Presynaptic spinophilin tunes neurexin signalling to control active zone architecture and function

Nature Communications

Volumn 6, Issue , 2015, Pages

  Muhammad, Karzan ^a,b,g   Reddy Alla, Suneel ^a,b   Driller, Jan H ^a   Schreiner, Dietmar ^c   Rey, Ulises ^b   Böhme, Mathias A ^b   Hollmann, Christina ^b   Ramesh, Niraja ^a   Depner, Harald ^a,b   Lützkendorf, Janine ^b   Matkovic, Tanja ^a,b   Götz, Torsten ^a,b   Bergeron, Dominique D ^b   Schmoranzer, Jan ^a,d   Goettfert, Fabian ^e   Holt, Mathew ^f   Wahl, Markus C ^a   Hell, Stefan W ^e   Scheiffele, Peter ^c   Walter, Alexander M ^b,d   Loll, Bernhard ^a   Sigrist, Stephan J ^a,b   more..

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSITY OF BASEL   (Switzerland)

^d LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^e MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^f DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^g MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE STRING PROTEIN; GLUTAMATE RECEPTOR; HORSERADISH PEROXIDASE; LIPRIN ALPHA; NEUREXIN; NEUREXIN 1; NEUROLIGIN; NEUROLIGIN 1; PDZ PROTEIN; PROTEIN; SPINOPHILIN; SPN PROTEIN; SYD 1 PROTEIN; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; DROSOPHILA PROTEIN; DSYD1 PROTEIN, DROSOPHILA; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; NEURABIN; NRX PROTEIN, DROSOPHILA;

CHEMICAL BINDING; FLY; GENE; GENE EXPRESSION; LIGNIN; MUTATION; PHENOTYPE; PROBABILITY; PROTEIN;

ACTION POTENTIAL; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DROSOPHILA; EXOCYTOSIS; FEMALE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE EXPRESSION; GENETIC CONSERVATION; IMMUNOPRECIPITATION; LIGAND BINDING; MALE; MICROSCOPY; MOTONEURON; NONHUMAN; NULL ALLELE; OPEN READING FRAME; PDZ DOMAIN; PHENOTYPE; POINT MUTATION; POSTSYNAPTIC DENSITY; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STIMULATED EMISSION DEPLETION MICROSCOPY; UPREGULATION; ANIMAL; METABOLISM; SYNAPSE; ULTRASTRUCTURE;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GTPASE-ACTIVATING PROTEINS; MALE; MICROFILAMENT PROTEINS; NERVE TISSUE PROTEINS; PDZ DOMAINS; SYNAPSES;

EID: 84959013884     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9362     Document Type: Article

References (70)

1. Sudhof, T. C. The presynaptic active zone. Neuron 75, 11-25 (2012).
2. Peled, E. S. & Isacoff, E. Y. Optical quantal analysis of synaptic transmission in wild-type and rab3-mutant Drosophila motor axons. Nat. Neurosci. 14, 519-526 (2011).
3. Melom, J. E., Akbergenova, Y., Gavornik, J. P. & Littleton, J. T. Spontaneous and evoked release are independently regulated at individual active zones. J. Neurosci. 33, 17253-17263 (2013).
4. Holderith, N. et al. Release probability of hippocampal glutamatergic terminals scales with the size of the active zone. Nat. Neurosci. 15, 988-997 (2012).
5. Dai, Y. et al. SYD-2 Liprin-alpha organizes presynaptic active zone formation through ELKS. Nat. Neurosci. 9, 1479-1487 (2006).
6. Kittel, R. J. et al. Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science 312, 1051-1054 (2006).
7. Spangler, S. A. & Hoogenraad, C. C. Liprin-α proteins: scaffold molecules for synapse maturation. Biochem. Soc. Trans. 35, 1278-1282 (2007).
8. Dean, C. et al. Neurexin mediates the assembely of presyanptic terminals. Nat. Neurosci. 6, 708-716 (2003).
9. Scheiffele, P., Fan, J., Choih, J., Fetter, R. & Serafini, T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101, 657-669 (2000).
10. Hu, Z. et al. Neurexin and neuroligin mediate retrograde synaptic inhibition in C. elegans. Science 337, 980-984 (2012).
11. Banovic, D. et al. Drosophila neuroligin 1 promotes growth and postsynaptic differentiation at glutamatergic neuromuscular junctions. Neuron 66, 724-738 (2010).
12. Knight, D., Xie, W. & Boulianne, G. L. Neurexins and neuroligins: recent insights from invertebrates. Mol. Neurobiol. 44, 426-440 (2011).
13. Owald, D. et al. Cooperation of Syd-1 with Neurexin synchronizes pre-with postsynaptic assembly. Nat. Neurosci. 15, 1219-1226 (2012).
14. Chen, Y. C. et al. Drosophila neuroligin 2 is required presynaptically and postsynaptically for proper synaptic differentiation and synaptic transmission. J. Neurosci. 32, 16018-16030 (2012).
15. Li, J., Ashley, J., Budnik, V. & Bhat, M. A. Crucial role of Drosophila neurexin in proper active zone apposition to postsynaptic densities, synaptic growth, and synaptic transmission. Neuron 55, 741-755 (2007).
16. Zeng, X. et al. Neurexin-1 is required for synapse formation and larvae associative learning in Drosophila. FEBS Lett. 581, 2509-2516 (2007).
17. Owald, D. et al. A Syd-1 homologue regulates pre- and postsynaptic maturation in Drosophila. J. Cell Biol. 188, 565-579 (2010).
18. Wentzel, C. et al. mSYD1A, a mammalian synapse-defective-1 protein, regulates synaptogenic signalling and vesicle docking. Neuron 78, 1012-1023 (2013).
19. Collins, C. A. & DiAntonio, A. Synaptic development: insights from Drosophila. Curr. Opin. Neurobiol. 17, 35-42 (2007).
20. Owald, D. & Sigrist, S. J. Assembling the presynaptic active zone. Curr. Opin. Neurobiol. 19, 311-318 (2009).
21. Fouquet, W. et al. Maturation of active zone assembly by Drosophila Bruchpilot. J. Cell Biol. 186, 129-145 (2009).
22. Depner, H., Lutzkendorf, J., Babkir, H. A., Sigrist, S. J. & Holt, M. G. Differential centrifugation-based biochemical fractionation of the Drosophila adult CNS. Nat. Protoc. 9, 2796-2808 (2014).
23. Parks, A. L. et al. Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat. Genet. 36, 288-292 (2004).
24. Allen, P. B., Ouime, C. C. & Greengard, P. Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc. Natl Acad. Sci. USA 94, 9956-9961 (1997).
25. Nakanishi, H. et al. Neurabin a novel neural tissue-specific actin filamentbinding protein involved in neurite formation. J. Cell Biol. 139, 951-961 (1997).
26. Muly, E. C. et al. Subcellular distribution of neurabin immunolabelling in primate prefrontal cortex: comparison with spinophilin. Cereb. Cortex 14, 1398-1407 (2004).
27. Muly, E. C., Smith, Y., Allen, P. & Greengard, P. Subcellular distribution of spinophilin immunolabelling in primate prefrontal cortex: localization to and within dendritic spines. J. Comp. Neurol. 469, 185-197 (2004).
28. Qin, G. et al. Four different subunits are essential for expressing the synaptic glutamate receptor at neuromuscular junctions of Drosophila. J. Neurosci. 25, 3209-3218 (2005).
29. Venken, K. J., He, Y., Hoskins, R. A. & Bellen, H. J. P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314, 1747-1751 (2006).
30. Liu, K. S. et al. RIM-binding protein, a central part of the active zone, is essential for neurotransmitter release. Science 334, 1565-1569 (2011).
31. Gottfert, F. et al. Coaligned dual-channel STED nanoscopy and molecular diffusion analysis at 20nm resolution. Biophys. J. 105, L01-L03 (2013).
32. Gustafsson, M. G. et al. Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys. J. 94, 4957-4970 (2008).
33. Schmid, A. et al. Activity-dependent site-specific changes of glutamate receptor composition in vivo. Nat. Neurosci. 11, 659-666 (2008).
34. Schuster, C. M., Davis, G. W., Fetter, R. D. & Goodman, C. S. Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth. Neuron 17, 641-654 (1996).
35. Kwon, H. B. et al. Neuroligin-1-dependent competition regulates cortical synaptogenesis and synapse number. Nat. Neurosci. 15, 1667-1674 (2012).
36. Sun, M. et al. Genetic interaction between Neurexin and CAKI/CMG is important for synaptic function in Drosophila neuromuscular junction. Neurosci. Res. 64, 362-371 (2009).
37. 2+-independent neurexin kinase. Cell 133, 328-339 (2008).
38. Ataman, B. et al. Nuclear trafficking of Drosophila Frizzled-2 during synapse development requires the PDZ protein dGRIP. Proc. Natl Acad. Sci. USA 103, 7841-7846 (2006).
39. Doyle, D. A. et al. Crystal structures of a complexed and peptide-free membrane protein-binding domain: molecular basis of peptide recognition by PDZ. Cell 85, 1067-1076 (1996).
40. Peled, E. S., Newman, Z. L. & Isacoff, E. Y. Evoked and spontaneous transmission favored by distinct sets of synapses. Curr. Biol. 24, 484-493 (2014).
41. Missler, M., Sudhof, T. C. & Biederer, T. Synaptic cell adhesion. Cold Spring Harb. Perspect. Biol. 4, a005694 (2012).
42. Sudhof, T. C. Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455, 903-911 (2008).
43. Feng, J. et al. Spinophilin regulates the formation and function of dendritic spines. Proc. Natl Acad. Sci. USA 97, 9287-9292 (2000).
44. Terry-Lorenzo, R. T. et al. Neurabin/protein phosphatase-1 complex regulates dendritic spine morphogenesis and maturation. Mol. Biol. Cell. 16, 2349-2362 (2005).
45. Allen, P. B. et al. Distinct roles for spinophilin and neurabin in dopaminemediated plasticity. Neuroscience 140, 897-911 (2006).
46. Sarrouilhe, D., di Tommaso, A., Metaye, T. & Ladeveze, V. Spinophilin: from partners to functions. Biochimie 88, 1099-1113 (2006).
47. Patel, M. R. et al. Hierarchical assembly of presynaptic components in defined C. elegans synapses. Nat. Neurosci. 9, 1488-1498 (2006).
48. Taru, H. & Jin, Y. The Liprin homology domain is essential for the homomeric interaction of SYD-2/Liprin-alpha protein in presynaptic assembly. J. Neurosci. 31, 16261-16268 (2011).
49. Chia, P. H., Li, P. & Shen, K. Cell biology in neuroscience: cellular and molecular mechanisms underlying presynapse formation. J. Cell Biol. 203, 11-22 (2013).
50. Ou, C. Y. & Shen, K. Setting up presynaptic structures at specific positions. Curr. Opin. Neurobiol. 20, 489-493 (2010).
51. Dai, S., Hall, D. D. & Hell, J. W. Supramolecular assemblies and localized regulation of voltage-gated ion channels. Physiol. Rev. 89, 411-452 (2009).
52. Chia, P. H., Patel, M. R. & Shen, K. NAB-1 instructs synapse assembly by linking adhesion molecules and F-actin to active zone proteins. Nat. Neurosci. 15, 234-242 (2012).
53. Penzes, P. et al. The neuronal Rho-GEF kalirin-7 interacts with PDZ domain-containing proteins and regulates dendritic morphogenesis. Neuron 29, 229-242 (2001).
54. Sarrouilhe, D. & Ladeveze, V. The tumour suppressor function of the scaffolding protein spinophilin. Atlas Genet. Cytogenet. Oncol. Haematol. 18, 691-700 (2014).
55. Buchsbaum, R. J., Connolly, B. A. & Feig, L. A. Regulation of p70 S6 kinase by complex formation between the Rac guanine nucleotide exchange factor (Rac-GEF) Tiam1 and the scaffold spinophilin. J. Biol. Chem. 278, 18833-18841 (2003).
56. Hata, Y., Buts, S. & Sudhof, T. C. CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J. Neurosci. 16, 2488-2494 (1996).
57. Biederer, T. & Sudhof, T. C. Mints as adaptors. Direct binding to neurexins and recruitment of munc18. J. Biol. Chem. 275, 39803-39806 (2000).
58. Grootjans, J. J., Reekmans, G., Ceulemans, H. & David, G. Syntenin-syndecan binding requires syndecan-synteny and the co-operation of both PDZ domains of syntenin. J. Biol. Chem. 275, 19933-19941 (2000).
59. Kurschnera, C., Mermelsteinb, P. G., Holdena, W. T. & Surmeierb, D. J. CIPP, a novel multivalent PDZ domain protein, selectively interacts with Kir4.0 family members, NMDA Receptor subunits, neurexins, and neuroligins. Mol. Cell. Neurosci. 11, 161-172 (1998).
60. 2+ channels to synaptic vesicle exocytosis. Nature 10, 939-948 (2003).
61. Dudanova, I., Tabuchi, K., Rohlmann, A., Sudhof, T. C. & Missler, M. Deletion of alpha-neurexins does not cause a major impairment of axonal pathfinding or synapse formation. J. Comp. Neurol. 502, 261-274 (2007).
62. Craig, A. M. & Kang, Y. Neurexin-neuroligin signalling in synapse development. Curr. Opin. Neurobiol. 17, 43-52 (2007).
63. Varoqueaux, F. et al. Neuroligins determine synapse maturation and function. Neuron 51, 741-754 (2006).
64. O'Connora, V. M., Shamotienkoa, O., Grishinb, E. & Betz, H. On the structure of the 'synaptosecretosome' Evidence for a neurexin/synaptotagmin/syntaxin/Ca2+ channel complex. FEBS Lett. 326, 255-260 (1993).
65. Zhang, W. et al. Extracellular domains of alpha-neurexins participate in regulating synaptic transmission by selectively affecting N- and P/Q-type Ca2+ channels. J. Neurosci. 25, 4330-4342 (2005).
66. Dudanova, I. et al. Important contribution of alpha-neurexins to Ca2+triggered exocytosis of secretory granules. J. Neurosci. 26, 10599-10613 (2006).
67. Sigrist, S. J., Reiff, D. F., Thiel, P. R., Steinert, J. R. & Schuster, C. M. Experiencedependent strengthening of Drosophila neuromuscular junctions. J. Neurosci. 23, 6546-6556 (2003).
68. Keegan, J., Schmerer, M., Ring, B. & Garza, D. The 62E early-late puff of Drosophila contains D-spinophilin, an ecdysone-inducible PDZ-domain protein dynamically expressed during metamorphosis. Genet. Res. 77, 27-39 (2001).
69. Andlauer, T. F. & Sigrist, S. J. Quantitative analysis of Drosophila larval neuromuscular junction morphology. Cold Spring Harb. Protoc. 2012, 490-493 (2012).
70. Mockli, N. & Auerbach, D. Quantitative beta-galactosidase assay suitable for high-throughput applications in the yeast two-hybrid system. Biotechniques 36, 872-876 (2004).