Macavirus latency-associated protein evades immune detection through regulation of protein synthesis in cis depending upon its glycin/glutamate-rich domain - 2017
Macavirus latency-associated protein evades immune detection through regulation of protein synthesis in cis depending upon its glycin/glutamate-rich domain
Dewals, Benjamin G ; Université de Liège - ULiège > Immunologie et vaccinologie
Language :
English
Title :
Macavirus latency-associated protein evades immune detection through regulation of protein synthesis in cis depending upon its glycin/glutamate-rich domain
Publication date :
23 October 2017
Journal title :
PLoS Pathogens
ISSN :
1553-7366
eISSN :
1553-7374
Publisher :
Public Library of Science, San Francisco, United States - California
Thorley-Lawson DA, Gross A, Persistence of the Epstein-Barr virus and the origins of associated lymphomas. The New England journal of medicine. 2004;350(13):1328–37. doi: 10.1056/NEJMra032015 15044644.
Mesri EA, Cesarman E, Boshoff C, Kaposi's sarcoma and its associated herpesvirus. Nat Rev Cancer. 2010;10(10):707–19. Epub 2010/09/25. doi: 10.1038/nrc2888 20865011.
Verma SC, Robertson ES, Molecular biology and pathogenesis of Kaposi sarcoma-associated herpesvirus. FEMS microbiology letters. 2003;222(2):155–63. Epub 2003/05/29. 12770701.
Fleckenstein B, Ensser A, Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, Gammaherpesviruses of New World primates. In: et al., editors. Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis. Cambridge: Cambridge University Press; 2007.
Russell GC, Stewart JP, Haig DM, Malignant catarrhal fever: a review. Vet J. 2009;179(3):324–35. Epub 2008/09/02. doi: 10.1016/j.tvjl.2007.11.007 18760944.
Blake N, Lee S, Redchenko I, Thomas W, Steven N, Leese A, et al. Human CD8+ T cell responses to EBV EBNA1: HLA class I presentation of the (Gly-Ala)-containing protein requires exogenous processing. Immunity. 1997;7(6):791–802. 9430224.
Voo KS, Fu T, Wang HY, Tellam J, Heslop HE, Brenner MK, et al. Evidence for the presentation of major histocompatibility complex class I-restricted Epstein-Barr virus nuclear antigen 1 peptides to CD8+ T lymphocytes. The Journal of experimental medicine. 2004;199(4):459–70. doi: 10.1084/jem.20031219 14769850; PubMed Central PMCID: PMC2211826.
Lepone L, Rappocciolo G, Knowlton E, Jais M, Piazza P, Jenkins FJ, et al. Monofunctional and polyfunctional CD8+ T cell responses to human herpesvirus 8 lytic and latency proteins. Clinical and vaccine immunology: CVI. 2010;17(10):1507–16. doi: 10.1128/CVI.00189-10 20719985; PubMed Central PMCID: PMC2952991.
Plowright W, Ferris RD, Scott GR, Blue wildebeest and the aetiological agent of bovine malignant catarrhal fever. Nature. 1960;188:1167–9. Epub 1960/12/31. 13736396.
Plowright W, Dinter Z, MB Malignant catarrhal fever virus. In: Virus infections of ruminants. Amsterdam: Elsevier; 1990. p. 123–50.
Plowright W, Malignant Catarrhal Fever in East Africa. I. Behaviour of the Virus in Free-Living Populations of Blue Wildebeest (Gorgon Taurinus Taurinus, Burchell). Res Vet Sci. 1965;6:56–68. Epub 1965/01/01. 14281668.
Plowright W, Malignant Catarrhal Fever in East Africa. Ii. Observations on Wildebeest Calves at the Laboratory and Contact Transmission of the Infection to Cattle. Res Vet Sci. 1965;6:69–83. 14281669.
Lankester F, Lugelo A, Kazwala R, Keyyu J, Cleaveland S, Yoder J, The economic impact of malignant catarrhal fever on pastoralist livelihoods. PLoS One. 2015;10(1):e0116059. doi: 10.1371/journal.pone.0116059 25629896; PubMed Central PMCID: PMC4309580.
Bedelian C, Nkedianye D, Herrero M, Maasai perception of the impact and incidence of malignant catarrhal fever (MCF) in southern Kenya. Prev Vet Med. 2007;78(3–4):296–316. Epub 2006/11/25. S0167-5877(06)00226-1 [pii] doi: 10.1016/j.prevetmed.2006.10.012 17123651.
Cleaveland S, Kusiluka L, Kuwai J, Bell C, Kazwala R. Assessing the impact of malignant catarrhal fever in Ngorongoro district, Tanzania http://www.participatoryepidemiology.info/MCF Report.pdf: Nairobi: Community-based Animal Health and Participatory Epidemiology Unit (CAPE), Organization for African Unity; 2001 [cited 2010 13/11/2010].
Mlilo D, Mhlanga M, Mwembe R, Sisito G, Moyo B, Sibanda B, The epidemiology of malignant catarrhal fever (MCF) and contribution to cattle losses in farms around Rhodes Matopos National Park, Zimbabwe. Tropical animal health and production. 2015;47(5):989–94. doi: 10.1007/s11250-015-0821-8 25863958.
Castro AE, Heuschele WP, Conference on malignant catarrhal fever. The bovine practitioner. 1985;20:162–8.
Dewals B, Boudry C, Farnir F, Drion PV, Vanderplasschen A, Malignant catarrhal fever induced by alcelaphine herpesvirus 1 is associated with proliferation of CD8+ T cells supporting a latent infection. PLoS One. 2008;3(2):e1627. Epub 2008/02/21. doi: 10.1371/journal.pone.0001627 18286184; PubMed Central PMCID: PMC2229840.
Dewals B, Myster F, Palmeira L, Gillet L, Ackermann M, Vanderplasschen A, Ex vivo bioluminescence detection of alcelaphine herpesvirus 1 infection during malignant catarrhal fever. Journal of virology. 2011;85(14):6941–54. Epub 2011/05/20. doi: 10.1128/JVI.00286-11 21593175; PubMed Central PMCID: PMC3126570.
Dewals BG, Vanderplasschen A, Malignant catarrhal fever induced by Alcelaphine herpesvirus 1 is characterized by an expansion of activated CD3+CD8+CD4- T cells expressing a cytotoxic phenotype in both lymphoid and non-lymphoid tissues. Vet Res. 2011;42(1):95. Epub 2011/08/24. 1297-9716-42-95 [pii] doi: 10.1186/1297-9716-42-95 21859474; PubMed Central PMCID: PMC3166908.
Palmeira L, Sorel O, Van Campe W, Boudry C, Roels S, Myster F, et al. An essential role for gamma-herpesvirus latency-associated nuclear antigen homolog in an acute lymphoproliferative disease of cattle. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(21):E1933–42. Epub 2013/05/01. doi: 10.1073/pnas.1216531110 23630278; PubMed Central PMCID: PMC3666693.
Blake N, Immune evasion by gammaherpesvirus genome maintenance proteins. The Journal of general virology. 2010;91(Pt 4):829–46. Epub 2010/01/22. vir.0.018242–0 [pii] doi: 10.1099/vir.0.018242-0 20089802.
Tellam J, Fogg MH, Rist M, Connolly G, Tscharke D, Webb N, et al. Influence of translation efficiency of homologous viral proteins on the endogenous presentation of CD8+ T cell epitopes. The Journal of experimental medicine. 2007;204(3):525–32. doi: 10.1084/jem.20062508 17312009; PubMed Central PMCID: PMCPMC2137904.
Tellam J, Rist M, Connolly G, Webb N, Fazou C, Wang F, et al. Translation efficiency of EBNA1 encoded by lymphocryptoviruses influences endogenous presentation of CD8+ T cell epitopes. European journal of immunology. 2007;37(2):328–37. doi: 10.1002/eji.200636153 17236233.
Tellam J, Sherritt M, Thomson S, Tellam R, Moss DJ, Burrows SR, et al. Targeting of EBNA1 for rapid intracellular degradation overrides the inhibitory effects of the Gly-Ala repeat domain and restores CD8+ T cell recognition. The Journal of biological chemistry. 2001;276(36):33353–60. doi: 10.1074/jbc.M104535200 11435434.
Tellam J, Smith C, Rist M, Webb N, Cooper L, Vuocolo T, et al. Regulation of protein translation through mRNA structure influences MHC class I loading and T cell recognition. Proceedings of the National Academy of Sciences of the United States of America. 2008;105(27):9319–24. doi: 10.1073/pnas.0801968105 18591662; PubMed Central PMCID: PMC2453702.
Tellam JT, Lekieffre L, Zhong J, Lynn DJ, Khanna R, Messenger RNA sequence rather than protein sequence determines the level of self-synthesis and antigen presentation of the EBV-encoded antigen, EBNA1. PLoS pathogens. 2012;8(12):e1003112. doi: 10.1371/journal.ppat.1003112 23300450; PubMed Central PMCID: PMC3531512.
Tellam JT, Zhong J, Lekieffre L, Bhat P, Martinez M, Croft NP, et al. mRNA Structural constraints on EBNA1 synthesis impact on in vivo antigen presentation and early priming of CD8+ T cells. PLoS pathogens. 2014;10(10):e1004423. doi: 10.1371/journal.ppat.1004423 25299404; PubMed Central PMCID: PMC4192603.
Yin Y, Manoury B, Fahraeus R, Self-inhibition of synthesis and antigen presentation by Epstein-Barr virus-encoded EBNA1. Science. 2003;301(5638):1371–4. doi: 10.1126/science.1088902 12958359.
Zaldumbide A, Ossevoort M, Wiertz EJ, Hoeben RC, In cis inhibition of antigen processing by the latency-associated nuclear antigen I of Kaposi sarcoma herpes virus. Molecular immunology. 2007;44(6):1352–60. doi: 10.1016/j.molimm.2006.05.012 16828498.
Gao J, Coulson JM, Whitehouse A, Blake N, Reduction in RNA levels rather than retardation of translation is responsible for the inhibition of major histocompatibility complex class I antigen presentation by the glutamic acid-rich repeat of herpesvirus saimiri open reading frame 73. Journal of virology. 2009;83(1):273–82. doi: 10.1128/JVI.01532-08 18945762; PubMed Central PMCID: PMC2612310.
Kwun HJ, da Silva SR, Qin H, Ferris RL, Tan R, Chang Y, et al. The central repeat domain 1 of Kaposi's sarcoma-associated herpesvirus (KSHV) latency associated-nuclear antigen 1 (LANA1) prevents cis MHC class I peptide presentation. Virology. 2011;412(2):357–65. doi: 10.1016/j.virol.2011.01.026 21324504; PubMed Central PMCID: PMC3097433.
Kwun HJ, da Silva SR, Shah IM, Blake N, Moore PS, Chang Y, Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 mimics Epstein-Barr virus EBNA1 immune evasion through central repeat domain effects on protein processing. Journal of virology. 2007;81(15):8225–35. Epub 2007/05/25. JVI.00411-07 [pii] doi: 10.1128/JVI.00411-07 17522213; PubMed Central PMCID: PMC1951309.
Bennett NJ, May JS, Stevenson PG, Gamma-herpesvirus latency requires T cell evasion during episome maintenance. PLoS Biol. 2005;3(4):e120. Epub 2005/03/17. 04-PLBI-RA-0882R2 [pii] doi: 10.1371/journal.pbio.0030120 15769185; PubMed Central PMCID: PMC1065266.
Ensser A, Pflanz R, Fleckenstein B, Primary structure of the alcelaphine herpesvirus 1 genome. Journal of virology. 1997;71(9):6517–25. Epub 1997/09/01. 9261371; PubMed Central PMCID: PMC191927.
Tscharke DC, Karupiah G, Zhou J, Palmore T, Irvine KR, Haeryfar SM, et al. Identification of poxvirus CD8+ T cell determinants to enable rational design and characterization of smallpox vaccines. The Journal of experimental medicine. 2005;201(1):95–104. doi: 10.1084/jem.20041912 15623576; PubMed Central PMCID: PMC2212779.
Kisselev AF, Goldberg AL, Proteasome inhibitors: from research tools to drug candidates. Chem Biol. 2001;8(8):739–58. 11514224.
Anton LC, Yewdell JW, Translating DRiPs: MHC class I immunosurveillance of pathogens and tumors. Journal of leukocyte biology. 2014;95(4):551–62. doi: 10.1189/jlb.1113599 24532645; PubMed Central PMCID: PMC3958739.
Yewdell JW, DRiPs solidify: progress in understanding endogenous MHC class I antigen processing. Trends in immunology. 2011;32(11):548–58. doi: 10.1016/j.it.2011.08.001 21962745; PubMed Central PMCID: PMC3200450.
Yewdell JW, Anton LC, Bennink JR, Defective ribosomal products (DRiPs): a major source of antigenic peptides for MHC class I molecules?J Immunol. 1996;157(5):1823–6. 8757297.
Apcher S, Komarova A, Daskalogianni C, Yin Y, Malbert-Colas L, Fahraeus R, mRNA translation regulation by the Gly-Ala repeat of Epstein-Barr virus nuclear antigen 1. Journal of virology. 2009;83(3):1289–98. doi: 10.1128/JVI.01369-08 19019958; PubMed Central PMCID: PMC2620890.
Cardinaud S, Starck SR, Chandra P, Shastri N, The synthesis of truncated polypeptides for immune surveillance and viral evasion. PLoS One. 2010;5(1):e8692. doi: 10.1371/journal.pone.0008692 20098683; PubMed Central PMCID: PMCPMC2809100.
Murat P, Zhong J, Lekieffre L, Cowieson NP, Clancy JL, Preiss T, et al. G-quadruplexes regulate Epstein-Barr virus-encoded nuclear antigen 1 mRNA translation. Nature chemical biology. 2014;10(5):358–64. doi: 10.1038/nchembio.1479 24633353; PubMed Central PMCID: PMC4188979.
Levitskaya J, Sharipo A, Leonchiks A, Ciechanover A, Masucci MG, Inhibition of ubiquitin/proteasome-dependent protein degradation by the Gly-Ala repeat domain of the Epstein-Barr virus nuclear antigen 1. Proceedings of the National Academy of Sciences of the United States of America. 1997;94(23):12616–21. 9356498; PubMed Central PMCID: PMC25057.
Apcher S, Daskalogianni C, Lejeune F, Manoury B, Imhoos G, Heslop L, et al. Major source of antigenic peptides for the MHC class I pathway is produced during the pioneer round of mRNA translation. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(28):11572–7. doi: 10.1073/pnas.1104104108 21709220; PubMed Central PMCID: PMC3136330.
Lee SP, Brooks JM, Al-Jarrah H, Thomas WA, Haigh TA, Taylor GS, et al. CD8 T cell recognition of endogenously expressed epstein-barr virus nuclear antigen 1. The Journal of experimental medicine. 2004;199(10):1409–20. doi: 10.1084/jem.20040121 15148339; PubMed Central PMCID: PMC2211813.
Tellam J, Connolly G, Green KJ, Miles JJ, Moss DJ, Burrows SR, et al. Endogenous presentation of CD8+ T cell epitopes from Epstein-Barr virus-encoded nuclear antigen 1. The Journal of experimental medicine. 2004;199(10):1421–31. doi: 10.1084/jem.20040191 15148340; PubMed Central PMCID: PMC2211806.
Dolan BP, Li L, Veltri CA, Ireland CM, Bennink JR, Yewdell JW, Distinct pathways generate peptides from defective ribosomal products for CD8+ T cell immunosurveillance. J Immunol. 2011;186(4):2065–72. doi: 10.4049/jimmunol.1003096 21228349; PubMed Central PMCID: PMC3408966.
Kurts C, Robinson BW, Knolle PA, Cross-priming in health and disease. Nature reviews Immunology. 2010;10(6):403–14. doi: 10.1038/nri2780 20498667.
Coppotelli G, Mughal N, Marescotti D, Masucci MG, High avidity binding to DNA protects ubiquitylated substrates from proteasomal degradation. The Journal of biological chemistry. 2011;286(22):19565–75. doi: 10.1074/jbc.M111.224782 21471195; PubMed Central PMCID: PMCPMC3103336.
Kwun HJ, Toptan T, Ramos da Silva S, Atkins JF, Moore PS, Chang Y, Human DNA tumor viruses generate alternative reading frame proteins through repeat sequence recoding. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(41):E4342–9. doi: 10.1073/pnas.1416122111 25271323; PubMed Central PMCID: PMCPMC4205619.
Toptan T, Fonseca L, Kwun HJ, Chang Y, Moore PS, Complex alternative cytoplasmic protein isoforms of the Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 generated through noncanonical translation initiation. Journal of virology. 2013;87(5):2744–55. doi: 10.1128/JVI.03061-12 23255808; PubMed Central PMCID: PMCPMC3571394.
Zhang G, Chan B, Samarina N, Abere B, Weidner-Glunde M, Buch A, et al. Cytoplasmic isoforms of Kaposi sarcoma herpesvirus LANA recruit and antagonize the innate immune DNA sensor cGAS. Proceedings of the National Academy of Sciences of the United States of America. 2016;113(8):E1034–43. doi: 10.1073/pnas.1516812113 26811480; PubMed Central PMCID: PMCPMC4776510.
Myster F, Palmeira L, Sorel O, Bouillenne F, DePauw E, Schwartz-Cornil I, et al. Viral semaphorin inhibits dendritic cell phagocytosis and migration but is not essential for gammaherpesvirus-induced lymphoproliferation in malignant catarrhal fever. Journal of virology. 2015;89(7):3630–47. doi: 10.1128/JVI.03634-14 25589653; PubMed Central PMCID: PMC4403426.
Plowright W, Herniman KA, Jessett DM, Kalunda M, Rampton CS, Immunisation of cattle against the herpesvirus of malignant catarrhal fever: failure of inactivated culture vaccines with adjuvant. Res Vet Sci. 1975;19(2):159–66. Epub 1975/09/01. 1166120.
Storkus WJ, Zeh HJ, 3rd, Salter RD, Lotze MT, Identification of T-cell epitopes: rapid isolation of class I-presented peptides from viable cells by mild acid elution. Journal of immunotherapy with emphasis on tumor immunology: official journal of the Society for Biological Therapy. 1993;14(2):94–103. 7506576.
