14-Deoxyandrographolide targets adenylate cyclase and prevents ethanol-induced liver injury through constitutive NOS dependent reduced redox signaling in rats

Food and Chemical Toxicology

Volumn 59, Issue , 2013, Pages 236-248

  Mandal, Samir ^a   Nelson, Vinod K ^b   Mukhopadhyay, Sibabrata ^a   Bandhopadhyay, Sukdeb ^a   Maganti, Lakshmi ^a   Ghoshal, Nanda ^a   Sen, Gargi ^a   Biswas, Tuli ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^b NATIONAL INSTITUTE OF PHARMACEUTICAL EDUCATION AND RESEARCH   (India)

Author keywords

Glutamylcysteine synthetase; 14 Deoxyandrographolide; Adenylate cyclase; Chronic alcoholism; Constitutive nitric oxide synthase; Hepatotoxicity

Indexed keywords

14 DEOXYANDROGRAPHOLIDE; ADENYLATE CYCLASE; ADENYLATE CYCLASE ACTIVATOR; CALMODULIN; CAVEOLIN 1; GLUTAMATE CYSTEINE LIGASE; NITRIC OXIDE SYNTHASE; UNCLASSIFIED DRUG;

ALCOHOL LIVER CIRRHOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; LIVER TOXICITY; MOLECULAR DOCKING; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION;

Γ-GLUTAMYLCYSTEINE SYNTHETASE; 14-DEOXYANDROGRAPHOLIDE; ADENYLATE CYCLASE; CHRONIC ALCOHOLISM; CONSTITUTIVE NITRIC OXIDE SYNTHASE; HEPATOTOXICITY;

ADENYLATE CYCLASE; ANDROGRAPHIS; ANIMALS; ANTIOXIDANTS; APOPTOSIS; CELLS, CULTURED; CYCLIC AMP; DITERPENES; FEMALE; GLUTAMATE-CYSTEINE LIGASE; HEP G2 CELLS; HUMANS; LIVER; LIVER DISEASES, ALCOHOLIC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; OXIDATION-REDUCTION; OXIDATIVE STRESS; PLANT LEAVES; RATS; RATS, SPRAGUE-DAWLEY; SECOND MESSENGER SYSTEMS;

EID: 84880118404     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2013.05.056     Document Type: Article

References (66)

1. Barve A., Khan R., Marsano L., Ravindra K.V., McClain C. Treatment of alcoholic liver disease. Annal. Hepatol. 2008, 7:5-15.
2. Bernstein F.C., Koetzle T.F., Williams G.J., Meyer E.F., Brice M.D., Rodgers J.R., Kennard O., Shimanouchi T., Tasumi M. The protein data bank: a computer-based archival file for macromolecular structures. J. Mol. Biol. 1977, 112:535-542.
3. Bhattacharyya K., Kar T., Bocelli G., Cantoni A., Pramanick S., Banerjee S., Mukhopadhyay S. Redetermination of 14-deoxyandrographolide. Acta Cryst. 2005, E61:o2743-o2745.
4. Canbay A., Friedman S., Gores G.J. Apoptosis: the nexus of liver injury and fibrosis. Hepatology 2004, 39:273-278.
5. Cerius2, Version 4.10, Accelrys, 2006. San Diego, CA, USA.
6. Chao C.Y., Lii C.K., Tsai I.T., Li C.C., Liu K.L., Tsai C.W., Chen H.W. Andrographolide inhibits ICAM-1 expression and NF-κB activation in TNF-α-treated EA.hy926 cells. J. Agric. Food Chem. 2011, 59:5263-5271.
7. Chen J.H., Hsiao G., Lee A.R., Wu C.C., Yen M.H. Andrographolide suppresses endothelial cell apoptosis via activation of phosphatidyl inositol-3-kinase/Akt pathway. Biochem. Pharmacol. 2004, 67:1337-1345.
8. Cottart C.H., Do L., Blanc M.C., Vaubourdolle M., Descamps G., Durand D., Galen F.X., Clot J.P. Hepatoprotective effect of endogenous nitric oxide during ischemia-reperfusion in the rat. Hepatology 1999, 29:809-813.
9. Day C.P. Treatment of alcoholic liver disease. Liver Transpl. 2007, 13:S69-S75.
10. De Meijer V.E., Sverdlov D.Y., Popov Y., Le H.D., Meisel J.A., Nose V., Schuppan D., Puder M. Broad-spectrum matrix metalloproteinase inhibition curbs inflammation and liver injury but aggravates experimental liver fibrosis in mice. PLoS ONE 2010, 5:e11256-e11268.
11. Dudzinski D.M., Michel T. Life history of eNOS: partners and pathways. Cardiovasc. Res. 2007, 75:247-260.
12. Fleming I., Busse R. Signal transduction of eNOS activation. Cardiovasc. Res. 1999, 43:532-541.
13. French S.W. The role of hypoxia in the pathogenesis of alcoholic liver disease. Hepatol. Res. 2004, 29:69-74.
14. Garcia-Cardena G., Martasek P., Masters B.S.S., Skidd P.M., Couet J., Li S., Lisanti M.P., Sessa W.C. Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the NOS caveolin binding domain in vivo. J. Biol. Chem. 1997, 272:25437-25440.
15. Gobejishvili L., Barve S., Joshi-Barve S., Uriarte S., Song Z., McClain C. Chronic ethanol-mediated decrease in cAMP primes macrophages to enhanced LPS-inducible NF-κB activity and TNF expression: relevance to alcoholic liver disease. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 291:G681-G688.
16. Gouillon Z.Q., Miyamoto K., Donohue T.M., Wan Y.J., French B.A., Nagao Y., Fu P., Reitz R.C., Hagbjork A., Yap C., Yuan Q.X., Ingelman-Sundberg M., French S.W. Role of CYP2E1 in the pathogenesis of alcoholic liver disease: modifications by cAMP and ubiquitin-proteasome pathway. Front. Biosci. 1999, 4:A16-A25.
17. Gramenzi A., Caputo F., Biselli M., Kuria F., Loggi E., Andreone P., Bernardi M. Alcoholic liver disease - pathophysiological aspects and risk factors. Aliment. Pharmacol. Ther. 2006, 24:1151-1161.
18. Greenberg S.S., Ouyang J., Zhao X., Xie J., Wang J., Giles T.D. Interaction of ethanol with inducible nitric oxide synthase messenger RNA and protein: direct effects on autacoids and endotoxin in vivo. J. Pharmacol. Exp. Ther. 1997, 282:1044-1054.
19. Gumpricht E., Dahl R., Yerushalmi B., Devereaux M.W., Sokol R.J. Nitric oxide ameliorates hydrophobic bile acid-induced apoptosis in isolated rat hepatocytes by non-mitochondrial pathways. J. Biol. Chem. 2002, 277:25823-25830.
20. Ha H.L., Shin H.J., Feitelson M.A., Yu D.Y. Oxidative stress and antioxidants in hepatic pathogenesis. World J. Gastroenterol. 2010, 16:6035-6043.
21. Harris M.B., Blackstone M.A., Sood S.G., Li C., Goolsby J.M., Venema V.J., Kemp B.E., Venema R.C. Acute activation and phosphorylation of endothelial nitric oxide synthase by HMG-CoA reductase inhibitors. Am. J. Physiol. Heart. Circ. Physiol. 2004, 287:H560-H566.
22. Insight II, Version 4.1, Accelrys, 2007. San Diego, CA, USA.
23. Insel P.A., Ostrom R.S. Forskolin as a tool for examining adenylyl cyclase expression, regulation, and G protein signaling. Cell. Mol. Neurobiol. 2003, 23:305-315.
24. James S.J., Rose S., Melnyk S., Jernigan S., Blossom S., Pavliv O., Gaylor D.W. Cellular and mitochondrial glutathione redox imbalance in lymphoblastoid cells derived from children with autism. FASEB J. 2009, 23:2374-2383.
25. Jimenez-Lopez J.M., Carrasco M.P., Segovia J.L., Marco C. Resistance of hepG2 cells against the adverse effects of ethanol related to neutral lipids and phospholipids metabolism. Biochem. Pharma. 2002, 63:1485-1490.
26. Jones G., Willett P., Glen R.C., Leach A.R., Taylor R. Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 1997, 267:727-748.
27. Ju H., Zou R., Venema V.J., Venema R.C. Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J. Biol. Chem. 1997, 272:18522-18525.
28. Kapil A., Koul I.B., Banerjee S.K., Gupta B.D. Antihepatotoxic effects of major diterpenoid constituents of Andrographis paniculata. Biochem. Pharmacol. 1993, 46:182-185.
29. Koukoulitsa C., Zervou M., Demetzos C., Mavromoustakos T. Comparative docking studies of labdane-type diterpenes with forskolin at the active site of adenylyl cyclase. Bioorg. Med. Chem. 2008, 16:8237-8243.
30. Kumar R.A., Sridevi K., Kumar N.V., Nanduri S., Rajagopal S. Anticancer and immunostimulatory compounds from Andrographis paniculata. J. Ethnopharmacol. 2004, 92:291-295.
31. Lee F.Y.J., Li Y., Zhu H., Yang S., Lin H.Z., Trush M., Diehl A.M. Tumor necrosis factor increases mitochondrial oxidant production and induces expression of uncoupling protein-2 in the regenerating mic liver. Hepatology 1999, 29:677-687.
32. Leite F., O'Brien S., Sylte M.J., Page T., Atapattu D., Czuprynski C.J. Inflammatory cytokines enhance the interaction of mannheimia haemolytica leukotoxin with bovine peripheral blood neutrophils in vitro. Infect. Immun. 2002, 70:4336-4343.
33. Levine R.L., Garland D., Oliver C.N., Amici A., Climent I., Lenz A.G., Ahn B.W., Shantiel S., Stadtman E.R. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 1990, 186:464-478.
34. Li J., Billiar T.R. Nitric oxide: determinants of nitric oxide protection and toxicity in liver. Am. J. Physiol. Gastrointest. Liver Physiol. 1999, 276:G1069-G1073.
35. Li Jm., Fenton R.A., Wheeler H.B., Powell C.C., Peyton B.D., Cutler B.S., Dobson J.S. Adenosine A2a receptors increase arterial endothelial cell nitric oxide. J. Surg. Res. 1998, 80:357-364.
36. Lieber C.S. Microsomal ethanol-oxidizing system (MEOS): the first 30 years a review. Alcohol. Clin. Exp. Res. 1999, 23:991-1007.
37. Lieber C.S., DeCarli L.M., Sorrell M.F. Experimental methods of ethanol administration. Hepatology 1989, 10:501-510.
38. Lindros K.O., Penttila K.E. Digitonin-collagenase perfusion for efficient separation of periportal or perivenous hepatocytes. Biochem. J. 1985, 228:757-760.
39. Mathurin P., Duchatelle V., Ramond M.J., Degott C., Bedossa P., Erlinger S., Benhamou J.P., Chaput J.C., Rueff B., Poynard T. Survival and prognostic factors in patients with severe biopsy-proven alcoholic hepatitis treated by prednisolone: randomized trial, new cohort, and simulation. Gastroenterol 1996, 110:1847-1853.
40. Michel J.B., Feron O., Sase K., Prabhakar P., Michel T. Caveolin versus calmodulin. Counterbalancing allosteric modulators of endothelial nitric oxide synthase. J. Biol. Chem. 1997, 272:25907-25912.
41. Moellering D., McAndrew J., Patel R.P., Forman H.J., Mulcahy R.T., Jo H., Darley-Usmar V.M. The induction of GSH synthesis by nanomolar concentrations of NO in endothelial cells: a role for gamma-glutamylcysteine synthetase and gamma-glutamyl transpeptidase. FEBS Lett. 1999, 448:292-296.
42. Moellering D., McAndrew J., Patel R.P., Cornwell T., Lincoln T., Cao X., Messina J.L., Forman H.J., Jo H., Darley-Usmar V.M. Nitric oxide-dependent induction of glutathione synthesis through increased expression of gamma glutamylcysteine synthetase. Arch. Biochem. Biophys. 1998, 358:74-82.
43. Mount P.F., Kemp B.E., Power D.A. Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. J. Mol. Cell. Cardiol. 2007, 42:271-279.
44. Mulcahy R.T., Wartman M.A., Bailey H.H., Gipp J.J. Constitutive and β-naphthoflavone-induced expression of the human γ-glutamylcysteine synthetase heavy subunit gene is regulated by a distal antioxidant response element/TRE sequence. J. Biol. Chem. 1997, 272:7445-7454.
45. Namkoong S., Kim C.K., Cho Y.L., Kim J.H., Lee H., Ha K.S., Choe J., Kim P.H., Won M.H., Kwon Y.J., Shim E.B., Kim Y.M. Forskolin increases angiogenesis through the coordinated cross-talk of PKA-dependent VEGF expression and Epac-mediated PI3K/Akt/eNOS signaling. Cell. Signal. 2009, 21:906-915.
46. Nanji A.A., Greenberg S.S., Tahan S.R., Fogt F., Loscalzo J., Sadrzadeh S.M.H., Xie J., Stamler J.S. Nitric oxide production in experimental alcoholic liver disease in the rat: role in protection from injury. Gastroenterol 1995, 109:899-907.
47. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 1979, 95:351-358.
48. Pinto C., Papa D., Hubner M., Tung-Chung Mou T.C., Lushington G.H., Seifert R. Activation and inhibition of adenylyl cyclase isoforms by forskolin analogs. J. Pharmacol. Exp. Ther. 2008, 325:27-36.
49. Roy D.N., Mandal S., Sen G., Mukhopadhyay S., Biswas T. 14-Deoxyandrographolide desensitizes hepatocytes to tumour necrosis factor alpha-induced apoptosis through calcium-dependent tumour necrosis factor receptor superfamily member 1A release via the NO/cGMP pathway. Br. J. Pharmacol. 2010, 160:1823-1843.
50. Salomon Y. Adenylate cyclase assay. Adv. Cyclic Nucleotide Res. 1979, 10:35-53.
51. Sauer H., Wartenberg M., Hescheler J. Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell. Physiol. Biochem. 2001, 11:173-186.
52. Seelig G.F., Meister A. Glutathione biosynthesis;-glutamylcysteine synthetase from rat kidney. Meth. Enzymol. 1985, 113:379-390.
53. Shen Y.C., Chen C.F., Chiou W.F. Suppression of rat neutrophil reactive oxygen species production and adhesion by the diterpenoid lacton andrographolide. Planta Med. 2000, 66:314-317.
54. Stewart S., Jones D., Day C.P. Alcoholic liver disease: new insights into mechanisms and preventative strategies. Trends. Mol. Med. 2001, 7:408-413.
55. Syapin P.J. Ethanol inhibition of inducible nitric oxide synthase activity in C6 glioma cells. Alcohol. Clin. Exp. Res. 1995, 19:262-267.
56. 2 increase calmodulin levels and cyclic AMP phosphodiesterase activity in cultured porcine thyroid cells. J. Endocr. 1988, 117:109-114.
57. Tan M.L., Kuroyanagi M., Sulaiman S.F., Najimudin N., Tengku Muhammad T.S. Cytotoxic activities of major diterpenoid constituents of Andrographis paniculata in a panel of human tumor cell lines. Pharm. Biol. 2005, 43:501-508.
58. Vysotskaya R.A., Loginov A.S., Varvanina G.G., Pilenitsyn A.Y. Significance of adenylate cyclase system of the liver in its chronic diseases. Bull. Exp. Biol. Med. 1998, 124:450-453.
59. Wang X., Abdel-Rahman A.A. Effect of chronic ethanol administration on hepatic eNOS activity and its association with caveolin-1 and calmodulin in female rats. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 289:G579-G585.
60. Xiao Y.F., Wu D.D., Liu S.X., Chen X., Ren L.F. Effect of arsenic trioxide on vascular endothelial cell proliferation and expression of vascular endothelial growth factor receptors Flt-1 and KDR in gastric cancer in nude mice. World J. Gastroenterol. 2007, 13:6498-6505.
61. Xu Z., Park S.S., Mueller R.A., Bagnell R.C., Patterson C., Boysen P.G. Adenosine produces nitric oxide and prevents mitochondrial oxidant damage in rat cardiomyocytes. Cardiovasc. Res. 2005, 65:803-812.
62. Yamamoto M., Okumura S., Oka N., Schwencke C., Ishikawa Y. Downregulation of caveolin expression by cAMP signal. Life Sci. 1999, 64:1349-1357.
63. Zang M., Zuccollo A., Hou X., Nagata D., Walsh K., Herscovitz H., Brecher P., Ruderman N.B., Cohen R.A. AMP-activated protein kinase is required for the lipid-lowering effect of metformin in insulin-resistant human HepG2 cells. J. Biol. Chem. 2004, 279:47898-47905.
64. Zhang C.Y., Tan B.K. Effects of 14-deoxyandrographolide and 14-deoxy-11,12-didehydroandrographolide on nitric oxide production in cultured human endothelial cells. Phytother Res. 1999, 13:157-159.
65. Zhang G., Liu Y., Ruoho A.E., Hurley J.H. Structure of the adenylyl cyclase catalytic core. Nature 1997, 386:247-253.
66. Zhou Z., Wang L., Song Z., Lambert J.C., McClain C.J., Kang Y.J. A critical involvement of oxidative stress in acute alcohol-induced hepatic TNF-α production. Am. J. Pathol. 2003, 163:1137-1146.