Loss of caveolin-1 from bronchial epithelial cells and monocytes in human subjects with asthma
Background Caveolin‐1 has emerged as a critical regulator of signaling pathways involved in lung fibrosis and inflammation. Methods Therefore, we investigated whether caveolin‐1 is deficient in asthmatic patients and in a murine model of asthma. Results Immunohistochemical analyses of endobronchial...
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| Published in | Allergy (Copenhagen) Vol. 67; no. 12; pp. 1601 - 1604 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Oxford
Blackwell Publishing Ltd
01.12.2012
Blackwell |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Background
Caveolin‐1 has emerged as a critical regulator of signaling pathways involved in lung fibrosis and inflammation.
Methods
Therefore, we investigated whether caveolin‐1 is deficient in asthmatic patients and in a murine model of asthma.
Results
Immunohistochemical analyses of endobronchial biopsies showed a remarkable loss of caveolin‐1 in the lungs of asthmatic patients compared with controls. This loss was most evident in bronchial epithelial cells and associated with an increase in the expression of extracellular matrix proteins: collagen I, tenascin, and periostin. Cultured primary bronchial epithelial cells of asthmatics had lower caveolin‐1 expression compared with control cells. In addition, caveolin‐1 expression was significantly decreased in peripheral blood monocytes from asthma patients. The loss of caveolin‐1 was also observed in a mouse model for asthma (mice sensitized and challenged with aspergillus fumigatus).
Conclusions
To our knowledge, this is the first demonstration that the regulatory protein caveolin‐1 is reduced in patients with asthma. |
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| AbstractList | Caveolin-1 has emerged as a critical regulator of signaling pathways involved in lung fibrosis and inflammation.BACKGROUNDCaveolin-1 has emerged as a critical regulator of signaling pathways involved in lung fibrosis and inflammation.Therefore, we investigated whether caveolin-1 is deficient in asthmatic patients and in a murine model of asthma.METHODSTherefore, we investigated whether caveolin-1 is deficient in asthmatic patients and in a murine model of asthma.Immunohistochemical analyses of endobronchial biopsies showed a remarkable loss of caveolin-1 in the lungs of asthmatic patients compared with controls. This loss was most evident in bronchial epithelial cells and associated with an increase in the expression of extracellular matrix proteins: collagen I, tenascin, and periostin. Cultured primary bronchial epithelial cells of asthmatics had lower caveolin-1 expression compared with control cells. In addition, caveolin-1 expression was significantly decreased in peripheral blood monocytes from asthma patients. The loss of caveolin-1 was also observed in a mouse model for asthma (mice sensitized and challenged with aspergillus fumigatus).RESULTSImmunohistochemical analyses of endobronchial biopsies showed a remarkable loss of caveolin-1 in the lungs of asthmatic patients compared with controls. This loss was most evident in bronchial epithelial cells and associated with an increase in the expression of extracellular matrix proteins: collagen I, tenascin, and periostin. Cultured primary bronchial epithelial cells of asthmatics had lower caveolin-1 expression compared with control cells. In addition, caveolin-1 expression was significantly decreased in peripheral blood monocytes from asthma patients. The loss of caveolin-1 was also observed in a mouse model for asthma (mice sensitized and challenged with aspergillus fumigatus).To our knowledge, this is the first demonstration that the regulatory protein caveolin-1 is reduced in patients with asthma.CONCLUSIONSTo our knowledge, this is the first demonstration that the regulatory protein caveolin-1 is reduced in patients with asthma. Caveolin-1 has emerged as a critical regulator of signaling pathways involved in lung fibrosis and inflammation. Therefore, we investigated whether caveolin-1 is deficient in asthmatic patients and in a murine model of asthma. Immunohistochemical analyses of endobronchial biopsies showed a remarkable loss of caveolin-1 in the lungs of asthmatic patients compared with controls. This loss was most evident in bronchial epithelial cells and associated with an increase in the expression of extracellular matrix proteins: collagen I, tenascin, and periostin. Cultured primary bronchial epithelial cells of asthmatics had lower caveolin-1 expression compared with control cells. In addition, caveolin-1 expression was significantly decreased in peripheral blood monocytes from asthma patients. The loss of caveolin-1 was also observed in a mouse model for asthma (mice sensitized and challenged with aspergillus fumigatus). To our knowledge, this is the first demonstration that the regulatory protein caveolin-1 is reduced in patients with asthma. Caveolin-1 has emerged as a critical regulator of signaling pathways involved in lung fibrosis and inflammation. Therefore, we investigated whether caveolin-1 is deficient in asthmatic patients and in a murine model of asthma. Immunohistochemical analyses of endobronchial biopsies showed a remarkable loss of caveolin-1 in the lungs of asthmatic patients compared to controls. This loss was most evident in bronchial epithelial cells, and associated with an increase in the expression of extracellular matrix proteins collagen I, tenascin, and periostin. Cultured primary bronchial epithelial cells of asthmatics had lower caveolin-1 expression compared to control cells. In addition, caveolin-1 expression was significantly decreased in peripheral blood monocytes from asthma patients. The loss of caveolin-1 was also observed in a mouse model for asthma (mice sensitized and challenged with aspergillus fumigatus). To our knowledge, this is the first demonstration that the regulatory protein caveolin-1 is reduced in patients with asthma. Background:Caveolin-1 has emerged as a critical regulator of signaling pathways involved in lung fibrosis and inflammation. Methods: Therefore, we investigated whether caveolin-1 is deficient in asthmatic patients and in a murine model of asthma. Results: Immunohistochemical analyses of endobronchial biopsies showed a remarkable loss of caveolin-1 in the lungs of asthmatic patients compared with controls. This loss was most evident in bronchial epithelial cells and associated with an increase in the expression of extracellular matrix proteins: collagen I, tenascin, and periostin. Cultured primary bronchial epithelial cells of asthmatics had lower caveolin-1 expression compared with control cells. In addition, caveolin-1 expression was significantly decreased in peripheral blood monocytes from asthma patients. The loss of caveolin-1 was also observed in a mouse model for asthma (mice sensitized and challenged with aspergillus fumigatus). Conclusions: To our knowledge, this is the first demonstration that the regulatory protein caveolin-1 is reduced in patients with asthma. [PUBLICATION ABSTRACT] Caveolin-1 has emerged as a critical regulator of signaling pathways involved in lung fibrosis and inflammation. Therefore, we investigated whether caveolin-1 is deficient in asthmatic patients and in a murine model of asthma. Immunohistochemical analyses of endobronchial biopsies showed a remarkable loss of caveolin-1 in the lungs of asthmatic patients compared with controls. This loss was most evident in bronchial epithelial cells and associated with an increase in the expression of extracellular matrix proteins: collagen I, tenascin, and periostin. Cultured primary bronchial epithelial cells of asthmatics had lower caveolin-1 expression compared with control cells. In addition, caveolin-1 expression was significantly decreased in peripheral blood monocytes from asthma patients. The loss of caveolin-1 was also observed in a mouse model for asthma (mice sensitized and challenged with aspergillus fumigatus). To our knowledge, this is the first demonstration that the regulatory protein caveolin-1 is reduced in patients with asthma. Background Caveolin‐1 has emerged as a critical regulator of signaling pathways involved in lung fibrosis and inflammation. Methods Therefore, we investigated whether caveolin‐1 is deficient in asthmatic patients and in a murine model of asthma. Results Immunohistochemical analyses of endobronchial biopsies showed a remarkable loss of caveolin‐1 in the lungs of asthmatic patients compared with controls. This loss was most evident in bronchial epithelial cells and associated with an increase in the expression of extracellular matrix proteins: collagen I, tenascin, and periostin. Cultured primary bronchial epithelial cells of asthmatics had lower caveolin‐1 expression compared with control cells. In addition, caveolin‐1 expression was significantly decreased in peripheral blood monocytes from asthma patients. The loss of caveolin‐1 was also observed in a mouse model for asthma (mice sensitized and challenged with aspergillus fumigatus). Conclusions To our knowledge, this is the first demonstration that the regulatory protein caveolin‐1 is reduced in patients with asthma. |
| Author | Bains, S. N. Hoffman, S. Chu, H. W. Joseph, K. Martin, R. Riemer, E. C. Tourkina, E. Atkinson, C. Tholanikunnel, B. |
| AuthorAffiliation | c Department of Microbiology & Immunology, Medical University of South Carolina, SC d Department of Biochemistry, Medical University of South Carolina b Division of Rheumatology & Immunology, Medical University of South Carolina, SC e Department of Medicine, National Jewish Health and the University of Colorado Health Sciences Center, CO f Department of Pathology & Laboratory Medicine, Medical University of South Carolina, SC a Division of Pulmonary, Allergy & Critical Care Medicine, Medical University of South Carolina, SC |
| AuthorAffiliation_xml | – name: c Department of Microbiology & Immunology, Medical University of South Carolina, SC – name: d Department of Biochemistry, Medical University of South Carolina – name: f Department of Pathology & Laboratory Medicine, Medical University of South Carolina, SC – name: b Division of Rheumatology & Immunology, Medical University of South Carolina, SC – name: e Department of Medicine, National Jewish Health and the University of Colorado Health Sciences Center, CO – name: a Division of Pulmonary, Allergy & Critical Care Medicine, Medical University of South Carolina, SC |
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| Keywords | Human Lung disease Allergy Immunopathology Monocyte Respiratory disease Dermatology Bronchus Epithelium Respiratory system Asthma Respiratory tract Caveolin 1 Immunology Bronchus disease Epithelial cell Obstructive pulmonary disease Allergen |
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| References_xml | – reference: Li L, Fan D, Wang C, Wang JY, Cui XB, Wu D et al. Angiotensin II increases periostin expression via Ras/p38 MAPK/CREB and ERK1/2/TGF-beta1 pathways in cardiac fibroblasts. Cardiovasc Res 2011;91:80-89. – reference: Chen CM, Wu MY, Chou HC, Lang YD, Wang LF. Downregulation of caveolin-1 in a murine model of acute allergic airway disease. Pediatr Neonatol 2011;52:5-10. – reference: Couet J, Li S, Okamoto T, Ikezu T, Lisanti MP. Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J Biol Chem 1997;272:6525-6533. – reference: Seymour BW, Schelegle ES, Pinkerton KE, Friebertshauser KE, Peake JL, Kurup VP et al. Second-hand smoke increases bronchial hyperreactivity and eosinophilia in a murine model of allergic aspergillosis. Clin Dev Immunol 2003;10:35-42. – reference: Bulek K, Swaidani S, Aronica M, Li X. Epithelium: the interplay between innate and Th2 immunity. Immunol Cell Biol 2010;88:257-268. – reference: Le Saux CJ, Teeters K, Miyasato SK, Hoffmann PR, Bollt O, Douet V et al. Down-regulation of caveolin-1, an inhibitor of transforming growth factor-beta signaling, in acute allergen-induced airway remodeling. J Biol Chem 2008;283:5760-5768. – reference: Mulligan RM, Atkinson C, Vertegel AA, Reukov V, Schlosser RJ. Cigarette smoke extract stimulates interleukin-8 production in human airway epithelium and is attenuated by superoxide dismutase in vitro. Am J Rhinol Allergy 2009;23:e1-e4. – reference: Sidhu SS, Yuan S, Innes AL, Kerr S, Woodruff PG, Hou L et al. Roles of epithelial cell-derived periostin in TGF-beta activation, collagen production, and collagen gel elasticity in asthma. Proc Natl Acad Sci USA 2010;107:14170-14175. – reference: Zhang S, Smartt H, Holgate ST, Roche WR. Growth factors secreted by bronchial epithelial cells control myofibroblast proliferation: an in vitro co-culture model of airway remodeling in asthma. Lab Invest 1999;79:395-405. – reference: Tourkina E, Richard M, Oates J, Hofbauer A, Bonner M, Gooz P et al. Caveolin-1 regulates leucocyte behaviour in fibrotic lung disease. Ann Rheum Dis 2010;69:1220-1226. – reference: Tourkina E, Bonner M, Oates J, Hofbauer A, Richard M, Znoyko S et al. Altered monocyte and fibrocyte phenotype and function in scleroderma interstitial lung disease: reversal by caveolin-1 scaffolding domain peptide. Fibrogenesis Tissue Repair 2011;4:15. – reference: Wang XM, Zhang Y, Kim HP, Zhou Z, Feghali-Bostwick CA, Liu F et al. Caveolin-1: a critical regulator of lung fibrosis in idiopathic pulmonary fibrosis. J Exp Med 2006;203:2895-2906. – reference: Tourkina E, Gooz P, Pannu J, Bonner M, Scholz D, Hacker S et al. Opposing effects of protein kinase C alpha and protein kinase Cepsilon on collagen expression by human lung fibroblasts are mediated via MEK/ERK and caveolin-1 signaling. J Biol Chem 2005;280:13879-13887. – reference: Tourkina E, Richard M, Gooz P, Bonner M, Pannu J, Harley R et al. Antifibrotic properties of caveolin-1 scaffolding domain in vitro and in vivo. Am J Physiol Lung Cell Mol Physiol 2008;294:L843-L861. – reference: Puddicombe SM, Davies DE. The role of MAP kinases in intracellular signal transduction in bronchial epithelium. Clin Exp Allergy 2000;30:7-11. – volume: 107 start-page: 14170 year: 2010 end-page: 14175 article-title: Roles of epithelial cell‐derived periostin in TGF‐beta activation, collagen production, and collagen gel elasticity in asthma publication-title: Proc Natl Acad Sci USA – volume: 10 start-page: 35 year: 2003 end-page: 42 article-title: Second‐hand smoke increases bronchial hyperreactivity and eosinophilia in a murine model of allergic aspergillosis publication-title: Clin Dev Immunol – volume: 23 start-page: e1 year: 2009 end-page: e4 article-title: Cigarette smoke extract stimulates interleukin‐8 production in human airway epithelium and is attenuated by superoxide dismutase in vitro publication-title: Am J Rhinol Allergy – volume: 30 start-page: 7 year: 2000 end-page: 11 article-title: The role of MAP kinases in intracellular signal transduction in bronchial epithelium publication-title: Clin Exp Allergy – volume: 283 start-page: 5760 year: 2008 end-page: 5768 article-title: Down‐regulation of caveolin‐1, an inhibitor of transforming growth factor‐beta signaling, in acute allergen‐induced airway remodeling publication-title: J Biol Chem – volume: 294 start-page: L843 year: 2008 end-page: L861 article-title: Antifibrotic properties of caveolin‐1 scaffolding domain in vitro and in vivo publication-title: Am J Physiol Lung Cell Mol Physiol – volume: 79 start-page: 395 year: 1999 end-page: 405 article-title: Growth factors secreted by bronchial epithelial cells control myofibroblast proliferation: an in vitro co‐culture model of airway remodeling in asthma publication-title: Lab Invest – volume: 203 start-page: 2895 year: 2006 end-page: 2906 article-title: Caveolin‐1: a critical regulator of lung fibrosis in idiopathic pulmonary fibrosis publication-title: J Exp Med – volume: 52 start-page: 5 year: 2011 end-page: 10 article-title: Downregulation of caveolin‐1 in a murine model of acute allergic airway disease publication-title: Pediatr Neonatol – volume: 91 start-page: 80 year: 2011 end-page: 89 article-title: Angiotensin II increases periostin expression via Ras/p38 MAPK/CREB and ERK1/2/TGF‐beta1 pathways in cardiac fibroblasts publication-title: Cardiovasc Res – volume: 4 start-page: 15 year: 2011 article-title: Altered monocyte and fibrocyte phenotype and function in scleroderma interstitial lung disease: reversal by caveolin‐1 scaffolding domain peptide publication-title: Fibrogenesis Tissue Repair – volume: 280 start-page: 13879 year: 2005 end-page: 13887 article-title: Opposing effects of protein kinase C alpha and protein kinase Cepsilon on collagen expression by human lung fibroblasts are mediated via MEK/ERK and caveolin‐1 signaling publication-title: J Biol Chem – volume: 272 start-page: 6525 year: 1997 end-page: 6533 article-title: Identification of peptide and protein ligands for the caveolin‐scaffolding domain. Implications for the interaction of caveolin with caveolae‐associated proteins publication-title: J Biol Chem – volume: 69 start-page: 1220 year: 2010 end-page: 1226 article-title: Caveolin‐1 regulates leucocyte behaviour in fibrotic lung disease publication-title: Ann Rheum Dis – volume: 88 start-page: 257 year: 2010 end-page: 268 article-title: Epithelium: the interplay between innate and Th2 immunity publication-title: Immunol Cell Biol – ident: e_1_2_9_15_1 doi: 10.1046/j.1365-2222.2000.00709.x – ident: e_1_2_9_6_1 doi: 10.1136/ard.2009.117580 – volume: 79 start-page: 395 year: 1999 ident: e_1_2_9_12_1 article-title: Growth factors secreted by bronchial epithelial cells control myofibroblast proliferation: an in vitro co‐culture model of airway remodeling in asthma publication-title: Lab Invest – ident: e_1_2_9_7_1 doi: 10.1152/ajplung.00295.2007 – ident: e_1_2_9_16_1 doi: 10.1093/cvr/cvr067 – ident: e_1_2_9_13_1 doi: 10.2500/ajra.2009.23.3400 – ident: e_1_2_9_4_1 doi: 10.1084/jem.20061536 – ident: e_1_2_9_5_1 doi: 10.1074/jbc.M701572200 – ident: e_1_2_9_9_1 doi: 10.1080/10446670310001598483 – ident: e_1_2_9_8_1 doi: 10.1016/j.pedneo.2010.12.006 – ident: e_1_2_9_3_1 doi: 10.1074/jbc.M412551200 – ident: e_1_2_9_2_1 doi: 10.1074/jbc.272.10.6525 – ident: e_1_2_9_10_1 doi: 10.1186/1755-1536-4-15 – ident: e_1_2_9_11_1 doi: 10.1038/icb.2009.113 – ident: e_1_2_9_14_1 doi: 10.1073/pnas.1009426107 – reference: 20065993 - Immunol Cell Biol. 2010 Mar-Apr;88(3):257-68 – reference: 10211992 - Lab Invest. 1999 Apr;79(4):395-405 – reference: 21722364 - Fibrogenesis Tissue Repair. 2011 Jul 01;4(1):15 – reference: 15691837 - J Biol Chem. 2005 Apr 8;280(14):13879-87 – reference: 10606925 - Clin Exp Allergy. 2000 Jan;30(1):7-11 – reference: 14575156 - Clin Dev Immunol. 2003 Mar;10(1):35-42 – reference: 21385650 - Pediatr Neonatol. 2011 Feb;52(1):5-10 – reference: 21367774 - Cardiovasc Res. 2011 Jul 1;91(1):80-9 – reference: 17178917 - J Exp Med. 2006 Dec 25;203(13):2895-906 – reference: 18203815 - Am J Physiol Lung Cell Mol Physiol. 2008 May;294(5):L843-61 – reference: 20410070 - Ann Rheum Dis. 2010 Jun;69(6):1220-6 – reference: 20660732 - Proc Natl Acad Sci U S A. 2010 Aug 10;107(32):14170-5 – reference: 18056268 - J Biol Chem. 2008 Feb 29;283(9):5760-8 – reference: 9045678 - J Biol Chem. 1997 Mar 7;272(10):6525-33 – reference: 19769800 - Am J Rhinol Allergy. 2009 Nov-Dec;23(6):e1-4 |
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| Snippet | Background
Caveolin‐1 has emerged as a critical regulator of signaling pathways involved in lung fibrosis and inflammation.
Methods
Therefore, we investigated... Caveolin-1 has emerged as a critical regulator of signaling pathways involved in lung fibrosis and inflammation. Therefore, we investigated whether caveolin-1... Background:Caveolin-1 has emerged as a critical regulator of signaling pathways involved in lung fibrosis and inflammation. Methods: Therefore, we investigated... Caveolin-1 has emerged as a critical regulator of signaling pathways involved in lung fibrosis and inflammation.BACKGROUNDCaveolin-1 has emerged as a critical... Caveolin-1 has emerged as a critical regulator of signaling pathways involved in lung fibrosis and inflammation. Therefore, we investigated whether caveolin-1... |
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| SubjectTerms | allergen Animal models Animals Aspergillus fumigatus Asthma Asthma - metabolism Biological and medical sciences Biopsy Bronchi - metabolism Caveolin 1 - deficiency Caveolin 1 - metabolism caveolin-1 Cellular biology Chronic obstructive pulmonary disease, asthma Collagen (type I) Dermatology Disease Models, Animal Epithelial cells Epithelial Cells - metabolism epithelium Extracellular matrix Extracellular Matrix Proteins - metabolism Female Fibrosis Fundamental and applied biological sciences. Psychology Fundamental immunology Gene expression Humans Immunohistochemistry Inflammation Lung Lung - metabolism Lung - pathology Medical sciences Mice Monocytes Monocytes - metabolism Peripheral blood Pneumology Proteins regulatory proteins Sarcoidosis. Granulomatous diseases of unproved etiology. Connective tissue diseases. Elastic tissue diseases. Vasculitis Signal Transduction Tenascin |
| Title | Loss of caveolin-1 from bronchial epithelial cells and monocytes in human subjects with asthma |
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