Analyze Diet
PloS one2023; 18(3); e0282738; doi: 10.1371/journal.pone.0282738

Equine alveolar macrophages and monocyte-derived macrophages respond differently to an inflammatory stimulus.

Abstract: Alveolar macrophages (AMs) are the predominant innate immune cell in the distal respiratory tract. During inflammatory responses, AMs may be supplemented by blood monocytes, which differentiate into monocyte-derived macrophages (MDMs). Macrophages play important roles in a variety of common equine lower airway diseases, including severe equine asthma (SEA). In an experimental model, an inhaled mixture of Aspergillus fumigatus spores, lipopolysaccharide, and silica microspheres (FLS), induced SEA exacerbation in susceptible horses. However, whether equine AMs and MDMs have differing immunophenotypes and cytokine responses to FLS stimulation is unknown. To address these questions, alveolar macrophages/monocytes (AMMs) were isolated from bronchoalveolar lavage fluid and MDMs derived from blood of six healthy horses. Separately, AMMs and MDMs were cultured with and without FLS for six hours after which cell surface marker expression and cytokine production were analyzed by flow cytometry and a bead-based multiplex assay, respectively. Results showed that regardless of exposure conditions, AMMs had significantly higher surface expression of CD163 and CD206 than MDMs. Incubation with FLS induced secretion of IL-1β, IL-8, TNF-α and IFN-γ in AMMs, and IL-8, IL-10 and TNF-α in MDMs. These results suggest that AMMs have a greater proinflammatory response to in vitro FLS stimulation than MDMs, inferring differing roles in equine lung inflammation. Variability in recruitment and function of monocyte-macrophage populations warrant more detailed in vivo investigation in both homeostatic and diseased states.
Publication Date: 2023-03-15 PubMed ID: 36920969PubMed Central: PMC10016717DOI: 10.1371/journal.pone.0282738Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The abstract describes a study that investigates the different responses of equine alveolar macrophages and monocyte-derived macrophages to inflammatory stimulus. The findings reveal that the two types of macrophages play different roles in equine lung inflammation.

Objective of the study

  • The main goal of this research was to understand how equine alveolar macrophages (AMs) and monocyte-derived macrophages (MDMs) respond to inflammatory triggers. The researchers wanted to determine whether and how these two types of cells differ in their responses to inflammation, particularly in the context of severe equine asthma (SEA).

Methodology of the study

  • The researchers isolated alveolar macrophages/monocytes (AMMs) from bronchoalveolar lavage fluid and derived MDMs from the blood of six healthy horses.
  • The cells were then cultured both with and without an inhaled mixture of an inflammatory trigger, termed as FLS, which included Aspergillus fumigatus spores, lipopolysaccharide, and silica microspheres. These compounds were used as they are known to induce SEA exacerbation in susceptible horses.
  • After six hours of incubation, the researchers studied the cells’ surface marker expression and cytokine production using flow cytometry and a bead-based multiplex assay, respectively.

Findings of the study

  • The results revealed significant differences between AMMs and MDMs. Even without any exposure to the FLS, AMMs had higher surface expression of the markers CD163 and CD206 compared to MDMs.
  • Upon exposure to the FLS, both AMMs and MDMs produced various cytokines, but in different amounts. AMMs substantially produced IL-1β, IL-8, TNF-α and IFN-γ, indicating a higher proinflammatory response. MDMs, on the other hand, produced IL-8, IL-10, and TNF-α.

Implications of the study

  • The findings suggest that AMMs and MDMs may have different roles in equine lung inflammation, given their distinct responses to FLS stimulation.
  • Furthermore, the variations in the recruitment and functions of these macrophage populations in response to inflammation suggest that a more detailed in vivo investigation is required. Such studies could help better understand the roles of these cell types both in keeping the physiological balance and in responses to diseases.

Cite This Article

APA
Kang H, Lee GKC, Bienzle D, Arroyo LG, Sears W, Lillie BN, Beeler-Marfisi J. (2023). Equine alveolar macrophages and monocyte-derived macrophages respond differently to an inflammatory stimulus. PLoS One, 18(3), e0282738. https://doi.org/10.1371/journal.pone.0282738

Publication

ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 18
Issue: 3
Pages: e0282738
PII: e0282738

Researcher Affiliations

Kang, Heng
  • Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada.
Lee, Gary Kwok Cheong
  • Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada.
  • IDEXX Laboratories Pty. Ltd., Rydalmere, New South Wales, Australia.
Bienzle, Dorothee
  • Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada.
Arroyo, Luis G
  • Department of Clinical Studies, University of Guelph, Guelph, Ontario, Canada.
Sears, William
  • Department of Population Medicine, University of Guelph, Guelph, Ontario, Canada.
Lillie, Brandon N
  • Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada.
Beeler-Marfisi, Janet
  • Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada.

MeSH Terms

  • Horses
  • Animals
  • Macrophages, Alveolar / metabolism
  • Tumor Necrosis Factor-alpha / metabolism
  • Interleukin-8 / metabolism
  • Macrophages / metabolism
  • Cytokines / metabolism
  • Cells, Cultured

Conflict of Interest Statement

The authors have declared that no competing interests exist.

References

This article includes 79 references
  1. Byrne AJ, Mathie SA, Gregory LG, Lloyd CM. Pulmonary macrophages: key players in the innate defence of the airways.. Thorax 2015 Dec;70(12):1189-96.
    doi: 10.1136/thoraxjnl-2015-207020pubmed: 26286722google scholar: lookup
  2. Joshi N, Walter JM, Misharin AV. Alveolar Macrophages.. Cell Immunol 2018 Aug;330:86-90.
    doi: 10.1016/j.cellimm.2018.01.005pubmed: 29370889google scholar: lookup
  3. Hashimoto D, Chow A, Noizat C, Teo P, Beasley MB, Leboeuf M, Becker CD, See P, Price J, Lucas D, Greter M, Mortha A, Boyer SW, Forsberg EC, Tanaka M, van Rooijen N, García-Sastre A, Stanley ER, Ginhoux F, Frenette PS, Merad M. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes.. Immunity 2013 Apr 18;38(4):792-804.
  4. Gentek R, Molawi K, Sieweke MH. Tissue macrophage identity and self-renewal.. Immunol Rev 2014 Nov;262(1):56-73.
    doi: 10.1111/imr.12224pubmed: 25319327google scholar: lookup
  5. Epelman S, Lavine KJ, Randolph GJ. Origin and functions of tissue macrophages.. Immunity 2014 Jul 17;41(1):21-35.
  6. Garbi N, Lambrecht BN. Location, function, and ontogeny of pulmonary macrophages during the steady state.. Pflugers Arch 2017 Apr;469(3-4):561-572.
    doi: 10.1007/s00424-017-1965-3pubmed: 28289977google scholar: lookup
  7. Gwyer Findlay E, Hussell T. Macrophage-mediated inflammation and disease: a focus on the lung.. Mediators Inflamm 2012;2012:140937.
    doi: 10.1155/2012/140937pmc: PMC3530802pubmed: 23304058google scholar: lookup
  8. Beeler-Marfisi J, Clark ME, Wen X, Sears W, Huber L, Ackerley C, Viel L, Bienzle D. Experimental induction of recurrent airway obstruction with inhaled fungal spores, lipopolysaccharide, and silica microspheres in horses.. Am J Vet Res 2010 Jun;71(6):682-9.
    doi: 10.2460/ajvr.71.6.682pubmed: 20513185google scholar: lookup
  9. Ainsworth DM, Wagner B, Erb HN, Young JC, Retallick DE. Effects of in vitro exposure to hay dust on expression of interleukin-17, -23, -8, and -1beta and chemokine (C-X-C motif) ligand 2 by pulmonary mononuclear cells isolated from horses chronically affected with recurrent airway disease.. Am J Vet Res 2007 Dec;68(12):1361-9.
    doi: 10.2460/ajvr.68.12.1361pubmed: 18052742google scholar: lookup
  10. Pirie RS, McLachlan G, McGorum BC. Evaluation of nebulised hay dust suspensions (HDS) for the diagnosis and investigation of heaves. 1: Preparation and composition of HDS.. Equine Vet J 2002 Jul;34(4):332-6.
    doi: 10.2746/042516402776249092pubmed: 12117103google scholar: lookup
  11. Kang H, Bienzle D, Lee GKC, Piché É, Viel L, Odemuyiwa SO, Beeler-Marfisi J. Flow cytometric analysis of equine bronchoalveolar lavage fluid cells in horses with and without severe equine asthma.. Vet Pathol 2022 Jan;59(1):91-99.
    doi: 10.1177/03009858211042588pmc: PMC8679174pubmed: 34521286google scholar: lookup
  12. Buechler C, Eisinger K, Krautbauer S. Diagnostic and prognostic potential of the macrophage specific receptor CD163 in inflammatory diseases.. Inflamm Allergy Drug Targets 2013 Dec;12(6):391-402.
    doi: 10.2174/18715281113126660060pubmed: 24090317google scholar: lookup
  13. Alves-Januzzi AB, Brunialti MKC, Salomao R. CD163 and CD206 expression does not correlate with tolerance and cytokine production in LPS-tolerant human monocytes.. Cytometry B Clin Cytom 2017 May;92(3):192-199.
    doi: 10.1002/cyto.b.21321pubmed: 26352275google scholar: lookup
  14. Buechler C, Ritter M, Orsó E, Langmann T, Klucken J, Schmitz G. Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro- and antiinflammatory stimuli.. J Leukoc Biol 2000 Jan;67(1):97-103.
    doi: 10.1002/jlb.67.1.97pubmed: 10648003google scholar: lookup
  15. Nawaz A, Aminuddin A, Kado T, Takikawa A, Yamamoto S, Tsuneyama K, Igarashi Y, Ikutani M, Nishida Y, Nagai Y, Takatsu K, Imura J, Sasahara M, Okazaki Y, Ueki K, Okamura T, Tokuyama K, Ando A, Matsumoto M, Mori H, Nakagawa T, Kobayashi N, Saeki K, Usui I, Fujisaka S, Tobe K. CD206(+) M2-like macrophages regulate systemic glucose metabolism by inhibiting proliferation of adipocyte progenitors.. Nat Commun 2017 Aug 18;8(1):286.
    doi: 10.1038/s41467-017-00231-1pmc: PMC5561263pubmed: 28819169google scholar: lookup
  16. Lee JW, Chun W, Lee HJ, Min JH, Kim SM, Seo JY, Ahn KS, Oh SR. The Role of Macrophages in the Development of Acute and Chronic Inflammatory Lung Diseases.. Cells 2021 Apr 14;10(4).
    doi: 10.3390/cells10040897pmc: PMC8070705pubmed: 33919784google scholar: lookup
  17. van der Veen TA, de Groot LES, Melgert BN. The different faces of the macrophage in asthma.. Curr Opin Pulm Med 2020 Jan;26(1):62-68.
  18. Tokunaga Y, Imaoka H, Kaku Y, Kawayama T, Hoshino T. The significance of CD163-expressing macrophages in asthma.. Ann Allergy Asthma Immunol 2019 Sep;123(3):263-270.
    doi: 10.1016/j.anai.2019.05.019pubmed: 31152786google scholar: lookup
  19. van Furth R. Macrophage activity and clinical immunology. Origin and kinetics of mononuclear phagocytes.. Ann N Y Acad Sci 1976;278:161-75.
  20. Hume DA, Irvine KM, Pridans C. The Mononuclear Phagocyte System: The Relationship between Monocytes and Macrophages.. Trends Immunol 2019 Feb;40(2):98-112.
    doi: 10.1016/j.it.2018.11.007pubmed: 30579704google scholar: lookup
  21. Landsman L, Jung S. Lung macrophages serve as obligatory intermediate between blood monocytes and alveolar macrophages.. J Immunol 2007 Sep 15;179(6):3488-94.
    doi: 10.4049/jimmunol.179.6.3488pubmed: 17785782google scholar: lookup
  22. Landsman L, Varol C, Jung S. Distinct differentiation potential of blood monocyte subsets in the lung.. J Immunol 2007 Feb 15;178(4):2000-7.
    doi: 10.4049/jimmunol.178.4.2000pubmed: 17277103google scholar: lookup
  23. Ożańska A, Szymczak D, Rybka J. Pattern of human monocyte subpopulations in health and disease.. Scand J Immunol 2020 Jul;92(1):e12883.
    doi: 10.1111/sji.12883pubmed: 32243617google scholar: lookup
  24. Gressler AE, Lübke S, Wagner B, Arnold C, Lohmann KL, Schnabel CL. Comprehensive Flow Cytometric Characterization of Bronchoalveolar Lavage Cells Indicates Comparable Phenotypes Between Asthmatic and Healthy Horses But Functional Lymphocyte Differences.. Front Immunol 2022;13:896255.
    doi: 10.3389/fimmu.2022.896255pmc: PMC9296846pubmed: 35874777google scholar: lookup
  25. Sage SE, Nicholson P, Peters LM, Leeb T, Jagannathan V, Gerber V. Single-cell gene expression analysis of cryopreserved equine bronchoalveolar cells.. Front Immunol 2022;13:929922.
    doi: 10.3389/fimmu.2022.929922pmc: PMC9467276pubmed: 36105804google scholar: lookup
  26. Arora S, Dev K, Agarwal B, Das P, Syed MA. Macrophages: Their role, activation and polarization in pulmonary diseases.. Immunobiology 2018 Apr-May;223(4-5):383-396.
    doi: 10.1016/j.imbio.2017.11.001pmc: PMC7114886pubmed: 29146235google scholar: lookup
  27. Hohl TM, Van Epps HL, Rivera A, Morgan LA, Chen PL, Feldmesser M, Pamer EG. Aspergillus fumigatus triggers inflammatory responses by stage-specific beta-glucan display.. PLoS Pathog 2005 Nov;1(3):e30.
  28. Loures FV, Araújo EF, Feriotti C, Bazan SB, Costa TA, Brown GD, Calich VL. Dectin-1 induces M1 macrophages and prominent expansion of CD8+IL-17+ cells in pulmonary Paracoccidioidomycosis.. J Infect Dis 2014 Sep 1;210(5):762-73.
    doi: 10.1093/infdis/jiu136pubmed: 24604821google scholar: lookup
  29. Laan TT, Bull S, Pirie RS, Fink-Gremmels J. Evaluation of cytokine production by equine alveolar macrophages exposed to lipopolysaccharide, Aspergillus fumigatus, and a suspension of hay dust.. Am J Vet Res 2005 Sep;66(9):1584-9.
    doi: 10.2460/ajvr.2005.66.1584pubmed: 16261833google scholar: lookup
  30. Park BS, Lee JO. Recognition of lipopolysaccharide pattern by TLR4 complexes.. Exp Mol Med 2013 Dec 6;45(12):e66.
    doi: 10.1038/emm.2013.97pmc: PMC3880462pubmed: 24310172google scholar: lookup
  31. Hussell T, Bell TJ. Alveolar macrophages: plasticity in a tissue-specific context.. Nat Rev Immunol 2014 Feb;14(2):81-93.
    doi: 10.1038/nri3600pubmed: 24445666google scholar: lookup
  32. Misharin AV, Morales-Nebreda L, Reyfman PA, Cuda CM, Walter JM, McQuattie-Pimentel AC, Chen CI, Anekalla KR, Joshi N, Williams KJN, Abdala-Valencia H, Yacoub TJ, Chi M, Chiu S, Gonzalez-Gonzalez FJ, Gates K, Lam AP, Nicholson TT, Homan PJ, Soberanes S, Dominguez S, Morgan VK, Saber R, Shaffer A, Hinchcliff M, Marshall SA, Bharat A, Berdnikovs S, Bhorade SM, Bartom ET, Morimoto RI, Balch WE, Sznajder JI, Chandel NS, Mutlu GM, Jain M, Gottardi CJ, Singer BD, Ridge KM, Bagheri N, Shilatifard A, Budinger GRS, Perlman H. Monocyte-derived alveolar macrophages drive lung fibrosis and persist in the lung over the life span.. J Exp Med 2017 Aug 7;214(8):2387-2404.
    doi: 10.1084/jem.20162152pmc: PMC5551573pubmed: 28694385google scholar: lookup
  33. Niessen NM, Baines KJ, Simpson JL, Scott HA, Qin L, Gibson PG, Fricker M. Neutrophilic asthma features increased airway classical monocytes.. Clin Exp Allergy 2021 Feb;51(2):305-317.
    doi: 10.1111/cea.13811pubmed: 33301598google scholar: lookup
  34. Maus UA, Janzen S, Wall G, Srivastava M, Blackwell TS, Christman JW, Seeger W, Welte T, Lohmeyer J. Resident alveolar macrophages are replaced by recruited monocytes in response to endotoxin-induced lung inflammation.. Am J Respir Cell Mol Biol 2006 Aug;35(2):227-35.
    doi: 10.1165/rcmb.2005-0241OCpubmed: 16543608google scholar: lookup
  35. Couëtil LL, Cardwell JM, Gerber V, Lavoie JP, Léguillette R, Richard EA. Inflammatory Airway Disease of Horses--Revised Consensus Statement.. J Vet Intern Med 2016 Mar-Apr;30(2):503-15.
    doi: 10.1111/jvim.13824pmc: PMC4913592pubmed: 26806374google scholar: lookup
  36. Bond S, Léguillette R, Richard EA, Couetil L, Lavoie JP, Martin JG, Pirie RS. Equine asthma: Integrative biologic relevance of a recently proposed nomenclature.. J Vet Intern Med 2018 Nov;32(6):2088-2098.
    doi: 10.1111/jvim.15302pmc: PMC6271326pubmed: 30294851google scholar: lookup
  37. Hotchkiss JW, Reid SW, Christley RM. A survey of horse owners in Great Britain regarding horses in their care. Part 2: Risk factors for recurrent airway obstruction.. Equine Vet J 2007 Jul;39(4):301-8.
    doi: 10.2746/042516407x180129pubmed: 17722720google scholar: lookup
  38. Ainsworth DM, Grünig G, Matychak MB, Young J, Wagner B, Erb HN, Antczak DF. Recurrent airway obstruction (RAO) in horses is characterized by IFN-gamma and IL-8 production in bronchoalveolar lavage cells.. Vet Immunol Immunopathol 2003 Nov 15;96(1-2):83-91.
    doi: 10.1016/S0165-2427(03)00142-9pubmed: 14522137google scholar: lookup
  39. Nolen-Walston RD, Harris M, Agnew ME, Martin BB, Reef VB, Boston RC, Davidson EJ. Clinical and diagnostic features of inflammatory airway disease subtypes in horses examined because of poor performance: 98 cases (2004-2010).. J Am Vet Med Assoc 2013 Apr 15;242(8):1138-45.
    pubmed: 23547679doi: 10.2460/javma.242.8.1138google scholar: lookup
  40. Franchini M, Gill U, von Fellenberg R, Bracher VD. Interleukin-8 concentration and neutrophil chemotactic activity in bronchoalveolar lavage fluid of horses with chronic obstructive pulmonary disease following exposure to hay.. Am J Vet Res 2000 Nov;61(11):1369-74.
    doi: 10.2460/ajvr.2000.61.1369pubmed: 11108181google scholar: lookup
  41. Odemuyia SO. Immunophenotypic Characteristics of Equine Monocytes and Alveolar Macrophages. 2012; 106.
  42. Laan TT, Bull S, Pirie R, Fink-Gremmels J. The role of alveolar macrophages in the pathogenesis of recurrent airway obstruction in horses.. J Vet Intern Med 2006 Jan-Feb;20(1):167-74.
  43. Karagianni AE, Kapetanovic R, Summers KM, McGorum BC, Hume DA, Pirie RS. Comparative transcriptome analysis of equine alveolar macrophages.. Equine Vet J 2017 May;49(3):375-382.
    doi: 10.1111/evj.12584pmc: PMC5412682pubmed: 27096353google scholar: lookup
  44. Steinbach F, Stark R, Ibrahim S, Gawad EA, Ludwig H, Walter J, Commandeur U, Mauel S. Molecular cloning and characterization of markers and cytokines for equid myeloid cells.. Vet Immunol Immunopathol 2005 Oct 18;108(1-2):227-36.
    doi: 10.1016/j.vetimm.2005.07.015pubmed: 16112744google scholar: lookup
  45. Ziegler A, Everett H, Hamza E, Garbani M, Gerber V, Marti E, Steinbach F. Equine dendritic cells generated with horse serum have enhanced functionality in comparison to dendritic cells generated with fetal bovine serum.. BMC Vet Res 2016 Nov 15;12(1):254.
    doi: 10.1186/s12917-016-0880-8pmc: PMC5111218pubmed: 27846835google scholar: lookup
  46. Martinez-Pomares L. The mannose receptor.. J Leukoc Biol 2012 Dec;92(6):1177-86.
    doi: 10.1189/jlb.0512231pubmed: 22966131google scholar: lookup
  47. Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SE, Pollard JW, Frampton J, Liu KJ, Geissmann F. A lineage of myeloid cells independent of Myb and hematopoietic stem cells.. Science 2012 Apr 6;336(6077):86-90.
    doi: 10.1126/science.1219179pubmed: 22442384google scholar: lookup
  48. Goerdt S, Orfanos CE. Other functions, other genes: alternative activation of antigen-presenting cells.. Immunity 1999 Feb;10(2):137-42.
    doi: 10.1016/s1074-7613(00)80014-xpubmed: 10072066google scholar: lookup
  49. Gordon S. Alternative activation of macrophages.. Nat Rev Immunol 2003 Jan;3(1):23-35.
    doi: 10.1038/nri978pubmed: 12511873google scholar: lookup
  50. Fabriek BO, Dijkstra CD, van den Berg TK. The macrophage scavenger receptor CD163.. Immunobiology 2005;210(2-4):153-60.
    doi: 10.1016/j.imbio.2005.05.010pubmed: 16164022google scholar: lookup
  51. Shi C, Pamer EG. Monocyte recruitment during infection and inflammation.. Nat Rev Immunol 2011 Oct 10;11(11):762-74.
    doi: 10.1038/nri3070pmc: PMC3947780pubmed: 21984070google scholar: lookup
  52. Kaku Y, Imaoka H, Morimatsu Y, Komohara Y, Ohnishi K, Oda H, Takenaka S, Matsuoka M, Kawayama T, Takeya M, Hoshino T. Overexpression of CD163, CD204 and CD206 on alveolar macrophages in the lungs of patients with severe chronic obstructive pulmonary disease.. PLoS One 2014;9(1):e87400.
  53. Tsuchiya K, Suzuki Y, Yoshimura K, Yasui H, Karayama M, Hozumi H, Furuhashi K, Enomoto N, Fujisawa T, Nakamura Y, Inui N, Yokomura K, Suda T. Macrophage Mannose Receptor CD206 Predicts Prognosis in Community-acquired Pneumonia.. Sci Rep 2019 Dec 10;9(1):18750.
    doi: 10.1038/s41598-019-55289-2pmc: PMC6904766pubmed: 31822747google scholar: lookup
  54. Weaver LK, Hintz-Goldstein KA, Pioli PA, Wardwell K, Qureshi N, Vogel SN, Guyre PM. Pivotal advance: activation of cell surface Toll-like receptors causes shedding of the hemoglobin scavenger receptor CD163.. J Leukoc Biol 2006 Jul;80(1):26-35.
    doi: 10.1189/jlb.1205756pubmed: 16799153google scholar: lookup
  55. Chauvin P, Morzadec C, de Latour B, Llamas-Gutierrez F, Luque-Paz D, Jouneau S, Vernhet L. Soluble CD163 is produced by monocyte-derived and alveolar macrophages, and is not associated with the severity of idiopathic pulmonary fibrosis.. Innate Immun 2022 Apr;28(3-4):138-151.
    doi: 10.1177/17534259221097835pmc: PMC9136464pubmed: 35522300google scholar: lookup
  56. Matute-Blanch C, Montalban X, Comabella M. Multiple sclerosis, and other demyelinating and autoimmune inflammatory diseases of the central nervous system.. Handb Clin Neurol 2017;146:67-84.
  57. Yu X, Guo C, Fisher PB, Subjeck JR, Wang XY. Scavenger Receptors: Emerging Roles in Cancer Biology and Immunology.. Adv Cancer Res 2015;128:309-64.
    doi: 10.1016/bs.acr.2015.04.004pmc: PMC4631385pubmed: 26216637google scholar: lookup
  58. Edelstein CL. Biomarkers of acute kidney injury.. Adv Chronic Kidney Dis 2008 Jul;15(3):222-34.
    doi: 10.1053/j.ackd.2008.04.003pmc: PMC3287955pubmed: 18565474google scholar: lookup
  59. Curto E, Messenger KM, Salmon JH, Gilger BC. Cytokine and chemokine profiles of aqueous humor and serum in horses with uveitis measured using multiplex bead immunoassay analysis.. Vet Immunol Immunopathol 2016 Dec;182:43-51.
    doi: 10.1016/j.vetimm.2016.09.008pubmed: 27863549google scholar: lookup
  60. Zak A, Siwinska N, Elzinga S, Barker VD, Stefaniak T, Schanbacher BJ, Place NJ, Niedzwiedz A, Adams AA. Effects of advanced age and pituitary pars intermedia dysfunction on components of the acute phase reaction in horses.. Domest Anim Endocrinol 2020 Jul;72:106476.
  61. Figueiredo MD, Vandenplas ML, Hurley DJ, Moore JN. Differential induction of MyD88- and TRIF-dependent pathways in equine monocytes by Toll-like receptor agonists.. Vet Immunol Immunopathol 2009 Jan 15;127(1-2):125-34.
    doi: 10.1016/j.vetimm.2008.09.028pubmed: 19019456google scholar: lookup
  62. Karagianni AE, Lisowski ZM, Hume DA, Scott Pirie R. The equine mononuclear phagocyte system: The relevance of the horse as a model for understanding human innate immunity.. Equine Vet J 2021 Mar;53(2):231-249.
    doi: 10.1111/evj.13341pubmed: 32881079google scholar: lookup
  63. Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity.. Immunity 2011 May 27;34(5):637-50.
    doi: 10.1016/j.immuni.2011.05.006pubmed: 21616434google scholar: lookup
  64. Pollard KM. Silica, Silicosis, and Autoimmunity.. Front Immunol 2016;7:97.
    doi: 10.3389/fimmu.2016.00097pmc: PMC4786551pubmed: 27014276google scholar: lookup
  65. Schroder K, Hertzog PJ, Ravasi T, Hume DA. Interferon-gamma: an overview of signals, mechanisms and functions.. J Leukoc Biol 2004 Feb;75(2):163-89.
    doi: 10.1189/jlb.0603252pubmed: 14525967google scholar: lookup
  66. Mantovani A, Biswas SK, Galdiero MR, Sica A, Locati M. Macrophage plasticity and polarization in tissue repair and remodelling.. J Pathol 2013 Jan;229(2):176-85.
    doi: 10.1002/path.4133pubmed: 23096265google scholar: lookup
  67. Eichinger KM, Egaña L, Orend JG, Resetar E, Anderson KB, Patel R, Empey KM. Alveolar macrophages support interferon gamma-mediated viral clearance in RSV-infected neonatal mice.. Respir Res 2015 Oct 5;16:122.
    doi: 10.1186/s12931-015-0282-7pmc: PMC4594958pubmed: 26438053google scholar: lookup
  68. Fenton MJ, Vermeulen MW, Kim S, Burdick M, Strieter RM, Kornfeld H. Induction of gamma interferon production in human alveolar macrophages by Mycobacterium tuberculosis.. Infect Immun 1997 Dec;65(12):5149-56.
  69. Darwich L, Coma G, Peña R, Bellido R, Blanco EJ, Este JA, Borras FE, Clotet B, Ruiz L, Rosell A, Andreo F, Parkhouse RM, Bofill M. Secretion of interferon-gamma by human macrophages demonstrated at the single-cell level after costimulation with interleukin (IL)-12 plus IL-18.. Immunology 2009 Mar;126(3):386-93.
  70. Wilson ME, McCandless EE, Olszewski MA, Robinson NE. Alveolar macrophage phenotypes in severe equine asthma.. Vet J 2020 Feb;256:105436.
    doi: 10.1016/j.tvjl.2020.105436pmc: PMC7768773pubmed: 32113585google scholar: lookup
  71. Hu X, Paik PK, Chen J, Yarilina A, Kockeritz L, Lu TT, Woodgett JR, Ivashkiv LB. IFN-gamma suppresses IL-10 production and synergizes with TLR2 by regulating GSK3 and CREB/AP-1 proteins.. Immunity 2006 May;24(5):563-74.
    doi: 10.1016/j.immuni.2006.02.014pubmed: 16713974google scholar: lookup
  72. Aharonson-Raz K, Singh B. Pulmonary intravascular macrophages and endotoxin-induced pulmonary pathophysiology in horses.. Can J Vet Res 2010 Jan;74(1):45-9.
    pmc: PMC2801311pubmed: 20357958
  73. Cavarra E, Martorana PA, Gambelli F, de Santi M, van Even P, Lungarella G. Neutrophil recruitment into the lungs is associated with increased lung elastase burden, decreased lung elastin, and emphysema in alpha 1 proteinase inhibitor-deficient mice.. Lab Invest 1996 Aug;75(2):273-80.
    pubmed: 8765327
  74. Losa García JE, Rodríguez FM, Martín de Cabo MR, García Salgado MJ, Losada JP, Villarón LG, López AJ, Arellano JL. Evaluation of inflammatory cytokine secretion by human alveolar macrophages.. Mediators Inflamm 1999;8(1):43-51.
    doi: 10.1080/09629359990711pmc: PMC1781780pubmed: 10704089google scholar: lookup
  75. Takatsu K. Interleukin-5 and IL-5 receptor in health and diseases.. Proc Jpn Acad Ser B Phys Biol Sci 2011;87(8):463-85.
    doi: 10.2183/pjab.87.463pmc: PMC3313690pubmed: 21986312google scholar: lookup
  76. Berghaus LJ, Giguère S, Sturgill TL. Effects of age and macrophage lineage on intracellular survival and cytokine induction after infection with Rhodococcus equi.. Vet Immunol Immunopathol 2014 Jul 15;160(1-2):41-50.
    doi: 10.1016/j.vetimm.2014.03.010pubmed: 24736188google scholar: lookup
  77. Karagianni AE, Kapetanovic R, McGorum BC, Hume DA, Pirie SR. The equine alveolar macrophage: functional and phenotypic comparisons with peritoneal macrophages.. Vet Immunol Immunopathol 2013 Oct 1;155(4):219-28.
  78. Grünig G, Hulliger C, Winder C, Hermann M, Jungi TW, von Fellenberg R. Spontaneous and lipopolysaccharide-induced expression of procoagulant activity by equine lung macrophages in comparison with blood monocytes and blood neutrophils.. Vet Immunol Immunopathol 1991 Sep;29(3-4):295-312.
    doi: 10.1016/0165-2427(91)90021-4pubmed: 1949591google scholar: lookup
  79. Jackson KA, Stott JL, Horohov DW, Watson JL. IL-4 induced CD23 (FcepsilonRII) up-regulation in equine peripheral blood mononuclear cells and pulmonary alveolar macrophages.. Vet Immunol Immunopathol 2004 Oct;101(3-4):243-50.
    doi: 10.1016/j.vetimm.2004.05.001pubmed: 15350754google scholar: lookup

Citations

This article has been cited 0 times.