Early and adult hippocampal TGF-β1 overexpression have opposite effects on behavior

TGF-β1 is an anti-inflammatory cytokine that is augmented in the brain of autistic patients and that can affect brain development. In this work, we studied the effects of overexpressing TGF-β1 in the dentate gyrus of adult or young mice on behavior. TGF-β1 overexpression during postnatal development...

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Autor principal: Depino, A.M
Otros Autores: Lucchina, L., Pitossi, F.
Formato: Capítulo de libro
Lenguaje:Inglés
Publicado: 2011
Acceso en línea:Registro en Scopus
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100 1 |a Depino, A.M. 
245 1 0 |a Early and adult hippocampal TGF-β1 overexpression have opposite effects on behavior 
260 |c 2011 
270 1 0 |m Depino, A.M.; Institute for Physiology, Molecular Biology and Neurosciences, CONICET-UBA, Ciudad Universitaria, Int. Guiraldes S/N, Pabellon 2, 2do piso, C1428EHA Buenos Aires, Argentina; email: adepino@conicet.gov.ar 
506 |2 openaire  |e Política editorial 
504 |a Ageta, H., Murayama, A., Migishima, R., Kida, S., Tsuchida, K., Yokoyama, M., Inokuchi, K., Activin in the brain modulates anxiety-related behavior and adult neurogenesis (2008) PLoS ONE, 3, pp. e1869 
504 |a Ansorge, M.S., Zhou, M., Lira, A., Hen, R., Gingrich, J.A., Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice (2004) Science, 306, pp. 879-881 
504 |a Ashwood, P., Enstrom, A., Krakowiak, P., Hertz-Picciotto, I., Hansen, R.L., Croen, L.A., Ozonoff, S., Van de Water, J., Decreased transforming growth factor beta1 in autism: a potential link between immune dysregulation and impairment in clinical behavioral outcomes (2008) J. Neuroimmunol., 204, pp. 149-153 
504 |a (2000) Diagnostic and Statistical Manual of Mental Disorders, Text Revision, , American Psychiatric Association, American Psychiatric Association, Washington, DC 
504 |a Battista, D., Ferrari, C.C., Gage, F.H., Pitossi, F.J., Neurogenic niche modulation by activated microglia: transforming growth factor beta increases neurogenesis in the adult dentate gyrus (2006) Eur. J. Neurosci., 23, pp. 83-93 
504 |a Benes, F.M., Lim, B., Matzilevich, D., Walsh, J.P., Subburaju, S., Minns, M., Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars (2007) Proc. Natl. Acad. Sci. USA, 104, pp. 10164-10169 
504 |a Blond, D., Campbell, S.J., Butchart, A.G., Perry, V.H., Anthony, D.C., Differential induction of interleukin-1beta and tumour necrosis factor-alpha may account for specific patterns of leukocyte recruitment in the brain (2002) Brain Res., 958, pp. 89-99 
504 |a Boisse, L., Mouihate, A., Ellis, S., Pittman, Q.J., Long-term alterations in neuroimmune responses after neonatal exposure to lipopolysaccharide (2004) J. Neurosci., 24, pp. 4928-4934 
504 |a Bottner, M., Krieglstein, K., Unsicker, K., The transforming growth factor-betas: structure, signaling, and roles in nervous system development and functions (2000) J. Neurochem., 75, pp. 2227-2240 
504 |a Brodkin, E.S., Hagemann, A., Nemetski, S.M., Silver, L.M., Social approach-avoidance behavior of inbred mouse strains towards DBA/2 mice (2004) Brain Res., 1002, pp. 151-157 
504 |a Casanova, M., Trippe, J., Radial cytoarchitecture and patterns of cortical connectivity in autism (2009) Philos. Trans. R. Soc. B: Biol. Sci., 364, pp. 1433-1436 
504 |a Crawley, J.N., Mouse behavioral assays relevant to the symptoms of autism (2007) Brain Pathol. (Zurich, Switzerland), 17, pp. 448-459 
504 |a Cunningham, C., Boche, D., Perry, V.H., Transforming growth factor beta1, the dominant cytokine in murine prion disease: influence on inflammatory cytokine synthesis and alteration of vascular extracellular matrix (2002) Neuropathol. Appl. Neurobiol., 28, pp. 107-119 
504 |a Depino, A., Ferrari, C., Pott Godoy, M.C., Tarelli, R., Pitossi, F.J., Differential effects of interleukin-1beta on neurotoxicity, cytokine induction and glial reaction in specific brain regions (2005) J. Neuroimmunol., 168, pp. 96-110 
504 |a Depino, A.M., Tsetsenis, T., Gross, C., GABA homeostasis contributes to the developmental programming of anxiety-related behavior (2008) Brain Res., 1210, pp. 189-199 
504 |a Deverman, B.E., Patterson, P.H., Cytokines and CNS development (2009) Neuron, 64, pp. 61-78 
504 |a Dow, A.L., Russell, D.S., Duman, R.S., Regulation of activin mRNA and Smad2 phosphorylation by antidepressant treatment in the rat brain: effects in behavioral models (2005) J. Neurosci., 25, pp. 4908-4916 
504 |a Fatemi, S.H., Snow, A.V., Stary, J.M., Araghi-Niknam, M., Reutiman, T.J., Lee, S., Brooks, A.I., Pearce, D.A., Reelin signaling is impaired in autism (2005) Biol. Psychiatry, 57, pp. 777-787 
504 |a Ferrari, C.C., Depino, A.M., Prada, F., Muraro, N., Campbell, S., Podhajcer, O., Perry, V.H., Pitossi, F.J., Reversible demyelination, blood-brain barrier breakdown, and pronounced neutrophil recruitment induced by chronic IL-1 expression in the brain (2004) Am. J. Pathol., 165, pp. 1827-1837 
504 |a Forster, E., Tielsch, A., Saum, B., Weiss, K.H., Johanssen, C., Graus-Porta, D., Muller, U., Frotscher, M., Reelin, Disabled 1, and beta 1 integrins are required for the formation of the radial glial scaffold in the hippocampus (2002) Proc. Natl. Acad. Sci. USA, 99, pp. 13178-13183 
504 |a Garbett, K., Ebert, P.J., Mitchell, A., Lintas, C., Manzi, B., Mirnics, K., Persico, A.M., Immune transcriptome alterations in the temporal cortex of subjects with autism (2008) Neurobiol. Dis., 30, pp. 303-311 
504 |a Gomes, F.C., Sousa Vde, O., Romao, L., Emerging roles for TGF-beta1 in nervous system development (2005) Int. J. Dev. Neurosci., 23, pp. 413-424 
504 |a Graciarena, M., Depino, A.M., Pitossi, F.J., Prenatal inflammation impairs adult neurogenesis and memory related behavior through persistent hippocampal TGFbeta(1) downregulation (2010) Brain Behav. Immun., 24, pp. 1301-1309 
504 |a Greco, C.M., Navarro, C.S., Hunsaker, M.R., Maezawa, I., Shuler, J.F., Tassone, F., Delany, M., Hagerman, R.J., Neuropathologic features in the hippocampus and cerebellum of three older men with fragile X syndrome (2011) Mol. Autism, 2, p. 2 
504 |a Gross, C., Zhuang, X., Stark, K., Ramboz, S., Oosting, R., Kirby, L., Santarelli, L., Hen, R., Serotonin1A receptor acts during development to establish normal anxiety-like behaviour in the adult (2002) Nature, 416, pp. 396-400 
504 |a Hofvander, B., Delorme, R., Chaste, P., Nyden, A., Wentz, E., Stahlberg, O., Herbrecht, E., Leboyer, M., Psychiatric and psychosocial problems in adults with normal-intelligence autism spectrum disorders (2009) BMC Psychiatry, 9, p. 35 
504 |a Ichtchenko, K., Nguyen, T., Sudhof, T.C., Structures, alternative splicing, and neurexin binding of multiple neuroligins (1996) J. Biol. Chem., 271, pp. 2676-2682 
504 |a Khazipov, R., Luhmann, H.J., Early patterns of electrical activity in the developing cerebral cortex of humans and rodents (2006) Trends Neurosci., 29, pp. 414-418 
504 |a Kolozsi, E., Mackenzie, R.N., Roullet, F.I., deCatanzaro, D., Foster, J.A., Prenatal exposure to valproic acid leads to reduced expression of synaptic adhesion molecule neuroligin 3 in mice (2009) Neuroscience, 163, pp. 1201-1210 
504 |a Kulkarni, A.B., Huh, C.G., Becker, D., Geiser, A., Lyght, M., Flanders, K.C., Roberts, A.B., Karlsson, S., Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death (1993) Proc. Natl. Acad. Sci. USA, 90, pp. 770-774 
504 |a Laumonnier, F., Bonnet-Brilhault, F., Gomot, M., Blanc, R., David, A., Moizard, M.P., Raynaud, M., Briault, S., X-linked mental retardation and autism are associated with a mutation in the NLGN4 gene, a member of the neuroligin family (2004) Am. J. Hum. Genet., 74, pp. 552-557 
504 |a Lawrence, Y.A., Kemper, T.L., Bauman, M.L., Blatt, G.J., Parvalbumin-, calbindin-, and calretinin-immunoreactive hippocampal interneuron density in autism (2010) Acta Neurol. Scand., 121, pp. 99-108 
504 |a Lintas, C., Sacco, R., Persico, A.M., (2011), Genome-wide expression studies in Autism spectrum disorder, Rett syndrome, and Down syndrome. Neurobiol. Dis; Lucchina, L., Carola, V., Pitossi, F., Depino, A.M., Evaluating the interaction between early postnatal inflammation and maternal care in the programming of adult anxiety and depression-related behaviors (2010) Behav. Brain Res., 213, pp. 56-65 
504 |a Magdaleno, S., Jensen, P., Brumwell, C.L., Seal, A., Lehman, K., Asbury, A., Cheung, T., Curran, T., BGEM: an in situ hybridization database of gene expression in the embryonic and adult mouse nervous system (2006) PLoS Biol., 4, pp. e86 
504 |a McFarlane, H.G., Kusek, G.K., Yang, M., Phoenix, J.L., Bolivar, V.J., Crawley, J.N., Autism-like behavioral phenotypes in BTBR T+tf/J mice (2008) Genes Brain Behav., 7, pp. 152-163 
504 |a Meyer, U., Nyffeler, M., Engler, A., Urwyler, A., Schedlowski, M., Knuesel, I., Yee, B.K., Feldon, J., The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology (2006) J. Neurosci., 26, pp. 4752-4762 
504 |a Okada, K., Hashimoto, K., Iwata, Y., Nakamura, K., Tsujii, M., Tsuchiya, K.J., Sekine, Y., Mori, N., Decreased serum levels of transforming growth factor-beta1 in patients with autism (2007) Prog. Neuropsychopharmacol. Biol. Psychiatry, 31, pp. 187-190 
504 |a Patterson, P.H., (2011), Maternal infection and immune involvement in autism. Trends Mol. Med; Paxinos, G., Watson, C., (1986) The Rat Brain in Stereotaxic Coordinates, , Academic Press, Orlando, FL 
504 |a Persico, A.M., D'Agruma, L., Maiorano, N., Totaro, A., Militerni, R., Bravaccio, C., Wassink, T.H., Keller, F., Reelin gene alleles and haplotypes as a factor predisposing to autistic disorder (2001) Mol. Psychiatry, 6, pp. 150-159 
504 |a Pierce, K., Courchesne, E., Evidence for a cerebellar role in reduced exploration and stereotyped behavior in autism (2001) Biol. Psychiatry, 49, pp. 655-664 
504 |a Radyushkin, K., Hammerschmidt, K., Boretius, S., Varoqueaux, F., El-Kordi, A., Ronnenberg, A., Winter, D., Ehrenreich, H., (2009), Neuroligin-3-deficient mice: model of a monogenic heritable form of autism with an olfactory deficit. Genes Brain Behav; Rasband, W.S., 1997-2009. ImageJ. In: Health, N.I.O. (Ed.), Bethesda; Saitoh, O., Karns, C.M., Courchesne, E., Development of the hippocampal formation from 2 to 42 years: MRI evidence of smaller area dentata in autism (2001) Brain, 124, pp. 1317-1324 
504 |a Schneider, T., Roman, A., Basta-Kaim, A., Kubera, M., Budziszewska, B., Schneider, K., Przewlocki, R., Gender-specific behavioral and immunological alterations in an animal model of autism induced by prenatal exposure to valproic acid (2008) PNEC, 33, pp. 728-740 
504 |a Smith, S.E., Li, J., Garbett, K., Mirnics, K., Patterson, P.H., Maternal immune activation alters fetal brain development through interleukin-6 (2007) J. Neurosci., 27, pp. 10695-10702 
504 |a Sun, M., Gewirtz, J.C., Bofenkamp, L., Wickham, R.J., Ge, H., O'Connor, M.B., Canonical TGF-beta signaling is required for the balance of excitatory/inhibitory transmission within the hippocampus and prepulse inhibition of acoustic startle (2010) J. Neurosci., 30, pp. 6025-6035 
504 |a Vargas, D.L., Nascimbene, C., Krishnan, C., Zimmerman, A.W., Pardo, C.A., Neuroglial activation and neuroinflammation in the brain of patients with autism (2005) Ann. Neurol., 57, pp. 67-81 
504 |a Weeber, E.J., Beffert, U., Jones, C., Christian, J.M., Forster, E., Sweatt, J.D., Herz, J., Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning (2002) J. Biol. Chem., 277, pp. 39944-39952 
504 |a Wegiel, J., Kuchna, I., Nowicki, K., Imaki, H., Marchi, E., Ma, S.Y., Chauhan, A., Wisniewski, T., The neuropathology of autism: defects of neurogenesis and neuronal migration, and dysplastic changes (2010) Acta Neuropathol., 119, pp. 755-770 
504 |a Weiss, J.M., Cuff, C.A., Berman, J.W., TGF-beta downmodulates cytokine-induced monocyte chemoattractant protein (MCP)-1 expression in human endothelial cells. A putative role for TGF-beta in the modulation of TNF receptor expression (1999) Endothelium, 6, pp. 291-302 
504 |a Wyss-Coray, T., Borrow, P., Brooker, M.J., Mucke, L., Astroglial overproduction of TGF-beta 1 enhances inflammatory central nervous system disease in transgenic mice (1997) J. Neuroimmunol., 77, pp. 45-50 
504 |a Zhang, H., Liu, X., Zhang, C., Mundo, E., Macciardi, F., Grayson, D.R., Guidotti, A.R., Holden, J.J., Reelin gene alleles and susceptibility to autism spectrum disorders (2002) Mol. Psychiatry, 7, pp. 1012-1017 
504 |a Zheng, F., Adelsberger, H., Muller, M.R., Fritschy, J.M., Werner, S., Alzheimer, C., Activin tunes GABAergic neurotransmission and modulates anxiety-like behavior (2009) Mol. Psychiatry, 14, pp. 332-346 
520 3 |a TGF-β1 is an anti-inflammatory cytokine that is augmented in the brain of autistic patients and that can affect brain development. In this work, we studied the effects of overexpressing TGF-β1 in the dentate gyrus of adult or young mice on behavior. TGF-β1 overexpression during postnatal development led to a long-term decrease in social interaction and to long-term increases in self-grooming and depression-related behaviors. Our analysis shows that these behavioral changes correlate with the long-term downregulation of TGF-β1 and IL-6 expression in the dentate gyrus, as well as to decreases in the mRNA levels of the synaptic protein neuroligin 3 and in the number of Reelin-positive neurons in the dentate gyrus. In contrast, chronic expression of TGF-β1 during adulthood led to transient opposite effects on these behaviors. These results show a central role of hippocampal TGF-β1 in the programming and modulation of social interaction, repetitive behavior and depression-related behavior. Finally, our data suggest a role of hippocampal TGF-β1 and early-life neuroinflammation in the development of the behavioral alterations observed in autism spectrum disorders. © 2011 Elsevier Inc.  |l eng 
536 |a Detalles de la financiación: Universidad de Buenos Aires, UBACyT GEF2010-2012 
536 |a Detalles de la financiación: Fundación Florencio Fiorini, 2009 
536 |a Detalles de la financiación: National Council for Scientific Research 
536 |a Detalles de la financiación: Consejo Nacional de Investigaciones Científicas y Técnicas, PIP2010-2012 
536 |a Detalles de la financiación: This work was supported by a CONICET Grant PIP2010-2012 , a University of Buenos Aires Grant UBACyT GEF2010-2012 and a Florencio Fiorini Foundation Grant 2009 . A.M.D. and F.P. are members of the Research Career of the National Council of Scientific and Technological Research (CONICET), Argentina. L.L. is fellow of the CONICET. We would like to thank Maria Isabel Farias for tissue processing for histology, and Dr. Juan Belforte and Dr. Lucia Chemes for critical reading of the manuscript. Appendix A 
593 |a Institute for Physiology, Molecular Biology and Neurosciences, CONICET-UBA, C1428EHA Buenos Aires, Argentina 
593 |a Department of Physiology, Molecular and Cellular Biology, FCEyN, University of Buenos Aires, C1428EHA Buenos Aires, Argentina 
593 |a Leloir Institute Foundation, Institute for Biochemical Investigations, CONICET, 1405 Buenos Aires, Argentina 
690 1 0 |a AUTISM 
690 1 0 |a BEHAVIOR 
690 1 0 |a MICE 
690 1 0 |a NEUROINFLAMMATION 
690 1 0 |a POSTNATAL PROGRAMMING 
690 1 0 |a TRANSFORMING GROWTH FACTOR-BETA 1 
690 1 0 |a INTERLEUKIN 6 
690 1 0 |a NEUROLIGIN 
690 1 0 |a REELIN 
690 1 0 |a TRANSFORMING GROWTH FACTOR BETA1 
690 1 0 |a ANIMAL EXPERIMENT 
690 1 0 |a ARTICLE 
690 1 0 |a BEHAVIOR 
690 1 0 |a COMPULSION 
690 1 0 |a CONTROLLED STUDY 
690 1 0 |a DENTATE GYRUS 
690 1 0 |a DEPRESSION 
690 1 0 |a GENE OVEREXPRESSION 
690 1 0 |a GROOMING 
690 1 0 |a HIPPOCAMPUS 
690 1 0 |a MALE 
690 1 0 |a MOUSE 
690 1 0 |a NERVE CELL 
690 1 0 |a NONHUMAN 
690 1 0 |a PRIORITY JOURNAL 
690 1 0 |a PROTEIN EXPRESSION 
690 1 0 |a SOCIAL INTERACTION 
690 1 0 |a ADENOVIRIDAE 
690 1 0 |a ANIMALS 
690 1 0 |a BEHAVIOR, ANIMAL 
690 1 0 |a DEPRESSION 
690 1 0 |a FEMALE 
690 1 0 |a GLIOSIS 
690 1 0 |a GROOMING 
690 1 0 |a HINDLIMB SUSPENSION 
690 1 0 |a HIPPOCAMPUS 
690 1 0 |a IMMUNOHISTOCHEMISTRY 
690 1 0 |a INTERPERSONAL RELATIONS 
690 1 0 |a MALE 
690 1 0 |a MICE 
690 1 0 |a MICE, INBRED C57BL 
690 1 0 |a MICE, TRANSGENIC 
690 1 0 |a PREGNANCY 
690 1 0 |a REAL-TIME POLYMERASE CHAIN REACTION 
690 1 0 |a RNA, MESSENGER 
690 1 0 |a STEREOTAXIC TECHNIQUES 
690 1 0 |a SWIMMING 
690 1 0 |a TRANSFORMING GROWTH FACTOR BETA1 
700 1 |a Lucchina, L. 
700 1 |a Pitossi, F. 
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