nature.com

Epstein–Barr virus infection in humans: from harmless to life endangering virus–lymphocyte interactions - Oncogene

  • ️Klein, G
  • ️Mon Feb 26 2007
  • Abbot SD, Rowe M, Cadwallader K, Ricksten A, Gordon J, Wang F et al. (1990). Epstein–Barr virus nuclear antigen 2 induces expression of the virus-encoded latent membrane protein. J Virol 64: 2126–2134.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Altiok E, Minarovits J, Hu LF, Contreras-Brodin B, Klein G, Ernberg I . (1992). Host-cell-phenotype-dependent control of the BCR2/BWR1 promoter complex regulates the expression of Epstein–Barr virus nuclear antigens 2–6 [published erratum appears in Proc Natl Acad Sci USA 1992; 89: 6225]. Proc Natl Acad Sci USA 89: 905–909.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atayar C, Poppema S, Visser L, van den Berg A . (2006). Cytokine gene expression profile distinguishes CD4+/CD57+ T cells of the nodular lymphocyte predominance type of Hodgkin's lymphoma from their tonsillar counterparts. J Pathol 208: 423–430.

    Article  CAS  PubMed  Google Scholar 

  • Babcock GJ, Decker LL, Volk M, Thorley-Lawson DA . (1998). EBV persistence in memory B cells in vivo. Immunity 9: 395–404.

    Article  CAS  PubMed  Google Scholar 

  • Bandobashi K, Liu A, Nagy N, Kis LL, Nishikawa J, Bjorkholm M et al. (2005). EBV infection induces expression of the transcription factors ATF-2/c-Jun in B lymphocytes but not in B-CLL cells. Virus Genes 30: 323–330.

    Article  CAS  PubMed  Google Scholar 

  • Baumforth KR, Flavell JR, Reynolds GM, Davies G, Pettit TR, Wei W et al. (2005). Induction of autotaxin by the Epstein–Barr virus promotes the growth and survival of Hodgkin lymphoma cells. Blood 106: 2138–2146.

    Article  CAS  PubMed  Google Scholar 

  • Bargou RC, Emmerich F, Krappmann D, Bommert K, Mapara MY, Arnold W et al. (1997). Constitutive nuclear factor-kappaB-RelA activation is required for proliferation and survival of Hodgkin's disease tumor cells. J Clin Invest 100: 2961–2969.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bechtel D, Kurth J, Unkel C, Kuppers R . (2005). 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 106: 4345–4350.

    Article  CAS  PubMed  Google Scholar 

  • Cabannes E, Khan G, Aillet F, Jarrett RF, Hay RT . (1999). Mutations in the IkBa gene in Hodgkin's disease suggest a tumour suppressor role for IkappaBalpha. Oncogene 18: 3063–3070.

    Article  CAS  PubMed  Google Scholar 

  • Caligaris-Cappio F, Hamblin TJ . (1999). B-cell chronic lymphocytic leukemia: a bird of a different feather. J Clin Oncol 17: 399–408.

    Article  CAS  PubMed  Google Scholar 

  • Carbone A, Gloghini A, Gruss HJ, Pinto A . (1995). CD40 ligand is constitutively expressed in a subset of T cell lymphomas and on the microenvironmental reactive T cells of follicular lymphomas and Hodgkin's disease. Am J Pathol 147: 912–922.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen F, Zou JZ, di Renzo L, Winberg G, Hu LF, Klein E et al. (1995). A subpopulation of normal B cells latently infected with Epstein–Barr virus resembles Burkitt lymphoma cells in expressing EBNA-1 but not EBNA-2 or LMP1. J Virol 69: 3752–3758.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chiang AK, Tao Q, Srivastava G, Ho FC . (1996). Nasal NK- and T-cell lymphomas share the same type of Epstein–Barr virus latency as nasopharyngeal carcinoma and Hodgkin's disease. Int J Cancer 68: 285–290.

    Article  CAS  PubMed  Google Scholar 

  • Contreras-Brodin B, Karlsson A, Nilsson T, Rymo L, Klein G . (1996). B cell-specific activation of the Epstein–Barr virus-encoded C promoter compared with the wide-range activation of the W promoter. J Gen Virol 77: 1159–1162.

    Article  CAS  PubMed  Google Scholar 

  • Contreras-Brodin BA, Anvret M, Imreh S, Altiok E, Klein G, Masucci MG . (1991). B cell phenotype-dependent expression of the Epstein–Barr virus nuclear antigens EBNA-2 to EBNA-6: studies with somatic cell hybrids. J Gen Virol 72: 3025–3033.

    Article  CAS  PubMed  Google Scholar 

  • Chaganti S, Bell AI, Pastor NB, Milner AE, Drayson M, Gordon J et al. (2005). Epstein–Barr virus infection in vitro can rescue germinal center B cells with inactivated immunoglobulin genes. Blood 106: 4249–4252.

    Article  CAS  PubMed  Google Scholar 

  • Deacon EM, Pallesen G, Niedobitek G, Crocker J, Brooks L, Rickinson AB et al. (1993). Epstein–Barr virus and Hodgkin's disease: transcriptional analysis of virus latency in the malignant cells. J Exp Med 177: 339–349.

    Article  CAS  PubMed  Google Scholar 

  • Doyle MG, Catovsky D, Crawford DH . (1993). Infection of leukaemic B lymphocytes by Epstein–Barr virus. Leukemia 7: 1858–1864.

    CAS  PubMed  Google Scholar 

  • Dukers DF, Meij P, Vervoort MB, Vos W, Scheper RJ, Meijer CJ et al. (2000). Direct immunosuppressive effects of EBV-encoded latent membrane protein 1. J Immunol 165: 663–670.

    Article  CAS  PubMed  Google Scholar 

  • Epstein MA, Achong BG, Barr YM. . (1964). Virus particles in cultured lymphoblasts from Burkitt's lymphoma. Lancet 15: 702–703.

    Article  Google Scholar 

  • Fahraeus R, Fu HL, Ernberg I, Finke J, Rowe M, Klein G et al. (1988). Expression of Epstein–Barr virus-encoded proteins in nasopharyngeal carcinoma. Int J Cancer 42: 329–338.

    Article  CAS  PubMed  Google Scholar 

  • Fahraeus R, Jansson A, Ricksten A, Sjöblom A, Rymo L . (1990). Epstein–Barr virus-encoded nuclear antigen 2 activates the viral latent membrane protein promoter by modulating the activity of a negative regulatory element. Proc Natl Acad Sci USA 87: 7390–7394.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falk K, Linde A, Johnson D, Lennette E, Ernberg I, Lundkvist A . (1995). Synthetic peptides deduced from the amino acid sequence of Epstein–Barr virus nuclear antigen 6 (EBNA 6): antigenic properties, production of monoreactive reagents, and analysis of antibody responses in man. J Med Virol 46: 349–357.

    Article  CAS  PubMed  Google Scholar 

  • Frisan T, Sjoberg J, Dolcetti R, Boiocchi M, De Re V, Carbone A et al. (1995). Local suppression of Epstein–Barr virus (EBV)-specific cytotoxicity in biopsies of EBV-positive Hodgkin's disease. Blood 86: 1493–1501.

    CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Harabuchi Y, Yamanaka N, Kataura A, Imai S, Kinoshita T, Mizuno F et al. (1990). Epstein–Barr virus in nasal T-cell lymphomas in patients with lethal midline granuloma. Lancet 335: 128–130.

    Article  CAS  PubMed  Google Scholar 

  • Henle W, Henle G, Lennette ET . (1979). The Epstein–Barr virus. Sci Am 241: 48–59.

    Article  CAS  PubMed  Google Scholar 

  • Hertel CB, Zhou XG, Hamilton-Dutoit SJ, Junker S . (2002). Loss of B cell identity correlates with loss of B cell-specific transcription factors in Hodgkin/Reed-Sternberg cells of classical Hodgkin lymphoma. Oncogene 21: 4908–4920.

    Article  CAS  PubMed  Google Scholar 

  • Hjalgrim H, Askling J, Rostgaard K, Hamilton-Dutoit S, Frisch M, Zhang JS et al. (2003). Characteristics of Hodgkin's lymphoma after infectious mononucleosis. N Engl J Med 349: 1324–1332.

    Article  CAS  PubMed  Google Scholar 

  • Hochberg D, Middeldorp JM, Catalina M, Sullivan JL, Luzuriaga K, Thorley-Lawson DA . (2004). Demonstration of the Burkitt's lymphoma Epstein–Barr virus phenotype in dividing latently infected memory cells in vivo. Proc Natl Acad Sci USA 101: 239–244.

    Article  CAS  PubMed  Google Scholar 

  • Horie R, Watanabe T, Morishita Y, Ito K, Ishida T, Kanegae Y et al. (2002). Ligand-independent signaling by overexpressed CD30 drives NF-kappaB activation in Hodgkin–Reed-Sternberg cells. Oncogene 21: 2493–2503.

    Article  CAS  PubMed  Google Scholar 

  • Ishida T, Ishii T, Inagaki A, Yano H, Komatsu H, Iida S et al. (2006). Specific recruitment of CC chemokine receptor 4-positive regulatory T cells in Hodgkin lymphoma fosters immune privilege. Cancer Res 66: 5716–5722.

    Article  CAS  PubMed  Google Scholar 

  • Kanzler H, Kuppers R, Hansmann ML, Rajewsky K . (1996). Hodgkin and Reed-Sternberg cells in Hodgkin's disease represent the outgrowth of a dominant tumor clone derived from (crippled) germinal center B cells. J Exp Med 184: 1495–1505.

    Article  CAS  PubMed  Google Scholar 

  • Kanzler H, Kuppers R, Helmes S, Wacker HH, Chott A, Hansmann ML et al. (2000). Hodgkin and Reed-Sternberg-like cells in B-cell chronic lymphocytic leukemia represent the outgrowth of single germinal-center B-cell-derived clones: potential precursors of Hodgkin and Reed-Sternberg cells in Hodgkin's disease. Blood 95: 1023–1031.

    CAS  PubMed  Google Scholar 

  • Kennedy G, Komano J, Sugden B . (2003). Epstein–Barr virus provides a survival factor to Burkitt's lymphomas. Proc Natl Acad Sci USA 100: 14269–14274.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kis LL, Nishikawa J, Takahara M, Nagy N, Matskova L, Takada K et al. (2005). In vitro EBV-infected subline of KMH2, derived from Hodgkin lymphoma, expresses only EBNA-1, while CD40 ligand and IL-4 induce LMP-1 but not EBNA-2. Int J Cancer 113: 937–945.

    Article  CAS  PubMed  Google Scholar 

  • Kis LL, Takahara M, Nagy N, Klein G, Klein E . (2006a). IL-10 can induce the expression of EBV-encoded latent membrane protein-1 (LMP-1) in the absence of EBNA-2 in B lymphocytes and in Burkitt lymphoma- and NK lymphoma-derived cell lines. Blood 107: 2928–2935.

    Article  CAS  PubMed  Google Scholar 

  • Kis LL, Takahara M, Nagy N, Klein G, Klein E . (2006b). Cytokine mediated induction of the major Epstein–Barr virus (EBV)-encoded transforming protein, LMP-1. Immunol Lett 104: 83–88.

    Article  CAS  PubMed  Google Scholar 

  • Klein G . (1994). Epstein–Barr virus strategy in normal and neoplastic B cells. Cell 77: 791–793.

    Article  CAS  PubMed  Google Scholar 

  • Komano J, Maruo S, Kurozumi K, Oda T, Takada K . (1999). Oncogenic role of Epstein–Barr virus-encoded RNAs in Burkitt's lymphoma cell line Akata. J Virol 73: 9827–9831.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kuppers R . (2002). Molecular biology of Hodgkin's lymphoma. Adv Cancer Res 84: 277–312.

    Article  PubMed  Google Scholar 

  • Kuppers R, Rajewsky K, Zhao M, Simons G, Laumann R, Fischer R et al. (1994). Hodgkin disease: Hodgkin and Reed-Sternberg cells picked from histological sections show clonal immunoglobulin gene rearrangements and appear to be derived from B cells at various stages of development. Proc Natl Acad Sci USA 91: 10962–10966.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurth J, Hansmann ML, Rajewsky K, Kuppers R . (2003). Epstein–Barr virus-infected B cells expanding in germinal centers of infectious mononucleosis patients do not participate in the germinal center reaction. Proc Natl Acad Sci USA 100: 4730–4735.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurth J, Spieker T, Wustrow J, Strickler GJ, Hansmann LM, Rajewsky K et al. (2000). EBV-infected B cells in infectious mononucleosis: viral strategies for spreading in the B cell compartment and establishing latency. Immunity 13: 485–495.

    Article  CAS  PubMed  Google Scholar 

  • Lennette ET, Rymo L, Yadav M, Masucci G, Merk K, Timar L et al. (1993). Disease-related differences in antibody patterns against EBV-encoded nuclear antigens EBNA 1, EBNA 2 and EBNA 6. Eur J Cancer 29A: 1584–1589.

    Article  CAS  PubMed  Google Scholar 

  • Levitskaya J, Coram M, Levitsky V, Imreh S, Steigerwald-Mullen PM, Klein G et al. (1995). Inhibition of antigen processing by the internal repeat region of the Epstein–Barr virus nuclear antigen-1. Nature 375: 685–688.

    Article  CAS  PubMed  Google Scholar 

  • Lewin N, Minarovits J, Weber G, Ehlin-Henriksson B, Wen T, Mellstedt H et al. (1991). Clonality and methylation status of the Epstein–Barr virus (EBV) genomes in in vivo-infected EBV-carrying chronic lymphocytic leukemia (CLL) cell lines. Int J Cancer 48: 62–66.

    Article  CAS  PubMed  Google Scholar 

  • Maeda A, Bandobashi K, Nagy N, Teramoto N, Gogolak P, Pokrovskaja K et al. (2001). Epstein–Barr virus can infect B-chronic lymphocytic leukemia cells but it does not orchestrate the cell cycle regulatory proteins. J Hum Virol 4: 227–237.

    CAS  PubMed  Google Scholar 

  • Mancao C, Altmann M, Jungnickel B, Hammerschmidt W . (2005). Rescue of ‘crippled’ germinal center B cells from apoptosis by Epstein–Barr virus. Blood 106: 4339–4344.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marshall NA, Christie LE, Munro LR, Culligan DJ, Johnston PW, Barker RN et al. (2004). Immunosuppressive regulatory T cells are abundant in the reactive lymphocytes of Hodgkin lymphoma. Blood 103: 1755–1762.

    Article  CAS  PubMed  Google Scholar 

  • Martin-Subero JI, Gesk S, Harder L, Sonoki T, Tucker PW, Schlegelberger B et al. (2002). Recurrent involvement of the REL and BCL11A loci in classical Hodgkin lymphoma. Blood 99: 1474–1477.

    Article  CAS  PubMed  Google Scholar 

  • Nakayama T, Hieshima K, Nagakubo D, Sato E, Nakayama M, Kawa K et al. (2004). Selective induction of Th2-attracting chemokines CCL17 and CCL22 in human B cells by latent membrane protein 1 of Epstein–Barr virus. J Virol 78: 1665–1674.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nilsson K, Ponten J . (1975). Classification and biological nature of established human hematopoietic cell lines. Int J Cancer 15: 321–341.

    Article  CAS  PubMed  Google Scholar 

  • Oudejans JJ, Jiwa M, van den Brule AJ, Grasser FA, Horstman A, Vos W et al. (1995). Detection of heterogeneous Epstein–Barr virus gene expression patterns within individual post-transplantation lymphoproliferative disorders. Am J Pathol 147: 923–933.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pallesen G, Hamilton-Dutoit SJ, Rowe M, Young LS . (1991). Expression of Epstein–Barr virus latent gene products in tumour cells of Hodgkin's disease. Lancet 337: 320–322.

    Article  CAS  PubMed  Google Scholar 

  • Pope JH, Horne MK, Scott W . (1968). Transformation of foetal human leukocytes in vitro by filtrates of a human leukaemic cell line containing herpes-like virus. Int J Cancer 3: 857–866.

    Article  CAS  PubMed  Google Scholar 

  • Rickinson AB, Finerty S, Epstein MA . (1982). Interaction of Epstein–Barr virus with leukaemic B cells in vitro. I. Abortive infection and rare cell line establishment from chronic lymphocytic leukaemic cells. Clin Exp Immunol 50: 347–354.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rickinson AB, Kieff E . (2001). Epstein–Barr virus. In: Knipe DM and Howley PM (eds). Fields Virology, 4th edn. Vol. 2. Lippincott Williams and Wilkins: Philadelphia, pp 2575–2628.

    Google Scholar 

  • Roschke V, Kopantzev E, Dertzbaugh M, Rudikoff S . (1997). Chromosomal translocations deregulating c-myc are associated with normal immune responses. Oncogene 14: 3011–3016.

    Article  CAS  PubMed  Google Scholar 

  • Rowe M, Lear AL, Croom-Carter D, Davies AH, Rickinson AB . (1992). Three pathways of Epstein–Barr virus gene activation from EBNA1-positive latency in B lymphocytes. J Virol 66: 122–131.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schaefer BC, Strominger JL, Speck SH . (1995). Redefining the Epstein–Barr virus-encoded nuclear antigen EBNA-1 gene promoter and transcription initiation site in group I Burkitt lymphoma cell lines. Proc Natl Acad Sci USA 92: 10565–10569.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwering I, Brauninger A, Klein U, Jungnickel B, Tinguely M, Diehl V et al. (2003). Loss of the B-lineage-specific gene expression program in Hodgkin and Reed-Sternberg cells of Hodgkin lymphoma. Blood 101: 1505–1512.

    Article  CAS  PubMed  Google Scholar 

  • Staratschek-Jox A, Wolf J, Diehl V . (2000). Hodgkin's disease. In: Masters JRW, Palsson BO (eds). Human Cell Culture. Vol. 3. Kluwer Academic Publishers: Dordrecht, pp 339–353.

    Google Scholar 

  • Takada K, Yamamoto K, Osato T . (1980). Analysis of the transformation of human lymphocytes by Epstein–Barr virus. II. Abortive response of leukemic cells to the transforming virus. Intervirology 13: 223–231.

    Article  CAS  PubMed  Google Scholar 

  • Takahara M, Kis LL, Nagy N, Liu A, Harabuchi Y, Klein G et al. (2006). Concomitant increase of LMP1 and CD25 (IL-2-receptor alpha) expression induced by IL-10 in the EBV-positive NK lines SNK6 and KAI3. Int J Cancer 119: 2775–2783.

    Article  CAS  PubMed  Google Scholar 

  • Teramoto N, Gogolak P, Nagy N, Maeda A, Kvarnung K, Bjorkholm M et al. (2000). Epstein–Barr virus-infected B-chronic lymphocyte leukemia cells express the virally encoded nuclear proteins but they do not enter the cell cycle. J Hum Virol 3: 125–136.

    CAS  PubMed  Google Scholar 

  • Tierney R, Kirby H, Nagra J, Rickinson A, Bell A . (2000). The Epstein–Barr virus promoter initiating B-cell transformation is activated by RFX proteins and the B-cell-specific activator protein BSAP/Pax5. J Virol 74: 10458–10467.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thorley-Lawson DA . (2001). Epstein–Barr virus: exploiting the immune system. Nat Rev Immunol 1: 75–82.

    Article  CAS  PubMed  Google Scholar 

  • Tomita Y, Avila-Carino J, Yamamoto K, Mellstedt H, Klein E . (1998). Recognition of B-CLL cells experimentally infected with EBV by autologous T lymphocytes. Immunol Lett 60: 73–79.

    Article  CAS  PubMed  Google Scholar 

  • Tsimberidou AM, Keating MJ, Bueso-Ramos CE, Kurzrock R . (2006). Epstein–Barr virus in patients with chronic lymphocytic leukemia: a pilot study. Leuk Lymphoma 47: 827–836.

    Article  PubMed  Google Scholar 

  • Tsuge I, Morishima T, Morita M, Kimura H, Kuzushima K, Matsuoka H . (1999). Characterization of Epstein–Barr virus (EBV)-infected natural killer (NK) cell proliferation in patients with severe mosquito allergy; establishment of an IL-2-dependent NK-like cell line. Clin Exp Immunol 115: 385–392.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van den Berg A, Visser L, Poppema S . (1999). High expression of the CC chemokine TARC in Reed-Sternberg cells. A possible explanation for the characteristic T-cell infiltration Hodgkin's lymphoma. Am J Pathol 154: 1685–1691.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vockerodt M, Belge G, Kube D, Irsch J, Siebert R, Tesch H et al. (2002). An unbalanced translocation involving chromosome 14 is the probable cause for loss of potentially functional rearranged immunoglobulin heavy chain genes in the Epstein–Barr virus-positive Hodgkin's lymphoma-derived cell line L591. Br J Haematol 119: 640–646.

    Article  CAS  PubMed  Google Scholar 

  • Walls EV, Doyle MG, Patel KK, Allday MJ, Catovsky D, Crawford DH . (1989). Activation and immortalization of leukaemic B cells by Epstein–Barr virus. Int J Cancer 44: 846–853.

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Tsang SF, Kurilla MG, Cohen JI, Kieff E . (1990). Epstein–Barr virus nuclear antigen 2 transactivates latent membrane protein LMP1. J Virol 64: 3407–3416.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Young L, Alfieri C, Hennessy K, Evans H, O'Hara C, Anderson KC et al. (1989). Expression of Epstein–Barr virus transformation-associated genes in tissues of patients with EBV lymphoproliferative disease. N Engl J Med 321: 1080–1085.

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Nagata H, Ikeuchi T, Mukai H, Oyoshi MK, Demachi A et al. (2003). Common cytological and cytogenetic features of Epstein–Barr virus (EBV)-positive natural killer (NK) cells and cell lines derived from patients with nasal T/NK-cell lymphomas, chronic active EBV infection and hydroa vacciniforme-like eruptions. Br J Haematol 121: 805–814.

    Article  PubMed  Google Scholar