15.
36. [36] Magrath I. The pathogenesis of Burkitt's lymphoma. Adv Cancer Res, 1990,55:133-270.
37. [37] Hummel M, Bentink S, Berger H, et al. A biologic definition of Burkitt's lymphoma from transcriptional and genomic profiling. N Engl J Med, 2006,354:2419-2430.
38. [38] Dave SS, Fu K, Wright GW, et al. Molecular diagnosis of Burkitt's lymphoma. N Engl J Med, 2006,354:2431-2442.
39. [39] Rickinson AB, Kieff E. Epstein-Barr virus. Knipe DM, Howley PM (eds). Fields Virology, 5th edition. Philadelphia, USA: Lippincott, Williams & Wilkins, 2007:2655-2700.
40. [40] Rowe M, Kelly GL, Bell AI, et al. Burkitt's lymphoma: the Rosetta Stone deciphering Epstein-Barr virus biology. Semin Cancer Biol, 2009,19:377-388.
41. [41] Thorley-Lawson DA. Epstein-Barr virus: exploiting the immune system. Nature Rev Immunol, 2001,1:75-82.
42. [42] Thorley-Lawson DA, Hawkins JB, Tracy SI, et al. The pathogenesis of Epstein-Barr virus persistent infection. Curr Opin Virol, 2013,3:227-232.
43. [43] Kurth J, Hansmann ML, Rajewsky K, et al. Epstein-Barr virusinfected B cells expanding in germinal centers of infectious mononucleosis patients do not participate in the germinal center reaction. Proc Natl Acad Sci U S A, 2003,100:4730-4735.
44. [44] Kurth J, Spieker T, Wustrow J, et al. EBV-infected B cells in infectious mononucleosis: viral strategies for spreading in the B cell compartment and establishing latency. Immunity, 2000,13:485-495.
45. [45] Roughan JE, Torgbor C, Thorley-Lawson DA. Germinal center B cells latently infected with Epstein-Barr virus proliferate extensively but do not increase in number. J Virol, 2010,84:1158-1168.
46. [46] Joseph AM, Babcock GJ, Thorley-Lawson DA. Cells expressing the Epstein-Barr virus growth program are present in and restricted to the naive B-cell subset of healthy tonsils. J Virol, 2000,74:9964-9971.
47. [47] Niedobitek G, Agathanggelou A, Herbst H, et al. Epstein-Barr virus (EBV) infection in infectious mononucleosis: virus latency, replication and phenotype of EBV-infected cells. J Pathol, 1997,182:151-159.
48. [48] Babcock GJ, Decker LL, Volk M, et al. EBV persistence in memory B cells in vivo. Immunity, 1998,9:395-404.
49. [49] Babcock GJ, Hochberg D, Thorley-Lawson AD. The expression pattern of Epstein-Barr virus latent genes in vivo is dependent upon the differentiation stage of the infected B cell. Immunity, 2000,13:497-506.
50. [50] Hislop AD, Taylor GS, Sauce D, et al. Cellular responses to viral infection in humans: lessons from Epstein-Barr virus. Annu Rev Immunol, 2007,25:587-617.
51. [51] Heath E, Begue-Pastor N, Chaganti S, et al. Epstein-Barr virus infection of naive B cells in vitro frequently selects clones with mutated immunoglobulin genotypes: implications for virus biology. PLoS Pathog, 2012,8:e1002697.
52. [52] Roughan JE, Thorley-Lawson DA. The intersection of Epstein-Barr virus with the germinal center. J Virol, 2009,83:3968-3976.
53. [53] Kuppers R. Mechanisms of B-cell lymphoma pathogenesis. Nat Rev Cancer, 2005,5:251-262.
54. [54] Gregory CD, Kirchgens C, Edwards CF, et al. Epstein-Barr virus-transformed human precursor B cell lines: altered growth phenotype of lines with germ-line or rearranged but nonexpressed heavy chain genes. Eur J Immunol, 1987,17:1199-1207.
55. [55] Mancao C, Altmann M, Jungnickel B, et al. Rescue of “crippled” germinal center B cells from apoptosis by Epstein-Barr virus. Blood, 2005,106:4339-4344.
56. [56] Bechtel D, Kurth J, Unkel C, et al. 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, 2005,106:4345-4350.
57. [57] Chaganti S, Bell AI, Pastor NB, et al. Epstein-Barr virus infection in vitro can rescue germinal center B cells with inactivated immunoglobulin genes. Blood, 2005,106:4249-4252.
58. [58] Brauninger A, Spieker T, Mottok A, et al. Epstein-Barr virus (EBV)-positive lymphoproliferations in post-transplant patients show immunoglobulin V gene mutation patterns suggesting interference of EBV with normal B cell differentiation processes. Eur J Immunol, 2003,33:1593-1602.
59. [59] Capello D, Cerri M, Muti G, et al. Molecular histogenesis of posttransplantation lymphoproliferative disorders. Blood, 2003,102:3775-3785.
60. [60] Timms JM, Bell A, Flavell JR, et al. Target cells of Epstein-Barrvirus (EBV)-positive post-transplant lymphoproliferative disease: similarities to EBV-positive Hodgkin’s lymphoma. Lancet, 2003,361:217-223.
61. [61] Caldwell RG, Wilson JB, Anderson SJ, et al. Epstein-Barr virus LMP2A drives B cell development and survival in the absence of normal B cell receptor signals. Immunity, 1998,9:405-411.
62. [62] Casola S, Otipoby KL, Alimzhanov M, et al. B cell receptor signal strength determines B cell fate. Nat Immunol, 2004,5:317-327.
63. [63] Mancao C, Hammerschmidt W. Epstein-Barr virus latent membrane protein 2A is a B-cell receptor mimic and essential for B-cell survival. Blood, 2007,110:3715-3721.
64. [64] Brauninger A, Schmitz R, Bechtel D, et al. Molecular biology of Hodgkin’s and Reed/Sternberg cells in Hodgkin’s lymphoma. Int J Cancer, 2006,118:1853-1861.
65. [65] Mosialos G, Birkenbach M, Yalamanchili R, et al. The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the Tumor Necrosis Factor receptor family. Cell, 1995,80:389-399.
66. [66] Floettmann JE, Rowe M. Epstein-Barr virus latent membrane protein-1 (LMP1) C-terminus activation region-2 (CTAR2) maps to the far C-terminus and requires oligomersation for NF-kB activation. Oncogene, 1997,15:1851-1858.
67. [67] 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, 1997,16:6131-6140.
68. [68] Henderson S, Rowe M, Gregory C, et al. Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell, 1991,65:1107-1115.
69. [69] Cader FZ, Vockerodt M, Bose S, et al. The EBV oncogene LMP1 protects lymphoma cells from cell death through the collagenmediated activation of DDR1. Blood, 2013,122:4237-4245.
70. [70] Kamranvar SA, Gruhne B, Szeles A, et al. Epstein-Barr virus promotes genomic instability in Burkitt's lymphoma. Oncogene, 2007,26:5115-5123.
71. [71] Gualandi G, Giselico L, Carloni M, et al. Enhancement of genetic instability in human B cells by Epstein-Barr virus latent infection. Mutagenesis, 2001,16:203-208.
72. [72] Lacoste S, Wiechec E, Dos Santos Silva AG, et al. Chromosomal rearrangements after ex vivo Epstein-Barr virus (EBV) infection of human B cells. Oncogene, 2010,29:503-515.
73. [73] Kamranvar SA, Chen X, Masucci MG. Telomere dysfunction and activation of alternative lengthening of telomeres in B-lymphocytes infected by Epstein-Barr virus. Oncogene, 2013,32:5522-5530.
74. [74] Kuhn-Hallek I, Sage DR, Stein L, et al. Expression of recombination activating genes (RAG-1 and RAG-2) in Epstein-Barr virus-bearing B cells. Blood, 1995,85:1289-1299.
75. [75] Epeldegui M, Hung YP, McQuay A, et al. Infection of human B cells with Epstein-Barr virus results in the expression of somatic hypermutation-inducing molecules and in the accrual of oncogene mutations. Mol Immunol, 2007,44:934-942.
76. [76] Dalldorf G. Lymphomas of African children with different forms or environmental influences. JAMA, 1962,181:1026-1028.
77. [77] Ziegler JL, Beckstead JA, Volberding PA, et al. Non-Hodgkin’s lymphoma in 90 homosexual men. Relation to generalized lymphadenopathy and the acquired immunodeficiency syndrome. N Engl J Med, 1984,311:565-570.
78. [78] Ziegler JL, Drew WL, Miner RC, et al. Outbreak of Burkitt’s-like lymphoma in homosexual men. Lancet, 1982,2:631-633.
79. [79] Wiggill TM, Mantina H, Willem P, et al. Changing pattern of lymphoma subgroups at a tertiary academic complex in a highprevalence HIV setting: a South African perspective. J Acquir Immune Defic Syndr, 2011,56:460-466.
80. [80] O’Conor GT. Persistent immunologic stimulation as a factor in oncogenesis, with special reference to Burkitt’s tumor. Am J Med, 1970,48:279-285.
81. [81] Donati D, Mok B, Chene A, et al. Increased B cell survival an preferential activation of the memory compartment by a malaria polyclonal B cell activator. J Immunol, 2006,177:3035-3044.
82. [82] Rasti N, Falk KI, Donati D, et al. Circulating Epstein-Barr virus in children living in malaria-endemic areas. Scand J Immunol, 2005,61:461-465.
83. [83] Moss DJ, Burrows SR, Castelino DJ, et al. A comparison of Epstein-Barr virus-specific T-cell immunity in malaria-endemic and -nonendemic regions of Papua New Guinea. Int J Cancer, 1983,31:727-732.
84. [84] Urban BC, Ferguson DJ, Pain A, et al. Plasmodium falciparuminfected erythrocytes modulate the maturation of dendritic cells. Nature, 1999,400:73-77.
85. [85] Whittle HC, Brown J, Marsh K, et al. T-cell control of Epstein-Barr virus-infected B cells is lost during P. falciparum malaria. Nature, 1984,312:449-450.
86. [86] Moormann AM, Chelimo K, Sumba PO, et al. Exposure to holoendemic malaria results in suppression of Epstein-Barr virusspecific T cell immunosurveillance in Kenyan children. J Infect Dis, 2007,195:799-808.
87. [87] Moormann AM, Chelimo K, Sumba OP, et al. Exposure to holoendemic malaria results in elevated Epstein-Barr virus loads in children. J Infect Dis, 2005,191:1233-1238.
88. [88] Njie R, Bell AI, Jia H, et al. The effects of acute malaria on Epstein-Barr virus (EBV) load and EBV-specific T cell immunity in Gambian children. J Infect Dis, 2009,199:31-38.
89. [89] Torgbor C, Awuah P, Deitsch K, et al. A multifactorial role for P. falciparum malaria in endemic Burkitt’s lymphoma pathogenesis. PLoS Pathog, 2014,10:e1004170.
90. [90] Rowe M, Khanna R, Jacob CA, et al. Restoration of endogenous antigen processing in Burkitt’s lymphoma cells by Epstein-Barr virus latent membrane protein-1: coordinate upregulation of peptide transporters and HLA-class I antigen expression. Eur J Immunol, 1995,25:1374-1384.
91. [91] Levitskaya J, Sharipo A, Leonchiks A, et al. Inhibition of ubiquitin/proteasome-dependent protein degradation by the Gly-Ala repeat domain of the Epstein-Barr virus nuclear antigen 1. Proc Natl Acad Sci U S A, 1997,94:12616-12621.
92. [92] Shimizu N, Tanabe-Tochikura A, Kuroiwa Y, et al. Isolation of Epstein-Barr virus (EBV)-negative cell clones from the EBV-positive Burkitt’s lymphoma (BL) line Akata: malignant phenotypes of BL cells are dependent on EBV. J Virol, 1994,68:6069-6073.
93. [93] Komano J, Sugiura M, Takada K. Epstein-Barr virus contributes to the malignant phenotype and to apoptosis resistance in Burkitt's lymphoma cell line Akata. J Virol, 1998,72:9150-9156.
94. [94] Ruf IK, Rhyne PW, Yang H, et al. Epstein-barr virus regulates c-MYC, apoptosis, and tumorigenicity in Burkitt lymphoma. Mol Cell Biol, 1999,19:1651-1660.
95. [95] Kennedy G, Komano J, Sugden B. Epstein-Barr virus provides a survival factor to Burkitt’s lymphomas. Proc Natl Acad Sci U S A, 2003,100:14269-14274.
96. [96] Saridakis V, Sheng Y, Sarkari F, 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.
97. [97] Ruf IK, Lackey KA, Warudkar S, et al. Protection from interferoninduced apoptosis by Epstein-Barr virus small RNAs is not mediated by inhibition of PKR. J Virol, 2005,79:14562-14569.
98. [98] Ruf IK, Rhyne PW, Yang C, et al. Epstein-Barr virus small RNAs potentiate tumorigenicity of Burkitt lymphoma cells independently of an effect on apoptosis. J Virol, 2000,74:10223-10228.
99. [99] Komano J, Maruo S, Kurozumi K, et al. Oncogenic role of Epstein-Barr virus-encoded RNAs in Burkitt's lymphoma cell line Akata. J Virol, 1999,73:9827-9831.
100. [100] Vereide DT, Seto E, Chiu YF, et al. Epstein-Barr virus maintains lymphomas via its miRNAs. Oncogene, 2014,33:1258-1264.
101. [101] Kelly GL, Milner AE, Tierney RJ, et al. Epstein-Barr virus nuclear antigen 2 (EBNA2) gene deletion is consistently linked with EBNA3A, -3B, and -3C expression in Burkitt's lymphoma cells and with increased resistance to apoptosis. J Virol, 2005,79:10709-10717.
102. [102] Kelly G, Bell A, Rickinson A. Epstein-Barr virus-associated Burkitt lymphomagenesis selects for downregulation of the nuclear antigen EBNA2. Nat Med, 2002,8:1098-1104.
103. [103] Kelly GL, Long HM, Stylianou J, et al. An Epstein-Barr virus antiapoptotic protein constitutively expressed in transformed cells and implicated in Burkitt lymphomagenesis: the Wp/BHRF1 link. PLoS Pathog, 2009,5:e1000341.
104. [104] Kelly GL, Stylianou J, Rasaiyaah J, et al. Different patterns of Epstein-Barr virus latency in endemic Burkitt lymphoma (BL) lead to distinct variants within the BL-associated gene expression signature. J Virol, 2013,87:2882-2894.
105. [105] Staege MS, Lee SP, Frisan T, et al. MYC overexpression imposes a nonimmunogenic phenotype on Epstein-Barr virus-infected B cells. Proc Natl Acad Sci U S A, 2002,99:4550-4555.
106. [106] Anderton E, Yee J, Smith P, et al. 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, 2008,27:421-433.
107. [107] Feederle R, Linnstaedt SD, Bannert H, et al. A viral microRNA cluster strongly potentiates the transforming properties of a human herpesvirus. PLoS Pathog, 2011,7:e1001294.
108. [108] Pajic A, Staege MS, Dudziak D, et al. Antagonistic effects of c-myc and Epstein-Barr virus latent genes on the phenotype of human B cells. Int J Cancer, 2001,93:810-816.
109. [109] Bellan C, Lazzi S, Hummel M, et al. Immunoglobulin gene analysis reveals 2 distinct cells of origin for EBV-positive and EBV-negative Burkitt lymphomas. Blood, 2005,106:1031-1036.
110. [110] Pelicci PG, Knowles DM, 2nd, Magrath I, et al. Chromosomal breakpoints and structural alterations of the c-myc locus differ in endemic and sporadic forms of Burkitt lymphoma. Proc Natl Acad Sci U S A, 1986,83:2984-2988.
111. [111] Guikema JE, de Boer C, Haralambieva E, et al. IGH switch breakpoints in Burkitt lymphoma: exclusive involvement of noncanonical class switch recombination. Genes Chromosomes Cancer, 2006,45:808-819.
112. [112] Shiramizu B, Barriga F, Neequaye J, et al. Patterns of chromosomal breakpoint locations in Burkitt's lymphoma: relevance to geography and Epstein-Barr virus association. Blood, 1991, 77:1516-1526.
113. [113] Schrader A, Bentink S, Spang R, et al. High Myc activity is an independent negative prognostic factor for diffuse large B cell lymphomas. Int J Cancer, 2012,131:E348-E361.
114. [114] Polack A, Hortnagel K, Pajic A, et al. c-myc activation renders proliferation of Epstein-Barr virus (EBV)-transformed cells independent of EBV nuclear antigen 2 and latent membrane protein 1. Proc Natl Acade Sci U S A, 1996,93:10411-10416.
115. [115] Janz S, Muller J, Shaughnessy J, et al. Detection of recombinations between c-myc and immunoglobulin switch alpha in murine plasma cell tumors and preneoplastic lesions by polymerase chain reaction. Proc Natl Acad Sci U S A, 1993,90:7361-7365.
116. [116] Muller JR, Janz S, Goedert JJ, et al. Persistence of immunoglobulin heavy chain/c-myc recombination-positive lymphocyte clones in the blood of human immunodeficiency virus-infected homosexual men. Proc Natl Acad Sci U S A, 1995,92:6577-6581.
117. [117] Klein G. Dysregulation of lymphocyte proliferation by chromosomal translocations and sequential genetic changes. BioEssays, 2000,22:414-422.
118. [118] Lin CY, Loven J, Rahl PB, et al. Transcriptional amplification in tumor cells with elevated c-Myc. Cell, 2012,151:56-67.
119. [119] McCarthy N. Tumorigenesis: megaphone MYC. Nat Rev Cancer, 2012,12:733.
120. [120] Nie Z, Hu G, Wei G, et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell, 2012,151:68-79.
121. [121] Pelengaris S, Khan M, Evan G. c-MYC: more than just a matter of life and death. Nat Rev Cancer, 2002,2:764-776.
122. [122] Strasser A, Harris AW, Bath ML, et al. Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and bcl-2. Nature, 1990,348:331-333.
123. [123] Michalak EM, Jansen ES, Happo L, et al. Puma and to a lesser extent Noxa are suppressors of Myc-induced lymphomagenesis. Cell Death Differ, 2009,16:684-696.
124. [124] Happo L, Cragg MS, Phipson B, et al. Maximal killing of lymphoma cells by DNA damage-inducing therapy requires not only the p53 targets Puma and Noxa, but also Bim. Blood, 2010,116:5256-5267.
125. [125] Sander S, Calado DP, Srinivasan L, et al. Synergy between PI3K signaling and MYC in Burkitt lymphomagenesis. Cancer Cell, 2012,22:167-179.
126. [126] Blyth K, Terry A, O’Hara M, et al. Synergy between a human c-myc transgene and p53 null genotype in murine thymic lymphomas: contrasting effects of homozygous and heterozygous p53 loss. Oncogene, 1995,10:1717-1723.
127. [127] Jacobs JJ, Scheijen B, Voncken JW, et al. Bmi-1 collaborates with c-Myc in tumorigenesis by inhibiting c-Myc-induced apoptosis via INK4a/ARF. Genes Dev, 1999,13:2678-2690.
128. [128] Eischen CM, Weber JD, Roussel MF, et al. Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes Dev, 1999,13:2658-2669.
129. [129] Drotar ME, Silva S, Barone E, et al. Epstein-Barr virus nuclear antigen-1 and Myc cooperate in lymphomagenesis. Int J Cancer, 2003,106:388-395.
130. [130] Farrell PJ, Allan GJ, Shanahan F, et al. p53 is frequently mutated in Burkitt’s lymphoma cell lines. EMBO J, 1991,10:2879-2887.
131. [131] Gaidano G, Ballerini P, Gong JZ, et al. p53 mutations in human lymphoid malignancies: association with Burkitt lymphoma and chronic lymphocytic leukemia. Proc Natl Acad Sci U S A, 1991,88:5413-5417.
132. [132] Wiman KG, Magnusson KP, Ramqvist T, et al. Mutant p53 detected in a majority of Burkitt lymphoma cell lines by monoclonal antibody PAb240. Oncogene, 1991,6:1633-1639.
133. [133] Bhatia KG, Gutierrez MI, Huppi K, et al. The pattern of p53 mutations in Burkitt’s lymphoma differs from that of solid tumors. Cancer Res, 1992,52:4273-4276.
134. [134] Preudhomme C, Dervite I, Wattel E, et al. Clinical significance of p53 mutations in newly diagnosed Burkitt’s lymphoma and acute lymphoblastic leukemia: a report of 48 cases. J Clin Oncol, 1995,13:812-820.
135. [135] Lindstrom MS, Wiman KG. Role of genetic and epigenetic changes in Burkitt lymphoma. Semin Cancer Biol, 2002,12:381-387.
136. [136] Schmitz R, Young RM, Ceribelli M, et al. Burkitt lymphoma pathogenesis and therapeutic targets from structural and functional genomics. Nature, 2012,490:116-120.
137. [137] Richter J, Schlesner M, Hoffmann S, et al. Recurrent mutation of the ID3 gene in Burkitt lymphoma identified by integrated genome, exome and transcriptome sequencing. Nat Genet, 2012,44:1316-1320.
138. [138] Love C, Sun Z, Jima D, et al. The genetic landscape of mutations in Burkitt lymphoma. Nat Genet, 2012,44:1321-1325.
139. [139] Johnston JM, Carroll WL. c-myc hypermutation in Burkitt’s lymphoma. Leuk Lymphoma, 1992,8:431-439.
140. [140] Cowling VH, Turner SA, Cole MD. Burkitt’s lymphoma-associated c-Myc mutations converge on a dramatically altered target gene response and implicate Nol5a/Nop56 in oncogenesis. Oncogene, 2014,33:3519-3527.
141. [141] Seitz V, Butzhammer P, Hirsch B, et al. Deep sequencing of MYC DNA-binding sites in Burkitt lymphoma. PLoS One, 2011,6:e26837.
142. [142] Burkitt D. Long-term remissions following one and two-dose chemotherapy for African lymphoma. Cancer, 1967,20:756-759.
143. [143] Ferry JA. Burkitt's lymphoma: clinicopathologic features and differential diagnosis. Oncologist, 2006,11:375-383.
144. [144] Oriol A, Ribera JM, Bergua J, et al. High-dose chemotherapy and immunotherapy in adult Burkitt lymphoma: comparison of results in human immunodeficiency virus-infected and noninfected patients. Cancer, 2008,113:117-125.
145. [145] Ngoma T, Adde M, Durosinmi M, et al. Treatment of Burkitt lymphoma in equatorial Africa using a simple three-drug combination followed by a salvage regimen for patients with persistent or recurrent disease. Br J Haematol, 2012,158:749-762.
146. [146] Magrath I. Towards curative therapy in Burkitt lymphoma: the role of early African studies in demonstrating the value of combination therapy and CNS prophylaxis. Adv Hematol, 2012,2012:130680.
147. [147] Appelbaum FR, Deisseroth AB, Graw RG Jr, et al. Prolonged complete remission following high dose chemotherapy of Burkitt's lymphoma in relapse. Cancer, 1978,41:1059-1063.
148. [148] Thomas DA, Faderl S, O'Brien S, et al. Chemoimmunotherapy with hyper-CVAD plus rituximab for the treatment of adult Burkitt and Burkitt-type lymphoma or acute lymphoblastic leukemia. Cancer, 2006,106:1569-1580.
149. [149] Molyneux EM, Rochford R, Griffin B, et al. Burkitt's lymphoma. Lancet, 2012,379:1234-1244.
150. [150] Vita M, Henriksson M. The Myc oncoprotein as a therapeutic target for human cancer. Semin Cancer Biol, 2006,16:318-330.
151. [151] Mertz JA, Conery AR, Bryant BM, et al. Targeting MYC dependence in cancer by inhibiting BET bromodomains. Proc Natl Acad Sci U S A, 2011,108:16669-16674.
152. [152] Soucek L, Whitfield J, Martins CP, et al. Modelling Myc inhibition as a cancer therapy. Nature, 2008,455:679-683.
153. [153] Rodon J, Dienstmann R, Serra V, et al. Development of PI3K inhibitors: lessons learned from early clinical trials. Nat Rev Clin Oncol, 2013,10:143-153.
154. [154] Kauffmann-Zeh A, Rodriguez-Viciana P, Ulrich E, et al. Suppression of c-Myc-induced apoptosis by Ras signaling through PI(3)K and PKB. Nature, 1997,385:544-548.
155. [155] Brennan P, Mehl AM, Jones M, et al. Phosphatidylinositol 3-kinase is essential for the proliferation of lymphoblastoid cells. Oncogene, 2002,21:1263-1271.
156. [156] Kelly GL, Grabow S, Glaser SP, et al. Targeting of MCL-1 kills MYC-driven mouse and human lymphomas even when they bear mutations in p53. Genes Dev, 2014,28:58-70.
157. [157] Lessene G, Czabotar PE, Colman PM. BCL-2 family antagonists for cancer therapy. Nat Rev Drug Discov, 2008,7:989-1000.
158. [158] Li N, Thompson S, Schultz DC, et al. Discovery of selective inhibitors against EBNA1 via high throughput in silico virtual screening. PLoS One, 2010,5:e10126.
159. [159] Kelly GL, Rickinson AB. Burkitt lymphoma: revisiting the pathogenesis of a virus-associated malignancy. Hematol Am Soc Hematol Educ Program, 2007,2007:277-284.