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Original Research

Modeling the pasture-associated severe equine asthma bronchoalveolar lavage fluid proteome identifies molecular events mediating neutrophilic airway inflammation

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Pages 43-63 | Published online: 02 May 2019

References

  • Wenzel SE. Asthma phenotypes: the evolution from clinical to molecular approaches. Nat Med. 2012;18(5):716–725. doi:10.1038/nm.267822561835
  • Coleman RA. Current animal models are not predictive for clinical asthma. Pulm Pharmacol Ther. 1999;12(2):87–89. doi:10.1006/pupt.1999.019310373387
  • Jatakanon A, Lim S, Barnes PJ. Changes in sputum eosinophils predict loss of asthma control. Am J Respir Crit Care Med. 2000;161(1):64–72. doi:10.1164/ajrccm.161.1.980910010619799
  • Douwes J, Gibson P, Pekkanen J, Pearce N. Non-eosinophilic asthma: importance and possible mechanisms. Thorax. 2002;57(7):643–648.12096210
  • Chang HS, Lee TH, Jun JA, et al. Neutrophilic inflammation in asthma: mechanisms and therapeutic considerations. Expert Rev Respir Med. 2017;11(1):29–40. doi:10.1080/17476348.2017.126891927918221
  • Lambrecht BN, Hammad H. The immunology of asthma. Nat Immunol. 2015;16(1):45–56. doi:10.1038/ni.304925521684
  • Jatakanon A, Uasuf C, Maziak W, Lim S, Chung KF, Barnes PJ. Neutrophilic inflammation in severe persistent asthma. Am J Respir Crit Care Med. 1999;160(5 Pt 1):1532–1539. doi:10.1164/ajrccm.160.5.980617010556116
  • Little SA, MacLeod KJ, Chalmers GW, Love JG, McSharry C, Thomson NC. Association of forced expiratory volume with disease duration and sputum neutrophils in chronic asthma. Am J Med. 2002;112(6):446–452.11959054
  • Wenzel SE, Szefler SJ, Leung DY, Sloan SI, Rex MD, Martin RJ. Bronchoscopic evaluation of severe asthma. Persistent inflammation associated with high dose glucocorticoids. Am J Respir Crit Care Med. 1997;156(3 Pt 1):737–743. doi:10.1164/ajrccm.156.3.96100469309987
  • Green RH, Brightling CE, Woltmann G, Parker D, Wardlaw AJ, Pavord ID. Analysis of induced sputum in adults with asthma: identification of subgroup with isolated sputum neutrophilia and poor response to inhaled corticosteroids. Thorax. 2002;57(10):875–879.12324674
  • Pavord ID, Brightling CE, Woltmann G, Wardlaw AJ. Non-eosinophilic corticosteroid unresponsive asthma. Lancet. 1999;353(9171):2213–2214. doi:10.1016/S0140-6736(99)01813-910392993
  • Wenzel SE, Schwartz LB, Langmack EL, et al. Evidence that severe asthma can be divided pathologically into two inflammatory subtypes with distinct physiologic and clinical characteristics. Am J Respir Crit Care Med. 1999;160(3):1001–1008. doi:10.1164/ajrccm.160.3.981211010471631
  • Fahy JV, Kim KW, Liu J, Boushey HA. Prominent neutrophilic inflammation in sputum from subjects with asthma exacerbation. J Allergy Clin Immunol. 1995;95(4):843–852.7722165
  • Martin RJ, Cicutto LC, Smith HR, Ballard RD, Szefler SJ. Airways inflammation in nocturnal asthma. Am Rev Respir Dis. 1991;143(2):351–357. doi:10.1164/ajrccm/143.2.3511990952
  • Chalmers GW, MacLeod KJ, Thomson L, Little SA, McSharry C, Thomson NC. Smoking and airway inflammation in patients with mild asthma. Chest. 2001;120(6):1917–1922.11742922
  • Anees W, Huggins V, Pavord ID, Robertson AS, Burge PS. Occupational asthma due to low molecular weight agents: eosinophilic and non-eosinophilic variants. Thorax. 2002;57(3):231–236.11867827
  • Sur S, Crotty TB, Kephart GM, et al. Sudden-onset fatal asthma. A distinct entity with few eosinophils and relatively more neutrophils in the airway submucosa? Am Rev Respir Dis. 1993;148(3):713–719. doi:10.1164/ajrccm/148.3.7138368644
  • Bruijnzeel PL, Uddin M, Koenderman L. Targeting neutrophilic inflammation in severe neutrophilic asthma: can we target the disease-relevant neutrophil phenotype? J Leukoc Biol. 2015;98(4):549–556. doi:10.1189/jlb.3VMR1214-600RR25977288
  • Chesne J, Braza F, Mahay G, Brouard S, Aronica M, Magnan A. IL-17 in severe asthma. Where do we stand? Am J Respir Crit Care Med. 2014;190(10):1094–1101. doi:10.1164/rccm.201405-0859PP25162311
  • Fernandes DJ, Xu KF, Stewart AG. Anti-remodelling drugs for the treatment of asthma: requirement for animal models of airway wall remodelling. Clin Exp Pharmacol Physiol. 2001;28(8):619–629.11473527
  • Sagar S, Akbarshahi H, Uller L. Translational value of animal models of asthma: challenges and promises. Eur J Pharmacol. 2015;759:272–277. doi:10.1016/j.ejphar.2015.03.03725823808
  • Robinson NE, Derksen FJ, Olszewski MA, Buechner-Maxwell VA. The pathogenesis of chronic obstructive pulmonary disease of horses. Br Vet J. 1996;152(3):283–306.8762605
  • Seahorn TL, Groves MG, Harrington KS, Beadle RE. Chronic obstructive pulmonary disease in horses in Louisiana. J Am Vet Med Assoc. 1996;208(2):248–251.8567383
  • Derksen FJ, Robinson NE, Armstrong PJ, Stick JA, Slocombe RF. Airway reactivity in ponies with recurrent airway obstruction (heaves). J Appl Physiol (1985). 1985;58(2):598–604. doi:10.1152/jappl.1985.58.2.5983980362
  • Jost U, Klukowska-Rotzler J, Dolf G, et al. A region on equine chromosome 13 is linked to recurrent airway obstruction in horses. Equine Vet J. 2007;39(3):236–241.17520975
  • Kaup FJ, Drommer W, Damsch S, Deegen E. Ultrastructural findings in horses with chronic obstructive pulmonary disease (COPD). II: pathomorphological changes of the terminal airways and the alveolar region. Equine Vet J. 1990;22(5):349–355.2226400
  • Pirie RS, Collie DD, Dixon PM, McGorum BC. Inhaled endotoxin and organic dust particulates have synergistic proinflammatory effects in equine heaves (organic dust-induced asthma). Clin Exp Allergy. 2003;33(5):676–683.12752598
  • Costa LR, Seahorn TL, Moore RM, Taylor HW, Gaunt SD, Beadle RE. Correlation of clinical score, intrapleural pressure, cytologic findings of bronchoalveolar fluid, and histopathologic lesions of pulmonary tissue in horses with summer pasture-associated obstructive pulmonary disease. Am J Vet Res. 2000;61(2):167–173.10685689
  • Leclere M, Lavoie-Lamoureux A, Gelinas-Lymburner E, David F, Martin JG, Lavoie JP. Effect of antigenic exposure on airway smooth muscle remodeling in an equine model of chronic asthma. Am J Respir Cell Mol Biol. 2011;45(1):181–187. doi:10.1165/rcmb.2010-0300OC20935189
  • Leclere M, Lavoie-Lamoureux A, Lavoie JP. Heaves, an asthma-like disease of horses. Respirology. 2011;16(7):1027–1046. doi:10.1111/j.1440-1843.2011.02033.x21824219
  • Bullone M, Lavoie JP. Asthma “of horses and men”–how can equine heaves help us better understand human asthma immunopathology and its functional consequences? Mol Immunol. 2015;66(1):97–105. doi:10.1016/j.molimm.2014.12.00525547716
  • Ferrari CR, Cooley J, Mujahid N, et al. Horses with pasture asthma have airway remodeling that is characteristic of human asthma. Vet Pathol. 2018;55(1):144–158. doi:10.1177/030098581774172929254472
  • Neurohr C, Huppmann P, Samweber B, et al. Prognostic value of bronchoalveolar lavage neutrophilia in stable lung transplant recipients. J Heart Lung Transplant. 2009;28(5):468–474. doi:10.1016/j.healun.2009.01.01419416775
  • Papi A, Bellettato CM, Braccioni F, et al. Infections and airway inflammation in chronic obstructive pulmonary disease severe exacerbations. Am J Respir Crit Care Med. 2006;173(10):1114–1121. doi:10.1164/rccm.200506-859OC16484677
  • Cohen-Cymberknoh M, Kerem E, Ferkol T, Elizur A. Airway inflammation in cystic fibrosis: molecular mechanisms and clinical implications. Thorax. 2013;68(12):1157–1162. doi:10.1136/thoraxjnl-2013-20320423704228
  • Leira R, Davalos A, Silva Y, et al. Early neurologic deterioration in intracerebral hemorrhage: predictors and associated factors. Neurology. 2004;63(3):461–467.15304576
  • Dominguez M, Miquel R, Colmenero J, et al. Hepatic expression of CXC chemokines predicts portal hypertension and survival in patients with alcoholic hepatitis. Gastroenterology. 2009;136(5):1639–1650. doi:10.1053/j.gastro.2009.01.05619208360
  • Chia S, Nagurney JT, Brown DF, et al. Association of leukocyte and neutrophil counts with infarct size, left ventricular function and outcomes after percutaneous coronary intervention for ST-elevation myocardial infarction. Am J Cardiol. 2009;103(3):333–337. doi:10.1016/j.amjcard.2008.09.08519166685
  • Papa A, Emdin M, Passino C, Michelassi C, Battaglia D, Cocci F. Predictive value of elevated neutrophil-lymphocyte ratio on cardiac mortality in patients with stable coronary artery disease. Clin Chim Acta. 2008;395(1–2):27–31. doi:10.1016/j.cca.2008.04.01918498767
  • Takahashi T, Hiasa Y, Ohara Y, et al. Relationship of admission neutrophil count to microvascular injury, left ventricular dilation, and long-term outcome in patients treated with primary angioplasty for acute myocardial infarction. Circ J. 2008;72(6):867–872.18503208
  • Tamhane UU, Aneja S, Montgomery D, Rogers EK, Eagle KA, Gurm HS. Association between admission neutrophil to lymphocyte ratio and outcomes in patients with acute coronary syndrome. Am J Cardiol. 2008;102(6):653–657. doi:10.1016/j.amjcard.2008.05.00618773982
  • Nunez J, Nunez E, Bodi V, et al. Usefulness of the neutrophil to lymphocyte ratio in predicting long-term mortality in ST segment elevation myocardial infarction. Am J Cardiol. 2008;101(6):747–752. doi:10.1016/j.amjcard.2007.11.00418328833
  • Kayrak M, Erdogan HI, Solak Y, et al. Prognostic value of neutrophil to lymphocyte ratio in patients with acute pulmonary embolism: a restrospective study. Heart Lung Circ. 2014;23(1):56–62. doi:10.1016/j.hlc.2013.06.00423856365
  • Halazun KJ, Hardy MA, Rana AA, et al. Negative impact of neutrophil-lymphocyte ratio on outcome after liver transplantation for hepatocellular carcinoma. Ann Surg. 2009;250(1):141–151. doi:10.1097/SLA.0b013e3181a77e5919561458
  • Gomez D, Farid S, Malik HZ, et al. Preoperative neutrophil-to-lymphocyte ratio as a prognostic predictor after curative resection for hepatocellular carcinoma. World J Surg. 2008;32(8):1757–1762. doi:10.1007/s00268-008-9552-618340479
  • Kishi Y, Kopetz S, Chun YS, Palavecino M, Abdalla EK, Vauthey JN. Blood neutrophil-to-lymphocyte ratio predicts survival in patients with colorectal liver metastases treated with systemic chemotherapy. Ann Surg Oncol. 2009;16(3):614–622. doi:10.1245/s10434-008-0267-619130139
  • Teramukai S, Kitano T, Kishida Y, et al. Pretreatment neutrophil count as an independent prognostic factor in advanced non-small-cell lung cancer: an analysis of Japan multinational trial organisation LC00-03. Eur J Cancer. 2009;45(11):1950–1958. doi:10.1016/j.ejca.2009.01.02319231158
  • Balch WE, Morimoto RI, Dillin A, Kelly JW. Adapting proteostasis for disease intervention. Science. 2008;319(5865):916–919. doi:10.1126/science.114144818276881
  • Bouchecareilh M, Balch WE. Proteostasis, an emerging therapeutic paradigm for managing inflammatory airway stress disease. Curr Mol Med. 2012;12(7):815–826.22697348
  • Bright LA, Mujahid N, Nanduri B, et al. Functional modelling of an equine bronchoalveolar lavage fluid proteome provides experimental confirmation and functional annotation of equine genome sequences. Anim Genet. 2011;42(4):395–405. doi:10.1111/j.1365-2052.2010.02158.x21749422
  • Costa LR, Eades SC, Venugopal CS, Moore RM. Plasma and pulmonary fluid endothelin in horses with seasonal recurrent airway obstruction. J Vet Intern Med. 2009;23(6):1239–1246. doi:10.1111/j.1939-1676.2009.0385.x19761476
  • Bright LA, Burgess SC, Chowdhary B, Swiderski CE, McCarthy FM. Structural and functional-annotation of an equine whole genome oligoarray. BMC Bioinformatics. 2009;10(Suppl 11):S8. doi:10.1186/1471-2105-10-S11-S8
  • Seahorn TL, Beadle RE, McGorum BC, Marley CL. Quantification of antigen-specific antibody concentrations in tracheal lavage fluid of horses with summer pasture-associated obstructive pulmonary disease. Am J Vet Res. 1997;58(12):1408–1411.9401689
  • McCarthy FM, Cooksey AM, Wang N, Bridges SM, Pharr GT, Burgess SC. Modeling a whole organ using proteomics: the avian bursa of Fabricius. Proteomics. 2006;6(9):2759–2771. doi:10.1002/pmic.20050064816596704
  • Pendarvis K, Kumar R, Burgess SC, Nanduri B. An automated proteomic data analysis workflow for mass spectrometry. BMC Bioinformatics. 2009;10(Suppl 11):S17. doi:10.1186/1471-2105-10-S11-S17
  • McCarthy FM, Bridges SM, Burgess SC. GOing from functional genomics to biological significance. Cytogenet Genome Res. 2007;117(1–4):278–287. doi:10.1159/00010318917675869
  • Manda P, Freeman MG, Bridges SM, et al. GOModeler–a tool for hypothesis-testing of functional genomics datasets. BMC Bioinformatics. 2010;11(Suppl 6):S29. doi:10.1186/1471-2105-11-S6-S29
  • Durinck S, Moreau Y, Kasprzyk A, et al. BioMart and Bioconductor: a powerful link between biological databases and microarray data analysis. Bioinformatics. 2005;21(16):3439–3440. doi:10.1093/bioinformatics/bti52516082012
  • Kramer A, Green J, Pollard J Jr., Tugendreich S. Causal analysis approaches in ingenuity pathway analysis. Bioinformatics. 2014;30(4):523–530. doi:10.1093/bioinformatics/btt70324336805
  • Nakagome K, Matsushita S, Nagata M. Neutrophilic inflammation in severe asthma. Int Arch Allergy Immunol. 2012;158(Suppl 1):96–102. doi:10.1159/00033780122627375
  • Ndukwu IM, Naureckas ET, Maxwell C, Waldman M, Leff AR. Relationship of cellular transmigration and airway response after allergen challenge. Am J Respir Crit Care Med. 1999;160(5 Pt 1):1516–1524. doi:10.1164/ajrccm.160.5.981212610556114
  • Marcal LE, Rehder J, Newburger PE, Condino-Neto A. Superoxide release and cellular gluthatione peroxidase activity in leukocytes from children with persistent asthma. Braz J Med Biol Res. 2004;37(11):1607–1613. S0100-879X200400110000315517074
  • Lacy P, Abdel-Latif D, Steward M, Musat-Marcu S, Man SF, Moqbel R. Divergence of mechanisms regulating respiratory burst in blood and sputum eosinophils and neutrophils from atopic subjects. J Immunol. 2003;170(5):2670–2679.12594296
  • Bedi P, Davidson DJ, McHugh BJ, Rossi AG, Hill AT. Blood neutrophils are reprogrammed in bronchiectasis. Am J Respir Crit Care Med. 2018. doi:10.1164/rccm.201712-2423OC
  • Oreo KM, Gibson PG, Simpson JL, Wood LG, McDonald VM, Baines KJ. Sputum ADAM8 expression is increased in severe asthma and COPD. Clin Exp Allergy. 2014;44(3):342–352. doi:10.1111/cea.1222324147597
  • Radeau T, Chavis C, Damon M, Michel FB. Crastes de Paulet A, Godard PH. Enhanced arachidonic acid metabolism and human neutrophil migration in asthma. Prostaglandins Leukot Essent Fatty Acids. 1990;41(2):131–138.2125732
  • Lavinskiene S, Bajoriuniene I, Malakauskas K, Jeroch J, Sakalauskas R. Sputum neutrophil count after bronchial allergen challenge is related to peripheral blood neutrophil chemotaxis in asthma patients. Inflamm Res. 2014;63(11):951–959. doi:10.1007/s00011-014-0770-025213267
  • Ozier A, Allard B, Bara I, et al. The pivotal role of airway smooth muscle in asthma pathophysiology. J Allergy (Cairo). 2011;2011:742710.22220184
  • Nissen G, Hollaender H, Tang FSM, et al. Tumstatin fragment selectively inhibits neutrophil infiltration in experimental asthma exacerbation. Clin Exp Allergy. 2018. doi:10.1111/cea.13236
  • Bullone M, Moran K, Lavoie-Lamoureux A, Lavoie JP. PI3K and MAPKs regulate neutrophil migration toward the airways in heaves. J Vet Intern Med. 2013;27(1):164–170. doi:10.1111/jvim.1200823194017
  • 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;61(11):1369–1374.11108181
  • Tessier L, Cote O, Clark ME, et al. Impaired response of the bronchial epithelium to inflammation characterizes severe equine asthma. BMC Genomics. 2017;18(1):708. doi:10.1186/s12864-016-3396-528886691
  • Kumar SD, Krishnamurthy K, Manikandan J, Pakeerappa PN, Pushparaj PN. Deciphering the key molecular and cellular events in neutrophil transmigration during acute inflammation. Bioinformation. 2011;6(3):111–114.21584186
  • Kidney JC, Proud D. Neutrophil transmigration across human airway epithelial monolayers: mechanisms and dependence on electrical resistance. Am J Respir Cell Mol Biol. 2000;23(3):389–395. doi:10.1165/ajrcmb.23.3.406810970831
  • Martin TR, Raghu G, Maunder RJ, Springmeyer SC. The effects of chronic bronchitis and chronic air-flow obstruction on lung cell populations recovered by bronchoalveolar lavage. Am Rev Respir Dis. 1985;132(2):254–260. doi:10.1164/arrd.1985.132.2.2544026050
  • Murphy AJ, Woollard KJ, Suhartoyo A, et al. Neutrophil activation is attenuated by high-density lipoprotein and apolipoprotein A-I in in vitro and in vivo models of inflammation. Arterioscler Thromb Vasc Biol. 2011;31(6):1333–1341. doi:10.1161/ATVBAHA.111.22625821474825
  • Montecucco F, Vuilleumier N, Pagano S, et al. Anti-Apolipoprotein A-1 auto-antibodies are active mediators of atherosclerotic plaque vulnerability. Eur Heart J. 2011;32(4):412–421. doi:10.1093/eurheartj/ehq52121224292
  • Marshall LJ, Perks B, Ferkol T, Shute JK. IL-8 released constitutively by primary bronchial epithelial cells in culture forms an inactive complex with secretory component. J Immunol. 2001;167(5):2816–2823.11509627
  • Arslan F, Smeets MB, Buttari B, et al. Lack of haptoglobin results in unbalanced VEGFalpha/angiopoietin-1 expression, intramural hemorrhage and impaired wound healing after myocardial infarction. J Mol Cell Cardiol. 2013;56:116–128. doi:10.1016/j.yjmcc.2012.12.01223274064
  • Yao X, Gordon EM, Figueroa DM, Barochia AV, Levine SJ. Emerging roles of Apolipoprotein E and Apolipoprotein A-I in the pathogenesis and treatment of lung disease. Am J Respir Cell Mol Biol. 2016;55(2):159–169. doi:10.1165/rcmb.2016-0060TR27073971
  • Yao X, Gordon EM, Barochia AV, Remaley AT, Levine SJ. The A‘s have it: developing apolipoprotein A-I mimetic peptides into a novel treatment for asthma. Chest. 2016;150(2):283–288. doi:10.1016/j.chest.2016.05.03527327118
  • Barochia AV, Kaler M, Cuento RA, et al. Serum apolipoprotein A-I and large high-density lipoprotein particles are positively correlated with FEV1 in atopic asthma. Am J Respir Crit Care Med. 2015;191(9):990–1000. doi:10.1164/rccm.201411-1990OC25692941
  • Gordon EM, Figueroa DM, Barochia AV, Yao X, Levine SJ. High-density lipoproteins and Apolipoprotein A-I: potential new players in the prevention and treatment of lung disease. Front Pharmacol. 2016;7:323. doi:10.3389/fphar.2016.0032327708582
  • Park SW, Lee EH, Lee EJ, et al. Apolipoprotein A1 potentiates lipoxin A4 synthesis and recovery of allergen-induced disrupted tight junctions in the airway epithelium. Clin Exp Allergy. 2013;43(8):914–927.23889245
  • Asano M, Komiyama K. Polymeric immunoglobulin receptor. J Oral Sci. 2011;53(2):147–156.21712618
  • Ladjemi MZ, Gras D, Dupasquier S, et al. Bronchial epithelial IgA secretion is impaired in asthma. Role of IL-4/IL-13. Am J Respir Crit Care Med. 2018;197(11):1396–1409. doi:10.1164/rccm.201703-0561OC29652177
  • Larsen K, Macleod D, Nihlberg K, et al. Specific haptoglobin expression in bronchoalveolar lavage during differentiation of circulating fibroblast progenitor cells in mild asthma. J Proteome Res. 2006;5(6):1479–1483. doi:10.1021/pr050462h16739999
  • Kim CK, Chung CY, Koh YY. Changes in serum haptoglobin level after allergen challenge test in asthmatic children. Allergy. 1998;53(2):184–189.9534918
  • Huynh ML, Malcolm KC, Kotaru C, et al. Defective apoptotic cell phagocytosis attenuates prostaglandin E2 and 15-hydroxyeicosatetraenoic acid in severe asthma alveolar macrophages. Am J Respir Crit Care Med. 2005;172(8):972–979. doi:10.1164/rccm.200501-035OC16040786
  • Uddin M, Nong G, Ward J, et al. Prosurvival activity for airway neutrophils in severe asthma. Thorax. 2010;65(8):684–689. doi:10.1136/thx.2009.12074120685741
  • Parfrey H, Farahi N, Porter L, Chilvers ER. Live and let die: is neutrophil apoptosis defective in severe asthma? Thorax. 2010;65(8):665–667. doi:10.1136/thx.2009.13427020685738
  • Alexis NE, Eldridge MW, Peden DB. Effect of inhaled endotoxin on airway and circulating inflammatory cell phagocytosis and CD11b expression in atopic asthmatic subjects. J Allergy Clin Immunol. 2003;112(2):353–361.12897742
  • Saffar AS, Alphonse MP, Shan L, Hayglass KT, Simons FE, Gounni AS. IgE modulates neutrophil survival in asthma: roleof mitochondrial pathway. J Immunol. 2007;178(4):2535–2541.17277162
  • Niedzwiedz A, Jaworski Z, Tykalowski B, Smialek M. Neutrophil and macrophage apoptosis in bronchoalveolar lavage fluid from healthy horses and horses with recurrent airway obstruction (RAO). BMC Vet Res. 2014;10:29. doi:10.1186/1746-6148-10-124460911
  • Brazil TJ, Dagleish MP, McGorum BC, Dixon PM, Haslett C, Chilvers ER. Kinetics of pulmonary neutrophil recruitment and clearance in a natural and spontaneously resolving model of airway inflammation. Clin Exp Allergy. 2005;35(7):854–865. doi:10.1111/j.1365-2222.2005.02231.x16008670
  • Zhang B, Hirahashi J, Cullere X, Mayadas TN. Elucidation of molecular events leading to neutrophil apoptosis following phagocytosis: cross-talk between caspase 8, reactive oxygen species, and MAPK/ERK activation. J Biol Chem. 2003;278(31):28443–28454. doi:10.1074/jbc.M21072720012736263
  • Coxon A, Rieu P, Barkalow FJ, et al. A novel role for the beta 2 integrin CD11b/CD18 in neutrophil apoptosis: a homeostatic mechanism in inflammation. Immunity. 1996;5(6):653–666.8986723
  • Watson RW, Redmond HP, Wang JH, Condron C, Bouchier-Hayes D. Neutrophils undergo apoptosis following ingestion of Escherichia coli. J Immunol. 1996;156(10):3986–3992.8621940
  • Gao H, Ying S, Dai Y. Pathological roles of neutrophil-mediated inflammation in asthma and its potential for therapy as a target. J Immunol Res. 2017;2017:3743048. doi:10.1155/2017/597457429359169
  • Mann BS, Chung KF. Blood neutrophil activation markers in severe asthma: lack of inhibition by prednisolone therapy. Respir Res. 2006;7:59. doi:10.1186/1465-9921-7-5916600024
  • Ciepiela O, Ostafin M, Demkow U. Neutrophils in asthma–a review. Respir Physiol Neurobiol. 2015;209:13–16. doi:10.1016/j.resp.2014.12.00425511380
  • Durham SR, Carroll M, Walsh GM, Kay AB. Leukocyte activation in allergen-induced late-phase asthmatic reactions. N Engl J Med. 1984;311(22):1398–1402. doi:10.1056/NEJM1984112931122026387491
  • Ward C, Kelly CA, Stenton SC, Duddridge M, Hendrick DJ, Walters EH. The relative contribution of bronchoalveolar macrophages and neutrophils to lucigenin- and luminol-amplified chemiluminescence. Eur Respir J. 1990;3(9):1008–1014.2289547
  • Kallenbach J, Baynes R, Fine B, Dajee D, Bezwoda W. Persistent neutrophil activation in mild asthma. J Allergy Clin Immunol. 1992;90(2):272–274.1323589
  • Monteseirin J, Camacho MJ, Bonilla I, et al. Respiratory burst in neutrophils from asthmatic patients. J Asthma. 2002;39(7):619–624.12442951
  • Teramoto S, Shu CY, Ouchi Y, Fukuchi Y. Increased spontaneous production and generation of superoxide anion by blood neutrophils in patients with asthma. J Asthma. 1996;33(3):149–155.8675493
  • Sakai C, Miura R, Shibata A. [Activation of neutrophil alkaline phosphatase of chronic myelogenous leukemia in vitro liquid culture: transferrin as a NAP-activating factor]. Nihon Ketsueki Gakkai Zasshi. 1987;50(3):582–588.3480674
  • Wettero J, Bengtsson T, Tengvall P. C1q-independent activation of neutrophils by immunoglobulin M-coated surfaces. J Biomed Mater Res. 2001;57(4):550–558.11553885
  • Madan T, Eggleton P, Kishore U, et al. Binding of pulmonary surfactant proteins A and D to Aspergillus fumigatus conidia enhances phagocytosis and killing by human neutrophils and alveolar macrophages. Infect Immun. 1997;65(8):3171–3179.9234771
  • Hokari Y, Seki T, Nakano H, et al. Isolation and identification of novel neutrophil-activating cryptides hidden in mitochondrial cytochrome C. Protein Pept Lett. 2012;19(6):680–687.22519541
  • Murphy BM, O‘Neill AJ, Adrain C, Watson RW, Martin SJ. The apoptosome pathway to caspase activation in primary human neutrophils exhibits dramatically reduced requirements for cytochrome C. J Exp Med. 2003;197(5):625–632.12615903
  • Pryde JG, Walker A, Rossi AG, Hannah S, Haslett C. Temperature-dependent arrest of neutrophil apoptosis. Failure of Bax insertion into mitochondria at 15 degrees C prevents the release of cytochrome c. J Biol Chem. 2000;275(43):33574–33584. doi:10.1074/jbc.M00100820010896657
  • Nakamura H, Herzenberg LA, Bai J, et al. Circulating thioredoxin suppresses lipopolysaccharide-induced neutrophil chemotaxis. Proc Natl Acad Sci U S A. 2001;98(26):15143–15148. doi:10.1073/pnas.19149879811742067
  • Bakkeheim E, Mowinckel P, Carlsen KH, Burney P, Carlsen KC. Altered oxidative state in schoolchildren with asthma and allergic rhinitis. Pediatr Allergy Immunol. 2011;22(2):178–185. doi:10.1111/j.1399-3038.2010.01092.x20633237
  • Brigham EP, McCormack MC, Takemoto CM, Matsui EC. Iron status is associated with asthma and lung function in US women. PLoS One. 2015;10(2):e0117545. doi:10.1371/journal.pone.011754525689633
  • Widmeier S, Bernard A, Tschopp A, et al. Surfactant protein A, exposure to endotoxin, and asthma in garbage collectors and in wastewater workers. Inhal Toxicol. 2007;19(4):351–360. doi:10.1080/0895837060114445617365040
  • Wang JY, Shieh CC, You PF, Lei HY, Reid KB. Inhibitory effect of pulmonary surfactant proteins A and D on allergen-induced lymphocyte proliferation and histamine release in children with asthma. Am J Respir Crit Care Med. 1998;158(2):510–518. doi:10.1164/ajrccm.158.2.97091119700129
  • Yamada Y, Nakamura H, Adachi T, et al. Elevated serum levels of thioredoxin in patients with acute exacerbation of asthma. Immunol Lett. 2003;86(2):199–205.12644323
  • Jeong HC, Lee SY, Lee EJ, et al. Proteomic analysis of peripheral T-lymphocytes in patients with asthma. Chest. 2007;132(2):489–496. doi:10.1378/chest.06-298017550934
  • The Gene Ontology Consortium. Expansion of the gene ontology knowledgebase and resources. Nucleic Acids Res. 2017;45(D1):D331–D338.27899567
  • Marks RM, Todd RF 3rd, Ward PA. Rapid induction of neutrophil-endothelial adhesion by endothelial complement fixation. Nature. 1989;339(6222):314–317.2725646
  • Reinhardt PH, Ward CA, Giles WR, Kubes P. Emigrated rat neutrophils adhere to cardiac myocytes via alpha 4 integrin. Circ Res. 1997;81(2):196–201.9242180
  • National Center for Biotechnology Information USNLoM. Neutrophil Infiltration. MeSH (Medical Subject Headings). 2000 Available from: https://www.ncbi.nlm.nih.gov/mesh/68020556(5/15/2018