A comparative study of the local cytokine response in the lungs of pigs experimentally infected with different PRRSV-1 strains: Upregulation of IL-1α in highly pathogenic strain induced lesions

Veterinary Immunology and Immunopathology

Volumn 164, Issue 3-4, 2015, Pages 137-147

  Amarilla, Shyrley P ^a   Gómez Laguna, Jaime ^b   Carrasco, Librado ^a   Rodríguez Gómez, Irene M ^a   Caridad y Ocerín, José M ^c   Morgan, Sophie B ^d   Graham, Simon P ^d   Frossard, Jean Pierre ^d   Drew, Trevor W ^d   Salguero, Francisco J ^d,e  

^a UNIVERSITY OF CÓRDOBA   (Spain)

^b CICAP Agrifood Research Center   (Spain)

^c Department of Statistics   (Spain)

^d VETERINARY LABORATORIES AGENCY   (United Kingdom)

^e UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

Cytokines; Highly pathogenic porcine reproductive and respiratory syndrome (HP PRRSV); IL 1 ; Lung; PRRSV 1 strains

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; LIVE VACCINE; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; VIRUS ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTERIVIRUS; ARTERIVIRUS INFECTION; ARTICLE; AUTOPSY; CIRCOVIRUS; CLINICAL OBSERVATION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; EXPERIMENTAL INFECTION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; LUNG ALVEOLUS MACROPHAGE; LUNG INFECTION; LUNG LESION; MALE; MICROSCOPY; MYCOPLASMA HYOPNEUMONIAE; NONHUMAN; PROTEIN EXPRESSION; SWINE; UPREGULATION; VIRUS IMMUNITY; VIRUS REPLICATION; VIRUS STRAIN; ANIMAL; BIOSYNTHESIS; BLOOD; IMMUNOLOGY; LUNG; PATHOLOGY; PIG; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS;

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

ANIMALS; ANTIGENS, VIRAL; CYTOKINES; INTERLEUKIN-1ALPHA; LUNG; PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME; PORCINE RESPIRATORY AND REPRODUCTIVE SYNDROME VIRUS; SWINE; UP-REGULATION;

EID: 84926416488     PISSN: 01652427     EISSN: 18732534     Source Type: Journal    
DOI: 10.1016/j.vetimm.2015.02.003     Document Type: Article

References (43)

1. Barranco I., Gomez-Laguna J., Rodriguez-Gomez I.M., Quereda J.J., Salguero F.J., Pallares F.J., Carrasco L. Immunohistochemical expression of IL-12, IL-10, IFN-alpha and IFN-gamma in lymphoid organs of porcine reproductive and respiratory syndrome virus-infected pigs. Vet. Immunol. Immunopathol. 2012, 149:262-271.
2. Barranco I., Gomez-Laguna J., Rodriguez-Gomez I.M., Salguero F.J., Pallares 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, 59:145-153.
3. Charerntantanakul W. Porcine reproductive and respiratory syndrome virus vaccines: immunogenicity, efficacy and safety aspects. World J. Virol. 2012, 1:23-30.
4. Choi C., Cho W.S., Kim B., Chae C. Expression of interferon-gamma and tumour necrosis factor-alpha in pigs experimentally infected with porcine reproductive and respiratory syndrome virus (PRRSV). J. Comp. Pathol. 2002, 127:106-113.
5. Chung H.K., Chae C. Expression of interleukin-10 and interleukin-12 in piglets experimentally infected with porcine reproductive and respiratory syndrome virus (PRRSV). J. Comp. Pathol. 2003, 129:205-212.
6. Chung H.K., Lee J.H., Kim S.H., Chae C. Expression of interferon-alpha and Mx1 protein in pigs acutely infected with porcine reproductive and respiratory syndrome virus (PRRSV). J. Comp. Pathol. 2004, 130:299-305.
7. Diaz 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.
8. Forsberg R., Storgaard T., Nielsen H.S., Oleksiewicz M.B., Cordioli P., Sala G., Hein J., Botner A. The genetic diversity of European type PRRSV is similar to that of the North American type but is geographically skewed within Europe. Virology 2002, 299:38-47.
9. García-Nicolás O., Baumann A., Vielle N.J., Gomez-Laguna J., Quereda J.J., Pallares F.J., Ramis G., Carrasco L., Summerfiled A. Virulence and genotype-associated infectivity of interferon-treated macrophages by porcine reproductive and respiratory syndrome viruses. Virus Res. 2014, 179:204-211.
10. García-Nicolás O., Quereda J.J., Gómez-Laguna J., Salguero F.J., Carrasco L., Ramis G., Pallarés F.J. Cytokines transcript levels in lung and lymphoid organs during genotype 1 porcine reproductive and respiratory syndrome virus (PRRSV) infection. Vet. Immunol. Immunopathol. 2014, 160:26-40.
11. 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, 42:9.
12. Gomez-Laguna J., Salguero F.J., Barranco I., Pallares F.J., Rodriguez-Gomez I.M., Bernabe 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.
13. Gomez-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.
14. 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, 435:372-384.
15. Guo B., Lager K.M., Schlink S.N., Kehrli M.E., Brockmeier S.L., Miller L.C., Swenson S.L., Faaberg K.S. Chinese and Vietnamese strains of HP-PRRSV cause different pathogenic outcomes in United States high health swine. Virology 2013, 446:238-250.
16. 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.
17. Halbur P.G., Paul P.S., Meng X.J., Lum M.A., Andrews J.J., Rathje J.A. Comparative pathogenicity of nine US porcine reproductive and respiratory syndrome virus (PRRSV) isolates in a five-week-old cesarean-derived, colostrum-deprived pig model. J. Vet. Diagn. Invest. 1996, 8:11-20.
18. Han D., Hu Y., Li L., Tian H., Chen Z., Wang L., Ma H., Yang H., Teng K. Highly pathogenic porcine reproductive and respiratory syndrome virus infection results in acute lung injury of the infected pigs. Vet. Microbiol. 2014, 169:135-146.
19. Han K., Seo H.W., Oh Y., Kang I., Park C., Chae C. Comparison of the virulence of European and North American genotypes of porcine reproductive and respiratory syndrome virus in experimentally infected pigs. Vet. J. 2013, 195:313-318.
20. Han K., Seo H.W., Park C., Oh Y., Kang I., Han H.J., Kim S.H., Chae C. Comparative pathogenicity of three Korean and one Lelystad type 1 porcine reproductive and respiratory syndrome virus (pan-European subtype 1) isolates in experimentally infected pigs. J. Comp. Pathol. 2013, 149:331-340.
21. Haynes J.S., Halbur P.G., Sirinarumitr T., Paul P.S., Meng X.J., Huffman E.L. 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.
22. Johnson W., Roof M., Vaughn E., Christopher-Hennings J., Johnson C.R., Murtaugh M.P. Pathogenic and humoral immune responses to porcine reproductive and respiratory syndrome virus (PRRSV) are related to viral load in acute infection. Vet. Immunol. Immunopathol. 2004, 102:233-247.
23. Karniychuk U.U., Geldhof M., Vanhee M., Van Doorsselaere J., Saveleva T.A., Nauwynck H.J. Pathogenesis and antigenic characterization of a new East European subtype 3 porcine reproductive and respiratory syndrome virus isolate. BMC Vet. Res. 2010, 6:30.
24. Kimura H., Yoshizumi M., Ishii H., Oishi K., Ryo A. Cytokine production and signaling pathways in respiratory virus infection. Front. Microbiol. 2013, 4:276.
25. Liu Y., Shi W., Zhou E., Wang S., Hu S., Cai X., Rong F., Wu J., Xu M., Li L. Dynamic changes in inflammatory cytokines in pigs infected with highly pathogenic porcine reproductive and respiratory syndrome virus. Clin. Vaccine Immunol. 2010, 17:1439-1445.
26. Loving C.L., Brockmeier S.L., Vincent A.L., Lager K.M., Sacco R.E. Differences in clinical disease and immune response of pigs challenged with a high-dose versus low-dose inoculum of porcine reproductive and respiratory syndrome virus. Viral Immunol. 2008, 21:315-325.
27. Martinez-Lobo F.J., Diez-Fuertes F., Segales J., Garcia-Artiga C., Simarro I., Castro J.M., Prieto C. Comparative pathogenicity of type 1 and type 2 isolates of porcine reproductive and respiratory syndrome virus (PRRSV) in a young pig infection model. Vet. Microbiol. 2011, 154:58-68.
28. Meulenberg J.J. PRRSV, the virus. Vet. Res. 2000, 31:11-21.
29. Morgan S.B., Graham S.P., Salguero F.J., Sanchez Cordon P.J., Mokhtar H., Rebel J.M., Weesendorp E., Bodman-Smith K.B., Steinbach F., Frossard J.P. Increased pathogenicity of European porcine reproductive and respiratory syndrome virus is associated with enhanced adaptive responses and viral clearance. Vet. Microbiol. 2013, 163:13-22.
30. Morgan S.B., Frossard J.P., Pallares F.J., Gough J., Stadejek T., Graham S.P., Steinbach F., Drew T.W., Salguero F.J. 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. 2014, 10.1111/tbed.12272.
31. Rodriguez-Gomez I.M., Gomez-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. 2013, 60:425-437.
32. Rodriguez-Gomez I.M., Gomez-Laguna J., Carrasco L. Impact of PRRSV on activation and viability of antigen presenting cells. World J. Virol. 2013, 2:146-151.
33. Salguero F.J., Sanchez-Cordon P.J., Nunez A., Fernandez de Marco M., Gomez-Villamandos J.C. Proinflammatory cytokines induce lymphocyte apoptosis in acute African swine fever infection. J. Comp. Pathol. 2005, 132:289-302.
34. Shang Y., Wang G., Yin S., Tian H., Du P., Wu J., Chen Y., Yang S., Jin Y., Zhang K., Lu Z., Liu X. Pathogenic characteristics of three genotype II porcine reproductive and respiratory syndrome viruses isolated from China. Virol. J. 2013, 10:7.
35. Snijder E.J., Kikkert M., Fang Y. Arterivirus molecular biology and pathogenesis. J. Gen. Virol. 2013, 94:2141-2163.
36. Stadejek T., Oleksiewicz M.B., Scherbakov A.V., Timina A.M., Krabbe J.S., Chabros K., Potapchuk D. Definition of subtypes in the European genotype of porcine reproductive and respiratory syndrome virus: nucleocapsid characteristics and geographical distribution in Europe. Arch. Virol. 2008, 153:1479-1488.
37. 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.
38. Thanawongnuwech R., Rungsipipat A., Disatian S., Saiyasombat R., Napakanaporn S., Halbur P.G. Immunohistochemical staining of IFN-gamma positive cells in porcine reproductive and respiratory syndrome virus-infected lungs. Vet. Immunol. Immunopathol. 2003, 91:73-77.
39. Van Reeth K., Nauwynck H. Proinflammatory cytokines and viral respiratory disease in pigs. Vet. Res. 2000, 31:187-213.
40. Van Reeth K., Van Gucht S., Pensaert M. In vivo studies on cytokine involvement during acute viral respiratory disease of swine: troublesome but rewarding. Vet. Immunol. Immunopathol. 2002, 87:161-168.
41. Wang G., Song T., Yu Y., Liu Y., Shi W., Wang S., Rong F., Dong J., Liu H., Cai X., Zhou E.M. Immune responses in piglets infected with highly pathogenic porcine reproductive and respiratory syndrome virus. Vet. Immunol. Immunopathol. 2011, 142:170-178.
42. Weesendorp E., Morgan S., Stockhofe-Zurwieden N., Popma-De Graaf D.J., Graham S.P., Rebel J.M. Comparative analysis of immune responses following experimental infection of pigs with European porcine reproductive and respiratory syndrome virus strains of differing virulence. Vet. Microbiol. 2013, 163:1-12.
43. Weesendorp E., Rebel J.M., Popma-De Graaf D.J., Fijten H.P., Stockhofe-Zurwieden N. Lung pathogenicity of European genotype 3 strain porcine reproductive and respiratory syndrome virus (PRRSV) differs from that of subtype 1 strains. Vet. Microbiol. 2014, 174:127-138. 10.1016/j.vetmic.