Tenascin expression and distribution in pleural inflammatory and fibrotic diseases

Our plain-English summary of Tenascin expression and distribution in pleural inflammatory and fibrotic diseases, by R. Kaarteenaho-Wiik, E. Lakari, Y. Soini, et al (The Journal of Histochemistry and Cytochemistry, 2000).

The study

• Authors: R. Kaarteenaho-Wiik, E. Lakari, Y. Soini, R. Pöllänen, V.L. Kinnula, P. Pääkkö
• Journal: The Journal of Histochemistry and Cytochemistry
• Published: 2000;48(9):1257-68
• Cited by: 33 articles, as counted by NIH iCite
• Read it: PubMed · Publisher

Abstract

We hypothesized that tenascin expression is increased in pleural inflammatory and fibrotic diseases and that its expression can be used as a marker of active pleural involvement. For this purpose we analyzed 71 histological samples of inflammatory and fibrotic pleura from patients with asbestos-induced pleural reaction (n = 6), postcardiac injury syndrome (n = 6), parapneumonic infection and/or empyema (n = 23), tuberculosis (n = 5, rheumatoid disease (n = 1), and fibrosis with inflammation of unknown etiology (n = 30). All 71 cases were studied by immunohistochemistry for tenascin. In 19 selected cases tenascin mRNA in situ hybridization was also performed. In every case, tenascin was increased by immunohistochemistry. Most prominent immunoreactivity was detected in areas of newly formed fibrosis. Increased tenascin mRNA expression by in situ hybridization was detected in the individual cells of the newly formed fibrosis underneath the fibrinous exudate. The tenascin mRNA-positive cells localized in areas in which by immunohistochemical studies the cells were positive for alpha-smooth muscle actin, desmin, and vimentin, suggesting a myofibroblast phenotype. Tenascin mRNA expression was also seen less frequently in areas in which some cells were positive for cytokeratin. These cells might represent mesothelial cells entrapped in the inflammatory lesion. Alternatively, they might represent fibroblast-type cells with aberrant cytokeratin expression. We conclude that in pleural inflammatory and fibrotic diseases tenascin immunoreactivity is increased and tenascin mRNA-positive cells localized mainly in the areas of myofibroblast- and, less often, mesothelial-type cells, suggesting that mainly myofibroblasts and, less commonly, also mesothelial cells might be responsible for tenascin expression in pleural inflammatory and fibrotic diseases. (J Histochem Cytochem 48:1257-1268, 2000)

In plain English

This laboratory study from Oulu University Hospital, Finland, examined pleural tissue taken in 1992 to 1998 from 71 patients with inflammatory or fibrotic (scarring) disease of the pleura, the lining around the lungs. Six patients had an asbestos-induced pleural fibrotic reaction. The others had postcardiac injury syndrome (6), parapneumonic infection and/or empyema (23), tuberculosis (5), rheumatoid disease (1) or no known cause (30). The article gives no exposure details or fiber types. The authors stained all samples for tenascin, a tissue-framework protein, and tested 19 for its mRNA. Normal pleura from five patients operated on for lung carcinoma showed no tenascin. All 71 patient samples were positive: strongly in all 34 with new scarring, and moderately in 31 with old, dense scarring. Tenascin mRNA was diffusely increased in 16 of 19 samples, and individual matrix cells with increased expression were seen in 11 of 19. Staining of neighbouring sections suggested most of these cells were myofibroblasts, while fewer were cytokeratin-positive. The authors could not match signals across sections with full certainty. The authors concluded that tenascin may serve as a marker of an acute, ongoing pleural reaction.

We wrote this plain-English summary from the full article with the help of AI, and a second AI model checked each sentence against the article. It is not the authors' wording; the abstract and the article are their own account.

What the study did and found

• Design: Laboratory (histological) study of archived pleural tissue samples. All cases were stained for tenascin (immunohistochemistry), 19 selected cases were also tested for tenascin mRNA (in situ hybridization), and normal pleura served as controls.
• Who was studied: Pleural samples from 71 patients at Oulu University Hospital, Finland, taken 1992 to 1998: asbestos-induced pleural fibrotic reaction (6), postcardiac injury syndrome (6), parapneumonic infection and/or empyema (23), tuberculosis (5), rheumatoid disease (1), unknown cause (30). Controls were uninvolved pleura from five patients who had surgery for lung carcinoma.
• Exposure: Asbestos-induced pleural fibrotic reaction was one of six diagnosis groups (6 patients). No fiber types, jobs or doses are given. The study measured tenascin in the tissue, not exposure.
• Main results:
  • Tenascin was not detectable in normal control pleura (5 cases).
  • Tenascin staining was scored as strong in 34 of 71 patient samples, which were all the cases with newly formed fibrosis.
  • Tenascin staining was scored as moderate in 31 of 71 patient samples, those with old fibrosis.
  • All 71 patient samples were strongly or moderately positive for tenascin, compared with the 5 tenascin-negative controls. This was tested with Fisher's exact test; the printed p-value has a lost comparison symbol before 0.00001.
  • The intensity and location of tenascin were similar in every disease group, including the asbestos group. The exceptions were the granulomatous cases (tuberculosis and rheumatoid disease).
  • In the asbestos group (6 cases), fibrinous exudate was seen in 5 of 6, polymorphonuclear leukocytes in 0 of 6, granulation tissue in 2 of 6, and dense fibrosis in 4 of 6.
  • By in situ hybridization, tenascin mRNA grains were diffusely increased in 16 of the 19 cases.
  • Individual large, oval mesenchymal cells of the matrix showed increased tenascin expression in 11 of 19 cases.
  • Serial-section staining showed that most of these cells were positive for alpha-smooth muscle actin, vimentin, desmin and human muscle actin, which suggested a myofibroblastic phenotype. Fewer were cytokeratin-positive. The cells were negative for FVIII-related antigen and CD34.
  • Individual cells with strong tenascin mRNA expression were seen significantly more often in samples from patients with infective causes (parapneumonia, empyema, tuberculosis) than in samples from other patients. They were also seen more often in samples with granulation tissue than in samples with only dense fibrosis. The reported p-values were 0.037 and 0.0001; the comparison symbols were lost in the text.
• The authors' conclusion: The authors concluded that tenascin is increased in pleural inflammatory and fibrotic diseases of varied causes and is actively made in newly formed fibrosis. They concluded it may serve as a marker for an acute and ongoing reaction. In their view it is produced mainly by myofibroblasts, and less often by mesothelial cells and/or fibroblasts with aberrant cytokeratin.
• Limitations the authors state:
  • The authors could not co-localize the expression signals in serial sections with 100% certainty, and they called for further confirmatory studies.
  • Mesothelial cells usually detach in these lesions, as they did in this material, which made mesothelial cells difficult to study.

Topics

The National Library of Medicine indexes this study under subjects our site covers: Pleural plaques and thickening.

Medical terms in this study, explained in our Lexicon: Pleura, Empyema, Fibrosis, Inflammation, Etiology, Immunohistochemistry, Exudate, Desmin.

Related studies

• Tenascin and fibronectin expression in human mesothelial cells and pleural mesothelioma cell-line cells — V.L. Kinnula, A. Linnala, et al. (1998)
• Decreased Cyp2E1 mRNA expression in human leucocytes in patients with fibrotic and inflammatory lung diseases — S. Helmig, J. Döhrel, et al. (2010)
• Tenascin XB Is a Novel Diagnostic Marker for Malignant Mesothelioma — K. Nakayama, M. Seike, et al. (2019)
• Expression of inducible nitric oxide synthase in healthy pleura and in malignant mesothelioma — Y. Soini, K. Kahlos, et al. (2000)
• Pulmonary inflammatory and fibrotic responses in Fischer 344 rats after intratracheal instillation exposure to Libby amphibole — D.J. Padilla-Carlin, M.C. Schladweiler, et al. (2011)
• Genes involved in innate immunity associated with asbestos-related fibrotic changes — M.K. Kukkonen, T. Vehmas, et al. (2014)

Browse more research in The Journal of Histochemistry and Cytochemistry, or return to medical research.