Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-24T09:38:36.067Z Has data issue: false hasContentIssue false
  • English
  • Français

Praziquantel and liposomized glucan-treatment modulated liver fibrogenesis and mastocytosis in mice infected with Mesocestoides vogae (M. corti, Cestoda) tetrathyridia

Published online by Cambridge University Press:  25 November 2005

G. HRČKOVA ,
S. VELEBNÝ ,
Z. DAXNEROVÁ  and
P. SOLÁR
G. HRČKOVA
Affiliation:
Parasitological Institute of the Slovak Academy of Sciences, Hlinkova 3, 04001 Košice, Slovak Republic
S. VELEBNÝ
Affiliation:
Parasitological Institute of the Slovak Academy of Sciences, Hlinkova 3, 04001 Košice, Slovak Republic
Z. DAXNEROVÁ
Affiliation:
Institute of Biology and Ecology, Faculty of Science, University of P.J. šafárik, Moyzesova 64, 040 00 Košice, Slovak Republic
P. SOLÁR
Affiliation:
Institute of Biology and Ecology, Faculty of Science, University of P.J. šafárik, Moyzesova 64, 040 00 Košice, Slovak Republic
Get access Rights & Permissions [Opens in a new window]

Abstract

β–glucans are immunomodulators able to activate innate immunity and to potentiate acquired immune reactions. We investigated the impact of co-administration of liposomized β-glucan on the larvicidal effect of the anthelmintic praziquantel (PZQ) in the livers and peritoneal cavities in mice infected with Mesocestoides vogae (M. corti). Also, within 2 weeks following therapy (up to day 29 p.i.) we examined collagen synthesis in the livers of mice by means of biochemical determination of hydroxyprolin concentration, total mast cell counts and cell proliferative capacity using immunohistochemical and radiometrical methods. After co-administration of liposomized glucan (LG) and PZQ efficacy (%) was significantly higher than after treatment with either compond alone, particularly in the peritoneal cavity compared to the liver. In comparison with the control, more intense collagenesis was found in the B-liver parts (high intensity of infection) and lowering of collagen content in the A-parts (very weak infection). This effect was strongest after LG treatment and co-administration of PZQ abolished the pro-fibrotic effect of LG. In all groups, mast cell counts were higher in the B-liver parts than in the A-parts and the dynamics of mastocytosis was profoundly modulated following therapy. Whereas the effect of PZQ was only moderate, early and very strong onset was seen after LG treatment. Administration of PZQ supressed LG induced-elevation of mast cells counts in both liver parts. Using DNA S-phase markers (BrdU and 3H-thymidine) the proliferative capacity was shown to be associated with several kinds of liver cells. Therapy significantly stimulated [3H]-thymidine incorporation (cell proliferation) only in the A-parts over that in control, the most after LG administration. In summary (i) the anthelmintic effect of PZQ could be enhanced after simultaneous administration of the immunomodulator β-glucan entrapped in a liposomal carrier, (ii) intense mastocytosis seen after treatment with LG seems to have a direct role in the glucan′s pro-fibrotic activity and can be abolished after co-administration of PZQ in a time-dependent manner, (iii) the pattern of cell proliferation indicates that in the case of PZQ treatment, the reparative processes of liver parenchyma are enhanced in an inverse correlation with the intensity of infection.

Keywords

Mesocestoides vogaepraziquantelβ-glucanliverhydroxyprolinefibrogenesismast cellscell proliferation
Type
Research Article
Information
Parasitology , Volume 132 , Issue 4 , April 2006 , pp. 581 - 594
Copyright
2005 Cambridge University Press

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

Amiot, F., Vuong, P., Defontaines, M., Pater, C., Dautry, F. and Liance, M. ( 1999). Secondary alveolar echinococcosis in lymphotoxin-α and tumor necrosis factor-α deficient mice: exacerbation of Echinococcus multilocularis larval growth is associated with cellular changes in the periparasitic granuloma. Parasite Immunology 21, 475–483.CrossRefGoogle Scholar
Andrews, P., Thomas, H., Pohlke, R. and Seubert, J. ( 1983). Praziquantel. Medical Research Reviews 66, 147–200.CrossRefGoogle Scholar
Bohn, J. A. and BeMiller, J. N. ( 1995). (1-3)-beta-D-glucans as biological response modifiers: A review of structure-functional activity relationships. Carbohydrate Polymers 28, 3–14.CrossRefGoogle Scholar
Brown, G. D. and Gordon, S. ( 2003). Fungal β-glucans and mammalian immunity. Immunity 19, 311–315.CrossRefGoogle Scholar
Burt, A. D. ( 1993). Cellular and molecular aspects of hepatic fibrosis. Journal of Pathology 170, 105–114.CrossRefGoogle Scholar
Chernin, J., Miller, H. R. P., Newlands, G. F. J. and McLaren, D. J. ( 1988). Proteinase phenotypes and fixation properties of rat mast cells in parasitic lesions caused by Mesocestoides corti: selective and site-specific recruitment of mast cell subsets. Parasite Immunology 10, 433–442.CrossRefGoogle Scholar
Cioli, D. and Pica-Mattoccia, L. ( 2003). Praziqauntel. Parasitology Research 90, 3–9.Google Scholar
Cook, R. M., Asworth, R. F. and Chernin, J. ( 1988). Cytotoxic activity of rat granulocytes against Mesocestoides corti. Parasite Immunology 10, 97–109.CrossRefGoogle Scholar
Ditteová, G., Velebný, S. and Hrčkova, G. ( 2003 a). The dose dependent effect of glucan on worm burden and pathology of mice infected with Mesocestoides corti (M. vogae) tetrathyridia. Helminthologia 40, 123–130.Google Scholar
Ditteová, G., Velebný, S. and Hrčkova, G. ( 2003 b). Modulation of liver fibrosis and pathophysiological changes in mice infected with Mesocestoides corti (M. vogae) after administration of glucan and liposomized glucan in combination with vitamin C. Journal of Helminthology 77, 219–226.Google Scholar
Etges, F. J. ( 1991). The proliferative tetrathyridium of Mesocestoides vogae sp.n. (Cestoda). Journal of Helminthological Society of Washington 58, 181–185.Google Scholar
Feger, F., Varadaradjalou, S., Gao, Z., Abraham, S. N. and Arock, M. ( 2002). The role of mast cells in host defense and their subversion by bacterial pathogens. Trends in Immunology 23, 151–158.CrossRefGoogle Scholar
Foreman, J. C. ( 1994). Mast cells and basophil leucocytes. In Textbook of Immunopharmacology. ( ed. Dale, M. M., Foreman, J. C. and Fan, T.-P. D.), pp. 21–34. Blackwell Scientific Publications, Oxford.
Garbuzenko, E., Nagler, A., Pickholtz, D., Gillery, P., Reich, R., Maquart, F. X. and Levi-Schaffer, F. ( 2002). Human mast cells stimulate fibroblast proliferation, collagen synthesis and lattice contraction: A direct role for mast cells in skin fibrosis. Clinical and Experimental Allergy 32, 237–246.CrossRefGoogle Scholar
Gemmell, M. A. and Parmeter, S. N. ( 1983). Effects of praziquantel against eggs of Taenia hydatigena and protoscolices and metacestodes of Echinoccocus granulosus. Veterinary Medicine Review 1, 3–9.Google Scholar
Gregoriadis, G. ( 1988). Fate of injected liposomes: observations on entrapped solute retention, vesicle clearance and tissue distribution in vivo. In Liposomes as Drug Carriers. ( ed. Gregoriadis, G.), pp. 3–18. John Wiley & Sons Ltd., Chichester.
Guerret, S., Vuitton, D. A., Liance, M., Pater, C. and Carbillet, J. P. ( 1998). Echinococcus multilocularis: relationship between susceptibility/resistance and liver fibrogenesis in experimental mice. Parasitology Research 84, 657–667.CrossRefGoogle Scholar
Henz, B. M., Maurer, M., Lippert, U., Worm, M. and Babina, M. ( 2001). Mast cells as initiators of immunity and host defense. Experimental Dermatology 10, 1–10.CrossRefGoogle Scholar
Hrčkova, G. and Velebný, S. ( 1994). Studies on the effects of free and liposomized albendazole on infection of Mesocestoides corti tetrathyridia (Cestoda: Cyclophyllidea) in laboratory mice. Comparative Biochemistry and Physiology 107C, 71–77.Google Scholar
Hrčkova, G. and Velebný, S. ( 1997). Effects of praziquantel and liposome-incorporated praziquantel on peritoneal macrophage activation in mice infected with Mesocestoides corti tetrathyridia (Cestoda). Parasitology 114, 475–482.CrossRefGoogle Scholar
Hrčkova, G. and Velebný, S. ( 2001). Treatment of Toxocara canis infection in mice with liposome-incorporated benzimidazole carbamates and immunomodulator glucan. Journal of Helminthology 75, 141–146.Google Scholar
Jenkins, P., Dixon, J. B., Rakha, N. K. and Carter, S. D. ( 1990). Regulation of macrophage-mediated larvicidal activity in Echinococcus granulosus and Mesocestoides corti (Cestoda) infection in mice. Parasitology 100, 309–315.CrossRefGoogle Scholar
Kogan, G. ( 2000). (1-3, 1-6)-β-D-glucans of yeasts and fungi and their biological activity. In Studies in Natural Products Chemistry23 ( ed. Ur-Rahman, A.), pp. 107–152. Elsevier, The Netherlands.CrossRef
Kougias, P., Wei, D., Rice, P. J., Ensley, H. E., Kalbfleisch, J., Williams, D. L. and Browder, W. I. ( 2001). Normal human fibroblasts express pattern recognition receptor for fungal (1-3)-β-D-glucans. Infection and Immunity 69, 3933–3938.CrossRefGoogle Scholar
Lee, T. D. G., Swieter, M. and Befus, A. D. ( 1986). Mast cell responses to helminth infection. Parasitology Today 2, 186–191.CrossRefGoogle Scholar
Levi-Schaffer, F. R., Kelav-Appelbaum, R. and Rubinchik, E. ( 1995). Human foreskin mast cell viability and functional activity is maintained ex vivo by coculture with fibroblasts. Cellular Immunology 162, 211–216.CrossRefGoogle Scholar
Lortat-Jacob, H., Baltzer, F., Desmouliere, A., Peyrol, S. and Grimaud, J. A. ( 1997). Lobular – but not periovular – inhibition of collagen deposition in the liver of S. mansoni infected mice using interferon-γ. Journal of Hepatology 26, 894–903.Google Scholar
Mahin, D. T. and Lofberg, R. T. ( 1966). A simplified method of sample preparation for determination of tritium, carbon-14 or sulfur-35 in blood or tissue by liquid scintillation counting. Analytical Biochemistry 16, 500–509.CrossRefGoogle Scholar
Matsumoto, K. and Nakamura, T. ( 1997). Hepatocyte growth factor as a tissue organiser for organogenesis and regeneration. Biochemical and Biophysical Research Communications 239, 639–644.CrossRefGoogle Scholar
Miyagawa, M., Katsuta, O., Tsuchitani, M. and Yoshikawa, K. ( 1996). Measurement of replicative DNA synthesis (RDS) by a 5-bromo-2′-deoxyuridine (BrdU) labelling technique for detection of hepatocyte proliferation. Journal of Veterinary Medical Science 59, 45–49.Google Scholar
Montero, R. and Ostrosky, P. ( 1997). Genotoxic activity of praziquantel. Mutation Research 387, 123–139.CrossRefGoogle Scholar
Novak, M. ( 1977). Efficacy of a new cesticide, praziquantel, against larval Mesocestoides corti and Taenia crassiceps in mice. Journal of Parasitology 63, 949–950.CrossRefGoogle Scholar
Pollacco, S., Nicholas, W. L., Mitchell, G. F. and Stewart, A. CH. ( 1978). T-cell dependent collagenous encapsulating response in the mouse liver to Mesocestoides corti (Cestoda). International Journal for Parasitology 8, 457–462.CrossRefGoogle Scholar
Puxeddu, I., Piliponsky, A. M., Bachelet, I. and Levi-Schaffer, F. ( 2003). Cells in focus. Mast cells in allergy and beyond. International Journal of Biochemistry and Cell Biology 35, 1601–1607.CrossRefGoogle Scholar
Sellge, G., Lorentz, A., Gebhardt, T., Levi-Schaffer, F., Bektas, H., Manns, M., Schuppan, D. and Bischoff, S. C. ( 2004). Human intestinal fibroblasts prevent apoptosis in human intestinal mast cells by a mechanism independent of stem cell factor, IL-3, IL-4, and nerve growth factor. Journal of Immunology 172, 260–267.CrossRefGoogle Scholar
Singh, K. P., Gerard, H. C., Hudson, A. P. and Boros, D. L. ( 2004). Expression of matrix metalloproteinases and their inhibitors during the resorption of schistosome egg-induced fibrosis in praziquantel-treated mice. Immunology 111, 343–352.CrossRefGoogle Scholar
Sotelo, J., Torres, B., Rubio-Donnadieu, F., Escobedo, F. and Rodriguez-Carbajal, J. ( 1985). Praziquantel in the treatment of neurocysticercosis: long-term follow up. Neurology 35, 752–755.CrossRefGoogle Scholar
Specht, D. and Voge, M. ( 1965). Asexual multiplication of Mesocestoides tetrathyridia in laboratory animals. Journal of Parasitology 51, 268–272.CrossRefGoogle Scholar
Specht, D. and Widmer, E. A. ( 1972). Response of mouse liver to infection with tetrathyridia of Mesocestoides (Cestoda). Journal of Parasitology 58, 431–437.CrossRefGoogle Scholar
Starke, W. A. and Oaks, J. A. ( 1999). Hymenolepis diminuta: Praziquantel removal of adult tapeworms is followed by apoptotic down-regulation of mucosal mastocytosis. Experimental Parasitology 92, 171–181.CrossRefGoogle Scholar
Steiner, K., Garbe, A., Diekmann, H. W. and Novak, H. ( 1976). The fate of praziquantel in the organism. I: Pharmacokinetics in animals. European Journal of Drug Metabolism and Pharmacokinetic 1, 85–95.Google Scholar
Stone, P. J. ( 2000). Potential use of collagen and elastin degradation markers for monitoring liver fibrosis in schistosomiasis. Acta Tropica 77, 97–99.CrossRefGoogle Scholar
Szebeni, J. ( 1998). The interaction of liposomes with the complement system. Critical Reviews in Therapeutic Drug Carrier Systems 15, 57–88.CrossRefGoogle Scholar
Takeishi, T., Hirano, K., Kobayashi, T., Hasegawa, G., Hatakeyama, K. and Naito, M. ( 1999). The role of Kupffer cells in liver regeneration. Archives of Histology and Cytology 62, 413–422.CrossRefGoogle Scholar
Thomas, H. and Gőnnert, R. ( 1978). The efficacy of praziquantel against experimental cysticercosis and hydatidosis. Zeitschrift für Parasitenkunde 55, 165–179.CrossRefGoogle Scholar
Thomas, H., Andrews, P. and Melhorn, H. ( 1982). New results on the effect of praziquantel in experimental cysticercosis. American Journal of Tropical Medicine and Hygiene 31, 803–810.CrossRefGoogle Scholar
Toplu, N., Yildiz, K. and Tunay, R. ( 2004). Massive cystic tetrathyridiosis in a dog. Journal for Small Animal Practice 45, 410–412.CrossRefGoogle Scholar
Urrea-París, M. A., Moreno, M. J., Casado, N. and Rodriguez-Caabeiro, F. ( 1999). Echinococcus granulosus: praziquantel treatment against the metacestode stage. Parasitology Research 85, 999–1006.CrossRefGoogle Scholar
Velebný, S., Hrčkova, G., Tomašovičová, O. and Dubinský, P. ( 1997). Toxocara canis in mice: Are liposomes and immunomodulator able to enhance the larvicidal effect of the anthelmintics? Helminthologia 34, 147–153.Google Scholar
Wakshull, E., Brunke-Reese, D., Lindermuth, J., Fisette, L., Nathans, R. S., Crowley, J. J., Tufts, J. C., Zimmerman, J., Mackin, W. and Adams, D. S. ( 1999). PGG-glucan, a soluble β-(1,3)-glucan, enhances the oxidative burst response, microbicidal activity, and activates an NF-κB-like factor in human PMN: Evidence for a glycosphingolipid β-(1,3)-glucan receptor. Immunopharmacology 41, 89–107.CrossRefGoogle Scholar
Wei, D., Zhang, L., Williams, D. L. and Browder, W. ( 2002). Glucan stimulates human dermal fibroblast collagen biosynthesis through a nuclear factor-1 dependent mechanism. Wound Repair and Regeneration 10, 161–168.CrossRefGoogle Scholar
White, T. R., Thompson, R. C. A., Penhale, W. J. and Chihara, G. ( 1988). The effect of lentinan on the resistance of mice to Mesocestoides corti. Parasitology Research 74, 563–568.CrossRefGoogle Scholar
WORLD HEALTH ORGANIZATION ( 1995). WHO Model Prescribing Information. Drugs used at Parasitic Diseases. WHO, Geneva.
Williams, D. L., Mueller, A. and Browder, W. ( 1996). Glucan-based macrophage stimulators. A review of their anti-infective potential. Clinical Immunotherapy 5, 392–399.CrossRefGoogle Scholar
Woessner, J. F. ( 1961). The determination of hydroxyproline in tissue and protein samples containing small proportion of this amino acid. Archives of Biochemistry and Biophysics 93, 440–447.CrossRefGoogle Scholar
Wu, J. and Zern, M. A. ( 2000). Hepatic stellate cells: a target for the treatment of liver fibrosis. Journal of Gastroenterology 35, 665–672.CrossRefGoogle Scholar