Cortical and hippocampal mitochondria bioenergetics and oxidative status during hyperglycemia and/or insulin-induced hypoglycemia

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1802, Issue 11, 2010, Pages 942-951

  Cardoso, Susana ^a,b   Santos, Maria S ^a,b   Seiça, Raquel ^c   Moreira, Paula I ^a,c  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Cortex; Hippocampus; Hyperglycemia; Insulin induced hypoglycemia; Mitochondria; Oxidative stress

Indexed keywords

CITRIC ACID; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HYDROGEN PEROXIDE; INSULIN; MANGANESE SUPEROXIDE DISMUTASE; STREPTOZOCIN; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BIOENERGY; BRAIN CORTEX; BRAIN MITOCHONDRION; CONTROLLED STUDY; ENZYME ACTIVITY; GLYCEMIC CONTROL; HIPPOCAMPUS; HYPERGLYCEMIA; HYPOGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; LEARNING; MALE; MEMORY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; RESPIRATORY CHAIN;

ANIMALS; BLOOD GLUCOSE; CEREBRAL CORTEX; DIABETES MELLITUS, EXPERIMENTAL; ENERGY METABOLISM; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; HEMOGLOBIN A, GLYCOSYLATED; HIPPOCAMPUS; HYPERGLYCEMIA; INSULIN; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; OXIDATION-REDUCTION; OXIDATIVE PHOSPHORYLATION; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; STREPTOZOCIN; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

RATTUS; RATTUS NORVEGICUS;

EID: 77956710094     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2010.07.001     Document Type: Article

References (65)

1. Wrighten S.A., Piroli G.G., Grillo C.A., Reagan L.P. A look inside the diabetic brain: contributors to diabetes-induced brain aging. Biochim. Biophys. Acta 2009, 1792:444-453.
2. Daneman D. Type 1 diabetes. Lancet 2006, 367:847-858.
3. Wessels A.M., Scheltens P., Barkhof F., Heine R.J. Hyperglycaemia as a determinant of cognitive decline in patients with type 1 diabetes. Eur. J. Pharmacol. 2008, 585:88-96.
4. McCrimmon R.J., Frier B.M. Hypoglycaemia, the most feared complication of insulin therapy. Diab. Metab. 1994, 20:503-512.
5. Wieloch T., Engelsen B., Westerberg E., Auer R. Lesions of the glutamatergic cortico-striatal projections in the rat ameliorate hypoglycemic brain damage in the striatum. Neurosci. Lett. 1985, 58:25-30.
6. Engelsen B., Westerberg E., Fonnum F., Wieloch T. Effect of insulin-induced hypoglycemia on the concentrations of glutamate and related amino acids and energy metabolites in the intact and decorticated rat neostriatum. J. Neurochem. 1986, 47:1634-1641.
7. Auer R.N. Hypoglycemic brain damage. Forensic Sci. Int. 2004, 146:105-110.
8. Suh S.W., Aoyama K., Matsumori Y., Liu J., Swanson R.A. Pyruvate administered after severe hypoglycemia reduces neuronal death and cognitive impairment. Diabetes 2005, 54:1452-1458.
9. Draelos M.T., Jacobson A.M., Weinger K., Widom B., Ryan C.M., Finkelstein D.M., Simonson D.C. Cognitive function in patients with insulin-dependent diabetes mellitus during hyperglycemia and hypoglycemia. Am. J. Med. 1995, 98:135-144.
10. Ryan C.M., Williams T.M. Effects of insulin-dependent diabetes on learning and memory efficiency in adults. J. Clin. Exp. Neuropsychol. 1993, 15:685-700.
11. Alvarez E.O., Beauquis J., Revsin Y., Banzan A.M., Roig P., De Nicola A.F., Saravia F. Cognitive dysfunction and hippocampal changes in experimental type 1 diabetes. Behav. Brain Res. 2009, 198:224-230.
12. Gispen W.H., Biessels G.J. Cognition and synaptic plasticity in diabetes mellitus. Trends Neurosci. 2000, 23:542-549.
13. Beal M.F. Mitochondria take center stage in aging and neurodegeneration. Ann. Neurol. 2005, 58:495-505.
14. Moreira P.I., Santos M.S., Seiça R., Oliveira C.R. Brain mitochondrial dysfunction as a link between Alzheimer's disease and diabetes. J. Neurol. Sci. 2007, 257:206-214.
15. Moreira P.I., Santos M.S., Sena C., Seiça R., Oliveira C.R. Insulin protects against amyloid β-peptide toxicity in brain mitochondria of diabetic rats. Neurobiol. Dis. 2005, 18:628-637.
16. Mastrocola R., Restivo F., Vercellinatto I., Danni O., Brignardello E., Aragno M., Boccuzzi G. Oxidative and nitrosative stress in brain mitochondria of diabetic rats. J. Endocrinol. 2005, 187:37-44.
17. Nakhaee A., Bokaeian M., Akbarzadeh A., Hashemi M. Sodium tungstate attenuate oxidative stress in brain tissue of streptozotocin-induced diabetic rats. Biol Trace Elem. Res. 2010, 136:221-231.
18. Ferrand-Drake M., Friberg H., Wieloch T. Mitochondrial permeability transition induced DNA-fragmentation in the rat hippocampus following hypoglycemia. Neuroscience 1999, 90:1325-1338.
19. Ballesteros J.R., Mishra O.P., McGowan J.E. Alterations in cerebral mitochondria during acute hypoglycemia. Biol. Neonate 2003, 84:159-163.
20. McGowan J.E., Chen L., Gao D., Trush M., Wei C. Increased mitochondrial reactive oxygen species production in newborn brain during hypoglycemia. Neurosci. Lett. 2006, 399:111-114.
21. Gornall A.G., Bardawill C.J., David M.M. Determination of serum proteins by means of the biuret reaction. J. Biol. Chem. 1949, 177:751-766.
22. Estabrook R.E. Mitochondrial respiratory control and the polarographic measurement of ADP/O ratios. Methods Enzymol. 1967, 10:41-47.
23. Chance B., Williams G.R. The respiratory chain and oxidative phosphorylation. Adv. Enzymol. Relat. Subj. Biochem. 1956, 17:65-134.
24. Kamo N., Muratsugu M., Hongoh R., Kobatake Y. Membrane potential of mitochondria measured with an electrode sensitive to tetraphenyl phosphonium and relationship between proton electrochemical potential and phosphorylation potential in steady state. J. Membr. Biol. 1979, 49:105-121.
25. +) to measure membrane potentials in mitochondria: membrane binding and respiratory effects. Biophys. J. 1984, 45:92.
26. Muratsugu M., Kamo N., Kurihara K., Kobatake Y. Selective electrode for dibenzyl dimethyl ammonium cation as indicator of the membrane potential in biological systems. Biochim. Biophys. Acta 1977, 464:613-619.
27. Ernster L., Nordenbrand K. Microsomal lipid peroxidation. Methods Enzymol. 1967, 10:574-580.
28. Barja G. Mitochondrial oxygen radical generation and leak: sites of production in states 4 and 3, organ specificity, and relation to aging and longevity. J. Bioenerg. Biomembr. 1999, 31:347-366.
29. Hissin P.J., Hilf R. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal. Biochem. 1976, 74:214-226.
30. Flohé L., Günzler W.A. Assays of glutathione peroxidase. Methods Enzymol. 1984, 105:114-121.
31. Carlberg I., Mannervik B. Glutathione reductase. Methods Enzymol. 1985, 113:484-490.
32. Flohé L., Otting F. Superoxide dismutase assays. Methods Enzymol. 1984, 105:93-104.
33. Ramakrishna V., Jailkhani R. Evaluation of oxidative stress in Insulin Dependent Diabetes Mellitus (IDDM) patients. Diagn. Pathol. 2007, 2:22.
34. Nordfeldt S., Ludvigsson J. Adverse events in intensively treated children and adolescents with type 1 diabetes. Acta Paediatr. 1999, 88:1184-1193.
35. McNay E.C., Williamson A., McCrimmon R.J., Sherwin R.S. Cognitive and neural hippocampal effects of long-term moderate recurrent hypoglycemia. Diabetes 2006, 55:1088-1095.
36. Herzog R.I., Chan O., Yu S., Dziura J., McNay E.C., Sherwin R.S. Effect of acute and recurrent hypoglycemia on changes in brain glycogen concentration. Endocrinology 2008, 149:1499-1504.
37. Suh S.W., Hamby A.M., Swanson R.A. Hypoglycemia, brain energetics, and hypoglycemic neuronal death. Glia 2007, 55:1280-1286.
38. Foster K.A., Galeffi F., Gerich F.J., Turner D.A., Müller M. Optical and pharmacological tools to investigate the role of mitochondria during oxidative stress and neurodegeneration. Prog. Neurobiol. 2006, 79:136-171.
39. Moreira P.I., Santos M.S., Moreno A.M., Proença T., Seiça R., Oliveira C.R. Effect of streptozotocin-induced diabetes on rat brain mitochondria. J. Neuroendocrinol. 2004, 16:32-38.
40. Cardoso S., Correia S., Santos R.X., Carvalho C., Santos M.S., Oliveira C.R., Perry G., Smith M.A., Zhu X., Moreira P.I. Insulin is a two-edged knife on the brain. J. Alzheimers Dis. 2009, 18:483-507.
41. Duarte A.I., Santos M.S., Seiça R., Oliveira C.R. Oxidative stress affects synaptosomal gamma-aminobutyric acid and glutamate transport in diabetic rats: the role of insulin. Diabetes 2004, 53:2110-2116.
42. Duarte A.I., Santos P., Oliveira C.R., Santos M.S., Rego C. Insulin neuroprotection against oxidative stress is mediated by Akt and GSK-3beta signaling pathways and changes in protein expression. Biochim. Biophys. Acta 2008, 1783:994-1002.
43. Agardh C.D., Kalimo H., Olsson Y., Siesjö B.K. Hypoglycemic brain injury: I. Metabolic and light microscopic findings in rat cerebral cortex during profound insulin-induced hypoglycemia and in the recovery period following glucose administration. Acta Neuropathol. 1980, 50:31-41.
44. Agardh C.D., Chapman A.G., Pelligrino D., Siesjö B.K. Influence of severe hypoglycemia on mitochondrial and plasma membrane function in rat brain. J. Neurochem. 1982, 38:662-668.
45. Moreira P.I., Duarte A.I., Santos M.S., Rego A.C., Oliveira C.R. An integrative view of the role of oxidative stress, mitochondria and insulin in Alzheimer's disease. J. Alzheimers Dis. 2009, 16:741-761.
46. Russell J.W., Golovoy D., Vincent A.M., Mahendru P., Olzmann J.A., Mentzer A., Feldman E.L. High glucose-induced oxidative stress and mitochondrial dysfunction in neurons. FASEB J. 2002, 16:1738-1748.
47. Patocková J., Marhol P., Tumová E., Krsiak M., Rokyta R., Stípek S., Crkovská J., Andel M. Oxidative stress in the brain tissue of laboratory mice with acute post insulin hypoglycemia. Physiol. Res. 2003, 52:131-135.
48. Bhardwaj S.K., Sharma M.L., Gulati G., Chhabra A., Kaushik R., Sharma P., Kaur G. Effect of starvation and insulin-induced hypoglycemia on oxidative stress scavenger system and electron transport chain complexes from rat brain, liver, and kidney. Mol. Chem. Neuropathol. 1998, 34:157-168.
49. Singh P., Jain A., Kaur G. Impact of hypoglycemia and diabetes on CNS: correlation of mitochondrial oxidative stress with DNA damage. Mol. Cell. Biochem. 2004, 260:153-159.
50. Baydas G., Nedzvetskii V.S., Tuzcu M., Yasar A., Kirichenko S.V. Increase of glial fibrillary acidic protein and S-100B in hippocampus and cortex of diabetic rats: effects of vitamin E. Eur. J. Pharmacol. 2003, 462:67-71.
51. Jain A., Mårtensson J., Stole E., Auld P.A., Meister A. Glutathione deficiency leads to mitochondrial damage in brain. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:1913-1917.
52. Jezek P., Hlavatá L. Mitochondria in homeostasis of reactive oxygen species in cell, tissues, and organism. Int. J. Biochem. Cell Biol. 2005, 37:2478-2503.
53. Aragno M., Mastrocola R., Brignardello E., Catalano M., Robino G., Manti R., Parola M., Danni O., Boccuzzi G. Dehydroepiandrosterone modulates nuclear factor-kappaB activation in hippocampus of diabetic rats. Endocrinology 2002, 143:3250-3258.
54. Kudin A.P., Malinska D., Kunz W.S. Sites of generation of reactive oxygen species in homogenates of brain tissue determined with the use of respiratory substrates and inhibitors. Biochim. Biophys. Acta 2008, 1777:689-695.
55. Hino K., Nishikawa M., Sato E., Inoue M. l-carnitine inhibits hypoglycemia-induced brain damage in the rat. Brain Res. 2005, 1053:77-87.
56. Mattson M.P., Zhang Y., Bose S. Growth factors prevent mitochondrial dysfunction, loss of calcium homeostasis, and cell injury, but not ATP depletion in hippocampal neurons deprived of glucose. Exp. Neurol. 1993, 121:1-13.
57. Isaev N.K., Stelmashook E.V., Dirnagl U., Plotnikov E.Y., Kuvshinova E.A., Zorov D.B. Mitochondrial free radical production induced by glucose deprivation in cerebellar granule neurons. Biochemistry (Mosc) 2008, 73:149-155.
58. Korshunov S.S., Skulachev V.P., Starkov A.A. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 1997, 416:15-18.
59. 2 formation by rat heart mitochondria on substrate availability and donor age. J. Bioenerg. Biomembr. 1997, 29:89-95.
60. Starkov A.A., Fiskum G., Chinopoulos C., Lorenzo B.J., Browne S.E., Patel M.S., Beal M.F. Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species. J. Neurosci. 2004, 24:7779-7788.
61. Srivastava A., Shivanandappa T. Hexachlorocyclohexane differentially alters the antioxidant status of the brain regions in rat. Toxicology 2005, 214:123-130.
62. Serpa R.F.B., De Jesus E.F.O., Anjos M.J., Lopes R.T., do Carmo M.G.T., Moreira S., Rocha M.S., Martinez A.M.B. Elemental concentration in the cortex and hippocampus of Wistar rats by X-ray total reflection fluorescence with synchrotron radiation. J. Radioanal. Nucl. Chem. 2006, 269:647-652.
63. Martínez-Tellez R., Gómez-Villalobos Mde J., Flores G. Alteration in dendritic morphology of cortical neurons in rats with diabetes mellitus induced by streptozotocin. Brain Res. 2005, 1048:108-115.
64. Xu L., Sapolsky R.M., Giffard R.G. Differential sensitivity of murine astrocytes and neurons from different brain regions to injury. Exp. Neurol. 2001, 169:416-424.
65. Bree A.J., Puente E.C., Daphna-Iken D., Fisher S.J. Diabetes increases brain damage caused by severe hypoglycemia. Am. J. Physiol. Endocrinol. Metab. 2009, 297:194-201.