Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-26T01:11:14.587Z Has data issue: false hasContentIssue false
  • English
  • Français

Paeoniflorin inhibits TGF-β1-mediated collagen production by Schistosoma japonicum soluble egg antigen in vitro

Published online by Cambridge University Press:  24 May 2007

D. CHU ,
Q. LUO ,
C. LI ,
Y. GAO ,
L. YU ,
W. WEI ,
Q. WU  and
J. SHEN
D. CHU
Affiliation:
Institute of Clinical Pharmacology, Anhui Medical Universityand the Key Laboratory of Antiinflammatory-immunopharmacology, Anhui, China Institute of Zoonoses of Anhui Medical University and the Key Laboratory of Gene Resource Utilization for Severe Diseases (Anhui Medical University), Ministry of Education of China
Q. LUO
Affiliation:
Institute of Zoonoses of Anhui Medical University and the Key Laboratory of Gene Resource Utilization for Severe Diseases (Anhui Medical University), Ministry of Education of China
C. LI
Affiliation:
Institute of Zoonoses of Anhui Medical University and the Key Laboratory of Gene Resource Utilization for Severe Diseases (Anhui Medical University), Ministry of Education of China
Y. GAO
Affiliation:
Institute of Clinical Pharmacology, Anhui Medical Universityand the Key Laboratory of Antiinflammatory-immunopharmacology, Anhui, China Institute of Zoonoses of Anhui Medical University and the Key Laboratory of Gene Resource Utilization for Severe Diseases (Anhui Medical University), Ministry of Education of China
L. YU
Affiliation:
Institute of Clinical Pharmacology, Anhui Medical Universityand the Key Laboratory of Antiinflammatory-immunopharmacology, Anhui, China Institute of Zoonoses of Anhui Medical University and the Key Laboratory of Gene Resource Utilization for Severe Diseases (Anhui Medical University), Ministry of Education of China
W. WEI
Affiliation:
Institute of Clinical Pharmacology, Anhui Medical Universityand the Key Laboratory of Antiinflammatory-immunopharmacology, Anhui, China
Q. WU
Affiliation:
Department of Pathology, Anhui Medical University
J. SHEN*
Affiliation:
Institute of Clinical Pharmacology, Anhui Medical Universityand the Key Laboratory of Antiinflammatory-immunopharmacology, Anhui, China Institute of Zoonoses of Anhui Medical University and the Key Laboratory of Gene Resource Utilization for Severe Diseases (Anhui Medical University), Ministry of Education of China
*
*Corresponding author: Institute of Zoonoses of Anhui Medical University and the Key Laboratory of Gene Resource Utilization for Severe Diseases, No. 81, Meishan Road, Hefei, Anhui, China. Tel./Fax: +86 551 5161057. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The main pathological characteristics of hepatic fibrosis in schistosomiasis are the proliferation of hepatic stellate cells (HSCs) and the deposition of collagen type I (Col I) and collagen type III (Col III). Transforming growth factor beta-1 (TGF-β1) plays an important role in hepatic fibrosis. Paeoniflorin (PAE) has been reported to have immunoregulatory effects; however, the mechanism of its anti-hepatic fibrosis in S. japonicum has not been elucidated. In the present study, we found that mouse peritoneal macrophages (PMφs) stimulated by soluble egg antigen (SEA) of S. japonicum could secrete TGF-β1, and the TGF-β1 in the peritoneal macrophage-conditioned medium (PMCM) could induce proliferation of HSCs and secretion of Col I and III. We selected PMCM at 1:2 dilution as the optimum PMCM (OPMCM). Then we treated HSCs pre-incubated with OPMCM with PAE, and found that the inhibition of HSC proliferation or Col I and III production were closely correlated with the concentration of PAE. Further investigation found that PAE significantly decreased the Smad3 transcription and phosphorylation in HSCs stimulated by OPMCM. In conclusion, SEA plays a key role in hepatic fibrosis by inducing TGF-β1 from PMφs. PAE can exert anti-fibrogenic effects by inhibiting HSCs proliferation and down-regulating Smad3 expression and phosphorylation through TGF-β1 signalling.

Keywords

Schistosoma japonicumtransforming growth factor-beta1peritoneal macrophagehepatic stellate cellproliferationcollagenSmad3
Type
Research Article
Information
Parasitology , Volume 134 , Issue 11 , October 2007 , pp. 1611 - 1621
Copyright
Copyright © Cambridge University Press 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bachman, K. E. and Park, B. H. (2005). Dual nature of TGF-beta signaling: tumor suppressor vs. tumor promoter. Current Opinion in Oncology 17, 49–54.CrossRefGoogle ScholarPubMed
Boros, D. L. (1989). Immunopathology of Schistosoma mansoni infection. Clinical Microbiology Reviews 2, 250–269.CrossRefGoogle ScholarPubMed
Callahan, J. F., Burgess, J. L., Fornwald, J. A., Gaster, L. M., Harling, J. D., Harrington, F. P., Heer, J., Kwon, C., Lehr, R., Mathur, A., Olson, B. A., Weinstock, J. and Laping, N. J. (2002). Identification of novel inhibitors of the transforming growth factor beta1 (TGF-beta1) type 1 receptor (ALK5). Journal of Medicinal Chemistry 45, 999–1001.CrossRefGoogle ScholarPubMed
Chang, D., Ramalho, L. N., Ramalho, F. S., Martinelli, A. L. and Zucoloto, S. (2006). Hepatic stellate cells in human schistosomiasis mansoni: a comparative immunohistochemical study with liver cirrhosis. Acta Tropica 97, 318–323.CrossRefGoogle ScholarPubMed
Chen, Y. X., Lu, C. H., Xie, W. F., Zhang, X. R., Zhang, Z. B., Wei, L. X., Jin, Y. X. and Guo, Y. J. (2005). Effects of ribozyme targeting platelet-derived growth factor receptor beta subunit gene on the proliferation and apoptosis of hepatic stellate cells in vitro. Chinese Medical Journal (English Edition) 118, 982–988.Google ScholarPubMed
Cioli, D. and Pica-Mattoccia, L. (2003). Praziquantel. Parasitology Research 90 Supp 1, S3–S9.CrossRefGoogle ScholarPubMed
Harn, D. A., Mitsuyama, M. and David, J. R. (1984). Schistosoma mansoni anti-egg monoclonal antibodies protect against cercarial challenge in vivo. The Journal of Experimental Medicine 159, 1371–1387.CrossRefGoogle ScholarPubMed
Geerts, A., Eliasson, C., Niki, T., Wielant, A., Vaeyens, F. and Pekny, M. (2001). Formation of normal desmin intermediate filaments in mouse hepatic stellate cells requires vimentin. Hepatology 33, 177–188.CrossRefGoogle ScholarPubMed
Gordon, S. (2003). Alternative activation of macrophages. Nature Reviews, Immunology 3, 23–35.CrossRefGoogle ScholarPubMed
Goumans, M. J., Lebrin, F. and Valdimarsdottir, G. (2003). Controlling the angiogenic switch: a balance between two distinct TGF-b receptor signaling pathways. Trends in Cardiovascular Medicine 13, 301–307.CrossRefGoogle ScholarPubMed
Gryseels, B., Polman, K., Clerinx, J. and Kestens, L. (2006). Human schistosomiasis. Lancet 368, 1106–1118.CrossRefGoogle ScholarPubMed
Hesse, M., Modolell, M., Laflamme, A. C., Schito, M., Fuentes, J. M., Cheever, A. W., Pearce, E. J. and Wynn, T. A. (2001). Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of L-arginine metabolism. Journal of Immunology 167, 6533–6544.CrossRefGoogle ScholarPubMed
Lappalainen, K., Jaaskelainen, I., Syrjanen, K., Urtti, A. and Syrjanen, S. (1994). Comparison of cell proliferation and toxicity assays using two cationic liposomes. Pharmaceutical Research 11, 1127–1131.CrossRefGoogle ScholarPubMed
Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265–275.CrossRefGoogle ScholarPubMed
Maher, J. J. (2001). Interactions between hepatic stellate cells and the immune system. Seminars in Liver Disease 21, 417–426.CrossRefGoogle ScholarPubMed
Mansy, S. S. (1998). Cellular constituent and intercellular adhesion in Schistosoma mansoni granuloma: an ultrastructural study. Journal of the Egyptian Society of Parasitology 28, 169–181.Google ScholarPubMed
Matsuoka, M., Zhang, M. Y. and Tsukamoto, H. (1990). Sensitization of hepatic lipocytes by high-fat diet to stimulatory effects of Kupffer cell-derived factors: implication in alcoholic liver fibrogenesis. Hepatology 11, 173–182.CrossRefGoogle ScholarPubMed
Noel, W., Raes, G., Hassanzadeh Ghassabeh, G., De Baetselier, P. and Beschin, A. (2004). Alternatively activated macrophages during parasite infections. Trends in Parasitology 20, 126–133.CrossRefGoogle ScholarPubMed
Otsuka, M., Tsuchiya, S. and Aramaki, Y. (2004). Involvement of ERK, a MAP kinase, in the production of TGF-beta by macrophages treated with liposomes composed of phosphatidylserine. Biochemical and Biophysical Research Communications 324, 1400–1405.CrossRefGoogle Scholar
Pearce, E. J. and Macdonald, A. S. (2002). The immunobiology of schistosomiasis. Nature Reviews, Immunology 2, 499–511.CrossRefGoogle ScholarPubMed
Purps, O., Lahme, B., Gressner, A. M., Meindl-Beinker, N. M. and Dooley, S. (2007). Loss of TGF-beta dependent growth control during HSC transdifferentiation. Biochemical and Biophysical Research Communications 353, 841–847.CrossRefGoogle ScholarPubMed
Roberts, A. B., Sporn, M. B., Assoian, R. K., Smith, J. M., Roche, N. S., Wakefield, L. M., Heine, U. I., Liotta, L. A., Falanga, V., Kehrl, J. H. and Fauci, A. S. (1986). Transforming growth factor type beta: rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro. Proceedings of the National Academy of Sciences, USA 83, 4167–4171.CrossRefGoogle ScholarPubMed
Shi, Y. and Massague, J. (2003). Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113, 685–700.CrossRefGoogle ScholarPubMed
Song, E., Ouyang, N., Horbelt, M., Antus, B., Wang, M. and Exton, M. S. (2000). Influence of alternatively and classically activated macrophages on fibrogenic activities of human fibroblasts. Cellular Immunology 204, 19–28.CrossRefGoogle ScholarPubMed
Southgate, V. R., Rollinson, D., Tchuem Tchuente, L. A. and Hagan, P. (2005). Towards control of schistosomiasis in sub-Saharan Africa. Journal of Helminthology 79, 181–185.CrossRefGoogle ScholarPubMed
Takakura, R., Kiyohara, T., Murayama, Y., Miyazaki, Y., Miyoshi, Y., Shinomura, Y. and Matsuzawa, Y. (2002). Enhanced macrophage responsiveness to lipopolysaccharide and CD40 stimulation in a murine model of inflammatory bowel disease: IL-10-deficient mice. Inflammation Research 51, 409–415.CrossRefGoogle Scholar
Tsuboi, H., Hossain, K., Akhand, A. A., Takeda, K., Du, J., Rifa'i, M., Dai, Y., Hayakawa, A., Suzuki, H. and Nakashima, I. (2004). Paeoniflorin induces apoptosis of lymphocytes through a redox-linked mechanism. Journal of Cellular Biochemistry 93, 162–172.CrossRefGoogle ScholarPubMed
Varga, J., Rosenbloom, J. and Jimenez, S. A. (1987). Transforming growth factor beta (TGF beta) causes a persistent increase in steady-state amounts of type I and type III collagen and fibronectin mRNAs in normal human dermal fibroblasts. The Biochemical Journal 247, 597–604.CrossRefGoogle ScholarPubMed
Verrecchia, F., Chu, M. L. and Mauviel, A. (2001). Identification of novel TGF-beta/Smad gene targets in dermal fibroblasts using a combined cDNA microarray/promoter transactivation approach. The Journal of Biological Chemistry 276, 17058–17062.CrossRefGoogle ScholarPubMed
Vetter, M., Chen, Z. J., Chang, G. D., Che, D., Liu, S. and Chang, C. H. (2003). Cyclosporin A disrupts bradykinin signaling through superoxide. Hypertension 41, 1136–1142.CrossRefGoogle ScholarPubMed
Wynn, T. A. (2003). IL-13 effector functions. Annual Review of Immunology 21, 425–456.CrossRefGoogle ScholarPubMed
Li, X., Di, D., Fu, B., Tang, H., Zhang, C., Cai, W. and Wu, T. (1984). Study on the purification and application of Schistosoma japonicum antigen. Journal of Zhejiang University (Chinese) 13, 115–118.Google Scholar
Yamahara, J., Yamada, T., Kimura, H., Sawada, T. and Fujimura, H. (1982). [Biologically active principles of crude drugs. Anti-allergic principles of “Shoseiryu-to.” I. Effect on delayed-type allergy reaction]. Yakugaku zasshi: Journal of the Pharmaceutical Society of Japan 102, 881–886.CrossRefGoogle ScholarPubMed
Zhang, J. P., Zhang, M., Jin, C., Zhou, B., Xie, W. F., Guo, C., Zhang, C. and Qian, D. H. (2001). Matrine inhibits production and actions of fibrogenic cytokines released by mouse peritoneal macrophages. Acta Pharmacologica Sinica 22, 765–768.Google ScholarPubMed
Zhang, X., Yu, W. P., Gao, L., Wei, K. B., Ju, J. L. and Xu, J. Z. (2004). Effects of lipopolysaccharides stimulated Kupffer cells on activation of rat hepatic stellate cells. World Journal of Gastroenterology 10, 610–613.CrossRefGoogle ScholarPubMed