Replication of Ljungan virus in cell culture: The genomic 5′-end, infectious cDNA clones and host cell response to viral infections

Virus Research

Volumn 130, Issue 1-2, 2007, Pages 129-139

  Ekström, Jens Ola ^a   Tolf, Conny ^a   Fahlgren, Camilla ^a   Johansson, E Susanne ^a   Arbrandt, Gustav ^a,b   Niklasson, Bo ^b   Edman, Kjell A ^a   Lindberg, A Michael ^a  

^a LINNAEUS UNIVERSITY   (Sweden)

^b Apodemus AB   (Sweden)

Author keywords

5 RACE; Infectious cDNA clone; Parechovirus; Picornavirus; Virus transmission

Indexed keywords

COMPLEMENTARY DNA;

5' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; CYTOLYSIS; CYTOPATHOGENIC EFFECT; HOST CELL; LJUNGAN VIRUS; MOLECULAR CLONING; NONHUMAN; PICORNAVIRUS; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSLATION; VIRUS INFECTION; VIRUS REPLICATION; VIRUS TRANSMISSION;

5' UNTRANSLATED REGIONS; ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; CYTOPATHOGENIC EFFECT, VIRAL; DNA, COMPLEMENTARY; PARECHOVIRUS; PLAQUE ASSAY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; SEQUENCE ANALYSIS; VIRUS CULTIVATION; VIRUS REPLICATION;

CLETHRIONOMYS GLAREOLUS; LJUNGAN VIRUS; PARECHOVIRUS; PICORNAVIRIDAE;

EID: 34548834185     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2007.06.004     Document Type: Article

References (68)

1. Abed Y., and Boivin G. Human parechovirus infections in Canada. Emerg. Infect. Dis. 12 6 (2006) 969-975
2. Ball T.B., Plummer F.A., and HayGlass K.T. Improved mRNA quantitation in LightCycler RT-PCR. Int. Arch. Allergy. Immunol. 130 1 (2003) 82-86
3. Belsham G.J., and Sonenberg N. RNA-protein interactions in regulation of picornavirus RNA translation. Microbiol. Rev. 60 3 (1996) 499-511
4. Boyer J.C., and Haenni A.L. Infectious transcripts and cDNA clones of RNA viruses. Virology 198 2 (1994) 415-426
5. Brown E.A., Day S.P., Jansen R.W., and Lemon S.M. The 5′ nontranslated region of hepatitis A virus RNA: secondary structure and elements required for translation in vitro. J. Virol. 65 11 (1991) 5828-5838
6. Chen D., and Patton J.T. Reverse transcriptase adds nontemplated nucleotides to cDNAs during 5′-RACE and primer extension. Biotechniques 30 3 (2001) 574-580 582
7. Coller B.A., Chapman N.M., Beck M.A., Pallansch M.A., Gauntt C.J., and Tracy S.M. Echovirus 22 is an atypical enterovirus. J. Virol. 64 6 (1990) 2692-2701
8. Crowell R.L., and Syverton J.T. The mammalian cell-virus relationship. VI. Sustained infection of HeLa cells by Coxsackie B3 virus and effect on superinfection. J. Exp. Med. 113 (1961) 419-435
9. Devaney M.A., Vakharia V.N., Lloyd R.E., Ehrenfeld E., and Grubman M.J. Leader protein of foot-and-mouth disease virus is required for cleavage of the p220 component of the cap-binding protein complex. J. Virol. 62 11 (1988) 4407-4409
10. Dildine S.L., and Semler B.L. Conservation of RNA-protein interactions among picornaviruses. J. Virol. 66 7 (1992) 4364-4376
11. Dobos P. Use of gum tragacanth overlay, applied at room temperature, in the plaque assay of fish and other animal viruses. J. Clin. Microbiol. 3 3 (1976) 373-375
12. Donoso Mantke O., Kallies R., Niklasson B., Nitsche A., and Niedrig M. A new quantitative real-time reverse transcriptase PCR assay and melting curve analysis for detection and genotyping of Ljungan virus strains. J. Virol. Methods 141 (2007) 71-77
13. Du Z., Yu J., Ulyanov N.B., Andino R., and James T.L. Solution structure of a consensus stem-loop D RNA domain that plays important roles in regulating translation and replication in enteroviruses and rhinoviruses. Biochemistry 43 38 (2004) 11959-11972
14. Duke G.M., Hoffman M.A., and Palmenberg A.C. Sequence and structural elements that contribute to efficient encephalomyocarditis virus RNA translation. J. Virol. 66 3 (1992) 1602-1609
15. Dulbecco R., and Vogt M. Plaque formation and isolation of pure lines with poliomyelitis viruses. J. Exp. Med. 99 2 (1954) 167-1182
16. Frohman M.A., Dush M.K., and Martin G.R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc. Natl. Acad. Sci. U.S.A. 85 23 (1988) 8998-9002
17. Ghazi F., Hughes P.J., Hyypiä T., and Stanway G. Molecular analysis of human parechovirus type 2 (formerly echovirus 23). J. Gen. Virol. 79 11 (1998) 2641-2650
18. Giachetti C., and Semler B.L. Role of a viral membrane polypeptide in strand-specific initiation of poliovirus RNA synthesis. J. Virol. 65 5 (1991) 2647-2654
19. Gingras A.C., Svitkin Y., Belsham G.J., Pause A., and Sonenberg N. Activation of the translational suppressor 4E-BP1 following infection with encephalomyocarditis virus and poliovirus. Proc. Natl. Acad. Sci. U.S.A. 93 11 (1996) 5578-5583
20. Gradi A., Svitkin Y.V., Imataka H., and Sonenberg N. Proteolysis of human eukaryotic translation initiation factor eIF4GII, but not eIF4GI, coincides with the shutoff of host protein synthesis after poliovirus infection. Proc. Natl. Acad. Sci. U.S.A. 95 19 (1998) 11089-11094
21. Harvala H., Kalimo H., Dahllund L., Santti J., Hughes P., Hyypiä T., and Stanway G. Mapping of tissue tropism determinants in coxsackievirus genomes. J. Gen. Virol. 83 7 (2002) 1697-1706
22. Herold J., and Andino R. Poliovirus requires a precise 5′ end for efficient positive-strand RNA synthesis. J. Virol. 74 14 (2000) 6394-6400
23. Hughes P.J., and Stanway G. The 2A proteins of three diverse picornaviruses are related to each other and to the H-rev107 family of proteins involved in the control of cell proliferation. J. Gen. Virol. 81 1 (2000) 201-207
24. Jackson W.T., Giddings Jr. T.H., Taylor M.P., Mulinyawe S., Rabinovitch M., Kopito R.R., and Kirkegaard K. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 3 5 (2005) e156
25. Jamison R.M. An electron microscopic study of the intracellular development of echovirus 22. Arch. Gesamte Virusforsch. 44 3 (1974) 184-194
26. Johansson E.S., Ekström J.-O., Shafren D.R., Frisk G., Hyypiä T., Edman K., and Lindberg A.M. Cell culture propagation and biochemical analysis of the Ljungan virus prototype strain. Biochem. Biophys. Res. Commun. 317 4 (2004) 1023-1029
27. Johansson E.S., Niklasson B., Tesh R.B., Shafren D.R., Travassos da Rosa A.P., and Lindberg A.M. Molecular characterization of M1146, an American isolate of Ljungan virus (LV) reveals the presence of a new LV genotype. J. Gen. Virol. 84 4 (2003) 837-844
28. Johansson S., Niklasson B., Maizel J., Gorbalenya A.E., and Lindberg A.M. Molecular analysis of three Ljungan virus isolates reveals a new, close-to-root lineage of the Picornaviridae with a cluster of two unrelated 2A proteins. J. Virol. 76 17 (2002) 8920-8930
29. Johnson H.N. Diseases derived from wildlife. Calif. Health 23 (1965) 35-39
30. Kim K.S., Tracy S., Tapprich W., Bailey J., Lee C.K., Kim K., Barry W.H., and Chapman N.M. 5′-Terminal deletions occur in coxsackievirus B3 during replication in murine hearts and cardiac myocyte cultures and correlate with encapsidation of negative-strand viral RNA. J. Virol. 79 11 (2005) 7024-7041
31. Kim M.-C., Kwon Y.-K., Joh S.-J., Lindberg A.M., Kwon J.-H., Kim J.-H., and Kim S.-J. Molecular analysis of duck hepatitis virus type 1 reveals a novel lineage close to the genus Parechovirus in the family Picornaviridae. J. Gen. Virol. 87 11 (2006) 3307-3316
32. Krogerus C., Egger D., Samuilova O., Hyypiä T., and Bienz K. Replication complex of human parechovirus 1. J. Virol. 77 15 (2003) 8512-8523
33. Le S.Y., Chen J.H., Sonenberg N., and Maizel Jr. J.V. Conserved tertiary structural elements in the 5′ nontranslated region of cardiovirus, aphthovirus and hepatitis A virus RNAs. Nucleic Acids Res. 21 10 (1993) 2445-2451
34. Lindberg A.M., and Johansson S. Phylogenetic analysis of Ljungan virus and A-2 plaque virus, new members of the Picornaviridae. Virus Res. 85 1 (2002) 61-70
35. Lindberg A.M., Polacek C., and Johansson S. Amplification and cloning of complete enterovirus genomes by long distance PCR. J. Virol. Methods 65 2 (1997) 191-199
36. Main A.J., Shope R.E., and Wallis R.C. Characterization of Whitney's Clethrionomy gapperi virus isolates from Massachusetts. J. Wildlife Dis. 12 2 (1976) 154-164
37. Maltese E., Bucci M., Macchia S., Latorre P., Pagnotti P., Pierangeli A., and Bercoff R.P. Inhibition of cap-dependent gene expression induced by protein 2A of hepatitis A virus. J. Gen. Virol. 81 5 (2000) 1373-1381
38. Mathews D.H., Sabina J., Zuker M., and Turner D.H. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol. 288 5 (1999) 911-940
39. Myers T.W., and Gelfand D.H. Reverse transcription and DNA amplification by a Thermus thermophilus DNA polymerase. Biochemistry 30 31 (1991) 7661-7666
40. Nagashima S., Sasaki J., and Taniguchi K. The 5′-terminal region of the Aichi virus genome encodes cis-acting replication elements required for positive- and negative-strand RNA synthesis. J. Virol. 79 11 (2005) 6918-6931
41. Nateri A.S., Hughes P.J., and Stanway G. In vivo and in vitro identification of structural and sequence elements of the human parechovirus 5′ untranslated region required for internal initiation. J. Virol. 74 14 (2000) 6269-6277
42. Nateri A.S., Hughes P.J., and Stanway G. Terminal RNA replication elements in human parechovirus 1. J. Virol. 76 24 (2002) 13116-13122
43. Niklasson B., Heller K.E., Schonecker B., Bildsoe M., Daniels T., Hampe C.S., Widlund P., Simonson W.T., Schaefer J.B., Rutledge E., Bekris L., Lindberg A.M., Johansson S., Örtqvist E., Persson B., and Lernmark A. Development of type 1 diabetes in wild bank voles associated with islet autoantibodies and the novel Ljungan virus. Int. J. Exp. Diabetes Res. 4 (2003) 35-44
44. Niklasson B., Hörnfeldt B., and Lundman B. Could myocarditis, insulin-dependent diabetes mellitus, and Guillain-Barre syndrome be caused by one or more infectious agents carried by rodents?. Emerg. Infect. Dis. 4 2 (1998) 187-193
45. Niklasson B., Hörnfeldt B., Nyholm E., Niedrig M., Donoso-Mantke O., Gelderblom H.R., and Lernmark A. Type 1 diabetes in Swedish bank voles (Clethrionomys glareolus): signs of disease in both colonized and wild cyclic populations at peak density. Ann. N.Y. Acad. Sci. 1005 (2003) 170-175
46. Niklasson B., Kinnunen L., Hörnfeldt B., Hörling J., Benemar C., Hedlund K.O., Matskova L., Hyypiä T., and Winberg G. A new picornavirus isolated from bank voles (Clethrionomys glareolus). Virology 255 1 (1999) 86-93
47. Niklasson B., Nyholm E., Feinstein R.E., Samsioe A., and Hörnfeldt B. Diabetes and myocarditis in voles and lemmings at cyclic peak densities-induced by Ljungan virus?. Oecologia 150 1 (2006) 1-7
48. Niklasson B., Samsioe A., Blixt M., Sandler S., Sjöholm A., Lagerquist E., Lernmark A., and Klitz W. Prenatal viral exposure followed by adult stress produces glucose intolerance in a mouse model. Diabetologia 49 9 (2006) 2192-2199
49. Novak J.E., and Kirkegaard K. Improved method for detecting poliovirus negative strands used to demonstrate specificity of positive-strand encapsidation and the ratio of positive to negative strands in infected cells. J. Virol. 65 6 (1991) 3384-3387
50. Oberste M.S., Maher K., and Pallansch M.A. Complete sequence of echovirus 23 and its relationship to echovirus 22 and other human enteroviruses. Virus Res. 56 2 (1998) 217-223
51. Polacek C., Lundgren A., Andersson A., and Lindberg A.M. Genomic and phylogenetic characterization of coxsackievirus B2 prototype strain Ohio-1. Virus Res. 59 2 (1999) 229-238
52. Prather S.O., and Taylor M.W. Host-dependent restriction of mengovirus replication. II. Effect of host restriction on late viral RNA synthesis and viral maturation. J. Virol. 15 4 (1975) 872-881
53. Racaniello V.R. Picornaviridae: the viruses and their replication. In: Knipe D.M., Howley P.M., Griffin D.E., Lamb R.A., Matrin M.A., Riozman B., and Straus S.E. (Eds). Fields Virology. 4 ed. (2001), Lippincott Williams & Wilkins, Philadelphia 658-722
54. Reagan K.J., Goldberg B., and Crowell R.L. Altered receptor specificity of coxsackievirus B3 after growth in rhabdomyosarcoma cells. J. Virol. 49 3 (1984) 635-640
55. Samsioe A., Feinstein R., Saade G., Sjöholm A., Hörnfeldt B., Fundele R., Klitz W., and Niklasson B. Intrauterine death, fetal malformation, and delayed pregnancy in Ljungan virus-infected mice. Birth Defects Res. B Dev. Reprod. Toxicol. 77 4 (2006) 251-256
56. Shaver D.N., Barron A.L., and Karzon D.T. Distinctive cytopathology of ECHO viruses types 22 and 23. Proc. Soc. Exp. Biol. Med. 106 (1961) 648-652
57. Stanway G., Brown F., Christian P., Hovi T., Hyypiä T., King A.M.Q., Knowles N.J., Lemon S.M., Minor P.D., Pallansch M.A., Palmenberg A.C., and Skern T. Family Picornaviridae. In: Fauquet C.M., Mayo M.A., Maniloff J., Desselberger U., and Ball L.A. (Eds). Virus Taxonomy. Eighth Report of the International Committee on Taxonomy of Viruses (2005), Elsevier/Academic Press, London 757-778
58. Stanway G., Joki-Korpela P., and Hyypiä T. Human parechoviruses-biology and clinical significance. Rev. Med. Virol. 10 1 (2000) 57-69
59. Stanway G., Kalkkinen N., Roivainen M., Ghazi F., Khan M., Smyth M., Meurman O., and Hyypiä T. Molecular and biological characteristics of echovirus 22, a representative of a new picornavirus group. J. Virol. 68 12 (1994) 8232-8238
60. Stewart S.R., and Semler B.L. RNA determinants of picornavirus cap-indipendent translation initiation. Semin. Virol. 8 3 (1997) 242-255
61. Swanstrom R., Varmus H.E., and Bishop J.M. The terminal redundancy of the retrovirus genome facilitates chain elongation by reverse transcriptase. J. Biol. Chem. 256 3 (1981) 1115-1121
62. Svitkin Y.V., Gradi A., Imataka H., Morino S., and Sonenberg N. Eukaryotic initiation factor 4GII (eIF4GII), but not eIF4GI, cleavage correlates with inhibition of host cell protein synthesis after human rhinovirus infection. J. Virol. 73 4 (1999) 3467-3472
63. Trottier M., Kallio P., Wang W., and Lipton H.L. High numbers of viral RNA copies in the central nervous system of mice during persistent infection with Theiler's virus. J. Virol. 75 16 (2001) 7420-7428
64. Wall R., and Taylor M.W. Host-dependent restriction of mengovirus replication. J. Virol. 4 5 (1969) 681-687
65. Whitney E., Roz A.P., and Rayner G.A. Two viruses isolated from rodents (Clethronomys gapperi and Microtus pennsylvanicus) trapped in St. Lawrence County, New York. J. Wildlife Dis. 6 (1970) 48-55
66. Wigand R., and Sabin A.B. Properties of ECHO types 22, 23 and 24 viruses. Arch. Gesamte Virusforsch. 11 (1961) 224-247
67. Zoll J., Galama J.M., van Kuppeveld F.J., and Melchers W.J. Mengovirus leader is involved in the inhibition of host cell protein synthesis. J. Virol. 70 8 (1996) 4948-4952
68. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31 13 (2003) 3406-3415