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04.12.2017 | Original Article

Repeated shock stress facilitates basolateral amygdala synaptic plasticity through decreased cAMP-specific phosphodiesterase type IV (PDE4) expression

verfasst von: Steve Ryan, Chenchen Li, Aurélie Menigoz, Rimi Hazra, Joanna Dabrowska, David Ehrlich, Katelyn Gordon, Donald G. Rainnie

Erschienen in: Brain Structure and Function | Ausgabe 4/2018

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Abstract

Previous studies have shown that exposure to stressful events can enhance fear memory and anxiety-like behavior as well as increase synaptic plasticity in the rat basolateral amygdala (BLA). We have evidence that repeated unpredictable shock stress (USS) elicits a long-lasting increase in anxiety-like behavior in rats, but the cellular mechanisms mediating this response remain unclear. Evidence from recent morphological studies suggests that alterations in the dendritic arbor or spine density of BLA principal neurons may underlie stress-induced anxiety behavior. Recently, we have shown that the induction of long-term potentiation (LTP) in BLA principal neurons is dependent on activation of postsynaptic D1 dopamine receptors and the subsequent activation of the cyclic adenosine 5′-monophosphate (cAMP)—protein kinase A (PKA) signaling cascade. Here, we have used in vitro whole-cell patch-clamp recording from BLA principal neurons to investigate the long-term consequences of USS on their morphological properties and synaptic plasticity. We provided evidence that the enhanced anxiety-like behavior in response to USS was not associated with any significant change in the morphological properties of BLA principal neurons, but was associated with a changed frequency dependence of synaptic plasticity, lowered LTP induction threshold, and reduced expression of phosphodiesterase type 4 enzymes (PDE4s). Furthermore, pharmacological inhibition of PDE4 activity with rolipram mimics the effects of chronic stress on LTP induction threshold and baseline startle. Our results provide the first evidence that stress both enhances anxiety-like behavior and facilitates synaptic plasticity in the amygdala through a common mechanism of PDE4-mediated disinhibition of cAMP-PKA signaling.

Abercrombie HC, Schaefer SM, Larson CL, Oakes TR, Lindgren KA et al (1998) Metabolic rate in the right amygdala predicts negative affect in depressed patients. Neuroreport 9:3301–3307CrossRefPubMed

Baillie GS, Houslay MD (2005) Arrestin times for compartmentalised cAMP signalling and phosphodiesterase-4 enzymes. Curr Opin Cel Biol 17(2):129–134CrossRef

Beylin AV, Shors TJ (1998) Stress enhances excitatory trace eyeblink conditioning and opposes acquisition of inhibitory conditioning. Behav Neurosci 112:1327–1338CrossRefPubMed

Blair HT, Schafe GE, Bauer EP, Rodrigues SM, LeDoux JE (2001) Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learn Mem 8:229–242CrossRefPubMed

Blitzer RD, Wong T, Nouranifar R, Iyengar R, Landau EM (1995) Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region. Neuron 15:1403–1414CrossRefPubMed

Blitzer RD, Connor JH, Brown GP, Wong T, Shenolikar S et al (1998) Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. Science 280:1940–1942CrossRefPubMed

Braga MF, Aroniadou-Anderjaska V, Li H (2004) The physiological role of kainate receptors in the amygdala. Mol Neurobiol 30:127–141CrossRefPubMed

Brown SM, Henning S, Wellman CL (2005) Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. Cereb Cortex 15(11):1714–1722CrossRefPubMed

Bureau Y, Handa M, Zhu Y, Laliberte F, Moore CS, Liu S, Huang Z, MacDonald D, Xu DG, Robertson GS (2006) Neuroanatomical and pharmacological assessment of Fos expression induced in the rat brain by the phosphodiesterase-4 inhibitor 6-(4-pyridylmethyl)-8-(3-nitrophenyl) quinoline. Neuropharmacology 51(5):974–985CrossRefPubMed

Caudal D, Godsil BP, Mailliet F, Bergerot D, Jay TM (2010) Acute stress induces contrasting changes in AMPA receptor subunit phosphorylation within the prefrontal cortex, amygdala and hippocampus. PLoS One 5:e15282CrossRefPubMedPubMedCentral

Chen CC, Yang CH, Huang CC, Hsu KS (2010) Acute stress impairs hippocampal mossy fiber-CA3 long-term potentiation by enhancing cAMP-specific phosphodiesterase 4 activity. Neuropsychopharmacology 35(7):1605–1617CrossRefPubMedPubMedCentral

Conrad CD, LeDoux JE, Magariños AM, McEwen BS (1999) Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav Neurosci 113(5):902–913CrossRefPubMed

Cook SC, Wellman CL (2004) Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 60(2):236–248CrossRefPubMed

Cordero MI, Venero C, Kruyt ND, Sandi C (2003) Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats. Evidence for a role of corticosterone. Horm Behav 44:338–345CrossRefPubMed

Cui H, Sakamoto H, Higashi S, Kawata M (2008) Effects of single-prolonged stress on neurons and their afferent inputs in the amygdala. Neuroscience 152(3):703–712CrossRefPubMed

Drevets WC (1999) Prefrontal cortical-amygdalar metabolism in major depression. Ann N Y Acad Sci 877:614–637CrossRefPubMed

Ehrlich DE, Rainnie DG (2015) Prenatal stress alters the development of socioemotional behavior and amygdala neuron excitability in rats. Neuropsychopharmacology 40(9):2135–2145CrossRef

Ehrlich DE, Ryan SJ, Rainnie DG (2012) Postnatal development of electrophysiological properties of principal neurons in the rat basolateral amygdala. J Physiol 590(19):4819–4838CrossRefPubMedPubMedCentral

Hazra R, Guo JD, Dabrowska J, Rainnie DG (2012) Differential distribution of serotonin receptor subtypes in BNST(ALG) neurons: modulation by unpredictable shock stress. Neuroscience 225:9–21CrossRefPubMedPubMedCentral

Huang T, McDonough CB, Abel T (2006) Compartmentalized PKA signaling events are required for synaptic tagging and capture during hippocampal late-phase long-term potentiation. Eur J Cell Biol 85(7):635–642CrossRefPubMedPubMedCentral

Hubert GW, Li C, Rainnie DG, Muly EC (2014) Effects of stress on AMPA receptor distribution and function in the basolateral amygdala. Brain Struct Funct 219(4):1169–1179CrossRefPubMed

Itoh T, Abe K, Tokumura M, Horiuchi M, Inoue O, Ibii N (2003) Different regulation of adenylyl cyclase and rolipram-sensitive phosphodiesterase activity on the frontal cortex and hippocampus in learned helplessness rats. Brain Res 991(1–2):142–149CrossRefPubMed

Josselyn SA (2010) Continuing the search for the engram: examining the mechanism of fear memories. J Psychiatry Neurosci 35(4):221–228CrossRefPubMedPubMedCentral

Kavushansky A, Richter-Levin G (2006) Effects of stress and corticosterone on activity and plasticity in the amygdala. J Neurosci Res 84(7):1580–1587CrossRefPubMed

Klussmann E (2016) Protein-protein interactions of PDE4 family members - Functions, interactions and therapeutic value. Cell Signal 28(7):713–718CrossRefPubMed

LeDoux JE (1993) Emotional memory systems in the brain. Behav Brain Res 58:69–79CrossRefPubMed

Li X, Baillie GS, Houslay MD (2009) Mdm2 directs the ubiquitination of beta-arrestin-sequestered cAMP phosphodiesterase-4D5. J Biol Chem 284(24):16170–16182CrossRefPubMedPubMedCentral

Li C, Dabrowska J, Hazra R, Rainnie DG (2011) Synergistic activation of dopamine D1 and TrkB receptors mediate gain control of synaptic plasticity in the basolateral amygdala. PLoS One 6:e26065CrossRefPubMedPubMedCentral

Liu RJ, Aghajanian GK (2008) Stress blunts serotonin- and hypocretin-evoked EPSCs in prefrontal cortex: role of corticosterone-mediated apical dendritic atrophy. Proc Natl Acad Sci USA 105(1):359–364CrossRefPubMedPubMedCentral

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408CrossRefPubMed

McEwen BS (2005) Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 54(5 Suppl 1):20–23CrossRefPubMed

McGaugh JL, Roozendaal B (2002) Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 12(2):205–210CrossRefPubMed

McGirr A, Lipina TV, Mun HS, Georgiou J, Al-Miri AH, Ng E, Zhai D, Elliot C, Cameron RT, Mullings JG, Liu F, Baillie GS, Clapcote SJ, Roder JD (2016) Specific inhibition of phosphodiesterase-4B results in anxiolysis and facilitates memory acquisition. Neuropsychopharmacology 41(4):1080–1092CrossRefPubMed

Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makhinson M, He Y, Ramsay MF, Morris RG, Morrison JH, O’Dell TJ, Grant SG (1998) Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396(6710):433–439CrossRefPubMed

Mitra R, Jadhav S, McEwen BS, Vyas A, Chattarji S (2005) Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc Natl Acad Sci USA 102:9371–9376CrossRefPubMedPubMedCentral

Moberg CA, Curtin JJ (2009) Alcohol selectively reduces anxiety but not fear: startle response during unpredictable versus predictable threat. J Abnorm Psychol 118(2):335–347CrossRefPubMedPubMedCentral

Moench KM, Maroun M, Kavushansky A, Wellman C (2015) Alterations in neuronal morphology in infralimbic cortex predict resistance to fear extinction following acute stress. Neurobiol Stress 3:23–33CrossRefPubMedPubMedCentral

Moita MA, Rosis S, Zhou Y, LeDoux JE, Blair HT (2004) Putting fear in its place: remapping of hippocampal place cells during fear conditioning. J Neurosci 2004 Aug 4 24(31):7015–7023

Nie T, McDonough CB, Huang T, Nguyen PV, Abel T (2007) Genetic disruption of protein kinase A anchoring reveals a role for compartmentalized kinase signaling in theta-burst long-term potentiation and spatial memory. J Neurosci 27(38):10278–10288CrossRefPubMedPubMedCentral

Nijholt IM, Ostroveanu A, de Bruyn M, Luiten PG, Eisel UL, Van der Zee EA (2007) Both exposure to a novel context and associative learning induce an upregulation of AKAP150 protein in mouse hippocampus. Neurobiol Learn Mem 87(4):693–696CrossRefPubMed

Otmakhova NA, Otmakhov N, Mortenson LH, Lisman JE (2000) Inhibition of the cAMP pathway decreases early long-term potentiation at CA1 hippocampal synapses. J Neurosci 20:4446–4451PubMed

Padival M, Quinette D, Rosenkranz JA (2013) Effects of repeated stress on excitatory drive of basal amygdala neurons in vivo. Neuropsychopharmacology 38(9):1748–1762CrossRefPubMedPubMedCentral

Pickel VM, Colago EE, Mania I, Molosh AI, Rainnie DG (2006) Dopamine D1 receptors co-distribute with N-methyl-_D-aspartic acid type-1 subunits and modulate synaptically-evoked N-methyl-_D-aspartic acid currents in rat basolateral amygdala. Neuroscience 142:671–690CrossRefPubMed

Pillai AG, Anilkumar S, Chattarji S (2012) The same antidepressant elicits contrasting patterns of synaptic changes in the amygdala vs hippocampus. Neuropsychopharmacology 37(12):2702–2711CrossRefPubMedPubMedCentral

Radley JJ, Sisti HM, Hao J, Rocher AB, McCall T, Hof PR, McEwen BS, Morrison JH (2004) Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 2004;125(1):1–6CrossRefPubMed

Rainnie DG (1999) Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J Neurophysiol 82(1):69–85CrossRefPubMed

Rainnie DG, Asprodini EK, Shinnick-Gallagher P (1993) Intracellular recordings from morphologically identified neurons of the basolateral amygdala. J Neurophysiol 69:1350–1362CrossRefPubMed

Rau V, DeCola JP, Fanselow MS (2005) Stress-induced enhancement of fear learning: an animal model of posttraumatic stress disorder. Neurosci Biobehav Rev 29(8):1207–1223CrossRefPubMed

Rauch SL, Whalen PJ, Shin LM, McInerney SC, Macklin ML et al (2000) Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol Psychiatry 47:769–776CrossRefPubMed

Reznikov LR, Grillo CA, Piroli GG, Pasumarthi RK, Reagan LP et al (2007) Acute stress-mediated increases in extracellular glutamate levels in the rat amygdala: differential effects of antidepressant treatment. Eur J Neurosci 25:3109–3114CrossRefPubMed

Rodriguez Manzanares PA, Isoardi NA, Carrer HF, Molina VA (2005) Previous stress facilitates fear memory, attenuates GABAergic inhibition, and increases synaptic plasticity in the rat basolateral amygdala. J Neurosci 25:8725–8734CrossRefPubMed

Rogan MT, Staubli UV, LeDoux JE (1997) Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390:604–607CrossRefPubMed

Rosenkranz JA, Venheim ER, Padival M (2010) Chronic stress causes amygdala hyperexcitability in rodents. Biol Psychiatry 67:1128–1136CrossRefPubMedPubMedCentral

Rutten K, Misner DL, Works M, Blokland A, Novak TJ et al (2008) Enhanced long-term potentiation and impaired learning in phosphodiesterase 4D-knockout (PDE4D) mice. Eur J Neurosci 28:625–632CrossRefPubMed

Rutten K, Wallace TL, Works M, Prickaerts J, Blokland A, Novak TJ, Santarelli L, Misner DL (2011) Enhanced long-term depression and impaired reversal learning in phosphodiesterase 4B-knockout (PDE4B(-/-)) mice. Neuropharmacology 61:138–147CrossRefPubMed

Ryan SJ, Ehrlich DE, Rainnie DG (2014) Morphology and dendritic maturation of developing principal neurons in the rat basolateral amygdala. Brain Struct Funct 221(2):839–854

Shors TJ, Foy MR, Levine S, Thompson RF (1990) Unpredictable and uncontrollable stress impairs neuronal plasticity in the rat hippocampus. Brain Res Bull 24(5):663–667CrossRefPubMed

Shors TJ, Weiss C, Thompson RF (1992) Stress-induced facilitation of classical conditioning. Science 257:537–539CrossRefPubMed

Sink KS, Walker DL, Yang Y, Davis M (2011) Calcitonin gene-related peptide in the bed nucleus of the stria terminalis produces an anxiety-like pattern of behavior and increases neural activation in anxiety-related structures. J Neurosci 31:1802–1810CrossRefPubMedPubMedCentral

Suvrathan A, Bennur S, Ghosh S, Tomar A, Anilkumar S, Chattarji S (2014) Stress enhances fear by forming new synapses with greater capacity for long-term potentiation in the amygdala. Philos Trans R Soc Lond B Biol Sci 369(1633)

Terrin A, Di Benedetto G, Pertegato V, Cheung YF, Baillie G, Lynch MJ, Elvassore N, Prinz A, Herberg FW, Houslay MD, Zaccolo M (2006) PGE(1) stimulation of HEK293 cells generates multiple contiguous domains with different [cAMP]: role of compartmentalized phosphodiesterases. J Cell Biol 175(3):441–451CrossRefPubMedPubMedCentral

Tsai SF, Huang TY, Chang CY, Hsu YC, Chen SJ, Yu L, Kuo YM, Jen CJ (2014) Social instability stress differentially affects amygdalar neuron adaptations and memory performance in adolescent and adult rats. Front Behav Neurosci 8:27PubMedPubMedCentral

Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3(7):RESEARCH0034

Villarreal G, King CY (2001) Brain imaging in posttraumatic stress disorder. Semin Clin Neuropsychiatry 6:131–145CrossRefPubMed

Vouimba RM, Yaniv D, Diamond D, Richter-Levin G (2004) Effects of inescapable stress on LTP in the amygdala versus the dentate gyrus of freely behaving rats. Eur J Neurosci 19:1887–1894CrossRefPubMed

Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S (2002) Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22(15):6810–6818PubMed

Vyas A, Pillai AG, Chattarji S (2004) Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 128(4):667–673CrossRef

Vyas A, Jadhav S, Chattarji S (2006) Prolonged behavioral stress enhances synaptic connectivity in the basolateral amygdala. Neuroscience 143:387–393CrossRefPubMed

Walker DL, Davis M (1997) Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci 17:9375–9383CrossRefPubMed

Walker DL, Toufexis DJ, Davis M (2003) Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur J Pharmacol 463(1–3):199–216CrossRefPubMed

Watanabe Y, Gould E, McEwen BS (1992a) Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 588:341–345CrossRefPubMed

Watanabe Y, Gould E, Daniels DC, Cameron H, McEwen BS (1992b) Tianeptine attenuates stress-induced morphological changes in the hippocampus. Eur J Pharmacol 222:157–162CrossRefPubMed

Werenicz A, Christoff RR, Blank M, Jobim PF, Pedroso TR, Reolon GK, Schröder N, Roesler R (2012) Administration of the phosphodiesterase type 4 inhibitor rolipram into the amygdala at a specific time interval after learning increases recognition memory persistence. Learn Mem 19(10):495–498CrossRefPubMed

Wood GE, Norris EH, Waters E, Stoldt JT, McEwen BS (2008) Chronic immobilization stress alters aspects of emotionality and associative learning in the rat. Behav Neurosci 122(2):282–292CrossRefPubMed

Zhang HT, Huang Y, Masood A, Stolinski LR, Li Y, Zhang L, Dlaboga D, Jin SL, Conti M, O’Donnell JM (2008) Anxiogenic-like behavioral phenotype of mice deficient in phosphodiesterase 4B (PDE4B). Neuropsychopharmacology 33(7):1611–1623CrossRefPubMed

Zhu D, Li C, Swanson AM, Villalba RM, Guo J, Zhang Z, Matheny S, Murakami T, Stephenson JR, Daniel S, Fukata M, Hall RA, Olson JJ, Neigh GN, Smith Y, Rainnie DG, Van Meir EG (2015) BAI1 regulates spatial learning and synaptic plasticity in the hippocampus. J Clin Invest. 125(4):1497–4508CrossRef

Titel: Repeated shock stress facilitates basolateral amygdala synaptic plasticity through decreased cAMP-specific phosphodiesterase type IV (PDE4) expression
verfasst von: Steve Ryan
Chenchen Li
Aurélie Menigoz
Rimi Hazra
Joanna Dabrowska
David Ehrlich
Katelyn Gordon
Donald G. Rainnie
Publikationsdatum: 04.12.2017
Verlag: Springer Berlin Heidelberg
Erschienen in: Brain Structure and Function / Ausgabe 4/2018
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-017-1575-z

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Repeated shock stress facilitates basolateral amygdala synaptic plasticity through decreased cAMP-specific phosphodiesterase type IV (PDE4) expression

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