Liver-homing of purified glucose oxidase: A novel in vivo model of physiological hepatic oxidative stress (H2O2)

Journal of Hepatology

Volumn 46, Issue 3, 2007, Pages 482-491

  Rost, Daniel ^a,b   Welker, Andreas ^a   Welker, Judith ^a   Millonig, Gunda ^a   Berger, Irina ^c   Autschbach, Frank ^c   Schuppan, Detlef ^a   Mueller, Sebastian ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b KLINIKUM LUDWIGSHAFEN   (Germany)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Glucose oxidase; Hydrogen peroxide; Kupffer cells; Liver disease; Oxidative stress; Redox regulation; Signal transduction

Indexed keywords

GLUCOSE OXIDASE; GLUTATHIONE; HEME OXYGENASE 1; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPERGILLUS NIGER; BLOOD FLOW; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; ENZYME INDUCTION; IN VIVO STUDY; INFLAMMATORY CELL; KUPFFER CELL; LETHAL DOSE; LIVER CELL; LIVER DISEASE; LIVER FUNCTION TEST; LIVER NECROSIS; MALE; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALS; ASPERGILLUS NIGER; BILE; DISEASE MODELS, ANIMAL; GLUCOSE OXIDASE; GLUTATHIONE; HEPATITIS; HYDROGEN PEROXIDE; INJECTIONS, INTRAVENOUS; KUPFFER CELLS; LIVER; MALE; OXIDATIVE STRESS; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES;

EID: 33846564416     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2006.09.025     Document Type: Article

References (61)

1. Kaplowitz N. Mechanisms of liver cell injury. J Hepatol 32 (2000) 39-47
2. Jaeschke H. Mechanisms of oxidant stress-induced acute tissue injury. Proc Soc Exp Biol Med 209 (1995) 104-111
3. Mueller S., Afdhal N.H., and Schuppan D. Iron, HCV, and liver cancer: hard metal setting the pace?. Gastroenterology 130 (2006) 2229-2234
4. Trauner M., Fickert P., and Stauber R.E. Inflammation-induced cholestasis. J Gastroenterol Hepatol 14 (1999) 946-959
5. Schmitt M., Kubitz R., Wettstein M., vom Dahl S., and Haussinger D. Retrieval of the mrp2 gene encoded conjugate export pump from the canalicular membrane contributes to cholestasis induced by tert-butyl hydroperoxide and chloro-dinitrobenzene. Biol Chem 381 (2000) 487-495
6. Reinehr R., Becker S., Keitel V., Eberle A., Grether-Beck S., and Haussinger D. Bile salt-induced apoptosis involves NADPH oxidase isoform activation. Gastroenterology 129 (2005) 2009-2031
7. Yerushalmi B., Dahl R., Devereaux M.W., Gumpricht E., and Sokol R.J. Bile acid-induced rat hepatocyte apoptosis is inhibited by antioxidants and blockers of the mitochondrial permeability transition. Hepatology 33 (2001) 616-626
8. Zhong Z., Froh M., Lehnert M., Schoonhoven R., Yang L., Lind H., et al. Polyphenols from Camellia sinenesis attenuate experimental cholestasis-induced liver fibrosis in rats. Am J Physiol Gastrointest Liver Physiol 285 (2003) G1004-G1013
9. Boigk G., Stroedter L., Herbst H., Waldschmidt J., Riecken E.O., and Schuppan D. Silymarin retards collagen accumulation in early and advanced biliary fibrosis secondary to complete bile duct obliteration in rats. Hepatology 26 (1997) 643-649
10. Halliwell B., and Gutteridge J.M.C. Free radicals in biology and medicine. 3rd ed. (1999), Clarendon Press, Oxford
11. Bright H.J., and Porter D.J. Flavoprotein oxidases. In: Boyer P.D. (Ed). The enzymes (1975), Academic Press, New York, San Francisco, London 421-503
12. Droge W. Free radicals in the physiological control of cell function. Physiol Rev 82 (2002) 47-95
13. Remacle J., Raes M., Toussaint O., Renard P., and Rao G. Low levels of reactive oxygen species as modulators of cell function. Mutat Res 316 (1995) 103-122
14. Khan A.U., and Wilson T. Reactive oxygen species as cellular messengers. Chem Biol 2 (1995) 437-445
15. Nathan C. Specificity of a third kind: reactive oxygen and nitrogen intermediates in cell signaling. J Clin Invest 111 (2003) 769-778
16. Geiszt M., and Leto T.L. The Nox family of NAD(P)H oxidases: host defense and beyond. J Biol Chem 279 (2004) 51715-51718
17. Mueller S., Pantopoulos K., Hentze M.W., and Stremmel W. A chemiluminescence approach to study the regulation of iron metabolism by oxidative stress. In: Stanley P.E. (Ed). Bioluminescence and chemiluminescence: Molecular reporting with photons (1997), Wiley, Baffins Lane, Chichester, Sussex 338-341
18. Mueller S. Sensitive and nonenzymatic measurement of hydrogen peroxide in biological systems. Free Radic Biol Med 29 (2000) 410-415
19. Mueller S., Pantopoulos K., Hübner C.A., Stremmel W., and Hentze M.W. IRP1 activation by extracellular oxidative stress in the perfused rat liver. J Biol Chem 276 (2001) 23192-23196
20. 2 concentration in stimulated human neutrophils. J Biolumin Chemilumin 10 (1995) 229-237
21. Mutze S., Hebling U., Stremmel W., Wang J., Arnhold J., Pantopoulos K., and Mueller S. Myeloperoxidase-derived hypochlorous acid antagonizes the oxidative stress-mediated activation of iron regulatory protein 1. J Biol Chem 278 (2003) 40542-40549
22. 2 release from intact peroxisomes. Biochem J 363 (2002) 483-491
23. Seglen P.O. Preparation of isolated rat liver cells. Methods Cell Biol 13 (1976) 29-83
24. Smedsrod B., Pertoft H., Eggertsen G., and Sundstrom C. Functional and morphological characterization of cultures of Kupffer cells and liver endothelial cells prepared by means of density separation in Percoll, and selective substrate adherence. Cell Tissue Res 241 (1985) 639-649
25. Rost D., Kartenbeck J., and Keppler D. Changes in the localization of the rat canalicular conjugate export pump Mrp2 in phalloidin-induced cholestasis. Hepatology 29 (1999) 814-821
26. Buchler M., Konig J., Brom M., Kartenbeck J., Spring H., Horie T., and Keppler D. cDNA cloning of the hepatocyte canalicular isoform of the multidrug resistance protein, cMrp, reveals a novel conjugate export pump deficient in hyperbilirubinemic mutant rats. J Biol Chem 271 (1996) 15091-15098
27. Ogawa K., Suzuki H., Hirohashi T., Ishikawa T., Meier P.J., Hirose K., Akizawa T., et al. Characterization of inducible nature of MRP3 in rat liver. Am J Physiol Gastrointest Liver Physiol 278 (2000) G438-G446
28. Stieger B., Hagenbuch B., Landmann L., Hochli M., Schroeder A., and Meier P.J. In situ localization of the hepatocytic Na+/Taurocholate cotransporting polypeptide in rat liver. Gastroenterology 107 (1994) 1781-1787
29. +-independent organic anion transporting polypeptide (oatp-1) in rats with bile duct ligation. J Hepatol 27 (1997) 1051-1056
30. Gerloff T., Stieger B., Hagenbuch B., Madon J., Landmann L., Roth J., et al. The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J Biol Chem 273 (1998) 10046-10050
31. Reichel C., Gao B., Van Montfoort J., Cattori V., Rahner C., Hagenbuch B., et al. Localization and function of the organic anion-transporting polypeptide Oatp2 in rat liver. Gastroenterology 117 (1999) 688-695
32. Cattori V., van Montfoort J.E., Stieger B., Landmann L., Meijer D.K., Winterhalter K.H., et al. Localization of organic anion transporting polypeptide 4 (Oatp4) in rat liver and comparison of its substrate specificity with Oatp1, Oatp2 and Oatp3. Pflugers Arch 443 (2001) 188-195
33. Rost D., Herrmann T., Sauer P., Schmidts H.L., Stieger B., Meier P.J., et al. Regulation of rat organic anion transporters in bile salt-induced cholestatic hepatitis: effect of ursodeoxycholate. Hepatology 38 (2003) 187-195
34. Buzello M., Boehm C., Orth S., Fischer B., Ehmke H., Ritz E., et al. Myocyte loss in early left ventricular hypertrophy of experimental renovascular hypertension. Virchows Arch 442 (2003) 364-371
35. Blessing E., Bea F., Kuo C.C., Campbell L.A., Chesebro B., and Rosenfeld M.E. Lesion progression and plaque composition are not altered in older apoE-/- mice lacking tumor necrosis factor-alpha receptor p55. Atherosclerosis 176 (2004) 227-232
36. Griffith O.W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106 (1980) 207-212
37. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27 (1969) 502-522
38. Samoszuk M., Ehrlich D., and Ramzi E. Preclinical safety studies of glucose oxidase. J Pharmacol Exp Ther 266 (1993) 1643-1648
39. Polfliet M.M., Fabriek B.O., Daniels W.P., Dijkstra C.D., and van den Berg T.K. The rat macrophage scavenger receptor CD163: expression, regulation and role in inflammatory mediator production. Immunobiology 211 (2006) 419-425
40. Westendorp M.O., Shatrov V.A., Schulze-Osthoff K., Frank R., Kraft M., Los M., et al. HIV-1 Tat potentiates TNF-induced NF-kappa B activation and cytotoxicity by altering the cellular redox state. EMBO J 14 (1995) 546-554
41. Halliwell B., and Whiteman M. Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean?. Br J Pharmacol 142 (2004) 231-255
42. Hentze M.W., and Kühn L.C. Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide and oxidative stress. Proc Natl Acad Sci USA 93 (1996) 8175-8182
43. 2 on the expression and function of iron-responsive element-containing mRNAs in B6 fibroblasts. J Biol Chem 22 (2001) 22
44. 2 and not superoxide determines the compartment-specific activation of transferrin receptor by iron regulatory protein 1. Free Radic Res 39 (2005) 817-824
45. Gerber C.E., Bruchelt G., Falk U.B., Kimpfler A., Hauschild O., Kuci S., et al. Reconstitution of bactericidal activity in chronic granulomatous disease cells by glucose-oxidase-containing liposomes. Blood 98 (2001) 3097-3105
46. Ismail G., Boxer L.A., and Baehner R.L. Utilization of liposomes for correction of the metabolic and bactericidal deficiencies in chronic granulomatous disease. Pediatr Res 13 (1979) 769-773
47. Nathan C.F., and Cohn Z.A. Antitumor effects of hydrogen peroxide in vivo. J Exp Med 154 (1981) 1539-1553
48. Christofidou-Solomidou M., Pietra G.G., Solomides C.C., Arguiris E., Harshaw D., Fitzgerald G.A., et al. Immunotargeting of glucose oxidase to endothelium in vivo causes oxidative vascular injury in the lungs. Am J Physiol Lung Cell Mol Physiol 278 (2000) L794-L805
49. Friedrich E.A., Aulenbacher P., Schlepper-Schafer J., and Suss R. Kupffer cells recognize trinitrobenzene-labeled erythrocytes. Immunol Lett 4 (1982) 167-170
50. Wiltrout R.H., Brunda M.J., Gorelik E., Peterson E.S., Dunn J.J., Leonhardt J., et al. Distribution of peritoneal macrophage populations after intravenous injection in mice: differential effects of eliciting and activating agents. J Reticuloendothel Soc 34 (1983) 253-269
51. Kalisz H.M., Hendle J., and Schmid R.D. Structural and biochemical properties of glycosylated and deglycosylated glucose oxidase from Penicillium amagasakiense. Appl Microbiol Biotechnol 47 (1997) 502-507
52. Smedsrod B., Melkko J., Araki N., Sano H., and Horiuchi S. Advanced glycation end products are eliminated by scavenger-receptor-mediated endocytosis in hepatic sinusoidal Kupffer and endothelial cells. Biochem J 322 Pt 2 (1997) 567-573
53. Matsumoto K., Sano H., Nagai R., Suzuki H., Kodama T., Yoshida M., et al. Endocytic uptake of advanced glycation end products by mouse liver sinusoidal endothelial cells is mediated by a scavenger receptor distinct from the macrophage scavenger receptor class A. Biochem J 352 Pt 1 (2000) 233-240
54. Takata K., Horiuchi S., Araki N., Shiga M., Saitoh M., and Morino Y. Endocytic uptake of nonenzymatically glycosylated proteins is mediated by a scavenger receptor for aldehyde-modified proteins. J Biol Chem 263 (1988) 14819-14825
55. Smedsrod B., Pertoft H., Gustafson S., and Laurent T.C. Scavenger functions of the liver endothelial cell. Biochem J 266 (1990) 313-327
56. Melkko J., Hellevik T., Risteli L., Risteli J., and Smedsrod B. Clearance of NH2-terminal propeptides of types I and III procollagen is a physiological function of the scavenger receptor in liver endothelial cells. J Exp Med 179 (1994) 405-412
57. Gow A.J., Branco F., Christofidou-Solomidou M., Black-Schultz L., Albelda S.M., and Muzykantov V.R. Immunotargeting of glucose oxidase: intracellular production of H2O2 and endothelial oxidative stress. Am J Physiol 277 (1999) L271-L281
58. Jaeschke H., Gores G.J., Cederbaum A.I., Hinson J.A., Pessayre D., and Lemasters J.J. Mechanisms of hepatotoxicity. Toxicol Sci 65 (2002) 166-176
59. Mueller S. Iron regulatory protein 1 as a sensor of reactive oxygen species. Biofactors 24 (2005) 171-181
60. Ballatori N., and Truong A.T. Altered hepatic junctional permeability, bile acid excretion and glutathione efflux during oxidant challenge. J Pharmacol Exp Ther 251 (1989) 1069-1075
61. Hentze M.W., Muckenthaler M.U., and Andrews N.C. Balancing acts: molecular control of mammalian iron metabolism. Cell 117 (2004) 285-297