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Pathogenicity of Human Herpesviruses due to Specific Pathogenicity Genes pp 283–297Cite as

Gene Expression in Burkitt’s Lymphoma Cells

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Part of the book series: Frontiers of Virology ((FRVIROLOGY,volume 3))

Summary

Development of Burkitt’s lymphoma involves translocation of the c-myc protooncogene to one of the immunoglobulin loci and other genetic changes which may include changes to the pim-1, c-fps/c-fes and p53 genes. Epstein-Barr virus is linked to endemic Burkitt’s lymphoma but Epstein-Barr virus gene expression in Burkitt’s lymphoma differs from that in B lymphocytes immortalised by Epstein-Barr virus. Only the EBNA-1 and EBER RNA genes of Epstein-Barr virus are expressed in Burkitt’s lymphoma cells. This restriction of virus gene expression may be a mechanism of evasion of immune surveillance and points to a role for the EBNA-1 gene in growth of Burkitt’s lymphoma cells.

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References

  • Adams JM, Harris AW, Pinkert CA, Corcoran LM, Alexander WS, Cory S, Palmiter RD, Brinster RL (1985) The c-myc oncogene driven by immunoglobulin enhancers induce lymphoid malignancy in trangenic mice. Nature 318: 533–538

    Article  PubMed  CAS  Google Scholar 

  • Bentley DL, Groudine M (1986) A block to elongation is largely responsible for decreased transcription of c-myc in differentiated HL60 cells. Nature 312: 702–706

    Article  Google Scholar 

  • Bentley DL, Groudine M (1988) Sequence requirements for premature termination of transcription in the human c-myc gene. Cell 53: 245–256

    Article  PubMed  CAS  Google Scholar 

  • Brown NA, Liu CR, Wang YF, Garcia CR (1988) B-cell lymphoproliferation and lymphomagenesis are associated with clonotypic intracellular terminal regions of the Epstein-Barr virus. J Virol 62: 962

    PubMed  CAS  Google Scholar 

  • Burkitt D (1983) The discovery of Burkitt’s lymphoma. Cancer 51: 1777–1786

    Article  PubMed  CAS  Google Scholar 

  • Cohen JH, Revillard JP, Magaud JP, Lenoir G, Vuillaume M, Mane AM, Vincent C, Bryon PA (1987) B-cell mutation stage of Burkitt’s lymphoma cell lines according to Epstein-Barr virus status and type of chromosome translocations. J Natl Cancer Inst 78: 235–242

    PubMed  CAS  Google Scholar 

  • Cohen JI, Wang F, Mannick J, Kieff E (1989) Epstein-Barr virus nuclear protein 2 is a key determinant of lymphocyte transformation. Proc Natl Acad Sci USA 86: 9558–9562

    Article  PubMed  CAS  Google Scholar 

  • de-Thè G (1982) Epidemiological of Epstein-Barr virus and associated diseases in man. In: Roizman B (ed) The herpesviruses vol 1. Plenum, New York, pp 25–104

    Google Scholar 

  • de-Thé G, Geser A, Day NE, Tukei PM, Williams EH, Beni DP, Smith PG, Dean AG, Bornkamm GW, Feorino P, Henle W (1978) Epidemiological evidence for a causal relationship between Epstein-Barr virus and Burkitt’s lymphoma: results of the Ugandan prospective study. Nature 274: 756–761

    Article  PubMed  Google Scholar 

  • Eick D, Bornkamm GW (1986) Transcriptional arrest within the first exon is a fast control mechanism in c-myc gene expression. Nucleic Acids Res 14: 8331–8346

    Article  PubMed  CAS  Google Scholar 

  • Eick D, Polack A, Kofler E, Lenoir GM, Rickinson AB, Bornkamm GW (1990) Expression of P0- and P3-RNA from the normal and translocated c-myc allele in Burkitt’s lymphoma cells. Oncogene 5: 1397–1402

    PubMed  CAS  Google Scholar 

  • Evan GI, Wyllie AH, Gilbert CS, Littlewood TD, Land H, Brooks M, Waters CM, Penn LZ, Hanock DC (1992) Induction of Apoptosis in Fibroblasts by c-myc Protein. Cell 69: 119–128

    Article  PubMed  CAS  Google Scholar 

  • Farrell PJ, Allan GJ, Shanahan F, Vousden KH, Crook T (1991) p53 is frequently mutated in Burkitt’s lymphoma cell lines. EMBO J 10: 2879–2887

    Google Scholar 

  • Frech G, Zimber-Strobl U, Sventzenich KO, Palish O, Lenoir GM, Bornkamm GW, MuellerLantzsch N (1990) Identification of Epstein-Barr virus terminal protein (TP1) in extracts of four lymphoid cell lines, expression in insect cells and detection of antibodies in human sera. J Virol 64: 2759–2767

    PubMed  CAS  Google Scholar 

  • Gaidano G, Ballerini P, Gong JZ, Inghirami G, Meri A, Newcomb EW, Macgrath IT, Knowles DM, Dalla-Favera R (1991) p53 mutations in human lymphoid malignancies: association with Burkitt lymphoma and chronic lymphocytic leukemia. Proc Natl Acad Sci USA 88: 5413–5417

    Google Scholar 

  • Gregory CD, Tursz T, Edwards CF, Tetaud C, Talbot M, Caillou B, Rickinson AB, Lipinski M (1987) Identification of a subset of normal B cells with a Burkitt’s lymphoma ( BL)-like phenotype. J Immunol 139: 313–318

    Google Scholar 

  • Gregory CD, Muray RJ, Edwards CF, Rickinson AB (1988) Down-regulation of cell adhesion molecules LFA-3 and ICAM-1 in Epstein-Barr virus-positive Burkitt’s lymphoma underlies tumour cell escape from virus-specific T cell surveillance. J Exp Med 167: 1811–1824

    Article  PubMed  CAS  Google Scholar 

  • Gregory CD, Dive C, Henderson S, Smith CA, Williams GT, Gordon J, Rickinson AB (1991) Activation of Epstein-Barr virus latent genes protects human B cells from death by apoptosis. Nature 349: 612–614

    Article  PubMed  CAS  Google Scholar 

  • Gunven P, Klein G, Klein E, Narin T, Singh S (1980) Surface immunoglobulins on Burkitt’s lymphoma biopsy cells from 91 patients. Int J Cancer 25: 711–719

    Article  PubMed  CAS  Google Scholar 

  • Hammerschmidt W, Sugden B (1989) Genetic analysis of immortalizing functions of Epstein-Barr virus in human B lymphocytes. Nature 340: 393–397

    Article  PubMed  CAS  Google Scholar 

  • Harris AW, Pinkert CA, Crawford M, Langdon WY, Brinster RL, Adams JM (1988) The Eµmyc transgenic mouse: a model for high-incidence spontaneous lymphoma and leukemia of early B cells. J Exp Med 167: 353–371

    Article  PubMed  CAS  Google Scholar 

  • Haupt Y, Alexander WS, Barri G, Klinken SP, Adams JM (1991) Novel zinc finger gene implicated as myc collaborator by retrovirally accelerated lymphomagenesis in Eµ-myc trangenic mice. Cell 65: 753–763

    Article  PubMed  CAS  Google Scholar 

  • Henderson S, Rowe M, Gregory C, Croom-Carter D, Wang F, Longnecker R, Kieff E, Rickinson A (1991) Induction of bc1–2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell 65: 1107–1115

    Article  PubMed  CAS  Google Scholar 

  • Hollstein M, Sidransky D, Vogelstein B, Harris CC (1991) p53 mutations in human cancers. Science 253: 49–53

    Google Scholar 

  • Jannson A, Masucci M, Rymo L (1992) Methylation of discrete sites within the enhancer region regulates the activity of the Epstein-Barr virus BamHI W promoter in Burkitt lymphoma lines. J Virol 66: 62–69

    Google Scholar 

  • Jiang W-Q, Szekely L, Wendel-Hausen V, Ringertz N, Klein G, Rosen A (1991) Colocalisation of the retinoblastoma protein and the Epstein-Barr virus encoded nuclear antigen EBNA5. Exp Cell Res 197: 314–318

    Article  PubMed  CAS  Google Scholar 

  • Jucker M, Schaadt M, Diehl V, Poppena S, Jones D, Tesch H (1990) Heterogeneous expression of proto-oncogenes in Hodgkin’s disease derived cell lines. Hemat Oncol 8: 191–204

    Article  CAS  Google Scholar 

  • Jucker M, Roebroek AJM, Mautner J, Koch K, Eick D, Diehl V, Van de Ven WJM, Tesch H (1992) Expression of truncated transcripts of the proto-oncogene c fpslfes in human lymphoma and lymphoid leukemia cell lines. Oncogene 7: 943–954

    PubMed  CAS  Google Scholar 

  • Keiff E, Liebowitz D (1990) Epstein-Barr virus and its replication. In: Fields, Knipe (eds) Virology, 2nd edn. pp 1889–1920

    Google Scholar 

  • Klein E, Klein G, Nadkarni JS, Nadkarni JJ, Wigzell H, Clifford P (1967) Surface IgM specificity on cells derived from a Burkitt’s lymphoma. Lancet ii; 1068–1070

    Google Scholar 

  • Klein G (1983) Specific chromosomal translocations and the genesis of B cell lymphoma. Cell 32: 311–315

    Article  PubMed  CAS  Google Scholar 

  • Klein G (1987) In defence of the “old” Burkitt lymphoma scenario. In: Klein G (ed) Advances in viral oncology, vol 7. Raven, New York, pp 207–211

    Google Scholar 

  • Klein G (1989) Virus latency and transformation: the strategy of Epstein-Barr virus. Cell 58: 5–8

    Article  PubMed  CAS  Google Scholar 

  • Klein G (1991) Comparative action of myc and bcl-2 in B cell malignancy. Cancer Cells 3: 141–143

    PubMed  CAS  Google Scholar 

  • Lacy J, Summers WP, Summers WC (1989) Post-transcriptional mechanisms of deregulation of MYC following conversion of a human B cell line by Epstein-Barr virus. EMBO J 8: 1973–1980

    PubMed  CAS  Google Scholar 

  • Lam KMC, Syed N, Whittle H, Crawford DH (1991) Circulating Epstein-Barr virus carrying B-cells in acute malaria. JAMA 265: 876–879

    Article  Google Scholar 

  • Laux G, Perricaudet M, Farrell PJ (1988) A spliced Epstein-Barr virus gene expressed in immortalized lymphocytes is created by circularization of the linear viral genome. EMBO J 7: 769–774

    PubMed  CAS  Google Scholar 

  • Lenoir GM, Bornkamm GW (1987) Burkitt’s Lymphoma, a human cancer model for the multistep development of cancer: proposal for a new scenario. In: Klein G (ed) Advances in viral oncology. Raven, New York, pp 173–206

    Google Scholar 

  • Ling NR, Hardie D, Lowe J, Johnson GD, Khan M, MacLennan ICM (1989) A Phenotypic study of cells from Burkitt lymphoma and EBV-B-lymphoblastoid lines and their relationship to cells in normal lymphoid tissues. Int J Cancer 43: 112–118

    Article  PubMed  CAS  Google Scholar 

  • Lombardi L, Grinani F, Sternas L, Cechova K, Inghiraci G, Dalla-Favera R (1990) Mechanism of negative feedback regulation of c-myc gene expression in B-cells and its inactivation in tumour cells. In: Potter M, Melchers F (eds) Mechanisms in B-cell neoplasia 1990-springer, Berlin Heidelberg New York, pp 253–301

    Google Scholar 

  • Maclennan ICM, Gray D (1986) Antigen-driven selection of virgin and memory cells. Immunol Rev 91: 61–85

    Article  PubMed  CAS  Google Scholar 

  • Magrath I (1990) The pathogensis of Burkitt’s lymphoma. Adv Cancer Res 53: 132–270

    Google Scholar 

  • Mannick JB, Cohen JI, Birkenback M, Marchini A, Kieff E (1991) The Epstein-Barr virus nuclear protein encoded by the leader of the EBNA RNAs is important in B-lymphocyte transformation. J Virol 65: 6826–6837

    PubMed  CAS  Google Scholar 

  • Masucci MG, Torsteinsdottir S, Colombani BJ, Brautbar C, Klein E, Klein G (1987) Down regulation of class 1 HLA antigens and of the Epstein-Barr virus-encoded latent membrane protein in Burkitt lymphoma lines. Proc Natl Acad Sci USA 84: 4567–4571

    Article  PubMed  CAS  Google Scholar 

  • McDonnell TJ, Korsmeyer SJ (1991) Progression from lymphoid hyperplasia to high grade malignant lymphoma in mice transgenic for the t (14:18) Nature 349: 254–256

    CAS  Google Scholar 

  • Meeker TC, Loeb J, Ayres M, Sellers W (1990) The human Pim-1 gene is selectively transcribed in different hemato-lymphoid cell lines in spite of a G+C-rich housekeeping promoter. Mol Cell Biol 10: 1680–1688

    PubMed  CAS  Google Scholar 

  • Murray RJ, Kurilla MG, Brooks JM, Thomas WA, Rowe M, Kieff E, Rickinson AB (1992) Identification of target antigens for the human cytotoxic T cell response of Epstein-Barr virus (EBV): Implications for the immune control of EBV-positive malignancies. J Exp Med (in press)

    Google Scholar 

  • Neri A, Barriga F, Inghirami G, Knowles DM, Neequaye J, Magrath IT, Dalla-Favera R (1991) Epstein-Barr virus infection precedes clonal expansion in Burkitt’s and acquired immunodeficiency syndrome-associated lymphoma. Blood 77: 1092–1095

    PubMed  CAS  Google Scholar 

  • Nudelman E, Kannagi R, Hakomori S, Parsons M, Lipinski M, WielsJ, Fellous M, Tursz T (1983) A glycolipid antigen associated with Burkitt lymphoma defined by a mono-clonal antibody. Science 220: 509–511

    CAS  Google Scholar 

  • Pettersson S, Cook GP, Bruggemann M, Williams GT, Neuberger MS (1990) A second B cell specific enhancer 3’ of the immunoglobulin heavy-chain locus. Nature 344: 165–168

    Article  PubMed  CAS  Google Scholar 

  • Polack A, Strobl L, Feederle R, Schweizer M, Koch E, Eick D, Wiegal J, Bornkamm GW (1991) The intron enhancer of the immunoglobulin kappa gene activates c-myc but does not induce the Burkitt-specific promoter shift. Oncogene 6: 2033–2040

    PubMed  CAS  Google Scholar 

  • Raab-Traub N, Flynn K (1986) The Structure of the termini of the Epstein-Barr virus as a marker of clonal cellular proliferation Cell 47: 883–889

    CAS  Google Scholar 

  • Rabbitts TH, Hamlyn PH, Baer R (1983) Altered nucleotide sequences of a translocated c-myc gene in Burkitt’s lymphoma. Nature 306: 760–765

    Article  PubMed  CAS  Google Scholar 

  • Rooney CM, Gregory CD, Rowe M, Finerty S, Edwards C, Rupani H, Rickinson AB (1986) Endemic Burkitt’s lymphoma: Phenotypic analysis of tumour biopsy cells and of the derived tumour cells lines. JNCI 77: 681–687

    Google Scholar 

  • Rowe M, Gregory C (1989) Epstein-Barr Virus and Burkitt’s Lymphoma. Adv Vir Oncol 8: 237–259

    Google Scholar 

  • Rowe DT, Joab I, Laux G (1990) Identification of the Epstein-Barr virus terminal protein gene products in latently infected lymphocytes. J Virol 64: 2866–2875

    PubMed  CAS  Google Scholar 

  • Rowe M, Rooney CM, Rickinson AB, Lenoir GM, Rupani H, Moss DJ, Stein H, Epstein MA (1985) Distinctions between endemic and sporadic forms of Epstein-Barr virus-positive Burkitt’s lymphoma. Int J Cancer 35: 435–441

    Article  PubMed  CAS  Google Scholar 

  • Rowe M, Rooney CM, Edwards CF, Lenoir GM, Rickinson AB (1986) Epstein-Barr virus status and tumour cell phenotype in sporadic Burkitt’s lymphoma. Int J Cancer 37: 3647–373

    Article  Google Scholar 

  • Rowe M, Rowe DT, Gregory CD, Young LS, Farrell PJ, Rupani H, Rickinson AB (1987) Differences in B cell growth phenotype reflect novel patterns in Epstein-Barr virus latent gene expression in Burkitt’s lymphoma cells. EMBO J 6: 2743–2751

    PubMed  CAS  Google Scholar 

  • Rustgi AK, Dyson N. Bernards R (1991) Amino-terminal domains of c-myc and N-myc proteins mediate binding to the retinoblastoma gene product. Nature 352: 541–544

    CAS  Google Scholar 

  • Sample J, Brooks L, Sample C, Young L, Rowe M, Gregory C, Rickinson A, Kieff E (1991) Restricted Epstein-Barr virus protein expression in Burkitt lymphoma is due to a different Epstein-Barr nuclear antigen 1 transcriptional initiation site. Proc Natl Acad Sci USA 88: 6343–6347

    Article  PubMed  CAS  Google Scholar 

  • Schaefer BC, Woisetschlaeger M, Strominger JL, Speck SH (1991) Exclusive expression of Epstein-Barr virus nuclear antigen 1 in Burkitt lymphoma arises from a third promoter, distinct from the promoters used in latently infected lymphocytes. Proc Natl Acad Sci USA 88: 6550–6554

    Article  PubMed  CAS  Google Scholar 

  • Schmidt EV, Pattengale PK, Weir L, Leder P (1988) Transgenic mice bearing the human c-myc gene activated by an immunoglobulin enhancer: a pre-B-cell lymphoma model. Proc Natl Acad Sci USA 85: 6047–6051

    Article  PubMed  CAS  Google Scholar 

  • Shiramizu B, Barriga F, Neequaye J, Jafri A, Dalla-Favera R, Neri A, Guttierez M, Levine P, Magrath I (1991) Patterns of chromosomal breakpoint locations in Burkitt’s lymphoma: relevance to geography and Epstein-Barr virus association. Blood 77: 1516–1526

    PubMed  CAS  Google Scholar 

  • Shirodkar S, Ewen M, DeCaprio, Morgan J, Livingston DM, Chittenden T (1992) The transcription factor E2F interacts with the retinoblastoma product and a p107-cyclin a complex in a cell cycle-regulated manner. Cell 68: 157–166

    Article  PubMed  CAS  Google Scholar 

  • Shtivelman E, Henglein B, Groitl P, Lipp M, Bishop JM (1989) Identification of a human transcription unit affected by the variant chromosomal translocations 2;8 and 8;22 of Burkitt lymphoma. Proc Natl Acad Sci USA 86: 3257–3260

    Article  PubMed  CAS  Google Scholar 

  • Sinclair AJ, Farrell PJ (1992) Epstein-Barr virus transcription factors. Cell Growth Diff 3: 557–563

    PubMed  CAS  Google Scholar 

  • Sinclair AJ, Jacquemin M, Brooks L, Shanahan F, Brimmell M, Rowe M, Farrell PJ (1994) Reduced signal transduction through glucocorticoid receptor in Burkitt’s lymphoma cell lines. Virology (in press)

    Google Scholar 

  • Smith PR, Griffin BE (1992) Transcription of the Epstein-Barr virus gene EBNA-1 from different promoters in nasopharyngeal carcinoma and B-lymphoblastoid cells. J Virol 66: 706–714

    PubMed  CAS  Google Scholar 

  • Spencer CA, Groudine M (1991) Control of c-myc Regulation in normal and neoplastic cells. Adv Cancer 56: 1–48

    Article  CAS  Google Scholar 

  • Spencer CA, LeStrange RC, Novak U, Hayward WS, Groudine M (1990) The block to transcription elongation is promoter dependent in normal and Burkitt’s lymphoma c-myc alleles. Genes Dev 4: 75–88

    Article  PubMed  CAS  Google Scholar 

  • Swaminathan S, Tomkinson B, Kieff E (1991). Recombinant Epstein-Barr virus with small RNA ( EBER) genes deleted transforms lymphocytes and replicates in vitro. Proc Natl Acad Sci USA 88: 1546–1550

    Google Scholar 

  • van Lohuizen M, Verbeek S, Scheijen B, Wientjens E, van der Gulden H, Berns A (1991) Identification of cooperating oncogenes in Eµ-myc transgenic mice by provirus tagging. Cell 65: 737–752

    Article  PubMed  Google Scholar 

  • Vousden KV, Crook TR, Farrell PJ (1993) Biological activities of p53 mutants in Burkitt’s lymphoma cells. J Gen Virol 74: 803–810

    Article  PubMed  CAS  Google Scholar 

  • Whittle HC, Brown J, Marsh K, Greenwood BM, Seidelin P, Tighe H, Wedderburn L (1984) T-cell control of Epstein-Barr virus-infected B cells is lost during P. falciparum malaria. Nature 312: 449–450

    Article  PubMed  CAS  Google Scholar 

  • Wiman WG, Magnusson KP, Ramqvist T, Klein G (1991) Mutant p53 detected in a majority of Burkitt lymphoma cell lines by monoclonal antibody PAb240. Oncogene 6: 1633–1638

    PubMed  CAS  Google Scholar 

  • Woisetschlaeger M, Yandava CN, Furmanski LA, Strominger JL, Speck SH (1990) Promoter switching in Epstein-Barr virus during the initial stages of infection of B lymphocytes. Proc Natl Acad Sci USA 87: 1725–1729

    Article  PubMed  CAS  Google Scholar 

  • Yao QY, Rickinson AB, Epstein MA (1985) A re-examination of the Epstein-Barr virus carrier state in healthy seropositive individuals. Int J Cancer 35: 35–42

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Ludwig Institute for Cancer Research, St. Mary’s Hospital Medical School, Norfolk Place, London, W2 1PG, UK

    Marc Jacquemin, Alison J. Sinclair & Paul J. Farrell

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  1. Marc Jacquemin
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  2. Alison J. Sinclair
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  3. Paul J. Farrell
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Editors and Affiliations

  1. Department of Molecular Virology, Institute of Microbiology, Faculty of Medicine, The Hebrew University of Jerusalem, POB 12272, 91120, Jerusalem, Israel

    Yechiel Becker

  2. Institut für Medizinische Virologie, Universität Heidelberg, Im Neuenheimer Feld 324, D-69120, Heidelberg, Germany

    Gholamreza Darai

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© 1994 Springer-Verlag Berlin Heidelberg

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Jacquemin, M., Sinclair, A.J., Farrell, P.J. (1994). Gene Expression in Burkitt’s Lymphoma Cells. In: Becker, Y., Darai, G. (eds) Pathogenicity of Human Herpesviruses due to Specific Pathogenicity Genes. Frontiers of Virology, vol 3. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-85004-2_17

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  • DOI: https://doi.org/10.1007/978-3-642-85004-2_17

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