Skip to main content
The American Journal of Pathology logoLink to The American Journal of Pathology
. 1996 Oct;149(4):1405–1415.

Elastin and collagen remodeling in emphysema. A scanning electron microscopy study.

G A Finlay 1, M D O'Donnell 1, C M O'Connor 1, J P Hayes 1, M X FitzGerald 1
PMCID: PMC1865175  PMID: 8863687

Abstract

The relationship between elastin degradation and emphysema is well known. Recent evidence suggests that a complex process of pulmonary remodeling occurs within the emphysematous lung. The aim of this study was to assess the extent of extracellular matrix remodeling in emphysema by ultrastructural examination of elastin and collagen templates in an animal model of emphysema and in human emphysematous lungs. Emphysema was induced in rats by the intratracheal administration of porcine pancreatic elastase. Human lung samples were obtained at surgical resection for lung carcinoma. Emphysema was confirmed morphometrically and quantitated using the mean linear intercept. Matching sections were treated with sodium hydroxide and formic acid to expose collagen and elastin templates, respectively. Scanning electron microscopy with stereo-pair imaging allowed three-dimensional visualization of the exposed templates. In emphysematous lungs from both sources, sheets of elastin were disrupted and perforated with multiple fenestrations. In elastase-induced emphysema, this disintegration was accompanied by a marked increase in thickness of collagen fibrils, which contrasted with the fine fibrillar network of control lungs. Similarly, a pattern of thickened fibrils and disorganized deposition of collagen was observed in human lungs. In conclusion, these findings support the novel concept of increased collagen deposition and aberrant collagen remodeling in the pathogenesis of emphysema.

Full text

PDF
1405

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Busch R. H., Lauhala K. E., Loscutoff S. M., McDonald K. E. Experimental pulmonary emphysema induced in the rat by intratracheally administered elastase: morphogenesis. Environ Res. 1984 Apr;33(2):497–513. doi: 10.1016/0013-9351(84)90044-6. [DOI] [PubMed] [Google Scholar]
  2. Cardoso W. V., Sekhon H. S., Hyde D. M., Thurlbeck W. M. Collagen and elastin in human pulmonary emphysema. Am Rev Respir Dis. 1993 Apr;147(4):975–981. doi: 10.1164/ajrccm/147.4.975. [DOI] [PubMed] [Google Scholar]
  3. Chrzanowski P., Keller S., Cerreta J., Mandl I., Turino G. M. Elastin content of normal and emphysematous lung parenchyma. Am J Med. 1980 Sep;69(3):351–359. doi: 10.1016/0002-9343(80)90004-2. [DOI] [PubMed] [Google Scholar]
  4. Dubick M. A., Rucker R. B., Cross C. E., Last J. A. Elastin metabolism in rodent lung. Biochim Biophys Acta. 1981 Feb 5;672(3):303–306. doi: 10.1016/0304-4165(81)90297-x. [DOI] [PubMed] [Google Scholar]
  5. Fitzpatrick M. Studies of human pulmonary connective tissue. III. Chemical changes in structural proteins with emphysema. Am Rev Respir Dis. 1967 Aug;96(2):254–265. doi: 10.1164/arrd.1967.96.2.254. [DOI] [PubMed] [Google Scholar]
  6. Fukuda Y., Masuda Y., Ishizaki M., Masugi Y., Ferrans V. J. Morphogenesis of abnormal elastic fibers in lungs of patients with panacinar and centriacinar emphysema. Hum Pathol. 1989 Jul;20(7):652–659. doi: 10.1016/0046-8177(89)90152-4. [DOI] [PubMed] [Google Scholar]
  7. Gardi C., Calzoni P., Marcolongo P., Cavarra E., Vanni L., Lungarella G. Collagen breakdown products and lung collagen metabolism: an in vitro study on fibroblast cultures. Thorax. 1994 Apr;49(4):312–318. doi: 10.1136/thx.49.4.312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kelly D., O'Donnell M. D., Dervan P., McGeeney K. F., Fitzpatrick J. M. The skeletal framework of human kidney and renal cell carcinoma. A scanning electron microscopic study. Urol Res. 1990;18(4):241–244. doi: 10.1007/BF00294765. [DOI] [PubMed] [Google Scholar]
  9. Kuhn C., 3rd, Tavassoli F. The scanning electron microscopy of elastase-induced emphysema. A comparison with emphysema in man. Lab Invest. 1976 Jan;34(1):2–9. [PubMed] [Google Scholar]
  10. Kuhn C., Yu S. Y., Chraplyvy M., Linder H. E., Senior R. M. The induction of emphysema with elastase. II. Changes in connective tissue. Lab Invest. 1976 Apr;34(4):372–380. [PubMed] [Google Scholar]
  11. Lang M. R., Fiaux G. W., Gillooly M., Stewart J. A., Hulmes D. J., Lamb D. Collagen content of alveolar wall tissue in emphysematous and non-emphysematous lungs. Thorax. 1994 Apr;49(4):319–326. doi: 10.1136/thx.49.4.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Morris S. M., Stone P. J., Snider G. L., Albright J. T., Franzblau C. Ultrastructural changes in hamster lung four hours to twenty-four days after exposure to elastase. Anat Rec. 1981 Nov;201(3):523–535. doi: 10.1002/ar.1092010309. [DOI] [PubMed] [Google Scholar]
  13. Muley T., Wiebel M., Schulz V., Ebert W. Elastinolytic activity of alveolar macrophages in smoking-associated pulmonary emphysema. Clin Investig. 1994 Mar;72(4):269–276. doi: 10.1007/BF00180039. [DOI] [PubMed] [Google Scholar]
  14. O'Donnell M. D., Cottell D. C., McGeeney K. F. Three-dimensional structure of lung elastin demonstrated by scanning electron microscopy/stereo-pair images. Microsc Res Tech. 1994 Oct 15;29(3):254–261. doi: 10.1002/jemt.1070290312. [DOI] [PubMed] [Google Scholar]
  15. O'Donnell M. D., McGeeney K. F. An alkali digestion method to expose connective tissue fibers: a scanning electron microscopy study of rat lung. J Electron Microsc Tech. 1991 Dec;19(4):486–490. doi: 10.1002/jemt.1060190411. [DOI] [PubMed] [Google Scholar]
  16. Pacini A., Gardi C., Corradeschi F., Viti A., Belli C., Calzoni P., Lungarella G. In vivo stimulation of lung collagen synthesis by collagen derived peptides. Res Commun Chem Pathol Pharmacol. 1990 Apr;68(1):89–101. [PubMed] [Google Scholar]
  17. Snider G. L. Emphysema: the first two centuries--and beyond. A historical overview, with suggestions for future research: Part 2. Am Rev Respir Dis. 1992 Dec;146(6):1615–1622. doi: 10.1164/ajrccm/146.6.1615. [DOI] [PubMed] [Google Scholar]
  18. Snider G. L., Lucey E. C., Stone P. J. Animal models of emphysema. Am Rev Respir Dis. 1986 Jan;133(1):149–169. doi: 10.1164/arrd.1986.133.1.149. [DOI] [PubMed] [Google Scholar]
  19. Sugimoto T., Ogata T. Scanning electron microscopic studies on the subepithelial tissue of the gastrointestinal mucosa of the rat. Arch Histol Cytol. 1989 Jul;52(3):257–265. doi: 10.1679/aohc.52.257. [DOI] [PubMed] [Google Scholar]
  20. Tetley T. D. New perspectives on basic mechanisms in lung disease. 6. Proteinase imbalance: its role in lung disease. Thorax. 1993 May;48(5):560–565. doi: 10.1136/thx.48.5.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. The definition of emphysema. Report of a National Heart, Lung, and Blood Institute, Division of Lung Diseases workshop. Am Rev Respir Dis. 1985 Jul;132(1):182–185. doi: 10.1164/arrd.1985.132.1.182. [DOI] [PubMed] [Google Scholar]
  22. Thurlbeck W. M. Measurement of pulmonary emphysema. Am Rev Respir Dis. 1967 May;95(5):752–764. doi: 10.1164/arrd.1967.95.5.752. [DOI] [PubMed] [Google Scholar]
  23. Thurlbeck W. M. Overview of the pathology of pulmonary emphysema in the human. Clin Chest Med. 1983 Sep;4(3):337–350. [PubMed] [Google Scholar]
  24. de Santi M. M., Martorana P. A., Cavarra E., Lungarella G. Pallid mice with genetic emphysema. Neutrophil elastase burden and elastin loss occur without alteration in the bronchoalveolar lavage cell population. Lab Invest. 1995 Jul;73(1):40–47. [PubMed] [Google Scholar]

Articles from The American Journal of Pathology are provided here courtesy of American Society for Investigative Pathology

RESOURCES