Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T09:49:55.023Z Has data issue: false hasContentIssue false

Role of neutrophils in equine asthma

Published online by Cambridge University Press:  24 May 2018

Benjamin Uberti
Affiliation:
Department of Clinical Veterinary Sciences, Faculty of Veterinary Sciences, Universidad Austral de Chile, Valdivia, Chile
Gabriel Morán*
Affiliation:
Department of Pharmacology, Faculty of Veterinary Sciences, Universidad Austral de Chile, Valdivia, Chile
*
*Corresponding author. E-mail: gmoran@uach.cl

Abstract

Neutrophilic bronchiolitis is the primary lesion in asthma-affected horses. Neutrophils are key actors in host defense, migrating toward sites of inflammation and infection, where they act as early responder cells toward external insults. However, neutrophils can also mediate tissue damage in various non-infectious inflammatory processes. Within the airways, these cells likely contribute to bronchoconstriction, mucus hypersecretion, and pulmonary remodeling by releasing pro-inflammatory mediators, including the cytokines interleukin (IL)-8 and IL-17, neutrophil elastase, reactive oxygen species (ROS), and neutrophil extracellular traps (NETs). The mechanisms that regulate neutrophil functions in the tissues are complex and incompletely understood. Therefore, the inflammatory activity of neutrophils must be regulated with exquisite precision and timing, a task achieved through a complex network of mechanisms that regulates neutrophil survival. The discovery and development of compounds that can help regulate ROS, NET formation, cytokine release, and clearance would be highly beneficial in the design of therapies for this disease in horses. In this review, neutrophil functions during inflammation will be discussed followed by a discussion of their contribution to airway tissue injury in equine asthma.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adler, KB, Holden-Stauffer, WJ and Repine, JE (1990). Oxygen metabolites stimulate release of high-molecular weight glycoconjugates by cell and organ cultures of rodent respiratory epithelium via arachidonic acid dependent mechanism. The Journal of Clinical Investigation 85: 7585.Google Scholar
Ainsworth, DM, Appleton, JA, Antczak, DF, Santiago, MA and Aviza, G (2002). IgG antibody responses to an inhaled antigen in horses with ‘heaves’ (recurrent airway obstruction). Veterinary Immunology and Immunopathology 84: 169180.Google Scholar
Ainsworth, DM, Grünig, G, Matychak, MB, Young, J, Wagner, B, Erb, HN and Antczak, DF (2003). Recurrent airway obstruction (RAO) in horses is characterized by IFN-γ and IL-8 production in bronchoalveolar lavage cells. Veterinary Immunology and Immunopathology 96: 8391.Google Scholar
Ainsworth, DM, Wagner, B, Franchini, M, Grunig, G, Erb, H and Tan, JY (2006). Time-dependent alterations in gene expression of interleukin-8 in the bronchial epithelium of horses with recurrent airway obstruction. American Journal of Veterinary Research 67: 669677.Google Scholar
Ainsworth, DM, Wagner, B, Erb, HN, Young, JC and Retallick, DE (2007). Effects of in vitro exposure to hay dust on expression of interleukin-17, −23, −8, and −1β and chemokine (C-X-C motif) ligand 2 by pulmonary mononuclear cells isolated from horses chronically affected with recurrent airway disease. American Journal of Veterinary Research 68: 13611369.Google Scholar
Ariel, A and Serhan, CN (2007). Resolvins and protectins in the termination program of acute inflammation. Trends in Immunology 28: 176183.Google Scholar
Art, T, Kirschvink, N, Smith, N and Lekeux, P (1999). Indices of oxidative stress in blood and pulmonary epithelium lining fluid in horses suffering from recurrent airway obstruction. Equine Veterinary Journal 31: 397401.Google Scholar
Barussi, FC, Bastos, FZ, Leite, LM, Fragoso, FY, Senegaglia, AC, Brofman, PR, Nishiyama, A, Pimpão, CT, Michelotto, PV Jr (2016). Intratracheal therapy with autologous bone marrow-derived mononuclear cells reduces airway inflammation in horses with recurrent airway obstruction. Respiratory Physiology and Neurobiology 232: 3542.Google Scholar
Barton, AK, Shety, T, Bondzio, A, Einspanier, R and Gehlen, H (2016). Metalloproteinases and their inhibitors are influenced by inhalative glucocorticoid therapy in combination with environmental dust reduction in equine recurrent airway obstruction. BMC Veterinary Research 12: 282.Google Scholar
Berndt, A, Derksen, FJ, Venta, PJ, Ewart, S, Yuzbasiyan-Gurkan, V and Robinson, NE (2007). Elevated amount of toll-like receptor 4 mRNA in bronchial epithelial cells is associated with airway inflammation in horses with recurrent airway obstruction. American Journal of Physiology Lung Cellular and Molecular Physiology 292: L936L943.Google Scholar
Bournazou, I, Pound, JD, Duffin, R, Bournazos, S, Melville, LA, Brown, SB, Rossi, AG and Gregory, CD (2009). Apoptotic human cells inhibit migration of granulocytes via release of lactoferrin. The Journal of Clinical Investigation 119: 2032.Google Scholar
Borlone, CF, Morales, N, Henriquez, C, Folch, H, Olave, C, Sarmiento, J, Uberti, B and Moran, G (2017). In vitro effects of tamoxifeno on equine neutrophils. Research in Veterinary Science 110: 6064.Google Scholar
Brazil, TJ, Dagleish, MP, McGorum, BC, Dixon, PM, Haslett, C and Chilvers, ER (2005). Kinetics of pulmonary neutrophil recruitment and clearance in a natural and spontaneously resolving model of airway inflammation. Clinical and Experimental Allergy 35: 854865.Google Scholar
Brinkmann, V, Reichard, U, Goosmann, C, Fauler, B, Uhlemann, Y, Weiss, DS, Weinrauch, Y and Zychlinsky, A (2004). Neutrophil extracellular traps kill bacteria. Science 303: 15321535.Google Scholar
Bronte, V, Apolloni, E, Cabrelle, A, Ronca, R, Serafini, P, Zamboni, P, Restifo, NP and Zanovello, P (2000). Identification of a CD11b(+)/Gr-1(+)/CD31(+) myeloid progenitor capable of activating or suppressing CD8(+) T cells. Blood 96: 38383846.Google Scholar
Bruijnzeel, PL, Uddin, M and Koenderman, L (2015). Targeting neutrophilic inflammation in severe neutrophilic asthma: can we target the disease-relevant neutrophil phenotype? Journal of Leukocytes Biology 98: 549556.Google Scholar
Bullone, M and Lavoie, JP (2015). Asthma, ‘of horses and men’ – how can equine heaves help us better understand human asthma immunopathology and its functional consequences? Molcular Immunology 66: 97105.Google Scholar
Bureau, F, Bonizzi, G, Kirschvink, N, Delhalle, S, Desmecht, D, Merville, MP, Bours, V and Lekeux, P (2000a). Correlation between nuclear factor-κB activity in bronchial brushing samples and lung dysfunction in an animal model of asthma. American Journal of Respiratory and Critical Care Medicine 161: 13141321.Google Scholar
Bureau, F, Delhalle, S, Bonizzi, G, Fievez, L, Dogne, S, Kirschvink, N, Vanderplasschen, A, Merville, MP, Bours, V and Lekeux, P (2000b). Mechanisms of persistent NF- κB activity in the bronchi of an animal model of asthma. Journal of Immunology 165: 58225830.Google Scholar
Casale, TB and Stoke, JR (2008). Immunomodulators for allergic respiratory disorders. Journal of Allergy and Clinical Immonology 121: 288296.Google Scholar
Cash, JL, Hart, R, Russ, A, Dixon, JP, Colledge, WH, Doran, J, Hendrick, AG, Carlton, MB and Greaves, DR (2008). Synthetic chemerin-derived peptides suppress inflammation through ChemR23. The Journal of Experimental Medicine 205: 767775.Google Scholar
Cesarini, C, Hamilton, E, Picandet, V and Lavoie, JP (2006). Theophylline does not potentiate the effects of a low dose of dexamethasone in horses with recurrent airway obstruction. Equine Veterinary Journal 38: 570573.Google Scholar
Cheng, OZ and Palaniyar, N (2013). NET balancing: a problem in inflammatory lung diseases. Frontiers in Immunology 4: 1.Google Scholar
Cooke, MS, Evans, MD, Dizdaroglu, M and Lunec, L (2003). Oxidative DNA damage: mechanisms, mutation, and disease. FASEB Journal 17: 11951214.Google Scholar
Cordeau, ME, Joubert, P, Dewachi, O, Hamid, Q and Lavoie, JP (2004). IL-4, IL-5 and IFN-γ mRNA expression in pulmonary lymphocytes in equine heaves. Veterinary Immunology and Immunopathology 97: 8796.Google Scholar
Côté, O, Clark, ME, Viel, L, Labbé, G, Seah, SY, Khan, MA, Douda, DN, Palaniyar, N and Bienzle, D (2014). Secretoglobin 1A1 and 1A1A differentially regulate neutrophil reactive oxygen species production, phagocytosis and extracellular trap formation. PLoS ONE 28: 9.Google Scholar
Csiszar, A, Wang, M, Lakatta, EG and Ungvari, Z (2008). Inflammation and endothelial dysfunction during aging: role of NF-kappaB. The Journal of Applied Physiology 105: 13331341.Google Scholar
Couetil, LL, Cardwell, JM, Gerber, V, Lavoie, JP, Leguillette, R and Richard, EA (2016). Inflammatory airway disease of horses – revised consensus statement. Journal of Veterinary Internal Medicine 30: 503515.Google Scholar
Curik, I, Fraser, D, Eder, C, Achmann, R, Swinburne, J, Binns, M, Crameri, R, Brem, G, Sölkner, J and Marti, E (2003). Association between MHC gene region and variation of serum IgE levels against specific mould allergens in the horse. Genetic Selection Evolution 35: 117190.Google Scholar
D'Alessio, FR, Tsushima, K, Aggarwal, NR, West, EE, Willett, MH, Britos, MF, Pipeling, MR, Brower, RG, Tuder, RM, McDyer, JF and King, LS (2009). CD4 + CD25 + Foxp3 + Tregs resolve experimental lung injury in mice and are present in humans with acute lung injury. The Journal of Clinical Investigation 119: 28982913.Google Scholar
Dalli, J, Norling, LV, Renshaw, D, Cooper, D, Leung, KY and Perretti, M (2008). Annexin 1 mediates the rapid anti-inflammatory effects of neutrophil-derived microparticles. Blood 112: 25122519.Google Scholar
Debrue, M, Hamilton, E, Joubert, P, Lajoie-Kadoch, S and Lavoie, JP (2005). Chronic exacerbation of equine heaves is associated with an increased expression of interleukin-17 mRNA in bronchoalveolar lavage cells. Veterinary Immunology and Immunopathology 105: 2531.Google Scholar
Deaton, CM, Marlin, DJ, Smith, NC, Roberts, CA, Harris, PA, Schroter, RC and Kelly, FJ (2005a). Antioxidant and inflammatory responses of healthy horses and horses affected by recurrent airway obstruction to inhaled ozone. Equine Veterinary Journal 37: 243249.Google Scholar
Deaton, CM, Marlin, DJ, Smith, NC, Harris, PA, Dagleish, MP, Schroter, RC and Kelly, FJ (2005b). Effect of acute airway inflammation on the pulmonary antioxidant status. Experimental Lung Research 31: 653670.Google Scholar
Deaton, CM, Marlin, DJ, Smith, NC, Harris, PA, Schroter, RC and Kelly, FJ (2006). Comparasion of the antioxidant status tracheal and bronchoalveolar epithelial lining fluids in recurrent airway obstruction. Equine Veterinary Journal 38: 417422.Google Scholar
DeLuca, L, Erb, HN, Young, JC, Perkins, GA and Ainsworth, DM (2008). The effect of adding oral dexamethasone to feed alterations on the airway cell inflammatory gene expression in stabled horses affected with recurrent airway obstruction. Journal of Veterinary Internal Medicine 22: 427435.Google Scholar
Doelman, CJA, Leurs, R, Oosterom, WC and Bast, A (1990). Mineral dust exposure and free radical-mediated lung damage. Experimental Lung Research 16: 4155.Google Scholar
Elliott, MR, Chekeni, FB, Trampont, PC, Lazarowski, ER, Kadl, A, Walk, SF, Park, D, Woodson, RI, Ostankovich, M, Sharma, P, Lysiak, JJ, Harden, TK, Leitinger, N and Ravichandran, KS (2009). Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461: 282286.Google Scholar
Fadok, VA, Bratton, DL, Konowal, A, Freed, PW, Westcott, JY and Henson, PM (1998). Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. The Journal of Clinical Investigation 101: 890898.Google Scholar
Franke, J and Abraham, G (2014). Concomitant inhibition of primary equine bronchial fibroblast proliferation and differentiation by selective β2-adrenoceptor agonists and dexamethasone. European Journal of Pharmacology 741: 205213.Google Scholar
Fairbairn, SM, Page, CP, Lees, P and Cunningham, FM (1993). Early neutrophil but not eosinophil or platelet recruitment to the lungs of allergic horses following antigen exposure. Clinical and Experimental Allergy 23: 821828.Google Scholar
Feleszko, W, Jaworska, J and Hamelmann, E (2006). Toll-like receptors – novel targets in allergic airway disease (probiotics, friends and relatives). European Journal of Pharmacology 533: 308318.Google Scholar
Franchini, M, Gilli, U, Akens, MK, Fellenberg, RV and Bracher, V (1998). The role of neutrophil chemotactic cytokines in the pathogenesis of equine chronic obstructive pulmonary disease (COPD). Veterinary Immunology and Immunopathology 66: 5365.Google Scholar
Franchini, M, Gill, U, Von Fellenberg, R and Bracher, VV (2000). Interleukin-8 concentration and neutrophil chemotactic activity in bronchoalveolar lavage fluid of horses with chronic obstructive pulmonary disease following exposure to hay. American Journal of Veterinary Research 11: 13691374.Google Scholar
Frossi, B, Carli, M, Daniel, KC, Rivera, J and Pucillo, C (2003). Oxidative stress stimulates IL-4 and IL-6 production in mast cells by an APE/Ref-1-dependent pathway. European Journal of Immunology 33: 21682177.Google Scholar
Gaffen, SL (2009). Structure and signalling in the IL-17 receptor family. Nature Review Immunology 9: 556567.Google Scholar
Gerber, V, Baleri, D, Klukowska-Rötzler, J, Swinburne, JE and Dolf, G (2009). Mixed inheritance of equine recurrent airway obstruction. Journal of Veterinary Internal Medicine 23: 626.Google Scholar
Giguere, S, Viel, L, Lee, E, MacKay, RJ, Hernandez, J and Franchini, M (2002). Cytokine induction in pulmonary airways of horses with heaves and effect of therapy with inhaled fluticasone propionate. Veterinary Immunology and Immunopathology 85: 147158.Google Scholar
Gude, DR, Alvarez, SE, Paugh, SW, Mitra, P, Yu, J, Griffiths, R, Barbour, SE, Milstien, S and Spiegel, S (2008). Apoptosis induces expression of sphingosine kinase 1 to release sphingosine-1-phosphate as a ‘come-and-get-me’ signal. FASEB Journal 22: 26292638.Google Scholar
Gupta, AK, Hasler, P, Holzgreve, W, Gebhardt, S and Hahn, S (2005). Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia. Human Immunology 66: 11461154.Google Scholar
Hallstrand, TS, Hackett, TL, Altemeier, WA, Matute-Bello, G, Hansbro, PM and Knight, DA (2014). Airway epithelial regulation of pulmonary immune homeostasis and inflammation. Clinical Immunology 151: 115.Google Scholar
Henriquez, C, Perez, B, Morales, N, Sarmiento, J, Carrasco, C, Morán, G and Folch, H (2014). Participation of T regulatory cells in equine recurrent airway obstruction. Veterinary Immunology and Immunopathology 158: 128134.Google Scholar
Herszberg, B, Ramos-Barbon, D, Tamaoka, M, Martin, JG and Lavoie, JP (2006). Heaves, an asthma-like equine disease, involves airway smooth muscle remodeling. Journal of Allergy Clinical Immunology 118: 382388.Google Scholar
Höhn, A, König, J and Grune, T (2013). Protein oxidation in aging and the removal of oxidized proteins. Journal of Proteomics 92: 132159.Google Scholar
Horohov, DW, Beadle, RE, Mouch, S and Pourciau, SS (2005). Temporal regulation of cytokine mRNA expression in equine recurrent airway obstruction. Veterinary Immunology and Immunopathology 108: 237245.Google Scholar
Jackson, CA, Berney, C, Jefcoat, AM and Robinson, NE (2000). Environment and prednisone interactions in the treatment of recurrent airway obstruction (heaves). Equine Veterinary Journal 32: 432438.Google Scholar
Joubert, P, Cordeau, ME and Lavoie, JP (2011). Cytokine mRNA expression of pulmonary macrophages varies with challenge but not with disease state in horses with heaves or in controls. Veterinary Immunology and Immunopathology 142: 236242.Google Scholar
Kamiya, H (2003). Mutagenic potentials of damaged nucleic acids produced by reactive oxygen/nitrogen species: approaches using synthetic oligonucleotides and nucleotides: survey and summary. Nucleic Acids Research 31: 517531.Google Scholar
Katsumata, U, Miura, M, Ichinose, M, Kimura, K, Takahashi, T, Inoue, H and Takishima, T (1990). Oxygen radicals produce airway constriction and hyperresponsiveness in anesthetized cats. The American Review of Respiratory Disease 141: 11581161.Google Scholar
Kirkham, PA and Barnes, PJ (2013). Oxidative stress in COPD. Chest 144: 266273.Google Scholar
Kirschvink, N, Smith, N, Fievez, L, Marlin, D and Gustin, P (2002). Effect of chronic airway inflammation and exercise on pulmonary systemic antioxidant status of healthy and heaves-affected horses. Equine Veterinary Journal 34: 563571.Google Scholar
Klier, J, Lehmann, B, Fuchs, S, Reese, S, Hirschmann, A, Coester, C, Winter, G and Gehlen, H (2015). Nanoparticulate CpG immunotherapy in RAO-affected horses: phase I and IIa study. Journal of Veterinary Internal Medicine 29: 286293.Google Scholar
Kleniewska, P and Pawliczak, R (2017). The participation of oxidative stress in the pathogenesis of bronchial asthma. Biomedicine and Pharmacotherapy 94: 100108.Google Scholar
Korn, A, Miller, D, Dong, L, Buckles, EL, Wagner, B and Ainsworth, DM (2015). Differential gene expression profiles and selected cytokine protein analysis of mediastinal lymph nodes of horses with chronic recurrent airway obstruction (RAO) support an interleukin-17 immune response. PLoS ONE 11: e0142622.Google Scholar
Künzle, F, Gerber, V, van der Haegen, A, Wampfler, B, Straub, R and Marti, E (2007). IgE-bearing cells in bronchoalveolar lavage fluid and allergen-specific IgE levels in sera from RAO-affected horses. Journal of Veterinary Medicine. A, Physiology, Pathology, Clinical Medicine 54: 4047.Google Scholar
Lauber, K, Bohn, E, Kröber, SM, Xiao, YJ, Blumenthal, SG, Lindemann, RK, Marini, P, Wiedig, C, Zobywalski, A, Baksh, S, Xu, Y, Autenrieth, IB, Schulze-Osthoff, K, Belka, C, Stuhler, G and Wesselborg, S (2003). Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113: 717730.Google Scholar
Lavoie, JP, Maghni, K, Desnoyers, M, Taha, R, Martin, JG and Hamid, Q (2000). Brocheoalveolar cells from horses with ‘heaves’ express a Th2-type cytokine profile. Proceedings of the Annual Veterinary Medical Forum 18: 751.Google Scholar
Lavoie, JP, Maghni, K, Desnoyers, M, Taha, R, Martin, JG and Hamid, Q (2001). Neutrophilic airway inflammation in horses with heaves is characterized by a Th2-type cytokine profile. American Journal of Respiratory and Critical Care Medicine 164: 14101413.Google Scholar
Leclere, M, Lefebvre-Lavoie, J, Beauchamp, G and Lavoie, JP (2010). Efficacy of oral prednisolone and dexamethasone in horses with recurrent airway obstruction in the presence of continuous antigen exposure. Equine Veterinary Journal 42: 316321.Google Scholar
Leguillette, R (2003). Recurrent airway obstruction-heaves. The Veterinary Clinics Equine Practice 19: 6368.Google Scholar
Ley, K, Laudanna, C, Cybulsky, MI and Nourshargh, S (2007). Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nature Review Immunology 7: 678689.Google Scholar
Li, XJ, Liu, DP, Chen, HL, Pan, XH, Kong, QY and Pang, QF (2012). Lactoferrin protects against lipopolysaccharide-induced acute lung injury in mice. International Immunopharmacology 12: 460464.Google Scholar
Louis, R and Djukanovic, R (2006). Is the neutrophil a worthy target in severe asthma and chronic obstructive pulmonary disease? Clinical and Experimental Allergy 36: 563567.Google Scholar
Mantovani, A, Cassatella, MA, Costantini, C and Jaillon, S (2011). Neutrophils in the activation and regulation of innate and adaptive immunity. Nature Reviews. Immunology 11: 519531.Google Scholar
Martinelli, S, Urosevic, M, Daryadel, A, Oberholzer, PA, Baumann, C, Fey, MF, Dummer, R, Simon, HU and Yousefi, S (2004). Induction of genes mediating interferon-dependent extracellular trap formation during neutrophil differentiation. The Journal of Biological Chemestry 279: 4412344132.Google Scholar
Manzenreiter, R, Kienberger, F, Marcos, V, Schilcher, K, Krautgartner, WD, Obermayer, A, Huml, M, Stoiber, W, Hector, A, Griese, M, Hannig, M, Studnicka, M, Vitkov, L and Hartl, D (2012). Ultrastructural characterization of cystic fibrosis sputum using atomic force and scanning electron microscopy. Journal of Cystic Fibrosis 11: 8492.Google Scholar
Mayadas, TN, Cullere, X and Lowell, CA (2014). The multifaceted functions of neutrophils. Annual Review of Pathology 9: 181218.Google Scholar
Moran, G and Folch, H (2011). Recurrent airway obstruction in horses – an allergic inflammation: a review. Veterinarni Medicina 56: 113.Google Scholar
Morán, G, Araya, O, Ortloff, A and Folch, H (2009). Cytologic bronchoalveolar lavage findings and humoral immune response against Aspergillus fumigatus in Chilotes horses with recurrent airway obstructions ‘heaves’. Archivos de Medicina Veterinaria 41: 8388.Google Scholar
Morán, G, Burgos, R, Araya, O and Folch, H (2010a). In vitro bioassay to detect reaginic antibodies from the serum of horses affected with recurrent airway obstruction. Veterinary Research Communications 34: 9199.Google Scholar
Morán, G, Folch, H, Burgos, R, Araya, O and Barria, M (2010b). Detection of reaginic antibodies against Faenia rectivirgula from the serum of horses affected with recurrent airway obstruction by an in vitro bioassay. Veterinary Research Communications 34: 719726.Google Scholar
Moran, G, Folch, H, Henriquez, C, Ortloff, A and Barria, M (2012). Reaginic antibodies from horses with recurrent airway obstruction produce mast cell stimulation. Veterinary Research Communication 36: 251258.Google Scholar
Murcia, RY, Vargas, A and Lavoie, JP (2016). The interleukin-17 induced activation and increased survival of equine neutrophils Is insensitive to glucocorticoids. PLoS ONE 11: e0154755.Google Scholar
Niedzwiedz, A and Jaworski, Z (2014). Oxidant-antioxidant status in the blood of horses with symptomatic recurrent airway obstruction (RAO). Journal of Veterinary Internal Medicine 28: 18451852.Google Scholar
Noutsios, GT and Floros, J (2014). Childhood asthma: causes, risks, and protective factors; a role of innate immunity. Swiss Medical Weekly 144: w14036.Google Scholar
Ortega-Gomez, A, Perretti, M and Soehnlein, O (2013). Resolution of inflammation: an integrated view. EMBO Molecular Medicine 5: 661674.Google Scholar
Ouyang, W, Kolls, JK and Zheng, Y (2008). The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28: 454467.Google Scholar
Papayannopoulos, V, Metzler, KD, Hakkim, A and Zychlinsky, A (2010). Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. The Journal of Cell Biology 191: 677691.Google Scholar
Perez, B, Henriquez, C, Sarmiento, J, Morales, N, Folch, H, Galesio, JS, Uberti, B and Morán, G (2016). Tamoxifen as a new therapeutic tool for neutrophilic lung inflammation. Respirology 21: 112118.Google Scholar
Perretti, M and D'Acquisto, F (2009). Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nature Reviews. Immunology 9: 6270.Google Scholar
Perretti, M and Solito, E (2004). Annexin 1 and neutrophil apoptosis. Biochemical Society Transactions 32: 507510.Google Scholar
Perretti, M, Chiang, N, La, M, Fierro, IM, Marullo, S, Getting, SJ, Solito, E and Serhan, CN (2002). Endogenous lipid- and peptide-derived anti-inflammatory pathways generated with glucocorticoid and aspirin treatment activate the lipoxin A4 receptor. Nature Medicine 8: 12961302.Google Scholar
Pietra, M, Peli, A, Bonato, A, Ducci, A and Cinotti, S (2007). Equine bronchoalveolar lavage cytokines in the development of recurrent airway obstruction. Veterinary Research Communications 31: 313316.Google Scholar
Pirie, RS, Collie, DDS, Dixon, PM and McGorum, BC (2002). Evaluation of nebulised hay dust suspensions (HDS) for the diagnosis and investigation of heaves. Effects of Inhaled HDS on Control and Heaves Horses. Equine Veterinary Journal 34: 337342.Google Scholar
Pirie, RS, Collie, DD, Dixon, PM and McGorum, BC (2003). Inhaled endotoxin and organic dust particulates have synergistic proinflammatory effects in equine heaves (organic dust induced asthma). Clinical and Experimental Allergy 33: 676683.Google Scholar
Pirie, RS, Couëtil, LL, Robinson, NE and Lavoie, JP (2016). Equine asthma: an appropriate, translational and comprehendible terminology? Equine Veterinary Journal 48: 403405.Google Scholar
Porto, BN and Stein, RT (2016). Neutrophil extracellular traps in pulmonary diseases: too much of a good thing? Frontiers in Immunology 7: 311.Google Scholar
Ramirez-Velazquez, C, Castillo, EC, Guido-Bayardo, L and Ortiz-Navarrete, V (2013). IL-17-producing peripheral blood CD177 + neutrophils increase in allergic asthmatic subjects. Allergy Asthma and Clinical Immunology 9: 23.Google Scholar
Ramseyer, A, Gaillard, C, Burger, D, Straub, R, Jost, U, Boog, C, Marti, E and Gerber, V (2007). Effects of genetic and environmental factors on chronic lower airway disease in horses. Journal of Veterinary Internal Medicine 21: 149156.Google Scholar
Reddy, VP, Beyaz, A, Perry, G, Cooke, M, Sayre, LM and Smith, MA (2005). The role of oxidative damage to nucleic acids in the pathogenesis of neurological disease. Neurodegenerative Diseases 6: 535544.Google Scholar
Ribechini, E, Greifenberg, V, Sandwick, S and Lutz, MB (2010). Subsets, expansion and activation of myeloid-derived suppressor cells. Medical Microbiology and Immunology 199: 273281.Google Scholar
Ribeiro, C and Brehelin, M (2006). Insect haemocytes: what type of cell is that? Journal of Insect Physiology 52: 417429.Google Scholar
Riihimäki, M, Raine, A, Art, T, Lekeux, P, Couëtil, L and Pringle, J (2008). Partial divergence of cytokine mRNA expression bronchial tissues compared to bronchoalveolar lavage cells in horses with recurrent airway obstruction. Veterinary Immunology and Immunopathology 122: 256264.Google Scholar
Robb, CT, Regan, KH, Dorward, DA and Rossi, AG (2016). Key mechanisms governing resolution of lung inflammation. Seminars in Immunopathology 38: 425448.Google Scholar
Robinson, NE (2001). International workshop on equine chronic airway disease Michigan State University. Equine Veterinary Journal 33: 519.Google Scholar
Robinson, NE, Derksen, FJ, Olszewski, M and Buechner-Maxwell, VA (1996). The pathogenesis of chronic obstructive pulmonary disease of horses. The British Veterinary Journal 152: 283306.Google Scholar
Robinson, NE, Berney, C, Behan, A and Derksen, FJ (2009). Fluticasone propionate aerosol is more effective for prevention than treatment of recurrent airway obstruction. Journal of Veterinary Internal Medicine 23: 12471253.Google Scholar
Saffarzadeh, M, Juenemann, C, Queisser, MA, Lochnit, G, Barreto, G, Galuska, SP, Lohmeyer, J and Preissner, KT (2012). Neutrophils extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS ONE 7: e32366.Google Scholar
Sarmiento, J, Perez, B, Morales, N, Henriquez, C, Vidal, L, Folch, H, Galecio, JS and Morán, G (2013). Apoptotic effects of tamoxifen on leukocytes from horse peripheral blood and bronchoalveolar lavage fluid. Veterinary Research Communications 37: 333338.Google Scholar
Savage, ND, de Boer, T, Walburg, KV, Joosten, SA, van Meijgaarden, K, Geluk, A and Ottenhoff, TH (2008). Human anti-inflammatory macrophages induce Foxp3 + GITR + CD25 + regulatory T cells, which suppress via membrane-bound TGFbeta-1. Journal of Immunology 181: 22202226.Google Scholar
Scannell, M, Flanagan, MB, deStefani, A, Wynne, KJ, Cagney, G, Godson, C and Maderna, P (2007). Annexin-1 and peptide derivatives are released by apoptotic cells and stimulate phagocytosis of apoptotic neutrophils by macrophages. Journal of Immunology 178: 45954605.Google Scholar
Schmidt-Weber, CB, Akdis, M and Akdis, CA (2007). TH17 cells in the big picture of immunology. The Journal of Allergy and Clinical Immunology 120: 247254.Google Scholar
Schuliga, M (2015). NF-kappaB signaling in chronic inflammatory airway disease. Biomolecules 5: 12661283.Google Scholar
Serhan, CN, Chiang, N and Van Dyke, TE (2008). Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nature Reviews. Immunology 8: 349361.Google Scholar
Scharrenberg, A, Gerber, V, Swinburne, JE, Wilson, AD, Klukowska-Rotzler, J, Laumen, E and Marti, E (2010). IgE, IgGa, IgGb and IgG(T) serum antibody levels in offspring of two sires affected with equine recurrent airway obstruction. Animal Genetic 41: 131137.Google Scholar
Sukkar, MB, Xie, S, Khorasani, NM, Kon, OM, Stanbridge, R, Issa, R and Chung, KF (2006). Toll-like receptor 2, 3, and 4 expression and function in human airway smooth muscle. Journal of Allergy Clinical Immunology 118: 641648.Google Scholar
Tahon, L, Baselgia, S, Gerber, V, Doherr, MG, Straub, R, Robinson, NE and Marti, E (2009). In vitro allergy test compared to intradermal testing in horses with recurrent airway obstruction. Veterinary Immunology and Immunopathology 127: 8593.Google Scholar
Takeda, K, Kaisho, T and Akira, S (2003). Toll-like receptors. Annual Review of Immunology 21: 335376.Google Scholar
Tintinger, GR, Anderson, R and Feldman, C (2013). Pharmacological approaches to regulate neutrophil activity. Seminars in Immunopathology 35: 395409.Google Scholar
Truman, LA, Ford, CA, Pasikowska, M, Pound, JD, Wilkinson, SJ, Dumitriu, IE, Melville, L, Melrose, LA, Ogden, CA, Nibbs, R, Graham, G, Combadiere, C and Gregory, CD (2008). CX3CL1/fractalkine is released from apoptotic lymphocytes to stimulate macrophage chemotaxis. Blood 112: 50265036.Google Scholar
Turlej, RK, Fievez, L, Sandersen, CF, Dogné, S, Kirschvink, N, Lekeux, P and Bureau, F (2001). Enhanced survival of lung granulocytes in an animal model of asthma: evidence for a role of GM-CSF activated STAT5 signaling pathway. Thorax 56: 696702.Google Scholar
Uddin, M, Lau, LC, Seumois, G, Vijayanand, P, Staples, KJ, Bagmane, D, Cornelius, V, Dorinsky, P, Davies, DE and Djukanovi´c, R (2013). EGF-induced bronchial epithelial cells drive neutrophil chemotactic and anti-apoptotic activity in asthma. PLoS ONE 8: e72502.Google Scholar
Urban, CF, Ermert, D, Schmid, M, Abu-Abed, U, Goosmann, C, Nacken, W, Brinkmann, V, Jungblut, PR and Zychlinsky, A (2009). Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathology 5: e1000639.Google Scholar
Weiss, EB and Bellino, JR (1986). Leukotriene-associated toxic oxygen metabolites induces airway hyperreactivity. Chest 89: 709716.Google Scholar
Xu, J, Zhang, X, Pelayo, R, Monestier, M, Ammollo, CT, Semeraro, F, Taylor, FB, Esmon, NL, Lupu, F and Esmon, CT (2009). Extracellular histones are major mediators of death in sepsis. Nature Medicine 15: 13181321.Google Scholar
Zuo, L, Otenbaker, NP, Rose, BA and Salisbury, KS (2013). Molecular mechanisms of reactive oxygen species-related pulmonary inflammation and asthma. Molecular Immunology 56: 5763.Google Scholar