Ageing and diabetes: implications for brain function

Biessels, Geert Jan; van der Heide, Lars P; Kamal, Amer; Bleys, Ronald L.A.W; Gispen, Willem Hendrik

doi:10.1016/s0014-2999(02)01486-3

Cited by 458Neurological Disease Mechanisms and TreatmentsNeuroscience and Neuropharmacology ResearchAdvanced Glycation End Products research

Ageing and diabetes: implications for brain function

Biessels, Geert Jan, van der Heide, Lars P, Kamal, Amer, Bleys, Ronald L.A.W, Gispen, Willem Hendrik·2002·European Journal of Pharmacology

DOI 10.1016/s0014-2999(02)01486-3

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Abstract

Diabetes mellitus is associated with moderate cognitive deficits and neurophysiological and structural changes in the brain, a condition that may be referred to as diabetic encephalopathy. Diabetes increases the risk of dementia, particularly in the elderly. The emerging view is that the diabetic brain features many symptoms that are best described as "accelerated brain ageing." The clinical characteristics of diabetic encephalopathy are discussed, as well as behavioural (e.g. spatial learning) and neurophysiological (e.g. hippocampal synaptic plasticity) findings in animal models. Animal models can make a substantial contribution to our understanding of the pathogenesis, which shares many features with the mechanisms underlying brain ageing. By unravelling the pathogenesis, targets for pharmacotherapy can be identified. This may allow treatment or prevention of this diabetic complication in the future. We discuss changes in glutamate receptor subtypes, in second-messenger systems and in protein kinases that may account for the alterations in synaptic plasticity. In addition, the possible role of cerebrovascular changes, oxidative stress, nonenzymatic protein glycation, insulin and alterations in neuronal calcium homeostasis are addressed.

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It is possible that IGT leads to elevations in glucose levels sufficient to worsen the effects of other subtle brain insults by perhaps increasing excitotoxic free radical-induced damage.
“Although our subjects were not diabetic, it is also possible that the IGT leads to elevations in glucose levels sufficient to worsen the effects of other subtle brain insults by perhaps increasing excitotoxic free radical-induced damage (for a review, see ref. 36).”
From Reduced glucose tolerance is associated with poor memory performance and hippocampal atrophy among normal elderly (2003) · cites this paper as [36]
Only one of the review articles that summarised the available data on the relationship between diabetes and cognitive dysfunction provided a quantitative estimate.
“Indeed, only one [7] of the review articles that summarised the available data pertaining to this relationship [4, 6 -11] provided a quantitative estimate.”
From Cognitive decline and dementia in diabetes—systematic overview of prospective observational studies (2005) · cites this paper as [8]

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Mankovsky, B., Metzger, B. E., Molitch, M. E., & Biller, J. (1996) · Journal of Diabetes and its Complications · doi:10.1016/s1056-8727(96)90006-9 · Cited by 134 · see citing works
Hyperinsulinemia: the missing link among oxidative stress and age-related diseases?
Facchini, F. S., Hua, N. W., Reaven, G. M., & Stoohs, R. A. (2000) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(00)00438-x · Cited by 134 · see citing works
Ultrastructural analysis of β-amyloid-induced apoptosis in cultured hippocampal neurons
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Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats
Biessels, G. J., Kamal, A., Ramakers, G. M., et al. (1996) · Diabetes · doi:10.2337/diabetes.45.9.1259 · Cited by 128 · see citing works
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Effect of diabetes on levels of lipid peroxides and glycolipids in rat brain
Kumar, J. S. S., & Menon, V. P. (1993) · Metabolism · doi:10.1016/0026-0495(93)90195-t · Cited by 121 · see citing works
Differential effects of normal aging on sources of standard N1, target N1 and target P300 auditory event-related brain potentials revealed by low resolution electromagnetic tomography (LORETA)
Anderer, P., Pascual-Marqui, R. D., Semlitsch, H. V., & Saletu, B. (1998) · Electroencephalography and Clinical Neurophysiology/Evoked Potentials Section · doi:10.1016/s0168-5597(97)00080-4 · Cited by 121 · see citing works
Gerontogenes mediate health and longevity in nematodes through increasing resistance to environmental toxins and stressors
Johnson, T. E., Cypser, J. R., de Castro, E., Castro, S., Henderson, S. T., Murakami, S., Rikke, B. A., Tedesco, P., & Link, C. D. (2000) · Experimental Gerontology · doi:10.1016/s0531-5565(00)00138-8 · Cited by 115 · see citing works
Thickened cerebral cortical capillary basement membranes in diabetics.
Pc, J., Brendel, K., & Meezan, E. (1982) · PubMed · Cited by 115 · see citing works
STZ transport and cytotoxicity. Specific enhancement in GLUT2-expressing cells
Schnedl, W. J., Ferber, S., Johnson, J. H., et al. (1994) · Diabetes · doi:10.2337/diabetes.43.11.1326 · Cited by 111 · see citing works
Visual electrophysiological responses in persons with type 1 diabetes
Parisi, V., & Uccioli, L. (2001) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.177 · Cited by 109 · see citing works
Effects of insulin-dependent diabetes on learning and memory efficiency in adults
Ryan, C. M., & Williams, T. M. (1993) · Journal of Clinical and Experimental Neuropsychology · doi:10.1080/01688639308402589 · Cited by 109 · see citing works
Impaired modulation of AMPA receptors by calcium-dependent processes in streptozotocin-induced diabetic rats.
Chabot, C., Massicotte, G., Milot, M., Trudeau, F., & Gagné, J. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00648-3 · Cited by 109 · see citing works
NMDA receptor subunits are modified transcriptionally and post-translationally in the brain of streptozotocin-diabetic rats
Luca, M. D., Ruts, L., Gardoni, F., Cattabeni, F., Biessels, G. J., & Gispen, W. H. (1999) · Diabetologia · doi:10.1007/s001250051217 · Cited by 107 · see citing works
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Voltage‐dependent calcium currents are enhanced in dorsal root ganglion neurones from the Bio Bred/Worchester diabetic rat.
Hall, K. E., Sima, A. A. F., & Wiley, J. W. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp020814 · Cited by 103 · see citing works
Accumulation of advanced glycation end products of the Maillard reaction with age in human hippocampal neurons
Kimur, T., Takamatsu, J., Ikeda, K., et al. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(96)12537-4 · Cited by 99 · see citing works
Learning and memory in streptozotocin-induced diabetic rats in a novel spatial/object discrimination task
Popović, M., Biessels, G. J., Isaacson, R. L., & Gispen, W. H. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00186-3 · Cited by 96 · see citing works
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Non-enzymic glycation of human extracellular superoxide dismutase
Adachi, T., Ohta, H., Hirano, K., Hayashi, K., & Marklund, S. L. (1991) · Biochemical Journal · doi:10.1042/bj2790263 · Cited by 88 · see citing works
Vascular Perfusion and Blood‐Brain Glucose Transport in Acute and Chronic Hyperglycemia
Harik, S. I., & LaManna, J. C. (1988) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1988.tb01179.x · Cited by 85 · see citing works
Ellenberg and Rifkin's Diabetes Mellitus: Theory and Practice
Rifkin, H., Porte, D., & Gallon, D. J. (1990) · Medical Entomology and Zoology · Cited by 85 · see citing works
Central Nervous System Findings in a Tenth Decade Autopsy Population
Peress, N. S., Kane, W. C., & Aronson, S. M. (1973) · Progress in Brain Research · doi:10.1016/s0079-6123(08)60707-4 · Cited by 84 · see citing works
Abnormalities of Cognitive Functions in IDDM Revealed by P300 Event-Related Potential Analysis: Comparison With Short-Latency Evoked Potentials and Psychometric Tests
Pozzessere, G., Valle, E., de Crignis, S., et al. (1991) · Diabetes · doi:10.2337/diab.40.8.952 · Cited by 84 · see citing works
Endothelial cell dysfunction and the pathogenesis of diabetic macroangiopathy
Laight, D. W., CARRIER, M. J., & Änggård, E. (1999) · Diabetes/Metabolism Research and Reviews · doi:10.1002/(sici)1520-7560(199907/08)15:4 · Cited by 82 · see citing works
Regional cerebral blood flow decreases during chronic and acute hyperglycemia.
BDuckrow, R., CBeard, D., & WBrennan, R. (1987) · Stroke · Cited by 82 · see citing works
Nonenzymatic glycation of peripheral and central nervous system proteins in experimental diabetes mellitus
Ryle, C., Leow, C. K., & Donaghy, M. (1997) · Muscle & Nerve · doi:10.1002/(sici)1097-4598(199705)20:5 · Cited by 80 · see citing works
Lipid peroxidation, glutathione levels and changes in glutathione‐related enzyme activities in streptozotocin‐induced diabetic rats
Mukherjee, B., MUKHERJEE, J. R., & Chatterjee, M. (1994) · Immunology and Cell Biology · doi:10.1038/icb.1994.17 · Cited by 80 · see citing works
Evidence by magnetic resonance imaging of cerebral alterations of atrophy type in young insulin-dependent diabetic patients
Lunetta, M., Damanti, A. R., Fabbri, G., Lombardo, M., Mauro, M. D., & Mughini, L. (1994) · Journal of Endocrinological Investigation · doi:10.1007/bf03348967 · Cited by 77 · see citing works
Risk for non-insulindependent diabetes in the normoglycaemic elderly is associated with impaired cognitive function
Vanhanen, M., Koivisto, K., Karjalainen, L., Helkala, E.-L., Laakso, M., Soininen, H., & Riekkinen, P. (1997) · NeuroReport · doi:10.1097/00001756-199704140-00041 · Cited by 77 · see citing works
Autonomic control of the cerebral circulation during normal and impaired peripheral circulatory control
Cencetti, S., Lagi, A., Cipriani, M., Fattorini, L., Bandinelli, G., & Bernardi, L. (1999) · Heart · doi:10.1136/hrt.82.3.365 · Cited by 75 · see citing works
Glucose intolerance, cognitive impairment and Alzheimer’s disease
Vanhanen, M., & Soininen, H. S. (1998) · Current Opinion in Neurology · doi:10.1097/00019052-199812000-00011 · Cited by 72 · see citing works
Brainstem auditory and visual evoked potentials in Type 1 (insulin-dependent) diabetic patients
Khardori, R. K., Soler, N. G., Good, D. C., et al. (1986) · Diabetologia · doi:10.1007/bf00903345 · Cited by 71 · see citing works
Severe Deterioration in Cognitive Function and Personality in Five Patients with Long‐standing Diabetes: A Complication of Diabetes or a Consequence of Treatment?
Gold, A. E., Deary, I. J., Jones, R. W., O’Hare, J. P., Reckless, J. P. D., & Frier, B. M. (1994) · Diabetic Medicine · doi:10.1111/j.1464-5491.1994.tb00314.x · Cited by 66 · see citing works
The calcium hypothesis of brain aging and neurodegenerative disorders: Significance in diabetic neuropathy
Biessels, G. J., & Gispen, W. H. (1996) · Life Sciences · doi:10.1016/0024-3205(96)00316-5 · Cited by 64 · see citing works
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Insulin Inhibits the Ubiquitin-Dependent Degrading Activity of the 26S Proteasome*
Bennett, R. G., Hamel, F. G., & Duckworth, W. C. (2000) · Endocrinology · doi:10.1210/endo.141.7.7575 · Cited by 62 · see citing works
Peripheral nerve function and metabolic control in diabetes mellitus
Troni, W., Carta, Q., Cantello, R. M., et al. (1984) · Annals of Neurology · doi:10.1002/ana.410160204 · Cited by 62 · see citing works
Excessive nonenzymatic glycosylation of peripheral and central nervous system myelin components in diabetic rats
Vlassara, H., Brownlee, M., & Cerami, A. (1983) · Diabetes · doi:10.2337/diabetes.32.7.670 · Cited by 62 · see citing works
Binding properties of glutamate receptors in streptozotocin-induced diabetes in rats
Gagné, J., Milot, M., Gélinas, S., et al. (1997) · Diabetes · doi:10.2337/diabetes.46.5.841 · Cited by 61 · see citing works
Oxidative state of glutathione in red blood cells and plasma of diabetic patients: in vivo and in vitro study.
Costagliola, C. (1990) · PubMed · Cited by 61 · see citing works
Characteristics of learning and memory in streptozocin-induced diabetic mice
Flood, J. F., Mooradian, A. D., & Morley, J. E. (1990) · Diabetes · doi:10.2337/diabetes.39.11.1391 · Cited by 60 · see citing works
Diabetes mellitus and brain atrophy: A computed tomography study in an elderly population
Soininen, H. S., Puranen, M. I., Helkala, E.-L., Laakso, M., & Riekkinen, P. J. (1992) · Neurobiology of Aging · doi:10.1016/0197-4580(92)90095-f · Cited by 59 · see citing works
Calcium signal prolongation in sensory neurones of mice with experimental diabetes
Kostyuk, E. P., Pronchuk, N., & Shmigol, A. (1995) · Neuroreport · doi:10.1097/00001756-199505090-00015 · Cited by 59 · see citing works
Regional Brain Glucose Metabolism and Blood Flow in Streptozocin-Induced Diabetic Rats
Jakobsen, J., Nedergaard, M., Aarslew-Jensen, M., et al. (1990) · Diabetes · doi:10.2337/diab.39.4.437 · Cited by 59 · see citing works
Regulation of Rat Sympathetic Nerve Density by Target Tissues and NGF in Maturity and Old Age
Thrasivoulou, C., & Cowen, T. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb00333.x · Cited by 57 · see citing works
Basement membrane of hypothalamus and cortex capillaries from normotensive and spontaneously hypertensive rats with streptozotocin-induced diabetes
Junker, U., Jäggi, C., Bestetti, G. E., & ROSSI, G. L. (1985) · Acta Neuropathologica · doi:10.1007/bf00686999 · Cited by 57 · see citing works
Effect of streptozotocin-induced diabetes on the activity of calcium channels in rat dorsal horn neurons
Voitenko, N. V., Kruglikov, I., Kostyuk, E. P., et al. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00453-4 · Cited by 56 · see citing works
Increased Hippocampal Ca2+ Channel Activity in Brain Aging and Dementia
Landfield, P. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb44422.x · Cited by 55 · see citing works
In vivo cerebrovascular reactivity in Wistar and Fischer 344 rat strains during aging
Lartaud, I., Boscs, L. B., Chillon, J., Atkinson, J., & Capdeville‐Atkinson, C. (1993) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1993.264.3.h851 · Cited by 55 · see citing works
Electrophysiological alterations of the central nervous system in diabetes mellitus
Mario, U. D., Morano, S., Valle, E., et al. (1995) · Diabetes/Metabolism Reviews · doi:10.1002/dmr.5610110306 · Cited by 54 · see citing works
The use of electrophysiology for the assessment of diabetic neuropathy
Arezzo, J. C. (1997) · Neuroscience Research Communications · doi:10.1002/(sici)1520-6769(199707)21:1 · Cited by 53 · see citing works
Changes of superoxide dismutase gene expression and activity in the brain of streptozotocin-induced diabetic rats
Huang, W., Juang, S., Liu, I.-M., et al. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00704-1 · Cited by 53 · see citing works
Functional Correlates of Reduced Central Conduction Velocity in Diabetic Subjects
Donald, M. W., Erdahl, D. L. W., Surridge, D., et al. (1984) · Diabetes · doi:10.2337/diab.33.7.627 · Cited by 52 · see citing works
Influence of diabetes mellitus on regional cerebral glucose metabolism and regional cerebral blood flow
Sabri, O., Hellwig, D., Schreckenberger, M., et al. (2000) · Nuclear Medicine Communications · doi:10.1097/00006231-200001000-00005 · Cited by 51 · see citing works
Cellular and Vessel Wall Morphology of Cerebral Cortical Arterioles after Short-Term Diabetes in Adult Rats
Moore, S. A., Bohlen, G., Miller, B. G., et al. (1985) · Journal of Vascular Research · doi:10.1159/000158613 · Cited by 50 · see citing works
Role of mitochondrial dysfunction in calcium signalling alterations in dorsal root ganglion neurons of mice with experimentally-induced diabetes
Kostyuk, E. P., Svichar, N., Shishkin, V., et al. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00471-0 · Cited by 49 · see citing works
Insulin Inhibition of Proteasome Activity in Intact Cells
Hamel, F. G., Bennett, R. G., Harmon, K. S., et al. (1997) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.6693 · Cited by 48 · see citing works
Glycation of Brain Actin in Experimental Diabetes
Pekiner, C., Cullum, N. A., Hughes, J., et al. (1993) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1993.tb02143.x · Cited by 47 · see citing works
Changes in calcium signalling in dorsal horn neurons in rats with streptozotocin-induced diabetes
Voitenko, N. V., Kostyuk, E. P., Kruglikov, I., et al. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00330-9 · Cited by 47 · see citing works
Beneficial effect of the Ca2+antagonist, nimodipine, on existing diabetic neuropathy in the BB/Wor rat
Kappelle, A. C., Biessels, G. J., Bravenboer, B., et al. (1994) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1994.tb14821.x · Cited by 46 · see citing works
Self-citation
beta-Amyloid neurotoxicity.
Forloni, G. (1993) · PubMed · Cited by 46 · see citing works
Nonenzymatic glycation of Na,K-ATPase. Effects on ATP hydrolysis and K+ occlusion.
Garner, M. H., Bahador, A., & Sachs, G. M. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)77223-2 · Cited by 45 · see citing works
Alterations in tissue antioxidant systems in the spontaneously diabetic (BB Wistar) rat
Wohaieb, S. A., & Godin, D. V. (1987) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y87-346 · Cited by 45 · see citing works
The effect of the calcium antagonist nifedipine on peripheral nerve function in streptozotocin-diabetic rats
Robertson, S., Cameron, N. E., & Cotter, M. A. (1992) · Diabetologia · doi:10.1007/bf00401363 · Cited by 44 · see citing works
Improved Visual Evoked Potential Latencies In Poorly Controlled Diabetic Patients After Short-Term Strict Metabolic Control
Ziegler, O., Guerci, B., Algan, M., et al. (1994) · Diabetes Care · doi:10.2337/diacare.17.10.1141 · Cited by 44 · see citing works
The functional significance of biochemical alterations in streptozotocin-induced diabetes
Bellush, L. L., Reid, S. G., & North, D. L. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90424-m · Cited by 43 · see citing works
The effect of gamma-linolenic acid–alpha-lipoic acid on functional deficits in the peripheral and central nervous system of streptozotocin-diabetic rats
Biessels, G. J., Smale, S., Duis, S., Kamal, A., & Gispen, W. H. (2001) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(00)00456-1 · Cited by 43 · see citing works
Self-citation
The effect of experimentally induced diabetes mellitus on the lipid order and composition of rat cerebral microvessels
Mooradian, A. D., & Smith, T. L. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90007-t · Cited by 42 · see citing works
Stress and behavior in streptozotocin diabetic rats: Biochemical correlates of passive avoidance learning.
Bellush, L. L., & Rowland, N. E. (1989) · Behavioral Neuroscience · doi:10.1037//0735-7044.103.1.144 · Cited by 41 · see citing works
Antioxidant Defense Systems in the Brains of Type II Diabetic Mice
Makar, T. K., Rimpel‐Lamhaouar, K., Abraham, D. G., et al. (1995) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1995.65010287.x · Cited by 38 · see citing works
Diminished muscarinic receptor-mediated cerebral blood flow response in streptozotocin-treated rats
Pelligrino, D. A., Miletich, D. J., & Albrecht, R. F. (1992) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1992.262.4.e447 · Cited by 38 · see citing works
Changes in adenosine sensitivity in the hippocampus of rats with streptozotocin‐induced diabetes
Morrison, P. D., Mackinnon, M. W. B., Bartrup, J. T., et al. (1992) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1992.tb09092.x · Cited by 37 · see citing works
Regulation of Multicatalytic Enzyme Activity by Insulin and the Insulin-Degrading Enzyme**This work was supported by the Department of Veterans Affairs Research Service and the Bly Memorial Research Fund.
Hamel, F. G., Bennett, R. G., & Duckworth, W. C. (1998) · Endocrinology · doi:10.1210/endo.139.10.6256 · Cited by 37 · see citing works
Effects of chronic nimodipine on working memory of old rats in relation to defects in synaptosomal calcium homeostasis
Batuecas, A., Pereira, R., Centeno, C., Pulido, J. A., Hernández, M., Bollati, A., Bogónez, E., & Satrústegui, J. (1998) · European Journal of Pharmacology · doi:10.1016/s0014-2999(98)00250-7 · Cited by 35 · see citing works
Cerebrovascular nerves in old rats show reduced accumulation of 5-hydroxytryptamine and loss of nerve fibres
Cowen, T., & Thrasivoulou, C. (1990) · Brain Research · doi:10.1016/0006-8993(90)90461-j · Cited by 34 · see citing works
Stress and behavior in streptozotocin diabetic rats: Biochemical correlates of passive avoidance learning.
Bellush, L. L., & Rowland, N. E. (1989) · Behavioral Neuroscience · doi:10.1037/0735-7044.103.1.144 · Cited by 34 · see citing works
Cerebral vascular autoregulation of blood flow and tissue PO2 in diabetic rats
Rubin, M. J., & Bohlen, H. G. (1985) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1985.249.3.h540 · Cited by 33 · see citing works
Distribution of Elements and Water in Peripheral Nerve of Streptozocin-Induced Diabetic Rats
Lowery, J., Eichberg, J., Saubermann, A. J., et al. (1990) · Diabetes · doi:10.2337/diab.39.12.1498 · Cited by 28 · see citing works
Hippocampal slices from long-term streptozotocin-injected rats are prone to epileptiform responses
Margineanu, D. G., Niespodziany, I., & Wülfert, E. (1998) · Neuroscience Letters · doi:10.1016/s0304-3940(98)00580-1 · Cited by 28 · see citing works
Abnormalities of cognitive functions in IDDM revealed by P300 event-related potential analysis. Comparison with short-latency evoked potentials and psychometric tests
Pozzessere, G., Valle, E., de Crignis, S., et al. (1991) · Diabetes · doi:10.2337/diabetes.40.8.952 · Cited by 28 · see citing works
Functional correlates of reduced central conduction velocity in diabetic subjects
Donald, M. W., Erdahl, D. L. W., Surridge, D. H., et al. (1984) · Diabetes · doi:10.2337/diabetes.33.7.627 · Cited by 28 · see citing works
Reduced adenosine uptake accelerates ischaemic block of population spikes in hippocampal slices from streptozotocin‐treated diabetic rats
Cassar, M., Jones, M. G., & Szatkowski, M. S. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00035.x · Cited by 25 · see citing works
Reduction of Nerves Containing Vasoactive Intestinal Polypeptide and Serotonin, but Not Neuropeptide Y and Catecholamine, in Cerebral Blood Vessels of the 8-Week Streptozotocin-Induced Diabetic Rat
Lagnado, M. L. J., CROWE, R., Lincoln, J., et al. (2008) · Blood Vessels · doi:10.1159/000158693 · Cited by 24 · see citing works
Regional Density of Perfused Capillaries and Cerebral Blood Flow in Untreated Short-Term and Long-Term Streptozotocin Diabetes
Knudsen, G. M., Göbel, U., Paulson, O. B., et al. (1991) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1991.75 · Cited by 24 · see citing works
Perivascular Nerves of the Human Basal Cerebral Arteries: II. Changes in Aging and Alzheimer's Disease
Bleys, R. L. A. W., Cowen, T., Groen, G. J., et al. (1996) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199609000-00030 · Cited by 24 · see citing works
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Effect of medium pH on glutathione redox cycle in cultured human umbilical vein endothelial cells
Ikebuchi, M., Kashiwagi, A., Asahina, T., et al. (1993) · Metabolism · doi:10.1016/0026-0495(93)90269-t · Cited by 22 · see citing works
Effect of Aging on Regulation of Brain Stem Circulation During Hypotension
Toyoda, Ḱ., Fujii, K., Takata, Y., Ibayashi, S., Fujikawa, M., & Fujishima, M. (1997) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199706000-00009 · Cited by 22 · see citing works
Visual evoked potentials in NIDDM: a longitudinal study
Moreo, G. L., Mariani, E., Pizzamiglio, G., et al. (1995) · Diabetologia · doi:10.1007/bf00400726 · Cited by 22 · see citing works
A comparison of cerebral blood flow during basal, hypotensive, hypoxic and hypercapnic conditions between normal and streptozotocin diabetic rats
Simpson, R. E., Phillis, J. W., & Buchannan, J. (1990) · Brain Research · doi:10.1016/0006-8993(90)90766-5 · Cited by 21 · see citing works
Insulin Inhibits the Ubiquitin-Dependent Degrading Activity of the 26S Proteasome
Bennett, R. G. (2000) · Endocrinology · doi:10.1210/en.141.7.2508 · Cited by 21 · see citing works
Chronic cerebral hypoperfusion-induced neuropathological changes in rats.
Nanri, M., Miyake, H., Murakami, Y., Matsumoto, K., & Watanabe, H. (1998) · PubMed · Cited by 19 · see citing works
Diabetes mellitus preserves synaptic plasticity in hippocampal slices from middle-aged rats
Tekkök, S. B., & Krnjević, K. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00662-9 · Cited by 19 · see citing works
Regional brain glucose metabolism and blood flow in streptozocin-induced diabetic rats
Jakobsen, J., Nedergaard, M., Aarslew-Jensen, M., et al. (1990) · Diabetes · doi:10.2337/diabetes.39.4.437 · Cited by 19 · see citing works
Distribution of elements and water in peripheral nerve of streptozocin-induced diabetic rats
Lowery, J., Eichberg, J., Saubermann, A. J., et al. (1990) · Diabetes · doi:10.2337/diabetes.39.12.1498 · Cited by 18 · see citing works
Neuronal excitability and conduction velocity changes in hippocampal slices from streptozotocin-treated diabetic rats
Candy, S. M., & Szatkowski, M. S. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02171-5 · Cited by 17 · see citing works
Regulation of Multicatalytic Enzyme Activity by Insulin and the Insulin-Degrading Enzyme
Hamel, F. G. (1998) · Endocrinology · doi:10.1210/en.139.10.4061 · Cited by 12 · see citing works
Chronic hyperglycaemia increases neuronal sensitivity to high potassium in hippocampal slices from streptozotocin-treated diabetic rats
Candy, S. M., & Szatkowski, M. S. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00954-4 · Cited by 11 · see citing works
Acute effect of streptozotocin induced diabetes on bar pressing for food reward in albino rats.
Kaleeswari, R., Thombre, D. P., & Chakrabarty, A. S. (1987) · PubMed · Cited by 7 · see citing works

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Risk of dementia in diabetes mellitus: a systematic review
Biessels, G. J., Staekenborg, S., Brunner, E., Brayne, C., & Scheltens, P. (2006) · The Lancet Neurology · doi:10.1016/s1474-4422(05)70284-2 · Cited by 2,187 · see citing works
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The Science of Stroke: Mechanisms in Search of Treatments
Moskowitz, M. A., Lo, E. H., & Iadecola, C. (2010) · Neuron · doi:10.1016/j.neuron.2010.07.002 · Cited by 1,930 · see citing works
Diabetes mellitus and risk of Alzheimer disease and decline in cognitive function
Arvanitakis, Z., Wilson, R. S., Bienias, J. L., Evans, D. A., & Bennett, D. A. (2004) · Archives of Neurology · doi:10.1001/archneur.61.5.661 · Cited by 1,258 · see citing works
Cognitive decline and dementia in diabetes—systematic overview of prospective observational studies
Cukierman, T., Gerstein, H. C., & Williamson, J. D. (2005) · Diabetologia · doi:10.1007/s00125-005-0023-4 · Cited by 1,049 · see citing works
The relationship between impaired glucose tolerance, type 2 diabetes, and cognitive function
Awad, N., Gagnon, M., & Messier, C. (2004) · Journal of Clinical and Experimental Neuropsychology · doi:10.1080/13803390490514875 · Cited by 551 · see citing works
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Authors: Biessels, G. J., van der Heide, L. P., Kamal, A., Bleys, R. L. A. W., & Gispen, W. H.
Affiliations: University Medical Center Utrecht (NL)
Corresponding author: Biessels, Geert Jan
ORCID: Biessels, Geert Jan
Kamal, Amer
Bleys, Ronald L.A.W
Venue: European Journal of Pharmacology
Publisher: Elsevier BV
Published: 2002-04
Volume: 441
Issue: 1-2
Pages: 1-14
ISSN: 0014-2999 (ISSN-L)
DOI: 10.1016/s0014-2999(02)01486-3
OpenAlex: W2141567007
Cited by: 458
References: 186
Citations by year: 2026: 2 · 2025: 7 · 2024: 5 · 2023: 11 · 2022: 14 · 2021: 21 · 2020: 22 · 2019: 19 · 2018: 14 · 2017: 18 · 2016: 22 · 2015: 25 · 2014: 34 · 2013: 26 · 2012: 30
FWCI: 2.38
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: European Journal of Pharmacology (publishedVersion)
PubMed (publishedVersion)
Utrecht University Repository (Utrecht University) (submittedVersion)
Topics: Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Advanced Glycation End Products research
Keywords: diabetes mellitus, brain aging, diabetic encephalopathy, dementia, cognitive impairment, hippocampal synaptic plasticity, spatial learning, glutamate receptor subtypes, second messenger signaling, protein kinases, cerebrovascular changes, oxidative stress, insulin, neuronal calcium homeostasis, animal models of diabetes
MeSH terms: Aging, Animals, Brain, Calcium, Cognition, Diabetes Mellitus, Humans, Neuronal Plasticity, Peripheral Nervous System Diseases, Synapses, Oxidative Stress

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Ageing and diabetes: implications for brain function

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