Synaptojanin cooperates in vivo with endophilin through an unexpected mechanism

eLife

Volumn 2015, Issue 4, 2015, Pages 1-50

  Dong, Yongming ^a   Gou, Yueyang ^b   Li, Yi ^b   Liu, Yan ^a   Bai, Jihong ^a,c  

^a Fred Hutchinson Cancer Research Center   (United States)

^b SICHUAN UNIVERSITY   (China)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

5 phosphatase; C. elegans; Endophilin; PI(4,5)P2; Proline rich domain; Sac1 phosphatase; Synaptic transmission; Synaptic vesicle; Synaptojanin

Indexed keywords

ENDOPHILIN; RECOMBINANT PROTEIN; SYNAPTOJANIN; DNA BINDING PROTEIN; MARINER TRANSPOSASES; NERVE PROTEIN; PHOSPHATASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TRANSPOSASE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENDOCYTOSIS; GENE INSERTION; GENETIC TRANSFORMATION; IMAGE ANALYSIS; IN VIVO STUDY; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; RECOMBINANT PLASMID; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; TRANSGENE; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; WHOLE CELL PATCH CLAMP; ANIMAL; GENE TRANSFER; GENETICS; MICROINJECTION; PHYSIOLOGY; SYNAPSE; TRANSGENIC ANIMAL;

CAENORHABDITIS ELEGANS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; DNA-BINDING PROTEINS; ENDOCYTOSIS; GENE TRANSFER TECHNIQUES; MICROINJECTIONS; NERVE TISSUE PROTEINS; PHOSPHORIC MONOESTER HYDROLASES; SYNAPSES; SYNAPTIC TRANSMISSION; TRANSPOSASES;

EID: 84929158363     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.05660     Document Type: Article

References (56)

1. Bai, J., Wang, C.T., Richards, D.A., Jackson, M.B., and Chapman, E.R. (2004). Fusion pore dynamics are regulated by synaptotagmin*t-SNARE interactions. Neuron 41, 929942.
2. Bai, J., Hu, Z., Dittman, J.S., Pym, E.C.G., and Kaplan, J.M. (2010). Endophilin functions as a membrane-bending molecule and is delivered to endocytic zones by exocytosis. Cell 143, 430-441.
3. Balaji, J., and Ryan, T.A. (2007). Single-vesicle imaging reveals that synaptic vesicle exocytosis and endocytosis are coupled by a single stochastic mode. Proc Natl Acad Sci USA 104, 20576-20581.
4. Betz, W.J., Mao, F., and Smith, C.B. (1996). Imaging exocytosis and endocytosis. Curr. Opin. Neurobiol. 6, 365-371.
5. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
6. Carlton, J.G., and Cullen, P.J. (2005). Coincidence detection in phosphoinositide signaling. Trends Cell Biol. 15, 540-547.
7. Ch'ng, Q., Sieburth, D., and Kaplan, J.M. (2008). Profiling synaptic proteins identifies regulators of insulin secretion and lifespan. PLoS Genet. 4,e1000283.
8. Chang-Ileto, B., Frere, S.G., Chan, R.B., Voronov, S.V., Roux, A., and Di Paolo, G. (2011). Synaptojanin 1-mediated PI(4,5)P2 hydrolysis is modulated by membrane curvature and facilitates membrane fission. Dev. Cell 20, 206-218.
9. Cremona, O., and De Camilli, P. (2001). Phosphoinositides in membrane traffic at the synapse. J. Cell. Sci. 114, 1041-1052.
10. Cremona, O., Di Paolo, G., Wenk, M.R., Luthi, A., Kim, W.T., Takei, K., Daniell, L., Nemoto, Y., Shears, S.B., Flavell, R.A., et al. (1999). Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99, 179-188.
11. De Camilli, P., and Takei, K. (1996). Molecular mechanisms in synaptic vesicle endocytosis and recycling. Neuron 16, 481-486.
12. de Heuvel, E., Bell, A.W., Ramjaun, A.R., Wong, K., Sossin, W.S., and McPherson, P.S. (1997). Identification of the major synaptojanin-binding proteins in brain. J. Biol. Chem. 272, 8710-8716.
13. Dickman, D.K., Horne, J.A., Meinertzhagen, I.A., and Schwarz, T.L. (2005). A slowed classical pathway rather than kiss-and-run mediates endocytosis at synapses lacking synaptojanin and endophilin. Cell 123, 521-533.
14. Dittman, J., and Kaplan, J.M. (2006) Factors regulating the abundance and localization of synaptobrevin in the plasma membrane. Proc. Natl. Acad. Sci. U.S.A. 103, 11399-11404.
15. Dittman, J., and Ryan, T.A. (2009). Molecular circuitry of endocytosis at nerve terminals. Annu. Rev. Cell Dev. Biol. 25, 133-160.
16. Evergren, E., Gad, H., Walther, K., Sundborger, A., Tomilin, N., and Shupliakov, O. (2007). Intersectin is a negative regulator of dynamin recruitment to the synaptic endocytic zone in the central synapse. J. Neurosci. 27, 379-390.
17. Farsad, K., Ringstad, N., Takei, K., Floyd, S.R., Rose, K., and De Camilli, P. (2001). Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J. Cell Biol. 155, 193-200.
18. Frøkjaer-Jensen, C., Davis, M.W., Ailion, M., and Jorgensen, E.M. (2012). Improved Mos1- mediated transgenesis in C. elegans. Nat. Methods 9, 117-118.
19. Gad, H., Ringstad, N., Löw, P., Kjaerulff, O., Gustafsson, J., Wenk, M., Di Paolo, G., Nemoto, Y., Crun, J., Ellisman, M.H., et al. (2000). Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron 27, 301-312.
20. Galic, M., Jeong, S., Tsai, F.-C., Joubert, L.-M., Wu, Y.I., Hahn, K.M., Cui, Y., and Meyer, T. (2012). External push and internal pull forces recruit curvature-sensing N-BAR domain proteins to the plasma membrane. Nat. Cell Biol. 14, 874-881.
21. Gallop, J.L., Jao, C.C., Kent, H.M., Butler, P.J.G., Evans, P.R., Langen, R., and McMahon, H.T. (2006). Mechanism of endophilin N-BAR domain-mediated membrane curvature. Embo J. 25, 2898-2910.
22. George, A.A., Hayden, S., Holzhausen, L.C., Ma, E.Y., Suzuki, S.C., and Brockerhoff, S.E. (2014). Synaptojanin 1 is required for endolysosomal trafficking of synaptic proteins in cone photoreceptor inner segments. PLoS ONE 9, e84394.
23. Guo, S. (1999). SAC1-like Domains of Yeast SAC1, INP52, and INP53 and of Human Synaptojanin Encode Polyphosphoinositide Phosphatases. Journal of Biological Chemistry 274, 12990-12995.
24. Harris, T.W., Hartwieg, E., Horvitz, H.R., and Jorgensen, E.M. (2000). Mutations in Synaptojanin Disrupt Synaptic Vesicle Recycling. J. Cell Biol. 150, 589-599.
25. Hughes, W.E., Cooke, F.T., and Parker, P.J. (2000). Sac phosphatase domain proteins. Biochem. J. 350 Pt 2, 337-352.
26. Irie, F., Okuno, M., Pasquale, E.B., and Yamaguchi, Y. (2005). EphrinB-EphB signalling regulates clathrin-mediated endocytosis through tyrosine phosphorylation of synaptojanin 1. Nat. Cell Biol. 7, 501-509.
27. Kay, A.R., Alfonso, A., Alford, S., Cline, H.T., Holgado, A.M., Sakmann, B., Snitsarev, V.A., Stricker, T.P., Takahashi, M., and Wu, L.G. (1999). Imaging synaptic activity in intact brain and slices with FM1-43 in C. elegans, lamprey, and rat. Neuron. 24, 809-17.
28. Krebs, C.E., Karkheiran, S., Powell, J.C., Cao, M., Makarov, V., Darvish, H., Di Paolo, G., Walker, R.H., Shahidi, G.A., Buxbaum, J.D., et al. (2013). The Sac1 domain of SYNJ1 identified mutated in a family with early-onset progressive Parkinsonism with generalized seizures. Hum. Mutat. 34, 1200-1207.
29. Lee, S.Y., Wenk, M.R., Kim, Y., Nairn, A.C., and De Camilli, P. (2004). Regulation of synaptojanin 1 by cyclin-dependent kinase 5 at synapses. Proc. Natl. Acad. Sci. U.S.A. 101, 546-551.
30. Liewald, J.F., Brauner, M., Stephens, G.J., Bouhours, M., Schultheis, C., Zhen, M., and Gottschalk, A. (2008). Optogenetic analysis of synaptic function. Nat. Methods. 5, 895-902.
31. Liu, Q., Hollopeter, G., and Jorgensen, E.M. (2009). Graded synaptic transmission at the Caenorhabditis elegans neuromuscular junction. Proc. Natl. Acad. Sci. U.S.A. 106, 10823-10828.
32. Lomasney, J.W., Cheng, H.F., Wang, L.P., Kuan, Y., Liu, S., Fesik, S.W., and King, K. (1996). Phosphatidylinositol 4,5-bisphosphate binding to the pleckstrin homology domain of phospholipase C-delta1 enhances enzyme activity. J. Biol. Chem. 271, 25316-25326.
33. Majerus, P.W., and York, J.D. (2009). Phosphoinositide phosphatases and disease. J. Lipid Res. 50 Suppl, S249-S254.
34. Manford, A., Xia, T., Saxena, A.K., Stefan, C., Hu, F., Emr, S.D., and Mao, Y. (2010). Crystal structure of the yeast Sac1: implications for its phosphoinositide phosphatase function. Embo J. 29, 1489-1498.
35. Mani, M., Lee, S.Y., Lucast, L., Cremona, O., Di Paolo, G., De Camilli, P., and Ryan, T.A. (2007). The Dual Phosphatase Activity of Synaptojanin1 Is Required for Both Efficient Synaptic Vesicle Endocytosis and Reavailability at Nerve Terminals. Neuron 56, 1004-1018.
36. McPherson, P.S., Garcia, E.P., Slepnev, V.I., David, C., Zhang, X., Grabs, D., Sossin, W.S., Bauerfeind, R., Nemoto, Y., and De Camilli, P. (1996). A presynaptic inositol-5- phosphatase. Nature 379, 353-357.
37. Micheva, K.D., Kay, B.K., and McPherson, P.S. (1997). Synaptojanin Forms Two Separate Complexes in the Nerve Terminal. J. Biol. Chem. 272, 27239-27245.
38. Milosevic, I., Giovedi, S., Lou, X., Raimondi, A., Collesi, C., Shen, H., Paradise, S., O'Toole, E., Ferguson, S., Cremona, O., et al. (2011). Recruitment of endophilin to clathrin- coated pit necks is required for efficient vesicle uncoating after fission. Neuron 72, 587601.
39. Pechstein, A., Bacetic, J., Vahedi-Faridi, A., Gromova, K., Sundborger, A., Tomlin, N., Krainer, G., Vorontsova, O., Schäfer, J.G., Owe, S.G., et al. (2010). Regulation of synaptic vesicle recycling by complex formation between intersectin 1 and the clathrin adaptor complex AP2. Proc. Natl. Acad. Sci. U.S.a. 107, 4206-4211.
40. Peter, B.J., Kent, H.M., Mills, I.G., Vallis, Y., Butler, P.J.G., Evans, P.R., and McMahon, H.T. (2004). BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495-499.
41. Pirruccello, M., and De Camilli, P. (2012). Inositol 5-phosphatases: insights from the Lowe syndrome protein OCRL. Trends Biochem. Sci. 37, 134-143.
42. Richmond, J.E., Davis, W.S., and Jorgensen, E.M. (1999). UNC-13 is required for synaptic vesicle fusion in C. elegans. Nat. Neurosci. 2, 959-964.
43. Ringstad, N., Nemoto, Y., and De Camilli, P. (1997). The SH3p4/Sh3p8/SH3p13 protein family: binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain. Proc. Natl. Acad. Sci. U.S.a. 94, 8569-8574.
44. Saheki, Y., and De Camilli, P. (2012). Synaptic vesicle endocytosis. Cold Spring Harb Perspect Biol 4, a005645.
45. Schuske, K.R., Richmond, J.E., Matthies, D.S., Davis, W.S., Runz, S., Rube, D.A., van der Bliek, A.M., and Jorgensen, E.M. (2003). Endophilin is required for synaptic vesicle endocytosis by localizing synaptojanin. Neuron 40, 749-762.
46. Song, W., and Zinsmaier, K.E. (2003). Endophilin and synaptojanin hook up to promote synaptic vesicle endocytosis. Neuron 40, 665-667.
47. Stahelin, R.V., Karathanassis, D., Murray, D., Williams, R.L., and Cho, W. (2007). Structural and membrane binding analysis of the Phox homology domain of Bemlp: basis of phosphatidylinositol 4-phosphate specificity. J. Biol. Chem. 282, 25737-25747.
48. Sullivan, J.M. (2011). A surprisingly singular role for endophilin in synaptic vesicle recycling. Neuron 72, 504-505.
49. Tsujishita, Y., Guo, S., Stolz, L.E., York, J.D., and Hurley, J.H. (2001). Specificity Determinants in Phosphoinositide Dephosphorylation-Crystal Structure of an Archetypal Inositol Polyphosphate 5-Phosphatase. Cell 105, 379-389.
50. Van Epps, H.A., Hayashi, M., Lucast, L., Stearns, G.W., Hurley, J.B., De Camilli, P., and Brockerhoff, S.E. (2004). The zebrafish nrc mutant reveals a role for the polyphosphoinositide phosphatase synaptojanin 1 in cone photoreceptor ribbon anchoring. J. Neurosci. 24, 8641-8650.
51. Varnai, P., Rother, K.I., and Balla, T. (1999). Phosphatidylinositol 3-kinase-dependent membrane association of the Bruton's tyrosine kinase pleckstrin homology domain visualized in single living cells. J. Biol. Chem. 274, 10983-10989.
52. Verstreken, P., Kjaerulff, O., Lloyd, T.E., Atkinson, R., Zhou, Y., Meinertzhagen, I.A., and Bellen, H.J. (2002). Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 109, 101-112.
53. Verstreken, P., Koh, T.-W., Schulze, K.L., Zhai, R.G., Hiesinger, P.R., Zhou, Y., Mehta, S.Q., Cao, Y., Roos, J., and Bellen, H.J. (2003). Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron 40, 733-748.
54. Voronov, S.V., Frere, S.G., Giovedi, S., Pollina, E.A., Borel, C., Zhang, H., Schmidt, C., Akeson, E.C., Wenk, M.R., Cimasoni, L., et al. (2008). Synaptojanin 1-linked phosphoinositide dyshomeostasis and cognitive deficits in mouse models of Down's syndrome. Proc. Natl. Acad. Sci. U.S.a. 105, 9415-9420.
55. Whisstock, J.C., Wiradjaja, F., Waters, J.E., and Gurung, R. (2002). The structure and function of catalytic domains within inositol polyphosphate 5-phosphatases. IUBMB Life 53, 15-23.
56. Wong, S.S.C., Kotera, I., Mills, E., Suzuki, H., and Truong, K. (2012). Split-intein mediated re-assembly of genetically encoded Ca(2+) indicators. Cell Calcium 51, 57-64.