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. 1995 Aug;69(8):4607–4618. doi: 10.1128/jvi.69.8.4607-4618.1995

The cardiovirulent phenotype of coxsackievirus B3 is determined at a single site in the genomic 5' nontranslated region.

Z Tu 1, N M Chapman 1, G Hufnagel 1, S Tracy 1, J R Romero 1, W H Barry 1, L Zhao 1, K Currey 1, B Shapiro 1
PMCID: PMC189260  PMID: 7609025

Abstract

We report the construction of chimeric coxsackievirus B3 (CVB3) strains in which sequences of an infectious cDNA copy of a noncardiovirulent CVB3 genome were replaced by the homologous sequences from a cardiovirulent CVB3 genome to identify which of 10 predicted genetic sites determine cardiovirulence. Cardiovirulent phenotype expression was consistently linked to nucleotide 234 (U in cardiovirulent CVB3 and C in avirulent CVB3) in the 5' nontranslated region. Reconstructions of the parental noncardiovirulent CVB3 genome from chimeras restored the noncardiovirulent phenotype when tested in mice. Inoculation of severe combined immunodeficient (scid) mice with the noncardiovirulent CVB3 strain resulted in massive cardiomyocyte necrosis in all animals. Sequence analysis of viral genomes isolated from twelve scid mouse hearts showed that only nucleotide position 234 was different (a C-->U transition) from that in the input parental noncardiovirulent CVB3 genome. Higher-order RNA structures predicted by two different algorithms did not demonstrate an obvious local effect caused by the C-->U change at nucleotide 234. Initial studies of parental and chimeric CVB3 replication in primary cultures of fetal murine heart fibroblasts and in adult murine cardiac myocytes demonstrated that viral RNA transcriptional efficiency is approximately 10-fold lower for noncardiovirulent CVB3 than for cardiovirulent CVB3. CVB3 did not shut off protein synthesis in murine cardiac fibroblasts, nor were levels of viral protein synthesis significantly different as a function of viral phenotype. Taken together, these data support a significant role for determination of the CVB3 cardiovirulence phenotype by nucleotide 234 in the 5' nontranslated region, possibly via a transcriptional mechanism.

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Selected References

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  1. Agol V. I., Drozdov S. G., Ivannikova T. A., Kolesnikova M. S., Korolev M. B., Tolskaya E. A. Restricted growth of attenuated poliovirus strains in cultured cells of a human neuroblastoma. J Virol. 1989 Sep;63(9):4034–4038. doi: 10.1128/jvi.63.9.4034-4038.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Agol V. I. The 5'-untranslated region of picornaviral genomes. Adv Virus Res. 1991;40:103–180. doi: 10.1016/S0065-3527(08)60278-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Almond J. W. The attenuation of poliovirus neurovirulence. Annu Rev Microbiol. 1987;41:153–180. doi: 10.1146/annurev.mi.41.100187.001101. [DOI] [PubMed] [Google Scholar]
  4. Andino R., Rieckhof G. E., Achacoso P. L., Baltimore D. Poliovirus RNA synthesis utilizes an RNP complex formed around the 5'-end of viral RNA. EMBO J. 1993 Sep;12(9):3587–3598. doi: 10.1002/j.1460-2075.1993.tb06032.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beck M. A., Chapman N. M., McManus B. M., Mullican J. C., Tracy S. Secondary enterovirus infection in the murine model of myocarditis. Pathologic and immunologic aspects. Am J Pathol. 1990 Mar;136(3):669–681. [PMC free article] [PubMed] [Google Scholar]
  6. Beck M. A., Tracy S. M. Murine cell-mediated immune response recognizes an enterovirus group-specific antigen(s). J Virol. 1989 Oct;63(10):4148–4156. doi: 10.1128/jvi.63.10.4148-4156.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Benndorf K., Boldt W., Nilius B. Sodium current in single myocardial mouse cells. Pflugers Arch. 1985 May;404(2):190–196. doi: 10.1007/BF00585418. [DOI] [PubMed] [Google Scholar]
  8. Borman A. M., Deliat F. G., Kean K. M. Sequences within the poliovirus internal ribosome entry segment control viral RNA synthesis. EMBO J. 1994 Jul 1;13(13):3149–3157. doi: 10.1002/j.1460-2075.1994.tb06613.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Borman A., Howell M. T., Patton J. G., Jackson R. J. The involvement of a spliceosome component in internal initiation of human rhinovirus RNA translation. J Gen Virol. 1993 Sep;74(Pt 9):1775–1788. doi: 10.1099/0022-1317-74-9-1775. [DOI] [PubMed] [Google Scholar]
  10. Caggana M., Chan P., Ramsingh A. Identification of a single amino acid residue in the capsid protein VP1 of coxsackievirus B4 that determines the virulent phenotype. J Virol. 1993 Aug;67(8):4797–4803. doi: 10.1128/jvi.67.8.4797-4803.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chapman N. M., Tu Z., Tracy S., Gauntt C. J. An infectious cDNA copy of the genome of a non-cardiovirulent coxsackievirus B3 strain: its complete sequence analysis and comparison to the genomes of cardiovirulent coxsackieviruses. Arch Virol. 1994;135(1-2):115–130. doi: 10.1007/BF01309769. [DOI] [PubMed] [Google Scholar]
  12. Chow L. H., Beisel K. W., McManus B. M. Enteroviral infection of mice with severe combined immunodeficiency. Evidence for direct viral pathogenesis of myocardial injury. Lab Invest. 1992 Jan;66(1):24–31. [PubMed] [Google Scholar]
  13. Christodoulou C., Colbere-Garapin F., Macadam A., Taffs L. F., Marsden S., Minor P., Horaud F. Mapping of mutations associated with neurovirulence in monkeys infected with Sabin 1 poliovirus revertants selected at high temperature. J Virol. 1990 Oct;64(10):4922–4929. doi: 10.1128/jvi.64.10.4922-4929.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Coller B. A., Chapman N. M., Beck M. A., Pallansch M. A., Gauntt C. J., Tracy S. M. Echovirus 22 is an atypical enterovirus. J Virol. 1990 Jun;64(6):2692–2701. doi: 10.1128/jvi.64.6.2692-2701.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dildine S. L., Semler B. L. Conservation of RNA-protein interactions among picornaviruses. J Virol. 1992 Jul;66(7):4364–4376. doi: 10.1128/jvi.66.7.4364-4376.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dildine S. L., Stark K. R., Haller A. A., Semler B. L. Poliovirus translation initiation: differential effects of directed and selected mutations in the 5' noncoding region of viral RNAs. Virology. 1991 Jun;182(2):742–752. doi: 10.1016/0042-6822(91)90615-i. [DOI] [PubMed] [Google Scholar]
  17. Duke G. M., Hoffman M. A., Palmenberg A. C. Sequence and structural elements that contribute to efficient encephalomyocarditis virus RNA translation. J Virol. 1992 Mar;66(3):1602–1609. doi: 10.1128/jvi.66.3.1602-1609.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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 Increased neurovirulence associated with a single nucleotide change in a noncoding region of the Sabin type 3 poliovaccine genome. Nature. 1985 Apr 11;314(6011):548–550. doi: 10.1038/314548a0. [DOI] [PubMed] [Google Scholar]
  19. Filman D. J., Syed R., Chow M., Macadam A. J., Minor P. D., Hogle J. M. Structural factors that control conformational transitions and serotype specificity in type 3 poliovirus. EMBO J. 1989 May;8(5):1567–1579. doi: 10.1002/j.1460-2075.1989.tb03541.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gauntt C. J., Trousdale M. D., LaBadie D. R., Paque R. E., Nealon T. Properties of coxsackievirus B3 variants which are amyocarditic or myocarditic for mice. J Med Virol. 1979;3(3):207–220. doi: 10.1002/jmv.1890030307. [DOI] [PubMed] [Google Scholar]
  21. Gebhard J. R., Ehrenfeld E. Specific interactions of HeLa cell proteins with proposed translation domains of the poliovirus 5' noncoding region. J Virol. 1992 May;66(5):3101–3109. doi: 10.1128/jvi.66.5.3101-3109.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gutell R. R., Larsen N., Woese C. R. Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. Microbiol Rev. 1994 Mar;58(1):10–26. doi: 10.1128/mr.58.1.10-26.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hellen C. U., Pestova T. V., Litterst M., Wimmer E. The cellular polypeptide p57 (pyrimidine tract-binding protein) binds to multiple sites in the poliovirus 5' nontranslated region. J Virol. 1994 Feb;68(2):941–950. doi: 10.1128/jvi.68.2.941-950.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hellen C. U., Witherell G. W., Schmid M., Shin S. H., Pestova T. V., Gil A., Wimmer E. A cytoplasmic 57-kDa protein that is required for translation of picornavirus RNA by internal ribosomal entry is identical to the nuclear pyrimidine tract-binding protein. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7642–7646. doi: 10.1073/pnas.90.16.7642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Herzum M., Ruppert V., Küytz B., Jomaa H., Nakamura I., Maisch B. Coxsackievirus B3 infection leads to cell death of cardiac myocytes. J Mol Cell Cardiol. 1994 Jul;26(7):907–913. doi: 10.1006/jmcc.1994.1108. [DOI] [PubMed] [Google Scholar]
  26. Hogle J. M., Chow M., Filman D. J. Three-dimensional structure of poliovirus at 2.9 A resolution. Science. 1985 Sep 27;229(4720):1358–1365. doi: 10.1126/science.2994218. [DOI] [PubMed] [Google Scholar]
  27. Huber S. A., Haisch C., Lodge P. A. Functional diversity in vascular endothelial cells: role in coxsackievirus tropism. J Virol. 1990 Sep;64(9):4516–4522. doi: 10.1128/jvi.64.9.4516-4522.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Huber S. A., Job L. P. Differences in cytolytic T cell response of BALB/c mice infected with myocarditic and non-myocarditic strains of coxsackievirus group B, type 3. Infect Immun. 1983 Mar;39(3):1419–1427. doi: 10.1128/iai.39.3.1419-1427.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hultman T., Ståhl S., Hornes E., Uhlén M. Direct solid phase sequencing of genomic and plasmid DNA using magnetic beads as solid support. Nucleic Acids Res. 1989 Jul 11;17(13):4937–4946. doi: 10.1093/nar/17.13.4937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Jacobson S. J., Konings D. A., Sarnow P. Biochemical and genetic evidence for a pseudoknot structure at the 3' terminus of the poliovirus RNA genome and its role in viral RNA amplification. J Virol. 1993 Jun;67(6):2961–2971. doi: 10.1128/jvi.67.6.2961-2971.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kandolf R., Canu A., Hofschneider P. H. Coxsackie B3 virus can replicate in cultured human foetal heart cells and is inhibited by interferon. J Mol Cell Cardiol. 1985 Feb;17(2):167–181. doi: 10.1016/s0022-2828(85)80019-5. [DOI] [PubMed] [Google Scholar]
  32. Kandolf R., Klingel K., Mertsching H., Canu A., Hohenadl C., Zell R., Reimann B. Y., Heim A., McManus B. M., Foulis A. K. Molecular studies on enteroviral heart disease: patterns of acute and persistent infections. Eur Heart J. 1991 Aug;12 (Suppl 500):49–55. doi: 10.1093/eurheartj/12.suppl_d.49. [DOI] [PubMed] [Google Scholar]
  33. Kaplan M. H., Klein S. W., McPhee J., Harper R. G. Group B coxsackievirus infections in infants younger than three months of age: a serious childhood illness. Rev Infect Dis. 1983 Nov-Dec;5(6):1019–1032. doi: 10.1093/clinids/5.6.1019. [DOI] [PubMed] [Google Scholar]
  34. Keeling P. J., Lukaszyk A., Poloniecki J., Caforio A. L., Davies M. J., Booth J. C., McKenna W. J. A prospective case-control study of antibodies to coxsackie B virus in idiopathic dilated cardiomyopathy. J Am Coll Cardiol. 1994 Mar 1;23(3):593–598. doi: 10.1016/0735-1097(94)90742-0. [DOI] [PubMed] [Google Scholar]
  35. Klingel K., Hohenadl C., Canu A., Albrecht M., Seemann M., Mall G., Kandolf R. Ongoing enterovirus-induced myocarditis is associated with persistent heart muscle infection: quantitative analysis of virus replication, tissue damage, and inflammation. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):314–318. doi: 10.1073/pnas.89.1.314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Klingel K., Kandolf R. The role of enterovirus replication in the development of acute and chronic heart muscle disease in different immunocompetent mouse strains. Scand J Infect Dis Suppl. 1993;88:79–85. [PubMed] [Google Scholar]
  37. Klump W. M., Bergmann I., Müller B. C., Ameis D., Kandolf R. Complete nucleotide sequence of infectious Coxsackievirus B3 cDNA: two initial 5' uridine residues are regained during plus-strand RNA synthesis. J Virol. 1990 Apr;64(4):1573–1583. doi: 10.1128/jvi.64.4.1573-1583.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Kono R. Enteroviruses other than poliovirus. Bull Pan Am Health Organ. 1976;10(4):337–340. [PubMed] [Google Scholar]
  39. La Monica N., Racaniello V. R. Differences in replication of attenuated and neurovirulent polioviruses in human neuroblastoma cell line SH-SY5Y. J Virol. 1989 May;63(5):2357–2360. doi: 10.1128/jvi.63.5.2357-2360.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Le S. Y., Chen J. H., Sonenberg N., Maizel J. V. Conserved tertiary structure elements in the 5' untranslated region of human enteroviruses and rhinoviruses. Virology. 1992 Dec;191(2):858–866. doi: 10.1016/0042-6822(92)90261-M. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Le S. Y., Zuker M. Common structures of the 5' non-coding RNA in enteroviruses and rhinoviruses. Thermodynamical stability and statistical significance. J Mol Biol. 1990 Dec 5;216(3):729–741. doi: 10.1016/0022-2836(90)90395-3. [DOI] [PubMed] [Google Scholar]
  42. Leslie K., Blay R., Haisch C., Lodge A., Weller A., Huber S. Clinical and experimental aspects of viral myocarditis. Clin Microbiol Rev. 1989 Apr;2(2):191–203. doi: 10.1128/cmr.2.2.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Lindberg A. M., Crowell R. L., Zell R., Kandolf R., Pettersson U. Mapping of the RD phenotype of the Nancy strain of coxsackievirus B3. Virus Res. 1992 Jul;24(2):187–196. doi: 10.1016/0168-1702(92)90006-u. [DOI] [PubMed] [Google Scholar]
  44. Lindberg A. M., Stålhandske P. O., Pettersson U. Genome of coxsackievirus B3. Virology. 1987 Jan;156(1):50–63. doi: 10.1016/0042-6822(87)90435-1. [DOI] [PubMed] [Google Scholar]
  45. Ling L. L., Keohavong P., Dias C., Thilly W. G. Optimization of the polymerase chain reaction with regard to fidelity: modified T7, Taq, and vent DNA polymerases. PCR Methods Appl. 1991 Aug;1(1):63–69. doi: 10.1101/gr.1.1.63. [DOI] [PubMed] [Google Scholar]
  46. Lodge P. A., Herzum M., Olszewski J., Huber S. A. Coxsackievirus B-3 myocarditis. Acute and chronic forms of the disease caused by different immunopathogenic mechanisms. Am J Pathol. 1987 Sep;128(3):455–463. [PMC free article] [PubMed] [Google Scholar]
  47. Macadam A. J., Ferguson G., Burlison J., Stone D., Skuce R., Almond J. W., Minor P. D. Correlation of RNA secondary structure and attenuation of Sabin vaccine strains of poliovirus in tissue culture. Virology. 1992 Aug;189(2):415–422. doi: 10.1016/0042-6822(92)90565-7. [DOI] [PubMed] [Google Scholar]
  48. Manolio T. A., Baughman K. L., Rodeheffer R., Pearson T. A., Bristow J. D., Michels V. V., Abelmann W. H., Harlan W. R. Prevalence and etiology of idiopathic dilated cardiomyopathy (summary of a National Heart, Lung, and Blood Institute workshop. Am J Cardiol. 1992 Jun 1;69(17):1458–1466. doi: 10.1016/0002-9149(92)90901-a. [DOI] [PubMed] [Google Scholar]
  49. Martin A. B., Webber S., Fricker F. J., Jaffe R., Demmler G., Kearney D., Zhang Y. H., Bodurtha J., Gelb B., Ni J. Acute myocarditis. Rapid diagnosis by PCR in children. Circulation. 1994 Jul;90(1):330–339. doi: 10.1161/01.cir.90.1.330. [DOI] [PubMed] [Google Scholar]
  50. Martino T. A., Liu P., Sole M. J. Viral infection and the pathogenesis of dilated cardiomyopathy. Circ Res. 1994 Feb;74(2):182–188. doi: 10.1161/01.res.74.2.182. [DOI] [PubMed] [Google Scholar]
  51. Meerovitch K., Nicholson R., Sonenberg N. In vitro mutational analysis of cis-acting RNA translational elements within the poliovirus type 2 5' untranslated region. J Virol. 1991 Nov;65(11):5895–5901. doi: 10.1128/jvi.65.11.5895-5901.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Meerovitch K., Pelletier J., Sonenberg N. A cellular protein that binds to the 5'-noncoding region of poliovirus RNA: implications for internal translation initiation. Genes Dev. 1989 Jul;3(7):1026–1034. doi: 10.1101/gad.3.7.1026. [DOI] [PubMed] [Google Scholar]
  53. Nicholson R., Pelletier J., Le S. Y., Sonenberg N. Structural and functional analysis of the ribosome landing pad of poliovirus type 2: in vivo translation studies. J Virol. 1991 Nov;65(11):5886–5894. doi: 10.1128/jvi.65.11.5886-5894.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Omata T., Kohara M., Kuge S., Komatsu T., Abe S., Semler B. L., Kameda A., Itoh H., Arita M., Wimmer E. Genetic analysis of the attenuation phenotype of poliovirus type 1. J Virol. 1986 May;58(2):348–358. doi: 10.1128/jvi.58.2.348-358.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Pestova T. V., Hellen C. U., Wimmer E. Translation of poliovirus RNA: role of an essential cis-acting oligopyrimidine element within the 5' nontranslated region and involvement of a cellular 57-kilodalton protein. J Virol. 1991 Nov;65(11):6194–6204. doi: 10.1128/jvi.65.11.6194-6204.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Rabausch-Starz I., Schwaiger A., Grünewald K., Müller-Hermelink H. K., Neu N. Persistence of virus and viral genome in myocardium after coxsackievirus B3-induced murine myocarditis. Clin Exp Immunol. 1994 Apr;96(1):69–74. doi: 10.1111/j.1365-2249.1994.tb06232.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Ren R. B., Moss E. G., Racaniello V. R. Identification of two determinants that attenuate vaccine-related type 2 poliovirus. J Virol. 1991 Mar;65(3):1377–1382. doi: 10.1128/jvi.65.3.1377-1382.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Rose J. K., Trachsel H., Leong K., Baltimore D. Inhibition of translation by poliovirus: inactivation of a specific initiation factor. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2732–2736. doi: 10.1073/pnas.75.6.2732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Rossmann M. G., Arnold E., Erickson J. W., Frankenberger E. A., Griffith J. P., Hecht H. J., Johnson J. E., Kamer G., Luo M., Mosser A. G. Structure of a human common cold virus and functional relationship to other picornaviruses. Nature. 1985 Sep 12;317(6033):145–153. doi: 10.1038/317145a0. [DOI] [PubMed] [Google Scholar]
  60. Rossmann M. G. The canyon hypothesis. Viral Immunol. 1989 Fall;2(3):143–161. doi: 10.1089/vim.1989.2.143. [DOI] [PubMed] [Google Scholar]
  61. Semler B. L., Johnson V. H., Tracy S. A chimeric plasmid from cDNA clones of poliovirus and coxsackievirus produces a recombinant virus that is temperature-sensitive. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1777–1781. doi: 10.1073/pnas.83.6.1777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Shepard D. A., Heinz B. A., Rueckert R. R. WIN 52035-2 inhibits both attachment and eclipse of human rhinovirus 14. J Virol. 1993 Apr;67(4):2245–2254. doi: 10.1128/jvi.67.4.2245-2254.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Skinner M. A., Racaniello V. R., Dunn G., Cooper J., Minor P. D., Almond J. W. 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. 1989 May 20;207(2):379–392. doi: 10.1016/0022-2836(89)90261-1. [DOI] [PubMed] [Google Scholar]
  64. Sole M. J., Liu P. Viral myocarditis: a paradigm for understanding the pathogenesis and treatment of dilated cardiomyopathy. J Am Coll Cardiol. 1993 Oct;22(4 Suppl A):99A–105A. doi: 10.1016/0735-1097(93)90470-l. [DOI] [PubMed] [Google Scholar]
  65. Sonenberg N. Poliovirus translation. Curr Top Microbiol Immunol. 1990;161:23–47. doi: 10.1007/978-3-642-75602-3_2. [DOI] [PubMed] [Google Scholar]
  66. Stanway G. Structure, function and evolution of picornaviruses. J Gen Virol. 1990 Nov;71(Pt 11):2483–2501. doi: 10.1099/0022-1317-71-11-2483. [DOI] [PubMed] [Google Scholar]
  67. Svitkin Y. V., Cammack N., Minor P. D., Almond J. W. Translation deficiency of the Sabin type 3 poliovirus genome: association with an attenuating mutation C472----U. Virology. 1990 Mar;175(1):103–109. doi: 10.1016/0042-6822(90)90190-3. [DOI] [PubMed] [Google Scholar]
  68. Svitkin Y. V., Meerovitch K., Lee H. S., Dholakia J. N., Kenan D. J., Agol V. I., Sonenberg N. Internal translation initiation on poliovirus RNA: further characterization of La function in poliovirus translation in vitro. J Virol. 1994 Mar;68(3):1544–1550. doi: 10.1128/jvi.68.3.1544-1550.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Svitkin Y. V., Pestova T. V., Maslova S. V., Agol V. I. Point mutations modify the response of poliovirus RNA to a translation initiation factor: a comparison of neurovirulent and attenuated strains. Virology. 1988 Oct;166(2):394–404. doi: 10.1016/0042-6822(88)90510-7. [DOI] [PubMed] [Google Scholar]
  70. Tabor S., Richardson C. C. DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4767–4771. doi: 10.1073/pnas.84.14.4767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Tracy S., Chapman N. M., Liu H. L. Molecular cloning and partial characterization of the coxsackievirus B3 genome. Brief report. Arch Virol. 1985;85(1-2):157–163. doi: 10.1007/BF01317016. [DOI] [PubMed] [Google Scholar]
  72. Tracy S., Chapman N. M., McManus B. M., Pallansch M. A., Beck M. A., Carstens J. A molecular and serologic evaluation of enteroviral involvement in human myocarditis. J Mol Cell Cardiol. 1990 Apr;22(4):403–414. doi: 10.1016/0022-2828(90)91476-n. [DOI] [PubMed] [Google Scholar]
  73. Tracy S., Chapman N. M., Tu Z. Coxsackievirus B3 from an infectious cDNA copy of the genome is cardiovirulent in mice. Arch Virol. 1992;122(3-4):399–409. doi: 10.1007/BF01317202. [DOI] [PubMed] [Google Scholar]
  74. Tracy S., Hufnagel G., Chapman N. Interesting problems in enteroviral inflammatory heart disease. Herz. 1992 Apr;17(2):79–84. [PubMed] [Google Scholar]
  75. Tracy S., Liu H. L., Chapman N. M. Coxsackievirus B3: primary structure of the 5' non-coding and capsid protein-coding regions of the genome. Virus Res. 1985 Oct;3(3):263–270. doi: 10.1016/0168-1702(85)90050-4. [DOI] [PubMed] [Google Scholar]
  76. Tracy S., Wiegand V., McManus B., Gauntt C., Pallansch M., Beck M., Chapman N. Molecular approaches to enteroviral diagnosis in idiopathic cardiomyopathy and myocarditis. J Am Coll Cardiol. 1990 Jun;15(7):1688–1694. doi: 10.1016/0735-1097(90)92846-t. [DOI] [PubMed] [Google Scholar]
  77. Trousdale M. D., Paque R. E., Gauntt C. J. Isolation of Coxsackievirus B3 temperture-sensitive mutants and their assignment to complementation groups. Biochem Biophys Res Commun. 1976 May 23;76(2):368–375. doi: 10.1016/0006-291x(77)90734-3. [DOI] [PubMed] [Google Scholar]
  78. Turner D. H., Sugimoto N., Freier S. M. RNA structure prediction. Annu Rev Biophys Biophys Chem. 1988;17:167–192. doi: 10.1146/annurev.bb.17.060188.001123. [DOI] [PubMed] [Google Scholar]
  79. Westrop G. D., Wareham K. A., Evans D. M., Dunn G., Minor P. D., Magrath D. I., Taffs F., Marsden S., Skinner M. A., Schild G. C. Genetic basis of attenuation of the Sabin type 3 oral poliovirus vaccine. J Virol. 1989 Mar;63(3):1338–1344. doi: 10.1128/jvi.63.3.1338-1344.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Why H. J., Meany B. T., Richardson P. J., Olsen E. G., Bowles N. E., Cunningham L., Freeke C. A., Archard L. C. Clinical and prognostic significance of detection of enteroviral RNA in the myocardium of patients with myocarditis or dilated cardiomyopathy. Circulation. 1994 Jun;89(6):2582–2589. doi: 10.1161/01.cir.89.6.2582. [DOI] [PubMed] [Google Scholar]
  81. Wimmer E., Hellen C. U., Cao X. Genetics of poliovirus. Annu Rev Genet. 1993;27:353–436. doi: 10.1146/annurev.ge.27.120193.002033. [DOI] [PubMed] [Google Scholar]
  82. Wong C. Y., Woodruff J. J., Woodruff J. F. Generation of cytotoxic T lymphocytes during coxsackievirus tb-3 infection. II. Characterization of effector cells and demonstration cytotoxicity against viral-infected myofibers1. J Immunol. 1977 Apr;118(4):1165–1169. [PubMed] [Google Scholar]
  83. Woodley S. L., McMillan M., Shelby J., Lynch D. H., Roberts L. K., Ensley R. D., Barry W. H. Myocyte injury and contraction abnormalities produced by cytotoxic T lymphocytes. Circulation. 1991 Apr;83(4):1410–1418. doi: 10.1161/01.cir.83.4.1410. [DOI] [PubMed] [Google Scholar]
  84. Woodruff J. F., Kilbourne E. D. The influence of quantitated post-weaning undernutrition on coxsackievirus B3 infection of adult mice. I. Viral persistence and increased severity of lesions. J Infect Dis. 1970 Feb;121(2):137–163. doi: 10.1093/infdis/121.2.137. [DOI] [PubMed] [Google Scholar]
  85. Woodruff J. F. Viral myocarditis. A review. Am J Pathol. 1980 Nov;101(2):425–484. [PMC free article] [PubMed] [Google Scholar]
  86. Zhang H. Y., Yousef G. E., Cunningham L., Blake N. W., OuYang X., Bayston T. A., Kandolf R., Archard L. C. Attenuation of a reactivated cardiovirulent coxsackievirus B3: The 5'-nontranslated region does not contain major attenuation determinants. J Med Virol. 1993 Oct;41(2):129–137. doi: 10.1002/jmv.1890410208. [DOI] [PubMed] [Google Scholar]
  87. Zuker M. On finding all suboptimal foldings of an RNA molecule. Science. 1989 Apr 7;244(4900):48–52. doi: 10.1126/science.2468181. [DOI] [PubMed] [Google Scholar]
  88. del Angel R. M., Papavassiliou A. G., Fernández-Tomás C., Silverstein S. J., Racaniello V. R. Cell proteins bind to multiple sites within the 5' untranslated region of poliovirus RNA. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8299–8303. doi: 10.1073/pnas.86.21.8299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. van der Werf S., Bradley J., Wimmer E., Studier F. W., Dunn J. J. Synthesis of infectious poliovirus RNA by purified T7 RNA polymerase. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2330–2334. doi: 10.1073/pnas.83.8.2330. [DOI] [PMC free article] [PubMed] [Google Scholar]

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