Skip to main content
Erschienen in: Brain Structure and Function 5/2015

01.09.2015 | Original Article

Localisation and stress-induced plasticity of GABAA receptor subunits within the cellular networks of the mouse dorsal raphe nucleus

verfasst von: Nicole L. Corteen, Jessica A. Carter, Uwe Rudolph, Delia Belelli, Jeremy J. Lambert, Jerome D. Swinny

Erschienen in: Brain Structure and Function | Ausgabe 5/2015

Einloggen, um Zugang zu erhalten

Abstract

The dorsal raphe nucleus (DRN) provides the major source of serotonin to the central nervous system (CNS) and modulates diverse neural functions including mood. Furthermore, DRN cellular networks are engaged in the stress–response at the CNS level allowing for adaptive behavioural responses, whilst stress-induced dysregulation of DRN and serotonin release is implicated in psychiatric disorders. Therefore, identifying the molecules regulating DRN activity is fundamental to understand DRN function in health and disease. GABAA receptors (GABAARs) allow for brain region, cell type and subcellular domain-specific GABA-mediated inhibitory currents and are thus key regulators of neuronal activity. Yet, the GABAAR subtypes expressed within the neurochemically diverse cell types of the mouse DRN are poorly described. In this study, immunohistochemistry and confocal microscopy revealed that all serotonergic neurons expressed immunoreactivity for the GABAAR alpha2 and 3 subunits, although the respective signals were co-localised to varying degrees with inhibitory synaptic marker proteins. Only a topographically located sub-population of serotonergic neurons exhibited GABAAR alpha1 subunit immunoreactivity. However, all GABAergic as well as non-GABAergic, non-serotonergic neurons within the DRN expressed GABAAR alpha1 subunit immunoreactivity. Intriguingly, immunoreactivity for the GABAAR gamma2 subunit was enriched on GABAergic rather than serotonergic neurons. Finally, repeated restraint stress increased the expression of the GABAAR alpha3 subunit at the mRNA and protein level. The study demonstrates the identity and location of distinct GABAAR subunits within the cellular networks of the mouse DRN and that stress impacts on the expression levels of particular subunits at the gene and protein level.
Literatur
Zurück zum Zitat Abramian AM, Comenencia-Ortiz E, Modgil A, Vien TN, Nakamura Y, Moore YE, Maguire JL, Terunuma M, Davies PA, Moss SJ (2014) Neurosteroids promote phosphorylation and membrane insertion of extrasynaptic GABAA receptors. Proc Natl Acad Sci USA 111(19):7132–7137. doi:10.1073/pnas.1403285111 PubMedCentralCrossRefPubMed Abramian AM, Comenencia-Ortiz E, Modgil A, Vien TN, Nakamura Y, Moore YE, Maguire JL, Terunuma M, Davies PA, Moss SJ (2014) Neurosteroids promote phosphorylation and membrane insertion of extrasynaptic GABAA receptors. Proc Natl Acad Sci USA 111(19):7132–7137. doi:10.​1073/​pnas.​1403285111 PubMedCentralCrossRefPubMed
Zurück zum Zitat Aronsson M, Fuxe K, Dong Y, Agnati LF, Okret S, Gustafsson J-A (1988) Localization of glucocorticoid receptor mRNA in the male rat brain by in situ hybridization. Proc Natl Acad Sci 85(23):9331–9335PubMedCentralCrossRefPubMed Aronsson M, Fuxe K, Dong Y, Agnati LF, Okret S, Gustafsson J-A (1988) Localization of glucocorticoid receptor mRNA in the male rat brain by in situ hybridization. Proc Natl Acad Sci 85(23):9331–9335PubMedCentralCrossRefPubMed
Zurück zum Zitat Baumann B, Bielau H, Krell D, Agelink M, Diekmann S, Wurthmann C, Trubner K, Bernstein H, Danos P, Bogerts B (2002) Circumscribed numerical deficit of dorsal raphe neurons in mood disorders. Psychol Med 32(1):93–103CrossRefPubMed Baumann B, Bielau H, Krell D, Agelink M, Diekmann S, Wurthmann C, Trubner K, Bernstein H, Danos P, Bogerts B (2002) Circumscribed numerical deficit of dorsal raphe neurons in mood disorders. Psychol Med 32(1):93–103CrossRefPubMed
Zurück zum Zitat Benson JA, Low K, Keist R, Mohler H, Rudolph U (1998) Pharmacology of recombinant gamma-aminobutyric acidA receptors rendered diazepam-insensitive by point-mutated alpha-subunits. FEBS Lett 431(3):400–404CrossRefPubMed Benson JA, Low K, Keist R, Mohler H, Rudolph U (1998) Pharmacology of recombinant gamma-aminobutyric acidA receptors rendered diazepam-insensitive by point-mutated alpha-subunits. FEBS Lett 431(3):400–404CrossRefPubMed
Zurück zum Zitat Browne SH, Kang J, Akk G, Chiang LW, Schulman H, Huguenard JR, Prince DA (2001) Kinetic and pharmacological properties of GABAAReceptors in single thalamic neurons and GABAA subunit expression. J Neurophysiol 86(5):2312–2322PubMed Browne SH, Kang J, Akk G, Chiang LW, Schulman H, Huguenard JR, Prince DA (2001) Kinetic and pharmacological properties of GABAAReceptors in single thalamic neurons and GABAA subunit expression. J Neurophysiol 86(5):2312–2322PubMed
Zurück zum Zitat Carter JA, Górecki DC, Mein CA, Ljungberg B, Hafizi S (2013) CpG dinucleotide-specific hypermethylation of the TNS3 gene promoter in human renal cell carcinoma. Epigenetics 8(7):739–747PubMedCentralCrossRefPubMed Carter JA, Górecki DC, Mein CA, Ljungberg B, Hafizi S (2013) CpG dinucleotide-specific hypermethylation of the TNS3 gene promoter in human renal cell carcinoma. Epigenetics 8(7):739–747PubMedCentralCrossRefPubMed
Zurück zum Zitat Celada P, Puig MV, Casanovas JM, Guillazo G, Artigas F (2001) Control of dorsal raphe serotonergic neurons by the medial prefrontal cortex: involvement of serotonin-1A, GABA(A), and glutamate receptors. J Neurosci 21(24):9917–9929PubMed Celada P, Puig MV, Casanovas JM, Guillazo G, Artigas F (2001) Control of dorsal raphe serotonergic neurons by the medial prefrontal cortex: involvement of serotonin-1A, GABA(A), and glutamate receptors. J Neurosci 21(24):9917–9929PubMed
Zurück zum Zitat Crestani F, Lorez M, Baer K, Essrich C, Benke D, Laurent JP, Belzung C, Fritschy J-M, Lüscher B, Mohler H (1999) Decreased GABAA-receptor clustering results in enhanced anxiety and a bias for threat cues. Nat Neurosci 2(9):833–839. doi:10.1038/12207 CrossRefPubMed Crestani F, Lorez M, Baer K, Essrich C, Benke D, Laurent JP, Belzung C, Fritschy J-M, Lüscher B, Mohler H (1999) Decreased GABAA-receptor clustering results in enhanced anxiety and a bias for threat cues. Nat Neurosci 2(9):833–839. doi:10.​1038/​12207 CrossRefPubMed
Zurück zum Zitat Dixon CI, Rosahl TW, Stephens DN (2008) Targeted deletion of the GABRA2 gene encoding alpha2-subunits of GABA(A) receptors facilitates performance of a conditioned emotional response, and abolishes anxiolytic effects of benzodiazepines and barbiturates. Pharmacol Biochem Behav 90(1):1–8. doi:10.1016/j.pbb.2008.01.015 CrossRefPubMed Dixon CI, Rosahl TW, Stephens DN (2008) Targeted deletion of the GABRA2 gene encoding alpha2-subunits of GABA(A) receptors facilitates performance of a conditioned emotional response, and abolishes anxiolytic effects of benzodiazepines and barbiturates. Pharmacol Biochem Behav 90(1):1–8. doi:10.​1016/​j.​pbb.​2008.​01.​015 CrossRefPubMed
Zurück zum Zitat Essrich C, Lorez M, Benson JA, Fritschy JM, Luscher B (1998) Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nat Neurosci 1(7):563–571. doi:10.1038/2798 CrossRefPubMed Essrich C, Lorez M, Benson JA, Fritschy JM, Luscher B (1998) Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nat Neurosci 1(7):563–571. doi:10.​1038/​2798 CrossRefPubMed
Zurück zum Zitat Fritschy J-M, Weinmann Oliver, Wenzel Andreas, Benke Dietmar (1998) Synapse-specific localisation of NMDA and GABAA receptor subunits revealed by antigen retrieval immunohistochemistry. J Comp Neurol 390:194–210CrossRefPubMed Fritschy J-M, Weinmann Oliver, Wenzel Andreas, Benke Dietmar (1998) Synapse-specific localisation of NMDA and GABAA receptor subunits revealed by antigen retrieval immunohistochemistry. J Comp Neurol 390:194–210CrossRefPubMed
Zurück zum Zitat Fu W, Le Maitre E, Fabre V, Bernard JF, David Xu ZQ, Hokfelt T (2010) Chemical neuroanatomy of the dorsal raphe nucleus and adjacent structures of the mouse brain. J Comp Neurol 518(17):3464–3494. doi:10.1002/cne.22407 CrossRefPubMed Fu W, Le Maitre E, Fabre V, Bernard JF, David Xu ZQ, Hokfelt T (2010) Chemical neuroanatomy of the dorsal raphe nucleus and adjacent structures of the mouse brain. J Comp Neurol 518(17):3464–3494. doi:10.​1002/​cne.​22407 CrossRefPubMed
Zurück zum Zitat Gao B, Fritschy JM, Benke D, Mohler H (1993) Neuron-specific expression of GABAA-Receptor subtypes: differential association of the alpha1 and alpha3 subunits with serotinergic and GABAergic neurons. Neuroscience 54(4):881–892CrossRefPubMed Gao B, Fritschy JM, Benke D, Mohler H (1993) Neuron-specific expression of GABAA-Receptor subtypes: differential association of the alpha1 and alpha3 subunits with serotinergic and GABAergic neurons. Neuroscience 54(4):881–892CrossRefPubMed
Zurück zum Zitat Gervasoni D, Peyron C, Rampon C, Barbagli B, Chouvet G, Urbain N, Fort P, Luppi PH (2000) Role and origin of the GABAergic innervation of dorsal raphe serotonergic neurons. J Neurosci 20(11):4217–4225. Pii: 20/11/4217PubMed Gervasoni D, Peyron C, Rampon C, Barbagli B, Chouvet G, Urbain N, Fort P, Luppi PH (2000) Role and origin of the GABAergic innervation of dorsal raphe serotonergic neurons. J Neurosci 20(11):4217–4225. Pii: 20/11/4217PubMed
Zurück zum Zitat Gunn BG, Cunningham L, Cooper MA, Corteen NL, Seifi M, Swinny JD, Lambert JJ, Belelli D (2013) Dysfunctional astrocytic and synaptic regulation of hypothalamic glutamatergic transmission in a mouse model of early-life adversity: relevance to neurosteroids and programming of the stress response. J Neurosci 33(50):19534–19554. doi:10.1523/JNEUROSCI.1337-13.2013 PubMedCentralCrossRefPubMed Gunn BG, Cunningham L, Cooper MA, Corteen NL, Seifi M, Swinny JD, Lambert JJ, Belelli D (2013) Dysfunctional astrocytic and synaptic regulation of hypothalamic glutamatergic transmission in a mouse model of early-life adversity: relevance to neurosteroids and programming of the stress response. J Neurosci 33(50):19534–19554. doi:10.​1523/​JNEUROSCI.​1337-13.​2013 PubMedCentralCrossRefPubMed
Zurück zum Zitat Jacobs BL, Azmitia EC (1992) Structure and function of the brain serotonin system. Physiol Rev 72(1):165–229PubMed Jacobs BL, Azmitia EC (1992) Structure and function of the brain serotonin system. Physiol Rev 72(1):165–229PubMed
Zurück zum Zitat Kennedy PJ, Feng J, Robison A, Maze I, Badimon A, Mouzon E, Chaudhury D, Damez-Werno DM, Haggarty SJ, Han M-H (2013) Class I HDAC inhibition blocks cocaine-induced plasticity by targeted changes in histone methylation. Nat Neurosci 16(4):434–440PubMedCentralCrossRefPubMed Kennedy PJ, Feng J, Robison A, Maze I, Badimon A, Mouzon E, Chaudhury D, Damez-Werno DM, Haggarty SJ, Han M-H (2013) Class I HDAC inhibition blocks cocaine-induced plasticity by targeted changes in histone methylation. Nat Neurosci 16(4):434–440PubMedCentralCrossRefPubMed
Zurück zum Zitat Keshavarzy F, Bonnet C, Bezhadi G, Cespuglio R (2014) Expression patterns of c-Fos early gene and phosphorylated ERK in the rat brain following 1-h immobilization stress: concomitant changes induced in association with stress-related sleep rebound. Brain Struct Funct. doi:10.1007/s00429-014-0728-6 PubMed Keshavarzy F, Bonnet C, Bezhadi G, Cespuglio R (2014) Expression patterns of c-Fos early gene and phosphorylated ERK in the rat brain following 1-h immobilization stress: concomitant changes induced in association with stress-related sleep rebound. Brain Struct Funct. doi:10.​1007/​s00429-014-0728-6 PubMed
Zurück zum Zitat Kittler JT, Delmas P, Jovanovic JN, Brown DA, Smart TG, Moss SJ (2000) Constitutive endocytosis of GABAA receptors by an association with the adaptin AP2 complex modulates inhibitory synaptic currents in hippocampal neurons. J Neurosci 20(21):7972–7977PubMed Kittler JT, Delmas P, Jovanovic JN, Brown DA, Smart TG, Moss SJ (2000) Constitutive endocytosis of GABAA receptors by an association with the adaptin AP2 complex modulates inhibitory synaptic currents in hippocampal neurons. J Neurosci 20(21):7972–7977PubMed
Zurück zum Zitat Kittler JT, Chen G, Honing S, Bogdanov Y, McAinsh K, Arancibia-Carcamo IL, Jovanovic JN, Pangalos MN, Haucke V, Yan Z (2005) Phospho-dependent binding of the clathrin AP2 adaptor complex to GABAA receptors regulates the efficacy of inhibitory synaptic transmission. Proc Natl Acad Sci USA 102(41):14871–14876PubMedCentralCrossRefPubMed Kittler JT, Chen G, Honing S, Bogdanov Y, McAinsh K, Arancibia-Carcamo IL, Jovanovic JN, Pangalos MN, Haucke V, Yan Z (2005) Phospho-dependent binding of the clathrin AP2 adaptor complex to GABAA receptors regulates the efficacy of inhibitory synaptic transmission. Proc Natl Acad Sci USA 102(41):14871–14876PubMedCentralCrossRefPubMed
Zurück zum Zitat Koester C, Rudolph U, Haenggi T, Papilloud A, Fritschy JM, Crestani F (2013) Dissecting the role of diazepam-sensitive gamma-aminobutyric acid type A receptors in defensive behavioral reactivity to mild threat. Pharmacol Biochem Behav 103(3):541–549. doi:10.1016/j.pbb.2012.10.004 CrossRefPubMed Koester C, Rudolph U, Haenggi T, Papilloud A, Fritschy JM, Crestani F (2013) Dissecting the role of diazepam-sensitive gamma-aminobutyric acid type A receptors in defensive behavioral reactivity to mild threat. Pharmacol Biochem Behav 103(3):541–549. doi:10.​1016/​j.​pbb.​2012.​10.​004 CrossRefPubMed
Zurück zum Zitat Kos CH (2004) Cre/loxP system for generating tissue-specific knockout mouse models. Nutr Rev 62(6 Pt 1):243–246PubMed Kos CH (2004) Cre/loxP system for generating tissue-specific knockout mouse models. Nutr Rev 62(6 Pt 1):243–246PubMed
Zurück zum Zitat Kralic JE, Sidler C, Parpan F, Homanics GE, Morrow AL, Fritschy JM (2006) Compensatory alteration of inhibitory synaptic circuits in cerebellum and thalamus of gamma-aminobutyric acid type A receptor alpha1 subunit knockout mice. J Comp Neurol 495(4):408–421. doi:10.1002/cne.20866 CrossRefPubMed Kralic JE, Sidler C, Parpan F, Homanics GE, Morrow AL, Fritschy JM (2006) Compensatory alteration of inhibitory synaptic circuits in cerebellum and thalamus of gamma-aminobutyric acid type A receptor alpha1 subunit knockout mice. J Comp Neurol 495(4):408–421. doi:10.​1002/​cne.​20866 CrossRefPubMed
Zurück zum Zitat Lamy CM, Beck SG (2010) Swim stress differentially blocks CRF receptor mediated responses in dorsal raphe nucleus. Psychoneuroendocrinology 35(9):1321–1332PubMedCentralCrossRefPubMed Lamy CM, Beck SG (2010) Swim stress differentially blocks CRF receptor mediated responses in dorsal raphe nucleus. Psychoneuroendocrinology 35(9):1321–1332PubMedCentralCrossRefPubMed
Zurück zum Zitat Lee HS, Kim MA, Valentino RJ, Waterhouse BD (2003) Glutamatergic afferent projections to the dorsal raphe nucleus of the rat. Brain Res 963(1–2):57–71PubMed Lee HS, Kim MA, Valentino RJ, Waterhouse BD (2003) Glutamatergic afferent projections to the dorsal raphe nucleus of the rat. Brain Res 963(1–2):57–71PubMed
Zurück zum Zitat Lemos JC, Zhang G, Walsh T, Kirby LG, Akanwa A, Brooks-Kayal A, Beck SG (2011) Stress-hyperresponsive WKY rats demonstrate depressed dorsal raphe neuronal excitability and dysregulated CRF-mediated responses. Neuropsychopharmacology 36(4):721–734. doi:10.1038/npp.2010.200 PubMedCentralCrossRefPubMed Lemos JC, Zhang G, Walsh T, Kirby LG, Akanwa A, Brooks-Kayal A, Beck SG (2011) Stress-hyperresponsive WKY rats demonstrate depressed dorsal raphe neuronal excitability and dysregulated CRF-mediated responses. Neuropsychopharmacology 36(4):721–734. doi:10.​1038/​npp.​2010.​200 PubMedCentralCrossRefPubMed
Zurück zum Zitat Lorenzo L-E, Russier M, Barbe A, Fritschy J-M, Bras H (2007) Differential organization of γ-aminobutyric acid type A and glycine receptors in the somatic and dendritic compartments of rat abducens motoneurons. J Comp Neurol 504(2):112–126. doi:10.1002/cne.21442 CrossRefPubMed Lorenzo L-E, Russier M, Barbe A, Fritschy J-M, Bras H (2007) Differential organization of γ-aminobutyric acid type A and glycine receptors in the somatic and dendritic compartments of rat abducens motoneurons. J Comp Neurol 504(2):112–126. doi:10.​1002/​cne.​21442 CrossRefPubMed
Zurück zum Zitat Low K, Crestani F, Keist R, Benke D, Brunig I, Benson JA, Fritschy JM, Rulicke T, Bluethmann H, Mohler H, Rudolph U (2000) Molecular and neuronal substrate for the selective attenuation of anxiety. Science 290(5489):131–134CrossRefPubMed Low K, Crestani F, Keist R, Benke D, Brunig I, Benson JA, Fritschy JM, Rulicke T, Bluethmann H, Mohler H, Rudolph U (2000) Molecular and neuronal substrate for the selective attenuation of anxiety. Science 290(5489):131–134CrossRefPubMed
Zurück zum Zitat Maguire EP, Mitchell EA, Greig SJ, Corteen N, Balfour DJ, Swinny JD, Lambert JJ, Belelli D (2013) Extrasynaptic glycine receptors of rodent dorsal raphe serotonergic neurons: a sensitive target for ethanol. Neuropsychopharmacology. doi:10.1038/npp.2013.326 PubMed Maguire EP, Mitchell EA, Greig SJ, Corteen N, Balfour DJ, Swinny JD, Lambert JJ, Belelli D (2013) Extrasynaptic glycine receptors of rodent dorsal raphe serotonergic neurons: a sensitive target for ethanol. Neuropsychopharmacology. doi:10.​1038/​npp.​2013.​326 PubMed
Zurück zum Zitat O’Hearn E, Molliver ME (1984) Organization of raphe-cortical projections in rat: a quantitative retrograde study. Brain Res Bull 13(6):709–726CrossRefPubMed O’Hearn E, Molliver ME (1984) Organization of raphe-cortical projections in rat: a quantitative retrograde study. Brain Res Bull 13(6):709–726CrossRefPubMed
Zurück zum Zitat Paxinos G, Franklin KBJ (2004) The mouse brain in stereotaxic coordinates. Compact 2nd edn. Elsevier Academic Press, Amsterdam; Boston Paxinos G, Franklin KBJ (2004) The mouse brain in stereotaxic coordinates. Compact 2nd edn. Elsevier Academic Press, Amsterdam; Boston
Zurück zum Zitat Peng Z, Hauer B, Mihalek RM, Homanics GE, Sieghart W, Olsen RW, Houser CR (2002) GABAA receptor changes in δ subunit-deficient mice: altered expression of α4 and γ2 subunits in the forebrain. J Comp Neurol 446(2):179–197. doi:10.1002/cne.10210 CrossRefPubMed Peng Z, Hauer B, Mihalek RM, Homanics GE, Sieghart W, Olsen RW, Houser CR (2002) GABAA receptor changes in δ subunit-deficient mice: altered expression of α4 and γ2 subunits in the forebrain. J Comp Neurol 446(2):179–197. doi:10.​1002/​cne.​10210 CrossRefPubMed
Zurück zum Zitat Petrov T, Krukoff TL, Jhamandas JH (1994) Chemically defined collateral projections from the pons to the central nucleus of the amygdala and hypothalamic paraventricular nucleus in the rat. Cell Tissue Res 277(2):289–295CrossRefPubMed Petrov T, Krukoff TL, Jhamandas JH (1994) Chemically defined collateral projections from the pons to the central nucleus of the amygdala and hypothalamic paraventricular nucleus in the rat. Cell Tissue Res 277(2):289–295CrossRefPubMed
Zurück zum Zitat Pfeiffer F, Simler R, Grenningloh G, Betz H (1984) Monoclonal antibodies and peptide mapping reveal structural similarities between the subunits of the glycine receptor of rat spinal cord. Proc Natl Acad Sci USA 81(22):7224–7227PubMedCentralCrossRefPubMed Pfeiffer F, Simler R, Grenningloh G, Betz H (1984) Monoclonal antibodies and peptide mapping reveal structural similarities between the subunits of the glycine receptor of rat spinal cord. Proc Natl Acad Sci USA 81(22):7224–7227PubMedCentralCrossRefPubMed
Zurück zum Zitat Pirker S, Schwarzer C, Wieselthaler A, Sieghart W, Sperk G (2000) GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101(4):815–850. Pii: S0306-4522(00)00442-5CrossRefPubMed Pirker S, Schwarzer C, Wieselthaler A, Sieghart W, Sperk G (2000) GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101(4):815–850. Pii: S0306-4522(00)00442-5CrossRefPubMed
Zurück zum Zitat Poltl A, Hauer B, Fuchs K, Tretter V, Sieghart W (2003) Subunit composition and quantitative importance of GABA(A) receptor subtypes in the cerebellum of mouse and rat. J Neurochem 87(6):1444–1455. Pii: 2315CrossRefPubMed Poltl A, Hauer B, Fuchs K, Tretter V, Sieghart W (2003) Subunit composition and quantitative importance of GABA(A) receptor subtypes in the cerebellum of mouse and rat. J Neurochem 87(6):1444–1455. Pii: 2315CrossRefPubMed
Zurück zum Zitat Poulopoulos A, Aramuni G, Meyer G, Soykan T, Hoon M, Papadopoulos T, Zhang M, Paarmann I, Fuchs C, Harvey K, Jedlicka P, Schwarzacher SW, Betz H, Harvey RJ, Brose N, Zhang W, Varoqueaux F (2009) Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 63(5):628–642. doi:10.1016/j.neuron.2009.08.023 CrossRefPubMed Poulopoulos A, Aramuni G, Meyer G, Soykan T, Hoon M, Papadopoulos T, Zhang M, Paarmann I, Fuchs C, Harvey K, Jedlicka P, Schwarzacher SW, Betz H, Harvey RJ, Brose N, Zhang W, Varoqueaux F (2009) Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 63(5):628–642. doi:10.​1016/​j.​neuron.​2009.​08.​023 CrossRefPubMed
Zurück zum Zitat Price ML, Lucki I (2001) Regulation of serotonin release in the lateral septum and striatum by corticotropin-releasing factor. J Neurosci 21(8):2833–2841PubMed Price ML, Lucki I (2001) Regulation of serotonin release in the lateral septum and striatum by corticotropin-releasing factor. J Neurosci 21(8):2833–2841PubMed
Zurück zum Zitat Renthal W, Maze I, Krishnan V, Covington HE 3rd, Xiao G, Kumar A, Russo SJ, Graham A, Tsankova N, Kippin TE, Kerstetter KA, Neve RL, Haggarty SJ, McKinsey TA, Bassel-Duby R, Olson EN, Nestler EJ (2007) Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56(3):517–529. doi:10.1016/j.neuron.2007.09.032 CrossRefPubMed Renthal W, Maze I, Krishnan V, Covington HE 3rd, Xiao G, Kumar A, Russo SJ, Graham A, Tsankova N, Kippin TE, Kerstetter KA, Neve RL, Haggarty SJ, McKinsey TA, Bassel-Duby R, Olson EN, Nestler EJ (2007) Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56(3):517–529. doi:10.​1016/​j.​neuron.​2007.​09.​032 CrossRefPubMed
Zurück zum Zitat Roche M, Commons KG, Peoples A, Valentino RJ (2003) Circuitry underlying regulation of the serotonergic system by swim stress. J Neurosci 23(3):970–977. Pii: 23/3/970PubMed Roche M, Commons KG, Peoples A, Valentino RJ (2003) Circuitry underlying regulation of the serotonergic system by swim stress. J Neurosci 23(3):970–977. Pii: 23/3/970PubMed
Zurück zum Zitat Shikanai H, Yoshida T, Konno K, Yamasaki M, Izumi T, Ohmura Y, Watanabe M, Yoshioka M (2012) Distinct neurochemical and functional properties of GAD67-containing 5-HT neurons in the rat dorsal raphe nucleus. J Neurosci 32(41):14415–14426. doi:10.1523/JNEUROSCI.5929-11.2012 CrossRefPubMed Shikanai H, Yoshida T, Konno K, Yamasaki M, Izumi T, Ohmura Y, Watanabe M, Yoshioka M (2012) Distinct neurochemical and functional properties of GAD67-containing 5-HT neurons in the rat dorsal raphe nucleus. J Neurosci 32(41):14415–14426. doi:10.​1523/​JNEUROSCI.​5929-11.​2012 CrossRefPubMed
Zurück zum Zitat Studer R, von Boehmer L, Haenggi T, Schweizer C, Benke D, Rudolph U, Fritschy JM (2006) Alteration of GABAergic synapses and gephyrin clusters in the thalamic reticular nucleus of GABAA receptor alpha3 subunit-null mice. Eur J Neurosci 24(5):1307–1315. doi:10.1111/j.1460-9568.2006.05006.x CrossRefPubMed Studer R, von Boehmer L, Haenggi T, Schweizer C, Benke D, Rudolph U, Fritschy JM (2006) Alteration of GABAergic synapses and gephyrin clusters in the thalamic reticular nucleus of GABAA receptor alpha3 subunit-null mice. Eur J Neurosci 24(5):1307–1315. doi:10.​1111/​j.​1460-9568.​2006.​05006.​x CrossRefPubMed
Zurück zum Zitat Sur C, Wafford KA, Reynolds DS, Hadingham KL, Bromidge F, Macaulay A, Collinson N, O’Meara G, Howell O, Newman R, Myers J, Atack JR, Dawson GR, McKernan RM, Whiting PJ, Rosahl TW (2001) Loss of the major GABA(A) receptor subtype in the brain is not lethal in mice. J Neurosci 21(10):3409–3418 PubMed Sur C, Wafford KA, Reynolds DS, Hadingham KL, Bromidge F, Macaulay A, Collinson N, O’Meara G, Howell O, Newman R, Myers J, Atack JR, Dawson GR, McKernan RM, Whiting PJ, Rosahl TW (2001) Loss of the major GABA(A) receptor subtype in the brain is not lethal in mice. J Neurosci 21(10):3409–3418 PubMed
Zurück zum Zitat Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J-I, Obata K, Kaneko T (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467(1):60–79. doi:10.1002/cne.10905 CrossRefPubMed Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J-I, Obata K, Kaneko T (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467(1):60–79. doi:10.​1002/​cne.​10905 CrossRefPubMed
Zurück zum Zitat Tretter V, Kerschner B, Milenkovic I, Ramsden SL, Ramerstorfer J, Saiepour L, Maric H-M, Moss SJ, Schindelin H, Harvey RJ, Sieghart W, Harvey K (2011) Molecular basis of the γ-aminobutyric acid A receptor α3 subunit interaction with the clustering protein gephyrin. J Biol Chem 286(43):37702–37711. doi:10.1074/jbc.M111.291336 PubMedCentralCrossRefPubMed Tretter V, Kerschner B, Milenkovic I, Ramsden SL, Ramerstorfer J, Saiepour L, Maric H-M, Moss SJ, Schindelin H, Harvey RJ, Sieghart W, Harvey K (2011) Molecular basis of the γ-aminobutyric acid A receptor α3 subunit interaction with the clustering protein gephyrin. J Biol Chem 286(43):37702–37711. doi:10.​1074/​jbc.​M111.​291336 PubMedCentralCrossRefPubMed
Zurück zum Zitat Uchida S, Hara K, Kobayashi A, Otsuki K, Yamagata H, Hobara T, Suzuki T, Miyata N, Watanabe Y (2011) Epigenetic status of Gdnf in the ventral striatum determines susceptibility and adaptation to daily stressful events. Neuron 69(2):359–372. doi:10.1016/j.neuron.2010.12.023 CrossRefPubMed Uchida S, Hara K, Kobayashi A, Otsuki K, Yamagata H, Hobara T, Suzuki T, Miyata N, Watanabe Y (2011) Epigenetic status of Gdnf in the ventral striatum determines susceptibility and adaptation to daily stressful events. Neuron 69(2):359–372. doi:10.​1016/​j.​neuron.​2010.​12.​023 CrossRefPubMed
Zurück zum Zitat Valentino RJ, Liouterman L, Van Bockstaele EJ (2001) Evidence for regional heterogeneity in corticotropin-releasing factor interactions in the dorsal raphe nucleus. J Comp Neurol 435(4):450–463. doi:10.1002/cne.1043 CrossRefPubMed Valentino RJ, Liouterman L, Van Bockstaele EJ (2001) Evidence for regional heterogeneity in corticotropin-releasing factor interactions in the dorsal raphe nucleus. J Comp Neurol 435(4):450–463. doi:10.​1002/​cne.​1043 CrossRefPubMed
Zurück zum Zitat Vithlani M, Hines RM, Zhong P, Terunuma M, Hines DJ, Revilla-Sanchez R, Jurd R, Haydon P, Rios M, Brandon N, Yan Z, Moss SJ (2013) The ability of BDNF to modify neurogenesis and depressive-like behaviors is dependent upon phosphorylation of tyrosine residues 365/367 in the GABA(A)-receptor gamma2 subunit. J Neurosci 33(39):15567–15577. doi:10.1523/JNEUROSCI.1845-13.2013 PubMedCentralCrossRefPubMed Vithlani M, Hines RM, Zhong P, Terunuma M, Hines DJ, Revilla-Sanchez R, Jurd R, Haydon P, Rios M, Brandon N, Yan Z, Moss SJ (2013) The ability of BDNF to modify neurogenesis and depressive-like behaviors is dependent upon phosphorylation of tyrosine residues 365/367 in the GABA(A)-receptor gamma2 subunit. J Neurosci 33(39):15567–15577. doi:10.​1523/​JNEUROSCI.​1845-13.​2013 PubMedCentralCrossRefPubMed
Zurück zum Zitat Waselus M, Valentino RJ, Van Bockstaele EJ (2005) Ultrastructural evidence for a role of γ-aminobutyric acid in mediating the effects of corticotropin-releasing factor on the rat dorsal raphe serotonin system. J Comp Neurol 482(2):155–165CrossRefPubMed Waselus M, Valentino RJ, Van Bockstaele EJ (2005) Ultrastructural evidence for a role of γ-aminobutyric acid in mediating the effects of corticotropin-releasing factor on the rat dorsal raphe serotonin system. J Comp Neurol 482(2):155–165CrossRefPubMed
Zurück zum Zitat Watanabe M, Fukaya M, Sakimura K, Manabe T, Mishina M, Inoue Y (1998) Selective scarcity of NMDA receptor channel subunits in the stratum lucidum (mossy fibre-recipient layer) of the mouse hippocampal CA3 subfield. Eur J Neurosci 10(2):478–487CrossRefPubMed Watanabe M, Fukaya M, Sakimura K, Manabe T, Mishina M, Inoue Y (1998) Selective scarcity of NMDA receptor channel subunits in the stratum lucidum (mossy fibre-recipient layer) of the mouse hippocampal CA3 subfield. Eur J Neurosci 10(2):478–487CrossRefPubMed
Zurück zum Zitat Wieland HA, Luddens H, Seeburg PH (1992) A single histidine in GABAA receptors is essential for benzodiazepine agonist binding. J Biol Chem 267(3):1426–1429PubMed Wieland HA, Luddens H, Seeburg PH (1992) A single histidine in GABAA receptors is essential for benzodiazepine agonist binding. J Biol Chem 267(3):1426–1429PubMed
Zurück zum Zitat Wisden W, Laurie DJ, Monyer H, Seeburg PH (1992) The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J Neurosci 12(3):1040–1062PubMed Wisden W, Laurie DJ, Monyer H, Seeburg PH (1992) The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J Neurosci 12(3):1040–1062PubMed
Zurück zum Zitat Wood SK, Zhang X-Y, Reyes BAS, Lee CS, Van Bockstaele EJ, Valentino RJ (2013) Cellular adaptations of dorsal raphe serotonin neurons associated with the development of active coping in response to social stress. Biol Psychiatry 73(11):1087–1094PubMedCentralCrossRefPubMed Wood SK, Zhang X-Y, Reyes BAS, Lee CS, Van Bockstaele EJ, Valentino RJ (2013) Cellular adaptations of dorsal raphe serotonin neurons associated with the development of active coping in response to social stress. Biol Psychiatry 73(11):1087–1094PubMedCentralCrossRefPubMed
Zurück zum Zitat Xu ZQ, Hokfelt T (1997) Expression of galanin and nitric oxide synthase in subpopulations of serotonin neurons of the rat dorsal raphe nucleus. J Chem Neuroanat 13(3):169–187CrossRefPubMed Xu ZQ, Hokfelt T (1997) Expression of galanin and nitric oxide synthase in subpopulations of serotonin neurons of the rat dorsal raphe nucleus. J Chem Neuroanat 13(3):169–187CrossRefPubMed
Zurück zum Zitat Yee BK, Keist R, von Boehmer L, Studer R, Benke D, Hagenbuch N, Dong Y, Malenka RC, Fritschy JM, Bluethmann H, Feldon J, Mohler H, Rudolph U (2005) A schizophrenia-related sensorimotor deficit links alpha 3-containing GABAA receptors to a dopamine hyperfunction. Proc Natl Acad Sci USA 102(47):17154–17159. doi:10.1073/pnas.0508752102 PubMedCentralCrossRefPubMed Yee BK, Keist R, von Boehmer L, Studer R, Benke D, Hagenbuch N, Dong Y, Malenka RC, Fritschy JM, Bluethmann H, Feldon J, Mohler H, Rudolph U (2005) A schizophrenia-related sensorimotor deficit links alpha 3-containing GABAA receptors to a dopamine hyperfunction. Proc Natl Acad Sci USA 102(47):17154–17159. doi:10.​1073/​pnas.​0508752102 PubMedCentralCrossRefPubMed
Metadaten
Titel
Localisation and stress-induced plasticity of GABAA receptor subunits within the cellular networks of the mouse dorsal raphe nucleus
verfasst von
Nicole L. Corteen
Jessica A. Carter
Uwe Rudolph
Delia Belelli
Jeremy J. Lambert
Jerome D. Swinny
Publikationsdatum
01.09.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 5/2015
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-014-0824-7

Weitere Artikel der Ausgabe 5/2015

Brain Structure and Function 5/2015 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Neu im Fachgebiet Neurologie

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.