Therapeutic value of melatonin post-treatment on CCl4-induced fibrotic rat liver

Canadian Journal of Physiology and Pharmacology

Volumn 94, Issue 2, 2016, Pages 119-130

  Mortezaee, Keywan ^a   Sabbaghziarani, Fatemeh ^a   Omidi, Ameneh ^a   Dehpour, Ahmad Reza ^a   Omidi, Negar ^b   Ghasemi, Soudabeh ^a   Pasbakhsh, Parichehr ^a   Kashani, Iraj Ragerdi ^a  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Carbon tetrachloride; Collagen; Fibrosis; Matrix metalloproteinase; Melatonin; Post treatment; Transforming growth factor 1

Indexed keywords

ALANINE AMINOTRANSFERASE; ALBUMIN; ASPARTATE AMINOTRANSFERASE; CARBON TETRACHLORIDE; COLLAGEN; COLLAGENASE 3; FAT DROPLET; GELATINASE B; HYDROXYPROLINE; MELATONIN; PHOSPHATE BUFFERED SALINE; PROTEIN BAX; PROTEIN BCL 2; TRANSFORMING GROWTH FACTOR BETA1;

ADULT; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALBUMIN BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CARBON TETRACHLORIDE-INDUCED LIVER FIBROSIS; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; GLYCOGEN ANALYSIS; IMMUNOFLUORESCENCE; LIVER TISSUE; MALE; MEMBRANE MICROPARTICLE; NONHUMAN; OIL RED O STAINING; OUTCOME ASSESSMENT; PERIODIC ACID SCHIFF STAIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; STAINING;

EID: 85027568993     PISSN: 00084212     EISSN: 12057541     Source Type: Journal    
DOI: 10.1139/cjpp-2015-0266     Document Type: Article

References (56)

1. Ali, S.A., Faddah, L., Abdel-Baky, A., and Bayoumi, A. 2010. Protective effect of l-carnitine and coenzyme Q10 on CCL4-induced liver injury in rats. Sci. Pharm. 78(4): 881-96.
2. Benyon, R.C., and Arthur, M. 2001. Extracellular matrix degradation and the role of hepatic stellate cells. Semin. Liver. Dis. 21(3): 373-84.
3. Bhandarkar, M.R., and Khan, A. 2004. Antihepatotoxic effect of Nymphaea stellata willd., against carbon tetrachloride-induced hepatic damage in albino rats. J. Ethnopharmacol. 91(1): 61-64.
4. Candelario-Jalil, E., Mohammed-Al-Dalain, S., Fernandez, O., Menendez, S., Perez-Davison, G., Merino, N., et al. 2001. Oxidative preconditioning affords protection against carbon tetrachloride-induced glycogen depletion and oxidative stress in rats. J. Appl. Toxicol. 21(4): 297-301.
5. Carvalho, A.B., Quintanilha, L.F., Dias, J.V., Paredes, B.D., Mannheimer, E.G., Carvalho, F.G., et al. 2008. Bone marrow multipotent mesenchymal stromal cells do not reduce fibrosis or improve function in a rat model of severe chronic liver injury. Stem Cells, 26(5): 1307-14.
6. Chen, R.J., Wu, H.H., and Wang, Y.J. 2015. Strategies to prevent and reverse liver fibrosis in humans and laboratory animals. Arch. Toxicol. 1-24. doi: 10.1007/j.Archt.2015.05.012.
7. Crespo, I., San-Miguel, B., Fernandez, A., de Urbina, J.O., Gonzalez-Gallego, J., and Tunon, M.J. 2015. Melatonin limits the expression of profibrogenic genes and ameliorates the progression of hepatic fibrosis in mice. Transl. Res. 165(2): 346-57.
8. Ding, J., Yu, J., Wang, C., Hu, W., Li, D., Luo, Y., et al. 2005. Ginkgo biloba extract alleviates liver fibrosis induced by CCl4 in rats. Liver. Int. 25(6): 1224-32.
9. Drobnik, J., and Dabrowski, R. 1998. Pinealectomy-induced elevation of collagen content in the intact skin is suppressed by melatonin application. Cytobios, 100(393): 49-55.
10. El-Samaligy, M.S., Afifi, N.N., and Mahmoud, E.A. 2006. Evaluation of hybrid liposomesencapsulated silymarin regarding physical stability and in vivo performance. Int. J. Pharm. 319(1): 121-29.
11. Fahmy, S.R. 2015. Anti-fibrotic effect of Holothuria arenicola extract against bile duct ligation in rats. BMC. Complement. Altern. Med. 15(1): 533-37.
12. Galli, A., Crabb, D., Price, D., Ceni, E., Salzano, R., Surrenti, C., et al. 2000. Peroxisome proliferator-activated receptor γ transcriptional regulation is involved in platelet-derived growth factor–induced proliferation of human hepatic stellate cells. Hepatology, 31(1): 101-08.
13. Guo, X.L., Liang, B., Wang, X.W., Fan, F.G., Jin, J., Lan, R., et al. 2013. Glycyrrhizic acid attenuates CCl4-induced hepatocyte apoptosis in rats via a p53-mediated pathway. World. J. Gastroenterol. 19(24): 3781-91.
14. Guzman, R.E., and Solter, P.F. 1999. Hepatic oxidative stress following prolonged sublethal microcystin LR exposure. Toxicol. Pathol. 27(5): 582-88.
15. Hardjo, M., Miyazaki, M., Sakaguchi, M., Masaka, T., Ibrahim, S., Kataoka, K., et al. 2009. Suppression of carbon tetrachloride-induced liver fibrosis by transplantation of a clonal mesenchymal stem cell line derived from rat bone marrow. Cell. Transplant. 18(1): 89-99.
16. Hayden, M.S., and Ghosh, S. 2011. NF-κB in immunobiology. Cell. Res. 21(2): 223-44.
17. Higashiyama, R., Inagaki, Y., Hong, Y.Y., Kushida, M., Nakao, S., Niioka, M., et al. 2007. Bone marrow–derived cells express matrix metalloproteinases and contribute to regression of liver fibrosis in mice. Hepatology, 45(1): 213-22.
18. Hong, R.T., Xu, J.M., and Mei, Q. 2009. Melatonin ameliorates experimental hepatic fibrosis induced by carbon tetrachloride in rats. World. J. Gastroenterol. 15(12): 1452-58.
19. Huang, G.J., Deng, J.S., Chiu, C.S., Liao, J.C., Hsieh, W.T., Sheu, M.J., et al. 2011. Hispolon protects against acute liver damage in the rat by inhibiting lipid peroxidation, proinflammatory Cytokine, and Oxidative stress and downregulating the expressions of iNOS, COX-2, and MMP-9. Evid. Based. Complement. Alternat. Med. 2012: 714-24.
20. Jaswal, A., and Shukla, S. 2015. Therapeutic efficacy of Nigella sativa Linn. seed extract against CCl4 induced hepatic injury in wistar rats. Indian. J. Exp. Biol. 53(1): 44-50.
21. Jonsson, J.R., Clouston, A.D., Ando, Y., Kelemen, L.I., Horn, M.J., Adamson, M.D., et al. 2001. Angiotensin-converting enzyme inhibition attenuates the progression of rat hepatic fibrosis. Gastroenterology, 121(1): 148-55.
22. Kaimori, A., Potter, J., Kaimori, J.y., Wang, C., Mezey, E., and Koteish, A. 2007. Transforming growth factor-β1 induces an epithelial-to-mesenchymal transition state in mouse hepatocytes in vitro. J. Biol. Chem. 282(30): 22089-101.
23. Kanzler, S., Lohse, A.W., Keil, A., Henninger, J., Dienes, H.P., Schirmacher, P., et al. 1999. TGF-β1 in liver fibrosis: an inducible transgenic mouse model to study liver fibrogenesis. Am. J. Physiol. 276(4): 1059-68.
24. Kus, I., Ogeturk, M., Oner, H., Sahin, S., Yekeler, H., and Sarsilmaz, M. 2005. Protective effects of melatonin against carbon tetrachloride-induced hepatotoxicity in rats: a light microscopic and biochemical study. Cell. Biochem. Funct. 23(3): 169-74.
25. Lee, H., Jeong, H., Park, S., Yoo, W., Choi, S., Choi, K., et al. 2015. Fusion protein of retinol-binding protein and albumin domain III reduces liver fibrosis. EMBO. Mol. Med. 7(6):819-30.
26. Ling, H., Roux, E., Hempel, D., Tao, J., Smith, M., Lonning, S., et al. 2013. Transforming growth factor β neutralization ameliorates pre-existing hepatic fibrosis and reduces cholangiocarcinoma in thioacetamide-treated rats. PLoS One, 8(1): e54499.
27. Malavolta, M., Piacenza, F., Basso, A., Giacconi, R., Costarelli, L., and Mocchegiani, E. 2015. Serum copper to zinc ratio: relationship with aging and health status. Mech. Ageing. Dev. doi: 10.1016/j.mad.2015.01.004.
28. Mazepa, R., Cuevas, M., Collado, P., and Gonzalez-Gallego, J. 1999. Melatonin increases muscle and liver glycogen content in nonexercised and exercised rats. Life. Sci. 66(2): 153-60.
29. Messner, M., Huether, G., Lorf, T., Ramadori, G., and Schworer, H. 2001. Presence of melatonin in the human hepatobiliary-gastrointestinal tract. Life. Sci. 69(5): 543-51.
30. Mormone, E., George, J., and Nieto, N. 2011. Molecular pathogenesis of hepatic fibrosis and current therapeutic approaches. Chem. Biol. Interact. 193(3): 225-31.
31. Mu, Y., Liu, P., Du, G., Du, J., Wang, G., Long, A., et al. 2009. Action mechanism of Yi Guan Jian Decoction on CCl 4 induced cirrhosis in rats. J. Ethnopharmacol. 121(1): 35-42.
32. Musso, G., Cassader, M., Bo, S., De Michieli, F., and Gambino, R. 2013. Sterol regulatory element-binding factor 2 (SREBF-2) predicts 7-year NAFLD incidence and severity of liver disease and lipoprotein and glucose dysmetabolism. Diabetes, 62(4): 1109-20.
33. Nakamura, H., Hirata, K., Yamashiro, K., Hiranuma, K., Shibata, K., Higashi, K., et al. 1994. Increase of hepatic mRNAS of profilin, actin and extracellular matrix proteins after carbon tetrachloride treatment and partial hepatectomy in rats. Biochem. Biophys. Res. Commun. 198(2): 568-73.
34. Ohta, Y., Kongo, M., Sasaki, E., Nishida, K., and Ishiguro, I. 2000. Therapeutic effect of melatonin on carbon tetrachloride-induced acute liver injury in rats. J. Pineal. Res. 28(2): 119-26.
35. Ohuchi, E., Imai, K., Fujii, Y., Sato, H., Seiki, M., and Okada, Y. 1997. Membrane type 1 matrix metalloproteinase digests interstitial collagens and other extracellular matrix macromolecules. J. Biol. Chem. 272(4): 2446-51.
36. Oyagi, S., Hirose, M., Kojima, M., Okuyama, M., Kawase, M., Nakamura, T., et al. 2006. Therapeutic effect of transplanting HGF-treated bone marrow mesenchymal cells into CCl 4-injured rats. J. Hepatol. 44(4): 742-48.
37. Sagor, A.T., Chowdhury, M.R., Tabassum, N., Hossain, H., Rahman, M., and Alam, A. 2015. Supplementation of fresh ucche (Momordica charantia L. var. muricata Willd) prevented oxidative stress, fibrosis and hepatic damage in CCl4 treated rats. BMC. Complement. Altern. Med. 15(1):115. doi: 10.1186/s12906-015-0636-1.
38. Salazar-Montes, A.M., Hernandez-Ortega, L.D., Lucano-Landeros, M.S., and Armendariz-Borunda, J. 2015. New gene therapy strategies for hepatic fibrosis. World. J. Gastroenterol. 21(13): 3813-25.
39. San-Miguel, B., Crespo, I., Sanchez, D.I, Gonzalez-Fernandez, B., Ortiz de Urbina, J.J., Tunon, M.J., et al. 2015. Melatonin inhibits autophagy and endoplasmic reticulum stress in mice with carbon tetrachloride-induced fibrosis. J. Pineal. Res. doi: 10.1111/jpi.12247.
40. Shaker, M., Houssen, M., Abo-Hashem, E., and Ibrahim, T. 2009. Comparison of vitamin E, L-carnitine and melatonin in ameliorating carbon tetrachloride and diabetes induced hepatic oxidative stress. J. Physiol. Biochem. 65(3): 225-33.
41. She, M., Deng, X., Guo, Z., Laudon, M., Hu, Z., Liao, D., et al. 2009. NEU-P11, a novel melatonin agonist, inhibits weight gain and improves insulin sensitivity in high-fat/highsucrose-fed rats. Pharmacol. Res. 59(4): 248-53.
42. Shieh, J.M., Wu, H.T., Cheng, K.C., and Cheng, J.T. 2009. Melatonin ameliorates high fat diet-induced diabetes and stimulates glycogen synthesis via a PKCζ-Akt-GSK3β pathway in hepatic cells. J. Pineal. Res. 47(4): 339-44.
43. Sola, S., Ma, X., Castro, R.E., Kren, B.T., Steer, C.J, and Rodrigues, C.M. 2003. Ursodeoxycholic acid modulates E2F-1 and p53 expression through a caspase-independent mechanism in transforming growth factor β1-induced apoptosis of rat hepatocytes. J. Biol. Chem. 278(49): 48831-38.
44. Tahan, G., Akin, H., Aydogan, F., Ramadan, S.S., Yapicier, O., Tarcin, O., et al. 2010. Melatonin ameliorates liver fibrosis induced by bile-duct ligation in rats. Can. J. Surg. 53(5): 313-18.
45. Tarantino, G., Conca, P., Riccio, A., Tarantino, M., Di Minno, M.N., Chianese, D., et al. 2008. Enhanced serum concentrations of transforming growth factor-beta1 in simple fatty liver: is it really benign?. J. Transl. Med. 6(72): 49.
46. Tarantino, G., and Finelli, C. 2013. What about non-alcoholic fatty liver disease as a new criterion to define metabolic syndrome?. World. J. Gastroenterol. 19(22): 3375-84.
47. Tarantino, G., Savastano, S., Capone, D., and Colao, A. 2011a. Spleen: A new role for an old player? World. J. Gastroenterol. 17(33): 3776-84.
48. Tarantino, G., Scopacasa, F., Colao, A., Capone, D., Tarantino, M., Grimaldi, E., et al. 2011b. Serum Bcl-2 concentrations in overweight-obese subjects with nonalcoholic fatty liver disease. World. J. Gastroenterol. 17(48): 5280-8.
49. Terai, S., Ishikawa, T., Omori, K., Aoyama, K., Marumoto, Y., Urata, Y., et al. 2006. Improved liver function in patients with liver cirrhosis after autologous bone marrow cell infusion therapy. Stem Cells, 24(10): 2292-98.
50. Tien, Y.C., Liao, J.C., Chiu, C.S., Huang, T.H., Huang, C.Y., Chang, W.T., et al. 2011. Esculetin ameliorates carbon tetrachloride-mediated hepatic apoptosis in rats. Int. J. Mol. Sci. 12(6): 4053-67.
51. Tu, X., Zheng, X., Li, H., Cao, Z., Chang, H., Luan, S., et al. 2015. microRNA-30 protect against CCl4-induced liver fibrosis by attenuating TGF-β signaling in hepatic stellate cells. Toxicol. Sci. 146(1):157-69.
52. Wang, M.Y., Anderson, G., Nowicki, D., and Jensen, J. 2008. Hepatic protection by noni fruit juice against CCl4-induced chronic liver damage in female SD rats. Plant. Foods. Hum. Nutr. 63(3): 141-45.
53. Wang, H., Wei, W., Wang, N.P., Gui, S.Y., Wu, L., Sun, W.Y., et al. 2005. Melatonin ameliorates carbon tetrachloride-induced hepatic fibrogenesis in rats via inhibition of oxidative stress. Life. Sci. 77(15): 1902-15.
54. Weber, L.W., Boll, M., and Stampfl, A. 2003. Hepatotoxicity and mechanism of action of haloalkanes: carbon tetrachloride as a toxicological model. Crit. Rev. Toxicol. 33(2): 105-36.
55. Yang, H., Zhao, L.F., Zhao, Z.F., Wang, Y., Zhao, J.J., and Zhang, L. 2012. Heme oxygenase-1 prevents liver fibrosis in rats by regulating the expression of PPARγ and NF-κB. World. J. Gastroenterol. 18(14): 1680-88.
56. Zavodnik, L., Zavodnik, I., Lapshina, E., Belonovskaya, E., Martinchik, D., Kravchuk, R., et al. 2005. Protective effects of melatonin against carbon tetrachloride hepatotoxicity in rats. Cell. Biochem. Funct. 23(5): 353-59.