Proteolytic processing of the porcine reproductive and respiratory syndrome virus replicase

Virus Research

Volumn 202, Issue , 2015, Pages 48-59

  Li, Yanhua ^a,b   Tas, Ali ^c   Sun, Zhi ^a   Snijder, Eric J ^c   Fang, Ying ^a,b  

^a SOUTH DAKOTA STATE UNIVERSITY   (United States)

^b KANSAS STATE UNIVERSITY   (United States)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Arterivirus; Cleavage site; Nidovirus; Nonstructural protein; Protease; Replication

Indexed keywords

NONSTRUCTURAL PROTEIN 1; NONSTRUCTURAL PROTEIN 1ALPHA; NONSTRUCTURAL PROTEIN 1BETA; NONSTRUCTURAL PROTEIN 2; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 5; NONSTRUCTURAL PROTEIN 6; NONSTRUCTURAL PROTEIN 7; NONSTRUCTURAL PROTEIN 7ALPHA; NONSTRUCTURAL PROTEIN 7BETA; NONSTRUCTURAL PROTEIN 8; PROTEIN PRECURSOR; PROTEINASE; RNA POLYMERASE; UNCLASSIFIED DRUG; RNA DIRECTED RNA POLYMERASE; VIRAL PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; BIOLOGICAL FUNCTIONS; CONTROLLED STUDY; EQUINE ARTERITIS VIRUS; GENOTYPE; IMMUNOPRECIPITATION; NONHUMAN; OPEN READING FRAME; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEOMICS; SITE DIRECTED MUTAGENESIS; TRANSIENT EXPRESSION; TRANSLATION INITIATION; VACCINIA VIRUS; VIRUS REPLICATION; ANIMAL; BIOLOGY; CELL LINE; ENZYMOLOGY; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING;

ARTERIVIRUS; EQUINE ARTERITIS VIRUS; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS;

ANIMALS; CELL LINE; COMPUTATIONAL BIOLOGY; IMMUNOPRECIPITATION; MUTAGENESIS, SITE-DIRECTED; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; PROTEOMICS; RNA REPLICASE; VIRAL PROTEINS;

EID: 84930039400     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2014.12.027     Document Type: Article

References (51)

1. Allende R., Lewis T.L., Lu Z., Rock D.L., Kutish G.F., Ali A., Doster A.R., Osorio F.A. North American and European porcine reproductive and respiratory syndrome viruses differ in non-structural protein coding regions. J. Gen. Virol. 1999, 80:307-315.
2. Barrette-Ng I.H., Ng K.K.S., Mark B.L., Van Aken D., Cherney M.M., Garen C., Kolodenko Y., Gorbalenya A.E., Snijder E.J., James M.N. Structure of arterivirus nsp4. The smallest chymotrypsin-like proteinase with an alpha/beta C-terminal extension and alternate conformations of the oxyanion hole. J. Biol. Chem. 2002, 277:39960-39966.
3. Brown E., Lawson S., Welbon C., Gnanandarajah J., Li J., Murtaugh M.P., Nelson E.A., Molina R.M., Zimmerman J.J., Rowland R.R., Fang Y. Antibody response to porcine reproductive and respiratory syndrome virus (PRRSV) nonstructural proteins and implications for diagnostic detection and differentiation of PRRSV types I and II. Clin. Vaccine Immunol. 2009, 16(5):628-635.
4. Chen Z., Lawson S., Sun Z., Zhou X., Guan X., Christopher-Hennings J., Nelson E.A., Fang Y. Identification of two auto-cleavage products of nonstructural protein 1 (nsp1) in porcine reproductive and respiratory syndrome virus infected cells: nsp1 function as interferon antagonist. Virology 2010, 398(1):87-97.
5. de Vries A.A., Chirnside E.D., Horzinek M.C., Rottier P.J. Structural proteins of equine arteritis virus. J. Virol. 1992, 66(11):6294-6303.
6. den Boon J.A., Faaberg K.S., Meulenberg J.J., Wassenaar A.L., Plagemann P.G., Gorbalenya A.E., Snijder E.J. Processing and evolution of the N-terminal region of the arterivirus replicase ORF1a protein: identification of two papainlike cysteine proteases. J. Virol. 1995, 69(7):4500-4505.
7. Fang Y., Rowland R.R., Roof M., Lunney J.K., Christopher-Hennings J., Nelson E.A. A full-length cDNA infectious clone of North American type 1 porcine reproductive and respiratory syndrome virus: expression of green fluorescent protein in the Nsp2 region. J. Virol. 2006, 80(23):11447-11455.
8. Fang Y., Snijder E.J. The PRRSV replicase: exploring the multifunctionality of an intriguing set of nonstructural proteins. Virus Res. 2010, 154(1-2):61-76.
9. Fang Y., Treffers E.E., Li Y., Tas A., Sun Z., van der Meer Y., de Ru A.H., van Veelen P.A., Atkins J.F., Snijder E.J., Firth A.E. Efficient -2 frameshifting by mammalian ribosomes to synthesize an additional arterivirus protein. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(43):E2920-E2928.
10. Frias-Staheli N., Giannakopoulos N.V., Kikkert M., Taylor S.L., Bridgen A., Paragas J., Richt J.A., Rowland R.R., Schmaljohn C.S., Lenschow D.J., Snijder E.J., Garcia-Sastre A., Virgin H.W.t. Ovarian tumor domain-containing viral proteases evade ubiquitin- and ISG15-dependent innate immune responses. Cell Host Microbe 2007, 2(6):404-416.
11. Fuerst T.R., Niles E.G., Studier F.W., Moss B. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. U. S. A. 1986, 83(21):8122-8126.
12. Han J., Rutherford M.S., Faaberg K.S. The porcine reproductive and respiratory syndrome virus nsp2 cysteine protease domain possesses both trans- and cis-cleavage activities. J. Virol. 2009, 83(18):9449-9463.
13. Holtkamp D.J., Kliebenstein J.B., Neumann E.J., Zimmerman J.J., Rotto H.F., Yoder T.K., Wang C., Yeske P.E., Mowrer C.L., Haley C.A. Assessment of the economic impact of porcine reproductive and respiratory syndrome virus on United States pork producers. J. Swine Health Prod. 2013, 21(2):72-84.
14. Johnson C.R., Yu W., Murtaugh M.P. Cross-reactive antibody responses to nsp1 and nsp2 of Porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 2007, 88(Pt 4):1184-1195.
15. Keffaber K.K. Reproductive failure of unknown etiology. Am. Assoc. Swine Pract. Newsl. 1989, 1:1-9.
16. Knoops K., Barcena M., Limpens R.W.A.L., Koster A.J., Mommaas A.M., Snijder E.J. Ultrastructural characterization of arterivirus replication structures: reshaping the endoplasmic reticulum to accommodate viral RNA synthesis. J. Virol. 2012, 86:2474-2487.
17. Lackner T., Muller A., Pankraz A., Becher P., Thiel H.J., Gorbalenya A.E., Tautz N. Temporal modulation of an autoprotease is crucial for replication and pathogenicity of an RNA virus. J. Virol. 2004, 78(19):10765-10775.
18. Lemm J.A., Rice C.M. Roles of nonstructural polyproteins and cleavage products in regulating Sindbis virus RNA replication and transcription. J. Virol. 1993, 67(4):1916-1926.
19. Lemm J.A., Rumenapf T., Strauss E.G., Strauss J.H., Rice C.M. Polypeptide requirements for assembly of functional Sindbis virus replication complexes: a model for the temporal regulation of minus- and plus-strand RNA synthesis. EMBO J. 1994, 13(12):2925-2934.
20. Li Y., Tas A., Snijder E.J., Fang Y. Identification of porcine reproductive and respiratory syndrome virus ORF1a-encoded non-structural proteins in virus-infected cells. J. Gen. Virol. 2012, 93(4):829-839.
21. Li Y., Treffers E.E., Napthine S., Tas A., Zhu L., Sun Z., Bell S., Mark B.L., van Veelen P.A., van Hemert M.J., Firth A.E., Brierley I., Snijder E.J., Fang Y. Transactivation of programmed ribosomal frameshifting by a viral protein. Proc. Natl. Acad. Sci. U. S. A. 2014, 111(21):E2172-E2181.
22. Liang Y., Gillam S. Mutational analysis of the rubella virus nonstructural polyprotein and its cleavage products in virus replication and RNA synthesis. J. Virol. 2000, 74(11):5133-5141.
23. Liang Y., Gillam S. Rubella virus RNA replication is cis-preferential and synthesis of negative- and positive-strand RNAs is regulated by the processing of nonstructural protein. Virology 2001, 282(2):307-319.
24. Lauck M., Sibley S.D., Hyeroba D., Tumukunde A., Weny G., Chapman C.A., Ting N., Switzer W.M., Kuhn J.H., Friedrich T.C., O'Connor D.H., Goldberg T.L. Exceptional simian hemorrhagic fever virus diversity in a wild African primate community. J. Virol. 2013, 87(1):688-691.
25. Makarova K.S., Aravind L., Koonin E.V. A novel superfamily of predicted cysteine proteases from eukaryotes, viruses and Chlamydia pneumoniae. Trends Biochem. Sci. 2000, 25(2):50-52.
26. Nelsen C.J., Murtaugh M.P., Faaberg K.S. Porcine reproductive and respiratory syndrome virus comparison: divergent evolution on two continents. J. Virol. 1999, 73(1):270-280.
27. Oh H.S., Pathak H.B., Goodfellow I.G., Arnold J.J., Cameron C.E. Insight into poliovirus genome replication and encapsidation obtained from studies of 3B-3C cleavage site mutants. J. Virol. 2009, 83(18):9370-9387.
28. Pedersen K.W., van der Meer Y., Roos N., Snijder E.J. Open reading frame 1a-encoded subunits of the arterivirus replicase induce endoplasmic reticulum-derived double-membrane vesicles which carry the viral replication complex. J. Virol. 1999, 73(3):2016-2026.
29. Pfister T., Jones K.W., Wimmer E. A cysteine-rich motif in poliovirus protein 2C(ATPase) is involved in RNA replication and binds zinc in vitro. J. Virol. 2000, 74(1):334-343.
30. Posthuma C.C., Pedersen K.W., Lu Z., Joosten R.G., Roos N., Zevenhoven-Dobbe J.C., Snijder E.J. Formation of the arterivirus replication/transcription complex: a key role for nonstructural protein 3 in the remodeling of intracellular membranes. J. Virol. 2008, 82(9):4480-4491.
31. Ropp S.L., Wees C.E., Fang Y., Nelson E.A., Rossow K.D., Bien M., Arndt B., Preszler S., Steen P., Christopher-Hennings J., Collins J.E., Benfield D.A., Faaberg K.S. Characterization of emerging European-like porcine reproductive and respiratory syndrome virus isolates in the United States. J. Virol. 2004, 78(7):3684-3703.
32. Shirako Y., Strauss J.H. 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. 1994, 68(3):1874-1885.
33. Snijder E.J., Kikkert M. Arteriviruses. Fields Virology 2013, 859-879. Lippincott Williams & Wilkins, Philadelphia, PA:. 6th ed. D.M. Knipe, P.M. Howley (Eds.).
34. Snijder E.J., Kikkert M., Fang Y. Arterivirus molecular biology and pathogenesis. J. Gen. Virol. 2013, 94(Pt 10):2141-2163.
35. Snijder E.J., van Tol H., Roos N., Pedersen K.W. Non-structural proteins 2 and 3 interact to modify host cell membranes during the formation of the arterivirus replication complex. J. Gen. Virol. 2001, 82(Pt 5):985-994.
36. Snijder E.J., Wassenaar A.L., van Dinten L.C., Spaan W.J., Gorbalenya A.E. The arterivirus nsp4 protease is the prototype of a novel group of chymotrypsin-like enzymes, the 3C-like serine proteases. J. Biol. Chem. 1996, 271(9):4864-4871.
37. Snijder E.J., Wassenaar A.L., Spaan W.J., Gorbalenya A.E. The arterivirus Nsp2 protease. An unusual cysteine protease with primary structure similarities to both papain-like and chymotrypsin-like proteases. J. Biol. Chem. 1995, 270(28):16671-16676.
38. Snijder E.J., Wassenaar A.L., Spaan W.J. Proteolytic processing of the replicase ORF1a protein of equine arteritis virus. J. Virol. 1994, 68(9):5755-5764.
39. Snijder E.J., Wassenaar A.L., Spaan W.J. The 5' end of the equine arteritis virus replicase gene encodes a papainlike cysteine protease. J. Virol. 1992, 66(12):7040-7048.
40. Sun Z., Chen Z., Lawson S.R., Fang Y. The cysteine protease domain of porcine reproductive and respiratory syndrome virus nonstructural protein 2 possesses deubiquitinating and interferon antagonism functions. J. Virol. 2010, 84(15):7832-7846.
41. Sun Y., Xue F., Guo Y., Ma M., Hao N., Zhang X.C., Lou Z., Li X., Rao Z. Crystal structure of porcine reproductive and respiratory syndrome virus leader protease Nsp1alpha. J. Virol. 2009, 83(21):10931-10940.
42. Tian X., Lu G., Gao F., Peng H., Feng Y., Ma G., Bartlam M., Tian K., Yan J., Hilgenfeld R., Gao G.F. Structure and cleavage specificity of the chymotrypsin-like serine protease (3CLSP/nsp4) of Porcine Reproductive and Respiratory Syndrome Virus (PRRSV). J. Mol. Biol. 2009, 392(4):977-993.
43. van Aken D., Zevenhoven-Dobbe J., Gorbalenya A.E., Snijder E.J. Proteolytic maturation of replicase polyprotein pp1a by the nsp4 main proteinase is essential for equine arteritis virus replication and includes internal cleavage of nsp7. J. Gen. Virol. 2006, 87(12):3473-3482.
44. van Dinten L.C., Wassenaar A.L., Gorbalenya A.E., Spaan W.J., Snijder E.J. Processing of the equine arteritis virus replicase ORF1b protein: identification of cleavage products containing the putative viral polymerase and helicase domains. J. Virol. 1996, 70(10):6625-6633.
45. van Kasteren P.B., Bailey-Elkin B.A., James T.W., Ninaber D.K., Beugeling C., Khajehpour M., Snijder E.J., Mark B.L., Kikkert M. Deubiquitinase function of arterivirus papain-like protease 2 suppresses the innate immune response in infected host cells. Proc. Natl. Acad. Sci. U. S. A. 2013, 110(9):E838-E847.
46. van Kasteren P.B., Beugeling C., Ninaber D.K., Frias-Staheli N., van Boheemen S., García-Sastre A., Snijder E.J., Kikkert M. Arterivirus and nairovirus ovarian tumor domain-containing Deubiquitinases target activated RIG-I to control innate immune signaling. J. Virol. 2012, 86(2):773-785.
47. Vatter H.A., Di H., Donaldson E.F., Radu G.U., Maines T.R., Brinton M.A. Functional analyses of the three simian hemorrhagic Fever virus nonstructural protein 1 papain-like proteases. J. Virol. 2014, 88(16):9129-9140.
48. Wassenaar A.L., Spaan W.J., Gorbalenya A.E., Snijder E.J. Alternative proteolytic processing of the arterivirus replicase ORF1a polyprotein: evidence that NSP2 acts as a cofactor for the NSP4 serine protease. J. Virol. 1997, 71(12):9313-9322.
49. Wensvoort G., Terpstra C., Pol J.M., ter Laak E.A., Bloemrad M., deKluyer E.P., Kragten C., van Buiten L., den Besten A., Wagenaar F., Broekhuijsen J.M., Moonen P.L.J.M., Zetstra T., de Boer E.A., Tibben H.J., de Jong M.F., van't Veld P., Groenland G.J.R., van Gennep J.A., Voets M.T.H., Verheijden J.H.M., Braamskamp J. Mystery swine disease in the Netherlands: the isolation of Lelystad virus. Vet. Quarterly 1991, 13:121-130.
50. Xu J., Mendez E., Caron P.R., Lin C., Murcko M.A., Collett M.S., Rice C.M. Bovine viral diarrhea virus NS3 serine proteinase: polyprotein cleavage sites, cofactor requirements, and molecular model of an enzyme essential for pestivirus replication. J. Virol. 1997, 71(7):5312-5322.
51. Ziebuhr J., Snijder E.J., Gorbalenya A.E. Virus-encoded proteinases and proteolytic processing in the Nidovirales. J. Gen. Virol. 2000, 81(Pt 4):853-879.