N-linked glycosylation of GP5 of porcine reproductive and respiratory syndrome virus is critically important for virus replication in vivo

Journal of Virology

Volumn 86, Issue 18, 2012, Pages 9941-9951

  Wei, Zuzhang ^a   Lin, Tao ^a   Sun, Lichang ^a   Li, Yanhua ^a   Wang, Xiaoming ^a   Gao, Fei ^a   Liu, Runxia ^a   Chen, Chunyan ^a   Tong, Guangzhi ^a   Yuan, Shishan ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GP5 PROTEIN; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTERIVIRUS; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; VIROGENESIS; VIRUS INFECTIVITY; VIRUS MUTANT; VIRUS NEUTRALIZATION; VIRUS REPLICATION; VIRUS STRAIN; VIRUS VIABILITY; WILD TYPE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; BASE SEQUENCE; BINDING SITES; CELL LINE; DNA, VIRAL; GLYCOSYLATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SWINE; VIRAL ENVELOPE PROTEINS; VIRUS REPLICATION;

PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS;

EID: 84866154869     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.07067-11     Document Type: Article

References (49)

1. Allende R, et al. 1999. North American and European porcine reproductive and respiratory syndrome viruses differ in non-structural protein coding regions. J. Gen. Virol. 80:307-315.
2. Ansari IH, Kwon B, Osorio FA, Pattnaik AK. 2006. Influence of Nlinked glycosylation of porcine reproductive and respiratory syndrome virus GP5 on virus infectivity, antigenicity, and ability to induce neutralizing antibodies. J. Virol. 80:3994-4004.
3. Braakman I, van Anken E. 2000. Folding of viral envelope glycoproteins in the endoplasmic reticulum. Traffic 1:533-539.
4. Chackerian B, Rudensey LM, Overbaugh J. 1997. Specific N-linked and O-linked glycosylation modifications in the envelope V1 domain of simian immunodeficiency virus variants that evolve in the host alter recognition by neutralizing antibodies. J. Virol. 71:7719-7727.
5. Chen Z, Li K, Plagemann PG. 2000. Neuropathogenicity and sensitivity to antibody neutralization of lactate dehydrogenase-elevating virus are determined by polylactosaminoglycan chains on the primary envelope glycoprotein. Virology 266:88-98.
6. Cruz JL, et al. 2010. Vectored vaccines to protect against PRRSV. Virus Res. 154:150-160.
7. Curling EM, et al. 1990. Recombinant human interferon-gamma. Differences in glycosylation and proteolytic processing lead to heterogeneity in batch culture. Biochem. J. 272:333-337.
8. Das PB, et al. 2011. Glycosylation of minor envelope glycoproteins of porcine reproductive and respiratory syndrome virus in infectious virus recovery, receptor interaction, and immune response. Virology 410:385-394.
9. Dea S, Gagnon CA, Mardassi H, Pirzadeh B, Rogan D. 2000. Current knowledge on the structural proteins of porcine reproductive and respiratory syndrome (PRRS) virus: comparison of the North American and European isolates. Arch. Virol. 145:659-688.
10. Delputte PL, Nauwynck HJ. 2004. Porcine arterivirus infection of alveolar macrophages is mediated by sialic acid on the virus. J. Virol. 78:8094-8101.
11. Delputte PL, et al. 2007. Porcine arterivirus attachment to the macrophage-specific receptor sialoadhesin is dependent on the sialic acidbinding activity of the N-terminal immunoglobulin domain of sialoadhesin. J. Virol. 81:9546-9550.
12. Diaz I, Darwich L, Pappaterra G, Pujols J, Mateu E. 2006. Different European-type vaccines against porcine reproductive and respiratory syndrome virus have different immunological properties and confer different protection to pigs. Virology 351:249-259.
13. Dobbe JC, van der Meer Y, Spaan WJ, Snijder EJ. 2001. Construction of chimeric arteriviruses reveals that the ectodomain of the major glycoprotein is not the main determinant of equine arteritis virus tropism in cell culture. Virology 288:283-294.
14. Doms RW, Lamb RA, Rose JK, Helenius A. 1993. Folding and assembly of viral membrane proteins. Virology 193:545-562.
15. Duan X, Nauwynck HJ, Pensaert MB. 1997. Effects of origin and state of differentiation and activation of monocytes/macrophages on their susceptibility to porcine reproductive and respiratory syndrome virus (PRRSV). Arch. Virol. 142:2483-2497.
16. Faaberg KS, Even C, Palmer GA, Plagemann PG. 1995. Disulfide bonds between two envelope proteins of lactate dehydrogenase-elevating virus are essential for viral infectivity. J. Virol. 69:613-617.
17. Faaberg KS, et al. 2006. Neutralizing antibody responses of pigs infected with natural GP5 N-glycan mutants of porcine reproductive and respiratory syndrome virus. Viral Immunol. 19:294-304.
18. Fang Y, et al. 2007. Diversity and evolution of a newly emerged North American type 1 porcine arterivirus: analysis of isolates collected between 1999 and 2004. Arch. Virol. 152:1009-1017.
19. Fang Y, Snijder EJ. 2010. The PRRSV replicase: exploring the multifunctionality of an intriguing set of nonstructural proteins. Virus Res. 154:61-76.
20. Firth AE, et al. 2011. Discovery of a small arterivirus gene that overlaps the GP5 coding sequence and is important for virus production. J. Gen. Virol. 92:1097-1106.
21. Forsberg R. 2005. Divergence time of porcine reproductive and respiratory syndrome virus subtypes. Mol. Biol. Evol. 22:2131-2134.
22. Helenius A, Aebi M. 2001. Intracellular functions of N-linked glycans. Science 291:2364-2369.
23. Johnson CR, Griggs TF, Gnanandarajah JS, Murtaugh MP. 2011. Novel structural protein in porcine reproductive and respiratory syndrome virus encoded in an alternative open reading frame 5 present in all arteriviruses. J. Gen. Virol. 92:1107-1116.
24. Lv J, Zhang J, Sun Z, Liu W, Yuan S. 2008. An infectious cDNA clone of a highly pathogenic porcine reproductive and respiratory syndrome virus variant associated with porcine high fever syndrome. J. Gen. Virol. 89: 2075-2079.
25. Mardassi H, Massie B, Dea S. 1996. Intracellular synthesis, processing, and transport of proteins encoded by ORFs 5 to 7 of porcine reproductive and respiratory syndrome virus. Virology 221:98-112.
26. Mateu E, Diaz I. 2008. The challenge of PRRS immunology. Vet. J. 177:345-351.
27. Mateu E, et al. 2006. Evolution of ORF5 of Spanish porcine reproductive and respiratory syndrome virus strains from 1991 to 2005. Virus Res. 115:198-206.
28. Mellquist JL, Kasturi L, Spitalnik SL, Shakin-Eshleman SH. 1998. The amino acid following an Asn-X-Ser/Thr sequon is an important determinant of N-linked core glycosylation efficiency. Biochemistry 37:6833-6837.
29. Meunier JC, et al. 1999. Analysis of the glycosylation sites of hepatitis C virus (HCV) glycoprotein E1 and the influence of E1 glycans on the formation of the HCV glycoprotein complex. J. Gen. Virol. 80:887-896.
30. Molenkamp R, et al. 2000. The arterivirus replicase is the only viral protein required for genome replication and subgenomic mRNA transcription. J. Gen. Virol. 81:2491-2496.
31. Murtaugh MP, Genzow M. 2011. Immunological solutions for treatment and prevention of porcine reproductive and respiratory syndrome (PRRS). Vaccine 29:8192-8204.
32. Nelsen CJ, Murtaugh MP, Faaberg KS. 1999. Porcine reproductive and respiratory syndrome virus comparison: divergent evolution on two continents. J. Virol. 73:270-280.
33. Nelson EA, Christopher-Hennings J, Benfield DA. 1994. Serum immune responses to the proteins of porcine reproductive and respiratory syndrome (PRRS) virus. J. Vet. Diagn. Invest. 6:410-415.
34. Pizzi M. 1950. Sampling variation of the fifty percent end-point, determined by the Reed-Muench (Behrens) method. Hum. Biol. 22:151-190.
35. Plagemann PG, Moennig V. 1992. Lactate dehydrogenase-elevating virus, equine arteritis virus, and simian hemorrhagic fever virus: a new group of positive-strand RNA viruses. Adv. Virus Res. 41:99-192.
36. Shakin-Eshleman SH, Spitalnik SL, Kasturi L. 1996. The amino acid at the X position of an Asn-X-Ser sequon is an important determinant of N-linked core-glycosylation efficiency. J. Biol. Chem. 271:6363-6366.
37. Shi X, Elliott RM. 2004. Analysis of N-linked glycosylation of hantaan virus glycoproteins and the role of oligosaccharide side chains in protein folding and intracellular trafficking. J. Virol. 78:5414-5422.
38. Snijder EJ, Meulenberg JJ. 1998. The molecular biology of arteriviruses. J. Gen. Virol. 79:961-979.
39. Tian D, et al. 2012. Arterivirus minor envelope proteins are a major determinant of viral tropism in cell culture. J. Virol. 86:3701-3712.
40. Tian D, Zheng H, Zhang R, Zhuang J, Yuan S. 2011. Chimeric porcine reproductive and respiratory syndrome viruses reveal full function of genotype 1 envelope proteins in the backbone of genotype 2. Virology 412:1-8.
41. Van Breedam W, et al. 2010. The M/GP(5) glycoprotein complex of porcine reproductive and respiratory syndrome virus binds the sialoadhesin receptor in a sialic acid-dependent manner. PLoS Pathog. 6:e1000730. doi:10.1371/journal.ppat.1000730.
42. Vanderheijden N, et al. 2003. Involvement of sialoadhesin in entry of porcine reproductive and respiratory syndrome virus into porcine alveolar macrophages. J. Virol. 77:8207-8215.
43. Vu HL, et al. 2011. Immune evasion of porcine reproductive and respiratory syndrome virus through glycan shielding involves both glycoprotein 5 as well as glycoprotein 3. J. Virol. 85:5555-5564.
44. Warrens AN, Jones MD, Lechler RI. 1997. Splicing by overlap extension by PCR using asymmetric amplification: an improved technique for the generation of hybrid proteins of immunological interest. Gene 186:29-35.
45. Wei X, et al. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
46. Wensvoort G, et al. 1991. Mystery swine disease in The Netherlands: the isolation of Lelystad virus. Vet. Q. 13:121-130.
47. Wissink EH, et al. 2004. Significance of the oligosaccharides of the porcine reproductive and respiratory syndrome virus glycoproteins GP2a and GP5 for infectious virus production. J. Gen. Virol. 85:3715-3723.
48. Wissink EH, et al. 2005. Envelope protein requirements for the assembly of infectious virions of porcine reproductive and respiratory syndrome virus. J. Virol. 79:12495-12506.
49. Wu WH, et al. 2001. A 10-kDa structural protein of porcine reproductive and respiratory syndrome virus encoded by ORF2b. Virology 287:183-191.