Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

In human diabetes, degenerative and functional disorders of the central nervous system, including depression, are common findings. Defective dentate gyrus (DG) neurogenesis is associated with affective-related disorders and depression. We previously demonstrated reduced DG neurogenesis in a pharmacological type 1 diabetes model, the streptozotocin (STZ)-treated mouse. Here, we explored DG neurogenesis in a spontaneous T1D model, the nonobese diabetic (NOD) mouse, at prediabetic and diabetic stages. Cell proliferation was assessed in the DG of 5, 8 and 12-week-old control C57BL/6 and BALB/c strains and NOD mice, killed 2 h after bromodeoxyuridine (BrdU) administration. Survival of the newly generated cells was studied in 15-week-old animals that were killed 21 days after BrdU injection. The number of proliferative BrdU-positive cells in the DG was, regardless of age, constantly and significantly lower in NOD than in control strains, showing the presence of hippocampal alterations far before clinical diabetes onset in NOD mice. Diabetes also strongly decreased cell survival in NOD DG. However, cell phenotype proportion, as assessed by co-localization with neuronal or glial markers and confocal microscopy, was not modified. Hippocampal neurogenesis is strongly diminished in the spontaneous NOD model, like in the STZ model. Notably, NOD hippocampal DG cell proliferation defect takes place during the prediabetic stage. Whether this early alteration might result, in this autoimmune strain, from hypothalamo-pituitary adrenal axis alterations and/or ongoing brain inflammatory process sharing many characteristics of aging is discussed and deserves further investigation. © 2007 Elsevier Inc. All rights reserved.

Registro:

Documento: Artículo
Título:Prominently decreased hippocampal neurogenesis in a spontaneous model of type 1 diabetes, the nonobese diabetic mouse
Autor:Beauquis, J.; Saravia, F.; Coulaud, J.; Roig, P.; Dardenne, M.; Homo-Delarche, F.; De Nicola, A.
Filiación:Institute of Biology and Experimental Medicine, CONICET, Laboratory of Neuroendocrine Biochemistry, Obligado 2490, 1428 Buenos Aires, Argentina
Department of Biochemistry, Faculty of Medicine, University of Buenos Aires, Argentina
CNRS 7059, Université Paris 7, Paris, France
CNRS 8147, Hôpital Necker, Paris, France
Palabras clave:BrdU; Dentate gyrus neurogenesis; GFAP; NeuN; NOD mouse; Type 1 diabetes mellitus; broxuridine; corticosterone; DNA; streptozocin; animal cell; animal experiment; animal model; animal tissue; article; autoimmunity; cell proliferation; cell survival; central nervous system disease; central nervous system function; confocal microscopy; controlled study; dentate gyrus; depression; female; hippocampus; hypophysis adrenal system; inflammation; insulin dependent diabetes mellitus; mood disorder; mouse; nonhuman; nonobese diabetic mouse; phenotype; priority journal; streptozocin diabetes; Age Factors; Analysis of Variance; Animals; Bromodeoxyuridine; Cell Count; Cell Proliferation; Corticosterone; Diabetes Mellitus, Type 1; Disease Models, Animal; Female; Glial Fibrillary Acidic Protein; Hippocampus; Mice; Mice, Inbred BALB C; Mice, Inbred C57BL; Mice, Inbred NOD; Neurons; Phosphopyruvate Hydratase
Año:2008
Volumen:210
Número:2
Página de inicio:359
Página de fin:367
DOI: http://dx.doi.org/10.1016/j.expneurol.2007.11.009
Título revista:Experimental Neurology
Título revista abreviado:Exp. Neurol.
ISSN:00144886
CODEN:EXNEA
CAS:broxuridine, 59-14-3; corticosterone, 50-22-6; DNA, 9007-49-2; streptozocin, 18883-66-4; Bromodeoxyuridine, 59-14-3; Corticosterone, 50-22-6; Glial Fibrillary Acidic Protein; Phosphopyruvate Hydratase, EC 4.2.1.11
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00144886_v210_n2_p359_Beauquis

Referencias:

  • Abrous, D.N., Koehl, M., Le Moal, M., Adult neurogenesis: from precursors to network and physiology (2005) Physiol. Rev., 85, pp. 523-569
  • Altman, J., Das, G.D., Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats (1965) J. Comp. Neurol., 124, pp. 319-335
  • Amrani, A., Chaouloff, F., Mormede, P., Dardenne, M., Homo-Delarche, F., Glucose, insulin, and open field responses to immobilization in nonobese diabetic (NOD) mice (1994) Physiol. Behav., 56, pp. 241-246
  • Anderson, R., Freedland, K., Clouse, R., Lustman, P., The prevalence of comorbid depression in adults with diabetes. A meta-analysis (2001) Diabetes Care, 24, pp. 1069-1078
  • Beauquis, J., Roig, P., Homo-Delarche, F., De Nicola, A., Saravia, F., Reduced hippocampal neurogenesis and number of hilar neurones in streptozotocin-induced diabetic mice: reversion by antidepressant treatment (2006) Eur. J. Neurosci., 23, pp. 1539-1546
  • Biessels, G.J., Gispen, W.H., The impact of diabetes on cognition: what can be learned from rodent models? (2005) Neurobiol. Aging, 26 (SUPPL. 1), pp. 36-41
  • Bizon, J.L., Gallagher, M., Production of new cells in the rat dentate gyrus over the lifespan: relation to cognitive decline (2003) Eur. J. Neurosci., 18, pp. 215-219
  • Bluthe, R., Jafarian-Tehrani, M., Michaud, B., Haour, F., Dantzer, R., Homo-Delarche, F., Increased sensitivity of prediabetic nonobese diabetic mouse to the behavioral effects of IL-1 (1999) Brain Behav. Immun., 13, pp. 303-314
  • Cameron, A., Gould, E., Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus (1994) Neuroscience, 61, pp. 203-209
  • Cameron, A., Hazel, T., McKay, R., Regulation of neurogenesis by growth factors and neurotransmitters (1998) J. Neurobiology, 36, pp. 287-306
  • Coggeshall, R., Lekan, H., Methods for determining numbers of cells and synapses: a case for more uniform standards of review (1996) J. Comp. Neurol., 364, pp. 6-15
  • de Kloet, E.R., Vreugdenhil, E., Oitzl, M.S., Joels, M., Brain corticosteroid receptor balance in health and disease (1998) Endocr. Rev., 19, pp. 269-301
  • Dheen, S.T., Tay, S.S., 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
  • Flood, J., Mooradian, A., Morley, J., Characteristics of learning and memory in streptozotocin-induced diabetic mice (1990) Diabetes, 39, pp. 1391-1398
  • Fujioka, T., Sakata, Y., Yamaguchi, K., Shibasaki, T., Kato, H., Nakamura, S., The effects of prenatal stress on the development of hypothalamic paraventricular neurons in fetal rats (1999) Neuroscience, 92, pp. 1079-1088
  • Garcia, A., Steiner, B., Kronenberg, G., Bick-Sander, A., Kempermann, G., Age-dependent expression of glucocorticoid- and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus (2004) Aging Cell, 3, pp. 363-371
  • Gardoni, F., Kamal, A., Bellone, C., Biessels, G.J., Ramakers, G., 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
  • Gispen, W.H., Biessels, G.J., Cognition and synaptic plasticity in diabetes mellitus (2000) Trends Neurosci., 23, pp. 542-549
  • 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
  • Gross, C.G., Neurogenesis in the adult brain: death of a dogma (2000) Nat. Rev., Neurosci, 1, pp. 67-73
  • Harizi, H., Homo-Delarche, F., Amrani, A., Coulaud, J., Mormède, P., Marked genetic differences in the regulation of blood glucose under immune and restraint stress reveals a wide range of corticosensitivity (2007) J. Neuroimmunol., 189, pp. 59-68
  • Hayes, N.L., Nowakowski, R.S., Dynamics of cell proliferation in the adult dentate gyrus of two inbred strains of mice (2002) Brain Res Dev. Brain Res., 134, pp. 77-85
  • Homo-Delarche, F., Neuroendocrine immuno-ontogeny of the pathogenesis of autoimmune disease in the nonobese diabetic (NOD) mouse (2004) ILAR J, 45, pp. 237-258
  • Hougaard, K.S., Andersen, M.B., Kjaer, S.L., Hansen, A.M., Werge, T., Lund, S.P., Prenatal stress may increase vulnerability to life events: comparison with the effects of prenatal dexamethasone (2005) Brain Res. Dev. Brain Res., 159, pp. 55-63
  • Ichikawa, M., Koh, C.S., Inaba, Y., Seki, C., Inoue, A., Itoh, M., Ishihara, Y., Komiyama, A., IgG subclass switching is associated with the severity of experimental autoimmune encephalomyelitis induced with myelin oligodendrocyte glycoprotein peptide in NOD mice (1999) Cell. Immunol., 191, pp. 97-104
  • Jackson-Guilford, J., Leander, J., Nisenbaum, L., The effect of streptozotocin-induced diabetes on cell proliferation in the rat dentate gyrus (2000) Neurosci. Lett., 293, pp. 91-94
  • Kempermann, G., Jessberger, S., Steiner, B., Kronenberg, G., Milestones of neuronal development in the adult hippocampus (2004) Trends Neurosci., 27, pp. 447-452
  • Kempermann, G., Kuhn, H., Gage, F., Genetic influence on neurogenesis in the dentate gyrus of adult mice (1997) Proc. Natl. Acad. Sci. U. S. A., 94, pp. 10409-10414
  • Lehmann, A., (1974) Atlas Stereotaxique du Cerveau de la Souris, , Editions du Centre National de la Recherche Scientifique, Paris
  • Lie, D.C., Song, H., Colamarino, S.A., Ming, G.L., Gage, F.H., Neurogenesis in the adult brain: new strategies for central nervous system diseases (2004) Annu. Rev. Pharmacol. Toxicol., 44, pp. 399-421
  • Mankovsky, B., Cerebrovascular disorders in patients with diabetes mellitus (1997) J. Diabetes Its Complicat., 10, pp. 228-242
  • McCall, A., The impact of diabetes on the CNS (1992) Diabetes, 41, pp. 557-570
  • McEwen, B., Magariños, A., Reagan, L., Studies of hormone action in the hippocampal formation. Possible relevance to depression and diabetes (2002) J. Psychosom. Res., 53, pp. 883-890
  • Ming, G.L., Song, H., Adult neurogenesis in the mammalian central nervous system (2005) Annu. Rev. Neurosci., 28, pp. 223-250
  • Mirescu, C., Gould, E., Stress and adult neurogenesis (2006) Hippocampus, 16, pp. 233-238
  • Monje, M.L., Toda, H., Palmer, T.D., Inflammatory blockade restores adult hippocampal neurogenesis (2003) Science, 302, pp. 1760-1765
  • Morita, M., Kita, Y., Morikawa, N., Iwami, M., Notsu, Y., Expression of arginine vasopressin and vasopressin V1a receptor mRNA in diabetic (db/db) mice (2001) Exp. Clin. Endocrinol. Diabetes, 109, pp. 261-266
  • Ott, A., Stolk, R., van Harskamp, F., Pols, H., Hofman, A., Breteler, M., Diabetes mellitus and the risk of dementia: the Rotterdam study (1999) Neurology, 58, pp. 1937-1941
  • 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, pp. 22-31
  • Saravia, F., Beauquis, J., Pietranera, L., De Nicola, A.F., Neuroprotective effects of estradiol in hippocampal neurons and glia of middle age mice (2007) Psychoneuroendocrinology, 32, pp. 480-492
  • Saravia, F.E., Beauquis, J., Revsin, Y., Homo-Delarche, F., de Kloet, E.R., De Nicola, A.F., Hippocampal neuropathology of diabetes mellitus is relieved by estrogen treatment (2006) Cell. Mol. Neurobiol., 26, pp. 941-955
  • Saravia, F., Gonzalez, S., Roig, P., Alves, V., Homo-Delarche, F., De Nicola, A.F., Diabetes increases the expression of hypothalamic neuropeptides in the spontaneous model of type 1 diabetes, the nonobese diabetic (NOD) mouse (2001) Cell. Mol. Neurobiol., 21, pp. 15-27
  • Saravia, F., Revsin, Y., Gonzalez-Deniselle, M.S., Roig, P., Lima, A., Homo-Delarche, F., De Nicola, A.F., Increased astrocyte reactivity in the hippocampus of murine models of type 1 diabetes: the nonobese diabetic (NOD) and streptozotocin-treated mice (2002) Brain Research, 957, pp. 345-353
  • Saravia, F., 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
  • Schlessinger, A.R., Cowan, W.M., Gottlieb, D.I., An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat (1975) J. Comp. Neurol., 159, pp. 149-175
  • Selvarajah, D., Tesfaye, S., Central nervous system involvement in diabetes mellitus (2006) Curr. Diab. Rep., 6, pp. 431-438
  • Sheffield, L.G., Berman, N.E., Microglial expression of MHC class II increases in normal aging of nonhuman primates (1998) Neurobiol. Aging, 19, pp. 47-55
  • Suh, S.W., Fan, Y., Hong, S.M., Liu, Z., Matsumori, Y., Weinstein, P.R., Swanson, R.A., Liu, J., Hypoglycemia induces transient neurogenesis and subsequent progenitor cell loss in the rat hippocampus (2005) Diabetes, 54, pp. 500-509
  • Terao, A., Apte-Deshpande, A., Dousman, L., Morairty, S., Eynon, B.P., Kilduff, T.S., Freund, Y.R., Immune response gene expression increases in the aging murine hippocampus (2002) J. Neuroimmunol., 132, pp. 99-112
  • Valastro, B., Cossette, N., Lavoie, N., Gagnon, F., Trudeau, J., Massicote, M., Up-regulation of glutamate receptors is associated with LTP defects in the early stages of diabetes mellitus (2002) Diabetologia, 45, pp. 642-650
  • West, M., Regionally specific loss of neurons in the aging human hippocampus (1993) Neurobiol. Aging, 14, pp. 287-293
  • Yamada, K., Rensing, N., Izumi, Y., De Erausquin, G., Gazit, V., Dorsey, D., Repetitive hypoglycemia in young rats impairs hippocampal long-term potentiation (2004) Pediatr. Res., 55, pp. 372-379

Citas:

---------- APA ----------
Beauquis, J., Saravia, F., Coulaud, J., Roig, P., Dardenne, M., Homo-Delarche, F. & De Nicola, A. (2008) . Prominently decreased hippocampal neurogenesis in a spontaneous model of type 1 diabetes, the nonobese diabetic mouse. Experimental Neurology, 210(2), 359-367.
http://dx.doi.org/10.1016/j.expneurol.2007.11.009
---------- CHICAGO ----------
Beauquis, J., Saravia, F., Coulaud, J., Roig, P., Dardenne, M., Homo-Delarche, F., et al. "Prominently decreased hippocampal neurogenesis in a spontaneous model of type 1 diabetes, the nonobese diabetic mouse" . Experimental Neurology 210, no. 2 (2008) : 359-367.
http://dx.doi.org/10.1016/j.expneurol.2007.11.009
---------- MLA ----------
Beauquis, J., Saravia, F., Coulaud, J., Roig, P., Dardenne, M., Homo-Delarche, F., et al. "Prominently decreased hippocampal neurogenesis in a spontaneous model of type 1 diabetes, the nonobese diabetic mouse" . Experimental Neurology, vol. 210, no. 2, 2008, pp. 359-367.
http://dx.doi.org/10.1016/j.expneurol.2007.11.009
---------- VANCOUVER ----------
Beauquis, J., Saravia, F., Coulaud, J., Roig, P., Dardenne, M., Homo-Delarche, F., et al. Prominently decreased hippocampal neurogenesis in a spontaneous model of type 1 diabetes, the nonobese diabetic mouse. Exp. Neurol. 2008;210(2):359-367.
http://dx.doi.org/10.1016/j.expneurol.2007.11.009