Cytosolic and mitochondrial isoforms of NADP+-dependent isocitrate dehydrogenases are expressed in cultured rat neurons, astrocytes, oligodendrocytes and microglial cells

Journal of Neurochemistry

Volumn 86, Issue 3, 2003, Pages 605-614

  Minich, Tobias ^a   Yokota, Sadaki ^b   Dringen, Ralf ^a,c  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF YAMANASHI   (Japan)

^c MONASH UNIVERSITY   (Australia)

Author keywords

Brain; Glutathione; NADPH; Oxidative stress; Pentose phosphate pathway

Indexed keywords

ISOCITRATE DEHYDROGENASE (NADP);

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN NERVE CELL; ENZYME ACTIVITY; ENZYME SYNTHESIS; MICROGLIA; MOLECULAR CLONING; NERVE CELL CULTURE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

AMINO ACID SEQUENCE; ANIMALS; ASTROCYTES; BASE SEQUENCE; CELL FRACTIONATION; CELLS, CULTURED; CLONING, MOLECULAR; CYTOSOL; ENZYME ACTIVATION; ISOCITRATE DEHYDROGENASE; ISOENZYMES; MICROGLIA; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; NEUROGLIA; NEURONS; OLIGODENDROGLIA; RATS; RATS, WISTAR; RNA, MESSENGER;

ANIMALIA;

EID: 0041803001     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.01871.x     Document Type: Article

References (58)

1. Almeida A. and Medina J. M. (1998) A rapid method for the isolation of metabolically active mitochondria from rat neurons and astrocytes in primary culture. Brain Res. Brain Res. Protoc. 2, 209-214.
2. Bajo M., Fruehauf J., Kim S. H., Fountoulakis M. and Lubec G. (2002) Proteomic evaluation of intermediary metabolism enzyme proteins in fetal Down's syndrome cerebral cortex. Proteomics 2, 1539-1546,
3. Baquer N. Z., Hothersall J. S. and McLean P. (1988) Function and regulation of the pentose phosphate pathway in brain. Curr. Top Cell Regul. 29, 265-289.
4. Beinert H. and Kennedy M. C. (1993) Aconitase, a two-faced protein: enzyme and iron regulatory factor. FASEB J. 7, 1442-1449.
5. Ben Yoseph O., Boxer P. A. and Ross B. D. (1994) Oxidative stress in the central nervous system: monitoring the metabolic response using the pentose phosphate pathway. Dev. Neurosci. 16, 328-336.
6. Clarke D. D. and Sokoloff L. (1999) Circulation and energy metabolism, in Basic Neurochemistry, Molecular, Cellular and Medical Aspects (Siegel G. J., Agranoff B. W., Albers R. W., Fisher S. K. and Uhler M. D., eds), pp. 637-670. Lippincott Williams und Wilkins, Philadelphia, PA, USA.
7. Comte B., Vincent G., Bouchard B., Benderdour M. and Des Rosiers C. (2002) Reverse flux through cardiac NADP (+)-isocitrate dehydrogenase under normoxia and ischemia. Am. J. Physiol. Heart Circ. Physiol. 283, H1505-H1514.
8. Dalziel K. (1980) Isocitrate dehydrogenase and related oxidative decarboxylases. FEBS Lett. 117, K45-K55.
9. Des Rosiers C., Fernandez C. A., David F. and Brunengraber H. (1994) Reversibility of the mitochondrial isocitrate dehydrogenase reaction in the perfused rat liver: evidence from isotopomer analysis of citric acid cycle intermediates. J. Biol. Chem. 269, 27179-27182.
10. Dringen R. (2000) Metabolism and functions of glutathione in brain. Prog. Neurobiol. 62, 649-671.
11. Dringen R., Kussmaul L. and Hamprecht B. (1998) Detoxification of exogenous hydrogen peroxide and organic hydroperoxides by cultured astroglial cells assessed by microtiter plate assay. Brain Res. Brain Res. Protoc. 2, 223-228.
12. Dringen R., Pfeiffer B. and Hamprecht B. (1999a) Synthesis of the antioxidant glutathione in neurons: supply by astrocytes of CysGly as precursor for neuronal glutathione. J. Neurosci. 19, 562-569.
13. Dringen R., Kussmaul L., Gutterer J. M., Hirrlinger J. and Hamprecht B. (1999b) The glutathione system of peroxide detoxification is less efficient in neurons than in astroglial cells. J. Neurochem. 72, 2523-2530.
14. Eggleston L. V. and Krebs H. A. (1974) Regulation of the pentose phosphate cycle. Biochem. J. 138, 425-435.
15. Emanuelsson O., Nielsen H., Brunak S. and von Heijne G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300, 1005-1016.
16. Frenkel R. (1972) Isolation and some properties of a cytosol and a mitochondrial malic enzyme from bovine brain. Arch. Biochem. Biophys. 152, 136-143.
17. Garcia-Nogales P., Almeida A. and Bolanos J. P. (2003) Peroxynitrite protects neurons against nitric oxide-mediated apoptosis: a key role for glucose-6-phosphate dehydrogenase activity in neuroprotection. J. Biol. Chem. 278, 864-874.
18. Geisbrecht B. V. and Gould S. J. (1999) The human PICD gene encodes a cytoplasmic and peroxisomal NADP(+)-dependent isocitrate dehydrogenase. J. Biol. Chem. 274, 30527-30533.
19. Giulian D. and Baker T. J. (1986) Characterization of ameboid microglia isolated from developing mammalian brain. J. Neurosci. 6, 2163-2178.
20. Goldberg D. M. and Ellis G. (1983) Isocitrate dehydrogenase, in Methods of Enzymatic Analysis (Bergmeyer H. U., Bergmeyer J. and Grassl M., eds), pp. 183-190. Verlag Chemie, Weinheim.
21. Gruer M. J., Artymiuk P. J. and Guest J. R. (1997) The aconitase family: three structural variations on a common theme. Trends Biochem. Sci. 22, 3-6.
22. Gunsalus I. C., Pederson T. C. and Sligar S. G. (1975) Oxygenase-catalyzed biological hydroxylations. Annu. Rev. Biochem. 44, 377-407.
23. Gutterer J. M., Dringen R., Hirrlinger J. and Hamprecht B. (1999) Purificafion of glutathione reductase from bovine brain, generation of an antiserum, and immunocytochemical localization of the enzyme in neural cells. J. Neurochem. 73, 1422-1430.
24. Halliwell B. and Gutteridge J. M. C. (1999) Free Radicals in Biology and Medicine. Oxford University Press, New York.
25. Hamprecht B. and Löffler F. (1985) Primary glial cultures as a model for studying hormone action. Methods Enzymol. 109, 341-345.
26. Haraguchi C. M., Mabuchi T. and Yokota S. (2003) Localization of a mitochondrial type of NADP-dependent isocitrate dehydrogenase in kidney and heart of rat: an immunocytochemical and biochemical study. J. Histochem. Cytochem. 51, 215-226.
27. Haselbeck, R. J., Colman R. F. and McAlister-Henn L. (1992) Isolation and sequence of a cDNA encoding porcine mitochondrial NADP-specific isocitrate dehydrogenase. Biochemistry 31, 6219-6223.
28. Henderson N. S. (1968) Intracellular location and genetic control of isozymes of NADP-dependent isocitrate dehydrogenase and malate dehydrogenase. Ann. NY Acad. Sci. 151, 429-440.
29. Hirrlinger J., Gutterer J. M., Kussmaul L., Hamprecht B. and Dringen R. (2000) Microglial cells in culture express a prominent glutathione system for the defense against reactive oxygen species. Dev Neurosci. 22, 384-392.
30. Hirrlinger J., Resch A., Gutterer J. M. and Dringen R. (2002) Oligodendroglial cells in culture effectively dispose of exogenous hydrogen peroxide: comparison with cultured neurones, astroglial and microglial cells. J. Neurochem. 82, 635-644.
31. Hoek J. B. and Rydstrom J. (1988) Physiological roles of nicotinamide nucleotide transhydrogenase. Biochem. J. 254, 1-10.
32. Huh T. L., Ryu J. H., Huh J. W., Sung H. C., Oh I. U., Song B. J. and Veech R. L. (1993) Cloning of a cDNA encoding bovine mitochondrial NADP(+)-specific isocitrate dehydrogenase and structural comparison with its isoenzymes from different species. Biochem. J. 292, 705-710.
33. Jennings G. T., Sechi S., Stevenson P. M., Tuckey R. C., Parmelee D. and McAlister-Henn L. (1994) Cytosolic NADP(+)-dependent isocitrate dehydrogenase. Isolation of rat cDNA and study of tissue-specific and developmental expression of mRNA. J. Biol. Chem. 269, 23128-23134.
34. Jo S. H., Son M. K., Koh H. J., Lee S. M., Song I. H., Kim Y. O., Lee Y. S., Jeong K. S., Kim W. B., Park J. W., Song B. J., Huh T. L. and Huh T. L. (2001) Control of mitochondrial redox balance and cellular defense against oxidative damage by mitochondrial NADP+-dependent isocitrate dehydrogenase. J. Biol. Chem. 276, 16168-16176.
35. Juurlink B. H. (1993) NADP-linked isozymes are the major forms of isocitrate dehydrogenase in mouse type-1-like astrocytes. Life Sci. 52, 1087-1090.
36. Kaplan R. S., Mayor J. A. and Wood D. O. (1993) The mitochondrial tricarboxylate transport protein. cDNA cloning, primary structure, and comparison with other mitochondrial transport proteins. J. Biol. Chem. 268, 13682-13690.
37. Kurz G. M., Wiesinger H. and Hamprecht B. (1993) Purification of cytosolic malic enzyme from bovine brain, generation of monoclonal antibodies, and immunocytochemical localization of the enzyme in glial cells of neural primary cultures. J. Neurochem. 60, 1467-1474.
38. Kussmaul L., Hamprecht B. and Dringen R. (1999) The detoxification of cumene hydroperoxide by the glutathione system of cultured astroglial cells hinges on hexose availability for the regeneration of NADPH. J. Neurochem. 73, 1246-1253.
39. Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
40. Lee C. P. and Emster L. (1989) Energy-linked nicotinamide nucleotide transhydrogenase 1963-88: a commentary on 'equilibrium studies of the energy-dependent and non-energy-dependent pyridine nucleotide transhydrogenase reactions'. Biochim. Biophys. Acta 1000, 371-376.
41. Lee S. M., Koh H. J., Park D. C., Song B. J., Huh T. L. and Park J. W. (2002) Cytosolic NADP(+)-dependent isocitrate dehydrogenase status modulates oxidative damage to cells. Free Radic. Biol. Med. 32, 1185-1196.
42. Löffler, F., Lohmann S. M., Walckhoff B., Walter U. and Hamprecht B. (1986) Immunocytochemical characterization of neuron-rich primary cultures of embryonic rat brain cells by established neuronal and glial markers and by monospecific antisera against cyclic nucleotide-dependent protein kinases and the synaptic vesicle protein synapsin I. Brain Res. 363, 205-221.
43. Loreck D. J., Van der Galarraga J. F. J., Phang J. M., Smith B. H. and Cummins C. J. (1987) Regulation of the pentose phosphate pathway in human astrocytes and gliomas. Metab. Brain Dis. 2, 31-46.
44. Loverde A. W. and Lehrer G. M. (1973) Subcellular distribution of isocitrate dehydrogenases in neonatal and adult mouse brain. J. Neurochem. 20, 441-448.
45. Lowry O. H., Rosebrough N. J., Farr A. L. and Randall R. J. (1951) Protein measurement with the folin phenol reagent. J. Biol. Chem. 193, 265-275.
46. Luo H., Shan X. and Wu J. (1996) Expression of human mitochondrial NADP-dependent isocitrate dehydrogenase during lymphocyte activation. J. Cell Biochem. 60, 495-507.
47. Macfarlane N., Mathews B. and Dalziel K. (1977) The purification and properties of NADP-dependent isocitrate dehydrogenase from ox-heart mitochondria. Eur. J. Biochem. 74, 553-559.
48. Nielsen H., Engelbrecht J., Brunak S. and von Heijne G. (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10, 1-6.
49. Numa S. (1974) Regulation of fatty-acid synthesis in higher animals. Ergeb Physiol. 69, 54-96.
50. Plaut G. W., Cook M. and Aogaichi T (1983) The subcellular location of isozymes of NADP-isocitrate dehydrogenase in tissues from pig, ox and rat. Biochim. Biophys. Acta 760, 300-308.
51. Rall T. W. and Lehninger A. L. (1952) Glutathione reductase of animal tissues. J. Biol. Chem. 194, 119-130.
52. Reynolds C. H., Kuchel P. W. and Dalziel K. (1978) Equilibrium binding of coenzymes and substrates to nicotinamide-adenine dinucleotide phosphate-linked isocitrate dehydrogenase from bovine heart mitochondria. Biochem. J. 171, 733-742.
53. Sazanov L. A. and Jackson J. B. (1994) Proton-translocating transhydrogenase and NAD- and NADP-linked isocitrate dehydrogenases operate in a substrate cycle which contributes to fine regulation of the tricarboxylic acid cycle activity in mitochondria. FEBS Lett. 344, 109-116.
54. Vogel R., Hamprecht B. and Wiesinger H. (1998) Malic enzyme isoforms in astrocytes: comparative study on activities in rat brain tissue and astroglia-rich primary cultures. Neurosci. Lett. 247, 123-126.
55. Vogel R., Wiesinger H., Hamprecht B. and Dringen R. (1999) The regeneration of reduced glutathione in rat forebrain mitochondria identifies metabolic pathways providing the NADPH required. Neurosci. Lett. 275, 97-100.
56. Wallace D. C. (2001) A mitochondrial paradigm for degenerative diseases and ageing. Novartis Found. Symp. 235, 247-263.
57. Winkler B. S., DeSantis N. and Solomon F. (1986) Multiple NADPH-producing pathways control glutathione (GSH) content in retina. Exp. Eye Res. 43, 829-847.
58. Yoshihara T., Hamamoto T., Munakata R., Tajiri R., Ohsumi M. and Yokota S. (2001) Localization of cytosolic NADP-dependent isocitrate dehydrogenase in the peroxisomes of rat liver cells: biochemical and immunocytochemical studies. J. Histochem. Cytochem. 49, 1123-1131.