GluA1 and its PDZ-interaction: A role in experience-dependent behavioral plasticity in the forced swim test

Neurobiology of Disease

Volumn 52, Issue , 2013, Pages 160-167

  Freudenberg, Florian ^a,b   Marx, Verena ^a,b,d   Mack, Volker ^b,e   Layer, Liliana E ^b,f   Klugmann, Matthias ^c   Seeburg, Peter H ^b   Sprengel, Rolf ^b   Celikel, Tansu ^a,d  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d RADBOUD UNIVERSITY   (Netherlands)

^e EVOTEC AG   (Germany)

^f PromoCellGmbH ^*  (Germany)

Author keywords

AMPA receptors; Behavioral despair; Depression; GluR A; GluR1; Gria1; Mouse; PDZ; Porsolt swim test

Indexed keywords

AMPA RECEPTOR; CELL PROTEIN; GLUA1 PROTEIN; LEUCINE; PDZ PROTEIN; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BINDING AFFINITY; BINDING SITE; BRAIN NERVE CELL; BRAIN REGION; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DEPRESSION; DISEASE ACTIVITY; FEMALE; FORCED SWIMMING TEST; FOREBRAIN; HIPPOCAMPUS; MALE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

ANIMALS; BEHAVIOR, ANIMAL; HELPLESSNESS, LEARNED; HIPPOCAMPUS; LEARNING; MICE; MICE, INBRED C57BL; NEURONAL PLASTICITY; NEURONS; PDZ DOMAINS; PROMOTER REGIONS, GENETIC; RECEPTORS, AMPA; SWIMMING;

EID: 84873567426     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.12.003     Document Type: Article

References (86)

1. Airan R.D., Meltzer L.A., Roy M., Gong Y., Chen H., Deisseroth K. High-speed imaging reveals neurophysiological links to behavior in an animal model of depression. Science 2007, 317:819-823.
2. Andrásfalvy B.K., Smith M.A., Borchardt T., Sprengel R., Magee J.C. Impaired regulation of synaptic strength in hippocampal neurons from GluR1-deficient mice. J. Physiol. 2003, 552:35-45.
3. Auer D.P., Pütz B., Kraft E., Lipinski B., Schill J., Holsboer F. Reduced glutamate in the anterior cingulate cortex in depression: an in vivo proton magnetic resonance spectroscopy study. Biol. Psychiatry 2000, 47:305-313.
4. Autry A.E., Adachi M., Nosyreva E., Na E.S., Los M.F., Cheng P., et al. NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 2011, 475:91-95.
5. Bannerman D.M., Deacon R.M.J., Brady S., Bruce A., Sprengel R., Seeburg P.H., et al. A comparison of GluR-A-deficient and wild-type mice on a test battery assessing sensorimotor, affective, and cognitive behaviors. Behav. Neurosci. 2004, 118:643-647.
6. Barbon A., Caracciolo L., Orlandi C., Musazzi L., Mallei A., La Via L., et al. Chronic antidepressant treatments induce a time-dependent up-regulation of AMPA receptor subunit protein levels. Neurochem. Int. 2011, 59:896-905.
7. Beneyto M., Kristiansen L.V., Oni-Orisan A., McCullumsmith R.E., Meador-Woodruff J.H. Abnormal glutamate receptor expression in the medial temporal lobe in schizophrenia and mood disorders. Neuropsychopharmacology 2007, 32:1888-1902.
8. Berman R.M., Cappiello A., Anand A., Oren D.A., Heninger G.R., Charney D.S., et al. Antidepressant effects of ketamine in depressed patients. Biol. Psychiatry 2000, 47:351-354.
9. Berton O., Nestler E.J. New approaches to antidepressant drug discovery: beyond monoamines. Nat. Rev. Neurosci. 2006, 7:137-151.
10. Bessa J.M., Ferreira D., Melo I., Marques F., Cerqueira J.J., Palha J.A., et al. The mood-improving actions of antidepressants do not depend on neurogenesis but are associated with neuronal remodeling. Mol. Psychiatry 2009, 14:764-773. (739).
11. Binesh N., Kumar A., Hwang S., Mintz J., Thomas M.A. Neurochemistry of late-life major depression: a pilot two-dimensional MR spectroscopic study. J. Magn. Reson. Imaging: JMRI 2004, 20:1039-1045.
12. Cai C., Coleman S.K., Niemi K., Keinänen K. Selective binding of synapse-associated protein 97 to GluR-A alpha-amino-5-hydroxy-3-methyl-4-isoxazole propionate receptor subunit is determined by a novel sequence motif. J. Biol. Chem. 2002, 277:31484-31490.
13. Celikel T., Marx V., Freudenberg F., Zivkovic A., Resnik E., Hasan M.T., et al. Select overexpression of homer1a in dorsal hippocampus impairs spatial working memory. Front. Neurosci. 2007, 1:97-110.
14. Chourbaji S., Vogt M.A., Fumagalli F., Sohr R., Frasca A., Brandwein C., et al. AMPA receptor subunit 1 (GluR-A) knockout mice model the glutamate hypothesis of depression. FASEB J. 2008, 22:3129-3134.
15. Cryan J.F., Mombereau C. In search of a depressed mouse: utility of models for studying depression-related behavior in genetically modified mice. Mol. Psychiatry 2004, 9:326-357.
16. Dachtler J., Fox K.D., Good M.A. Gender specific requirement of GluR1 receptors in contextual conditioning but not spatial learning. Neurobiol. Learn. Mem. 2011, 96:461-467.
17. Dalla C., Pitychoutis P., Kokras N. Sex Differences in Response to Stress and Expression of Depressive-Like Behaviours in the Rat. Current Topics in Behavioral Neurosciences 2011, 8:97-118. J. Neill, J. Kulkarni (Eds.).
18. Duman R.S., Voleti B. Signaling pathways underlying the pathophysiology and treatment of depression: novel mechanisms for rapid-acting agents. Trends Neurosci. 2012, 35:47-56.
19. Durand C.M., Betancur C., Boeckers T.M., Bockmann J., Chaste P., Fauchereau F., et al. Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nat. Genet. 2007, 39:25-27.
20. Durand C.M., Perroy J., Loll F., Perrais D., Fagni L., Bourgeron T., et al. SHANK3 mutations identified in autism lead to modification of dendritic spine morphology via an actin-dependent mechanism. Mol. Psychiatry 2012, 17:71-84.
21. Duric V., Banasr M., Stockmeier C.A., Simen A.A., Newton S.S., Overholser J.C., et al. Altered expression of synapse and glutamate related genes in post-mortem hippocampus of depressed subjects. Int. J. Neuropsychopharmacol. 2012, i:1-14.
22. Ehlers M.D., Heine M., Groc L., Lee M.-C., Choquet D. Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity. Neuron 2007, 54:447-460.
23. Farley S., Apazoglou K., Witkin J.M., Giros B., Tzavara E.T. Antidepressant-like effects of an AMPA receptor potentiator under a chronic mild stress paradigm. Int. J. Neuropsychopharmacol. 2010, 1-12.
24. Fitzgerald P.J., Barkus C., Feyder M., Wiedholz L.M., Chen Y.-C., Karlsson R.-M., et al. Does gene deletion of AMPA GluA1 phenocopy features of schizoaffective disorder?. Neurobiol. Dis. 2010, 40:608-621.
25. Frey M.C., Sprengel R., Nevian T. Activity pattern-dependent long-term potentiation in neocortex and hippocampus of GluA1 (GluR-A) subunit-deficient mice. J. Neurosci. 2009, 29:5587-5596.
26. Gauthier J., Champagne N., Lafrenière R.G., Xiong L., Spiegelman D., Brustein E., et al. De novo mutations in the gene encoding the synaptic scaffolding protein SHANK3 in patients ascertained for schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:7863-7868.
27. Gibbons A.S., Brooks L., Scarr E., Dean B. AMPA receptor expression is increased post-mortem samples of the anterior cingulate from subjects with major depressive disorder. J. Affect. Disord. 2012, 136:1232-1237.
28. Gould T.D., O'Donnell K.C., Dow E.R., Du J., Chen G., Manji H.K. Involvement of AMPA receptors in the antidepressant-like effects of lithium in the mouse tail suspension test and forced swim test. Neuropharmacology 2008, 54:577-587.
29. Hajszan T., Dow A., Warner-Schmidt J.L., Szigeti-Buck K., Sallam N.L., Parducz A., et al. Remodeling of hippocampal spine synapses in the rat learned helplessness model of depression. Biol. Psychiatry 2009, 65:392-400.
30. Hasler G., van der Veen J.W., Tumonis T., Meyers N., Shen J., Drevets W.C. Reduced prefrontal glutamate/glutamine and gamma-aminobutyric acid levels in major depression determined using proton magnetic resonance spectroscopy. Arch. Gen. Psychiatry 2007, 64:193-200.
31. Hayashi Y., Shi S.H., Esteban J.A., Piccini A., Poncer J.C., Malinow R. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 2000, 287:2262.
32. Hoffman D.A., Sprengel R., Sakmann B. Molecular dissection of hippocampal theta-burst pairing potentiation. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:7740-7745.
33. Humeau Y., Reisel D., Johnson A.W., Borchardt T., Jensen V., Gebhardt C., et al. A pathway-specific function for different AMPA receptor subunits in amygdala long-term potentiation and fear conditioning. J. Neurosci. Off. J. Soc. Neurosci. 2007, 27:10947-10956.
34. Jensen V., Kaiser K.M.M., Borchardt T., Adelmann G., Rozov A., Burnashev N., et al. A juvenile form of postsynaptic hippocampal long-term potentiation in mice deficient for the AMPA receptor subunit GluR-A. J. Physiol. 2003, 553:843-856.
35. Jernigan C.S., Goswami D.B., Austin M.C., Iyo A.H., Chandran A., Stockmeier C.A., et al. The mTOR signaling pathway in the prefrontal cortex is compromised in major depressive disorder. Prog. Neuropsychopharmacol. Biol. Psychiatry 2011, 35:1774-1779.
36. Kim C.-H., Takamiya K., Petralia R.S., Sattler R., Yu S., Zhou W., et al. Persistent hippocampal CA1 LTP in mice lacking the C-terminal PDZ ligand of GluR1. Nat. Neurosci. 2005, 8:985-987.
37. Koike H., Iijima M., Chaki S. Involvement of AMPA receptor in both the rapid and sustained antidepressant-like effects of ketamine in animal models of depression. Behav. Brain Res. 2011, 224:107-111.
38. Krishnan V., Nestler E.J. Animal models of depression: molecular perspectives. Mol. Func. Model. Neuropsychiatr. 2011, 121-147.
39. Leonard A.S., Davare M.A., Horne M., Garner C.C., Hell J.W. SAP97 is associated with the α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit. J. Biol. Chem. 1998, 273:19518.
40. Li X., Tizzano J.P., Griffey K., Clay M., Lindstrom T., Skolnick P. Antidepressant-like actions of an AMPA receptor potentiator (LY392098). Neuropharmacology 2001, 40:1028-1033.
41. Li N., Lee B., Liu R.-J., Banasr M., Dwyer J.M., Iwata M., et al. mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science 2010, 329:959-964.
42. Lissin D.V., Gomperts S.N., Carroll R.C., Christine C.W., Kalman D., Kitamura M., et al. Activity differentially regulates the surface expression of synaptic AMPA and NMDA glutamate receptors. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:7097-7102.
43. Lu W., Shi Y., Jackson A.C., Bjorgan K., During M.J., Sprengel R., et al. Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 2009, 62:254-268.
44. Mack V., Burnashev N., Kaiser K.M., Rozov A., Jensen V., Hvalby O., et al. Conditional restoration of hippocampal synaptic potentiation in Glur-A-deficient mice. Science 2001, 292:2501-2504.
45. Maeng S., Zarate C.A., Du J., Schloesser R.J., McCammon J., Chen G., et al. Cellular mechanisms underlying the antidepressant effects of ketamine: role of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors. Biol. Psychiatry 2008, 63:349-352.
46. Martínez-Turrillas R., Frechilla D., Del Río J. Chronic antidepressant treatment increases the membrane expression of AMPA receptors in rat hippocampus. Neuropharmacology 2002, 43:1230-1237.
47. Martínez-Turrillas R., Del Río J., Frechilla D. Sequential changes in BDNF mRNA expression and synaptic levels of AMPA receptor subunits in rat hippocampus after chronic antidepressant treatment. Neuropharmacology 2005, 49:1178-1188.
48. Mayford M., Bach M.E., Huang Y.-Y., Wang L., Robert D., Kandel E.R., et al. Control of memory formation through regulated expression of a CaMKII transgene. Science 1996, 274:1678.
49. Meador-Woodruff J.H., Hogg A.J., Smith R.E. Striatal ionotropic glutamate receptor expression in schizophrenia, bipolar disorder, and major depressive disorder. Brain Res. Bull. 2001, 55:631-640.
50. Moghaddam B., Adams B., Verma A., Daly D. Activation of glutamatergic neurotransmission by ketamine: a novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. J. Neurosci. Off. J. Soc. Neurosci. 1997, 17:2921-2927.
51. Monory K., Massa F., Egertová M., Eder M., Blaudzun H., Westenbroek R., et al. The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 2006, 51:455-466.
52. Musleh W., Bi X., Tocco G., Yaghoubi S., Baudry M. Glycine-induced long-term potentiation is associated with structural and functional modifications of alpha-amino-3-hydroxyl-5-methyl-4-isoxazolepropionic acid receptors. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:9451-9456.
53. Nations K.R., Dogterom P., Bursi R., Schipper J., Greenwald S., Zraket D., et al. Examination of Org 26576, an AMPA receptor positive allosteric modulator, in patients diagnosed with major depressive disorder: an exploratory, randomized, double-blind, placebo-controlled trial. J. Psychopharmacol. 2012, 26(12):1525-1539.
54. Norrholm S.D., Ouimet C.C. Altered dendritic spine density in animal models of depression and in response to antidepressant treatment. Synapse 2001, 42:151-163.
55. Padovan C.M., Guimarães F.S. Antidepressant-like effects of NMDA-receptor antagonist injected into the dorsal hippocampus of rats. Pharmacol. Biochem. Behav. 2004, 77:15-19.
56. Papp M., Moryl E. Antidepressant activity of non-competitive and competitive NMDA receptor antagonists in a chronic mild stress model of depression. Eur. J. Pharmacol. 1994, 263:1-7.
57. Papp M., Moryl E. Antidepressant-like effects of 1-aminocyclopropanecarboxylic acid and D-cycloserine in an animal model of depression. Eur. J. Pharmacol. 1996, 316:145-151.
58. Petit-Demouliere B., Chenu F., Bourin M. Forced swimming test in mice: a review of antidepressant activity. Psychopharmacology 2005, 177:245-255.
59. Pittenger C., Duman R.S. Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 2008, 33:88-109.
60. Porsolt R., Le Pichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977, 266:730-732.
61. Price R.B., Nock M.K., Charney D.S., Mathew S.J. Effects of intravenous ketamine on explicit and implicit measures of suicidality in treatment-resistant depression. Biol. Psychiatry 2009, 66:522-526.
62. Przegaliński E., Tatarczyńska E., Dereń-Wesołek A., Chojnacka-Wojcik E. Antidepressant-like effects of a partial agonist at strychnine-insensitive glycine receptors and a competitive NMDA receptor antagonist. Neuropharmacology 1997, 36:31-37.
63. Rogers S.W., Huhes T.E., Hollmann M., Gasic G.P., Deneris E.S., Heinemann S. The characterization and localization of the glutamate receptor subunit GluRl in the rat brain. J. Neurosci. 1991, 11:2713-2724.
64. Rosa M.L.N.M., Guimarães F.S., Pearson R.C.A., Del Bel E.A. Effects of single or repeated restraint stress on GluR1 and GluR2 flip and flop mRNA expression in the hippocampal formation. Brain Res. Bull. 2002, 59:117-124.
65. Sanacora G., Gueorguieva R., Epperson C.N., Wu Y.-T., Appel M., Rothman D.L., et al. Subtype-specific alterations of gamma-aminobutyric acid and glutamate in patients with major depression. Arch. Gen. Psychiatry 2004, 61:705-713.
66. Sanacora G., Treccani G., Popoli M. Towards a glutamate hypothesis of depression: an emerging frontier of neuropsychopharmacology for mood disorders. Neuropharmacology 2012, 62:63-77.
67. Sanderson D.J., Good M.A., Seeburg P.H., Sprengel R., Rawlins J.N.P., Bannerman D.M. The role of the GluR-A (GluR1) AMPA receptor subunit in learning and memory. Progress in Brain Research 2008, vol. 9:159-78. W. Sossin, J.-C. Lacaille, V. Castellucci, S. Belleville (Eds.).
68. Sanderson D.J., Hindley E., Smeaton E., Denny N., Taylor A., Barkus C., et al. Deletion of the GluA1 AMPA receptor subunit impairs recency-dependent object recognition memory. Learn. Mem. 2011, 18:181-190.
69. Sans N., Racca C., Petralia R.S., Wang Y.-X., McCallum J., Wenthold R.J. Synapse-associated protein 97 selectively associates with a subset of AMPA receptors early in their biosynthetic pathway. J. Neurosci. 2001, 21:7506-7516.
70. Schmitt W.B., Sprengel R., Mack V., Draft R.W., Seeburg P.H., Deacon R.M.J., et al. Restoration of spatial working memory by genetic rescue of GluR-A-deficient mice. Nat. Neurosci. 2005, 8:270-272.
71. Sheline Y.I., Mittler B.L., Mintun M.A. The hippocampus and depression. Eur. Psychiatry 2002, 17(Suppl. 3):300-305.
72. Shi S., Hayashi Y., Esteban J.A., Malinow R. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 2001, 105:331-343.
73. Skolnick P., Popik P., Trullas R. Glutamate-based antidepressants: 20years on. Trends Pharmacol. Sci. 2009, 30:563-569.
74. Songyang Z., Fanning A., Fu C., Xu J., Marfatia S., Chishti A., et al. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 1997, 275:73-77.
75. Toth E., Gersner R., Wilf-Yarkoni A., Raizel H., Dar D.E., Richter-Levin G., et al. Age-dependent effects of chronic stress on brain plasticity and depressive behavior. J. Neurochem. 2008, 107:522-532.
76. Toyooka K., Iritani S., Makifuchi T., Shirakawa O., Kitamura N., Maeda K., et al. Selective reduction of a PDZ protein, SAP-97, in the prefrontal cortex of patients with chronic schizophrenia. J. Neurochem. 2002, 83:797-806.
77. Trullas R., Skolnick P. Functional antagonists at the NMDA receptor complex exhibit antidepressant actions. Eur. J. Pharmacol. 1990, 185:1-10.
78. Uchino S., Wada H., Honda S., Nakamura Y., Ondo Y., Uchiyama T., et al. Direct interaction of post-synaptic density-95/Dlg/ZO-1 domain-containing synaptic molecule Shank3 with GluR1 alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor. J. Neurochem. 2006, 97:1203-1214.
79. Vanderklish P., Neve R., Bahr B.A., Arai A., Hennegriff M., Larson J., et al. Translational suppression of a glutamate receptor subunit impairs long-term potentiation. Synapse 1992, 12:333-337.
80. Watanabe Y., Gould E., Daniels D.C., Cameron H., McEwen B.S. Tianeptine attenuates stress-induced morphological changes in the hippocampus. Eur. J. Pharmacol. 1992, 222:157-162.
81. Watanabe Y., Gould E., McEwen B.S. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 1992, 588:341-345.
82. West A.P. Neurobehavioral studies of forced swimming: the role of learning and memory in the forced swim test. Prog. Neuropsychopharmacol. Biol. Psychiatry 1990, 14:863-877.
83. Williams J.M., Guévremont D., Mason-Parker S.E., Luxmanan C., Tate W.P., Abraham W.C. Differential trafficking of AMPA and NMDA receptors during long-term potentiation in awake adult animals. J. Neurosci. 2007, 27:14171-14178.
84. Zamanillo D., Sprengel R., Hvalby O., Jensen V., Burnashev N., Rozov A., et al. Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 1999, 284:1805-1811.
85. Zarate C.A., Singh J.B., Carlson P.J., Brutsche N.E., Ameli R., Luckenbaugh D.A., et al. A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression. Arch. Gen. Psychiatry 2006, 63:856.
86. Zhou W., Zhang L., Guoxiang X., Mojsilovic-Petrovic J., Takamaya K., Sattler R., et al. GluR1 controls dendrite growth through its binding partner, SAP97. J. Neurosci. 2008, 28:10220-10233.