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European Archives of Psychiatry and Clinical Neuroscience

Published in:

01-10-2014 | Original Paper

Impact of adolescent GluA1 AMPA receptor ablation in forebrain excitatory neurons on behavioural correlates of mood disorders

Authors: Miriam A. Vogt, Hasan Elkin, Natascha Pfeiffer, Rolf Sprengel, Peter Gass, Dragos Inta

Published in: European Archives of Psychiatry and Clinical Neuroscience | Issue 7/2014

Abstract

Glutamatergic dysfunctions have recently been postulated to play a considerable role in mood disorders. However, molecular mechanisms underlying these effects have been poorly deciphered. Previous work demonstrated the contribution of GluA1-containing AMPA receptors (AMPAR) to a depression-like and anxiety-like phenotype. Here we investigated the effect of temporally and spatially restricted gene manipulation of GluA1 on behavioural correlates of mood disorders in mice. Here we show that tamoxifen-induced GluA1 deletion restricted to forebrain glutamatergic neurons of post-adolescent mice does not induce depression- and anxiety-like changes. This differs from the phenotype of mice with global AMPAR deletion suggesting that for mood regulation AMPAR may be particularly important on inhibitory interneurons or already early in development.

Sanacora G, Treccani G, Popoli M (2012) Towards a glutamate hypothesis of depression: an emerging frontier of neuropsychopharmacology for mood disorders. Neuropharmacology 62:63–77. doi:10.1016/j.neuropharm.2011.07.036 PubMedCrossRefPubMedCentral

Engin E, Treit D, Dickson CT (2009) Anxiolytic- and antidepressant-like properties of ketamine in behavioural and neurophysiological animal models. Neuroscience 161:359–369. doi:10.1016/j.neuroscience.2009.03.038 PubMedCrossRef

Zarate CA Jr, Singh JB, Carlson PJ, Brutsche NE, Ameli R, Luckenbaugh DA, Charney DS, Manji HK (2006) A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression. Arch Gen Psychiatry 63:856–864. doi:10.1001/archpsyc.63.8.856 PubMedCrossRef

Inta D, Trusel M, Riva MA, Sprengel R, Gass P (2009) Differential c-Fos induction by different NMDA receptor antagonists with antidepressant efficacy: potential clinical implications. Int J Neuropsychopharmacol 12:1133–1136. doi:10.1017/S1461145709990319 PubMedCrossRef

Inta D, Filipovic D, Lima-Ojeda JM, Dormann C, Pfeiffer N, Gasparini F, Gass P (2012) The mGlu5 receptor antagonist MPEP activates specific stress-related brain regions and lacks neurotoxic effects of the NMDA receptor antagonist MK-801: significance for the use as anxiolytic/antidepressant drug. Neuropharmacology 62:2034–2039. doi:10.1016/j.neuropharm.2011.12.035 PubMedCrossRef

Lima-Ojeda JM, Vogt MA, Pfeiffer N, Dormann C, Köhr G, Sprengel R, Gass P, Inta D (2013) Pharmacological blockade of GluN2B-containing NMDA receptors induces antidepressant-like effects lacking psychotomimetic action and neurotoxicity in the perinatal and adult rodent brain. Prog Neuropsychopharmacol Biol Psychiatry 45:28–33. doi:10.1016/j.pnpbp.2013.04.017 PubMedCrossRef

McAllister AK (2007) Dynamic aspects of CNS synapse formation. Annu Rev Neurosci 30:425–450. doi:10.1146/annurev.neuro.29.051605.112830 PubMedCrossRefPubMedCentral

Machado-Vieira R, Manji HK, Zarate CA (2009) The role of the tripartite glutamatergic synapse in the pathophysiology and therapeutics of mood disorders. Neuroscientist 15:525–539. doi:10.1177/1073858409336093 PubMedCrossRefPubMedCentral

Kallarackal AJ, Kvarta MD, Cammarata E, Jaberi L, Cai X, Bailey AM, Thompson SM (2013) Chronic stress induces a selective decrease in AMPA receptor-mediated synaptic excitation at hippocampal temporoammonic-CA1 synapses. J Neurosci 33:15669–15674. doi:10.1523/JNEUROSCI.2588-13.2013 PubMedCrossRefPubMedCentral

10.

Wiedholz LM, Owens WA, Horton RE, Feyder M, Karlsson RM, Hefner K, Sprengel R, Celikel T, Daws LC, Holmes A (2008) Mice lacking the AMPA GluR1 receptor exhibit striatal hyperdopaminergia and ‘schizophrenia-related’ behaviors. Mol Psychiatry 13:631–640. doi:10.1038/sj.mp.4002056 PubMedCrossRef

11.

Chourbaji S, Vogt MA, Fumagalli F, Sohr R, Frasca A, Brandwein C, Hortnagl H, Riva MA, Sprengel R, Gass P (2008) AMPA receptor subunit 1 (GluR-A) knockout mice model the glutamate hypothesis of depression. FASEB J 22:3129–3134. doi:10.1096/fj.08-106450 PubMedCrossRef

12.

Fitzgerald PJ, Barkus C, Feyder M, Wiedholz LM, Chen YC, Karlsson RM, Machado-Vieira R, Graybeal C, Sharp T, Zarate C, Harvey-White J, Du J, Sprengel R, Gass P, Bannerman D, Holmes A (2010) Does gene deletion of AMPA GluA1 phenocopy features of schizoaffective disorder? Neurobiol Dis 40:608–621. doi:10.1016/j.nbd.2010.08.005 PubMedCrossRefPubMedCentral

13.

Mathew SJ, Manji HK, Charney DS (2008) Novel drugs and therapeutic targets for severe mood disorders. Neuropsychopharmacology 33:2080–2092. doi:10.1038/sj.npp.1301652 PubMedCrossRef

14.

Havekes R, Abel T (2009) Genetic dissection of neural circuits and behaviour in Mus musculus. Adv Genet 65:1–38. doi:10.1016/S0065-2660(09)65001-X PubMedCrossRefPubMedCentral

15.

Urani A, Chourbaji S, Gass P (2005) Mutant mouse models of depression: candidate genes and current mouse lines. Neurosci Biobehav Rev 29:805–828. doi:10.1016/j.pbb.2011.02.019 PubMedCrossRef

16.

Inta D, Vogt MA, Elkin H, Weber T, Lima-Ojeda JM, Schneider M, Luoni A, Riva MA, Gertz K, Hellmann-Regen J, Kronenberg G, Meyer-Lindenberg A, Sprengel R, Gass P (2014) Phenotype of mice with inducible ablation of GluA1 AMPA receptors during late adolescence: relevance for mental disorders. Hippocampus 24:424–435. doi:10.1002/hipo.22236 PubMedCrossRef

17.

Chourbaji S, Pfeiffer N, Dormann C, Brandwein C, Fradley R, Sheardown M, Gass P (2010) The suitability of 129SvEv mice for studying depressive-like behaviour: both males and females develop learned helplessness. Behav Brain Res 211:105–110. doi:10.1016/j.bbr.2010.03.019 PubMedCrossRef

18.

Lazic SE, Essioux L (2013) Improving basic and translational science by accounting for litter-to-litter variation in animal models. BMC Neurosci 14:37. doi:10.1186/1471-2202-14-37 PubMedCrossRefPubMedCentral

19.

Chourbaji S, Brandwein C, Vogt MA, Dormann C, Hellweg R, Gass P (2008) Nature vs. nurture: can enrichment rescue the behavioural phenotype of BDNF heterozygous mice? Behav Brain Res 192:254–258. doi:10.1016/j.bbr.2008.04.015 PubMedCrossRef

20.

Chourbaji S, Zacher C, Sanchis-Segura C, Dormann C, Vollmayr B, Gass P (2005) Learned helplessness: validity and reliability of depressive-like states in mice. Brain Res Brain Res Protoc 16:70–78. doi:10.1016/j.brainresprot.2005.09.002 PubMedCrossRef

21.

Vogt MA, Chourbaji S, Brandwein C, Dormann C, Sprengel R, Gass P (2008) Suitability of tamoxifen-induced mutagenesis for behavioral phenotyping. Exp Neurol 211:25–33. doi:10.1016/j.expneurol.2007.12.012 PubMedCrossRef

22.

Fuss J, Ben Abdallah NM, Hensley FW, Weber KJ, Hellweg R, Gass P (2010) Deletion of running-induced hippocampal neurogenesis by irradiation prevents development of an anxious phenotype in mice. PLoS One 5. doi:10.1371/journal.pone.0012769

23.

Inta D, Vogt MA, Luoni A, Filipovic D, Lima-Ojeda JM, Pfeiffer N, Gasparini F, Riva MA, Gass P (2013) Significant increase in anxiety during aging in mGlu5 receptor knockout mice. Behav Brain Res 241C:27–31. doi:10.1016/j.bbr.2012.11.042 CrossRef

24.

Bannerman DM, Deacon RM, Brady S, Bruce A, Sprengel R, Seeburg PH, Rawlins JN (2004) A comparison of GluR-A-deficient and wild-type mice on a test battery assessing sensorimotor, affective, and cognitive behaviors. Behav Neurosci 118:643–647. doi:10.1037/0735-7044.118.3.643 PubMedCrossRef

25.

Freund TF (2003) Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci 26:489–495. doi:10.1016/S0166-2236(03)00227-3 PubMedCrossRef

26.

Croarkin PE, Levinson AJ, Daskalakis ZJ (2011) Evidence for GABAergic inhibitory deficits in major depressive disorder. Neurosci Biobehav Rev 35:818–825. doi:10.1016/j.neubiorev.2010.10.002 PubMedCrossRef

27.

Filipović D, Zlatković J, Gass P, Inta D (2013) The differential effects of acute vs. chronic stress and their combination on hippocampal parvalbumin and inducible heat shock protein 70 expression. Neuroscience 236:47–54. doi:10.1016/j.neuroscience.2013.01.033 PubMedCrossRef

28.

Hu W, Zhang M, Czéh B, Flügge G, Zhang W (2010) Stress impairs GABAergic network function in the hippocampus by activating nongenomic glucocorticoid receptors and affecting the integrity of the parvalbumin-expressing neuronal network. Neuropsychopharmacology 35:1693–1707. doi:10.1038/npp.2010.31 PubMedPubMedCentral

29.

Leranth C, Szeidemann Z, Hsu M, Buzsaki G (1996) AMPA receptors in the rat and primate hippocampus: a possible absence of GluR2/3 subunits in most interneurons. Neuroscience 70:631–652. doi:10.1016/S0306-4522(96)83003-X PubMedCrossRef

Title: Impact of adolescent GluA1 AMPA receptor ablation in forebrain excitatory neurons on behavioural correlates of mood disorders
Authors: Miriam A. Vogt
Hasan Elkin
Natascha Pfeiffer
Rolf Sprengel
Peter Gass
Dragos Inta
Publication date: 01-10-2014
Publisher: Springer Berlin Heidelberg
Published in: European Archives of Psychiatry and Clinical Neuroscience / Issue 7/2014
Print ISSN: 0940-1334
Electronic ISSN: 1433-8491
DOI: https://doi.org/10.1007/s00406-014-0509-5

At a glance: The STEP trials

Springer Medicine

Impact of adolescent GluA1 AMPA receptor ablation in forebrain excitatory neurons on behavioural correlates of mood disorders

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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