Swine, human or avian influenza viruses differentially activates porcine dendritic cells cytokine profile

Veterinary Immunology and Immunopathology

Volumn 154, Issue 1-2, 2013, Pages 25-35

  Mussá, Tufária ^a   Ballester, Maria ^b   Silva Campa, Erika ^c   Baratelli, Massimiliano ^a   Busquets, Núria ^a   Lecours, Marie Pier ^d   Dominguez, Javier ^e   Amadori, Massimo ^f   Fraile, Lorenzo ^a,g   Hernández, Jesús ^c   Montoya, María ^a,h  

^a CENTRE DE RECERCA EN SANITAT ANIMAL CRESA   (Spain)

^b CSIC   (Spain)

^c Laboratorio de Inmunología   (Mexico)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

^e INIA   (Spain)

^f ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLA LOMBARDIA E DELL EMILIA ROMAGNA   (Italy)

^g UNIVERSITY OF LLEIDA   (Spain)

^h IRTA   (Spain)

Author keywords

Cytokines; Dendritic cells; Influenza virus; Transcription factors

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; I KAPPA B; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 18; MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; AVIAN INFLUENZA VIRUS; CONTROLLED STUDY; DENDRITIC CELL; GENE EXPRESSION; IN VITRO STUDY; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H7N1; INFLUENZA VIRUS A H7N2; NONHUMAN; PANDEMIC INFLUENZA; SWINE; SWINE INFLUENZA VIRUS; VIRUS CELL INTERACTION;

ANIMALS; BONE MARROW CELLS; CYTOKINES; DENDRITIC CELLS; GENE EXPRESSION REGULATION; HUMANS; INFLUENZA A VIRUS; RECEPTORS, CELL SURFACE; SWINE; TRANSCRIPTOME;

AVIAN INFLUENZA VIRUS; ORTHOMYXOVIRIDAE; SUIDAE; SUS; SWINE INFLUENZA VIRUS;

EID: 84879252160     PISSN: 01652427     EISSN: 18732534     Source Type: Journal    
DOI: 10.1016/j.vetimm.2013.04.004     Document Type: Article

References (74)

1. Baltimore D. NF-kappaB is 25. Nat. Immunol. 2011, 12:683-685.
2. Barbe F., Atanasova K., Van Reeth K. Cytokines and acute phase proteins associated with acute swine influenza infection in pigs. Vet. J. 2011, 187:48-53.
3. Barbe F., Saelens X., Braeckmans D., Lefevre F., Reeth K.V. Role of IFN-alpha during the acute stage of a swine influenza virus infection. Res. Vet. Sci. 2009, 88:172-178.
4. Baratelli, M., Córdoba, L., Pérez, L.J., Maldonado, J., Fraile, L., Núñez, J.I., Montoya, M. Genetic characterization of influenza A viruses circulating in pigs in north-east Spain during the period 2006-2007, submitted.
5. Bertran K., Busquets N., Abad F.X., Garcia de la Fuente J., Solanes D., Cordon I., Costa T., Dolz R., Majo N. Highly (H5N1) and low (H7N2) pathogenic avian influenza virus infection in falcons via nasochoanal route and ingestion of experimentally infected prey. PLoS ONE 2012, 7:e32107.
6. Bertran K., Perez-Ramirez E., Busquets N., Dolz R., Ramis A., Darji A., Abad F.X., Valle R., Chaves A., Vergara-Alert J., Barral M., Hofle U., Majo N. Pathogenesis and transmissibility of highly (H7N1) and low (H7N9) pathogenic avian influenza virus infection in red-legged partridge (Alectoris rufa). Vet. Res. 2011, 42:24.
7. Boliar S., Chambers T.M. A new strategy of immune evasion by influenza A virus: inhibition of monocyte differentiation into dendritic cells. Vet. Immunol. Immunopathol. 2010, 136:201-210.
8. Busquets N., Segales J., Cordoba L., Mussa T., Crisci E., Martin-Valls G.E., Simon-Grife M., Perez-Simo M., Perez-Maillo M., Nunez J.I., Abad F.X., Fraile L., Pina S., Majo N., Bensaid A., Domingo M., Montoya M. Experimental infection with H1N1 European swine influenza virus protects pigs from an infection with the 2009 pandemic H1N1 human influenza virus. Vet. Res. 2010, 41:74.
9. Carrasco C.P., Rigden R.C., Schaffner R., Gerber H., Neuhaus V., Inumaru S., Takamatsu H., Bertoni G., McCullough K.C., Summerfield A. Porcine dendritic cells generated in vitro: morphological, phenotypic and functional properties. Immunology 2001, 104:175-184.
10. Cella M., Facchetti F., Lanzavecchia A., Colonna M. Plasmacytoid dendritic cells activated by influenza virus and CD40L drive a potent TH1 polarization. Nat. Immunol. 2000, 1:305-310.
11. Crocker P.R., Varki A. Siglecs, sialic acids and innate immunity. Trends Immunol. 2001, 22:337-342.
12. Chaves A.J., Busquets N., Campos N., Ramis A., Dolz R., Rivas R., Valle R., Abad F.X., Darji A., Majo N. Pathogenesis of highly pathogenic avian influenza A virus (H7N1) infection in chickens inoculated with three different doses. Avian Pathol 2011, 40:163-172.
13. Chaves A.J., Busquets N., Valle R., Rivas R., Vergara-Alert J., Dolz R., Ramis A., Darji A., Majo N. Neuropathogenesis of a highly pathogenic avian influenza virus (H7N1) in experimentally infected chickens. Vet. Res. 2011, 42:106.
14. Davenport F.M., Hennessy A.V., Francis T. Epidemiologic and immunologic significance of age distribution of antibody to antigenic variants of influenza virus. J. Exp. Med. 1953, 98:641-656.
15. De Vleeschauwer A., Van Reeth K. Prior infection of pigs with swine influenza viruses is a barrier to infection with avian influenza viruses. Vet. Microbiol. 2010, 146(3-4):340-345. 10.1016/j.vetmic.2010.05.013.
16. Ehrlich L.C., Hu S., Peterson P.K., Chao C.C. IL-10 down-regulates human microglial IL-8 by inhibition of NF-kappaB activation. Neuroreport 1998, 9:1723-1726.
17. Ellis J., Clark E., Haines D., West K., Krakowka S., Kennedy S., Allan G.M. Porcine circovirus-2 and concurrent infections in the field. Vet. Microbiol. 2004, 98:159-163.
18. Facci M.R., Auray G., Meurens F., Buchanan R., van Kessel J., Gerdts V. Stability of expression of reference genes in porcine peripheral blood mononuclear and dendritic cells. Vet. Immunol. Immunopathol. 2011, 141:11-15.
19. Flory E., Kunz M., Scheller C., Jassoy C., Stauber R., Rapp U.R., Ludwig S. Influenza virus-induced NF-kappaB-dependent gene expression is mediated by overexpression of viral proteins and involves oxidative radicals and activation of IkappaB kinase. J. Biol. Chem. 2000, 275:8307-8314.
20. Freer G., Matteucci D. Influence of dendritic cells on viral pathogenicity. PLoS Pathog 2009, 5:e1000384.
21. Garoufalis E., Kwan I., Lin R., Mustafa A., Pepin N., Roulston A., Lacoste J., Hiscott J. Viral induction of the human beta interferon promoter: modulation of transcription by NF-kappa B/rel proteins and interferon regulatory factors. J. Virol. 1994, 68:4707-4715.
22. Garten R.J., Davis C.T., Russell C.A., Shu B., Lindstrom S., Balish A., Sessions W.M., Xu X., Skepner E., Deyde V., Okomo-Adhiambo M., Gubareva L., Barnes J., Smith C.B., Emery S.L., Hillman M.J., Rivailler P., Smagala J., de Graaf M., Burke D.F., Fouchier R.A., Pappas C., Alpuche-Aranda C.M., Lopez-Gatell H., Olivera H., Lopez I., Myers C.A., Faix D., Blair P.J., Yu C., Keene K.M., Dotson P.D., Boxrud D., Sambol A.R., Abid S.H., St George K., Bannerman T., Moore A.L., Stringer D.J., Blevins P., Demmler-Harrison G.J., Ginsberg M., Kriner P., Waterman S., Smole S., Guevara H.F., Belongia E.A., Clark P.A., Beatrice S.T., Donis R., Katz J., Finelli L., Bridges C.B., Shaw M., Jernigan D.B., Uyeki T.M., Smith D.J., Klimov A.I., Cox N.J. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 2009, 325:197-201.
23. Hale B.G., Albrecht R.A., Garcia-Sastre A. Innate immune evasion strategies of influenza viruses. Future Microbiol 2010, 5:23-41.
24. Hargadon K.M., Zhou H., Albrecht R.A., Dodd H.A., Garcia-Sastre A., Braciale T.J. Major histocompatibility complex class II expression and hemagglutinin subtype influence the infectivity of type A influenza virus for respiratory dendritic cells. J. Virol. 2011, 85:11955-11963.
25. Hay A.J., Gregory V., Douglas A.R., Lin Y.P. The evolution of human influenza viruses. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2001, 356:1861-1870.
26. Inaba K., Metlay J.P., Crowley M.T., Witmer-Pack M., Steinman R.M. Dendritic cells as antigen presenting cells in vivo. Int. Rev. Immunol. 1990, 6:197-206.
27. Ioannidis L.J., Verity E.E., Crawford S., Rockman S.P., Brown L.E. Abortive replication of influenza virus in mouse dendritic cells. J. Virol. 2012, 86:5922-5925.
28. Kawai T., Akira S. Antiviral signaling through pattern recognition receptors. J. Biochem. 2007, 141:137-145.
29. Kawai T., Akira S. Toll-like receptor and RIG-I-like receptor signaling. Ann. N. Y. Acad. Sci. 2008, 1143:1-20.
30. Kekarainen T., Montoya M., Dominguez J., Mateu E., Segales J. Porcine circovirus type 2 (PCV2) viral components immunomodulate recall antigen responses. Vet. Immunol. Immunopathol. 2008, 124:41-49.
31. Kumar N., Xin Z.T., Liang Y., Ly H. NF-kappaB signaling differentially regulates influenza virus RNA synthesis. J. Virol. 2008, 82:9880-9889.
32. Lentsch A.B., Shanley T.P., Sarma V., Ward P.A. In vivo suppression of NF-kappa B and preservation of I kappa B alpha by interleukin-10 and interleukin-13. J. Clin. Invest. 1997, 100:2443-2448.
33. Liu Y.J. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol. 2005, 23:275-306.
34. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
35. Ludwig S., Planz O. Influenza viruses and the NF-kappaB signaling pathway - towards a novel concept of antiviral therapy. Biol. Chem. 2008, 389:1307-1312.
36. Maldonado J., Van Reeth K., Riera P., Sitja M., Saubi N., Espuna E., Artigas C. Evidence of the concurrent circulation of H1N2, H1N1 and H3N2 influenza A viruses in densely populated pig areas in Spain. Vet. J. 2006, 172:377-381.
37. Malmgaard L. Induction and regulation of IFNs during viral infections. J. Interferon Cytokine Res. 2004, 24:439-454.
38. Matikainen S., Siren J., Tissari J., Veckman V., Pirhonen J., Severa M., Sun Q., Lin R., Meri S., Uze G., Hiscott J., Julkunen I. Tumor necrosis factor alpha enhances influenza A virus-induced expression of antiviral cytokines by activating RIG-I gene expression. J. Virol. 2006, 80:3515-3522.
39. McKinstry K.K., Strutt T.M., Buck A., Curtis J.D., Dibble J.P., Huston G., Tighe M., Hamada H., Sell S., Dutton R.W., Swain S.L. IL-10 deficiency unleashes an influenza-specific Th17 response and enhances survival against high-dose challenge. J. Immunol. 2009, 182:7353-7363.
40. Monteiro J.M., Harvey C., Trinchieri G. Role of interleukin-12 in primary influenza virus infection. J. Virol. 1998, 72:4825-4831.
41. Mussa T., Rodriguez-Carino C., Pujol M., Cordoba L., Busquets N., Crisci E., Dominguez J., Fraile L., Montoya M. Interaction of porcine conventional dendritic cells with swine influenza virus. Virology 2011, 420:125-134.
42. Natarajan K., Singh S., Burke T.R., Grunberger D., Aggarwal B.B. Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:9090-9095.
43. Ocana-Macchi M., Ricklin M.E., Python S., Monika G.A., Stech J., Stech O., Summerfield A. Avian influenza A virus PB2 promotes interferon type I inducing properties of a swine strain in porcine dendritic cells. Virology 2012, 427:1-9.
44. OIE, 2010. Manual of diagnostic tests and vaccines for terrestrial animals. http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.08.08_SWINE_INFLUENZA.pdf.
45. Olvera A., Sibila M., Calsamiglia M., Segales J., Domingo M. Comparison of porcine circovirus type 2 load in serum quantified by a real time PCR in postweaning multisystemic wasting syndrome and porcine dermatitis and nephropathy syndrome naturally affected pigs. J. Virol. Methods 2004, 117:75-80.
46. Osterlund P., Pirhonen J., Ikonen N., Ronkko E., Strengell M., Makela S.M., Broman M., Hamming O.J., Hartmann R., Ziegler T., Julkunen I. Pandemic H1N1 2009 influenza A virus induces weak cytokine responses in human macrophages and dendritic cells and is highly sensitive to the antiviral actions of interferons. J. Virol. 2010, 84:1414-1422.
47. Ramos I., Fernandez-Sesma A. Cell receptors for influenza a viruses and the innate immune response. Front Microbiol 2012, 3:117.
48. Randall R.E., Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 2008, 89:1-47.
49. Reed L.J., Muench H. A simple method of estimating fifty per cent endpoint. Am. J. Hyg. 1938, 493-497.
50. Rimmelzwaan G.F., Baars M., Claas E.C., Osterhaus A.D. Comparison of RNA hybridization, hemagglutination assay, titration of infectious virus and immunofluorescence as methods for monitoring influenza virus replication in vitro. J. Virol. Methods 1998, 74:57-66.
51. Rogers G.N., Paulson J.C. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 1983, 127:361-373.
52. Sibila M., Calsamiglia M., Segales J., Blanchard P., Badiella L., Le Dimna M., Jestin A., Domingo M. Use of a polymerase chain reaction assay and an ELISA to monitor porcine circovirus type 2 infection in pigs from farms with and without postweaning multisystemic wasting syndrome. Am. J. Vet. Res. 2004, 65:88-92.
53. Simon-Grife M., Martin-Valls G.E., Vilar M.J., Garcia-Bocanegra I., Mora M., Martin M., Mateu E., Casal J. Seroprevalence and risk factors of swine influenza in Spain. Vet. Microbiol. 2011, 149:56-63.
54. Smale S.T. Hierarchies of NF-kappaB target-gene regulation. Nat. Immunol. 2011, 12:689-694.
55. Smith G.J., Vijaykrishna D., Bahl J., Lycett S.J., Worobey M., Pybus O.G., Ma S.K., Cheung C.L., Raghwani J., Bhatt S., Peiris J.S., Guan Y., Rambaut A. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 2009.
56. Steinman R.M., Hemmi H. Dendritic cells: translating innate to adaptive immunity. Curr. Top. Microbiol. Immunol. 2006, 311:17-58.
57. Summerfield A., Guzylack-Piriou L., Schaub A., Carrasco C.P., Tache V., Charley B., McCullough K.C. Porcine peripheral blood dendritic cells and natural interferon-producing cells. Immunology 2003, 110:440-449.
58. Summerfield A., McCullough K.C. The porcine dendritic cell family. Dev. Comp. Immunol. 2009, 33:299-309.
59. Tamura S., Kurata T. Defense mechanisms against influenza virus infection in the respiratory tract mucosa. Jpn. J. Infect. Dis. 2004, 57:236-247.
60. To K.K., Hung I.F., Li I.W., Lee K.L., Koo C.K., Yan W.W., Liu R., Ho K.Y., Chu K.H., Watt C.L., Luk W.K., Lai K.Y., Chow F.L., Mok T., Buckley T., Chan J.F., Wong S.S., Zheng B., Chen H., Lau C.C., Tse H., Cheng V.C., Chan K.H., Yuen K.Y. Delayed clearance of viral load and marked cytokine activation in severe cases of pandemic H1N1 2009 influenza virus infection. Clin. Infect. Dis. 2010, 50:850-859.
61. van der Sluijs K.F., van Elden L.J., Xiao Y., Arens R., Nijhuis M., Schuurman R., Florquin S., Jansen H.M., Lutter R., van der Poll T. IL-12 deficiency transiently improves viral clearance during the late phase of respiratory tract infection with influenza A virus in mice. Antiviral Res. 2006, 70:75-84.
62. van Eijk M., White M.R., Batenburg J.J., Vaandrager A.B., van Golde L.M., Haagsman H.P., Hartshorn K.L. Interactions of influenza A virus with sialic acids present on porcine surfactant protein D. Am. J. Respir. Cell Mol. Biol. 2004, 30:871-879.
63. Van Poucke S.G., Nicholls J.M., Nauwynck H.J., Van Reeth K. Replication of avian, human and swine influenza viruses in porcine respiratory explants and association with sialic acid distribution. Virol J 2010, 7:38.
64. Van Reeth K. Avian and swine influenza viruses: our current understanding of the zoonotic risk. Vet. Res. 2007, 38:243-260.
65. Van Reeth K., Brown I.H., Durrwald R., Foni E., Labarque G., Lenihan P., Maldonado J., Markowska-Daniel I., Pensaert M., Pospisil Z., Koch G. Seroprevalence of H1N1, H3N2 and H1N2 influenza viruses in pigs in seven European countries in 2002-2003. Influenza Other Respi. Viruses 2008, 2:99-105.
66. Van Reeth K., Gregory V., Hay A., Pensaert M. Protection against a European H1N2 swine influenza virus in pigs previously infected with H1N1 and/or H3N2 subtypes. Vaccine 2003, 21:1375-1381.
67. Van Reeth K., Nauwynck H., Pensaert M. Clinical effects of experimental dual infections with porcine reproductive and respiratory syndrome virus followed by swine influenza virus in conventional and colostrum-deprived pigs. J. Vet. Med. B Infect. Dis. Vet. Public Health 2001, 48:283-292.
68. Varki N.M., Varki A. Diversity in cell surface sialic acid presentations: implications for biology and disease. Lab. Invest. 2007, 87:851-857.
69. Videira P.A., Amado I.F., Crespo H.J., Alguero M.C., Dall'Olio F., Cabral M.G., Trindade H. Surface alpha 2-3- and alpha 2-6-sialylation of human monocytes and derived dendritic cells and its influence on endocytosis. Glycoconj. J. 2008, 25:259-268.
70. Wang J.P., Bowen G.N., Padden C., Cerny A., Finberg R.W., Newburger P.E., Kurt-Jones E.A. Toll-like receptor-mediated activation of neutrophils by influenza A virus. Blood 2008, 112:2028-2034.
71. Wang X., Li M., Zheng H., Muster T., Palese P., Beg A.A., Garcia-Sastre A. Influenza A virus NS1 protein prevents activation of NF-kappaB and induction of alpha/beta interferon. J. Virol. 2000, 74:11566-11573.
72. Webster R.G., Bean W.J., Gorman O.T., Chambers T.M., Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol. Rev. 1992, 56:152-179.
73. Weis W., Brown J.H., Cusack S., Paulson J.C., Skehel J.J., Wiley D.C. Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature 1988, 333:426-431.
74. Wurzer W.J., Ehrhardt C., Pleschka S., Berberich-Siebelt F., Wolff T., Walczak H., Planz O., Ludwig S. NF-kappaB-dependent induction of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) and Fas/FasL is crucial for efficient influenza virus propagation. J. Biol. Chem. 2004, 279:30931-30937.