A single nucleotide in stem loop II of 5′-untranslated region contributes to virulence of Enterovirus 71 in mice

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Yeh, Ming Te ^a   Wang, Shainn Wei ^a   Yu, Chun Keung ^a   Lin, Kuei Hsiang ^b   Lei, Huan Yao ^a   Su, Ih Jen ^c   Wang, Jen Ren ^a,c  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^c NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; URIDINE; VIRUS RNA;

5' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENTEROVIRUS 71; GENE MAPPING; GENETIC TRANSFECTION; GENOMIC FRAGMENT; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR CLONING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; REPLICON; RNA TRANSLATION; SINGLE NUCLEOTIDE POLYMORPHISM; SURVIVAL RATE; SURVIVAL TIME; VIRUS ISOLATION; VIRUS LOAD; VIRUS REPLICATION; VIRUS SURVIVAL; VIRUS TRANSCRIPTION; VIRUS VIRULENCE; ANIMAL; BRAIN; CONFORMATION; ENTEROVIRUS; ENTEROVIRUS INFECTION; GENETICS; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; MOLECULAR GENETICS; MORTALITY; PATHOGENICITY; PATHOLOGY; REGULATORY SEQUENCE; SEQUENCE HOMOLOGY; VIROLOGY; VIRULENCE; WESTERN BLOTTING;

HUMAN ENTEROVIRUS 71; MUS;

5' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; BRAIN; ENTEROVIRUS; ENTEROVIRUS INFECTIONS; MICE; MICE, INBRED ICR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; REGULATORY SEQUENCES, NUCLEIC ACID; RNA, VIRAL; SEQUENCE HOMOLOGY, NUCLEIC ACID; SURVIVAL RATE; VIRULENCE; VIRUS REPLICATION;

EID: 80055119062     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027082     Document Type: Article

References (61)

1. Brown BA, Pallansch MA, (1995) Complete nucleotide sequence of enterovirus 71 is distinct from poliovirus. Virus Res 39: 195-205.
2. Wimmer E, Hellen CU, Cao X, (1993) Genetics of poliovirus. Annu Rev Genet 27: 353-436.
3. Pelletier J, Kaplan G, Racaniello VR, Sonenberg N, (1988) Cap-independent translation of poliovirus mRNA is conferred by sequence elements within the 5′ noncoding region. Mol Cell Biol 8: 1103-1112.
4. Bedard KM, Semler BL, (2004) Regulation of picornavirus gene expression. Microbes Infect 6: 702-713.
5. Xiang W, Harris KS, Alexander L, Wimmer E, (1995) Interaction between the 5′-terminal cloverleaf and 3AB/3CDpro of poliovirus is essential for RNA replication. J Virol 69: 3658-3667.
6. Ochs K, Saleh L, Bassili G, Sonntag VH, Zeller A, et al. (2002) Interaction of translation initiation factor eIF4B with the poliovirus internal ribosome entry site. J Virol 76: 2113-2122.
7. Pelletier J, Sonenberg N, (1988) Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334: 320-325.
8. Thompson SR, Sarnow P, (2003) Enterovirus 71 contains a type I IRES element that functions when eukaryotic initiation factor eIF4G is cleaved. Virology 315: 259-266.
9. Ho M, (2000) Enterovirus 71: the virus, its infections and outbreaks. J Microbiol Immunol Infect 33: 205-216.
10. Chumakov M, Voroshilova M, Shindarov L, Lavrova I, Gracheva L, et al. (1979) Enterovirus 71 isolated from cases of epidemic poliomyelitis-like disease in Bulgaria. Arch Virol 60: 329-340.
11. Fujimoto T, Chikahira M, Yoshida S, Ebira H, Hasegawa A, et al. (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.
12. Cardosa MJ, Krishnan S, Tio PH, Perera D, Wong SC, (1999) Isolation of subgenus B adenovirus during a fatal outbreak of enterovirus 71-associated hand, foot, and mouth disease in Sibu, Sarawak. Lancet 354: 987-991.
13. Samuda GM, Chang WK, Yeung CY, Tang PS, (1987) Monoplegia caused by Enterovirus 71: an outbreak in Hong Kong. Pediatr Infect Dis J 6: 206-208.
14. Gilbert GL, Dickson KE, Waters MJ, Kennett ML, Land SA, et al. (1988) Outbreak of enterovirus 71 infection in Victoria, Australia, with a high incidence of neurologic involvement. Pediatr Infect Dis J 7: 484-488.
15. Nagy G, Takatsy S, Kukan E, Mihaly I, Domok I, (1982) Virological diagnosis of enterovirus type 71 infections: experiences gained during an epidemic of acute CNS diseases in Hungary in 1978. Arch Virol 71: 217-227.
16. Blomberg J, Lycke E, Ahlfors K, Johnsson T, Wolontis S, et al. (1974) Letter: New enterovirus type associated with epidemic of aseptic meningitis and-or hand, foot, and mouth disease. Lancet 2: 112.
17. Ho M, Chen ER, Hsu KH, Twu SJ, Chen KT, et al. (1999) An epidemic of enterovirus 71 infection in Taiwan. Taiwan Enterovirus Epidemic Working Group. N Engl J Med 341: 929-935.
18. Li L, He Y, Yang H, Zhu J, Xu X, et al. (2005) Genetic characteristics of human enterovirus 71 and coxsackievirus A16 circulating from 1999 to 2004 in Shenzhen, People's Republic of China. J Clin Microbiol 43: 3835-3839.
19. Solomon T, Lewthwaite P, Perera D, Cardosa MJ, McMinn P, et al. (2010) Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis 10: 778-790.
20. Weng KF, Chen LL, Huang PN, Shih SR, (2010) Neural pathogenesis of enterovirus 71 infection. Microbes Infect 12: 505-510.
21. Arita M, Ami Y, Wakita T, Shimizu H, (2008) Cooperative effect of the attenuation determinants derived from poliovirus sabin 1 strain is essential for attenuation of enterovirus 71 in the NOD/SCID mouse infection model. J Virol 82: 1787-1797.
22. Chua BH, Phuektes P, Sanders SA, Nicholls PK, McMinn PC, (2008) The molecular basis of mouse adaptation by human enterovirus 71. J Gen Virol 89: 1622-1632.
23. Evans DM, Dunn G, Minor PD, Schild GC, Cann AJ, et al. (1985) Increased neurovirulence associated with a single nucleotide change in a noncoding region of the Sabin type 3 poliovaccine genome. Nature 314: 548-550.
24. Guillot S, Otelea D, Delpeyroux F, Crainic R, (1994) Point mutations involved in the attenuation/neurovirulence alternation in type 1 and 2 oral polio vaccine strains detected by site-specific polymerase chain reaction. Vaccine 12: 503-507.
25. Rezapkin GV, Fan L, Asher DM, Fibi MR, Dragunsky EM, et al. (1999) Mutations in Sabin 2 strain of poliovirus and stability of attenuation phenotype. Virology 258: 152-160.
26. De Jesus N, Franco D, Paul A, Wimmer E, Cello J, (2005) Mutation of a single conserved nucleotide between the cloverleaf and internal ribosome entry site attenuates poliovirus neurovirulence. J Virol 79: 14235-14243.
27. Dunn JJ, Bradrick SS, Chapman NM, Tracy SM, Romero JR, (2003) The stem loop II within the 5′ nontranslated region of clinical coxsackievirus B3 genomes determines cardiovirulence phenotype in a murine model. J Infect Dis 187: 1552-1561.
28. Tu Z, Chapman NM, Hufnagel G, Tracy S, Romero JR, et al. (1995) The cardiovirulent phenotype of coxsackievirus B3 is determined at a single site in the genomic 5′ nontranslated region. J Virol 69: 4607-4618.
29. Rinehart JE, Gomez RM, Roos RP, (1997) Molecular determinants for virulence in coxsackievirus B1 infection. J Virol 71: 3986-3991.
30. Wang YF, Chou CT, Lei HY, Liu CC, Wang SM, et al. (2004) A mouse-adapted enterovirus 71 strain causes neurological disease in mice after oral infection. J Virol 78: 7916-7924.
31. Sambrook J, Russell DW, (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press.
32. Kung YH, Huang SW, Kuo PH, Kiang D, Ho MS, et al. (2010) Introduction of a strong temperature-sensitive phenotype into enterovirus 71 by altering an amino acid of virus 3D polymerase. Virology 396: 1-9.
33. Zuker M, (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415.
34. Reuter JS, Mathews DH, (2010) RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics 11: 129.
35. De Rijk P, Wuyts J, De Wachter R, (2003) RnaViz 2: an improved representation of RNA secondary structure. Bioinformatics 19: 299-300.
36. Chen CS, Yao YC, Lin SC, Lee YP, Wang YF, et al. (2007) Retrograde axonal transport: a major transmission route of enterovirus 71 in mice. J Virol 81: 8996-9003.
37. Yamayoshi S, Yamashita Y, Li J, Hanagata N, Minowa T, et al. (2009) Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nat Med 15: 798-801.
38. Gromeier M, Bossert B, Arita M, Nomoto A, Wimmer E, (1999) Dual stem loops within the poliovirus internal ribosomal entry site control neurovirulence. J Virol 73: 958-964.
39. Ishii T, Shiroki K, Iwai A, Nomoto A, (1999) Identification of a new element for RNA replication within the internal ribosome entry site of poliovirus RNA. J Gen Virol 80 (Pt 4): 917-920.
40. Dunn JJ, Chapman NM, Tracy S, Romero JR, (2000) Genomic determinants of cardiovirulence in coxsackievirus B3 clinical isolates: localization to the 5′ nontranslated region. J Virol 74: 4787-4794.
41. Barton DJ, O'Donnell BJ, Flanegan JB, (2001) 5′ cloverleaf in poliovirus RNA is a cis-acting replication element required for negative-strand synthesis. EMBO J 20: 1439-1448.
42. Malnou CE, Poyry TA, Jackson RJ, Kean KM, (2002) Poliovirus internal ribosome entry segment structure alterations that specifically affect function in neuronal cells: molecular genetic analysis. J Virol 76: 10617-10626.
43. Kauder SE, Racaniello VR, (2004) Poliovirus tropism and attenuation are determined after internal ribosome entry. The Journal of Clinical Investigation 113: 1743-1753.
44. Ishii T, Shiroki K, Hong DH, Aoki T, Ohta Y, et al. (1998) A new internal ribosomal entry site 5′ boundary is required for poliovirus translation initiation in a mouse system. J Virol 72: 2398-2405.
45. Shiroki K, Ishii T, Aoki T, Kobashi M, Ohka S, et al. (1995) A new cis-acting element for RNA replication within the 5′ noncoding region of poliovirus type 1 RNA. J Virol 69: 6825-6832.
46. Lee CK, Kono K, Haas E, Kim KS, Drescher KM, et al. (2005) Characterization of an infectious cDNA copy of the genome of a naturally occurring, avirulent coxsackievirus B3 clinical isolate. J Gen Virol 86: 197-210.
47. Bradrick SS, Lieben EA, Carden BM, Romero JR, (2001) A predicted secondary structural domain within the internal ribosome entry site of echovirus 12 mediates a cell-type-specific block to viral replication. J Virol 75: 6472-6481.
48. Klingel K, Hohenadl C, Canu A, Albrecht M, Seemann M, et al. (1992) Ongoing enterovirus-induced myocarditis is associated with persistent heart muscle infection: quantitative analysis of virus replication, tissue damage, and inflammation. Proceedings of the National Academy of Sciences of the United States of America 89: 314-318.
49. Omata T, Kohara M, Kuge S, Komatsu T, Abe S, et al. (1986) Genetic analysis of the attenuation phenotype of poliovirus type 1. Journal of virology 58: 348-358.
50. Gamarnik AV, Andino R, (2000) Interactions of viral protein 3CD and poly(rC) binding protein with the 5′ untranslated region of the poliovirus genome. Journal of virology 74: 2219-2226.
51. Gamarnik AV, Andino R, (1998) Switch from translation to RNA replication in a positive-stranded RNA virus. Genes & development 12: 2293-2304.
52. Skinner MA, Racaniello VR, Dunn G, Cooper J, Minor PD, et al. (1989) New model for the secondary structure of the 5′ non-coding RNA of poliovirus is supported by biochemical and genetic data that also show that RNA secondary structure is important in neurovirulence. J Mol Biol 207: 379-392.
53. Gutierrez AL, Denova-Ocampo M, Racaniello VR, del Angel RM, (1997) Attenuating mutations in the poliovirus 5′ untranslated region alter its interaction with polypyrimidine tract-binding protein. J Virol 71: 3826-3833.
54. Pilipenko EV, Viktorova EG, Guest ST, Agol VI, Roos RP, (2001) Cell-specific proteins regulate viral RNA translation and virus-induced disease. EMBO J 20: 6899-6908.
55. Lin JY, Shih SR, Pan M, Li C, Lue CF, et al. (2009) hnRNP A1 interacts with the 5′ untranslated regions of enterovirus 71 and Sindbis virus RNA and is required for viral replication. J Virol 83: 6106-6114.
56. Drake JW, (1999) The distribution of rates of spontaneous mutation over viruses, prokaryotes, and eukaryotes. Annals of the New York Academy of Sciences 870: 100-107.
57. Sun H-Y, Ou N-Y, Wang S-W, Liu W-C, Cheng T-F, et al. (2011) Novel Nucleotide and Amino Acid Covariation between the 5′UTR and the NS2/NS3 Proteins of Hepatitis C Virus: Bioinformatic and Functional Analyses. PLoS One 6: e25530.
58. Nishimura Y, Shimojima M, Tano Y, Miyamura T, Wakita T, et al. (2009) Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nat Med 15: 794-797.
59. Mota J, Rico-Hesse R, (2011) Dengue virus tropism in humanized mice recapitulates human dengue fever. PloS one 6: e20762.
60. Mota J, Rico-Hesse R, (2009) Humanized mice show clinical signs of dengue fever according to infecting virus genotype. Journal of virology 83: 8638-8645.
61. Berges BK, Rowan MR, (2011) The utility of the new generation of humanized mice to study HIV-1 infection: transmission, prevention, pathogenesis, and treatment. Retrovirology 8: 65.