Роль консервативных и гипервариабельных иммунодоминантных эпитопов внутренних белков вирусов гриппа А в формировании цитотоксического Т-клеточного иммунного ответа
- Авторы: Найхин А.Н.1, Лосев И.В.1
-
Учреждения:
- ФГБУ «НИИ экспериментальной медицины» СЗО РАМН
- Выпуск: Том 60, № 1 (2015)
- Страницы: 11-16
- Раздел: ОБЗОРЫ
- Дата подачи: 09.07.2020
- Дата принятия к публикации: 09.07.2020
- Дата публикации: 28.02.2015
- URL: https://virusjour.crie.ru/jour/article/view/307
- ID: 307
Цитировать
Полный текст
Аннотация
Цитотоксический Т-клеточный иммунитет имеет важное значение в предотвращении развития гриппозной инфекции и смягчении ее тяжести. Сведения о механизмах индукции вирусспецифических CD8+ Т-лимфоцитов (ВЦТЛ) у людей способствуют лучшему пониманию эпидемиологии гриппа и путей совершенствования его вакцинопрофилактики. В последние годы благодаря появлению новых иммунологических и генно-инженерных методик в мировой литературе накоплен материал об особенностях формирования ВЦТЛ-иммунного ответа к различным эпитопам внутренних белков вирусов гриппа А. В настоящем обзоре обобщены эти сведения. Основное внимание уделяется: (i) формированию гетеросубтипического ВЦТЛ-иммунного ответа к консервативным иммунодоминантным сайтам; (ii) механизмам ухода от контроля гриппозной инфекции хозяйскими ВЦТЛ с помощью эволюционных escape-мутаций; (iii) роли хозяйского HLA-гаплотипа на развитие этого типа иммунного ответа. Обсуждается важность цитируемых материалов для функциональной и прикладной иммунологии, а также для вакцинного дела.
Об авторах
А. Н. Найхин
ФГБУ «НИИ экспериментальной медицины» СЗО РАМН
Автор, ответственный за переписку.
Email: vaccine@mail.ru
Найхин Анатолий Нойевич, д-р мед. наук, проф.
197376, Санкт-Петербург
РоссияИ. В. Лосев
ФГБУ «НИИ экспериментальной медицины» СЗО РАМН
Email: fake@neicon.ru
197376, Санкт-Петербург Россия
Список литературы
- Taylor P.M., Askonas B.A. Influenza nucleoprotein-specific cytotoxic T-cell clones are protective in vivo. Immunology. 1986; 58 (3): 417– 20.
- McMichael A.J., Gotch F.M., Noble G.R., Beare P.A. Cytotoxic T-cell immunity to influenza. N. Engl. J. Med. 1983; 309 (1): 13–7.
- Yewdell J.W. Confronting complexity: real-world immunodominance in antiviral CD8+ T cell responses. Immunity. 2006; 25: 533–43.
- Boon A.C., de Mutsert G., Graus Y.M., Fouchier R.A., Sintnicolaas K., Osterhaus A.D., Rimmelzwaan G.F. The magnitude and specificity of influenza A virus-specific cytotoxic T-lymphocyte responses in humans is related to HLA-A and –B phenotype. Virol. 2002; 76: 582- 590.
- Chen W., Pang K., Masterman K.A. et al. Reversal in the immunodominance hierarchy in secondary CD8+ T cell responses to influenza A virus: roles for cross-presentation and lysis-independent immunodomination. J. Immunol. 2004; 173: 5021–7.
- Belz G.T., Xie W., Doherty P.C. Diversity of epitope and cytokine profiles for primary and secondary influenza A virus-specific CD8+ T cell responses. J. Immunol. 2001; 166: 4627–33.
- Boon A.C., de Mutsert G., Graus Y.M. et al. Sequence variation in a newly identified HLA-B35-restricted epitope in the influenza A virus nucleoprotein associated with escape from cytotoxic T lymphocytes. J. Virol. 2002; 76 (5): 2567–72.
- Boon A.C., de Mutsert G., Fouchier R.A., Osterhaus A.D., Rimmelzwaan G.F. The hypervariable immunodominant NP418–426 epitope from the influenza A virus nucleoprotein is recognized by cytotoxic T lymphocytes with high functional avidity. J. Virol. 2006; 80 (12): 6024–32.
- DiBrino M.T., Tsuchida T., Turner R.V. et al. An HLA-B35-restricted epitope modified at an anchor residue results in an antagonist peptide. Eur. J. Immunol. 1993; 26: 335–339.
- Huet S., Nixon D.F., Rothbard J.B. Structural homologies between two HLA B27–restricted peptides suggests residues important for interaction with HLA B27. Int. Immunol. 1990; 2: 311–6.
- McMichael A.J., Gotch F.M., Rothbard J. HLA B37 determines an influenza virus nucleoprotein epitope recognized by cytotoxic T lymphocytes. J. Exp. Med. 1986; 164: 1397–406.
- Rimmelzwaan G.F., Kreijtz J.H., Bodewes R., Fouchier R.A., Osterhaus A.D. Influenza virus CTL epitopes, remarkably conserved and remarkably variable. Vaccine. 2009; 27: 6363–5.
- Sutton J., Rowland-Jones S., Rosenberg W. et al. A sequence pattern for peptides presented to cytotoxic T lymphocytes by HLA B8 revealed by analysis of epitopes and eluted peptides. Eur. J. Immunol. 1993; 23: 447–453.
- Heiny A.T., Miotto O., Srinivasan K.N., Khan A.M., Zhang G.L., Brusic V. et al. Evolutionarily conserved protein sequences of influenza A viruses, avian and human, as vaccine targets. PloS ONE (2007)./ www.plosone.org/ Issue 11/e1190.
- Tan P.T., Heiny A.T., Miotto O., Salmon J., Marques E.T., Lemonnier F., August J.T.. Conservation and diversity of influenza A (H1N1) HLA-restricted T cell epitope candidates for epitope-based vaccines. PloS ONE (2010) / www.plosone.org/vol.5/Issue 1/e8754.
- Voeten J.T.M., Bestebroer N.M., Nieuwkoop N.J., Fouchier R.A., Osterhaus A.D., Rimmelzwaan G.F. Antigenic drift in the influenza A virus (H3N2) nucleoprotein and escape from recognition by cytotoxic T lymphocytes. J. Virol. 2000; 74 (15): 6800–7.
- Wu K.-W., Chien C.-Y., Li S.-W., King C.-C., Chang C.-H. Highly conserved influenza A virus epitope sequences as candidates of H3N2 flu vaccine targets. Genomics. 2012; doi: 10.1016/j. ygeno.2012.06.003.
- Marsh S., Parham P., Barber L. The HLA facts book. Academic Press, London. United Kingdom. 2000.
- Assarsson E., Bui H.-H., Sidney J., Zhang Q., Glenn J., Oseroff C. et al. Immunomic analysis of the repertoire of T-cell specificites for influenza A virus in humans. J. Virol. 2008; 82 (24): 12 241–51.
- Berkhoff E.G., Boon A.C., Nieuwkoop N.J., Fouchier R.A., Sintnicolaas K., Osterhaus A.D., Rimmelzwaan G.F. A mutation in the HLA-B82705-restricted NP383–391 epitope affects the human influenza A virus-specific cytotoxic T-lympocyte response in vitro. J. Virol. 2004; 78 (10): 5216–22.
- Berkhoff E.G., de Wit E., Geelhoed-Mieras M.M., Boon A.C., Symons J., Fouchier R.A. et al. Functional constraints of influenza A virus epitopes limit escape from cytotoxic T lymphocytes. J. Virol. 2005; 79: 11 239–46.
- Berkhoff E.G., Geelhoed-Mieras M.M., Fouchier R.A., Osterhaus A.D., Rimmelzwaan G.F. Assessment of the extent of variation in influenza A virus cytotoxic T-lymphocyte epitopes by using virusspecific CD8+ T-cell clones. J. General Virology. 2007; 88: 530–5.
- Stanekova Z., Vareckova E. Conserved epitopes of influenza A virus inducing protective immunity and their prospects for universal vaccine development. Virology J. 2010; 7: 351.
- Найхин А.Н. Противогриппозный иммунитет: отечественный вклад в изучение проблемы и перспективные направления развития исследований. Мед. академ. журнал. 2010; 10 (4): 249–55. [Naykhin A.N. Anti-influenza immunity: the contribution of Russian scientists to the research work and promising directions. Med. Academic J. 2010; 10 (4): 249–55]. (in Russian)
- Найхин А.Н., Чиркова Т.В.. Петухова Г.Д., Кореньков Д.А., Донина С.А., Руденко Л.Г. Стимуляция гомо- и гетерологической Т-клеточной иммунологической памяти у волонтеров, привитых живой реассортантной гриппозной вакциной типа А(Н5N2). Вопросы вирусологии. 2012; 1: 38–42. [Naikhin A.N., Chirkova T.V., Petukhova G.D., Korenkov D.A., Donina S.A., Rudenko L.G. Stimulation of homo- and heterologic T-cell immunological memory in volunteers inoculated with live influenza A (H5N2) reassortant vaccine. Voprosy virusologii. 2012; 1: 38–42]. (in Russian)
- Найхин А.Н. Гетеросубтипический иммунитет к вирусам гриппа А: эпидемиологические данные, вовлеченность разных иммунологических факторов, вакцинация. Вопросы вирусологии. 2012; 57 (3): 4–9. [Naikhin A.N. Heterosubtypic immunity to influenza A viruses: epidemiological data, involvement of different immunological factors, vaccination. Voprosy virusologii. 2012; 57 (3): 4–9]. (in Russian)
- Epstein S.L. Prior H1N1 influenza infection and susceptibility of Cleveland Family Study participants during the H2N2 pandemic of 1957: an experiment of nature. J. Infect. Dis. 2006; 193 (1): 49–53.
- Grebe K.M., Yewdell J.W., Bennink J.R. Heterosubtypic immunity to influenza A virus: where do we stend? Microbes Infect. 2008; 10 (July (9)): 1024–9.
- Kreijtz J.H., Bodewes R., van Amerongen G. et al. Primary influenza A virus infection induces cross-protective immunity against a lethal infection with a heterosubtypic virus strain in mice. Vaccine. 2007; 25 (January(4)): 612–20.
- Kreijtz J.H., de Mutsert G., van Baalen C.A. et al. Cross-recognition of avian H5N1 influenza virus by human cytotoxic T-lymphocyte populations directed to human influenza A virus. J. Virol. 2008; 82 (11): 5161–6.
- Koup R.A. Virus escape from CTL recognition. J. Exp. Med. 1994; 180: 779–82.
- Oldstone M.B. How viruses escape from cytotoxic T lymphocytes: molecular parameters and players. Virology. 1997; 234: 179–85.
- Borrow P., Lewicki H., Wei X. et al. Antiviral pressure exerted by HIV-I-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat. Med. 1997; 3: 205–11.
- Jugovic P., Hill A.M., Tomazin R. et al. Inhibition of major histocompatibility complex class I antigen presentation in pig and primate cells by herpes simplex virus type 1 and 2 ICP47. J. Virol. 1998; 72: 5076–84.
- Khanna R., Burrows S.R., Argaet V., Moss D.J. Endoplasmie reticulum signal sequence facilitated transport of peptide epitopes restores immunogenicity of an antigen processing defective tumour cell line. Int. Immunol. 1994; 6: 639–45.
- Moskophidis D., Zinkernagel R.M. Immunobiology of cytotoxic Tcell escape mutants of lymphocytic choriomeningitis virus. J. Virol. 1995; 69: 2187–93.
- Pircher H.D., Moskophidis D., Rohrer U. et al. Viral escape by selection of cytotoxic T cell-resistant virus variants in vivo. Nature. 1990; 346: 629–33.
- Bertoletti A., Costanzo A., Chisari F.V. et al. Cytotoxic T lymphocyte response to a wild type hepatitis B virus epitope in patients chronically infected by variant viruses carrying substitutions within the epitope. J. Exp. Med. 1994; 180: 933–43.
- Bertoletti A., Sette A., Chisari F.V. et al. Natural variants of cytotoxic epitopes are T-cell receptor antagonists for antiviral cytotoxic T cells. Nature. 1994; 369: 407–10.
- Borrows J.M., Borrows S.R., Poulsen L.M. et al. Unusually high frequency of Epstein-Barr virus genetic variants in Papua New Guinea that can escape cytotoxic T-cell recognition: implications for virus evolution. J. Virol. 1996; 70: 2490–6.
- de Campos-Lima P.O., Levitsky V., Brooks J. et al. T cell responses and virus evolution: loss of HLA A11-restricted CTL epitopes in EpsteinBarr virus isolates from highly A11-positive populations by selective mutation of anchor residues. J. Exp. Med. 1994; 179: 1297–305.
- Guglietta S., Garbuglia A.R., Pacciani et al. Positive selection of cytotoxic T lymphocyte escape variants during acute hepatitis C virus infection. Eur. J. Immunol. 2005; 35: 2627–37.
- Man S., Newbery H., Crotzer V.l. et al. Definition of human T cell epitope from influenza A non-structural protein 1 using HLA-A21 transgenic mice. Inf. Immunol. 1995; 7: 597–605.
- Rimmelzwaan G.F., Fouchier R.A., Osterhaus A. Influenza virusspecific cytotoxic T lymphocytes: a correlate of protection and a basis for vaccine development. Current Opinion in Biotechnology. 2007; 18: 529–36.
- Ploegh H.L. Viral strategies of immune evasion. Science. 1998; 280: 248–53.
- Boon A.C., de Mutsert G., van Baarle D., Smith D.J., Lapedes A.S., Fouchier R.A. et al. Recognition of homo- and heterosubtypic variants of influenza A viruses by human CD8+ T lymphocytes. J. Immunol. 2004; 172: 2453–60.
- Portela A., Digard Р. The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J. Gen. Virol. 2002; 83 (April (Pt 4)): 723–34.
- Gog J.R., Rimmelzwaan G.F., Osterhaus A.D. Grenfell B.T. Population dynamics of rapid fixation in cytotoxic T lymphocyte escape mutants of influenza A. PNAS. 2003; 100 (19): 11 143–7.
- Macken C., Lu H., Goodman J., Boykin L. The value of a database in surveillance and vaccine selection. Options for the control of influenza IV. Elsevier Science. Amsterdam. The Netherlands, 2001: 103–6.
- Rimmelzwaan G.F., Berkhoff E.G., Nieuwkoop N. J. et al. Functional compensation of a detrimental amino acid substitution in a cytotoxic-T-lymphocyte epitope of influenza A viruses by comutations. J. Virolog. 2004; 78 (16): 8946–9.
- Rimmelzwaan G.F., Berkhoff E.G., Nieuwkoop N.J., Smith D.J., Fouchier R.A., Osterhaus A.D. Full restoration of viral fitness by multiple compensatory co-mutations in the nucleoprotein of influenza A virus cytotoxic T-lymphocyte escape mutants. J. General Virology. 2005; 86: 1801–5.
- Alexander-Miller M.A. High-avidity Cd8+ T cell: optimal soldiers in the war against viruses and tumors. Immonol. Res. 2005; 31: 13–24.
- Derby M., Alexander-Miller M., Tse R., Berzofsky J. High-avidity CTL exploit two complementary mechanisms to provide better protection against viral infection than low-avidity CTL. J. Immunol. 2001; 166: 1690–7.
- O’Connor D.H., Allen T.M., Vogel T.U. et al. Acute phase cytotoxic T lymphocyte escape is a hallmark of simian immunodeficiency virus infection. Nat. Med. 2002; 8: 493–9.
- Zeh H.J., Perry-Lalley III.D., Dudley M.E. High-avidity CTLs for two self-antigens demonstrate superior in vitro and in vivo antitumor efficacy. J. Immunol. 1999; 162: 989–94.
- Berkhoff E.G., Geelhoed-Mieras M.M., Verschuren E.J., Baalen C.A., Gruters R.A., Fouchier R.A., Osterhaus A.D., Rimmelzwaan G.F. The loss of immunodominant epitopes affects interferon-γ production and lytic activity of the human influenza virus-specific cytotoxic T lymphocyte response in vitro. J. Clinical and Exp. Immunol. 2007; 148: 296–306.
- Bodewes R., Geelhoed-Mieras M.M., Nieuwkoop N.J., Hanson J.A., David C.S., Fouchier R.A., Osterhaus A.D., Rimmelzwaan G.F. Redundancy of the influenza A virus-specific cytotoxic T lymphocyte response in HLA-B*2705 transgenic mice limits the impact of a mutation in the immunodominant NP383–391 epitope on influenza pathogenesis. Virus Research. 2011; 155: 123–30.
- Carrat F., Flahault F. Influenza vaccine: The challenge of antigenic drift. Vaccine. 2007; 25: 6852–62.
- EIhefnawi M., ALAidi O., Mohamed N., Kamar M., EI-Azab I., Zaba S., Siam R. Identification of novel conserved functional motifs across most influenza A viral strains. Virology J. 2011; 8: 44.
- Li C., Rappuoli R., Xu X.-N. Correlates of protection against influenza infection in humans – on the path to a universal vaccine? Current Opinion in Immunology. 2013; 25: 470–6.