[en] Among proteases, metalloproteases are implicated in tissue remodeling, as shown in numerous diseases including allergy. ADAMs (A Disintegrin And Metalloprotease) metalloproteases are implicated in physiologic processes such as cytokine and growth factor shedding, cell migration, adhesion, or repulsion. Our aim was to measure ADAM-12 expression in airway epithelium and to define its role during the allergic response. To raise this question, we analyzed the ADAM-12 expression ex vivo after allergen exposure in patients with allergic rhinitis and in vitro in cultured primary human airway epithelial cells (AEC). Clones of BEAS-2B cells transfected with the full-length form of ADAM-12 were generated to study the consequences of ADAM-12 up-regulation on AEC function. After allergen challenge, a strong increase of ADAM-12 expression was observed in airway epithelium from patients with allergic rhinitis but not from control subjects. In contrast with the other HB-epidermal growth factor sheddases, ADAM-10 and -17, TNF-alpha in vitro increased the expression of ADAM-12 by AEC, an effect amplified by IL-4 and IL-13. Up-regulation of ADAM-12 in AEC increased the expression of alpha3 and alpha4 integrins and to the modulation of cell migration on fibronectin but not on collagen. Moreover, overexpression of ADAM-12 in BEAS-2B enhanced the secretion of CXCL1 and CXCL8 and their capacity to recruit neutrophils. CD47 was strongly decreased by ADAM-12 overexpression, a process associated with a reduced adhesion of neutrophils. These effects were mainly dependent on epidermal growth factor receptor activation. In summary, ADAM-12 is produced during allergic reaction by AEC and might increase neutrophil recruitment within airway mucosa.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Rocks, Natacha ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, humaines et path.
Estrella, C
Paulissen, Geneviève ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Quesada Calvo, Florence ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques
Noël, Agnès ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie cellulaire et moléculaire appliquée à l'homme
Vilain, E.
Lassalle, P.
Tillie-Leblond, I.
Cataldo, Didier ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, humaines et path.
Gosset, P
Language :
English
Title :
Role of A Disintegrin and Metalloprotease-12 in Neutrophil Recruitment Induced by Airway Epithelium.
Publication date :
2009
Journal title :
American Journal of Respiratory Cell and Molecular Biology
ISSN :
1044-1549
eISSN :
1535-4989
Publisher :
American Thoracic Society, New York, United States - New York
Bousquet, J., Jeffery, P.K., Busse, W.W., Johnson, M., Vignola, A.M., Asthma: From bronchoconstriction to airways inflammation and remodeling (2000) American Journal of Respiratory and Critical Care Medicine, 161 (5), pp. 1720-1745
Lamblin, C., Gosset, P., Tillie-Leblond, I., Saulnier, F., Marquette, C.-H., Wallaert, B., Tonnel, A.B., Bronchial neutrophilia in patients with noninfectious status asthmaticus (1998) American Journal of Respiratory and Critical Care Medicine, 157 (2), pp. 394-402
Gosset, P., Tillie-Leblond, I., Malaquin, F., Durieu, J., Wallaert, B., Tonnel, A.-B., Interleukin-8 secretion in patients with allergic rhinitis after an allergen challenge: Interleukin-8 is not the main chemotactic factor present in nasal lavages (1997) Clinical and Experimental Allergy, 27 (4), pp. 379-388
Vignola, A.M., Riccobono, L., Mirabella, A., Profita, M., Chanez, P., Bellia, V., Mautino, G., Bonsignore, G., Sputum metalloproteinase-9/tissue inhibitor of metalloproteinase-1 ratio correlates with airflow obstruction in asthma and chronic bronchitis (1998) American Journal of Respiratory and Critical Care Medicine, 158 (6), pp. 1945-1950
Mautino, G., Oliver, N., Chanez, P., Bousquet, J., Capony, F., Increased Release of Matrix Metalloproteinase-9 in Bronchoalveolar Lavage Fluid and by Alveolar Macrophages of Asthmatics (1997) American Journal of Respiratory Cell and Molecular Biology, 17 (5), pp. 583-591
Cataldo, D.D., Tournoy, K.G., Vermaelen, K., Munaut, C., Foidart, J.-M., Louis, R., Noel, A., Pauwels, R.A., Matrix metalloproteinase-9 deficiency impairs cellular infiltration and bronchial hyperresponsiveness during allergen-induced airway inflammation (2002) American Journal of Pathology, 161 (2), pp. 491-498
Cataldo, D., Munaut, C., Noel, A., Frankenne, F., Bartsch, P., Foidart, J.M., Louis, R., MMP-2- And MMP-9-linked gelatinolytic activity in the sputum from patients with asthma and chronic obstructive pulmonary disease (2000) Int Arch Allergy Immunol, 123, pp. 259-267
Van Eerdewegh, P., Little, R.D., Dupuis, J., Del Mastro, R.G., Falls, K., Simon, J., Torrey, D., Keith, T.P., Association of the ADAM33 gene with asthma and bronchial hyperresponsiveness (2002) Nature, 418 (6896), pp. 426-430. , DOI 10.1038/nature00878
King, N.E., Zimmermann, N., Pope, S.M., Fulkerson, P.C., Nikolaidis, N.M., Mishra, A., Witte, D.P., Rothenberg, M.E., Expression and regulation of a disintegrin and metalloproteinase (ADAM) 8 in experimental asthma (2004) American Journal of Respiratory Cell and Molecular Biology, 31 (3), pp. 257-265. , DOI 10.1165/rcmb.2004-0026OC
Paulissen, G., Rocks, N., Quesada-Calvo, F., Gosset, P., Foidart, J.-M., Noel, A., Louis, R., Cataldo, D.D., Expression of ADAMs and their inhibitors in sputum from patients with asthma (2006) Molecular Medicine, 12 (7-8), pp. 171-179. , DOI 10.2119/2006-00028.Paulissen
Blobel, C.P., ADAMs: Key components in EGFR signalling and development (2005) Nat Rev Mol Cell Biol, 6, pp. 32-43
Porter, S., Clark, I.M., Kevorkian, L., Edwards, D.R., The ADAMTS metalloproteinases (2005) Biochem J, 386, pp. 15-27
Gilpin, B.J., Loechel, F., Mattei, M.-G., Engvall, E., Albrechtsen, R., Wewer, U.M., A novel secreted form of human ADAM 12 (meltrin alpha) provokes myogenesis in vivo (1998) Journal of Biological Chemistry, 273 (1), pp. 157-166. , DOI 10.1074/jbc.273.1.157
Brzoska, E., Bello, V., Darribere, T., Moraczewski, J., Integrin alpha3 subunit participates in myoblast adhesion and fusion in vitro (2006) Differentiation, 74 (2-3), pp. 105-118. , DOI 10.1111/j.1432-0436.2005.00059.x
Thodeti, C.K., Albrechtsen, R., Grauslund, M., Asmar, M., Larsson, C., Takada, Y., Mercurio, A.M., Wewer, U.M., ADAM12/syndecan-4 signaling promotes beta1 integrin-dependent cell spreading through protein kinase Calpha and RhoA (2003) Journal of Biological Chemistry, 278 (11), pp. 9576-9584. , DOI 10.1074/jbc.M208937200
Thodeti, C.K., Frohlich, C., Nielsen, C.K., Takada, Y., Fassler, R., Albrechtsen, R., Wewer, U.M., ADAM12-mediated focal adhesion formation is differently regulated by beta1 and beta3 integrins (2005) FEBS Letters, 579 (25), pp. 5589-5595. , DOI 10.1016/j.febslet.2005.09.024, PII S0014579305011348
Asakura, M., Kitakaze, M., Takashima, S., Liao, Y., Ishikura, F., Yoshinaka, T., Ohmoto, H., Higashiyama, S., Cardiac hypertrophy is inhibited by antagonism of ADAM12 processing of HB-EGF: Metalloproteinase inhibitors as a new therapy (2002) Nature Medicine, 8 (1), pp. 35-40. , DOI 10.1038/nm0102-35
Rocks, N., Estrella, C., Paulissen, G., Quesada-Calvo, F., Gilles, C., Gueders, M., Crahay, C., Noël, A., The metalloproteinase ADAM-12 regulates bronchial epithelial cell proliferation and apoptosis (2008) Cell Prolif, 41, pp. 988-1001
White, J.M., ADAMs: Modulators of cell-cell and cell-matrix interactions (2003) Curr Opin Cell Biol, 15, pp. 598-606
Peduto, L., Reuter, V.E., Sehara-Fujisawa, A., Shaffer, D.R., Scher, H.I., Blobel, C.P., ADAM12 is highly expressed in carcinoma-associated stroma and is required for mouse prostate tumor progression (2006) Oncogene, 25 (39), pp. 5462-5466. , DOI 10.1038/sj.onc.1209536, PII 1209536
Le Pabic, H., Bonnier, D., Wewer, U.M., Coutand, A., Musso, O., Baffet, G., Clement, B., Theret, N., ADAM12 in human liver cancers: TGF-beta-regulated expression in stellate cells is associated with matrix remodeling (2003) Hepatology, 37 (5), pp. 1056-1066. , DOI 10.1053/jhep.2003.50205
Kodama, T., Ikeda, E., Okada, A., Ohtsuka, T., Shimoda, M., Shiomi, T., Yoshida, K., Okada, Y., ADAM12 is selectively overexpressed in human glioblastomas and is associated with glioblastoma cell proliferation and shedding of heparin-binding epidermal growth factor (2004) American Journal of Pathology, 165 (5), pp. 1743-1753
Bradding, P., Mediwake, R., Feather, I.H., Madden, J., Church, M.K., Holgate, S.T., Howarth, P.H., TNF alpha is localized to nasal mucosal mast cells and is released in acute allergic rhinitis (1995) Clin Exp Allergy, 25, pp. 406-415
Bachert, C., Wagenmann, M., Hauser, U., Proinflammatory cytokines: Measurement in nasal secretion and induction of adhesion receptor expression (1995) Int Arch Allergy Immunol, 107, pp. 106-108
Demoly, P., Crampette, L., Lebel, B., Campbell, A.M., Mondain, M., Bousquet, J., Expression of cyclo-oxygenases 1 and 2 proteins in upper respiratory mucosa (1998) Clinical and Experimental Allergy, 28 (3), pp. 278-283. , DOI 10.1046/j.1365-2222.1998.00212.x
Just, N., Tillie-Leblond, I., Guery, B.P.H., Fourneau, C., Tonnel, A.-B., Gosset, P., Keratinocyte growth factor (KGF) decreases ICAM-1 and VCAM-1 cell expression on bronchial epithelial cells (2003) Clinical and Experimental Immunology, 132 (1), pp. 61-69. , DOI 10.1046/j.1365-2249.2003.02102.x
Mukaida, N., Pathophysiological roles of interleukin-8/CXCL8 in pulmonary diseases (2003) Am J Physiol, 284, pp. L566-L577
Subramanian, S., Boder, E.T., Discher, D.E., Phylogenetic divergence of CD47 interactions with human signal regulatory protein alpha reveals locus of species specificity: Implications for the binding site (2007) Journal of Biological Chemistry, 282 (3), pp. 1805-1818. , http://www.jbc.org/cgi/reprint/282/3/1805, DOI 10.1074/jbc.M603923200
Zen, K., Parkos, C.A., Leukocyte-epithelial interactions (2003) Curr Opin Cell Biol, 15, pp. 557-564
Mette, S.A.P.J., Buck, C.A., Albelda, S.M., Distribution of integrin cell adhesion receptors on normal bronchial epithelial cells and lung cancer cells in vitro and in vivo (1993) Am J Respir Cell Mol Biol, 8, pp. 562-572
Huang, J., Bridges, L.C., White, J.M., Selective modulation of integrin-mediated cell migration by distinct ADAM family members (2005) Molecular Biology of the Cell, 16 (10), pp. 4982-4991. , DOI 10.1091/mbc.E05-03-0258
Kuhn III, C., Boldt, J., King Jr., T.E., Crouch, E., Vartio, T., McDonald, J.A., An immunohistochemical study of architectural remodeling and connective tissue synthesis in pulmonary fibrosis (1989) American Review of Respiratory Disease, 140 (6), pp. 1693-1703
White, S.R., Dorscheid, D.R., Rabe, K.F., Wojcik, K.R., Hamann, K.J., Role of very late adhesion integrins in mediating repair of human airway epithelial cell monolayers after mechanical injury (1999) Am J Respir Cell Mol Biol, 20, pp. 787-796
Puchelle, E., Zahm, J.-M., Tournier, J.-M., Coraux, C., Airway epithelial repair, regeneration, and remodeling after injury in chronic obstructive pulmonary disease (2006) Proceedings of the American Thoracic Society, 3 (8), pp. 726-733. , http://pats.atsjournals.org/cgi/reprint/3/8/726, DOI 10.1513/pats.200605-126SF
Liu, Y., Shaw, S.K., Ma, S., Yang, L., Luscinskas, F.W., Parkos, C.A., Regulation of Leukocyte Transmigration: Cell Surface Interactions and Signaling Events (2004) Journal of Immunology, 172 (1), pp. 7-13
Parkos, C.A., Colgan, S.P., Diamond, M.S., Nusrat, A., Liang, T.W., Springer, T.A., Madara, J.L., Expression and polarization of intercellular adhesion molecule-1 on human intestinal epithelia: Consequences for CD11b/CD18-mediated interactions with neutrophils (1996) Molecular Medicine, 2 (4), pp. 489-505
Taguchi, M., Sampath, D., Koga, T., Castro, M., Look, D.C., Nakajima, S., Holtzman, M.J., Patterns for RANTES secretion and intercellular adhesion molecule 1 expression mediate transepithelial T cell traffic based on analyses in vitro and in vivo (1998) Journal of Experimental Medicine, 187 (12), pp. 1927-1940. , DOI 10.1084/jem.187.12.1927
Shinohara, M., Ohyama, N., Murata, Y., Okazawa, H., Ohnishi, H., Ishikawa, O., Matozaki, T., CD47 regulation of epithelial cell spreading and migration, and its signal transduction (2006) Cancer Science, 97 (9), pp. 889-895. , DOI 10.1111/j.1349-7006.2006.00245.x
Liu, Y., Merlin, D., Burst, S.L., Pochet, M., Madara, J.L., Parkos, C.A., The role of CD47 in neutrophil transmigration: Increased rate of migration correlates with increased cell surface expression of CD47 (2001) Journal of Biological Chemistry, 276 (43), pp. 40156-40166
Parkos, C.A., Colgan, S.P., Liang, T.W., Nusrat, A., Bacarra, A.E., Carnes, D.K., Madara, J.L., CD47 mediates post-adhesive events required for neutrophil migration across polarized intestinal epithelia (1996) Journal of Cell Biology, 132 (3), pp. 437-450. , DOI 10.1083/jcb.132.3.437
Ohnishi, H., Kobayashi, H., Okazawa, H., Ohe, Y., Tomizawa, K., Sato, R., Matozaki, T., Ectodomain shedding of SHPS-1 and its role in regulation of cell migration (2004) Journal of Biological Chemistry, 279 (27), pp. 27878-27887. , DOI 10.1074/jbc.M313085200
Lemjabbar, H., Basbaum, C., Platelet-activating factor receptor and ADAM10 mediate responses to Staphylococcus aureus in epithelial cells (2002) Nature Medicine, 8 (1), pp. 41-46. , DOI 10.1038/nm0102-41
Shao, M.X., Ueki, I.F., Nadel, J.A., Tumor necrosis factor alpha-converting enzyme mediates muc5ac mucin expression in cultured human airway epithelial cells (2003) Proc Natl Acad Sci USA, 100, pp. 11618-11623
Nadel, J.A., Role of epidermal growth factor receptor activation in regulating mucin synthesis (2001) Respiratory Research, 2 (2), pp. 85-89. , DOI 10.1186/rr43
Le Quement, C., Guenon, I., Gillon, J.Y., Lagente, V., Boichot, E., Mmp-12 induces IL-8/CXCL8 secretion through EGFR and ERK1/2 activation in epithelial cells (2008) Am J Physiol, 294, pp. L1076-L1084