Control of plasma membrane lipid homeostasis by the extended synaptotagmins

Nature Cell Biology

Volumn 18, Issue 5, 2016, Pages 504-515

  Saheki, Yasunori ^a,d   Bian, Xin ^a   Schauder, Curtis M ^a   Sawaki, Yujin ^a   Surma, Michal A ^b   Klose, Christian ^b   Pincet, Frederic ^a,c   Reinisch, Karin M ^a   De Camilli, Pietro ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LIPOTYPE GMBH   (Germany)

^c SORBONNE UNIVERSITÉ   (France)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; DIACYLGLYCEROL; EXTENDED SYNAPTOTAGMIN; GLYCEROLIPID; SYNAPTOTAGMIN; UNCLASSIFIED DRUG; CALCIUM; CARRIER PROTEIN; LIPID TRANSFER PROTEIN; MEMBRANE LIPID; PHOSPHOLIPASE C; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE;

ARTICLE; BILAYER MEMBRANE; CELL MEMBRANE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; IN VITRO STUDY; LIPID HOMEOSTASIS; LIPID METABOLISM; LIPID STORAGE; LIPID TRANSPORT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; STIMULUS RESPONSE; CRISPR CAS SYSTEM; CYTOSOL; ENZYME ACTIVATION; GENE INACTIVATION; HELA CELL LINE; HOMEOSTASIS; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CALCIUM; CARRIER PROTEINS; CELL MEMBRANE; CRISPR-CAS SYSTEMS; CYTOSOL; DIGLYCERIDES; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; GENE KNOCKOUT TECHNIQUES; HELA CELLS; HOMEOSTASIS; HUMANS; MEMBRANE LIPIDS; SYNAPTOTAGMINS; TRANSCRIPTION ACTIVATOR-LIKE EFFECTOR NUCLEASES; TYPE C PHOSPHOLIPASES;

EID: 84963582640     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3339     Document Type: Article

References (47)

1. Holthuis, J. C., & Levine, T. P. Lipid traffic: floppy drives and a superhighway. Nat. Rev. Mol. Cell Biol. 6, 209-220 (2005
2. Elbaz, Y., & Schuldiner, M. Staying in touch: the molecular era of organelle contact sites. Trends Biochem. Sci. 36, 616-623 (2011
3. Friedman, J. R., & Voeltz, G. K. The ER in 3D: a multifunctional dynamic membrane network. Trends Cell Biol. 21, 709-717 (2011
4. Toulmay, A., & Prinz, W. A. Lipid transfer and signaling at organelle contact sites: the tip of the iceberg. Curr. Opin. Cell Biol. 23, 458-463 (2011
5. Stefan, C. J., et al. Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell 144, 389-401 (2011
6. Mesmin, B., et al. A four-step cycle driven by PI(4)P hydrolysis directs sterol/PI(4)P exchange by the ER-Golgi tether OSBP. Cell 155, 830-843 (2013
7. Prinz, W. A. Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics. J. Cell Biol. 205, 759-769 (2014
8. Giordano, F., et al. PI(4, 5)P2-dependent and Ca(2C)-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153, 1494-1509 (2013
9. Toulmay, A., & Prinz, W. A. A conserved membrane-binding domain targets proteins to organelle contact sites. J. Cell Sci. 125, 49-58 (2012
10. Manford, A. G., Stefan, C. J., Yuan, H. L., Macgurn, J. A., & Emr, S. D. ER-To-plasma membrane tethering proteins regulate cell signaling and ER morphology. Dev. Cell 23, 1129-1140 (2012
11. Fernandez-Busnadiego, R., Saheki, Y., & De Camilli, P. Three-dimensional architecture of extended synaptotagmin-mediated endoplasmic reticulum-plasma membrane contact sites. Proc. Natl Acad. Sci. USA 112, E2004-E2013 (2015
12. Idevall-Hagren, O., Lu, A., Xie, B., & De Camilli, P. Triggered Ca2C influx is required for extended synaptotagmin 1-induced ER-plasma membrane tethering. EMBO J. 34, 2291-2305 (2015
13. Min, S. W., Chang, W. P., & Sudhof, T. C. E-Syts, a family of membranous Ca2C-sensor proteins with multiple C2 domains. Proc. Natl Acad. Sci. USA 104, 3823-3828 (2007
14. Craxton, M. Genomic analysis of synaptotagmin genes. Genomics 77, 43-49 (2001
15. Craxton, M. Evolutionary genomics of plant genes encoding N-Terminal-TM-C2 domain proteins and the similar FAM62 genes and synaptotagmin genes of metazoans. BMC Genomics 8, 259 (2007
16. Levy, A., Zheng, J. Y., & Lazarowitz, S. G. Synaptotagmin SYTA forms ER-plasma membrane junctions that are recruited to plasmodesmata for plant virus movement. Curr. Biol. 25, 2018-2025 (2015
17. Perez-Sancho, J., et al. The Arabidopsis synaptotagmin1 is enriched in endoplasmic reticulum-plasma membrane contact sites and confers cellular resistance to mechanical stresses. Plant Physiol. 168, 132-143 (2015
18. Kopec, K. O., Alva, V., & Lupas, A. N. Homology of SMP domains to the TULIP superfamily of lipid-binding proteins provides a structural basis for lipid exchange between ER and mitochondria. Bioinformatics 26, 1927-1931 (2010
19. Kopec, K. O., Alva, V., & Lupas, A. N. Bioinformatics of the TULIP domain superfamily. Biochem. Soc. Trans. 39, 1033-1038 (2011
20. Qiu, X., et al. Crystal structure of cholesteryl ester transfer protein reveals a long tunnel and four bound lipid molecules. Nat. Struct. Mol. Biol. 14, 106-113 (2007
21. Oram, J. F., Wolfbauer, G., Vaughan, A. M., Tang, C., & Albers, J. J. Phospholipid transfer protein interacts with and stabilizes ATP-binding cassette transporter A1 and enhances cholesterol efflux from cells. J. Biol. Chem. 278, 52379-52385 (2003
22. Schauder, C. M., et al. Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer. Nature 510, 552-555 (2014
23. Kornmann, B., et al. An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325, 477-481 (2009
24. AhYoung, A. P., et al. Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly. Proc. Natl Acad. Sci. USA 112, E3179-E3188 (2015
25. Morgan, A. J., & Jacob, R. Ionomycin enhances Ca2C influx by stimulating storeregulated cation entry and not by a direct action at the plasma membrane. Biochem. J. 300, 665-672 (1994
26. Willars, G. B., Nahorski, S. R., & Challiss, R. A. Differential regulation of muscarinic acetylcholine receptor-sensitive polyphosphoinositide pools and consequences for signaling in human neuroblastoma cells. J. Biol. Chem. 273, 5037-5046 (1998
27. Horowitz, L. F., et al. Phospholipase C in living cells: activation, inhibition, Ca2C requirement, and regulation of M current. J. Gen. Physiol. 126, 243-262 (2005
28. Suh, B. C., Horowitz, L. F., Hirdes, W., Mackie, K., & Hille, B. Regulation of KCNQ2/KCNQ3 current by G protein cycling: the kinetics of receptor-mediated signaling by Gq. J. Gen. Physiol. 123, 663-683 (2004
29. Cohen, C. M., Kalish, D. I., Jacobson, B. S., & Branton, D. Membrane isolation on polylysine-coated beads. Plasma membrane from HeLa cells. J. Cell Biol. 75, 119-134 (1977
30. Codazzi, F., Teruel, M. N., & Meyer, T. Control of astrocyte Ca(2C) oscillations and waves by oscillating translocation and activation of protein kinase C. Curr. Biol. 11, 1089-1097 (2001
31. Varnai, P., & Balla, T. Visualization of phosphoinositides that bind pleckstrin homology domains: calcium-And agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J. Cell Biol. 143, 501-510 (1998
32. Gallegos, L. L., Kunkel, M. T., & Newton, A. C. Targeting protein kinase C activity reporter to discrete intracellular regions reveals spatiotemporal differences in agonistdependent signaling. J. Biol. Chem. 281, 30947-30956 (2006
33. Merida, I., Avila-Flores, A., & Merino, E. Diacylglycerol kinases: at the hub of cell signalling. Biochem. J. 409, 1-18 (2008
34. Kim, Y. J., Guzman-Hernandez, M. L., Wisniewski, E., & Balla, T. Phosphatidylinositol-Phosphatidic Acid Exchange by Nir2 at ER-PM contact sites maintains phosphoinositide signaling competence. Dev. Cell 33, 549-561 (2015
35. Whatmore, J., Wiedemann, C., Somerharju, P., Swigart, P., & Cockcroft, S. Resynthesis of phosphatidylinositol in permeabilized neutrophils following phospholipase Cbeta activation: transport of the intermediate, phosphatidic acid, from the plasma membrane to the endoplasmic reticulum for phosphatidylinositol resynthesis is not dependent on soluble lipid carriers or vesicular transport. Biochem. J. 341, 435-444 (1999
36. Chang, C. L., et al. Feedback regulation of receptor-induced Ca2C signaling mediated by E-Syt1 and Nir2 at endoplasmic reticulum-plasma membrane junctions. Cell Rep. 5, 813-825 (2013
37. Chang, C. L., & Liou, J. Phosphatidylinositol 4, 5-bisphosphate homeostasis regulated by Nir2 and Nir3 proteins at endoplasmic reticulum-plasma membrane junctions. J. Biol. Chem. 290, 14289-14301 (2015
38. Schapire, A. L., et al. Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20, 3374-3388 (2008
39. Yamazaki, T., Kawamura, Y., Minami, A., & Uemura, M. Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell 20, 3389-3404 (2008
40. Aguilar, P. S., Engel, A., & Walter, P. The plasma membrane proteins Prm1 and Fig1 ascertain fidelity of membrane fusion during yeast mating. Mol. Biol. Cell 18, 547-556 (2007
41. Idevall-Hagren, O., Dickson, E. J., Hille, B., Toomre, D. K., & De Camilli, P. Optogenetic control of phosphoinositide metabolism. Proc. Natl Acad. Sci. USA 109, E2316-E2323 (2012
42. Shibata, Y., et al. The reticulon and DP1/Yop1p proteins form immobile oligomers in the tubular endoplasmic reticulum. J. Biol. Chem. 283, 18892-18904 (2008
43. Sampaio, J. L., et al. Membrane lipidome of an epithelial cell line. Proc. Natl Acad. Sci. USA 108, 1903-1907 (2011
44. Herzog, R., et al. A novel informatics concept for high-Throughput shotgun lipidomics based on the molecular fragmentation query language. Genome Biol. 12, R8 (2011
45. Kim, H., et al. Surrogate reporters for enrichment of cells with nuclease-induced mutations. Nat. Methods 8, 941-943 (2011
46. Sanjana, N. E., et al. A transcription activator-like effector toolbox for genome engineering. Nat. Protoc. 7, 171-192 (2012
47. Mali, P., et al. RNA-guided human genome engineering via Cas9. Science 339, 823-826 (2013