Screening and identification of severe acute respiratory syndrome-associated coronavirus-specific CTL epitopes

Journal of Immunology

Volumn 177, Issue 4, 2006, Pages 2138-2145

  Zhou, Minghai ^a,e   Xu, Dongping ^b   Li, Xiaojuan ^a   Li, Hongtao ^a,e   Shan, Ming ^a   Tang, Jiaren ^c   Wang, Min ^b   Wang, Fu Sheng ^b   Zhu, Xiaodong ^a,e   Tao, Hua ^a   He, Wei ^b   Tien, Po ^a   Gao, George F ^a,d  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b BEIJING 302 HOSPITAL   (China)

^c INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ANGIOTENSIN CONVERTING ENZYME 2 RECEPTOR; DIPEPTIDYL CARBOXYPEPTIDASE; DNA VACCINE; EPITOPE; GAMMA INTERFERON; HLA A ANTIGEN; HLA A2 ANTIGEN; LYSYLLEUCYLPROLYLASPARTYLASPARTYLPHENYLALANYLMETHIONYLGLYCYLCYSTEINYLVALINE; NUCLEOCAPSID PROTEIN; RECEPTOR; UNCLASSIFIED DRUG; VIRUS SPIKE PROTEIN; VITRONECTIN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; ANTIGENICITY; ARTICLE; BINDING SITE; CELL STIMULATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DATA BASE; ENZYME LINKED IMMUNOSPOT ASSAY; HUMAN; HUMAN CELL; IMMUNIZATION; IMMUNOPATHOGENESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; SARS CORONAVIRUS; SCREENING; SEQUENCE ANALYSIS; SEVERE ACUTE RESPIRATORY SYNDROME; TRANSGENIC MOUSE; VIRUS SHEDDING;

EID: 33746898241     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.4.2138     Document Type: Article

References (65)

1. World Health Organization Multicentre Collaborative Network for Severe Acute Respiratory Syndrome Diagnosis. 2003. A multicentre collaboration to investigate the cause of severe acute respiratory syndrome. Lancet 361: 1730-1733.
2. Anonymous. 2003. Global surveillance for severe acute respiratory syndrome (SARS). Wkly. Epidemiol. Rec. 78: 100-119.
3. Lee, N., D. Hui, A. Wu, P. Chan, P. Cameron, G. M. Joynt, A. Ahuja, M. Y. Yung, C. B. Leung, K. F. To, et al. 2003. A major outbreak of severe acute respiratory syndrome in Hong Kong. N. Engl. J. Med. 348: 1986-1994.
4. Zhao, Z., F. Zhang, M. Xu, K. Huang, W. Zhong, W. Cai, Z. Yin, S. Huang, Z. Deng, M. Wei, et al. 2003. Description and clinical treatment of an early outbreak of severe acute respiratory syndrome (SARS) in Guangzhou, PR China. J. Med. Microbiol. 52: 715-720.
5. Zhong, N. S., B. J. Zheng, Y. M. Li, Poon, Z. H. Xie, K. H. Chan, P. H. Li, S. Y. Tan, Q. Chang, J. P. Xie, et al. 2003. Epidemiology and cause of severe acute respiratory syndrome (SARS) in Guangdong, People's Republic of China, in February, 2003. Lancet 362: 1353-1358.
6. Drosten, C., S. Gunther, W. Preiser, S. van der Werf, H. R. Brodt, S. Becker, H. Rabenau, M. Panning, L. Kolesnikova, R. A. Fouchier, et al. 2003. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348: 1967-1976.
7. Fouchier, R. A., T. Kuiken, M. Schutten, G. van Amerongen, G. J. van Doornum, B. G. van den Hoogen, M. Peiris, W. Lim, K. Stohr, and A. D. Osterhaus. 2003. Aetiology: Koch's postulates fulfilled for SARS virus. Nature 423: 240.
8. Ksiazek, T. G., D. Erdman, C. S. Goldsmith, S. R. Zaki, T. Peret, S. Emery, S. Tong, C. Urbani, J. A. Comer, W. Lim, et al. 2003. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 348: 1953-1966.
9. Kuiken, T., R. A. Fouchier, M. Schutten, G. F. Rimmelzwaan, G. van Amerongen, D. van Riel, J. D. Lantan, T. de Jong, G. van Doornum, W. Lim, et al. 2003. Newly discovered eoronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362: 263-270.
10. Peiris, J. S., S. T. Lai, L. L. Poon, Y. Guan, L. Y. Yam, W. Lim, J. Nicholls, W. K. Yee, W. W. Yan, M. T. Cheung, et al. 2003. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361: 1319-1325.
11. Guan, Y., B. J. Zheng, Y. Q. He, X. L. Liu, Z. X. Zhuang, C. L. Cheung, S. W. Luo, P. H. Li, L. J. Zhang, Y. J. Guan, et al. 2003. Isolation and characterization of viruses related to the SARS eoronavirus from animals in southern China. Science 302: 276-278.
12. Chinese, S. M. E. C. 2004. Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science 303: 1666-1669.
13. Peiris, J. S., C. M. Chu, V. C. Cheng, K. S. Chan, I. F. Hung, L. L. Poon, K. I. Law, B. S. Tang, T. Y. Hon, C. S. Chan, et al. 2003. Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study. Lancet 361: 1767-1772.
14. Nicholls, J. M., L. L. Poon, K. C. Lee, W. F. Ng, S. T. Lai, C. Y. Leung, C. M. Chu, P. K. Hui, K. L. Mak, W. Lim, et al. 2003. Lung pathology of fatal severe acute respiratory syndrome. Lancet 361: 1773-174.
15. Yan, H., G. Xiao, J. Zhang, Y. Hu, F. Yuan, D. K. Cole, C. Zheng, and G. F. Gao. 2004. SARS coronavirus induces apoptosis in Vero E6 cells. J. Med. Virol. 73: 323-324.
16. Booth, C. M., L. M. Matukas, G. A. Tomlinson, A. R. Rachlis, D. B. Rose, H. A. Dwosh, S. L. Walmsley, T. Mazzulli, M. Avendano, P. Derkach, et al. 2003. Clinical features and short-term outcomes of 144 patients with SARS in the greater Toronto area. J. Am. Med. Assoc. 289: 2801-2809.
17. + T lymphocyte subsets during the acute phase of severe acute respiratory syndrome. Chin. Med. J. 116: 985-987.
18. Poutanen, S. M., D. E. Low, B. Henry, S. Finkelstein, D. Rose, K. Green, R. Tellier, R. Draker, D. Adachi, M. Ayers, et al. 2003. Identification of severe acute respiratory syndrome in Canada. N. Engl. J. Med. 348: 1995-2005.
19. Lin, M., H. K. Tseng, J. A. Trejaut, H. L. Lee, J. H. Loo, C. C. Chu, P. J. Chen, Y. W. Su, K. H. Lim, Z. U. Tsai, et al. 2003. Association of HLA class I with severe acute respiratory syndrome Coronavirus infection. BMC Med. Genet. 4: 9-15.
20. Ng, M. H., K. M. Lau, L. Li, S. H. Cheng, W. Y. Chan, P. K. Hui, B. Zee, C. B. Leung, and J. J. Sung. 2004. Association of human-leukocyte-antigen class I (B*0703) and class II (DRB1*0301) genotypes with susceptibility and resistance to the development of severe acute respiratory syndrome. J. Infect. Dis. 190: 515-518.
21. Gao, W., A. Tamin, A. Soloff, L. D'Aiuto, E. Nwanegbo, P. D. Rohbins, W. J. Bellini, S. Barratt-Boyes, and A. Gambotto. 2003. Effects of a SARS-associated coronavirus vaccine in monkeys. Lancet 362: 1895-184.
22. Bisht, H., A. Roberts, L. Vogel, A. Bukreyev, P. L. Collins, B. R. Murphy, K. Subbarao, and B. Moss. 2004. Severe acute respiratory syndrome coronavirus spike protein expressed by attenuated vaccinia virus protectively immunizes mice. Proc. Natl. Acad. Sci. USA 101: 6641-6646.
23. Yang, Z. Y., W. P. Kong, Y. Huang, A. Roberts, B. R. Murphy, K. Subbarao, and G. J. Nabel. 2004. A DNA vaccine induces SARS coronavirus neutralization and protective immunity in mice. Nature 428: 561-564.
24. Leung, D. T., F. C. Tam, C. H. Ma, P. K. Chan, J. L. Cheung, H. Niu, J. S. Tam, and P. L. Lim. 2004. Antibody response of patients with severe acute respiratory syndrome (SARS) targets the viral nucleocapsid. J. Infect. Dis. 190: 379-386.
25. Shi, Y., Z. Wan, L. Li, P. Li, C. Li, Q. Ma, and C. Cao. 2004. Antibody responses against SARS-coronavirus and its nucleocaspid in SARS patients. J. Clin. Virol. 31: 66-68.
26. He, Y., Y. Zhou, H. Wu, B. Luo, J. Chen, W. Li, and S. Jiang. 2004. Identification of immunodoininant sites on the spike protein of severe acute respiratory syndrome (SARS) coronavirus: implication for developing SARS diagnostics and vaccines. J. Immunol. 173: 4050-4057.
27. Li, W., M. J. Moore, N. Vasilieva, J. Sui, S. K. Wong, M. A. Berne, M. Somasundaran, J. L. Sullivan, K. Luzuriaga, T. C. Greenough, et al. 2003. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426: 450-454.
28. Prabakaran, P., X. Xiao, and D. S. Dimitrov. 2004. A model of the ACE2 structure and function as a SARS-CoV receptor. Biochem. Biophys. Res. Commun. 314: 235-241.
29. He, Y., P. Siddiqui, Y. Zhou, and S. Jiang. 2005. Receptor-binding domain of severe acute respiratory syndrome coronavirus spike protein contains multiple conformation-dependent epitopes that induce highly potent neutralizing antibodies. J. Immunol. 174: 4908-4915.
30. Wong, S. K., W. Li, M. J. Moore, H. Choe, and M. Farzan. 2004. A 193-amino acid fragment of the SARS coronavirus S protein efficiently binds angiotensin-converting enzyme 2. J. Biol. Chem. 279: 3197-3201.
31. Wang, Y. D., W. Y. Sin, G. B. Xu, H. H. Yang, T. Y. Wong, X. W. Pang, X. Y. He, H. G. Zhang, J. N. Ng, C. S. Cheng, et al. 2004. T-cell epitopes in severe acute respiratory syndrome (SARS) coronavirus spike protein elicit a specific T-cell immune response in patients who recover from SARS. J. Virol. 78: 5612-5618.
32. + T-cell epitope SSp-1 of SARS-CoV spike protein. Blood 104: 200-206.
33. Parker, K. C., M. A. Bednarek, L. K. Hull, U. Utz, B. Cunningham, H. J. Zweerink, W. E. Biddison, and J. E. Coligan. 1992. Sequence motifs important for peptide binding to the human MHC class I molecule. HLA-A2. J. Immunol. 149: 3580-3587.
34. Bertoletti, A., A. Costanzo, F. V. Chisari, M. Levrero, M. Artini, A. Sette, A. Penna, T. Giuberti, F. Fiaccadori, and C. Ferrari. 1994. 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. 180: 933-943.
35. Collins, E. J., D. N. Garboczi, and D. C. Wiley. 1994. Three-dimensional structure of a peptide extending from one end of a class I MHC binding site. Nature 371: 626-629.
36. Visseren, M. J., S. H. van der Burg, E. I. van der Voort, R. M. Brandt, P. I. Schrier, P. van der Bruggen, T. Boon, C. J. Melief, and W. M. Kast. 1997. Identification of HLA-A*0201-restricted CTL epitopes encoded by the tumor-specific MAGE-2 gene product. Int. J. Cancer 73: 125-130.
37. Trojan, A., M. Witzens, J. L. Schultze, R. H. Vonderheide, S. Harig, A. M. Krackhardt, R. A. Stahel, and J. G. Gribben. 2001. Generation of cytotoxic T lymphocytes against native and altered peptides of human leukocyte antigen-A*0201 restricted epitopes from the human epithelial cell adhesion molecule. Cancer Res. 61: 4761-4765.
38. Shieh, D. C., D. T. Lin, B. S. Yang, H. L. Kuan, and K. J. Kao. 1996. High frequency of HLA-A*0207 subtype in Chinese population. Transfusion 36: 818-814.
39. Parker, K. C., M. A. Bednarek, and J. E. Coligan. 1994. Scheme for ranking potential HLA-A2 binding peptides based on independent binding of individual peptide side-chains. J. Immunol. 152: 163-175.
40. Kuhrober, A., J. Wild, H. P. Pudollek, F. V. Chisari, and J. Reimann. 1997. DNA vaccination with plasmids encoding the intracellular (HBcAg) or secreted (HBeAg) form of the core protein of hepatitis B virus primes T cell responses to two overlapping Kb- and Kd-restricted epitopes. Int. Immunol. 9: 1203-1212.
41. Garboczi, D. N., D. T. Hung, and D. C. Wiley. 1992. HLA-A2-peptide complexes: refolding and crystallization of molecules expressed in Eseherichia coli and complexed with single antigenic peptides. Proc. Natl. Acad. Sci. USA 89: 3429-3433.
42. Zhou, M., Y. Xu, Z. Lou, D. K. Cole, X. Li, Y. Liu, P. Tien, Z. Rao, and G. F. Gao. 2004. Complex assembly, crystallization and preliminary X-ray crystallographic studies of MHC H-2Kd eomplexed with an HBV-core nonapeptide. Acta Crystallogr. D Biol. Crystallogr. 60: 1473-1475.
43. Gricks, C. S., E. Rawlings, L. Foroni, J. A. Madrigal, and P. L. Amlot. 2001. Somatically mutated regions of immunoglobulin on human B-cell lymphomas code for peptides that bind to autologous major histocompatibility complex class 1, providing a potential target for cytotoxic T cells. Cancer Res. 61: 5145-5152.
44. + T-cell epitopes by a computer algorithm and an enzyme-linked immunospot assay. Blood 98: 1872-1881.
45. + T-cell epitopes. Blood 99: 2100-2106.
46. Altman, J. D., P. A. Moss, P. J. Goulder, D. H. Barouch, M. G. McHeyzer-Williams, J. I. Bell, A. J. McMichael, and M. M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science 274: 94-94.
47. Vitiello, A., D. Marchesini, J. Furze, L. A. Sherman, and R. W. Chesnut. 1991. Analysis of the HLA-restricted influenza-specific cytotoxic T lymphocyte response in transgenic mice carrying a chimeric human-mouse class I major histocompatibility complex. J. Exp. Med. 173: 1007-1015.
48. + cytotoxic T lymphocytes in rhesus monkeys. J. Immunol. 151: 5096-5105.
49. Li, H., M. Zhou, J. Han, X. Zhu, T. Dong, G. F. Gao, and P. Tien. 2005. Generation of murine CTL by a hepatitis B virus-specific peptide and evaluation of the adjuvant effect of heat shock protein glycoprotein 96 and its terminal fragments. J. Immunol. 174: 195-204.
50. Nie, Y., P. Wang, X. Shi, G. Wang, J. Chen, A. Zheng, W. Wang, Z. Wang, X. Qu, M. Luo, et al. 2004. Highly infectious SARS-CoV pseudotyped virus reveals the cell tropism and its correlation with receptor expression. Biochem. Biophys. Res. Commun. 321: 994-1000.
51. Lagging, L. M., K. Meyer, D. Hoft, M. Houghton, R. B. Belshe, and R. Ray. 1995. Immune responses to plasmid DNA encoding the hepatitis C virus core protein. J. Virol. 69: 5859-5863.
52. Dutton, R. W., L. M. Bradley, and S. L. Swain. 1998. T cell memory. Annu. Rev. Immunol. 16: 201-204.
53. + T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat. Immunol. 2: 415-422.
54. van Stipdonk, M. J., E. E. Lemmens, and S. P. Schoenberger. 2001. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat. Immunol. 2: 423-429.
55. Kaech, S. M., E. J. Wherry, and R. Ahmed. 2002. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2: 251-262.
56. + effector and memory T cell generation. Nat. Immunol. 4: 835-842.
57. Wherry, E. J., V. Teichgraber, T. C. Becker, D. Masopust, S. M. Kaech, R. Antia, U. H. von Andrian, and R. Ahmed. 2003. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol. 4: 225-234.
58. Peiris, J. S., K. Y. Yuen, A. D. Osterhaus, and K. Stohr. 2003. The severe acute respiratory syndrome. N. Engl. J. Med. 349: 2431-244.
59. + T cell contraction is controlled by early inflammation. Nat. Immunol. 5: 809-817.
60. Finlay, B. B., R. H. See, and R. C. Brunham. 2004. Rapid response research to emerging infectious diseases: lessons from SARS. Nat. Rev. Microbiol. 2: 602-607.
61. Loa, C. C., T. L. Lin, C. C. Wu, T. Bryan, H. L. Thacker, T. Hooper, and D. Schrader. 2001. Humoral and cellular immune responses in turkey poults infected with turkey coronavirus. Poult. Sci. 80: 1416-1424.
62. Collisson, E. W., J. Pei, J. Dzielawa, and S. H. Seo. 2000. Cytotoxic T lymphocytes are critical in the control of infectious bronchitis virus in poultry. Dev. Camp. Immunol. 24: 187-200.
63. Seo, S. H., and E. W. Collisson. 1998. Cytotoxic T lymphocyte responses to infectious bronchitis virus infection. Adv. Exp. Med. Biol. 440: 455-460.
64. Stohlman, S. A., C. C. Bergmann, R. C. van der Veen, and D. R. Hinton. 1995. Mouse hepatitis virus-specific cytotoxic T lymphocytes protect from lethal infection without eliminating virus from the central nervous system. J. Virol. 69: 684-694.
65. + T cells to severe acute respiratory syndrome (SARS) coronavirus in recovered SARS patients and healthy individuals. J. Immunol. 175: 591-598.