The mechanisms of exocytosis in mast cells

Advances in Experimental Medicine and Biology

Volumn 716, Issue , 2011, Pages 107-122

  Blank, Ulrich ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALMODULIN; CARRIER PROTEIN; CELL PROTEIN; COMPLEXIN I PROTEIN; COMPLEXIN II PROTEIN; FC EPSILON RECEPTOR I; FC RECEPTOR; MAMMALIAN UNC 13 4; MEMBRANE FUSION PROTEIN; N ETHYLMALEIMIDE SENSITIVE FACTOR; PHOSPHATASE; PHOSPHOTRANSFERASE; PROTEIN KINASE C; PROTEIN SM; RAB PROTEIN; REGULATOR PROTEIN; SECRETORY CARRIER MEMBRANE PROTEIN; SNARE PROTEIN; SOLUBLE N ETHYLMALEIMIDE SENSITIVE FACTOR ATTACHMENT PROTEIN; SOLUBLE N ETHYLMALEIMIDE SENSITIVE FACTOR ATTACHMENT PROTEIN ALPHA; SYNAPTOTAGMIN; UNCLASSIFIED DRUG;

CALCIUM TRANSPORT; CELL ACTIVATION; CELL GRANULE; CELL KINETICS; CELL SECRETION; COMPLEX FORMATION; CROSS COUPLING REACTION; CYTOLOGY; CYTOSKELETON; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME MECHANISM; EXOCYTOSIS; HUMAN; LIPID MEMBRANE; MAST CELL; MAST CELL DEGRANULATION; MEDIATOR RELEASE; MEMBRANE FUSION; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; METABOLISM;

ANIMALS; EXOCYTOSIS; HUMANS; MAST CELLS; MEMBRANE FUSION; SIGNAL TRANSDUCTION;

EID: 79960918521     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4419-9533-9_7     Document Type: Review

References (110)

1. Blank U,Rivera J. The ins and outs oflgE-dependent mast-cell exocytosis. Trends Immunol 2004; 25(5):266-73.
2. Sudhof T. The synaptic vesicule cycle: a cascade of protein-protein interactions. Nature 1995; 375:645-53.
3. Alvarez de Toledo G, Fernandez J. Compound versus multigranular exocytosis in peritoneal cells. J Gen Physiol 1990; 95:397-402.
4. Rohlich P. Membrane-associated actin filaments in the cortical cytoplasm of the rat mast cell. Exp Cell Res 1975; 93(2):293-8.
5. Pejler G, Abrink M, Ringvall M et al. Mast cell proteases. Adv Immunol 2007; 95:167-255. (Pubitemid 47380506)
6. Monck JR, Oberhauser AF, Alvarez de Toledo G et al. Is swelling of the secretory granule matrix the force that dilates the exocytotic fusion pore? Biophys J 1991; 59(1):39-47.
7. Crivellato E, Nico B, Mallardi F et al. Piecemeal degranulation as a general secretory mechanism? Anat Rec A Discov Mol Cell Evol Biol 2003; 274(1):778-84.
8. Dvorak AM, Hammond ME, Morgan E et al. Evidence for a vesicular transport mechanism in guinea pig basophilic leukocytes. Lab Invest 1980; 42(2):263-76. (Pubitemid 10147712)
9. Williams RM, Webb WW. Single granule pH cycling in antigen-induced mast cell secretion [In Process Citation]. J Cell Sci 2000; 113(Pt 21):3839-50.
10. Galli S, Dvorak A, Dvorak H. Basophils and Mast Cells: Morphologic Insights into their Biology, Secretory Patterns and Function. Prog Allergy 1984; 34:1-141. (Pubitemid 14163358)
11. Alvarez de Toledo G, Fernandez JM. Patch-clamp measurements reveal multimodal distribution of granule sizes in rat mast cells. J Cell Biol 1990; 110(4):1033-9.
12. Griffiths G. Secretory lysosomes-a special mechanism of regulated secretion in haemopoietic cells. Trends Cell Biology 1996; 6:329-32. (Pubitemid 26283437)
13. Raposo G, Tenza D, Mecheri S et al. Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation. Mol Biol Cell 1997; 8(12):2631-45. (Pubitemid 27528227)
14. Sudhof TC, Rothman JE. Membrane fusion: grappling with SNARE and SM proteins. Science 2009: 323(5913):474-7.
15. HongW. SNAREs and traffic. Biochim Biophys Acta 2005; 1744(2):120-44. (Pubitemid 40798921)
16. Lippert U, Ferrari DM, Jahn R. Endobrevin/VAMP8 mediates exocytotic release of hexosaminidase from rat basophilic leukaemia cells. FEBS Lett 2007; 581(18):3479-84. (Pubitemid 47048197)
17. Puri N, Kruhlak MJ, Whiteheart SW et al. Mast cell degranulation requires N-ethylmaleimide-sensitive factor-mediated SNARE disassembly. J Immunol 2003; 171(10):5345-52. (Pubitemid 37432820)
18. Guo Z, Turner C, Castle D. Relocation of the t-SNARE SNAP-23 from lamellipodia-like cell surface projections regulates compound exocytosis in mast cells. Cell 1998; 94(4):537-48. (Pubitemid 28391869)
19. Paumet F, Le Mao J, Martin S et al. Soluble NSF attachment protein receptors (SNAREs) in RBL-2H3 mast cells: functional role of syntaxin 4 in exocytosis and identification of a vesicle-associated membrane protein 8-containing secretory compartment. J Immunol 2000;164(11):5850-7. (Pubitemid 30389829)
20. Sander LE, Frank SP, Bolat S et al. Vesicle associated membrane protein (VAMP)-7 and VAMP-8, but not VAMP-2 or VAMP-3, are required for activation-induced degranulation of mature human mast cells. Eur J Immunol 2008; 38(3):855-63.
21. Vaidyanathan VV, Puri N, Roche PA. The last exon of SNAP-23 regulates granule exocytosis from mast cells. J Biol Chem 2001; 276(27):25101-6.
22. Tiwari N, Wang CC, Brochetta C et al. VAMP-8 segregates mast cell-preformed mediator exocytosis from cytokine trafficking pathways. Blood 2008; 1 ll(7):3665-74.
23. Puri N, Roche PA. Mast cells possess distinct secretory granule subsets whose exocytosis is regulated by different SNARE isoforms. Proc Natl Acad Sci USA 2008; 105(7):2580-5. (Pubitemid 351520556)
24. Baram D, Adachi R, Medalia O et al. Synaptotagmin II negatively regulates Ca2t-triggered exocytosis of lysosomes in mast cells. J Exp Med 1999; 189(10):1649-58.
25. Tuvim MJ, Mospan AR, Burns KA et al. Synaptotagmin 2 couples mucin granule exocytosis to Ca2t signaling from endoplasmic reticulum. J Biol Chem 2009; 284(15):9781-7.
26. Miesenbock G, De Angelis DA, Rothman JE. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 1998; 394(6689):192-5. (Pubitemid 28325974)
27. Hibi T, Hirashima N, Nakanishi M. Rat basophilic leukemia cells express syntaxin-3 and VAMP-7 in granule membranes. Biochem Biophys Res Commun 2000; 271(1):36-41. (Pubitemid 30444852)
28. Weber T, Zemelman BV, McNew JA et al. Snarepins-minimal machinery for membrane fusion. Cell 1998; 92(6):759-72.
29. Lang T, Jahn R. Core proteins of the secretory machinery. Handb Exp Pharmacol 2008; (184):107-27.
30. Kanda H, Tamori Y, Shinoda H et al. Adipocytes from Munc18c-null mice show increased sensitivity to insulin-stimulated GLUT4 externalization. J Clin Invest 2005; 115(2):291-301. (Pubitemid 40385471)
31. Oh E, Spurlin BA, Pessin JE et al. Munc18c heterozygous knockout mice display increased susceptibility for severe glucose intolerance. Diabetes 2005; 54(3):638-47. (Pubitemid 40322065)
32. Burgoyne RD, Barclay JW, Ciufo LF et al. The functions of Munc18-1 in regulated exocytosis. Ann N Y Acad Sci 2009; 1152:76-86.
33. Shen J, Tareste DC, Paumet F et al. Selective activation of cognate SNAREpins by Sec1/Munc18 proteins. Cell 2007; 128(1):183-95. (Pubitemid 46048894)
34. Ho A, Morishita W, Atasoy D et al. Genetic analysis of Mint/X11 proteins: essential presynaptic functions of a neuronal adaptor protein family. J Neurosci 2006; 26(50):13089-101. (Pubitemid 44954627)
35. Higashio H, Nishimura N, Ishizaki H et al. Doc2 alpha and Munc13-4 regulate Ca(2t) -dependent secretory lysosome exocytosis in mast cells. J Immunol 2008; 180(7):4774-84.
36. Fukuda M, Imai A, Nashida Tetal. Slp4-a/granuphilin-a interacts with syntaxin-2/3 in a Munc18-2-dependent manner. J Biol Chem 2005; 280(47):39175-84. (Pubitemid 41713869)
37. Lam PP, Hyvarinen K, Kauppi M et al. A cytosolic splice variant of Cab45 interacts with Munc18b and impacts on amylase secretion by pancreatic acini. Mol Biol Cell 2007; 18(7):2473-80. (Pubitemid 47025713)
38. Martin-Verdeaux S, Pombo I, Iannascoli B et al. Analysis of Munc18-2 compartmentation in mast cells reveals a role for microtubules in granule exocytosis. J Cell Sci 2003; 116:325-34. (Pubitemid 36163873)
39. Nigam R, Sepulveda J, Tuvim M et al. Expression and transcriptional regulation of Munc18 isoforms in mast cells. Biochim Biophys Acta 2005; 1728(1-2):77-83. (Pubitemid 40409957)
40. Tadokoro S, Kurimoto T, Nakanishi M et al. Munc18-2 regulates exocytotic membrane fusion positively interacting with syntaxin-3 in RBL-2H3 cells. Mol Immunol 2007; 44(13):3427-33. (Pubitemid 46678193)
41. Cote M, Menager MM, Burgess A et al. Munc18-2 deficiency causes familial hemophagocytic lymphohistiocytosis type 5 and impairs cytotoxic granule exocytosis in patient NK cells. J Clin Invest 2009.
42. zur Stadt U., Rohr J., Seifert W., et al. Familial hemophagocytic lymphohistiocytosis type 5 (FHL-5) is caused by mutations in Munc18-2 and impaired binding to syntaxin 11 Am J Hum Genet 2009 85 4 482-92
43. Brochetta C, Vita F, Tiwari N et al. Involvement ofMunc18 isoforms in the regulation of granule exocytosis in neutrophils. Biochim Biophys Acta 2008; 1783(10):1781-91.
44. Rizo J, Rosenmund C. Synaptic vesicle fusion. Nat Struct Mol Biol 2008; 15(7):665-74. (Pubitemid 351932007)
45. Goishi K, Mizuno K, Nakanishi H et al. Involvement of Rab27 in antigen-induced histamine release from rat basophilic leukemia 2H3 cells. Biochem Biophys Res Commun 2004; 324(1):294-301. (Pubitemid 39311493)
46. Neeft M, Wieffer M, de Jong AS et al. Munc13-4 is an effector of rab27a and controls secretion oflysosomes in hematopoietic cells. Mol Biol Cell 2005; 16(2):731-41. (Pubitemid 40173984)
47. Feldmann J, Callebaut I, Raposo G et al. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell 2003; 115(4):461-73. (Pubitemid 37456808)
48. Menager MM, Menasche G, Romao M et al. Secretory cytotoxic granule maturation and exocytosis require the effector protein hMunc13-4. Nat Immunol 2007; 8(3):257-67. (Pubitemid 46745375)
49. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 2009; 10(8):513-25.
50. Roa M, Paumet F, Lemao J et al. Involvement of the ras-like GTPase rab3d in RBL-2H3 mast cell exocytosis following stimulation via high affinity IgE receptors (Fc epsilon RI). J Immunol 1997; 159(6):2815-23. (Pubitemid 127681303)
51. Tuvim MJ, Adachi R, Chocano JF et al. Rab3D, a small GTPase, is localized on mast cell secretory granules and translocates to the plasma membrane upon exocytosis. Am J Respir Cell Mol Biol 1999; 20(1):79-89. (Pubitemid 129504845)
52. Smith J, Thompson N, Armstrong Jet al. Rat Basophilic Leukaemia (RBL) cells overexpressing rab3a have a reversible block in antigen-stimulated exocytosis. Biochem J 1997; 323:321-8. (Pubitemid 27183111)
53. Riedel D, Antonin W, Fernandez-Chacon R et al. Rab3D is not required for exocrine exocytosis but for maintenance of normally sized secretory granules. Mol Cell Biol 2002; 22(18):6487-97.
54. Mizuno K, Tolmachova T, Ushakov DS et al. Rab27b regulates mast cell granule dynamics and secretion. Traffic 2007; 8(7):883-92. (Pubitemid 46971634)
55. Fukuda M. Versatile Role of Rab27 in Membrane Trafficking: Focus on the Rab27 Effector Families. J Biochem (Tokyo) 2005; 137(1):9-16.
56. Wu XS, Rao K, Zhang H et al. Identification of an organelle receptor for myosin-Va. Nat Cell Biol 2002: 4(4):271-8. (Pubitemid 34308852)
57. Maximov A, Tang J, Yang X et al. Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science 2009; 323(5913):516-21.
58. 2+sensitivity of the fusion process. J Cell Sci 2005; 118(Pt 10):2239-46. (Pubitemid 40872845)
59. Baram D, Mekori YA, Sagi-Eisenberg R. Synaptotagmin regulates mast cell functions. Immunol Rev 2001; 179:25-34. (Pubitemid 32171271)
60. Grimberg E, Peng Z, Hammel I et al. Synaptotagmin III is a critical factor for the formation of the perinuclear endocytic recycling compartment and determination of secretory granules size. J Cell Sci 2003; 116(Pt 1):145-54. (Pubitemid 36113973)
61. Haberman Y, Grimberg E, Fukuda M et al. Synaptotagmin IX, a possible linker between the perinuclear endocytic recycling compartment and the microtubules. J Cell Sci 2003; 116(Pt 21):4307-18. (Pubitemid 37369588)
62. Haberman Y, Ziv I, Gorzalczany Y et al. Classical protein kinase C(s) regulates targeting of synaptotagmin IX to the endocytic recycling compartment. J Cell Sci 2005; 118(Pt 8):1641-9. (Pubitemid 40691892)
63. Fernandez-Chacon R, de Toledo GA, Hammer RE et al. Analysis of SCAMP1 function in secretory vesicle exocytosis by means of gene targeting in mice. J Biol Chem 1999; 274(46):32551-4. (Pubitemid 129535279)
64. Castle JD, Guo Z, Liu L. Function of the t-SNARE SNAP-23 and secretory carrier membrane proteins (SCAMPs) in exocytosis in mast cells. Mol Immunol 2002; 38(16-18):1337-40. (Pubitemid 35253773)
65. Guo Z, Liu L, Cafiso D et al. Perturbation of a very late step of regulated exocytosis by a secretory carrier membrane protein (SCAMP2)-derived peptide. J Biol Chem 2002; 277(38):35357-63.
66. Liu L, Guo Z, Tieu Q et al. Role of secretory carrier membrane protein SCAMP2 in granule exocytosis. Mol Biol Cell 2002; 13(12):4266-78. (Pubitemid 35471184)
67. Peng Z, Beaven M.A. An essential role for phospholipase D in the activation of protein kinase C and degranulation in mast cells. J Immunol 2005; 174(9):5201-8. (Pubitemid 40593157)
68. Ichikawa S, Walde P. Phospholipase D-mediated aggregation, fusion and precipitation of phospholipid vesicles. Langmuir 2004; 20(3):941-9.
69. Koffer A, Tatham P, Gomperts B. Changes in the state ofActin during the exocytotic reaction ofpermeabilized rat mast cell. The Journal of Cell Biology 1990; 111:919-27.
70. Oliver C, Sahara N, Kitani S et al. Binding of monoclonal antibody AA4 to gangliosides on rat basophilic leukemia cells produces changes similar to those seen with Fc epsilon receptor activation. J Cell Biol 1992; 116(3):635-46.
71. Nielsen EH. A filamentous network surrounding secretory granules from mast cells. J Cell Sci 1990; 96 (Pt 1):43-6. (Pubitemid 120033935)
72. Pendleton A, Koffer A. Effects of latrunculin reveal requirements for the actin cytoskeleton during secretion from mast cells. Cell Motil Cytoskeleton 2001; 48(1):37-51. (Pubitemid 32037405)
73. Deng Z, Zink T, Chen HY et al. Impact of actin rearrangement and degranulation on the membrane structure of primary mast cells: a combined atomic force and laser scanning confocal microscopy investigation. Biophys J 2009; 96(4):1629-39.
74. Norman J, Price L, Ridley A et al. The small GTP-binding proteins, Rac and Rho, regulate cytoskeletal organization and exocytosis in mast cells by parallel pathways. Mol Biol Cell 1996; 7:1429-42. (Pubitemid 26304204)
75. Hong-Geller E, Holowka D, Siraganian RP et al. Activated Cdc42/Rac reconstitutes Fcvarepsilon Rl-mediated Ca2t mobilization and degranulation in mutant RBLmast cells. Proc NatlAcad SciUSA 2001; 98(3):1154-9. (Pubitemid 32121202)
76. Nishida K, Yamasaki S, Ito Y et al. Fc{epsilon}RI-mediated mast cell degranulation requires calcium-independent microtubule-dependent translocation of granules to the plasma membrane. J Cell Biol 2005; 170(1):115-26. (Pubitemid 40994101)
77. Smith AJ, Pfeiffer JR, Zhang J et al. Microtubule-dependent transport of secretory vesicles in RBL-2H3 cells. Traffic 2003; 4(5):302-12. (Pubitemid 36582632)
78. Clark RH, Stinchcombe JC, Day A et al. Adaptor protein 3-dependent microtubule-mediated movement of lytic granules to the immunological synapse. Nat Immunol 2003; 4(11):1111-20. (Pubitemid 37428039)
79. Pombo I, Martin-Verdeaux S, Iannascoli B et al. IgE receptor type I-dependent regulation ofa Rab3D-associated kinase. Apossible link in the calcium-dependent assembly ofSNARE complexes. J Biol Chem 2001; 12:12.
80. Turner KM, Burgoyne RD, Morgan A. Protein phosphorylation and the regulation of synaptic membrane traffic. Trends Neurosci 1999; 22(10):459-64. (Pubitemid 29447730)
81. Ozawa K, Yamada K, Kazanietz MG et al. Different isozymes of protein kinase C mediate feedback inhibition of phospholipase C and stimulatory signals for exocytosis in rat RBL-2H3 cells. J Biol Chem 1993; 268(4):2280-3. (Pubitemid 23057836)
82. Nechushtan H, Leitges M, Cohen C et al. Inhibition of degranulation and interleukin-6 production in mast cells derived from mice deficient in protein kinase Cbeta. Blood 2000; 95(5):1752-7. (Pubitemid 30120839)
83. Leitges M, Gimborn K, Elis W et al. Protein kinase C-delta is a negative regulator of antigen-induced mast cell degranulation. Mol Cell Biol 2002; 22(12):3970-80. (Pubitemid 34556568)
84. Ludowyke RI, Scurr LL, McNally CM. Calcium ionophore-induced secretion from mast cells correlates with myosin light chain phosphorylation by protein kinase C. J Immunol 1996; 157(11):5130-8. (Pubitemid 126449596)
85. Fujita Y, Sasaki T, Fukui K et al. Phosphorylation of Munc-18/n-Sec1/rbSec1 by protein Kinase C. The Journal of Biological Chemistry 1996; 271:7265-8.
86. Reed GL, Houng AK, Fitzgerald ML. Human platelets contain SNARE proteins and a Sec1p homologue that interacts with syntaxin 4 and is phosphorylated after thrombin activation: implications for platelet secretion. Blood 1999; 93(8):2617-26. (Pubitemid 29181194)
87. Chung SH, Polgar J, Reed GL. Protein kinase C phosphorylation of syntaxin 4 in thrombin-activated human platelets. J Biol Chem 2000; 275(33):25286-91.
88. Hepp R, Puri N, Hohenstein AC et al. Phosphorylation of SNAP-23 regulates exocytosis from mast cells. J Biol Chem 2005; 280(8):6610-20. (Pubitemid 40341212)
89. Suzuki K, Verma IM. Phosphorylation of SNAP-23 by IkappaB kinase 2 regulates mast cell degranulation. Cell 2008; 134(3):485-95.
90. Cabaniols JP, Ravichandran V, Roche PA. Phosphorylation ofSNAP-23 by the novel kinase SNAK regulates t-SNARE complex assembly. Mol Biol Cell 1999; 10(12):4033-41.
91. Marash M, Gerst JE. Phosphorylation of the autoinhibitory domain of the Sso t-SNAREs promotes binding of the Vsm1 SNARE regulator in yeast. Mol Biol Cell 2003; 14(8):3114-25. (Pubitemid 37013114)
92. Ludowyke RI, Holst J, Mudge LM et al. Transient translocation and activation of protein phosphatase 2A during mast cell secretion. J Biol Chem 2000; 275(9):6144-52. (Pubitemid 30129899)
93. Holst J, Sim AT, Ludowyke RI. Protein phosphatases 1 and 2A transiently associate with myosin during the peak rate of secretion from mast cells. Mol Biol Cell 2002; 13(3):1083-98. (Pubitemid 34250367)
94. Wang X, Huynh H, Gjorloff-Wingren A et al. Enlargement ofsecretory vesicles by protein tyrosine phosphatase PTP-MEG2 in rat basophilic leukemia mast cells and Jurkat T-cells. J Immunol 2002; 168(9):4612-9. (Pubitemid 34441367)
95. Huynh H, Bottini N, Williams S et al. Control of vesicle fusion by a tyrosine phosphatase. Nat Cell Biol 2004; 6(9):831-9. (Pubitemid 39207248)
96. Foreman JC, Mongar JL, Gomperts BD. Calcium ionophores and movement of calcium ions following the physiological stimulus to a secretory process. Nature 1973; 245(5423):249-51.
97. Chin D, Means AR. Calmodulin: a prototypical calcium sensor. Trends Cell Biol 2000; 10(8):322-8. (Pubitemid 30445239)
98. Peachell PT, Pearce FL. Effect of calmodulin inhibitors on histamine secretion from mast cells. Agents Actions 1985; 16(1-2):43-4. (Pubitemid 15108456)
99. Sullivan R, Burnham M, Torok K et al. Calmodulin regulates the disassembly of cortical F-actin in mast cells but is not required for secretion. Cell Calcium 2000; 28(1):33-46.
100. Choi OH, Adelstein RS, Beaven M.A. Secretion from rat basophilic RBL-2H3 cells is associated with diphosphorylation of myosin light chains by myosin light chain kinase as well as phosphorylation by protein kinase C. J Biol Chem 1994; 269(1):536-41. (Pubitemid 24026692)
101. Buxton DB, Adelstein RS. Calcium-dependent threonine phosphorylation of nonmuscle myosin in stimulated RBL-2H3 mast cells. J Biol Chem 2000; 275(44):34772-9.
102. Risinger C, Bennett MK. Differential phosphorylation of syntaxin and synaptosome-associated protein of 25 kDa (SNAP-25) isoforms. Journal of Neurochemistry 1999; 72(2):614-24. (Pubitemid 29055223)
103. Quetglas S, Iborra C, Sasakawa N et al. Calmodulin and lipid binding to synaptobrevin regulates calcium-dependent exocytosis. EMBO J 2002; 21(15):3970-9. (Pubitemid 34857430)
104. Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 2000; 1(1):31-9.
105. Mukherjee S, Maxfield FR. Role of membrane organization and membrane domains in endocytic lipid trafficking. Traffic 2000; 1(3):203-11.
106. Lafont F, Verkade P, Galli T et al. Raft association of SNAP receptors acting in apical trafficking in Madin-Darby canine kidney cells. Proc Natl Acad Sci USA 1999; 96(7):3734-8. (Pubitemid 29168979)
107. Lang T, Bruns D, Wenzel D et al. SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J 2001; 20(9):2202-13. (Pubitemid 32410590)
108. 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 USA 2001; 98(10):5619-24. (Pubitemid 32435691)
109. Pombo I, Rivera J, Blank U. Munc18-2/syntaxin3 complexes are spatially separated from syntaxin3-containing SNARE complexes. FEBS Lett 2003; 550(1-3):144-8. (Pubitemid 37281372)
110. Puri N, Roche PA. Ternary SNARE complexes are enriched in lipid rafts during mast cell exocytosis. Traffic 2006; 7(11):1482-94. (Pubitemid 44524521)