Hostname: page-component-f554764f5-wjqwx Total loading time: 0 Render date: 2025-04-09T10:25:24.563Z Has data issue: false hasContentIssue false
  • English
  • Français

Induction of tumour necrosis factor, interleukin-1β and matrix metalloproteinases in pulmonary fibrosis of rats infected with Angiostrongylus cantonensis

Published online by Cambridge University Press:  12 April 2024

W.C. Tu  and
S.C. Lai
W.C. Tu
Affiliation:
Department of Entomology, National Chung-Hsing University, Taichung 402, Taiwan:
S.C. Lai*
Affiliation:
Department of Parasitology, Chung Shan Medical University, 110 Section 1, Chien-Kuo North Road, Taichung 402, Taiwan
*
*Author for correspondence Fax:+886-4-23823381 E-mail: shih@ csmu.edu.tw
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

In angiostrongyliasis, chronic parasite-induced granuloma formation can lead to tissue destruction and fibrosis. Here, the histomorphology of granulomatous fibrosis and proteinase production in the lungs of Angiostrongylus cantonensis-infected Sprague-Dawley rats were investigated. The relationship between metalloproteinases and granulomatous fibrosis was investigated following infection of each rat with 60 infective larvae. Granulomata and fibrosis were marked in the lungs of rats on day 180 post-inoculation. Reverse transcriptase polymerase chain reaction of lung mRNA showed an up-expression of proinflammatory cytokine including tumour necrosis factor alpha (TNF-α) and interleukin-1 beta (IL-1β). According to Western blot analysis, matrix metalloproteinase-2 (MMP-2) proenzyme was presented in the lungs of uninfected and infected rats, and partial conversion of 72 kDa proenzyme to the 64kDa active form occurred in infected rats. In addition, increased protein levels of MMP-9 and MMP-13 were detected in infected lungs, but were undetectable in controls. The results suggest that TNF-α, IL-1β, MMP-2, -9, and -13 may be associated with the granulomatous fibrosis.

Type
Research Article
Information
Journal of Helminthology , Volume 80 , Issue 3 , September 2006 , pp. 305 - 311
Copyright
Copyright © Cambridge University Press 2006

References

Alicata, J.E. (1965) Biology and distribution of the rat lungworm, Angiostrongylus cantonensis, and its relationship to eosinophilic meningoencephalitis and other neurological disorders of man and animals. Advances in Parasitology 3, 223–248.CrossRefGoogle Scholar
Ash, L.R. (1970) Diagnostic morphology of the third-stage larvae of Angiostrongylus cantonensis, Angiostrongylus vasorum, Aelurostrongylus abstrusus, and Anafilaroides rostratus (Nematoda: Metastrongyloidea). Journal of Parasitology 56, 249–253.CrossRefGoogle ScholarPubMed
Birkedal-Hansen, H. (1995) Proteolytic remodeling of extracellular matrix. Current Opinion in Cell Biology 7, 728–735.CrossRefGoogle ScholarPubMed
Cataldo, D., Munaut, C., Noel, A., Frankenne, F., Bartsch, P., Foidart, J.M. & Louis, R. (2000) MMP-2 and MMP-9-linked gelatinolytic activity in the sputum from patients with asthma and chronic obstructive pulmonary disease. International Archives of Allergy and Immunology 123, 259–267.CrossRefGoogle ScholarPubMed
Chen, K.M., Lee, H.H., Lu, K.H., Tseng, Y.K., Hsu, L.S., Chou, H.L. & Lai, S.C. (2004) Association of matrix metalloproteinase-9 and Purkinje cell degeneration in mouse cerebellum caused by Angiostrongylus cantonensis . International Journal for Parasitology 34, 1147–1156.CrossRefGoogle ScholarPubMed
Corbel, M., Caulet-Maugendre, S., Germain, N., Lagente, V. & Boichot, E. (2003) Enhancement of gelatinase activity during development of subepithelial fibrosis in a murine model of asthma. Clinical and Experimental Allergy 33, 696–704.CrossRefGoogle Scholar
Crouch, E. (1990) Pathobiology of pulmonary fibrosis. American Journal of Physiology. Lung Cellular and Molecular Physiology 259, L159–L184.CrossRefGoogle ScholarPubMed
Dunsmore, S.E. & Rannels, D.E. (1996) Extracellular matrix biology in the lung. American Journal of Physiology. Lung Cellular and Molecular Physiology 270, L3–L27.CrossRefGoogle ScholarPubMed
Fukuda, Y., Ishizaki, M., Kudoh, S., Kitaichi, M. & Yamanaka, N. (1998) Localization of matrix metalloproteinase-1, -2, and -9 and tissue inhibitor of metalloproteinase-2 in interstitial lung diseases. Laboratory Investigation 78, 687–698.Google ScholarPubMed
Gharaee-Kermani, M. & Phan, S.H. (1997) Lung interleukin-5 expression in murine bleomycin-induced pulmonary fibrosis. American Journal of Respiratory Cell and Molecular Biology 16, 438–447.CrossRefGoogle ScholarPubMed
Gharaee-Kermani, M. & Phan, S.H. (2001) Role of cytokines and cytokine therapy in wound healing and fibrotic diseases. Current Pharmaceutical Design 7, 1083–1103.CrossRefGoogle ScholarPubMed
Hsu, L.S., Lee, H.H., Chen, K.M., Chou, H.L. & Lai, S.C. (2005) Matrix metalloproteinase-2, and -9 in granulomatous fibrosis of rat infected with Angiostrongylus cantonensis . Annals of Tropical Medicine and Parasitology 99, 61–70.CrossRefGoogle ScholarPubMed
Huaux, F., Liu, T. McGarry, B., Ullenbruch, M. & Phan, S.H. (2003) Dual roles of IL-4 in lung injury and fibrosis. Journal of Immunology 170, 2083–2092.CrossRefGoogle ScholarPubMed
Kolb, M., Margetts, P.J., Anthony, D.C., Pitossi, F. & Gauldie, J. (2001) Transient expression of IL-1β induces acute lung injury and chronic repair leading to pulmonary fibrosis. Journal of Clinical Investigation 107, 1529–1536.CrossRefGoogle ScholarPubMed
Lai, S.C., Twu, J.J., Jiang, S.T., Hsu, J.D., Chen, K.M., Chiaing, H.C., Wang, C.J. & Lee, H.H. (2004) Induction of matrix-metalloproteinase-9 in the pathogenesis of eosinophilic meningitis caused by Angiostrongylus cantonensis . Annals of Tropical Medicine and Parasitology 98, 715–724.CrossRefGoogle ScholarPubMed
Lee, C.G., Homer, R.J., Cohn, L., Link, H., Jung, S., Craft, J.E., Graham, B.S., Johnson, T.R. & Elias, J.A. (2002) Transgenic overexpression of interleukin (IL)-10 in the lung causes mucus metaplasia, tissue inflammation, and airway remodeling via IL-13-dependent and -independent pathways. Journal of Biological Chemistry 277, 35466–35474.CrossRefGoogle ScholarPubMed
Lee, H.H., Chou, H.L., Chen, K.M. & Lai, S.C. (2004) Association of matrix-metalloproteinase-9 in eosinophilic meningitis of BALB/c mice caused by Angiostrongylus cantonensis . Parasitology Research 94, 321–328.CrossRefGoogle ScholarPubMed
Lindo, J.F., Waugh, C., Hall, J., Cunningham-Myrie, C., Ashley, D., Eberhard, M.L., Sullivan, J.J., Bishop, H.S., Robinson, D.G., Holtz, T. & Robinson, R.D. (2002) Enzootic Angiostrongylus cantonensis in rats and snails after an outbreak of human eosinophilic meningitis, Jamaica. Emerging Infectious Diseases 8, 324–326.CrossRefGoogle ScholarPubMed
Matrisian, L.M. (1992) The matrix-degrading metalloproteinases. Bioessays 14, 455–463.CrossRefGoogle ScholarPubMed
Mauviel, A. (1993) Cytokine regulation of metalloproteinase gene expression. Journal of Cellular Biochemistry 53, 288–295.CrossRefGoogle ScholarPubMed
O'Connor, C.M. & FitzGerald, M.X. (1994) Matrix metalloproteases and lung disease. Thorax 49, 602–609.CrossRefGoogle ScholarPubMed
Ohnishi, K., Takagi, M., Kurokawa, Y., Satomi, S. & Konttinen, Y.T. (1998) Matrix metalloproteinase-mediated extracellular matrix protein degradation in human pulmonary emphysema. Laboratory Investigation 78, 1077–1087.Google ScholarPubMed
Pardo, A. & Selman, M. (1996) Matrix metalloproteinases and lung injury. Brazilian Journal of Medical and Biological Research 29, 1109–1115.Google ScholarPubMed
Parsons, J.C. & Grieve, R.B. (1990) Effect of egg dosage and host genotype on liver trapping in murine larval toxocariasis. Journal of Parasitology 76, 53–58.CrossRefGoogle ScholarPubMed
Selman, M., Ruiz, V., Cabrera, S., Segura, L., Ramirez, R., Barrios, R. & Pardo, A. (2000) TIMP-1, -2, -3, and -4 in idiopathic pulmonary fibrosis. A prevailing nondegradative lung microenvironment? American Journal of Physiology. Lung Cellular and Molecular Physiology 279, L562–L574.CrossRefGoogle ScholarPubMed
Sime, P.J., Marr, R.A., Gauldie, D., Xing, Z., Hewlett, B.R., Graham, F.L. & Gauldie, J. (1998) Transfer of tumor necrosis factor-α to rat lung induces severe pulmonary inflammation and patchy interstitial fibrogenesis with induction of transforming growth factor-β1 and myofibroblasts. American Journal of Pathology 153, 825–832.CrossRefGoogle ScholarPubMed
Siwik, D.A., Chang, D.L.F. & Colucci, W.S. (2000) Interleukin-1β and tumor necrosis factor-α decrease collagen synthesis and increase matrix metalloproteinase activity in cardiac fibroblasts in vitro. Circulation Research 86, 1259–1265.CrossRefGoogle ScholarPubMed
Teng, S., Kurata, S., Katoh, I., Georgieva, G.S., Nosaka, T., Mitaka, C. & Imai, T. (2004) Cytokine mRNA expression in unilateral ischemic-reperfused rat lung with salt solution supplemented with low-endotoxin or standard bovine serum albumin. American Journal of Physiology. Lung Cellular and Molecular Physiology 286, L137–L142.CrossRefGoogle ScholarPubMed
Wallace, W.A., Ramage, E.A., Lamb, D. & Howie, S.E. (1995) A type 2 (Th2-like) pattern of immune response predominates in the pulmonary interstitium of patients with cryptogenic fibrosing alveolitis (CFA). Clinical and Experimental Immunology 101, 436–441.CrossRefGoogle ScholarPubMed
Winkler, M.K. & Fowlkes, J.L. (2002) Metalloproteinase and growth factor interactions: do they play a role in pulmonary fibrosis? American Journal of Physiology. Lung Cellular and Molecular Physiology 283, L1–L11.CrossRefGoogle ScholarPubMed
Yii, C.Y., Chen, C.Y., Fresh, T.W., Chen, T. & Cross, J.H. (1968) Human angiostrongyliasis involving the lungs. Chinese Journal of Microbiology (Taipei) 1, 148–150.Google Scholar
Zhu, Y.K., Liu, X., Ertl, R.F., Kohyama, T., Wen, F.Q., Wang, H., Spurzem, J.R., Romberger, D.J. & Rennard, S.I. (2001) Retinoic acid attenuates cytokine-driven fibroblast degradation of extracellular matrix in three-dimensional culture. American Journal of Physiology. Lung Cellular and Molecular Physiology 25, 620–627.Google ScholarPubMed