mTORC1-dependent protein synthesis underlying rapid antidepressant effect requires GABABR signaling

Neuropharmacology

Volumn 73, Issue , 2013, Pages 192-203

  Workman, E R ^a   Niere, Farr ^a   Raab Graham, Kimberly F ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Calcium imaging; Hippocampal neurons; L type calcium channels; MTORC1; NMDA receptors; Prefrontal cortex; Protein synthesis; Rapid antidepressant

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; AMPA RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM CHANNEL L TYPE; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; RO 25 6891; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIDEPRESSANT ACTIVITY; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; DENDRITE; ENZYME ACTIVATION; ENZYME ACTIVITY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SUBUNIT; PROTEIN SYNTHESIS; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION; UPREGULATION;

CALCIUM IMAGING; GABA(B) RECEPTORS; HIPPOCAMPAL NEURONS; L-TYPE CALCIUM CHANNELS; MTORC1; NMDA RECEPTORS; PREFRONTAL CORTEX; PROTEIN SYNTHESIS; RAPID ANTIDEPRESSANT;

2-AMINO-5-PHOSPHONOVALERATE; ANIMALS; BACLOFEN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM; CALCIUM CHANNELS, L-TYPE; CELLS, CULTURED; CYTOSKELETAL PROTEINS; EXCITATORY AMINO ACID ANTAGONISTS; GABA ANTAGONISTS; GABA-B RECEPTOR AGONISTS; HIPPOCAMPUS; HUMANS; IMMOBILITY RESPONSE, TONIC; MALE; MICE; MULTIPROTEIN COMPLEXES; NERVE TISSUE PROTEINS; ORGANOPHOSPHORUS COMPOUNDS; PIPERIDINES; PREFRONTAL CORTEX; PRIMARY CELL CULTURE; RECEPTORS, AMPA; RECEPTORS, GABA-B; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84885086397     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.05.037     Document Type: Article

References (57)

1. Akerboom, J., Rivera, J.D., Guilbe, M.M., Malave, E.C., Hernandez, H.H., Tian, L., Hires, S.A., Marvin, J.S., Looger, L.L., Schreiter, E.R., 2009. Crystal structures of the GCaMP calcium sensor reveal the mechanism of fluorescence signal change and aid rational design. The Journal of Biological Chemistry 284, 6455-6464.
2. Autry, A.E., Adachi, M., Nosyreva, E., Na, E.S., Los, M.F., Cheng, P.F., Kavalali, E.T., Monteggia, L.M., 2011. NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 475, 91-95.
3. Bray, J.G., Mynlieff, M., 2011. Involvement of protein kinase C and protein kinase A in the enhancement of L-type calcium current by GABAB receptor activation in neonatal hippocampus. Neuroscience 179, 62-72.
4. Breton, J.D., Stuart, G.J., 2012. Somatic and dendritic GABA(B) receptors regulate neuronal excitability via different mechanisms. Journal of Neurophysiology 108, 2810-2818.
5. Cammalleri, M., Lutjens, R., Berton, F., King, A.R., Simpson, C., Francesconi, W., Sanna, P.P., 2003. Time-restricted role for dendritic activation of the mTOR-p70S6K pathway in the induction of late-phase long-term potentiation in the CA1. Proceedings of the National Academy of Sciences of the United States of America 100, 14368-14373.
6. Castagne, V., Moser, P., Roux, S., Porsolt, R.D., 2011. Rodent models of depression: forced swim and tail suspension behavioral despair tests in rats and mice. Current Protocols in Neuroscience. Editorial Board, Jacqueline N Crawley [et al] (Chapter 8), Unit 8 10A.
7. Catterall, W.A., Goldin, A.L., Waxman, S.G., 2005. International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltagegated sodium channels. Pharmacological Reviews 57, 397-409.
8. Chalifoux, J.R., Carter, A.G., 2010. GABAB receptors modulate NMDA receptor calcium signals in dendritic spines. Neuron 66, 101-113.
9. Chalifoux, J.R., Carter, A.G., 2011a. GABAB receptor modulation of synaptic function. Current Opinion in Neurobiology 21, 339-344.
10. Chalifoux, J.R., Carter, A.G., 2011b. GABAB receptor modulation of voltage-sensitive calcium channels in spines and dendrites. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 31, 4221-4232.
11. Chang, M.C., Park, J.M., Pelkey, K.A., Grabenstatter, H.L., Xu, D., Linden, D.J., Sutula, T.P., McBain, C.J., Worley, P.F., 2010. Narp regulates homeostatic scaling of excitatory synapses on parvalbumin-expressing interneurons. Nature Neuroscience 13, 1090-1097.
12. De Simoni, A., Griesinger, C.B., Edwards, F.A., 2003. Development of rat CA1 neurones in acute versus organotypic slices: role of experience in synaptic morphology and activity. The Journal of Physiology 550, 135-147.
13. Diazgranados, N., Ibrahim, L., Brutsche, N.E., Newberg, A., Kronstein, P., Khalife, S., Kammerer, W.A., Quezado, Z., Luckenbaugh, D.A., Salvadore, G., et al, 2010. A randomized add-on trial of an N-methyl-D-aspartate antagonist in treatment-resistant bipolar depression. Archives of General Psychiatry 67, 793-802.
14. Duman, C.H., 2010. Models of depression. Vitamins and Hormones 82, 1-21.
15. Duman, R.S., Li, N., Liu, R.J., Duric, V., Aghajanian, G., 2012. Signaling pathways underlying the rapid antidepressant actions of ketamine. Neuropharmacology 62, 35-41.
16. Farber, N.B., Newcomer, J.W., Olney, J.W., 1998. The glutamate synapse in neuropsychiatric disorders. Focus on schizophrenia and Alzheimer's disease. Progress in Brain Research 116, 421-437.
17. Ghose, S., Winter, M.K., McCarson, K.E., Tamminga, C.A., Enna, S.J., 2011. The GABAβ receptor as a target for antidepressant drug action. British Journal of Pharmacology 162, 1-17.
18. Gong, R., Park, C.S., Abbassi, N.R., Tang, S.J., 2006. Roles of glutamate receptors and the mammalian target of rapamycin (mTOR) signaling pathway in activity-dependent dendritic protein synthesis in hippocampal neurons. The Journal of Biological Chemistry 281, 18802-18815.
19. Guetg, N., Abdel Aziz, S., Holbro, N., Turecek, R., Rose, T., Seddik, R., Gassmann, M., Moes, S., Jenoe, P., Oertner, T.G., et al., 2010. NMDA receptor-dependent GABAB receptor internalization via CaMKII phosphorylation of serine 867 in GABAB1. Proceedings of the National Academy of Sciences of the United States of America 107, 13924-13929.
20. Harlow, H.F., Suomi, S.J., 1974. Induced depression in monkeys. Behavioral Biology 12, 273-296.
21. Hay, N., Sonenberg, N., 2004. Upstream and downstream of mTOR. Genes & Development 18, 1926-1945.
22. Hegner, B., Lange, M., Kusch, A., Essin, K., Sezer, O., Schulze-Lohoff, E., Luft, F.C., Gollasch, M., Dragun, D., 2009. mTOR regulates vascular smooth muscle cell differentiation from human bone marrow-derived mesenchymal progenitors. Arteriosclerosis, Thrombosis, and Vascular Biology 29, 232-238.
23. Henry, F.E., McCartney, A.J., Neely, R., Perez, A.S., Carruthers, C.J., Stuenkel, E.L., Inoki, K., Sutton, M.A., 2012. Retrograde changes in presynaptic function driven by dendritic mTORC1. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 32, 17128-17142.
24. Hoeffer, C.A., Klann, E., 2009. Biology of the NMDA receptor. In: V.D., A.M. (Ed.), NMDA Receptors and Translational Control. CRC Press, Boca Raton (FL). (Chapter 6).
25. Hoeffer, C.A., Klann, E., 2010. mTOR signaling: at the crossroads of plasticity, memory and disease. Trends in Neurosciences 33, 67-75.
26. Ibrahim, L., Duncan, W., Luckenbaugh, D.A., Yuan, P., Machado-Vieira, R., Zarate Jr, C.A., 2011. Rapid antidepressant changes with sleep deprivation in major depressive disorder are associated with changes in vascular endothelial growth factor (VEGF): a pilot study. Brain Research Bulletin 86, 129-133.
27. Ivenshitz, M., Segal, M., 2010. Neuronal density determines network connectivity and spontaneous activity in cultured hippocampus. Journal of Neurophysiology 104, 1052-1060.
28. Kessler, R.C., Berglund, P., Demler, O., Jin, R., Koretz, D., Merikangas, K.R., Rush, A.J., Walters, E.E., Wang, P.S., 2003. The epidemiology of major depressive disorder: results from the National Comorbidity Survey Replication (NCS-R). JAMA: The Journal of the American Medical Association 289, 3095-3105.
29. Lee, H.H., Deeb, T.Z., Walker, J.A., Davies, P.A., Moss, S.J., 2011. NMDA receptor activity downregulates KCC2 resulting in depolarizing GABAA receptor-mediated currents. Nature Neuroscience 14, 736-743.
30. Li, N., Lee, B., Liu, R.J., Banasr, M., Dwyer, J.M., Iwata, M., Li, X.Y., Aghajanian, G., Duman, R.S., 2010. mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science 329, 959-964.
31. Ma, D., Zerangue, N., Raab-Graham, K., Fried, S.R., Jan, Y.N., Jan, L.Y., 2002. Diverse trafficking patterns due to multiple traffic motifs in G protein-activated inwardly rectifying potassium channels from brain and heart. Neuron 33, 715-729.
32. Magee, J., Hoffman, D., Colbert, C., Johnston, D., 1998. Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. Annual Review of Physiology 60, 327-346.
33. Margeta-Mitrovic, M., Jan, Y.N., Jan, L.Y., 2000. A trafficking checkpoint controls GABA(B) receptor heterodimerization. Neuron 27, 97-106.
34. Mathews, D.C., Henter, I.D., Zarate, C.A., 2012. Targeting the glutamatergic system to treat major depressive disorder: rationale and progress to date. Drugs 72, 1313-1333.
35. Matthews, K., Christmas, D., Swan, J., Sorrell, E., 2005. Animal models of depression: navigating through the clinical fog. Neuroscience and Biobehavioral Reviews 29, 503-513.
36. Miller, W.R., Seligman, M.E., Kurlander, H.M., 1975. Learned helplessness, depression, and anxiety. The Journal of Nervous and Mental Disease 161, 347-357.
37. Murrough, J.W., 2012. Ketamine as a novel antidepressant: from synapse to behavior. Clinical Pharmacology and Therapeutics 91, 303-309.
38. Padgett, C.L., Slesinger, P.A., 2010. GABAB receptor coupling to G-proteins and ion channels. Advances in Pharmacology 58, 123-147.
39. Panja, D., Dagyte, G., Bidinosti, M., Wibrand, K., Kristiansen, A.M., Sonenberg, N., Bramham, C.R., 2009. Novel translational control in Arc-dependent long term potentiation consolidation in vivo. The Journal of Biological Chemistry 284, 31498-31511.
40. Paoletti, P., Neyton, J., 2007. NMDA receptor subunits: function and pharmacology. Current Opinion in Pharmacology 7, 39-47.
41. 2+ spikes by GABAB receptors in cortical pyramidal neurons is mediated by a direct Gi/o-beta-subunit interaction with Cav1 channels. The Journal of Physiology 591, 1599-1612.
42. Porsolt, R.D., Bertin, A., Blavet, N., Deniel, M., Jalfre, M., 1979. Immobility induced by forced swimming in rats: effects of agents which modify central catecholamine and serotonin activity. European Journal of Pharmacology 57, 201-210.
43. Preskorn, S.H., Baker, B., Kolluri, S., Menniti, F.S., Krams, M., Landen, J.W., 2008. An innovative design to establish proof of concept of the antidepressant effects of the NR2B subunit selective N-methyl-D-aspartate antagonist, CP-101,606, in patients with treatment-refractory major depressive disorder. Journal of Clinical Psychopharmacology 28, 631-637.
44. Quinlan, E.M., Philpot, B.D., Huganir, R.L., Bear, M.F., 1999. Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nature Neuroscience 2, 352-357.
45. Raab-Graham, K.F., Haddick, P.C., Jan, Y.N., Jan, L.Y., 2006. Activity- and mTOR-dependent suppression of Kv1.1 channel mRNA translation in dendrites. Science 314, 144-148.
46. Roubicek, J., Matejcek, M., Porsolt, R., 1975. Computer analysed EEG and behavioral changes after psychoactive drugs. International Journal of Neurology 10, 33-40.
47. Rush, A.J., Trivedi, M.H., Stewart, J.W., Nierenberg, A.A., Fava, M., Kurian, B.T., Warden, D., Morris, D.W., Luther, J.F., Husain, M.M., et al, 2011. Combining medications to enhance depression outcomes (CO-MED): acute and long-term outcomes of a single-blind randomized study. The American Journal of Psychiatry 168, 689-701.
48. Rush, A.J., Trivedi, M.H., Wisniewski, S.R., Stewart, J.W., Nierenberg, A.A., Thase, M.E., Ritz, L., Biggs, M.M., Warden, D., Luther, J.F., et al, 2006. Bupropion-SR, sertraline, or venlafaxine-XR after failure of SSRIs for depression. The New England Journal of Medicine 354, 1231-1242.
49. Skolnick, P., Popik, P., Trullas, R., 2009. Glutamate-based antidepressants: 20 years on. Trends in Pharmacological Sciences 30, 563-569.
50. Slattery, D.A., Desrayaud, S., Cryan, J.F., 2005. GABAB receptor antagonist-mediated antidepressant-like behavior is serotonin-dependent. The Journal of Pharmacology and Experimental Therapeutics 312, 290-296.
51. Takei, N., Inamura, N., Kawamura, M., Namba, H., Hara, K., Yonezawa, K., Nawa, H., 2004. Brain-derived neurotrophic factor induces mammalian target of rapamycin-dependent local activation of translation machinery and protein synthesis in neuronal dendrites. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 24, 9760-9769.
52. Terunuma, M., Vargas, K.J., Wilkins, M.E., Ramirez, O.A., Jaureguiberry-Bravo, M., Pangalos, M.N., Smart, T.G., Moss, S.J., Couve, A., 2010. Prolonged activation of NMDA receptors promotes dephosphorylation and alters postendocytic sorting of GABAB receptors. Proceedings of the National Academy of Sciences of the United States of America 107, 13918-13923.
53. Trullas, R., Skolnick, P., 1990. Functional antagonists at the NMDA receptor complex exhibit antidepressant actions. European Journal of Pharmacology 185, 1-10.
54. Wheeler, D.G., Groth, R.D., Ma, H., Barrett, C.F., Owen, S.F., Safa, P., Tsien, R.W., 2012. Ca(V)1 and Ca(V)2 channels engage distinct modes of Ca(2+) signaling to control CREB-dependent gene expression. Cell 149, 1112-1124.
55. 2+ influx via L-type calcium channels activates the Src/ERK/cyclic-AMP response element binding protein signal pathway and BCL-2 expression in rat hippocampal neurons: a potential initiation mechanism for estrogen-induced neuroprotection. Neuroscience 135, 59-72.
56. Yan, H.C., Cao, X., Das, M., Zhu, X.H., Gao, T.M., 2010. Behavioral animal models of depression. Neuroscience Bulletin 26, 327-337.
57. Zarate Jr., C.A., Singh, J.B., Carlson, P.J., Brutsche, N.E., Ameli, R., Luckenbaugh, D.A., Charney, D.S., Manji, H.K., 2006. A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression. Archives of General Psychiatry 63, 856-864.