Presynaptic Protein Synthesis Is Required for Long-Term Plasticity of GABA Release

Neuron

Volumn 92, Issue 2, 2016, Pages 479-492

  Younts, Thomas J ^a   Monday, Hannah R ^a   Dudok, Barna ^b,c   Klein, Matthew E ^a   Jordan, Bryen A ^a   Katona, István ^b   Castillo, Pablo E ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

CB1 receptor; endocannabinoid; GABA; inhibition; interneuron; LTD; presynaptic; protein translation; superresolution microscopy; synaptic plasticity

Indexed keywords

4 AMINOBUTYRIC ACID; CANNABINOID 1 RECEPTOR; MAMMALIAN TARGET OF RAPAMYCIN; 1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; BENZOXAZINE DERIVATIVE; MORPHOLINE DERIVATIVE; NAPHTHALENE DERIVATIVE; PIPERIDINE DERIVATIVE; PYRAZOLE DERIVATIVE; TARGET OF RAPAMYCIN KINASE;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AXON; CONTROLLED STUDY; EMBRYO; FEMALE; HIPPOCAMPAL NEURONAL CULTURE; HIPPOCAMPAL SLICE; IN VITRO STUDY; INTERNEURON; LONG TERM DEPRESSION; MALE; MOUSE; NERVE CELL PLASTICITY; NERVE ENDING; NONHUMAN; PERIKARYON; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; RIBOSOME; SIGNAL TRANSDUCTION; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL BODY; CYTOLOGY; FLUORESCENCE IMAGING; HIPPOCAMPUS; IMAGE PROCESSING; METABOLISM; MICROSCOPY; MOLECULAR DYNAMICS; NERVE CELL; NERVE CELL INHIBITION; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; PYRAMIDAL NERVE CELL; SPRAGUE DAWLEY RAT; THREE DIMENSIONAL IMAGING;

ANIMALS; AXONS; BENZOXAZINES; CELL BODY; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; INTERNEURONS; LONG-TERM SYNAPTIC DEPRESSION; MICE; MICE, INBRED C57BL; MICROSCOPY; MOLECULAR DYNAMICS SIMULATION; MORPHOLINES; NAPHTHALENES; NEURAL INHIBITION; NEURONAL PLASTICITY; NEURONS; OPTICAL IMAGING; PATCH-CLAMP TECHNIQUES; PIPERIDINES; PRESYNAPTIC TERMINALS; PROTEIN BIOSYNTHESIS; PYRAMIDAL CELLS; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; RIBOSOMES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84992437521     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.09.040     Document Type: Article

References (66)

1. Adermark, L., Talani, G., Lovinger, D.M., Endocannabinoid-dependent plasticity at GABAergic and glutamatergic synapses in the striatum is regulated by synaptic activity. Eur. J. Neurosci. 29 (2009), 32–41.
2. Akins, M.R., Leblanc, H.F., Stackpole, E.E., Chyung, E., Fallon, J.R., Systematic mapping of fragile X granules in the mouse brain reveals a potential role for presynaptic FMRP in sensorimotor functions. J. Comp. Neurol. 520 (2012), 3687–3706.
3. Alvarez, J., Giuditta, A., Koenig, E., Protein synthesis in axons and terminals: significance for maintenance, plasticity and regulation of phenotype. With a critique of slow transport theory. Prog. Neurobiol. 62 (2000), 1–62.
4. Argaw, A., Duff, G., Zabouri, N., Cécyre, B., Chainé, N., Cherif, H., Tea, N., Lutz, B., Ptito, M., Bouchard, J.F., Concerted action of CB1 cannabinoid receptor and deleted in colorectal cancer in axon guidance. J. Neurosci. 31 (2011), 1489–1499.
5. Baleriola, J., Walker, C.A., Jean, Y.Y., Crary, J.F., Troy, C.M., Nagy, P.L., Hengst, U., Axonally synthesized ATF4 transmits a neurodegenerative signal across brain regions. Cell 158 (2014), 1159–1172.
6. Barna, L., Dudok, B., Miczán, V., Horváth, A., László, Z.I., Katona, I., Correlated confocal and super-resolution imaging by VividSTORM. Nat. Protoc. 11 (2016), 163–183.
7. Barnes, S.J., Opitz, T., Merkens, M., Kelly, T., von der Brelie, C., Krueppel, R., Beck, H., Stable mossy fiber long-term potentiation requires calcium influx at the granule cell soma, protein synthesis, and microtubule-dependent axonal transport. J. Neurosci. 30 (2010), 12996–13004.
8. Basu, J., Srinivas, K.V., Cheung, S.K., Taniguchi, H., Huang, Z.J., Siegelbaum, S.A., A cortico-hippocampal learning rule shapes inhibitory microcircuit activity to enhance hippocampal information flow. Neuron 79 (2013), 1208–1221.
9. Beaumont, V., Zhong, N., Fletcher, R., Froemke, R.C., Zucker, R.S., Phosphorylation and local presynaptic protein synthesis in calcium- and calcineurin-dependent induction of crayfish long-term facilitation. Neuron 32 (2001), 489–501.
10. Berghuis, P., Rajnicek, A.M., Morozov, Y.M., Ross, R.A., Mulder, J., Urbán, G.M., Monory, K., Marsicano, G., Matteoli, M., Canty, A., et al. Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 316 (2007), 1212–1216.
11. Biró, A.A., Holderith, N.B., Nusser, Z., Release probability-dependent scaling of the postsynaptic responses at single hippocampal GABAergic synapses. J. Neurosci. 26 (2006), 12487–12496.
12. Buffington, S.A., Huang, W., Costa-Mattioli, M., Translational control in synaptic plasticity and cognitive dysfunction. Annu. Rev. Neurosci. 37 (2014), 17–38.
13. Cajigas, I.J., Tushev, G., Will, T.J., tom Dieck, S., Fuerst, N., Schuman, E.M., The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron 74 (2012), 453–466.
14. Calixto, E., Thiels, E., Klann, E., Barrionuevo, G., Early maintenance of hippocampal mossy fiber–long-term potentiation depends on protein and RNA synthesis and presynaptic granule cell integrity. J. Neurosci. 23 (2003), 4842–4849.
15. Castillo, P.E., Presynaptic LTP and LTD of excitatory and inhibitory synapses. Cold Spring Harb. Perspect. Biol., 4, 2012, a005728.
16. Castillo, P.E., Younts, T.J., Chávez, A.E., Hashimotodani, Y., Endocannabinoid signaling and synaptic function. Neuron 76 (2012), 70–81.
17. Chevaleyre, V., Castillo, P.E., Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38 (2003), 461–472.
18. Chevaleyre, V., Heifets, B.D., Kaeser, P.S., Südhof, T.C., Castillo, P.E., Endocannabinoid-mediated long-term plasticity requires cAMP/PKA signaling and RIM1alpha. Neuron 54 (2007), 801–812.
19. Christie, S.B., Akins, M.R., Schwob, J.E., Fallon, J.R., The FXG: a presynaptic fragile X granule expressed in a subset of developing brain circuits. J. Neurosci. 29 (2009), 1514–1524.
20. Crispino, M., Chun, J.T., Cefaliello, C., Perrone Capano, C., Giuditta, A., Local gene expression in nerve endings. Dev. Neurobiol. 74 (2014), 279–291.
21. Darnell, J.C., Klann, E., The translation of translational control by FMRP: therapeutic targets for FXS. Nat. Neurosci. 16 (2013), 1530–1536.
22. Dieterich, D.C., Hodas, J.J., Gouzer, G., Shadrin, I.Y., Ngo, J.T., Triller, A., Tirrell, D.A., Schuman, E.M., In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons. Nat. Neurosci. 13 (2010), 897–905.
23. Droz, B., Leblond, C.P., Axonal migration of proteins in the central nervous system and peripheral nerves as shown by radioautography. J. Comp. Neurol. 121 (1963), 325–346.
24. Dudok, B., Barna, L., Ledri, M., Szabó, S.I., Szabadits, E., Pintér, B., Woodhams, S.G., Henstridge, C.M., Balla, G.Y., Nyilas, R., et al. Cell-specific STORM super-resolution imaging reveals nanoscale organization of cannabinoid signaling. Nat. Neurosci. 18 (2015), 75–86.
25. Dupret, D., O'Neill, J., Csicsvari, J., Dynamic reconfiguration of hippocampal interneuron circuits during spatial learning. Neuron 78 (2013), 166–180.
26. Fukudome, Y., Ohno-Shosaku, T., Matsui, M., Omori, Y., Fukaya, M., Tsubokawa, H., Taketo, M.M., Watanabe, M., Manabe, T., Kano, M., Two distinct classes of muscarinic action on hippocampal inhibitory synapses: M2-mediated direct suppression and M1/M3-mediated indirect suppression through endocannabinoid signalling. Eur. J. Neurosci. 19 (2004), 2682–2692.
27. Gomes, C., Merianda, T.T., Lee, S.J., Yoo, S., Twiss, J.L., Molecular determinants of the axonal mRNA transcriptome. Dev. Neurobiol. 74 (2014), 218–232.
28. Hagena, H., Manahan-Vaughan, D., Differentiation in the protein synthesis-dependency of persistent synaptic plasticity in mossy fiber and associational/commissural CA3 synapses in vivo. Front. Integr. Nuerosci., 7, 2013, 10.
29. Heifets, B.D., Chevaleyre, V., Castillo, P.E., Interneuron activity controls endocannabinoid-mediated presynaptic plasticity through calcineurin. Proc. Natl. Acad. Sci. USA 105 (2008), 10250–10255.
30. Holt, C.E., Schuman, E.M., The central dogma decentralized: new perspectives on RNA function and local translation in neurons. Neuron 80 (2013), 648–657.
31. Howlett, A.C., Barth, F., Bonner, T.I., Cabral, G., Casellas, P., Devane, W.A., Felder, C.C., Herkenham, M., Mackie, K., Martin, B.R., et al. International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol. Rev. 54 (2002), 161–202.
32. Huang, C.C., Hsu, K.S., Local protein synthesis and GABAB receptors regulate the reversibility of long-term potentiation at murine hippocampal mossy fibre-CA3 synapses. J. Physiol. 561 (2004), 91–108.
33. Huang, Y.Y., Li, X.C., Kandel, E.R., cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 79 (1994), 69–79.
34. Huang, B., Wang, W., Bates, M., Zhuang, X., Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319 (2008), 810–813.
35. Huber, K.M., Kayser, M.S., Bear, M.F., Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288 (2000), 1254–1257.
36. Irving, A.J., Coutts, A.A., Harvey, J., Rae, M.G., Mackie, K., Bewick, G.S., Pertwee, R.G., Functional expression of cell surface cannabinoid CB(1) receptors on presynaptic inhibitory terminals in cultured rat hippocampal neurons. Neuroscience 98 (2000), 253–262.
37. Jones, E.G., Powell, T.P., Synapses on the axon hillocks and initial segments of pyramidal cell axons in the cerebral cortex. J. Cell Sci. 5 (1969), 495–507.
38. Jung, K.M., Sepers, M., Henstridge, C.M., Lassalle, O., Neuhofer, D., Martin, H., Ginger, M., Frick, A., DiPatrizio, N.V., Mackie, K., et al. Uncoupling of the endocannabinoid signalling complex in a mouse model of fragile X syndrome. Nat. Commun., 3, 2012, 1080.
39. Jung, H., Gkogkas, C.G., Sonenberg, N., Holt, C.E., Remote control of gene function by local translation. Cell 157 (2014), 26–40.
40. Kano, M., Ohno-Shosaku, T., Hashimotodani, Y., Uchigashima, M., Watanabe, M., Endocannabinoid-mediated control of synaptic transmission. Physiol. Rev. 89 (2009), 309–380.
41. Katona, I., Sperlágh, B., Sík, A., Käfalvi, A., Vizi, E.S., Mackie, K., Freund, T.F., Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J. Neurosci. 19 (1999), 4544–4558.
42. Kelly, A., Mullany, P.M., Lynch, M.A., Protein synthesis in entorhinal cortex and long-term potentiation in dentate gyrus. Hippocampus 10 (2000), 431–437.
43. Klausberger, T., Marton, L.F., O'Neill, J., Huck, J.H., Dalezios, Y., Fuentealba, P., Suen, W.Y., Papp, E., Kaneko, T., Watanabe, M., et al. Complementary roles of cholecystokinin- and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations. J. Neurosci. 25 (2005), 9782–9793.
44. Klein, M.E., Castillo, P.E., Jordan, B.A., Coordination between translation and degradation regulates inducibility of mGluR-LTD. Cell Rep., 2015 S2211-1247(15)00166-7.
45. Koenig, E., Martin, R., Titmus, M., Sotelo-Silveira, J.R., Cryptic peripheral ribosomal domains distributed intermittently along mammalian myelinated axons. J. Neurosci. 20 (2000), 8390–8400.
46. Martin, K.C., Casadio, A., Zhu, H., Yaping, E., Rose, J.C., Chen, M., Bailey, C.H., Kandel, E.R., Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91 (1997), 927–938.
47. Moerke, N.J., Aktas, H., Chen, H., Cantel, S., Reibarkh, M.Y., Fahmy, A., Gross, J.D., Degterev, A., Yuan, J., Chorev, M., et al. Small-molecule inhibition of the interaction between the translation initiation factors eIF4E and eIF4G. Cell 128 (2007), 257–267.
48. Njoo, C., Agarwal, N., Lutz, B., Kuner, R., The cannabinoid receptor CB1 interacts with the WAVE1 complex and plays a role in actin dynamics and structural plasticity in neurons. PLoS Biol., 13, 2015, e1002286.
49. Palay, S.L., Palade, G.E., The fine structure of neurons. J. Biophys. Biochem. Cytol. 1 (1955), 69–88.
50. Puighermanal, E., Marsicano, G., Busquets-Garcia, A., Lutz, B., Maldonado, R., Ozaita, A., Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling. Nat. Neurosci. 12 (2009), 1152–1158.
51. Roland, A.B., Ricobaraza, A., Carrel, D., Jordan, B.M., Rico, F., Simon, A., Humbert-Claude, M., Ferrier, J., McFadden, M.H., Scheuring, S., Lenkei, Z., Cannabinoid-induced actomyosin contractility shapes neuronal morphology and growth. eLife, 3, 2014, e03159.
52. Santini, E., Huynh, T.N., Klann, E., Mechanisms of translation control underlying long-lasting synaptic plasticity and the consolidation of long-term memory. Prog. Mol. Biol. Transl. Sci. 122 (2014), 131–167.
53. Sekine, Y., Zyryanova, A., Crespillo-Casado, A., Fischer, P.M., Harding, H.P., Ron, D., Stress responses. Mutations in a translation initiation factor identify the target of a memory-enhancing compound. Science 348 (2015), 1027–1030.
54. Shigeoka, T., Jung, H., Jung, J., Turner-Bridger, B., Ohk, J., Lin, J.Q., Amieux, P.S., Holt, C.E., Dynamic Axonal Translation in Developing and Mature Visual Circuits. Cell 166 (2016), 181–192.
55. Sonenberg, N., Hinnebusch, A.G., Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136 (2009), 731–745.
56. Steward, O., Ribak, C.E., Polyribosomes associated with synaptic specializations on axon initial segments: localization of protein-synthetic machinery at inhibitory synapses. J. Neurosci. 6 (1986), 3079–3085.
57. Taylor, A.M., Berchtold, N.C., Perreau, V.M., Tu, C.H., Li Jeon, N., Cotman, C.W., Axonal mRNA in uninjured and regenerating cortical mammalian axons. J. Neurosci. 29 (2009), 4697–4707.
58. Tcherkezian, J., Brittis, P.A., Thomas, F., Roux, P.P., Flanagan, J.G., Transmembrane receptor DCC associates with protein synthesis machinery and regulates translation. Cell 141 (2010), 632–644.
59. Twitchell, W., Brown, S., Mackie, K., Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons. J. Neurophysiol. 78 (1997), 43–50.
60. Wilhelm, B.G., Mandad, S., Truckenbrodt, S., Kröhnert, K., Schäfer, C., Rammner, B., Koo, S.J., Claßen, G.A., Krauss, M., Haucke, V., et al. Composition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins. Science 344 (2014), 1023–1028.
61. Xue, S., Barna, M., Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat. Rev. Mol. Cell Biol. 13 (2012), 355–369.
62. Yin, H.H., Davis, M.I., Ronesi, J.A., Lovinger, D.M., The role of protein synthesis in striatal long-term depression. J. Neurosci. 26 (2006), 11811–11820.
63. Yoon, B.C., Jung, H., Dwivedy, A., O'Hare, C.M., Zivraj, K.H., Holt, C.E., Local translation of extranuclear lamin B promotes axon maintenance. Cell 148 (2012), 752–764.
64. Younts, T.J., Chevaleyre, V., Castillo, P.E., CA1 pyramidal cell theta-burst firing triggers endocannabinoid-mediated long-term depression at both somatic and dendritic inhibitory synapses. J. Neurosci. 33 (2013), 13743–13757.
65. Yuan, S., Burrell, B.D., Endocannabinoid-dependent long-term depression in a nociceptive synapse requires coordinated presynaptic and postsynaptic transcription and translation. J. Neurosci. 33 (2013), 4349–4358.
66. Zhang, Xh., Poo, M.M., Localized synaptic potentiation by BDNF requires local protein synthesis in the developing axon. Neuron 36 (2002), 675–688.