Temperature-sensitive mutants of enterovirus 71 show attenuation in cynomolgus monkeys

Journal of General Virology

Volumn 86, Issue 5, 2005, Pages 1391-1401

  Arita, Minetaro ^a   Shimizu, Hiroyuki ^a   Nagata, Noriyo ^a   Ami, Yasushi ^a   Suzaki, Yuriko ^a   Sata, Tetsutaro ^a   Iwasaki, Takuya ^b   Miyamura, Tatsuo ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b NAGASAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; ORAL POLIOMYELITIS VACCINE;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CULTURE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENTEROVIRUS 71; GENETIC ENGINEERING; GENETIC IDENTIFICATION; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR CLONING; MONKEY; MONKEY DISEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; TEMPERATURE SENSITIVE MUTANT; TEMPERATURE SENSITIVITY; VIRUS ATTENUATION; VIRUS MUTANT; VIRUS MUTATION; VIRUS PATHOGENESIS; VIRUS STRAIN; VIRUS VIRULENCE;

3' UNTRANSLATED REGIONS; 5' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; BRAIN; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM VIRAL DISEASES; DISEASE MODELS, ANIMAL; ENTEROVIRUS; ENTEROVIRUS INFECTIONS; FEMALE; MACACA FASCICULARIS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PLAQUE ASSAY; POLIOVIRUS; RNA REPLICASE; SPINAL CORD; VIRULENCE;

ENTEROVIRUS; HUMAN ENTEROVIRUS 71; MACACA FASCICULARIS; POLIOVIRUS;

EID: 18144429034     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.80784-0     Document Type: Article

References (63)

1. Abubakar, S., Chee, H. Y., Shafee, N., Chua, K. B. & Lam, S. K. (1999). Molecular detection of enteroviruses from an outbreak of hand, foot and mouth disease in Malaysia in 1997. Scand J Infect Dis 31, 331-335.
2. Ahmad, K. (2000). Hand, foot, and mouth disease outbreak reported in Singapore. Lancet 356, 1338.
3. Arita, M., Shimizu, H. & Miyamura, T. (2004). Characterization of in vitro and in vivo phenotypes of poliovirus type 1 mutants with reduced viral protein synthesis activity. J Gen Virol 85, 1933-1944.
4. Bouchard, M. J., Lam, D. H. & Racaniello, V. R. (1995). Determinants of attenuation and temperature sensitivity in the type 1 poliovirus Sabin vaccine. J Virol 69, 4972-4978.
5. Brown, B. A. & Pallansch, M. A. (1995). Complete nucleotide sequence of enterovirus 71 is distinct from poliovirus. Virus Res 39, 195-205.
6. Brown, B. A., Oberste, M. S., Alexander, J. P., Jr, Kennett, M. L. & Pallansch, M. A. (1999). Molecular epidemiology and evolution of enterovirus 71 strains isolated from 1970 to 1998. J Virol 73, 9969-9975.
7. Chan, L. G., Parashar, U. D., Lye, M. S. & 9 other authors (2000). Deaths of children during an outbreak of hand, foot, and mouth disease in Sarawak, Malaysia: clinical and pathological characteristics of the disease. Clin Infect Dis 31, 678-683.
8. Chen, Y.-C., Yu, C.-K., Wang, Y.-F., Liu, C.-C., Su, I.-J. & Lei, H.-Y. (2004). A murine oral enterovirus 71 infection model with central nervous system involvement. J Gen Virol 85, 69-77.
9. Christodoulou, C., Colbere-Garapin, F., Macadam, A., Taffs, L. F., Marsden, S., Minor, P. & Horaud, F. (1990). Mapping of mutations associated with neurovirulence in monkeys infected with Sabin 1 poliovirus revertants selected at high temperature. J Virol 64, 4922-4929.
10. Chumakov, M., Voroshilova, M., Shindarov, L. & 16 other authors (1979). Enterovirus 71 isolated from cases of epidemic poliomyelitis-like disease in Bulgaria. Arch Virol 60, 329-340.
11. Evans, D. M., Dunn, G., Minor, P. D., Schild, G. C., Cann, A. J., Stanway, G., Almond, J. W., Currey, K. & Maizel, J. V., Jr (1985). Increased neurovirulence associated with a single nucleotide change in a noncoding region of the Sabin type 3 poliovaccine genome. Nature 314, 548-550.
12. Fujimoto, T., Chikahira, M., Yoshida, S., Ebira, H., Hasegawa, A., Totsuka, A. & Nishio, O. (2002). Outbreak of central nervous system disease associated with hand, foot, and mouth disease in Japan during the summer of 2000: detection and molecular epidemiology of enterovirus 71. Microbiol Immunol 46, 621-627.
13. Georgescu, M. M., Tardy-Panit, M., Guillot, S., Crainic, R. & Delpeyroux, F. (1995). Mapping of mutations contributing to the temperature sensitivity of the Sabin 1 vaccine strain of poliovirus. J Virol 69, 5278-5286.
14. Hagiwara, A., Yoneyama, T. & Hashimoto, I. (1983). Isolation of a temperature-sensitive strain of enterovirus 71 with reduced neurovirulence for monkeys. J Gen Virol 64, 499-502.
15. Hansen, J. L., Long, A. M. & Schultz, S. C. (1997). Structure of the RNA-dependent RNA polymerase of poliovirus. Structure 5, 1109-1122.
16. Hashimoto, I. & Hagiwara, A. (1983). Comparative studies on the neurovirulence of temperature-sensitive and temperature-resistant viruses of enterovirus 71 in monkeys. Acta Neuropathol 60, 266-270.
17. Hashimoto, I., Hagiwara, A. & Kodama, H. (1978). Neurovirulence in cynomolgus monkeys of enterovirus 71 isolated from a patient with hand, foot and mouth disease. Arch Virol 56, 257-261.
18. Herrero, L. J., Lee, C. S. M., Hurrelbrink, R. J., Chua, B. H., Chua, K. B. & McMinn, P. C. (2003). Molecular epidemiology of enterovirus 71 in peninsular Malaysia, 1997-2000. Arch Virol 148, 1369-1385.
19. Ho, M., Chen, E.-R., Hsu, K.-H., Twu, S.-J., Chen, K.-T., Tsai, S.-F., Wang, J.-R. & Shih, S.-R. (1999). An epidemic of enterovirus 71 infection in Taiwan. N Engl J Med 341, 929-935.
20. Hogle, J. M., Chow, M. & Filman, D. J. (1985). Three-dimensional structure of poliovirus at 2.9 Å resolution. Science 229, 1358-1365.
21. Horie, H., Koike, S., Kurata, T. & 11 other authors (1994). Transgenic mice carrying the human poliovirus receptor: new animal model for study of poliovirus neurovirulence. J Virol 68, 681-688.
22. Kärber, G. (1931). Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. Arch Exp Pathol Pharmakol 162, 480-483 (in German).
23. Kauder, S. E. & Racaniello, V. R. (2004). Poliovirus tropism and attenuation are determined after internal ribosome entry. J Clin Invest 113, 1743-1753.
24. Kawamura, N., Kohara, M., Abe, S., Komatsu, T., Tago, K., Arita, M. & Nomoto, A. (1989). Determinants in the 5′ noncoding region of poliovirus Sabin 1 RNA that influence the attenuation phenotype. J Virol 63, 1302-1309.
25. Koike, S., Horie, H., Sato, Y., Ise, I., Taya, C., Nomura, T., Yoshioka, I., Yonekawa; H. & Nomoto, A. (1993). Poliovirus-sensitive transgenic mice as a new animal model. Dev Biol Stand 78, 101-107.
26. Komatsu, H., Shimizu, Y., Takeuchi, Y., Ishiko, H. & Takada, H. (1999). Outbreak of severe neurologic involvement associated with enterovirus 71 infection. Pediatr Neurol 20, 17-23.
27. Kuo, R.-L., Kung, S.-H., Hsu, Y.-Y. & Liu, W.-T. (2002). Infection with enterovirus 71 or expression of its 2A protease induces apoptotic cell death. J Gen Virol 83, 1367-1376.
28. Li, M.-L., Hsu, T.-A., Chen, T.-C., Chang, S.-C., Lee, J.-C., Chen, C.-C., Stollar, V. & Shih, S.-R. (2002). The 3C protease activity of enterovirus 71 induces human neural cell apoptosis. Virology 293, 386-395.
29. Lin, T.-Y., Twu, S.-J., Ho, M.-S., Chang, L.-Y. & Lee, C.-Y. (2003). Enterovirus 71 outbreaks, Taiwan: occurrence and recognition. Emerg Infect Dis 9, 291-293.
30. Lu, H.-H., Alexander, L. & Wimmer, E. (1995). Construction and genetic analysis of dicistronic polioviruses containing open reading frames for epitopes of human immunodeficiency virus type 1 gp120. J Virol 69, 4797-4806.
31. Lu, C.-Y., Lee, C.-Y., Kao, C.-L. & 8 other authors (2002). Incidence and case-fatality rates resulting from the 1998 enterovirus 71 outbreak in Taiwan. J Med Virol 67, 217-223.
32. Lum, L. C. S., Wong, K. T., Lam, S. K. & 7 other authors (1998). Fatal enterovirus 71 encephalomyelitis. J Pediatr 133, 795-798.
33. Macadam, A. J., Arnold, C., Howlett, J. & 9 other authors (1989). Reversion of the attenuated and temperature-sensitive phenotypes of the Sabin type 3 strain of poliovirus in vaccinees. Virology 172, 408-414.
34. Macadam, A. J., Pollard, S. R., Ferguson, G., Dunn, G., Skuce, R., Almond, J. W. & Minor, P. D. (1991). The 5′ noncoding region of the type 2 poliovirus vaccine strain contains determinants of attenuation and temperature sensitivity. Virology 181, 451-458.
35. Malnou, C. E., Werner, A., Borman, A. M., Westhof, E. & Kean, K. M. (2003). Effects of vaccine strain mutations in domain V of the internal ribosome entry segment compared in the wild type poliovirus type 1 context. J Biol Chem 279, 10261-10269.
36. McMinn, P. C. (2002). An overview of the evolution of enterovirus 71 and its clinical and public health significance. FEMS Microbiol Rev 26, 91-107.
37. McMinn, P., Stratov, I. & Dowse, G. (1999). Enterovirus 71 outbreak in Western Australia associated with acute flaccid paralysis. Preliminary report. Commun Dis Intell 23, 199.
38. McMinn, P., Lindsay, K., Perera, D., Chan, H. M., Chan, K. P. & Cardosa, M. J. (2001a). Phylogenetic analysis of enterovirus 71 strains isolated during linked epidemics in Malaysia, Singapore, and Western Australia. J Virol 75, 7732-7738.
39. McMinn, P., Stratov, I., Nagarajan, L. & Davis, S. (2001b). Neurological manifestations of enterovirus 71 infection in children during an outbreak of hand, foot, and mouth disease in Western Australia. Clin Infect Dis 32, 236-242.
40. Minor, P. D. (1992). The molecular biology of poliovaccines. J Gen Virol 73, 3065-3077.
41. Minor, P. D., Dunn, G., Evans, D. M. A. & 8 other authors (1989). The temperature sensitivity of the Sabin type 3 vaccine strain of poliovirus: molecular and structural effects of a mutation in the capsid protein VP3. J Gen Virol 70, 1117-1123.
42. Muzychenko, A. R., Lipskaya, G. Yu., Maslova, S. V., Svitkin, Y. V., Pilipenko, E. V., Nottay, B. K., Kew, O. M. & Agol, V. I. (1991). Coupled mutations in the 5′-untranslated region of the Sabin poliovirus strains during in vivo passages: structural and functional implications. Virus Res 21, 111-122.
43. Nagata, N., Shimizu, H., Ami, Y. & 7 other authors (2002). Pyramidal and extrapyramidal involvement in experimental infection of cynomolgus monkeys with enterovirus 71. J Med Virol 67, 207-216.
44. Nagata, N., Iwasaki, T., Ami, Y. & 8 other authors (2004). Differential localization of neurons susceptible to enterovirus 71 and poliovirus type 1 in the central nervous system of cynomolgus monkeys after intravenous inoculation. J Gen Virol 85, 2981-2989.
45. Omata, T., Kohara, M., Kuge, S. & 8 other authors (1986). Genetic analysis of the attenuation phenotype of poliovirus type 1. J Virol 58, 348-358.
46. Paul, A. V., Mugavero, J., Yin, J., Hobson, S., Schultz, S., van Boom, J. H. & Wimmer, E. (2000). Studies on the attenuation phenotype of polio vaccines: poliovirus RNA polymerase derived from Sabin type 1 sequence is temperature sensitive in the uridylylation of VPg. Virology 272, 72-84.
47. Pilipenko, E. V., Blinov, V. M., Romanova, L. I., Sinyakov, A. N., Maslova, S. V. & Agol, V. I. (1989). Conserved structural domains in the 5′-untranslated region of picornaviral genomes: an analysis of the segment controlling translation and neurovirulence. Virology 168, 201-209.
48. Pulli, T., Koskimies, P. & Hyypiä, T. (1995). Molecular comparison of coxsackie A virus serotypes. Virology 212, 30-38.
49. Ren, R., Costantini, F., Gorgacz, E. J., Lee, J. J. & Racaniello, V. R. (1990). Transgenic mice expressing a human poliovirus receptor: a new model for poliomyelitis. Cell 63, 353-362.
50. Rowe, A., Ferguson, G. L., Minor, P. D. & Macadam, A. J. (2000). Coding changes in the poliovirus protease 2A compensate for 5′NCR domain V disruptions in a cell-specific manner. Virology 269, 284-293.
51. Sambrook, J. & Russell, D. (2001). Molecular Cloning: a Laboratory Manual, 3rd edn, pp. 13.19-13.25. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
52. Schmidt, N. J., Lennette, E. H. & Ho, H. H. (1974). An apparently new enterovirus isolated from patients with disease of the central nervous system. J Infect Dis 129, 304-309.
53. Shimizu, H., Utama, A., Yoshii, K. & 13 other authors (1999). Enterovirus 71 from fatal and nonfatal cases of hand, foot and mouth disease epidemics in Malaysia, Japan and Taiwan in 1997-1998. Jpn J Infect Dis 52, 12-15.
54. Svitkin, Y. V., Maslova, S. V. & Agol, V. I. (1985). The genomes of attenuated and virulent poliovirus strains differ in their in vitro translation efficiencies. Virology 147, 243-252.
55. Svitkin, Y. V., Pestova, T. V., Maslova, S. V. & Agol, V. I. (1988). Point mutations modify the response of poliovirus RNA to a translation initiation factor: a comparison of neurovirulent and attenuated strains. Virology 166, 394-404.
56. Svitkin, Y. V., Cammack, N., Minor, P. D. & Almond, J. W. (1990). Translation deficiency of the Sabin type 3 poliovirus genome: association with an attenuating mutation C472→U. Virology 175, 103-109.
57. Tardy-Panit, M., Blondel, B., Martin, A., Tekaia, F., Horaud, F. & Delpeyroux, F. (1993). A mutation in the RNA polymerase of poliovirus type 1 contributes to attenuation in mice. J Virol 67, 4630-4638.
58. Thompson, S. R. & Sarnow, P. (2003). Enterovirus 71 contains a type I IRES element that functions when eukaryotic initiation factor eIF4G is cleaved. Virology 315, 259-266.
59. Wang, J.-R., Tuan, Y.-C., Tsai, H.-P., Yan, J.-J., Liu, C.-C. & Su, I. J. (2002). Change of major genotype of enterovirus 71 in outbreaks of hand-foot-and-mouth disease in Taiwan between 1998 and 2000. J Clin Microbiol 40, 10-15.
60. Wang, S.-M., Lei, H.-Y., Huang, K.-J., Wu, J.-M., Wang, J.-R., Yu, C.-K., Su, I.-J. & Liu, C.-C. (2003). Pathogenesis of enterovirus 71 brainstem encephalitis in pediatric patients: roles of cytokines and cellular immune activation in patients with pulmonary edema. J Infect Dis 188, 564-570.
61. Wang, Y.-F., Chou, C.-T., Lei, H.-Y. & 8 other authors (2004). A mouse-adapted enterovirus 71 strain causes neurological disease in mice after oral infection. J Virol 78, 7916-7924.
62. Westrop, G. D., Wareham, K. A., Evans, D. M. A. & 8 other authors (1989). Genetic basis of attenuation of the Sabin type 3 oral poliovirus vaccine. J Virol 63, 1338-1344.
63. Zhao, W. D., Lahser, F. C. & Wimmer, E. (2000). Genetic analysis of a poliovirus/hepatitis C virus (HCV) chimera: interaction between the poliovirus cloverleaf and a sequence in the HCV 5′ nontranslated region results in a replication phenotype. J Virol 74, 6223-6226.