Insulin-induced recurrent hypoglycemia exacerbates diabetic brain mitochondrial dysfunction and oxidative imbalance

Neurobiology of Disease

Volumn 49, Issue 1, 2013, Pages 1-12

  Cardoso, Susana ^a,b   Santos, Renato X ^a,b   Correia, Sónia C ^a,b   Carvalho, Cristina ^a,b   Santos, Maria S ^a,b   Baldeiras, Inês ^a,c,d   Oliveira, Catarina R ^a,d   Moreira, Paula I ^a,d  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c CENTRO HOSPITALAR E UNIVERSITÁRIO DE COIMBRA   (Portugal)

^d UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Cortex; Hippocampus; Long term hyperglycemia; Mitochondria; Neurodegeneration; Oxidative stress; Recurrent hypoglycemia

Indexed keywords

ACONITATE HYDRATASE; ADENOSINE TRIPHOSPHATE; ALPHA TOCOPHEROL; CASPASE 9; GLUCOSE; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; INSULIN; MALONALDEHYDE; MANGANESE SUPEROXIDE DISMUTASE; PROTEIN DISULFIDE REDUCTASE (GLUTATHIONE); SYNAPTOPHYSIN; ANTIDIABETIC AGENT; CASP9 PROTEIN, RAT; SUPEROXIDE DISMUTASE; SYP PROTEIN, RAT;

ADVERSE OUTCOME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD LEVEL; BRAIN CORTEX; BRAIN MITOCHONDRION; BRAIN REGION; CELL ISOLATION; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISEASE EXACERBATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; ENZYME ASSAY; GLUCOSE BLOOD LEVEL; HIPPOCAMPUS; HUMAN; HYPOGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; RECURRENT DISEASE; RESPIRATION CONTROL; RESPIRATORY CHAIN; ANIMAL; BRAIN; CHEMICALLY INDUCED; DRUG EFFECTS; ENERGY METABOLISM; EXPERIMENTAL DIABETES MELLITUS; METABOLISM; MITOCHONDRION; PHYSIOLOGY; RANDOMIZATION; WISTAR RAT;

ACONITATE HYDRATASE; ALPHA-TOCOPHEROL; ANIMALS; BRAIN; CASPASE 9; DIABETES MELLITUS, EXPERIMENTAL; ENERGY METABOLISM; GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; HYPOGLYCEMIA; HYPOGLYCEMIC AGENTS; INSULIN; MALE; MALONDIALDEHYDE; MITOCHONDRIA; RANDOM ALLOCATION; RATS, WISTAR; SUPEROXIDE DISMUTASE; SYNAPTOPHYSIN;

EID: 84866491588     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.08.008     Document Type: Article

References (74)

1. Adam-Vizi V., Starkov A.A. Calcium and mitochondrial reactive oxygen species generation: how to read the facts. J. Alzheimers Dis. 2010, 20(Suppl. 2):S413-S426.
2. Addabbo F., et al. The Krebs cycle and mitochondrial mass are early victims of endothelial dysfunction: proteomic approach. Am. J. Pathol. 2009, 174:34-43.
3. Al-Noori S., et al. Recurrent hypoglycemia alters hypothalamic expression of the regulatory proteins FosB and synaptophysin. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295:R1446-R1454.
4. Auer R.N. Hypoglycemic brain damage. Metab. Brain Dis. 2004, 19:169-175.
5. Awad A.S. Role of AT1 receptors in permeability of the blood-brain barrier in diabetic hypertensive rats. Vascul. Pharmacol. 2006, 45:141-147.
6. Baek B.S., et al. Regional difference of ROS generation, lipid peroxidation, and antioxidant enzyme activity in rat brain and their dietary modulation. Arch. Pharm. Res. 1999, 22:361-366.
7. Bhutada P., et al. Protection of cholinergic and antioxidant system contributes to the effect of berberine ameliorating memory dysfunction in rat model of streptozotocin-induced diabetes. Behav. Brain Res. 2011, 220:30-41.
8. Brands A.M., et al. The effects of type 1 diabetes on cognitive performance: a meta-analysis. Diabetes Care 2005, 28:726-735.
9. Cardoso S., et al. Cortical and hippocampal mitochondria bioenergetics and oxidative status during hyperglycemia and/or insulin-induced hypoglycemia. Biochim. Biophys. Acta 2010, 1802:942-951.
10. Carlberg I., Mannervik B. Glutathione reductase. Methods Enzymol. 1985, 113:484-490.
11. Chance B., Williams G.R. The respiratory chain and oxidative phosphorylation. Adv. Enzymol. Relat. Subj. Biochem. 1956, 17:65-134.
12. Correia S.C., et al. Cyanide preconditioning protects brain endothelial and NT2 neuron-like cells against glucotoxicity: role of mitochondrial reactive oxygen species and HIF-1α. Neurobiol. Dis. 2012, 45:206-218.
13. Dave K.R., et al. Recurrent hypoglycemia exacerbates cerebral ischemic damage in streptozotocin-induced diabetic rats. Stroke 2011, 42:1404-1411.
14. Devisser A. Differential impact of diabetes and hypertension in the brain: adverse effects in grey matter. Neurobiol. Dis. 2011, 44:161-173.
15. Ding Y., et al. Functional improvement after motor training is correlated with synaptic plasticity in rat thalamus. Neurol. Res. 2002, 24:829-836.
16. Duarte J.M., et al. Caffeine consumption attenuates neurochemical modifications in the hippocampus of streptozotocin-induced diabetic rats. J. Neurochem. 2009, 111:368-379.
17. Dubinsky J.M. Heterogeneity of nervous system mitochondria: location, location, location!. Exp. Neurol. 2009, 218:293-307.
18. Estabrook R.E. Mitochondrial respiratory control and the polarographic measurement of ADP/O ratios. Methods Enzymol. 1967, 10:41-47.
19. Flohe L., Gunzler W.A. Assays of glutathione peroxidase. Methods Enzymol. 1984, 105:114-121.
20. Flohe L., Otting F. Superoxide dismutase assays. Methods Enzymol. 1984, 105:93-104.
21. Gornall A.G., et al. Determination of serum proteins by means of the biuret reaction. J. Biol. Chem. 1949, 177:751-766.
22. Grillo C.A., et al. Immunocytochemical analysis of synaptic proteins provides new insights into diabetes-mediated plasticity in the rat hippocampus. Neuroscience 2005, 136:477-486.
23. Herzog R.I., et al. Effect of acute and recurrent hypoglycemia on changes in brain glycogen concentration. Endocrinology 2008, 149:1499-1504.
24. Hissin P.J., Hilf R. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal. Biochem. 1976, 4:214-226.
25. Hussain S., et al. Age-related changes in antioxidant enzymes, superoxide dismutase, catalase, glutathione peroxidase and glutathione in different regions of mouse brain. Int. J. Dev. Neurosci. 1995, 13:811-817.
26. Jacob R.J., et al. Effects of recurrent hypoglycemia on brainstem function in diabetic BB rats: protective adaptation during acute hypoglycemia. Diabetes 1999, 48:141-145.
27. Jacobson A.M., et al. Biomedical risk factors for decreased cognitive functioning in type 1 diabetes: an 18 year follow-up of the Diabetes Control and Complications Trial (DCCT) cohort. Diabetologia 2011, 54:245-255.
28. +) to measure membrane potentials in mitochondria: membrane binding and respiratory effects. Biophys. J. 1984, 45:92.
29. Jezek P., Hlavata L. Mitochondria in homeostasis of reactive oxygen species in cell, tissues, and organism. Int. J. Biochem. Cell Biol. 2005, 37:2478-2503.
30. Jourdain P., et al. Remodeling of hippocampal synaptic networks by a brief anoxia-hypoglycemia. J. Neurosci. 2002, 22:3108-3116.
31. Kamboj S.S., Sandhir R. Protective effect of N-acetylcysteine supplementation on mitochondrial oxidative stress and mitochondrial enzymes in cerebral cortex of streptozotocin-treated diabetic rats. Mitochondrion 2011, 11:214-222.
32. Kamo N., et al. 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.
33. Kapoor R., et al. Bacopa monnieri modulates antioxidant responses in brain and kidney of diabetic rats. Environ. Toxicol. Pharmacol. 2009, 27:62-69.
34. Karaagac N., et al. Changes in prooxidant-antioxidant balance in tissues of rats following long-term hyperglycemic status. Endocr. Res. 2011, 36:124-133.
35. Kario K., et al. Diabetic brain damage in hypertension: role of renin-angiotensin system. Hypertension 2005, 45:887-893.
36. Krebs H.A., Holzach O. The conversion of citrate into cis-aconitate and isocitrate in the presence of aconitase. Biochem. J. 1952, 52:527-528.
37. Leese G.P., et al. Frequency of severe hypoglycemia requiring emergency treatment in type 1 and type 2 diabetes: a population-based study of health service resource use. Diabetes Care 2003, 26:1176-1180.
38. Maiese K., et al. Oxidative stress biology and cell injury during type 1 and type 2 diabetes mellitus. Curr. Neurovasc. Res. 2007, 4:63-71.
39. Malone J.I., et al. Hyperglycemic brain injury in the rat. Brain Res. 2006, 1076:9-15.
40. McCrimmon R.J. Update in the CNS response to hypoglycemia. J. Clin. Endocrinol. Metab. 2012, 97:1-8.
41. McNay E.C. The impact of recurrent hypoglycemia on cognitive function in aging. Neurobiol. Aging 2005, 26(Suppl. 1):76-79.
42. Modi P. Diabetes beyond insulin: review of new drugs for treatment of diabetes mellitus. Curr. Drug Discov. Technol. 2007, 4:39-47.
43. Moreira P.I., Oliveira C.R. Mitochondria as potential targets in antidiabetic therapy. Handb. Exp. Pharmacol. 2011, 331-356.
44. Moreira P.I., et al. Amyloid beta-peptide promotes permeability transition pore in brain mitochondria. Biosci. Rep. 2001, 21:789-800.
45. Moreira P.I., et al. Effect of amyloid beta-peptide on permeability transition pore: a comparative study. J. Neurosci. Res. 2002, 69:257-267.
46. Moreira P.I., et al. Insulin protects against amyloid beta-peptide toxicity in brain mitochondria of diabetic rats. Neurobiol. Dis. 2005, 18:628-637.
47. Moreira P.I., et al. Mitochondria as a therapeutic target in Alzheimer's disease and diabetes. CNS Neurol. Disord. Drug Targets 2009, 8:492-511.
48. Moreira P.I., et al. An integrative view of the role of oxidative stress, mitochondria and insulin in Alzheimer's disease. J. Alzheimers Dis. 2009, 16:741-761.
49. Moreira P.I., et al. Mitochondrial dysfunction is a trigger of Alzheimer's disease pathophysiology. Biochim. Biophys. Acta 2010, 1802:2-10.
50. Muratsugu M., et al. Selective electrode for dibenzyl dimethyl ammonium cation as indicator of the membrane potential in biological systems. Biochim. Biophys. Acta 1977, 464:613-619.
51. Ouyang Y.B., et al. Is neuronal injury caused by hypoglycemic coma of the necrotic or apoptotic type?. Neurochem. Res. 2000, 25:661-667.
52. Oztaş B., Küçük M. Influence of acute arterial hypertension on blood-brain barrier permeability in streptozocin-induced diabetic rats. Neurosci. Lett. 1995, 188:53-56.
53. Perez-Matute P., et al. Reactive species and diabetes: counteracting oxidative stress to improve health. Curr. Opin. Pharmacol. 2009, 9:771-779.
54. Ramakrishna V., Jailkhani R. Evaluation of oxidative stress in insulin dependent diabetes mellitus (IDDM) patients. Diagn. Pathol. 2007, 2:22.
55. Rongzhu L., et al. Effects of acrylonitrile on antioxidant status of different brain regions in rats. Neurochem. Int. 2009, 55:552-557.
56. Russell J.W., et al. High glucose-induced oxidative stress and mitochondrial dysfunction in neurons. FASEB J. 2002, 16:1738-1748.
57. Russo V.C., et al. Effects of fluctuating glucose levels on neuronal cells in vitro. Neurochem. Res. 2012, 37:1768-1782.
58. Sharifi A.M., et al. Involvement of caspase-8, -9, and -3 in high glucose-induced apoptosis in PC12 cells. Neurosci. Lett. 2009, 459:47-51.
59. Sharma B., Singh N. Experimental hypertension induced vascular dementia: Pharmacology, biochemical and behavioral recuperation by angiotensin receptor blocker and acetylcholinesterase inhibitor. Pharmacol. Biochem. Behav. 2012, 102:101-108.
60. Singh P., et al. Expression of neuronal plasticity markers in hypoglycemia induced brain injury. Mol. Cell. Biochem. 2002, 247:69-74.
61. Singh P., et al. Impact of hypoglycemia and diabetes on CNS: correlation of mitochondrial oxidative stress with DNA damage. Mol. Cell. Biochem. 2004, 260:153-159.
62. Srivastava A., Shivanandappa T. Hexachlorocyclohexane differentially alters the antioxidant status of the brain regions in rat. Toxicology 2005, 214:123-130.
63. St-Pierre J., et al. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 2002, 277:44784-44790.
64. Sullivan P.G., et al. Mitochondrial uncoupling as a therapeutic target following neuronal injury. J. Bioenerg. Biomembr. 2004, 36:353-356.
65. Turner C.P., et al. A1 adenosine receptors mediate hypoglycemia-induced neuronal injury. J. Mol. Endocrinol. 2004, 32:129-144.
66. Valko M., et al. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007, 39:44-84.
67. Valtorta F., et al. Synaptophysin: leading actor or walk-on role in synaptic vesicle exocytosis?. Bioessays 2004, 26:445-453.
68. Vatassery G.T., Younoszai R. Alpha tocopherol levels in various regions of the central nervous systems of the rat and guinea pig. Lipids 1978, 13:828-831.
69. Warren R.E., Frier B.M. Hypoglycaemia and cognitive function. Diabetes Obes. Metab. 2005, 7:493-503.
70. Wong S.H., et al. Lipoperoxides in plasma as measured by liquid-chromatographic separation of malondialdehyde-thiobarbituric acid adduct. Clin. Chem. 1987, 33:214-220.
71. Wright R.J., et al. Effects of acute insulin-induced hypoglycemia on spatial abilities in adults with type 1 diabetes. Diabetes Care 2009, 32:1503-1506.
72. Wrighten S.A., et al. A look inside the diabetic brain: contributors to diabetes-induced brain aging. Biochim. Biophys. Acta 2009, 1792:444-453.
73. Yan L.J., et al. Oxidative damage during aging targets mitochondrial aconitase. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:11168-11172.
74. Zherebitskaya E., et al. Development of selective axonopathy in adult sensory neurons isolated from diabetic rats: role of glucose-induced oxidative stress. Diabetes 2009, 58:1356-1364.