MMP-19 Deficiency Promotes Tenascin-C Accumulation and Allergen-induced Airway Inflammation.

[en] Matrix metalloproteinases (MMPs) recently appeared as key regulators of inflammation, allowing recruitment and clearance of inflammatory cells and modifying the biological activity of many peptidic mediators by cleavage. MMP-19 is a newly described MMP and preferentially cleaves matrix proteins such as collagens and tenascin-C. The role of MMP-19 in asthma has not been described to date. The purpose of the present study was to assess MMP-19 expression in a murine asthma model and to address biological effects of MMP-19 deficiency in mice. Allergenexposed wild-type (WT) mice displayed an increased expression of MMP-19 mRNA and an increased number of MMP-19-positive cells in the lungs detected by immunohistochemistry. After allergen challenge of MMP-19 knockout (MMP-19-/-) mice, an exacerbated eosinophilic inflammation was detected in bronchoalveolar lavage fluid and bronchial tissue along with an increased airway responsiveness to methacholine. A shift towards increased Th2-driven inflammation in MMP-19-/- mice was demonstrated by 1) increased numbers of cells expressing the IL-33 receptor T1/ST2 in lung parenchyma, 2) increased IgG1 levels in serum and 3) higher levels of IL-13 and CCL11 in lung extracts. Tenascin-C was found accumulated in peribronchial areas of MMP-19-/- after allergen challenges as assessed by Western blot and immunohistochemistry analysis. We conclude that MMP-19 is a new mediator in asthma, preventing tenascin-C accumulation and directly or indirectly controlling Th2-driven airway eosinophilia and airway hyperreactivity. Our data suggest that MMP-19 might act on Th2 inflammation homeostasis through preventing tenascin protein accumulation.

Disciplines :

Biochemistry, biophysics & molecular biology
Rheumatology

Author, co-author :

Guéders, Maud ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement

Hirst, S.

Quesada Calvo, Florence ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques

Paulissen, Geneviève ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement

Hacha, Jonathan ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement

Gilles, Christine ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement

Gosset, P.

Louis, Renaud ; Université de Liège - ULiège > Département des sciences cliniques > Pneumologie - Allergologie

Foidart, Jean-Michel ; Université de Liège - ULiège > Département des sciences cliniques > Gynécologie - Obstétrique - Labo de biologie des tumeurs et du développement

Lopez-Otin, C.

Noël, Agnès ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie cellulaire et moléculaire appliquée à l'homme

Cataldo, Didier ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, humaines et path.

Language :

English

Title :

MMP-19 Deficiency Promotes Tenascin-C Accumulation and Allergen-induced Airway Inflammation.

Publication date :

2010

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

Volume :

Issue :

Pages :

286-95

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 17 January 2010

Statistics

Number of views

247 (24 by ULiège)

Number of downloads

248 (4 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Bousquet J, Chanez P, Lacoste JY, Barneon G, Ghavanian N, Enander I, Venge P, Ahlstedt S, Simony-Lafontaine J, Godard P. Eosinophilic inflammation in asthma. N Engl J Med 1990;323:1033-1039.
Louis R, Lau LC, Bron AO, Roldaan AC, Radermecker M, Djukanovic R. The relationship between airways inflammation and asthma severity. Am J Respir Crit Care Med 2000;161:9-16.
Louis R, Sele J, Henket M, Cataldo D, Bettiol J, Seiden L, Bartsch P. Sputum eosinophil count in a large population of patients with mild to moderate steroid-naive asthma: distribution and relationship with methacholine bronchial hyperresponsiveness. Allergy 2000;57:907-912.
Wills-Karp W. Interleukin-13 in asthma pathogenesis. Immunol Rev 2002;202:175-190.
Cataldo DD, Gueders MM, Rocks N, Sounni NE, Evrard B, Bartsch P, Louis R, Noel A, Foidart JM. Pathogenic role of matrix metalloproteases and their inhibitors in asthma and chronic obstructive pulmonary disease and therapeutic relevance of matrix metalloproteases inhibitors. Cell Mol Biol 2003;49:875-884.
Gueders MM, Foidart JM, Noel A, Cataldo DD. Matrix metalloproteinases (MMPs) and tissue inhibitors of MMPs in the respiratory tract: potential implications in asthma and other lung diseases. Eur J Pharmacol 2006;533:133-144.
Greenlee KJ, Werb Z, Kheradmand F. Matrix metalloproteinases in lung: multiple, multifarious, and multifaceted. Physiol Rev 2007;87:69-98.
Cauwe B, Van den Steen PE, Opdenakker G. The biochemical, biological, and pathological kaleidoscope of cell surface substrates processed by matrix metalloproteinases. Crit Rev Biochem Mol Biol 2007;42:113-185.
McQuibban GA, Gong JH, Tam EM, McCulloch CA, Clark-Lewis I, Overall CM. Inflammation dampened by gelatinase: a cleavage of monocyte chemoattractant protein-3. Science 2000;289:1202-1206.
Van Den Steen PE, Wuyts A, Husson SJ, Proost P, Van Damme J, Opdenakker G. Gelatinase B/MMP-9 and neutrophil collagenase/MMP-8 process the chemokines human GCP-2/CXCL6, ENA-78/CXCL5 and mouse GCP-2/LIX and modulate their physiological activities. Eur J Biochem 2003;270:3739-3749.
Cataldo DD, Tournoy KG, Vermaelen K, Munaut C, Foidart JM, Louis R, Noel A, Pauwels RA. Matrix metalloproteinase-9 deficiency impairs cellular infiltration and bronchial hyperresponsiveness during allergen-induced airway inflammation. Am J Pathol 2002;161:491-498.
Kelly EA, Busse WW, Jarjour NN. Increased matrix metalloproteinase-9 in the airway after allergen challenge. Am J Respir Crit Care Med 2000;162:1157-1161.
Cataldo DD, Bettiol J, Noel A, Bartsch P, Foidart JM, Louis R. Matrix metalloproteinase-9, but not tissue inhibitor of matrix metalloproteinase-1, increases in the sputum from allergic asthmatic patients after allergen challenge. Chest 2002;122:1553-1559.
Cataldo DD, Gueders M, Munaut C, Rocks N, Bartsch P, Foidart JM, Noel A, Louis R. Matrix metalloproteinases and tissue inhibitors of matrix metalloproteinases mRNA transcripts in the bronchial secretions of asthmatics. Lab Invest 2004;84:418-424.
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. Am J Respir Cell Mol Biol 1997;17:583-591.
Prikk K, Maisi P, Pirila E, Reintam MA, Salo T, Sorsa T, Sepper R. Airway obstruction correlates with collagenase-2 (MMP-8) expression and activation in bronchial asthma. Lab Invest 2002;82:1535-1545.
Corry DB, Rishi K, Kanellis J, Kiss A, Song LZ, Xu J, Feng L, Werb Z, Kheradmand F. Decreased allergic lung inflammatory cell egression and increased susceptibility to asphyxiation in MMP2-deficiency. Nat Immunol 2002;3:347-353.
Gueders MM, Balbin M, Rocks N, Foidart JM, Gosset P, Louis R, Shapiro S, Lopez-Otin C, Noel A, Cataldo DD. Matrix metalloproteinase-8 deficiency promotes granulocytic allergen-induced airway inflammation. J Immunol 2005;175:2589-2597.
Kumagai K, Ohno I, Okada S, Ohkawara Y, Suzuki K, Shinya T, Nagase H, Iwata K, Shirato K. Inhibition of matrix metalloproteinases prevents allergen-induced airway inflammation in a murine model of asthma. J Immunol 1999;162:4212-4219.
Gueders MM, Bertholet P, Perin F, Rocks N, Maree R, Botta V, Louis R, Foidart JM, Noel A, Evrard B, et al. A novel formulation of inhaled doxycycline reduces allergen-induced inflammation, hyperresponsiveness and remodeling by matrix metalloproteinases and cytokines modulation in a mouse model of asthma. Biochem Pharmacol 2008;75:514-526.
Mueller MS, Harnasch M, Kolb C, Kusch J, Sadowski T, Sedlacek R. The murine ortholog of matrix metalloproteinase 19: its cloning, gene organization, and expression. Gene 2000;256:101-111.
Pendas AM, Knauper V, Puente XS, Llano E, Mattei MG, Apte S, Murphy G, Lopez-Otin C. Identification and characterization of a novel human matrix metalloproteinase with unique structural characteristics, chromosomal location, and tissue distribution. J Biol Chem 1997;272:4281-4286.
Konttinen YT, Ainola M, Valleala H, Ma J, Ida H, Mandelin J, Kinne RW, Santavirta S, Sorsa T, Lopez-Otin C, et al. Analysis of 16 different matrix metalloproteinases (MMP-1 to MMP-20) in the synovial membrane: different profiles in trauma and rheumatoid arthritis. Ann Rheum Dis 1999;58:691-697.
Sadowski T, Dietrich S, Koschinsky F, Ludwig A, Proksch E, Titz B, Sedlacek R. Matrix metalloproteinase 19 processes the laminin 5 gamma 2 chain and induces epithelial cell migration. Cell Mol Life Sci 2005;62:870-880.
Stracke JO, Hutton M, Stewart M, Pendas AM, Smith B, Lopez-Otin C, Murphy G, Knauper V. Biochemical characterization of the catalytic domain of human matrix metalloproteinase 19. Evidence for a role as a potent basement membrane degrading enzyme. J Biol Chem 2000;275:14809-14816.
Laitinen A, Altraja A, Kämpe M, Linden M, Virtanen I, Laitinen LA. Tenascin is increased in airway basement membrane of asthmatics and decreased by an inhaled steroid. Am J Respir Crit Care Med 1997;156:951-958.
Torrego A, Hew M, Oates T, Sukkar M, Fan Chung K. Expression and activation of TGF-beta isoforms in acute allergen-induced remodelling in asthma. Thorax 2007;62:307-313.
Kariyawasam HH, Aizen M, Barkans J, Robinson DS, Kay AB. Remodeling and airway hyperresponsiveness but not cellular inflammation persists after allergen challenge in asthma. Am J Respir Crit Care Med 2007;175:896-904.
Sadowski T, Dietrich S, Koschinsky F, Sedlacek R. Matrix metalloproteinase 19 regulates insulin-like growth factor-mediated proliferation, migration, and adhesion in human keratinocytes through proteolysis of insulin-like growth factor binding protein-3. Mol Biol Cell 2003;14:4569-4580.
Hartnell A, Heinemann A, Conroy DM, Wait R, Sturm GJ, Caversaccio M, Jose PJ, Williams TJ. Identification of selective basophil chemoattractants in human nasal polyps as insulin-like growth factor-1 and insulin-like growth factor-2. J Immunol 2004;173:6448-6457.
Sedlacek R, Mauch S, Kolb B, Schatzlein C, Eibel H, Peter HH, Schmitt J, Krawinkel U. Matrix metalloproteinase MMP-19 (RASI-1) is expressed on the surface of activated peripheral blood mononuclear cells and is detected as an autoantigen in rheumatoid arthritis. Immunobiology 1998;198:408-423.
Pendas AM, Folgueras AR, Llano E, Caterina J, Frerard F, Rodriguez F, Astudillo A, Noel A, Birkedal-Hansen H, Lopez-Otin C. Dietinduced obesity and reduced skin cancer susceptibility in matrix metalloproteinase 19-deficient mice. Mol Cell Biol 2004;24:5304-5313.
Jost M, Folgueras AR, Frérart F, Pendas AM, Blacher S, Houard X, Berndt S, Munaut C, Cataldo D, Alvarez J, et al. Earlier onset of tumoral angiogenesis in matrix-metalloproteinase-19-deficient mice. Cancer Res 2006;66:5234-5241.
Hantos Z, Daroczy B, Suki B, Nagy S, Fredberg JJ. Input impedance and peripheral inhomogeneity of dog lungs. J Appl Physiol 1992;72:168-178.
Xu D, Chan WL, Leung BP, Hunter D, Schulz K, Carter RW, McInnes IB, Robinson JH, Liew FY. Selective expression and functions of interleukin 18 receptor on T helper (Th) type 1 but not Th2 cells. J Exp Med 1998;188:1485-1492. (Pubitemid 28489585)
Mangan NE, Dasvarma A, McKenzie AN, Fallon PG. T1/ST2 expression on Th2 cells negatively regulates allergic pulmonary inflammation. Eur J Immunol 2007;37:1302-1312.
Chan C, Burgess JK, Ratoff JC, O'Connor BJ, Greenough A, Lee TH, Hirst SJ. Extracellular matrix regulates enhanced eotaxin expression in asthmatic airway smooth muscle cells. Am J Respir Crit Care Med 2006;174:379-385.
Djonov V, Hogger K, Sedlacek R, Laissue J, Draeger A. MMP-19: cellular localization of a novel metalloproteinase within normal breast tissue and mammary gland tumours. J Pathol 2001;195:147-155.
Jose PJ, Griffiths-Johnson DA, Collins PD, Walsh DT, Moqbel R, Totty NF, Truong O, Hsuan JJ, Williams TJ. Eotaxin: a potent eosinophil chemoattractant cytokine detected in a guinea pig model of allergic airways inflammation. J Exp Med 1994;179:881-887. (Pubitemid 24065646)
Kanda A, Adachi T, Kayaba H, Yamada Y, Ueki S, Yamaguchi K, Hamada K, Fujita M, Chihara J. Red blood cells regulate eosinophil chemotaxis by scavenging RANTES secreted from endothelial cells. Clin Exp Allergy 2004;34:1621-1626. (Pubitemid 39389341)
Locati M, Deuschle U, Massardi ML, Martinez FO, Sironi M, Sozzani S, Bartfai T, Mantovani A. Analysis of the gene expression profile activated by the CC chemokine ligand 5/RANTES and by lipopolysaccharide in human monocytes. J Immunol 2002;168:3557-3562. (Pubitemid 34250425)
Morse B, Sypek JP, Donaldson DD, Haley KJ, Lilly CM. Effects of IL-13 on airway responses in the guinea pig. Am J Physiol Lung Cell Mol Physiol 2002;282:L44-L49. (Pubitemid 34654179)
Scmhmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, Zurawski G, Moshrefi M, Qin J, Li X, et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type-2 associated cytokines. Immunity 2005;23:479-490.
Peng Q, Matsuda T, Hirst SJ. Signaling pathways regulating interleukin- 13-stimulated chemokine release from airway smooth muscle. Am J Respir Crit Care Med 2004;169:596-603.
Karjalainen EM, Lindqvist A, Laitinen LA, Kava T, Altraja A, Halme M, Laitinen A. Airway inflammation and basement membrane tenascin in newly diagnosed atopic and nonatopic asthma. Respir Med 2003;97:1045-1051.
Holloway JW, Koppelman GH. Identifying novel genes contributing to asthma pathogenesis. Curr Opin Allergy Clin Immunol 2007;7:69-74.
Nakahara H, Gabazza EC, Fujimoto H, Nishii Y, D'Alessandro-Gabazza CN, Bruno NE, Takagi T, Hayashi T, Maruyama J, Maruyama K, et al. Deficiency of tenascin C attenuates allergen-induced bronchial asthma in the mouse. Eur J Immunol 2006;36:3334-3345.
Midwood KS, Mao Y, Hsia HC, Valenick LV, Schwarzbauer JE. Modulation of cell-fibronectin matrix interactions during lung tissue repair. J Investig Dermatol Symp Proc 2006;11:73-78.
Nishio T, Kawaguchi S, Yamamoto M, Kawasaki T, Hase T. Tenascin-C regulates proliferation and migration of cultured astrocytes in a scratch wound assay. Neuroscience 2005;132:87-102.
Taooka Y, Chen J, Yednock T, Sheppard D. The integrin alpha9beta1 mediates adhesion to activated endothelial cells and transendothelial neutrophil migration trough interaction with vascular cell adhesion molecule-1. J Cell Biol 1999;145:413-420.
Flood-Page P, Menzies-Gow A, Phipps S, Ying S, Wangoo A, Ludwig MS, Barnes N, Robinson D, Barry Kay A. Anti-IL-5 treatment reduces deposition of ECM proteins in the bronchial subepithelial basement membrane of mild atopic asthmatics. J Clin Invest 2003;112:1029-1036.
Härkönen E, Virtanen I, Linnala A, Laitinen LL, Kinnula VL. Modulation of fibronectin and tenascin production in human bronchial epithelial cells by inflammatory cytokines in vitro. Am J Respir Cell Mol Biol 1995;13:109-115.