دورية أكاديمية

Ethanol exposure during the brain growth spurt affects social behavior and increases susceptibility to acute ethanol effects during adolescence in male mice.

التفاصيل البيبلوغرافية
العنوان: Ethanol exposure during the brain growth spurt affects social behavior and increases susceptibility to acute ethanol effects during adolescence in male mice.
المؤلفون: Demarque KC; Laboratório de Biologia Celular, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil., Dutra-Tavares AC; Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil., Nunes-Freitas AL; Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil., Araújo UC; Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil., Manhães AC; Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil., Abreu-Villaça Y; Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil., Filgueiras CC; Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil., Ribeiro-Carvalho A; Departamento de Ciências, Faculdade de Formação de Professores da Universidade do Estado do Rio de Janeiro, São Gonçalo, Brazil.
المصدر: International journal of developmental neuroscience : the official journal of the International Society for Developmental Neuroscience [Int J Dev Neurosci] 2020 May; Vol. 80 (3), pp. 197-207. Date of Electronic Publication: 2020 Mar 18.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: John Wiley & Sons, Inc Country of Publication: United States NLM ID: 8401784 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1873-474X (Electronic) Linking ISSN: 07365748 NLM ISO Abbreviation: Int J Dev Neurosci Subsets: MEDLINE
أسماء مطبوعة: Publication: 2020- : Hoboken, NJ : John Wiley & Sons, Inc.
Original Publication: Oxford : New York : Pergamon Press, c1983-
مواضيع طبية MeSH: Social Behavior*, Behavior, Animal/*drug effects , Cerebral Cortex/*drug effects , Ethanol/*pharmacology, Animals ; Cerebral Cortex/metabolism ; Corticosterone/blood ; Hydroxyindoleacetic Acid/metabolism ; Male ; Mice ; Motor Activity/drug effects ; Receptor, Serotonin, 5-HT2A/metabolism
مستخلص: The brain is particularly vulnerable to ethanol effects during its growth spurt. Outcomes of early ethanol exposure such as hyperactivity have been extensively investigated; however, persons with fetal alcohol spectrum disorder frequently have social impairments and are heavy drinkers. Despite that, scant information is available regarding the neurobiological basis of these latter behavioral issues. Here, Swiss mice exposed to ethanol (Etoh, 5 g/kg i.p., alternate days) or saline during the brain growth spurt [postnatal day (PN) 2 to 8] were used to assess social behavior after an ethanol challenging during adolescence. At PN39, animals were administered with a single ethanol dose (1 g/Kg) or water by gavage and were then evaluated in the three-chamber sociability test. We also evaluated corticosterone serum levels and the frontal cerebral cortex serotoninergic system. Etoh males showed reductions in sociability. Ethanol challenging reverted these alterations in social behavior, reduced corticosterone levels, and increased the 5-HT 2 receptor binding of male Etoh mice. No alterations were observed in 5-HT and 5-HIAA contents. These data support the idea that ethanol exposure during the brain growth spurt impacts social abilities during adolescence, alters ethanol reexposure effects, and suggests that stress response and serotoninergic system play roles in this phenomenon.
(© 2020 International Society for Developmental Neuroscience.)
References: Abreu-Villaça, Y., Carvalho-Graça, A. C., Skinner, G., Lotufo, B. M., Duarte-Pinheiro, V. H. S., Ribeiro-Carvalho, A., … Filgueiras, C. C. (2018). Hyperactivity and memory/learning deficits evoked by developmental exposure to nicotine and/or ethanol are mitigated by cAMP and cGMP signaling cascades activation. Neurotoxicology, 66, 150-159. https://doi.org/10.1016/j.neuro.2018.04.003.
Akiyoshi, J., Hough, C., & Chuang, D. M. (1993). Paradoxical increase of 5-hydroxytryptamine2 receptors and 5-hydroxytryptamine2 receptor mRNA in cerebellar granule cells after persistent 5-hydroxytryptamine2 receptor stimulation. Molecular Pharmacology, 43, 349-355.
Alati, R., Clavarino, A., Najman, J. M., O’Callaghan, M., Bor, W., Mamun, A. A., & Williams, G. M. (2008). The developmental origin of adolescent alcohol use: Findings from the Mater University Study of Pregnancy and its outcomes. Drug and Alcohol Dependence, 98, 136-143. https://doi.org/10.1016/j.drugalcdep.2008.05.011.
Azmitia, E. C., Singh, J. S., & Whitaker-Azmitia, P. M. (2011). Increased serotonin axons (immunoreactive to 5-HT transporter) in postmortem brains from young autism donors. Neuropharmacology, 60, 1347-1354. https://doi.org/10.1016/j.neuropharm.2011.02.002.
Baculis, B. C., Diaz, M. R., & Fernando Valenzuela, C. (2015). Third trimester-equivalent ethanol exposure increases anxiety-like behavior and glutamatergic transmission in the basolateral amygdala. Pharmacology, Biochemistry and Behavior, 137, 78-85. https://doi.org/10.1016/j.pbb.2015.08.009.
Bandeira, F., Lent, R., & Herculano-Houzel, S. (2009). Changing numbers of neuronal and non-neuronal cells underlie postnatal brain growth in the rat. Proceedings of the National Academy of Sciences, 106, 14108-14113. https://doi.org/10.1073/pnas.0804650106.
Barth, C. R., Luft, C., Funchal, G. A., de Oliveira, J. R., Porto, B. N., & Donadio, M. V. F. (2016). LPS-induced neonatal stress in mice affects the response profile to an inflammatory stimulus in an age and sex-dependent manner. Developmental Psychobiology, 58, 600-613. https://doi.org/10.1002/dev.21404.
Bolognese, A. C., Yang, W. L., Hansen, L. W., Sharma, A., Nicastro, J. M., Coppa, G. F., & Wang, P. (2018). Activation of invariant natural killer T cells redirects the inflammatory response in neonatal sepsis. Frontiers in Immunology, 9, 833. https://doi.org/10.3389/fimmu.2018.00833.
Brand, I., Fliegel, S., Spanagel, R., & Noori, H. R. (2013). Global ethanol-induced enhancements of monoaminergic neurotransmission: A meta-analysis study. Alcoholism, Clinical and Experimental Research, 37, 2048-2057. https://doi.org/10.1111/acer.12207.
Buckner, J. D., & Turner, R. J. (2009). Social anxiety disorder as a risk factor for alcohol use disorders: A prospective examination of parental and peer influences. Drug and Alcohol Dependence, 100, 128-137. https://doi.org/10.1016/j.drugalcdep.2008.09.018.
Caruso, M. J., Seemiller, L. R., Fetherston, T. B., Miller, C. N., Reiss, D. E., Cavigelli, S. A., & Kamens, H. M. (2018). Adolescent social stress increases anxiety-like behavior and ethanol consumption in adult male and female C57BL/6J mice. Scientific Reports, 8, 10040. https://doi.org/10.1038/s41598-018-28381-2.
CDC. (2009). Alcohol use among pregnant and nonpregnant women of childbearing age: United States, 1991-2005. Morbidity and Mortality Weekly Report, 58, 529-532.
Chow, P. I., Portnow, S., Zhang, D., Salemink, E., Wiers, R. W., & Teachman, B. A. (2018). Comorbid interpretation and expectancy bias in social anxiety and alcohol use. Anxiety, Stress, & Coping, 31, 669-685. https://doi.org/10.1080/10615806.2018.1521958.
Denny, C. H., Acero, C. S., Naimi, T. S., & Kim, S. Y. (2019). Consumption of alcohol beverages and binge drinking among pregnant women aged 18-44 years-United States, 2015-2017. Morbidity and Mortality Weekly Report, 68, 365-368. https://doi.org/10.15585/mmwr.mm6816a1.
Diaz, M. R., Mooney, S. M., & Varlinskaya, E. I. (2016). Acute prenatal exposure to ethanol on gestational day 12 elicits opposing deficits in social behaviors and anxiety-like behaviors in Sprague Dawley rats. Behavioral Brain Research, 310, 11-19. https://doi.org/10.1016/j.bbr.2016.05.003.
Diestelkamp, S., Kriston, L., Arnaud, N., Wartberg, L., Sack, P. M., Härter, M., & Thomasius, R. (2015). Drinking patterns of alcohol intoxicated adolescents in the emergency department: A latent class analysis. Addictive Behaviors, 50, 51-59. https://doi.org/10.1016/j.addbeh.2015.06.009.
Ethen, M. K., Ramadhani, T. A., Scheuerle, A. E., Canfield, M. A., Wyszynski, D. F., Druschel, C. M., & Romitti, P. A. (2009). Alcohol consumption by women before and during pregnancy. Maternal and Child Health Journal, 13, 274-285. https://doi.org/10.1007/s10995-008-0328-2.
Favoretto, C. A., Macedo, G. C., & Quadros, I. M. H. (2017). Effects of ethanol on social avoidance induced by chronic social defeat stress in mice. Stress, 20, 68-74. https://doi.org/10.1080/10253890.2017.1280667.
Filgueiras, C. C., Krahe, T. E., & Medina, A. E. (2010). Phosphodiesterase type 1 inhibition improves learning in rats exposed to alcohol during the third trimester equivalent of human gestation. Neuroscience Letters, 473, 202-207. https://doi.org/10.1016/j.neulet.2010.02.046.
Filgueiras, C. C., Ribeiro-Carvalho, A., Nunes, F., Abreu-Villaça, Y., & Manhães, A. C. (2009). Early ethanol exposure in mice increases laterality of rotational side preference in the free-swimming test. Pharmacology, Biochemistry and Behavior, 93, 148-154. https://doi.org/10.1016/j.pbb.2009.04.023.
Fish, E. W., Holloway, H. T., Rumple, A., Baker, L. K., Wieczorek, L. A., Moy, S., … Parnell, S. E. (2016). Acute alcohol exposure during neurulation: Behavioral and brain structural consequences in adolescent C57BL/6J mice. Behavioral Brain Research, 311, 70-80. https://doi.org/10.1016/j.bbr.2016.05.004.
Gilles, D. M., Turk, C. L., & Fresco, D. M. (2006). Social anxiety, alcohol expectancies, and self-efficacy as predictors of heavy drinking in college students. Addictive Behaviors, 31, 388-398. https://doi.org/10.1016/j.addbeh.2005.05.020.
Gil-Mohapel, J., Boehme, F., Kainer, L., & Christie, B. R. (2010). Hippocampal cell loss and neurogenesis after fetal alcohol exposure: Insights from different rodent models. Brain Research Reviews, 64, 283-303. https://doi.org/10.1016/j.brainresrev.2010.04.011.
Haley, D. W., Handmaker, N. S., & Lowe, J. (2006). Infant stress reactivity and prenatal alcohol exposure. Alcoholism, Clinical and Experimental Research, 30, 2055-2064. https://doi.org/10.1111/j.1530-0277.2006.00251.x.
Hamilton, D. A., Akers, K. G., Rice, J. P., Johnson, T. E., Candelaria-Cook, F. T., Maes, L. I., … Savage, D. D. (2010). Prenatal exposure to moderate levels of ethanol alters social behavior in adult rats: Relationship to structural plasticity and immediate early gene expression in frontal cortex. Behavioral Brain Research, 207, 290-304. https://doi.org/10.1016/j.bbr.2009.10.012.
Hamilton, D. A., Barto, D., Rodriguez, C. I., Magcalas, C. M., Fink, B. C., Rice, J. P., … Savage, D. D. (2014). Effects of moderate prenatal ethanol exposure and age on social behavior, spatial response perseveration errors and motor behavior. Behavioral Brain Research, 269, 44-54. https://doi.org/10.1016/j.bbr.2014.04.029.
Hellemans, K. G. C., Sliwowska, J. H., Verma, P., & Weinberg, J. (2010). Prenatal alcohol exposure: Fetal programming and later life vulnerability to stress, depression and anxiety disorders. Neuroscience and Biobehavioral Reviews, 34, 791-807. https://doi.org/10.1016/j.neubiorev.2009.06.004.
Hellemans, K. G. C., Verma, P., Yoon, E., Yu, W. K., Young, A. H., & Weinberg, J. (2010). Prenatal alcohol exposure and chronic mild stress differentially alter depressive- and anxiety-like behaviors in male and female offspring. Alcoholism, Clinical and Experimental Research, 34, 633-645. https://doi.org/10.1111/j.1530-0277.2009.01132.x.
Hofmann, C. E., Ellis, L., Yu, W. K., & Weinberg, J. (2007). Hypothalamic? Pituitary? Adrenal responses to 5-HT 1A and 5-HT 2A/C agonists are differentially altered in female and male rats prenatally exposed to ethanol. Alcoholism, Clinical and Experimental Research, 31, 345-355. https://doi.org/10.1111/j.1530-0277.2006.00316.x.
Kim, J.-W., Seung, H., Kwon, K. J., Ko, M. J., Lee, E. J., Oh, H. A., … Bahn, G. H. (2014). Subchronic treatment of Donepezil rescues impaired social, hyperactive, and stereotypic behavior in valproic acid-induced animal model of autism. PLoS ONE, 9, e104927. https://doi.org/10.1371/journal.pone.0104927.
Krahe, T. E., Filgueiras, C. C., & Medina, A. E. (2016). Effects of developmental alcohol and valproic acid exposure on play behavior of ferrets. International Journal of Developmental Neuroscience, 52, 75-81. https://doi.org/10.1016/j.ijdevneu.2016.03.007.
Li, Y., Ke, J., Peng, C., Wu, F., & Song, Y. (2018). microRNA-300/NAMPT regulates inflammatory responses through activation of AMPK/mTOR signaling pathway in neonatal sepsis. Biomedicine & Pharmacotherapy, 108, 271-279. https://doi.org/10.1016/j.biopha.2018.08.064.
Lima, C. S., Nunes-Freitas, A. L., Ribeiro-Carvalho, A., Filgueiras, C. C., Manhães, A. C., Meyer, A., & Abreu-Villaça, Y. (2011). Exposure to methamidophos at adulthood adversely affects serotonergic biomarkers in the mouse brain. Neurotoxicology, 32, 718-724. https://doi.org/10.1016/j.neuro.2011.08.002.
Lima, S. C., Dutra-Tavares, A. C., Nunes, F., Nunes-Freitas, A. L., Ribeiro-Carvalho, A., Filgueiras, C. C., … Abreu-Villaça, Y. (2013). Methamidophos exposure during the early postnatal period of mice: Immediate and late-emergent effects on the cholinergic and serotonergic systems and behavior. Toxicological Sciences, 134, 125-139. https://doi.org/10.1093/toxsci/kft095.
López-Cruz, L., San-Miguel, N., Bayarri, P., Baqi, Y., Müller, C. E., Salamone, J. D., & Correa, M. (2016). Ethanol and caffeine effects on social interaction and recognition in mice: Involvement of adenosine A2A and A1 receptors. Frontiers in Behavioural Neurosciences, 10, 1-15. https://doi.org/10.3389/fnbeh.2016.00206.
Lugo, J., Marino, M., Cronise, K., & Kelly, S. (2003). Effects of alcohol exposure during development on social behavior in rats. Physiology & Behavior, 78, 185-194. https://doi.org/10.1016/S0031-9384(02)00971-X.
Makkonen, I., Riikonen, R., Kokki, H., Airaksinen, M. M., & Kuikka, J. T. (2008). Serotonin and dopamine transporter binding in children with autism determined by SPECT. Developmental Medicine and Child Neurology, 50, 593-597. https://doi.org/10.1111/j.1469-8749.2008.03027.x.
Malone, S. M., Mcgue, M., & Iacono, W. G. (2010). Mothers' maximum drinks ever consumed in 24 hours predicts mental health problems in adolescent offspring. J Child Psychol Psychiatry, 51, 1067-1075. https://doi.org/10.1111/j.1469-7610.2010.02219.x.
Mantha, K., Kleiber, M., & Singh, S. (2013). Neurodevelopmental timing of ethanol exposure may contribute to observed heterogeneity of behavioral deficits in a mouse model of fetal alcohol spectrum disorder (FASD). Journal of Behavioral and Brain Science, 3, 85-99.
Marquardt, K., & Brigman, J. L. (2016). The impact of prenatal alcohol exposure on social, cognitive and affective behavioral domains: Insights from rodent models. Alcohol, 118, 6072-6078. https://10.1016/j.alcohol.2015.12.002.
Momino, W., Félix, T. M., Abeche, A. M., Zandoná, D. I., Scheibler, G. G., Chambers, C., … Schüler-Faccini, L. (2012). Maternal drinking behavior and fetal alcohol spectrum disorders in adolescents with criminal behavior in southern Brazil. Genetics and Molecular Biology, 35, 960-965. https://doi.org/10.1590/S1415-47572012000600011.
Mooney, S. M., & Varlinskaya, E. I. (2011). Acute prenatal exposure to ethanol and social behavior: Effects of age, sex, and timing of exposure. Behavioral Brain Research, 216, 358-364. https://doi.org/10.1016/j.bbr.2010.08.014.
Morrow, A. L., Porcu, P., Boyd, K. N., & Grant, K. A. (2006). Hypothalamic-pituitary-adrenal axis modulation of GABAergic neuroactive steroids influences ethanol sensitivity and drinking behavior. Dialogues in Clinical Neuroscience, 8, 463-477.
Murphy, D. G. M., Daly, E., Schmitz, N., Toal, F., Murphy, K., Curran, S., … Travis, M. (2006). Cortical serotonin 5-HT 2A receptor binding and social communication in adults with Asperger's syndrome: An in vivo SPECT study. American Journal of Psychiatry, 163, 934-936. https://doi.org/10.1176/ajp.2006.163.5.934.
Nakamura, K., Sekine, Y., Ouchi, Y., Tsujii, M., Yoshikawa, E., Futatsubashi, M., … Mori, N. (2010). Brain serotonin and dopamine transporter bindings in adults with high-functioning autism. Archives of General Psychiatry, 67, 59. https://doi.org/10.1001/archgenpsychiatry.2009.137.
Niccols, A. (2007). Fetal alcohol syndrome and the developing socio-emotional brain. Brain and Cognition, 65, 135-142. https://doi.org/10.1016/j.bandc.2007.02.009.
Nunes, F., Ferreira-Rosa, K., Pereira, M. D. S., Kubrusly, R. C., Manhães, A. C., Abreu-Villaça, Y., & Filgueiras, C. C. (2011). Acute administration of vinpocetine, a phosphodiesterase type 1 inhibitor, ameliorates hyperactivity in a mice model of fetal alcohol spectrum disorder. Drug and Alcohol Dependence, 119, 81-87. https://doi.org/10.1016/j.drugalcdep.2011.05.024.
Olney, J. W., Tenkova, T., Dikranian, K., Qin, Y.-Q., Labruyere, J., & Ikonomidou, C. (2002). Ethanol-induced apoptotic neurodegeneration in the developing C57BL/6 mouse brain. Developmental Brain Research, 133, 115-126. https://doi.org/10.1016/S0165-3806(02)00279-1.
Pascual, M., Montesinos, J., Marcos, M., Torres, J.-L., Costa-Alba, P., García-García, F., … Guerri, C. (2017). Gender differences in the inflammatory cytokine and chemokine profiles induced by binge ethanol drinking in adolescence. Addiction Biology, 22, 1829-1841. https://doi.org/10.1111/adb.12461.
Rasmussen, C., Becker, M., Mclennan, J., Urichuk, L., & Andrew, G. (2011). An evaluation of social skills in children with and without prenatal alcohol exposure. Child: Care, Health and Development, 37, 711-718. https://doi.org/10.1111/j.1365-2214.2010.01152.x.
Roebuck, T. M., Mattson, S. N., & Riley, E. P. (1999). Behavioral and psychosocial profiles of alcohol-exposed children. Alcoholism: Clinical and Experimental Research, 23, 1070-1076.
Sari, Y., & Zhou, F. C. (2004). Prenatal alcohol exposure causes long-term serotonin neuron deficit in mice. Alcoholism, Clinical and Experimental Research, 28, 941-948. https://doi.org/10.1097/01.ALC.0000128228.08472.39.
Smith, J. P., & Randall, C. L. (2012). Anxiety and alcohol use disorders: Comorbidity and treatment considerations. Alcohol Research, 34, 414-431.
Spear, L. P. 2000. The adolescent brain and age-related behavioral manifestations. Neuroscience & Biobehavioral Reviews, 24(4), 417-463.
Tatiana, B., Barbara, B., Chaffin, M., Bard, D., Isurina, G., Tsvetkova, L., & Volkova, E. (2013). Women's alcohol consumption and risk for alcohol-exposed pregnancies in russia. Addiction, 107, 109-117. https://doi.org/10.1111/j.1360-0443.2011.03569.x.Women.
Yoshitake, T., Kehr, J., Yoshitake, S., Fujino, K., Nohta, H., & Yamaguchi, M. (2004). Determination of serotonin, noradrenaline, dopamine and their metabolites in rat brain extracts and microdialysis samples by column liquid chromatography with fluorescence detection following derivatization with benzylamine and 1,2-diphenylethylenediamine. Journal of Chromatography B, 807, 177-183. https://doi.org/10.1016/j.jchromb.2004.03.069.
معلومات مُعتمدة: Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq); Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ)
فهرسة مساهمة: Keywords: corticosterone; development; serotoninergic system; social behavior
المشرفين على المادة: 0 (Receptor, Serotonin, 5-HT2A)
3K9958V90M (Ethanol)
54-16-0 (Hydroxyindoleacetic Acid)
W980KJ009P (Corticosterone)
تواريخ الأحداث: Date Created: 20200221 Date Completed: 20210303 Latest Revision: 20210303
رمز التحديث: 20231215
DOI: 10.1002/jdn.10017
PMID: 32077124
قاعدة البيانات: MEDLINE
الوصف
تدمد:1873-474X
DOI:10.1002/jdn.10017