mGlu5 receptors regulate synaptic sumoylation via a transient PKC-dependent diffusional trapping of Ubc9 into spines

Nature Communications

Volumn 5, Issue , 2014, Pages

  Loriol, Céline ^a,b   Cassé, Frédéric ^a,b   Khayachi, Anouar ^a,b   Poupon, Gwénola ^a,b   Chafai, Magda ^b   Deval, Emmanuel ^b   Gwizdek, Carole ^a,b   Martin, Stéphane ^a,b  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; METABOTROPIC RECEPTOR 5; PROTEIN KINASE C; PROTEIN UBC9; GRM5 PROTEIN, MOUSE; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN-CONJUGATING ENZYME UBC9;

BIOCHEMISTRY; BRAIN; CHEMICAL CUE; CHEMICAL REACTION; DIFFUSION; ENZYME ACTIVITY; GENE EXPRESSION; MOLECULAR ANALYSIS; PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLEACHING; CONTROLLED STUDY; DIFFUSION; FEMALE; HIPPOCAMPUS; NERVE CELL; NONHUMAN; PHOSPHORYLATION; RAT; REGULATORY MECHANISM; SPINE; SUMOYLATION; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; ANIMAL; CELL CULTURE; CYTOLOGY; ENZYMOLOGY; GENETICS; METABOLISM; MOUSE; SYNAPSE;

ANIMALS; CELLS, CULTURED; HIPPOCAMPUS; MICE; NEURONS; PROTEIN KINASE C; RECEPTOR, METABOTROPIC GLUTAMATE 5; SUMOYLATION; SYNAPSES; SYNAPTIC TRANSMISSION; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84950133238     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6113     Document Type: Article

References (55)

1. Mabb, A. M. & Ehlers, M. D. Ubiquitination in postsynaptic function and plasticity. Annu. Rev. Cell Dev. Biol. 26, 179-210 (2010).
2. Martin, S., Wilkinson, K. A., Nishimune, A. & Henley, J. M. Emerging extranuclear roles of protein SUMOylation in neuronal function and dysfunction. Nat. Rev. Neurosci. 8, 948-959 (2007).
3. Krumova, P. & Weishaupt, J. H. Sumoylation in neurodegenerative diseases. Cell. Mol. Life Sci. 70, 2123-2959 (2012).
4. Gwizdek, C., Cassé, F. & Martin, S. Protein sumoylation in brain development, neuronal morphology and spinogenesis. Neuromolecular Med. 15, 677-691 (2013).
5. Matunis, M. J., Coutavas, E. & Blobel, G. A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J. Cell Biol. 135, 1457-1470 (1996).
6. Mahajan, R., Delphin, C., Guan, T., Gerace, L. & Melchior, F. A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 88, 97-107 (1997).
7. Meulmeester, E. & Melchior, F. Cell biology: SUMO. Nature 452, 709-711 (2008).
8. Martin, S. Extranuclear functions of protein sumoylation in the central nervous system. Med. Sci. (Paris) 25, 693-698 (2009).
9. Hietakangas, V. et al. PDSM, a motif for phosphorylation-dependent SUMO modification. Proc. Natl Acad. Sci. USA 103, 45-50 (2006).
10. Mohideen, F. et al. A molecular basis for phosphorylation-dependent SUMO conjugation by the E2 UBC9. Nat. Struct. Mol. Biol. 16, 945-952 (2009).
11. Hickey, C. M., Wilson, N. R. & Hochstrasser, M. Function and regulation of SUMO proteases. Nat. Rev. Mol. Cell Biol. 13, 755-766 (2012).
12. Janer, A. et al. SUMOylation attenuates the aggregation propensity and cellular toxicity of the polyglutamine expanded ataxin-7. Hum. Mol. Genet. 19, 181-195 (2010).
13. Krumova, P. et al. Sumoylation inhibits {alpha}-synuclein aggregation and toxicity. J. Cell Biol. 194, 49-60 (2011).
14. Oh, Y., Kim, Y. M., Mouradian, M. M. & Chung, K. C. Human Polycomb protein 2 promotes alpha-synuclein aggregate formation through covalent SUMOylation. Brain Res. 1381, 78-89 (2011).
15. Verger, A., Perdomo, J. & Crossley, M. Modification with SUMO. A role in transcriptional regulation. EMBO Rep. 4, 137-142 (2003).
16. Ulrich, H. D. Mutual interactions between the SUMO and ubiquitin systems: a plea of no contest. Trends Cell Biol. 15, 525-532 (2005).
17. Shalizi, A. et al. A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311, 1012-1017 (2006).
18. Shalizi, A. et al. PIASx is a MEF2 SUMO E3 ligase that promotes postsynaptic dendritic morphogenesis. J. Neurosci. 27, 10037-10046 (2007).
19. Onishi, A. et al. Pias3-dependent SUMOylation directs rod photoreceptor development. Neuron 61, 234-246 (2009).
20. Martin, S., Nishimune, A., Mellor, J. R. & Henley, J. M. SUMOylation regulates kainate-receptor-mediated synaptic transmission. Nature 447, 321-325 (2007).
21. van Niekerk, E. A. et al. Sumoylation in axons triggers retrograde transport of the RNA-binding protein La. Proc. Natl Acad. Sci. USA 104, 12913-12918 (2007).
22. Chao, H. W., Hong, C. J., Huang, T. N., Lin, Y. L. & Hsueh, Y. P. SUMOylation of the MAGUK protein CASK regulates dendritic spinogenesis. J. Cell Biol. 182, 141-155 (2008).
23. Konopacki, F. A. et al. Agonist-induced PKC phosphorylation regulates GluK2 SUMOylation and kainate receptor endocytosis. Proc. Natl Acad. Sci. USA 108, 19772-19777 (2011).
24. Craig, T. J. et al. Homeostatic synaptic scaling is regulated by protein SUMOylation. J. Biol. Chem. 287, 22781-22788 (2012).
25. Chamberlain, S. E. et al. SUMOylation and phosphorylation of GluK2 regulate kainate receptor trafficking and synaptic plasticity. Nat. Neurosci. 15, 845-852 (2012).
26. Loriol, C., Parisot, J., Poupon, G., Gwizdek, C. & Martin, S. Developmental regulation and spatiotemporal redistribution of the sumoylation machinery in the rat central nervous system. PLoS ONE 7, e33757 (2012).
27. Loriol, C., Khayachi, A., Poupon, G., Gwizdek, C. & Martin, S. Activity-dependent regulation of the sumoylation machinery in rat hippocampal neurons. Biol. Cell 105, 30-45 (2013).
28. Thalhammer, A. et al. CaMKII translocation requires local NMDA receptor-mediated Ca2+ signaling. EMBO J. 25, 5873-5883 (2006).
29. Bingol, B. & Schuman, E. M. Activity-dependent dynamics and sequestration of proteasomes in dendritic spines. Nature 441, 1144-1148 (2006).
30. Niswender, C. M. & Conn, P. J. Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu. Rev. Pharmacol. Toxicol. 50, 295-322 (2010).
31. Wang, H. & Zhuo, M. Group I metabotropic glutamate receptor-mediated gene transcription and implications for synaptic plasticity and diseases. Front. Pharmacol. 3, 189 (2012).
32. Gurskaya, N. G. et al. Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat. Biotechnol. 24, 461-465 (2006).
33. Chudakov, D. M., Lukyanov, S. & Lukyanov, K. A. Tracking intracellular protein movements using photoswitchable fluorescent proteins PS-CFP2 and Dendra2. Nat. Protoc. 2, 2024-2032 (2007).
34. Mangmool, S. & Kurose, H. G(i/o) protein-dependent and -independent actions of Pertussis Toxin (PTX). Toxins (Basel) 3, 884-899 (2011).
35. Uyama, Y., Imaizumi, Y. & Watanabe, M. Cyclopiazonic acid, an inhibitor of Ca(2+)-ATPase in sarcoplasmic reticulum, increases excitability in ileal smooth muscle. Br. J. Pharmacol. 110, 565-572 (1993).
36. Stork, A. P. & Cocks, T. M. Pharmacological reactivity of human epicardial coronary arteries: phasic and tonic responses to vasoconstrictor agents differentiated by nifedipine. Br. J. Pharmacol. 113, 1093-1098 (1994).
37. Bleasdale, J. E. et al. Selective inhibition of receptor-coupled phospholipase C-dependent processes in human platelets and polymorphonuclear neutrophils. J. Pharmacol. Exp. Ther. 255, 756-768 (1990).
38. Herbert, J. M., Augereau, J. M., Gleye, J. & Maffrand, J. P. Chelerythrine is a potent and specific inhibitor of protein kinase C. Biochem. Biophys. Res. Commun. 172, 993-999 (1990).
39. Myers, M. A., McPhail, L. C. & Snyderman, R. Redistribution of protein kinase C activity in human monocytes: correlation with activation of the respiratory burst. J. Immunol. 135, 3411-3416 (1985).
40. Yung, B. Y., Hsiao, T. F., Wei, L. L. & Hui, E. K. Sphinganine potentiation of dimethyl sulfoxide-induced granulocyte differentiation, increase of alkaline phosphatase activity and decrease of protein kinase C activity in a human leukemia cell line (HL-60). Biochem. Biophys. Res. Commun. 199, 888-896 (1994).
41. Chakrabarti, S. R. & Nucifora, G. The leukemia-associated gene TEL encodes a transcription repressor which associates with SMRT and mSin3A. Biochem. Biophys. Res. Commun. 264, 871-877 (1999).
42. Bernier-Villamor, V., Sampson, D. A., Matunis, M. J. & Lima, C. D. Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108, 345-356 (2002).
43. Knipscheer, P. et al. Ubc9 sumoylation regulates SUMO target discrimination. Mol. Cell 31, 371-382 (2008).
44. Chakrabarti, S. R. et al. Modulation of TEL transcription activity by interaction with the ubiquitin-conjugating enzyme UBC9. Proc. Natl Acad. Sci. USA 96, 7467-7472 (1999).
45. Kato, H. K., Kassai, H., Watabe, A. M., Aiba, A. & Manabe, T. Functional coupling of the metabotropic glutamate receptor, InsP3 receptor and L-type Ca2+ channel in mouse CA1 pyramidal cells. J. Physiol. 590, 3019-3034 (2012).
46. Plotkin, J. L. et al. Regulation of dendritic calcium release in striatal spiny projection neurons. J. Neurophysiol. 110, 2325-2336 (2013).
47. Su, Y. F., Yang, T., Huang, H., Liu, L. F. & Hwang, J. Phosphorylation of Ubc9 by Cdk1 enhances SUMOylation activity. PLoS ONE 7, e34250 (2012).
48. Jakobs, A. et al. Ubc9 fusion-directed SUMOylation (UFDS): a method to analyze function of protein SUMOylation. Nat. Methods 4, 245-250 (2007).
49. Martin, S., Bouschet, T., Jenkins, E. L., Nishimune, A. & Henley, J. M. Bidirectional regulation of kainate receptor surface expression in hippocampal neurons. J. Biol. Chem. 283, 36435-36440 (2008).
50. Martin, S. et al. Corticosterone alters AMPAR mobility and facilitates bidirectional synaptic plasticity. PLoS ONE 4 (2009).
51. Nakamura, Y., Iga, K., Shibata, T., Shudo, M. & Kataoka, K. Glial plasmalemmal vesicles: a subcellular fraction from rat hippocampal homogenate distinct from synaptosomes. Glia 9, 48-56 (1993).
52. Feligioni, M., Holman, D., Haglerod, C., Davanger, S. & Henley, J. M. Ultrastructural localisation and differential agonist-induced regulation of AMPA and kainate receptors present at the presynaptic active zone and postsynaptic density. J. Neurochem. 99, 549-560 (2006).
53. Lee, Y. J. et al. SUMOylation participates in induction of ischemic tolerance. J. Neurochem. 109, 257-267 (2009).
54. Rottach, A., Kremmer, E., Nowak, D., Leonhardt, H. & Cardoso, M. C. Generation and characterization of a rat monoclonal antibody specific for multiple red fluorescent proteins. Hybridoma 27, 337-343 (2008).
55. Martin, S., Vincent, J. P. & Mazella, J. Recycling ability of the mouse and the human neurotensin type 2 receptors depends on a single tyrosine residue. J. Cell Sci. 115, 165-173 (2002).