Enzymatic reduction of labile iron by organelles of the rat liver. Superior role of an NADH-dependent activity in the outer mitochondrial membrane

Biochimie

Volumn 90, Issue 10, 2008, Pages 1591-1601

  Pamp, K ^a   Kerkweg, U ^a   Korth, H G ^b   Homann, F ^a   Rauen, U ^a   Sustmann, R ^b   de Groot, H ^a   Petrat, F ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

Ferric reductases; Liver cells; Mitochondria; Reactive oxygen species

Indexed keywords

ASCORBIC ACID; CYTOCHROME C OXIDASE; FERRIC ION; IRON; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUPEROXIDE; UBIQUINOL CYTOCHROME C REDUCTASE;

ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; ENZYME ACTIVITY; IRON METABOLISM; LIVER CYTOSOL; LIVER METABOLISM; LIVER MICROSOME; LIVER MITOCHONDRION; MALE; NONHUMAN; OXIDATION REDUCTION REACTION; RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; CYTOSOL; ELECTRON SPIN RESONANCE SPECTROSCOPY; FERRIC COMPOUNDS; IRON; LIVER; MALE; MITOCHONDRIAL MEMBRANES; MUSCLE, SKELETAL; NAD; NADP; ORGANELLES; OXIDATION-REDUCTION; PHENANTHROLINES; RATS; SPECTROPHOTOMETRY;

MAMMALIA; RATTUS;

EID: 50949114725     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2008.06.010     Document Type: Article

References (66)

1. Fenton H.J.H. Oxidation of tartaric acid in the presence of iron. J. Chem. Soc. 6 (1894) 899-910
2. Kakhlon O., and Cabantchik Z.I. The labile iron pool: characterization, measurement, and participation in cellular processes. Free Radic. Biol. Med. 33 (2002) 1037-1046
3. Petrat F., de Groot H., Sustmann R., and Rauen U. The chelatable iron pool in living cells: a methodically defined quantity. Biol. Chem. 383 (2002) 489-502
4. Halliwell B., and Gutteridge J.M.C. Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol. 186 (1990) 1-85
5. Lehnen-Beyel I., de Groot H., and Rauen U. Enhancement of iron toxicity in L929 cells by d-glucose: accelerated (re-)reduction. Biochem. J. 368 (2002) 517-526
6. Woodmansee A.N., and Imlay J.A. Reduced flavins promote oxidative DNA damage in non-respiring Escherichia coli by delivering electrons to intracellular free iron. J. Biol. Chem. 277 (2002) 34055-34066
7. Henle E.S., and Linn S. Formation, prevention, and repair of DNA damage by iron/hydrogen peroxide. J. Biol. Chem. 272 (1997) 19095-19098
8. Pierre J.L., Fontecave M., and Crichton R.R. Chemistry for an essential biological process: the reduction of ferric iron. Biometals 15 (2002) 341-346
9. Thorstensen K., and Romslo I. Uptake of iron from transferrin by isolated rat hepatocytes. J. Biol. Chem. 263 (1988) 8844-8850
10. 2-transferrin reductase and iron uptake in K562 cells are not directly related. Eur. J. Biochem. 192 (1990) 475-480
11. Kukielka E., Puntarulo S., and Cederbaum A.I. Interaction of ferric complexes with rat liver nuclei to catalyze NADH- and NADPH-dependent production of oxygen radicals. Arch. Biochem. Biophys. 273 (1989) 319-330
12. Puntarulo S., and Cederbaum A.I. Inhibition of the oxidation of hydroxyl radical scavenging agents after alkaline phosphatase treatment of rat liver microsomes. Biochim. Biophys. Acta 1074 (1991) 12-18
13. 2 generation, and ferric reduction. Arch. Biochem. Biophys. 331 (1996) 69-78
14. Petrat F., Paluch S., Dogruöz E., Dörfler P., Kirsch M., Korth H.-G., Sustmann R., and de Groot H. Reduction of iron(III) ions complexed to physiological ligands by lipoyl dehydrogenase and other flavoenzymes in vitro. Implications for an enzymatic reduction of Fe(III) ions of the labile iron pool. J. Biol. Chem. 278 (2003) 46403-46413
15. 2 liberated by sources other than xanthine oxidase. Biol. Chem. Hoppe-Seyler 372 (1991) 35-41
16. Clayton D.A., and Doda J.N. Isolation of mitochondria from cells and tissues. In: Spector D.L., Goldman R.D., and Leinwand L.A. (Eds). Cells: A Laboratory Manual. 1. Culture and Biochemical Analysis of Cells (1998), Cold Spring Harbor Laboratory Press, New York 41.41-41.47
17. Paigen K., and Wenner C. The intracellular location of the glycolytic dehydrogenases in liver and hepatoma. Arch. Biochem. Biophys. 97 (1962) 213-216
18. Lambert N., and Freedman R.B. The latency of rat liver microsomal protein disulphide-isomerase. Biochem. J. 228 (1985) 635-645
19. Pederson T., and Spann T.P. Preparation of nuclei from tissue and suspension cultures. In: Spector D.L., Goldman R.D., and Leinwand L.A. (Eds). Cells: A Laboratory Manual. 1. Culture and Biochemical Analysis of Cells (1998), Cold Spring Harbor Laboratory Press, New York 43.41-43.14
20. Ernster L., and Nordenbrand K. Skeletal muscle mitochondria. In: Eastbrook R.W. (Ed). Methods in Enzymology. Oxidation and Phosphorylation (1967), Academic Press, New York 86-94
21. Schnaitman C., and Greenwalt J.W. Enzymatic properties of the inner and outer membranes of rat liver mitochondria. J. Cell Biol. 38 (1968) 158-175
22. Bergmeyer H.U. Methods of Enzymatic Analyses Vol. 2 (1983), Verlag Chemie, Weinheim 189-191 p
23. de Groot H., and Noll T. Enzymic determination of inorganic phosphates, organic phosphates and phosphate-liberating enzymes by use of nucleoside phosphorylase-xanthine oxidase (dehydrogenase)-coupled reactions. Biochem. J. 229 (1985) 255-260
24. Bergmeyer H.U. Methods of Enzymatic Analyses Vol. 2 (1983), Verlag Chemie, Weinheim 208-209 p
25. Bergmeyer H.U. Methods of Enzymatic Analyses Vol. 2 (1983), Verlag Chemie, Weinheim 232-233 p
26. Lai J.C.K., Sheu K.-F.R., Kim Y.T., Clarke D.D., and Blass J.P. The subcellular localization of glutamate dehydrogenase (GDH): is GDH a marker for mitochondria in brain?. Neurochem. Res. 11 (1986) 733-744
27. Sottocasa G.L., Kuylenstierna B., Ernster L., and Bergstrand A. An electron-transport system associated with the outer membrane of liver mitochondria. A biochemical and morphological study. J. Cell Biol. 32 (1967) 415-438
28. Dallner G., Siekevitz P., and Palade G.E. Biogenesis of endoplasmic reticulum membranes. II. Synthesis of constitutive microsomal enzymes in developing rat hepatocyte. J. Cell Biol. 30 (1966) 97-117
29. Orrenius S., Ericsson J.L.E., and Ernster L. Phenorbital-induced synthesis of the microsomal drug-metabolizing enzyme system and its relationship to the proliferation of endoplasmatic membranes. A morphological and biochemical study. J. Cell Biol. 25 (1965) 627-639
30. Blouin A., Bolender R.P., and Weibel E.R. Distribution of organelles and membranes between hepatocytes and nonhepatocytes in the rat liver parenchyma. J. Cell Biol. 72 (1977) 441-455
31. Darnell J., Harvey L., and Baltimore D. Molekulare Zellbiologie (1994), Walter de Gruyter, Berlin 162-163 p
32. Weibel E.R., Stäubli W., Gnägi H.R., and Hess F.A. Correlated morphometric and biochemical studies on the liver cell. I. Morphometric model, stereologic methods, and normal morphometric data for rat liver. J. Cell Biol. 42 (1969) 68-91
33. Tyler D.D. The Mitochondrion in Health and Disease (1992), VCH Publishers, New York 70 p
34. Chauveau J., Moule Y., and Rouiller C. Isolation of pure and unaltered liver nuclei. Morphology and biochemical composition. Exp. Cell Res. 11 (1956) 317-321
35. Frederiks W.M., and James J. Isolation and separation of rat liver nuclei. Acta Histochem. 20 Suppl (1979) 147-158
36. Bironaite D., and Öllinger K. The hepatoxicity of rhein involves impairment of mitochondrial functions. Chem.-Biol. Interact. 103 (1997) 35-50
37. Kean E.A., Gutman M., and Singer T.P. Studies on the respiratory chain-linked nicotinamide adenine dinucleotide dehydrogenase. XXII. Rhein, a competitive inhibitor of the dehydrogenase. J. Biol. Chem. 246 (1971) 2346-2353
38. Askwith C., and Kaplan J. Iron and copper transport in yeast and its relevance to human disease. Trends Biochem. Sci. 23 (1998) 135-138
39. Li L., and Kaplan J. A mitochondrial-vacuolar signaling pathway in yeast that affects iron and copper metabolism. J. Biol. Chem. 279 (2004) 33653-33661
40. Zhang Y., Lyver E.R., Knight S.A.B., Pain D., Lesuisse E., and Dancis A. Mrs3p, Mrs4p, and frataxin provide iron for Fe-S cluster synthesis in mitochondria. J. Biol. Chem. 281 (2006) 22493-22502
41. Berry M.N., Gregory R.B., Grivell A.R., Phillips J.W., and Schön A. The capacity of reducing-equivalent shuttles limits glycolysis during ethanol oxidation. Eur. J. Biochem. 225 (1994) 557-564
42. Meijer A.J. Amino acids as regulators and components of nonproteinogenic pathways. J. Nutr 133 (2003) 2057S-2062S
43. Leopold J.A., Cap A., Scribner A.W., Stanton R., and Loscalzo J. Glucose-6-phosphate dehydrogenase deficiency promotes endothelial oxidant stress and decreases endothelial nitric oxide bioavailability. FASEB J. 15 (2001) 1771-1773
44. Forth W., and Rummel W. Vitamine, Spurenelemente. In: Forth W., Henschler D., and Rummel W. (Eds). Allgemeine und spezielle Pharmakologie und Toxikologie (1983), Bibliographisches Institut, Mannheim, Wien, Zürich 414-415
45. Gries F.A., Toeller M., and Koschnisky T. Ernährungsstörungen. In: Siegenthaler W., Kaufmann W., Hornbostel H., and Waller H.D. (Eds). Lehrbuch der inneren Medizin (1984), Georg Thieme Verlag, Stuttgart, New York 282-284
46. Galleano M., and Puntarulo S. Mild iron overload effect on rat liver nuclei. Toxicology 93 (1994) 125-134
47. Kukielka E., and Cederbaum A.I. NADPH- and NADH-dependent oxygen radical generation by rat liver nuclei in the presence of redox cycling agents and iron. Arch. Biochem. Biophys. 283 (1990) 326-333
48. Flatmark T., and Romslo I. Energy-dependent accumulation of iron by isolated rat liver mitochondria. Requirement of reducing equivalents and evidence for a unidirectional flux of Fe(II) across the inner membrane. J. Biol. Chem. 250 (1975) 6433-6438
49. Barnes R., Connelly J.L., and Jones O.T.G. The utilization of iron and its complexes by mammalian mitochondria. Biochem. J. 128 (1972) 1043-1055
50. Taketani S., Tanaka-Yoshioka A., Masaki R., Tashiro Y., and Tokunaga R. Association of ferrochelatase with complex I in bovine heart mitochondria. Biochim. Biophys. Acta 883 (1986) 277-283
51. Williams D.M., Loukopoulos D., Lee G.R., and Cartwright G.E. Role of copper in mitochondrial iron metabolism. Blood 48 (1976) 77-85
52. Ramirez L.A.G., and Lemeshko V.V. A possible restriction of ferro- and ferricyanide oxidoreductase activities of rat liver mitochondria by the outer membrane. Arch. Biochem. Biophys. 443 (2005) 11-20
53. Kukielka E., Dicker E., and Cederbaum A.I. Increased production of reactive oxygen species by rat liver mitochondria after chronic ethanol treatment. Arch. Biochem. Biophys. 309 (1994) 377-386
54. Hirai K.-I., Ikeda K., and Wang G.-Y. Paraquat damage of rat liver mitochondria by superoxide production depends on extramitochondrial NADH. Toxicology 72 (1992) 1-16
55. Bernardi P., and Azzone G.F. Cytochrome c as an electron shuttle between the outer and inner mitochondrial membranes. J. Biol. Chem. 256 (1981) 7187-7192
56. Szczesna-Kaczmarek A. Regulating effect of mitochondrial lactate dehydrogenase on oxidation of cytoplasmatic NADH via an "external" pathway in skeletal muscle mitochondria. Int. J. Biochem. 24 (1992) 657-661
57. Szczesna-Kaczmarek A., Litwinska D., and Popinigis J. Oxidation of NADH via an "external" pathway in skeletal-muscle mitochondria and its possible role in the repayment of lactacid oxygen debt. Int. J. Biochem. 16 (1984) 1231-1235
58. Fischer J.C., Ruitenbeek W., Trijbels J.M.F., Veerkamp J.H., Stadhouders A.M., Sengers R.C.A., and Janssen A.J.M. Estimation of NADH oxidation in human skeletal muscle mitochondria. Clin. Chim. Acta 155 (1986) 263-274
59. Crow K.E., Braggins T.J., Batt R.D., and Hardman M.J. Rat liver cytosolic malate dehydrogenase: purification, kinetic, properties, role in control of free cytosolic NADH concentration. J. Biol. Chem. 257 (1982) 14217-14225
60. Khan S., and O'Brien P.J. Modulating hypoxia-induced hepatocyte injury by affecting intracellular redox state. Biochim. Biophys. Acta 1269 (1995) 153-161
61. Petrat F., de Groot H., and Rauen U. Subcellular distribution of chelatable iron: a laser scanning microscopic study in isolated rat hepatocytes and rat liver endothelial cells. Biochem. J. 356 (2001) 61-69
62. Smith R.M., and Martell A.E. Critical Stability Constants Vol. 2 (1990), Plenum Press, New York 251 p
63. Rauen U., Kerkweg U., Weisheit D., Petrat F., Sustmann R., and de Groot H. Cold-induced apoptosis of hepatocytes: mitochondrial permeability transition triggered by nonmitochondrial chelatable iron. Free Radic. Biol. Med. 35 (2003) 1664-1678
64. Sturm B., Bistrich U., Sarsero J.P., Rauen U., Scheiber-Mojdehkar B., de Groot H., Ioannou P., and Petrat F. Friedreich's ataxia: no changes in mitochondrial labile iron in human lymphoblasts and fibroblasts. A decrease in antioxidative capacity?. J. Biol. Chem. 280 (2005) 6701-6708
65. Caraceni P., Van Thiel D.H., and Borle A.B. Dual effect of deferoxamine on free radical formation and reoxygenation injury in isolated hepatocytes. Am. J. Physiol. 269 (1995) G132-G137
66. Rauen U., Petrat F., Sustmann R., and de Groot H. Iron-induced mitochondrial permeability transition in cultured hepatocytes. J. Hepatol. 40 (2004) 607-615