Comparative analysis of cytokine transcript profiles within mediastinal lymph node compartments of pigs after infection with porcine reproductive and respiratory syndrome genotype 1 strains differing in pathogenicity

Veterinary Research

Volumn 46, Issue 1, 2015, Pages

  García Nicolás, Obdulio ^a   Rosales, Rubén S ^b   Pallarés, Francisco J ^a   Risco, David ^c   Quereda, Juan J ^d   Graham, Simon P ^b   Frossard, Jean Pierre ^b   Morgan, Sophie B ^b   Steinbach, Falko ^b,e   Drew, Trevor W ^b   Strickland, Tony S ^b   Salguero, Francisco J ^b,e  

^a UNIVERSITY OF MURCIA   (Spain)

^b VETERINARY LABORATORIES AGENCY   (United Kingdom)

^c UNIVERSITY OF EXTREMADURA   (Spain)

^d CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^e UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; LELYSTAD VIRUS; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SUIDAE; SUS;

CYTOKINE; TRANSCRIPTOME; VIRUS RNA;

ANIMAL; GENETICS; IMMUNOLOGY; LYMPH NODE; MEDIASTINUM; METABOLISM; PATHOGENICITY; PIG; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VETERINARY; VIROLOGY; VIRULENCE;

ANIMALS; CYTOKINES; LYMPH NODES; MEDIASTINUM; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; SWINE; TRANSCRIPTOME; VIRULENCE;

EID: 84925270998     PISSN: 09284249     EISSN: 12979716     Source Type: Journal    
DOI: 10.1186/s13567-015-0161-8     Document Type: Article

References (63)

1. Hopper SA, White ME, Twiddy N (1992) An outbreak of blue-eared pig disease porcine reproductive and respiratory syndrome in four pig herds in Great Britain. Vet Rec 131:140-144
2. Done SH, Paton DJ (1995) Porcine reproductive and respiratory syndrome: clinical disease, pathology and immunosuppression. Vet Rec 136:32-35
3. Rossow KD (1998) Porcine reproductive and respiratory syndrome. Vet Pathol 35:1-20
4. Zimmerman JJ, Benfield DA, Murtaugh MP, Osorio F, Stenvenson GW, Torremorell M (2006) Porcine reproductive and respiratory syndrome virus (porcine arterivirus). InStraw BE, Zimmerman JJ, D'Allaire S, Taylor DJ (eds) Ames, Iowa5. Holtkamp DJ, Kliebenstein JB, Neumann EJ, Zimmerman JJ, Rotto HF, Yoder TK, Wang C, Yeske PE, Mowrer CL, Haley CA (2013) Assessment of the economic impact of porcine reproductive and respiratory syndrome virus on United States pork producers. J Swine Health Prod 21:72-84
5. Holtkamp DJ, Kliebenstein JB, Neumann EJ, Zimmerman JJ, Rotto HF, Yoder TK, Wang C, Yeske PE, Mowrer CL, Haley CA (2013) Assessment of the economic impact of porcine reproductive and respiratory syndrome virus on United States pork producers. J Swine Health Prod 21:72-84
6. Nelsen CJ, Murtaugh MP, Faaberg KS (1999) Porcine reproductive and respiratory syndrome virus comparison: divergent evolution on two continents. J Virol 73:270-280
7. Stadejek T, Oleksiewicz MB, Scherbakov AV, Timina AM, Krabbe JS, Chabros K, Potapchuk D (2008) Definition of subtypes in the European genotype of porcine reproductive and respiratory syndrome virus: nucleocapsid characteristics and geographical distribution in Europe. Arch Virol 153:1479-1488
8. Stadejek T, Stankevicius A, Murtaugh MP, Oleksiewicz MB (2013) Molecular evolution of PRRSV in Europe: current state of play. Vet Microbiol 165:21-28
9. Karniychuk UU, Geldhof M, Vanhee M, Van Doorsselaere J, Saveleva TA, Nauwynck HJ (2010) Pathogenesis and antigenic characterization of a new East European subtype 3 porcine reproductive and respiratory syndrome virus isolate. BMC Vet Res 6:30
10. Morgan SB, Graham SP, Salguero FJ, Sánchez-Cordón PJ, Mokhtar H, Rebel JM, Weesendorp E, Bodman-Smith KB, Steinbach F, Frossard JP (2013) Increased pathogenicity of European porcine reproductive and respiratory syndrome virus is associated with enhanced adaptive responses and viral clearance. Vet Microbiol 163:13-22
11. Weesendorp E, Morgan S, Stockhofe-Zurwieden N, Popma-De Graaf DJ, Graham SP, Rebel JM (2013) Comparative analysis of immune responses following experimental infection of pigs with European porcine reproductive and respiratory syndrome virus strains of differing virulence. Vet Microbiol 163:1-12
12. Lee YJ, Park CK, Nam E, Kim SH, Lee OS, du Lee S, Lee C (2009) Generation of a porcine alveolar macrophage cell line for the growth of porcine reproductive and respiratory syndrome virus. J Virol Methods 163:410-415
13. Van Gorp H, Van Breedam W, Delputte PL, Nauwynck HJ (2008) Sialoadhesin and CD163 join forces during entry of the porcine reproductive and respiratory syndrome virus. J Gen Virol 89:2943-2953
14. Albina E, Carrat C, Charley B (1998) Interferon-alpha response to swine arterivirus (PoAV), the porcine reproductive and respiratory syndrome virus. J Interferon Cytokine Res 18:485-490
15. Meier WA, Galeota J, Osorio FA, Husmann RJ, Schnitzlein WM, Zuckermann FA (2003) Gradual development of the interferon-gamma response of swine to porcine reproductive and respiratory syndrome virus infection or vaccination. Virology 309:18-31
16. Mateu E, Diaz I (2008) The challenge of PRRS immunology. Vet J 177:345-351
17. Lopez OJ, Osorio FA (2004) Role of neutralizing antibodies in PRRSV protective immunity. Vet Immunol Immunopathol 102:155-163
18. Xiao Z, Batista L, Dee S, Halbur P, Murtaugh MP (2004) 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 78:5923-5933
19. Barranco I, Gómez-Laguna J, Rodríguez-Gómez IM, Quereda JJ, Salguero FJ, Pallarés FJ, Carrasco L (2012) 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 149:262-271
20. Gómez-Laguna J, Salguero FJ, Barranco I, Pallarés FJ, Rodríguez-Gómez IM, Bernabé A, Carrasco L (2010) Cytokine expression by macrophages in the lung of pigs infected with the porcine reproductive and respiratory syndrome virus. J Comp Pathol 142:51-60
21. Binns RM, Pabst, (1994) Lymphoid tissue structure and lymphocyte trafficking in the pig. Vet Immunol Immunopathol 43:79-87
22. Rezk SA, Nathwani BN, Zhao X, Weiss LM (2013) Follicular dendritic cells: origin, function, and different disease-associated patterns. Hum Pathol 44:937-950
23. Lin CM, Jeng CR, Hsiao SH, Liu JP, Chang CC, Chiou MT, Tsai YC, Chia MY, Pang VF (2011) Immunopathological characterization of porcine circovirus type 2 infection-associated follicular changes in inguinal lymph nodes using high-throughput tissue microarray. Vet Microbiol 149:72-84
24. Mendrick DL (2011) Transcriptional profiling to identify biomarkers of disease and drug response. Pharmacogenomics 12:235-249
25. Lunney JK, Fritz ER, Reecy JM, Kuhar D, Prucnal E, Molina R, Christopher-Hennings J, Zimmerman J, Rowland RR (2010) Interleukin-8, interleukin-1beta, and interferon-gamma levels are linked to PRRS virus clearance. Viral Immunol 23:127-134
26. Miller LC, Fleming D, Arbogast A, Bayles DO, Guo B, Lager KM, Henningson JN, Schlink SN, Yang HC, Faaberg KS, Kehrli ME, Jr (2012) Analysis of the swine tracheobronchial lymphnode transcriptomic response to infection with a Chinese highly pathogenic strain of porcine reproductive and respiratory syndrome virus. BMC Vet Res 8:208
27. Wysocki M, Chen H, Steibel JP, Kuhar D, Petry D, Bates J, Johnson R, Ernst CW, Lunney JK (2012) Identifying putative candidate genes and pathways involved in immune responses to porcine reproductive and respiratory syndrome virus (PRRSV) infection. Anim Genet 43:328-332
28. García-Nicolás O, Quereda JJ, Gómez-Laguna J, Salguero FJ, Carrasco L, Ramis G, Pallarés FJ (2014) Cytokines transcript levels in lung and lymphoid organs during genotype 1 Porcine Reproductive and Respiratory Syndrome Virus (PRRSV) infection. Vet Immunol Immunopathol 160:26-40
29. Okuducu AF, Hahne JC, Von Deimling A, Wernert N (2005) Laser-assisted microdissection, techniques and applications in pathology (review). Int J Mol Med 15:763-769
30. Aranday-Cortes E, Bull NC, Villarreal-Ramos B, Gough J, Hicks D, Ortiz-Peláez A, Vordermeier HM, Salguero FJ (2013) Upregulation of IL-17A, CXCL9 and CXCL10 in early-stage granulomas induced by Mycobacterium bovis in cattle. Transbound Emerg Dis 60:525-537
31. Cheng L, Zhang S, MacLennan GT, Williamson SR, Davidson DD, Wang M, Jones TD, Lopez-Beltran A, Montironi R (2013) Laser-assisted microdissection in translational research: theory, technical considerations, and future applications. Appl Immunohistochem Mol Morphol 21:31-47
32. Halbur PG, Paul PS, Frey ML, Landgraf J, Eernisse K, Meng XJ, Andrews JJ, Lum MA, Rathje JA (1996) Comparison of the antigen distribution of two US porcine reproductive and respiratory syndrome virus isolates with that of the Lelystad virus. Vet Pathol 33:159-170
33. Irving JA, Cain G, Parr A, Howard M, Angus B, Cattan AR (1996) OCT embedded sections of pathological specimens as a source of high quality RNA for reverse transcriptase/polymerase chain reaction. J Clin Pathol 49:258-259
34. Barranco I, Gómez-Laguna J, Rodríguez-Gómez IM, Salguero FJ, Pallarés FJ, Bernabé A, Carrasco L (2011) Immunohistochemical detection of extrinsic and intrinsic mediators of apoptosis in porcine paraffin-embedded tissues. Vet Immunol Immunopathol 139:210-216
35. Frossard JP, Fearnley C, Naidu B, Errington J, Westcott DG, Drew TW (2012) Porcine reproductive and respiratory syndrome virus: antigenic and molecular diversity of British isolates and implications for diagnosis. Vet Microbiol 158:308-315
36. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta DeltaC(T)). Methods 25:402-408
37. Delgado-Ortega M, Melo S, Meurens F (2011) Expression of SOCS1-7 and CIS mRNA in porcine tissues. Vet Immunol Immunopathol 144:493-498
38. Jones M, Cordell JL, Beyers AD, Tse AG, Mason DY (1993) Detection of T and B cells in many animal species using cross-reactive anti-peptide antibodies. J Immunol 150:5429-5435
39. Batista L, Pijoan C, Dee S, Olin M, Molitor T, Joo HJ, Xiao Z, Murtaugh M (2004) Virological and immunological responses to porcine reproductive and respiratory syndrome virus in a large population of gilts. Can J Vet Res 68:267-273
40. Mason DY, Cordell JL, Brown MH, Borst J, Jones M, Pulford K, Jaffe E, Ralfkiaer E, Dallenbach F, Stein H, Pileri S, Gatter KC (1995) CD79a: a novel marker for B-cell neoplasms in routinely processed tissue samples. Blood 86:1453-1459
41. Marquet F, Bonneau M, Pascale F, Urien C, Kang C, Schwartz-Cornil I, Bertho N (2011) Characterization of dendritic cells subpopulations in skin and afferent lymph in the swine model. PLoS One 6:e16320
42. Soulas C, Conerly C, Kim WK, Burdo TH, Alvarez X, Lackner AA, Williams KC (2011) Recently infiltrating MAC387(+) monocytes/macrophages a third macrophage population involved in SIV and HIV encephalitic lesion formation. Am J Pathol 178:2121-2135
43. Morgan SB, Frossard JP, Pallares FJ, Gough J, Stadejek T, Graham SP, Steinbach F, Drew TW, Salguero FJ Pathology and virus distribution in the lung and lymphoid tissues of pigs experimentally inoculated with three distinct Type 1 PRRS virus isolates of varying pathogenicity. Transbound Emerg Dis, in press
44. He Y, Wang G, Liu Y, Shi W, Han Z, Wu J, Jiang C, Wang S, Hu S, Wen H, Dong J, Liu H, Cai X (2012) Characterization of thymus atrophy in piglets infected with highly pathogenic porcine reproductive and respiratory syndrome virus. Vet Microbiol 160:455-462
45. Gómez-Laguna J, Salguero FJ, Fernández de Marco M, Barranco I, Rodríguez-Gómez IM, Quezada M, Carrasco L (2013) Type 2 Porcine Reproductive and Respiratory Syndrome Virus infection mediated apoptosis in B- and T-cell areas in lymphoid organs of experimentally infected pigs. Transbound Emerg Dis 60:273-278
46. Rodríguez-Gómez IM, Barranco I, Amarilla SP, García-Nicolás O, Salguero FJ, Carrasco L, Gómez-Laguna J (2014) Activation of extrinsic- and Daxx-mediated pathways in lymphoid tissue of PRRSV-infected pigs. Vet Microbiol 172:186-194
47. Overend C, Mitchell R, He D, Rompato G, Grubman MJ, Garmendia AE (2007) Recombinant swine beta interferon protects swine alveolar macrophages and MARC-145 cells from infection with Porcine reproductive and respiratory syndrome virus. J Gen Virol 88:925-931
48. Sadler AJ, Williams BR (2008) Interferon-inducible antiviral effectors. Nat Rev Immunol 8:559-568
49. Labarque GG, Nauwynck HJ, Van Reeth K, Pensaert MB (2000) Effect of cellular changes and onset of humoral immunity on the replication of porcine reproductive and respiratory syndrome virus in the lungs of pigs. J Gen Virol 81:1327-1334
50. 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. Vet Res 34:249-260
51. Subramaniam S, Kwon B, Beura LK, Kuszynski CA, Pattnaik AK, Osorio FA (2010) Porcine reproductive and respiratory syndrome virus non-structural protein 1 suppresses tumor necrosis factor-alpha promoter activation by inhibiting NF-κB and Sp1. Virology 406:270-279
52. Murtaugh MP, Xiao Z, Zuckermann F (2002) Immunological responses of swine to porcine reproductive and respiratory syndrome virus infection. Viral Immunol 15:533-547
53. Zuckermann FA, Garcia EA, Luque ID, Christopher-Hennings J, Doster A, Brito M, Osorio F (2007) 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 123:69-85
54. Jung K, Renukaradhya GJ, Alekseev KP, Fang Y, Tang Y, Saif LJ (2009) 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 90:2713-2723
55. Dalpke A, Heeg K, Bartz H, Baetz A (2008) Regulation of innate immunity by suppressor of cytokine signaling (SOCS) proteins. Immunobiology 213:225-235
56. Alexander WS (2002) Suppressors of Cytokine Signalling (SOCS) in the immune system. Nat Rev Immunol 2:410-416
57. Royaee AR, Husmann RJ, Dawson HD, Calzada-Nova G, Schnitzlein WM, Zuckermann FA, Lunney JK (2004) Deciphering the involvement of innate immune factors in the development of the host response to PRRSV vaccination. Vet Immunol Immunopathol 102:199-216
58. Zhou P, Zhai S, Zhou X, Lin P, Jiang T, Hu X, Jiang Y, Wu B, Zhang Q, Xu X, Li JP, Liu B (2007) 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 7:947-959
59. Vignali DA, Kuchroo VK (2012) IL-12 family cytokines: immunological playmakers. Nat Immunol 13:722-728
60. Cooper AM, Khader SA (2007) IL-12p40: an inherently agonistic cytokine. Trends Immunol 28:33-38
61. Shimizu J, Kaneko F, Suzuki N (2013) Skewed helper T-Cell responses to IL-12 ramily cytokines produced by antigen-presenting cells and the genetic background in Behcet's Disease. Genet Res Int 2013:363859
62. Gimeno M, Darwich L, Diaz I, de la Torre E, Pujols J, Martin M, Inumaru S, Cano E, Domingo M, Montoya M, Mateu E (2011) Cytokine profiles and phenotype regulation of antigen presenting cells by genotype-I porcine reproductive and respiratory syndrome virus isolates. Vet Res 42:9
63. Silva-Campa E, Córdoba L, Fraile L, Flores-Mendoza L, Montoya M, Hernández J (2009) European genotype of porcine reproductive and respiratory síndrome (PRRSV) infects monocyte-derived dendritic cells but not induce Treg cells. Virology 396:264-271