Alphavirus-specific cytotoxic T lymphocytes recognize a cross-reactive epitope from the capsid protein and can eliminate virus from persistently infected macrophages

Journal of Virology

Volumn 72, Issue 6, 1998, Pages 5146-5153

  Linn, May La ^a   Mateo, L ^a   Gardner, J ^a   Suhrbier, A ^a,b  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; EPITOPE;

ALPHA VIRUS; ANIMAL CELL; ARTHRITIS; ARTICLE; CYTOTOXIC T LYMPHOCYTE; ENCEPHALITIS; MACROPHAGE; MOUSE; NONHUMAN; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; VIREMIA;

EID: 0031954470     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.6.5146-5153.1998     Document Type: Article

References (71)

1. Aaskov, J. G., D. A. Dalglish, J. J. Harper, J. F. Douglas, M. D. Donaldson, and P. J. Hertzog. 1987. Natural killer cells in viral arthritis. Clin. Exp. Immunol. 68:23-32.
2. Adebajo, A. O. 1996. Rheumatic manifestations of tropical diseases. Curr. Opin. Rheumatol. 8:85-89.
3. Amor, S., M. F. Scallan, M. M. Morris, H. Dyson, and J. K. Fazakerley. 1996. Role of immune responses in protection and pathogenesis during Semliki Forest virus encephalitis. J. Gen. Virol. 77:281-291.
4. Atkinson, T., A. D. Barrett, A. Mackenzie, and N. J. Dimmock. 1986. Persistence of virulent Semliki Forest virus in mouse brain following co-inoculation with defective interfering particles. J. Gen. Virol. 67:1189-1194.
5. Blackman, M. J., and A. G. Morris. 1984. Gamma Interferon production and cytotoxicity of spleen cells from mice infected with Semliki Forest virus. J. Gen. Virol. 65:955-961.
6. Boege, U., W. Wengler, G. Wengler, and B. Wittmann-Liebold. 1981. Primary structure of the core proteins of the alphaviruses Semliki Forest virus and Sindbis virus. Virology 113:293-303.
7. Brighton, S. W. 1984. Chloroquine phosphate treatment of chronic Chikungunya arthritis. An open pilot study. S. Afr. Med. J. 66:217-218.
8. Busch, D. H., C. Jassoy, U. Brinckmann, H. Girschick, and H. I. Huppertz. 1996. Detection of Borrelia burgdorferi-specific CD8+ cytotoxic T cells in patients with Lyme arthritis. J. Immunol. 157:3534-3541.
9. Chantier J. K., A. J. Tingle, and R. E. Petty. 1985. Persistent rubella virus infection associated with chronic arthritis in children. N. Engl. J. Med. 313:1117-1123.
10. Clark, G. G., F. J. Dein, C. L. Crabbs, J. W. Carpenter, and D. M. Watts. 1987. Antibody response of sandhill and whooping cranes to an eastern equine encephalitis virus vaccine. J. Wildl. Dis. 23:539-544.
11. Curran, M., B. Harvey, S. Crerar, G. Oliver, R. D'Sousza, H. Myint, C. Rann, and R. Andrews. 1996. Australia's notifiable diseases status, 1996. Commun. Dis. Intell. 21:281-307.
12. Deresiewicz, R. L., S. J. Thaler, L. Hsu, and A. A. Zamani. 1997. Clinical and neuroradiographic manifestations of eastern equine encephalitis. N. Engl. J. Med. 336:1867-1874.
13. Dethlefs, S., M. Brahic, and E. L. Larsson-Sciard. 1997. An early, abundant cytotoxic T-lymphocyte response against Theiler's virus is critical for preventing viral persistence. J. Virol. 71:8875-8878.
14. Eaton, B. T., and A. J. Hapel. 1976. Persistent noncytolytic togavirus infection of primary mouse muscle cells. Virology 72:266-271.
15. Faragher, S. G., A. D. Meek, C. M. Rice, and L. Dalgarno. 1988. Genome sequences of a mouse-avirulent and a mouse-virulent strain of Ross River virus. Virology 163:509-526.
16. Fish, K. N., W. Britt, and J. A. Nelson. 1996. A novel mechanism for persistence of human cytomegalovirus in macrophages. J. Virol. 70:1855-1862.
17. Fraser, J. R. 1986. Epidemic polyarthritis and Ross River virus disease. Clin. Rheum. Dis. 12:369-388.
18. Fraser, J. R., and G. J. Becker. 1984. Mononuclear cell types in chronic synovial effusions of Ross River virus disease. Aust. N. Z. J. Med. 14:505-506.
19. Fraser, J. R., V. M. Ratnamohan, J. P. Bowling, G. J. Becker, and G. A. Varigos. 1983. The exanthem of Ross River virus infection: histology, location of virus antigen and nature of inflammatory infiltrate. J. Clin. Pathol. 36:1256-1263.
20. Friedman, R. M., and J. M. Ramseur. 1979. Mechanisms of persistent infections by cytopathic viruses in tissue culture. Arch. Virol. 60:83-103.
21. Gorrell, M. D., J. A. Lemm, C. M. Rice, and D. E. Griffin. 1997. Immunization with nonstructural proteins promotes functional recovery of alphavirus-infected neurons. J. Virol. 71:3415-3419.
22. Guidotti, L. G., and F. V. Chisari. 1996. To kill or to cure: options in host defense against viral infection. Curr. Opin. Immunol. 8:478-483.
23. Hapel, A. J. 1975. The protective role of thymus-derived lymphocytes in arbovirus-induced meningoencephalitis. Scand. J. Immunol. 4:267-278.
24. Hober, D., L. Andreoletti, L. Shen, M. C. Copin, A. Desmidt, and P. Wattre. 1996. Coxsackievirus B3-induced chronic myocarditis in mouse: use of whole blood culture to study the activation of TNF alpha-producing cells. Microbiol. Immunol. 40:837-845.
25. Hwang, S. Y., P. J. Hertzog, K. A. Holland, S. H. Sumarsono, M. J. Tymms, J. A. Hamilton, G. Whitry, I. Bertoncello, and I. Kola. 1995. A null mutation in the gene encoding a type I Interferon receptor component eliminates antiproliferative and antiviral responses to interferons alpha and beta and alters macrophage responses. Proc. Natl. Acad. Sci. USA 92:11284-11288.
26. Itescu, S. 1996. Rheumatic aspects of acquired immunodeficiency syndrome. Curr. Opin. Rheumatol. 8:346-353.
27. Johnston, R. E., and C. J. Peters. 1996. Alphaviruses, p. 843. In B. N. Fields, D. M. Knipe, P. M. Howley, et al. (ed.), Fields virology Lippincott-Raven Publishers, Philadelphia, Pa.
28. Journeaux, S. F., W. G. Brown, and J. G. Aaskov. 1987. Prolonged infection of human synovial cells with Ross River virus. J. Gen. Virol. 68:3165-3169.
29. Kagi, D., and H. Hengartner. 1996. Different roles for cytotoxic T cells in the control of infections with cytopathic versus noncytopathic viruses. Curr. Opin. Immunol. 8:472-477.
30. Kamada, M., Y. Ando, Y. Fukunaga, T. Kumanomido, H. Imagawa, R. Wada, and Y. Akiyama. 1980. Equine Getah virus infection: isolation of the virus pr from racehorses during an enzootic in Japan. Am. J. Trop. Med. Hyg. 29: 984-988.
31. Kennedy, A. C., J. Fleming, and L. Solomon. 1980. Chikungunya viral arthropathy: a clinical description. J. Rheumatol. 7:231-236.
32. Kujala, P., M. Rikkonen, T. Ahola, M. Kelve, M. Saarma, and L. Kaariainen. 1997. Monoclonal antibodies specific for Semliki Forest virus replicase protein nsP2. J. Gen. Virol. 78:343-351.
33. Laakkonen, P., M. Hyvonen, J. Peranen, and L. Kaariainen. 1994. Expression of Semliki Forest virus nsP1-specific methyltransferase in insect cells and in Escherichia coli. J. Virol. 68:7418-7425.
34. Lahesmaa, R., M. C. Shanafelt, L. Steinman, and G. Peltz. 1994. Immunopathogenesis of human inflammatory arthritis: lessons from Lyme and reactive arthritis. J. Infect. Dis. 170:978-985.
35. Lee, S., K. E. Owen, H. K. Choi, H. Lee, G. Lu, G. Wengler, D. T. Brown, M. G. Rossmann, and R. J. Kuhn. 1996. Identification of a protein binding site on the surface of the alphavirus nucleocapsid and its implication in virus assembly. Structure 4:531-541.
36. Lehane, M. J., and C. J. Leake. 1982. A kinetic and ultrastructural comparison of alphavirus infection of cultured mosquito and vertebrate cells. J. Trop. Med. Hyg. 85:229-238.
37. Levine, B., J. M. Hardwick, and D. E. Griffin. 1994. Persistence of alphaviruses in vertebrate hosts. Trends Microbiol. 2:25-28.
38. Lichtensteiger, C. A., W. P. Cheevers, and W. C. Davis. 1993. CD8+ cytotoxic T lymphocytes against antigenic variants of caprine arthritis-encephalitis virus. J. Gen. Virol. 74:2111-2116.
39. Linn, M. L., A. J. D. Bellett, P. G. Parsons, and A. Suhrbier. 1995. Complete removal of mycoplasma from viral preparations using solvent extraction. J. Virol. Methods 52:51-54.
40. Linn, M. L., J. Aaskov, and A. Suhrbier. 1996. Antibody dependent enhancement and persistence in macrophages of an arbovirus associated with arthritis. J. Gen. Virol. 77:407-412.
41. Linn, M. L., and A. Suhrbier. 1997. Persistence of Ross River virus in macrophages. Arbovirus Res. Aust. 7:153-159.
42. Lovett, A. E., C. S. Hahn, C. M. Rice, T. K. Frey, and J. S. Wolinsky. 1993. Rubella virus-specific cytotoxic T-lymphocyte responses: identification of the capsid as a target of major histocompatibility complex class I-restricted lysis and definition of two epitopes. J. Virol. 67:5849-5858.
43. Martin, J. H., R. C. Weir, and L. Dalgarno. 1979. Replication of standard and defective Ross River virus in BHK cells: patterns of viral RNA and polypeptide synthesis. Arch. Virol. 61:87-103.
44. Mathew, A., I. Kurane, A. L. Rothman, L. L. Zeng, M. A. Brinton, and F. A. Ennis. 1996. Dominant recognition by human CD8+ cytotoxic T lymphocytes of dengue virus nonstructural proteins NS3 and NS1.2a. J. Clin. Invest. 98:1684-1691.
45. 44a. Mateo, L. Unpublished information.
46. Muellbacher, A., and R. V. Blanden. 1978. Murine cytotoxic T-cell response to alphavirus is associated mainly with H-2Dk. Immunogenetics 7:551-561.
47. k during differentiation and stimulation converts stem cells of low responder genotype to T cells of responder phenotype. J. Exp. Med. 49:786-790.
48. Muellbacher, A., I. D. Marshall, and R. V. Blanden. 1979. Cross-reactive cytotoxic T cells to alphavirus infection. Scand. J. Immunol. 10:291-296.
49. Musiani, M., M. Zerbini, G. Gentilomi, M. Plazzi, G. Gallinella, and S. Venturoli. 1995. Parvovirus B19 clearance from peripheral blood after acute infection. J. Infect. Dis. 172:1360-1363.
50. Nanagara, R., F. Li, A. Beutler, A. Hudson, and H. R. Schumacher, Jr. 1995. Alteration of Chlamydia trachomatis biologic behavior in synovial membranes. Suppression of surface antigen production in reactive arthritis and Reiter's syndrome. Arthritis Rheum. 38:1410-1417.
51. Narayan, O., M. C. Zink, M. Gorrell, M. McEntee, D. Sharma, and R. Adams. 1992. Lentivirus induced arthritis in animals. J. Rheumatol. Suppl. 32:25-32.
52. Niewiesk, S., U. Brinckmann, B. Bankamp, S. Sirak, U. G. Liebert, and V. ter Meulen. 1993. Susceptibility to measles virus-induced encephalitis in mice correlates with impaired antigen presentation to cytotoxic T lymphocytes. J. Virol. 67:75-81.
53. Nocton, J. J., F. Dressler, B. J. Rutledge, P. N. Rys, D. H. Persing, and A. C. Steere. 1994. Detection of Borrelia hurgdorferi DNA by polymerase chain reaction in synovial fluid from patients with Lyme arthritis. N. Engl. J. Med. 330:229-234.
54. Oldstone, M. B. 1997. How viruses escape from cytotoxic T lymphocytes: molecular parameters and players. Virology 234:179-185.
55. Peck, R., A. Brown, and C. J. Wust. 1979. In vitro heterologous cytotoxicity by T effector cells from mice immunized with Sindbis virus. J. Immunol. 123:1763-1766.
56. Rammensee, H. G., T. Friede, and S. Stevanoviic. 1995. MHC ligands and peptide motifs: first listing. Immunogenetics 41:178-228.
57. Reeves, W. C., G. A. Hutson, R. E. Bellamy, and R, P. Scrivani. 1958. Chronic latent infections of birds with western equine encephalomyelitis virus. Proc. Soc. Exp. Biol. Med. 97:733-736.
58. Rosen, L., D. J. Gubler, and P. H. Bennett. 1981. Epidemic polyarthritis (Ross River) virus infection in the Cook Islands. Am. J. Trop. Med. Hyg. 30:1294-1302.
59. Rwaguma, E. B., J. J. Lutwama, S. D. Sempala, N. Kiwanuka, J. Kamugisha, S. Okware, G. Bagambisa, R. Lanciotti, J. T. Roehrig, and D. J. Gubler. 1997. Emergence of epidemic O'nyong-nyong fever in southwestern Uganda, after an absence of 35 years. Emerg. Infect. Dis. 3:77. (Letter.)
60. Sarmiento, R. E., R. Tirado, and B. Gomez. 1997. Reinfection-induced in crease of rubella persistently infected cells in a macrophage-like cell line. Virus Res. 50:15-22.
61. Scalzo, A. A., S. L. Elliott, J. Cox, J. Gardner, D. J. Moss, and A. Suhrbier. 1995. Induction of protective cytotoxic T cells to murine cytomegalovirus by using a nonapeptide and a human-compatable adjuvant (Montanide ISA 720). J. Virol. 69:1306-1309.
62. Seay, A. R., D. E. Griffin, and R. T. Johnson. 1981. Experimental viral polymyositis: age dependency and immune responses to Ross River virus infection in mice. Neurology 31:656-660.
63. + T cells prevents lesions of demyelination in Semliki Forest virus infection. J. Virol. 67:7629-7633.
64. Sweet, M. J., and D. A. Hume. 1995. RAW264 macrophages stably transfected with an HIV-1 LTR reporter gene provide a sensitive bioassay for analysis of signalling pathways in macrophages stimulated with lipopolysaccharide, TNF-alpha or taxol. J. Inflamm. 45:126-135.
65. Thomson, S., R. Khanna, J. Gardner, S. R. Burrows, B. Coupar, D. J. Moss, and A. Suhrbier. 1995. Minimal epitopes expressed in a recombinant polyepitope protein are processed and presented to CD8+ cytotoxic T cells: implications for vaccine design. Proc. Natl. Acad. Sci. USA 92:5845-5849.
66. Vene, S., C. Franzen, and B. Niklasson. 1994. Development of specific antibody patterns and clinical symptoms following Ockelbo virus infection. Arch. Virol. 134:61-71.
67. Verder, H., E. Dickmeiss, S. Haahr, E. Kappelgaard, J. Leerboy, A. Moller-Larsen, H. Nielsen, P. Platz, and C. Koch. 1986. Late-onset rubella syndrome: coexistence of immune complex disease and defective cytotoxic effector cell function. Clin. Exp. Immunol. 63:367-375.
68. Wakefield, A. J., R. Sim, A. N. Akbar, R. E. Pounder, and A. P. Dhillon. 1997. In situ immune responses in Crohn's disease: a comparison with acute and persistent measles virus infection. J. Med. Virol. 51:90-100.
69. Weaver, S. C., R. Salas, R. Rico-Hesse, G. V. Ludwig, M. S. Oberste, J. Boshell, and R. B. Tesh. 1996. Re-emergence of epidemic Venezuelan equine encephalomyelitis in South America. VEE Study Group. Lancet 348:436-440.
70. Westaway, E. G. 1973. Proteins specified by group B togaviruses in mammalian cells during productive infections. Virology 51:454-465.
71. Yu, S., and J. G. Aaskov. 1994. Development of a candidate vaccine against Ross River virus infection. Vaccine 12:1118-1124.