Cockroach Allergens Induce Biphasic Asthma-Like Pulmonary Inflammation in Outbred Mice

References

• Mannino DM, Homa DM, Akinbami LJ, Ford ES, Redd SC. Chronic obstructive pulmonary disease surveillance–United States, 1971–2000. MMWR Surveill Summ 2002; 51:1–16.
   PubMed Web of Science ®Google Scholar
• National Heart Lung and Blood Institute. Guidelines for the Diagnosis and Management of Asthma. Bethesda, MD. Washington, DC: U.S. Department of Health and Human Services, National Institutes of Health, 2007.
   Google Scholar
• CDC. Morbidity and Mortality Weekly Report: Surveillance for Asthma. Atlanta, GA: Centers for Disease Control and Prevention, 2002.
   Google Scholar
• National Heart Lung and Blood Institute. Morbidity and Mortality: 2007 Chart Book on Cardiovascular, Lung and Blood Diseases. 2007.
   Google Scholar
• Humbert M, Menz G, Ying S, Corrigan CJ, Robinson DS, Durham SR, Kay AB. The immunopathology of extrinsic (atopic) and intrinsic (non-atopic) asthma: more similarities than differences. Immunol Today 1999; 20:528–533.
   PubMedGoogle Scholar
• Walker C. The immunology of extrinsic and intrinsic asthma. Agents Actions Suppl 1993; 43:97–106.
   PubMedGoogle Scholar
• Bener A, Ehlayel M, Sabbah A. The pattern and genetics of pediatric extrinsic asthma risk factors in polluted environment. Eur Ann Allergy Clin Immunol 2007; 39:58–63.
   PubMedGoogle Scholar
• Bryant-Stephens T. Asthma disparities in urban environments. J Allergy Clin Immunol 2009; 123:1199–1206; quiz 1207–1198.
   PubMed Web of Science ®Google Scholar
• Gold DR, Wright R. Population disparities in asthma. Annu Rev Public Health 2005; 26:89–113.
   PubMed Web of Science ®Google Scholar
• Forno E, Celedon JC. Asthma and ethnic minorities: socioeconomic status and beyond. Curr Opin Allergy Clin Immunol 2009; 9:154–160.
   PubMed Web of Science ®Google Scholar
• Kleinman MT, Sioutas C, Froines JR, Fanning E, Hamade A, Mendez L, Meacher D, Oldham M. Inhalation of concentrated ambient particulate matter near a heavily trafficked road stimulates antigen-induced airway responses in mice. Inhal Toxicol 2007; 19(Suppl 1):117–126.
   PubMed Web of Science ®Google Scholar
• Northridge J, Ramirez OF, Stingone JA, Claudio L. The role of housing type and housing quality in urban children with asthma. J Urban Health 2010; 87(2):211–224.
   Google Scholar
• Wichmann HE. Diesel exhaust particles. Inhal Toxicol 2007; 19(Suppl 1):241–244.
   PubMed Web of Science ®Google Scholar
• Rotsides DZ, Goldstein IF, Canfield SM, Perzanowski M, Mellins RB, Hoepner L, Ashby-Thompson M, Jacobson JS. Asthma, allergy, and IgE levels in NYC head start children. Respir Med 2010; 104:345–355.
   PubMedGoogle Scholar
• Rosenstreich DL, Eggleston P, Kattan M, Baker D, Slavin RG, Gergen P, Mitchell H, McNiff-Mortimer K, Lynn H, Ownby D, Malveaux F. The role of cockroach allergy and exposure to cockroach allergen in causing morbidity among inner-city children with asthma. N Engl J Med 1997; 336:1356–1363.
   PubMed Web of Science ®Google Scholar
• Kim J, McKinley L, Siddiqui J, Bolgos GL, Remick DG. Prevention and reversal of pulmonary inflammation and airway hyperresponsiveness by dexamethasone treatment in a murine model of asthma induced by house dust. Am J Physiol Lung Cell Mol Physiol 2004; 287:L503–L509.
   Google Scholar
• Mckinley L, Kim J, Bolgos GL, Siddiqui J, Remick DG. Reproducibility of a novel model of murine asthma-like pulmonary inflammation. Clin Exp Immunol 2004; 136:224–231.
   PubMedGoogle Scholar
• Narala VR, Ranga R, Smith MR, Berlin AA, Standiford TJ, Lukacs NW, Reddy RC. Pioglitazone is as effective as dexamethasone in a cockroach allergen-induced murine model of asthma. Respir Res 2007; 8:90.
   PubMedGoogle Scholar
• Wilson J, Dixon SL, Breysse P, Jacobs D, Adamkiewicz G, Chew GL, Dearborn D, Krieger J, Sandel M, Spanier A. Housing and allergens: a pooled analysis of nine US studies. Environ Res 2010; 110:189–198.
   PubMed Web of Science ®Google Scholar
• Bousquet J, Chanez P, Lacoste JY, Barneon G, Ghavanian N, Enander I, Venge P, Ahlstedt S, Simony-Lafontaine J, Godard P, Michel FB. Eosinophilic inflammation in asthma. N Engl J Med 1990; 323:1033–1039.
   PubMed Web of Science ®Google Scholar
• Gleich GJ. The eosinophil and bronchial asthma: current understanding. J Allergy Clin Immunol 1990; 85:422–436.
   PubMed Web of Science ®Google Scholar
• Galli SJ. New concepts about the mast cell. N Engl J Med 1993; 328:257–265.
   PubMed Web of Science ®Google Scholar
• Broide DH, Gleich GJ, Cuomo AJ, Coburn DA, Federman EC, Schwartz LB, Wasserman SI. Evidence of ongoing mast cell and eosinophil degranulation in symptomatic asthma airway. J Allergy Clin Immunol 1991; 88:637–648.
   PubMed Web of Science ®Google Scholar
• Walker C, Kaegi MK, Braun P, Blaser K. Activated T cells and eosinophilia in bronchoalveolar lavages from subjects with asthma correlated with disease severity. J Allergy Clin Immunol 1991; 88:935–942.
   PubMed Web of Science ®Google Scholar
• Frew AJ, Kay AB. Eosinophils and T-lymphocytes in late-phase allergic reactions. J Allergy Clin Immunol 1990; 85:533–539.
   PubMedGoogle Scholar
• Choi IW, Sun K, Kim YS, Ko HM, Im SY, Kim JH, You HJ, Lee YC, Lee JH, Park YM, Lee HK. TNF-alpha induces the late-phase airway hyperresponsiveness and airway inflammation through cytosolic phospholipase A(2) activation. J Allergy Clin Immunol 2005; 116:537–543.
   PubMed Web of Science ®Google Scholar
• Kim YS, Ko HM, Kang NI, Song CH, Zhang X, Chung WC, Kim JH, Choi IH, Park YM, Kim GY, Im SY, Lee HK. Mast cells play a key role in the development of late airway hyperresponsiveness through TNF-alpha in a murine model of asthma. Eur J Immunol 2007; 37:1107–1115.
   PubMed Web of Science ®Google Scholar
• Mizutani N, Nabe T, Yoshino S. Complement C3a regulates late asthmatic response and airway hyperresponsiveness in mice. J Immunol 2009; 183:4039–4046.
   PubMedGoogle Scholar
• Zhang XD, Fedan JS, Lewis DM, Siegel PD. Asthmalike biphasic airway responses in Brown Norway rats sensitized by dermal exposure to dry trimellitic anhydride powder. J Allergy Clin Immunol 2004; 113:320–326.
   PubMed Web of Science ®Google Scholar
• Vaickus LJ, Bouchard J, Kim J, Natarajan S, Remick DG. Assessing pulmonary pathology by detailed examination of respiratory function. Am J Pathol 2010; 177:1861–1869.
   PubMedGoogle Scholar
• Vaickus LJ, Bouchard J, Kim J, Natarajan S, Remick DG. Inbred and outbred mice have equivalent variability in a cockroach allergen-induced model of asthma. Comp Med 2010; 60:420–426.
   Google Scholar
• Vaickus LJ, Bouchard J, Kim J, Natarajan S, Remick DG. Oral tolerance inhibits pulmonary eosinophilia in a cockroach allergen induced model of asthma: a randomized laboratory study. Respir Res 2010; 11:160.
   Google Scholar
• Vaickus LJ, Bouchard J, Kim J, Natarajan S, Remick DG. Assessing pulmonary pathology by detailed examination of respiratory function. Am J Pathol 1869; 177:1861–1869.
   Google Scholar
• Schneider T, Issekutz AC. Quantitation of eosinophil and neutrophil infiltration into rat lung by specific assays for eosinophil peroxidase and myeloperoxidase. Application in a Brown Norway rat model of allergic pulmonary inflammation. J Immunol Methods 1996; 198:1–14.
   PubMedGoogle Scholar
• Sur S, Wild JS, Choudhury BK, Sur N, Alam R, Klinman DM. Long term prevention of allergic lung inflammation in a mouse model of asthma by CpG oligodeoxynucleotides. J Immunol 1999; 162:6284–6293.
   PubMed Web of Science ®Google Scholar
• Barnes PJ. Pathophysiology of asthma. Br J Clin Pharmacol 1996; 42:3–10.
   PubMed Web of Science ®Google Scholar
• Bates ME, Sedgwick JB, Zhu Y, Liu LY, Heuser RG, Jarjour NN, Kita H, Bertics PJ. Human airway eosinophils respond to chemoattractants with greater eosinophil-derived neurotoxin release, adherence to fibronectin, and activation of the Ras-ERK pathway when compared with blood eosinophils. J Immunol 2010; 184:7125–7133.
   PubMed Web of Science ®Google Scholar
• Afshar R, Medoff BD, Luster AD. Allergic asthma: a tale of many T cells. Clin Exp Allergy 2008; 38:1847–1857.
   PubMed Web of Science ®Google Scholar
• Baraldo S, Lokar Oliani K, Turato G, Zuin R, Saetta M. The role of lymphocytes in the pathogenesis of asthma and COPD. Curr Med Chem 2007; 14:2250–2256.
   PubMed Web of Science ®Google Scholar
• Nakae S, Ho LH, Yu M, Monteforte R, Iikura M, Suto H, Galli SJ. Mast cell-derived TNF contributes to airway hyperreactivity, inflammation, and TH2 cytokine production in an asthma model in mice. J Allergy Clin Immunol 2007; 120:48–55.
   PubMed Web of Science ®Google Scholar
• Kim J, McKinley L, Natarajan S, Bolgos GL, Siddiqui J, Copeland S, Remick DG. Anti-tumor necrosis factor-alpha antibody treatment reduces pulmonary inflammation and methacholine hyper-responsiveness in a murine asthma model induced by house dust. Clin Exp Allergy 2006; 36:122–132.
   PubMed Web of Science ®Google Scholar
• Koyama H, Tokuyama K, Nishimura H, Mizuno T, Mayuzumi H, Ohki Y, Arakawa H, Mochizuki H, Morikawa A. Effect of disodium cromoglycate on airway mucus secretion during antigen-induced late asthmatic responses in a murine model of asthma. Int Arch Allergy Immunol 2005; 138:189–196.
   PubMedGoogle Scholar
• Hamilton AL, Watson RM, Wyile G, O‘Byrne PM. Attenuation of early and late phase allergen-induced bronchoconstriction in asthmatic subjects by a 5-lipoxygenase activating protein antagonist, BAYx 1005. Thorax 1997; 52:348–354.
   PubMed Web of Science ®Google Scholar
• Nagarkar DR, Wang Q, Shim J, Zhao Y, Tsai WC, Lukacs NW, Sajjan U, Hershenson MB. CXCR2 is required for neutrophilic airway inflammation and hyperresponsiveness in a mouse model of human rhinovirus infection. J Immunol 2009; 183:6698–6707.
   PubMed Web of Science ®Google Scholar
• Grigoras A, Grigoras CC, Mihaescus T, Floarea-Strat A, Andriescu C, Cotutiu C. Neutrophilic inflammation–indicative of asthma severity. Pneumologia 2010; 59:13–18.
   PubMedGoogle Scholar
• Fahy JV. Eosinophilic and neutrophilic inflammation in asthma: insights from clinical studies. Proc Am Thorac Soc 2009; 6:256–259.
   PubMedGoogle Scholar
• Takahashi G, Tanaka H, Wakahara K, Nasu R, Hashimoto M, Miyoshi K, Takano H, Yamashita H, Inagaki N, Nagai H. Effect of diesel exhaust particles on house dust mite-induced airway eosinophilic inflammation and remodeling in mice. J Pharmacol Sci 2010; 112:192–202.
   PubMed Web of Science ®Google Scholar
• Gibson PG. Inflammatory phenotypes in adult asthma: clinical applications. Clin Respir J 2009; 3:198–206.
   PubMed Web of Science ®Google Scholar
• Busse WW, Sedgwick JB. Eosinophils in asthma. Ann Allergy 1992; 68:286–290.
   PubMedGoogle Scholar
• Calhoun WJ, Sedgwick J, Busse WW. The role of eosinophils in the pathophysiology of asthma. Ann N Y Acad Sci 1991; 629:62–72.
   PubMed Web of Science ®Google Scholar
• Conroy DM, Williams TJ. Eotaxin and the attraction of eosinophils to the asthmatic lung. Respir Res 2001; 2:150–156.
   PubMed Web of Science ®Google Scholar
• Alam R, Forsythe P, Stafford S, Fukuda Y. Transforming growth factor beta abrogates the effects of hematopoietins on eosinophils and induces their apoptosis. J Exp Med 1994; 179:1041–1045.
   PubMed Web of Science ®Google Scholar
• Stern M, Meagher L, Savill J, Haslett C. Apoptosis in human eosinophils. Programmed cell death in the eosinophil leads to phagocytosis by macrophages and is modulated by IL-5. J Immunol 1992; 148:3543–3549.
   PubMed Web of Science ®Google Scholar
• Yamaguchi Y, Hayashi Y, Sugama Y, Miura Y, Kasahara T, Kitamura S, Torisu M, Mita S, Tominaga A, Takatsu K. Highly purified murine interleukin 5 (IL-5) stimulates eosinophil function and prolongs in vitro survival. IL-5 as an eosinophil chemotactic factor. J Exp Med 1988; 167:1737–1742.
   PubMed Web of Science ®Google Scholar
• Dubois GR, Bruijnzeel PL. IL-4-induced migration of eosinophils in allergic inflammation. Ann N Y Acad Sci 1994; 725:268–273.
   PubMedGoogle Scholar
• Pope SM, Brandt EB, Mishra A, Hogan SP, Zimmermann N, Matthaei KI, Foster PS, Rothenberg ME. IL-13 induces eosinophil recruitment into the lung by an IL-5- and eotaxin-dependent mechanism. J Allergy Clin Immunol 2001; 108:594–601.
   PubMed Web of Science ®Google Scholar
• Horie S, Okubo Y, Hossain M, Sato E, Nomura H, Koyama S, Suzuki J, Isobe M, Sekiguchi M. Interleukin-13 but not interleukin-4 prolongs eosinophil survival and induces eosinophil chemotaxis. Intern Med 1997; 36:179–185.
   PubMed Web of Science ®Google Scholar
• Castilow EM, Meyerholz DK, Varga SM. IL-13 is required for eosinophil entry into the lung during respiratory syncytial virus vaccine-enhanced disease. J Immunol 2008; 180:2376–2384.
   PubMed Web of Science ®Google Scholar
• Vasconcelos JF, Teixeira MM, Barbosa-Filho JM, Agra MF, Nunes XP, Giulietti AM, Ribeiro-Dos-Santos R, Soares MB. Effects of umbelliferone in a murine model of allergic airway inflammation. Eur J Pharmacol 2009; 609:126–131.
   PubMedGoogle Scholar
• De Vooght V, Vanoirbeek JAJ, Haenen S, Verbeken E, Nemery B, Hoet PHM. Oropharyngeal aspiration: an alternative route for challenging in a mouse model of chemical-induced asthma. Toxicology 2009; 259:84–89.
   PubMed Web of Science ®Google Scholar
• Rao GV, Tinkle S, Weissman DN, Antonini JM, Kashon ML, Salmen R, Battelli LA, Willard PA, Hoover MD, Hubbs AF. Efficacy of a technique for exposing the mouse lung to particles aspirated from the pharynx [erratum appears in J Toxicol Environ Health A 2003 Dec 26; 66(24):2365]. J Toxicol Environ Health A 2003; 66:1441–1452.
   PubMed Web of Science ®Google Scholar
• Sung S, Rose CE, Fu SM. Intratracheal priming with ovalbumin- and ovalbumin 323-339 peptide-pulsed dendritic cells induces airway hyperresponsiveness, lung eosinophilia, goblet cell hyperplasia, and inflammation. J Immunol 2001; 166:1261–1271.
   PubMedGoogle Scholar
• Kohl J, Baelder R, Lewkowich IP, Pandey MK, Hawlisch H, Wang L, Best J, Herman NS, Sproles AA, Zwirner J, Whitsett JA, Gerard C, Sfyroera G, Lambris JD, Wills-Karp M. A regulatory role for the C5a anaphylatoxin in type 2 immunity in asthma. J Clin Invest 2006; 116:783–796.
   PubMed Web of Science ®Google Scholar
• Lajoie S, Lewkowich IP, Suzuki Y, Clark JR, Sproles AA, Dienger K, Budelsky AL, Wills-Karp M. Complement-mediated regulation of the IL-17A axis is a central genetic determinant of the severity of experimental allergic asthma. Nat Immunol 2010; 11:928–935.
   PubMed Web of Science ®Google Scholar
• Adachi M, Konno S, Gonokami Y, Kobayashi H. Studies on biphasic animal model of asthma–lymphocytes and eosinophils. Nihon Kyobu Shikkan Gakkai Zasshi 1993; 31(Suppl):185–190.
   PubMedGoogle Scholar
• Mizutani N, Inui S, Yoshino S, Nabe T. Intratracheal sensitization/challenge-induced biphasic asthmatic response and airway hyperresponsiveness in guinea pigs. Biol Pharm Bull 2010; 33: 1949–1952.
   PubMedGoogle Scholar
• Toward TJ, Broadley KJ. Early and late bronchoconstrictions, airway hyper-reactivity, leucocyte influx and lung histamine and nitric oxide after inhaled antigen: effects of dexamethasone and rolipram. Clin Exp Allergy 2004; 34:91–102.
   PubMed Web of Science ®Google Scholar
• Nabe T, Zindl CL, Jung YW, Stephens R, Sakamoto A, Kohno S, Atkinson TP, Chaplin DD. Induction of a late asthmatic response associated with airway inflammation in mice. Eur J Pharmacol 2005; 521:144–155.
   PubMedGoogle Scholar
• Busse WW, Banks-Schlegel S, Wenzel SE. Pathophysiology of severe asthma. J Allergy Clin Immunol 2000; 106:1033–1042.
   PubMedGoogle Scholar
• Wenzel SE, Busse WW . Severe asthma: lessons from the severe asthma research program. J Allergy Clin Immunol 2007; 119:14–21; quiz 22–13.
   PubMed Web of Science ®Google Scholar