Virology Journal | |
Identification of a new cell line permissive to porcine reproductive and respiratory syndrome virus infection and replication which is phenotypically distinct from MARC-145 cell line | |
Carl A Gagnon2  Mario Jacques2  Jérôme RE del Castillo1  Marie-Ève Lebel2  Cynthia Lévesque2  Nedzad Music2  Jian Jun Jia2  Chantale Provost2  | |
[1] Groupe de Recherche en Pharmacologie Animale du Québec (GREPAQ), Faculté de médecine vétérinaire Université de Montréal, 3200 rue Sicotte, Saint-Hyacinthe, Québec, J2S 7C6, Canada;Groupe de recherche sur les maladies infectieuses du porc (GREMIP), Centre de recherche en infectiologie porcine (CRIP), Faculté de médecine vétérinaire Université de Montréal, 3200 rue Sicotte, Saint-Hyacinthe, J2S 7C6, Québec, Canada | |
关键词: Cytokines; TNF-α; IFNγ; Type 1 IFN; Cell permissivity; Virus replication; SJPL cells; PRRSV; Porcine reproductive and respiratory syndrome virus; | |
Others : 1153196 DOI : 10.1186/1743-422X-9-267 |
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received in 2012-06-19, accepted in 2012-11-01, 发布年份 2012 | |
【 摘 要 】
Background
Airborne transmitted pathogens, such as porcine reproductive and respiratory syndrome virus (PRRSV), need to interact with host cells of the respiratory tract in order to be able to enter and disseminate in the host organism. Pulmonary alveolar macrophages (PAM) and MA104 derived monkey kidney MARC-145 cells are known to be permissive to PRRSV infection and replication and are the most studied cells in the literature. More recently, new cell lines developed to study PRRSV have been genetically modified to make them permissive to the virus. The SJPL cell line origin was initially reported to be epithelial cells of the respiratory tract of swine. Thus, the goal of this study was to determine if SJPL cells could support PRRSV infection and replication in vitro.
Results
The SJPL cell growth was significantly slower than MARC-145 cell growth. The SJPL cells were found to express the CD151 protein but not the CD163 and neither the sialoadhesin PRRSV receptors. During the course of the present study, the SJPL cells have been reported to be of monkey origin. Nevertheless, SJPL cells were found to be permissive to PRRSV infection and replication even if the development of the cytopathic effect was delayed compared to PRRSV-infected MARC-145 cells. Following PRRSV replication, the amount of infectious viral particles produced in SJPL and MARC-145 infected cells was similar. The SJPL cells allowed the replication of several PRRSV North American strains and were almost efficient as MARC-145 cells for virus isolation. Interestingly, PRRSV is 8 to 16 times more sensitive to IFNα antiviral effect in SJPL cell in comparison to that in MARC-145 cells. PRRSV induced an increase in IFNβ mRNA and no up regulation of IFNα mRNA in both infected cell types. In addition, PRRSV induced an up regulation of IFNγ and TNF-α mRNAs only in infected MARC-145 cells.
Conclusions
In conclusion, the SJPL cells are permissive to PRRSV. In addition, they are phenotypically different from MARC-145 cells and are an additional tool that could be used to study PRRSV pathogenesis mechanisms in vitro.
【 授权许可】
2012 Provost et al.; licensee BioMed Central Ltd.
【 预 览 】
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【 参考文献 】
- [1]Neumann EJ, Kliebenstein JB, Johnson CD, Mabry JW, Bush EJ, Seitzinger AH, Green AL, Zimmerman JJ: Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States. J Am Vet Med Assoc 2005, 227:385-392.
- [2]Keffaber KK: Reproductive failure of unknown etiology. Am Assoc Swine Prac News 1989, 1(2):1-9.
- [3]Loula T: Mystery pig disease. Agri-Practice 1991, 12:23-34.
- [4]Wensvoort G, Terpstra C, Pol JM, ter Laak EA, Bloemraad M, de Kluyver EP, Kragten C, van Buiten L, den Besten A, Wagenaar F, et al.: Mystery swine disease in The Netherlands: the isolation of Lelystad virus. Vet Q 1991, 13:121-130.
- [5]Albina E: [Porcine reproductive and respiratory syndrome: ten years of experience (1986-1996) with this undesirable viral infection]. Vet Res 1997, 28:305-352.
- [6]Rossow KD, Bautista EM, Goyal SM, Molitor TW, Murtaugh MP, Morrison RB, Benfield DA, Collins JE: Experimental porcine reproductive and respiratory syndrome virus infection in one-, four-, and 10-week-old pigs. J Vet Diagn Invest 1994, 6:3-12.
- [7]Benfield DA, Nelson E, Collins JE, Harris L, Goyal SM, Robison D, Christianson WT, Morrison RB, Gorcyca D, Chladek D: Characterization of swine infertility and respiratory syndrome (SIRS) virus (isolate ATCC VR-2332). J Vet Diagn Invest 1992, 4:127-133.
- [8]Collins JE, Benfield DA, Christianson WT, Harris L, Hennings JC, Shaw DP, Goyal SM, McCullough S, Morrison RB, Joo HS, et al.: Isolation of swine infertility and respiratory syndrome virus (isolate ATCC VR-2332) in North America and experimental reproduction of the disease in gnotobiotic pigs. J Vet Diagn Invest 1992, 4:117-126.
- [9]Cavanagh D: Nidovirales: a new order comprising coronaviridae and arteriviridae. Arch Virol 1997, 142:629-633.
- [10]Johnson CR, Griggs TF, Gnanandarajah J, Murtaugh MP: Novel structural protein in porcine reproductive and respiratory syndrome virus encoded by an alternative ORF5 present in all arteriviruses. J Gen Virol 2011, 92:1107-1116.
- [11]Music N, Gagnon CA: The role of porcine reproductive and respiratory syndrome (PRRS) virus structural and non-structural proteins in virus pathogenesis. Anim Health Res Rev 2010, 11:135-163.
- [12]Firth AE, Zevenhoven-Dobbe JC, Wills NM, Go YY, Balasuriya UB, Atkins JF, Snijder EJ, Posthuma CC: Discovery of a small arterivirus gene that overlaps the GP5 coding sequence and is important for virus production. J Gen Virol 2011, 92:1097-1106.
- [13]Gorbalenya AE, Enjuanes L, Ziebuhr J, Snijder EJ: Nidovirales: evolving the largest RNA virus genome. Virus Res 2006, 117:17-37.
- [14]Dea S, Gagnon CA, Mardassi H, Pirzadeh B, Rogan D: Current knowledge on the structural proteins of porcine reproductive and respiratory syndrome (PRRS) virus: comparison of the North American and European isolates. Arch Virol 2000, 145:659-688.
- [15]Meng XJ: Heterogeneity of porcine reproductive and respiratory syndrome virus: implications for current vaccine efficacy and future vaccine development. Vet Microbiol 2000, 74:309-329.
- [16]Hanada K, Suzuki Y, Nakane T, Hirose O, Gojobori T: The origin and evolution of porcine reproductive and respiratory syndrome viruses. Mol Biol Evol 2005, 22:1024-1031.
- [17]Beyer J, Fichtner D, Schirrmeier H, Polster U, Weiland E, Wege H: Porcine reproductive and respiratory syndrome virus (PRRSV): kinetics of infection in lymphatic organs and lung. J Vet Med B Infect Dis Vet Public Health 2000, 47:9-25.
- [18]Duan X, Nauwynck HJ, Pensaert MB: Virus quantification and identification of cellular targets in the lungs and lymphoid tissues of pigs at different time intervals after inoculation with porcine reproductive and respiratory syndrome virus (PRRSV). Vet Microbiol 1997, 56:9-19.
- [19]Halbur PG, Miller LD, Paul PS, Meng XJ, Huffman EL, Andrews JJ: Immunohistochemical identification of porcine reproductive and respiratory syndrome virus (PRRSV) antigen in the heart and lymphoid system of three-week-old colostrum-deprived pigs. Vet Pathol 1995, 32:200-204.
- [20]Halbur PG, Paul PS, Frey ML, Landgraf J, Eernisse K, Meng XJ, Andrews JJ, Lum MA, Rathje JA: Comparison of the antigen distribution of two US porcine reproductive and respiratory syndrome virus isolates with that of the Lelystad virus. Vet Pathol 1996, 33:159-170.
- [21]Sur JH, Doster AR, Christian JS, Galeota JA, Wills RW, Zimmerman JJ, Osorio FA: Porcine reproductive and respiratory syndrome virus replicates in testicular germ cells, alters spermatogenesis, and induces germ cell death by apoptosis. J Virol 1997, 71:9170-9179.
- [22]Rossow KD, Benfield DA, Goyal SM, Nelson EA, Christopher-Hennings J, Collins JE: Chronological immunohistochemical detection and localization of porcine reproductive and respiratory syndrome virus in gnotobiotic pigs. Vet Pathol 1996, 33:551-556.
- [23]Pol JM, van Dijk JE, Wensvoort G, Terpstra C: Pathological, ultrastructural, and immunohistochemical changes caused by Lelystad virus in experimentally induced infections of mystery swine disease (synonym: porcine epidemic abortion and respiratory syndrome (PEARS)). Vet Q 1991, 13:137-143.
- [24]Magar R, Larochelle R, Robinson Y, Dubuc C: Immunohistochemical detection of porcine reproductive and respiratory syndrome virus using colloidal gold. Can J Vet Res 1993, 57:300-304.
- [25]Cheon DS, Chae C, Lee YS: Detection of nucleic acids of porcine reproductive and respiratory syndrome virus in the lungs of naturally infected piglets as determined by in-situ hybridization. J Comp Pathol 1997, 117:157-163.
- [26]Teifke JP, Dauber M, Fichtner D, Lenk M, Polster U, Weiland E, Beyer J: Detection of European porcine reproductive and respiratory syndrome virus in porcine alveolar macrophages by two-colour immunofluorescence and in-situ hybridization-immunohistochemistry double labelling. J Comp Pathol 2001, 124:238-245.
- [27]Haynes JS, Halbur PG, Sirinarumitr T, Paul PS, Meng XJ, Huffman EL: Temporal and morphologic characterization of the distribution of porcine reproductive and respiratory syndrome virus (PRRSV) by in situ hybridization in pigs infected with isolates of PRRSV that differ in virulence. Vet Pathol 1997, 34:39-43.
- [28]Sur JH, Cooper VL, Galeota JA, Hesse RA, Doster AR, Osorio FA: In vivo detection of porcine reproductive and respiratory syndrome virus RNA by in situ hybridization at different times postinfection. J Clin Microbiol 1996, 34:2280-2286.
- [29]Voicu IL, Silim A, Morin M, Elazhary MA: Interaction of porcine reproductive and respiratory syndrome virus with swine monocytes. Vet Rec 1994, 134:422-423.
- [30]Wang X, Eaton M, Mayer M, Li H, He D, Nelson E, Christopher-Hennings J: Porcine reproductive and respiratory syndrome virus productively infects monocyte-derived dendritic cells and compromises their antigen-presenting ability. Arch Virol 2007, 152:289-303.
- [31]Patel D, Nan Y, Shen M, Ritthipichai K, Zhu X, Zhang YJ: Porcine reproductive and respiratory syndrome virus inhibits type I interferon signaling by blocking STAT1/STAT2 nuclear translocation. J Virol 2010, 84:11045-11055.
- [32]Bautista EM, Goyal SM, Yoon IJ, Joo HS, Collins JE: Comparison of porcine alveolar macrophages and CL 2621 for the detection of porcine reproductive and respiratory syndrome (PRRS) virus and anti-PRRS antibody. J Vet Diagn Invest 1993, 5:163-165.
- [33]Kim HS, Kwang J, Yoon IJ, Joo HS, Frey ML: Enhanced replication of porcine reproductive and respiratory syndrome (PRRS) virus in a homogeneous subpopulation of MA-104 cell line. Arch Virol 1993, 133:477-483.
- [34]Lee YJ, Park CK, Nam E, Kim SH, Lee OS, du Lee S, Lee C: Generation of a porcine alveolar macrophage cell line for the growth of porcine reproductive and respiratory syndrome virus. J Virol Methods 2010, 163:410-415.
- [35]Sagong M, Park CK, Kim SH, Lee KK, Lee OS, du Lee S, Cha SY, Lee C: Human telomerase reverse transcriptase-immortalized porcine monomyeloid cell lines for the production of porcine reproductive and respiratory syndrome virus. J Virol Methods 2012, 179:26-32.
- [36]An TQ, Tian ZJ, He YX, Xiao Y, Jiang YF, Peng JM, Zhou YJ, Liu D, Tong GZ: Porcine reproductive and respiratory syndrome virus attachment is mediated by the N-terminal domain of the sialoadhesin receptor. Vet Microbiol 2010, 143:371-378.
- [37]Calvert JG, Slade DE, Shields SL, Jolie R, Mannan RM, Ankenbauer RG, Welch SK: CD163 expression confers susceptibility to porcine reproductive and respiratory syndrome viruses. J Virol 2007, 81:7371-7379.
- [38]Dee S, Otake S, Oliveira S, Deen J: Evidence of long distance airborne transport of porcine reproductive and respiratory syndrome virus and Mycoplasma hyopneumoniae. Vet Res 2009, 40:39.
- [39]Huang YW, Fang Y, Meng XJ: Identification and characterization of a porcine monocytic cell line supporting porcine reproductive and respiratory syndrome virus (PRRSV) replication and progeny virion production by using an improved DNA-launched PRRSV reverse genetics system. Virus Res 2009, 145:1-8.
- [40]Ferrari M, Scalvini A, Losio MN, Corradi A, Soncini M, Bignotti E, Milanesi E, Ajmone-Marsan P, Barlati S, Bellotti D, Tonelli M: Establishment and characterization of two new pig cell lines for use in virological diagnostic laboratories. J Virol Methods 2003, 107:205-212.
- [41]Seo SH, Goloubeva O, Webby R, Webster RG: Characterization of a porcine lung epithelial cell line suitable for influenza virus studies. J Virol 2001, 75:9517-9525.
- [42]Silversides DW, Music N, Jacques M, Gagnon CA, Webby R: Investigation of the species origin of the St. Jude Porcine Lung epithelial cell line (SJPL) made available to researchers. J Virol 2010, 84:5454-5455.
- [43]Magar R, Larochelle R, Dea S, Gagnon CA, Nelson EA, Christopher-Hennings J, Benfield DA: Antigenic comparison of Canadian and US isolates of porcine reproductive and respiratory syndrome virus using monoclonal antibodies to the nucleocapsid protein. Can J Vet Res 1995, 59:232-234.
- [44]Van Gorp H, Van Breedam W, Delputte PL, Nauwynck HJ: Sialoadhesin and CD163 join forces during entry of the porcine reproductive and respiratory syndrome virus. J Gen Virol 2008, 89:2943-2953.
- [45]Das PB, Dinh PX, Ansari IH, de Lima M, Osorio FA, Pattnaik AK: The Minor Envelope Glycoproteins GP2a and GP4 of Porcine Reproductive and Respiratory Syndrome Virus Interact with the Receptor CD163. J Virol 2010, 84:1731-1740.
- [46]Shanmukhappa K, Kim JK, Kapil S: Role of CD151, A tetraspanin, in porcine reproductive and respiratory syndrome virus infection. Virol J 2007, 4:62.
- [47]Delputte PL, Van Breedam W, Delrue I, Oetke C, Crocker PR, Nauwynck HJ: Porcine arterivirus attachment to the macrophage-specific receptor sialoadhesin is dependent on the sialic acid-binding activity of the N-terminal immunoglobulin domain of sialoadhesin. J Virol 2007, 81:9546-9550.
- [48]Mogensen TH, Paludan SR: Molecular pathways in virus-induced cytokine production. Microbiol Mol Biol Rev 2001, 65:131-150.
- [49]Kim O, Sun Y, Lai FW, Song C, Yoo D: 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. Virol 2010, 402:315-326.
- [50]Chang HW, Jeng CR, Liu JJ, Lin TL, Chang CC, Chia MY, Tsai YC, Pang VF: Reduction of porcine reproductive and respiratory syndrome virus (PRRSV) infection in swine alveolar macrophages by porcine circovirus 2 (PCV2)-induced interferon-alpha. Vet Microbiol 2005, 108:167-177.
- [51]Gomez-Laguna J, Salguero FJ, Pallares FJ, Fernandez de Marco M, Barranco I, Ceron JJ, Martinez-Subiela S, Van Reeth K, Carrasco L: Acute phase response in porcine reproductive and respiratory syndrome virus infection. Comp Immunol Microbiol Infect Dis 2010, 33:e51-58.
- [52]Shi X, Wang L, Zhi Y, Xing G, Zhao D, Deng R, Zhang G: Porcine reproductive and respiratory syndrome virus (PRRSV) could be sensed by professional beta interferon-producing system and had mechanisms to inhibit this action in MARC-145 cells. Virus Res 2010, 153:151-156.
- [53]Genini S, Delputte PL, Malinverni R, Cecere M, Stella A, Nauwynck HJ, Giuffra E: Genome-wide transcriptional response of primary alveolar macrophages following infection with porcine reproductive and respiratory syndrome virus. J Gen Virol 2008, 89:2550-2564.
- [54]Auger E, Deslandes V, Ramjeet M, Contreras I, Nash JH, Harel J, Gottschalk M, Olivier M, Jacques M: Host-pathogen interactions of Actinobacillus pleuropneumoniae with porcine lung and tracheal epithelial cells. Infect Immun 2009, 77:1426-1441.
- [55]Brockmeier SL, Lager KM, Grubman MJ, Brough DE, Ettyreddy D, Sacco RE, Gauger PC, Loving CL, Vorwald AC, Kehrli ME Jr, Lehmkuhl HD: Adenovirus-mediated expression of interferon-alpha delays viral replication and reduces disease signs in swine challenged with porcine reproductive and respiratory syndrome virus. Viral Immunol 2009, 22:173-180.
- [56]Mateu E, Diaz I: The challenge of PRRS immunology. Vet J 2008, 177:345-351.
- [57]Kimman TG, Cornelissen LA, Moormann RJ, Rebel JM, Stockhofe-Zurwieden N: Challenges for porcine reproductive and respiratory syndrome virus (PRRSV) vaccinology. Vaccine 2009, 27:3704-3718.
- [58]Song C, Krell P, Yoo D: Nonstructural protein 1alpha subunit-based inhibition of NF-kappaB activation and suppression of interferon-beta production by porcine reproductive and respiratory syndrome virus. Virol 2010, 407:268-280.
- [59]Beura LK, Sarkar SN, Kwon B, Subramaniam S, Jones C, Pattnaik AK, Osorio FA: Porcine reproductive and respiratory syndrome virus nonstructural protein 1beta modulates host innate immune response by antagonizing IRF3 activation. J Virol 2010, 84:1574-1584.
- [60]Lee SM, Schommer SK, Kleiboeker SB: Porcine reproductive and respiratory syndrome virus field isolates differ in in vitro interferon phenotypes. Vet Immunol Immunopathol 2004, 102:217-231.
- [61]Choi C, Chae C: Expression of tumour necrosis factor-alpha is associated with apoptosis in lungs of pigs experimentally infected with porcine reproductive and respiratory syndrome virus. Res Vet Sci 2002, 72:45-49.
- [62]Kim TS, Benfield DA, Rowland RR: Porcine reproductive and respiratory syndrome virus-induced cell death exhibits features consistent with a nontypical form of apoptosis. Virus Res 2002, 85:133-140.
- [63]Labarque G, Van Gucht S, Nauwynck H, Van Reeth K, Pensaert M: Apoptosis in the lungs of pigs infected with porcine reproductive and respiratory syndrome virus and associations with the production of apoptogenic cytokines. Vet Res 2003, 34:249-260.
- [64]Miller LC, Fox JM: Apoptosis and porcine reproductive and respiratory syndrome virus. Vet Immunol Immunopathol 2004, 102:131-142.
- [65]Gagnon CA, Lachapelle G, Langelier Y, Massie B, Dea S: Adenoviral-expressed GP5 of porcine respiratory and reproductive syndrome virus differs in its cellular maturation from the authentic viral protein but maintains known biological functions. Arch Virol 2003, 148:951-972.
- [66]Costers S, Lefebvre DJ, Delputte PL, Nauwynck HJ: Porcine reproductive and respiratory syndrome virus modulates apoptosis during replication in alveolar macrophages. Arch Virol 2008, 153:1453-1465.
- [67]Gagnon CA, Del Castillo JR, Music N, Fontaine G, Harel J, Tremblay D: Development and use of a multiplex real-time quantitative polymerase chain reaction assay for detection and differentiation of Porcine circovirus-2 genotypes 2a and 2b in an epidemiological survey. J Vet Diagn Invest 2008, 20:545-558.
- [68]Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K: In Situ Hybridization and Immunohistochemistry, Immunohistochemistry. In Short protocols in molecular biology. Volume 2. 5th edition. Edited by Ausubel FM. New York: John Wiley & Sons; 2005:14.25-14.28.
- [69]Integrated DNA technologies http://www.idtdna.com/Scitools/Applications/Primerquest/ webcite
- [70]Littell RC, Milliken GA, Stoup WW, Wolfinger RD, Schabenberger O: SAS for mixed models. Second edition. Cary: SAS publishing; 2006:840.
- [71]Littell RC, Pendergast J, Natarajan R: Modelling covariance structure in the analysis of repeated measures data. Stat Med 2000, 19:1793-1819.