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Study of a BALB/c Mouse Model for Allergic Asthma

  • Published : 2008.12.01

Abstract

Allergic asthma is a worldwide public health problem and a major socioeconomic burden disease. It is a chronic inflammatory disease marked by airway eosinophilia and goblet cell hyperplasia with mucus hypersecretion. Mouse models have proven as a valuable tool for studying human asthma. In the present report we describe a comparison of mouse asthma models. The experiments were designed as follows: Group I was injected with ovalbumin (OVA, i.p.) on day 1 and challenged with 1% OVA (aerosol exposure) on days $14{\sim}21$. Group II was injected on day 1, 14 and aerosol-immunized on days $14{\sim}21$. Group III was injected on day 1, 14 and immunized by 1% OVA aerosol on days $18{\sim}21$. We assessed asthma induction by determining the total number of white blood cells (WBC) and eosinophils as well as by measuring cytokine levels in bronchoalveolar lavage fluid (BALF). In addition, we evaluated the histopathological changes of the lungs and determined the concentration of immunoglobulin E (IgE) in serum. Total WBC, eosinophils, Th2 cytokines (IL-4, IL-13) and IgE were significantly increased in group I relative to the other groups. Moreover, histopathological studies show that group I mice show an increase in the infiltration of inflammatory cell-in peribronchial and perivascular areas as well as an overall increase in the number of mucus-containing goblet cells relative to other groups. These data suggest that group I can be a useful model for the study of human asthma pathobiology and the evaluation of existing and novel therapeutic agents.

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References

  1. Abraham, W.M. (1995). Animal models of late bronchial responses. Eur. Respir. Rev., 5, 211-217
  2. Armin, B., Thomas, T. and David, A.G. (2008). Editorial: Experimental models of asthma. J. Occu. Med. and Toxicol., 3, Suppl 1, S1 https://doi.org/10.1186/1745-6673-3-1
  3. Barnes, P.J., Chung, K.F. and Page, C.P. (1998). Inflammatory mediators of asthma: an update. Pharmacol. Rev., 50, 515-596
  4. Blanchard, C., Mishra, A., Saito-Akei, H., Monk, P., Anderson, I. and Rothenberg, M.E. (2005). Inhibition of human interleukin- 13-induced respiratory and esophageal inflammation by anti-human interleukin-13 antibody (CAT-354). Clin. Exp. Allergy, 35, 1096-1103 https://doi.org/10.1111/j.1365-2222.2005.02299.x
  5. Bousquet, J., Chanez, P., Lacoste, J.Y., Barneron, G., Ggavanian, N., Enander, I., Venge, P., Ahlstedt, S., Simony- Lafontaine, J. and Goard, P. (1990). Eosinophilic inflammation in asthma. N. Engl. J. Med., 323, 1033-1039 https://doi.org/10.1056/NEJM199010113231505
  6. Bousquet, J, Jeffery, P.K., Busse, W.W., Johnson, M. and Vignola, A.M. (2000). Asthma: from bronchoconstriction to airways inflammation and remodeling. Am. J. Respir. Crit. Care. Med., 161, 1720-1745 https://doi.org/10.1164/ajrccm.161.5.9903102
  7. Cho, J.Y., Miller, M., Baek, K.J., Han. J.W., Nayar, J., Lee, S.Y., McElwain, K., McElwain, S., Friedman, S. and Broide, D.H. (2004). Inhibition of airway remodeling in IL-5 deficient mice. J. Clin. Invest., 113, 551-560 https://doi.org/10.1172/JCI19133
  8. De Weck, A.L., Mayer, P., Stumper, B., Schiessel, B. and Pickat, L. (1997). Dog allergy, a model for allergy genetics. Int. Arch. Allergy Immunol., 113, 55-57 https://doi.org/10.1159/000237507
  9. El-Hashim, A.Z., Wyss, D. and Zuany-Amorim, C. (2002). Kinetics of airway hyperresponsiveness and airway eosinophilia in BALB/c mice and their modulation by different dexamethasone treatment regimens. Pulmonary pharmacol. & Thera., 15, 467-475 https://doi.org/10.1006/pupt.2002.0388
  10. Eric, R., Secor, J., William, F., Carson, I.V., Anurag, S., Mellisa, P., Linda, A., Guernsey, C.M., Schramm and Roger S.T. (2008) Oral bromelain attenuates inflammation in an ovalbumin- induced murine model of asthma. eCAM., 5, 61-69 https://doi.org/10.1093/ecam/nel110
  11. Flood-Page, P., Menzies-Gow, A., Phipps, S., Ying, S., Wangoo, A., Ludwig, M.S., Barnes, N., Robinson, D. and Kay, A.B. (2003). Anti-IL-5 treatment reduces deposition of ECM proteins in the bronchial subepithelial basement membrane of mild atopic asthmatics. J. Clin. Invest., 112, 1029-1036 https://doi.org/10.1172/JCI17974
  12. Fred Wonga, W.S., Hua, Z. and Wupeng, L. (2007). Cysteinyl leukotriene receptor antagonist MK-571 alters bronchoalveolar lavage fluid proteome in a mouse asthma model. Euro. J. Phar., 575, 134-141 https://doi.org/10.1016/j.ejphar.2007.07.027
  13. Fulkerson, P., Fischetti, C., Hassman, L., Nikolaidis, N.M. and Rothenberg, M.E. (2006). Persistent effects induced by IL- 13 in the lung. Am. J. Respir. Cell. Mol. Biol., 35, 337- 346 https://doi.org/10.1165/rcmb.2005-0474OC
  14. Hamid, Q., Tulic, M.K., Liu, M.C. and Moqbel, R. (2003). Inflammatory cells in asthma: mechanisms and implications for therapy. J. Allergy Clin. Immunol., 111, S5-S17 https://doi.org/10.1067/mai.2003.22
  15. Heo, Y. and Kim, K.H. (2002). Development of subacute animal model to predict occurance of systemic anaphylaxis following vaccination and evaluation of various immunotoxicological parameters. J. Toxicol. Pub. Health, 18, 205- 213
  16. Hessel, E.M., Van Oosterhout, A.J., Hofstra, C.L., De Bie, J.J., Garssen, J., Van Loveren, H., et al. (1995). Bronchoconstriction and airway hyperresponsiveness after ovalbumin inhalation in sensitized mice. Eur. J. Pharmacol., 293, 401-412 https://doi.org/10.1016/S0014-2999(95)80099-9
  17. Humbert, M., Durham, S.R., Kimmitt, P., Powell, N., Assoufi, B., Pfister, R., Menz, G., Kay, A.B. and Corrigan, C.J. (1997). Elevated expression of messenger ribonucleic acid encoding IL-13 in the bronchial mucosa of atopic and nonatopic subjects with asthma. J. Allergy Clin. Immunol., 99, 657-665 https://doi.org/10.1016/S0091-6749(97)70028-9
  18. Kim, H.A. and Heo, Y. (2001). Significance of a highly specific and sensitive enzyme linked immunosorent assay on evaluation of environmental toxicant-mediated allergic responses. J. Toxicol. Pub. Health, 17, 197-199
  19. Itoh, K., Takahashi, E., Mukaiyama, O., Sathoh, Y. and Yamaguchi, T. (1996). Relationship between airway eosinophilia and airway hyperresponsiveness in a late asthmatic model of guinea pigs. Int. Arch. Allergy Immunol., 109, 86-94 https://doi.org/10.1159/000237236
  20. Jiang, J.H., Li, G. Z., Chai, O.H. and Song, C.H. (2005). Increased intraepithelial mast cells in pulmonary airways of mouse asthma model. The Korean J. Anat., 38, 173- 179
  21. Johnson, P.R.A., Roth, M., Tamm, M., Hughes, M., Ge, Q., King, G., Burgess, J.K. and Black, J.L. (2001). Airway smooth muscle cell proliferation is increased in asthma. Am. J. Respir. Crit. Care Med., 164, 474-477 https://doi.org/10.1164/ajrccm.164.3.2010109
  22. Karol, M.H. (1994). Animal models of occupational asthma. Eur. Respir. J., 7, 555-568 https://doi.org/10.1183/09031936.94.07030555
  23. Kasaian, M.T., Donaldson, D.D., Tchistiakova, L., Marquette, K., Tan, X.Y., Ahmed, A., Jacobson, B.A., Widom, A., Cook, T.A., Xu, X., Barry, A.B., Goldman, S.J. and Abraham, W.M. (2007). Efficacy of IL-13 neutralization in a sheep model of experimental asthma. Am. J. Respir. Cell. Mol. Biol. 36, 368-376 https://doi.org/10.1165/rcmb.2006-0244OC
  24. Kay, A.B., Barata, L., Meng, Q., Durham, S.R. and Ying, S. (1997). Eosinophils and eosinophil-associated cytokines in allergic inflammation. Int. Arch. Allergy Immunol., 113, 196-199 https://doi.org/10.1159/000237545
  25. Kazuhiko, S and Masami, K. (2003). Mouse Model of Airway Remodeling. Ame. J. Res. Critical Care Med., 168, 959- 967 https://doi.org/10.1164/rccm.200210-1188OC
  26. Kips, J.C. (2001). Cytokines in asthma. Eur. Respir. J. Suppl., 34, 24-33
  27. Kumar, R.K. and Foster, P.S. (2002). Modeling allergic asthma in mice: pitfalls and opportunities. Am. J. Respir. Cell. Mol. Biol., 27, 267-272 https://doi.org/10.1165/rcmb.F248
  28. Martin, L.B., Kita, H., Leiferman, K.M. and Gleich, G.J. (1996). Eosinophils in allergy: role in disease, degranulation and cytokines. Int. Arch. Allergy Immunol., 109, 207-215 https://doi.org/10.1159/000237239
  29. McDonald, D.M. (2001). Angiogenesis and remodeling of airway vasculature in chronic inflammation. Am. J. Respir. Crit. Care Med., 164, 39-45 https://doi.org/10.1164/ajrccm.164.supplement_2.2106065
  30. Meryl, H., Karol, J.M., Matheson, R.W., Lange, R.L. and Michael, I.L. (2001). Use of tumor necrosis factor receptor (TNFR)-knockout mice to probe the mechanism of chemically-induced asthma J. Toxicol. Pub. Health, 17, 305-307
  31. Owen, C.E. (2007). Immunoglobulin E: role in asthma and allergic disease: lessons from the clinic. Pharmacol. Ther., 113, 121-133 https://doi.org/10.1016/j.pharmthera.2006.07.003
  32. Padrid, P. (1992). Chronic lower airway disease in the dog and cat. Probl. Vet. Med. 4, 320-344
  33. Paramesh, H. (2002). Epidemiology of asthma in India. Indian J. Pediatr., 69, 309-312
  34. Park, S.J., Shin, W.H., Seo, J.W. and Kim, E.J. (2007). Anthocyanins inhibit airway inflammation and hyperresponsiveness in a murine asthma model. Food and Chemical Toxicol., 45, 1459-1467 https://doi.org/10.1016/j.fct.2007.02.013
  35. Rakesh, K.K., Cristna, H. and Paul, S.F. (2008) The "Classical" ovalbumin challenge model of asthma in mice. Current Drug Targets, 9, 485-494 https://doi.org/10.2174/138945008784533561
  36. Sofia, F.R., William, R.F., Kenneth, J.B. and Emma, J.K. (2008) Establishing the phenotype in novel acute and chronic murine models of allergic asthma. Internal. Immunopharmcol. 8, 756-763 https://doi.org/10.1016/j.intimp.2008.01.025
  37. Swirski, F.K., Sajic, D., Robbins, C.S., Gajewska, B.U., Jordana, M. and Stampfli, M.R. (2002). Chronic exposure to innocuous antigen in sensitized mice leads to suppressed airway eosinophilia that is reversed by granulocyte macrophage colony-stimulating factor. J. Immunol. 169, 3499- 3506 https://doi.org/10.4049/jimmunol.169.7.3499
  38. Tattersfield A.E., Knox, A.J., Britton, J.R. and Hall, I.P. (2002). Asthma. Lancet, 360, 1313-1322 https://doi.org/10.1016/S0140-6736(02)11312-2
  39. Temelkovski, J., Hogan, S.P., Shepherd, D.P., Foster, P.S. and Kumar, R.K. (1998). An improved murine model of asthma: selective airway inflammation, epithelial lesions and increased methacholine responsiveness following chronic exposure to aerosolised allergen. Thorax, 53, 849-856 https://doi.org/10.1136/thx.53.10.849
  40. Torres, R., Picado, C. and Mora F. (2005). Use of the mouse to unravel allergic asthma: a review of the pathogenesis of allergic asthma in mouse models and its similarity to the condition in humans. Arch. Bronconeumol. 41, 141- 152 https://doi.org/10.1016/S1579-2129(06)60415-1
  41. Toward, T.J., Smith, N. and Broadley, K.J. (2004). Effect of phosphodiesterase-5 inhibitor, sidenafil (Viagra), in animal models of airways disease. Am. J. Respir. Crit. Care Med., 169, 227-234 https://doi.org/10.1164/rccm.200211-1372OC
  42. Weiss, K.B. and Sullivan, S.D. (2001). The health economics of asthma and rhinitis. I. Assessing the economic impact. J. Allergy Clin. Immunol., 107, 3-8 https://doi.org/10.1067/mai.2001.112262
  43. Yang, G., Li, L., Volk, A., Emmell, E., Petley, T., Giles-Komar, J., Rafferty, P., Lakshminarayanan, M., Griswold, D.E., Bugelski, P.J. and Das, A.M. (2005). Therapeutic dosing with anti-interleukin-13 monoclonal antibody inhibits asthma progression in mice. J. Pharmacol. Exp. Ther., 313, 8-15
  44. Yang, G., Volk, A., Petley, T., Emmell, E., Giles-Komar, J., Shang, X., Li, J., Das, A.M., Shealy, D., Griswold, D.E. et al. (2004). Anti-IL-13 monoclonal antibody inhibits airway hyperresponsiveness, inflammation and airway remodeling. Cytokine, 28, 224-232 https://doi.org/10.1016/j.cyto.2004.08.007
  45. Yoshida, M., Watson, R.M., Rerecich, T. and O'Byrne, P.M. (2005). Different profiles of T-cell IKN-gamma and IL-12 in allergen-induced early and dual responders with asthma. J. Allergy Clin. Immunol., 115, 1004-1009 https://doi.org/10.1016/j.jaci.2005.02.003
  46. Yuk, J.E., Woo, J.S., Yun, C.Y., Lee, J.S., Kim, J.H., Song, G.Y., Uang, E.J., Hur, I.K. and Kim, I.S. (2007). Effects of lactose-$\beta$-sitosterol and $\beta$-sitosterol on ovalbumin-induced lung inflammation in actively sensitized mice. Inter. Immuno., 7, 1517-1527 https://doi.org/10.1016/j.intimp.2007.07.026