Artículo

Vinuesa, A.; Pomilio, C.; Menafra, M.; Bonaventura, M.M.; Garay, L.; Mercogliano, M.F.; Schillaci, R.; Lux Lantos, V.; Brites, F.; Beauquis, J.; Saravia, F. "Juvenile exposure to a high fat diet promotes behavioral and limbic alterations in the absence of obesity" (2016) Psychoneuroendocrinology. 72:22-33
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Abstract:

The incidence of metabolic disorders including obesity, type 2 diabetes and metabolic syndrome have seriously increased in the last decades. These diseases – with growing impact in modern societies – constitute major risk factors for neurodegenerative disorders such as Alzheimer's disease (AD), sharing insulin resistance, inflammation and associated cognitive impairment. However, cerebral cellular and molecular pathways involved are not yet clearly understood. Thus, our aim was to study the impact of a non-severe high fat diet (HFD) that resembles western-like alimentary habits, particularly involving juvenile stages where the brain physiology and connectivity are in plain maturation. To this end, one-month-old C57BL/6J male mice were given either a control diet or HFD during 4 months. Exposure to HFD produced metabolic alterations along with changes in behavioral and central parameters, in the absence of obesity. Two-month-old HFD mice showed increased glycemia and plasmatic IL1β but these values normalized at the end of the HFD protocol at 5 months of age, probably representing an acute response that is compensated at later stages. After four months of HFD exposure, mice presented dyslipidemia, increased Lipoprotein-associated phospholipase A2 (Lp-PLA2) activity, hepatic insulin resistance and inflammation. Alterations in the behavioral profile of the HFD group were shown by the impediment in nest building behavior, deficiencies in short and mid-term spatial memories, anxious and depressive- like behavior. Regarding the latter disruptions in emotional processing, we found an increased neural activity in the amygdala, shown by a greater number of c-Fos+ nuclei. We found that hippocampal adult neurogenesis was decreased in HFD mice, showing diminished cell proliferation measured as Ki67+ cells and neuronal differentiation in SGZ by doublecortin labeling. These phenomena were accompanied by a neuroinflammatory and insulin-resistant state in the hippocampus, depicted by a reactive phenotype in Iba1+ microglia cells (increased in number and soma size) and an impaired response to insulin given by decreased phosphorylated Akt levels and increased levels of inhibitory phosphorylation of IRS1. Our data portray a set of alterations in behavioral and neural parameters as a consequence of an early-life exposure to a quite moderate high fat diet, many of which can resemble AD-related features. These results highly emphasize the need to study how metabolic and neurodegenerative disorders are interrelated in deep, thus allowing the finding of successful preventive and therapeutic approaches. © 2016 Elsevier Ltd

Registro:

Documento: Artículo
Título:Juvenile exposure to a high fat diet promotes behavioral and limbic alterations in the absence of obesity
Autor:Vinuesa, A.; Pomilio, C.; Menafra, M.; Bonaventura, M.M.; Garay, L.; Mercogliano, M.F.; Schillaci, R.; Lux Lantos, V.; Brites, F.; Beauquis, J.; Saravia, F.
Filiación:Neurobiology of Aging, Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina
Instituto de Biología y Medicina Experimental, CONICET, Buenos Aires, Argentina
Facultad de Farmacia y Bioquímica, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:Cognitive performance; Emotionality; High fat diet; Hippocampal neuroinflammation; Neurogenesis; Periadolescence; insulin receptor substrate 1; insulin receptor substrate 2; interleukin 1beta; Ki 67 antigen; phospholipase A2; protein c fos; protein kinase B; tumor necrosis factor alpha; adult; amygdala; animal experiment; animal model; animal tissue; anxiety; Article; behavior change; cell proliferation; controlled study; dentate gyrus; depression; disease association; dyslipidemia; enzyme activity; enzyme phosphorylation; gene expression; insulin resistance; lipid composition; lipid diet; male; memory disorder; motivation; mouse; nervous system inflammation; nonhuman; obesity; population exposure; priority journal; protein blood level; protein expression; protein phosphorylation; short term memory; spatial memory; amygdala; animal; animal behavior; C57BL mouse; cognitive defect; dyslipidemia; hippocampus; hyperinsulinism; inflammation; lipid diet; metabolism; nervous system development; pathology; pathophysiology; physiology; Amygdala; Animals; Behavior, Animal; Cognitive Dysfunction; Diet, High-Fat; Dyslipidemias; Hippocampus; Hyperinsulinism; Inflammation; Male; Mice; Mice, Inbred C57BL; Neurogenesis
Año:2016
Volumen:72
Página de inicio:22
Página de fin:33
DOI: http://dx.doi.org/10.1016/j.psyneuen.2016.06.004
Título revista:Psychoneuroendocrinology
Título revista abreviado:Psychoneuroendocrinology
ISSN:03064530
CODEN:PSYCD
CAS:insulin receptor substrate 1, 175335-32-7; insulin receptor substrate 2, 223747-03-3; phospholipase A2, 9001-84-7; protein kinase B, 148640-14-6
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03064530_v72_n_p22_Vinuesa

Referencias:

  • Andersen, S.L., Trajectories of brain development: point of vulnerability or window of opportunity? (2003) Neurosci. Biobehav. Rev., 27, pp. 3-18
  • 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
  • Beauquis, J., Saravia, F., Coulaud, J., Roig, P., Dardenne, M., Homo-Delarche, F., De Nicola, A., Prominently decreased hippocampal neurogenesis in a spontaneous model of type 1 diabetes, the nonobese diabetic mouse (2008) Exp. Neurol., 210, pp. 359-367
  • Beauquis, J., Homo-Delarche, F., Giroix, M.H., Ehses, J., Coulaud, J., Roig, P., Portha, B., Saravia, F., Hippocampal neurovascular and hypothalamic–pituitary–adrenal axis alterations in spontaneously type 2 diabetic GK rats (2010) Exp. Neurol., 222, pp. 125-134
  • Beauquis, J., Vinuesa, A., Pomilio, C., Pavia, P., Galvan, V., Saravia, F., Neuronal and glial alterations, increased anxiety, and cognitive impairment before hippocampal amyloid deposition in PDAPP mice, model of Alzheimer's disease (2014) Hippocampus, 24, pp. 257-269
  • Biessels, G., Kappelle, A., Bravenboer, B., Gispen, W., Cerebral function in diabetes mellitus (1994) Diabetologia, 37, pp. 643-650
  • Blank, M.L., Hall, M.N., Cress, E.A., Snyder, F., Inactivation of 1-alkyl-2-acetyl-sn-glycero-3-phosphocholine by a plasma acetylhydrolase: higher activities in hypertensive rats (1983) Biochem. Biophys. Res. Commun., 113, pp. 666-671
  • Boitard, C., Etchamendy, N., Sauvant, J., Aubert, A., Tronel, S., Marighetto, A., Laye, S., Ferreira, G., Juvenile, but not adult exposure to high-fat diet impairs relational memory and hippocampal neurogenesis in mice (2012) Hippocampus, 22, pp. 2095-2100
  • Boitard, C., Cavaroc, A., Sauvant, J., Aubert, A., Castanon, N., Laye, S., Ferreira, G., Impairment of hippocampal-dependent memory induced by juvenile high-fat diet intake is associated with enhanced hippocampal inflammation in rats (2014) Brain Behav. Immun., 40, pp. 9-17
  • Boitard, C., Maroun, M., Tantot, F., Cavaroc, A., Sauvant, J., Marchand, A., Laye, S., Ferreira, G., Juvenile obesity enhances emotional memory and amygdala plasticity through glucocorticoids (2015) J. Neurosci., 35, pp. 4092-4103
  • Bomfim, T.R., Forny-Germano, L., Sathler, L.B., Brito-Moreira, J., Houzel, J.C., Decker, H., Silverman, M.A., De Felice, F.G., An anti-diabetes agent protects the mouse brain from defective insulin signaling caused by Alzheimer's disease—associated Abeta oligomers (2012) J. Clin. Invest., 122, pp. 1339-1353
  • Bonaventura, M.M., Catalano, P.N., Chamson-Reig, A., Arany, E., Hill, D., Bettler, B., Saravia, F., Lux-Lantos, V.A., GABAB receptors and glucose homeostasis: evaluation in GABAB receptor knockout mice (2008) Am. J. Physiol. Endocrinol. Metab., 294, pp. E157-E167
  • Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding (1976) Anal. Biochem., 7, pp. 248-254
  • Broadbent, N.J., Squire, L.R., Clark, R.E., Spatial memory, recognition memory, and the hippocampus (2004) Proc. Natl. Acad. Sci. U. S. A., 101, pp. 14515-14520
  • Calvo-Ochoa, E., Arias, C., Cellular and metabolic alterations in the hippocampus caused by insulin signaling dysfunction and its association with cognitive impairment during aging and Alzheimer's disease: studies in animal models (2015) Diabetes Metab. Res. Rev., 31, pp. 1-13
  • Camus, M.C., Chapman, M.J., Forgez, P., Laplaud, P.M., Distribution and characterization of the serum lipoproteins and apoproteins in the mouse, Mus musculus (1983) J. Lipid Res., 24, pp. 1210-1228
  • Castanon, N., Luheshi, G., Laye, S., Role of neuroinflammation in the emotional and cognitive alterations displayed by animal models of obesity (2015) Front. Neurosci., 9, p. 229
  • Deacon, R.M., Altimiras, F.J., Bazan-Leon, E.A., Pyarasani, R.D., Nachtigall, F.M., Santos, L.S., Tsolaki, A.G., Cogram, P., Natural AD-Like neuropathology in octodon degus: impaired burrowing and neuroinflammation (2015) Curr. Alzheimer Res., 12, pp. 314-322
  • Deacon, R., Assessing burrowing, nest construction, and hoarding in mice (2012) J. Vis. Exp., p. e2607
  • Dineley, K.T., Jahrling, J.B., Denner, L., Insulin resistance in Alzheimer's disease (2014) Neurobiol. Dis., 72 (Pt. A), pp. 92-103
  • de la Monte, S.M., Tong, M., Brain metabolic dysfunction at the core of Alzheimer's disease (2014) Biochem. Pharmacol., 88, pp. 548-559
  • Fanselow, M.S., Dong, H.W., Are the dorsal and ventral hippocampus functionally distinct structures? (2010) Neuron, 65, pp. 7-19
  • Fehm, H.L., Kern, W., Peters, A., The selfish brain: competition for energy resources (2006) Prog. Brain Res., 153, pp. 129-140
  • Filali, M., Lalonde, R., Age-related cognitive decline and nesting behavior in an APPswe/PS1 bigenic model of Alzheimer's disease (2009) Brain Res., 1292, pp. 93-99
  • Freeman, L.R., Haley-Zitlin, V., Rosenberger, D.S., Granholm, A.C., Damaging effects of a high-fat diet to the brain and cognition: a review of proposed mechanisms (2014) Nutr. Neurosci., 17, pp. 241-251
  • Garay, L.I., Gonzalez Deniselle, M.C., Brocca, M.E., Lima, A., Roig, P., De Nicola, A.F., Progesterone down-regulates spinal cord inflammatory mediators and increases myelination in experimental autoimmune encephalomyelitis (2012) Neuroscience, 226, pp. 40-50
  • Grillo, C.A., Mulder, P., Macht, V.A., Kaigler, K.F., Wilson, S.P., Wilson, M.A., Reagan, L.P., Dietary restriction reverses obesity-induced anhedonia (2014) Physiol. Behav., 128, pp. 126-132
  • Henke, P.G., Limbic system modulation of stress ulcer development (1990) Ann. N. Y. Acad. Sci., 597, pp. 201-206
  • LeDoux, J., The emotional brain, fear, and the amygdala (2003) Cell. Mol. Neurobiol., 23, pp. 727-738
  • Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method (2001) Methods, 25, pp. 402-408
  • Maren, S., Synaptic mechanisms of associative memory in the amygdala (2005) Neuron, 47, pp. 783-786
  • Miller, A.A., Spencer, S.J., Obesity and neuroinflammation: a pathway to cognitive impairment (2014) Brain Behav. Immun., 42, pp. 10-21
  • Moll, L., Schubert, M., The role of insulin and insulin-like growth factor-1/FoxO-mediated transcription for the pathogenesis of obesity-associated dementia (2012) Curr. Gerontol. Geriatr. Res., 2012, p. 384094
  • Moon, M.L., Joesting, J.J., Lawson, M.A., Chiu, G.S., Blevins, N.A., Kwakwa, K.A., Freund, G.G., The saturated fatty acid, palmitic acid, induces anxiety-like behavior in mice (2014) Metabolism, 63, pp. 1131-1140
  • Moser, M.B., Moser, E.I., Distributed encoding and retrieval of spatial memory in the hippocampus (1998) J. Neurosci., 18, pp. 7535-7542
  • Muzzio, M.L., Miksztowicz, V., Brites, F., Aguilar, D., Repetto, E.M., Wikinski, R., Tavella, M., Berg, G.A., Metalloproteases 2 and 9: Lp-PLA(2) and lipoprotein profile in coronary patients (2009) Arch. Med. Res., 40, pp. 48-53
  • Papazoglou, I.K., Jean, A., Gertler, A., Taouis, M., Vacher, C.M., Hippocampal GSK3beta as a molecular link between obesity and depression (2015) Mol. Neurobiol., 52, pp. 363-374
  • Pomilio, C., Pavia, P., Gorojod, R.M., Vinuesa, A., Alaimo, A., Galvan, V., Kotler, M.L., Saravia, F., Glial alterations from early to late stages in a model of Alzheimer's disease: evidence of autophagy involvement in Abeta internalization (2016) Hippocampus, 26, pp. 194-210
  • Puder, J.J., Munsch, S., Psychological correlates of childhood obesity (2010) Int. J. Obes. (Lond.), 34 (Suppl. 2), pp. S37-S43
  • Russo, I., Barlati, S., Bosetti, F., Effects of neuroinflammation on the regenerative capacity of brain stem cells (2011) J. Neurochem., 116, pp. 947-956
  • Santos, L.E., Beckman, D., Ferreira, S.T., Microglial dysfunction connects depression and Alzheimer's disease (2015) Brain Behav. Immun., pp. 30056-30058. , pii: S0889-1591(15) [Epubaheadofprint]
  • 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
  • Sobesky, J.L., Barrientos, R.M., De May, H.S., Thompson, B.M., Weber, M.D., Watkins, L.R., Maier, S.F., High-fat diet consumption disrupts memory and primes elevations in hippocampal IL-1beta, an effect that can be prevented with dietary reversal or IL-1 receptor antagonism (2014) Brain Behav. Immun., 42, pp. 22-32
  • Spear, L.P., The adolescent brain and age-related behavioral manifestations (2000) Neurosci. Biobehav. Rev., 24, pp. 417-463
  • Stranahan, A.M., Arumugam, T.V., Cutler, R.G., Lee, K., Egan, J.M., Mattson, M.P., Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons (2008) Nat. Neurosci., 11, pp. 309-317
  • Tanti, A., Belzung, C., Hippocampal neurogenesis: a biomarker for depression or antidepressant effects? Methodological considerations and perspectives for future research (2013) Cell Tissue Res., 354, pp. 203-219
  • Vadas, O., Burke, J.E., Zhang, X., Berndt, A., Williams, R.L., Structural basis for activation and inhibition of class I phosphoinositide 3-kinases (2011) Sci. Signal., 4, p. re2
  • Valdivia, S., Patrone, A., Reynaldo, M., Perello, M., Acute high fat diet consumption activates the mesolimbic circuit and requires orexin signaling in a mouse model (2014) PLoS One, 9, p. e87478
  • Valladolid-Acebes, I., Fole, A., Martin, M., Morales, L., Cano, M.V., Ruiz-Gayo, M., Del Olmo, N., Spatial memory impairment and changes in hippocampal morphology are triggered by high-fat diets in adolescent mice. Is there a role of leptin? (2013) Neurobiol. Learn. Mem., 106, pp. 18-25
  • Velloso, L.A., Folli, F., Saad, M.J., TLR4 at the crossroads of nutrients, gut microbiota, and metabolic inflammation (2015) Endocr. Rev., 36, pp. 245-271
  • Vendruscolo, L.F., Gueye, A.B., Darnaudery, M., Ahmed, S.H., Cador, M., Sugar overconsumption during adolescence selectively alters motivation and reward function in adult rats (2010) PLoS One, 5, p. e9296
  • WHO, (2015), http://www.who.int/dietphysicalactivity/childhood; Wesson, D.W., Wilson, D.A., Age and gene overexpression interact to abolish nesting behavior in Tg2576 amyloid precursor protein (APP) mice (2011) Behav. Brain Res., 216, pp. 408-413
  • Yirmiya, R., Rimmerman, N., Reshef, R., Depression as a microglial disease (2015) Trends Neurosci., 38, pp. 637-658

Citas:

---------- APA ----------
Vinuesa, A., Pomilio, C., Menafra, M., Bonaventura, M.M., Garay, L., Mercogliano, M.F., Schillaci, R.,..., Saravia, F. (2016) . Juvenile exposure to a high fat diet promotes behavioral and limbic alterations in the absence of obesity. Psychoneuroendocrinology, 72, 22-33.
http://dx.doi.org/10.1016/j.psyneuen.2016.06.004
---------- CHICAGO ----------
Vinuesa, A., Pomilio, C., Menafra, M., Bonaventura, M.M., Garay, L., Mercogliano, M.F., et al. "Juvenile exposure to a high fat diet promotes behavioral and limbic alterations in the absence of obesity" . Psychoneuroendocrinology 72 (2016) : 22-33.
http://dx.doi.org/10.1016/j.psyneuen.2016.06.004
---------- MLA ----------
Vinuesa, A., Pomilio, C., Menafra, M., Bonaventura, M.M., Garay, L., Mercogliano, M.F., et al. "Juvenile exposure to a high fat diet promotes behavioral and limbic alterations in the absence of obesity" . Psychoneuroendocrinology, vol. 72, 2016, pp. 22-33.
http://dx.doi.org/10.1016/j.psyneuen.2016.06.004
---------- VANCOUVER ----------
Vinuesa, A., Pomilio, C., Menafra, M., Bonaventura, M.M., Garay, L., Mercogliano, M.F., et al. Juvenile exposure to a high fat diet promotes behavioral and limbic alterations in the absence of obesity. Psychoneuroendocrinology. 2016;72:22-33.
http://dx.doi.org/10.1016/j.psyneuen.2016.06.004