Experimental Hematology
Volume 37, Issue 6 , Pages 715-727.e3 , June 2009

Absence of α4 but not β2 integrins restrains development of chronic allergic asthma using mouse genetic models

  • Ena Ray Banerjee

      Affiliations

    • Department of Medicine, Division of Allergy and Infectious Diseases, University of Washington, Seattle, Wash., USA
    • Dr. Banerjee's current affiliation is with Advinus Therapeutics Pvt Ltd, Pune, India.
  • ,
  • Yi Jiang

      Affiliations

    • Department of Medicine, Division of Hematology, University of Washington, Seattle, Wash., USA
  • ,
  • William R. Henderson Jr.

      Affiliations

    • Department of Medicine, Division of Allergy and Infectious Diseases, University of Washington, Seattle, Wash., USA
  • ,
  • Yvette Latchman

      Affiliations

    • Puget Sound Blood Center, Seattle, Wash., USA
  • ,
  • Thalia Papayannopoulou

      Affiliations

    • Department of Medicine, Division of Hematology, University of Washington, Seattle, Wash., USA
    • Corresponding Author InformationOffprint requests to: Thalia Papayannopoulou, M.D., Division of Hematology, University of Washington, Campus Box 357710, Seattle, WA 98195-7710

Received 13 November 2008 ,Revised 26 March 2009 ,Accepted 27 March 2009.

References 

  1. Wills-Karp M. Immunologic basis of antigen-induced airway hyperresponsiveness. Annu Rev Immunol. 1999;17:255–281
  2. Shum BO, Rolph MS, Sewell WA. Mechanisms in allergic airway inflammation-lessons from studies in the mouse. Expert Rev Mol Med. 2008;10:e15
  3. Elias JA, Zhu Z, Chupp G, Homer RJ. Airway remodeling in asthma. J Clin Invest. 1999;104:1001–1006
  4. Kariyawasam HH, Robinson DS. The role of eosinophils in airway tissue remodelling in asthma. Curr Opin Immunol. 2007;19:681–686
  5. Benayoun L, Druilhe A, Dombret M-C, Aubier M, Pretolani M. Airway structural alterations selectively associated with severe asthma. Am J Respir Crit Care Med. 2003;167:1360–1368
  6. Ebina M, Takahashi T, Chiba T, Motomiya M. Cellular hypertrophy and hyperplasia of airway smooth muscles underlying bronchial asthma: a 3-d morphometric study. Am Rev Respir Dis. 1993;148:720–726
  7. Hoshino M, Nakamura Y, Sim JJ. Expression of growth factors and remodelling of the airway wall in bronchial asthma. Thorax. 1998;53:21–27
  8. Jeffery PK. Remodeling in asthma and chronic obstructive lung disease. Am J Respir Crit Care Med. 2001;164:28S–38
  9. Payne DNR, Rogers AV, Adelroth E, et al. Early thickening of the reticular basement membrane in children with difficult asthma. Am J Respir Crit Care Med. 2003;167:78–82
  10. Tanaka H, Yamada G, Saikai T, et al. Increased airway vascularity in newly diagnosed asthma using a high-magnification bronchovideoscope. Am J Respir Crit Care Med. 2003;168:1495–1499
  11. Zhou L, Li J, Goldsmith AM, et al. Human bronchial smooth muscle cell lines show a hypertrophic phenotype typical of severe asthma. Am J Respir Crit Care Med. 2004;169:703–711
  12. Epstein MM. Do mouse models of allergic asthma mimic clinical disease?. Int Arch Allergy Immunol. 2004;133:84–100
  13. Borchers MT, Crosby J, Farmer S, et al. Blockade of CD49d inhibits allergic airway pathologies independent of effects on leukocyte recruitment. Am J Physiol Lung Cell Mol Physiol. 2001;280:L813–L821
  14. Chin JE, Hatfield CA, Winterrowd GE, et al. Airway recruitment of leukocytes in mice is dependent on alpha4-integrins and vascular cell adhesion molecule-1. Am J Physiol Lung Cell Mol Physiol. 1997;272:L219–L229
  15. Henderson WR, Chi EY, Albert RK, et al. Blockade of CD49d (alpha 4 integrin) on intrapulmonary but not circulating leukocytes inhibits airway inflammation and hyperresponsiveness in a mouse model of asthma. J Clin Invest. 1997;100:3083–3092
  16. Koo GC, Shah K, Ding GJF, et al. A small molecule very late antigen-4 antagonist can inhibit ovalbumin-induced lung inflammation. Am J Respir Crit Care Med. 2003;167:1400–1409
  17. Laberge S, Rabb H, Issekutz T, Martin J. Role of VLA-4 and LFA-1 in allergen-induced airway hyperresponsiveness and lung inflammation in the rat. Am J Respir Crit Care Med. 1995;151:822–829
  18. Nakajima H, Sano H, Nishimura T, Yoshida S, Iwamoto I. Role of vascular cell adhesion molecule 1/very late activation antigen 4 and intercellular adhesion molecule 1/lymphocyte function-associated antigen 1 interactions in antigen-induced eosinophil and T cell recruitment into the tissue. J Exp Med. 1994;179:1145–1154
  19. Lee S-H, Prince JE, Rais M, et al. Differential requirement for CD18 in T-helper effector homing. Nat Med. 2003;9:1281–1286
  20. Kanwar S, Smith C, Shardonofsky F, Burns A. The role of MAC-1 (CD11b/CD18) in antigen-induced airway eosinophilia in mice. Am J Respir Cell Mol Biol. 2001;25:170–177
  21. Schneider T, Issekutz TB, Issekutz AC. The role of alpha 4 (CD49d) and beta 2 (CD18) integrins in eosinophil and neutrophil migration to allergic lung inflammation in the brown Norway rat. Am J Respir Cell Mol Biol. 1999;20:448–457
  22. Banerjee ER, Jiang Y, Henderson WR, Scott LM, Papayannopoulou T. Alpha4 and beta2 integrins have nonredundant roles for asthma development, but for optimal allergen sensitization only alpha4 is critical. Exp Hematol. 2007;35:605–617
  23. Barthel SR, Johansson MW, McNamee DM, Mosher DF. Roles of integrin activation in eosinophil function and the eosinophilic inflammation of asthma. J Leukoc Biol. 2008;83:1–12
  24. Scott LM, Priestley GV, Papayannopoulou T. Deletion of alpha4 integrins from adult hematopoietic cells reveals roles in homeostasis, regeneration, and homing. Mol Cell Biol. 2003;23:9349–9360
  25. Iwata A, Nishio K, Winn RK, Chi EY, Henderson WR, Harlan JM. A broad-spectrum caspase inhibitor attenuates allergic airway inflammation in murine asthma model. J Immunol. 2003;170:3386–3391
  26. Henderson WR, Chi EY, Maliszewski CR. Soluble IL-4 receptor inhibits airway inflammation following allergen challenge in a mouse model of asthma. J Immunol. 2000;164:1086–1095
  27. Henderson WR, Lewis DB, Albert RK, et al. The importance of leukotrienes in airway inflammation in a mouse model of asthma. J Exp Med. 1996;184:1483–1494
  28. Cho JY, Miller M, Baek KJ, et al. Inhibition of airway remodeling in IL-5-deficient mice. J Clin Invest. 2004;113:551–560
  29. Henderson W, Banerjee E, Chi E. Differential effects of (s)- and (r)-enantiomers of albuterol in a mouse asthma model. J Allergy Clin Immunol. 2005;116:332–340
  30. Lloyd C, Gutierrez-Ramos J. Animal models to study chemokine receptor function: in vivo mouse models of allergic airway inflammation. Methods Mol Biol. 2004;239:199–210
  31. Larbi KY, Allen AR, Tam FWK, et al. VCAM-1 has a tissue-specific role in mediating interleukin-4-induced eosinophil accumulation in rat models: evidence for a dissociation between endothelial-cell VCAM-1 expression and a functional role in eosinophil migration. Blood. 2000;96:3601–3609
  32. Lobb R, Hemler M. The pathophysiologic role of alpha 4 integrins in vivo. J Clin Invest. 1994;94:1722–1728
  33. Banerjee ER, Latchman YE, Jiang Y, Priestley GV, Papayannopoulou T. Distinct changes in adult lymphopoiesis in Rag2(-/-) mice fully reconstituted by alpha4-deficient adult bone marrow cells. Exp Hematol. 2008;36:1004–1013
  34. Moir LM, Burgess JK, Black JL. Transforming growth factor beta 1 increases fibronectin deposition through integrin receptor alpha 5 beta 1 on human airway smooth muscle. J Allergy Clin Immunol. 2008;121:1034–1039e1034
  35. Takeda K, Haczku A, Lee J, Irvin C, Gelfand E. Strain dependence of airway hyperresponsiveness reflects differences in eosinophil localization in the lung. Am J Physiol Lung Cell Mol Physiol. 2001;281:L394–402
  36. Berlin AA, Hogaboam CM, Lukacs NW. Inhibition of SCF attenuates peribronchial remodeling in chronic cockroach allergen-induced asthma. Lab Invest. 2006;86:557–565
  37. Dolgachev V, Berlin AA, Lukacs NW. Eosinophil activation of fibroblasts from chronic allergen-induced disease utilizes stem cell factor for phenotypic changes. Am J Pathol. 2008;172:68–76
  38. Kovach NL, Lin N, Yednock T, Harlan JM, Broudy VC. Stem cell factor modulates avidity of alpha 4 beta 1 and alpha 5 beta 1 integrins expressed on hematopoietic cell lines. Blood. 1995;85:159–167
  39. Al-Muhsen SZ, Shablovsky G, Olivenstein R, Mazer B, Hamid Q. The expression of stem cell factor and c-kit receptor in human asthmatic airways. Clin Exp Allergy. 2004;34:911–916
  40. Tan BL, Yazicioglu MN, Ingram D, et al. Genetic evidence for convergence of c-kit- and alpha 4 integrin-mediated signals on class IA PI-3kinase and the Rac pathway in regulating integrin-directed migration in mast cells. Blood. 2003;101:4725–4732
  41. Reuter S, Taube C. Mast cells and the development of allergic airway disease. J Occup Med Toxicol. 2008;3(Suppl 1):S2
  42. Abonia JP, Hallgren J, Jones T, et al. Alpha-4 integrins and VCAM-1, but not MAdCAM-1, are essential for recruitment of mast cell progenitors to the inflamed lung. Blood. 2006;108:1588–1594
  43. Gonzalo J-A, Qiu Y, Lora JM, et al. Coordinated involvement of mast cells and T cells in allergic mucosal inflammation: critical role of the CC chemokine ligand 1:CCR8 axis. J Immunol. 2007;179:1740–1750
  44. Hojo M, Maghni K, Issekutz TB, Martin JG. Involvement of alpha -4 integrins in allergic airway responses and mast cell degranulation in vivo. Am J Respir Crit Care Med. 1998;158:1127–1133
  45. Harrington LE, Hatton RD, Mangan PR, et al. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol. 2005;6:1123–1132
  46. Park H, Li Z, Yang XO, et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol. 2005;6:1133–1141
  47. Song C, Luo L, Lei Z, et al. IL-17-producing alveolar macrophages mediate allergic lung inflammation related to asthma. J Immunol. 2008;181:6117–6124
  48. Schnyder-Candrian S, Togbe D, Couillin I, et al. Interleukin-17 is a negative regulator of established allergic asthma. J Exp Med. 2006;203:2715–2725
  49. Lewkowich IP, Lajoie S, Clark JR, Herman NS, Sproles AA, Wills-Karp M. Allergen uptake, activation, and IL-23 production by pulmonary myeloid DCs drives airway hyperresponsiveness in asthma-susceptible mice. PLoS ONE. 2008;3:e3879
  50. Jain D, Keslacy S, Tliba O, et al. Essential role of IFNbeta and CD38 in TNFalpha-induced airway smooth muscle hyper-responsiveness. Immunobiology. 2008;213:499–509
  51. Kim BE, Leung DYM, Boguniewicz M, Howell MD. Loricrin and involucrin expression is down-regulated by Th2 cytokines through STAT-6. Clin Immunol. 2008;126:332
  52. Kumar RK, Herbert C, Webb DC, Li L, Foster PS. Effects of anticytokine therapy in a mouse model of chronic asthma. Am J Respir Crit Care Med. 2004;170:1043–1048
  53. Broide DH. Immunologic and inflammatory mechanisms that drive asthma progression to remodeling. J Allergy Clin Immunol. 2008;121:560–570
  54. Lee CG, Homer RJ, Zhu Z, et al. Interleukin-13 induces tissue fibrosis by selectively stimulating and activating transforming growth factor beta (1). J Exp Med. 2001;194:809–822
  55. Nath P, Yee Leung S, Williams AS, et al. Complete inhibition of allergic airway inflammation and remodelling in quadruple IL-4/5/9/13 -/- mice. Clin Exp Allergy. 2007;37:1427–1435
  56. Kumar RK, Herbert C, Yang M, Koskinen AML, McKenzie ANJ, Foster PS. Role of interleukin-13 in eosinophil accumulation and airway remodelling in a mouse model of chronic asthma. Clin Exp Allergy. 2002;32:1104–1111
  57. Lai W-Q, Goh HH, Bao Z, Wong WSF, Melendez AJ, Leung BP. The role of sphingosine kinase in a murine model of allergic asthma. J Immunol. 2008;180:4323–4329
  58. Roth M, Johnson PRA, Borger P, et al. Dysfunctional interaction of C/EBP{alpha} and the glucocorticoid receptor in asthmatic bronchial smooth-muscle cells. N Engl J Med. 2004;351:560–574
  59. Ulyanova T, Priestley G, Banerjee E, Papayannopoulou T. Unique and redundant roles of alpha4 and beta2 integrins in kinetics of recruitment of lymphoid vs myeloid cell subsets to the inflamed peritoneum revealed by studies of genetically deficient mice. Exp Hematol. 2007;35:1256–1265
  60. Koerner-Rettberg C, Doths S, Stroet A, Schwarze J. Reduced lung function in a chronic asthma model is associated with prolonged inflammation, but independent of peribronchial fibrosis. PLoS ONE. 2008;3:e1575

PII: S0301-472X(09)00117-9

doi: 10.1016/j.exphem.2009.03.010

Experimental Hematology
Volume 37, Issue 6 , Pages 715-727.e3 , June 2009