Antioxidant capacity contributes to protection of ketone bodies against oxidative damage induced during hypoglycemic conditions

Experimental Neurology

Volumn 211, Issue 1, 2008, Pages 85-96

  Haces, María L ^a   Hernández Fonseca, Karla ^a   Medina Campos, Omar N ^b   Montiel, Teresa ^a   Pedraza Chaverri, José ^b   Massieu, Lourdes ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b Universidad Nacional Autonoma de Mexico Facultad de Quimica   (Mexico)

Author keywords

hydroxybutyrate; Acetoacetate; Antioxidant capacity; Brain; Hypoglycemia; Iodoacetate; Oxidative stress; Scavenger

Indexed keywords

3 HYDROXYBUTYRIC ACID; ACETOACETIC ACID; ADENOSINE TRIPHOSPHATE; HYDROXYL RADICAL; IODOACETIC ACID; KETONE BODY; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; HIPPOCAMPUS; HYPOGLYCEMIA; LIPID PEROXIDATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ADENOSINE TRIPHOSPHATE; ALKYLATING AGENTS; ANALYSIS OF VARIANCE; ANIMALS; ANTIOXIDANTS; CELL COUNT; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; HIPPOCAMPUS; HYPOGLYCEMIA; INSULIN; IODOACETATES; KETONE BODIES; MALE; NEURONS; OXIDATION-REDUCTION; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 43049127389     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2007.12.029     Document Type: Article

References (74)

1. Adibhatla M.R., and Hatcher J.F. Phospholipase A2, reactive oxygen species, and lipid peroxidation in cerebral ischemia. Free Radic. Biol. Med. 40 (2006) 376-387
2. Ballesteros J.R., Mishra O.P., and McGowan J.E. Alterations in cerebral mitochondria during acute hypoglycemia. Biol. Neonate 84 (2003) 159-163
3. Berridge M.V., and Tan S. Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT): subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Arch. Biochem. Biophys. 303 (1993) 474-482
4. Bindokas V.P., Jordán J., Chong C.L., and Miller R.J. Superoxide production in rats hippocampal neurons: selective imaging with hydroethidine. J. Neurosci. 16 (1996) 1324-1336
5. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
6. Bulteau A.L., Lundberg K.C., Humphries K.M., Sadek H.A., Szweda P.A., Friguet B., and Szweda L.I. Oxidative modification and inactivation of the proteasome coronary during occlusion/reperfusion. J. Biol. Chem. 276 (2001) 30057-30063
7. Esterbauer H., Schaur R.J., and Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 11 (1991) 1-128
8. Ferrington D.A., and Kapphahn R.J. Catalytic site-specific inhibition of the 20S proteasome by 4-hydroxynonenal. FEBS Lett. 578 (2004) 217-223
9. Floriano-Sánchez E., Villanueva C., Medina-Campos O.N., Rocha D., Sánchez-González D.J., Cárdenas-Rodríguez N., and Pedraza-Chaverri J. Nordihydroguaiaretic acid is a potent in vitro scavenger of peroxynitrite, singlet oxygen, hydroxyl radical, superoxide anion and hypochlorous acid and prevents in vivo ozone-induced tyrosine nitration in lungs. Free Radic. Res. 40 (2006) 523-533
10. Friguet B., and Szweda L.I. Inhibition of the multicatalytic proteinase (proteasome) by 4-hydroxy-2-nonenal cross-linked protein. FEBS Lett. 405 (1997) 21-25
11. García O., and Massieu L. Strategies for neuroprotection against L-trans-2,4-pyrrolidine dicarboxylate-induced neuronal damage during energy impairment in vitro. J. Neurosci. Res. 64 (2001) 418-428
12. Gluck M.R., Jayatilleke E., Shaw S., Rowan A.J., and Haroutunian V. CNS oxidative stress associated with kainic acid rodent model of experimental epilepsy. Epilepsy Res. 39 (2000) 63-71
13. Gomes A., Fernandes E., and Lima J.L. Fluorescence probes used for detection of reactive oxygen species. J. Biochem. Biophys. Methods 65 (2005) 45-80
14. Hawkins R.A., Williamson D.H., and Krebs H.A. Ketone-body utilization by adult and suckling rat brain in vivo. Biochem. J. 122 (1971) 13-18
15. Hawkins R.A., and Biebuyck J.F. Ketone bodies are selectively used by individual brain regions. Science 205 (1979) 325-327
16. Hernández-Fonseca K., and Massieu L. Disruption of endoplasmic reticulum calcium stores is involved in neuronal death induced by glycolysis inhibition in cultured hippocampal neurons. J. Neurosci. Res. 82 (2005) 196-205
17. Hernández-Fonseca, K., Cárdenas-Rodríguez, N., Pedraza-Chaverri, J., Massieu, L., in press. Calcium-dependent production of reactive oxygen species is involved in neuronal damage induced during glycolysis inhibition in cultured hippocampal neurons. J. Neurosci. Res. doi:10.1002/jnr.21634.
18. Hockenbery D.M., Oltvai Z.N., Yin X.-M., Milliman C.L., and Korsmeye S.J. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75 (1993) 241-251
19. Izumi Y., Ishii K., Katsuki H., Benz A.M., and Zorumski C.F. beta-Hydroxybutyrate fuels synaptic function during development. Histological and physiological evidence in rat hippocampal slices. J. Clin. Invest. 101 (1998) 1121-1132
20. Jain S.K., Kannan K., and Lim G. Ketosis (acetoacetate) can generate oxygen radicals and cause increased lipid peroxidation and growth inhibition in human endothelial cells. Free Radic. Biol. Med. 25 (1998) 1083-1088
21. Jain S.K., and McVie R. Hyperketonemia can increase lipid peroxidation and lower glutathione levels in human erythrocytes in vitro and in type I diabetic patients. Diabetes 48 (1999) 1850-1855
22. Kashiwaya Y., King M.T., and Veech R.L. Substrate signaling by insulin: a ketone bodies ratio mimics insulin action in heart. Am. J. Cardiol. 80 (1997) 50A-64A
23. Kashiwaya Y., Takeshima T., Mori N., Nakashima K., Clarke K., and Veech R.L. D-beta-Hydroxybutyrate protects neurons in models of Alzheimer's and Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 5440-5444
24. Kim Y., Davis L.M., Sullivan P.G., Maalouf M., Simeone T.A., van Brederode J., and Rho J.M. Ketone bodies are protective against oxidative stress in neocortical neurons. J. Neurochem. 101 (2007) 1316-1326
25. Kossoff E.H., Pyzik P.L., McGrogan J.R., Vining E.P., and Freeman J.M. Efficacy of the ketogenic diet for infantile spasms. Pediatrics 109 (2002) 780-783
26. Lincoln B.C., Des Rosiers C., and Brunengraber H. Metabolism of S-3-hydroxybutyrate in the perfused rat liver. Arch. Biochem. Biophys. 259 (1987) 149-156
27. Love S. Oxidative stress in brain ischemia. Brain Pathol. 9 (1999) 119-131
28. Maalouf M., Sullivan P.G., Davis L., Kim D.Y., and Rho J.M. Ketones inhibit mitochondrial production of reactive oxygen species production following glutamate excitotoxicity by increasing NADH oxidation. Neuroscience 145 (2007) 256-264
29. Malcolm C.S., Benwell K.R., Lamb H., Bebbington D., and Porter R.H. Characterization of iodoacetate-mediated neurotoxicity in vitro using primary cultures of rat cerebellar granule cells. Free Radic. Biol. Med. 28 (2000) 102-107
30. Massieu L., Del Rio P., and Montiel T. Neurotoxicity of glutamate uptake inhibition in vivo: correlation with succinate dehydrogenase activity and prevention by energy substrates. Neuroscience 106 (2001) 669-677
31. Massieu L., Haces M.L., Montiel T., and Hernández-Fonseca K. Acetoacetate protects hippocampal neurons against glutamate-mediated neuronal damage during glycolysis inhibition. Neuroscience 120 (2003) 365-378
32. Masuda R., Monahan J.W., and Kashiwaya Y. D-beta-hydroxybutyrate is neuroprotective against hypoxia in serum-free hippocampal primary cultures. J. Neurosci. Res. 80 (2005) 501-509
33. McGowan J.E., Chen L., Gao D., Trush M., and Wei C. Increased mitochondrial reactive oxygen species production in newborn brain during hypoglycemia. Neurosci. Lett. 399 (2006) 111-114
34. Medina-Campos O.N., Barrera D., Segoviano-Murillo S., Rocha D., Maldonado P.D., Mendoza-Patino N., and Pedraza-Chaverri J. S-allylcysteine scavenges singlet oxygen and hypochlorous acid and protects LLC-PK(1) cells of potassium dichromate-induced toxicity. Food Chem. Toxicol. 45 (2007) 2030-2039
35. Mejía-Toiber J., Montiel T., and Massieu L. D-β-Hydroxybutyrate prevents glutamate-mediated lipoperoxidation and neuronal damage elicited during glycolysis inhibition in vivo. Neurochem. Res. 31 (2006) 1399-1408
36. Mellanby J., and Williamson D.H. Acetoacetate. In: Bergmeyer H.U. (Ed). Methods of Enzymatic Analysis (1965), Academic Press, New York 454-457
37. Mosmann T. Rapid colorimetric assay for cellular growth and survival. Application to proliferation and cytotoxicity assay. J. Immunol. Methods 65 (1983) 55-63
38. Nehlig A., and Pereira de Vasconcelos A. Glucose and ketone bodies utilization by the brain of neonatal rats. Prog. Neurobiol. 40 (1993) 163-221
39. Noh H.S., Hah Y.S., Nilufar R., Han J., Bong J.H., Kang S.S., Cho G.J., and Choi W.S. Acetoacetate protects neuronal cells from oxidative glutamate toxicity. J. Neurosci. Res. 83 (2006) 702-709
40. Nordli D.R., Kuroda M.M., Carroll J., Koenigsberger D.Y., Hirsch L.J., Bruner H.J., Seidel W.T., and De Vivo D.C. Experience with ketogenic diet in infants. Pediatrics 108 (2001) 129-133
41. Okada K., Wangpoengtrakul C., Osawa T., Toyokuni S., Tanaka K., and Uchida K. 4-Hydroxy-2-nonenal-mediated impairment of intracellular proteolysis during oxidative stress. Identification of proteasomes as target molecules. J. Biol. Chem. 274 (1999) 23787-23793
42. Owen O.E., Morgan A.P., Kemp H.G., Sullivan J.M., Herrera M.G., and Cahill Jr. G.F. Brain metabolism during fasting. J. Clin. Invest. 46 (1967) 1589-1595
43. Pan J.W., Bebin E.M., Chu W.J., and Hetherington H.P. Ketosis and epilepsy: 31P spectroscopic imaging at 4.1 T. Epilepsia 40 (1999) 703-707
44. Patočková J., Marhol P., Tumova E., Krsiak M., Rokyta R., Stipek S., Crkovska J., and Andel M. Oxidative stress in the brain tissue of laboratory mice with acute post insulin hypoglycemia. Physiol. Res. 52 (2003) 131-135
45. Pedraza-Chaverri J., Medina-Campos O.N., and Segoviano-Murillo S. Effect of heating on peroxynitrite scavenging capacity of garlic. Food Chem. Toxicol. 45 (2007) 622-627
46. Petersen D.R., and Doorn J.A. Reactions of 4-hydroxynonenal with proteins and cellular targets. Free Radic. Biol. Med. 37 (2004) 937-945
47. Rego A.C., Santos M.S., and Oliveira C.R. Adenosine triphosphate degradation products after oxidative stress and metabolic dysfunction in cultured retinal cells. J. Neurochem. 69 (1997) 1228-1235
48. Rego A.C., Santos M.S., and Oliveira C.R. Influence of the antioxidants vitamin E and idebenone on retinal cell injury mediated by chemical ischemia, hypoglycemia, or oxidative stress. Free Radic. Biol. Med. 26 (1999) 1405-1417
49. Robinson K.M., Janes M.S., Pehar M.P., Monette J.S., Ross M.F., Hagen T.M., Murphy M.P., and Beckman J.S. Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc. Natl. Acad. Sci. 103 (2006) 15038-15043
50. Sato N., Shimizu H., Shimomura Y., Suwa K., Mori M., and Kobayashi I. Mechanism of inhibitory action of ketone bodies on the production of reactive oxygen intermediates (ROIS) by polymorphonuclear leukocytes. Life Sci. 51 (1992) 113-118
51. Sato K., Kashiwaya Y., Keon C.A., Tsuchiya N., King M.T., Radda G.K., Chance B., Clarke K., and Veech R.L. Insulin, ketone bodies, and mitochondrial energy transduction. FASEB J. 9 (1995) 651-658
52. Shringarpure R., Grune T., Sitte N., and Davies K.J. 4-Hydroxynonenal-modified amyloid-beta peptide inhibits the proteasome: possible importance in Alzheimer's disease. Cell. Mol. Life Sci. 57 (2000) 1802-1809
53. Singh P., Jain A., and Kaur G. Impact of hypoglycemia and diabetes on CNS: correlation of mitochondrial oxidative stress with DNA damage. Mol. Cell. Biochem. 260 (2004) 153-159
54. Smith S.L., Heal D.J., and Martin K.F. KTX 0101: a potential metabolic approach to cytoprotection in major surgery and neurological disorders. CNS Drug Rev. 11 (2005) 113-140
55. Sperling O., Bromberg Y., Oelsner H., and Zoref-Shani E. Reactive oxygen species play an important role in iodacetate-induced neurotoxicity in primary rat neuronal cultures and in differentiated PC12 cells. Neurosci. Lett. 351 (2003) 137-140
56. Suh S.W., Aoyama K., Chen Y., Garnier P., Matsumori Y., Gum E., Liu J., and Swanson R.A. Hypoglycemic neuronal death and cognitive impairment are prevented by poly(ADP-ribose) polymerase inhibitors administered after hypoglycemia. J. Neurosci. 23 (2003) 10681-10690
57. Suh S.W., Gum E.T., Hamby A.M., Chan P.H., and Swanson R.A. Hypoglycemic neuronal death is triggered by glucose reperfusion and activation of neuronal NADPH oxidase. J. Clin. Invest. 117 (2007) 910-918
58. Suzuki M., Suzuki M., Sato K., Dohi, Sato T., Matsuura A., and Hiraide A. Effect of beta-hydroxybutyrate, a cerebral function improving agent, on cerebral hypoxia, anoxia and ischemia in mice and rats. Jpn. J. Pharmacol. 87 (2001) 143-150
59. Suzuki M., Suzuki M., Kitamura Y., Mori S., Sato K., Dohi S., Sato T., Matsuura A., and Hiraide A. β-hydroxybutyrate, a cerebral function improving agent, protects rat brain against ischemic damage caused by permanent and transient focal cerebral ischemia. Jpn. J. Pharmacol. 89 (2002) 36-43
60. Szweda L.I., Uchida K., Tsai L., and Stadtman E.R. Inactivation of glucose-6-phosphate dehydrogenase by 4-hydroxy-2-nonenal. Selective modification of an active-site lysine. J. Biol. Chem. 268 (1993) 3342-3347
61. Tieu K., Perier C., Caspersen C., Teismann P., Wu D.C., Yan S.D., Naini A., Vila M., Jackson-Lewis V., Ramasamy R., and Przedborski S. D-beta-hydroxybutyrate rescues mitochondrial respiration and mitigates features of Parkinson disease. J. Clin. Invest. 112 (2003) 892-901
62. Tomizawa S., Imai H., Tsukada S., Simizu T., Honda F., Nakamura M., Nagano T., Urano Y., Matsuoka Y., Fukasaku N., and Saito N. The detection and quantification of highly reactive oxygen species using the novel HPF fluorescence probe in a rat model of focal cerebral ischemia. Neurosci. Res. 53 (2005) 304-313
63. Uchida K., and Stadtman E.R. Covalent attachment of 4-hydroxynonenal to glyceraldehyde-3-phosphate dehydrogenase. A possible involvement of intra- and intermolecular cross-linking reaction. J. Biol. Chem. 268 (1993) 6388-6393
64. Uto A., Dux E., Kusumoto M., and Hossmann K.A. Delayed neuronal death after brief histotoxic hypoxia in vitro. J. Neurochem. 64 (1995) 2185-2192
65. Vander Jagt D.L., Hunsaker L.A., Vander Jagt T.J., Gomez M.S., Gonzales D.M., Deck L.M., and Royer R.E. Inactivation of glutathione reductase by 4-hydroxynonenal and other endogenous aldehydes. Biochem. Pharmacol. 53 (1997) 1133-1140
66. Veech R.L., Chance B., Kashiwaya Y., Lardy H.A., and Cahill Jr. G.F. Ketone bodies, potential therapeutic uses. IUBMB Life 51 (2001) 241-247
67. Vining E.P.G. Clinical efficacy of the ketogenic diet. Epilepsy Res. 37 (1999) 181-190
68. Williamson D.H., and Mellanby J. D(-)-β-hydroxybutyrate. In: Bergmeyer H.U. (Ed). Methods of Enzymatic Analysis (1965), Academic press, New York 459-461
69. Willmore L.J. Post-traumatic epilepsy: cellular mechanisms and implications for treatment. Epilepsia 31 (1990) S67-S73
70. Yamada K.A., Rensing N., and Thio L.L. Ketogenic diet reduces hypoglycemia-induced neuronal death in young rats. Neurosci. Lett. 385 (2005) 210-214
71. Yudkoff M., Daikhin Y., Nissim I., Lazarow A., and Nissim I. Ketogenic diet, amino acid metabolism and seizure control. J. Neurosci. Res. 66 (2001) 931-940
72. Zeevalk G.D., and Nicklas W.J. Chemically induced hypoglycemia and anoxia: relationship to glutamate receptor-mediated toxicity in retina. J. Pharmacol. Exp. Ther. 253 (1990) 1285-1292
73. Zhao H., Kalivendi S., Zhang H., Joseph J., Nithipatikom K., Vásquez-Vivar J., and Kalyanaraman B. Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide. Free Radic. Biol. Med. 34 (2003) 1359-1368
74. Ziegler D.R., Ribeiro L.C., Hagenn M., Siqueira I.R., Araújo E., Torres I.L., Gottfried C., Netto C.A., and Gonçalves C.A. Ketogenic diet increases glutathione peroxidase activity in the rat hippocampus. Neurochem. Res. 28 (2003) 1793-1797