Monocytes play an essential role in the defense against bacterial pathogens. Bone marrow (BM) and peripheral blood (PB) monocytes in pigs consist of the main "steady-state" subpopulations: CD14 hi/CD163-/SLA-DR- and CD14 low/CD163+/SLA-DR+. During inflammation, the subpopulation of "inflammatory" monocytes expressing very high levels of CD163, but lacking the SLA-DR molecule (being CD14 low/CD163+/SLA-DR-) appears in the BM and PB and replaces the CD14 low/CD163+/SLA-DR+ subpopulation. However, current knowledge of monocyte migration into inflamed tissues in pigs is limited. The aim of the present study was to evaluate the distribution of "inflammatory" CD14 low/CD163+/SLA-DR- monocytes during experimental inflammation induced by Actinobacillus pleuropneumoniae (APP) and a possible role for chemokines in attracting "inflammatory" CD14 low/CD163+/SLA-DR- monocytes into the tissues. Monocyte subpopulations were detected by flow cytometry. Chemokines and chemokine receptors were detected by RT-qPCR. The "steady-state" monocytes were found in the BM, PB, spleen and lungs of control pigs. After APP-infection, "inflammatory" monocytes replaced the "steady-state" subpopulation in BM, PB, spleen and moreover, they appeared in an unaffected area, demarcation zone and necrotic area of the lungs and in tracheobronchial lymph nodes. They did not appear in mesenteric lymph nodes. Levels of mRNA for various chemokines with their appropriate receptors were found to be elevated in BM (CCL3-CCR1/CCR5, CCL8-CCR2/CCR5, CCL19-CCR7), necrotic area of the lungs (CCL3-CCR1, CCL5-CCR1/CCR3, CCL11-CCR3, CCL22/CCR4) and tracheobronchial lymph nodes (CCL3-CCR1) and therefore they could play a role in attracting monocytes into inflamed tissues. In conclusion, "inflammatory" monocytes appear in different lymphoid tissues and the lungs after APP infection in pigs. Various chemokines could drive this process.

Veterinary Research Institute Hudcova 70 Brno 621 00 Czech Republic

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Serbina NV, Jia T, Hohl TM, Pamer EG. Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol. 2008;44:421–452. PubMed PMC

Leon B, Lopez-Bravo M, Ardavin C. Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity. 2007;44:519–531. PubMed

Ingersoll MA, Platt AM, Potteaux S, Randolph GJ. Monocyte trafficking in acute and chronic inflammation. Trends Immunol. 2011;44:470–477. PubMed PMC

Cheong C, Matos I, Choi JH, Dandamudi DB, Shrestha E, Longhi MP, Jeffrey KL, Anthony RM, Kluger C, Nchinda G, Koh H, Rodriguez A, Idoyaga J, Pack M, Velinzon K, Park CG, Steinman RM. Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209(+) dendritic cells for immune T cell areas. Cell. 2010;44:416–429. PubMed PMC

Bonneau M, Epardaud M, Payot F, Niborski V, Thoulouze MI, Bernex F, Charley B, Riffault S, Guilloteau LA, Schwartz-Cornil I. Migratory monocytes and granulocytes are major lymphatic carriers of Salmonella from tissue to draining lymph node. J Leukoc Biol. 2006;44:268–276. PubMed

Calabro S, Tortoli M, Baudner BC, Pacitto A, Cortese M, O'Hagan DT, De-Gregorio E, Seubert A, Wack A. Vaccine adjuvants alum and MF59 induce rapid recruitment of neutrophils and monocytes that participate in antigen transport to draining lymph nodes. Vaccine. 2011;44:1812–1823. PubMed

Leirião P, Del-Fresno C, Ardavín C. Monocytes as effector cells: activated Ly-6C(high) mouse monocytes migrate to the lymph nodes through the lymph and cross-present antigens to CD8+ T cells. Eur J Immunol. 2012;44:2042–2051. PubMed

Sponaas AM, Rosario AP F d, Voisine C, Mastelic B, Thompson J, Koernig S, Jarra W, Renia L, Mauduit M, Potocnik AJ, Langhorne J. Migrating monocytes recruited to the spleen play an important role in control of blood stage malaria. Blood. 2009;44:5522–5531. PubMed

Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, Figueiredo JL, Kohler RH, Chudnovskiy A, Waterman P, Aikawa E, Mempel TR, Libby P, Weissleder R, Pittet MJ. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science. 2009;44:612–616. PubMed PMC

Shi C, Jia T, Mendez-Ferrer S, Hohl TM, Serbina NV, Lipuma L, Leiner I, Li MO, Frenette PS, Pamer EG. Bone marrow mesenchymal stem and progenitor cells induce monocyte emigration in response to circulating toll-like receptor ligands. Immunity. 2011;44:590–601. PubMed PMC

Zimmermann HW, Seidler S, Nattermann J, Gassler N, Hellerbrand C, Zernecke A, Tischendorf JJ, Luedde T, Weiskirchen R, Trautwein C, Tacke F. Functional contribution of elevated circulating and hepatic non-classical CD14 + CD16+ monocytes to inflammation and human liver fibrosis. PLoS One. 2010;44:e11049. PubMed PMC

Janatpour MJ, Hudak S, Sathe M, Sedgwick JD, McEvoy LM. Tumor necrosis factor-dependent segmental control of MIG expression by high endothelial venules in inflamed lymph nodes regulates monocyte recruitment. J Exp Med. 2001;44:1375–1384. PubMed PMC

Leon B, Ardavin C. Monocyte migration to inflamed skin and lymph nodes is differentially controlled by L-selectin and PSGL-1. Blood. 2008;44:3126–3130. PubMed

Leuschner F, Panizzi P, Chico-Calero I, Lee WW, Ueno T, Cortez-Retamozo V, Waterman P, Gorbatov R, Marinelli B, Iwamoto Y, Chudnovskiy A, Figueiredo JL, Sosnovik DE, Pittet MJ, Swirski FK, Weissleder R, Nahrendorf M. Angiotensin-converting enzyme inhibition prevents the release of monocytes from their splenic reservoir in mice with myocardial infarction. Circ Res. 2010;44:1364–1373. PubMed PMC

Jia T, Serbina NV, Brandl K, Zhong MX, Leiner IM, Charo IF, Pamer EG. Additive roles for MCP-1 and MCP-3 in CCR2-mediated recruitment of inflammatory monocytes during Listeria monocytogenes infection. J Immunol. 2008;44:6846–6853. PubMed PMC

Serbina NV, Pamer EG. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol. 2006;44:311–317. PubMed

Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol. 2005;44:953–964. PubMed

Ondrackova P, Matiasovic J, Volf J, Dominguez J, Faldyna M. Phenotypic characterisation of the monocyte subpopulations in healthy adult pigs and Salmonella-infected pigs by seven-colour flow cytometry. Res Vet Sci. 2013;44:240–245. PubMed

Ondrackova P, Nechvatalova K, Kucerova Z, Leva L, Dominguez J, Faldyna M. Porcine mononuclear phagocyte subpopulations in the lung, blood and bone marrow: dynamics during inflammation induced by Actinobacillus pleuropneumoniae. Vet Res. 2010;44:64. PubMed PMC

Fairbairn L, Kapetanovic R, Sester DP, Hume DA. The mononuclear phagocyte system of the pig as a model for understanding human innate immunity and disease. J Leukoc Biol. 2011;44:855–871. PubMed

Baarsch MJ, Foss DL, Murtaugh MP. Pathophysiologic correlates of acute porcine pleuropneumonia. Am J Vet Res. 2000;44:684–690. PubMed

Bosse JT, Janson H, Sheehan BJ, Beddek AJ, Rycroft AN, Kroll JS, Langford PR. Actinobacillus pleuropneumoniae: pathobiology and pathogenesis of infection. Microbes Infect. 2002;44:225–235. PubMed

Mortensen S, Skovgaard K, Hedegaard J, Bendixen C, Heegaard PM. Transcriptional profiling at different sites in lungs of pigs during acute bacterial respiratory infection. Innate Immun. 2011;44:41–53. PubMed

Ondrackova P, Kovaru H, Kovaru F, Matiasovic J, Leva L, Faldyna M. The effect of adenosine on pro-inflammatory cytokine production by porcine T cells. Vet Immunol Immunopathol. 2012;44:332–339. PubMed

Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000;44:365–386. PubMed

Nygard AB, Jorgensen CB, Cirera S, Fredholm M. Selection of reference genes for gene expression studies in pig tissues using SYBR green qPCR. BMC Mol Biol. 2007;44:67–72. PubMed PMC

Bonecchi R, Galliera E, Borroni EM, Corsi MM, Locati M, Mantovani A. Chemokines and chemokine receptors: an overview. Front Biosci. 2009;44:540–551. PubMed

Nahrendorf M, Swirski FK, Aikawa E, Stangenberg L, Wurdinger T, Figueiredo JL, Libby P, Weissleder R, Pittet MJ. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med. 2007;44:3037–3047. PubMed PMC

Moreno S, Alvarez B, Poderoso T, Revilla C, Ezquerra A, Alonso F, Dominguez J. Porcine monocyte subsets differ in the expression of CCR2 and in their responsiveness to CCL2. Vet Res. 2010;44:76. PubMed PMC

Zhang Y, Miura K, Li J, Tullo G, Zhu F, Hong L, Lin T, Su XZ, Long C. Macrophage migration inhibitory factor homolog from Plasmodium yoelii modulates monocyte recruitment and activation in spleen during infection. Parasitol Res. 2012;44:1755–1763. PubMed PMC

Yoshida R, Imai T, Hieshima K, Kusuda J, Baba M, Kitaura M, Nishimura M, Kakizaki M, Nomiyama H, Yoshie O. Molecular cloning of a novel human CC chemokine EBI1-ligand chemokine that is a specific functional ligand for EBI1, CCR7. J Biol Chem. 1997;44:13803–13809. PubMed

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