Airway epithelial cells produce neurotrophins and promote the survival of eosinophils during allergic airway inflammation

Journal of Allergy and Clinical Immunology

Volumn 117, Issue 4, 2006, Pages 787-794

  Hahn, Christian ^a   Islamian, Ariyan Pirayesh ^a   Renz, Harald ^a   Nockher, Wolfgang Andreas ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

airway epithelium; Allergy; asthma; brain derived neutrotrophic factor; eosinophils; nerve growth factor; neurotrophin; survival

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CYTOKINE; INTERLEUKIN 1BETA; K 252A; NERVE GROWTH FACTOR; NEUROTROPHIN; PROTEIN TYROSINE KINASE A; TUMOR NECROSIS FACTOR ALPHA;

ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHUS HYPERREACTIVITY; CELL INTERACTION; CELL SURVIVAL; COCULTURE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EOSINOPHILIA; FEMALE; IMMUNOHISTOCHEMISTRY; LUNG LAVAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RESPIRATORY EPITHELIUM; SURVIVAL TIME; TH2 CELL; UPREGULATION;

ANIMALS; ASTHMA; BASE SEQUENCE; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL SURVIVAL; CYTOKINES; EOSINOPHILS; EPITHELIAL CELLS; FEMALE; INFLAMMATION MEDIATORS; MICE; MICE, INBRED BALB C; MODELS, BIOLOGICAL; NERVE GROWTH FACTORS; RECEPTOR, TRKA; RECEPTOR, TRKB; RESPIRATORY HYPERSENSITIVITY; RESPIRATORY SYSTEM; RNA, MESSENGER;

EID: 33644768626     PISSN: 00916749     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jaci.2005.12.1339     Document Type: Article

References (37)

1. Lee N.A., Gelfand E.W., and Lee J.J. Pulmonary T cells and eosinophils: coconspirators or independent triggers of allergic respiratory pathology?. J Allergy Clin Immunol 107 (2001) 945-957
2. Kay A.B. Asthma and inflammation. J Allergy Clin Immunol 87 (1991) 893-910
3. Walsh G.M. Eosinophil apoptosis: mechanisms and clinical relevance in asthmatic and allergic inflammation. Br J Haematol 111 (2000) 61-67
4. Tai P.C., Sun L., and Spry C.J. Effects of IL-5, granulocyte/macrophage colony-stimulating factor (GM-CSF) and IL-3 on the survival of human blood eosinophils in vitro. Clin Exp Immunol 85 (1991) 312-316
5. Yamaguchi Y., Suda T., Ohta S., Tominaga K., Miura Y., and Kasahara T. Analysis of the survival of mature human eosinophils: interleukin-5 prevents apoptosis in mature human eosinophils. Blood 78 (1991) 2542-2547
6. Nassenstein C., Braun A., Erpenbeck V.J., Lommatzsch M., Schmidt S., Krug N., et al. The neurotrophins nerve growth factor, brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4 are survival and activation factors for eosinophils in patients with allergic bronchial asthma. J Exp Med 198 (2003) 455-467
7. Lewin G.R., and Barde Y.A. Physiology of the neurotrophins. Annu Rev Neurosci 19 (1996) 289-317
8. Pattarawarapan M., and Burgess K. Molecular basis of neurotrophin-receptor interactions. J Med Chem 46 (2003) 5277-5291
9. Nockher W.A., and Renz H. Neurotrophins in inflammatory lung diseases: modulators of cell differentiation and neuroimmune interactions. Cytokine Growth Factor Rev 14 (2003) 559-578
10. Braun A., Lommatzsch M., Mannsfeldt A., Neuhaus-Steinmetz U., Fischer A., Schnoy N., et al. Cellular sources of enhanced brain-derived neurotrophic factor production in a mouse model of allergic inflammation. Am J Respir Cell Mol Biol 21 (1999) 537-546
11. Braun A., Appel E., Baruch R., Herz U., Botchkarev V., Paus R., et al. Role of nerve growth factor in a mouse model of allergic airway inflammation and asthma. Eur J Immunol 28 (1998) 3240-3251
12. Virchow J.C., Julius P., Lommatzsch M., Luttmann W., Renz H., and Braun A. Neurotrophins are increased in bronchoalveolar lavage fluid after segmental allergen provocation. Am J Respir Crit Care Med 158 (1998) 2002-2005
13. Kassel O., de Blay F., Duvernelle C., Olgart C., Israel-Biet D., Krieger P., et al. Local increase in the number of mast cells and expression of nerve growth factor in the bronchus of asthmatic patients after repeated inhalation of allergen at low-dose. Clin Exp Allergy 31 (2001) 1432-1440
14. Walsh G.M. Eosinophil-epithelial cell interactions: a special relationship?. Clin Exp Allergy 31 (2001) 351-354
15. Davidson D.J., Kilanowski F.M., Randell S.H., Sheppard D.N., and Dorin J.R. A primary culture model of differentiated murine tracheal epithelium. Am J Physiol Lung Cell Mol Physiol 279 (2000) L766-L778
16. Berg M.M., Sternberg D.W., Parada L.F., and Chao M.V. K-252a inhibits nerve growth factor-induced trk proto-oncogene tyrosine phosphorylation and kinase activity. J Biol Chem 267 (1992) 13-16
17. Tapley P., Lamballe F., and Barbacid M. K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk family of oncogenes and neurotrophin receptors. Oncogene 7 (1992) 371-381
18. Schuhmann B., Dietrich A., Sel S., Hahn C., Klingenspor M., Lommatzsch M., et al. A role for brain-derived neurotrophic factor in B cell development. J Neuroimmunol 163 (2004) 15-23
19. Wegmann M., Fehrenbach M., Fehrenbach A., Held T., Schramm C., Garn H., et al. Involvement of distal airways in a chronic model of experimental asthma. Clin Exp Allergy 35 (2005) 1263-1271
20. Ricci A., Felici L., Mariotta S., Mannino F., Schmid G., Terzano C., et al. Neurotrophin and neurotrophin receptor protein expression in the human lung. Am J Respir Cell Mol Biol 30 (2004) 12-19
21. Nockher W.A., and Renz H. Neurotrophins in clinical diagnostics: pathophysiology and laboratory investigation. Clin Chim Acta 352 (2005) 49-74
22. Carr M.J., Hunter D.D., and Undem B.J. Neurotrophins and asthma. Curr Opin Pulm Med 7 (2001) 1-7
23. Braun A., Nockher W.A., and Renz H. Neuro-immune interactions in the pathogenesis of bronchial asthma (2002), Marcel Dekker Inc, New York p. 311-42
24. Bonini S., Rasi G., Bracci-Laudiero M.L., Procoli A., and Aloe L. Nerve growth factor: neurotrophin or cytokine?. Int Arch Allergy Immunol 131 (2003) 80-84
25. Sousa A.R., Lane S.J., Nakhosteen J.A., Lee T.H., and Poston R.N. Expression of interleukin-1 beta (IL-1beta) and interleukin-1 receptor antagonist (IL-1ra) on asthmatic bronchial epithelium. Am J Respir Crit Care Med 154 (1996) 1061-1066
26. Keatings V.M., Collins P.D., Scott D.M., and Barnes P.J. Differences in interleukin-8 and tumor necrosis factor-alpha in induced sputum from patients with chronic obstructive pulmonary disease or asthma. Am J Respir Crit Care Med 153 (1996) 530-534
27. Robinson D., Hamid Q., Bentley A., Ying S., Kay A.B., and Durham S.R. Activation of CD4+ T cells, increased TH2-type cytokine mRNA expression, and eosinophil recruitment in bronchoalveolar lavage after allergen inhalation challenge in patients with atopic asthma. J Allergy Clin Immunol 92 (1993) 313-324
28. Path G., Braun A., Meents N., Kerzel S., Quarcoo D., Raap U., et al. Augmentation of allergic early-phase reaction by nerve growth factor. Am J Respir Crit Care Med 166 (2002) 818-826
29. Kerzel S., Path G., Nockher W.A., Quarcoo D., Raap U., Groneberg D.A., et al. Pan-neurotrophin receptor p75 contributes to neuronal hyperreactivity and airway inflammation in a murine model of experimental asthma. Am J Respir Cell Mol Biol 28 (2003) 170-178
30. Pawankar R. Epithelial cells as immunoregulators in allergic airway diseases. Curr Opin Allergy Clin Immunol 2 (2002) 1-5
31. Tomee J.F., van Weissenbruch R., de Monchy J.G., and Kauffman H.F. Interactions between inhalant allergen extracts and airway epithelial cells: effect on cytokine production and cell detachment. J Allergy Clin Immunol 102 (1998) 75-85
32. Moqbel R., Ying S., Barkans J., Newman T.M., Kimmitt P., Wakelin M., et al. Identification of messenger RNA for IL-4 in human eosinophils with granule localization and release of the translated product. J Immunol 155 (1995) 4939-4947
33. Schmid-Grendelmeier P., Altznauer F., Fischer B., Bizer C., Straumann A., Menz G., et al. Eosinophils express functional IL-13 in eosinophilic inflammatory diseases. J Immunol 169 (2002) 1021-1027
34. Burgel P.R., Lazarus S.C., Tam D.C., Ueki I.F., Atabai K., Birch M., et al. Human eosinophils induce mucin production in airway epithelial cells via epidermal growth factor receptor activation. J Immunol 167 (2001) 5948-5954
35. Wong C.K., Wang C.B., Ip W.K., Tian Y.P., and Lam C.W. Role of p38 MAPK and NF-kB for chemokine release in coculture of human eosinophils and bronchial epithelial cells. Clin Exp Immunol 139 (2005) 90-100
36. Hamada A., Watanabe N., Ohtomo H., and Matsuda H. Nerve growth factor enhances survival and cytotoxic activity of human eosinophils. Br J Haematol 93 (1996) 299-302
37. Raap U., Goltz C., Deneka N., Bruder M., Renz H., Kapp A., et al. Brain-derived neurotrophic factor is increased in atopic dermatitis and modulates eosinophil functions compared with that seen in nonatopic subjects. J Allergy Clin Immunol 115 (2005) 1268-1275