The mast cell: Where endocytosis and regulated exocytosis meet

Immunological Reviews

Volumn 217, Issue 1, 2007, Pages 292-303

  Sagi Eisenberg, Ronit ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Endocytosis; Exocytosis; Mast cells; NCS 1; Synaptotagmin

Indexed keywords

NEURONAL CALCIUM SENSOR; SYNAPTOTAGMIN; SYNAPTOTAGMIN II;

CELL FUNCTION; ENDOCYTOSIS; EXOCYTOSIS; HUMAN; MAST CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SECRETORY GRANULE;

ANIMALS; CALCIUM-BINDING PROTEINS; DOWN-REGULATION; ENDOCYTOSIS; EXOCYTOSIS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; MAST CELLS; NEURONAL CALCIUM-SENSOR PROTEINS; NEUROPEPTIDES; PROTEIN KINASE C-ALPHA; RATS; RECEPTORS, IGE; SECRETORY VESICLES; SYNAPTOTAGMINS;

EID: 34248194283     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2007.00516.x     Document Type: Review

References (138)

1. Hamawy MM, Mergenhagen SE, Siraganian RP. Protein tyrosine phosphorylation as a mechanism of signalling in mast cells and basophils. Cell Signal 1995 7 : 535 544.
2. Razin E, Pecht I, Rivera J. Signal transduction in the activation of mast cells and basophils. Immunol Today 1995 16 : 370 373.
3. Rivera VM, Brugge JS. Clustering of Syk is sufficient to induce tyrosine phosphorylation and release of allergic mediators from rat basophilic leukemia cells. Mol Cell Biol 1995 15 : 1582 1590.
4. Beaven MA, Baumgartner RA. Downstream signals initiated in mast cells by Fc epsilon RI and other receptors. Curr Opin Immunol 1996 8 : 766 772.
5. Santini F, Beaven MA. Tyrosine phosphorylation of a mitogen-activated protein kinase-like protein occurs at a late step in exocytosis. Studies with tyrosine phosphatase inhibitors and various secretagogues in rat RBL-2H3 cells. J Biol Chem 1993 268 : 22716 22722.
6. Zhang C, Baumgartner RA, Yamada K, Beaven MA. Mitogen-activated protein (MAP) kinase regulates production of tumor necrosis factor-alpha and release of arachidonic acid in mast cells. Indications of communication between p38 and p42 MAP kinases. J Biol Chem 1997 272 : 13397 13402.
7. Gordon JR, Galli SJ. Mast cells as a source of both preformed and immunologically inducible TNF-alpha/cachectin. Nature 1990 346 : 274 276.
8. Galli SJ, Gordon JR, Wershil BK. Cytokine production by mast cells and basophils. Curr Opin Immunol 1991 3 : 865 872.
9. Segal DM, Taurog J, Metzger H. Dimeric immunoglobulin E serves as a unit signal for mast cell degranulation. Proc Natl Acad Sci USA 1977 74 : 2993 2997.
10. Scharenberg AM, Kinet JP. Initial events in Fc epsilon RI signal transduction. J Allergy Clin Immunol 1994 94 : 1214 1216.
11. Kinet JP. The high-affinity IgE receptor (Fc epsilon RI): from physiology to pathology. Annu Rev Immunol 1999 17 : 931 972.
12. Lagunoff D, Martin TW, Read G. Agents that release histamine from mast cells. Annu Rev Pharmacol Toxicol 1983 23 : 331 351.
13. Beub JL, Mously M, Bronner C, Rouot B, Landry Y. Activation of Gi-like proteins, a receptor-independent effect of kinins in mast cells. Mol Pharmacol 1990 38 : 816 822.
14. Aridor M, Traub LM, Sagi-Eisenberg R. Exocytosis in mast cells by basic secretagogues: evidence for direct activation of GTP-binding proteins. J Cell Biol 1990 111 : 909 917.
15. Aridor M, Sagi-Eisenberg R. Neomycin is a potent secretagogue of mast cells that directly activates a GTP-binding protein that involved in exocytosis. J Cell Biol 1990 111 : 2885 2891.
16. Aridor M, Rajmilevich G, Beaven MA, Sagi-Eisenberg R. Activation of exocytosis by the heterotrimeric G protein Gi3. Science 1993 262 : 1569 1572.
17. Mousli M, Bronner C, Landry Y, Bockaert J, Rout B. Direct activation of GTP-binding regulatory proteins (G-proteins) by substance P and compound 48/80. FEBS Lett 1990 259 : 260 262.
18. Atkinson TP, Kaliner MA, Hohman RJ. Phospholipase C-g1 is translocated to the plasma membrane of rat basophilic leukemia cells in response to aggregation of the IgE receptors. J Immunol 1992 148 : 2194 2200.
19. Park DJ, Min HK, Rhee SG. IgE-induced tyrosine phosphorylation of phospholipase C-g1 in rat basophilic leukemia cells. J Biol Chem 1991 266 : 24237 24240.
20. Gruchalle RS, Dinh TJ, Kennerly DA. Phospholipase D (PLD) activity increases during mast cell activation. FASEB J 1989 3 : A788:3264.
21. Lin P, Wiggan GA, Gilfillan AM. Activation of phospholipase D in a rat mast (RBL-2H3) cell line. J Immunol 1991 146 : 1609 1616.
22. Choi W, et al. Activation of RBL-2H3 mast cells is dependent on tyrosine phosphorylation of phospholipase D2 by Fyn and Fgr. Mol Cell Biol 2004 24 : 6980 6992.
23. Hitomi T, et al. Phospholipase D1 regulates high-affinity IgE receptor-induced mast cell degranulation. Blood 2004 104 : 4122 4128.
24. McGivney A, Morita Y, Crews FT, Hirata F, Axelrod J, Siraganian RP. Phospholipase activation in the IgE-mediated and calcium ionophore A23187-induced release of histamine from rat basophilic leukemia cells. Arch Biochem Biophys 1981 212 : 572 580.
25. Yamada K, Okano Y, Miura K, Nozawa Y. A major role for phospholipase A2 in antigen-induced arachidonic acid release in rat mast cells. Biochem J 1987 247 : 95 99.
26. Yano H, et al. Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells. J Biol Chem 1993 268 : 25846 25856.
27. Marquardt DL, Alongi JL, Walker LL. The phosphatidylinositol 3-kinase inhibitor wortmannin blocks mast cell exocytosis but not IL-6 production. J Immunol 1996 156 : 1942 1945.
28. Beaven M, Moore JP, Smith GA, Hesketh TR, Metcalfe JC. The calcium signal and phosphatidylinositol breakdown in 2H3 cells. J Biol Chem 1984 259 : 7137 7142.
29. Beaven MA, Rogers J, Moore JP, Hesketh TB, Smith GA, Metcalfe JC. The mechanism of the calcium signal and correlation with histamine release in 2H3 cells. J Biol Chem 1984 259 : 7129 7136.
30. Barclay JW, Morgan A, Burgoyne RD. Calcium-dependent regulation of exocytosis. Cell Calcium 2005 38 : 343 353.
31. Foreman JC, Mongar JL. The role of the alkaline earth ions in anaphylactic histamine secretion. J Physiol 1972 244 : 753 769.
32. Penner R, Matthews G, Neher E. Regulation of calcium influx by second messengers in rat mast cells. Nature 1988 334 : 499 504.
33. Neher E. The influence of intracellular calcium concentration on degranulation of dialysed mast cells from rat peritoneum. J Physiol 1988 395 : 193 214.
34. Hide M, Beaven M. Calcium influx in rat mast cell (RBL-2H3) line. J Biol Chem 1991 266 : 15221 15229.
35. Brose N, Petrenko AG, Sudhof TC, Jahn R. Synaptotagmin: a calcium sensor on the synaptic vesicle surface. Science 1992 256 : 1021 1025.
36. Elfernik LA, Peterson MR, Scheller RH. A role for synaptotagmin (p65) in regulated exocytosis. Cell 1993 72 : 153 159.
37. Bauerfeind R, Jelinek R, Huttner WB. Synaptotagmin I- and II-deficient PC12 cells exhibit calcium-independent, depolarization-induced neurotransmitter release from synaptic-like microvesicles. FEBS Lett 1995 364 : 328 334.
38. Geppert M, Goda Y, Hammer RE, Li C, Rosahl TW, Stevens CF, Sudhof TC. Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell 1994 79 : 717 727.
39. McFerran BW, Graham ME, Burgoyne RD. Neuronal Ca2+ sensor 1, the mammalian homologue of frequenin, is expressed in chromaffin and PC12 cells and regulates neurosecretion from dense-core granules. J Biol Chem 1998 273 : 22768 22772.
40. Rohn WM, Rouille Y, Waguri S, Hoflack B. Bi-directional trafficking between the trans-Golgi network and the endosomal/lysosomal system. J Cell Sci 2000 113 : 2093 2101.
41. Lombardi D, Soldati T, Riederer MA, Goda Y, Zerial M, Pfeffer SR. Rab9 functions in transport between late endosomes and the trans Golgi network. EMBO J 1993 12 677 682.
42. Mallet WG, Maxfield FR. Chimeric forms of furin and TGN38 are transported with the plasma membrane in the trans-Golgi network via distinct endosomal pathways. J Cell Biol 1999 146 : 345 359.
43. Roquemore EP, Banting G. Efficient trafficking of TGN38 from the endosome to the trans-Golgi network requires a free hydroxyl group at position 331 in the cytosolic domain. Mol Biol Cell 1998 9 : 2125 2144.
44. Hopkins CR, Trowbridge IS. Internalization and processing of transferrin and the transferrin receptor in human carcinoma A431 cells. J Cell Biol 1983 97 : 508 521.
45. Galperin E, Benjamin S, Rapaport D, Rotem-Yehudar R, Tolchinsky S, Horowitz M. EHD3: a protein that resides in recycling tubular and vesicular membrane structures and interacts with EHD1. Traffic 2002 3 : 575 589.
46. Lin SX, Gundersen GG, Maxfield FR. Export from pericentriolar endocytic recycling compartment to cell surface depends on stable, detyrosinated (glu) microtubules and kinesin. Mol Biol Cell 2002 13 : 96 109.
47. Nichols BJ, et al. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J Cell Biol 2001 153 : 529 541.
48. Wilcke M, Johannes L, Galli T, Mayau V, Goud B, Salamero J. Rab 11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-Golgi network. J Cell Biol 2000 151 : 1207 1220.
49. Mallard F, et al. Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J Cell Biol 2002 156 : 653 664.
50. Grimberg E, Peng Z, Hammel I, Sagi-Eisenberg R. 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 : 145 154.
51. Schwartz LB, Austen KF. Enzymes of the mast cell granule. J Invest Dermatol 1980 74 : 349 353.
52. Suarez QC. The distribution of four lysosomal integral membrane proteins (LIMPs) in rat basophilic leukemia cells. Tissue Cell 1987 19 : 495 504.
53. Bonifacino JS, Yuan L, Sandoval IV. Internalization and recycling to serotonin-containing granules of the 80K integral membrane protein exposed on the surface of secreting rat basophilic leukaemia cells. J Cell Sci 1989 92 : 701 712.
54. Xu K, Williams RM, Holowka D, Baird B. Stimulated release of fluorescently labeled IgE fragments that efficiently accumulate in secretory granules after endocytosis in RBL-2H3 mast cells. J Cell Sci 1998 111 : 2385 2396.
55. Griffiths GM. Secretory lysosomes - a special mechanism of regulated secretion in haemopoietic cells. Trends Cell Biol 1996 6 : 329 332.
56. Dell'Angelica EC, Mullins C, Caplan S, Bonifacino JS. Lysosome-related organelles. FASEB J 2000 14 : 1265 1278.
57. Stinchcombe JC, Griffiths GM. Regulated secretion from hemopoietic cells. J Cell Biol 1999 147 : 1 6.
58. Stinchcombe JC, Page LJ, Griffiths GM. Secretory lysosome biogenesis in cytotoxic T lymphocytes from normal and Chediak Higashi syndrome patients. Traffic 2000 1 : 435 444.
59. Bossi G, Griffiths GM. CTL secretory lysosomes: biogenesis and secretion of a harmful organelle. Semin Immunol 2005 17 : 87 94.
60. Raposo G, Tenza D, Mecheri S, Peronet R, Bonnerot C, Desaymard C. Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation. Mol Biol Cell 1997 8 : 2631 2645.
61. Vincent-Schneider H, Thery C, Mazzeo D, Tenza D, Raposo G, Bonnerot C. Secretory granules of mast cells accumulate mature and immature MHC class II molecules. J Cell Sci 2001 114 : 323 334.
62. Baram D, et al. Synaptotagmin II negatively regulates Ca2+-triggered exocytosis of lysosomes in mast cells. J Exp Med 1999 189 : 1649 1658.
63. Shao X, Davletov BA, Sutton RB, Sudhof TC, Rizo J. Bipartite Ca2+-binding motif in C2 domains of synaptotagmin and protein kinase C. Science 1996 273 : 248 251.
64. Kee Y, Scheller RH. Localization of synaptotagmin-binding domains on syntaxin. J Neurosci 1996 16 : 1975 1981.
65. Sudhof TC, Rizo J Synaptotagmins: C2-domain proteins that regulate membrane traffic. Neuron 1996 17 : 379 388.
66. Sutton RB, Davletov BA, Berghuis AM, Sudhof TC, Sprang SR. Structure of the first C2 domain of synaptotagmin I: a novel Ca2+/phospholipid-binding fold. Cell 1995 80 : 929 938.
67. Yoshihara M, Montana ES. The synaptotagmins: calcium sensors for vesicular trafficking. Neuroscientist 2004 10 : 566 574.
68. Mizuta M, et al. Localization and functional role of synaptotagmin III in insulin secretory vesicles in pancreatic beta-cells. Diabetes 1997 46 : 2002 2006.
69. Sugita S, et al. Synaptotagmin VII as a plasma membrane Ca(2+) sensor in exocytosis. Neuron 2001 30 : 459 473.
70. Fukuda M, Kowalchyk JA, Zhang X, Martin TF, Mikoshiba K. Synaptotagmin IX regulates Ca2+-dependent secretion in PC12 cells. J Biol Chem 2002 277 : 4601 4604.
71. Saegusa C, Fukuda M, Mikoshiba K. Synaptotagmin V is targeted to dense-core vesicles that undergo calcium-dependent exocytosis in PC12 cells. J Biol Chem 2002 277 : 24499 24505.
72. Chapman ER, Hanson PI, An S, Jahn R. Ca2+ regulates the interaction between synaptotagmin and syntaxin 1. J Biol Chem 1995 270 : 23667 23671.
73. Fernandez-Chacon R, et al. Synaptotagmin I functions as a calcium regulator of release probability. Nature 2001 410 : 41 49.
74. Fukuda M, Aruga J, Niinobe M, Aimoto S, Mikoshiba K. Inositol-1,3,4,5- tetrakisphosphate binding to C2B domain of IP4BP/synaptotagmin II. J Biol Chem 1994 269 : 29206 29211.
75. Zhang JZ, Davletov BA, Sudhof TC, Anderson RG. Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling. Cell 1994 78 : 751 760.
76. Haucke V, De Camilli P. AP-2 recruitment to synaptotagmin stimulated by tyrosine-based endocytic motifs. Science 1999 285 : 1268 1271.
77. Haucke V, Wenk MR, Chapman ER, Farsad K, De Camilli P. Dual interaction of synaptotagmin with mu2- and alpha-adaptin facilitates clathrin-coated pit nucleation. EMBO J 2000 19 : 6011 6019.
78. Martina JA, Bonangelino CJ, Aguilar RC, Bonifacino JS. Stonin 2: an adaptor-like protein that interacts with components of the endocytic machinery. J Cell Biol 2001 153 : 1111 1120.
79. Walther K, Diril MK, Jung N, Haucke V. Functional dissection of the interactions of stonin 2 with the adaptor complex AP-2 and synaptotagmin. Proc Natl Acad Sci USA 2004 101 : 964 969.
80. Nonet ML, Grundahl K, Meyer BJ, Rand JB. Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 1993 73 : 1291 1305.
81. Lang J, Fukuda M, Zhang H, Mikoshiba K, Wollheim CB. The first C2 domain of synaptotagmin is required for exocytosis of insulin from pancreatic beta-cells: action of synaptotagmin at low micromolar calcium. EMBO J 1997 16 : 5837 5846.
82. Gao Z, Reavey-Cantwell J, Young RA, Jegier P, Wolf BA. Synaptotagmin III/VII isoforms mediate Ca2+-induced insulin secretion in pancreatic islet beta cells. J Biol Chem 2000 275 : 36079 36085.
83. Gut A, Kiraly CE, Fukuda M, Mikoshiba K, Wollheim CB, Lang J. Expression and localisation of synaptotagmin isoforms in endocrine (&bgr)-cells: their function in insulin exocytosis. J Cell Sci 2001 114 : 1709 1716.
84. Martinez I, Chakrabarti S, Hellevik T, Morehead J, Fowler K, Andrews NW. Synaptotagmin VII regulates Ca2+-dependent exocytosis of lysosomes in fibroblasts. J Cell Biol 2000 148 : 1141 1150.
85. Gerasimenko JV, Gerasimenko OV, Petersen OH. Membrane repair: Ca(2+)-elicited lysosomal exocytosis. Curr Biol 2001 11 : R971 R974.
86. Baram D, Linial M, Mekori YA, Sagi-Eisenberg R. Ca2+-dependent exocytosis in mast cells is stimulated by the Ca2+ sensor, synaptotagmin I. J Immunol 1998 161 : 5120 5123.
87. Haberman Y, Grimberg E, Fukuda M, Sagi-Eisenberg R. Synaptotagmin IX, a possible linker between the perinuclear endocytic recycling compartment and the microtubules. J Cell Sci 2003 116 : 4307 4318.
88. Haberman Y, Ziv I, Gorzalczany Y, Fukuda M, Sagi-Eisenberg R. Classical protein kinase C(s) regulates targeting of synaptotagmin IX to the endocytic recycling compartment. J Cell Sci 2005 118 : 1641 1649.
89. Geppert M, Archer BT 3rd., Sudhof TC. Synaptotagmin II. A novel differentially distributed form of synaptotagmin. J Biol Chem 1991 266 : 13548 13552.
90. Sannes PL, Spicer SS. The heterophagic granules of mast cells: dipeptidyl aminopeptidase II activity and resistance to exocytosis. Am J Pathol 1979 94 : 447 457.
91. Jamur MC, Vugman I, Hand AR. Ultrastructural and cytochemical studies of acid phosphatase and trimetaphosphatase in rat peritoneal mast cells developing in vivo. Cell Tissue Res 1986 244 : 557 563.
92. Jamur MC, Vugman I. Acid phosphatase activity during maturation of rat mesentery mast cells. Cell Mol Biol 1987 33 : 69 72.
93. Jamur MC, Vugman I. Rat peritoneal mast cell regranulation and acid phosphatase and trimetaphosphatase activity induced after stimulation by 48/80. A fluorescence, ultrastructural, and cytochemical study. Cell Mol Biol 1988 34 : 231 237.
94. Lindmark IM, et al. Synaptotagmin II could confer Ca2+ sensitivity to phagocytosis in human neutrophils. Biochim Biophy Acta (BBA) - Mol Cell Res 2002 1590 : 159 166.
95. Atiya-Nasagi Y, Cohen H, Medalia O, Fukudan M, Sagi-Eisenberg R. O-glycosylation is essential for intracellular targeting of synaptotagmins I and II in non-neuronal specialized secretory cells. J Cell Sci 2005 118 : 1363 1372.
96. Henz BM, Maurer M, Lippert U, Worm M, Babina M. Mast cells as initiators of immunity and host defense. Exp Dermatol 2001 10 : 1 10.
97. Abraham SN, Malaviya R. Mast cells in infection and immunity. Infect Immun 1997 65 : 3501 3508.
98. Warbrick EV, Taylor AM, Botchkarev VA, Coleman JW. Rat connective tissue-type mast cells express MHC class II: up-regulation by IFN-gamma. Cell Immunol 1995 163 : 222 228.
99. Fox CC, Jewell SD, Whitacre CC. Rat peritoneal mast cells present antigen to a PPD-specific T cell line. Cell Immunol 1994 158 : 253 264.
100. Baram D, Peng Z, Medalia O, Mekori Y, Sagi-Eisenberg R. Synaptotagmin II negatively regulates MHC class II presentation by mast cells. Mol Immunol 2002 38 : 1347 1352.
101. Peng Z, Grimberg E, Sagi-Eisenberg R. Suppression of synaptotagmin II restrains phorbol ester-induced down-regulation of protein kinase Cα by diverting the kinase from a degradative pathway to the recycling endocytic compartment. J Cell Sci 2002 115 : 3083 3092.
102. Berntson A, Morgans C. Distribution of the presynaptic calcium sensors, synaptotagmin I/II and synaptotagmin III, in the goldfish and rodent retinas. J Vis 2003 3 : 274 280.
103. Ren M, Xu G, Zeng J, De LCC, Adesnik M, Sabatini DD. Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc Natl Acad Sci USA 1998 95 : 6187 6192.
104. Sheff DR, Daro EA, Hull M, Mellman I. The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J Cell Biol 1999 145 : 123 139.
105. Barbosa MD, et al. Identification of the homologous beige and Chediak-Higashi syndrome genes. Nature 1996 382 : 262 265.
106. Iezzi M, Kouri G, Fukuda M, Wollheim CB. Synaptotagmin V and IX isoforms control Ca2+-dependent insulin exocytosis. J Cell Sci 2004 117 : 3119 3127.
107. Fukuda M. RNA interference-mediated silencing of synaptotagmin IX, but not synaptotagmin I, inhibits dense-core vesicle exocytosis in PC12 cells. Biochem J 2004 380 : 875 879.
108. Iezzi M, Eliasson L, Fukuda H, Wollheim CB. Adenovirus-mediated silencing of synaptotagmin 9 inhibits Ca2+-dependent insulin secretion in islets. FEBS Lett 2005 579 : 5241 5246.
109. Ghosh RN, Mallet WG, Soe TT, McGraw TE, Maxfield FR. An endocytosed TGN38 chimeric protein is delivered to the TGN after trafficking through the endocytic recycling compartment in CHO cells. J Cell Biol 1998 142 : 923 936.
110. Mallard F, Antony C, Tenza D, Salamero J, Goud B, Johannes L. Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of shiga toxin B-fragment transport. J Cell Biol 1998 143 : 973 990.
111. Saint-Pol A, et al. Clathrin adaptor epsinR is required for retrograde sorting on early endosomal membranes. Dev Cell 2004 6 : 525 538.
112. Haberman Y, et al. Synaptotagmin (Syt) IX is an essential determinant for protein sorting to secretory granules in mast cells. Blood 2007 109 : 3385 3392.
113. Braunewell KH, Gundelfinger ED. Intracellular neuronal calcium sensor proteins: a family of EF-hand calcium-binding proteins in search of a function. Cell Tissue Res 1999 295 : 1 12.
114. Hilfiker S. Neuronal calcium sensor-1: a multifunctional regulator of secretion. Biochem Soc Trans 2003 31 : 828 832.
115. Rettig J, Neher E. Emerging roles of presynaptic proteins in Ca2+-triggered exocytosis. Science 2002 298 : 781 785.
116. Burgoyne RD. The neuronal calcium-sensor proteins. Biochim Biophys Acta 2004 1742 : 59 68.
117. Jeromin A, et al. N-terminal myristoylation regulates calcium-induced conformational changes in neuronal calcium sensor-1. J Biol Chem 2004 279 : 27158 27167.
118. Pongs O, et al. Frequenin - a novel calcium-binding protein that modulates synaptic efficacy in the Drosophila nervous system. Neuron 1993 11 : 15 28.
119. Rivosecchi R, Pongs O, Theil T, Mallart A. Implication of frequenin in the facilitation of transmitter release in Drosophila. J Physiol 1994 474 : 223 232.
120. Guo W, Malin SA, Johns DC, Jeromin A, Nerbonne JM. Modulation of Kv4-encoded K+ currents in the mammalian myocardium by neuronal calcium sensor-1. J Biol Chem 2002 277 : 26436 26643.
121. Gomez M, et al. Ca2+ signaling via the neuronal calcium sensor-1 regulates associative learning and memory in C. elegans. Neuron 2001 30 : 241 248.
122. Chen XL, et al. Overexpression of rat neuronal calcium sensor-1 in rodent NG108-15 cells enhances synapse formation and transmission. J Physiol 2001 532 : 649 659.
123. Taverna E, Francolini M, Jeromin A, Hilfiker S, Roder J, Rosa P. Neuronal calcium sensor 1 and phosphatidylinositol 4-OH kinase {beta} interact in neuronal cells and are translocated to membranes during nucleotide-evoked exocytosis. J Cell Sci 2002 115 : 3909 3922.
124. Scalettar BA, et al. Neuronal calcium sensor-1 binds to regulated secretory organelles and functions in basal and stimulated exocytosis in PC12 cells. J Cell Sci 2002 115 : 2399 2412.
125. Pan CY, Jeromin A, Lundstrom K, Yoo SH, Roder J, Fox AP. Alterations in exocytosis induced by neuronal Ca2+ sensor-1 in bovine chromaffin cells. J Neurosci 2002 22 : 2427 2433.
126. Hendricks KB, Wang BQ, Schnieders EA, Thorner J. Yeast homologue of neuronal frequenin is a regulator of phosphatidylinositol-4-OH kinase. Nat Cell Biol 1999 1 : 234 241.
127. Zhao X, et al. Interaction of neuronal calcium sensor-1 (NCS-1) with phosphatidylinositol 4-kinase beta stimulates lipid kinase activity and affects membrane trafficking in COS-7 cells. J Biol Chem 2001 276 : 40183 40189.
128. Kapp-Barnea Y, Melnikov S, Shefler I, Jeromin A, Sagi-Eisenberg R. Neuronal calcium sensor-1 and phosphatidylinositol 4-kinase {beta} regulate IgE receptor-triggered exocytosis in cultured mast cells. J Immunol 2003 171 : 5320 5327.
129. Cockcroft S, De Matteis MA. Inositol lipids as spatial regulators of membrane traffic. J Membr Biol 2001 180 : 187 194.
130. De Matteis MA, Godi A. PI-loting membrane traffic. Nat Cell Biol 2004 6 : 487 492.
131. Gruenberg J. Lipids in endocytic membrane transport and sorting. Curr Opin Cell Biol 2003 15 : 382 388.
132. Itoh T, Takenawa T. Phosphoinositide-binding domains: functional units for temporal and spatial regulation of intracellular signalling. Cell Signal 2002 14 : 733 743.
133. Haucke V. Phosphoinositide regulation of clathrin-mediated endocytosis. Biochem Soc Trans 2005 33 : 1285 1289.
134. Wang YJ, et al. Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 2003 114 : 299 310.
135. Hirst J, Motley A, Harasaki K, Peak Chew SY, Robinson MS. EpsinR: an ENTH domain-containing protein that interacts with AP-1. Mol Biol Cell 2003 14 : 625 641.
136. Kapp-Barnea Y, Ninio-Many L, Hirschberg K, Fukuda M, Jeromin A, Sagi-Eisenberg R. Neuronal calcium sensor-1 and phosphatidylinositol 4-kinase beta stimulate extracellular signal-regulated kinase 1/2 signaling by accelerating recycling through the endocytic recycling compartment. Mol Biol Cell 2006 17 : 4130 4141.
137. Di Fiore PP, De Camilli P. Endocytosis and signaling. An inseparable partnership. Cell 2001 106 : 1 4.
138. Kholodenko BN. MAP kinase cascade signaling and endocytic trafficking: a marriage of convenience? Trends Cell Biol 2002 12 : 173 177.