Lipid transport by TMEM24 at ER-plasma membrane contacts regulates pulsatile insulin secretion

Science

Volumn 355, Issue 6326, 2017, Pages

  Lees, Joshua A ^a,b   Messa, Mirko ^a,b   Sun, Elizabeth Wen ^a,b   Wheeler, Heather ^a,b   Torta, Federico ^a,b   Wenk, Markus R ^a,b   De Camilli, Pietro ^a,b   Reinisch, Karin M ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; GLUCOSE; GLYCEROLIPID; GLYCEROPHOSPHOLIPID; INSULIN; LIPID; LIPID TRANSFER PROTEIN; MEMBRANE PROTEIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHATIDYLSERINE; TRANSMEMBRANE PROTEIN 24; UNCLASSIFIED DRUG; C2CD2L PROTEIN, HUMAN;

CELLS AND CELL COMPONENTS; CHEMICAL BINDING; DIABETES; HORMONE; LIPID; MEMBRANE; PROTEIN; SECRETION;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CARBOXY TERMINAL SEQUENCE; CELL CONTACT; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSOL; DISSOCIATION; ENDOPLASMIC RETICULUM; EXOCYTOSIS; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; INSULIN RELEASE; INTRACELLULAR SIGNALING; LIPID ANALYSIS; LIPID BILAYER; LIPID HYDROLYSIS; LIPID TRANSPORT; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN LIPID INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN-BOUND FRACTION; RAT; REGULATORY MECHANISM; SYNAPTOTAGMIN LIKE MITOCHONDRIAL AND LIPID BINDING PROTEIN DOMAIN; ANIMAL; CHLOROCEBUS AETHIOPS; CV-1 CELL LINE; GENE INACTIVATION; GENETICS; HELA CELL LINE; HYDROLYSIS; LIPID METABOLISM; METABOLISM; PHOSPHORYLATION; SECRETION (PROCESS); TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM SIGNALING; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOPLASMIC RETICULUM; GENE KNOCKOUT TECHNIQUES; HELA CELLS; HUMANS; HYDROLYSIS; INSULIN; LIPID METABOLISM; MEMBRANE PROTEINS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHORYLATION;

EID: 85013491996     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aah6171     Document Type: Article

References (68)

1. S. Tavassoli et al., Plasma membrane: Endoplasmic reticulum contact sites regulate phosphatidylcholine synthesis. EMBO Rep. 14, 434-440 (2013). doi: 10.1038/embor.2013.36; pmid: 23519169
2. J. C. M. Holthuis, T. P. Levine, Lipid traffic: Floppy drives and a superhighway. Nat. Rev. Mol. Cell Biol. 6, 209-220 (2005). doi: 10.1038/nrm1591; pmid: 15738987
3. C. J. Stefan et al., Osh Proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell 144, 389-401 (2011). doi: 10.1016/j.cell.2010.12.034
4. C. J. Stefan, A. G. Manford, S. D. Emr, ER-PM connections: Sites of information transfer and inter-organelle communication. Curr. Opin. Cell Biol. 25, 434-442 (2013). doi: 10.1016/j.ceb.2013.02.020; pmid: 23522446
5. Y. Saheki et al., Control of plasma membrane lipid homeostasis by the extended synaptotagmins. Nat. Cell Biol. 18, 504-515 (2016). doi: 10.1038/ncb3339; pmid: 27065097
6. J. Chung et al., PI4P/phosphatidylserine countertransport at ORP5- and ORP8-mediated ER-plasma membrane contacts. Science 349, 428-432 (2015). doi: 10.1126/science.aab1370; pmid: 26206935
7. B. Mesmin 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). doi: 10.1016/j.cell.2013.09.056; pmid: 24209621
8. A. T. Gatta et al., A new family of StART domain proteins at membrane contact sites has a role in ER-PM sterol transport. eLife 4, (2015). doi: 10.7554/eLife.07253; pmid: 26001273
9. J. Moser von Filseck et al., Phosphatidylserine transport by ORP/Osh proteins is driven by phosphatidylinositol 4-phosphate. Science 349, 432-436 (2015). doi: 10.1126/ science.aab1346; pmid: 26206936
10. A. G. Manford, C. J. Stefan, H. L. Yuan, J. A. Macgurn, S. D. Emr, ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology. Dev. Cell 23, 1129-1140 (2012). doi: 10.1016/ j.devcel.2012.11.004; pmid: 23237950
11. A. Toulmay, W. A. Prinz, A conserved membrane-binding domain targets proteins to organelle contact sites. J. Cell Sci. 125, 49-58 (2012). doi: 10.1242/jcs.085118; pmid: 22250200
12. V. Alva, A. N. Lupas, The TULIP superfamily of eukaryotic lipid-binding proteins as a mediator of lipid sensing and transport. Biochim. Biophys. Acta 1861 (8 Pt. B), 913-923 (2016). pmid: 26825693
13. A. Pottekat et al., Insulin biosynthetic interaction network component, TMEM24, facilitates insulin reserve pool release. Cell Rep. 4, 921-930 (2013). doi: 10.1016/ j.celrep.2013.07.050; pmid: 24012759
14. J. C. Hou, L. Min, J. E. Pessin, Insulin granule biogenesis, trafficking and exocytosis. Vitam. Horm. 80, 473-506 (2009). doi: 10.1016/S0083-6729(08)00616-X; pmid: 19251047
15. P. Rorsman, E. Renström, Insulin granule dynamics in pancreatic beta cells. Diabetologia 46, 1029-1045 (2003). doi: 10.1007/s00125-003-1153-1; pmid: 12879249
16. B. A. Spurlin, D. C. Thurmond, Syntaxin 4 facilitates biphasic glucose-stimulated insulin secretion from pancreatic beta-cells. Mol. Endocrinol. 20, 183-193 (2006). doi: 10.1210/me.2005-0157; pmid: 16099818
17. S. Daniel, M. Noda, S. G. Straub, G. W. Sharp, Identification of the docked granule pool responsible for the first phase of glucose-stimulated insulin secretion. Diabetes 48, 1686-1690 (1999). doi: 10.2337/diabetes.48.9.1686; pmid: 10480595
18. T. K. Bratanova-Tochkova et al., Triggering and augmentation mechanisms, granule pools, and biphasic insulin secretion. Diabetes 51 (suppl. 1), S83-S90 (2002). doi: 10.2337/ diabetes.51.2007.S83; pmid: 11815463
19. A. Wuttke, J. Sågetorp, A. Tengholm, Distinct plasmamembrane PtdIns(4)P and PtdIns(4,5)P2 dynamics in secretagogue-stimulated beta-cells. J. Cell Sci. 123, 1492-1502 (2010). doi: 10.1242/jcs.060525; pmid: 20375060
20. S. Thore, A. Wuttke, A. Tengholm, Rapid turnover of phosphatidylinositol-4,5-bisphosphate in insulin-secreting cells mediated by Ca2+ and the ATP-to-ADP ratio. Diabetes 56, 818-826 (2007). doi: 10.2337/db06-0843; pmid: 17327453
21. 2-binding effector proteins for vesicle exocytosis. Biochim. Biophys. Acta 1851, 785-793 (2015). doi: 10.1016/j.bbalip.2014.09.017; pmid: 25280637
22. B. Hille, E. J. Dickson, M. Kruse, O. Vivas, B.-C. C. Suh, Phosphoinositides regulate ion channels. Biochim. Biophys. Acta 1851, 844-856 (2015). doi: 10.1016/j.bbalip.2014.09.010; pmid: 25241941
23. B. Xie et al., Plasma membrane phosphatidylinositol 4,5-bisphosphate regulates Ca2+-influx and insulin secretion from pancreatic β cells. Cell Chem. Biol. 23, 816-826 (2016). doi: 10.1016/j.chembiol.2016.06.009
24. F. Giordano et al., PI(4,5)P(2)-dependent and Ca2+-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153, 1494-1509 (2013). doi: 10.1016/j.cell.2013.05.026; pmid: 23791178
25. T. Schikorski, S. M. Young Jr., Y. Hu, Horseradish peroxidase cDNA as a marker for electron microscopy in neurons. J. Neurosci. Methods 165, 210-215 (2007). doi: 10.1016/ j.jneumeth.2007.06.004; pmid: 17631969
26. N. B. Caberoy, Y. Zhou, G. Alvarado, X. Fan, W. Li, Efficient identification of phosphatidylserine-binding proteins by ORF phage display. Biochem. Biophys. Res. Commun. 386, 197-201 (2009). doi: 10.1016/j.bbrc.2009.06.010; pmid: 19520055
27. O. Idevall-Hagren, E. J. Dickson, B. Hille, D. K. Toomre, P. De Camilli, Optogenetic control of phosphoinositide metabolism. Proc. Natl. Acad. Sci. U.S.A. 109, E2316-E2323 (2012). doi: 10.1073/pnas.1211305109; pmid: 22847441
28. M. J. Kennedy et al., Rapid blue-light-mediated induction of protein interactions in living cells. Nat. Methods 7, 973-975 (2010). doi: 10.1038/nmeth.1524; pmid: 21037589
29. J. Rizo, T. C. Südhof, C2-domains, structure and function of a universal Ca2+-binding domain. J. Biol. Chem. 273, 15879-15882 (1998). doi: 10.1074/jbc.273.26.15879; pmid: 9632630
30. J. Liou et al., STIM is a Ca2+ sensor essential for Ca2+-storedepletion-triggered Ca2+ influx. Curr. Biol. 15, 1235-1241 (2005). doi: 10.1016/j.cub.2005.05.055; pmid: 16005298
31. P. G. Hogan, R. S. Lewis, A. Rao, Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu. Rev. Immunol. 28, 491-533 (2010). doi: 10.1146/annurev. immunol.021908.132550; pmid: 20307213
32. K. Nishikawa, A. Toker, F. J. Johannes, Z. Songyang, L. C. Cantley, Determination of the specific substrate sequence motifs of protein kinase C isozymes. J. Biol. Chem. 272, 952-960 (1997). doi: 10.1074/jbc.272.2.952; pmid: 8995387
33. E. L. Huttlin et al., A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143, 1174-1189 (2010). doi: 10.1016/j.cell.2010.12.001; pmid: 21183079
34. D. Toullec et al., The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J. Biol. Chem. 266, 15771-15781 (1991). pmid: 1874734
35. J. Liu et al., Calcineurin is a common target of cyclophilincyclosporin A and FKBP-FK506 complexes. Cell 66, 807-815 (1991). doi: 10.1016/0092-8674(91)90124-H; pmid: 1715244
36. M. Sumi et al., The newly synthesized selective Ca2+/ calmodulin dependent protein kinase II inhibitor KN-93 reduces dopamine contents in PC12h cells. Biochem. Biophys. Res. Commun. 181, 968-975 (1991). doi: 10.1016/0006-291X (91)92031-E; pmid: 1662507
37. R. M. Mulkey, S. Endo, S. Shenolikar, R. C. Malenka, Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369, 486-488 (1994). doi: 10.1038/369486a0; pmid: 7515479
38. I. Kameshita, A. Ishida, H. Fujisawa, Phosphorylation and activation of Ca2+/calmodulin-dependent protein kinase phosphatase by Ca2+/calmodulin-dependent protein kinase II. FEBS Lett. 456, 249-252 (1999). doi: 10.1016/S0014-5793(99) 00958-8; pmid: 10456318
39. K. O. Kopec, V. Alva, A. N. Lupas, 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). doi: 10.1093/bioinformatics/btq326; pmid: 20554689
40. C. M. Schauder et al., Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer. Nature 510, 552-555 (2014). doi: 10.1038/nature13269; pmid: 24847877
41. A. P. AhYoung et al., Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly. Proc. Natl. Acad. Sci. U.S.A. 112, E3179-E3188 (2015). doi: 10.1073/pnas.1422363112; pmid: 26056272
42. H. Yu et al., Extended synaptotagmins are Ca2+-dependent lipid transfer proteins at membrane contact sites. Proc. Natl. Acad. Sci. U.S.A. 113, 4362-4367 (2016). doi: 10.1073/ pnas.1517259113; pmid: 27044075
43. K. Maeda et al., Interactome map uncovers phosphatidylserine transport by oxysterol-binding proteins. Nature 501, 257-261 (2013). doi: 10.1038/nature12430; pmid: 23934110
44. J. L. Sampaio et al., Membrane lipidome of an epithelial cell line. Proc. Natl. Acad. Sci. U.S.A. 108, 1903-1907 (2011). doi: 10.1073/pnas.1019267108; pmid: 21245337
45. Y. J. Kim, M.-L. G. Hernandez, T. Balla, Inositol lipid regulation of lipid transfer in specialized membrane domains. Trends Cell Biol. 23, 270-278 (2013). doi: 10.1016/j.tcb.2013.01.009; pmid: 23489878
46. J. C. Hay, T. F. Martin, Phosphatidylinositol transfer protein required for ATP-dependent priming of Ca2+-activated secretion. Nature 366, 572-575 (1993). doi: 10.1038/366572a0; pmid: 8255295
47. D. J. James, T. F. J. Martin, CAPS and Munc13: CATCHRs that SNARE Vesicles. Front. Endocrinol. (Lausanne) 4, 187 (2013). doi: 10.3389/fendo.2013.00187; pmid: 24363652
48. L. Kang et al., Munc13-1 is required for the sustained release of insulin from pancreatic beta cells. Cell Metab. 3, 463-468 (2006). doi: 10.1016/j.cmet.2006.04.012; pmid: 16697276
49. D. A. Eberhard, C. L. Cooper, M. G. Low, R. W. Holz, Evidence that the inositol phospholipids are necessary for exocytosis. Loss of inositol phospholipids and inhibition of secretion in permeabilized cells caused by a bacterial phospholipase C and removal of ATP. Biochem. J. 268, 15-25 (1990). doi: 10.1042/ bj2680015; pmid: 2160809
50. L. D. Gaspers et al., Hormone-induced calcium oscillations depend on cross-coupling with inositol 1,4,5-trisphosphate oscillations. Cell Reports 9, 1209-1218 (2014). doi: 10.1016/ j.celrep.2014.10.033; pmid: 25456123
51. 3. Science 251, 75-78 (1991). doi: 10.1126/science.1986413; pmid: 1986413
52. Y. J. Kim, M.-L. L. Guzman-Hernandez, E. Wisniewski, T. Balla, Phosphatidylinositol-phosphatidic acid exchange by Nir2 at ER-PM contact sites maintains phosphoinositide signaling competence. Dev. Cell 33, 549-561 (2015). doi: 10.1016/ j.devcel.2015.04.028; pmid: 26028218
53. C.-L. L. Chang, J. Liou, Phosphatidylinositol 4,5-bisphosphate homeostasis regulated by Nir2 and Nir3 Proteins at endoplasmic reticulum-plasma membrane junctions. J. Biol. Chem. 290, 14289-14301 (2015). doi: 10.1074/ jbc.M114.621375; pmid: 25887399
54. R. Dong et al., Endosome-ER contacts control actin nucleation and retromer function through VAP-dependent regulation of PI4P. Cell 166, 408-423 (2016). doi: 10.1016/ j.cell.2016.06.037; pmid: 27419871
55. T.-W. Chen et al., Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013). doi: 10.1038/nature12354; pmid: 23868258
56. F. A. Ran et al., Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281-2308 (2013). doi: 10.1038/ nprot.2013.143; pmid: 24157548
57. U. K. Laemmli, Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685 (1970). doi: 10.1038/227680a0; pmid: 5432063
58. O. Idevall-Hagren, P. Decamilli, Manipulation of plasma membrane phosphoinositides using photoinduced protein-protein interactions. Methods Mol. Biol. 1148, 109-128 (2014). doi: 10.1007/978-1-4939-0470-9-8; pmid: 24718798
59. G. R. Hammond, M. P. Machner, T. Balla, A novel probe for phosphatidylinositol 4-phosphate reveals multiple pools beyond the Golgi. J. Cell Biol. 205, 113-126 (2014). doi: 10.1083/jcb.201312072; pmid: 24711504
60. T. P. Stauffer, S. Ahn, T. Meyer, Receptor-induced transient reduction in plasma membrane PtdIns(4,5)P2 concentration monitored in living cells. Curr. Biol. 8, 343-346 (1998). doi: 10.1016/S0960-9822(98)70135-6; pmid: 9512420
61. H. Liu et al., Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322, 1535-1539 (2008). doi: 10.1126/science.1163927; pmid: 18988809
62. H. E. Hohmeier et al., Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes 49, 424-430 (2000). doi: 10.2337/diabetes.49.3.424; pmid: 10868964
63. S. Doublié, Preparation of selenomethionyl proteins for phase determination. Methods Enzymol. 276, 523-530 (1997). doi: 10.1016/S0076-6879(97)76075-0
64. W. Kabsch, XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010). doi: 10.1107/S0907444909047337; pmid: 20124692
65. G. M. Sheldrick, A short history of SHELX. Acta Crystallogr. A 64, 112-122 (2008). doi: 10.1107/S0108767307043930; pmid: 18156677
66. P. D. Adams et al., PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010). doi: 10.1107/ S0907444909052925; pmid: 20124702
67. P. Emsley, B. Lohkamp, W. G. Scott, K. Cowtan, Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010). doi: 10.1107/S0907444910007493; pmid: 20383002
68. C. Nasuhoglu et al., Nonradioactive analysis of phosphatidylinositides and other anionic phospholipids by anion-exchange high-performance liquid chromatography with suppressed conductivity detection. Anal. Biochem. 301, 243-254 (2002). doi: 10.1006/abio.2001.5489; pmid: 11814295