Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-27T09:02:58.023Z Has data issue: false hasContentIssue false

The combined treatment of praziquantel with osteopontin immunoneutralization reduces liver damage in Schistosoma japonicum-infected mice

Published online by Cambridge University Press:  06 February 2012

BO-LIN CHEN
Affiliation:
Department of Gastroenterology, Xiangya Hospital, Central South University, Changsha, 410008, Hunan Province, China
GUI-YING ZHANG*
Affiliation:
Department of Gastroenterology, Xiangya Hospital, Central South University, Changsha, 410008, Hunan Province, China
SHI-PING WANG
Affiliation:
Department of Parasitology, College of Xiangya Basic Medicine, Central South University, Changsha, 410008, Hunan Province, China
QIAN LI
Affiliation:
Department of Gastroenterology, Xiangya Hospital, Central South University, Changsha, 410008, Hunan Province, China
MEI-HUA XU
Affiliation:
Department of Gastroenterology, Xiangya Hospital, Central South University, Changsha, 410008, Hunan Province, China
YUE-MING SHEN
Affiliation:
Department of Gastroenterology, Changsha Central Hospital, Changsha, 410004, Hunan Province, China
LU YAN
Affiliation:
Department of Gastroenterology, Xiangya Hospital, Central South University, Changsha, 410008, Hunan Province, China
HUAN GU
Affiliation:
Department of Gastroenterology, Xiangya Hospital, Central South University, Changsha, 410008, Hunan Province, China
JIA LI
Affiliation:
Department of Gastroenterology, Xiangya Hospital, Central South University, Changsha, 410008, Hunan Province, China
Y. L. HUANG
Affiliation:
Division of Phamaceutical Science, School of Pharmacy, University of Auckland, Private Bag 92019, Auckland, New Zealand
YI-BING MU
Affiliation:
Department of Gastroenterology, Xiangya Hospital, Central South University, Changsha, 410008, Hunan Province, China
*
*Corresponding author: Department of Gastroenterology, Xiangya Hospital, Central South University, Changsha, 410008, Hunan Province,China. Tel: +86 1387 3186462. Fax: +86 0731 84327321. E-mail: guiyingzhang@hotmail.com

Summary

The aim of this study was to evaluate the therapeutic effects of osteopontin neutralization treatment on schistosome-induced liver injury in BALB/C mice. We randomly divided 100 BALB/C mice into groups A, B, C, D and group E. Mice in all groups except group A were abdominally infected with schistosomal cercariae to induce a schistosomal hepatopathological model. Mice in group C, D and group E were respectively administered with praziquantel, praziquantel plus colchicine and praziquantel plus neutralizing osteopontin antibody. We extracted mouse liver tissues at 3 and 9 weeks after the ‘stool-eggs-positive’ day, observed liver histopathological changes by haematoxylin-eosin and Masson trichrome staining and detected the expression of osteopontin, alpha-smooth muscle actin (α-SMA) and transforming growth factor-beta (TGF-β1) by immunohistochemistry, RT-PCR and Western blot. We found that praziquantel plus neutralizing osteopontin antibody treatment significantly decreased the granuloma dimension, the percentage of collagen and the expression of osteopontin, α-SMA and TGF-β1 compared to praziquantel plus colchicine treatment in both the acute and chronic stage of schistosomal liver damage (P<0·05). So we believe that the combined regimen of osteopontin immunoneutralization and anti-helminthic treatment can reduce the granulomatous response and liver fibrosis during the schistosomal hepatopathologic course.

Type
Research Article
Copyright
Published by Cambridge University Press 2012

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

Anthony, B., Allen, J. T., Li, Y. S. and McManus, D. P. (2010). Hepatic stellate cells and parasite-induced liver fibrosis. Parasites & Vectors 3, 60. doi: 10.1186/1756-3305-3-60.CrossRefGoogle ScholarPubMed
Bartley, P. B., Ramm, G. A., Jones, M. K., Ruddell, R. G., Li, Y. and McManus, D. P. (2006). A contributory role for activated hepatic stellate cells in the dynamics of Schistosoma japonicum egg-induced fibrosis. International Journal for Parasitology 36, 9931001. doi: 10.1016/j.ijpara.2006.04.015.CrossRefGoogle ScholarPubMed
Bergquist, R. and Tanner, M. (2010). Controlling schistosomiasis in Southeast Asia: a tale of two countries. Advances in Parasitology 72, 109144. doi: 10.1016/S0065-308X(10)72005-4.CrossRefGoogle ScholarPubMed
Burke, M. L., Jones, M. K., Gobert, G. N., Li, Y. S., Ellis, M. K. and McManus, D. P. (2009). Immunopathogenesis of human schistosomiasis. Parasite Immunology 31, 163176. doi: 10.1111/j.1365-3024.2009.01098.x.CrossRefGoogle ScholarPubMed
Chabas, D. (2005). Osteopontin, a multi-faceted molecule. Medecine Sciences (Paris) 21, 832888. doi: 10.1051/medsci/20052110832.CrossRefGoogle ScholarPubMed
Chapadeiro, E. and Pitanga, L. C. (1996). On the reversal of schistosomiasis hepatic fibrosis after specific therapy. Histopathologic study. Revista da Sociedade Brasileira de Medicina Tropical 30, 5356.CrossRefGoogle Scholar
Chen, B. L., Zhang, G. Y., Yuan, W. J., Wang, S. P., Shen, Y. M., Yan, L., Gu, H. and Li, J. (2011). Osteopontin expression is associated with hepatopathologic changes in Schistosoma japonicum–infected mice. World Journal of Gastroenterology 17, 50755082.CrossRefGoogle ScholarPubMed
Coutinho, H. M., Acosta, L. P., Wu, H. W., McGarvey, S. T., Su, L., Langdon, G. C., Jiz, M. A., Jarilla, B., Olveda, R. M., Friedman, J. F. and Kurtis, J. D. (2007). Th2 cytokines are associated with persistent hepatic fibrosis in human Schistosoma japonicum infection. The Journal of Infectious Diseases 195, 288295. doi: 10.1086/510313.CrossRefGoogle ScholarPubMed
Doenhoff, M. J., Kusel, J. R., Coles, G. C. and Cioli, D. (2002). Resistance of Schistosoma mansoni to praziquantel: is there a problem? Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 465469.CrossRefGoogle ScholarPubMed
Fornari, A., Rhoden, E. L., Zettler, C. G., Ribeiro, E. P. and Rhoden, C. R. (2011). Effects of the chronic use of finasteride and doxazosin mesylate on the histomorphometric characteristics of the prostate: experimental study in rats. International Urology and Nephrology 43, 3945. doi: 10.1007/s11255-010-9770-3.CrossRefGoogle ScholarPubMed
Gabele, E., Brenner, D. A. and Rippe, R. A. (2003). Liver fibrosis: signals leading to the amplification of the fibrogenic hepatic stellate cell. Frontiers in Bioscience 8, 6977. doi: 10.2741/887.Google Scholar
Garjito, T. A., Sudomo, M., Abdullah, , Dahlan, M. and Nurwidayati, A. (2008). Schistosomiasis in Indonesia: past and present. Parasitology International 57, 277280. doi: 10.1016/j.parint.2008.04.008.CrossRefGoogle ScholarPubMed
Giachelli, C. M. and Steitz, S. (2000). Osteopontin: A versatile regulator of inflammation and biomineralization. Matrix Biology 19, 615622. doi: 10.1016/S0945-053X(00)00108-6.CrossRefGoogle Scholar
Gryseels, B., Polman, K., Clerinx, J. and Kestens, L. (2006). Human schistosomiasis. The Lancet 368, 11061118. doi: 10.1016/S0140-6736(06)69440-3.CrossRefGoogle ScholarPubMed
Kiefer, F. W., Zeyda, M., Gollinger, K., Pfau, B., Neuhofer, A., Weichhart, T., Säemann, M. D., Geyeregger, R., Schlederer, M., Kenner, L. and Stulnig, T. M. (2010). Neutralization of osteopontin inhibits obesity-induced inflammation and insulin resistance. Diabetes 59, 935946. doi: 10.2337/db09-0404.CrossRefGoogle ScholarPubMed
Lenga, Y., Koh, A., Perera, A. S., McCulloch, C. A., Sodek, J. and Zohar, R. (2008). Osteopontin expression is required for myofibroblast differentiation. Circulation Research 102, 319327. doi: 10.1161/circresaha.107.160408.CrossRefGoogle ScholarPubMed
Lorena, D., Darby, I. A., Gadeau, A. P., Leen, L. L., Rittling, S., Porto, L. C., Rosenbaum, J. and Desmoulière, A. (2006). Osteopontin expression in normal and fibrotic liver. Altered liver healing in osteopontin-deficient mice. Journal of Hepatology 44, 383390. doi:10.1016/j.jhep.2005.07.024.CrossRefGoogle ScholarPubMed
McManus, D. P., Li, Y., Gray, D. J. and Ross, A. G. (2009). Conquering ‘snail fever': schistosomiasis and its control in China. Expert Review of Anti-infective Therapy 7, 473485. doi: 10.1586/eri.09.17.CrossRefGoogle ScholarPubMed
Moreira, R. K. (2007). Hepatic stellate cells and liver fibrosis. Archives of Pathology & Laboratory Medicine 131, 17281734.CrossRefGoogle ScholarPubMed
Morimoto, J., Kon, S., Matsui, Y. and Uede, T. (2010). Osteopontin; as a target molecule for the treatment of inflammatory diseases. Current Drug Targets 11, 494505.CrossRefGoogle ScholarPubMed
O'Regan, A. and Berman, J. S. (2000). Osteopontin: A key cytokine in cell mediated and granulomatous inflammation. International Journal of Experimental Pathology 81, 373390. doi: 10.1046/j.1365-2613.2000.00163.x.CrossRefGoogle ScholarPubMed
Paiva, L. A., Maya-Monteiro, C. M., Bandeira-Melo, C., Silva, P. M., El-Cheikh, M. C., Teodoro, A. J., Borojevic, R., Perez, S. A. and Bozza, P. T. (2010). Interplay of cysteinyl leukotrienes and TGF-β in the activation of hepatic stellate cells from Schistosoma mansoni granulomas. Biochimica et Biophysica Acta 1801, 13411348. doi: 10.1016/j.bbalip.2010.08.014.CrossRefGoogle ScholarPubMed
Ramaiah, S. K. and Rittling, S. (2008). Pathophysiological role of osteopontin in hepatic inflammation, toxicity, and cancer. Toxicological Sciences 103, 413. doi: 10.1093/toxsci/kfm246.CrossRefGoogle ScholarPubMed
Reeves, H. L. and Friedman, S. L. (2002). Activation of hepatic stellate cells – a key issue in liver fibrosis. Frontiers in Bioscience 7, d808d826. doi: 10.2741/reeves.CrossRefGoogle ScholarPubMed
Shimada, M., Kirinoki, M., Shimizu, K., Kato-Hayashi, N., Chigusa, Y., Kitikoon, V., Pongsasakulchoti, P. and Matsuda, H. (2010). Characteristics of granuloma formation and liver fibrosis in murine schistosomiasis mekongi: a morphological comparison between Schistosoma mekongi and S. japonicum infection. Parasitology 137, 17811789. doi: 10.1017/S0031182010000806.CrossRefGoogle ScholarPubMed
Singh, M., Foster, C. R., Dalal, S. and Singh, K. (2010). Osteopontin: role in extracellular matrix deposition and myocardial remodeling post-MI. Journal of Molecular and Cellular Cardiology 48, 538543. doi: 10.1016/j.yjmcc.2009.06.015.CrossRefGoogle ScholarPubMed
Ueno, T., Miyazaki, E., Ando, M., Nureki, S. and Kumamoto, T. (2010). Osteopontin levels are elevated in patients with eosinophilic pneumonia. Respirology 15, 11111121. doi: 10.1111/j.1440-1843.2010.01825.x.CrossRefGoogle ScholarPubMed
von Lichtenberg, F. V. (1962). Host response to eggs of S. mansoni. I. Granuloma formation in the unsensitized laboratory mouse. The American Journal of Pathology 41, 711731.Google ScholarPubMed
Wada, W., Kuwano, H., Hasegawa, Y. and Kojima, I. (2004). The dependence of transforming growth factor-beta-induced collagen production on autocrine factor activin A in hepatic stellate cells. Endocrinology 145, 27532759. doi: 10.1210/en.2003-1663.CrossRefGoogle ScholarPubMed
Xu, X., Wen, X., Chi, Y., He, L., Zhou, S., Wang, X., Zhao, J., Liu, F. and Su, C. (2010). Activation-induced T helper cell death contributes to Th1/Th2 polarization following murine Schistosoma japonicum infection. Journal of Biomedicine and Biotechnology 2010, 202397. doi: 10.1155/2010/202397.CrossRefGoogle ScholarPubMed