Interaction of Epstein-Barr virus (EBV) with human B-lymphocytes

Biochemical and Biophysical Research Communications

Volumn 396, Issue 1, 2010, Pages 67-73

  Klein, George ^a   Klein, Eva ^a   Kashuba, Elena ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Apoptosis; Burkitt lymphoma; Cell cycle control; Cell transformation; EBNA; Epstein Barr virus; Protein protein interaction

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; CD23 ANTIGEN; CHECKPOINT KINASE 2; COMPLEMENT COMPONENT C3D RECEPTOR; CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 2A; EPSTEIN BARR VIRUS ANTIGEN 1; EPSTEIN BARR VIRUS ANTIGEN 2; HEAT SHOCK PROTEIN 70; HISTONE DEACETYLASE 1; INTERLEUKIN 2 RECEPTOR ALPHA; JAGGED1; LATENT MEMBRANE PROTEIN 1; LATENT MEMBRANE PROTEIN 2; MYC PROTEIN; NOTCH1 RECEPTOR; NOTCH2 RECEPTOR; NOTCH3 RECEPTOR; NOTCH4 RECEPTOR; NUCLEAR RECEPTOR COREPRESSOR; OCTAMER TRANSCRIPTION FACTOR 2; PROTEIN MDM2; PROTEIN P53; RETINOBLASTOMA PROTEIN; SURVIVAL MOTOR NEURON PROTEIN 1; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR PAX5; TRANSCRIPTION FACTOR PU 1;

ARTICLE; B LYMPHOCYTE; BURKITT LYMPHOMA; CELL IMMORTALIZATION; CELL SURVIVAL; EPSTEIN BARR VIRUS; GENE EXPRESSION; HUMAN; LYMPHOCYTE PROLIFERATION; MALIGNANT TRANSFORMATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; TUMOR PROMOTION; VIRUS CARCINOGENESIS; VIRUS CELL INTERACTION; VIRUS GENOME;

B-LYMPHOCYTES; BURKITT LYMPHOMA; CELL CYCLE; E2F1 TRANSCRIPTION FACTOR; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 4, HUMAN; HUMANS; RETINOBLASTOMA PROTEIN; TUMOR SUPPRESSOR PROTEIN P53;

HUMAN HERPESVIRUS 4; PRIMATES;

EID: 77952300025     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2010.02.146     Document Type: Article

References (100)

1. E. Klein, G. Klein (Ed.), Burkitt lymphoma, Semin. Cancer Biol. 19 (6) (2009).
2. Pope J.H., Scott W., and Moss D.J. Human lymphoid cell transformation by Epstein-Barr virus. Nat. New Biol. 246 (1973) 140-141
3. Henle G., Henle W., and Diehl V. Relation of Burkitt's tumor-associated herpes-type virus to infectious mononucleosis. Proc. Natl. Acad. Sci. USA 59 (1968) 94-101
4. Siemer D., Kurth J., Lang S., Lehnerdt G., Stanelle J., and Kuppers R. EBV transformation overrides gene expression patterns of B cell differentiation stages. Mol. Immunol. 45 (2008) 3133-3141
5. Reedman B.M., and Klein G. Cellular localization of an Epstein-Barr virus (EBV)-associated complement-fixing antigen in producer and non-producer lymphoblastoid cell lines. Int. J. Cancer 11 (1973) 499-520
6. Hammerschmidt W., and Sugden B. Genetic analysis of immortalizing functions of Epstein-Barr virus in human B lymphocytes. Nature 340 (1989) 393-397
7. Cohen J.I., Wang F., Mannick J., and Kieff E. Epstein-Barr virus nuclear protein 2 is a key determinant of lymphocyte transformation. Proc. Natl. Acad. Sci. USA 86 (1989) 9558-9562
8. Tomkinson B., Robertson E., and Kieff E. Epstein-Barr virus nuclear proteins EBNA-3A and EBNA-3C are essential for B-lymphocyte growth transformation. J. Virol. 67 (1993) 2014-2025
9. Kempkes B., Pich D., Zeidler R., Sugden B., and Hammerschmidt W. Immortalization of human B lymphocytes by a plasmid containing 71 kilobase pairs of Epstein-Barr virus DNA. J. Virol. 69 (1995) 231-238
10. Kempkes B., Spitkovsky D., Jansen-Durr P., Ellwart J.W., Kremmer E., Delecluse H.J., Rottenberger C., Bornkamm G.W., and Hammerschmidt W. B-cell proliferation and induction of early G1-regulating proteins by Epstein-Barr virus mutants conditional for EBNA2. EMBO J. 14 (1995) 88-96
11. Mannick J.B., Cohen J.I., Birkenbach M., Marchini A., and Kieff E. The Epstein-Barr virus nuclear protein encoded by the leader of the EBNA RNAs is important in B-lymphocyte transformation. J. Virol. 65 (1991) 6826-6837
12. Kaye K.M., Izumi K.M., and Kieff E. Epstein-Barr virus latent membrane protein 1 is essential for B-lymphocyte growth transformation. Proc. Natl. Acad. Sci. USA 90 (1993) 9150-9154
13. Rawlins D.R., Milman G., Hayward S.D., and Hayward G.S. Sequence-specific DNA binding of the Epstein-Barr virus nuclear antigen (EBNA-1) to clustered sites in the plasmid maintenance region. Cell 42 (1985) 859-868
14. Jones C.H., Hayward S.D., and Rawlins D.R. Interaction of the lymphocyte-derived Epstein-Barr virus nuclear antigen EBNA-1 with its DNA-binding sites. J. Virol. 63 (1989) 101-110
15. Yates J., Warren N., Reisman D., and Sugden B. A cis-acting element from the Epstein-Barr viral genome that permits stable replication of recombinant plasmids in latently infected cells. Proc. Natl. Acad. Sci. USA 81 (1984) 3806-3810
16. Reisman D., and Sugden B. Trans activation of an Epstein-Barr viral transcriptional enhancer by the Epstein-Barr viral nuclear antigen 1. Mol. Cell. Biol. 6 (1986) 3838-3846
17. Kennedy G., and Sugden B. EBNA-1, a bifunctional transcriptional activator. Mol. Cell. Biol. 23 (2003) 6901-6908
18. Altmann M., Pich D., Ruiss R., Wang J., Sugden B., and Hammerschmidt W. Transcriptional activation by EBV nuclear antigen 1 is essential for the expression of EBV's transforming genes. Proc. Natl. Acad. Sci. USA 103 (2006) 14188-14193
19. Shire K., Ceccarelli D.F., Avolio-Hunter T.M., and Frappier L. EBP2, a human protein that interacts with sequences of the Epstein-Barr virus nuclear antigen 1 important for plasmid maintenance. J. Virol. 73 (1999) 2587-2595
20. Wu H., Kapoor P., and Frappier L. Separation of the DNA replication, segregation, and transcriptional activation functions of Epstein-Barr nuclear antigen 1. J. Virol. 76 (2002) 2480-2490
21. Kapoor P., Lavoie B.D., and Frappier L. EBP2 plays a key role in Epstein-Barr virus mitotic segregation and is regulated by aurora family kinases. Mol. Cell. Biol. 25 (2005) 4934-4945
22. Sears J., Ujihara M., Wong S., Ott C., Middeldorp J., and Aiyar A. The amino terminus of Epstein-Barr Virus (EBV) nuclear antigen 1 contains AT hooks that facilitate the replication and partitioning of latent EBV genomes by tethering them to cellular chromosomes. J. Virol. 78 (2004) 11487-11505
23. Komano J., Sugiura M., and Takada K. Epstein-Barr virus contributes to the malignant phenotype and to apoptosis resistance in Burkitt's lymphoma cell line Akata. J. Virol. 72 (1998) 9150-9156
24. Kennedy G., Komano J., and Sugden B. Epstein-Barr virus provides a survival factor to Burkitt's lymphomas. Proc. Natl. Acad. Sci. USA 100 (2003) 14269-14274
25. Holowaty M.N., Zeghouf M., Wu H., Tellam J., Athanasopoulos V., Greenblatt J., and Frappier L. Protein profiling with Epstein-Barr nuclear antigen-1 reveals an interaction with the herpesvirus-associated ubiquitin-specific protease HAUSP/USP7. J. Biol. Chem. 278 (2003) 29987-29994
26. Fischer N., Kremmer E., Lautscham G., Mueller-Lantzsch N., and Grasser F.A. Epstein-Barr virus nuclear antigen 1 forms a complex with the nuclear transporter karyopherin alpha2. J. Biol. Chem. 272 (1997) 3999-4005
27. Ito S., Ikeda M., Kato N., Matsumoto A., Ishikawa Y., Kumakubo S., and Yanagi K. Epstein-Barr virus nuclear antigen-1 binds to nuclear transporter karyopherin alpha1/NPI-1 in addition to karyopherin alpha2/Rch1. Virology 266 (2000) 110-119
28. Kim A.L., Maher M., Hayman J.B., Ozer J., Zerby D., Yates J.L., and Lieberman P.M. An imperfect correlation between DNA replication activity of Epstein-Barr virus nuclear antigen 1 (EBNA1) and binding to the nuclear import receptor, Rch1/importin alpha. Virology 239 (1997) 340-351
29. Zhang D., Frappier L., Gibbs E., Hurwitz J., and O'Donnell M. Human RPA (hSSB) interacts with EBNA1, the latent origin binding protein of Epstein-Barr virus. Nucleic Acids Res. 26 (1998) 631-637
30. Murakami M., Lan K., Subramanian C., and Robertson E.S. Epstein-Barr virus nuclear antigen 1 interacts with Nm23-H1 in lymphoblastoid cell lines and inhibits its ability to suppress cell migration. J. Virol. 79 (2005) 1559-1568
31. Lin A., Wang S., Nguyen T., Shire K., and Frappier L. The EBNA1 protein of Epstein-Barr virus functionally interacts with Brd4. J. Virol. 82 (2008) 12009-12019
32. Henkel T., Ling P.D., Hayward S.D., and Peterson M.G. Mediation of Epstein-Barr virus EBNA2 transactivation by recombination signal-binding protein J kappa. Science 265 (1994) 92-95
33. Johannsen E., Koh E., Mosialos G., Tong X., Kieff E., and Grossman S.R. Epstein-Barr virus nuclear protein 2 transactivation of the latent membrane protein 1 promoter is mediated by J kappa and PU.1. J. Virol. 69 (1995) 253-262
34. Wu D.Y., Kalpana G.V., Goff S.P., and Schubach W.H. Epstein-Barr virus nuclear protein 2 (EBNA2) binds to a component of the human SNF-SWI complex, hSNF5/Ini1. J. Virol. 70 (1996) 6020-6028
35. Grossman S.R., Johannsen E., Tong X., Yalamanchili R., and Kieff E. The Epstein-Barr virus nuclear antigen 2 transactivator is directed to response elements by the J kappa recombination signal binding protein. Proc. Natl. Acad. Sci. USA 91 (1994) 7568-7572
36. Barth S., Liss M., Voss M.D., Dobner T., Fischer U., Meister G., and Grasser F.A. Epstein-Barr virus nuclear antigen 2 binds via its methylated arginine-glycine repeat to the survival motor neuron protein. J. Virol. 77 (2003) 5008-5013
37. Tong X., Drapkin R., Yalamanchili R., Mosialos G., and Kieff E. The Epstein-Barr virus nuclear protein 2 acidic domain forms a complex with a novel cellular coactivator that can interact with TFIIE. Mol. Cell. Biol. 15 (1995) 4735-4744
38. Wang L., Grossman S.R., and Kieff E. Epstein-Barr virus nuclear protein 2 interacts with p300, CBP, and PCAF histone acetyltransferases in activation of the LMP1 promoter. Proc. Natl. Acad. Sci. USA 97 (2000) 430-435
39. Lee J.M., Lee K.H., Farrell C.J., Ling P.D., Kempkes B., Park J.H., and Hayward S.D. EBNA2 is required for protection of latently Epstein-Barr virus-infected B cells against specific apoptotic stimuli. J. Virol. 78 (2004) 12694-12697
40. Robertson E.S., Grossman S., Johannsen E., Miller C., Lin J., Tomkinson B., and Kieff E. Epstein-Barr virus nuclear protein 3C modulates transcription through interaction with the sequence-specific DNA-binding protein J kappa. J. Virol. 69 (1995) 3108-3116
41. Krauer K.G., Kienzle N., Young D.B., and Sculley T.B. Epstein-Barr nuclear antigen-3 and -4 interact with RBP-2N, a major isoform of RBP-J kappa in B lymphocytes. Virology 226 (1996) 346-353
42. Krauer K.G., Burgess A., Buck M., Flanagan J., Sculley T.B., and Gabrielli B. The EBNA-3 gene family proteins disrupt the G2/M checkpoint. Oncogene 23 (2004) 1342-1353
43. Kashuba E., Kashuba V., Pokrovskaja K., Klein G., and Szekely L. Epstein-Barr virus encoded nuclear protein EBNA-3 binds XAP-2, a protein associated with hepatitis B virus X antigen. Oncogene 19 (2000) 1801-1806
44. Kashuba E., Pokrovskaja K., Klein G., and Szekely L. Epstein-Barr virus-encoded nuclear protein EBNA-3 interacts with the epsilon-subunit of the T-complex protein 1 chaperonin complex. J. Hum. Virol. 2 (1999) 33-37
45. Kashuba E.V., Gradin K., Isaguliants M., Szekely L., Poellinger L., Klein G., and Kazlauskas A. Regulation of transactivation function of the aryl hydrocarbon receptor by the Epstein-Barr virus-encoded EBNA-3 protein. J. Biol. Chem. 281 (2006) 1215-1223
46. Kashuba E., Kashuba V., Sandalova T., Klein G., and Szekely L. Epstein-Barr virus encoded nuclear protein EBNA-3 binds a novel human uridine kinase/uracil phosphoribosyltransferase. BMC Cell Biol. 3 (2002) 23
47. Mannick J.B., Tong X., Hemnes A., and Kieff E. The Epstein-Barr virus nuclear antigen leader protein associates with hsp72/hsc73. J. Virol. 69 (1995) 8169-8172
48. Kawaguchi Y., Nakajima K., Igarashi M., Morita T., Tanaka M., Suzuki M., Yokoyama A., Matsuda G., Kato K., Kanamori M., and Hirai K. Interaction of Epstein-Barr virus nuclear antigen leader protein (EBNA-LP) with HS1-associated protein X-1: implication of cytoplasmic function of EBNA-LP. J. Virol. 74 (2000) 10104-10111
49. Han I., Harada S., Weaver D., Xue Y., Lane W., Orstavik S., Skalhegg B., and Kieff E. EBNA-LP associates with cellular proteins including DNA-PK and HA95. J. Virol. 75 (2001) 2475-2481
50. Kashuba E., Mattsson K., Pokrovskaja K., Kiss C., Protopopova M., Ehlin-Henriksson B., Klein G., and Szekely L. EBV-encoded EBNA-5 associates with P14ARF in extranucleolar inclusions and prolongs the survival of P14ARF-expressing cells. Int. J. Cancer 105 (2003) 644-653
51. Kashuba E., Yurchenko M., Szirak K., Stahl J., Klein G., and Szekely L. Epstein-Barr virus-encoded EBNA-5 binds to Epstein-Barr virus-induced Fte1/S3a protein. Exp. Cell Res. 303 (2005) 47-55
52. Portal D., Rosendorff A., and Kieff E. Epstein-Barr nuclear antigen leader protein coactivates transcription through interaction with histone deacetylase 4. Proc. Natl. Acad. Sci. USA 103 (2006) 19278-19283
53. Echendu C.W., and Ling P.D. Regulation of Sp100A subnuclear localization and transcriptional function by EBNA-LP and interferon. J. Interferon Cytokine Res. 28 (2008) 667-678
54. Touitou R., Hickabottom M., Parker G., Crook T., and Allday M.J. Physical and functional interactions between the corepressor CtBP and the Epstein-Barr virus nuclear antigen EBNA3C. J. Virol. 75 (2001) 7749-7755
55. Radkov S.A., Touitou R., Brehm A., Rowe M., West M., Kouzarides T., and Allday M.J. Epstein-Barr virus nuclear antigen 3C interacts with histone deacetylase to repress transcription. J. Virol. 73 (1999) 5688-5697
56. Knight J.S., Lan K., Subramanian C., and Robertson E.S. Epstein-Barr virus nuclear antigen 3C recruits histone deacetylase activity and associates with the corepressors mSin3A and NCoR in human B-cell lines. J. Virol. 77 (2003) 4261-4272
57. Cotter II M.A., and Robertson E.S. Modulation of histone acetyltransferase activity through interaction of epstein-barr nuclear antigen 3C with prothymosin alpha. Mol. Cell. Biol. 20 (2000) 5722-5735
58. Grundhoff A.T., Kremmer E., Tureci O., Glieden A., Gindorf C., Atz J., Mueller-Lantzsch N., Schubach W.H., and Grasser F.A. Characterization of DP103, a novel DEAD box protein that binds to the Epstein-Barr virus nuclear proteins EBNA2 and EBNA3C. J. Biol. Chem. 274 (1999) 19136-19144
59. Krauer K.G., Buck M., Belzer D.K., Flanagan J., Chojnowski G.M., and Sculley T.B. The Epstein-Barr virus nuclear antigen-6 protein co-localizes with EBNA-3 and survival of motor neurons protein. Virology 318 (2004) 280-294
60. Knight J.S., and Robertson E.S. Epstein-Barr virus nuclear antigen 3C regulates cyclin A/p27 complexes and enhances cyclin A-dependent kinase activity. J. Virol. 78 (2004) 1981-1991
61. Knight J.S., Sharma N., and Robertson E.S. SCFSkp2 complex targeted by Epstein-Barr virus essential nuclear antigen. Mol. Cell. Biol. 25 (2005) 1749-1763
62. Subramanian C., Cotter II M.A., and Robertson E.S. Epstein-Barr virus nuclear protein EBNA-3C interacts with the human metastatic suppressor Nm23-H1: a molecular link to cancer metastasis. Nat. Med. 7 (2001) 350-355
63. Kashuba E., Yurchenko M., Yenamandra S.P., Snopok B., Isaguliants M., Szekely L., and Klein G. EBV-encoded EBNA-6 binds and targets MRS18-2 to the nucleus, resulting in the disruption of pRb-E2F1 complexes. Proc. Natl. Acad. Sci. USA 105 (2008) 5489-5494
64. Saha A., Murakami M., Kumar P., Bajaj B., Sims K., and Robertson E.S. Epstein-Barr virus nuclear antigen 3C augments Mdm2-mediated p53 ubiquitination and degradation by deubiquitinating Mdm2. J. Virol. 83 (2009) 4652-4669
65. Yalamanchili R., Tong X., Grossman S., Johannsen E., Mosialos G., and Kieff E. Genetic and biochemical evidence that EBNA 2 interaction with a 63-kDa cellular GTG-binding protein is essential for B lymphocyte growth transformation by EBV. Virology 204 (1994) 634-641
66. Kieff E., and Rikinson A. Epstein-Barr virus and its replication. In: Knipe D.M., Fields B.N., and Howley P.M. (Eds). Fields Virology (2007), Lippincott-Williams & Wilkins Publishers, Philadelphia 2603-2654
67. Sinclair A.J., Palmero I., Peters G., and 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. EMBO J. 13 (1994) 3321-3328
68. L.L. Kis, D. Salamon, E.K. Persson, N. Nagy, F.A. Scheeren, H. Spits, G. Klein, E. Klein, IL-21 imposes a type II EBV gene expression on type III and type I B cells by the repression of C- and activation of LMP-1-promoter, Proc. Natl. Acad. Sci. USA 107 (2010) 872-877.
69. Seto E.S., Bellen H.J., and Lloyd T.E. When cell biology meets development: endocytic regulation of signaling pathways. Genes Dev. 16 (2002) 1314-1336
70. Allman D., Punt J.A., Izon D.J., Aster J.C., and Pear W.S. An invitation to T and more: notch signaling in lymphopoiesis. Cell 109 Suppl. (2002) S1-S11
71. Kienzle N., Young D.B., Liaskou D., Buck M., Greco S., and Sculley T.B. Intron retention may regulate expression of Epstein-Barr virus nuclear antigen 3 family genes. J. Virol. 73 (1999) 1195-1204
72. Marshall D., and Sample C. Epstein-Barr virus nuclear antigen 3C is a transcriptional regulator. J. Virol. 69 (1995) 3624-3630
73. Lin J., Johannsen E., Robertson E., and Kieff E. Epstein-Barr virus nuclear antigen 3C putative repression domain mediates coactivation of the LMP1 promoter with EBNA-2. J. Virol. 76 (2002) 232-242
74. Kuzhandaivelu N., Cong Y.S., Inouye C., Yang W.M., and Seto E. XAP2, a novel hepatitis B virus X-associated protein that inhibits X transactivation. Nucleic Acids Res. 24 (1996) 4741-4750
75. Maruo S., Johannsen E., Illanes D., Cooper A., and Kieff E. Epstein-Barr virus nuclear protein EBNA3A is critical for maintaining lymphoblastoid cell line growth. J. Virol. 77 (2003) 10437-10447
76. Hertle M.L., Popp C., Petermann S., Maier S., Kremmer E., Lang R., Mages J., and Kempkes B. Differential gene expression patterns of EBV infected EBNA-3A positive and negative human B lymphocytes. PLoS Pathog. 5 (2009) e1000506
77. Parker G.A., Touitou R., and Allday M.J. Epstein-Barr virus EBNA3C can disrupt multiple cell cycle checkpoints and induce nuclear division divorced from cytokinesis. Oncogene 19 (2000) 700-709
78. Knight J.S., Sharma N., and Robertson E.S. 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 (2005) 18562-18566
79. Maruo S., Wu Y., Ishikawa S., Kanda T., Iwakiri D., and Takada K. Epstein-Barr virus nuclear protein EBNA3C is required for cell cycle progression and growth maintenance of lymphoblastoid cells. Proc. Natl. Acad. Sci. USA 103 (2006) 19500-19505
80. Harada S., and Kieff E. Epstein-Barr virus nuclear protein LP stimulates EBNA-2 acidic domain-mediated transcriptional activation. J. Virol. 71 (1997) 6611-6618
81. Nitsche F., Bell A., and Rickinson A. Epstein-Barr virus leader protein enhances EBNA-2-mediated transactivation of latent membrane protein 1 expression: a role for the W1W2 repeat domain. J. Virol. 71 (1997) 6619-6628
82. Ling P.D., Peng R.S., Nakajima A., Yu J.H., Tan J., Moses S.M., Yang W.H., Zhao B., Kieff E., Bloch K.D., and Bloch D.B. Mediation of Epstein-Barr virus EBNA-LP transcriptional coactivation by Sp100. EMBO J. 24 (2005) 3565-3575
83. Szekely L., Pokrovskaja K., Jiang W.Q., de The H., Ringertz N., and Klein G. The Epstein-Barr virus-encoded nuclear antigen EBNA-5 accumulates in PML-containing bodies. J. Virol. 70 (1996) 2562-2568
84. Szekely L., Jiang W.Q., Pokrovskaja K., Wiman K.G., Klein G., and Ringertz N. Reversible nucleolar translocation of Epstein-Barr virus-encoded EBNA-5 and hsp70 proteins after exposure to heat shock or cell density congestion. J. Gen. Virol. 76 Pt. 10 (1995) 2423-2432
85. Pokrovskaja K., Mattsson K., Kashuba E., Klein G., and Szekely L. Proteasome inhibitor induces nucleolar translocation of Epstein-Barr virus-encoded EBNA-5. J. Gen. Virol. 82 (2001) 345-358
86. Mattsson K., Pokrovskaja K., Kiss C., Klein G., and Szekely L. Proteins associated with the promyelocytic leukemia gene product (PML)-containing nuclear body move to the nucleolus upon inhibition of proteasome-dependent protein degradation. Proc. Natl. Acad. Sci. USA 98 (2001) 1012-1017
87. Kashuba E., Mattsson K., Klein G., and Szekely L. P14ARF induces the relocation of HDM2 and p53 to extranucleolar sites that are targeted by PML bodies and proteasomes. Mol. Cancer 2 (2003) 18
88. Allday M.J., Inman G.J., Crawford D.H., and Farrell P.J. DNA damage in human B cells can induce apoptosis, proceeding from G1/S when p53 is transactivation competent and G2/M when it is transactivation defective. EMBO J. 14 (1995) 4994-5005
89. Pokrovskaja K., Okan I., Kashuba E., Lowbeer M., Klein G., and Szekely L. Epstein-Barr virus infection and mitogen stimulation of normal B cells induces wild-type p53 without subsequent growth arrest or apoptosis. J. Gen. Virol. 80 Pt. 4 (1999) 987-995
90. Snopok B., Yurchenko M., Szekely L., Klein G., and Kashuba E. SPR-based immunocapture approach to creating an interfacial sensing architecture: mapping of the MRS18-2 binding site on retinoblastoma protein. Anal. Bioanal. Chem. 386 (2006) 2063-2073
91. Muller J.R., Janz S., Goedert J.J., Potter M., and Rabkin C.S. 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. USA 92 (1995) 6577-6581
92. Evan G.I., Wyllie A.H., Gilbert C.S., Littlewood T.D., Land H., Brooks M., Waters C.M., Penn L.Z., and Hancock D.C. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69 (1992) 119-128
93. Shimizu N., Tanabe-Tochikura A., Kuroiwa Y., and Takada K. 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. 68 (1994) 6069-6073
94. Nagy N., Maeda A., Bandobashi K., Kis L.L., Nishikawa J., Trivedi P., Faggioni A., Klein G., and Klein E. SH2D1A expression in Burkitt lymphoma cells is restricted to EBV positive group I lines and is downregulated in parallel with immunoblastic transformation. Int. J. Cancer 100 (2002) 433-440
95. Purtilo D.T., Cassel C.K., Yang J.P., and Harper R. X-linked recessive progressive combined variable immunodeficiency (Duncan's disease). Lancet 1 (1975) 935-940
96. Nichols K.E., Harkin D.P., Levitz S., Krainer M., Kolquist K.A., Genovese C., Bernard A., Ferguson M., Zuo L., Snyder E., Buckler A.J., Wise C., Ashley J., Lovett M., Valentine M.B., Look A.T., Gerald W., Housman D.E., and Haber D.A. Inactivating mutations in an SH2 domain-encoding gene in X-linked lymphoproliferative syndrome. Proc. Natl. Acad. Sci. USA 95 (1998) 13765-13770
97. Sayos J., Wu C., Morra M., Wang N., Zhang X., Allen D., Van Schaik S., Notarangelo L., Geha R., Roncarolo M.G., Oettgen H., De Vries J.E., Aversa G., and Terhorst C. The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature 395 (1998) 462-469
98. Nagy N., Matskova L., Kis L.L., Hellman U., Klein G., and Klein E. The proapoptotic function of SAP provides a clue to the clinical picture of X-linked lymphoproliferative disease. Proc. Natl. Acad. Sci. USA 106 (2009) 11966-11971
99. Nagy N., Klein G., and Klein E. To the genesis of Burkitt lymphoma: regulation of apoptosis by EBNA-1 and SAP may determine the fate of Ig-myc translocation carrying B lymphocytes. Semin. Cancer Biol. 19 (2009) 407-410
100. Bellan C., Lazzi S., Hummel M., Palummo N., de Santi M., Amato T., Nyagol J., Sabattini E., Lazure T., Pileri S.A., Raphael M., Stein H., Tosi P., and Leoncini L. Immunoglobulin gene analysis reveals 2 distinct cells of origin for EBV-positive and EBV-negative Burkitt lymphomas. Blood 106 (2005) 1031-1036