The inhibitory effect of α/β-hydrolase domain-containing 6 (ABHD6) on the surface targeting of GluA2- and GluA3-containing AMPA receptors

Frontiers in Molecular Neuroscience

Volumn 10, Issue , 2017, Pages

  Wei, Mengping ^a   Jia, Moye ^a   Zhang, Jian ^a   Yu, Lulu ^a   Zhao, Yunzhi ^a   Chen, Yingqi ^a   Ma, Yimeng ^a   Zhang, Wei ^b   Shi, Yun S ^c   Zhang, Chen ^a  

^a PEKING UNIVERSITY   (China)

^b HEBEI MEDICAL UNIVERSITY   (China)

^c NANJING UNIVERSITY   (China)

Author keywords

ABHD6; AMPA receptor; Glutamates; Protein protein interactions; Receptor trafficking

Indexed keywords

ALPHA BETA HYDROLASE DOMAIN CONTAINING 6; AMPA RECEPTOR; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 3; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; ARTICLE; CELL PERMEABILIZATION; CONFOCAL LASER SCANNING MICROSCOPY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; VOLTAGE CLAMP TECHNIQUE; WESTERN BLOTTING;

EID: 85018864670     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2017.00055     Document Type: Article

References (45)

1. Anggono, V., and Huganir, R. L. (2012). Regulation of AMPA receptor trafficking and synaptic plasticity. Curr. Opin. Neurobiol. 22, 461–469. doi: 10.1016/j.conb. 2011.12.006
2. Angulo, M. C., Lambolez, B., Audinat, E., Hestrin, S., and Rossier, J. (1997). Subunit composition, kinetic, and permeation properties of AMPA receptors in single neocortical nonpyramidal cells. J. Neurosci. 17, 6685–6696.
3. Bredt, D., and Nicholl, R. A. (2003). AMPA receptor trafficking at excitatory synapses. Neuron 40, 361–379. doi: 10.1016/S0896-6273(03)00640-8
4. Burnashev, N., Monyer, H., Seeburg, P. H., and Sakmann, B. (1992). Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 8, 189–198. doi: 10.1016/0896-6273(92) 90120-3
5. Cao, M., Xu, J., Shen, C., Kam, C., Huganir, R. L., and Xia, J. (2007). PICK1-ICA69 heteromeric BAR domain complex regulates synaptic targeting and surface expression of AMPA receptors. J. Neurosci. 27, 12945–12956. doi: 10.1523/JNEUROSCI.2040-07.2007
6. Chen, L., Bao, S., Qiao, X., and Thompson, R. F. (1999). Impaired cerebellar synapse maturation in waggler, a mutant mouse with a disrupted neuronal calcium channel gamma subunit. Proc. Natl. Acad. Sci. U.S.A. 96, 12132–12137. doi: 10.1073/pnas.96.21.12132
7. Chen, L., Chetkovich, D. M., Petralia, R. S., Sweeney, N. T., Kawasaki, Y., Wenthold, R. J., et al. (2000). Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408, 936–943. doi: 10.1038/35050030
8. Cheng, J., Dong, J., Cui, Y., Wang, L., Wu, B., and Zhang, C. (2012). Interacting partners of AMPA-type glutamate receptors. J. Mol. Neurosci. 48, 441–447. doi: 10.1007/s12031-012-9724-6
9. Coombs, I. D., Soto, D., Zonouzi, M., Renzi, M., Shelley, C., Farrant, M., et al. (2012). Cornichons modify channel properties of recombinant and glial AMPA receptors. J. Neurosci. 32, 9796–9804. doi: 10.1523/JNEUROSCI.0345-12. 2012
10. Erlenhardt, N., Yu, H., Abiraman, K., Yamasaki, T., Wadiche, J. I., Tomita, S., et al. (2016). Porcupine controls Hippocampal AMPAR levels, composition, and synaptic transmission. Cell Rep. 14, 782–794. doi: 10.1016/j.celrep.2015.1 2.078
11. Gill, M. B., Kato, A. S., Roberts, M. F., Yu, H., Wang, H., Tomita, S., et al. (2011). Cornichon-2 modulates AMPA receptor-transmembrane AMPA receptor regulatory protein assembly to dictate gating and pharmacology. J. Neurosci. 31, 6928–6938. doi: 10.1523/JNEUROSCI.6271-10.2011
12. Gill, M. B., Kato, A. S., Wang, H., and Bredt, D. S. (2012). AMPA receptor modulation by cornichon-2 dictated by transmembrane AMPA receptor regulatory protein isoform. Eur. J. Neurosci. 35, 182–194. doi: 10.1111/j.1460-9568.2011.07948.x
13. Gu, X., Mao, X., Lussier, M. P., Hutchison, M. A., Zhou, L., Hamra, F. K., et al. (2016a). AMPA receptor kinetics in hippocampal neurons. Nat. Commun. 6, 1–18. doi: 10.1038/ncomms10873
14. Gu, X., Mao, X., Lussier, M. P., Hutchison, M. A., Zhou, L., Hamra, F. K., et al. (2016b). GSG1L suppresses AMPA receptor-mediated synaptic transmission and uniquely modulates AMPA receptor kinetics in hippocampal neurons. Nat. Commun. 7:10873. doi: 10.1038/ncomms10873
15. Harmel, N., Cokic, B., Zolles, G., Berkefeld, H., Mauric, V., Fakler, B., et al. (2012). AMPA receptors commandeer an ancient cargo exporter for use as an auxiliary subunit for signaling. PLoS ONE 7:e30681. doi: 10.1371/journal.pone.0030681
16. Hashimoto, K., Fukaya, M., Qiao, X., Sakimura, K., Watanabe, M., and Kano, M. (1999). Impairment of AMPA receptor function in cerebellar granule cells of ataxic mutant mouse stargazer. J. Neurosci. 19, 6027–6036.
17. Henley, J. M., and Wilkinson, K. A. (2016). Synaptic AMPA receptor composition in development, plasticity and disease. Nat. Rev. Neurosci. 17, 337–350. doi: 10.1038/nrn.2016.37
18. Herring, B. E., Shi, Y., Suh, Y. H., Zheng, C. Y., Blankenship, S. M., Roche, K. W., et al. (2013). Cornichon proteins determine the subunit composition of synaptic AMPA receptors. Neuron 77, 1083–1096. doi: 10.1016/j.neuron.2013. 01.017
19. Hollmann, M., and Heinemann, S. (1994). Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31–108. doi: 10.1146/annurev.neuro.17.1.31
20. Huganir, R. L., and Nicoll, R. A. (2013). AMPARs and synaptic plasticity: the last 25 years. Neuron 80, 704–717. doi: 10.1016/j.neuron.2013.10.025
21. Jackson, A. C., and Nicoll, R. A. (2011). The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits. Neuron 70, 178–199. doi: 10.1016/j.neuron.2011.04.007
22. Jiang, W., Hua, R., Wei, M., Li, C., Qiu, Z., Yang, X., et al. (2015). An optimized method for high-titer lentivirus preparations without ultracentrifugation. Sci. Rep. 5:13875. doi: 10.1038/srep13875
23. Kato, A. S., Gill, M. B., Ho, M. T., Yu, H., Tu, Y., Siuda, E. R., et al. (2010). Hippocampal AMPA receptor gating controlled by both TARP and cornichon proteins. Neuron 68, 1082–1096. doi: 10.1016/j.neuron.2010.11.026
24. Keinänen, K., Wisden, W., Sommer, B., Werner, P., Herb, A., Verdoorn, T. A., et al. (1990). A family of AMPA-selective glutamate receptors. Science 249, 556–560. doi: 10.1126/science.2166337
25. Lee, J. C., Greig, A., Ravindranathan, A., Parks, T. N., and Rao, M. S. (1998). Molecular analysis of AMPA-specific receptors: subunit composition, editing, and calcium influx determination in small amounts of tissue. Brain Res. Protoc. 3, 142–154. doi: 10.1016/S1385-299X(98)00035-X
26. Letts, V. A., Felix, R., Biddlecome, G. H., Arikkath, J., Mahaffey, C. L., Valenzuela, A., et al. (1998). The mouse stargazer gene encodes a neuronal Ca2+-channel gamma subunit. Nat. Genet. 19, 340–347. doi: 10.1038/1228
27. Li, W., Xu, X., and Pozzo-Miller, L. (2016). Excitatory synapses are stronger in the hippocampus of Rett syndrome mice due to altered synaptic trafficking of AMPA-type glutamate receptors. Proc. Natl. Acad. Sci. U.S.A. 113, E1575– E1584. doi: 10.1073/pnas.1517244113
28. Lu, W., Shi, Y., Jackson, A. C., Bjorgan, K., During, M. J., Sprengel, R., et al. (2009). Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62, 254–268. doi: 10.1016/j.neuron.2009. 02.027
29. Mauric, V., Mölders, A., Harmel, N., Heimrich, B., Sergeeva, O. A., and Klöcker, N. (2013). Ontogeny repeats the phylogenetic recruitment of the cargo exporter cornichon into AMPA receptor signaling complexes. Mol. Cell. Neurosci. 56, 10–17. doi: 10.1016/j.mcn.2013.02.001
30. Milstein, A. D., and Nicoll, R. A. (2008). Regulation of AMPA receptor gating and pharmacology by TARP auxiliary subunits auxiliary subunits. Trends Pharmacol. Sci. 29, 333–339. doi: 10.1016/j.tips.2008.04.004
31. Priel, A., Kolleker, A., Ayalon, G., Gillor, M., Osten, P., and Stern-Bach, Y. (2005). Stargazin reduces desensitization and slows deactivation of the AMPA-type glutamate receptors. J. Neurosci. 25, 2682–2686. doi: 10.1523/JNEUROSCI. 4834-04.2005
32. Schwenk, J., Harmel, N., Brechet, A., Zolles, G., Berkefeld, H., Müller, C. S., et al. (2012). High-resolution proteomics unravel architecture and molecular diversity of native AMPA receptor complexes. Neuron 74, 621–633. doi: 10. 1016/j.neuron.2012.03.034
33. Schwenk, J., Harmel, N., Zolles, G., Bildl, W., Kulik, A., Heimrich, B., et al. (2009). Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors. Science 323, 1313–1319. doi: 10.1126/science.116 7852
34. Shi, Y., Lu, W., Milstein, A. D., and Nicoll, R. A. (2009). Report the stoichiometry of AMPA receptors and TARPs varies by neuronal cell type. Neuron 62, 633–640. doi: 10.1016/j.neuron.2009.05.016
35. Shi, Y., Suh, Y. H., Milstein, A. D., Isozaki, K., Schmid, S. M., Roche, K. W., et al. (2010). Functional comparison of the effects of TARPs and cornichons on AMPA receptor trafficking and gating. Proc. Natl. Acad. Sci. U. S. A. 107, 16315–16319. doi: 10.1073/pnas.1011706107
36. Terashima, A., Cotton, L., Dev, K. K., Meyer, G., Zaman, S., Duprat, F., et al. (2004). Regulation of synaptic strength and AMPA receptor subunit composition by PICK1. J. Neurosci. 24, 5381–5390. doi: 10.1523/JNEUROSCI.4378-03. 2004
37. Tomita, S., Sekiguchi, M., Wada, K., Nicoll, R. A., and Bredt, D. S. (2006). Stargazin controls the pharmacology of AMPA receptor potentiators. Proc. Natl. Acad. Sci. U.S.A. 103, 10064–10067.
38. Tomita, S., Shenoy, A., Fukata, Y., Nicoll, R. A., and Bredt, D. S. (2007). Stargazin interacts functionally with the AMPA receptor glutamate-binding module. Neuropharmacology 52, 87–91. doi: 10.1016/j.neuropharm.2006. 07.012
39. Vandenberghe, W., Nicoll, R. A., and Bredt, D. S. (2005). Stargazin is an AMPA receptor auxiliary subunit. Proc. Natl. Acad. Sci. U. S. A. 102, 485–490. doi: 10.1073/pnas.0408269102
40. Wei, M., Zhang, J., Jia, M., Yang, C., Pan, Y., Li, S., et al. (2016). α/β-Hydrolase domain-containing 6 (ABHD6) negatively regulates the surface delivery and synaptic function of AMPA receptors. Proc. Natl. Acad. Sci. U.S.A. 6:201524589. doi: 10.1073/pnas.1524589113
41. Xu, J., Wang, N., Luo, J., and Xia, J. (2016). Syntabulin regulates the trafficking of PICK1-containing vesicles in neurons. Sci. Rep. 6:20924. doi: 10.1038/srep 20924
42. Yang, X., Hou, D., Jiang, W., and Zhang, C. (2014). Intercellular protein-protein interactions at synapses. Protein Cell 5, 420–444. doi: 10.1007/s13238-014-0054-z
43. Zhang, C., Atasoy, D., Arac, D., Yang, X., Fucillo, M. V., Robison, A. J., et al. (2010). Neurexins physically and functionally interact with GABAA receptors. Neuron 66, 403–416. doi: 10.1016/j.neuron.2010.04.008
44. Zhang, C., Milunsky, J. M., Newton, S., Ko, J., Zhao, G., Maher, A., et al. (2009). A Neuroligin-4 missense mutation associated with autism impairs neuroligin-4 folding and ER export clinical evaluation. J. Neurosci. 29, 10843–10854. doi: 10.1523/JNEUROSCI.1248-09.2009
45. Ziff, E. B. (2007). TARPs and the AMPA receptor trafficking paradox. Neuron 53, 627–633. doi: 10.1016/j.neuron.2007.02.006