The cellular interactome for glycoprotein 5 of the Chinese highly pathogenic porcine reproductive and respiratory syndrome virus

doi:10.1016/S2095-3119(15)61186-8

摘要/Abstract

Abstract: The glycoprotein 5 (GP5) of porcine reproductive and respiratory syndrome virus (PRRSV) is a multi-functional protein that plays important roles in virus assembly, entry and viral anti-host responses. In the present study, we investigated the cellular binding partners of GP5 by using lentivirus transduction coupled with immunoprecipitation and mass spectrometry. There were about 40 cellular proteins identified with high Confidence Icons by MS/MS. Ingenuity Pathway Analysis (IPA) indicated that these proteins could be assigned to different functional classes and networks. Furthermore, we validated some of the interactions by co-immunoprecipitation (Co-IP) and confocal microscopy, including those with mitofilin, a mitochondrial inner membrane protein that might be involved in PRRSV or GP5-induced apoptosis, and calnexin, a protein chaperone that might facilitate the folding and maturation of GP5. The interactome data contribute to understand the role and molecular mechanisms of GP5 in PRRSV pathogenesis.

Key words: PRRSV , glycoprotein 5 (GP5) , interactome profile , mitofilin , calnexin

DU Ji-ge, GE Xin-na, DONG Hong, ZHANG Ning, ZHOU Lei, GUO Xin, YANG Han-chun. [J]. Journal of Integrative Agriculture, 2016, 15(8): 1833-1845.

DU Ji-ge, GE Xin-na, DONG Hong, ZHANG Ning, ZHOU Lei, GUO Xin, YANG Han-chun. The cellular interactome for glycoprotein 5 of the Chinese highly pathogenic porcine reproductive and respiratory syndrome virus[J]. Journal of Integrative Agriculture, 2016, 15(8): 1833-1845.

参考文献

Ansari I H, Kwon B, Osorio F A, Pattnaik A K. 2006. Influence of N-linked glycosylation of porcine reproductive and respiratory syndrome virus GP5 on virus infectivity, antigenicity, and ability to induce neutralizing antibodies. Journal of Virology, 80, 3994–4004.

Bautista E M, Molitor T W. 1997. Cell-mediated immunity to porcine reproductive and respiratory syndrome virus in swine. Viral Immunology, 10, 83–94.

Budihardjo I, Oliver H, Lutter M, Luo X, Wang X. 1999. Biochemical pathways of caspase activation during apoptosis. Annual Review of Cell and Developmental Biology, 15, 269–290.

Cao J, Li B, Fang L, Chen H, Xiao S. 2012. Pathogenesis of nonsuppurative encephalitis caused by highly pathogenic porcine reproductive and respiratory syndrome virus. Journal of Veterinary Diagnostic Investigation, 24, 767–771.

Cavanagh D. 1997. Nidovirales: A new order comprising Coronaviridae and Arteriviridae. Archives of Virology, 142, 629–633.

Chen Z, Li K, Plagemann P G. 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.

Conzelmann K K, Visser N, Van Woensel P, Thiel H J. 1993. Molecular characterization of porcine reproductive and respiratory syndrome virus, a member of the arterivirus group. Virology, 193, 329–339.

Dea S, Gagnon C A, 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. Archives of Virology, 145, 659–688.

Delputte P L, Costers S, Nauwynck H J. 2005. Analysis of porcine reproductive and respiratory syndrome virus attachment and internalization: distinctive roles for heparan sulphate and sialoadhesin. Journal of General Virology, 86, 1441–1445.

Dong J, Zhang N, Ge X, Zhou L, Guo X, Yang H. 2014. The interaction of nonstructural protein 9 with retinoblastoma protein benefits the replication of genotype 2 porcine reproductive and respiratory syndrome virus in vitro. Virology, 464–465, 432–440.

Fang Y, Snijder E J. 2010. The PRRSV replicase: exploring the multifunctionality of an intriguing set of nonstructural proteins. Virus Research, 154, 61–76.

Fernandez A, Suarez P, Castro J M, Tabares E, Diaz-Guerra M. 2002. Characterization of regions in the GP5 protein of porcine reproductive and respiratory syndrome virus required to induce apoptotic cell death. Virus Research, 83, 103–118.

Gieffers C, Korioth F, Heimann P, Ungermann C, Frey J. 1997. Mitofilin is a transmembrane protein of the inner mitochondrial membrane expressed as two isoforms. Experimental Cell Research, 232, 395–399.

Gruener M, Bravo I G, Momburg F, Alonso A, Tomakidi P. 2007. The E5 protein of the human papillomavirus type 16 down-regulates HLA-I surface expression in calnexin-expressing but not in calnexin-deficient cells. Virology Journal, 4, 246–251.

Helenius A, Aebi M. 2001. Intracellular functions of N-linked glycans. Science, 291, 2364–2369.

Helenius A, Aebi M. 2004. Roles of N-linked glycans in the endoplasmic reticulum. Annual Review of Biochemistry, 73, 1019–1049.

Hou Y, Chen J, Tong G, Tian Z, Zhou Y, Li G, Li, Peng J, An T, Yang H. 2008. A recombinant plasmid co-expressing swine ubiquitin and the GP5 encoding-gene of porcine reproductive and respiratory syndrome virus induces protective immunity in piglets. Vaccine, 26, 1438–1449.

John G B, Shang Y L, Li L, Renken C, Mannella C A, Selker J M, Rangell L, Bennett M J, Zha J P. 2005. The mitochondrial inner membrane protein mitofilin controls cristae morphology. Molecular Biology of the Cell, 16, 1543–1554.

Johnson C R, Griggs T F, Gnanandarajah J, Murtaugh M P. 2011. Novel structural protein in porcine reproductive and respiratory syndrome virus encoded by an alternative ORF5 present in all arteriviruses. Journal of General Virology, 92, 1107–1116.

Jourdan S S, Osorio F, Hiscox J A. 2012. An interactome map of the nucleocapsid protein from a highly pathogenic North American porcine reproductive and respiratory syndrome virus strain generated using SILAC-based quantitative proteomics. Proteomics, 12, 1015–1023.

Keffaber K. 1989. Reproductive failure of unknown etiology. American Association of Swine Practitioners. Newslett. 1, 9

Kim O, Sun Y, Lai F W, Song C, Yoo D. 2010. Modulation of type I interferon induction by porcine reproductive and respiratory syndrome virus and degradation of CREB-binding protein by non-structural protein 1 in MARC-145 and HeLa cells. Virology, 402, 315–326.

Kumar S. 2007. Caspase function in programmed cell death. Cell Death and Differentiation, 14, 32–43.

Labarque G, Van Gucht S, Nauwynck H, Van Reeth K, Pensaert M. 2003. Apoptosis in the lungs of pigs infected with porcine reproductive and respiratory syndrome virus and associations with the production of apoptogenic cytokines. Veterinary Reseach, 34, 249–260.

Lee J, Park J S, Moon J Y, Kim K Y, Moon H M. 2003. The influence of glycosylation on secretion, stability, and immunogenicity of recombinant HBV pre-S antigen synthesized in Saccharomyces cerevisiae. Biochemical and Biophysical Research Communications, 303, 427–432.

Lee S M, Kleiboeker S B. 2007. Porcine reproductive and respiratory syndrome virus induces apoptosis through a mitochondria-mediated pathway. Virology, 365, 419–434.

Li L, Zhao Q, Ge X, Teng K, Kuang Y, Chen Y, Guo X, Yang H. 2012. Chinese highly pathogenic porcine reproductive and respiratory syndrome virus exhibits more extensive tissue tropism for pigs. Virology Journal, 9, 1981–1981.

Li S, Zheng H, Mao A P, Zhong B, Li Y, Liu Y, Gao Y, Ran Y, Tien P, Shu H B. 2010. Regulation of virus-triggered signaling by OTUB1- and OTUB2-mediated deubiquitination of TRAF3 and TRAF6. The Journal of Biological Chemistry, 285, 4291–4297.

Li Y, Zhou L, Zhang J, Ge X, Zhou R, Zheng H, Geng G, Guo X, Yang H. 2014. Nsp9 and Nsp10 contribute to the fatal virulence of highly pathogenic porcine reproductive and respiratory syndrome virus emerging in China. PLoS Pathogens, 10, e1004216.

Loemba H D, Mounir S, Mardassi H, Archambault D, Dea S. 1996. Kinetics of humoral immune response to the major structural proteins of the porcine reproductive and respiratory syndrome virus. Archives of Virology, 141, 751–761.

Meier W A, Wheeler J, Husmann R J, Osorio F A, Zuckermann F A. 2000. Characteristics of the immune response of pigs to wild-type PRRS virus or to commercially available vaccines: An unconventional response. In: American Association of Swine Practitioners. Indianapolis, IN. Mar 11–14, 2000. pp. 415–418.

Mengeling W L, Lager K M, Vorwald A C. 1994. Temporal characterization of transplacental infection of porcine fetuses with porcine reproductive and respiratory syndrome virus. American Journal of Veterinary Research, 55, 1391–1398.

Meulenberg J J, Petersen-den Besten A, De Kluyver E P, Moormann R J, Schaaper W M, Wensvoort G. 1995. Characterization of proteins encoded by ORFs 2 to 7 of Lelystad virus. Virology, 206, 155–163.

Miller L C, Fox J M. 2004. Apoptosis and porcine reproductive and respiratory syndrome virus. Veterinary Immunology and Immunopathology, 102, 131–142.

Miura S, Kawana K, Schust D J, Fujii T, Yokoyama T, Iwasawa Y, Nagamatsu T, Adachi K, Tomio A, Tomio K, Kojima S, Yasugi T, Kozuma S, Taketani Y. 2010. CD1d, a sentinel molecule bridging innate and adaptive immunity, is downregulated by the human papillomavirus (HPV) E5 protein: a possible mechanism for immune evasion by HPV. Journal of Virology, 84, 11614–11623.

Murtaugh M P, Xiao Z, Zuckermann F. 2002. Immunological responses of swine to porcine reproductive and respiratory syndrome virus infection. Viral Immunology, 15, 533–547.

Nielsen J, Botner A, Bille-Hansen V, Oleksiewicz M B, Storgaard T. 2002. Experimental inoculation of late term pregnant sows with a field isolate of porcine reproductive and respiratory syndrome vaccine-derived virus. Veterinary Microbiology, 84, 1–13.

Odgren P R, Toukatly G, Bangs P L, Gilmore R, Fey E G. 1996. Molecular characterization of mitofilin (HMP), a mitochondria-associated protein with predicted coiled coil and intermembrane space targeting domains. Journal of Cell Science, 109, 2253–2264.

Pieren M, Galli C, Denzel A, Molinari M. 2005. The use of calnexin and calreticulin by cellular and viral glycoproteins. Journal of Biological Chemistry, 280, 28265–28271.

Plana J, Vayreda M, Vilarrasa J, Bastons M, Rosell R, Martinez M, San Gabriel A, Pujols J, Badiola J L, Ramos J A. 1992. Porcine epidemic abortion and respiratory syndrome (mystery swine disease). Isolation in Spain of the causative agent and experimental reproduction of the disease. Veterinary Microbiology, 33, 203–211.

Rossow K D, Collins J E, Goyal S M, Nelson E A, Christopher-Hennings J, Benfield D A. 1995. Pathogenesis of porcine reproductive and respiratory syndrome virus infection in gnotobiotic pigs. Veterinary Pathology, 32, 361–373.

Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes S A, Mannella C A, Korsmeyer S J. 2002. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Developmental Cell, 2, 55–67.

Suarez P, Diaz-Guerra M, Prieto C, Esteban M, Castro J M, Nieto A, Ortin J. 1996. Open reading frame 5 of porcine reproductive and respiratory syndrome virus as a cause of virus-induced apoptosis. Journal of Virology, 70, 2876–2882.

Terpstra C, Wensvoort G, Pol J M. 1991. Experimental reproduction of porcine epidemic abortion and respiratory syndrome (mystery swine disease) by infection with Lelystad virus: Koch’s postulates fulfilled. The Veterinary Quarterly, 13, 131–136.

Thanawongnuwech R, Halbur P G, Andrews J J. 1997. Immunohistochemical detection of porcine reproductive and respiratory syndrome virus antigen in neurovascular lesions. Journal of Veterinary Diagnostic Investigation, 9, 334–337.

Tian K, Yu X, Zhao T, Feng Y, Cao Z, Wang C, Hu Y, Chen X, Hu D, Tian X, Liu D, Zhang S, Deng X, Ding Y, Yang L, Zhang Y, Xiao H, Qiao M, Wang B, Hou L, et al. 2007. Emergence of fatal PRRSV variants: Unparalleled outbreaks of atypical PRRS in China and molecular dissection of the unique hallmark. PLoS One, 2, e526.

Wang L, Zhou L, Zhang H, Li Y, Ge X, Guo X, Yu K, Yang H. 2014. Interactome profile of the host cellular proteins and the nonstructural protein 2 of porcine reproductive and respiratory syndrome virus. PLoS ONE, 9, e99176.

Wang X, Li C, Zhou L, Zhang N, Wang X, Ge X, Guo X, Yang H. 2014. Porcine reproductive and respiratory syndrome virus counteracts the porcine intrinsic virus restriction factors-IFITM1 and Tetherin in MARC-145 cells. Virus Research, 191, 92–100.

Weesendorp E, Stockhofe-Zurwieden N, Fijten H, Rebel J M. 2013. Phenotypic modulation and cytokine profiles of antigen presenting cells by European subtype 1 and 3 porcine reproductive and respiratory syndrome virus strains in vitro and in vivo. Veterinary Microbiology, 167, 638–650.

Wei X, Decker J M, Wang S, Hui H, Kappes J C, Wu X, Salazar-Gonzalez J F, Salazar M G, Kilby J M, Saag M S, Komarova N L, Nowak M A, Hahn B H, Kwong P D, Shaw G M. 2003. Antibody neutralization and escape by HIV-1. Nature, 422, 307–312.

Wei Z, Lin T, Sun L, Li Y, Wang X, Gao F, Liu R, Chen C, Tong G, Yuan S. 2012. N-Linked glycosylation of GP5 of porcine reproductive and respiratory syndrome virus is critically important for virus replication in vivo. Journal of Virology, 86, 9941–9951.

Wissink E H, Kroese M V, van Wijk H A, Rijsewijk F A, Meulenberg J J, Rottier P J. 2005. Envelope protein requirements for the assembly of infectious virions of porcine reproductive and respiratory syndrome virus. Journal of Virology, 79, 12495–12506.

Wissink E H, van Wijk H A, Kroese M V, Weiland E, Meulenberg J J, Rottier P J, van Rijn P A. 2003. The major envelope protein, GP5, of a European porcine reproductive and respiratory syndrome virus contains a neutralization epitope in its N-terminal ectodomain. Journal of General Virology, 84, 1535–1543.

Yang R, Zhao G, Liang S, Zhang Y, Sun L, Chen H, Liu D. 2012. Mitofilin regulates cytochrome c release during apoptosis by controlling mitochondrial cristae remodeling. Biochemical and Biophysical Research Communications, 428, 93–98.

Zhang H, Guo X, Ge X, Chen Y, Sun Q, Yang H. 2009. Changes in the cellular proteins of pulmonary alveolar macrophage infected with porcine reproductive and respiratory syndrome virus by proteomics analysis. Journal of Proteome Research, 8, 3091–3097.

Zhou L, Yang H. 2010. Porcine reproductive and respiratory syndrome in China. Virus Research, 154, 31–37.

Zhou L, Zhang J, Zeng J, Yin S, Li Y, Zheng L, Guo X, Ge X, Yang H. 2009. The 30-amino-acid deletion in the Nsp2 of highly pathogenic porcine reproductive and respiratory syndrome virus emerging in China is not related to its virulence. Journal of Virology, 83, 5156–516.