The emergence of virulent strains of porcine reproductive and respiratory syndrome virus (PRRSV), causing atypical and severe outbreaks, has been notified worldwide. This study assesses the expression, distribution and kinetics of PRRSV N-protein, CD163 and CD107a in the lung and tonsil from experimentally-infected piglets with three different PRRSV-1 strains: a virulent PRRSV-1 subtype 3 strain (SU1-bel) and two low-virulent subtype 1 strains, Lelystad virus (LV) and 215–06. SU1-bel replicated more efficiently in the lungs and tonsils. The number of CD163+ cells decreased in both tissues from all infected groups at 7 dpi, followed by an increase at the end of the study, highlighting a negative correlation with the number of N-protein+-infected cells. A significant increase in CD107a was observed in all infected groups at 35 dpi but no differences were observed among them. Whereas the initial decrease of CD163+ cells appears to be associated to virus replication and cell death, the later recovery of the CD163+ population may be due to either the induction of CD163 in immature cells, the recruitment of CD163+ cells in the area of infection, or both. These results highlight the ability of macrophage subpopulations in infected animals to recover and restore their potential biological functions at one-month post-infection, with the greatest improvement observed in SU1-bel-infected animals.
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Álvarez B, Martínez P, Yuste M, Poderoso T, Alonso F, Domínguez J, Revilla C (2014) Phenotypic and functional heterogeneity of CD169+ and CD163+ macrophages from porcine lymph nodes and spleen. Dev Comp Immunol 44(1):44–49. https://doi.org/10.1016/j.dci.2013.11.010
Amarilla SP, Gómez-Laguna J, Carrasco L, Rodríguez-Gómez IM, Ocerín JMC, Morgan SB, Salguero FJ (2015) 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. Vet Immunol Immunopathol 164(3–4):137–147. https://doi.org/10.1016/j.vetimm.2015.02.003
Bullido R, Moral MG, Alonso F, Ezquerra A, Zapata A, Sanchez C, Dominguez J (1997) Monoclonal antibodies specific for porcine monocytes/macrophages: macrophage heterogeneity in the pig evidenced by the expression of surface antigens. Tissue Antigens 49(4):403–413. https://doi.org/10.1111/j.1399-0039.1997.tb02769.x
Burkard C, Lillico SG, Reid E, Jackson B, Mileham AJ, Ait-Ali T, Archibald AL (2017) Precision engineering for PRRSV resistance in pigs: macrophages from genome edited pigs lacking CD163 SRCR5 domain are fully resistant to both PRRSV genotypes while maintaining biological function. PLoS Pathog 13(2):e1006206. https://doi.org/10.1371/journal.ppat.1006206
Canelli E, Catella A, Borghetti P, Ferrari L, Ogno G, De Angelis E, Bonilauri P (2017) Phenotypic characterization of a highly pathogenic Italian porcine reproductive and respiratory syndrome virus (PRRSV) type 1 subtype 1 isolate in experimentally infected pigs. Vet Microbiol 210:124–133. https://doi.org/10.1016/j.vetmic.2017.09.002
Cao J, Grauwet K, Vermeulen B, Devriendt B, Jiang P, Favoreel H, Nauwynck H (2013) Suppression of NK cell-mediated cytotoxicity against PRRSV-infected porcine alveolar macrophages in vitro. Vet Microbiol 164(3–4):261–269. https://doi.org/10.1016/j.vetmic.2013.03.001
Domenech N, Rodrı́guez-Carreño MP, Filgueira P, Alvarez B, Chamorro S, Domı́nguez J (2003) Identification of porcine macrophages with monoclonal antibodies in formalin-fixed, paraffin-embedded tissues. Vet Immunol Immunopathol 94(1–2):77–81. https://doi.org/10.1016/S0165-2427(03)00084-9
Duan X, Nauwynck HJ, Pensaert MB (1997) Virus quantification and identification of cellular targets in the lungs and lymphoid tissues of pigs at different time intervals after inoculation with porcine reproductive and respiratory syndrome virus (PRRSV). Vet Microbiol 56(1–2):9–19. https://doi.org/10.1016/S0378-1135(96)01347-8
Eskelinen EL (2006) Roles of LAMP-1 and LAMP-2 in lysosome biogenesis and autophagy. Mol Asp Med 27(5–6):495–502. https://doi.org/10.1016/j.mam.2006.08.005
Frydas IS, Verbeeck M, Cao J, Nauwynck HJ (2013) Replication characteristics of porcine reproductive and respiratory syndrome virus (PRRSV) European subtype 1 (Lelystad) and subtype 3 (Lena) strains in nasal mucosa and cells of the monocytic lineage: indications for the use of new receptors of PRRSV (Lena). Vet Res 44(1):73. https://doi.org/10.1186/1297-9716-44-73
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(1):51–60. https://doi.org/10.1016/j.jcpa.2009.07.004
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(3):273–278. https://doi.org/10.1111/j.1865-1682.2012.01338.x
Gorbalenya AE, Krupovic M, Siddell S, Varsani A, Kuhn JH (2018). Riboviria: establishing a single taxon that comprises RNA viruses at the basal rank of virus taxonomy. Retrieved 6 April 2019, from International Committee on Taxonomy of Viruses (ICTV) website: https://talk.ictvonline.org/taxonomy/p/taxonomy-history?taxnode_id=20186087
Han J, Wang Y, Faaberg KS (2006) Complete genome analysis of RFLP 184 isolates of porcine reproductive and respiratory syndrome virus. Virus Res 122(1–2):175–182. https://doi.org/10.1016/j.virusres.2006.06.003
Hu SP, Zhang Z, Liu YG, Tian ZJ, Wu DL, Cai XH, He XJ (2013) Pathogenicity and distribution of highly pathogenic porcine reproductive and respiratory syndrome virus in pigs. Transbound Emerg Dis 60(4):351–359. https://doi.org/10.1111/j.1865-1682.2012.01354.x
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(1):30. https://doi.org/10.1186/1746-6148-6-30
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(3):249–260. https://doi.org/10.1051/vetres:2003001
Min BK, Suk K, Lee WH (2013) Stimulation of CD107 affects LPS-induced cytokine secretion and cellular adhesion through the ERK signaling pathway in the human macrophage-like cell line, THP-1. Cell Immunol 281(2):122–128. https://doi.org/10.1016/j.cellimm.2013.02.003
Morgan SB, Graham SP, Salguero FJ, Cordon PS, Mokhtar H, Rebel JMJ, 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(1–2):13–22. https://doi.org/10.1016/j.vetmic.2012.11.024
Morgan SB, Frossard JP, Pallares FJ, Gough J, Stadejek T, Graham SP, Salguero FJ (2016) 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 63(3):285–295. https://doi.org/10.1111/tbed.12272
Nieuwenhuis N, Duinhof TF, Van Nes A (2012) Economic analysis of outbreaks of porcine reproductive and respiratory syndrome virus in nine sow herds. Vet Rec 170(9):225. https://doi.org/10.1136/vr.100101
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(1–2):186–194. https://doi.org/10.1016/j.vetmic.2014.05.025
Sánchez C, Doménech N, Vázquez J, Alonso F, Ezquerra A, Domínguez J (1999) The porcine 2A10 antigen is homologous to human CD163 and related to macrophage differentiation. J Immunol 162(9):5230–5237. https://doi.org/10.1016/s0165-2427(96)05728-5
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(12):2943–2953. https://doi.org/10.1099/vir.0.2008/005009-0
Wang G, He Y, Tu Y, Liu Y, Zhou EM, Han Z, Cai X (2014) Comparative analysis of apoptotic changes in peripheral immune organs and lungs following experimental infection of piglets with highly pathogenic and classical porcine reproductive and respiratory syndrome virus. Virol J 11(1):2. https://doi.org/10.1186/1743-422X-11-2
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(1–2):1–12. https://doi.org/10.1016/j.vetmic.2012.09.013
Weesendorp E, Rebel JM, Popma-De Graaf DJ, Fijten HP, Stockhofe-Zurwieden N (2014) Lung pathogenicity of European genotype 3 strain porcine reproductive and respiratory syndrome virus (PRRSV) differs from that of subtype 1 strains. Vet Microbiol 174(1–2):127–138. https://doi.org/10.1016/j.vetmic.2014.09.010
Xiao S, Mo D, Wang Q, Jia J, Qin L, Yu X, Chen Y (2010) Aberrant host immune response induced by highly virulent PRRSV identified by digital gene expression tag profiling. BMC Genomics 11(1):544. https://doi.org/10.1186/1471-2164-11-544
Authors would like to thank Gema Muñoz for her technical assistance and Simon P. Graham and Sophie B. Morgan for their work in the evaluation of the immunopathogenesis of these infections in the initial studies. J. Gómez-Laguna is supported by a “Ramón y Cajal” contract of the Spanish Ministry of Economy and Competitiveness (RYC-2014-16735). This work was partially supported by the Spanish Ministry of Education and Science (Grants #AGL2009-12438 and #AGL2016-76111-R).
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Sánchez-Carvajal, J.M., Rodríguez-Gómez, I.M., Carrasco, L. et al. Kinetics of the expression of CD163 and CD107a in the lung and tonsil of pigs after infection with PRRSV-1 strains of different virulence. Vet Res Commun 43, 187–195 (2019). https://doi.org/10.1007/s11259-019-09755-x