Phenotype of mice with inducible ablation of GluA1 AMPA receptors during late adolescence: Relevance for mental disorders

Hippocampus

Volumn 24, Issue 4, 2014, Pages 424-435

  Inta, Dragos ^a   Vogt, Miriam A ^a   Elkin, Hasan ^a   Weber, Tillmann ^b   Lima Ojeda, Juan M ^a   Schneider, Miriam ^a   Luoni, Alessia ^c   Riva, Marco A ^c   Gertz, Karen ^d   Hellmann Regen, Julian ^d   Kronenberg, Golo ^d   Meyer Lindenberg, Andreas ^a   Sprengel, Rolf ^e   Gass, Peter ^a  

^a CENTRAL INSTITUTE OF MENTAL HEALTH   (Germany)

^b MEDICAL FACULTY MANNHEIM HEIDELBERG UNIVERSITY   (Germany)

^c UNIVERSITY OF MILAN   (Italy)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

Author keywords

Cognitive dysfunction; Excitatory neurons; GluA2; Neuropsychiatric disorders; Pharmacogenetics

Indexed keywords

AMPA RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CRE RECOMBINASE; DOPAMINE; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 1; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 2;

ACOUSTIC REFLEX; ADOLESCENCE; ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BRAIN NERVE CELL; COGNITIVE DEFECT; CONTROLLED STUDY; DOPAMINE BRAIN LEVEL; EXPERIMENTAL BEHAVIORAL TEST; EXPERIMENTAL HYPERACTIVITY; EXPERIMENTAL SOCIAL BEHAVIOR TEST; EXPLORATORY BEHAVIOR TEST; GENE DELETION; GENE EXPRESSION; GENETIC MANIPULATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LOXP SITE; MALE; MEMORY DISORDER; MENTAL DISEASE; NONHUMAN; OPEN FIELD TEST; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PUZZLE BOX TEST; RADIAL ARM MAZE TEST; RAT; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR GENE; SENSORY GATING; SOCIABILITY TEST; SOCIAL BEHAVIOR; STARTLE REFLEX; WORKING MEMORY; ANIMAL; CORPUS STRIATUM; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIPPOCAMPUS; MAZE TEST; METABOLISM; MOTOR ACTIVITY; MOUSE; NERVE CELL; PHYSIOLOGY; SHORT TERM MEMORY; TRANSGENIC MOUSE;

ANIMALS; COGNITION DISORDERS; CORPUS STRIATUM; DOPAMINE; HIPPOCAMPUS; MAZE LEARNING; MEMORY, SHORT-TERM; MENTAL DISORDERS; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; NEURONS; PHENOTYPE; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SENSORY GATING; SOCIAL BEHAVIOR;

EID: 84904243262     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22236     Document Type: Article

References (44)

1. 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.
2. Ben Abdallah NM, Fuss J, Trusel M, Galsworthy MJ, Bobsin K, Colacicco G, Deacon RM, Riva MA, Kellendonk C, Sprengel R, Lipp HP, Gass P. 2011. The puzzle box as a simple and efficient behavioral test for exploring impairments of general cognition and executive functions in mouse models of schizophrenia. Exp Neurol 227:42-52.
3. Bottiger BW, Teschendorf P, Krumnikl JJ, Vogel P, Galmbacher R, Schmitz B, Motsch J, Martin E, Gass P. 1999. Global cerebral ischemia due to cardiocirculatory arrest in mice causes neuronal degeneration and early induction of transcription factor genes in the hippocampus. Brain Res Mol Brain Res 65:135-142.
4. Braff DL, Swerdlow NR, Geyer MA. 1999. Symptom correlates of prepulse inhibition deficits in male schizophrenic patients. Am J Psychiatry 156:596-602.
5. Chourbaji S, Hellweg R, Brandis D, Zorner B, Zacher C, Lang UE, Henn FA, Hortnagl H, Gass P. 2004. Mice with reduced brain-derived neurotrophic factor expression show decreased choline acetyltransferase activity, but regular brain monoamine levels and unaltered emotional behavior. Brain Res Mol Brain Res 121:28-36.
6. 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.
7. Corti C, Xuereb JH, Crepaldi L, Corsi M, Michielin F, Ferraguti F. 2011. Altered levels of glutamatergic receptors and Na+/K+ ATPase-alpha1 in the prefrontal cortex of subjects with schizophrenia. Schizophr Res 128:7-14.
8. Dubreuil D, Tixier C, Dutrieux G, Edeline JM. 2003. Does the radial arm maze necessarily test spatial memory? Neurobiol Learn Mem 79:109-117.
9. Dubroqua S, Serrano L, Boison D, Feldon J, Gargiulo PA, Yee BK. 2012. Intact working memory in the absence of forebrain neuronal glycine transporter 1. Behav Brain Res 230:208-214.
10. Erdmann G, Schutz G, Berger S. 2007. Inducible gene inactivation in neurons of the adult mouse forebrain. BMC Neurosci 8:63.
11. 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.
12. Fuchs EC, Zivkovic AR, Cunningham MO, Middleton S, Lebeau FE, Bannerman DM, Rozov A, Whittington MA, Traub RD, Rawlins JN, Monyer H. 2007. Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior. Neuron 53:591-604.
13. Fumagalli F, Caffino L, Vogt MA, Frasca A, Racagni G, Sprengel R, Gass P, Riva MA. 2010. AMPA GluR-A receptor subunit mediates hippocampal responsiveness in mice exposed to stress. Hippocampus 21:1028-1035.
14. 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:e12769.
15. Geiger JR, Melcher T, Koh DS, Sakmann B, Seeburg PH, Jonas P, Monyer H. 1995. Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15:193-204.
16. Geyer MA. 2006. Are cross-species measures of sensorimotor gating useful for the discovery of procognitive cotreatments for schizophrenia? Dialogues Clin Neurosci 2006;8:9-16.
17. Hammond JC, McCullumsmith RE, Funk AJ, Haroutunian V, Meador-Woodruff JH. 2010. Evidence for abnormal forward trafficking of AMPA receptors in frontal cortex of elderly patients with schizophrenia. Neuropsychopharmacology 35:2110-2119.
18. Havekes R, Abel T. 2009. Genetic dissection of neural circuits and behavior in Mus musculus. Adv Genet 65:1-38.
19. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R. 2000. Driving AMPA receptors into synapses by LTP and CaMKII: Requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267.
20. Hayashi-Takagi A, Takaki M, Graziane N, Seshadri S, Murdoch H, Dunlop AJ, Makino Y, Seshadri AJ, Ishizuka K, Srivastava DP, Xie Z, Baraban JM, Houslay MD, Tomoda T, Brandon NJ, Kamiya A, Yan Z, Penzes P, Sawa A. 2010. Disrupted-in-schizophrenia 1 (DISC1) regulates spines of the glutamate synapse via Rac1. Nat Neurosci 13:327-332.
21. Hellweg R, Zueger M, Fink K, Hortnagl H, Gass P. 2007. Olfactory bulbectomy in mice leads to increased BDNF levels and decreased serotonin turnover in depression-related brain areas. Neurobiol Dis 25:1-7.
22. Hermes G, Li N, Duman C, Duman R. 2010. Post-weaning chronic social isolation produces profound behavioral dysregulation with decreases in prefrontal cortex synaptic-associated protein expression in female rats. Physiol Behav 104:354-359.
23. Inta D, Monyer H, Sprengel R, Meyer-Lindenberg A, Gass P. 2009. Mice with genetically altered glutamate receptors as models of schizophrenia: A comprehensive review. Neurosci Biobehav Rev 34:285-294.
24. Inta D, Vogt MA, Lima-Ojeda JM, Pfeiffer N, Schneider M, Gass P. 2011. Lack of long-term behavioral alterations after early postnatal treatment with tropisetron: Implications for developmental psychobiology. Pharmacol Biochem Behav 99:35-41.
25. Inta D, Vogt MA, Perreau-Lenz S, Schneider M, Pfeiffer N, Wojcik SM, Spanagel R, Gass P. 2012. Sensorimotor gating, working and social memory deficits in mice with reduced expression of the vesicular glutamate transporter VGLUT1. Behav Brain Res 228:328-332.
26. Inta D, Vogt MA, Pfeiffer N, Kohr G, Gass P. 2013. Dichotomy in the anxiolytic versus antidepressant effect of C-terminal truncation of the GluN2A subunit of NMDA receptors. Behav Brain Res 247C:227-231.
27. Kaidanovich-Beilin O, Lipina T, Vukobradovic I, Roder J, Woodgett JR. 2011. Assessment of social interaction behaviors. J Vis Exp 48:e2473.
28. Kopec CD, Real E, Kessels HW, Malinow R. 2007. GluR1 links structural and functional plasticity at excitatory synapses. J Neurosci 27:13706-13718.
29. Kwon OB, Longart M, Vullhorst D, Hoffman DA, Buonanno A. 2005. Neuregulin-1 reverses long-term potentiation at CA1 hippocampal synapses. J Neurosci 25:9378-9383.
30. 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.
31. Lorenc-Koci E, Rommelspacher H, Schulze G, Wernicke C, Kuter K, Smialowska M, Wieronska J, Zieba B, Ossowska K. 2006. Parkinson's disease-like syndrome in rats induced by 2, 9-dimethyl-beta-carbolinium ion, a beta-carboline occurring in the human brain. Behav Pharmacol 17:463-473.
32. Meador-Woodruff JH, Healy DJ. 2000. Glutamate receptor expression in schizophrenic brain. Brain Res Brain Res Rev 31:288-294.
33. Mohn AR Gainetdinov RR, Caron MG, Koller BH. 1999. Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Cell 98:427-436.
34. Rogers SW, Hughes TE, Hollmann M, Gasic GP, Deneris ES, Heinemann S. 1991. The characterization and localization of the glutamate receptor subunit GluR1 in the rat brain. J Neurosci 11:2713-2724.
35. Shi S, Hayashi Y, Esteban JA, Malinow R. 2001. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105:331-343.
36. Sik A, Hajos N, Gulacsi A, Mody I, Freund TF. 1998. The absence of a major Ca2+ signaling pathway in GABAergic neurons of the hippocampus. Proc Natl Acad Sci USA 95:3245-3250.
37. Sprengel R, Suchanek B, Amico C, Brusa R, Burnashev N, Rozov A, Hvalby O, Jensen V, Paulsen O, Andersen P, Kim JJ, Thompson RF, Sun W, Webster LC, Grant SG, Eilers J, Konnerth A, Li J, McNamara JO, Seeburg PH. 1998. Importance of the intracellular domain of NR2 subunits for NMDA receptor function in vivo. Cell 92:279-289.
38. van den Buuse M. 2010. Modeling the positive symptoms of schizophrenia in genetically modified mice: Pharmacology and methodology aspects. Schizophr Bull 36:246-270.
39. Vekovischeva OY, Aitta-Aho T, Echenko O, Kankaanpaa A, Seppala T, Honkanen A, Sprengel R, Korpi ER. 2004. Reduced aggression in AMPA-type glutamate receptor GluR-A subunit-deficient mice. Genes Brain Behav 3:253-265.
40. 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.
41. Wefers B, Hitz C, Holter SM, Trumbach D, Hansen J, Weber P, Putz B, Deussing JM, de Angelis MH, Roenneberg T, Zheng F, Alzheimer C, Silva A, Wurst W, Kuhn R. 2012. MAPK signaling determines anxiety in the juvenile mouse brain but depression-like behavior in adults. PLoS One 7:e35035.
42. Wenthold RJ, Petralia RS, Blahos J II, Niedzielski AS. 1996. Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J Neurosci 16:1982-1989.
43. 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.
44. Zamanillo D, Sprengel R, Hvalby O, Jensen V, Burnashev N, Rozov A, Kaiser KM, Koster HJ, Borchardt T, Worley P, Lubke J, Frotscher M, Kelly PH, Sommer B, Andersen P, Seeburg PH, Sakmann B. 1999. Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284:1805-1811.