Consequences of the α-ketoglutarate dehydrogenase inhibition for neuronal metabolism and survival: Implications for neurodegenerative diseases

Current Medicinal Chemistry

Volumn 19, Issue 34, 2012, Pages 5895-5906

  Trofimova, L K ^a   Araujo W L ^b,c   Strokina, A A ^d   Fernie, A R ^b   Bettendorff, L ^e   Bunik, V I ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^d INSTITUTE OF HYDROBIOLOGY   (Ukraine)

^e UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

ketoglutarate dehydrogenase; Cellular models of neurodegeneration; Metabolic engineering; Metabolic profiling; Mitochondria in neurodegenerative diseases; Succinyl phosphonate; Tricarboxylic acid cycle

Indexed keywords

OXOGLUTARATE DEHYDROGENASE;

ANIMAL CELL; ARTICLE; CELL METABOLISM; CELL VIABILITY; CONTROLLED STUDY; DEGENERATIVE DISEASE; DISEASE MODEL; ENZYME ACTIVITY; ENZYME INHIBITION; NONHUMAN; PATHOPHYSIOLOGY; RAT; REACTION ANALYSIS;

ANIMALS; CARBOHYDRATES; CELLS, CULTURED; CITRIC ACID CYCLE; ENZYME INHIBITORS; KETOGLUTARATE DEHYDROGENASE COMPLEX; METABOLOME; MITOCHONDRIA; MODELS, BIOLOGICAL; NEURODEGENERATIVE DISEASES; NEURONS; ORGANOPHOSPHONATES; OXIDATION-REDUCTION; RATS; SUCCINATES;

EID: 84871268346     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/092986712804143367     Document Type: Article

References (71)

1. Bunik, V. I.; Schloss, J. V.; Pinto, J. T.; Dudareva, N.; Cooper, A. J. L. A survey of oxidative paracatalytic reactions catalyzed by enzymes that generate carbanionic intermediates: implications for ROS production, cancer etiology, and neurodegenerative diseases. Adv. Enzymol Relat. Areas Mol Biol, 2011, 77, 307-360.
2. Gibson, G. E.; Blass, J. P.; Beal, M. F.; Bunik, V. The alphα-ketoglutaratedehydrogenase complex: A mediator between mitochondria and oxidative stress in neurodegeneration. Mol Neurobiol, 2005, 31(1-3), 43-63.
3. Parkhomenko, Y. M.; Kudryavtsev, P. A.; Pylypchuk, S. Y.; Chekhivska, L. I.; Stepanenko, S. P.; Sergiichuk, A. A.; Bunik, V. I. Chronic alcoholism in rats induces a compensatory response, preserving brain thiamine diphosphate, but the brain 2-oxo acid dehydrogenases are inactivated despite unchanged coenzyme levels. J. Neurochem., 2011, 117(6), 1055-1065.
4. Bunik, V. I.; Denton, T. T.; Xu, H.; Thompson, CM.; Cooper, A. J. L.; Gibson, G. E. Phosphonate analogs of α-ketoglutarate inhibit the activity of the aketoglutarate dehydrogenase complex isolated from brain and in cultured cells. Biochemistry, 2005, 44, 10552-10561.
5. Bunik, V. I.; Biryukov, A. I.; Zhukov, Y. N. Inhibition of pigeon breast muscle alphα-ketoglutarate dehydrogenase by phosphonate analogues of alphaketoglutarate. FEBS Lett, 1992, 303(2-3), 197-201.
6. Araújo, W. L.; Nunes-Nesi, A.; Trenkamp, S.; Bunik, V. I.; Fernie, A. R. Inhibition of 2-oxoglutarate dehydrogenase in potato tuber suggests the enzyme is limiting for respiration and confirms its importance in nitrogen assimilation. Plant Physiol, 2008, 148(4), 1782-1796.
7. Bunik, V. I.; Fernie, A. R. Metabolic control exerted by the 2-oxoglutarate dehydrogenase reaction: a cross-kingdom comparison of the crossroad between energy production and nitrogen assimilation. Biochem. J., 2009, 422(3), 405-421.
8. Bunik, V. I.; Lovat, M.; Groznaya, A.; Graf, A.; Dunaeva, T.; Trofimova, L.; Sokolova, N. Succinyl phosphonate, a protector of the 2-oxoglutarate dehydrogenase complex, corrects behavioral impairments in rats exposed to hypoxia or ethanol. Alzheimers Dement, 2009, 5(4, Supplement 1), P476-P477.
9. van der Merwe, M. J.; Osorio, S.; Araujo, W. L.; Balbo, I; Nunes-Nesi, A.; Maximova, E.; Carrari, F.; Bunik, V. I.; Persson, S.; Fernie, A. R. Tricarboxylic acid cycle activity regulates tomato root growth via effects on secondary cell wall production. Plant Physiol, 2010, 153(2), 611-621.
10. Trofimova, L.; Lovat, M.; Groznaya, A.; Efimova, E.; Dunaeva, T.; Maslova, M.; Graf, A.; Bunik, V. Behavioral impact of the regulation of the brain 2-oxoglutarate dehydrogenase complex by synthetic phosphonate analog of 2-oxoglutarate: implications into the role of the complex in neurodegenerative diseases. Int. J. Alzheimers Dis., 2010, doi:10.4061/2010/749061 (Article ID 749061).
11. Graf, A.; Trofimova, L.; Loshinskaja, A.; Mkrtchyan, G.; Strokina, A.; Lovat, M.; Tylicky, A.; Strumilo, S.; Bettendorff, L.; Bunik, V. I. Upregulation of 2-oxoglutarate dehydrogenase as a stress response. Int. J. Biochem. Cell Biol, 2012, 10.1016/j.biocel2012.07.002 (0).
12. Araújo, W. L.; Tohge, T.; Osorio, S.; Lohse, M.; Balbo, I; Krahnert, I; Sienkiewicz-Porzucek, A.; Usadel, B.; Nunes-Nesi, A.; Fernie, A. R. Antisense inhibition of the 2-oxoglutarate dehydrogenase complex in tomato demonstrates its importance for plant respiration and during leaf senescence and fruit maturation. Plant Cell, 2012, 24(6), 2328-2351.
13. Graf, A.; Kabysheva, M.; Klimuk, E.; Trofimova, L.; Dunaeva, T.; Zündorf, G.; Kahlert, S.; Reiser, G.; Storozhevykh, T.; Pinelis, V; Sokolova, N; Bunik, V Role of 2-oxoglutarate dehydrogenase in brain pathologies involving glutamate neurotoxicity. J. Mol Catal B Enzym., 2009, 61(1-2), 80-87.
14. Zündorf, G.; Kahlert, S.; Bunik, VI; Reiser, G. α- Ketoglutarate dehydrogenase contributes to production of reactive oxygen species in glutamate-stimulated hippocampal neurons in situ. Neuroscience, 2009, 158(2), 610-616.
15. Kabysheva, M. S.; Storozhevykh, T. P.; Pinelis, V. G.; Bunik, V. I. Synthetic regulators of the 2-oxoglutarate oxidative decarboxylation alleviate the glutamate excitotoxicity in cerebellar granule neurons. Biochem. Pharmacol, 2009, 77(9), 1531-1540.
16. Bunik, VI; Kabysheva, M. S.; Klimuk, E. I.; Storozhevykh, T. P.; Pinelis, VG. Phosphono analogues of 2-oxoglutarate protect cerebellar granule neurons upon glutamate excitotoxicity. Ann. N. Y. Acad. Sci, 2009, 1171, 521-529.
17. Shi, X.; Yao, D.; Chen, C. Identification of N-Acetyltaurine as a Novel Metabolite of Ethanol through Metabolomics-guided Biochemical Analysis. J. Biol Chem., 2012, 287(9), 6336-6349.
18. Lodi, A.; Ronen, S. M. Magnetic resonance spectroscopy detectable metabolomic fingerprint of response to antineoplastic treatment. Plos One, 2011, 6(10), e26155.
19. Johansen, K. K.; Wang, L.; Aasly, J. O.; White, L. R.; Matson, W. R.; Henchcliffe, C; Beal, M. F.; Bogdanov, M. Metabolomic profiling in LRRK2-related Parkinson's disease. Plos One, 2009, 4 (10).
20. Lisec, J.; Schauer, N.; Kopka, J.; Willmitzer, L.; Fernie, A. R. Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc, 2006, 1(1), 387-396.
21. O'Brien, J.; Wilson, I; Orton, T.; Pognan, F. Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur. J. Biochem., 2000, 267(17), 5421-5426.
22. Renner, C; Zemitzsch, N; Fuchs, B.; Geiger, K. D.; Hermes, M.; Hengstler, J.; Gebhardt, R.; Meixensberger, J.; Gaunitz, F. Carnosine retards tumor growth in vivo in an NIH3T3-HER2/neu mouse model. Mol Cancer, 2010, 9, 2.
23. Bettendorff, L.; Peeters, M.; Jouan, C; Wins, P.; Schoffeniels, E. Determination of thiamin and its phosphate esters in cultured neurons and astrocytes using an ion-pair reversed-phase high-performance liquid chromatographic method. Anal Biochem., 1991, 198(1), 52-59.
24. Dunckelmann, R. J.; Ebinger, F.; Schulze, A.; Wanders, R. J. A.; Rating, D.; Mayatepek, E. 2-ketoglutarate dehydrogenase deficiency with intermittent 2-ketoglutaric aciduria. Neuropediatrics, 2000, 31(1), 35-38.
25. Ketting, D.; Wadman, S. K.; Bruinvis, L.; Sweetman, L. The occurrence of lactyl lactate and succinyl lactate in the urine of patients screened for inherited metabolic disease. Clin. Chim. Acta, 1985, 146(1), 29-35.
26. Habbal, Z. M.; Chidiac-Tannoury, R. Lactic acid dimer: an artifact in the gas chromatographic analysis of urine with massive lactic acid aciduria. Clin. Chem., 2001, 47(5), 979-980.
27. Cooper, A. J. L. The role of glutamine transaminase K (GTK) in sulfur and alpha-keto acid metabolism in the brain, and in the possible bioactivation of neurotoxicants. Neurochem. Int., 2004, 44(8), 557-577.
28. Ma, T. C.; Campana, A.; Lange, P. S.; Lee, H.-H.; Banerjee, K.; Bryson, J. B.; Mahishi, L.; Alam, S.; Giger, R. J.; Barnes, S.; Morris, S. M., Jr.; Willis, D. E.; Twiss, J. L.; Filbin, M. T.; Ratan, R. R. A large-scale chemical screen for regulators of the arginase 1 promoter identifies the soy isoflavone daidzeinas a clinically approved small molecule that can promote neuronal protection or regeneration via a cAMP-independent pathway. J. Neurosci, 2010, 30(2), 739-748.
29. Cai, D. M.; Deng, K. W.; Mellado, W.; Lee, J.; Ratan, R. R.; Filbin, M. T. Arginase I and Polyamines act downstream from cyclic AMP in overcoming inhibition of axonal growth MAG and myelin in vitro. Neuron, 2002, 35(4), 711-719.
30. Christian, B. E.; Haque, M. E.; Spremulli, L. L. The effect of spermine on the initiation of mitochondrial protein synthesis. Biochem. Biophys. Res. Commun., 2010, 391(1), 942-946.
31. Deng, H.; Bloomfield, V. A.; Benevides, J. M.; Thomas, G. J. Structural basis of polyamine-DNA recognition: spermidine and spermine interactions with genomic B-DNAs of different GC content probed by Raman spectroscopy. Nucleic Acids Res, 2000, 28(17), 3379-3385.
32. Hobi, R.; Kuenzle, C. C. Deoxyribonucleic acid turnover in immature neurons of the rat cerebral cortex Neuroscience Letters, 1985, 58(3), 311-314.
33. Cheshchevik, V; Janssen, A. J. M.; Dremza, IK.; Zavodnik, IB.; Bunik, V. I. In Mitochondrial Physiology - The Many Functions of the Organism in our Cells. Renner-Sattler, K.; Gnaiger, E., Eds.; Steiger Druck GmbH: Axams, Austria 2010, pp 76-77.
34. Bunik, VI; Schloss, J. V; Pinto, J. T; Gibson, G. E.; Cooper, A. J. L. Enzymecatalyzed side reactions with molecular oxygen may contribute to cell signaling and neurodegenerative diseases. Neurochem. Res., 2007, 32(4-5), 871-891.
35. Sá Santos, S.; Gibson, G. E.; Cooper, A. J. L.; Denton, T. T; Thompson, CM.; Bunik, VI; Alves, P. M.; Sonnewald, U. Inhibitors of the α-ketoglutarate dehydrogenase complex alter [1-13C]glucose and [U-13C]glutamate metabolism in cerebellar granule neurons. J. Neurosci. Res., 2006, 83(3), 450-458.
36. Wilgus, H.; Roskoski, R. Inactivation of tyrosine hydroxylase activity by ascorbate in vitro and in rat PC12 cells. J. Neurochem., 1988, 51(4), 1232-1239.
37. Hutson, S. M.; Islam, M. M.; Zaganas, I. Interaction between glutamate dehydrogenase (GDH) and L-leucine catabolic enzymes: Intersecting metabolic pathways. Neurochem. Int., 2011, 58(4), 518-524.
38. Islam, M. M.; Nautiyal, M.; Wynn, R. M.; Mobley, J. A.; Chuang, D. T.; Hutson, S. M. Branched-chain amino acid metabolon: interaction of glutamate dehydrogenase with the mitochondrial branched-chain aminotrans ferase (BCATm). J. Biol. Chem., 2010, 285(1), 265-276.
39. Fahien, L. A.; Macdonald, M. J.; Teller, J. K.; Fibich, B.; Fahien, C. M. Kinetic advantages of hetero-enzyme complexes with glutamate dehydrogenase and the alphα-ketoglutarate dehydrogenase complex. J. Biol. Chem., 1989, 264(21), 12303-12312.
40. Fahien, L. A.; Teller, J. K. Glutamate-malate metabolism in liver mitochondria. A model constructed on the basis of mitochondrial levels of enzymes, specificity, dissociation constants, and stoichiometry of heteroenzyme complexes. J. Biol. Chem., 1992, 267(15), 10411-10422.
41. Islam, M. M.; Wallin, R.; Wynn, R. M.; Conway, M.; Fujii, H.; Mobley, J. A.; Chuang, D. T.; Hutson, S. M. A novel branched-chain amino acid metabolon - Protein-protein interactions in a supramolecular complex. J. Biol. Chem., 2007, 282(16), 11893-11903.
42. Zhadkevich, M. M.; Baratova, L. A.; Matveev, D. V. The amino acids of the blood in patients with peritonitis: the significance of Fisher's index [Article in Russian] Lab. Delo, 1989, 2(2), 29-32.
43. Zhadkevich, M. M.; Gelfand, B. R.; Matveev, D. V.; Belikov, V. M.; Latov, V. K.; Baratova, L. A. The influence of enteral probe nutrition on protein metabolism in patients with peritonitis [Article in Russian]. Vestnik Khirurgii, 1989, 142(1), 19-21.
44. Fernstrom, J. D.; Fernstrom, M. H. Tyrosine, phenylalanine, and catecholamine synthesis and function in the brain. J. Nutr., 2007, 137(6), 1539S-1547S.
45. Cole, J. T.; Mitala, C. M.; Kundu, S.; Verma, A.; Elkind, J. A.; Nissim, I.; Cohen, A. S. Dietary branched chain amino acids ameliorate injury-induced cognitive impairment. Proc. Natl. Acad. Sci. USA, 2010, 107(1), 366-371.
46. Grioli, S.; Lomeo, C.; Quattropani, M. C.; Spignoli, G.; Villardita, C. Pyroglutamic acid improves the age associated memory impairment. Fundam. Clin. Pharmacol., 1990, 4(2), 169-173.
47. Orlowski, M.; Meister, A. The gamma-glutamyl cycle: A possible transport system for amino acids. Proc. Natl. Acad. Sci. USA, 1970, 67(3), 1248-1255.
48. Viña, J. R.; Palacin, M.; Puertes, I. R.; Hernandez, R.; Viña, J. Role of the gamma-glutamyl cycle in the regulation of amino acid translocation. Am J Physiol., 1989, 257(6), E916-E922.
49. Hanigan, M. H.; Ricketts, W. A. Extracellular glutathione is a source of cysteine for cells that express gamma-glutamyl transpeptidase. Biochemistry, 1993, 32(24), 6302-6306.
50. Cui, X.; Zuo, P.; Zhang, Q.; Li, X.; Hu, Y.; Long, J.; Packer, L.; Liu, J. Chronic systemic D-galactose exposure induces memory loss, neuro degeneration, and oxidative damage in mice: Protective effects of R-alphalipoic acid. J. Neurosci. Res., 2006, 84(3), 647-654.
51. Haverkorn van Rijsewijk, B. R. B.; Nanchen, A.; Nallet, S.; Kleijn, R. J.; Sauer, U. Large-scale 13C-flux analysis reveals distinct transcriptional control of respiratory and fermentative metabolism in Escherichia coli. Mol Syst Biol, 2011, 7.
52. Davis, W. L.; Goodman, D. B. P. Evidence for the glyoxylate cycle in human liver. Anat. Rec., 1992, 234(4), 461-468.
53. Davis, W. L.; Jones, R. G.; Farmer, G. R.; Dickerson, T.; Cortinas, E.; Cooper, O. J.; Crawford, L.; Goodman, D. B. P. Identification of glyoxylate cycle enzymes in chick liver-the effect of vitamin D3: cytochemistry and biochemistry. Anat. Rec., 1990, 227(3), 271-284.
54. Volvenkin, S. V.; Popov, V. N.; Eprintsev, A. T. Subcellular localization and properties of glyoxylate cycle enzymes in the liver of rats with alloxan diabetes. Biochemistry (Moscow), 1999, 64(9), 994-999.
55. Morgunov, I. G.; Kondrashova, M. N.; Kamzolova, S. V.; Sokolov, A. P.; Fedotcheva, N. I.; Finogenova, T. V. Evidence of the glyoxylate cycle in the liver of newborn rats. Med. Sci. Monit., 2005, 11(2), BR57-BR60.
56. Popov, V. N.; Igamberdiev, A. U.; Schnarrenberger, C.; Volvenkin, S. V. Induction of glyoxylate cycle enzymes in rat liver upon food starvation. FEBS Lett., 1996, 390(3), 258-260.
57. Rodionov, R. N.; Murry, D. J.; Vaulman, S. F.; Stevens, J. W.; Lentz, S. R. Human alanine-glyoxylate aminotransferase 2 lowers asymmetric dimethylarginine and protects from inhibition of nitric oxide production. J. Biol. Chem., 2010, 285(8), 5385-5391.
58. Gon, S.; Napolitano, R.; Rocha, W.; Coulon, S.; Fuchs, R. P. Increase in dNTP pool size during the DNA damage response plays a key role in spontaneous and induced-mutagenesis in Escherichia coli. Proc. Natl. Acad. Sci. USA, 2011, 108(48), 19311-19316.
59. Wu, G. Amino acids: metabolism, functions, and nutrition. Amino Acids, 2009, 37(1), 1-17.
60. Cho, B.-K.; Federowicz, S.; Park, Y.-S.; Zengler, K.; Palsson, B. O. Deciphering the transcriptional regulatory logic of amino acid metabolism. Nat. Chem. Biol., 2012, 8(1), 65-71.
61. Noguchi, Y.; Meyer, T.; Tiao, G.; Fischer, J. E.; Hasselgren, P. O. Sepsis increases putrescine concentration and protein synthesis in mucosa of small intestine in rats. Shock, 1996, 5(5), 333-340.
62. Mihm, S.; Risso, A.; Stöhr, M.; Oberdorfer, F.; Dröge, W. Downregulation of T cell growth factor production by ornithine decarboxylase and its product putrescine: D, L-alpha-difluoromethylornithine suppresses general protein synthesis but augments simultaneously the production of interleukin-2. Exp. Cell Res., 1989, 180(2), 383-398.
63. Muhyaddin, M.; Roberts, P. J.; Woodruff, G. N. Presynaptic gammaaminobutyric acid receptors in the rat anococcygeus muscle and their antagonism by 5-aminovaleric acid. Br. J. Pharmacol., 1982, 77(1), 163-168.
64. Bibb, J. A.; Mayford, M. R.; Tsien, J. Z.; Alberini, C. M. Cognition Enhancement Strategies. J. Neurosci., 2010, 30(45), 14987-14992.
65. Bunik, V. I.; Strumilo, S. Regulation of catalysis within cellular network: metabolic and signaling implications of the 2-oxoglutarate oxidative decarboxylation. Curr. Chem. Biol., 2009, 3(3), 279-290.
66. McCandless, D. W. Energy metabolism in the lateral vestibular nucleus in pyrithiamin-induced thiamin deficiency. Ann. N. Y. Acad. Sci., 1982, 378, 355-364.
67. Butterworth, R. F.; Leong, D. K. In Biochemistry and Physiology of Thiamine Diphosphate Enzymes. Bisswanger, H.; Schellenberger, A., Eds.; Vch Pub: Weinheim, New York. 1996, pp 409-416.
68. Zeiger, S. L. H.; McKenzie, J. R.; Stankowski, J. N.; Martin, J. A.; Cliffel, D. E.; McLaughlin, B. Neuron specific metabolic adaptations following multi-day exposures to oxygen glucose deprivation. Biochim. Biophys. Acta, 2010, 1802(11), 1095-1104.
69. Gourine, A. V.; Wood, J. D.; Burnstock, G. Purinergic signalling in autonomic control. Trends Neurosci., 2009, 32(5), 241-248.
70. Koizumi, S.; Fujishita, K.; Inoue, K. Regulation of cell-to-cell communication mediated by astrocytic AT P in the CNS. Purinergic Signal., 2005, 1(3), 211-217.
71. Mason, E. F.; Rathmell, J. C. Cell metabolism: An essential link between cell growth and apoptosis. Biochim. Biophys. Acta, 2011, 1813(4), 645-654.