Lipids in regulated exocytosis: What are they doing?

Frontiers in Endocrinology

Volumn 4, Issue SEP, 2013, Pages

  Ammar, Mohamed Raafet ^a   Kassas, Nawal ^a   Chasserot Golaz, Sylvette ^a   Bader, Marie France ^a   Vitale, Nicolas ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Cholesterol; Chromaffin cell; Exocytosis; Membrane fusion; Phosphatidic acids; Phosphoinositides

Indexed keywords

EID: 84885404828     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2013.00125     Document Type: Review

References (57)

1. Bader MF, Doussau F, Chasserot-Golaz S, Vitale N, Gasman S. Coupling actin and membrane dynamics during calcium-regulated exocytosis:a role for Rho and ARF GTPases. Biochim Biophys Acta (2004) 1742:37-49. doi:10.1016/j.bbamcr.2004.09.028.
2. Jahn R, Fasshauer D. Molecular machines governing exocytosis of synaptic vesicles. Nature (2012) 490:201-7. doi:10.1038/nature11320.
3. Sutton RB, Fasshauer D, Jahn R, Brunger AT. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature (1998) 395:347-53. doi:10.1038/26412.
4. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, Parlati F, et al. SNAREpins:minimal machinery for membrane fusion. Cell (1998) 92:759-72. doi:10.1016/S0092-8674(00)81404-X.
5. Ma C, Su L, Seven AB, Xu Y, Rizo J. Reconstitution of the vital functions of Munc18 and Munc13 in neurotransmitter release. Science (2013) 339:421-5. doi:10.1126/science.1230473.
6. Martin TF. Role of PI(4,5)P(2) in vesicle exocytosis and membrane fusion. Subcell Biochem (2012) 59:111-30. doi:10.1007/978-94-007-3015-1_4.
7. Darios F, Connell E, Davletov B. Phospholipases and fatty acid signalling in exocytosis. J Physiol (2007) 585:699-704. doi:10.1113/jphysiol.2007.136812.
8. Chasserot-Golaz S, Coorssen JR, Meunier FA, Vitale N. Lipid dynamics in exocytosis. Cell Mol Neurobiol (2010) 30:1335-42. doi:10.1007/s10571-010-9577-x.
9. Chasserot-Golaz S, Vitale N, Umbrecht-Jenck E, Knight D, Gerke V, Bader MF. Annexin 2 promotes the formation of lipid microdomains required for calcium-regulated exocytosis of dense-core vesicles. Mol Biol Cell (2005) 16:1108-19. doi:10.1091/mbc. E04-07-0627.
10. Chamberlain LH, Burgoyne RD, Gould GW. SNARE proteins are highly enriched in lipid rafts in PC12 cells:implications for the spatial control of exocytosis. Proc Natl Acad Sci U S A (2001) 98:5619-24. doi:10.1073/pnas.091502398.
11. Lang T. SNARE proteins and "membrane rafts". J Physiol (2007) 585:693-8. doi:10.1113/jphysiol.2007.134346.
12. Umbrecht-Jenck E, Demais V, Calco V, Bailly Y, Bader MF, Chasserot-Golaz S. S100A10-mediated translocation of annexin-A2 to SNARE proteins in adrenergic chromaffin cells undergoing exocytosis. Traffic (2010) 11:958-71. doi:10.1111/j.1600-0854.2010.01065.x.
13. Ceridono M, Ory S, Momboisse F, Chasserot-Golaz S, Houy S, Calco V, et al. Selective recapture of secretory granule components after full collapse exocytosis in neuroendocrine chromaffin cells. Traffic (2011) 12:72-88. doi:10.1111/j.1600-0854.2010.01125.x.
14. Vitale N, Caumont AS, Chasserot-Golaz S, Du G, Wu S, Sciorra VA, et al. Phospholipase D1:a key factor for the exocytotic machinery in neuroendocrine cells. EMBO J (2001) 20:2424-34. doi:10.1093/emboj/20.10.2424.
15. Ory S, Ceridono M, Momboisse F, Houy S, Chasserot-Golaz S, Heintz D, et al. Phospholipid scramblase-1-induced lipid reorganization regulates compensatory endocytosis in neuroendocrine cells. J Neurosci (2013) 33:3545-56. doi:10.1523/JNEUROSCI.3654-12.2013.
16. Aikawa Y, Martin TF. ARF6 regulates a plasma membrane pool of phosphatidylinositol(4,5)bisphosphate required for regulated exocytosis. J Cell Biol (2003) 162:647-59. doi:10.1083/jcb.200212142.
17. Eberhard DA, Cooper CL, Low MG, Holz RW. 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 (1990) 268:15-25.
18. Holz RW, Hlubek MD, Sorensen SD, Fisher SK, Balla T, Ozaki S, et al. A pleckstrin homology domain specific for phosphatidylinositol 4, 5-bisphosphate (PtdIns-4,5-P2) and fused to green fluorescent protein identifies plasma membrane PtdIns-4,5-P2 as being important in exocytosis. J Biol Chem (2000) 275:17878-85. doi:10.1074/jbc. M000925200.
19. Milosevic I, Sorensen JB, Lang T, Krauss M, Nagy G, Haucke V, et al. Plasmalemmal phosphatidylinositol-4,5-bisphosphate level regulates the releasable vesicle pool size in chromaffin cells. J Neurosci (2005) 25:2557-65. doi:10.1523/JNEUROSCI.3761-04.2005.
20. Chasserot-Golaz S, Hubert P, Thierse D, Dirrig S, Vlahos CJ, Aunis D, et al. Possible involvement of phosphatidylinositol 3-kinase in regulated exocytosis:studies in chromaffin cells with inhibitor LY294002. J Neurochem (1998) 70:2347-56. doi:10.1046/j.1471-4159.1998.70062347.x.
21. Wen PJ, Osborne SL, Morrow IC, Parton RG, Domin J, Meunier FA. Ca2+-regulated pool of phosphatidylinositol-3-phosphate produced by phosphatidylinositol 3-kinase C2alpha on neurosecretory vesicles. Mol Biol Cell (2008) 19:5593-603. doi:10.1091/mbc. E08-06-0595.
22. Wen PJ, Osborne SL, Zanin M, Low PC, Wang HT, Schoenwaelder SM, et al. Phosphatidylinositol(4,5)bisphosphate coordinates actin-mediated mobilization and translocation of secretory vesicles to the plasma membrane of chromaffin cells. Nat Commun (2011) 2:491. doi:10.1038/ncomms1500.
23. Tryoen-Toth P, Chasserot-Golaz S, Tu A, Gherib P, Bader MF, Beaumelle B, et al. HIV-1 Tat protein inhibits neurosecretion by binding to phosphatidylinositol 4,5-bisphosphate. J Cell Sci (2013) 126:454-63. doi:10.1242/jcs.111658.
24. Meunier FA, Osborne SL, Hammond GR, Cooke FT, Parker PJ, Domin J, et al. Phosphatidylinositol 3-kinase C2alpha is essential for ATP-dependent priming of neurosecretory granule exocytosis. Mol Biol Cell (2005) 210:4841-51. doi:10.1091/mbc. E05-02-0171.
25. Osborne SL, Wen PJ, Boucheron C, Nguyen HN, Hayakawa M, Kaizawa H, et al. PIKfyve negatively regulates exocytosis in neurosecretory cells. J Biol Chem (2008) 283:2804-13. doi:10.1074/jbc. M704856200.
26. Bader MF, Vitale N. Phospholipase D in calcium-regulated exocytosis:lessons from chromaffin cells. Biochim Biophys Acta (2009) 1791:936-41. doi:10.1016/j.bbalip.2009.02.016.
27. Waselle L, Gerona RR, Vitale N, Martin TF, Bader MF, Regazzi R. Role of phosphoinositide signaling in the control of insulin exocytosis. Mol Endocrinol (2005) 19:3097-106. doi:10.1210/me.2004-0530.
28. Zeniou-Meyer M, Zabari N, Ashery U, Chasserot-Golaz S, Haeberle AM, Demais V, et al. Phospholipase D1 production of phosphatidic acid at the plasma membrane promotes exocytosis of large dense-core granules at a late stage. J Biol Chem (2007) 282:21746-57. doi:10.1074/jbc. M702968200.
29. Bauer CS, Woolley RJ, Teschemacher AG, Seward EP. Potentiation of exocytosis by phospholipase C-coupled G-protein-coupled receptors requires the priming protein Munc13-1. J Neurosci (2007) 27:212-9. doi:10.1523/JNEUROSCI.4201-06.2007.
30. Barclay JW, Craig TJ, Fisher RJ, Ciufo LF, Evans GJ, Morgan A, et al. Phosphorylation of Munc18 by protein kinase C regulates the kinetics of exocytosis. J Biol Chem (2003) 278:10538-45. doi:10.1074/jbc. M211114200.
31. Yang Y, Craig TJ, Chen X, Ciufo LF, Takahashi M, Morgan A, et al. Phosphomimetic mutation of Ser-187 of SNAP-25 increases both syntaxin binding and highly Ca2+-sensitive exocytosis. J Gen Physiol (2007) 129:233-44. doi:10.1085/jgp.200609685.
32. Zhang Z, Hui E, Chapman ER, Jackson MB. Phosphatidylserine regulation of Ca2+-triggered exocytosis and fusion pores in PC12 cells. Mol Biol Cell (2009) 20:5086-95. doi:10.1091/mbc. E09-08-0691.
33. Latham CF, Osborne SL, Cryle MJ, Meunier FA. Arachidonic acid potentiates exocytosis and allows neuronal SNARE complex to interact with Munc18a. J Neurochem (2007) 100:1543-54.
34. Vitale N. Synthesis of fusogenic lipids through activation of phospholipase D1 by GTPases and the kinase RSK2 is required for calcium-regulated exocytosis in neuroendocrine cells. Biochem Soc Trans (2010) 38:167-71. doi:10.1042/BST0380167.
35. Koch M, Holt M. Coupling exo- and endocytosis:an essential role for PIP(2) at the synapse. Biochim Biophys Acta (2012) 1821:1114-32. doi:10.1016/j.bbalip.2012.02.008.
36. Schiavo G, Gu QM, Prestwich GD, Sollner TH, Rothman JE. Calcium-dependent switching of the specificity of phosphoinositide binding to synaptotagmin. Proc Natl Acad Sci U S A (1996) 93:13327-32. doi:10.1073/pnas.93.23.13327.
37. Lam AD, Tryoen-Toth P, Tsai B, Vitale N, Stuenkel EL. SNARE-catalyzed fusion events are regulated by syntaxin1A-lipid interactions. Mol Biol Cell (2008) 19:485-97. doi:10.1091/mbc. E07-02-0148.
38. Loyet KM, Kowalchyk JA, Chaudhary A, Chen J, Prestwich GD, Martin TF. Specific binding of phosphatidylinositol 4,5-bisphosphate to calcium-dependent activator protein for secretion (CAPS), a potential phosphoinositide effector protein for regulated exocytosis. J Biol Chem (1998) 273:8337-43. doi:10.1074/jbc.273.14.8337.
39. Du G, Altshuller YM, Vitale N, Huang P, Chasserot-Golaz S, Morris AJ, et al. Regulation of phospholipase D1 subcellular cycling through coordination of multiple membrane association motifs. J Cell Biol (2003) 162:305-15. doi:10.1083/jcb.200302033.
40. Liao H, Ellena J, Liu L, Szabo G, Cafiso D, Castle D. Secretory carrier membrane protein SCAMP2 and phosphatidylinositol 4,5-bisphosphate interactions in the regulation of dense core vesicle exocytosis. Biochemistry (2007) 46:10909-20. doi:10.1021/bi701121j.
41. Chasserot-Golaz S, Vitale N, Sagot I, Delouche B, Dirrig S, Pradel LA, et al. Annexin II in exocytosis:catecholamine secretion requires the translocation of p36 to the subplasmalemmal region in chromaffin cells. J Cell Biol (1996) 133:1217-36. doi:10.1083/jcb.133.6.1217.
42. Honigmann A, van den Bogaart G, Iraheta E, Risselada HJ, Milovanovic D, Mueller V, et al. Phosphatidylinositol 4,5-bisphosphate clusters act as molecular beacons for vesicle recruitment. Nat Struct Mol Biol (2013) 20:679-86. doi:10.1038/nsmb.2570.
43. Khuong TM, Habets RL, Kuenen S, Witkowska A, Kasprowicz J, Swerts J, et al. Synaptic PI(3,4,5)P3 is required for syntaxin1A clustering and neurotransmitter release. Neuron (2013) 77:1097-108. doi:10.1016/j.neuron.2013.01.025.
44. Rickman C, Medine CN, Dun AR, Moulton DJ, Mandula O, Halemani ND, et al. t-SNARE protein conformations patterned by the lipid microenvironment. J Biol Chem (2010) 285:13535-41. doi:10.1074/jbc. M109.091058.
45. James DJ, Khodthong C, Kowalchyk JA, Martin TF. Phosphatidylinositol 4,5-bisphosphate regulates SNARE-dependent membrane fusion. J Cell Biol (2008) 182:355-66. doi:10.1083/jcb.200801056.
46. Trifaro JM, Gasman S, Gutierrez LM. Cytoskeletal control of vesicle transport and exocytosis in chromaffin cells. Acta Physiol (Oxf) (2008) 192:165-72. doi:10.1111/j.1748-1716.2007.01808.x.
47. Hammond GR, Dove SK, Nicol A, Pinxteren JA, Zicha D, Schiavo G. Elimination of plasma membrane phosphatidylinositol (4,5)-bisphosphate is required for exocytosis from mast cells. J Cell Sci (2006) 119:2084-94. doi:10.1242/jcs.02912.
48. Sheu L, Pasyk EA, Ji J, Huang X, Gao X, Varoqueaux F, et al. Regulation of insulin exocytosis by Munc13-1. J Biol Chem (2003) 278:27556-63. doi:10.1074/jbc. M303203200.
49. Jang JH, Lee CS, Hwang D, Ryu SH. Understanding of the roles of phospholipase D and phosphatidic acid through their binding partners. Prog Lipid Res (2011) 51:71-81. doi:10.1016/j.plipres.2011.12.003.
50. Honda A, Nogami M, Yokozeki T, Yamazaki M, Nakamura H, Watanabe H, et al. Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell (1999) 99:521-32. doi:10.1016/S0092-8674(00)81540-8.
51. Mima J, Wickner W. Complex lipid requirements for SNARE- and SNARE chaperone-dependent membrane fusion. J Biol Chem (2009) 284:27114-22. doi:10.1074/jbc. M109.010223.
52. Darios F, Davletov B. Omega-3 and omega-6 fatty acids stimulate cell membrane expansion by acting on syntaxin 3. Nature (2006) 440:813-7. doi:10.1038/nature04598.
53. Darios F, Wasser C, Shakirzyanova A, Giniatullin A, Goodman K, Munoz-Bravo JL, et al. Sphingosine facilitates SNARE complex assembly and activates synaptic vesicle exocytosis. Neuron (2009) 62:683-94. doi:10.1016/j.neuron.2009.04.024.
54. Chernomordik LV, Kozlov MM. Membrane hemifusion:crossing a chasm in two leaps. Cell (2005) 123:375-82. doi:10.1016/j.cell.2005.10.015.
55. Mrowczynska L, Lindqvist C, Iglic A, Hagerstrand H. Spontaneous curvature of ganglioside GM1-effect of cross-linking. Biochem Biophys Res Commun (2012) 422:776-9. doi:10.1016/j.bbrc.2012.05.083.
56. Zimmerberg J, Chernomordik LV. Membrane fusion. Adv Drug Deliv Rev (1999) 38:197-205. doi:10.1016/S0169-409X(99)00029-0.
57. Lai AL, Tamm LK, Ellena JF, Cafiso DS. Synaptotagmin 1 modulates lipid acyl chain order in lipid bilayers by demixing phosphatidylserine. J Biol Chem (2011) 286:25291-300. doi:10.1074/jbc. M111.258848.