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. 1996;6(1):64–86. doi: 10.1007/BF02174046

Viral cysteine proteinases

Alexander E Gorbalenya 1,2,, Eric J Snijder 3
PMCID: PMC7104566  PMID: 32288276

Summary

Dozens of novel cysteine proteinases have been identified in positive single-stranded RNA viruses and, for the first time, in large double-stranded DNA viruses. The majority of these proteins are distantly related to papain or chymotrypsin and may be direct descendants of primordial proteolytic enzymes. Virus genome synthesis and expression, virion formation, virion entry into the host cell, as well as cellular architecture and functioning can be under the control of viral cysteine proteinases during infection. RNA virus proteinases mediate their liberation from giant multidomain precursors in which they tend to occupy conserved positions. These proteinases possess a narrow substrate specificity, can cleave in cis and in trans, and may also have additional, nonproteolytic functions. The mechanisms of catalysis, substrate recognition and RNA binding were highlighted by the recent analysis of the three-dimensional structure of the chymotrypsin-like cysteine proteinases of two RNA viruses.

Keywords: Cysteine Proteinase, Chymotrypsin, Papain, Virion Entry, Substrate Recognition

References

  • 1.Summers D.F., Maizel J.V.J. Proc. Natl. Acad. Sci. USA. 1968;59:966–966. doi: 10.1073/pnas.59.3.966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2 a.Jacobson M.F., Baltimore D. Proc. Natl. Acad. Sci. USA. 1968;61:77–77. doi: 10.1073/pnas.61.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2 b.Holland J.J., Kiehn E.D. Proc. Natl. Acad. Sci. USA. 1968;60:1015–1015. doi: 10.1073/pnas.60.3.1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Krausslich H.G., Wimmer E. Annu. Rev. Biochem. 1988;57:701–701. doi: 10.1146/annurev.bi.57.070188.003413. [DOI] [PubMed] [Google Scholar]
  • 4.Skern T., Liebig H.-D. Methods Enzymol. 1994;244:583–583. doi: 10.1016/0076-6879(94)44042-5. [DOI] [PubMed] [Google Scholar]
  • 5.Matthews D.A., Smith W.W., Ferre R.A., Condon B., Budahazi G., Sisson W., Villafranca J.E., Janson C.A., McElroy H.E., Gribskov C.L., Worland S. Cell. 1994;77:761–761. doi: 10.1016/0092-8674(94)90059-0. [DOI] [PubMed] [Google Scholar]
  • 6.Palmenberg A.C. Annu. Rev. Microbiol. 1990;44:603–603. doi: 10.1146/annurev.mi.44.100190.003131. [DOI] [PubMed] [Google Scholar]
  • 7.Grubman M.J., Zellner M., Bablanian G., Mason P.W., Piccone M.E. Virology. 1995;213:581–581. doi: 10.1006/viro.1995.0030. [DOI] [PubMed] [Google Scholar]
  • 8.Piccone M.E., Zellner M., Kumosinski T.F., Mason P.W., Grubman M.J. J. Virol. 1995;69:4950–4950. doi: 10.1128/jvi.69.8.4950-4956.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Roberts P.J., Belsham G.J. Virology. 1995;213:140–140. doi: 10.1006/viro.1995.1554. [DOI] [PubMed] [Google Scholar]
  • 10.Gauss-Muller V., Jurgensen D., Deutzmann R. Virology. 1991;182:861–861. doi: 10.1016/0042-6822(91)90630-t. [DOI] [PubMed] [Google Scholar]
  • 11.Jia X.-Y., Ehrenfeld E., Summers D.F. J. Virol. 1991;65:2595–2595. doi: 10.1128/jvi.65.5.2595-2600.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Petithory J.R., Masiarz F.R., Kirsch J.F., Santi D.V., Malcolm B.A. Proc. Natl. Acad. Sci. USA. 1991;88:11510–11510. doi: 10.1073/pnas.88.24.11510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13 a.Allaire M., Chernaia M.M., Malcolm B.A., James M.N.G. Nature. 1994;369:72–72. doi: 10.1038/369072a0. [DOI] [PubMed] [Google Scholar]
  • 13 b.Bergmann, E., Chernaia, M., Hwang, K.Y., Mosimann, S., Plotch, S., Gluzman, Y., Li, J., Malcolm, B. and James, M., Abstracts of the IXth Meeting of the European Study Group on the Molecular Biology of Picornaviruses, D5, Gmunden, Austria, 1996.
  • 14.Dessens J.T., Lomonossoff G.P. Virology. 1991;184:738–738. doi: 10.1016/0042-6822(91)90444-g. [DOI] [PubMed] [Google Scholar]
  • 15.Margis R., Viry M., Pinck M., Pinck L. Virology. 1991;185:779–779. doi: 10.1016/0042-6822(91)90549-q. [DOI] [PubMed] [Google Scholar]
  • 16.Boniotti B., Wirblich C., Sibilia M., Meyers G., Thiel H.-J., Rossi C. J. Virol. 1994;68:6487–6487. doi: 10.1128/jvi.68.10.6487-6495.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Dougherty W.G., Semler B.L. Microbiol. Rev. 1993;57:781–781. doi: 10.1128/mr.57.4.781-822.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Lu Y., Lu X., Denison M.R. J. Virol. 1995;69:3554–3554. doi: 10.1128/jvi.69.6.3554-3559.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Baker S.C., Yokomori K., Dong S., Carlisle R., Gorbalenya A.E., Koonin E.V., Lai M.M.C. J. Virol. 1993;67:6056–6056. doi: 10.1128/jvi.67.10.6056-6063.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Den Boon J.A., Faaberg K.S., Meulenberg J.J.M., Wassenaar A.L.M., Plagemann P.G.W., Gorbalenya A.E., Snijder E.J. J. Virol. 1995;69:4500–4500. doi: 10.1128/jvi.69.7.4500-4505.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Snijder E.J., Wassenaar A.L.M., Spaan W.J.M., Gorbalenya A.E. J. Biol. Chem. 1995;270:16671–16671. doi: 10.1074/jbc.270.28.16671. [DOI] [PubMed] [Google Scholar]
  • 22.Wiskerchen M., Belzer S.K., Collet M.S. J. Virol. 1991;65:4508–4508. doi: 10.1128/jvi.65.8.4508-4514.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Stark R., Meyers G., Rumenapf T., Thiel H.-J. J. Virol. 1993;67:7088–7088. doi: 10.1128/jvi.67.12.7088-7095.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Grakoui A., McCourt D.W., Wychowski C., Feinstone S.M., Rice C.M. Proc. Natl. Acad. Sci. USA. 1993;90:10583–10583. doi: 10.1073/pnas.90.22.10583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Hijikata M., Mizushima H., Akagi T., Mori S., Kakiuchi N., Kato N., Tanaka T., Kimura K., Shimotohno K. J. Virol. 1993;67:4665–4665. doi: 10.1128/jvi.67.8.4665-4675.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Strauss E.G., De Groot R.J., Levinson R., Strauss J.H. Virology. 1992;191:932–932. doi: 10.1016/0042-6822(92)90268-T. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27 a.Marr L.D., Wang C.-Y., Frey T.K. Virology. 1994;198:586–586. doi: 10.1006/viro.1994.1070. [DOI] [PubMed] [Google Scholar]
  • 27 b.Chen J.-P., Strauss J.H., Strauss E.G., Frey T.K. J. Virol. 1996;70:4707–4707. doi: 10.1128/jvi.70.7.4707-4713.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Bransom K.L., Dreher T.W. Virology. 1994;198:148–148. doi: 10.1006/viro.1994.1017. [DOI] [PubMed] [Google Scholar]
  • 29.Rozanov M.N., Drugeon G., Haenni A.-L. Arch. Virol. 1995;140:273–273. doi: 10.1007/BF01309862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Lawrence D.M., Rozanov M.N., Hillman B.I. Virology. 1995;207:127–127. doi: 10.1006/viro.1995.1058. [DOI] [PubMed] [Google Scholar]
  • 31.Agranovsky A.A., Koonin E.V., Boyko V.P., Maiss E., Frotschl R., Lunina N.A., Atabekov J.G. Virology. 1994;198:311–311. doi: 10.1006/viro.1994.1034. [DOI] [PubMed] [Google Scholar]
  • 32.Choi G.H., Pawlyk D.M., Nuss D.L. Virology. 1991;183:747–747. doi: 10.1016/0042-6822(91)91004-z. [DOI] [PubMed] [Google Scholar]
  • 33.Shapira R., Nuss D.L. J. Biol. Chem. 1991;266:19419–19419. [PubMed] [Google Scholar]
  • 34.Murphy F.A., Fauquet C.M., Bishop D.H.L., Ghabrial S.A., Jarvis A.W., Martelli G.P., Mayo M.A., Summers M.D., editors. Virus Taxonomy. Vienna, Austria: Springer; 1995. [Google Scholar]
  • 35.Pelham H.R. Eur. J. Biochem. 1978;85:457–457. doi: 10.1111/j.1432-1033.1978.tb12260.x. [DOI] [PubMed] [Google Scholar]
  • 36.Gorbalenya A.E., Svitkin Yu.V., Kazachkov Yu.A., Agol V.I. FEBS Lett. 1979;108:1–1. doi: 10.1016/0014-5793(79)81164-3. [DOI] [PubMed] [Google Scholar]
  • 37.Palmenberg A.C., Pallansch M.A., Rueckert R.R. J. Virol. 1979;32:770–770. doi: 10.1128/jvi.32.3.770-778.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Svitkin Yu.V., Gorbalenya A.E., Kazachkov Yu.A., Agol V.I. FEBS Lett. 1979;108:6–6. doi: 10.1016/0014-5793(79)81165-5. [DOI] [PubMed] [Google Scholar]
  • 39.Gorbalenya A.E., Svitkin Yu.V. Biochemistry (USSR) 1983;48:385–385. [Google Scholar]
  • 40.Palmenberg A.C., Rueckert R.R. J. Virol. 1982;41:244–244. doi: 10.1128/jvi.41.1.244-249.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Argos P., Kamer G., Nicklin M.J.H., Wimmer E. Nucleic Acids Res. 1984;12:7251–7251. doi: 10.1093/nar/12.18.7251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Franssen H., Leunissen J., Goldbach R., Lomonosoff G.P., Zimmern D. EMBO J. 1984;3:855–855. doi: 10.1002/j.1460-2075.1984.tb01896.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Goldbach R. Semin. Virol. 1990;1:335–335. [Google Scholar]
  • 44.Jore J., De Geus B., Jackson R.J., Pouwels P.H., Enger-Valk B.E. J. Gen. Virol. 1988;69:1627–1627. doi: 10.1099/0022-1317-69-7-1627. [DOI] [PubMed] [Google Scholar]
  • 45.Ypma-Wong M.F., Dewalt P.G., Johnson V.H., Lamb J.G., Semler B.L. Virology. 1988;166:265–265. doi: 10.1016/0042-6822(88)90172-9. [DOI] [PubMed] [Google Scholar]
  • 46.Kitamura N., Semler B.L., Rothberg P.G., Larsen G.R., Adler C.J., Dorner A.J., Emini E.A., Hanecak R., Lee J.J., Van der Werf S., Anderson C.W., Wimmer E. Nature. 1981;291:547–547. doi: 10.1038/291547a0. [DOI] [PubMed] [Google Scholar]
  • 47.Blinov V.M., Gorbalenya A.E., Donchenko A.P. Dokl. Akad. Nauk USSR. 1984;279:502–502. [PubMed] [Google Scholar]
  • 48.Ivanoff L.A., Towatari T., Ray J., Korant B.D., Petteway S.R., Jr. Proc. Natl. Acad. Sci. USA. 1986;83:5392–5392. doi: 10.1073/pnas.83.15.5392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Bazan J.F., Fletterick R.J. Proc. Natl. Acad. Sci. USA. 1988;85:7872–7872. doi: 10.1073/pnas.85.21.7872. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Gorbalenya A.E., Donchenko A.P., Blinov V.M., Koonin E.V. FEBS Lett. 1989;243:103–103. doi: 10.1016/0014-5793(89)80109-7. [DOI] [PubMed] [Google Scholar]
  • 51.Dougherty W.G., Parks T.D., Cary S.M., Bazan J.F., Fletterick R.J. Virology. 1989;172:302–302. doi: 10.1016/0042-6822(89)90132-3. [DOI] [PubMed] [Google Scholar]
  • 52.Blinov V.M., Donchenko A.P., Gorbalenya A.E. Dokl. Akad. Nauk USSR. 1985;281:984–984. [PubMed] [Google Scholar]
  • 53.Toyoda H., Nicklin M.J.H., Murray M.G., Anderson C.W., Dunn J.J., Studier F.W., Wimmer E. Cell. 1986;45:761–761. doi: 10.1016/0092-8674(86)90790-7. [DOI] [PubMed] [Google Scholar]
  • 54.Bernstein H.D., Sonenberg N., Baltimore D. Mol. Cell. Biol. 1985;5:2913–2913. doi: 10.1128/mcb.5.11.2913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Ding M., Schlesinger M. Virology. 1989;171:280–280. doi: 10.1016/0042-6822(89)90539-4. [DOI] [PubMed] [Google Scholar]
  • 56.Hardy W.R., Strauss J.H. J. Virol. 1989;63:4653–4653. doi: 10.1128/jvi.63.11.4653-4664.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57.Oh C., Carrington J.C. Virology. 1989;173:692–692. doi: 10.1016/0042-6822(89)90582-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Carrington J.C., Cary S.M., Parks T.D., Dougherty W.G. EMBO J. 1989;8:365–365. doi: 10.1002/j.1460-2075.1989.tb03386.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Strauss J.H., editor. Seminars in Virology, Vol. 1. New York, NY, U.S.A.: W.B. Saunders; 1990. pp. 307–384. [Google Scholar]
  • 60.Malcolm B.A. Protein Sci. 1995;4:1439–1439. doi: 10.1002/pro.5560040801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 61.Weber J.M., Tihanyi K. Methods Enzymol. 1994;244:595–595. doi: 10.1016/0076-6879(94)44043-3. [DOI] [PubMed] [Google Scholar]
  • 62.Weber J.M. Curr. Top. Microbiol. Immunol. 1995;199/I:227–227. doi: 10.1007/978-3-642-79496-4_12. [DOI] [PubMed] [Google Scholar]
  • 63.Rancourt C., Tihanyi K., Bourbonniere M., Weber J.M. Proc. Natl. Acad. Sci. USA. 1994;91:844–844. doi: 10.1073/pnas.91.3.844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Grierson A.W., Nicholson R., Talbot P., Webster A., Kemp G. J. Gen. Virol. 1994;75:2761–2761. doi: 10.1099/0022-1317-75-10-2761. [DOI] [PubMed] [Google Scholar]
  • 65.Ohkawa T., Majima K., Maeda S. J. Virol. 1994;68:6619–6619. doi: 10.1128/jvi.68.10.6619-6625.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 66.Slack J.M., Kuzio J., Faulkner P. J. Gen. Virol. 1995;76:1091–1091. doi: 10.1099/0022-1317-76-5-1091. [DOI] [PubMed] [Google Scholar]
  • 67.Liu D.X., Brown T.D.K. Virology. 1995;209:420–420. doi: 10.1006/viro.1995.1274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 68.Ziebuhr J., Herold J., Siddell S.G. J. Virol. 1995;69:4331–4331. doi: 10.1128/jvi.69.7.4331-4338.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 69.Snijder E.J., Wassenaar A.L.M., Spaan W.J.M. J. Virol. 1992;66:7040–7040. doi: 10.1128/jvi.66.12.7040-7048.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 70.Koonin E.V., Choi G.H., Nuss D.L., Shapira R., Carrington J.C. Proc. Natl. Acad. Sci. USA. 1991;88:10647–10647. doi: 10.1073/pnas.88.23.10647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 71.Kashiwazaki S., Minobe Y., Omura T., Hibino H. J. Gen. Virol. 1990;71:2781–2781. doi: 10.1099/0022-1317-71-12-2781. [DOI] [PubMed] [Google Scholar]
  • 72.Shen P., Kaniewska M., Smith C., Beachy R.N. Virology. 1993;193:621–621. doi: 10.1006/viro.1993.1170. [DOI] [PubMed] [Google Scholar]
  • 73.Turnbull-Ross A.D., Mayo M.A., Reavy B., Murant A.F. J. Gen. Virol. 1993;74:555–555. doi: 10.1099/0022-1317-74-4-555. [DOI] [PubMed] [Google Scholar]
  • 74.Koonin E.V., Gorbalenya A.E., Purdy M.A., Rozanov M.N., Reyes G.R., Bradley D.W. Proc. Natl. Acad. Sci. USA. 1992;89:8259–8259. doi: 10.1073/pnas.89.17.8259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 75.Koonin E.V., Dolja V.V. Crit. Rev. Biochem. Mol. Biol. 1993;28:375–375. doi: 10.3109/10409239309078440. [DOI] [PubMed] [Google Scholar]
  • 76.Lee H.-J., Shieh C.-K., Gorbalenya A.E., Koonin E.V., La Monica N., Tuler J., Bagdzhadzhyan A., Lai M.M.C. Virology. 1991;180:567–567. doi: 10.1016/0042-6822(91)90071-I. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 77.Herold J., Raabe T., Schelle-Prinz B., Siddell S.G. Virology. 1993;195:680–680. doi: 10.1006/viro.1993.1419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 78.Karasev A.V., Boyko V.P., Gowda S., Nikolaeva O.V., Hilf M.E., Koonin E.V., Niblett C.L., Cline K., Gumpf D.J., Lee R.F., Garnsey S.M., Lewandowski D.J., Dawson W.O. Virology. 1995;208:511–511. doi: 10.1006/viro.1995.1182. [DOI] [PubMed] [Google Scholar]
  • 79.Gorbalenya A.E. In: Molecular Basis of Virus Evolution. Gibbs A.J., Calisher C.H., Garcia-Arenal F., editors. Cambridge, U.K.: Cambridge University Press; 1995. pp. 49–66. [Google Scholar]
  • 80.Gorbalenya A.E., Koonin E.V., Lai M.M.C. FEBS Lett. 1991;288:201–201. doi: 10.1016/0014-5793(91)81034-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81.Medina M., Domingo E., Brangwyn J.K., Belsham G.J. Virology. 1993;194:355–355. doi: 10.1006/viro.1993.1267. [DOI] [PubMed] [Google Scholar]
  • 82.Parks T.D., Howard E.D., Wolpert T.J., Arp D.J., Dougherty W.G. Virology. 1995;210:194–194. doi: 10.1006/viro.1995.1331. [DOI] [PubMed] [Google Scholar]
  • 83.Kim D.-H., Park Y.S., Kim S.S., Lew J., Nam H.G., Choi K.Y. Virology. 1995;213:517–517. doi: 10.1006/viro.1995.0024. [DOI] [PubMed] [Google Scholar]
  • 84.Menard R., Chatel H., Dupras R., Plouffe C., Laliberte J.-F. Eur. J. Biochem. 1995;229:107–107. doi: 10.1111/j.1432-1033.1995.tb20444.x. [DOI] [PubMed] [Google Scholar]
  • 85.Oberst M.D., Gollan T.J., Gupta M., Peura S.R., Zydlewski J.D., Sudarsanan P., Lawson T.G. Virology. 1993;193:28–28. doi: 10.1006/viro.1993.1100. [DOI] [PubMed] [Google Scholar]
  • 86 a.Lawson T.G., Gronros D.L., Werner J.A., Wey A.C., DiGeorge A.M., Lockhart J.L., Wilson J.W., Wintrode P.L. J. Biol. Chem. 1994;269:28429–28429. [PubMed] [Google Scholar]
  • 86 b.Tibbles K.W., Brierley I., Cavanagh D., Brown T.D.K. J. Gen. Virol. 1995;76:3059–3059. doi: 10.1099/0022-1317-76-12-3059. [DOI] [PubMed] [Google Scholar]
  • 87.Webster A., Kemp G. J. Gen. Virol. 1993;74:1415–1415. doi: 10.1099/0022-1317-74-7-1415. [DOI] [PubMed] [Google Scholar]
  • 88.Piccone M.E., Rieder E., Mason P.W., Grubman M.J. J. Virol. 1995;69:5376–5376. doi: 10.1128/jvi.69.9.5376-5382.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 89.Lemm J.A., Rumenapf T., Strauss E.G., Strauss J.H., Rice C.M. EMBO J. 1994;13:2925–2925. doi: 10.1002/j.1460-2075.1994.tb06587.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 90.Hambridge S.J., Sarnow P. Proc. Natl. Acad. Sci. USA. 1992;89:10272–10272. doi: 10.1073/pnas.89.21.10272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 91.Liebig H.-D., Ziegler E., Yan R., Hartmuth K., Klump H., Kowalski H., Blaas D., Sommergruber W., Frasel L., Lamphear B., Rhoads R., Kuechler E., Skern T. Biochemistry. 1993;32:7581–7581. doi: 10.1021/bi00080a033. [DOI] [PubMed] [Google Scholar]
  • 92.Macadam A.J., Ferguson G., Fleming T., Stone D.M., Almond J.W., Minor P.D. EMBO J. 1994;13:924–924. doi: 10.1002/j.1460-2075.1994.tb06336.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 93.Ziegler E., Borman A.M., Deliat F.G., Liebig H.-D., Judovic D., Kean K.M., Skern T., Kuechler E. Virology. 1995;213:549–549. doi: 10.1016/s0042-6822(95)90001-2. [DOI] [PubMed] [Google Scholar]
  • 94.Ventoso I., Carrasco L. J. Virol. 1995;69:6280–6280. doi: 10.1128/jvi.69.10.6280-6288.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 95.Molla A., Paul A.V., Schmid M., Jang S.K., Wimmer E. Virology. 1993;196:739–739. doi: 10.1006/viro.1993.1531. [DOI] [PubMed] [Google Scholar]
  • 96.Ansardi D.C., Pal-Ghosh R., Porter D., Morrow C.D. J. Virol. 1995;69:1359–1359. doi: 10.1128/jvi.69.2.1359-1366.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 97.Lu H.-H., Li X., Cuconati A., Wimmer E. J. Virol. 1995;69:7445–7445. doi: 10.1128/jvi.69.12.7445-7452.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 98.Yu S.F., Benton P., Bovee M., Sessions J., Lloyd R.E. J. Virol. 1995;69:247–247. doi: 10.1128/jvi.69.1.247-252.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 99.Andino R., Rieckhof G.E., Baltimore D. Cell. 1990;63:369–369. doi: 10.1016/0092-8674(90)90170-j. [DOI] [PubMed] [Google Scholar]
  • 100.Andino R., Rieckhof G.E., Achacoso P.L., Baltimore D. EMBO J. 1993;12:3587–3587. doi: 10.1002/j.1460-2075.1993.tb06032.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 101.Leong L.E.-C., Walker P.A., Porter A.G. J. Biol. Chem. 1993;268:25735–25735. [PubMed] [Google Scholar]
  • 102.Walker P.A., Leong L.E.-C., Porter A.G. J. Biol. Chem. 1995;270:14510–14510. doi: 10.1074/jbc.270.24.14510. [DOI] [PubMed] [Google Scholar]
  • 103.Xiang W., Harris K.S., Alexander L., Wimmer E. J. Virol. 1995;69:3658–3658. doi: 10.1128/jvi.69.6.3658-3667.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 104.Blair W.S., Nguyen J.H.C., Parsley T.B., Semler B.L. Virology. 1996;218:1–1. doi: 10.1006/viro.1996.0160. [DOI] [PubMed] [Google Scholar]
  • 105.Kasschau K.D., Carrington J.C. Virology. 1995;209:268–268. doi: 10.1006/viro.1995.1254. [DOI] [PubMed] [Google Scholar]
  • 106.Restrepo-Hartwig M.A., Carrington J.C. J. Virol. 1992;66:5662–5662. doi: 10.1128/jvi.66.9.5662-5666.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 107.Cotten M., Weber J.M. Virology. 1995;213:494–494. doi: 10.1006/viro.1995.0022. [DOI] [PubMed] [Google Scholar]
  • 108.Webster A., Leith I.R., Hay R.T. J. Virol. 1994;68:7292–7292. doi: 10.1128/jvi.68.11.7292-7300.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 109.Kirchweger R., Ziegler E., Lamphear B.J., Waters D., Liebig H.-D., Sommergruber W., Sobrino F., Hohenadl C., Blaas D., Rhoads R.E., Skern T. J. Virol. 1994;68:5677–5677. doi: 10.1128/jvi.68.9.5677-5684.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 110.Sommergruber W., Ahorn H., Klump H., Seipelt J., Zoephel A., Fessl F., Krystek E., Blaas D., Kuechler E., Liebig H.-D., Skern T. Virology. 1994;198:741–741. doi: 10.1006/viro.1994.1089. [DOI] [PubMed] [Google Scholar]
  • 111.Lamphear B.J., Kirchweger R., Skern T., Rhoads R.E. J. Biol. Chem. 1995;270:21975–21975. doi: 10.1074/jbc.270.37.21975. [DOI] [PubMed] [Google Scholar]
  • 112.Davies M.V., Pelletier J., Meerovitch K., Sonenberg N., Kaufman R.J. J. Biol. Chem. 1991;266:14714–14714. [PubMed] [Google Scholar]
  • 113.Clark M.E., Hammerle T., Wimmer E., Dasgupta A. EMBO J. 1991;10:2941–2941. doi: 10.1002/j.1460-2075.1991.tb07844.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 114.Clark M.E., Lieberman P.M., Berk A.J., Dasgupta A. Mol. Cell. Biol. 1993;13:1232–1232. doi: 10.1128/mcb.13.2.1232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 115.Das S., Dasgupta A. J. Virol. 1993;67:3326–3326. doi: 10.1128/jvi.67.6.3326-3331.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 116.Falk M.M., Grigera P.R., Bergmann I.E., Zibert A., Multhaup G., Beck E. J. Virol. 1990;64:748–748. doi: 10.1128/jvi.64.2.748-756.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 117.Tesar M., Marquardt O. Virology. 1990;174:364–364. doi: 10.1016/0042-6822(90)90090-e. [DOI] [PubMed] [Google Scholar]
  • 118.Joachims M., Harris K.S., Etchison D. Virology. 1995;211:451–451. doi: 10.1006/viro.1995.1427. [DOI] [PubMed] [Google Scholar]
  • 119.Chen P.H., Ornelles D.A., Shenk T. J. Virol. 1993;67:3507–3507. doi: 10.1128/jvi.67.6.3507-3514.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 120.Tihanyi K., Bourbonniere M., Houde A., Rancourt C., Weber J.M. J. Biol. Chem. 1993;268:1780–1780. [PubMed] [Google Scholar]
  • 121.Keyvani-Amineh H., Labrecque P., Cai F., Carstens E.B., Weber J.M. Virus Res. 1995;37:87–87. doi: 10.1016/0168-1702(95)00018-l. [DOI] [PubMed] [Google Scholar]
  • 122.Hellen C.U.T., Facke M., Krausslich H.-G., Lee C.-K., Wimmer E. J. Virol. 1991;65:4226–4226. doi: 10.1128/jvi.65.8.4226-4231.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 123 a.Hellen C.U.T., Lee C.-K., Wimmer E. J. Virol. 1992;66:3330–3330. doi: 10.1128/jvi.66.6.3330-3338.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 123 b.Kraulis P.J. J. Appl. Crystallogr. 1991;24:946–946. [Google Scholar]
  • 124.Lawson M.A., Semler B.L. Virology. 1992;191:309–309. doi: 10.1016/0042-6822(92)90193-s. [DOI] [PubMed] [Google Scholar]
  • 125.Peters S.A., Voorhorst W.G.B., Wellink J., Van Kammen A. Virology. 1992;191:90–90. doi: 10.1016/0042-6822(92)90169-p. [DOI] [PubMed] [Google Scholar]
  • 126.Orr D.C., Long A.C., Kay J., Dunn B.M., Cameron J.M. J. Gen. Virol. 1989;70:2931–2931. doi: 10.1099/0022-1317-70-11-2931. [DOI] [PubMed] [Google Scholar]
  • 127.Sommergruber W., Ahorn H., Zophel A., Maurer-Fogy I., Fessl F., Schnorrenberg G., Liebig H.-D., Blaas D., Kuehler E., Skern T. J. Biol. Chem. 1992;267:22639–22639. [PubMed] [Google Scholar]
  • 128.Jewell D.A., Swietnicki W., Dunn B.M., Malcolm B.A. Biochemistry. 1992;31:7862–7862. doi: 10.1021/bi00149a017. [DOI] [PubMed] [Google Scholar]
  • 129.Hall, D.J. and Palmenberg, A.C., Virus Genes, (1996) in press. [DOI] [PubMed]
  • 130.Malcolm B.A., Chin S.M., Jewell D.A., Stratton-Thomas J.R., Thudium K.B., Ralston R., Rosenberg S. Biochemistry. 1992;31:3358–3358. doi: 10.1021/bi00128a008. [DOI] [PubMed] [Google Scholar]
  • 131.Harmon S.A., Updike W., Jia X.Y., Summers D.F., Ehrenfeld E. J. Virol. 1992;66:5242–5242. doi: 10.1128/jvi.66.9.5242-5247.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 132.Tesar M., Pak I., Jia X.-Y., Richards O.C., Summers D.F., Ehrenfeld E. Virology. 1994;198:524–524. doi: 10.1006/viro.1994.1063. [DOI] [PubMed] [Google Scholar]
  • 133.Martin A., Escriou N., Chao S.-F., Girard M., Lemon S.M., Wychowski C. Virology. 1995;213:213–213. doi: 10.1006/viro.1995.1561. [DOI] [PubMed] [Google Scholar]
  • 134.Wirblich C., Sibilia M., Boniotti M.B., Rossi C., Thiel H.-J., Meyers G. J. Virol. 1995;69:7159–7159. doi: 10.1128/jvi.69.11.7159-7168.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 135.Shirako Y., Strauss J.H. Virology. 1990;177:54–54. doi: 10.1016/0042-6822(90)90459-5. [DOI] [PubMed] [Google Scholar]
  • 136.Choi G.H., Shapira R., Nuss D.L. Proc. Natl. Acad. Sci. USA. 1991;88:1167–1167. doi: 10.1073/pnas.88.4.1167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 137.Dong S., Baker S.C. Virology. 1994;204:541–541. doi: 10.1006/viro.1994.1567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 138.Bonilla P.J., Hughes S.A., Pinon J.D., Weiss S.R. Virology. 1995;209:489–489. doi: 10.1006/viro.1995.1281. [DOI] [PubMed] [Google Scholar]
  • 139.Hughes S.A., Bonilla P.J., Weiss S.R. J. Virol. 1995;69:809–809. doi: 10.1128/jvi.69.2.809-813.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 140.Kadare G., Rozanov M., Haenni A.-L. J. Gen. Virol. 1995;76:2853–2853. doi: 10.1099/0022-1317-76-11-2853. [DOI] [PubMed] [Google Scholar]
  • 141.Snijder E.J., Wassenaar A.L.M., Van Dinten L.C., Spaan W.J.M., Gorbalenya A.E. J. Biol. Chem. 1996;271:4864–4864. doi: 10.1074/jbc.271.9.4864. [DOI] [PubMed] [Google Scholar]
  • 142.Hans F., Sanfacon H. J. Gen. Virol. 1995;76:917–917. doi: 10.1099/0022-1317-76-4-917. [DOI] [PubMed] [Google Scholar]
  • 143.Hemmer O., Greif C., Dufourcq P., Reinbolt J., Fritsch C. Virology. 1995;206:362–362. doi: 10.1016/s0042-6822(95)80051-4. [DOI] [PubMed] [Google Scholar]
  • 144.Margis R., Viry M., Pinck M., Bardonnet N., Pinck L. Virology. 1994;200:79–79. doi: 10.1006/viro.1994.1165. [DOI] [PubMed] [Google Scholar]
  • 145.Margis R., Pinck L. Virology. 1992;190:884–884. doi: 10.1016/0042-6822(92)90931-e. [DOI] [PubMed] [Google Scholar]
  • 146.Gorbalenya A.E., Koonin E.V., Donchenko A.P., Blinov V.M. Nucleic Acids Res. 1989;17:4847–4847. doi: 10.1093/nar/17.12.4847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 147 a.Reed K.E., Grakoui A., Rice C.M. J. Virol. 1995;69:4127–4127. doi: 10.1128/jvi.69.7.4127-4136.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 147 b.Bonilla, P.J., Hughes, S.A. and Weiss, S.R., J. Virol., (1996) in press.
  • 148.Nicklin M.J.H., Toyoda H., Murray M.G., Wimmer E. Biotechnology. 1986;4:36–36. [Google Scholar]
  • 149.Dougherty W.G., Parks T.D. Virology. 1991;183:449–449. doi: 10.1016/0042-6822(91)90974-g. [DOI] [PubMed] [Google Scholar]
  • 150.Cordingley M.G., Callahan P.L., Sardana V.V., Garsky V.M., Colonno R.J. J. Biol. Chem. 1990;265:9062–9062. [PubMed] [Google Scholar]
  • 151.Mirzayan C., Ingraham R., Wimmer E. J. Gen. Virol. 1991;72:1159–1159. doi: 10.1099/0022-1317-72-5-1159. [DOI] [PubMed] [Google Scholar]
  • 152.Charini W.A., Todd S., Gutman G.A., Semler B.L. J. Virol. 1994;68:6547–6547. doi: 10.1128/jvi.68.10.6547-6552.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 153.Cao X., Wimmer E. EMBO J. 1996;15:23–23. [PMC free article] [PubMed] [Google Scholar]
  • 154.Harris K.S., Reddigari S.R., Nicklin M.J.H., Hammerle T., Wimmer E. J. Virol. 1992;66:7481–7481. doi: 10.1128/jvi.66.12.7481-7489.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 155.Blair W.S., Li X., Semler B.L. J. Virol. 1993;67:2336–2336. doi: 10.1128/jvi.67.4.2336-2343.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 156.Molla A., Harris K.S., Paul A.V., Shin S.H., Mugavero J., Wimmer E. J. Biol. Chem. 1994;269:27015–27015. [PubMed] [Google Scholar]
  • 157.Ryan M., Belsham G.J., King A.M.Q. Virology. 1989;173:35–35. doi: 10.1016/0042-6822(89)90219-5. [DOI] [PubMed] [Google Scholar]
  • 158.Dessens J.T., Lomonossoff G.P. Virology. 1992;189:225–225. doi: 10.1016/0042-6822(92)90698-o. [DOI] [PubMed] [Google Scholar]
  • 159.Sommergruber W., Casari G., Fessl F., Seipelt J., Skern T. Virology. 1994;204:815–815. doi: 10.1006/viro.1994.1599. [DOI] [PubMed] [Google Scholar]
  • 160.Yu S.F., Lloyd R.E. Virology. 1992;186:725–725. doi: 10.1016/0042-6822(92)90039-r. [DOI] [PubMed] [Google Scholar]
  • 161.De Groot R.J., Hardy W.R., Shirako Y., Strauss J.H. EMBO J. 1990;9:2631–2631. doi: 10.1002/j.1460-2075.1990.tb07445.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 162.Mangel W.F., McGrath W.J., Toledo D.L., Anderson C.W. Nature. 1993;361:274–274. doi: 10.1038/361274a0. [DOI] [PubMed] [Google Scholar]
  • 163.Webster A., Hay R.T., Kemp G. Cell. 1993;72:97–97. doi: 10.1016/0092-8674(93)90053-s. [DOI] [PubMed] [Google Scholar]
  • 164 a.Voss T., Meyer R., Sommergruber W. Protein Sci. 1995;4:2526–2526. doi: 10.1002/pro.5560041209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 164 b.Guarne, A., Kirchweger, R., Verdaguer, N., Skern, T. and Fita, I., Abstracts of the IXth Meeting of the European Study Group on the Molecular Biology of Picornaviruses, D15, Gmunden, Austria, 1996.
  • 165.Keefe L.J., Ginell S.L., Westbrook E.M., Anderson C.W. Protein Sci. 1995;4:1658–1658. doi: 10.1002/pro.5560040826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 166.Gorbalenya A.E., Koonin E.V. Soviet Sci. Rev. D: Physicochem. Biol. 1993;11:1–1. [Google Scholar]
  • 167.Malcolm B.A., Lowe C., Shechosky S., McKay R.T., Yang C.C., Shah V.J., Simon R.J., Vederas J.C., Santi D.V. Biochemistry. 1995;34:8172–8172. doi: 10.1021/bi00025a024. [DOI] [PubMed] [Google Scholar]
  • 168.Lawson M.A., Semler B.L. Proc. Natl. Acad. Sci. USA. 1991;88:9919–9919. doi: 10.1073/pnas.88.22.9919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 169.Kean K., Howell M.T., Grunert S., Girard M., Jackson R.J. Virology. 1993;194:360–360. doi: 10.1006/viro.1993.1268. [DOI] [PubMed] [Google Scholar]
  • 170.Yu S.F., Lloyd R.E. Virology. 1991;182:615–615. doi: 10.1016/0042-6822(91)90602-8. [DOI] [PubMed] [Google Scholar]
  • 171.Kean K.M., Teterina N.L., Marc D., Girard M. Virology. 1991;181:609–609. doi: 10.1016/0042-6822(91)90894-h. [DOI] [PubMed] [Google Scholar]
  • 172.Hammerle T., Hellen C.U.T., Wimmer E. J. Biol. Chem. 1991;266:5412–5412. [PubMed] [Google Scholar]
  • 173 a.Denison, M.R. and Lu, Y.-Q., Abstracts of the IVth International Symposium on Positive Strand RNA Viruses, Utrecht, The Netherlands, 1995, P5–29.
  • 173 b.Kleina L.G., Grubman M.J. J. Virol. 1992;66:7168–7168. doi: 10.1128/jvi.66.12.7168-7175.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 174.Kim J.C., Spence R.A., Currier P.F., Lu X., Denison M.R. Virology. 1995;208:1–1. doi: 10.1006/viro.1995.1123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 175.Cheah K.-C., Leong L.E.-C., Porter A.G. J. Biol. Chem. 1990;265:7180–7180. [PubMed] [Google Scholar]
  • 176.Miyashita K., Utsumi R., Utsumi T., Komano T., Satoh N. Biosci. Biotechnol. Biochem. 1995;59:121–121. doi: 10.1271/bbb.59.121. [DOI] [PubMed] [Google Scholar]
  • 177.Hammerle T., Molla A., Wimmer E. J. Virol. 1992;66:6028–6028. doi: 10.1128/jvi.66.10.6028-6034.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 178.Gorbalenya A.E., Blinov V.M., Donchenko A.P. FEBS Lett. 1986;194:253–253. doi: 10.1016/0014-5793(86)80095-3. [DOI] [PubMed] [Google Scholar]
  • 179.Brenner S. Nature. 1988;334:528–528. doi: 10.1038/334528a0. [DOI] [PubMed] [Google Scholar]
  • 180.Hellen C.U.T., Wimmer E. Curr. Opin. Biotechnol. 1992;3:643–643. doi: 10.1016/0958-1669(92)90010-G. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 181.Carrasco L. Pharmacol. Ther. 1994;64:215–215. doi: 10.1016/0163-7258(94)90040-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 182.Molla A., Hellen C.U.T., Wimmer E. J. Virol. 1993;67:4688–4688. doi: 10.1128/jvi.67.8.4688-4695.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 183.Skiles J.W., McNeil D. Tetrahedron Lett. 1990;31:7277–7277. [Google Scholar]
  • 184.Singh S.B., Cordingley M.G., Ball R.G., Smith J.L., Dombrowski A.W., Goetz M.A. Tetrahedron Lett. 1991;32:5279–5279. [Google Scholar]
  • 185.McCall J.O., Kadam S., Katz L. Biotechnology. 1994;12:1012–1012. doi: 10.1038/nbt1094-1012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 186.Sham H.L., Rosenbrook W., Kati W., Betebenner D.A., Wideburg N.E., Saldivar A., Plattner J.J., Norbeck D.W. J. Chem. Soc., Perkin Trans. 1995;1:1081–1081. [Google Scholar]
  • 187.Cornish J.A., Murray H., Kemp G.D., Gani D. Bioorg. Med. Chem. Lett. 1995;5:25–25. [Google Scholar]
  • 188.Ding J., McGrath W.J., Sweet R.M., Mangel W.F. EMBO J. 1996;15:1778–1778. [PMC free article] [PubMed] [Google Scholar]

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