Anti-inflammatory/anti-fibrotic effects of the hepatoprotective silymarin and the schistosomicide praziquantel against Schistosoma mansoni-induced liver fibrosis

Parasites and Vectors

Volumn 5, Issue 1, 2012, Pages

  El Lakkany, Naglaa M ^a   Hammam, Olfat A ^b   El Maadawy, Walaa H ^a   Badawy, Afkar A ^b   Ain Shoka, Afaf A ^c   Ebeid, Fatma A ^a  

^a Giza   (Egypt)

^b Theodor Bilharz Research Institute   (Egypt)

^c CAIRO UNIVERSITY   (Egypt)

Author keywords

hydroxyproline; liver fibrosis; mast cells; matrix metalloproteinase 2; praziquantel; Schistosoma mansoni; silymarin; transforming growth factor 1

Indexed keywords

GELATINASE A; GLUTATHIONE; HYDROXYPROLINE; PRAZIQUANTEL; SILYMARIN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIFIBROTIC ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DRUG ACTIVITY; GRANULOMA; HEPATITIS; HISTOPATHOLOGY; LIVER FIBROSIS; LIVER FUNCTION TEST; LIVER PROTECTION; MALE; MAST CELL; MORBIDITY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SCHISTOSOMA MANSONI; TISSUE MICROARRAY; WORM;

ANIMALS; DRUG THERAPY, COMBINATION; HYDROXYPROLINE; LIVER; LIVER CIRRHOSIS; LIVER FUNCTION TESTS; MALE; MAST CELLS; MATRIX METALLOPROTEINASE 2; MICE; PARASITE EGG COUNT; PRAZIQUANTEL; PROTECTIVE AGENTS; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SCHISTOSOMICIDES; SILYMARIN; TRANSFORMING GROWTH FACTOR BETA1;

MUS; SCHISTOSOMA MANSONI; SILYBUM MARIANUM;

EID: 84855605794     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/1756-3305-5-9     Document Type: Article

References (55)

1. Temporal expression of chemokines dictates the hepatic inflammatory infiltrate in a murine model of schistosomiasis. Burke ML, McManus DP, Ramm GA, Duke M, Li Y, Jones MK, Gobert GN, PLOS Negl Trop Dis 2010 4 598 10.1371/journal.pntd.0000598 20161726
2. Role of cytokines in the formation and downregulation of hepatic circumoval granulomas and hepatic fibrosis in Schistosoma mansoni infected mice. Cheever AW, Jankovic D, Yap GS, Kullberg MC, Sher A, Wynn TA, Mem Inst Oswaldo Cruz 1998 93 25 32 9921320
3. Gene expression of transforming growth factor 1 and extracellular matrix proteins in murine Schistosoma mansoni infection. Kresina TF, He Q, Degli Esposti S, Zern MA, Gastroenterology 1994 107 773 780 10.1016/0016-5085(94) 90126-0 8076764 (Pubitemid 24265525)
4. Dynamic changes of type I, II and IV collagen synthesis and distribution of collagen-producing cells in carbon tetrachloride induced rat liver fibrosis. Du WD, Zhang YE, Zhai WR, Zhou XM, World J Gastroenterol 1999 5 397 403 11819476
5. Effects of vitamin E on experimental hepatic fibrosis in rats. Wang YF, Li QF, Wang H, Mao Q, Wu CQ, World J Gastroenterol 1998 4 157
6. Evaluation of role of mast cells in the development of liver fibrosis using mast cell-deficient rats and mice. Sugihara A, Tsujimura T, Fujita Y, Nakata Y, Terada N, J Hepatol 1999 30 859 867 10.1016/S0168-8278(99)80140-8 10365813 (Pubitemid 29248987)
7. Mast cell infiltration and chemokine expression in progressive renal disease. Jones SE, Kelly DJ, Cox AJ, Zhang Y, Gow RM, Gilbert RE, Kidney Int 2003 64 906 913 10.1046/j.1523-1755.2003.00183.x 12911540 (Pubitemid 37013826)
8. 4induced hepatic fibrosis. Jeong D, Lee G, Jeong W, Do S, Yang H, Yuan D, Park H, Kim K, Jeong K, World J Gastroenterol 2005 11 1141 1148 15754394 (Pubitemid 40352999)
9. Dual expression of matrix metalloproteinase-2 and membrane-type-1-matrix metalloproteinase in fibrotic human livers. Takahara T, Furui K, Yata Y, Jin B, Zhang LP, Nambu S, Sato H, Seiki M, Watanabe A, Hepatology 1997 26 1521 1529 10.1002/hep.510260620 9397993 (Pubitemid 27520018)
10. Treatment of hepatic fibrosis: almost there. Albanis E, Safadi R, Friedman S, Curr Gastroenterol Rep 2003 5 48 56 10.1007/s11894-003-0009-7 12530948 (Pubitemid 38899271)
11. Drugs for the control of parasitic diseases: current status and development in schistosomiasis. Fenwick A, Savioli L, Engels D, Robert Bergquist N, Todd MH, Trends Parasitol 2003 19 509 515 10.1016/j.pt.2003.09.005 14580962 (Pubitemid 37329660)
12. Association of the therapeutic activity of praziquantel with the reversal of Symmers' fibrosis induced by Schistosoma mansoni. Homeida MA, el Tom I, Nash T, Bennett JL, Am J Trop Med Hyg 1991 45 360 365 1928571
13. Biochemical bases of the pharmacological action of the flavonoid silymarin and of its structural isomer silibinin. Valenzuela A, Garrido A, Biol Res 1994 27 105 112 8640239 (Pubitemid 24257808)
14. Effect of silybin on the hepatic microsomal drug metabolizing enzyme system in the rat. Down WH, Chasseaud LF, Grundy RK, Arzneim Forsch/Drug Res 1974 24 1986 1988
15. Effects of silibinin and of a synthetic analogue on isolated rat hepatic stellate cells and myofibroblasts. Fuchs EC, Weyhenmeyer R, Weiner OH, Arzneim Forsch/Drug Res 1997 47 1383 1387 (Pubitemid 28015506)
16. Silymarin treatment reduces granuloma and hepatic fibrosis in experimental schistosomiasis. Mata-Santos HA, Lino FG, Rocha CC, Paiva CN, Castelo Branco MT, Pyrrho Ados S, Parasitol Res 2010 107 1429 1434 10.1007/s00436-010-2014-8 20694562
17. Silymarin protects against liver damage in BALB/c mice exposed to Fumonisin B1 despite increasing accumulation of free sphingoid bases. He Q, Kim J, Sharma RP, Toxicol Sci 2004 80 335 342 10.1093/toxsci/kfh148 15103051 (Pubitemid 39136388)
18. Praziquantel, a new broad-spectrum antischistosomal agent. Gonnert R, Andrews P, Z Parasitenkd 1977 52 129 150 10.1007/BF00389899 410178 (Pubitemid 8155044)
19. Laboratory cultivation of schistosome vector snails and maintenance of schistosome life cycles. Liang YS, John BI, Boyd DA, Proceeding of the 1st Sino-American Symposium 1987 1 34 48
20. An improved perfusion technique for recovering adult schistosomes from laboratory animals. Duvall RH, De Witt WB, Am J Trop Med Hyg 1967 16 483 486 4952149
21. Conditions affecting the accuracy of potassium hydroxide digestion techniques for counting Schistosoma mansoni eggs in tissues. Cheever AW, Bull World Health Organ 1968 39 328 331 4881073
22. New approach to the screening of drugs in experimental schistosomiasis mansoni in mice. Pellegrino J, Oliveira CA, Faria J, Cunha AS, Am J Trop Med Hyg 1962 11 201 215 14484966
23. Host response to eggs of Schistosoma mansoni. I. Granuloma formation in the sensitized laboratory mouse. Von Lichtenberg FC, Am J Pathol 1962 41 711 731 13930476
24. Tissue sulfhydryl groups. Ellman G, Arch Biochem Biophys 1959 88 70 77
25. The determination of hydroxyproline in tissue and protein samples containing small proportions of this amino acid. Woessner JF, Arch Biochem Biophys 1961 93 440 447 10.1016/0003-9861(61)90291-0 13786180
26. Protein A, avidin and biotin in immunohistochemistry. Hsu SM, Raine L, J Histochem Cytochem 1981 29 1349 1353 10.1177/29.11.6172466 6172466
27. Detection of hepatocellular carcinomas and dysplastic nodules in cirrhotic liver: accuracy of ultrasonography in transplant patients. Kim CK, Lim JH, Lee WJ, J Ultrasound Med 2001 20 99 104 11211142
28. Prognostic values of matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-2 expression in bladder cancer. Kanayama H, Yokota K, Kurokawa Y, Murakami Y, Nishitani M, Kagawa S, Cancer 1998 82 1359 1366 10.1002/(SICI)1097-0142(19980401)82:7<1359::AID-CNCR20>3.0.CO;2-4 9529029 (Pubitemid 28155399)
29. A toluidine blue method for demonstrating mast cells. Churukian CJ, Schenk EA, J Histopathol 1981 4 85 86 (Pubitemid 11045411)
30. Comparative analysis of mast cell count in normal oral mouse and oral pyogenic granuloma. Kamel R, Dahiya P, Palaskar S, Shetty VP, J Clin Exp Dent 2011 3 1 4
31. Schistosomiasis and hepatic fibrosis regression. Andrade ZA, Acta Tropica 2008 108 79 82 10.1016/j.actatropica.2008.04.003 18501873
32. Murine schistosomiasis as a model for human schistosomiasis mansoni: similarities and discrepancies. Abdul-Ghani RA, Hassan AA, Parasitol Res 2010 107 1 8 10.1007/s00436-010-1855-5 20369252
33. Antioxidant and hepatoprotective effects of Ginkgo biloba phytosomes in carbon tetrachloride-induced liver injury in rodents. Naik SR, Panda VS, Liver Int 2007 27 393 399 10.1111/j.1478-3231.2007.01463.x 17355462 (Pubitemid 46416631)
34. Therapy with bone marrow cells reduces liver alterations in mice chronically infected by Schistosoma mansoni. Oliveira SA, Souza BS, Guimaraes-Ferreira CA, Barreto ES, Souza SC, Freitas LA, Ribeiro-Dos-Santos R, Soares MB, Braz J Med Biol Res 2009 42 812 815 10.1590/S0100-879X2009000900007 19738986
35. Preventive effect of malotilate on carbon tetrachloride-induced liver damage and collagen accumulation in the rat. Ala-kokko L, Stenback F, Ryhanen L, Biochem J 1987 246 503 509 2825640 (Pubitemid 17121888)
36. Dynamics of hepatic connective tissue matrix constituents during murine Schistosoma mansoni infection. El-Meneza S, Olds GR, Kresina TF, Mahmoud AAF, Hepatology 1989 9 50 56 10.1002/hep.1840090108 2535698 (Pubitemid 19046301)
37. Dynamics of collagen, MMP and TIMP gene expression during the granulomatous, fibrotic process induced by Schistosoma mansoni eggs. Singh KP, Gerard HC, Hudson AP, Boros DL, Ann Trop Med Parasitol 2004 98 581 593 10.1179/000349804225021316 15324465 (Pubitemid 39215513)
38. Imbalance of pro- and antifibrogenic genes and bile duct injury in murine Schistosoma mansoni infection-induced liver fibrosis. Loebermann M, Sombetzki M, Langner C, Fuchsbichler A, Gumhold J, Silbert D, Riebold D, Holtfreter M, Fickert P, Nizze H, Trauner M, Reisinger EC, Trop Med Int Health 2009 14 1418 1425 10.1111/j.1365-3156.2009.02387.x 19747186
39. Silybin and silymarin-new and emerging applications in medicine. Gazák R, Walterová D, Kren V, Curr Med Chem 2007 14 315 338 10.2174/092986707779941159 17305535
40. Inhibitory effects of silymarin on hepatic fibrosis induced by dimethylnitrosamine: experiment with rats. Zhao XY, Wang BE, Wang TL, Li XM, Zhonghua Yi Xue Za Zhi 2006 86 2563 2566 17198567
41. Pirfenidone inhibits carbon tetrachloride- and albumin complex-induced liver fibrosis in rodents by preventing activation of hepatic stellate Cells. Zhao XY, Zeng X, Li XM, Wang TL, Wang BE, Clin Exp Pharmacol Physiol 2009 36 963 968 10.1111/j.1440-1681.2009.05194.x 19413596
42. Silybin, a component of sylimarin, exerts anti-inflammatory and anti-fibrogenic effects on human hepatic stellate cells. Trappoliere M, Caligiuri A, Schmid M, Bertolani C, Failli P, Vizzutti F, Novo E, di Manzano C, Marra F, Loguercio C, Pinzani M, J Hepatol 2009 50 1102 1111 10.1016/j.jhep.2009.02.023 19398228
43. Mast cells. Weber S, Kruger-Krasagakes S, Grabbe J, Zuberbier T, Czarnetzki BM, Int J Dermatol 1995 34 1 10 10.1111/j.1365-4362.1995.tb04366.x 7896475
44. Deleterious effects of silymarin on the expression of genes controlling endothelial nitric oxide synthase activity in carbon tetrachloride-treated rat livers. Cho YK, Yun JW, Park JH, Kim HJ, Park DI, Sohn CI, Jeon WK, Kim BI, Jin W, Kwon YH, Shin MK, Yoo TM, Kang JH, Park CS, Life Sci 2009 85 281 290 10.1016/j.lfs.2009.06.001 19527736
45. Silymarin modulates the oxidant-antioxidant imbalance during diethylnitrosamine induced oxidative stress in rats. Pradeep K, Mohan CV, Gobianand K, Karthikeyan S, Eur J Pharmacol 2007 560 110 116 10.1016/j.ejphar.2006.12.023 17300777 (Pubitemid 46341309)
46. Silymarin protection against major reactive oxygen species released by environmental toxins: exogenous H2O2 exposure in erythrocytes. Kiruthiga PV, Shafreen RB, Pandian SK, Devi KP, Basic Clin Pharmacol Toxicol 2007 100 414 419 10.1111/j.1742-7843.2007.00069.x 17516996 (Pubitemid 46776391)
47. Use of praziquantel for clinical treatment and morbidity control of schistosomiasis japonica in China: a review of 30 years' experience. Chen MG, Acta Tropica 2005 96 168 176 10.1016/j.actatropica.2005.07.011 16125657 (Pubitemid 41463747)
48. Reversibility of schistosomal periportal thickening/fibrosis after praziquantel therapy: a twenty-six month follow-up study in Ethiopia. Berhe N, Myrvang B, Gundersen SG, Am J Trop Med Hyg 2008 78 228 234 18256420 (Pubitemid 351844555)
49. Evidence for a long-term effect of a single dose of praziquantel on Schistosoma mansoni-induced hepatosplenic lesions in northern Uganda. Frenzel K, Grigull L, Odongo-Aginya E, Ndugwa CM, Loroni-Lakwo T, Schweigmann U, Vester U, Spannbrucker N, Doehring E, Am J Trop Med Hyg 1999 60 927 931 10403322 (Pubitemid 29296216)
50. Expression of matrix metalloproteinases and their inhibitors during the resorption of schistosome egg-induced fibrosis in praziquantel-treated mice. Singh KP, Gerard HC, Hudson AP, Boros DL, Immunology 2004 111 343 352 10.1111/j.0019-2805.2004.01817.x 15009436 (Pubitemid 38365758)
51. New insight into the antifibrotic effects of praziquantel on mice in infection with Schistosoma japonicum. Liang Y, Luo J, Yuan Q, Zheng D, Liu Y, Shi L, Chen A, Ren Y, Sun K, Sun Y, Wang Y, Zhang Z, PLOS One 2011 6 20247 10.1371/journal.pone.0020247 21629648
52. Silymarin protects against acute ethanol-induced hepatotoxicity in mice. Song Z, Deaciuc I, Song M, Lee DY, Liu Y, Ji X, Mc Clain C, Alcohol Clin Exp Res 2006 30 407 413 10.1111/j.1530-0277.2006.00063.x 16499481 (Pubitemid 43341346)
53. Impact of treatment with praziquantel, silymarin and/or beta-glucan on pathophysiological markers of liver damage and fibrosis in mice infected with Mesocestoides vogae (Cestoda) tetrathyridia. Velebn S, Hrckova G, Kogan G, J Helminthol 2008 82 211 219 18394210
54. Immunostimulatory effect of Silybum marianum (milk thistle) extract. Wilasrusmee C, Kittur S, Shah G, Siddiqui J, Bruch D, Wilasrusmee S, Kittur DS, Med Sci Monit 2002 8 R439 443 12444368
55. Milk thistle for the treatment of liver disease: A systematic review and meta-analysis. Jacobs BP, Dennehy C, Ramirez G, Sapp J, Lawrence VA, Am J Med 2002 113 506 515 10.1016/S0002-9343(02)01244-5 12427501 (Pubitemid 35335804)