Membrane Lipids in Presynaptic Function and Disease

Neuron

Volumn 90, Issue 1, 2016, Pages 11-25

  Lauwers, Elsa ^a,b   Goodchild, Rose ^a,b   Verstreken, Patrik ^a,b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE LIPID; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; POLYPHOSPHOINOSITIDE; SYNAPTOJANIN; SYNAPTOJANIN 1; SYNTAXIN 1A; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; ION CHANNEL; PHOSPHATIDYLINOSITOL; SNARE PROTEIN;

BIPOLAR DISORDER; CHANNEL GATING; DOWN SYNDROME; ENDOCYTOSIS; EXOCYTOSIS; FRIEDREICH ATAXIA; HUMAN; MEMBRANE CURVATURE; MEMBRANE FLUIDITY; MEMBRANE STRUCTURE; MEMBRANE TRANSPORT; NERVE CELL EXCITABILITY; NERVE DEGENERATION; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PARKINSON DISEASE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REVIEW; SCHIZOPHRENIA; SYNAPSE VESICLE; ANIMAL; GENETICS; LIPID METABOLISM; METABOLISM; PROTEIN TRANSPORT; SYNAPTIC TRANSMISSION;

ANIMALS; BIPOLAR DISORDER; ENDOCYTOSIS; EXOCYTOSIS; HUMANS; ION CHANNELS; LIPID METABOLISM; MEMBRANE LIPIDS; MEMBRANE PROTEINS; NEUROTRANSMITTER AGENTS; PARKINSON DISEASE; PHOSPHATIDYLINOSITOLS; PRESYNAPTIC TERMINALS; PROTEIN TRANSPORT; SCHIZOPHRENIA; SNARE PROTEINS; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 84977479621     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.02.033     Document Type: Review

References (165)

1. Ambroso, M.R., Hegde, B.G., Langen, R., Endophilin A1 induces different membrane shapes using a conformational switch that is regulated by phosphorylation. Proc. Natl. Acad. Sci. U S A 111 (2014), 6982–6987.
2. Antonescu, C.N., Aguet, F., Danuser, G., Schmid, S.L., Phosphatidylinositol-(4,5)-bisphosphate regulates clathrin-coated pit initiation, stabilization, and size. Mol. Biol. Cell 22 (2011), 2588–2600.
3. Antonny, B., Mechanisms of membrane curvature sensing. Annu. Rev. Biochem. 80 (2011), 101–123.
4. Antonny, B., Vanni, S., Shindou, H., Ferreira, T., From zero to six double bonds: phospholipid unsaturation and organelle function. Trends Cell Biol. 25 (2015), 427–436.
5. Aoyagi, K., Sugaya, T., Umeda, M., Yamamoto, S., Terakawa, S., Takahashi, M., The activation of exocytotic sites by the formation of phosphatidylinositol 4,5-bisphosphate microdomains at syntaxin clusters. J. Biol. Chem. 280 (2005), 17346–17352.
6. Arranz, A.M., Delbroek, L., Van Kolen, K., Guimarães, M.R., Mandemakers, W., Daneels, G., Matta, S., Calafate, S., Shaban, H., Baatsen, P., et al. LRRK2 functions in synaptic vesicle endocytosis through a kinase-dependent mechanism. J. Cell Sci. 128 (2015), 541–552.
7. Bar-On, D., Wolter, S., van de Linde, S., Heilemann, M., Nudelman, G., Nachliel, E., Gutman, M., Sauer, M., Ashery, U., Super-resolution imaging reveals the internal architecture of nano-sized syntaxin clusters. J. Biol. Chem. 287 (2012), 27158–27167.
8. Bartels, T., Ahlstrom, L.S., Leftin, A., Kamp, F., Haass, C., Brown, M.F., Beyer, K., The N-terminus of the intrinsically disordered protein α-synuclein triggers membrane binding and helix folding. Biophys. J. 99 (2010), 2116–2124.
9. Bayot, A., Reichman, S., Lebon, S., Csaba, Z., Aubry, L., Sterkers, G., Husson, I., Rak, M., Rustin, P., Cis-silencing of PIP5K1B evidenced in Friedreich's ataxia patient cells results in cytoskeleton anomalies. Hum. Mol. Genet. 22 (2013), 2894–2904.
10. Berman, D.E., Dall'Armi, C., Voronov, S.V., McIntire, L.B.J., Zhang, H., Moore, A.Z., Staniszewski, A., Arancio, O., Kim, T.-W., Di Paolo, G., Oligomeric amyloid-β peptide disrupts phosphatidylinositol-4,5-bisphosphate metabolism. Nat. Neurosci. 11 (2008), 547–554.
11. Bozek, K., Wei, Y., Yan, Z., Liu, X., Xiong, J., Sugimoto, M., Tomita, M., Pääbo, S., Sherwood, C.C., Hof, P.R., et al. Organization and evolution of brain lipidome revealed by large-scale analysis of human, chimpanzee, macaque, and mouse tissues. Neuron 85 (2015), 695–702.
12. Bruckner, R.J., Mansy, S.S., Ricardo, A., Mahadevan, L., Szostak, J.W., Flip-flop-induced relaxation of bending energy: implications for membrane remodeling. Biophys. J. 97 (2009), 3113–3122.
13. Burré, J., Sharma, M., Südhof, T.C., Definition of a molecular pathway mediating α-synuclein neurotoxicity. J. Neurosci. 35 (2015), 5221–5232.
14. Caccin, P., Scorzeto, M., Damiano, N., Marin, O., Megighian, A., Montecucco, C., The synaptotagmin juxtamembrane domain is involved in neuroexocytosis. FEBS Open Biol. 5 (2015), 388–396.
15. Chan, R.B., Oliveira, T.G., Cortes, E.P., Honig, L.S., Duff, K.E., Small, S.A., Wenk, M.R., Shui, G., Di Paolo, G., Comparative lipidomic analysis of mouse and human brain with Alzheimer disease. J. Biol. Chem. 287 (2012), 2678–2688.
16. Chandra, S., Chen, X., Rizo, J., Jahn, R., Südhof, T.C., A broken alpha -helix in folded alpha -Synuclein. J. Biol. Chem. 278 (2003), 15313–15318.
17. Chang-Ileto, B., Frere, S.G., Chan, R.B., Voronov, S.V., Roux, A., Di Paolo, G., Synaptojanin 1-mediated PI(4,5)P2 hydrolysis is modulated by membrane curvature and facilitates membrane fission. Dev. Cell 20 (2011), 206–218.
18. Chapman, E.R., Synaptotagmin: a Ca(2+) sensor that triggers exocytosis?. Nat. Rev. Mol. Cell Biol. 3 (2002), 498–508.
19. Cheng, D., Jenner, A.M., Shui, G., Cheong, W.F., Mitchell, T.W., Nealon, J.R., Kim, W.S., McCann, H., Wenk, M.R., Halliday, G.M., Garner, B., Lipid pathway alterations in Parkinson's disease primary visual cortex. PLoS ONE, 6, 2011, e17299.
20. Cohen, J.S., Brown, H.A., Phospholipases stimulate secretion in RBL mast cells. Biochemistry 40 (2001), 6589–6597.
21. Cossec, J.-C., Lavaur, J., Berman, D.E., Rivals, I., Hoischen, A., Stora, S., Ripoll, C., Mircher, C., Grattau, Y., Olivomarin, J.-C., et al. Trisomy for synaptojanin1 in Down syndrome is functionally linked to the enlargement of early endosomes. Hum. Mol. Genet. 21 (2012), 3156–3172.
22. Cremona, O., Di Paolo, G., Wenk, M.R., Lüthi, A., Kim, W.T., Takei, K., Daniell, L., Nemoto, Y., Shears, S.B., Flavell, R.A., et al. Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99 (1999), 179–188.
23. Darios, F., Wasser, C., Shakirzyanova, A., Giniatullin, A., Goodman, K., Munoz-Bravo, J.L., Raingo, J., Jorgačevski, J., Kreft, M., Zorec, R., et al. Sphingosine facilitates SNARE complex assembly and activates synaptic vesicle exocytosis. Neuron 62 (2009), 683–694.
24. Dason, J.S., Smith, A.J., Marin, L., Charlton, M.P., Vesicular sterols are essential for synaptic vesicle cycling. J. Neurosci. 30 (2010), 15856–15865.
25. Davletov, B., Montecucco, C., Lipid function at synapses. Curr. Opin. Neurobiol. 20 (2010), 543–549.
26. 2+/phospholipid binding. J. Biol. Chem. 268 (1993), 26386–26390.
27. Di Paolo, G., De Camilli, P., Phosphoinositides in cell regulation and membrane dynamics. Nature 443 (2006), 651–657.
28. Di Paolo, G., Kim, T.-W., Linking lipids to Alzheimer's disease: cholesterol and beyond. Nat. Rev. Neurosci. 12 (2011), 284–296.
29. Di Paolo, G., Moskowitz, H.S., Gipson, K., Wenk, M.R., Voronov, S., Obayashi, M., Flavell, R., Fitzsimonds, R.M., Ryan, T.A., De Camilli, P., Impaired PtdIns(4,5)P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking. Nature 431 (2004), 415–422.
30. Ellis, S.R., Brown, S.H., In Het Panhuis, M., Blanksby, S.J., Mitchell, T.W., Surface analysis of lipids by mass spectrometry: more than just imaging. Prog. Lipid Res. 52 (2013), 329–353.
31. Engel, L.A., Jing, Z., O'Brien, D.E., Sun, M., Kotzbauer, P.T., Catalytic function of PLA2G6 is impaired by mutations associated with infantile neuroaxonal dystrophy but not dystonia-parkinsonism. PLoS ONE, 5, 2010, e12897.
32. Ford, M.G.J., Mills, I.G., Peter, B.J., Vallis, Y., Praefcke, G.J.K., Evans, P.R., McMahon, H.T., Curvature of clathrin-coated pits driven by epsin. Nature 419 (2002), 361–366.
33. Fusco, G., De Simone, A., Gopinath, T., Vostrikov, V., Vendruscolo, M., Dobson, C.M., Veglia, G., Direct observation of the three regions in α-synuclein that determine its membrane-bound behaviour. Nat. Commun., 5, 2014, 3827.
34. Gallop, J.L., Jao, C.C., Kent, H.M., Butler, P.J.G., Evans, P.R., Langen, R., McMahon, H.T., Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J. 25 (2006), 2898–2910.
35. Galvagnion, C., Buell, A.K., Meisl, G., Michaels, T.C.T., Vendruscolo, M., Knowles, T.P.J., Dobson, C.M., Lipid vesicles trigger α-synuclein aggregation by stimulating primary nucleation. Nat. Chem. Biol. 11 (2015), 229–234.
36. Gamper, N., Shapiro, M.S., Regulation of ion transport proteins by membrane phosphoinositides. Nat. Rev. Neurosci. 8 (2007), 921–934.
37. Garcia-Cazorla, À., Mochel, F., Lamari, F., Saudubray, J.-M., The clinical spectrum of inherited diseases involved in the synthesis and remodeling of complex lipids. A tentative overview. J. Inherit. Metab. Dis. 38 (2015), 19–40.
38. George, A.A., Hayden, S., Holzhausen, L.C., Ma, E.Y., Suzuki, S.C., Brockerhoff, S.E., Synaptojanin 1 is required for endolysosomal trafficking of synaptic proteins in cone photoreceptor inner segments. PLoS ONE, 9, 2014, e84394.
39. Gimber, N., Tadeus, G., Maritzen, T., Schmoranzer, J., Haucke, V., Diffusional spread and confinement of newly exocytosed synaptic vesicle proteins. Nat. Commun., 6, 2015, 8392.
40. Gong, L.-W., De Camilli, P., Regulation of postsynaptic AMPA responses by synaptojanin 1. Proc. Natl. Acad. Sci. U S A 105 (2008), 17561–17566.
41. Groffen, A.J., Martens, S., Díez Arazola, R., Cornelisse, L.N., Lozovaya, N., de Jong, A.P.H., Goriounova, N.A., Habets, R.L.P., Takai, Y., Borst, J.G., et al. Doc2b is a high-affinity Ca2+ sensor for spontaneous neurotransmitter release. Science 327 (2010), 1614–1618.
42. Grossfield, A., Feller, S.E., Pitman, M.C., A role for direct interactions in the modulation of rhodopsin by omega-3 polyunsaturated lipids. Proc. Natl. Acad. Sci. U S A 103 (2006), 4888–4893.
43. Guo, S., Stolz, L.E., Lemrow, S.M., York, J.D., SAC1-like domains of yeast SAC1, INP52, and INP53 and of human synaptojanin encode polyphosphoinositide phosphatases. J. Biol. Chem. 274 (1999), 12990–12995.
44. Haass, C., Take five–BACE and the gamma-secretase quartet conduct Alzheimer's amyloid beta-peptide generation. EMBO J. 23 (2004), 483–488.
45. Hammond, G.R.V., Balla, T., Polyphosphoinositide binding domains: key to inositol lipid biology. Biochim. Biophys. Acta 1851 (2015), 746–758.
46. Hansen, S.B., Tao, X., MacKinnon, R., Structural basis of PIP2 activation of the classical inward rectifier K+ channel Kir2.2. Nature 477 (2011), 495–498.
47. Harel, A., Wu, F., Mattson, M.P., Morris, C.M., Yao, P.J., Evidence for CALM in directing VAMP2 trafficking. Traffic 9 (2008), 417–429.
48. Harris, T.W., Hartwieg, E., Horvitz, H.R., Jorgensen, E.M., Mutations in synaptojanin disrupt synaptic vesicle recycling. J. Cell Biol. 150 (2000), 589–600.
49. Hilgemann, D.W., Feng, S., Nasuhoglu, C., The complex and intriguing lives of PIP2 with ion channels and transporters. Sci. STKE, 2001, 2001, re19.
50. Huang, C.L., Feng, S., Hilgemann, D.W., Direct activation of inward rectifier potassium channels by PIP2 and its stabilization by Gbetagamma. Nature 391 (1998), 803–806.
51. Jähne, S., Rizzoli, S.O., Helm, M.S., The structure and function of presynaptic endosomes. Exp. Cell Res. 335 (2015), 172–179.
52. Ji, J., Kline, A.E., Amoscato, A., Samhan-Arias, A.K., Sparvero, L.J., Tyurin, V.A., Tyurina, Y.Y., Fink, B., Manole, M.D., Puccio, A.M., et al. Lipidomics identifies cardiolipin oxidation as a mitochondrial target for redox therapy of brain injury. Nat. Neurosci. 15 (2012), 1407–1413.
53. Jost, M., Simpson, F., Kavran, J.M., Lemmon, M.A., Schmid, S.L., Phosphatidylinositol-4,5-bisphosphate is required for endocytic coated vesicle formation. Curr. Biol. 8 (1998), 1399–1402.
54. Kaether, C., Haass, C., A lipid boundary separates APP and secretases and limits amyloid beta-peptide generation. J. Cell Biol. 167 (2004), 809–812.
55. Kamel, F., Goldman, S.M., Umbach, D.M., Chen, H., Richardson, G., Barber, M.R., Meng, C., Marras, C., Korell, M., Kasten, M., et al. Dietary fat intake, pesticide use, and Parkinson's disease. Parkinsonism Relat. Disord. 20 (2014), 82–87.
56. Khelashvili, G., Galli, A., Weinstein, H., Phosphatidylinositol 4,5-biphosphate (PIP(2)) lipids regulate the phosphorylation of syntaxin N-terminus by modulating both its position and local structure. Biochemistry 51 (2012), 7685–7698.
57. Khuong, T.M., Habets, R.L.P., Kuenen, S., Witkowska, A., Kasprowicz, J., Swerts, J., Jahn, R., van den Bogaart, G., Verstreken, P., Synaptic PI(3,4,5)P3 is required for Syntaxin1A clustering and neurotransmitter release. Neuron 77 (2013), 1097–1108.
58. Kim, W.T., Chang, S., Daniell, L., Cremona, O., Di Paolo, G., De Camilli, P., Delayed reentry of recycling vesicles into the fusion-competent synaptic vesicle pool in synaptojanin 1 knockout mice. Proc. Natl. Acad. Sci. U S A 99 (2002), 17143–17148.
59. Kolomiytseva, I.K., Perepelkina, N.I., Zharikova, A.D., Popov, V.I., Membrane lipids and morphology of brain cortex synaptosomes isolated from hibernating Yakutian ground squirrel. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 151 (2008), 386–391.
60. Kononenko, N.L., Haucke, V., Molecular mechanisms of presynaptic membrane retrieval and synaptic vesicle reformation. Neuron 85 (2015), 484–496.
61. Koo, S.J., Kochlamazashvili, G., Rost, B., Puchkov, D., Gimber, N., Lehmann, M., Tadeus, G., Schmoranzer, J., Rosenmund, C., Haucke, V., Maritzen, T., Vesicular Synaptobrevin/VAMP2 Levels Guarded by AP180 Control Efficient Neurotransmission. Neuron 88 (2015), 330–344.
62. Kozlov, M.M., McMahon, H.T., Chernomordik, L.V., Protein-driven membrane stresses in fusion and fission. Trends Biochem. Sci. 35 (2010), 699–706.
63. 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. The Sac1 domain of SYNJ1 identified mutated in a family with early-onset progressive Parkinsonism with generalized seizures. Hum. Mutat. 34 (2013), 1200–1207.
64. Kurian, M.A., Meyer, E., Vassallo, G., Morgan, N.V., Prakash, N., Pasha, S., Hai, N.A., Shuib, S., Rahman, F., Wassmer, E., et al. Phospholipase C beta 1 deficiency is associated with early-onset epileptic encephalopathy. Brain 133 (2010), 2964–2970.
65. Kurian, M.A., McNeill, A., Lin, J.P., Maher, E.R., Childhood disorders of neurodegeneration with brain iron accumulation (NBIA). Dev. Med. Child Neurol. 53 (2011), 394–404.
66. Lam, A.D., Tryoen-Toth, P., Tsai, B., Vitale, N., Stuenkel, E.L., SNARE-catalyzed fusion events are regulated by Syntaxin1A-lipid interactions. Mol. Biol. Cell 19 (2008), 485–497.
67. Lang, T., Bruns, D., Wenzel, D., Riedel, D., Holroyd, P., Thiele, C., Jahn, R., SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J. 20 (2001), 2202–2213.
68. Lee, S.-J., Liyanage, U., Bickel, P.E., Xia, W., Lansbury, P.T. Jr., Kosik, K.S., A detergent-insoluble membrane compartment contains A beta in vivo. Nat. Med. 4 (1998), 730–734.
69. Leoni, V., Caccia, C., The impairment of cholesterol metabolism in Huntington disease. Biochim. Biophys. Acta 1851 (2015), 1095–1105.
70. Lewis, K.T., Maddipati, K.R., Taatjes, D.J., Jena, B.P., Neuronal porosome lipidome. J. Cell. Mol. Med. 18 (2014), 1927–1937.
71. Li, G., Larson, E.B., Sonnen, J.A., Shofer, J.B., Petrie, E.C., Schantz, A., Peskind, E.R., Raskind, M.A., Breitner, J.C., Montine, T.J., Statin therapy is associated with reduced neuropathologic changes of Alzheimer disease. Neurology 69 (2007), 878–885.
72. Li, J., Lü, S., Liu, Y., Pang, C., Chen, Y., Zhang, S., Yu, H., Long, M., Zhang, H., Logothetis, D.E., et al. Identification of the Conformational transition pathway in PIP2 Opening Kir Channels. Sci. Rep., 5, 2015, 11289.
73. Liu, J., Sun, Y., Drubin, D.G., Oster, G.F., The mechanochemistry of endocytosis. PLoS Biol., 7, 2009, e1000204.
74. Mani, M., Lee, S.Y., Lucast, L., Cremona, O., Di Paolo, G., De Camilli, P., Ryan, T.A., The dual phosphatase activity of synaptojanin1 is required for both efficient synaptic vesicle endocytosis and reavailability at nerve terminals. Neuron 56 (2007), 1004–1018.
75. Mapstone, M., Cheema, A.K., Fiandaca, M.S., Zhong, X., Mhyre, T.R., MacArthur, L.H., Hall, W.J., Fisher, S.G., Peterson, D.R., Haley, J.M., et al. Plasma phospholipids identify antecedent memory impairment in older adults. Nat. Med. 20 (2014), 415–418.
76. Marszalek, J.R., Lodish, H.F., Docosahexaenoic acid, fatty acid-interacting proteins, and neuronal function: breastmilk and fish are good for you. Annu. Rev. Cell Dev. Biol. 21 (2005), 633–657.
77. Martens, S., Kozlov, M.M., McMahon, H.T., How synaptotagmin promotes membrane fusion. Science 316 (2007), 1205–1208.
78. 2-binding effector proteins for vesicle exocytosis. Biochim. Biophys. Acta 1851 (2015), 785–793.
79. Martín, V., Fabelo, N., Santpere, G., Puig, B., Marín, R., Ferrer, I., Díaz, M., Lipid alterations in lipid rafts from Alzheimer's disease human brain cortex. J. Alzheimers Dis. 19 (2010), 489–502.
80. Massol, R.H., Boll, W., Griffin, A.M., Kirchhausen, T., A burst of auxilin recruitment determines the onset of clathrin-coated vesicle uncoating. Proc. Natl. Acad. Sci. U S A 103 (2006), 10265–10270.
81. Masuda, M., Takeda, S., Sone, M., Ohki, T., Mori, H., Kamioka, Y., Mochizuki, N., Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. EMBO J. 25 (2006), 2889–2897.
82. Matta, S., Van Kolen, K., da Cunha, R., van den Bogaart, G., Mandemakers, W., Miskiewicz, K., De Bock, P.-J., Morais, V.A., Vilain, S., Haddad, D., et al. LRRK2 controls an EndoA phosphorylation cycle in synaptic endocytosis. Neuron 75 (2012), 1008–1021.
83. McIntire, L.B.J., Berman, D.E., Myaeng, J., Staniszewski, A., Arancio, O., Di Paolo, G., Kim, T.-W., Reduction of synaptojanin 1 ameliorates synaptic and behavioral impairments in a mouse model of Alzheimer's disease. J. Neurosci. 32 (2012), 15271–15276.
84. McIntosh, T.J., The effect of cholesterol on the structure of phosphatidylcholine bilayers. Biochim. Biophys. Acta 513 (1978), 43–58.
85. McMahon, H.T., Boucrot, E., Membrane curvature at a glance. J. Cell Sci. 128 (2015), 1065–1070.
86. McMahon, H.T., Gallop, J.L., Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438 (2005), 590–596.
87. Messa, M., Fernández-Busnadiego, R., Sun, E.W., Chen, H., Czapla, H., Wrasman, K., Wu, Y., Ko, G., Ross, T., Wendland, B., De Camilli, P., Epsin deficiency impairs endocytosis by stalling the actin-dependent invagination of endocytic clathrin-coated pits. eLife, 3, 2014, e03311.
88. Miller, S.E., Mathiasen, S., Bright, N.A., Pierre, F., Kelly, B.T., Kladt, N., Schauss, A., Merrifield, C.J., Stamou, D., Höning, S., Owen, D.J., CALM regulates clathrin-coated vesicle size and maturation by directly sensing and driving membrane curvature. Dev. Cell 33 (2015), 163–175.
89. Milosevic, I., Sørensen, J.B., Lang, T., Krauss, M., Nagy, G., Haucke, V., Jahn, R., Neher, E., Plasmalemmal phosphatidylinositol-4,5-bisphosphate level regulates the releasable vesicle pool size in chromaffin cells. J. Neurosci. 25 (2005), 2557–2565.
90. Milosevic, I., Giovedi, S., Lou, X., Raimondi, A., Collesi, C., Shen, H., Paradise, S., O'Toole, E., Ferguson, S., Cremona, O., De Camilli, P., Recruitment of endophilin to clathrin-coated pit necks is required for efficient vesicle uncoating after fission. Neuron 72 (2011), 587–601.
91. Milovanovic, D., Honigmann, A., Koike, S., Göttfert, F., Pähler, G., Junius, M., Müllar, S., Diederichsen, U., Janshoff, A., Grubmüller, H., et al. Hydrophobic mismatch sorts SNARE proteins into distinct membrane domains. Nat. Commun., 6, 2015, 5984.
92. Mitchell, D.C., Niu, S.L., Litman, B.J., Optimization of receptor-G protein coupling by bilayer lipid composition I: kinetics of rhodopsin-transducin binding. J. Biol. Chem. 276 (2001), 42801–42806.
93. Morel, E., Chamoun, Z., Lasiecka, Z.M., Chan, R.B., Williamson, R.L., Vetanovetz, C., Dall'Armi, C., Simoes, S., Point Du Jour, K.S., McCabe, B.D., et al. Phosphatidylinositol-3-phosphate regulates sorting and processing of amyloid precursor protein through the endosomal system. Nat. Commun., 4, 2013, 2250.
94. Murray, D.H., Tamm, L.K., Clustering of syntaxin-1A in model membranes is modulated by phosphatidylinositol 4,5-bisphosphate and cholesterol. Biochemistry 48 (2009), 4617–4625.
95. Murray, D.H., Tamm, L.K., Molecular mechanism of cholesterol- and polyphosphoinositide-mediated syntaxin clustering. Biochemistry 50 (2011), 9014–9022.
96. Narkis, G., Ofir, R., Landau, D., Manor, E., Volokita, M., Hershkowitz, R., Elbedour, K., Birk, O.S., Lethal contractural syndrome type 3 (LCCS3) is caused by a mutation in PIP5K1C, which encodes PIPKI gamma of the phophatidylinsitol pathway. Am. J. Hum. Genet. 81 (2007), 530–539.
97. Narkis, G., Ofir, R., Manor, E., Landau, D., Elbedour, K., Birk, O.S., Lethal congenital contractural syndrome type 2 (LCCS2) is caused by a mutation in ERBB3 (Her3), a modulator of the phosphatidylinositol-3-kinase/Akt pathway. Am. J. Hum. Genet. 81 (2007), 589–595.
98. Neef, A.B., Schultz, C., Selective fluorescence labeling of lipids in living cells. Angew. Chem. Int. Ed. Engl. 48 (2009), 1498–1500.
99. Neuringer, M., Connor, W.E., Lin, D.S., Barstad, L., Luck, S., Biochemical and functional effects of prenatal and postnatal omega 3 fatty acid deficiency on retina and brain in rhesus monkeys. Proc. Natl. Acad. Sci. U S A 83 (1986), 4021–4025.
100. Olgiati, S., De Rosa, A., Quadri, M., Criscuolo, C., Breedveld, G.J., Picillo, M., Pappatà, S., Quarantelli, M., Barone, P., De Michele, G., Bonifati, V., PARK20 caused by SYNJ1 homozygous Arg258Gln mutation in a new Italian family. Neurogenetics 15 (2014), 183–188.
101. Oliveira, T.G., Chan, R.B., Bravo, F.V., Miranda, A., Silva, R.R., Zhou, B., Marques, F., Pinto, V., Cerqueira, J.J., Di Paolo, G., Sousa, N., The impact of chronic stress on the rat brain lipidome. Mol. Psychiatry 21 (2016), 80–88.
102. Paisan-Ruiz, C., Bhatia, K.P., Li, A., Hernandez, D., Davis, M., Wood, N.W., Hardy, J., Houlden, H., Singleton, A., Schneider, S.A., Characterization of PLA2G6 as a locus for dystonia-parkinsonism. Ann. Neurol. 65 (2009), 19–23.
103. Pandolfo, M., Friedreich ataxia: the clinical picture. J. Neurol. 256:Suppl 1 (2009), 3–8.
104. Perera, R.M., Zoncu, R., Lucast, L., De Camilli, P., Toomre, D., Two synaptojanin 1 isoforms are recruited to clathrin-coated pits at different stages. Proc. Natl. Acad. Sci. U S A 103 (2006), 19332–19337.
105. Peter, B.J., Kent, H.M., Mills, I.G., Vallis, Y., Butler, P.J.G., Evans, P.R., McMahon, H.T., BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303 (2004), 495–499.
106. Pinot, M., Vanni, S., Pagnotta, S., Lacas-Gervais, S., Payet, L.A., Ferreira, T., Gautier, R., Goud, B., Antonny, B., Barelli, H., Lipid cell biology. Polyunsaturated phospholipids facilitate membrane deformation and fission by endocytic proteins. Science 345 (2014), 693–697.
107. Pitman, M.C., Grossfield, A., Suits, F., Feller, S.E., Role of cholesterol and polyunsaturated chains in lipid-protein interactions: molecular dynamics simulation of rhodopsin in a realistic membrane environment. J. Am. Chem. Soc. 127 (2005), 4576–4577.
108. Posor, Y., Eichhorn-Gruenig, M., Puchkov, D., Schöneberg, J., Ullrich, A., Lampe, A., Müller, R., Zarbakhsh, S., Gulluni, F., Hirsch, E., et al. Spatiotemporal control of endocytosis by phosphatidylinositol-3,4-bisphosphate. Nature 499 (2013), 233–237.
109. Posor, Y., Eichhorn-Grünig, M., Haucke, V., Phosphoinositides in endocytosis. Biochim. Biophys. Acta 1851 (2015), 794–804.
110. Puchkov, D., Haucke, V., Greasing the synaptic vesicle cycle by membrane lipids. Trends Cell Biol. 23 (2013), 493–503.
111. Quadri, M., Fang, M., Picillo, M., Olgiati, S., Breedveld, G.J., Graafland, J., Wu, B., Xu, F., Erro, R., Amboni, M., et al., International Parkinsonism Genetics Network. Mutation in the SYNJ1 gene associated with autosomal recessive, early-onset Parkinsonism. Hum. Mutat. 34 (2013), 1208–1215.
112. Qualmann, B., Koch, D., Kessels, M.M., Let's go bananas: revisiting the endocytic BAR code. EMBO J. 30 (2011), 3501–3515.
113. Quetglas, S., Leveque, C., Miquelis, R., Sato, K., Seagar, M., Ca2+-dependent regulation of synaptic SNARE complex assembly via a calmodulin- and phospholipid-binding domain of synaptobrevin. Proc. Natl. Acad. Sci. U S A 97 (2000), 9695–9700.
114. Rappley, I., Myers, D.S., Milne, S.B., Ivanova, P.T., Lavoie, M.J., Brown, H.A., Selkoe, D.J., Lipidomic profiling in mouse brain reveals differences between ages and genders, with smaller changes associated with alpha-synuclein genotype. J. Neurochem. 111 (2009), 15–25.
115. Restituito, S., Khatri, L., Ninan, I., Mathews, P.M., Liu, X., Weinberg, R.J., Ziff, E.B., Synaptic autoregulation by metalloproteases and γ-secretase. J. Neurosci. 31 (2011), 12083–12093.
116. Rigoni, M., Caccin, P., Gschmeissner, S., Koster, G., Postle, A.D., Rossetto, O., Schiavo, G., Montecucco, C., Equivalent effects of snake PLA2 neurotoxins and lysophospholipid-fatty acid mixtures. Science 310 (2005), 1678–1680.
117. Ringstad, N., Nemoto, Y., De Camilli, P., 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 (1997), 8569–8574.
118. ®: a new approach to management of early Alzheimer's disease. J Nutr. Health Aging 18 (2014), 291–299.
119. Rizzoli, S.O., Synaptic vesicle recycling: steps and principles. EMBO J. 33 (2014), 788–822.
120. Rohrbough, J., Rushton, E., Palanker, L., Woodruff, E., Matthies, H.J., Acharya, U., Acharya, J.K., Broadie, K., Ceramidase regulates synaptic vesicle exocytosis and trafficking. J. Neurosci. 24 (2004), 7789–7803.
121. Saarikangas, J., Zhao, H., Pykäläinen, A., Laurinmäki, P., Mattila, P.K., Kinnunen, P.K.J., Butcher, S.J., Lappalainen, P., Molecular mechanisms of membrane deformation by I-BAR domain proteins. Curr. Biol. 19 (2009), 95–107.
122. Saito, T., Stopkova, P., Diaz, L., Papolos, D.F., Boussemart, L., Lachman, H.M., Polymorphism screening of PIK4CA: possible candidate gene for chromosome 22q11-linked psychiatric disorders. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 116B (2003), 77–83.
123. Salim, K., Bottomley, M.J., Querfurth, E., Zvelebil, M.J., Gout, I., Scaife, R., Margolis, R.L., Gigg, R., Smith, C.I., Driscoll, P.C., et al. Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. EMBO J. 15 (1996), 6241–6250.
124. Sastry, P.S.S., Lipids of nervous tissue: composition and metabolism. Prog. Lipid Res. 24 (1985), 69–176.
125. Schuske, K.R., Richmond, J.E., Matthies, D.S., Davis, W.S., Runz, S., Rube, D.A., van der Bliek, A.M., Jorgensen, E.M., Endophilin is required for synaptic vesicle endocytosis by localizing synaptojanin. Neuron 40 (2003), 749–762.
126. Shi, X., Bi, Y., Yang, W., Guo, X., Jiang, Y., Wan, C., Li, L., Bai, Y., Guo, J., Wang, Y., et al. Ca2+ regulates T-cell receptor activation by modulating the charge property of lipids. Nature 493 (2013), 111–115.
127. Sijben, J.W.C., De Wilde, M.C., Wieggers, R., Groenendijk, M., Kamphuis, P.J.G.H., A multi nutrient concept to enhance synapse formation and function : science behind a medical food for Alzheimer's disease. OCL 18 (2011), 267–270.
128. Sina, F., Shojaee, S., Elahi, E., Paisán-Ruiz, C., R632W mutation in PLA2G6 segregates with dystonia-parkinsonism in a consanguineous Iranian family. Eur. J. Neurol. 16 (2009), 101–104.
129. Sorre, B., Callan-Jones, A., Manzi, J., Goud, B., Prost, J., Bassereau, P., Roux, A., Nature of curvature coupling of amphiphysin with membranes depends on its bound density. Proc. Natl. Acad. Sci. U S A 109 (2012), 173–178.
130. Sparks, D.L., Sabbagh, M.N., Connor, D.J., Lopez, J., Launer, L.J., Browne, P., Wasser, D., Johnson-Traver, S., Lochhead, J., Ziolwolski, C., Atorvastatin for the treatment of mild to moderate Alzheimer disease: preliminary results. Arch. Neurol. 62 (2005), 753–757.
131. Spillantini, M.G., Goedert, M., The α-synucleinopathies: Parkinson's disease, dementia with Lewy bodies, and multiple system atrophy. Ann. N Y Acad. Sci. 920 (2000), 16–27.
132. Stopkova, P., Saito, T., Fann, C.S.J., Papolos, D.F., Vevera, J., Paclt, I., Zukov, I., Stryjer, R., Strous, R.D., Lachman, H.M., Polymorphism screening of PIP5K2A: a candidate gene for chromosome 10p-linked psychiatric disorders. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 123B (2003), 50–58.
133. Südhof, T.C., The synaptic vesicle cycle. Annu. Rev. Neurosci. 27 (2004), 509–547.
134. Südhof, T.C., The presynaptic active zone. Neuron 75 (2012), 11–25.
135. Sumi-Akamaru, H., Beck, G., Kato, S., Mochizuki, H., Neuroaxonal dystrophy in PLA2G6 knockout mice. Neuropathology 35 (2015), 289–302.
136. Takamori, S., Holt, M., Stenius, K., Lemke, E.A., Grønborg, M., Riedel, D., Urlaub, H., Schenck, S., Brügger, B., Ringler, P., et al. Molecular anatomy of a trafficking organelle. Cell 127 (2006), 831–846.
137. Thiele, C., Hannah, M.J., Fahrenholz, F., Huttner, W.B., Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat. Cell Biol. 2 (2000), 42–49.
138. van den Bogaart, G., Meyenberg, K., Risselada, H.J., Amin, H., Willig, K.I., Hubrich, B.E., Dier, M., Hell, S.W., Grubmüller, H., Diederichsen, U., Jahn, R., Membrane protein sequestering by ionic protein-lipid interactions. Nature 479 (2011), 552–555.
139. Van Epps, H.A., Hayashi, M., Lucast, L., Stearns, G.W., Hurley, J.B., De Camilli, P., Brockerhoff, S.E., The zebrafish nrc mutant reveals a role for the polyphosphoinositide phosphatase synaptojanin 1 in cone photoreceptor ribbon anchoring. J. Neurosci. 24 (2004), 8641–8650.
140. Vennekate, W., Schröder, S., Lin, C.-C., van den Bogaart, G., Grunwald, M., Jahn, R., Walla, P.J., Cis- and trans-membrane interactions of synaptotagmin-1. Proc. Natl. Acad. Sci. U S A 109 (2012), 11037–11042.
141. Verstreken, P., Koh, T.-W., Schulze, K.L., Zhai, R.G., Hiesinger, P.R., Zhou, Y., Mehta, S.Q., Cao, Y., Roos, J., Bellen, H.J., Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron 40 (2003), 733–748.
142. Vicinanza, M., D'Angelo, G., Di Campli, A., De Matteis, M.A., Function and dysfunction of the PI system in membrane trafficking. EMBO J. 27 (2008), 2457–2470.
143. 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. Synaptojanin 1-linked phosphoinositide dyshomeostasis and cognitive deficits in mouse models of Down's syndrome. Proc. Natl. Acad. Sci. U S A 105 (2008), 9415–9420.
144. Watanabe, S., Liu, Q., Davis, M.W., Hollopeter, G., Thomas, N., Jorgensen, N.B., Jorgensen, E.M., Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions. eLife, 2, 2013, e00723.
145. Waugh, M.G., PIPs in neurological diseases. Biochim. Biophys. Acta - Mol. Cell Biol. Lipids 1851 (2015), 1066–1082.
146. Wei, S., Ong, W.Y., Thwin, M.M., Fong, C.W., Farooqui, A.A., Gopalakrishnakone, P., Hong, W., Group IIA secretory phospholipase A2 stimulates exocytosis and neurotransmitter release in pheochromocytoma-12 cells and cultured rat hippocampal neurons. Neuroscience 121 (2003), 891–898.
147. Weissenhorn, W., Crystal structure of the endophilin-A1 BAR domain. J. Mol. Biol. 351 (2005), 653–661.
148. Wen, P.J., Osborne, S.L., Meunier, F.A., Dynamic control of neuroexocytosis by phosphoinositides in health and disease. Prog. Lipid Res. 50 (2011), 52–61.
149. Wenk, M.R., Pellegrini, L., Klenchin, V.A., Di Paolo, G., Chang, S., Daniell, L., Arioka, M., Martin, T.F., De Camilli, P., PIP kinase Igamma is the major PI(4,5)P(2) synthesizing enzyme at the synapse. Neuron 32 (2001), 79–88.
150. Wheeler, T.G., Benolken, R.M., Anderson, R.E., Visual membranes: specificity of fatty acid precursors for the electrical response to illumination. Science 188 (1975), 1312–1314.
151. Wierda, K.D.B., Toonen, R.F.G., de Wit, H., Brussaard, A.B., Verhage, M., Interdependence of PKC-dependent and PKC-independent pathways for presynaptic plasticity. Neuron 54 (2007), 275–290.
152. Williams, D., Vicôgne, J., Zaitseva, I., McLaughlin, S., Pessin, J.E., Evidence that electrostatic interactions between vesicle-associated membrane protein 2 and acidic phospholipids may modulate the fusion of transport vesicles with the plasma membrane. Mol. Biol. Cell 20 (2009), 4910–4919.
153. Wills, A.-M., Hubbard, J., Macklin, E.A., Glass, J., Tandan, R., Simpson, E.P., Brooks, B., Gelinas, D., Mitsumoto, H., Mozaffar, T., et al., MDA Clinical Research Network. Hypercaloric enteral nutrition in patients with amyotrophic lateral sclerosis: a randomised, double-blind, placebo-controlled phase 2 trial. Lancet 383 (2014), 2065–2072.
154. Winkler, E., Kamp, F., Scheuring, J., Ebke, A., Fukumori, A., Steiner, H., Generation of Alzheimer disease-associated amyloid β42/43 peptide by γ-secretase can be inhibited directly by modulation of membrane thickness. J. Biol. Chem. 287 (2012), 21326–21334.
155. Wood, P.L., Filiou, M.D., Otte, D.M., Zimmer, A., Turck, C.W., Lipidomics reveals dysfunctional glycosynapses in schizophrenia and the G72/G30 transgenic mouse. Schizophr. Res. 159 (2014), 365–369.
156. Yoshihara, M., Littleton, J.T., Synaptotagmin I functions as a calcium sensor to synchronize neurotransmitter release. Neuron 36 (2002), 897–908.
157. Yu, Y., Ramachandran, P.V., Wang, M.C., Shedding new light on lipid functions with CARS and SRS microscopy. Biochim. Biophys. Acta 1841 (2014), 1120–1129.
158. Zaydman, M.A., Silva, J.R., Delaloye, K., Li, Y., Liang, H., Larsson, H.P., Shi, J., Cui, J., Kv7.1 ion channels require a lipid to couple voltage sensing to pore opening. Proc. Natl. Acad. Sci. U S A 110 (2013), 13180–13185.
159. Zhang, Y., Appelkvist, E.-L., Kristensson, K., Dallner, G., The lipid compositions of different regions of rat brain during development and aging. Neurobiol. Aging 17 (1996), 869–875.
160. Zhang, Z., Hui, E., Chapman, E.R., Jackson, M.B., Phosphatidylserine regulation of Ca2+-triggered exocytosis and fusion pores in PC12 cells. Mol. Biol. Cell 20 (2009), 5086–5095.
161. Zhao, H., Michelot, A., Koskela, E.V., Tkach, V., Stamou, D., Drubin, D.G., Lappalainen, P., Membrane-sculpting BAR domains generate stable lipid microdomains. Cell Rep. 4 (2013), 1213–1223.
162. Zhong, S., Hsu, F., Stefan, C.J., Wu, X., Patel, A., Cosgrove, M.S., Mao, Y., Allosteric activation of the phosphoinositide phosphatase Sac1 by anionic phospholipids. Biochemistry 51 (2012), 3170–3177.
163. Zhou, L., McInnes, J., Verstreken, P., Ultrafast synaptic endocytosis cycles to the center stage. Dev. Cell 28 (2014), 5–6.
164. Zhu, L., Zhong, M., Elder, G.A., Sano, M., Holtzman, D.M., Gandy, S., Cardozo, C., Haroutunian, V., Robakis, N.K., Cai, D., Phospholipid dysregulation contributes to ApoE4-associated cognitive deficits in Alzheimer's disease pathogenesis. Proc. Natl. Acad. Sci. U S A 112 (2015), 11965–11970.
165. Zoncu, R., Perera, R.M., Sebastian, R., Nakatsu, F., Chen, H., Balla, T., Ayala, G., Toomre, D., De Camilli, P.V., Loss of endocytic clathrin-coated pits upon acute depletion of phosphatidylinositol 4,5-bisphosphate. Proc. Natl. Acad. Sci. U S A 104 (2007), 3793–3798.