Abstract
This study is to determine the role and mechanism of hippocampal acetylation in prenatal stress (PS) induced depression-like behavior of male offspring rats. PS-induced depression rat model was established. Sucrose preference and forced swim test were used to observe the behavior changes of male offspring rats. Hippocampal acetylation was induced by Trichostatin A injection. Quantitative real-time PCR and Western blot were used to determine the changes of AMPARs in acetylated hippocampus. The behavioral tests proved that AMPA was involved in the PS-induced depression-like behavior in offspring rats. Hippocampal acetylation significantly increased the preference to sucrose of PS-induced offspring rats and reduced the immobile time in forced swimming test, suggesting that acetylation could improve PS-induced depression-like behaviors. In addition, PS inhibited the expression levels of GluA1-3 subunits of AMPARs in the offspring hippocampus, while Hippocampal acetylation could reverse this effect by increasing GluA1-3 expression. PS-induced reduction of GluA1-3 subunits of AMPARs may be an important potential mechanism of offspring depression. Hippocampal acetylation may improve PS-induced offspring depression-like behavior through the enhanced expression of AMPARs (GluA1-3 subunits).
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Beebe B, Badalamenti A, Jaffe J et al (2008) Distressed mothers and their infants use a less efficient timing mechanism in creating expectancies of each other’s looking patterns. J Psycholinguist Res 37(5):293–307
Champagne FA (2010) Epigenetic influence of social experiences across the lifespan. Dev Psychobiol 52(4):299–311
Talge NM, Neal C, Glover V (2007) Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? J Child Psychol Psychiatry 48(3–4):245–261
Zeng J, Zhu ZL, Li H et al (2015) Maternal stress in gestation: birth outcomes and stress-related hormone response of the neonates. Pediatr Neonatol 56(6):376–381
Lixia Guan Ning, Jia Xiaoyan, Zha et al (2013) The involvement of ERK/CREB/Bcl-2 in depression-like behavior in prenatally stressed offspring rats. Brain Res Bull 99:1–8
Jia N, Yang K, Sun Q et al (2010) Prenatal stress causes dendritic atrophy of pyramidal neurons in hippocampal CA3 region by glutamate in offspring rats. Dev Neurobiol 70(2):114–125
Niciu MJ, Ionescu DF, Richards EM et al (2014) Glutamate and its receptors in the pathophysiology and treatment of major depressive disorder. J Neural Transm 121:907–924
Aleksandrova LR, Phillips AG, Wang YT (2017) Antidepressant effects of ketamine and the roles of AMPA glutamate receptors and other mechanisms beyond NMDA receptor antagonism. J Psychiatry Neurosci 42(2):160–175
Beneyto M, Meador-Woodruff JH (2004) Expression of transcripts encoding AMPA receptor subunits and associated postsynaptic proteins in the macaque brain. J Comp Neurol 468:530–554
Wiedholz LM, Owens WA, Horton RE et al (2008) Mice lacking the AMPA GluR1 receptor exhibit striatal hyperdopaminergia and ‘schizophrenia-related’ behaviors. Mol Psychiatry 13:631–640
Li X, Tizzano JP, Griffey K, Clay M et al (2001) Antidepressant-like actions of an AMPA receptor potentiator (LY392098). Neuropharmacology 40:1028–1033
Li X, Witkin JM, Need AB et al (2003) Enhancement of antidepressant potency by a potentiator of AMPA receptors. Cell Mol Neurobiol 23:419–430
Kllarackal AJ, Kvarta MD, Cammarata E et al (2013) Chronic stress induces a selective decrease in AMPA receptor-mediated synaptic excitation at hippocampal temporoammonic-CA1 synapses. J Neurosci 33:15669–15674
Machado-Vieira R, Henter ID, Zarate CA Jr (2015) New targets for rapid antidepressant action. Prog Neurobiol 152:21–37
Ferland Chantelle L., Erin P, Harris et al (2014) Facilitation of the HPA axis to a novel acute stress following chronic stress exposure modulates histone acetylation and the ERK/MAPK pathway in the dentate gyrus of male rats. Endocrinology 155(8):2942–2952
Sarkar A, Chachra P, Kennedy P et al (2014) Hippocampal Hdac4 contributes to postnatal fluoxetine-evoked depression-like behavior. Neuropsychopharmacology 39(9):2221–2232
Erburu M, Muñoz-Cobo I, Dominguez-Andrés et al (2015) Chronic stress and antidepressant induced changes in Hdac5 and Sirt2 affect synaptic plasticity. Eur Neuropsychopharmacol 25(11):2036–2048
Sun H, Jia N, Guan L et al (2013) Involvement of NR1, NR2A different expression in brain regions in anxiety-like behavior of prenatally stressed offspring. Behav Brain Res 15(257):1–7
Koehl M, Darnaudéry M, Dulluc J, Van Reeth O, Moal ML, Maccari S (1999) Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both gender. J Neurobiol 40:302–315
Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, New York
Rodríguez MJ, Robledo P, Andrade C et al (2005) In vivo co-ordinated interactions between inhibitory systems to control glutamate-mediated hippocampal excitability. J Neurochem 95(3):651–661
Liu H, Wen LM, Qiao H et al (2013) Modulation of hippocampal glutamate and NMDA/AMPA receptor by homocysteine in chronic unpredictable mild stress-induced rat depression. Sheng Li Xue Bao 65(1):61–71
Inokoshi J, Katagiri M, Arima S et al (1999) Neuronal differentiation of neuro 2a cells by inhibitors of cell cycle progression, trichostatin A and butyrolactone I. Biochem Biophys Res Commun 256(2):372–376
Wang H, Florian D, Yan L et al (2013) Histone deacetylase inhibitors facilitate partner preference formation in female prairie voles. Nat Neurosci 16(7):919–924
Guan L, Jia N, Zhao X, Zhang X et al (2013) The involvement of ERK/CREB/Bcl-2 in depression-like behavior in prenatally stressed offspring rats. Brain Res Bull 99:1–8
Jia N, Li Q, Sun H et al (2015) Alterations of group I mGluRs and BDNF associated with behavioral abnormity in prenatally stressed offspring rats. Neurochem Res 40:1074–1082
Sun H, Guan L, Zhu Z et al (2013) Reduced levels of NR1 and NR2A with depression-like behavior in different brain regions in prenatally stressed juvenile offspring. PLoS ONE 8(11):e81775
Chourbaji S, Vogt MA, Fumagalli F et al (2008) AMPA receptor subunit 1 (GluR-A) knockout mice model the glutamate hypothesis of depression. FASEB J 22(9):3129–3134
Heim C, Binder EB (2012) Current research trends in early life stress and depression: review of human studies on sensitive periods, gene-environment interactions, and epigenetics. Exp Neurol 233:102–111
Booij SH, Bos EH, De Jonge P et al (2014) Markers of stress and inflam-mation as potential mediators of the relationship between exercise and depressive symptoms: findings from the trails study. Psychophysiology 52(3):352–358
Davis DA, Bortolato M, Godar SC et al (2013) Prenatal exposure to urban air nanoparticles in mice causes altered neuronal differentiation and depression-like responses. PLoS ONE 8:e64128
Levenson JM, Sweatt JD (2005) Epigenetic mechanisms in memory formation. Nat Rev Neurosci 6:108–118
Maddox SA, Schafe GE, Ressler KJ (2013) Exploring epigenetic regulation of fear memory and biomarkers associated with post-traumatic stress disorder. Front Psychiatry 4:62
Miller CA, Sweatt JD (2007) Covalent modification of DNA regulates memory formation. Neuron 53:857–869
Nasca C, Zelli D, Bigio B et al (2015) Stress dynamically regulates behavior and glutamatergic gene expression in hippocampus by opening a window of epigenetic plasticity. Proc Natl Acad Sci USA 112(48):14960–14965
An XL, Tai FD (2013) AVP and Glu systems interact to regulate levels of anxiety in BALB/cJ mice. Zool Res 35(4):319–325
Duric V, Banasr M, Stockmeier CA et al (2013) Altered expression of synapse and glutamate related genes in post-mortem hippocampus of depressed subjects. Int J Neuropsychopharmacol 16(1):69–82
Yuen EY, Wei J, Liu W et al (2012) Repeated stress causes cognitive impairment by suppressing glutamate receptor expression and function in prefrontal cortex. Neuron 73(5):962–977
Penn AC, Balik A, Wozny C et al (2012) Activity-mediated AMPA receptor remodeling, driven by alternative splicing in the ligand-binding domain. Neuron 76(3):503–510
Viltart O, Vanbesien-Mailliot CC (2007) Impact of prenatal stress on neuroendocrine programming. Sci World J 7:1493–1537
Cottrell EC, Seckl JR (2009) Prenatal stress, glucocorticoids and the programming of adult disease. Front Behav Neurosci 3:19
Welberg LAM, Seckl JR, Holmes MC (2001) Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour. Neuroscience 104(1):71–79
Mueller BR, Bale TL (2008) Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 28(36):9055–9065
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This work was supported by National Natural Science Foundation of China (No. 81271497) and Medical and Health Technology Development Project of Shandong Province (No. 2015WS0452).
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Lu, Y., Zhang, J., Zhang, L. et al. Hippocampal Acetylation may Improve Prenatal-Stress-Induced Depression-Like Behavior of Male Offspring Rats Through Regulating AMPARs Expression. Neurochem Res 42, 3456–3464 (2017). https://doi.org/10.1007/s11064-017-2393-7
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DOI: https://doi.org/10.1007/s11064-017-2393-7