Age-dependent poliovirus replication in the mouse central nervous system is determined by internal ribosome entry site-mediated translation

Journal of Virology

Volumn 80, Issue 6, 2006, Pages 2589-2595

  Kauder, Steven ^a,b   Kan, Sherry ^a,c   Racaniello, Vincent R ^a  

^a Columbia University College of Physicians and Surgeons ^*  (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD155 ANTIGEN; MESSENGER RNA; UNCLASSIFIED DRUG; VIRUS RECEPTOR;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; HUMAN; HUMAN ADENOVIRUS; HUMAN CELL; HUMAN RHINOVIRUS; INTERNAL RIBOSOME ENTRY SITE; MOUSE; NEWBORN; NONHUMAN; PARALYSIS; POLIOMYELITIS VIRUS; PRIORITY JOURNAL; SPECIES DIFFERENCE; SPINAL CORD; TRANSGENIC MOUSE; VIRUS INFECTION; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BRAIN; CELL LINE; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION REGULATION, VIRAL; HELA CELLS; HUMANS; MICE; MICE, TRANSGENIC; POLIOMYELITIS; POLIOVIRUS; PROTEIN BIOSYNTHESIS; RECOMBINATION, GENETIC; RHINOVIRUS; RIBOSOMES; SPINAL CORD; VIRULENCE; VIRUS REPLICATION;

ANIMALIA; HUMAN ADENOVIRUS; HUMAN RHINOVIRUS SP.; MURINAE; MUS MUSCULUS; POLIOVIRUS;

EID: 33644755623     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.6.2589-2595.2006     Document Type: Article

References (43)

1. Arruda, E., T. R. Boyle, B. Winther, D. C. Pevear, J. M. Gwaltney, Jr., and F. G. Hayden. 1995. Localization of human rhinovirus replication in the upper respiratory tract by in situ hybridization. J. Infect. Dis. 171:1329-1333.
2. Bardin, P. G., S. L. Johnston, G. Sanderson, B. S. Robinson, M. A. Pickett, D. J. Fraenkel, and S. T. Holgate. 1994. Detection of rhinovirus infection of the nasal mucosa by oligonucleotide in situ hybridization. Am. J. Respir. Cell Mol. Biol. 10:207-213.
3. Belsham, G. J., and N. Sonenberg. 1996. RNA-protein interactions in regulation of picornavirus RNA translation. Microbiol. Rev. 60:499-511.
4. Borman, A., and R. J. Jackson. 1992. Initiation of translation of human rhinovirus RNA: mapping the internal ribosome entry site. Virology 188: 685-696.
5. Borman, A. M., P. Le Mercier, M. Girard, and K. M. Kean. 1997. Comparison of picornaviral IRES-driven internal initiation of translation in cultured cells of different origins. Nucleic Acids Res. 25:925-932.
6. Both, G. W., Y. Furuichi, S. Muthukrishnan, and A. J. Shatkin. 1975. Ribosome binding to rcovirus mRNA in protein synthesis requires 5′ terminal 7-methylguanosine. Cell 6:185-195.
7. Chen, C. Y., and P. Sarnow. 1995. Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science 268:415-417.
8. Couch, R. B. 2001. Rhinoviruses, p. 777-798. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 4th ed., vol. 1. Lippincott Williams & Wilkins, Philadelphia, Pa.
9. Creancier, L., D. Morello, P. Mercier, and A. C. Prats. 2000. Fibroblast growth factor 2 internal ribosome entry site (IRES) activity ex vivo and in transgenic mice reveals a stringent tissue-specific regulation. J. Cell Biol. 150:275-281.
10. Dick, E. C. 1968. Experimental infections of chimpanzees with human rhinovirus types 14 and 43. Proc. Soc. Exp. Biol. Med. 127:1079-1081.
11. Douglas, R. G., Jr., B. R. Alford, and R. B. Couch. 1968. Atraumatic nasal biopsy for studies of respiratory virus infection in volunteers. Antimicrob. Agents Chemother. 8:340-343.
12. Duechler, M., S. Ketter, T. Skern, E. Kuechler, and D. Blaas. 1993. Rhinoviral receptor discrimination: mutational changes in the canyon regions of human rhinovirus types 2 and 14 indicate a different site of interaction. J. Gen. Virol. 74:2287-2291.
13. Fannjiang, Y., C. H. Kim, R. L. Huganir, S. Zou, T. Lindsten, C. B. Thompson, T. Mito, R. J. Traystman, T. Larsen, D. E. Griffin, A. S. Mandir, T. M. Dawson, S. Dike, A. L. Sappington, D. A. Kerr, E. A. Jonas, L. K. Kaczmarek, and J. M. Hardwick. 2003. BAK alters neuronal excitability and can switch from anti- to pro-death function during postnatal development. Dev. Cell 4:575-585.
14. Gromeier, M., L. Alexander, and E. Wimmer. 1996. Internal ribosomal entry site substitution eliminates neurovirulence in intergeneric poliovirus recombinants. Proc. Natl. Acad. Sci. USA 93:2370-2375.
15. Gromeier, M., B. Bossert, M. Arita, A. Nomoto, and E. Wimmer. 1999. Dual stem loops within the poliovirus internal ribosomal entry site control neurovirulence. J. Virol. 73:958-964.
16. Harris, J. R., and V. R. Racaniello. 2005. Amino acid changes in proteins 2B and 3A mediate rhinovirus type 39 growth in mouse cells. J. Virol. 79:5363-5373.
17. Harris, J. R., and V. R. Racaniello. 2003. Changes in rhinovirus protein 2C allow efficient replication in mouse cells. J. Virol. 77:4773-4780.
18. Hughes, S. A., H. M. Thaker, and V. R. Racaniello. 2003. Transgenic mouse model for echovirus myocarditis and paralysis. Proc. Natl. Acad. Sci. USA 100:15906-15911.
19. Ida-Hosonuma, M., T. Iwasaki, T. Yoshikawa, N. Nagata, Y. Sato, T. Sata, M. Yoneyama, T. Fujita, C. Taya, H. Yonekawa, and S. Koike. 2005. The alpha/beta interferon response controls tissue tropism and pathogenicity of poliovirus. J. Virol. 79:4460-4469.
20. Kauder, S. E., and V. R. Racaniello. 2004. Poliovirus tropism and attenuation are determined after internal ribosome entry. J. Clin. Investig. 113:1743-1753.
21. Khatib, R., J. L. Chason, B. K. Silberberg, and A. M. Lerner. 1980. Age-dependent pathogenicity of group B coxsackieviruses in Swiss-Webster mice: infectivity for myocardium and pancreas. J. Infect. Dis. 141:394-403.
22. Kisch, A. L., P. A. Webb, and K. M. Johnson. 1964. Further properties of five newly recognized picornaviruses (rhinoviruses). Am. J. Hyg. 79:125-133.
23. Koike, S., C. Taya, T. Kurata, S. Abe, I. Ise, H. Yonekawa, and A. Nomoto. 1991. Transgenic mice susceptible to poliovirus. Proc. Natl. Acad. Sci. USA 88:951-955.
24. Kozak, M. 1979. Inability of circular mRNA to attach to eukaryotic ribosomes. Nature 280:82-85.
25. Kozak, M. 1989. The scanning model for translation: an update. J. Cell Biol. 108:229-241.
26. Labrada, L., X. H. Liang, W. Zheng, C. Johnston, and B. Levine. 2002. Age-dependent resistance to lethal alphavirus encephalitis in mice: analysis of gene expression in the central nervous system and identification of a novel interferon-inducible protective gene, mouse ISG12. J. Virol. 76:11688-11703.
27. Lawrence, D. M., M. M. Vaughn, A. R. Belman, J. S. Cole, and G. F. Rall. 1999. Immune response-mediated protection of adult but not neonatal mice from neuron-restricted measles virus infection and central nervous system disease. J. Virol. 73:1795-1801.
28. Lewis, J., G. A. Oyler, K. Ueno, Y. R. Fannjiang, B. N. Chau, J. Vornov, S. J. Korsmeyer, S. Zou, and J. M. Hardwick. 1999. Inhibition of virus-induced neuronal apoptosis by Bax. Nat. Med. 5:832-835.
29. Lomax, N. B., and F. H. Yin. 1989. Evidence for the role of the P2 protein of human rhinovirus in its host range change. J. Virol. 63:2396-2399.
30. McCright, I. J., I. Tsunoda, F. G. Whitby, and R. S. Fujinami. 1999. Theiler's viruses with mutations in loop 1 of VP1 lead to altered tropism and pathogenesis. J. Virol. 73:2814-2824.
31. Mendelsohn, C. L., E. Wimmer, and V. R. Racaniello. 1989. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 56:855-865.
32. Pelletier, J., G. Kaplan, V. R. Racaniello, and N. Sonenberg. 1988. Cap-independent translation of poliovirus mRNA is conferred by sequence elements within the 5′ noncoding region. Mol. Cell. Biol. 8:1103-1112.
33. Pelletier, J., and N. Sonenberg. 1988. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334:320-325.
34. Pilipenko, E. V., T. V. Pestova, V. G. Kolupaeva, E. V. Khitrina, A. N. Poperechnaya, V. I. Agol, and C. U. Hellen. 2000. A cell cycle-dependent protein serves as a template-specific translation initiation factor. Genes Dev. 14:2028-2045.
35. Pinto, C. A., and R. F. Haff. 1969. Experimental infection of gibbons with rhinovirus. Nature 224:131-311.
36. Pitkaranta, A., and F. G. Hayden. 1998. Rhinoviruses: important respiratory pathogens. Ann. Med. 30:529-537.
37. Reithmayer, M., A. Reischl, L. Snyers, and D. Blaas. 2002. Species-specific receptor recognition by a minor-group human rhinovirus (HRV): HRV serotype IA distinguishes between the murine and the human low-density lipoprotein receptor. J. Virol. 76:6957-6965.
38. Ren, R. B., F. Costantini, E. J. Gorgacz, J. J. Lee, and V. R. Racaniello. 1990. Transgenic mice expressing a human poliovirus receptor: a new model for poliomyelitis. Cell 63:353-362.
39. Shaw-Jackson, C., and T. Michiels. 1999. Absence of internal ribosome entry site-mediated tissue specificity in the translation of a bicistronic transgene. J. Virol. 73:2729-2738.
40. Tracy, S., K. Hofling, S. Pirruccello, P. H. Lane, S. M. Reyna, and C. J. Gauntt. 2000. Group B coxsackievirus myocarditis and pancreatitis: connection between viral virulence phenotypes in mice. J. Med. Virol. 62: 70-81.
41. Turner, R. B., B. Winther, J. O. Hendley, N. Mygind, and J. M. Gwaltney, Jr. 1984. Sites of virus recovery and antigen detection in epithelial cells during experimental rhinovirus infection. Acta Otolaryngol. Suppl. 413:9-14.
42. Yanagiya, A., S. Ohka, N. Hashida, M. Okamura, C. Taya, N. Kamoshita, K. Iwasaki, Y. Sasaki, H. Yonekawa, and A. Nomoto. 2003. Tissue-specific replicating capacity of a chimeric poliovirus that carries the internal ribosome entry site of hepatitis C virus in a new mouse model transgenic for the human poliovirus receptor. J. Virol. 77:10479-10487.
43. Yin, F. H., and N. B. Lomax. 1983. Host range mutants of human rhinovirus in which nonstructural proteins are altered. J. Virol. 48:410-418.