Understanding asthma using animal models

Allergy, Asthma and Immunology Research

Volumn 1, Issue 1, 2009, Pages 10-18

  Shin, Yoo Seob ^a   Takeda, Katsuyuki ^a   Gelfand, Erwin W ^a  

^a DEPARTMENT OF MEDICINE   (United States)

Author keywords

Animal model; Asthma; Mouse

Indexed keywords

ASTHMA; BRONCHUS HYPERREACTIVITY; DENDRITIC CELL; ELECTRIC FIELD; GUINEA PIG; INFLAMMATION; LUNG FUNCTION; MOUSE; MOUSE STRAIN; NONHUMAN; OUTCOME ASSESSMENT; PHENOTYPE; RABBIT; RAT; REVIEW; SENSITIZATION;

EID: 77953967688     PISSN: 20927355     EISSN: 20927363     Source Type: Journal    
DOI: 10.4168/aair.2009.1.1.10     Document Type: Review

References (74)

1. Asher MI, Montefort S, Bjorksten B, Lai CK, Strachan DP, Weiland SK, Williams H; ISAAC Phase Three Study Group. Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys. Lancet 2006;368:733-43.
2. Janson C, Anto J, Burney P, Chinn S, de Marco R, Heinrich J, Jarvis D, Kuenzli N, Leynaert B, Luczynska C, Neukirch F, Svanes C, Sunyer J, Wjst M; European Community Respiratory Health Survey II. The European Community Respiratory Health Survey: what are the main results so far? European Community Respiratory Health Survey II. Eur Respir J 2001;18:598-611.
3. Alvarez J, Surs W, Leung DY, Ikle D, Gelfand EW, Szefler SJ. Steroid-resistant asthma: immunologic and pharmacologic features. J Allergy Clin Immunol 1992;89:714-21.
4. Busse WW, Lemanske RF Jr. Asthma. N Engl J Med 2001;344:350-62.
5. Woodcock A, Lowe LA, Murray CS, Simpson BM, Pipis SD, Kissen P, Simpson A, Custovic A; NAC Manchester Asthma and Allergy Study Group. Early life environmental control: effect on symptoms, sensitization, and lung function at age 3 years. Am J Respir Crit Care Med 2004;170:433-9.
6. Illi S, von Mutius E, Lau S, Niggemann B, Gruber C, Wahn U; Multicentre Allergy Study (MAS) group. Perennial allergen sensitisation early in life and chronic asthma in children: a birth cohort study. Lancet 2006;368:763-70.
7. Stein RT, Sherrill D, Morgan WJ, Holberg CJ, Halonen M, Taussig LM, Wright AL, Martinez FD. Respiratory syncytial virus in early life and risk of wheeze and allergy by age 13 years. Lancet 1999;354:541-5.
8. Venables KM, Chan-Yeung M. Occupational asthma. Lancet 1997;349:1465-9.
9. Trasande L, Thurston GD. The role of air pollution in asthma and other pediatric morbidities. J Allergy Clin Immunol 2005;115:689-99.
10. Stoddard JJ, Miller T. Impact of parental smoking on the prevalence of wheezing respiratory illness in children. Am J Epidemiol 1995;141:96-102.
11. Bice DE, Seagrave J, Green FH. Animal models of asthma: potential usefulness for studying health effects of inhaled particles. Inhal Toxicol 2000;12:829-62.
12. Karol MH. Animal models of occupational asthma. Eur Respir J 1994;7:555-68.
13. Persson CG, Erjefalt JS, Korsgren M, Sundler F. The mouse trap. Trends Pharmacol Sci 1997;18:465-7.
14. Kips JC, Anderson GP, Fredberg JJ, Herz U, Inman MD, Jordana M, Kemeny DM, Lotvall J, Pauwels RA, Plopper CG, Schmidt D, Sterk PJ, Van Oosterhout AJ, Vargaftig BB, Chung KF. Murine models of asthma. Eur Respir J 2003;22:374-82.
15. Schneider T, van Velzen D, Moqbel R, Issekutz AC. Kinetics and quantitation of eosinophil and neutrophil recruitment to allergic lung inflammation in a brown Norway rat model. Am J Respir Cell Mol Biol 1997;17:702-12. (Pubitemid 127348661)
16. Bautsch W, Hoymann HG, Zhang Q, Meier-Wiedenbach I, Raschke U, Ames RS, Sohns B, Flemme N, Meyer zu Vilsendorf A, Grove M, Klos A, Kohl J. Cutting edge: guinea pigs with a natural C3a-receptor defect exhibit decreased bronchoconstriction in allergic airway disease: evidence for an involvement of the C3a anaphylatoxin in the pathogenesis of asthma. J Immunol 2000;165:5401-5.
17. Colasurdo GN, Hemming VG, Prince GA, Gelfand AS, Loader JE, Larsen GL. Human respiratory syncytial virus produces prolonged alterations of neural control in airways of developing ferrets. Am J Respir Crit Care Med 1998;157:1506-11.
18. Evans MJ, Fanucchi MV, Baker GL, Van Winkle LS, Pantle LM, Nishio SJ, Schelegle ES, Gershwin LJ, Miller LA, Hyde DM, Sannes PL, Plopper CG. Atypical development of the tracheal basement membrane zone of infant rhesus monkeys exposed to ozone and allergen. Am J Physiol Lung Cell Mol Physiol 2003;285:L931-9.
19. Fairbairn SM, Page CP, Lees P, Cunningham FM. Early neutrophil but not eosinophil or platelet recruitment to the lungs of allergic horses following antigen exposure. Clin Exp Allergy 1993;23:821-8.
20. Noelpp B, Noelpp-Eschenhagen I. Experimental bronchial asthma in the guinea pig. IV. Experimental asthma in the guinea pig as an experimental model. Int Arch Allergy Appl Immunol 1952;3:207-17.
21. Ricciardolo FL, Nijkamp F, De Rose V, Folkerts G. The guinea pig as an animal model for asthma. Curr Drug Targets 2008;9:452-65.
22. Watanabe A, Hayashi H. Allergen-induced biphasic bronchoconstriction in rats. Int Arch Allergy Appl Immunol 1990;93:26-34.
23. Bellofiore S, Martin JG. Antigen challenge of sensitized rats increases airway responsiveness to methacholine. J Appl Physiol 1988;65:1642-6.
24. Eidelman DH, Bellofiore S, Martin JG. Late airway responses to antigen challenge in sensitized inbred rats. Am Rev Respir Dis 1988;137:1033-7.
25. Lowell FC. Observations on Heaves. An Asthma-Like Syndrome in the Horse. J Allergy Clin Immunol 1964;35:322-30.
26. Michoud MC, Pare PD, Boucher R, Hogg JC. Airway responses to histamine and methacholine in Ascaris suum-allergic rhesus monkeys. J Appl Physiol 1978;45:846-51. (Pubitemid 9180411)
27. Ewart SL, Kuperman D, Schadt E, Tankersley C, Grupe A, Shubitowski DM, Peltz G, Wills-Karp M. Quantitative trait loci controlling allergen-induced airway hyperresponsiveness in inbred mice. Am J Respir Cell Mol Biol 2000;23:537-45.
28. McIntire JJ, Umetsu SE, Akbari O, Potter M, Kuchroo VK, Barsh GS, Freeman GJ, Umetsu DT, DeKruyff RH. Identification of Tapr (an airway hyperreactivity regulatory locus) and the linked Tim gene family. Nat Immunol 2001;2:1109-16.
29. Morokata T, Ishikawa J, Ida K, Yamada T. C57BL/6 mice are more susceptible to antigen-induced pulmonary eosinophilia than BALB/c mice, irrespective of systemic T helper 1/T helper 2 responses. Immunology 1999;98:345-51.
30. Takeda K, Hamelmann E, Joetham A, Shultz LD, Larsen GL, Irvin CG, Gelfand EW. Development of eosinophilic airway inflammation and airway hyperresponsiveness in mast cell-deficient mice. J Exp Med 1997;186:449-54.
31. Fuchs B, Braun A. Improved mouse models of allergy and allergic asthma - chances beyond ovalbumin. Curr Drug Targets 2008;9:495-502.
32. Conrad ML, Yildirim AO, Sonar SS, Kilic A, Sudowe S, Lunow M, Teich R, Renz H, Garn H. Comparison of adjuvant and adjuvantfree murine experimental asthma models. Clin Exp Allergy 2009;39:1246-54.
33. Eisenbarth SC, Piggott DA, Huleatt JW, Visintin I, Herrick CA, Bottomly K. Lipopolysaccharide-enhanced, toll-like receptor 4-de pendent T helper cell type 2 responses to inhaled antigen. J Exp Med 2002;196:1645-51.
34. Swirski FK, Sajic D, Robbins CS, Gajewska BU, Jordana M, Stampfli MR. Chronic exposure to innocuous antigen in sensitized mice leads to suppressed airway eosinophilia that is reversed by granulocyte macrophage colony-stimulating factor. J Immunol 2002;169:3499-506.
35. Barrett EG, Rudolph K, Bowen LE, Muggenburg BA, Bice DE. Effect of inhaled ultrafine carbon particles on the allergic airway response in ragweed-sensitized dogs. Inhal Toxicol 2003;15:151-65.
36. Kurup VP, Choi H, Murali PS, Resnick A, Fink JN, Coffman RL. Role of particulate antigens of Aspergillus in murine eosinophilia. Int Arch Allergy Immunol 1997;112:270-8. (Pubitemid 27091180)
37. Chapoval SP, Iijima K, Marietta EV, Smart MK, Chapoval AI, Andrews AG, David CS. Allergic inflammatory response to short ragweed allergenic extract in HLA-DQ transgenic mice lacking CD4 gene. J Immunol 2002;168:890-9.
38. Lambert AL, Winsett DW, Costa DL, Selgrade MK, Gilmour MI. Transfer of allergic airway responses with serum and lymphocytes from rats sensitized to dust mite. Am J Respir Crit Care Med 1998;157:1991-9.
39. Warner RL, Lukacs NW, Shapiro SD, Bhagarvathula N, Nerusu KC, Varani J, Johnson KJ. Role of metalloelastase in a model of allergic lung responses induced by cockroach allergen. Am J Pathol 2004;165:1921-30.
40. Blease K, Jakubzick C, Westwick J, Lukacs N, Kunkel SL, Hogaboam CM. Therapeutic effect of IL-13 immunoneutralization during chronic experimental fungal asthma. J Immunol 2001;166:5219-24.
41. Obiefuna PC, Batra VK, Nadeem A, Borron P, Wilson CN, Mustafa SJ. A novel A1 adenosine receptor antagonist, L-97-1 [3-[2-(4-aminophenyl)-ethyl]-8-benzyl- 7-{2-ethyl-(2-hydroxy-ethyl)-amino]-ethyl}-1-propyl-3,7-dihydro-purine-2, 6-dione], reduces allergic responses to house dust mite in an allergic rabbit model of asthma. J Pharmacol Exp Ther 2005;315:329-36.
42. Goplen N, Karim MZ, Liang Q, Gorska MM, Rozario S, Guo L, Alam R. Combined sensitization of mice to extracts of dust mite, ragweed, and Aspergillus species breaks through tolerance and establishes chronic features of asthma. J Allergy Clin Immunol 2009;123:925-32.e11.
43. Seitzer U, Bussler H, Kullmann B, Petersen A, Becker WM, Ahmed J. Mouse strain specificity of the IgE response to the major allergens of Phleum pratense. Int Arch Allergy Immunol 2005;136:347-55. (Pubitemid 41094498)
44. Blyth DI, Pedrick MS, Savage TJ, Hessel EM, Fattah D. Lung inflammation and epithelial changes in a murine model of atopic asthma. Am J Respir Cell Mol Biol 1996;14:425-38. (Pubitemid 126440511)
45. McMillan SJ, Lloyd CM. Prolonged allergen challenge in mice leads to persistent airway remodelling. Clin Exp Allergy 2004;34:497-507.
46. Joetham A, Takeda K, Taube C, Miyahara N, Kanehiro A, Dakhama A, Gelfand EW. Airway hyperresponsiveness in the absence of CD4+ T cells after primary but not secondary challenge. Am J Respir Cell Mol Biol 2005;33:89-96.
47. Kanehiro A, Ikemura T, Makela MJ, Lahn M, Joetham A, Dakhama A, Gelfand EW. Inhibition of phosphodiesterase 4 attenuates airway hyperresponsiveness and airway inflammation in a model of secondary allergen challenge. Am J Respir Crit Care Med 2001;163:173-84.
48. Bousquet J, Jeffery PK, Busse WW, Johnson M, Vignola AM. Asthma. From bronchoconstriction to airways inflammation and remodeling. Am J Respir Crit Care Med 2000;161:1720-45. (Pubitemid 30329053)
49. Fish JE, Peters SP. Airway remodeling and persistent airway obstruction in asthma. J Allergy Clin Immunol 1999;104:509-16.
50. Temelkovski J, Hogan SP, Shepherd DP, Foster PS, Kumar RK. An improved murine model of asthma: selective airway inflammation, epithelial lesions and increased methacholine responsiveness following chronic exposure to aerosolised allergen. Thorax 1998;53:849-56.
51. Wegmann M. Animal models of chronic experimental asthma - strategies for the identification of new therapeutic targets. J Occup Med Toxicol 2008;3 Suppl 1:S4.
52. Fernandez-Rodriguez S, Ford WR, Broadley KJ, Kidd EJ. Establishing the phenotype in novel acute and chronic murine models of allergic asthma. Int Immunopharmacol 2008;8:756-63.
53. Kim CH, Ahn JH, Kim SJ, Lee SY, Kim YK, Kim KH, Moon HS, Song JS, Park SH, Kwon SS. Co-administration of vaccination with DNA encoding T cell epitope on the Der p and BCG inhibited airway remodeling in a murine model of chronic asthma. J Asthma 2006;43:345-53.
54. Koya T, Kodama T, Takeda K, Miyahara N, Yang ES, Taube C, Joetham A, Park JW, Dakhama A, Gelfand EW. Importance of myeloid dendritic cells in persistent airway disease after repeated allergen exposure. Am J Respir Crit Care Med 2006;173:42-55.
55. Shinagawa K, Kojima M. Mouse model of airway remodeling: strain differences. Am J Respir Crit Care Med 2003;168:959-67.
56. Boyce JA, Austen KF. No audible wheezing: nuggets and conundrums from mouse asthma models. J Exp Med 2005;201:1869-73.
57. Larsen GL, Renz H, Loader JE, Bradley KL, Gelfand EW. Airway response to electrical field stimulation in sensitized inbred mice. Passive transfer of increased responsiveness with peribronchial lymph nodes. J Clin Invest 1992;89:747-52.
58. Saloga J, Renz H, Lack G, Bradley KL, Greenstein JL, Larsen G, Gelfand EW. Development and transfer of immediate cutaneous hypersensitivity in mice exposed to aerosolized antigen. J Clin Invest 1993;91:133-40.
59. Hamelmann E, Tadeda K, Oshiba A, Gelfand EW. Role of IgE in the development of allergic airway inflammation and airway hyperresponsiveness - a murine model. Allergy 1999;54:297-305. (Pubitemid 29232384)
60. Swirski FK, Gajewska BU, Alvarez D, Ritz SA, Cundall MJ, Cates EC, Coyle AJ, Gutierrez-Ramos JC, Inman MD, Jordana M, Stampfli MR. Inhalation of a harmless antigen (ovalbumin) elicits immune activation but divergent immunoglobulin and cytokine activities in mice. Clin Exp Allergy 2002;32:411-21.
61. Taube C, Miyahara N, Ott V, Swanson B, Takeda K, Loader J, Shultz LD, Tager AM, Luster AD, Dakhama A, Gelfand EW. The leukotriene B4 receptor (BLT1) is required for effector CD8+ T cell-mediated, mast cell-dependent airway hyperresponsiveness. J Immunol 2006;176:3157-64.
62. Koya T, Matsuda H, Takeda K, Matsubara S, Miyahara N, Balhorn A, Dakhama A, Gelfand EW. IL-10-treated dendritic cells decrease airway hyperresponsiveness and airway inflammation in mice. J Allergy Clin Immunol 2007;119:1241-50.
63. Koya T, Matsuda H, Matsubara S, Miyahara N, Dakhama A, Takeda K, Gelfand EW. Differential effects of dendritic cell transfer on airway hyperresponsiveness and inflammation. Am J Respir Cell Mol Biol 2009;41:271-80.
64. Lambrecht BN, De Veerman M, Coyle AJ, Gutierrez-Ramos JC, Thielemans K, Pauwels RA. Myeloid dendritic cells induce Th2 responses to inhaled antigen, leading to eosinophilic airway inflammation. J Clin Invest 2000;106:551-9. (Pubitemid 30666388)
65. de Heer HJ, Hammad H, Kool M, Lambrecht BN. Dendritic cell subsets and immune regulation in the lung. Semin Immunol 2005;17:295-303.
66. Lambrecht BN. Lung dendritic cells: targets for therapy in allergic disease. Curr Mol Med 2008;8:393-400.
67. Cieslewicz G, Tomkinson A, Adler A, Duez C, Schwarze J, Takeda K, Larson KA, Lee JJ, Irvin CG, Gelfand EW. The late, but not early, asthmatic response is dependent on IL-5 and correlates with eosinophil infiltration. J Clin Invest 1999;104:301-8.
68. Hamelmann E, Schwarze J, Takeda K, Oshiba A, Larsen GL, Irvin CG, Gelfand EW. Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am J Respir Crit Care Med 1997;156:766-75.
69. Lundblad LK, Irvin CG, Hantos Z, Sly P, Mitzner W, Bates JH. Penh is not a measure of airway resistance! Eur Respir J 2007;30:805.
70. Bates JH, Irvin CG. Measuring lung function in mice: the phenotyping uncertainty principle. J Appl Physiol 2003;94:1297-306.
71. Martin TR, Gerard NP, Galli SJ, Drazen JM. Pulmonary responses to bronchoconstrictor agonists in the mouse. J Appl Physiol 1988;64:2318-23.
72. Larsen GL, Fame TM, Renz H, Loader JE, Graves J, Hill M, Gelfand EW. Increased acetylcholine release in tracheas from allergen-exposed IgE-immune mice. Am J Physiol 1994;266:L263-70.
73. Evans CM, Fryer AD, Jacoby DB, Gleich GJ, Costello RW. Pretreatment with antibody to eosinophil major basic protein prevents hyperresponsiveness by protecting neuronal M2 muscarinic receptors in antigen-challenged guinea pigs. J Clin Invest 1997;100:2254-62.
74. Taube C, Wei X, Swasey CH, Joetham A, Zarini S, Lively T, Takeda K, Loader J, Miyahara N, Kodama T, Shultz LD, Donaldson DD, Hamelmann EH, Dakhama A, Gelfand EW. Mast cells, Fc epsilon RI, and IL-13 are required for development of airway hyperresponsiveness after aerosolized allergen exposure in the absence of adjuvant. J Immunol 2004;172:6398-406.