Molecular biological properties of the Эpstein-Barr virus LMP1 gene: structure, function and polymorphism
- Authors: Smirnova K.V.1, Diduk S.V.1, Senyuta N.B.1, Gurtsevitch V.E.1
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Affiliations:
- Federal State Budgetary Ssientific Institution “N.N.Blokhin Cancer Research Center”
- Issue: Vol 60, No 3 (2015)
- Pages: 5-13
- Section: REVIEWS
- Submitted: 10.07.2020
- Accepted: 10.07.2020
- Published: 28.06.2015
- URL: https://virusjour.crie.ru/jour/article/view/327
- ID: 327
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Abstract
About the authors
K. V. Smirnova
Federal State Budgetary Ssientific Institution “N.N.Blokhin Cancer Research Center”
Author for correspondence.
Email: smirnovakv@rambler.ru
Kseniya Smirnova, MD, PhD
115478, Moscow
Russian FederationS. V. Diduk
Federal State Budgetary Ssientific Institution “N.N.Blokhin Cancer Research Center”
Email: fake@neicon.ru
115478, Moscow Russian Federation
N. B. Senyuta
Federal State Budgetary Ssientific Institution “N.N.Blokhin Cancer Research Center”
Email: fake@neicon.ru
115478, Moscow Russian Federation
V. E. Gurtsevitch
Federal State Budgetary Ssientific Institution “N.N.Blokhin Cancer Research Center”
Email: fake@neicon.ru
115478, Moscow Russian Federation
References
- Young L.S., Rickinson A.B. Epstein-Barr virus: 40 years on. Nat. Rev. Cancer. 2004; 4(10): 757–68.
- Shimakaze M., Sasagawa T., Kawahara K., Yutsudo M., Kusuoka H., Kozuka T. Expression of Epstein-Barr virus in cutaneous T-cell lymphoma including mycosis fungoides. Int. J. Cancer. 2001; 92: 226–31.
- Fahraeus R., Rymo L., Rhim J. S., Klein G. Morphological transformation of human keratinocytes expressing the LMP gene of Epstein-Barr virus. Nature. 1990; 345: 447-9.
- Kaye K., Izumi K., Kieff E. Epstein-Barr virus latent membrane protein 1 is essential for B-lymphocyte growth transformation. Proc. Natl. Acad. Sci. USA. 1993; 90: 9150–4.
- Mosialos G., Birkenbach M., Yalamanchili R., Van Arsdale T., Ware C., Kieff E. The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family. Cell. 1995; 80(3): 389–99.
- Nitta T., Chiba A., Yamashita A., Rowe M., Israel A., Reth M. et al. NF-kB is required for cell death induction by latent membrane protein 1 of Epstein–Barr virus. Cell. Signal. 2003; 15: 423–33.
- Aviel S., Winberg G., Massucci M., Ciechanover A. Degradation of the Epstein-Barr virus latent membrane protein 1 (LMP1) by the ubiquitin-proteasome pathway. J. Biolog. Chem. 2000; 275(31): 23491–9.
- Mainou B.A., Raab-Traub N. LMP1 strain variants: biological and molecular properties. J. Virol. 2006; 80: 6458–68.
- Bentz G.L., Whitehurst C.B., Pagano J.S. Epstein-Barr virus latent membrane protein 1 (LMP1) C-terminal-activating region 3 contributes to LMP1-mediated cellular migration via its interaction with Ubc9. J. Virol. 2011; 85(19): 10144–53.
- Jime´nez-Ramı´rez С., Brooks A.J., Forshell L.P., Yakimchuk K., Zhao B., Fulgham T.Z. et al. Epstein-Barr virus EBNA-3C is targeted to and regulates expression from the bidirectional LMP-1/2B promoter. J. Virol. 2006; 80(22): 11200–8.
- Erickson K.D., Berger C., Coffin W.F., Schiff E., Walling D.M., Martin J.M. Unexpected absence of the Epstein-Barr virus (EBV) lyLMP-1 open reading frame in tumor virus isolates: lack of correlation between Met129 status and EBV strain identity. J. Virol. 2003; 77(7): 4415–22.
- Erickson K.D., Martin J.M. The late lytic LMP-1 protein of EpsteinBarr virus can negatively regulate LMP-1 signaling. J. Virol. 2000; 74(2): 1057–60.
- Martel-Renoir D., Grunewald V., Touitou R., Schwaab G., Joab I. Qualitative analysis of the expression of Epstein-Barr virus lytic genes in nasopharyngeal carcinoma biopsies. J. Gen. Virol. 1995; 76(Pt 6): 1401–8.
- Pandya J., Walling D.M. Oncogenic activity of Epstein-Barr virus latent membrane protein 1 (LMP-1) is down-regulated by lytic LMP-1. J. Virol. 2006; 80(16): 8038–46.
- Kaye K.M., Devergne O., Harada J.N., Izumi K.M., Yalamanchili R., Kieff E. et al. Tumor necrosis factor receptor associated factor 2 is a mediator of NF-kB activation by latent infection membrane protein 1, the Epstein–Barr virus transforming protein. Proc. Natl. Acad. Sci. USA. 1996; 93: 11085–90.
- Kieser A., Kaiser C., Hammerschmidt W. LMP1 signal transduction differs substantially from TNF receptor 1 signaling in the molecular functions of TRADD and TRAF2. EMBO J. 1999; 18(9): 2511–21.
- Wu L., Nakano H., Wu Z. The C-terminal activating region 2 of the Epstein-Barr virus-encoded latent membrane protein 1 activates NF-kB through TRAF6 and TAK1. J. Biol. Chem. 2006; 281(4): 2162–9.
- Luftig M., Yasui T., Soni V., Kang M.-S., Jacobson N., Cahir-McFarland E. et al. Epstein–Barr virus latent infection membrane protein 1 TRAF-binding site induces NIK/IKKα-dependent noncanonical NFkB activation.Proc. Natl. Acad. Sci. USA. 2004; 101(1): 141–6.
- Takanashi M., Li J., Shirakata M., Mori S., Hirai K. Tumorigenicity of mouse BALB/c 3T3 fibroblast cells which express Epstein-Barr virus-encoded LMP1 and show normal growth phenotypes in vitro is correlated with loss of transforming growth factor-b1-mediated growth inhibition. Arch. Virol. 1999; 144: 241–57.
- Prokova V, Mosialos G., Kardassis D. Inhibition of transforming growth factor β signaling and Smad-dependent activation of transcription by the latent membrane protein 1 of Epstein-Barr virus. J. Biol. Chem. 2002; 277(11): 9342–50.
- Zanke B.W., Rubie E.A., Winnett E., Tibbles L.A., Zon L., Kyriakis J. et al. The stress-activated protein kinase pathway mediates cell death following injury induced by cis-platinum, UV irradiation or heat. Curr. Biol. 1996; 6: 606–13.
- Fritz G., Kaina B. Activation of c-Jun N-terminal kinase 1 by UV irradiation is inhibited by wortmannin without affecting c-jun expression. Mol. Cell. Biol. 1999; 19(3): 1768–74.
- Berberichl I., Shu G., Siebelt F., Woodgett J.R., Kyriakis J.M., Clark E.A. Cross-linking CD40 on B cells preferentially induces stress-activated protein kinases rather than mitogen-activated protein kinases. EMBO J. 1996; 15(1): 92–101.
- Reinhard C., Shamoon B., Shyamala V., Williams L.T. Tumor necrosis factor a-induced activation of c-jun N-terminal kinase is mediated by TRAF2. EMBO J. 1997; 16(5): 1080–92.
- Kieser A., Kilger E., Gires O., Ueffing M., Kolch W., Hammerschmidt W. Epstein–Barr virus latent membrane protein-1 triggers AP-1 activity via the c-Jun N-terminal kinase cascade. EMBO J. 1997; 16: 6478–85.
- Dawson C.W., Port R.J., Young L.S. The role of the EBV-encoded latent membrane proteins LMP1 and LMP2 in the pathogenesis of nasopharingeal carcinoma (NPC). Semin. Cancer Biol. 2012; 22: 144–53.
- Eliopoulos A.G., Gallagher N.J., Blake S.M.S., Dawson C.V., Young L.S. Activation of the p38 mitogen-activated protein kinase pathway by Epstein-Barr virus-encoded latent membrane protein 1 coregulates interleukin-6 and interleukin-8 production. J. Biol. Chem. 1999; 274(23): 16085–96.
- Luka J., Kallin B., Klein G. Induction of Epstein-Barr virus (EBV) cycle in latently infected cells by n-butyrate. Virology. 1979; 92: 228–31.
- Shirakata M., Imadome K.-I., Okazaki K., Hirai K. Activation of TRAF5 and TRAF6 signal cascades negatively regulates the latent replication origin of Epstein-Barr virus through p38 mitogen-activated protein kinase. J. Virol. 2001; 75(11): 5059–68.
- Fielding C.A., Sandvej K., Mehl A., Brennan P., Jones M., Rowe M. Epstein-Barr virus LMP-1 natural sequence variants differ in their potential to activate cellular signaling pathways. J. Virol. 2001; 75(19): 9129–41.
- Gires O., Kohlhuber F., Kilger E., Baumann M., Kieser A., Kaiser C. et al. Latent membrane protein 1 of Epstein–Barr virus interacts with JAK3 and activates STAT proteins. EMBO J. 1999; 18(11): 3064–73.
- Riches D.W.H., Chan E.D., Zahradka E.A., Winston B.W., Remigio L.K., Lake F.R. Cooperative signaling by tumor necrosis factor receptors CD120a (p55) and CD120b (p75) in the expression of nitric oxide and inducible nitric oxide synthase by mouse macrophages. J. Biol. Chem. 1998; 273(35): 22800–6.
- Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J. 1992; 6: 3051–64.
- Kleinert H., Euchenhofer C., Ihrig-Biedert I., Forstermann U. In murine 3T3 fibroblasts, different second messenger pathways resulting in the induction of NO synthase II (iNOS) converge in the activation of transcription factor NF-kB. J. Biol. Chem. 1996; 271(11): 6039–44.
- Yu J.S., Tsai H.C., Wu C.C., Weng L.P., Li H.P., Chung P.J. et al. Induction of inducible nitric oxide synthase by Epstein-Barr virus B95-8-derived LMP1 in Balb/3T3 cells promotes stress-induced cell death and impairs LMP1-mediated transformation. Oncogene. 2002; 14(21): 8047–61.
- Li L., Li W., Xiao L., Xu J., Chen X., Tang M. et al. Viral oncoprotein LMP1 disrupts p53-induced cell cycle arrest and apoptosis through modulating K63-linked ubiquitination of p53. Cell Cycle. 2012; 11: 2327–36.
- Guo L., Tang M., Yang L., Xiao L., Bode A.M., Li L. et al. EpsteinBarr virus oncoprotein LMP1 mediates survivin upregulation by p53 contributing to G1/S cell cycle progression in nasopharyngeal carcinoma. Int. J. Mol. Med. 2012; 29: 574–80.
- Horikawa T., Yoshizaki T., Kondo S., Furukawa M., Kaizaki Y., Pagano J.S. Epstein-Barr Virus latent membrane protein 1 induces Snail and epithelial-mesenchymal transition in metastatic nasopharyngeal carcinoma. Br. J. Cancer. 2011; 104(7): 1160–7.
- Edwards R.H., Sitki-Green D., Moore D.T., Raab-Traub N. Potential selection of LMP1 variants in nasopharyngeal carcinoma. J. Virol. 2004; 78(2): 868–81.
- Hu L.-F., Zabarovsky E.R., Chen F., Cao S.-L., Ernberg I., Klein G. et al. Isolation and sequencing of the Epstein-Barr virus BNLF-1 gene (LMP1) from a Chinese nasopharyngeal carcinoma. J. Gener. Virol. 1991; 72: 2399–400.
- Blake S.M., Eliopoulos A.G., Dawson C.W., Young L.S. The transmembrane domains of the EBV-encoded latent membrane protein 1 (LMP1) variant Cao regulate enhanced signalling activity. Virology. 2001; 282: 278–87.
- Johnson R.J., Stack M., Hazlewood S.A., Jones M., Blackmore C.G., Hu L.-F. et al. The 30-base-pair deletion in chinese variants of the Epstein-Barr virus LMP1 gene is not the major effector of functional differences between variant LMP1 genes in human lymphocytes. J. Virol. 1998; 72(5): 4038–48.
- Fischer N., Kopper B., Graf N., Schlehofer J., Grässer F., MuellerLantzsch N. Functional analysis of different LMP1 proteins isolated from Epstein-Barr virus-positive carriers. Virus Res. 1999; 60: 41–54.
- Knecht H., Bachmann E., Brousset P., Sandvej K., Nadal D., Bachmann F. et al. Deletions within the LMPl oncogene of Epstein-Barr virus are clustered in Hodgkin’s disease and identical to those observed in nasopharyngeal carcinoma. Blood. 1993; 82(10): 2937–42.
- Chang Y.-S., Su I.-J., Chung P.-J., Shu Ch.-H., Ng Ch.-K., Wu S.-J. et al. Detection of an Epstein-Barr virus variant in T-cell-lymphoma tissues identical to the distinct strain observed in nasopharyngeal carcinoma in the Taiwanese population. Int. J. Cancer. 1995; 62: 673–7.
- Cheung S.-T., Lo K.-W., Leung S., Chan W.-Y., Choi P., Jonhson P. et al. Prevalence of LMP1 deletion variant of Epstein-Barr virus in nasopharyngeal carcinoma and gastric tumors in Hong Kong. Int. J. Cancer. 1996; 66: 711–2.
- Sandvej K., Peh S., Andresen B., Pallesen G. Identification of potential hot spots in the carboxy-terminal part of the EpsteinBarr virus (EBV) BNLF-1 gene in both malignant and benign EBV-associated diseases: high frequency of a 30 –bp deletion in Malaysian and Danish periferal T-cell lymphomas. Blood. 1994; 84: 4053–60.
- Knecht H., Bachmann E., Brousset P., Rothenbergar S., Einsele H., Lestou V. et al. Mutational hot spots within the carboxy terminal region of the LMP1 oncogene of Epstein-Barr virus are frequent in lymphoproliferative disorders. Oncogene. 1995; 10: 523–8.
- Knecht H., Martius F., Bachmann E., Hoffman T., Zimmermann D., Rothenberger S. et al. A deletion mutant of the LMP-1 oncogene of Epstein-Barr virus is associated with evolution of angioimmunoblastic lymphadenopathy into B immunoblastic lymphoma. Leukemia. 1995; 9: 458.
- Dolcetti R., Zancai P., de Re V., Gloghini A., Bigoni B., Pivetta B. et al. Epstein-Barr virus strains with latent membrane protein-1 deletions: prevalence in the Italian population and high association with human immunodeficiency virus-related Hodgkin’s disease. Blood. 1997; 89: 1723–31.
- Khanim F., Yao Q.-Y., Niedobitek G., Sihota S., Rickinson A.B., Young L.S. Analysis of Epstein-Barr virus gene polymorphisms in normal donors and in virus-associated tumors from different geographic locations. Blood. 1996; 88(9): 3491–501.
- Sandvej K., Gratama J.W., Munch M., Zhou X.G., Bolhuis R.L., Andersen B.S. et al. Sequence analysis of the Epstein-Barr virus (EBV) latent membrane protein-1 gene and promoter region: identification of 4 variants among wild-type EBV isolates. Blood. 1997; 90: 323–30.
- Hayashi K., Chen W.-C., Chen Y.-Y., Murakami I., Chen H.-L., Ohara N. et al. Deletion of Epstein-Barr virus latent membrane protein 1 gene in Japanese and Brazilian gastric carcinomas, metastatic lesions, and reactive lymphocytes. Am. J. Pathol. 1998; 152(1): 191–8.
- Walling D., Shebib N., Weaver S., Nichols M.,. Flaitz C., WebsterCyriaque J. The molecular epidemiology and evolution of EpsteinBarr virus: sequence variation and genetic recombination in the latent membrane protein-1 gene. J. Infect. Dis. 1999; 179: 763–74.
- Itakura O., Yamada S., Narita M., Kikuta H. High prevalence of a 30-base pair deletion and single-base mutations within the carboxy terminal end of the LMP-1 oncogene of Epstein-Barr virus in the Japanese population. Oncogene. 1996; 13: 1549–53.
- Palefsky J., Berline J., Penaranda M., Lennette E., Greenspan D., Greenspan J. Sequence variation of latent membrane protein-1 of Epstein-Barr virus strains associated with hairy leukoplakia. J. Infect. Dis. 1996; 173: 710–4.
- Rothenberger S., Bachmann E., Knecht H. Molecular and functional analysis of the Epstein-Barr virus LMP1 oncogene promotor in lymphoproliferative diseases. Exp. Hematol. 1997; 25: 1326.
- Edwards R., Seillier Moisewitsch F., Raab-Traub N. Signature amino acids changes in latent membrane protein 1 distinguish Epstein-Barr virus strains. Virology. 1999; 261: 79–95.
- Tang W., Pavlish O.A., Spiegelman V.S., Parkhitko A.A., Fuchs S.Y. Interaction of Epstein-Barr virus latent membrane protein 1 with SCFHOS/β-TrCP E3 ubiquitin ligase regulates extent of NF-kB activation. J. Biol.Chem. 2003; 278(49): 48942–9.
- Смирнова К.В., Дидук С.В., Гурцевич В.Э. Функциональный анализ вариантов латентного мембранного белка 1 (LMP1) вируса Эпштейна-Барр у больных лимфопролиферативными заболеваниями. Биомедицинская химия. 2011; 57(1): 114–26.