Cytokines transcript levels in lung and lymphoid organs during genotype 1 Porcine Reproductive and Respiratory Syndrome Virus (PRRSV) infection

Veterinary Immunology and Immunopathology

Volumn 160, Issue 1-2, 2014, Pages 26-40

  García Nicolás, Obdulio ^a   Quereda, Juan José ^b   Gómez Laguna, Jaime ^c   Salguero, Francisco Javier ^d   Carrasco, Librado ^e   Ramis, Guillermo ^a   Pallarés, Francisco José ^a  

^a UNIVERSITY OF MURCIA   (Spain)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^c CICAP Agrifood Research Center   (Spain)

^d UNIVERSITY OF SURREY   (United Kingdom)

^e UNIVERSITY OF CÓRDOBA   (Spain)

Author keywords

Cytokines; Immune response; PRRSV; Transcript levels

Indexed keywords

ALPHA INTERFERON; BETA ACTIN; CYCLOPHILIN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P35; INTERLEUKIN 12P40; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENOTYPE; IMMUNE RESPONSE; INNATE IMMUNITY; LUNG LESION; LUNG PARENCHYMA; LYMPH NODE; LYMPHOID ORGAN; NONHUMAN; PHARYNX; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; RESPIRATORY SYSTEM; RETROPHARYNGEAL LYMPH NODE; SWINE; TARGET ORGAN; TONSIL; TRACHEOBRONCHIAL LYMPH NODE; UPREGULATION; VIRUS INFECTION; VIRUS PATHOGENESIS; VIRUS REPLICATION; ANIMAL; ARTERIVIRUS; GENE EXPRESSION REGULATION; GENETICS; GERMFREE ANIMAL; LUNG; LYMPHOID TISSUE; METABOLISM; PATHOLOGY; VIREMIA; VIROLOGY;

PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUIDAE; SUS;

ANIMALS; CYTOKINES; GENE EXPRESSION REGULATION; LUNG; LYMPHOID TISSUE; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SPECIFIC PATHOGEN-FREE ORGANISMS; SWINE; VIREMIA; VIRUS REPLICATION;

EID: 84901619041     PISSN: 01652427     EISSN: 18732534     Source Type: Journal    
DOI: 10.1016/j.vetimm.2014.03.008     Document Type: Article

References (68)

1. Albina E., Carrat C., Charley B. Interferon-alpha response to swine arterivirus (PoAV), the porcine reproductive and respiratory syndrome virus. J. Interferon. Cytokine. Res. 1998, 18(7):485-490.
2. Barranco I., Gómez-Laguna J., Rodríguez-Gómez I.M., Salguero F.J., Pallarés F.J., Carrasco L. Differential expression of proinflammatory cytokines in the lymphoid organs of porcine reproductive and respiratory syndrome virus-infected pigs. Transbound. Emerg. Dis. 2012, 59(2):145-153.
3. Barranco I., Gómez-Laguna J., Rodríguez-Gómez I.M., Quereda J.J., Salguero F.J., Pallarés F.J., Carrasco L. Immunohistochemical expression of IL-12, IL-10, IFN-α and IFN-γ in lymphoid organs of porcine reproductive and respiratory syndrome virus-infected pigs. Vet. Immunol. Immunopathol. 2012, 149:262-271.
4. Baumann A., Mateu E., Murtaugh M.P., Summerfield A. Impact of genotype 1 and 2 of porcine reproductive and respiratory syndrome viruses on interferon-α responses by plasmacytoid dendritic cells. Vet. Res. 2013, 44:33. 10.1186/1297-9716-44-33.
5. Beura L.K., Sarkar S.N., Kwon B., Subramaniam S., Jones C., Pattnaik A.K., Osorio F.A. Porcine reproductive and respiratory syndrome virus nonstructural protein 1beta modulates host innate immune response by antagonizing IRF3 activation. J. Virol. 2009, 84(3):1574-1584.
6. Brysha M., Zhang J.G., Bertolino P., Corbin J.E., Alexander W.S., Hilton D.J., Starr R. Suppressor of cytokine signaling-1 attenuates the duration of interferon gamma signal transduction in vitro and in vivo. J. Biol. Chem. 2001, 276:22086-22089.
7. Carter Q.L., Curiel R.E. Interleukin-12 (IL-12) ameliorates the effects of porcine respiratory and reproductive syndrome virus (PRRSV) infection. Vet. Immunol. Immunopathol. 2005, 107:105-118.
8. Cho J.G., Dee S.A. Porcine reproductive and respiratory syndrome virus. Theriogenology 2006, 66:655-662.
9. Darwich L., Diaz I., Mateu E. Certainties, doubts and hypotheses in porcine reproductive and respiratory syndrome virus immunobiology. Virus. Res. 2010, 154:123-132.
10. Darwich L., Gimeno M., Sibila M., Diaz I., de la Torre E., Dotti S., Kuzemtseva L., Martin M., Pujols J., Mateu E. Genetic and immunobiological diversities of porcine reproductive and respiratory syndrome genotype I strains?. Vet. Microbiol. 2011, 150(1-2):49-62.
11. Díaz I., Darwich L., Pappaterra G., Pujols J., Mateu E. Different European-type vaccines against porcine reproductive and respiratory syndrome virus have different immunological properties and confer different protection to pigs. Virology 2006, 351:249-259.
12. Díaz I., Gimeno M., Darwich L., Navarro N., Kuzemtseva L., López S., Galindo I., Segalés J., Martín M., Pujols J., Mateu E. Characterization of homologous and heterologous adaptive immune responses in porcine reproductive and respiratory syndrome virus infection. Vet. Res. 2012, 43(1):30. 10.1186/1297-9716-43-30.
13. Ding L., Linsley P.S., Huang L.Y., Germain R.N., Shevach E.M. IL-10inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J. Immunol. 1993, 151:1224-1234.
14. du Manoir J.M., Albright B.N., Stevenson G., Thompson S.H., Mitchell G.B., Clark M.E., Caswell J.L. Variability of neutrophil and pulmonary alveolar macrophage function in swine. Vet. Immunol. Immunopathol. 2002, 89:175-186.
15. Duvigneau J.C., Hartl R.T., Groiss S., Gemeiner M. Quantitative simultaneous multiplex real-time PCR for the detection of porcine cytokines?. J. Immunol. Methods 2005, 306(1-2):16-27.
16. Emmott E., Rodgers M.A., Macdonald A., McCrory S., Ajuh P., Hiscox J.A. Quantitative proteomics using stable isotope labeling with amino acids in cell culture reveals changes in the cytoplasmic, nuclear, and nucleolar proteomes in Vero cells infected with the coronavirus infectious bronchitis virus. Mol. Cell. Proteomics 2010, 9:1920-1936.
17. Gabler N.K., Spencer J.D., Webel D.M., Spurlock M.E. n-3 PUFA attenuate lipopolysaccharide-induced down-regulation of toll-like receptor 4 expression in porcine adipose tissue but does not alter the expression of other immune modulators. J. Nutr. Biochem. 2008, 19:8-15.
18. García-Nicolás O., Baumann A., Vielle N.J., Gómez-Laguna J., Quereda J.J., Pallarés F.J., Ramis G., Carrasco L., Summerfield A. Virulence and genotype-associated infectivity of interferon-treated macrophages by porcine reproductive and respiratory syndrome viruses. Virus. Res. 2014, 179:204-211.
19. Gimeno M., Darwich L., Diaz I., de la Torre E., Pujols J., Martin M., Inumaru S., Cano E., Domingo M., Montoya M., Mateu E. Cytokine profiles and phenotype regulation of antigen presenting cells by genotype-I porcine reproductive and respiratory syndrome virus isolates. Vet. Res. 2011, 42(1):9. 10.1186/1297-9716-42-9.
20. Gómez-Laguna J., et al. Changes in lymphocyte subsets and cytokines during European porcine reproductive and respiratory syndrome: increased expression of IL-12 and IL-10 and proliferation of CD4()CD8(high). Viral. Immunol. 2009, 22:261-271.
21. Gómez-Laguna J., Salguero F.J., Pallares F.J., Fernandez de Marco M., Barranco I., Ceron J.J., Martínez-Subiela S., Van Reeth K., Carrasco L. Acute phase response in porcine reproductive and respiratory syndrome virus infection. Comp. Immunol. Microbiol. Infect. Dis. 2010, 33:51-58.
22. Gómez-Laguna J., Salguero F.J., Barranco I., Pallarés F.J., Rodríguez-Gómez I.M., Bernabé A., Carrasco L. Cytokine expression by macrophages in the lung of pigs infected with the porcine reproductive and respiratory syndrome virus. J. Comp. Pathol. 2010, 142:51-60.
23. Gómez-Laguna J., Salguero F.J., Pallares F.J., Carrasco L. Immunopathogenesis of porcine reproductive and respiratory syndrome in the respiratory tract of pigs. Vet. J. 2013, 195:148-155.
24. Guo B., Lager K.M., Henningson J.N., Miller L.C., Schlink S.N., Kappes M.A., Kehrli M.E., Brockmeier S.L., Nicholson T.L., Yang H.C., Faaberg K.S. Experimental infection of United States swine with a Chinese highly pathogenic strain of porcine reproductive and respiratory syndrome virus. Virology 2013, 435(2):372-384.
25. Graham S.P., Everett H.E., Haines F.J., Johns H.L., Sosan O.A., Salguero F.J., Clifford D.J., Steinbach F., Drew T.W., Crooke H.R. Challenge of pigs with classical swine fever viruses after C-strain vaccination reveals remarkably rapid protection and insights into early immunity. PLoS ONE 2012, 7(1):e29310. 10.1371/journal.pone.0029310.
26. Halbur P.G., Paul P.S., Frey M.L., Landgraf J., Eernisse K., Meng X.J., Lum M.A., Andrews J.J., Rathje J.A. Comparison of the pathogenicity of two US porcine reproductive and respiratory syndrome virus isolates with that of the Lelystad virus. Vet. Pathol. 1995, 32:648-660.
27. Holtkamp D.J., Kliebenstein J.B., Neumann E.J., Zimmerman J.J., Rotto H.F., Yoder T.K., Wang C., Yeske P.E., Mowrer C.L., Haley C.A. Assessment of the economic impact of porcine reproductive and respiratory syndrome virus on United States pork producers. J. Swine. Health. Prod. 2013, 21(2):72-84.
28. Jung K., Renukaradhya G.J., Alekseev K.P., Fang Y., Tang Y., Saif L.J. Porcine reproductive and respiratory syndrome virus modifies innate immunity and alters disease outcome in pigs subsequently infected with porcine respiratory coronavirus: implications for respiratory viral co-infections. J. Gen.Virol. 2009, 90:2713-2723.
29. Kim O., Sun Y., Lai F.W., 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. Virology 2010, 402(2):315-326.
30. Kim.C.J., Kovacs-Nolan J.A., Yang C., Archbold T., Fan M.Z., Mine Y. L-Tryptophan exhibits therapeutic function in a porcine model of dextran sodium sulfate (DSS)-induced colitis. J. Nutr. Biochem. 2010, 21:468-475.
31. Kimman G., Cornelissen L.A., Moormann R.J., Rebel J.M.J., Stockhofe-Zurwieden N. Challenges for porcine reproductive and respiratory syndrome virus (PRRSV). Vaccinology 2009, 27:3704-3718.
32. King, A.M.Q., Adams, J.M., Carstens, E.B., Lefkowitz, E.J. (Eds.), 2012. 9th Report of the International Committee on Taxonomy of Viruses. Elsevier, Academic Press, London, UK, pp. 796-805.
33. Kittawornrat A., Engle M., Panyasing Y., Olsen C., Schwartz K., Rice A., Lizano S., Wang C., Zimmerman J. Kinetics of the porcine reproductive and respiratory syndrome virus (PRRSV) humoral immune response in swine serum and oral fluids collected from individual boars. BMC Vet. Res. 2013, 28(9):61. 10.1186/1746-6148-9-61.
34. Kuzemtseva L., de la Torre E., Martín G., Soldevila F., Ait-Ali T., Mateu E., Darwich L. Regulation of toll-like receptors 3, 7 and 9 in porcine alveolar macrophages by different genotype 1 strains. Vet Immunol Immunopathol 2014, 158:189-198.
35. Lamontagne L., Page C., Larochelle R., Longtin D., Magar R. Polyclonal activation of B cells occurs in lymphoid organs from porcine reproductive and respiratory syndrome virus (PRRSV)-infected pigs. Vet. Immunol. Immunopathol. 2001, 82:165-182.
36. López O.J., Osorio F.A. Role of neutralizing antibodies in PRRSV protective immunity. Vet. Immunol. Immunopathol. 2004, 102(3):155-163.
37. López-Fuertes L., Campos E., Doménech N., Ezquerra A., Castro J.M., Domínguez J., Alonso F. Porcine reproductive and respiratory syndrome (PRRS) virus down-modulates TNF-alpha production in infected macrophages. Virus. Res. 2000, 69:41-46.
38. Lurchachaiwong W., Payungporn S., Srisatidnarakul U., Mungkundar C., Theamboonlers A., Poovorawan Y. Rapid detection and strain identification of porcine reproductive and respiratory syndrome virus (PRRSV) by real-time RT-PCR. Lett. Appl. Microbiol. 2007, 10.1111/j.1472-765X.2007.02259.x.
39. Mateu E., Diaz I. The challenge of PRRS immunology. Vet. J. 2008, 177(3):345-351.
40. Meier W.A., Galeota J., Osorio F.A., Husmann R., Schnitzlein W., Zuckermann F.A. Gradualdevelopmentoftheinterferon-gammaresponseofswinetoporcinereproductiveandrespiratorysyndromevirusinfectionorvaccination. Virology 2003, 309:18-31.
41. Mitchell R.N., Kumar V. Immune diseases. Basic Pathology 2004, 103-164. Elsevier Science, Philadelphia. 7th ed. V. Kumar, R. Cotran, S.L. Robbins (Eds.).
42. Molina R.M., Cha S.H., Chittick W., Lawson S., Murtaugh M.P., Nelson E.A., Christopher-Hennings J., Yoon K.J., Evans R., Rowland R.R. Immune response against porcine reproductive and respiratory syndrome virus during acute and chronic infection. Vet. Immunol. Immunopathol. 2008, 126:283-292.
43. Moue M., Tohno M., Shimazu T., Kido T., Aso H., Saito T., Kitazawa H. Toll-like receptor 4 and cytokine expression involved in functional immune response in an originally established porcine intestinal epitheliocyte cell line. Biochis. Biophy. Acta. 2007, 1780:134-144.
44. Murtaugh M.P., Xiao Z., Zuckermann F. Immunological responses of swine to porcine reproductive and respiratory syndrome virus infection. Viral. Immunol. 2002, 15:533-547.
45. Nan Y., Wang R., Shen M., Faaberg K.S., Samal S.K., Zhang Y.J. Induction of type I interferons by a novel porcine reproductive and respiratory syndrome virus isolate. Virology 2012, 432(2):261-270.
46. Patton J.B., Rowland R.R., Yoo D.W., Chang K.O. Modulation of CD163 receptor expression and replication of porcine reproductive and respiratory syndrome virus in porcine macrophages. Virus. Res. 2009, 140(12):161171.
47. Quereda J.J., Ramis G., Pallarés F.J., Chapat L., Goubier A., Joisel F., Charreyre C., Villar D., Muñoz A. Interleukin-4, interleukin-5, and interleukin-13 gene expression in cultured mononuclear cells from porcine circovirus type 2 - vaccinated pigs after cells were challenged with porcine circovirus type 2 open reading frame 2 antigen. Am. J. Vet. Res. 2013, 74:110-114.
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. Rossow K.D. Porcine reproductive and respiratory syndrome. Vet. Pathol. 1998, 35:1-20.
50. Rodríguez-Gómez I.M., Gómez-Laguna J., Barranco I., Pallares F.J., Ramis G., Salguero F.J., Carrasco L. Downregulation of antigen-presenting cells in tonsil and lymph nodes of porcine reproductive and respiratory syndrome virus-infected pigs. Transbound. Emerg. Dis. 2012, 60(5):425-437.
51. Rodríguez-Gómez I.M., Gómez-Laguna J., Carrasco L. Impact of PRRSV on activation and viability of antigen presenting cells. World J Virol. 2013, 2:146-151.
52. Royaee A.R., Husmann R.J., Dawson H.D., Calzada-Nova G., Schnitzlein W.M., Zuckermann F.A., Lunney J.K. Deciphering the involvement of innate immune factors in the development of the host response to PRRSV vaccination. Vet. Immunol. Immunopathol. 2004, 102:199-216.
53. Sagong M., Lee C. Porcine reproductive and respiratory syndrome virus nucleocapsid protein modulates interferon-β production by inhibiting IRF3 activation in immortalized porcine alveolar macrophages. Arch. Virol. 2011, 156(12):2187-2195.
54. Silva-Campa E., Córdoba L., Fraile L., Flores-Mendoza L., Montoya M., Hernández J. European genotype of porcine reproductive and respiratory syndrome (PRRSV) infects monocyte-derived dendritic cells but not induce Treg cells. Virology 2009, 396:264-271.
55. Skovgaard K., Mortensen S., Boye M., Poulsen K.T., Campbell F.M., Eckersall P.D., Heegaard P.M. Rapid and widely disseminated acute phase protein response after experimental bacterial infection of pigs. Vet. Res. 2009, 40(3):23. 10.1051/vetres/2009006.
56. Subramaniam S., Kwon B., Beura L.K., Kuszynski C.A., Pattnaik A.K., Osorio F.A. Porcine reproductive and respiratory syndrome virus non-structural protein 1 suppresses tumor necrosis factor-alpha promoter activation by inhibiting NF-κB and Sp1. Virology 2010, 10.1016/j.virol.2010.07.016.
57. Suradhat S., Thanawongnuwech R., Poovorawan Y. Upregulation of IL-10 gene expression in porcine peripheral blood mononuclear cells by porcine reproductive and respiratory syndrome virus. J. Gen. Virol. 2003, 84:453-459.
58. Thanawongnuwech R., Thacker B., Halbur P., Thacker E.L. Increased production of proinflammatory cytokines following infection with porcine reproductive and respiratory syndrome virus and Mycoplasma hyopneumoniae. Clin. Diagn. Lab. Immunol. 2004, 11(5):901-908.
59. Trinchieri G. Interleukin-12: a cytokine produced by antigen-presenting cells with immunoregulatory functions in the generation of T-helper cells type 1 and cytotoxic lymphocytes. Blood 1994, 84:400-4027.
60. Trinchieri G., Pflanz S., Kastelein R.A. The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 2003, 19:641-644.
61. Van Breedam W., Delputte P.L., Van Gorp H., Misinzo G., Vanderheijden N., Duan X., Nauwynck H.J. Porcine reproductive and respiratory syndrome virus entry into the porcine macrophage. J. Gen. Virol. 2010, 91:1659-1667.
62. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3(7). (research0034. 1-0034.11).
63. Wang R., Xiao Y., Opriessnig T., Ding Y., Yu Y., Nan Y., Ma Z., Halbur P.G., Zhang Y.J. Enhancing neutralizing antibody production by an interferon-inducing porcine reproductive and respiratory syndrome virus strain. Vaccine 2013, 31(47):5537-5543.
64. Weesendorp E., Morgan S., Stockhofe-Zurwieden N., Popma-De Graaf D., Graham S., Rebel S. Comparative analysis of immune responses following experimental infection of pigs with European porcine reproductive and respiratory syndrome virus strains of differing virulence?. Vet. Microbiol. 2012, 163(1-2):1-12.
65. Wolf S.F., Temple P.A., Kobayashi M., Young D., Dicig M., Lowe L., Dzialo R., Fitz L., Ferenz C., Hewick R.M., et al. Cloning of cDNA for natural killer cell stimulatory factor, a heterodimeric cytokine with multiple biologic effects on T and natural killer cells. J. Immunol. 1991, 146:3074-3081.
66. Xiao Z., Batista L., Dee S., Halbur P., Murtaugh M.P. The level of virus-specific T-cell and macrophage recruitment in porcine reproductive and respiratory syndrome virus infection in pigs is independent of virus load. J. Virol. 2004, 78:5923-5933.
67. Zhou P., Zhai S., Zhou X., Lin P., Jiang T., Xueying H., Jiang Y., Wu B., Zhang Q., Xu X., Li J., Liu B. Molecular characterization of transcriptome-wide interactions between highly pathogenic porcine reproductive and respiratory syndrome virus and porcine alveolar macrophages in vivo. Int. J. Biol. Sci. 2011, 7:947-959.
68. Zuckermann F.A., Garcia E.A., Luque I.D., Christopher-Hennings J., Doster A., Brito M., Osorio F. Assessment of the efficacy of commercial porcine reproductive and respiratory syndrome virus (PRRSV) vaccines based on measurement of serologic response, frequency of gamma-IFN-producing cells and virological parameters of protection upon challenge. Vet. Microbiol. 2007, 123:69-85.