Polyprotein processing as a strategy for gene expression in RNA viruses

Seminars in Virology

Volumn 8, Issue 1, 1997, Pages 15-23

  Spall, Valerie E ^a   Shanks, M ^a   Lomonossoff, G P ^a  

^a JOHN INNES CENTRE   (United Kingdom)

Author keywords

Flaviviridae; Picorna like supergroup; Polyprotein processing; Protease; Retroviridae; Togaviridae

Indexed keywords

PROTEIN PRECURSOR; VIRUS ENZYME; VIRUS PROTEIN;

GENE EXPRESSION; NONHUMAN; PROTEIN PROCESSING; REVIEW; RNA VIRUS;

FLAVIVIRIDAE; PICORNA; RETROVIRIDAE; RNA VIRUSES; TOGAVIRIDAE;

EID: 0030810414     PISSN: 10445773     EISSN: None     Source Type: Journal    
DOI: 10.1006/smvy.1997.0102     Document Type: Article

References (80)

1. Summer, D. F., and Maizel, J. V. (1968) Evidence for large precursor proteins in poliovirus synthesis. Proc. Natl Acad. Sci. USA 59, 966-971.
2. Jacobson, M. F., and Baltimore, D. (1968) Polypeptide cleavages in the formation of poliovirus proteins. Proc. Natl. Acad. Sci. USA 61, 77-84.
3. Dougherty, W. G., and Semler, B. L. (1993) Expression of virus-encoded proteinases: Functional and structural similarities with cellular enzymes. Microbiol. Rev. 57, 781-822.
4. King, A. M. Q., Lomonossoff, G. P., and Ryan, M. D. (1991) Picornaviruses and their relatives in the plant kingdom. Semin. Virol. 2, 11-19.
5. Bazan, J. F., and Fletterick, R. J. (1988) Viral cysteine proteases are homologous to the trypsin-like family of serine proteases: Structural and functional implications. Proc. Natl. Acad. Sci. U.S.A. 85, 7872-7876.
6. Gorbalenya, A. E., Donchenko, A. P., Blinov, V. M., and Koonin, E. V. (1989) Cysteine proteinase of positive strand RNA viruses and chymotrypsin-like serine proteases: A distinct protein super-family with a common structural fold. FEBS Lett. 243, 103-114.
7. Allaire, M., Chernaia, M. M., Malcolm, B. A., and James, N. G. (1994) Picornaviral 3C cysteine proteinases have a fold similar to chymotrypsin-like serine proteinases. Nature 369, 72-76.
8. 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., and Warland, S. (1994) Structure of human rhinovirus 3C protease reveals a trypsin-like polypeptide fold, RNA-binding site and means for cleaving precursor polyprotein. Cell 77, 761-771.
9. Krausslich, H.-G., and Wimmer, E. (1988) Viral proteinases. Annu. Rev. Biochem. 57: 701-754.
10. Lawson, M. A., and Semler, B. L. (1990) Picornavirus protein processing - Enzymes, substrates, and genetic regulation. Curr. Top. Microbiol. Immunol. 161, 49-80.
11. Palmenberg, A. C. (1990) Proteolytic processing of picornaviral polyprotein. Annu. Rev. Microbiol. 44, 603-623.
12. Malcolm, B. A. (1995) The picornaviral 3C proteinases: Cysteine nucleophiles in serine proteinase folds. Protein Sci. 4, 1439-1445.
13. Schultheiβ, T., Kusov, Y. Y., and Gauss-Müller, V. (1994) Proteinase 3C of hepatitis A virus (HAV) cleaves the HAV polyprotein P2-P3 at all sites including VP1/2A and 2A/2B. Virology 198, 275-281.
14. Schultheiβ, T., Sommergruber, W., Kusov, Y. Y., and Gauss-Müller, V (1995) Cleavage specificity of purified recombinant hepatitis A virus 3C proteinase on natural substrates. J. Virol. 69, 1727-1733.
15. Schultheiβ, T., Emerson, S. U., Purcell, R. H., and Gauss-Müller, V (1995) Polyprotein processing in echovirus 22: a first assessment. Biochem. Biophys. Res. Commun. 217, 1120-1127.
16. Toyoda, H., Nicklin, M. J. H., Murray, M. G., Anderson, W., Dunn, J. J., Studier, F. W., and Wimmer, E. (1986) A second virus-encoded proteinase involved in proteolytic processing of poliovirus polyprotein. Cell 45, 761-770.
17. Sommergruber, W., Zorn, M., Blaas, D., Fessl, F., Volkmann, P., Maurer-Fogy, I., Pallai, P., Merluzzi, V., Matteo, M., Skern, T., and Keuchler, E. (1989) Polypeptide 2A of human rhinovirus type 2: Identification as a protease and characterisation by mutational analysis. Virology 169, 68-77.
18. Palmenberg, A. C., Parks, G. D., Hall, D. J., Ingraham, R. H., Seng, T. W., and Pallai, P. V (1992) Proteolytic processing of the cardioviral P2 region. Primary 2A/2B cleavage in clone-derived precursors. Virology 190, 754-762.
19. Ryan, M. D., King, A. M. Q., and Thomas, G. P. (1991) Cleavage of foot-and-mouth disease virus polyprotein is mediated by residues located within a 19 amino acid sequence. J. Gen. Virol. 72, 2727-2732.
20. Devaney, M. A., Vakharia, V N., Lloyd, R. E., Ehrenfeld, E., and Grubman, M. J. (1988) 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, 4407-4409.
21. Lloyd, R. E., Grubman, M. J., and Ehrenfeld, E. (1988) Relationship of p220 cleavage during picornavirus infection to 2A proteinase sequences. J. Virol. 62, 4216-4223.
22. Jore, J., de Geus, B., Jackson, R. J., Pouwels, P. H., and Enger-Valk, B. E. (1988) Poliovirus protein 3CD is the active protease for processing of the precursor protein P1 in vitro. J. Gen. Virol. 69, 1627-1636.
23. Ypma-Wong, M. F., Dewalt, P. G., Johnson, V. H., Lamb, J. G., and Semler, B. L. (1988) Protein 3CD is the major poliovirus proteinase responsible for cleavage of the P1 capsid precursor. Virology 166, 165-270.
24. Parks, G. D., Baker, J. C., and Palmenberg, A. C. (1989) Proteolytic cleavage of encephalomyocarditis virus capsid region substrates by precursors to the 3C enzyme. J. Virol. 63, 1054-1058.
25. Harmon, S. A., Updike, W., Jia, X., Summers, D. F., and Ehrenfeld, E. (1992) Polyprotein processing in cis and in trans by hepatitis A virus 3C protease cloned and expressed in Escherichia coli. J. Virol. 66, 5242-5247.
26. Hellen, C. U. T., and Wimmer, E. (1992) Maturation of poliovirus capsid proteins. Virology 187, 391-397.
27. Turnbull-Ross, A. D., Mayo, M. A., Reavy, B., and Murant, A. F. (1993) Sequence analysis of the parsnip yellow fleck virus polyprotein: evidence of affinities with picornaviruses. J. Gen. Virol. 74, 555-561.
28. Shen, P., Kaniewska, M., Smith, C., and Beachy, R. N. (1993) Nucleotide sequence and genomic organisation of rice tungro spherical virus. Virology 193, 621-630.
29. Thole, V., and Hull, R. (1996) Rice tungo spherical virus: nucleotide sequence of the 3′ genomic half and studies on the two small 3′ open reading frames. Virus. Genes 13, 239-246.
30. Peters, S. A., Voorhorst, W. G. B., Wery, J., Wellink, J., and van Kammen, A. (1992) A regulatory role for the 32K protein in the proteolytic processing of cowpea mosaic virus polyproteins. Virology 191, 81-89.
31. Dessens, J. T., and Lomonossoff, G. P. (1992) Sequence upstream of the 24K proteinase enhances cleavage of the cowpea mosaic virus B RNA-encoded polyprotein at the junction between the 24K and 87K proteins. Virology 189, 225-232.
32. Peters, S. A., Mesnard, J., Kooter, I., Verver, J., Wellink, J., and van Kammen, A. (1995) The cowpea mosaic virus RNA 1-encoded 112kDa protein may function as a VPg precursor in vivo. J. Gen. Virol 76, 1807-1813.
33. Dorssers, L., van der Krol, S., van der Meer, J., van Kammen, A., and Zabel, P. (1984) Purification of cowpea mosaic virus RNA replication complex: Identification of a virus-encoded 110,000-dalton polypeptide responsible for RNA chain elongation. Proc. Natl. Acad. Sci. USA 81, 1951-1955.
34. Holness, C. L., Lomonossoff, G. P., Evans, D., and Maule, A. J. (1989) Identification of the initiation codons for translation of cowpea mosaic virus middle component RNA using site-directed mutagenesis of an infectious cDNA clone. Virology 172, 311-320.
35. Vos, P., Verver, J., Jaegle, M., Wellink, J., van Kammen, A., and Goldbach, R. (1988) Two viral proteins involved in the proteolytic processing of the cowpea mosaic virus polyproteins. Nucleic Acids Res. 16, 1967-1985.
36. Riechmann, J. L., Lain, S., and Garcia, J. A. (1992) Highlights and prospects of potyvirus molecular biology. J. Gen. Virol 73, 1-16.
37. Verchot, J., Koonin, E. V., and Carrington, J. C. (1991) The 35-kDa protein from the N-terminus of the potyviral polyprotein functions as a third virus-encoded proteinase. Virology 185, 527-535.
38. Carrington, J. C., Cary, S. M., Parks, T. D., and Dougherty, W. G. (1989) A second proteinase encoded by a plant potyvirus genome. EMBO J. 8, 365-370.
39. Verchot, J., Herndon, K. L., and Carrington, J. C. (1992) Mutational analysis of the tobacco etch potyviral 35kDa proteinase: Identification of essential residues and requirements for autoproteolysis. Virology 190, 298-306.
40. Verchot, J., and Carrington, J. C. (1995) Debilitation of plant potyvirus infectivity by P1 proteinase-inactivating mutations and restoration by second-site modifications. J. Virol. 69, 1582-1590.
41. Pirone, T. P., and Thornbury, D. W. (1983) Role of virion and helper component in regulating aphid transmission of tobacco etch virus. Phytopathology 73, 872-875.
42. Cronin, S., Verchot, J., Haldeman-Cahill, R., Schaad, M. C., and Carrington, J. C. (1995) Long-distance movement factor: A transport function of potyvirus helper component proteinase. Plant Cell 7, 549-559.
43. Oh, C., and Carrington, J. C. (1989) Identification of essential residues in potyvirus proteinase HC-Pro by site-directed mutagenesis. Virology 173, 692-699.
44. Dougherty, W. G., Cary, S. M., and Parks, T. D. (1989) Molecular genetic analysis of a plant virus polyprotein cleavage site: A model. Virology 171, 356-364.
45. Dougherty, W. G., and Parks, T. D. (1989) Molecular genetic and biochemical evidence for the involvement of the heptapeptide cleavage sequence in determining the reaction profile at two tobacco etch virus cleavage sites in cell-free assays. Virology 172, 145-155.
46. Dougherty, W. G., Parks, T. D., Smith, H. A., and Lindbo, J. A. (1990) in Viral Genes and Plant Pathogenesis. (Pirone, T. P., and Shaw, J. G., Eds.), pp. 124-139, Springer-Verlag, Wein and New York.
47. Riechmann, J. L., Cervera, M. T., and Garcia, J. A. (1995) Processing of the plum pox virus polyprotein at the PS-OK1 junction is not required for virus viability. J. Gen. Virol. 76, 951-956.
48. Parks, T. D., and Dougherty, W. G. (1991) Substrate recognition by the NIa proteinase of two potyviruses involves multiple domains: Characterization using genetically engineered hybrid proteinase molecules. Virology 182, 17-27.
49. Parks, T. D., Howard, E. D., Wolpert, T. J., Arp, D., and Dougherty, W. G. (1995) Expression and purification of a recombinant tobacco etch virus NIa proteinase: Biochemical analyses of the full-length and a naturally occurring truncated proteinase form. Virology 210, 194-201.
50. Hijikata, M., Kato, N., Ootsuyama, Y., and Nakagawa, M. (1991) Gene mapping of the putative structural region of the hepatitis C virus genome by in vitro processing analysis. Proc. Natl. Acad. Sci. USA 88, 5547-5551.
51. Santolini, E., Migliaccio, G., and La Monica, N. (1994) Biosynthesis and biochemical properties of the hepatitis C virus core protein. J. Virol. 68, 3631-3641.
52. Grakoui, A., McCourt, D. W., Wychowski, C., Feinstone, S., and Rice, C. M. (1993) A second hepatitis C virus-encoded proteinase. Proc. Natl. Acad. Sci. USA 90, 10583-10587.
53. Hijikata, M., Mizushima, H., Akagi, T., Mori, S., Kakiuchi, N., Kato, N., Tanaka, T., Kimura, K., and Shimotohno, K. (1993) Two distinct proteinase activities are required for the processing of a putative nonstructural precursor protein of hepatitis C virus. J. Virol. 67, 4665-4675.
54. Bartenschlager, R. L., Ahlborn-Laake, L., Mous, J., and Jacobsen, H. (1993) Nonstructural protein 3 of the hepatitis C virus encodes a serine-type proteinase required for the cleavage at the NS3/4 and NS4/5 junctions. J. Virol. 67, 3835-3844.
55. Eckard, M. R., Selby, M., Masiarz, F., Lee, C., Berger, K., Crawford, K., Kuo, C., Kuo, G., Houghton, M., and Choo, Q. L. (1993) The hepatitis C virus encodes a serine proteinase involved in processing of the putative nonstructural proteins from the viral polyprotein precursor. Biochem. Biophys. Res. Commun. 192, 399-406.
56. Grakoui, A., McCourt, D. W., Wychowski, C., Feinstone, S. M., and Rice, C. M. (1993) Characterization of the hepatitis C virus encoded serine proteinase: Determination of proteinase-dependent polyprotein cleavage sites. J. Virol. 67, 2832-2843.
57. Tomei, L., Failla, C., Santolini, E., De Francesco, R., and La-Monica, N. (1993) NS3 is a serine proteinase required for processing of hepatitis C virus polyprotein. J. Virol. 67, 4017-4026.
58. Steinkühler, C., Urbani, A., Tomei, L., Biasiol, G., Sardana, M., Bianchi, E., Pessi, A., and de Francesco, R. (1996) Activity of purified hepatitis C virus protease NS3 on peptide substrates. J. Virol. 70, 6694-6700.
59. Failla, C., Tomei, L., and DeFrancesco, R. (1994) Both NS3 and NS4A are required for proteolytic processing of hepatitis C virus nonstructural proteins. J. Virol. 68, 3753-3760.
60. Failla, C., Tomei, L., and DeFrancesco, R. (1995) An amino-terminal domain of the hepatitis C virus NS3 protease is essential for interaction with NS4A. J. Virol. 69, 1769-1777.
61. Satoh, S., Tamji, Y., Hijikata, M., Kimura, K., and Shimotohno, K. (1995) The N-terminal region of hepatitis C virus nonstructural protein 3 (NS3) is essential for stable complex formation with NS4A. J. Virol 69, 4255-4260.
62. Sawicki, D. L., and Sawicki, S. G. (1994) Alphavirus positive and negative strand RNA synthesis and the role of the polyproteins in formation of viral replication complexes. Arch. Virol. Suppl. 9, 393-405.
63. Strauss, J. H., and Strauss, E. G. (1994) The alphaviruses: Gene expression, replication, and evolution. Microbiol Rev. 58, 491-562.
64. Ding, M., and Schlesinger, M. J. (1989) Evidence that Sindbis virus nsP2 is an autoprotease which processes the virus nonstructural polyprotein. Virology 171, 280-284.
65. Hardy, W. R., and Strauss, J. H. (1989) Processing the nonstructural polyproteins of Sindbis virus: The nonstructural proteinase is in the C-terminal half of nsP2 and functions both in cis and in trans. J. Virol. 63, 4653-4665.
66. Shirako, Y., and Strauss, J. H. (1994) Regulation of Sindbis virus RNA replication: Uncleaved P123 and nsP4 function in minus-strand RNA synthesis, whereas cleaved products from P123 are required for efficient plus-strand RNA synthesis. J. Virol. 68, 1874-1885.
67. de Groot, R. J., Hardy, W. R., Shirako, Y, and Strauss, J. H. (1990) Cleavage-site preferences of Sindbis virus polyproteins containing the non-structural proteinase: Evidence for temporal regulation of polyprotein processing in vivo. EMBO J. 9, 2631-2638.
68. Shirako, Y, and Strauss, J. H. (1990) Cleavage between nsP1 and nsP2 initiates the processing pathway of Sindbis virus nonstructural polyprotein P123. Virology 177, 54-64.
69. Dé, I., Sawicki, S. G., and Sawicki, D. L. (1996) Sindbis virus RNA-negative mutants that fail to convert from minus-strand to plus-strand synthesis: Role of the nsP2 protein. J. Virol. 70, 2706-2719.
70. Scupham, R. K., Jones, K. J., Sagik, B. P., and Bose, H. R., Jr. (1977) Virus-directed post-translational cleavage in Sindbis virus-infected cells. J. Virol. 22, 568-570.
71. Aliperti, G., and Schlesinger, M. J. (1978) Evidence for an autoprotease activity of Sindbis virus capsid protein. Virology 90, 366-369.
72. Choi, H.-K., Tong, L., Minor, W., Dumas, P., Boege, U., Rossmann, M. G., and Wengler, G. (1991) Structure of Sindbis virus core protein reveals a chymotrypsin-like serine proteinase and the organization of the virion. Nature 354, 37-43.
73. Oroszlan, S., and Luftig, R. B. (1990) Retroviral Proteinases. Curr. Topics Microbiol. Immunol. 157, 153-185.
74. Stephens, E., and Compans, R. W. (1988) Assembly of animal viruses at cellular membrane. Annu. Rev. Microbiol. 42, 489-516.
75. Pearl, L. H., and Taylor, W. R. (1987). A structural model for the retroviral proteases. Nature 329, 351-354.
76. Miller, M., Jaskolski, M., Rao, J. K. M., Leis, J., and Wlodawer, A. (1989) Crystal structure of a retroviral protease proves relationship to aspartic protease family. Nature 337, 576-579.
77. Navia, M. A., Fitzgerald, P. M. D., McKeever, B. M., Leu, C.-T., Heimbach, J. C., Herber, W. K., Sigal, I. S., Darke, P. L., and Springer, J. P. (1989). Three-dimensional structure of aspartyl protease from human immunodeficiency virus HIV-1. Nature 337, 615-620.
78. Ohlendorf, D. H., Foundling, S. I., Wendoloski, J. J., Sedlacek, J., Strop, P., and Salemme, F. R. (1992) Structural studies of the retroviral proteinase from avian myeloblastosis associated virus. Proteins Struct. Funct. Genet. 14, 382-391.
79. Weber, I. T., Miller, M., Jaskolski, M., Leis, J., Skalka, A. M., and Wlodawer, A. (1989) Molecular modelling of the HIV-1 protease and its substrate binding site. Science 243, 928-931.
80. Wlodawyer, A., Miller, M., Jaskolski, M., Sathyanarayana, B. K., Baldwin, E., Weber, I. T., Selk, L. M., Clawson, L., Schneider, J., and Kent, S. B. H. (1989) Conserved folding in retroviral proteases: Crystal structure of a synthetic HIV-1 protease. Science 245, 616-621.