Insulin and IGF-I prevent brain atrophy and DNA loss in diabetes

Brain Research

Volumn 1303, Issue , 2009, Pages 179-194

  Šerbedžija, Predrag ^a   Madl, James E ^a   Ishii, Douglas N ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Brain edema; Dementia, Insulin like growth factor; Diabetic neuropathy; Encephalopathy; Neurodegeneration

Indexed keywords

ACTIN; ALPHA TUBULIN; BETA TUBULIN; DNA; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE AMMONIA LIGASE; INSULIN; MYELIN BASIC PROTEIN; PROTEOLIPID PROTEIN; RECOMBINANT SOMATOMEDIN C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ATROPHY; BRAIN CORTEX; BRAIN WATER; CEREBROSPINAL FLUID; CONTROLLED STUDY; GENE LOSS; HIPPOCAMPUS; HYPERGLYCEMIA; KIDNEY MASS; LATERAL BRAIN VENTRICLE; LEARNING DISORDER; MALE; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; RAT; STREPTOZOCIN DIABETES;

ANIMALS; ATROPHY; BODY WATER; BRAIN; DIABETES COMPLICATIONS; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; DNA; DRUG COMBINATIONS; DRUG SYNERGISM; INJECTIONS, INTRAVENTRICULAR; INSULIN; INSULIN-LIKE GROWTH FACTOR I; MALE; MEMORY DISORDERS; NERVE TISSUE PROTEINS; ORGAN SIZE; RATS; RATS, WISTAR; TREATMENT OUTCOME;

RATTUS;

EID: 71849107467     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.09.063     Document Type: Article

References (67)

1. Araki Y., Nomura M., Tanaka H., Yamamoto H., Yamamoto T., Tsukaguchi I., and Nakamura H. MRI of the brain in diabetes mellitus. Neuroradiology 36 (1994) 101-103
2. Bailey C.H., and Kandel E.R. Structural changes accompanying memory storage. Annu. Rev. Physiol. 55 (1993) 397-426
3. Biessels G.J., Kamal A., Ramakers G.M., Urban I.J., Spruijt B.M., Erkelens D.W., and Gispen W.H. Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats. Diabetes 45 (1996) 1259-1266
4. Biessels G.J., Kamal A., Urban I.J., Spruijt B.M., Erkelens D.W., and Gispen W.H. Water maze learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: effects of insulin treatment. Brain Res. 800 (1998) 125-135
5. Bodkin N.L., Sportsman R., DiMarchi R.D., and Hansen B.C. Insulin-like growth factor-I in non-insulin-dependent diabetic monkeys: basal plasma concentrations and metabolic effects of exogenously administered biosynthetic hormone. Metabolism 40 (1991) 1131-1137
6. Brands A.M., Biessels G.J., Kappelle L.J., de Haan E.H., de Valk H.W., Algra A., and Kessels R.P. Cognitive functioning and brain MRI in patients with type 1 and type 2 diabetes mellitus: a comparative study. Dement. Geriatr. Cogn. Disord. 23 (2007) 343-350
7. Britton M., Rafols J., Alousi S., and Dunbar J.C. The effects of middle cerebral artery occlusion on central nervous system apoptotic events in normal and diabetic rats. Int. J. Exp. Diabesity Res. 4 (2003) 13-20
8. Bruning J.C., Gautam D., Burks D.J., Gillette J., Schubert M., Orban P.C., Klein R., Krone W., Muller-Wieland D., and Kahn C.R. Role of brain insulin receptor in control of body weight and reproduction. Science 289 (2000) 2122-2125
9. Busiguina S., Fernandez A.M., Barrios V., Clark R., Tolbert D.L., Berciano J., and Torres-Aleman I. Neurodegeneration is associated to changes in serum insulin-like growth factors. Neurobiol. Dis. 7 (2000) 657-665
10. Carro E., Trejo J.L., Spuch C., Bohl D., Heard J.M., and Torres-Aleman I. Blockade of the insulin-like growth factor I receptor in the choroid plexus originates Alzheimer's-like neuropathology in rodents: new cues into the human disease?. Neurobiol. Aging 27 (2006) 1618-1631
11. Coleman E., Judd R., Hoe L., Dennis J., and Posner P. Effects of diabetes mellitus on astrocyte GFAP and glutamate transporters in the CNS. Glia 48 (2004) 166-178
12. Craft S., Peskind E., Schwartz M.W., Schellenberg G.D., Raskind M., and Porte Jr. D. Cerebrospinal fluid and plasma insulin levels in Alzheimer's disease: relationship to severity of dementia and apolipoprotein E genotype. Neurology 50 (1998) 164-168
13. Cukierman T., Gerstein H.C., and Williamson J.D. Cognitive decline and dementia in diabetes-systematic overview of prospective observational studies. Diabetologia 48 (2005) 2460-2469
14. de Haas Ratzliff A., and Soltesz I. Differential expression of cytoskeletal proteins in the dendrites of parvalbumin-positive interneurons versus granule cells in the adult rat dentate gyrus. Hippocampus 10 (2000) 162-168
15. Dejgaard A., Gade A., Larsson H., Balle V., Parving A., and Parving H.H. Evidence for diabetic encephalopathy. Diabet. Med. 8 (1991) 162-167
16. den Heijer T., Vermeer S.E., van Dijk E.J., Prins N.D., Koudstaal P.J., Hofman A., and Breteler M.M. Type 2 diabetes and atrophy of medial temporal lobe structures on brain MRI. Diabetologia 46 (2003) 1604-1610
17. Donald M.W., Bird C.E., Lawson J.S., Letemendia F.J., Monga T.N., Surridge D.H., Varette-Cerre P., Williams D.L., Williams D.M., and Wilson D.L. Delayed auditory brainstem responses in diabetes mellitus. J. Neurol. Neurosurg. Psychiatry 44 (1981) 641-644
18. Edge J.A., Jakes R.W., Roy Y., Hawkins M., Winter D., Ford-Adams M.E., Murphy N.P., Bergomi A., Widmer B., and Dunger D.B. The UK case-control study of cerebral oedema complicating diabetic ketoacidosis in children. Diabetologia 49 (2006) 2002-2009
19. Emerick A.J., Richards M.P., Kartje G.L., Neafsey E.J., and Stubbs Jr. E.B. Experimental diabetes attenuates cerebral cortical-evoked forelimb motor responses. Diabetes 54 (2005) 2764-2771
20. Engert F., and Bonhoeffer T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399 (1999) 66-70
21. Fernyhough P., Mill J.F., Roberts J.L., and Ishii D.N. Stabilization of tubulin mRNAs by insulin and insulin-like growth factor I during neurite formation. Brain Res. Mol. Brain Res. 6 (1989) 109-120
22. Fifkova E., and Morales M. Actin matrix of dendritic spines, synaptic plasticity, and long-term potentiation. Int. Rev. Cytol. 139 (1992) 267-307
23. Fox M.A., Chen R.S., and Holmes C.S. Gender differences in memory and learning in children with insulin-dependent diabetes mellitus (IDDM) over a 4-year follow-up interval. J. Pediatr. Psychol. 28 (2003) 569-578
24. Glaser N.S., Wootton-Gorges S.L., Marcin J.P., Buonocore M.H., Dicarlo J., Neely E.K., Barnes P., Bottomly J., and Kuppermann N. Mechanism of cerebral edema in children with diabetic ketoacidosis. J. Pediatr. 145 (2004) 164-171
25. Goya L., de la Puente A., Ramos S., Martin M.A., Escriva F., Alvarez C., and Pascual-Leone A.M. Regulation of IGF-I and -II by insulin in primary cultures of fetal rat hepatocytes. Endocrinology 142 (2001) 5089-5096
26. Janson J., Laedtke T., Parisi J.E., O'Brien P., Petersen R.C., and Butler P.C. Increased risk of type 2 diabetes in Alzheimer disease. Diabetes 53 (2004) 474-481
27. Kamal A., Biessels G.J., Gispen W.H., and Ramakers G.M. Synaptic transmission changes in the pyramidal cells of the hippocampus in streptozotocin-induced diabetes mellitus in rats. Brain Res. 1073-1074 (2006) 276-280
28. Kawashima R., Kojima H., Nakamura K., Arahata A., Fujita Y., Tokuyama Y., Saito T., Furudate S., Kurihara T., Yagishita S., Kitamura K., and Tamai Y. Alterations in mRNA expression of myelin proteins in the sciatic nerves and brains of streptozotocin-induced diabetic rats. Neurochem. Res. 32 (2007) 1002-1010
29. Lechuga-Sancho A.M., Arroba A.I., Frago L.M., Paneda C., Garcia-Caceres C., Delgado Rubin de Celix A., Argente J., and Chowen J.A. Activation of the intrinsic cell death pathway, increased apoptosis and modulation of astrocytes in the cerebellum of diabetic rats. Neurobiol. Dis. 23 (2006) 290-299
30. Lee M.K., Tuttle J.B., Rebhun L.I., Cleveland D.W., and Frankfurter A. The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil. Cytoskeleton 17 (1990) 118-132
31. Lunetta M., Damanti A.R., Fabbri G., Lombardo M., Di Mauro M., and Mughini L. Evidence by magnetic resonance imaging of cerebral alterations of atrophy type in young insulin-dependent diabetic patients. J. Endocrinol. Invest. 17 (1994) 241-245
32. Lupien S.B., Bluhm E.J., and Ishii D.N. Systemic insulin-like growth factor-I administration prevents cognitive impairment in diabetic rats, and brain IGF regulates learning/memory in normal adult rats. J. Neurosci. Res. 74 (2003) 512-523
33. Lupien S.B., Bluhm E.J., and Ishii D.N. Effect of IGF-I on DNA, RNA, and protein loss associated with brain atrophy and impaired learning in diabetic rats. Neurobiol. Dis. 21 (2006) 487-495
34. Minamide L.S., and Bamburg J.R. A filter paper dye-binding assay for quantitative determination of protein without interference from reducing agents or detergents. Anal. Biochem. 190 (1990) 66-70
35. Mohiuddin L., Fernyhough P., and Tomlinson D.R. Reduced levels of mRNA encoding endoskeletal and growth-associated proteins in sensory ganglia in experimental diabetes. Diabetes 44 (1995) 25-30
36. Murialdo G., Barreca A., Nobili F., Rollero A., Timossi G., Gianelli M.V., Copello F., Rodriguez G., and Polleri A. Relationships between cortisol, dehydroepiandrosterone sulphate and insulin-like growth factor-I system in dementia. J. Endocrinol. Invest. 24 (2001) 139-146
37. Olchovsky D., Bruno J.F., Wood T.L., Gelato M.C., Leidy Jr. J.W., Gilbert Jr. J.M., and Berelowitz M. Altered pituitary growth hormone (GH) regulation in streptozotocin-diabetic rats: a combined defect of hypothalamic somatostatin and GH-releasing factor. Endocrinology 126 (1990) 53-61
38. Ott A., Stolk R.P., van Harskamp F., Pols H.A., Hofman A., and Breteler M.M. Diabetes mellitus and the risk of dementia: The Rotterdam study. Neurology 53 (1999) 1937-1942
39. Ozkaya Y.G., Agar A., Hacioglu G., and Yargicoglu P. Exercise improves visual deficits tested by visual evoked potentials in streptozotocin-induced diabetic rats. Tohoku J. Exp. Med. 213 (2007) 313-321
40. Palo J., Reske-Nielsen E., and Riekkinen P. Enzyme and protein studies of demyelination in diabetes. J. Neurol. Sci. 33 (1977) 171-178
41. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1986), Academic Press, Sydney; Orlando
42. Perros P., Deary I.J., Sellar R.J., Best J.J., and Frier B.M. Brain abnormalities demonstrated by magnetic resonance imaging in adult IDDM patients with and without a history of recurrent severe hypoglycemia. Diabetes Care 20 (1997) 1013-1018
43. Piotrowski P. Morphology of experimental diabetes and cerebral ischemia in the rat brain. Folia Neuropathol. 37 (1999) 252-255
44. Piotrowski P., Wierzbicka K., and Smialek M. Neuronal death in the rat hippocampus in experimental diabetes and cerebral ischaemia treated with antioxidants. Folia Neuropathol. 39 (2001) 147-154
45. Pozzessere G., Rizzo P.A., Valle E., Mollica M.A., Meccia A., Morano S., Di Mario U., Andreani D., and Morocutti C. Early detection of neurological involvement in IDDM and NIDDM. Multimodal evoked potentials versus metabolic control. Diabetes Care 11 (1988) 473-480
46. Prescott J.H., Richardson J.T., and Gillespie C.R. Cognitive function in diabetes mellitus: the effects of duration of illness and glycaemic control. Br. J. Clin. Psychol. 29 Pt. 2 (1990) 167-175
47. Pulford B.E., and Ishii D.N. Uptake of circulating insulin-like growth factors (IGFs) into cerebrospinal fluid appears to be independent of the IGF receptors as well as IGF-binding proteins. Endocrinology 142 (2001) 213-220
48. Razay G., and Wilcock G.K. Hyperinsulinaemia and Alzheimer's disease. Age Ageing 23 (1994) 396-399
49. Recio-Pinto E., and Ishii D.N. Effects of insulin, insulin-like growth factor-II and nerve growth factor on neurite outgrowth in cultured human neuroblastoma cells. Brain Res. 302 (1984) 323-334
50. Recio-Pinto E., Rechler M.M., and Ishii D.N. Effects of insulin, insulin-like growth factor-II, and nerve growth factor on neurite formation and survival in cultured sympathetic and sensory neurons. J. Neurosci. 6 (1986) 1211-1219
51. Reger M.A., Watson G.S., Frey Jr. W.H., Baker L.D., Cholerton B., Keeling M.L., Belongia D.A., Fishel M.A., Plymate S.R., Schellenberg G.D., Cherrier M.M., and Craft S. Effects of intranasal insulin on cognition in memory-impaired older adults: modulation by APOE genotype. Neurobiol. Aging 27 (2006) 451-458
52. Reske-Nielsen E., and Lundbaek K. Diabetic encephalopathy. Diffuse and focal lesions of the brain in long-term diabetes. Acta Neurol Scand Suppl. 39 Suppl. 4 (1963) 273-290
53. Rivera E.J., Goldin A., Fulmer N., Tavares R., Wands J.R., and de la Monte S.M. Insulin and insulin-like growth factor expression and function deteriorate with progression of Alzheimer's disease: link to brain reductions in acetylcholine. J. Alzheimers Dis. 8 (2005) 247-268
54. Rizk N.N., Rafols J., and Dunbar J.C. Cerebral ischemia induced apoptosis and necrosis in normal and diabetic rats. Brain Res. 1053 (2005) 1-9
55. Rollero A., Murialdo G., Fonzi S., Garrone S., Gianelli M.V., Gazzerro E., Barreca A., and Polleri A. Relationship between cognitive function, growth hormone and insulin-like growth factor I plasma levels in aged subjects. Neuropsychobiology 38 (1998) 73-79
56. Ryan C.M., Williams T.M., Finegold D.N., and Orchard T.J. Cognitive dysfunction in adults with type 1 (insulin-dependent) diabetes mellitus of long duration: effects of recurrent hypoglycaemia and other chronic complications. Diabetologia 36 (1993) 329-334
57. Schmidt R.E., Beaudet L.N., Plurad S.B., and Dorsey D.A. Axonal cytoskeletal pathology in aged and diabetic human sympathetic autonomic ganglia. Brain Res. 769 (1997) 375-383
58. Schubert M., Brazil D.P., Burks D.J., Kushner J.A., Ye J., Flint C.L., Farhang-Fallah J., Dikkes P., Warot X.M., Rio C., Corfas G., and White M.F. Insulin receptor substrate-2 deficiency impairs brain growth and promotes tau phosphorylation. J. Neurosci. 23 (2003) 7084-7092
59. Schubert M., Gautam D., Surjo D., Ueki K., Baudler S., Schubert D., Kondo T., Alber J., Galldiks N., Kustermann E., Arndt S., Jacobs A.H., Krone W., Kahn C.R., and Bruning J.C. Role for neuronal insulin resistance in neurodegenerative diseases. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 3100-3105
60. Schummers J., Yu H., and Sur M. Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Science 320 (2008) 1638-1643
61. Seigel G.M., Lupien S.B., Campbell L.M., and Ishii D.N. Systemic IGF-I treatment inhibits cell death in diabetic rat retina. J. Diabetes Complicat. 20 (2006) 196-204
62. Sjobeck M., Haglund M., and Englund E. Decreasing myelin density reflected increasing white matter pathology in Alzheimer's disease-a neuropathological study. Int. J. Geriatr. Psychiatry 20 (2005) 919-926
63. Tan K., and Baxter R.C. Serum insulin-like growth factor I levels in adult diabetic patients: the effect of age. J. Clin. Endocrinol. Metab. 63 (1986) 651-655
64. Wang C., Li Y., Wible B., Angelides K.J., and Ishii D.N. Effects of insulin and insulin-like growth factors on neurofilament mRNA and tubulin mRNA content in human neuroblastoma SH-SY5Y cells. Brain Res. Mol. Brain Res. 13 (1992) 289-300
65. Watanabe T., Miyazaki A., Katagiri T., Yamamoto H., Idei T., and Iguchi T. Relationship between serum insulin-like growth factor-1 levels and Alzheimer's disease and vascular dementia. J. Am. Geriatr. Soc. 53 (2005) 1748-1753
66. Woods S.C., Seeley R.J., Baskin D.G., and Schwartz M.W. Insulin and the blood-brain barrier. Curr. Pharm. Des. 9 (2003) 795-800
67. Wuarin L., Namdev R., Burns J.G., Fei Z.J., and Ishii D.N. Brain insulin-like growth factor-II mRNA content is reduced in insulin-dependent and non-insulin-dependent diabetes mellitus. J. Neurochem. 67 (1996) 742-751