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Table S1. Immunization program of inactivated H1N1 and PoIFNα in pigs
Table S2. Primer sequences used in this study
Table S3. Antiviral activities of PoIFNα toward different cell lines
10.1007s12250-019-00102-7-ESM1.pdf |
Arend WP, Palmer G, Gabay C (2008) IL-1, IL-18, and IL-33 families of cytokines. Immunol Rev 223:20–38
doi: 10.1111/imr.2008.223.issue-1
Beilharz MW, McDonald W, Watson MW, Heng J, McGeachie J, Lawson CM (1997) Low-dose oral type Ⅰ interferons reduce early virus replication of murine cytomegalovirus in vivo. J Interferon Cytokine Res 17:625–630
doi: 10.1089/jir.1997.17.625
Biron CA (2001) Interferons alpha and beta as immune regulators–a new look. Immunity 14:661–664
doi: 10.1016/S1074-7613(01)00154-6
Bracci L, Canini I, Puzelli S, Sestili P, Venditti M, Spada M, Donatelli I, Belardelli F, Proietti E (2005) Type Ⅰ IFN is a powerful mucosal adjuvant for a selective intranasal vaccination against influenza virus in mice and affects antigen capture at mucosal level. Vaccine 23:2994–3004
doi: 10.1016/j.vaccine.2004.12.006
Braun D, Caramalho I, Demengeot J (2002) IFN-alpha/beta enhances BCR-dependent B cell responses. Int Immunol 14:411–419
doi: 10.1093/intimm/14.4.411
Brod SA, Nelson L, Jin R, Wolinsky JS (1999) Ingested interferon alpha induces Mx mRNA. Cytokine 11:492–499
doi: 10.1006/cyto.1998.0450
Brown IH (2000) The epidemiology and evolution of influenza viruses in pigs. Vet Microbiol 74:29–46
doi: 10.1016/S0378-1135(00)00164-4
Chen C, Li J, Bi Y, Yang L, Meng S, Zhou Y, Jia X, Meng S, Sun L, Liu W (2013) Synthetic B- and T-cell epitope peptides of porcine reproductive and respiratory syndrome virus with Gp96 as adjuvant induced humoral and cell-mediated immunity. Vaccine 31:1838–1847
doi: 10.1016/j.vaccine.2013.01.049
Cheng G, Zhao X, Yan W, Wang W, Zuo X, Huang K, Liu Y, Chen J, Wang J, Cong W, Liu M, Gao H, Chen J, Lu Y, Zheng Z (2007) Alpha interferon is a powerful adjuvant for a recombinant protein vaccine against foot-and-mouth disease virus in swine, and an effective stimulus of in vivo immune response. Vaccine 25:5199–5208
doi: 10.1016/j.vaccine.2007.04.089
Chiou CJ, Tseng LP, Deng MC, Jiang PR, Tasi SL, Chung TW, Huang YY, Liu DZ (2009) Mucoadhesive liposomes for intranasal immunization with an avian influenza virus vaccine in chickens. Biomaterials 30:5862–5868
doi: 10.1016/j.biomaterials.2009.06.046
da Cunha IA, Zulpo DL, Bogado AL, de Barros LD, Taroda A, Igarashi M, Navarro IT, Garcia JL (2012) Humoral and cellular immune responses in pigs immunized intranasally with crude rhoptry proteins of Toxoplasma gondii plus Quil-A. Vet Parasitol 186:216–221
doi: 10.1016/j.vetpar.2011.11.034
Dawson HD, Beshah E, Nishi S, Solano-Aguilar G, Morimoto M, Zhao A, Madden KB, Ledbetter TK, Dubey JP, Shea-Donohue T, Lunney JK, Urban JF Jr (2005) Localized multigene expression patterns support an evolving Th1/Th2-like paradigm in response to infections with Toxoplasma gondii and Ascaris suum. Infect Immun 73: 1116–1128
Diaz-San Segundo F, Moraes MP, de Los Santos T, Dias CC, Grubman MJ (2010) Interferon-induced protection against foot-and-mouth disease virus infection correlates with enhanced tissue-specific innate immune cell infiltration and interferon-stimulated gene expression. J Virol 84:2063–2077
doi: 10.1128/JVI.01874-09
Duvigneau JC, Hartl RT, Groiss S, Gemeiner M (2005) Quantitative simultaneous multiplex real-time PCR for the detection of porcine cytokines. J Immunol Methods 306:16–27
doi: 10.1016/j.jim.2005.06.021
Eisfeld AJ, Neumann G, Kawaoka Y (2015) At the centre: influenza A virus ribonucleoproteins. Nat Rev Microbiol 13:28–41
doi: 10.1038/nrmicro3367
Feng N, Jaimes MC, Lazarus NH, Monak D, Zhang C, Butcher EC, Greenberg HB (2006) Redundant role of chemokines CCL25/ TECK and CCL28/MEC in IgA + plasmablast recruitment to the intestinal lamina propria after rotavirus infection. J Immunol 176:5749–5759
doi: 10.4049/jimmunol.176.10.5749
Foster N, Hulme SD, Barrow PA (2003) Induction of antimicrobial pathways during early-phase immune response to Salmonella spp. in murine macrophages: gamma interferon (IFN-gamma) and upregulation of IFN-gamma receptor alpha expression are required for NADPH phagocytic oxidase gp91-stimulated oxidative burst and control of virulent Salmonella spp. Infect Immun 71:4733–4741
doi: 10.1128/IAI.71.8.4733-4741.2003
Giacomini P, Tecce R, Gambari R, Sacchi A, Fisher PB, Natali PG (1988) Recombinant human IFN-gamma, but not IFN-alpha or IFN-beta, enhances MHC- and non-MHC-encoded glycoproteins by a protein synthesis-dependent mechanism. J Immunol 140:3073–3081
Goodbourn S, Didcock L, Randall RE (2000) Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J Gen Virol 81:2341–2364
doi: 10.1099/0022-1317-81-10-2341
Gosling J, Dairaghi DJ, Wang Y, Hanley M, Talbot D, Miao Z, Schall TJ (2000) Cutting edge: identification of a novel chemokine receptor that binds dendritic cell- and T cell-active chemokines including ELC, SLC, and TECK. J Immunol 164:2851–2856
doi: 10.4049/jimmunol.164.6.2851
Hilbert DM, Cancro MP, Scherle PA, Nordan RP, Van Snick J, Gerhard W, Rudikoff S (1989) T cell derived IL-6 is differentially required for antigen-specific antibody secretion by primary and secondary B cells. J Immunol 143:4019–4024
Hromadnikova I, Li S, Kotlabova K, Dickinson AM (2016) Influence of in vitro IL-2 or IL-15 alone or in combination with Hsp 70 derived 14-mer peptide (TKD) on the expression of NK cell activatory and inhibitory receptors on peripheral blood T Cells, B Cells and NKT cells. PLoS ONE 11:e0151535
doi: 10.1371/journal.pone.0151535
Hu L, Lin XY, Yang ZX, Yao XP, Li GL, Peng SZ, Wang Y (2015) A multiplex PCR for simultaneous detection of classical swine fever virus, African swine fever virus, highly pathogenic porcine reproductive and respiratory syndrome virus, porcine reproductive and respiratory syndrome virus and pseudorabies in swines. Pol J Vet Sci 18:715–723
doi: 10.1515/pjvs-2015-0093
Hyland K, Foss DL, Johnson CR, Murtaugh MP (2004) Oral immunization induces local and distant mucosal immunity in swine. Vet Immunol Immunopathol 102:329–338
doi: 10.1016/j.vetimm.2004.09.015
Itoh K, Hirohata S (1995) The role of IL-10 in human B cell activation, proliferation, and differentiation. J Immunol 154:4341–4350
Lazarus NH, Kunkel EJ, Johnston B, Wilson E, Youngman KR, Butcher EC (2003) A common mucosal chemokine (mucosae-associated epithelial chemokine/CCL28) selectively attracts IgA plasmablasts. J Immunol 170:3799–3805
doi: 10.4049/jimmunol.170.7.3799
Le Bon A, Schiavoni G, D'Agostino G, Gresser I, Belardelli F, Tough DF (2001) Type i interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo. Immunity 14:461–470
doi: 10.1016/S1074-7613(01)00126-1
Lee YJ, Lee C (2012) Cytokine production in immortalized porcine alveolar macrophages infected with porcine reproductive and respiratory syndrome virus. Vet Immunol Immunopathol 150:213–220
doi: 10.1016/j.vetimm.2012.09.007
Lung O, Beeston A, Ohene-Adjei S, Pasick J, Hodko D, Hughes KB, Furukawa-Stoffer T, Fisher M, Deregt D (2012) Electronic microarray assays for avian influenza and Newcastle disease virus. J Virol Methods 185:244–253
doi: 10.1016/j.jviromet.2012.07.005
Mamber SW, Lins J, Gurel V, Hutcheson DP, Pinedo P, Bechtol D, Krakowka S, Fields-Henderson R, Cummins JM (2016) Lowdose oral interferon modulates expression of inflammatory and autoimmune genes in cattle. Vet Immunol Immunopathol 172:64–71
doi: 10.1016/j.vetimm.2016.03.006
McBride S, Hoebe K, Georgel P, Janssen E (2006) Cell-associated double-stranded RNA enhances antitumor activity through the production of type Ⅰ IFN. J Immunol 177:6122–6128
doi: 10.4049/jimmunol.177.9.6122
Meng S, Yang L, Xu C, Qin Z, Xu H, Wang Y, Sun L, Liu W (2011) Recombinant chicken interferon-alpha inhibits H9N2 avian influenza virus replication in vivo by oral administration. J Interferon Cytokine Res 31:533–538
doi: 10.1089/jir.2010.0123
Meurens F, Berri M, Whale J, Dybvig T, Strom S, Thompson D, Brownlie R, Townsend HG, Salmon H, Gerdts V (2006) Expression of TECK/CCL25 and MEC/CCL28 chemokines and their respective receptors CCR9 and CCR10 in porcine mucosal tissues. Vet Immunol Immunopathol 113:313–327
doi: 10.1016/j.vetimm.2006.05.014
Myers KP, Olsen CW, Gray GC (2007) Cases of swine influenza in humans: a review of the literature. Clin Infect Dis 44:1084–1088
doi: 10.1086/512813
Namangala B, Inoue N, Kohara J, Kuboki N, Sakurai T, Hayashida K, Sugimoto C (2006) Evidence for the immunostimulatory effects of low-dose orally delivered human IFN-alpha in cattle. J Interferon Cytokine Res 26:675–681
doi: 10.1089/jir.2006.26.675
Ogawa H, Taira O, Hirai T, Takeuchi H, Nagao A, Ishikawa Y, Tuchiya K, Nunoya T, Ueda S (2009) Multiplex PCR and multiplex RT-PCR for inclusive detection of major swine DNA and RNA viruses in pigs with multiple infections. J Virol Methods 160:210–214
doi: 10.1016/j.jviromet.2009.05.010
O'Keefe GM, Nguyen VT, Benveniste EN (1999) Class Ⅱ transac-tivator and class Ⅱ MHC gene expression in microglia: modulation by the cytokines TGF-beta, IL-4, IL-13 and IL-10. Eur J Immunol 29:1275–1285
doi: 10.1002/(ISSN)1521-4141
Proietti E, Bracci L, Puzelli S, Di Pucchio T, Sestili P, De Vincenzi E, Venditti M, Capone I, Seif I, De Maeyer E, Tough D, Donatelli I, Belardelli F (2002) Type Ⅰ IFN as a natural adjuvant for a protective immune response: lessons from the influenza vaccine model. J Immunol 169:375–383
doi: 10.4049/jimmunol.169.1.375
Qu H, Yang L, Meng S, Xu L, Bi Y, Jia X, Li J, Sun L, Liu W (2013) The differential antiviral activities of chicken interferon alpha (ChIFN-alpha) and ChIFN-beta are related to distinct interferon-stimulated gene expression. PLoS ONE 8:e59307
doi: 10.1371/journal.pone.0059307
Rabinowich H, Sedlmayr P, Herberman RB, Whiteside TL (1993) Response of human NK cells to IL-6 alterations of the cell surface phenotype, adhesion to fibronectin and laminin, and tumor necrosis factor-alpha/beta secretion. J Immunol 150:4844–4855
Radvanyi LG, Banerjee A, Weir M, Messner H (1999) Low levels of interferon-alpha induce CD86 (B7.2) expression and accelerates dendritic cell maturation from human peripheral blood mononuclear cells. Scand J Immunol 50:499–509
doi: 10.1046/j.1365-3083.1999.00625.x
Rajao DS, Anderson TK, Gauger PC, Vincent AL (2014) Pathogenesis and vaccination of influenza A virus in swine. Curr Top Microbiol Immunol 385:307–326
Santini SM, Lapenta C, Logozzi M, Parlato S, Spada M, Di Pucchio T, Belardelli F (2000) Type Ⅰ interferon as a powerful adjuvant for monocyte-derived dendritic cell development and activity in vitro and in Hu-PBL-SCID mice. J Exp Med 191:1777–1788
doi: 10.1084/jem.191.10.1777
Scholtissek C, Burger H, Kistner O, Shortridge KF (1985) The nucleoprotein as a possible major factor in determining host specificity of influenza H3N2 viruses. Virology 147:287–294
doi: 10.1016/0042-6822(85)90131-X
Sommereyns C, Paul S, Staeheli P, Michiels T (2008) IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog 4:e1000017
doi: 10.1371/journal.ppat.1000017
Striz I, Brabcova E, Kolesar L, Sekerkova A (2014) Cytokine networking of innate immunity cells: a potential target of therapy. Clin Sci (Lond) 126:593–612
doi: 10.1042/CS20130497
Tormo AJ, Letellier MC, Sharma M, Elson G, Crabe S, Gauchat JF (2012) IL-6 activates STAT5 in T cells. Cytokine 60:575–582
doi: 10.1016/j.cyto.2012.07.002
Tovey MG (2002) Oromucosal cytokine therapy: mechanism(s) of action. Taehan Kan Hakhoe Chi 8:125–131
Tovey MG, Lallemand C, Thyphronitis G (2008) Adjuvant activity of type Ⅰ interferons. Biol Chem 389:541–545
Veckman V, Osterlund P, Fagerlund R, Melen K, Matikainen S, Julkunen I (2006) TNF-alpha and IFN-alpha enhance influenza-A-virus-induced chemokine gene expression in human A549 lung epithelial cells. Virology 345:96–104
doi: 10.1016/j.virol.2005.09.043
Yoo JK, Baker DP, Fish EN (2010) Interferon-beta modulates type 1 immunity during influenza virus infection. Antivir Res 88:64–71
doi: 10.1016/j.antiviral.2010.07.006
Zaballos A, Gutierrez J, Varona R, Ardavin C, Marquez G (1999) Cutting edge: identification of the orphan chemokine receptor GPR-9-6 as CCR9, the receptor for the chemokine TECK. J Immunol 162:5671–5675
Zhou JH, Wang YN, Chang QY, Ma P, Hu Y, Cao X (2018) Type Ⅲ interferons in viral infection and antiviral immunity. Cell Physiol Biochem 51:173–185
doi: 10.1159/000495172
Abstract: Interferon, a natural protein that is produced by a variety of cells during viral infection, activates the transcription of multiple functional genes in cells, regulates synergy among various signaling pathways, and mediates many biological functions such as antiviral activity, immune regulation, and cell growth. However, clinical research on interferon in livestock is lacking. In this study, recombinant porcine interferon (PoIFNα) was used as an adjuvant, in combination with inactivated influenza virus, to vaccinate 6-week-old pigs via nasal infusion. The transcription of target genes was then monitored and the functions of PoIFNα were determined with respect to the activation of mucosal immunity. We found that a combination of low-dose PoIFNα and inactivated influenza virus could significantly up-regulate the expression of immunoregulatory cytokines such as IL-2, IL-18, IFN-γ, IL-6, and IL-10 by real-time PCR, suggesting the induction of a strong mucosal innate immune response after administration. In addition, low-dose PoIFNα can significant enhancing the transcription of genes encoding homing factors including CCR9 and CCR10 (P < 0.001), thereby resulting in the induction of higher levels of HA-specific antibodies (P < 0.05), which can be determined by ELISA and IFA. Post-immunization challenges with H1N1 virus demonstrated that PoIFNα, combined with inactivated influenza virus, could alleviate clinical signs in pigs during the early stages of viral infection. These studies reveal low-dose PoIFNα as a potential mucosal adjuvant for influenza virus in pigs.
Table S1. Immunization program of inactivated H1N1 and PoIFNα in pigs
Table S2. Primer sequences used in this study
Table S3. Antiviral activities of PoIFNα toward different cell lines