Abstract
Over the past decade, we have seen an alarming number of high-profile outbreaks of newly emerging and re-emerging viruses. Recent outbreaks of avian influenza viruses, Middle East respiratory syndrome coronaviruses, Zika virus and Ebola virus present great threats to global health. Considering the pivotal role of host T-cell immunity in the alleviation of symptoms and the clearance of viruses in patients, there are three issues to be primarily concerned about T-cell immunity when a new virus emerges: first, does the population possess pre-existing T-cells against the new virus through previous infections of genetically relevant viruses; second, does a proper immune response arise in the patients to provide protection through an immunopathogenic effect; lastly, how long can the virus-specific immune memory persist. Herein, we summarize the current updates on the characteristics of human T-cell immunological responses against recently emerged or re-emerged viruses, and emphasize the necessity for timely investigation on the T-cell features of these viral diseases, which may provide beneficial recommendations for clinical diagnosis and vaccine development.
Keywords: emerging viruses, avian influenza, H7N9, MERS-CoV, Zika, Ebola, human immunity, T-cell, cross-reactivity
Acknowledgements
We are grateful to Professor Fuping Zhang, Ms. Huarong Huang, Mr. Kun Xu, and Ms. Yongli Zhang for their kind assistance with the preparation of this manuscript. This work was supported by the National Key Research and Development Program of China (2017YFC1200202), the China Mega-Project on Infectious Disease Prevention (2016ZX10004222-003), and the National Natural Science Foundation of China (81401312, 81373141). George F. Gao is a leading principal investigator at the National Natural Science Foundation of China Innovative Research Group (81621091).
References
- Al-Qahtani A.A., Lyroni K., Aznaourova M., Tseliou M., Al-Anazi M. R., Al-Ahdal M.N., Alkahtani S., Sourvinos G., Tsatsanis C. Middle east respiratory syndrome corona virus spike glycoprotein suppresses macrophage responses via DPP4-mediated induction of IRAK-M and PPARgamma. Oncotarget. 2017;8:9053–9066. doi: 10.18632/oncotarget.14754. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Assiri A., Al-Tawfiq J.A., Al-Rabeeah A.A., Al-Rabiah F.A., Al-Hajjar S., Al-Barrak A., Flemban H., Al-Nassir W.N., Balkhy H.H., Al-Hakeem R.F., Makhdoom H.Q., Zumla A.I., Memish Z.A. Epidemiological, demographic, and clinical characteristics of 47 cases of Middle East respiratory syndrome coronavirus disease from Saudi Arabia: a descriptive study. Lancet Infect Dis. 2013;13:752–761. doi: 10.1016/S1473-3099(13)70204-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baize S., Leroy E.M., Georges-Courbot M.C., Capron M., Lansoud-Soukate J., Debré P., Fisher-Hoch S.P., McCormick J.B., Georges A.J. Defective humoral responses and extensive intravascular apoptosis are associated with fatal outcome in Ebola virus-infected patients. Nat Med. 1999;5:423–426. doi: 10.1038/7422. [DOI] [PubMed] [Google Scholar]
- Baize S., Pannetier D., Oestereich L., Rieger T., Koivogui L., Magassouba N.F., Soropogui B., Sow M.S., Keïta S., De Clerck H., Tiffany A., Dominguez G., Loua M., Traoré A., Kolié M., Malano E.R., Heleze E., Bocquin A., Mély S., Raoul H., Caro V., Cadar D., Gabriel M., Pahlmann M., Tappe D., Schmidt-Chanasit J., Impouma B., Diallo A.K., Formenty P., Van Herp M., Günther S. Emergence of Zaire Ebola virus disease in Guinea. N Engl J Med. 2014;371:1418–1425. doi: 10.1056/NEJMoa1404505. [DOI] [PubMed] [Google Scholar]
- Bardina S.V., Bunduc P., Tripathi S., Duehr J., Frere J.J., Brown J.A., Nachbagauer R., Foster G.A., Krysztof D., Tortorella D., Stramer S. L., García-Sastre A., Krammer F., Lim J.K. Enhancement of Zika virus pathogenesis by preexisting antiflavivirus immunity. Science. 2017;356:175–180. doi: 10.1126/science.aal4365. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blom K., Sandberg J.T., Loré K., Ljunggren H.G. Prospects for induction of CD8 T cell-mediated immunity to Zika virus infection by yellow fever virus vaccination. J Intern Med. 2017;282:206–208. doi: 10.1111/joim.12638. [DOI] [PubMed] [Google Scholar]
- Brasil P., Calvet G.A., Siqueira A.M., Wakimoto M., de Sequeira P.C., Nobre A., Quintana M.S.B., Mendonça M.C.L., Lupi O., de Souza R.V., Romero C., Zogbi H., Bressan C.S., Alves S.S., Lourenço-de-Oliveira R., Nogueira R.M.R., Carvalho M.S., de Filippis A.M.B., Jaenisch T. Zika virus outbreak in Rio de Janeiro, Brazil: clinical characterization, epidemiological and virological aspects. PLoS Negl Trop Dis. 2016;10:e0004636. doi: 10.1371/journal.pntd.0004636. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Calvet G., Aguiar R.S., Melo A.S.O., Sampaio S.A., de Filippis I., Fabri A., Araujo E.S.M., de Sequeira P.C., de Mendonça M.C.L., de Oliveira L., Tschoeke D.A., Schrago C.G., Thompson F.L., Brasil P., dos Santos F.B., Nogueira R.M.R., Tanuri A., de Filippis A.M.B. Detection and sequencing of Zika virus from amniotic fluid of fetuses with microcephaly in Brazil: a case study. Lancet Infect Dis. 2016;16:653–660. doi: 10.1016/S1473-3099(16)00095-5. [DOI] [PubMed] [Google Scholar]
- Cao-Lormeau V.M., Blake A., Mons S., Lastère S., Roche C., Vanhomwegen J., Dub T., Baudouin L., Teissier A., Larre P., Vial A.L., Decam C., Choumet V., Halstead S.K., Willison H.J., Musset L., Manuguerra J.C., Despres P., Fournier E., Mallet H.P., Musso D., Fontanet A., Neil J., Ghawché F. Guillain-Barré Syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet. 2016;387:1531–1539. doi: 10.1016/S0140-6736(16)00562-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cha R.H., Joh J.S., Jeong I., Lee J.Y., Shin H.S., Kim G., Kim Y., Kim Y. Renal complications and their prognosis in Korean Patients with Middle East respiratory syndrome-coronavirus from the Central MERS-CoV Designated Hospital. J Korean Med Sci. 2015;30:1807–1814. doi: 10.3346/jkms.2015.30.12.1807. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Channappanavar R., Perlman S. Pathogenic human coronavirus infections: causes and consequences of cytokine storm and immunopathology. Semin Immunopathol. 2017;39:529–539. doi: 10.1007/s00281-017-0629-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen J., Cui G., Lu C., Ding Y., Gao H., Zhu Y., Wei Y., Wang L., Uede T., Li L., Diao H. Severe infection with avian influenza A virus is associated with delayed immune recovery in survivors. Medicine. 2016;95:e2606. doi: 10.1097/MD.0000000000002606. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chowell G., Nishiura H. Transmission dynamics and control of Ebola virus disease (EVD): a review. BMC Med. 2014;12:196. doi: 10.1186/s12916-014-0196-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chu K.H., Tsang W.K., Tang C.S., Lam M.F., Lai F.M., To K.F., Fung K.S., Tang H.L., Yan W.W., Chan H.W.H., Lai T.S.T., Tong K.L., Lai K.N. Acute renal impairment in coronavirus-associated severe acute respiratory syndrome. Kidney Int. 2005;67:698–705. doi: 10.1111/j.1523-1755.2005.67130.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cobey S., Hensley S.E. Immune history and influenza virus susceptibility. Curr Opin Virol. 2017;22:105–111. doi: 10.1016/j.coviro.2016.12.004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- D’Ortenzio E., Matheron S., Yazdanpanah Y., de Lamballerie X., Hubert B., Piorkowski G., Maquart M., Descamps D., Damond F., Leparc-Goffart I. Evidence of sexual transmission of Zika Virus. N Engl J Med. 2016;374:2195–2198. doi: 10.1056/NEJMc1604449. [DOI] [PubMed] [Google Scholar]
- de Araújo T.V.B., Rodrigues L.C., de Alencar Ximenes R.A., de Barros Miranda-Filho D., Montarroyos U.R., de Melo A.P.L., Valongueiro S., de Albuquerque M.F.P.M., Souza W.V., Braga C., Filho S.P.B., Cordeiro M.T., Vazquez E., Di Cavalcanti Souza Cruz D., Henriques C.M.P., Bezerra L.C.A., da Silva Castanha P.M., Dhalia R., Marques-Júnior E.T.A., Martelli C.M.T. Association between Zika virus infection and microcephaly in Brazil, January to May, 2016: preliminary report of a case-control study. Lancet Infect Dis. 2016;16:1356–1363. doi: 10.1016/S1473-3099(16)30318-8. [DOI] [PubMed] [Google Scholar]
- de Groot R.J., Baker S.C., Baric R.S., Brown C.S., Drosten C., Enjuanes L., Fouchier R.A.M., Galiano M., Gorbalenya A.E., Memish Z. A., Perlman S., Poon L.L.M., Snijder E.J., Stephens G.M., Woo P.C.Y., Zaki A.M., Zambon M., Ziebuhr J. Middle East respiratory syndrome coronavirus (MERS-CoV): announcement of the coronavirus study group. J Virol. 2013;87:7790–7792. doi: 10.1128/JVI.01244-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deng Y.Q., Zhao H., Li X.F., Zhang N.N., Liu Z.Y., Jiang T., Gu D.Y., Shi L., He J.A., Wang H.J., Sun Z.Z., Ye Q., Xie D.Y., Cao W.C., Qin C.F. Isolation, identification and genomic characterization of the Asian lineage Zika virus imported to China. Sci China Life Sci. 2016;59:428–430. doi: 10.1007/s11427-016-5043-4. [DOI] [PubMed] [Google Scholar]
- Diao H., Cui G., Wei Y., Chen J., Zuo J., Cao H., Chen Y., Yao H., Tian Z., Li L. Severe H7N9 infection is associated with decreased antigen-presenting capacity of CD14+ cells. PLoS ONE. 2014;9:e92823. doi: 10.1371/journal.pone.0092823. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dick G.W.A., Kitchen S.F., Haddow A.J. Zika Virus (I) Isolations and serological specificity. Trans R Soc Tropical Med Hygiene. 1952;46:509–520. doi: 10.1016/0035-9203(52)90042-4. [DOI] [PubMed] [Google Scholar]
- Duan S., Meliopoulos V.A., McClaren J.L., Guo X.Z.J., Sanders C.J., Smallwood H.S., Webby R.J., Schultz-Cherry S.L., Doherty P.C., Thomas P.G. Diverse heterologous primary infections radically alter immunodominance hierarchies and clinical outcomes following H7N9 influenza challenge in mice. PLoS Pathog. 2015;11:e1004642. doi: 10.1371/journal.ppat.1004642. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Duvvuri V.R., Duvvuri B., Alice C., Wu G.E., Gubbay J.B., Wu J. Preexisting CD4+ T-cell immunity in human population to avian influenza H7N9 virus: whole proteome-wide immunoinformatics analyses. PLoS ONE. 2014;9:e91273. doi: 10.1371/journal.pone.0091273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Elong Ngono A., Vizcarra E.A., Tang W.W., Sheets N., Joo Y., Kim K., Gorman M.J., Diamond M.S., Shresta S. Mapping and role of the CD8+ T cell response during primary Zika virus infection in mice. Cell Host Microbe. 2017;21:35–46. doi: 10.1016/j.chom.2016.12.010. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Faure E., Poissy J., Goffard A., Fournier C., Kipnis E., Titecat M., Bortolotti P., Martinez L., Dubucquoi S., Dessein R., Gosset P., Mathieu D., Guery B. Distinct immune response in two MERS-CoV-infected patients: can we go from bench to bedside? PLoS ONE. 2014;9:e88716. doi: 10.1371/journal.pone.0088716. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gao H., Yao H., Yang S., Li L. From SARS to MERS: evidence and speculation. Front Med. 2016;10:377–382. doi: 10.1007/s11684-016-0466-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gao H.N., Lu H.Z., Cao B., Du B., Shang H., Gan J.H., Lu S.H., Yang Y.D., Fang Q., Shen Y.Z., Xi X.M., Gu Q., Zhou X.M., Qu H.P., Yan Z., Li F.M., Zhao W., Gao Z.C., Wang G.F., Ruan L.X., Wang W.H., Ye J., Cao H.F., Li X.W., Zhang W.H., Fang X.C., He J., Liang W.F., Xie J., Zeng M., Wu X.Z., Li J., Xia Q., Jin Z.C., Chen Q., Tang C., Zhang Z.Y., Hou B.M., Feng Z.X., Sheng J.F., Zhong N.S., Li L.J. Clinical findings in 111 cases of influenza A (H7N9) virus infection. N Engl J Med. 2013;368:2277–2285. doi: 10.1056/NEJMoa1305584. [DOI] [PubMed] [Google Scholar]
- Goraya M.U., Wang S., Munir M., Chen J.L. Induction of innate immunity and its perturbation by influenza viruses. Protein Cell. 2015;6:712–721. doi: 10.1007/s13238-015-0191-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Govero J., Esakky P., Scheaffer S.M., Fernandez E., Drury A., Platt D. J., Gorman M.J., Richner J.M., Caine E.A., Salazar V., Moley K.H., Diamond M.S. Zika virus infection damages the testes in mice. Nature. 2016;540:438–442. doi: 10.1038/nature20556. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grant E.J., Quiñones-Parra S.M., Clemens E.B., Kedzierska K. Human influenza viruses and CD8+ T cell responses. Curr Opin Virol. 2016;16:132–142. doi: 10.1016/j.coviro.2016.01.016. [DOI] [PubMed] [Google Scholar]
- Da Guan W., Mok C.K.P., Chen Z.L., Feng L.Q., Li Z.T., Huang J.C., Ke C.W., Deng X., Ling Y., Wu S.G., Niu X.F., Perera R.A., Da Xu Y., Zhao J., Zhang L.Q., Li Y.M., Chen R.C., Peiris M., Chen L., Zhong N.S. Characteristics of traveler with Middle East respiratory syndrome, China, 2015. Emerg Infect Dis. 2015;21:2278–2280. doi: 10.3201/eid2112.151232. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Guo J., Huang F., Liu J., Chen Y., Wang W., Cao B., Zou Z., Liu S., Pan J., Bao C., Zeng M., Xiao H., Gao H., Yang S., Zhao Y., Liu Q., Zhou H., Zhu J., Liu X., Liang W., Yang Y., Zheng S., Yang J., Diao H., Su K., Shao L., Cao H., Wu Y., Zhao M., Tan S., Li H., Xu X., Wang C., Zhang J., Wang L., Wang J., Xu J., Li D., Zhong N., Cao X., Gao G.F., Li L., Jiang C. The serum profile of hypercytokinemia factors identified in H7N9-infected patients can predict fatal outcomes. Sci Rep. 2015;5:10942. doi: 10.1038/srep10942. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Halstead S.B. Dengue. Lancet. 2007;370:1644–1652. doi: 10.1016/S0140-6736(07)61687-0. [DOI] [PubMed] [Google Scholar]
- Hazin A.N., Poretti A., Di Cavalcanti Souza Cruz D., Tenorio M., van der Linden A., Pena L.J., Brito C., Gil L.H.V., de Barros Miranda-Filho D., Marques E.T.A., Turchi Martelli C.M., Alves J.G.B., Huisman T.A., Huisman T.A. Computed tomographic findings in microcephaly associated with Zika virus. N Engl J Med. 2016;374:2193–2195. doi: 10.1056/NEJMc1603617. [DOI] [PubMed] [Google Scholar]
- Hong K.H., Choi J.P., Hong S.H., Lee J., Kwon J.S., Kim S.M., Park S. Y., Rhee J.Y., Kim B.N., Choi H.J., Shin E.C., Pai H., Park S.H., Kim S.H. Thorax in press. 2017. Predictors of mortality in Middle East respiratory syndrome (MERS) [DOI] [PubMed] [Google Scholar]
- Huang F., Guo J., Zou Z., Liu J., Cao B., Zhang S., Li H., Wang W., Sheng M., Liu S., Pan J., Bao C., Zeng M., Xiao H., Qian G., Hu X., Chen Y., Chen Y., Zhao Y., Liu Q., Zhou H., Zhu J., Gao H., Yang S., Liu X., Zheng S., Yang J., Diao H., Cao H., Wu Y., Zhao M., Tan S., Guo D., Zhao X., Ye Y., Wu W., Xu Y., Penninger J.M., Li D., Gao G.F., Jiang C., Li L. Angiotensin II plasma levels are linked to disease severity and predict fatal outcomes in H7N9-infected patients. Nat Commun. 2014;5:3595. doi: 10.1038/ncomms4595. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huang H., Li S., Zhang Y., Han X., Jia B., Liu H., Liu D., Tan S., Wang Q., Bi Y., Liu W.J., Hou B., Gao G.F., Zhang F. CD8+ T cell immune response in immunocompetent mice during Zika virus infection. J Virol. 2017;91:e00900–17. doi: 10.1128/JVI.00900-17. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kam Y.W., Leite J.A., Lum F.M., Tan J.J.L., Lee B., Judice C.C., Teixeira D.A.T., Andreata-Santos R., Vinolo M.A., Angerami R., Resende M.R., Freitas A.R.R., Amaral E., Junior R.P., Costa M.L., Guida J.P., Arns C.W., Ferreira L.C.S., Renia L., Proenca-Modena J. L., Ng L.F.P., Costa F.T.M., Zika-Unicamp N. Specific biomarkers associated with neurological complications and congenital central nervous system abnormalities from Zika virus-infected patients in Brazil. J Infect Dis. 2017;216:172–181. doi: 10.1093/infdis/jix261. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klenerman P., Zinkernagel R.M. Original antigenic sin impairs cytotoxic T lymphocyte responses to viruses bearing variant epitopes. Nature. 1998;394:482–485. doi: 10.1038/28860. [DOI] [PubMed] [Google Scholar]
- Kun Xu Y.S. J Virol in press. 2017. Recombinant Chimpanzee Adenovirus Vaccine Ad- C7-M/E protects against Zika virus infection and testis damage. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lai L., Rouphael N., Xu Y., Natrajan M.S., Beck A., Hart M., Feldhammer M., Feldpausch A., Hill C., Wu H., Fairley J.K., Lankford- Turner P., Kasher N., Rago P., Hu Y.J., Edupuganti S., Patel S.M., Murray K.O., Mulligan M.J., Mulligan M.J. Clin Infect Dis in press. 2017. OUP accepted manuscript. [Google Scholar]
- Lan J., Deng Y., Chen H., Lu G., Wang W., Guo X., Lu Z., Gao G.F., Tan W. Tailoring subunit vaccine immunity with adjuvant combinations and delivery routes using the Middle East respiratory coronavirus (MERS-CoV) receptor-binding domain as an antigen. PLoS ONE. 2014;9:e112602. doi: 10.1371/journal.pone.0112602. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee L.Y., Ha do L.A., Simmons C., de Jong M.D., Chau N.V., Schumacher R., Peng Y.C., McMichael A.J., Farrar J.J., Smith G.L., Townsend A.R., Askonas B.A., Rowland-Jones S., Dong T. Memory T cells established by seasonal human influenza A infection cross-react with avian influenza A (H5N1) in healthy individuals. J Clin Invest. 2008;118:3478–3490. doi: 10.1172/JCI32460. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu J., Sun Y., Qi J., Chu F., Wu H., Gao F., Li T., Yan J., Gao G. F. The membrane protein of severe acute respiratory syndrome coronavirus acts as a dominant immunogen revealed by a clustering region of novel functionally and structurally defined cytotoxic T-lym- phocyte epitopes. J Infect Dis. 2010;202:1171–1180. doi: 10.1086/656315. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu J., Wu B., Zhang S., Tan S., Sun Y., Chen Z., Qin Y., Sun M., Shi G., Wu Y., Sun M., Liu N., Ning K., Ma Y., Gao B., Yan J., Zhu F., Wang H., Gao G.F. Conserved epitopes dominate cross- CD8+ T-cell responses against influenza A H1N1 virus among Asian populations. Eur J Immunol. 2013;43:2055–2069. doi: 10.1002/eji.201343417. [DOI] [PubMed] [Google Scholar]
- Liu J., Wu P., Gao F., Qi J., Kawana-Tachikawa A., Xie J., Vavricka C. J., Iwamoto A., Li T., Gao G.F. Novel immunodominant peptide presentation strategy: a featured HLA-A*2402-restricted cytotoxic T-lymphocyte epitope stabilized by intrachain hydrogen bonds from severe acute respiratory syndrome coronavirus nucleocapsid protein. J Virol. 2010;84:11849–11857. doi: 10.1128/JVI.01464-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu J., Xiao H., Wu Y., Liu D., Qi X., Shi Y., Gao G.F. H7N9: a low pathogenic avian influenza A virus infecting humans. Curr Opin Virol. 2014;5:91–97. doi: 10.1016/j.coviro.2014.03.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu J., Zhang S., Tan S., Yi Y., Wu B., Cao B., Zhu F., Wang C., Wang H., Qi J., Gao G.F. Cross-allele cytotoxic T lymphocyte responses against 2009 pandemic H1N1 influenza A virus among HLAA24 and HLA-A3 supertype-positive individuals. J Virol. 2012;86:13281–13294. doi: 10.1128/JVI.01841-12. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu J., Zhang S., Tan S., Zheng B., Gao G.F. Revival of the identification of cytotoxic T-lymphocyte epitopes for immunological diagnosis, therapy and vaccine development. Exp Biol Med (Maywood) 2011;236:253–267. doi: 10.1258/ebm.2010.010278. [DOI] [PubMed] [Google Scholar]
- Liu W.J. On the ground in Western Africa: from the outbreak to the elapse of Ebola. Protein Cell. 2016;7:621–623. doi: 10.1007/s13238-016-0305-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu W.J., Lan J., Liu K., Deng Y., Yao Y., Wu S., Chen H., Bao L., Zhang H., Zhao M., Wang Q., Han L., Chai Y., Qi J., Zhao J., Meng S., Qin C., Gao G.F., Tan W. Protective T cell responses featured by concordant recognition of Middle East respiratory syndrome coronavirus-derived CD8+ T cell epitopes and host MHC. J Immunol. 2017;198:873–882. doi: 10.4049/jimmunol.1601542. [DOI] [PubMed] [Google Scholar]
- Liu W.J., Tan S., Zhao M., Quan C., Bi Y., Wu Y., Zhang S., Zhang H., Xiao H., Qi J., Yan J., Liu W., Yu H., Shu Y., Wu G., Gao G.F. Cross-immunity against avian influenza A(H7N9) virus in the healthy population is affected by antigenicity-dependent substitutions. J Infect Dis. 2016;214:1937–1946. doi: 10.1093/infdis/jiw471. [DOI] [PubMed] [Google Scholar]
- Liu W.J., Zhao M., Liu K., Xu K., Wong G., Tan W., Gao G.F. T-cell immunity of SARS-CoV: implications for vaccine development against MERS-CoV. Antiviral Res. 2017;137:82–92. doi: 10.1016/j.antiviral.2016.11.006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ma W., Li S., Ma S., Jia L., Zhang F., Zhang Y., Zhang J., Wong G., Zhang S., Lu X., Liu M., Yan J., Li W., Qin C., Han D., Qin C., Wang N., Li X., Gao G.F. Zika virus causes testis damage and leads to male infertility in mice. Cell. 2016;167:1511–1524. doi: 10.1016/j.cell.2016.11.016. [DOI] [PubMed] [Google Scholar]
- Mandl J.N., Ahmed R., Barreiro L.B., Daszak P., Epstein J.H., Virgin H.W., Feinberg M.B. Reservoir host immune responses to emerging zoonotic viruses. Cell. 2015;160:20–35. doi: 10.1016/j.cell.2014.12.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mansuy J.M., Dutertre M., Mengelle C., Fourcade C., Marchou B., Delobel P., Izopet J., Martin-Blondel G. Zika virus: high infectious viral load in semen, a new sexually transmitted pathogen. Lancet Infect Dis. 2016;16:405. doi: 10.1016/S1473-3099(16)00138-9. [DOI] [PubMed] [Google Scholar]
- McElroy A.K., Akondy R.S., Davis C.W., Ellebedy A.H., Mehta A.K., Kraft C.S., Lyon G.M., Ribner B.S., Varkey J., Sidney J., Sette A., Campbell S., Ströher U., Damon I., Nichol S.T., Spiropoulou C.F., Ahmed R. Human Ebola virus infection results in substantial immune activation. Proc Natl Acad Sci USA. 2015;112:4719–4724. doi: 10.1073/pnas.1502619112. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McElroy A.K., Erickson B.R., Flietstra T.D., Rollin P.E., Nichol S.T., Towner J.S., Spiropoulou C.F. Biomarker correlates of survival in pediatric patients with Ebola virus disease. Emerg Infect Dis. 2014;20:1683–1690. doi: 10.3201/eid2010.140430. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McMaster S.R., Gabbard J.D., Koutsonanos D.G., Compans R.W., Tripp R.A., Tompkins S.M., Kohlmeier J.E. Memory T cells generated by prior exposure to influenza cross react with the novel H7N9 influenza virus and confer protective heterosubtypic immunity. PLoS ONE. 2015;10:e0115725. doi: 10.1371/journal.pone.0115725. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McMichael A.J. The original sin of killer T cells. Nature. 1998;394:421–422. doi: 10.1038/28738. [DOI] [PubMed] [Google Scholar]
- Mongkolsapaya J., Dejnirattisai W., Xu X., Vasanawathana S., Tangthawornchaikul N., Chairunsri A., Sawasdivorn S., Duangchinda T., Dong T., Rowland-Jones S., Yenchitsomanus P., McMichael A., Malasit P., Screaton G. Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat Med. 2003;9:921–927. doi: 10.1038/nm887. [DOI] [PubMed] [Google Scholar]
- Mongkolsapaya J., Duangchinda T., Dejnirattisai W., Vasanawathana S., Avirutnan P., Jairungsri A., Khemnu N., Tangthawornchaikul N., Chotiyarnwong P., Sae-Jang K., Koch M., Jones Y., McMichael A., Xu X., Malasit P., Screaton G. T cell responses in dengue hemorrhagic fever: are cross-reactive T cells suboptimal. J Immunol. 2006;176:3821–3829. doi: 10.4049/jimmunol.176.6.3821. [DOI] [PubMed] [Google Scholar]
- Ng O.W., Chia A., Tan A.T., Jadi R.S., Leong H.N., Bertoletti A., Tan Y.J. Memory T cell responses targeting the SARS coronavirus persist up to 11 years post-infection. Vaccine. 2016;34:2008–2014. doi: 10.1016/j.vaccine.2016.02.063. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Olival K.J., Hosseini P.R., Zambrana-Torrelio C., Ross N., Bogich T.L., Daszak P. Host and viral traits predict zoonotic spillover from mammals. Nature. 2017;546:646–650. doi: 10.1038/nature22975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Paquin-Proulx D., Leal F.E., Terrassani Silveira C.G., Maestri A., Brockmeyer C., Kitchen S.M., Cabido V.D., Kallas E.G., Nixon D.F. T-cell responses in individuals infected with Zika virus and in those vaccinated against dengue virus. Pathog Immun. 2017;2:274–292. doi: 10.20411/pai.v2i2.188. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pardy R.D., Rajah M.M., Condotta S.A., Taylor N.G., Sagan S.M., Richer M.J. Analysis of the T cell response to Zika virus and identification of a novel CD8+ T cell epitope in immunocompetent mice. PLoS Pathog. 2017;13:e1006184. doi: 10.1371/journal.ppat.1006184. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Quiñones-Parra S., Grant E., Loh L., Nguyen T.H.O., Campbell K.A., Tong S.Y.C., Miller A., Doherty P.C., Vijaykrishna D., Rossjohn J., Gras S., Kedzierska K. Preexisting CD8+ T-cell immunity to the H7N9 influenza A virus varies across ethnicities. Proc Natl Acad Sci USA. 2014;111:1049–1054. doi: 10.1073/pnas.1322229111. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Quiñones-Parra S.M., Clemens E.B., Wang Z., Croom H.A., Kedzierski L., McVernon J., Vijaykrishna D., Kedzierska K. A role of influenza virus exposure history in determining pandemic susceptibility and CD8+ T cell responses. J Virol. 2016;90:6936–6947. doi: 10.1128/JVI.00349-16. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ruibal P., Oestereich L., Lüdtke A., Becker-Ziaja B., Wozniak D.M., Kerber R., Korva M., Cabeza-Cabrerizo M., Bore J.A., Koundouno F.R., Duraffour S., Weller R., Thorenz A., Cimini E., Viola D., Agrati C., Repits J., Afrough B., Cowley L.A., Ngabo D., Hinzmann J., Mertens M., Vitoriano I., Logue C.H., Boettcher J.P., Pallasch E., Sachse A., Bah A., Nitzsche K., Kuisma E., Michel J., Holm T., Zekeng E.G., García-Dorival I., Wölfel R., Stoecker K., Fleischmann E., Strecker T., Di Caro A., Avšič-Županc T., Kurth A., Meschi S., Mély S., Newman E., Bocquin A., Kis Z., Kelterbaum A., Molkenthin P., Carletti F., Portmann J., Wolff S., Castilletti C., Schudt G., Fizet A., Ottowell L.J., Herker E., Jacobs T., Kretschmer B., Severi E., Ouedraogo N., Lago M., Negredo A., Franco L., Anda P., Schmiedel S., Kreuels B., Wichmann D., Addo M.M., Lohse A.W., De Clerck H., Nanclares C., Jonckheere S., Van Herp M., Sprecher A., Xiaojiang G., Carrington M., Miranda O., Castro C.M., Gabriel M., Drury P., Formenty P., Diallo B., Koivogui L., Magassouba N.F., Carroll M.W., Günther S., Muñoz-Fontela C. Unique human immune signature of Ebola virus disease in Guinea. Nature. 2016;533:100–104. doi: 10.1038/nature17949. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sanchez A., Wagoner K.E., Rollin P.E. Sequence-Based human leukocyte antigen-B typing of patients infected with Ebola virus in Uganda in 2000: identification of alleles associated with fatal and nonfatal disease outcomes. J Infect Dis. 2007;196:S329–S336. doi: 10.1086/520588. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sobarzo A., Ochayon D.E., Lutwama J.J., Balinandi S., Guttman O., Marks R.S., Kuehne A.I., Dye J.M., Yavelsky V., Lewis E.C., Lobel L. Persistent immune responses after Ebola virus infection. N Engl J Med. 2013;369:492–493. doi: 10.1056/NEJMc1300266. [DOI] [PubMed] [Google Scholar]
- Stettler K., Beltramello M., Espinosa D.A., Graham V., Cassotta A., Bianchi S., Vanzetta F., Minola A., Jaconi S., Mele F., Foglierini M., Pedotti M., Simonelli L., Dowall S., Atkinson B., Percivalle E., Simmons C.P., Varani L., Blum J., Baldanti F., Cameroni E., Hewson R., Harris E., Lanzavecchia A., Sallusto F., Corti D. Specificity, cross-reactivity, and function of antibodies elicited by Zika virus infection. Science. 2016;353:823–826. doi: 10.1126/science.aaf8505. [DOI] [PubMed] [Google Scholar]
- Su S., Wong G., Liu Y., Gao G.F., Li S., Bi Y. MERS in South Korea and China: a potential outbreak threat. Lancet. 2015;385:2349–2350. doi: 10.1016/S0140-6736(15)60859-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Su S., Wong G., Shi W., Liu J., Lai A.C.K., Zhou J., Liu W., Bi Y., Gao G.F. Epidemiology, genetic recombination, and pathogenesis of coronaviruses. Trends Microbiol. 2016;24:490–502. doi: 10.1016/j.tim.2016.03.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tan S., Zhang S., Wu B., Zhao Y., Zhang W., Han M., Wu Y., Shi G., Liu Y., Yan J., Wu G., Wang H., Gao G.F., Zhu F., Liu W.J. Hemagglutinin-specific CD4+ T-cell responses following 2009- pH1N1 inactivated split-vaccine inoculation in humans. Vaccine. 2017;35:5644–5652. doi: 10.1016/j.vaccine.2017.08.061. [DOI] [PubMed] [Google Scholar]
- Tappe D., Pérez-Girón J.V., Zammarchi L., Rissland J., Ferreira D.F., Jaenisch T., Gómez-Medina S., Günther S., Bartoloni A., Muñoz-Fontela C., Schmidt-Chanasit J. Cytokine kinetics of Zika virus-infected patients from acute to reconvalescent phase. Med Microbiol Immunol. 2016;205:269–273. doi: 10.1007/s00430-015-0445-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thorson A., Formenty P., Lofthouse C., Broutet N. Systematic review of the literature on viral persistence and sexual transmission from recovered Ebola survivors: evidence and recommendations. BMJ Open. 2016;6:e008859. doi: 10.1136/bmjopen-2015-008859. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van de Sandt C.E., Hillaire M.L.B., Geelhoed-Mieras M.M., Osterhaus A.D.M.E., Fouchier R.A.M., Rimmelzwaan G.F. Human influenza A virus-specific CD8+ T-cell response is long-lived. J Infect Dis. 2015;212:81–85. doi: 10.1093/infdis/jiv018. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van de Sandt C.E., Kreijtz J.H.C.M., de Mutsert G., Geelhoed-Mieras M. M., Hillaire M.L.B., van Vogelzang- Trierum S.E., Osterhaus A.D.M. E., Fouchier R.A.M., Rimmelzwaan G.F. Human cytotoxic T lymphocytes directed to seasonal influenza A viruses cross-react with the newly emerging H7N9 virus. J Virol. 2014;88:1684–1693. doi: 10.1128/JVI.02843-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang Q., Yang H., Liu X., Dai L., Ma T., Qi J., Wong G., Peng R., Liu S., Li J., Li S., Song J., Liu J., He J., Yuan H., Xiong Y., Liao Y., Li J., Yang J., Tong Z., Griffin B.D., Bi Y., Liang M., Xu X., Qin C., Cheng G., Zhang X., Wang P., Qiu X., Kobinger G., Shi Y., Yan J., Gao G.F. Molecular determinants of human neutralizing antibodies isolated from a patient infected with Zika virus. Sci Transl Med. 2016;8:369. doi: 10.1126/scitranslmed.aai8336. [DOI] [PubMed] [Google Scholar]
- Wang Z., Loh L., Kedzierski L., Kedzierska K. Avian influenza viruses, inflammation, and CD8+ T cell immunity. Front Immunol. 2016;7:60. doi: 10.3389/fimmu.2016.00060. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang Z., Wan Y., Qiu C., Quiñones-Parra S., Zhu Z., Loh L., Tian D., Ren Y., Hu Y., Zhang X., Thomas P.G., Inouye M., Doherty P.C., Kedzierska K., Xu J. Recovery from severe H7N9 disease is associated with diverse response mechanisms dominated by CD8+ T cells. Nat Commun. 2015;6:6833. doi: 10.1038/ncomms7833. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang Z., Zhang A., Wan Y., Liu X., Qiu C., Xi X., Ren Y., Wang J., Dong Y., Bao M., Li L., Zhou M., Yuan S., Sun J., Zhu Z., Chen L., Li Q., Zhang Z., Zhang X., Lu S., Doherty P.C., Kedzierska K., Xu J. Early hypercytokinemia is associated with interferoninduced transmembrane protein-3 dysfunction and predictive of fatal H7N9 infection. Proc Natl Acad Sci USA. 2014;111:769–774. doi: 10.1073/pnas.1321748111. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wauquier N., Becquart P., Padilla C., Baize S., Leroy E.M. Human fatal zaire Ebola virus infection is associated with an aberrant innate immunity and with massive lymphocyte apoptosis. PLoS Negl Trop Dis. 2010;4:e837. doi: 10.1371/journal.pntd.0000837. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wen J., Elong Ngono A., Angel Regla-Nava J., Kim K., Gorman M.J., Diamond M.S., Shresta S. Dengue virus-reactive CD8+ T cells mediate cross-protection against subsequent Zika virus challenge. Nat Commun. 2017;8:1459. doi: 10.1038/s41467-017-01669-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wen J., Tang W.W., Sheets N., Ellison J., Sette A., Kim K., Shresta S. Identification of Zika virus epitopes reveals immunodominant and protective roles for dengue virus cross-reactive CD8+ T cells. Nat Microbiol. 2017;2:17036. doi: 10.1038/nmicrobiol.2017.36. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wong G., Gao G.F., Qiu X. Can Ebola virus become endemic in the human population. Protein Cell. 2016;7:4–6. doi: 10.1007/s13238-015-0231-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wong G., Liu W., Liu Y., Zhou B., Bi Y., Gao G.F. MERS, SARS, and Ebola: the role of super-spreaders in infectious disease. Cell Host Microbe. 2015;18:398–401. doi: 10.1016/j.chom.2015.09.013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wu Y., Gao G.F. Lessons learnt from the human infections of avian-origin influenza A H7N9 virus: live free markets and human health. Sci China Life Sci. 2013;56:493–494. doi: 10.1007/s11427-013-4496-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zaki A.M., van Boheemen S., Bestebroer T.M., Osterhaus A.D.M.E., Fouchier R.A.M. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med. 2012;367:1814–1820. doi: 10.1056/NEJMoa1211721. [DOI] [PubMed] [Google Scholar]
- Zeng X., Blancett C.D., Koistinen K.A., Schellhase C.W., Bearss J.J., Radoshitzky S.R., Honnold S.P., Chance T.B., Warren T.K., Froude J.W., Cashman K.A., Dye J.M., Bavari S., Palacios G., Kuhn J.H., Sun M.G. Identification and pathological characterization of persistent asymptomatic Ebola virus infection in rhesus monkeys. Nat Microbiol. 2017;2:17113. doi: 10.1038/nmicrobiol.2017.113. [DOI] [PubMed] [Google Scholar]
- Zhang Y., Chen W., Wong G., Bi Y., Yan J., Sun Y., Chen E., Yan H., Lou X., Mao H., Xia S., Gao G.F., Shi W., Chen Z. Highly diversified Zika viruses imported to China, 2016. Protein Cell. 2016;7:461–464. doi: 10.1007/s13238-016-0274-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhao J., Zhao J., Mangalam A.K., Channappanavar R., Fett C., Meyerholz D.K., Agnihothram S., Baric R.S., David C.S., Perlman S. Airway memory CD4+ T cells mediate protective immunity against emerging respiratory coronaviruses. Immunity. 2016;44:1379–1391. doi: 10.1016/j.immuni.2016.05.006. [DOI] [PMC free article] [PubMed] [Google Scholar]