Fructose 1,6-bisphosphate reduced TNF-α-induced apoptosis in galactosamine sensitized rat hepatocytes through activation of nitric oxide and cGMP production

European Journal of Pharmacology

Volumn 610, Issue 1-3, 2009, Pages 128-133

  Calafell, Roser ^a   Boada, Jordi ^a   Santidrian, Antonio F ^a   Gil, Joan ^a   Roig, Teresa ^a   Perales, Jose C ^a   Bermudez, Jordi ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Apoptosis; Cyclic guanosine monophosphate; Fructose 1,6 bisphosphate; Galactosamine; Hepatitis; Nitric oxide

Indexed keywords

CYCLIC GMP; FRUCTOSE 1,6 BISPHOSPHATE; GALACTOSAMINE; GUANYLATE CYCLASE; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVATION; HEPATITIS; LIVER CELL; LIVER PROTECTION; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ANIMALS; APOPTOSIS; CELLS, CULTURED; CULTURE MEDIA, SERUM-FREE; CYCLIC GMP; DOSE-RESPONSE RELATIONSHIP, DRUG; FRUCTOSEDIPHOSPHATES; GALACTOSAMINE; HEPATOCYTES; MALE; NITRIC OXIDE; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 65049089033     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2009.03.044     Document Type: Article

References (58)

1. Ahn S.M., Yoon H.Y., Lee B.G., Park K.C., Chung J.H., Moon C.H., and Lee S.H. Fructose-1,6-diphosphate attenuates prostaglandin E2 production and cyclo-oxygenase-2 expression in UVB-irradiated HaCaT keratinocytes. Br. J. Pharmacol. 137 (2002) 497-503
2. Alves Filho J.C., Santos R.C., Castaman T.A., and De Oliveira J.R. Anti-inflammatory effects of fructose-1,6-bisphosphate on carrageenan-induced pleurisy in rat. Pharmacol. Res. 49 (2004) 245-248
3. Angermuller S., Schumann J., Fahimi H.D., and Tiegs G. Ultrastructural alterations of mitochondria in pre-apoptotic and apoptotic hepatocytes of TNF alpha-treated galactosamine-sensitized mice. Ann. N. Y. Acad. Sci. 887 (1999) 12-7, 12-17
4. Bartrons R., Hue L., Van Schaftingen E., and Hers H.G. Hormonal control of fructose 2,6-bisphosphate concentration in isolated rat hepatocytes. Biochem. J. 214 (1983) 829-837
5. Bordignon N.F., Meier G.C., Alves Filho J.C., Lunardelli A., Caberlon E., Peres A., and Rodrigues D.O. Immunomodulatory effect of fructose-1,6-bisphosphate on T-lymphocytes. Int. Immunopharmacol. 3 (2003) 267-272
6. Brune B. The intimate relation between nitric oxide and superoxide in apoptosis and cell survival. Antioxid. Redox. Signal. 7 (2005) 497-507
7. Cary S.P., Winger J.A., Derbyshire E.R., and Marletta M.A. Nitric oxide signaling: no longer simply on or off. Trends Biochem. Sci. 31 (2006) 231-239
8. Chojkier M., and Fierer J. d-galactosamine hepatotoxicity is associated with endotoxin sensitivity and mediated by lymphoreticular cells in mice. Gastroenterology 88 (1985) 115-121
9. Cuesta E., Boada J., Calafell R., Perales J.C., Roig T., and Bermudez J. Fructose 1,6-bisphosphate prevented endotoxemia, macrophage activation, and liver injury induced by d-galactosamine in rats. Crit. Care Med. 34 (2006) 807-814
10. De Oliveira J.R., Rosa J.L., Ambrosio S., and Bartrons R. Effect of galactosamine on hepatic carbohydrate metabolism: protective role of fructose 1,6-bisphosphate. Hepatology 15 (1992) 1147-1153
11. Donohoe P.H., Fahlman C.S., Bickler P.E., Vexler Z.S., and Gregory G.A. Neuroprotection and intracellular Ca2+ modulation with fructose-1,6-bisphosphate during in vitro hypoxia-ischemia involves phospholipase C-dependent signaling. Brain Res. 917 (2001) 158-166
12. Fahlman C.S., Bickler P.E., Sullivan B., and Gregory G.A. Activation of the neuroprotective ERK signaling pathway by fructose-1,6-bisphosphate during hypoxia involves intracellular Ca2+ and phospholipase C. Brain Res. 958 (2002) 43-51
13. Fouad D., Siendones E., Costan G., and Muntane J. Role of NF-kappaB activation and nitric oxide expression during PGE1 protection against d-galactosamine-induced cell death in cultured rat hepatocytes. Liver Int. 24 (2004) 227-236
14. Galanos C., Freudenberg M.A., and Reutter W. Galactosamine-induced sensitization to the lethal effects of endotoxin. Proc. Natl. Acad. Sci. USA. 76 (1979) 5939-5943
15. Gamez A., Alva N., Roig T., Bermudez J., and Carbonell T. Beneficial effects of fructose 1,6-biphosphate on hypothermia-induced reactive oxygen species injury in rats. Eur. J. Pharmacol. 590 (2008) 115-119
16. Genesca M., Sola A., Azuara D., De Oca J., and Hotter G. Apoptosis inhibition during preservation by fructose-1,6-diphosphate and theophylline in rat intestinal transplantation. Crit. Care Med. 33 (2005) 827-834
17. Gerassimou C., Kotanidou A., Zhou Z., Simoes D.D.C., Roussos C., and Papapetropoulos A. Regulation of the expression of soluble guanylyl cyclase by reactive oxygen species. Br. J. Pharmacol. 150 (2007) 1084-1091
18. Guzik T.J., West N.E.J., Pillai R., Taggart D.P., and Channon K.M. Nitric oxide modulates superoxide release and peroxynitrite formation in human blood vessels. Hypertension 39 (2002) 1088-1094
19. Hardin C.D., and Roberts T.M. Metabolism of exogenously applied fructose 1,6-bisphosphate in hypoxic vascular smooth muscle. Am. J. Physiol. 267 (1994) H2325-H2332
20. Hardin C.D., Lazzarino G., Tavazzi B., Di Pierro D., Roberts T.M., Giardina B., and Rovetto M.J. Myocardial metabolism of exogenous FDP is consistent with transport by a dicarboxylate transporter. Am. J. Physiol. 281 (2001) H2654-H2660
21. Hirokawa F., Nakai T., and Yamaue H. Storage solution containing fructose-1,6-bisphosphate inhibits the excess activation of Kupffer cells in cold liver preservation. Transplantation 74 (2002) 779-783
22. Hotter G., Closa D., Prados M., Fernandez-Cruz L., Prats N., Gelpi E., and Rosello-Catafau J. Intestinal preconditioning is mediated by a transient increase in nitric oxide. Biochem. Biophys. Res. Commun. 222 (1996) 27-32
23. Keppler D., and Decker K. Studies on the mechanism of galactosamine-1-phosphate and its inhibition of UDP-glucose pyrophosphorylase. Eur. J. Biochem. 10 (1969) 219-225
24. Keppler D.O., Rudigier J.F., Bischoff E., and Decker K.F. The trapping of uridine phosphates by d-galactosamine. d-glucosamine, and 2-deoxy-d-galactose. A study on the mechanism of galactosamine hepatitis. Eur. J. Biochem. 17 (1970) 246-253
25. Kim Y.M., Kim T.H., Chung H.T., Talanian R.V., Yin X.M., and Billiar T.R. Nitric oxide prevents tumor necrosis factor alpha-induced rat hepatocyte apoptosis by the interruption of mitochondrial apoptotic signaling through S-nitrosylation of caspase-8. Hepatology 32 (2000) 770-778
26. Kim J.S., Ohshima S., Pediaditakis P., and Lemasters J.J. Nitric oxide protects rat hepatocytes against reperfusion injury mediated by the mitochondrial permeability transition. Hepatology 39 (2004) 1533-1543
27. Lazzarino G., Tavazzi B., Di Pierro D., and Giardina B. Ischemia and reperfusion: effect of fructose-1,6-bisphosphate. Free Radic. Res. Commun. 16 (1992) 325-339
28. Leist M., Gantner F., Bohlinger I., Germann P.G., Tiegs G., and Wendel A. Murine hepatocyte apoptosis induced in vitro and in vivo by TNF-alpha requires transcriptional arrest. J. Immunol. 153 (1994) 1778-1788
29. Leist M., Gantner F., Bohlinger I., Tiegs G., Germann P.G., and Wendel A. Tumor necrosis factor-induced hepatocyte apoptosis precedes liver failure in experimental murine shock models. Am. J. Pathol. 146 (1995) 1220-1234
30. Li J., and Billiar T.R. The anti-apoptotic actions of nitric oxide in hepatocytes. Cell Death Differ. 6 (1999) 952-955
31. Li J., Bombeck C.A., Yang S., Kim Y.M., and Billiar T.R. Nitric oxide suppresses apoptosis via interrupting caspase activation and mitochondrial dysfunction in cultured hepatocytes. J. Biol. Chem. 274 (1999) 17325-17333
32. Li J., Yang S., and Billiar T.R. Cyclic nucleotides suppress tumor necrosis factor alpha -mediated apoptosis by inhibiting caspase activation and cytochrome c release in primary hepatocytes via a mechanism independent of Akt activation. J. Biol. Chem. 275 (2000) 13026-13034
33. Lopes R.P., Lunardelli A., Preissler T., Leite C.E., Alves-Filho J.C., Nunes F.B., De Oliveira J.R., and Bauer M.E. The effects of fructose-1,6-bisphosphate and dexamethasone on acute inflammation and T-cell proliferation. Inflamm. Res. 55 (2006) 354-358
34. Meurer S., Pioch S., Gross S., and Muller-Esterl W. Reactive oxygen species induce tyrosine phosphorylation of and Src kinase recruitment to NO-sensitive guanylyl cyclase. J. Biol. Chem. 280 (2005) 33149-33156
35. Mihas A.A., Maliakkal R.J., Mihas T.A., Kanji V.K., and Markov A.K. Effects of fructose-1,6-diphosphate on the activity of rat liver nitric oxide synthase in vitro. Pharmacology 54 (1997) 43-48
36. Mihas A.A., Kanji V.K., Mihas T.A., Joseph R.M., Markov A.K., and Heuman D.M. Fructose diphosphate attenuates the acetaminophen-induced liver injury in the rat. Evidence for involvement of nitric oxide. Res. Commun. Mol. Pathol. Pharmacol. 113-114 (2003) 253-266
37. Mojena M., Hortelano S., Castrillo A., Diaz-Guerra M.J., Garcia-Barchino M.J., Saez G.T., and Bosca L. Protection by nitric oxide against liver inflammatory injury in animals carrying a nitric oxide synthase-2 transgene. FASEB J. 15 (2001) 583-585
38. Moresco R.N., Santos R.C., Alves Filho J.C., and De Oliveira J.R. Effect of fructose-1,6-bisphosphate in the cold storage solution after 12 and 36 h of rat liver preservation. Transplant. Proc. 36 (2004) 2593-2595
39. Muntane J., Rodriguez F.J., Segado O., Quintero A., Lozano J.M., Siendones E., Pedraza C.A., Delgado M., O'Valle F., Garcia R., Montero J.L., de La M.M., and Mino G. TNF-alpha dependent production of inducible nitric oxide is involved in PGE(1) protection against acute liver injury. Gut 47 (2000) 553-562
40. Mustafa S.B., Flickinger B.D., and Olson M.S. Suppression of lipopolysaccharide-induced nitric oxide synthase expression by platelet-activating factor receptor antagonists in the rat liver and cultured rat Kupffer cells. Hepatology 30 (1999) 1206-1214
41. Muzaffar S., Shukla N., Angelini G., and Jeremy J.Y. Nitroaspirins and morpholinosydnonimine but not aspirin inhibit the formation of superoxide and the expression of gp91phox induced by endotoxin and cytokines in pig pulmonary artery vascular smooth muscle cells and endothelial cells. Circulation 110 (2004) 1140-1147
42. Nunes F.B., Simoes Pires M.G., Alves Filho J.C., Wachter P.H., and Rodrigues D.O. Physiopathological studies in septic rats and the use of fructose 1,6-bisphosphate as cellular protection. Crit. Care Med. 30 (2002) 2069-2074
43. Nunes F.B., Graziottin C.M., Alves Filho J.C., Lunardelli A., Pires M.G., Wachter P.H., and De Oliveira J.R. An assessment of fructose-1,6-bisphosphate as an antimicrobial and anti-inflammatory agent in sepsis. Pharmacol. Res. 47 (2003) 35-41
44. Quintero A., Pedraza C.A., Siendones E., ElSaid A.M.K., Colell A., Ruiz C., Montero J.L., De la Mata M., Fernández-Checa J.C., Miño G., and Muntané J. PGE1 protection against apoptosis induced by d-galactosamine is not related to the modulation of intracellular free radical production in primary culture of rat hepatocytes. Free Radic. Res. 36 (2002) 345-355
45. Rao M.R., Olinde K.D., and Markov A.K. In vitro induction of nitric oxide by fructose-1,6-diphosphate in the cardiovascular system of rats. Mol. Cell Biochem. 185 (1998) 171-175
46. Reinehr R., Becker S., Eberle A., Grether-Beck S., and Haussinger D. Involvement of NADPH oxidase isoforms and Src family kinases in CD95-dependent hepatocyte apoptosis. J. Biol. Chem. 280 (2005) 27179-27194
47. Roig T., De Oliveira J.R., Bartrons R., and Bermudez J. Fructose 1,6-bisphosphate protects against d-galactosamine toxicity in isolated rat hepatocytes. Am. J. Physiol. 266 (1994) C1722-C1728
48. Roig T., Bartrons R., and Bermudez J. Exogenous fructose 1,6-bisphosphate reduces K+ permeability in isolated rat hepatocytes. Am. J. Physiol. 273 (1997) C473-C478
49. Sano W., Watanabe F., Tamai H., Furuya E., and Mino M. Beneficial effect of fructose-1,6-bisphosphate on mitochondrial function during ischemia-reperfusion of rat liver. Gastroenterology 108 (1995) 1785-1792
50. Senft A.P., Dalton T.P., and Shertzer H.G. Determining glutathione and glutathione disulfide using the fluorescence probe o-phthalaldehyde. Anal. Biochem. 280 (2000) 80-86
51. Siendones E., Fouad D., Abou-Elella A.M., Quintero A., Barrera P., and Muntane J. Role of nitric oxide in d-galactosamine-induced cell death and its protection by PGE1 in cultured hepatocytes. Nitric Oxide 8 (2003) 133-143
52. Siendones E., Fouad D., Diaz-Guerra M.J., de La M.M., Bosca L., and Muntane J. PGE1-induced NO reduces apoptosis by d-galactosamine through attenuation of NF-kappaB and NOS-2 expression in rat hepatocytes. Hepatology 40 (2004) 1295-1303
53. Siendones E., Jimenez-Gómez L.A., Montero J.L., Gómez-Díaz C., Villalba J.M., and Muntane J. PGE1 abolishes the mitochondrial-independent cell death pathway induced by d-galactosamine in primary culture of rat hepatocytes. J. Gastroenterol. Hepatol. 20 (2005) 108-116
54. Sola A., Rosello-Catafau J., Gelpi E., and Hotter G. Fructose-1,6-biphosphate in rat intestinal preconditioning: involvement of nitric oxide. Gut 48 (2001) 168-175
55. Sola A., De Oca J., Alfaro V., Xaus C., Jaurrieta E., and Hotter G. Protective effects of exogenous fructose-1,6-biphosphate during small bowel transplantation in rats. Surgery 135 (2004) 518-526
56. Vexler Z.S., Wong A., Francisco C., Manabat C., Christen S., Tauber M., Ferriero D.M., and Gregory G. Fructose-1,6-bisphosphate preserves intracellular glutathione and protects cortical neurons against oxidative stress. Brain Res. 960 (2003) 90-98
57. Vodovotz Y., Kim P.K., Bagci E.Z., Ermentrout G.B., Chow C.C., Bahar I., and Billiar T.R. Inflammatory modulation of hepatocyte apoptosis by nitric oxide: in vivo, in vitro, and in silico studies. Curr. Mol. Med. 4 (2004) 753-762
58. Wang Y., Kim P.K., Peng X., Loughran P., Vodovotz Y., Zhang B., and Billiar T.R. Cyclic AMP and cyclic GMP suppress TNFalpha-induced hepatocyte apoptosis by inhibiting FADD up-regulation via a protein kinase A-dependent pathway. Apoptosis 11 (2006) 441-451