Presynaptic DLG regulates synaptic function through the localization of voltage-activated Ca2+ Channels

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Astorga, César ^a   Jorquera, Ramón A ^a,b   Ramírez, Mauricio ^a   Kohler, Andrés ^a   López, Estefanía ^a   Delgado, Ricardo ^c   Córdova, Alex ^a   Olguín, Patricio ^a   Sierralta, Jimena ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b Universidad Central del Caribe School of Medicine   (Puerto Rico)

^c UNIVERSITY OF CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

CAC PROTEIN, DROSOPHILA; CALCIUM CHANNEL; DISCS LARGE 1 PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; TUMOR SUPPRESSOR PROTEIN;

ACTION POTENTIAL; ANIMAL; DROSOPHILA MELANOGASTER; GENETICS; METABOLISM; PHYSIOLOGY; SYNAPSE;

ACTION POTENTIALS; ANIMALS; CALCIUM CHANNELS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; SYNAPSES; TUMOR SUPPRESSOR PROTEINS;

EID: 84985994308     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep32132     Document Type: Article

References (44)

1. Kim, E., Niethammer, M., Rothschild, A., Nung Jan, Y. & Sheng, M. Clustering of Shaker-type K+ channels by interaction with a family of membrane-associated guanylate kinases. Nature 378, 85-88 (1995).
2. Velthuis te, A. J. W., Admiraal, J. F. & Bagowski, C. P. Molecular evolution of the MAGUK family in metazoan genomes. BMC Evol Biol 7, 129-10 (2007).
3. Kim, E. & Sheng, M. PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5, 771-781 (2004).
4. Aoki, C. et al. Electron microscopic immunocytochemical detection of PSD-95, PSD-93, SAP-102, and SAP-97 at postsynaptic, presynaptic, and nonsynaptic sites of adult and neonatal rat visual cortex. Synapse 40, 239-257 (2001).
5. Woods, D. F. & Bryant, P. J. The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66, 451-464 (1991).
6. Chetkovich, D. M., Chen, L., Stocker, T. J., Nicoll, R. A. & Bredt, D. S. Phosphorylation of the postsynaptic density-95 (PSD-95)/discs large/zona occludens-1 binding site of stargazin regulates binding to PSD-95 and synaptic targeting of AMPA receptors. J. Neurosci. 22, 5791-5796 (2002).
7. Mendoza-Topaz, C. et al. DLGS97/SAP97 is Developmentally Upregulated and is required for Complex Adult Behaviors and Synapse Morphology and Function. Journal of Neuroscience 28, 304-314 (2008).
8. Lahey, T., Gorczyca, M., Jia, X. X. & Budnik, V. The Drosophila tumor suppressor gene dlg is required for normal synaptic bouton structure. Neuron 13, 823-835 (1994).
9. Budnik, V. et al. Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron 17, 627-640 (1996).
10. Karunanithi, S., Barclay, J. W., Brown, I. R., Robertson, R. M. & Atwood, H. L. Enhancement of presynaptic performance in transgenic Drosophila overexpressing heat shock protein Hsp70. Synapse 44, 8-14 (2002).
11. Woods, D. F. & Bryant, P. J. Molecular cloning of the lethal(1)discs large-1 oncogene of Drosophila. Developmental Biology 134, 222-235 (1989).
12. Thomas, U. et al. Synaptic clustering of the cell adhesion molecule fasciclin II by discs-large and its role in the regulation of presynaptic structure. Neuron 19, 787-799 (1997).
13. Feng, Y., Ueda, A. & Wu, C.-F. A modified minimal hemolymph-like solution, HL3.1, for physiological recordings at the neuromuscular junctions of normal and mutant Drosophila larvae. J Neurogenet 18, 377-402 (2004).
14. Guan, B., Hartmann, B., Kho, Y. H., Gorczyca, M. & Budnik, V. The Drosophila tumor suppressor gene, dlg, is involved in structural plasticity at a glutamatergic synapse. CURBIO 6, 695-706 (1996).
15. Ataman, B. et al. Nuclear trafficking of Drosophila Frizzled-2 during synapse development requires the PDZ protein dGRIP. Proceedings of the National Academy of Sciences 103, 7841-7846 (2006).
16. Bachmann, A. et al. A Perisynaptic Menage a Trois between Dlg, DLin-7, and Metro Controls Proper Organization of Drosophila Synaptic Junctions. Journal of Neuroscience 30, 5811-5824 (2010).
17. DiAntonio, A., Petersen, S. A., Heckmann, M. & Goodman, C. S. Glutamate receptor expression regulates quantal size and quantal content at the Drosophila neuromuscular junction. Journal of Neuroscience 19, 3023-3032 (1999).
18. Pawlu, C., DiAntonio, A. & Heckmann, M. Postfusional control of quantal current shape. Neuron 42, 607-618 (2004).
19. DiAntonio, A. In The Fly Neuromuscular Junction: Structure and Function Second Edition 75, 165-179 (Elsevier, 2006).
20. Chen, K. & Featherstone, D. E. Discs-large (DLG) is clustered by presynaptic innervation and regulates postsynaptic glutamate receptor subunit composition in Drosophila. BMC Biol 3, 1 (2005).
21. Koh, Y. H., Popova, E., Thomas, U., Griffith, L. C. & Budnik, V. Regulation of DLG localization at synapses by CaMKII-dependent phosphorylation. Cell 98, 353-363 (1999).
22. Morimoto, T., Nobechi, M., Komatsu, A., Miyakawa, H. & Nose, A. Subunit-specific and homeostatic regulation of glutamate receptor localization by CaMKII in Drosophila neuromuscular junctions. NSC 165, 1284-1292 (2010).
23. Shin, H., Hsueh, Y. P., Yang, F. C., Kim, E. & Sheng, M. An intramolecular interaction between Src homology 3 domain and guanylate kinase-like domain required for channel clustering by postsynaptic density-95/SAP90. J. Neurosci. 20, 3580-3587 (2000).
24. Wu, H. et al. Intramolecular interactions regulate SAP97 binding to GKAP. The EMBO Journal 19, 5740-5751 (2000).
25. Zucker, R. S. The calcium hypothesis and modulation of transmitter release by hyperpolarizing pulses. Biophysj 52, 347-350 (1987).
26. Zucker, R. S. & Regehr, W. G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355-405 (2002).
27. Jan, L. Y. & Jan, Y. N. Properties of the larval neuromuscular junction in Drosophila melanogaster. The Journal of Physiology 262, 189-214 (1976).
28. Peled, E. S. & Isacoff, E. Y. Optical quantal analysis of synaptic transmission in wild-type and rab3-mutant Drosophila motor axons. Nature Publishing Group 14, 519-526 (2011).
29. Eggermann, E., Bucurenciu, I., Goswami, S. P. & Jonas, P. Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses. Nat. Rev. Neurosci. 13, 7-21 (2011).
30. Kawasaki, F., Felling, R. & Ordway, R. W. A temperature-sensitive paralytic mutant defines a primary synaptic calcium channel in Drosophila. J. Neurosci. 20, 4885-4889 (2000).
31. Kawasaki, F., Zou, B., Xu, X. & Ordway, R. W. Active zone localization of presynaptic calcium channels encoded by the cacophony locus of Drosophila. J. Neurosci. 24, 282-285 (2004).
32. Dickman, D. K., Kurshan, P. T. & Schwarz, T. L. Mutations in a Drosophila alpha2delta voltage-gated calcium channel subunit reveal a crucial synaptic function. J. Neurosci. 28, 31-38 (2008).
33. Yao, C.-K., Verstreken, P., Ohyama, T. & Bellen, H. J. Straightjacket is required for the synaptic stabilization of cacophony, a voltagegated calcium channel alpha1 subunit. The Journal of Cell Biology 181, 157-170 (2008).
34. Bichet, D. et al. The I-II loop of the Ca2+ channel alpha1 subunit contains an endoplasmic reticulum retention signal antagonized by the beta subunit. Neuron 25, 177-190 (2000).
35. Butz, S., Okamoto, M. & Südhof, T. C. A tripartite protein complex with the potential to couple synaptic vesicle exocytosis to cell adhesion in brain. Cell 94, 773-782 (1998).
36. Lee, S., Fan, S., Makarova, O., Straight, S. & Margolis, B. A novel and conserved protein-protein interaction domain of mammalian Lin-2/CASK binds and recruits SAP97 to the lateral surface of epithelia. Molecular and Cellular Biology 22, 1778-1791 (2002).
37. Bachmann, A. et al. Cell type-specific recruitment of Drosophila Lin-7 to distinct MAGUK-based protein complexes defines novel roles for Sdt and Dlg-S97. Journal of Cell Science 117, 1899-1909 (2004).
38. Südhof, T. C. Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 80, 675-690 (2013).
39. Muller, M., Liu, K. S. Y., Sigrist, S. J. & Davis, G. W. RIM Controls Homeostatic Plasticity through Modulation of the Readily- Releasable Vesicle Pool. Journal of Neuroscience 32, 16574-16585 (2012).
40. Muhammad, K. et al. Presynaptic spinophilin tunes neurexin signalling to control active zone architecture and function. Nat Commun 6, 8362 (2015).
41. Mendoza, C. et al. Novel isoforms of Dlg are fundamental for neuronal development in Drosophila. J. Neurosci. 23, 2093-2101 (2003).
42. Dietzl, G. et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156 (2007).
43. Mallart, A. & Martin, A. R. An analysis of facilitation of transmitter release at the neuromuscular junction of the frog. The Journal of Physiology 193, 679-644 (1967).
44. Betz, W. J. Depression of transmitter release at the neuromuscular junction of the frog. The Journal of Physiology 206, 629-644 (1970).