Skip to main content
Top
Published in: Respiratory Research 1/2008

Open Access 01-12-2008 | Research

Changes in elastin, elastin binding protein and versican in alveoli in chronic obstructive pulmonary disease

Authors: Mervyn J Merrilees, Pamela ST Ching, Brent Beaumont, Aleksander Hinek, Thomas N Wight, Peter N Black

Published in: Respiratory Research | Issue 1/2008

Login to get access

Abstract

Background

COPD is characterised by loss of alveolar elastic fibers and by lack of effective repair. Elastic fibers are assembled at cell surfaces by elastin binding protein (EBP), a molecular chaperone whose function can be reversibility inhibited by chondroitin sulphate of matrix proteoglycans such as versican. This study aimed to determine if alveoli of patients with mild to moderate COPD contained increased amounts of versican and a corresponding decrease in EBP, and if these changes were correlated with decreases in elastin and FEV1.

Methods

Lung samples were obtained from 26 control (FEV1 ≥ 80% predicted, FEV1/VC >0.7) and 17 COPD patients (FEV1 ≥ 40% – <80% predicted, FEV1/VC ≤ 0.7) who had undergone a lobectomy for bronchial carcinoma. Samples were processed for histological and immuno-staining. Volume fractions (V v) of elastin in alveolar walls and alveolar rims were determined by point counting, and versican and EBP assessed by grading of staining intensities.

Results

Elastin Vv was positively correlated with FEV1 for both the alveolar walls (r = 0.66, p < 0.001) and rims (r = 0.41, p < 0.01). Versican was negatively correlated with FEV1 in both regions (r = 0.30 and 0.32 respectively, p < 0.05), with the highest staining intensities found in patients with the lowest values for FEV1. Conversely, staining intensities for EBP in alveolar walls and rims and were positively correlated with FEV1 (r = 0.43 and 0.46, p < 0.01).

Conclusion

Patients with mild to moderate COPD show progressively increased immuno-staining for versican and correspondingly decreased immuno-staining for EBP, with decreasing values of FEV1. These findings may explain the lack of repair of elastic fibers in the lungs of patients with moderate COPD. Removal of versican may offer a strategy for effective repair.
Literature
1.
go back to reference Chrzanowski P, Keller S, Cerreta J, Mandl I, Turino GM: Elastin content of normal and emphysematous lung parenchyma. Am J Med 1980, 69:351–359.CrossRefPubMed Chrzanowski P, Keller S, Cerreta J, Mandl I, Turino GM: Elastin content of normal and emphysematous lung parenchyma. Am J Med 1980, 69:351–359.CrossRefPubMed
2.
go back to reference Pecora LJ, Manne WR, Baum GL, Feldman DP, Recavarren J: Biochemical study of ground substance in normal and emphysematous lungs. Am Rev Respir Dis 1967, 95:623.PubMed Pecora LJ, Manne WR, Baum GL, Feldman DP, Recavarren J: Biochemical study of ground substance in normal and emphysematous lungs. Am Rev Respir Dis 1967, 95:623.PubMed
3.
go back to reference Cardoso WV, Sekhon HS, Hyde DM, Thurlbeck WM: Collagen and elastin in human pulmonary emphysema. Am Rev Respir Dis 1993, 147:975–981.CrossRefPubMed Cardoso WV, Sekhon HS, Hyde DM, Thurlbeck WM: Collagen and elastin in human pulmonary emphysema. Am Rev Respir Dis 1993, 147:975–981.CrossRefPubMed
4.
go back to reference Black PN, Ching PST, Beaumont B, Ranasinghe S, Taylor G, Merrilees MJ: Changes in elastic fibres in the small airways and alveoli in COPD. European Respiratory Journal published on-line 23rd January 2008. 10.1183/09031936.00017207 Black PN, Ching PST, Beaumont B, Ranasinghe S, Taylor G, Merrilees MJ: Changes in elastic fibres in the small airways and alveoli in COPD. European Respiratory Journal published on-line 23rd January 2008. 10.1183/09031936.00017207
5.
go back to reference Ohnishi K, Takagi M, Kurokawa Y, Satomi S, Konttinen YT: Matrix metalloproteinase-mediated extracellular matrix protein degradation in human pulmonary emphysema. Lab Invest 1998,78(9):1077–1087.PubMed Ohnishi K, Takagi M, Kurokawa Y, Satomi S, Konttinen YT: Matrix metalloproteinase-mediated extracellular matrix protein degradation in human pulmonary emphysema. Lab Invest 1998,78(9):1077–1087.PubMed
6.
go back to reference Segura-Valdez L, Pardo A, Gaxiola M, Uhal BD, Becerril C, Selman M: Upregulation of gelatinases A and B, collagenases 1 and 2, and increased parenchymal cell death in COPD. Chest 2000, 117:684–694.CrossRefPubMed Segura-Valdez L, Pardo A, Gaxiola M, Uhal BD, Becerril C, Selman M: Upregulation of gelatinases A and B, collagenases 1 and 2, and increased parenchymal cell death in COPD. Chest 2000, 117:684–694.CrossRefPubMed
7.
go back to reference Finlay GA, O'Driscoll LR, Russell KJ, D'Arcy EM, Masterson JB, FitzGerald MX, O'Connor CM: Matrix metalloproteinase expression and production by alveolar macrophages in emphysema. Am J Respir Crit Care Med 1997,156(1):240–247.CrossRefPubMed Finlay GA, O'Driscoll LR, Russell KJ, D'Arcy EM, Masterson JB, FitzGerald MX, O'Connor CM: Matrix metalloproteinase expression and production by alveolar macrophages in emphysema. Am J Respir Crit Care Med 1997,156(1):240–247.CrossRefPubMed
8.
go back to reference Cataldo D, Munaut C, Noel A, Frankenne F, Bartsch P, Foidart JM, Louis R: MMP-2- and MMP-9-linked gelatinolytic activity in the sputum from patients with asthma and chronic obstructive pulmonary disease. Int Arch Allergy Immunol 2000,123(3):259–267.CrossRefPubMed Cataldo D, Munaut C, Noel A, Frankenne F, Bartsch P, Foidart JM, Louis R: MMP-2- and MMP-9-linked gelatinolytic activity in the sputum from patients with asthma and chronic obstructive pulmonary disease. Int Arch Allergy Immunol 2000,123(3):259–267.CrossRefPubMed
9.
go back to reference Beeh KM, Beier J, Kornmann O, Buhl R: Sputum matrix metalloproteinase-9, tissue inhibitor of metalloprotinease-1, and their molar ratio in patients with chronic obstructive pulmonary disease, idiopathic pulmonary fibrosis and healthy subjects. Respir Med 2003, 97:634–639.CrossRefPubMed Beeh KM, Beier J, Kornmann O, Buhl R: Sputum matrix metalloproteinase-9, tissue inhibitor of metalloprotinease-1, and their molar ratio in patients with chronic obstructive pulmonary disease, idiopathic pulmonary fibrosis and healthy subjects. Respir Med 2003, 97:634–639.CrossRefPubMed
10.
go back to reference Snider GL, Lucey EC, Stone PJ: State of the art: Animal models of emphysema. Am Rev Resp Dis 1986, 133:149–169.CrossRefPubMed Snider GL, Lucey EC, Stone PJ: State of the art: Animal models of emphysema. Am Rev Resp Dis 1986, 133:149–169.CrossRefPubMed
11.
go back to reference Snider GL: Emphysema; the first two centuries – and beyond. A historical overview, with suggestions for future research; Part 2. Am Rev Resp Dis 1992, 146:1615–1622.CrossRefPubMed Snider GL: Emphysema; the first two centuries – and beyond. A historical overview, with suggestions for future research; Part 2. Am Rev Resp Dis 1992, 146:1615–1622.CrossRefPubMed
12.
go back to reference Chambers RC, Laurent GJ: The lung. In Extracellular Matrix, Tissue Function. Volume 1. Edited by: Comper WD. The Netherlands, Harwood Academic Publishers GmbH; 1996:378–409. Chambers RC, Laurent GJ: The lung. In Extracellular Matrix, Tissue Function. Volume 1. Edited by: Comper WD. The Netherlands, Harwood Academic Publishers GmbH; 1996:378–409.
13.
go back to reference Hinek A, Pshezhetsky AV, Itzstein MV, Starcher B: Lysosomal sialidase (neuraminidase 1) is targeted to cell surface in the multiprotein complex that facilitates elastic fiber assembly. J Biol Chem 2006, 281:3698–3710.CrossRefPubMed Hinek A, Pshezhetsky AV, Itzstein MV, Starcher B: Lysosomal sialidase (neuraminidase 1) is targeted to cell surface in the multiprotein complex that facilitates elastic fiber assembly. J Biol Chem 2006, 281:3698–3710.CrossRefPubMed
14.
go back to reference Hinek A, Mecham RP, Keeley F, Rabinovitch M: Impaired elastin fiber assembly related to reduced 67-kD elastin-binding protein in fetal lamb ductus arteriosus and in cultured aortic smooth muscle cells treated with chondroitin sulfate. J Clin Invest 1991, 88:2083–2094.CrossRefPubMedPubMedCentral Hinek A, Mecham RP, Keeley F, Rabinovitch M: Impaired elastin fiber assembly related to reduced 67-kD elastin-binding protein in fetal lamb ductus arteriosus and in cultured aortic smooth muscle cells treated with chondroitin sulfate. J Clin Invest 1991, 88:2083–2094.CrossRefPubMedPubMedCentral
15.
go back to reference Hinek A, Boyle J, Rabinovitch M: Vascular smooth muscle cells detachment from elastin and migration through elastic laminae is promoted by chondroitin sulfate-induced "shedding" of the 67-kD cell surface elastin binding protein. Exp Cell Res 1992, 203:344–353.CrossRefPubMed Hinek A, Boyle J, Rabinovitch M: Vascular smooth muscle cells detachment from elastin and migration through elastic laminae is promoted by chondroitin sulfate-induced "shedding" of the 67-kD cell surface elastin binding protein. Exp Cell Res 1992, 203:344–353.CrossRefPubMed
16.
go back to reference Merrilees MJ, Hankin EJ, Black JL, Beaumont B: Matrix proteoglycans and remodelling of interstitial lung tissue in lymphangioleiomyomatosis. The Journal of Pathology 2004, 203:653–60.CrossRefPubMed Merrilees MJ, Hankin EJ, Black JL, Beaumont B: Matrix proteoglycans and remodelling of interstitial lung tissue in lymphangioleiomyomatosis. The Journal of Pathology 2004, 203:653–60.CrossRefPubMed
17.
go back to reference Hinek A, Rabinovitch M, Keeley F, Callahan J: The 67 elastin/laminin-binding protein is related to a alternatively spliced b-Galactosidase. J Clin Invest 1993, 91:1198–1205.CrossRefPubMedPubMedCentral Hinek A, Rabinovitch M, Keeley F, Callahan J: The 67 elastin/laminin-binding protein is related to a alternatively spliced b-Galactosidase. J Clin Invest 1993, 91:1198–1205.CrossRefPubMedPubMedCentral
18.
go back to reference Huang R, Merrilees M, Braun K, Beaumont B, Lemire J, Clowes AW, Hinek A, Wight T: Inhibition of versican synthesis by antisense alters smooth muscle cell phenotype and induces elastic fiber formation in vitro and in neointima after vessel injury. Circulation Research 2006, 98:370–377.CrossRefPubMed Huang R, Merrilees M, Braun K, Beaumont B, Lemire J, Clowes AW, Hinek A, Wight T: Inhibition of versican synthesis by antisense alters smooth muscle cell phenotype and induces elastic fiber formation in vitro and in neointima after vessel injury. Circulation Research 2006, 98:370–377.CrossRefPubMed
19.
go back to reference Hinek A, Braun KR, Liu K, Wang Y, Wight T: Retrovirally mediated overexpression of versican V3 reverses impaired elastogenesis and heightened proliferation exhibited by fibroblasts from Costello syndrome and Hurler disease patients. Am J Pathol 2004, 164:119–131.CrossRefPubMedPubMedCentral Hinek A, Braun KR, Liu K, Wang Y, Wight T: Retrovirally mediated overexpression of versican V3 reverses impaired elastogenesis and heightened proliferation exhibited by fibroblasts from Costello syndrome and Hurler disease patients. Am J Pathol 2004, 164:119–131.CrossRefPubMedPubMedCentral
20.
go back to reference Merrilees MJ, Tiang KM, Scott L: Changes in collagen fibril diameters across artery walls including a correlation with glycosaminoglycan content. Conn Tiss Res 1987, 16:237–257.CrossRef Merrilees MJ, Tiang KM, Scott L: Changes in collagen fibril diameters across artery walls including a correlation with glycosaminoglycan content. Conn Tiss Res 1987, 16:237–257.CrossRef
21.
go back to reference Merrilees MJ, Beaumont B, Scott L: Comparison of deposits of versican, biglycan and decorin in saphenous vein and internal thoracic, radial and coronary arteries: correlation to patency. Coronary Artery Disease 2001, 12:7–16.CrossRefPubMed Merrilees MJ, Beaumont B, Scott L: Comparison of deposits of versican, biglycan and decorin in saphenous vein and internal thoracic, radial and coronary arteries: correlation to patency. Coronary Artery Disease 2001, 12:7–16.CrossRefPubMed
22.
go back to reference Lemire JM, Braun KR, Maurel P, Kaplan ED, Schwartz SM, Wight TN: Versican/PG-M isoforms in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 1999,19(9):1630–1639.CrossRefPubMed Lemire JM, Braun KR, Maurel P, Kaplan ED, Schwartz SM, Wight TN: Versican/PG-M isoforms in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 1999,19(9):1630–1639.CrossRefPubMed
23.
go back to reference Morris SM, Stone PJ, Snider GL, Albright T, Franzblau C: Ultrastructural changes in hamster lung four hours to twenty-four days after exposure to elastase. Anat Rec 1981, 201:523–535.CrossRefPubMed Morris SM, Stone PJ, Snider GL, Albright T, Franzblau C: Ultrastructural changes in hamster lung four hours to twenty-four days after exposure to elastase. Anat Rec 1981, 201:523–535.CrossRefPubMed
24.
go back to reference Osman M, Cantor JO, Roffman S, Keller S, Turino GM, Mandl I: Cigarette smoke impairs elastin resynthesis in lungs of hampsters with elastase-induced emphysema. Am Rev Resp Dis 1985, 132:640–643.PubMed Osman M, Cantor JO, Roffman S, Keller S, Turino GM, Mandl I: Cigarette smoke impairs elastin resynthesis in lungs of hampsters with elastase-induced emphysema. Am Rev Resp Dis 1985, 132:640–643.PubMed
25.
go back to reference Belton JC, Crise N, McLaughlin RF Jr, Tueller EE: Ultrastructural alterations in collagen associated with microscopic foci of human emphysema. Hum Pathol 1977, 8:669–677.CrossRefPubMed Belton JC, Crise N, McLaughlin RF Jr, Tueller EE: Ultrastructural alterations in collagen associated with microscopic foci of human emphysema. Hum Pathol 1977, 8:669–677.CrossRefPubMed
26.
go back to reference Fukuda Y, Masuda Y, Ishizaki M: Morphogenesis of abnormal elastic fibers in panacinar and centriacinar emphysema. Hum Pathol 1989, 20:652–659.CrossRefPubMed Fukuda Y, Masuda Y, Ishizaki M: Morphogenesis of abnormal elastic fibers in panacinar and centriacinar emphysema. Hum Pathol 1989, 20:652–659.CrossRefPubMed
27.
go back to reference Hinek A, Rabinovitch M: 67-kD elastin-binding protein is a protective "companion" of extracellular insoluble elastin and intracellular tropoelastin. J Cell Bio 1994, 126:563–574.CrossRef Hinek A, Rabinovitch M: 67-kD elastin-binding protein is a protective "companion" of extracellular insoluble elastin and intracellular tropoelastin. J Cell Bio 1994, 126:563–574.CrossRef
28.
go back to reference Hinek A, Wrenn DS, Mecham RP, Barondes SH: The elastin receptor: a galactosidase-binding protein. Science 1988, 239:1539–1541.CrossRefPubMed Hinek A, Wrenn DS, Mecham RP, Barondes SH: The elastin receptor: a galactosidase-binding protein. Science 1988, 239:1539–1541.CrossRefPubMed
29.
go back to reference Mecham RP, Whitehouse L, Hay M, Hinek A, Sheetz MP: Ligand affinity of the 67-kDa elastin/laminin binding protein is modulated by the proteins lectin domain: visualization of elastin/laminin receptor complexes with gold tagged ligands. J Cell Biol 1991, 113:187–194.CrossRefPubMed Mecham RP, Whitehouse L, Hay M, Hinek A, Sheetz MP: Ligand affinity of the 67-kDa elastin/laminin binding protein is modulated by the proteins lectin domain: visualization of elastin/laminin receptor complexes with gold tagged ligands. J Cell Biol 1991, 113:187–194.CrossRefPubMed
30.
go back to reference Hinek A: Nature and the multiple functions of the 67 kD elastin-/laminin binding protein. Cell Adhes Commun 1994, 2:185–193.CrossRefPubMed Hinek A: Nature and the multiple functions of the 67 kD elastin-/laminin binding protein. Cell Adhes Commun 1994, 2:185–193.CrossRefPubMed
31.
go back to reference Hinek A: Biological roles of the non-integrin elastin/laminin receptor. Biol Chem 1996, 377:471–480.PubMed Hinek A: Biological roles of the non-integrin elastin/laminin receptor. Biol Chem 1996, 377:471–480.PubMed
32.
go back to reference Privitera S, Prody CA, Callahan JW, Hinek A: The 67-kDa enzymatically inactive alternatively spliced variant of beta-galactosidase is identical to the elastin/laminin-binding protein. J Biol Chem 1998, 273:6319–6326.CrossRefPubMed Privitera S, Prody CA, Callahan JW, Hinek A: The 67-kDa enzymatically inactive alternatively spliced variant of beta-galactosidase is identical to the elastin/laminin-binding protein. J Biol Chem 1998, 273:6319–6326.CrossRefPubMed
33.
go back to reference Hinek A, Wilson S: Impaired elastogenesis in Hurler disease: dermatan sulphate accumulation linked to deficiency in elastin binding protein and elastic fiber assembly. Am J Pathol 2000, 156:925–938.CrossRefPubMedPubMedCentral Hinek A, Wilson S: Impaired elastogenesis in Hurler disease: dermatan sulphate accumulation linked to deficiency in elastin binding protein and elastic fiber assembly. Am J Pathol 2000, 156:925–938.CrossRefPubMedPubMedCentral
34.
go back to reference Hinek A, Smith A, Cutiongco EM, Callahan JW, Weksberg R: Decreased elastin deposition and high proliferation of fibroblasts from Costello syndrome are related to functional deficiency in the 67-kD elastin-binding protein. Amer J Hum Genet 2000, 66:859–872.CrossRefPubMedPubMedCentral Hinek A, Smith A, Cutiongco EM, Callahan JW, Weksberg R: Decreased elastin deposition and high proliferation of fibroblasts from Costello syndrome are related to functional deficiency in the 67-kD elastin-binding protein. Amer J Hum Genet 2000, 66:859–872.CrossRefPubMedPubMedCentral
35.
go back to reference Merrilees MJ, Lemire JM, Fischer JW, Kinsella MG, Braun KR, Clowes AW, Wight TN: Retrovirally mediated overexpression of versican V3 by arterial smooth muscle cells induces tropoelastin synthesis and elastic fibre formation in vitro and in neointima after vascular injury. Circulation Research 2002, 90:481–487.CrossRefPubMed Merrilees MJ, Lemire JM, Fischer JW, Kinsella MG, Braun KR, Clowes AW, Wight TN: Retrovirally mediated overexpression of versican V3 by arterial smooth muscle cells induces tropoelastin synthesis and elastic fibre formation in vitro and in neointima after vascular injury. Circulation Research 2002, 90:481–487.CrossRefPubMed
36.
go back to reference Karlinsky JB: Glycosaminoglycans in emphysematous and fibrotic hamster lungs. Am Rev Resp Dis 1982, 125:85–88.PubMed Karlinsky JB: Glycosaminoglycans in emphysematous and fibrotic hamster lungs. Am Rev Resp Dis 1982, 125:85–88.PubMed
37.
go back to reference Lafuma C, Moczar M, Lange F, Bignon J, Robert L: Biosynthesis of hyaluronic acid, heparin sufate and structural glycoproteins in hamster lung explants during elastase induced emphysema. Conn Tiss Res 1985, 13:169–179.CrossRef Lafuma C, Moczar M, Lange F, Bignon J, Robert L: Biosynthesis of hyaluronic acid, heparin sufate and structural glycoproteins in hamster lung explants during elastase induced emphysema. Conn Tiss Res 1985, 13:169–179.CrossRef
38.
go back to reference Van Straaten JF, Coers W, Noordhoek JA, Huitema S, Flipsen JT, Kauffman HF, Timens W, Postma DS: Proteoglycan changes in the extracellular matrix of lung tissue from patients with pulmonary emphysema. Mod Pathol 1999,12(7):697–705.PubMed Van Straaten JF, Coers W, Noordhoek JA, Huitema S, Flipsen JT, Kauffman HF, Timens W, Postma DS: Proteoglycan changes in the extracellular matrix of lung tissue from patients with pulmonary emphysema. Mod Pathol 1999,12(7):697–705.PubMed
39.
go back to reference Bensadoun ES, Burke AK, Hogg JC, Roberts CR: Proteoglycan deposition in pulmonary fibrosis. Am J Respir Crit Care Med 1996, 154:1819–1828.CrossRefPubMed Bensadoun ES, Burke AK, Hogg JC, Roberts CR: Proteoglycan deposition in pulmonary fibrosis. Am J Respir Crit Care Med 1996, 154:1819–1828.CrossRefPubMed
40.
go back to reference Bensadoun ES, Burke AK, Hogg JC, Roberts CR: Proteoglycans in granulomatous lung diseases. Eur Resp J 1997, 10:2731–2737.CrossRef Bensadoun ES, Burke AK, Hogg JC, Roberts CR: Proteoglycans in granulomatous lung diseases. Eur Resp J 1997, 10:2731–2737.CrossRef
41.
go back to reference Huang J, Olivenstein R, Taha R, Hamid Q, Ludwig M: Enhanced proteoglycan deposition in the airway wall of atopic asthmatics. Am J Respir Crit Care Med 1999, 160:725–729.CrossRefPubMed Huang J, Olivenstein R, Taha R, Hamid Q, Ludwig M: Enhanced proteoglycan deposition in the airway wall of atopic asthmatics. Am J Respir Crit Care Med 1999, 160:725–729.CrossRefPubMed
42.
go back to reference Lowry MH, McAllister BP, Jyh-Chang J, Brown LS, Hughey RP, Cruikshank WW, Amar S, Lucey EC, Braun K, Johnson P, Wight T, Joyce-Brady M: Lung lining fluid glutathione attenuates IL-13 induced asthma. Am J Respir Cell Mol Biol 2007., (Epub): 10.1165/rcmb.2007–0128OC Lowry MH, McAllister BP, Jyh-Chang J, Brown LS, Hughey RP, Cruikshank WW, Amar S, Lucey EC, Braun K, Johnson P, Wight T, Joyce-Brady M: Lung lining fluid glutathione attenuates IL-13 induced asthma. Am J Respir Cell Mol Biol 2007., (Epub): 10.1165/rcmb.2007–0128OC
43.
go back to reference Faggian J, Fosang AJ, Zieba M, Wallace MJ, Hooper SB: Changes in versican and chondroitin sulphate proteoglycans during structural development of the lung. Am J Regul Integr Comp Physiol 2007, 293:R784-R792.CrossRef Faggian J, Fosang AJ, Zieba M, Wallace MJ, Hooper SB: Changes in versican and chondroitin sulphate proteoglycans during structural development of the lung. Am J Regul Integr Comp Physiol 2007, 293:R784-R792.CrossRef
44.
go back to reference Wright RR: Elastic tissue of normal and emphysematous lungs: a tridimensional histological study. Am J Pathol 1961, 39:355–363.PubMedPubMedCentral Wright RR: Elastic tissue of normal and emphysematous lungs: a tridimensional histological study. Am J Pathol 1961, 39:355–363.PubMedPubMedCentral
45.
go back to reference Fukuda Y, Ferrans VJ, Crystal RG: The development of alveolar septa in fetal sheep lung. An ultrastructural and immunohistochemical study. Am J Anat 1984, 167:405–439.CrossRef Fukuda Y, Ferrans VJ, Crystal RG: The development of alveolar septa in fetal sheep lung. An ultrastructural and immunohistochemical study. Am J Anat 1984, 167:405–439.CrossRef
46.
go back to reference Maquart F-X, Pasco S, Ramont L, Hornebeck W, Monboisse J-C: An introduction to matrikines: extracellular matrix-derived peptides which regulate cell activity. Implication in tumor invasion. Crit Rev Oncol/Hemat 2004, 49:199–202.CrossRef Maquart F-X, Pasco S, Ramont L, Hornebeck W, Monboisse J-C: An introduction to matrikines: extracellular matrix-derived peptides which regulate cell activity. Implication in tumor invasion. Crit Rev Oncol/Hemat 2004, 49:199–202.CrossRef
47.
go back to reference Lucey EC, Golstein RH, Stone PJ, Snider GL: Remodeling of alveolar walls after elastase treatmentof Hampsters. Am J Respir Crit Care Med 1998, 158:555–564.CrossRefPubMed Lucey EC, Golstein RH, Stone PJ, Snider GL: Remodeling of alveolar walls after elastase treatmentof Hampsters. Am J Respir Crit Care Med 1998, 158:555–564.CrossRefPubMed
Metadata
Title
Changes in elastin, elastin binding protein and versican in alveoli in chronic obstructive pulmonary disease
Authors
Mervyn J Merrilees
Pamela ST Ching
Brent Beaumont
Aleksander Hinek
Thomas N Wight
Peter N Black
Publication date
01-12-2008
Publisher
BioMed Central
Published in
Respiratory Research / Issue 1/2008
Electronic ISSN: 1465-993X
DOI
https://doi.org/10.1186/1465-9921-9-41

Other articles of this Issue 1/2008

Respiratory Research 1/2008 Go to the issue