Artículo

Revsin, Y.; Saravia, F.; Roig, P.; Lima, A.; De Kloet, E.R.; Homo-Delarche, F.; De Nicola, A.F. "Neuronal and astroglial alterations in the hippocampus of a mouse model for type 1 diabetes" (2005) Brain Research. 1038(1):22-31
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Abstract:

The influence of diabetes mellitus on brain pathology is increasingly recognized. Previous contributions of our laboratory demonstrated in models of type 1 diabetes (nonobese diabetic and streptozotocin (STZ)-treated mice), a marked astrogliosis and neurogenesis deficit in hippocampus and increased expression of hypothalamic neuropeptides. In the present investigation, we further analyzed alterations of astroglia and neurons in the hippocampus of mice 1 month after STZ-induced diabetes. Results showed that these STZ-diabetic mice presented: (a) increased number of astrocytes positive for apolipoprotein-E (Apo-E), a marker of ongoing neuronal dysfunction; (b) abnormal expression of early gene products associated with neuronal activation, including a high number of Jun + neurons in CA1 and CA3 layers and dentate gyrus, and of Fos-expressing neurons in CA3 layer; (c) augmented activity of NADPH-diaphorase, linked to oxidative stress, in CA3 region. These data support the concept that uncontrolled diabetes leads to hippocampal pathology, which adjoin to changes in other brain structures such as hypothalamus and cerebral cortex. © 2005 Elsevier B.V. All rights reserved.

Registro:

Documento: Artículo
Título:Neuronal and astroglial alterations in the hippocampus of a mouse model for type 1 diabetes
Autor:Revsin, Y.; Saravia, F.; Roig, P.; Lima, A.; De Kloet, E.R.; Homo-Delarche, F.; De Nicola, A.F.
Filiación:Lab. of Neuroendocrine Biochemistry, Inst. of Biol. and Exp. Medicine, Obligado 2490, (1428) Buenos Aires, Argentina
Department of Human Biochemistry, Faculty of Medicine, University of Buenos Aires, Argentina
Department of Medical Pharmacology, Leiden University, Netherlands
CNRS UMR 7059, University Paris 7/D. Diderot, Paris, France
Lab. of Neuroendocrine Biochemistry, Inst. de Biol. Y Med. Experimental, Obligado 2490, 1428, Buenos Aires, Argentina
Palabras clave:Apolipoprotein-E, Fos, Jun, NADPH-diaphorase; Astrocytes; Diabetes mellitus; Hippocampus; Neurodegeneration; Neurons; Streptozotocin; apolipoprotein E; gene product; molecular marker; protein c fos; protein c jun; reduced nicotinamide adenine dinucleotide phosphate dehydrogenase; streptozocin; animal experiment; animal model; animal tissue; article; brain cortex; brain region; cell activation; cell count; controlled study; dentate gyrus; enzyme activity; female; gene expression; gene mutation; genetic analysis; genetic linkage; hippocampus; insulin dependent diabetes mellitus; macroglia; mouse; nerve cell lesion; nonhuman; oxidative stress; priority journal; streptozocin diabetes
Año:2005
Volumen:1038
Número:1
Página de inicio:22
Página de fin:31
DOI: http://dx.doi.org/10.1016/j.brainres.2004.12.032
Título revista:Brain Research
Título revista abreviado:Brain Res.
ISSN:00068993
CODEN:BRREA
CAS:reduced nicotinamide adenine dinucleotide phosphate dehydrogenase, 9001-68-7; streptozocin, 18883-66-4
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00068993_v1038_n1_p22_Revsin

Referencias:

  • Bering, R., Johansen, F.F., Expression of somatostatin mRNA and peptide in rat hippocampus after cerebral ischemia (1993) Regul. Pept., 49, pp. 41-48
  • Bestetti, B., Rossi, G.L., Hypothalamic lesions in rats with long-term streptozotocin-induced diabetes mellitus (1980) Acta Neuropathol., 52, pp. 119-127
  • Biessels, G.J., Kappelle, A.C., Bravenboer, B., Erkelens, D., Gispen, W.H., Cerebral function in diabetes mellitus (1994) Diabetologia, 37, pp. 643-650
  • Biessels, G., Kamal, A., Ramakers, G.M., Urban, I.J., Spruijt, B.M., Erkelens, D.W., Gispen, W.H., Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats (1996) Diabetes, 45, pp. 1259-1266
  • Biessels, G.J., Van Der Heide, L.P., Kamal, A., Bleys, A.W., Gispen, W.H., Ageing and diabetes: Implications for brain function (2002) Eur. J. Pharmacol., 441, pp. 1-14
  • Boschert, U., Merlo-Pich, E., Higgins, G., Roses, A.D., Catsicas, S., Apolipoprotein e expression by neurons surviving excitotoxic stress (1999) Neurobiol. Dis., 6, pp. 508-514
  • Bredt, D.S., Hwang, P.M., Snyder, S.H., Localization of nitric oxide synthase indicating a neural role for nitric oxide (1990) Nature, 347, pp. 768-770
  • Chabot, C.H., Massicotte, G., Milot, M., Trudeau, F., Gagne, J., Impaired modulation of AMPA receptors by calcium-dependent processes in streptozotocin-induced diabetic rats (1997) Brain Res., 768, pp. 249-256
  • De Kloet, E.R., Oitzl, M., Joels, M., Stress and cognition: Are corticosteroids good or bad guys? (1999) Trends Neurosci., 22, pp. 422-426
  • De Nicola, A.F., Magariños, A.M., Foglia, V.G., Neuroendocrine regulation in experimental diabetes (Houssay Lecture) (1991) Diabetes, pp. 3-8. , H. Rifkin J.A. Colwell S.I. Taylor Elsevier Science Publishers
  • Dheen, S.T., Tay, S.S.W., Wong, W.C., Arginine vasopressin- and oxytocin-like immunoreactive neurons in the hypothalamic paraventricular and supraoptic nuclei of streptozotocin-induced diabetic rats (1994) Arch. Histol. Cytol., 57, pp. 461-472
  • Dragunow, M., Axotomized medial septal-diagonal band neurons express Jun-like immunoreactivity (1992) Mol. Brain Res., 15, pp. 141-144
  • Eilers, A., Whitfield, J., Shah, B., Spadoni, C., Desmond, H., Ham, J., Direct inhibition of c-Jun N-terminal kinase in sympathetic neurones prevents c-jun promoter and NGF withdrawal-induced death (2001) J. Neurochem., 76, pp. 1439-1454
  • Eng, L.F., Ghirnikar, R.S., GFAP and astrogliosis (1994) Brain Pathol., 4, pp. 229-237
  • Fagan, A.M., Murphy, B.A., Patel, S.N., Kilbridge, J.F., Mobley, W.C., Bu, G., Holtzman, D.M., Evidence for normal aging of the septo-hippocampal cholinergic system in apoE (-/-) mice but impaired clearance of axonal degeneration products following injury (1998) Exp. Neurol., 151, pp. 314-325
  • Ferguson, S.C., Deary, I.J., Evans, J.C., Ellard, S., Hattersley, A.T., Frier, B.M., Apolipoprotein-E influences aspects of intellectual ability in type 1 diabetes (2003) Diabetes, 52, pp. 145-148
  • Flood, J.F., Mooradian, A.D., Morley, J.E., Characteristics of learning and memory in streptozocin-induced diabetic mice (1990) Diabetes, 39, pp. 1391-1398
  • Franceschi, M., Cecchetto, R., Minicucci, S., Smizne, G., Baio, G., Canal, N., Cognitive processes in insulin-dependent diabetes (1984) Diabetes Care, 7, pp. 228-231
  • Fujita, S.C., Sakuta, K., Tsuchiya, R., Hamanaka, H., Apolipoprotein e is found in astrocytes but not in microglia in the normal mouse brain (1999) Neurosci. Res., 35, pp. 123-133
  • Gardoni, F., Kamal, A., Bellone, C., Biessels, G.J., Ramakers, G.M.J., Cattabeni, F., Gispen, W.H., Di Luca, M., Effects of streptozotocin-diabetes on the hippocampal NMDA receptor complex in rats (2002) J. Neurochem., 80, pp. 438-447
  • Garthwaite, J., Glutamate, nitric oxide and cell-cell signaling in the nervous system (1991) Trends Neurosci., 14, pp. 60-67
  • Gibson, M.J., De Nicola, A.F., Krieger, D.T., Streptozotocin-induced diabetes is associated with reduced immunoreactive-beta endorphin concentrations in neurointermediate lobe and with disrupted circadian periodicity of plasma corticosterone levels (1985) Neuroendocrinology, 41, pp. 64-71
  • Gispen, W.H., Biessels, G.J., Cognition and synaptic plasticity in diabetes mellitus (2000) Trends Neurosci., 23, pp. 542-549
  • Gold, A.E., Deary, L.J., Jones, R.W., O'Hare, J.P., Reckless, J.P., Frier, B.M., Severe deterioration in cognitive function and personality in patients with long-standing diabetes: A complication of diabetes or a consequence of treatment? (1994) Diabet. Med., 11, pp. 499-505
  • Goss, J.R., Finch, C.E., Morgan, D.G., Age-related changes in glial fibrillary acidic protein mRNA in the mouse brain (1991) Neurobiol. Aging, 12, pp. 165-170
  • Grootendorst, J., Mulder, M., Haasdijt, E., De Kloet, R.E., Jaarsma, D., Presence of apolipoprotein e immunoreactivity in degenerating neurons of mice is dependent on the severity of kainic acid-induced lesion (2000) Brain Res., 868, pp. 165-175
  • Han, S., Einstein, G., Weisgraber, W.J., Strittmatter, A.M., Saunders, M., Pericak-Vance, M., Roses, A.D., Schmechel, D.E., Apolipoprotein e is localized to the cytoplasm of human cortical neurons: A light and electron microscopy study (1994) J. Neuropathol. Exp. Neurol., 53, pp. 535-544
  • Helgason, C.M., Blood glucose and stroke (1988) Stroke, 19, pp. 1049-1053
  • Herzog, K.H., Morgan, J.I., Cellular immediate-early genes and cell death in the nervous system (1996) Neuropathol. Appl. Neurobiol., 22, pp. 484-488
  • Hu, J., Ladu, M.J., Van Eldik, L.J., Apolipoprotein e attenuates β-amyloid-induced astrocyte activation (1998) J. Neurochem., 71, pp. 1626-1634
  • Hugues, P.E., Alexi, T., Walton, M., Williams, C.E., Dragunow, M., Clark, R.G., Gluckman, P.D., Activity and injury-dependent expression of inducible transcription factors, growth factors and apoptosis-related genes within the central nervous system (1999) Prog. Neurobiol., 57, pp. 421-450
  • Ignatius, M.J., Gebicke-Harter, P.J., Pate Skene, J.H., Schilling, J.W., Weisgraber, K.H., Mahley, R.W., Shooter, E.M., Expression of apolipoprotein e during nerve degeneration and regeneration (1986) Proc. Natl. Acad. Sci. U. S. A., 83, pp. 1125-1129
  • Jackson-Guilford, J., Leander, J.D., Nisenbaum, L.K., The effect of streptozotocin-induced diabetes on cell proliferation in the rat dentate gyrus (2000) Neurosci. Lett., 29, pp. 91-94
  • Kamal, A., Biessels, G.J., Urban, I.J., Gispen, W.H., Hippocampal synaptic plasticity in streptozotocin-diabetic rats: Interaction of diabetes and ageing (1999) Neuroscience, 90, pp. 737-745
  • Keilhoff, G., Fansa, H., Wolf, G., Differences in peripheral nerve degeneration/regeneration between wild-type and neuronal nitric oxide synthase knockout mice (2002) J. Neurosci. Res., 68, pp. 432-441
  • Labombarda, F., Gonzalez, S., Roig, P., Lima, A., Guennoun, R., Schumacher, M., De Nicola, A.F., Modulation of NADPH-diaphorase and glial fibrillary acidic protein by progesterone in astrocytes from normal and injured rat spinal cord (2000) J. Steroid Biochem. Mol. Biol., 73, pp. 159-169
  • Launer, L.J., Rodriguez, B.L., Peila, R., Type 2 diabetes, APOE gene, and the risk for dementia and related pathologies (2002) Diabetes, 51, pp. 1256-1262
  • Leah, J.D., Herdegen, T., Bravo, R., Selective expression of Jun proteins following axotomy and axonal transport block in peripheral nerves in the rat: Evidence for a role in the regeneration process (1991) Brain Res., 566, pp. 198-207
  • Li, Z.G., Zhang, W., Grunberger, G., Sima, A.A.F., Hippocampal neuronal apoptosis in type 1 diabetes (2002) Brain Res., 946, pp. 221-231
  • Luo, Y., Kaur, C.H., Ling, E.A., Neuronal and glial response in the rat hypothalamus-neurohypophysis complex with streptozotocin-induced diabetes (2002) Brain Res., 925, pp. 42-54
  • Magariños, A.M., McEwen, B.S., Experimental diabetes in rats causes hippocampal dendritic and synaptic reorganization and increased glucocorticoid reactivity to stress (2000) Proc. Natl. Acad. Sci. U. S. A., 97, pp. 11056-11061
  • Magistretti, P., Pellerin, L., Astrocytes couple synaptic activity to glucose utilization in the brain (1999) News Physiol. Sci., 14, pp. 177-182
  • Mankovsky, B.N., Cerebrovascular disorders in patients with diabetes mellitus (1997) J. Diabetes Its Complicat., 10, pp. 228-242
  • Mc Call, A.L., The impact of diabetes on the CNS (1992) Diabetes, 41, pp. 557-570
  • Metzger, R.E., Ladu, M.J., Pan, J.B., Getz, G.S., Fraail, D.E., Falduto, M.T., Neurons of the human frontal cortex display apolipoprotein e immunoreactivity: Implications for Alzheimer's disease (1996) J. Neuropathol. Exp. Neurol., 55, pp. 372-380
  • Morgan, J.I., Curran, T., Stimulus-transcription coupling in the nervous system: Involvement of the inducible proto-oncogenes fos and jun (1991) Annu. Rev. Neurosci., 14, pp. 421-451
  • Morgan, J.I., Curran, T., The immediate-early gene response and neuronal death and regeneration (1995) Neuroscientist, 1, pp. 68-75
  • Mukai, N., Hori, S., Pomeroy, M., Cerebral lesions in rats with streptozotocin-induced diabetes (1980) Acta Neuropathol. (Berlin), 51, pp. 79-84
  • Ott, A., Stolk, R.P., Van Harskamp, F., Pols, H.A.P., Hofman, A., Breteler, M.M.B., Diabetes mellitus and the risk of dementia: The Rotterdam study (1999) Neurology, 58, pp. 1937-1941
  • Ovtscharoff, W., Bozhilova-Pastirova, A., Christova, T., Postnatal development of neurons expressing NADPH-diaphorase and parvalbumin in the parietal cortex of male and female rats (2002) Acta Histochem., 104, pp. 23-28
  • Paxinos, G., Watson, C., (1983) The Rat Brain in Stereotaxic Coordinates, , Academic Press New York
  • Peila, R., Rodriguez, B.L., Launer, L., Type 2 Diabetes, APOE gene and risk for dementia and related pathologies. The Honolulu-Asia aging study (2002) Diabetes, 51, pp. 1256-1262
  • Pietrowski, P.K., Wierzbicka, Smiatek, M., Neuronal death in the rat hippocampus in experimental diabetes and cerebral ischaemia treated with antioxidants (2001) Folia Neuropathol., 39, pp. 147-154
  • Poirier, J., Apolipoprotein e in animal models of CNS injury and in Alzheimer's disease (1994) Trends Neurosci., 17, pp. 525-530
  • Pozas, E., Ballabriga, J., Planas, A.M., Ferrer, I., Kainic acid-induced excitotoxicity is associated with a complex c-Fos and c-Jun responses which does not preclude either cell death or survival (1997) J. Neurobiol., 33, pp. 232-246
  • Ridet, J.L., Malhotra, S.K., Privat, A., Gage, F.H., Reactive astrocytes: Cellular and molecular cues to biological function (1997) Trends Neurosci., 20, pp. 570-577
  • Saravia, F.E., Gonzalez, S., Roig, P., Alves, V., Homo-Delarche, F., De Nicola, A.F., Diabetes increases the expression of hypothalamic neuropeptides in a spontaneous model of type I diabetes, the nonobese diabetic (NOD) mouse (2001) Cell. Mol. Neurobiol., 21, pp. 15-27
  • Saravia, F.E., Pietranera, L., Lima, A., Roig, P., Revsin, Y., De Nicola, A.F., Deoxycorticosterone stimulates the activity of nicotinamide adenine dinucleotide phosphate-diaphorase/nitric oxide synthase immunoreactivity in the hypothalamic nuclei of rats (2002) Neurosci. Lett., 329, pp. 344-348
  • Saravia, F.E., Revsin, Y., Gonzalez Deniselle, M.C., Gonzalez, S., Roig, P., Lima, A., Homo-Delarche, F., De Nicola, A.F., Increased astrocyte reactivity in the hippocampus of murine models of type I diabetes: The nonobese diabetic (NOD) and streptozotocin treated mice (2002) Brain Res., 957, pp. 345-353
  • Saravia, F.E., Revsin, Y., Lux-Lantos, V., Beauquis, J., Homo-Delarche, F., De Nicola, A.F., Oestradiol restores cell proliferation in dentate gyrus and subventricular zone of streptozotocin-diabetic mice (2004) J. Neuroendocrinol., 16, pp. 704-710
  • Schoenle, E.J., Schoenle, D., Molinari, L., Largo, R.H., Impaired intellectual development in children with type 1 diabetes: Association with HbA,o, age and diagnosis and sex (2002) Diabetologia, 45, pp. 108-114
  • Serino, R., Ueta, Y., Tokunoga, M., Hara, Y., Nomura, M., Kabashima, N., Shibuta, I., Yamashita, H., Upregulation of hypothalamic nitric oxide synthase gene expression in streptozotocin-induced diabetic rats (1998) Diabetologia, 41, pp. 640-648
  • Sheng, M., Greenberg, M.E., The regulation and function of c-fos and other immediate early genes in the nervous system (1990) Neuron, 4, pp. 477-485
  • Smith, D.R., Hoyt, E.C., Gallagher, M., Schwabe, R.F., Lund, P.K., Effect of age and cognitive status on basal level AP-1 activity in rat hippocampus (2001) Neurobiol. Aging, 22, pp. 773-786
  • Stewart, R., Liolitsa, D., Type 2 diabetes mellitus, cognitive impairment and dementia (1999) Diabet. Med., 16, pp. 93-112
  • Strittmatter, W.J., Roses, A.D., Apolipoprotein e and Alzheimer's disease (1996) Annu. Rev. Neurosci., 19, pp. 53-77
  • Valastro, B., Cossette, N., Lavoie, N., Gagnon, S., Trudeau, F., Massicotte, G., Up-regulation of glutamate receptors is associated with LTP defects in the early stages of diabetes mellitus (2002) Diabetologia, 45, pp. 642-650
  • Veinbergs, I., Jung, M.W., Young, S.J., Van Uden, E., Groves, P.M., Masliah, E., Altered long-term potentiation in the hippocampus of apolipoprotein E-deficient mice (1998) Neurosci. Lett., 249, pp. 71-74
  • Vernet, D., Bonavera, J.J., Swerdloff, R.S., Gonzalez-Cadavid, N.F., Wang, C., Spontaneous expression of inducible nitric oxide synthase in the hypothalamus and other brain regions of aging rats (1998) Endocrinology, 139, pp. 3254-3261
  • Vicent, S.R., Kimura, H., Histochemical mapping of nitric oxide synthase in the rat brain (1992) Neuroscience, 46, pp. 755-784
  • Wallace, M.N., Fredens, K., Activated astrocytes of the mouse hippocampus contain high levels of NADPH-diaphorase (1992) NeuroReport, 3, pp. 953-956
  • Walton, M., MacGibbon, G., Young, D., Sirimanne, E., Williams, C., Gluckman, P., Dragunow, M., Do, M., C-Jun, c-Fos and amyloid precursor protein play a role in neuronal death or survival? (1998) J. Neurosci. Res., 53, pp. 330-342
  • Weeber, E.J., Beffert, U., Jones, C., Christian, J.M., Forster, E., Sweat, J.D., Herz, J., Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning (2002) J. Biol. Chem., 277, pp. 39944-39952
  • Wilkinson, D.G., Bhatt, S., Ryseck, R., Bravo, R., Tissue-specific expression of c-jun and jun B during organogenesis in the mouse (1989) Development, 106, pp. 465-471
  • Zhang, J., Zhang, D., McQuade, J.S., Behbehani, M., Tsien, J.Z., Xu, M., C-Fos regulates neuronal excitability and survival (2002) Nat. Genet., 4, pp. 416-420
  • Zheng, H., Li, Y.F., Weiss, M., Mayhan, W.G., Patel, K.P., Neuronal expression of fos protein in the forebrain of diabetic rats (2002) Brain Res., 956, pp. 268-275

Citas:

---------- APA ----------
Revsin, Y., Saravia, F., Roig, P., Lima, A., De Kloet, E.R., Homo-Delarche, F. & De Nicola, A.F. (2005) . Neuronal and astroglial alterations in the hippocampus of a mouse model for type 1 diabetes. Brain Research, 1038(1), 22-31.
http://dx.doi.org/10.1016/j.brainres.2004.12.032
---------- CHICAGO ----------
Revsin, Y., Saravia, F., Roig, P., Lima, A., De Kloet, E.R., Homo-Delarche, F., et al. "Neuronal and astroglial alterations in the hippocampus of a mouse model for type 1 diabetes" . Brain Research 1038, no. 1 (2005) : 22-31.
http://dx.doi.org/10.1016/j.brainres.2004.12.032
---------- MLA ----------
Revsin, Y., Saravia, F., Roig, P., Lima, A., De Kloet, E.R., Homo-Delarche, F., et al. "Neuronal and astroglial alterations in the hippocampus of a mouse model for type 1 diabetes" . Brain Research, vol. 1038, no. 1, 2005, pp. 22-31.
http://dx.doi.org/10.1016/j.brainres.2004.12.032
---------- VANCOUVER ----------
Revsin, Y., Saravia, F., Roig, P., Lima, A., De Kloet, E.R., Homo-Delarche, F., et al. Neuronal and astroglial alterations in the hippocampus of a mouse model for type 1 diabetes. Brain Res. 2005;1038(1):22-31.
http://dx.doi.org/10.1016/j.brainres.2004.12.032