Multiple protective effects of melatonin against maternal cholestasis-induced oxidative stress and apoptosis in the rat fetal liver-placenta-maternal liver trio

Journal of Pineal Research

Volumn 43, Issue 2, 2007, Pages 130-139

  Perez, Maria J ^a   Castaño, Beatriz ^b   Gonzalez Buitrago, Jose M ^a   Marin, Jose J G ^b  

^a HOSPITAL UNIVERSITARIO DE SALAMANCA   (Spain)

^b UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

Antioxidant; Bax; Bile acid; Caspase; Glutathione; Pregnancy

Indexed keywords

ASCORBIC ACID; BILIVERDIN; CARRIER PROTEIN; CASPASE 3; GLUTATHIONE; GLUTATHIONE DISULFIDE; MELATONIN; OXIDOREDUCTASE; PROTEIN BAX; SILYMARIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL PROTECTION; CHOLESTASIS; COMMON BILE DUCT; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; FETUS LIVER; MATERNAL DISEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PEROXIDATION; PLACENTA; PREGNANCY; PROTEIN EXPRESSION; RAT; UPREGULATION;

ANIMALS; APOPTOSIS; BODY WEIGHT; CHOLESTASIS; FEMALE; GLUTATHIONE; LIPID PEROXIDATION; LIVER; MELATONIN; MOTHERS; ORGAN SIZE; ORGANIC ANION TRANSPORTERS, SODIUM-DEPENDENT; OXIDATIVE STRESS; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS; RATS; RATS, WISTAR; RNA, MESSENGER; SYMPORTERS;

EID: 34447534370     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2007.00453.x     Document Type: Article

References (55)

1. Faubion WA, Guicciardi ME, Miyoshi H et al. Toxic bile salts induce rodent hepatocyte apoptosis via direct activation of Fas. J Clin Invest 1999 103 : 137 145.
2. Yerushalmi B, Dahl R, Devereaux MW et al. Bile acid-induced rat hepatocyte apoptosis is inhibited by antioxidants and blockers of the mitochondrial permeability transition. Hepatology 2001 33 : 616 626.
3. Pascual MJ, Serrano MA, El-Mir MY et al. Relationship between asymptomatic hypercholanemia of pregnancy and progesterone metabolism. Clin Sci 2002 102 : 587 593.
4. Vallejo M, Briz O, Serrano MA et al. Potential role of trans-inhibition of the bile salt export pump by progesterone metabolites in the etiopathogenesis of intrahepatic cholestasis of pregnancy. J Hepatol 2006 44 : 1150 1157.
5. Lammert F, Marschall HU, Matern S. Intrahepatic cholestasis of pregnancy. Curr Treat Options Gastroenterol 2003 6 : 123 132.
6. Serrano MA, Brites D, Larena MG et al. Beneficial effect of ursodeoxycholic acid on alterations induced by cholestasis of pregnancy in bile acid transport across the human placenta. J Hepatol 1998 28 : 829 839.
7. Serrano MA, Macias RI, Vallejo M et al. Effect of ursodeoxycholic acid on the impairment induced by maternal cholestasis in the rat placenta-maternal liver tandem excretory pathway. J Pharmacol Exp Ther 2003 305 : 515 524.
8. Perez MJ, Macias RI, Duran C et al. Oxidative stress and apoptosis in fetal rat liver induced by maternal cholestasis. Protective effect of ursodeoxycholic acid. J Hepatol 2005 43 : 324 332.
9. Perez MJ, Macias RI, Marin JJ. Maternal cholestasis induces placental oxidative stress and apoptosis. Protective effect of ursodeoxycholic acid. Placenta 2006 27 : 34 41.
10. Briz O, Macias RI, Perez MJ et al. Excretion of fetal biliverdin by the rat placenta-maternal liver tandem. Am J Physiol Regul Integr Comp Physiol 2006 290 : R749 756.
11. Sedlak TW, Snyder SH. Bilirubin benefits: cellular protection by a biliverdin reductase antioxidant cycle. Pediatrics 2004 113 : 1776 1782.
12. Block G, Dietrich M, Norkus EP et al. Factors associated with oxidative stress in human populations. Am J Epidemiol 2002 156 : 274 285.
13. Leevy CM, Thompson A, Baker H. Vitamins and liver injury. Am J Clin Nutr 1970 23 : 493 499.
14. Wilson JX. Vitamin C transport in animals and plants. In : Vitamin C: Its Function and Biochemistry in Animals and Plants. Asard H, May JM, Smirnoff N, eds. BIOS Scientific Publishers, Oxford, UK, 1970 pp. 97 117.
15. Daruwala R, Song J, Koh WS et al. Cloning and functional characterization of the human sodium-dependent vitamin C transporters hSVCT1 and hSVCT2. FEBS Lett 1999 460 : 480 484.
16. Tsukaguchi H, Tokui T, Mackenzie B et al. A family of mammalian Na+-dependent L-ascorbic acid transporters. Nature 1999 399 : 70 75.
17. Ohta Y, Kongo M, Sasaki E et al. Protective effect of melatonin against alpha-naphthylisothiocyanate-induced liver injury in rats. J Pineal Res 2000 29 : 15 23.
18. Daniels WM, Reiter RJ, Melchiorri D et al. Melatonin counteracts lipid peroxidation induced by carbon tetrachloride but does not restore glucose-6 phosphatase activity. J Pineal Res 1995 19 : 1 6.
19. Lopez PM, Finana IT, De Agueda MC et al. Protective effect of melatonin against oxidative stress induced by ligature of extra-hepatic biliary duct in rats: comparison with the effect of S-adenosyl-L-methionine. J Pineal Res 2000 28 : 143 149.
20. Ohta Y, Imai Y, Matsura T et al. Successively postadministered melatonin prevents disruption of hepatic antioxidant status in rats with bile duct ligation. J Pineal Res 2005 39 : 367 374.
21. Tan DX, Chen LD, Poeggeler B et al. Melatonin: a potent, endogenous hydroxyl radical scavenger. Endocrine J 1993 1 : 57 60.
22. Allegra M, Reiter RJ, Tan DX et al. The chemistry of melatonin's interaction with reactive species. J Pineal Res 2003 34 : 1 10.
23. Rosen J, Than NN, Koch D et al. Interactions of melatonin and its metabolites with the ABTS cation radical: extension of the radical scavenger cascade and formation of a novel class of oxidation products, C2-substituted 3-indolinones. J Pineal Res 2006 41 : 374 381.
24. Tan DX, Manchester LC, Terron MP et al. One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species J Pineal Res 2007 42 : 28 42.
25. Rodriguez C, May JC, Sainz RM et al. Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 2004 36 : 1 9.
26. Tomas-Zapico C, Coto-Montes A. A proposed mechanism to explain the stimulatory effect of melatonin on antioxidative enzymes. J Pineal Res 2005 39 : 99 104.
27. Kuntz E. Silymarin in the Treatment of Liver Diseases. Falk Foundation e. V, Freiburg, 1998 pp. 8 50.
28. Gonzalez-Correa JA, de la Cruz JP, Gordillo J et al. Effects of silymarin MZ-80 on hepatic oxidative stress in rats with biliary obstruction. Pharmacology 2002 64 : 18 27.
29. Comoglio A, Tomasi A, Malandrino S et al. Scavenging effect of silipide, a new silybinphospholipid complex, on ethanol-derived free radicals. Biochem Pharmacol 1995 50 : 1313 1316.
30. Campos R, Garrido A, Guerra R et al. Silybin dihemisuccinate protects against glutathione depletion and lipid peroxidation induced by acetaminophen on rat liver. Planta Med 1989 55 : 417 419.
31. Bindoli A, Cavallini L, Silliprandi N. Inhibitory action of silymarin of lipid peroxide formation in rat liver mitochondria and microsomes. Biochem Pharmacol 1977 26 : 2405 2409.
32. Monte MJ, Morales AI, Arevalo M et al. Reversible impairment of neonatal hepatobiliary function by maternal cholestasis. Hepatology 1996 23 : 1208 1217.
33. Tietze F. Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 1969 27 : 502 522.
34. Griffith OW. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 1980 106 : 207 212.
35. Niehaus WG, Samuelsson B. Formation of malonaldehyde from phospholipid arachidonate during microsomal lipid peroxidation. Eur J Biochem 1968 6 : 126 130.
36. Markwell MA, Haas SM, Bieber LL et al. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 1978 87 : 206 210.
37. Hasegawa JI, Kamada S, Kamiike W et al. Involvement of CPP32/Yama (-like) proteases in Fas-mediated apoptosis. Cancer Res 1996 56 : 1713 1718.
38. Huang TJ, Trakshel GM, Maines MD. Detection of ten variants of biliverdin reductase in rat liver by two-dimensional gel electrophoresis. J Biol Chem 1989 264 : 7844 7849.
39. Okatani Y, Okamoto K, Hayashi K et al. Maternal-fetal transfer of melatonin in pregnant women near term. J Pineal Res 1998 25 : 129 134.
40. Reiter RJ. Melatonin: lowering the high price of free radicals. News Physiol Sci 2000 15 : 246 250.
41. Leon J, Acuna-Castroviejo D, Escames G et al. Melatonin mitigates mitochondrial malfunction. J Pineal Res 2005 38 : 1 9.
42. Ressmeyer AR, Mayo JC, Zelosko V et al. Antioxidant properties of the melatonin metabolite N-acetyl-5-methoxykynuramine (AMF): scavenging of free radicals and prevention of protein destruction. Redox Rep 2003 8 : 205 213.
43. Okatani Y, Wakatsuki A, Shinohara K et al. Melatonin protects against oxidative mitochondrial damage induced in rat placenta by ischemia reperfussion. J Pineal Res 2001 31 : 173 178.
44. Reyes H. The spectrum of liver and gastrointestinal disease seen in cholestasis of pregnancy. Gastroenterol Clin North Am 1992 21 : 905 921.
45. Edwards J, La Grange L, Wang M et al. Fetoprotectivity of the flavanolignan compound siliphos against ethanol-induced toxicity. Phytother Res 2000 14 : 517 521.
46. Muriel P, Moreno MG. Effects of silymarin and vitamins E and C on liver damage induced by prolonged biliary obstruction in the rat. Basic Clin Pharmacol Toxicol 2004 94 : 99 104.
47. Hagymasi K, Kocsis I, Lugasi A et al. Extrahepatic biliary obstruction: can silymarin protect liver function Phytother Res 2002 16 : S78 S80.
48. Maines MD, Ewing JF, Huang TJ et al. Nuclear localization of biliverdin reductase in the rat kidney: response to nephrotoxins that induce heme oxygenase-1. J Pharmacol Exp Ther 2001 296 : 1091 1097.
49. Sotiriou S, Gispert S, Cheng J et al. Ascorbic-acid transporter Slc23a1 is essential for vitamin C transport into the brain and for perinatal survival. Nat Med 2002 8 : 514 517.
50. Ohta Y, Kongo M, Sasaki E et al. Change in hepatic antioxidant defense system with liver injury development in rats with a single α- naphthylisothiocyanate intoxication. Toxicology 1999 139 : 265 275.
51. Kannan R, Stolz A, Ji Q, Prasad PD, Ganapathy V. Vitamin C transport in human lens epithelial cells: evidence for the presence of SVCT2. Exp Eye Res 2001 73 : 159 165.
52. Andrabi SA, Sayeed I, Siemen D et al. Direct inhibition of the mitochondrial permeability transition pore: a possible mechanism responsible for antiapoptotic effects of melatonin. FASEB J 2004 18 : 869 871.
53. Jou MJ, Peng TI, Reiter RJ et al. Visualization of the antioxidative effects of melatonin at the mitochondrial level during oxidative stress-induced apoptosis of rat brain astrocytes. J Pineal Res 2004 37 : 55 70.
54. Manna SK, Mukhopadhyay A, Van NT et al. Silymarin suppresses TNF-induced activation of NF-kB, c-Jun N-terminal kinase, and apoptosis. J Immunol 1999 163 : 6800 6809.
55. Varghese L, Agarwal C, Tyagi A et al. Silibinin efficacy against human hepatocellular carcinoma. Clin Cancer Res 2005 11 : 8441 8448.