Protein trafficking in immune cells

Immunobiology

Volumn 214, Issue 7, 2009, Pages 507-525

  Benado, Anat ^a   Nasagi Atiya, Yafit ^a   Sagi Eisenberg, Ronit ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Endocytosis; Exocytosis; GTPase; Immune cells; Mast cells; Sorting; Synaptotagmin

Indexed keywords

ADAPTOR PROTEIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; BETA SECRETASE; CASEIN KINASE II; CD1 ANTIGEN; CD63 ANTIGEN; COAT PROTEIN; COAT PROTEIN COMPLEX I; COAT PROTEIN COMPLEX II; FAS LIGAND; INTERLEUKIN 6; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PADGEM PROTEIN; RAB11 PROTEIN; RAB27A PROTEIN; RAB7 PROTEIN; RAC1 PROTEIN; SNARE PROTEIN; SYNAPTOBREVIN 2; SYNAPTOSOMAL ASSOCIATED PROTEIN 23; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN; SYNAPTOTAGMIN I; SYNAPTOTAGMIN II; TUMOR NECROSIS FACTOR ALPHA; TYROSINASE RELATED PROTEIN 1;

ARTICLE; CELL MEMBRANE; CELL TRANSPORT; CHEDIAK HIGASHI SYNDROME; ENDOCYTOSIS; ENDOSOME; EXOCYTOSIS; GENE MUTATION; GRISCELLI SYNDROME; HUMAN; IMMUNOCOMPETENT CELL; LYSOSOME; MAST CELL; MICROTUBULE; NONHUMAN; OCULAR ALBINISM; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; SECRETORY GRANULE; T LYMPHOCYTE; TRANSPORT VESICLE; UBIQUITINATION;

EID: 68749122260     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2008.11.011     Document Type: Article

References (175)

1. Alfalah M., Jacob R., Preuss U., Zimmer K.P., Naim H., and Naim H.Y. O-linked glycans mediate apical sorting of human intestinal sucrase-isomaltase through association with lipid rafts. Curr. Biol. 9 (1999) 593-596
2. Amoui M., Draberova L., Tolar P., and Draber P. Direct interaction of Syk and Lyn protein tyrosine kinases in rat basophilic leukemia cells activated via type I Fc epsilon receptors. Eur. J. Immunol. 27 (1997) 321-328
3. Anitei M., Baust T., Czupalla C., Parshyna I., Bourel L., Thiele C., Krause E., and Hoflack B. Protein networks supporting AP-3 function in targeting lysosomal membrane proteins. Mol. Biol. Cell 19 (2008) 1942-1951
4. Aridor M., Fish K.N., Bannykh S., Weissman J., Roberts T.H., Lippincott-Schwartz J., and Balch W.E. The Sar1 GTPase coordinates biosynthetic cargo selection with endoplasmic reticulum export site assembly. J. Cell Biol. 152 (2001) 213-230
5. Arvan P., and Castle D. Sorting and storage during secretory granule biogenesis: looking backward and looking forward. Biochem. J. 332 (1998) 593-610
6. Atiya-Nasagi Y., Cohen H., Medalia O., Fukudan M., and Sagi-Eisenberg R. O-glycosylation is essential for intracellular targeting of synaptotagmins I and II in non-neuronal specialized secretory cells. J. Cell Sci. 118 (2005) 1363-1372
7. Baram D., Linial M., Mekori Y.A., and Sagi-Eisenberg R. Ca2+-dependent exocytosis in mast cells is stimulated by the Ca2+ sensor, synaptotagmin I. J. Immunol. 161 (1998) 5120-5123
8. Baram D., Adachi R., Medalia O., Tuvim M., Dickey B.F., Mekori Y.A., and Sagi-Eisenberg R. Synaptotagmin II negatively regulates Ca2+-triggered exocytosis of lysosomes in mast cells. J. Exp. Med. 189 (1999) 1649-1658
9. Baram D., Peng Z., Medalia O., Mekori Y., and Sagi-Eisenberg R. Synaptotagmin II negatively regulates MHC class II presentation by mast cells. Mol. Immunol. 38 (2002) 1347-1352
10. Barois N., and Bakke O. The adaptor protein AP-4 as a component of the clathrin coat machinery: a morphological study. Biochem. J. 385 (2005) 503-510
11. Baust T., Czupalla C., Krause E., Bourel-Bonnet L., and Hoflack B. Proteomic analysis of adaptor protein 1A coats selectively assembled on liposomes. Proc. Natl. Acad. Sci. USA 103 (2006) 3159-3164
12. Blagoveshchenskaya A.D., Norcott J.P., and Cutler D.F. Lysosomal targeting of P-selectin is mediated by a novel sequence within its cytoplasmic tail. J. Biol. Chem. 273 (1998) 2729-2737
13. Blagoveshchenskaya A.D., Hewitt E.W., and Cutler D.F. Di-leucine signals mediate targeting of tyrosinase and synaptotagmin to synaptic-like microvesicles within PC12 cells. Mol. Biol. Cell 10 (1999) 3979-3990
14. Blott E.J., Bossi G., Clark R., Zvelebil M., and Griffiths G.M. Fas ligand is targeted to secretory lysosomes via a proline-rich domain in its cytoplasmic tail. J. Cell Sci. 114 (2001) 2405-2416
15. Boehm M., Aguilar R.C., and Bonifacino J.S. Functional and physical interactions of the adaptor protein complex AP-4 with ADP-ribosylation factors (ARFs). EMBO J. 20 (2001) 6265-6276
16. Boman A.L. GGA proteins: new players in the sorting game. J. Cell Sci. 114 (2001) 3413-3418
17. Bonifacino J.S. The GGA proteins: adaptors on the move. Nat. Rev. Mol. Cell. Biol. 5 (2004) 23-32
18. Bonifacino J.S., and Dell'Angelica E.C. Molecular bases for the recognition of tyrosine-based sorting signals. J. Cell Biol. 145 (1999) 923-926
19. Bonifacino J.S., and Traub L.M. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72 (2003) 395-447
20. Bossi G., and Griffiths G.M. Degranulation plays an essential part in regulating cell surface expression of Fas ligand in T cells and natural killer cells. Nat. Med. 5 (1999) 90-96
21. Bossi G., Booth S., Clark R., Davis E.G., Liesner R., Richards K., Starcevic M., Stinchcombe J., Trambas C., Dell'Angelica E.C., and Griffiths G.M. Normal lytic granule secretion by cytotoxic T lymphocytes deficient in BLOC-1, -2 and -3 and Myosins Va, VIIa and XV. Traffic 6 (2005) 243-251
22. Chapman E.R., Hanson P.I., An S., and Jahn R. Ca2+ regulates the interaction between synaptotagmin and syntaxin 1. J. Biol. Chem. 270 (1995) 23667-23671
23. Charette S.J., and Cosson P. A LYST/beige homolog is involved in biogenesis of Dictyostelium secretory lysosomes. J. Cell Sci. 120 (2007) 2338-2343
24. Charette S.J., and Cosson P. Altered composition and secretion of lysosome-derived compartments in Dictyostelium AP-3 mutant cells. Traffic 9 (2008) 588-596
25. Chen W.J., Goldstein J.L., and Brown M.S. NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J. Biol. Chem. 265 (1990) 3116-3123
26. Clark R.H., Stinchcombe J.C., Day A., Blott E., Booth S., Bossi G., Hamblin T., Davies E.G., and Griffiths G.M. Adaptor protein 3-dependent microtubule-mediated movement of lytic granules to the immunological synapse. Nat. Immunol. 4 (2003) 1111-1120
27. Daugherty B.L., Straley K.S., Sanders J.M., Phillips J.W., Disdier M., McEver R.P., and Green S.A. AP-3 adaptor functions in targeting P-Selectin to secretory granules in endothelial cells. Traffic 2 (2001) 406-413
28. Dell'Angelica E.C., Mullins C., Caplan S., and Bonifacino J.S. Lysosome-related organelles. FASEB J. 4 (2000) 1265-1278
29. Dell'Angelica E.C., Shotelersuk V., Aguilar R.C., Gahl W.A., and Bonifacino J.S. Altered trafficking of lysosomal proteins in Hermansky-Pudlak syndrome due to mutations in the beta 3A subunit of the AP-3 adaptor. Mol. Cell. 3 (1999) 11-21
30. Detter J.C., Zhang Q., Mules E.H., Novak E.K., Mishra V.S., Li W., McMurtrie E.B., Tchernev V.T., Wallace M.R., Seabra M.C., Swank R.T., and Kingsmore S.F. Rab geranylgeranyl transferase alpha mutation in the gunmetal mouse reduces Rab prenylation and platelet synthesis. Proc. Natl. Acad. Sci. USA 97 (2000) 4144-4149
31. Di Pietro S.M., Falcon-Perez J.M., Tenza D., Setty S.R.G., Marks M.S., Raposo G., and Dell'Angelica E.C. BLOC-1 interacts with BLOC-2 and the AP-3 complex to facilitate protein trafficking on endosomes. Mol. Biol. Cell 17 (2006) 4027-4038
32. Dittie A.S., Thomas L., Thomas G., and Tooze S.A. Interaction of furin in immature secretory granules from neuroendocrine cells with the AP-1 adaptor complex is modulated by casein kinase II phosphorylation. EMBO J. 16 (1997) 4859-4870
33. Donaldson J.G., Cassel D., Kahn R.A., and Klausner R.D. ADP-ribosylation factor, a small GTP-binding protein, is required for binding of the coatomer protein {beta}-COP to Golgi membranes. Proc. Natl. Acad. Sci. USA 89 (1992) 6408-6412
34. Ehrlich M., Boll W., van Oijen A., Hariharan R., Chandran K., Nibert M.L., and Kirchhausen T. Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118 (2004) 591-605
35. Fasshauer D. Structural insights into the SNARE mechanism. Biochim. Biophys. Acta 1641 (2003) 87-97
36. Faundez V., Horng J.T., and Kelly R.B. ADP ribosylation factor 1 is required for synaptic vesicle budding in PC12 cells. J. Cell Biol. 138 (1997) 505-515
37. Faundez V., Horng J.T., and Kelly R.B. A function for the AP3 coat complex in synaptic vesicle formation from endosomes. Cell 93 (1998) 423-432
38. Faundez V.V., and Kelly R.B. The AP-3 complex required for endosomal synaptic vesicle biogenesis is associated with casein kinase Ia-like isoform. Mol. Biol. Cell 10 (2000) 2591-2604
39. Faurschou M., and Borregaard N. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect. 5 (2003) 1317-1327
40. Feany M.B., Yee A.G., Delvy M.L., and Buckley K.M. The synaptic vesicle proteins SV2, synaptotagmin and synaptophysin are sorted to separate cellular compartments in CHO fibroblasts. J. Cell Biol. 123 (1993) 575-584
41. Feldmann J., Callebaut I., Raposo G., Certain S., Bacq D., Dumont C., Lambert N., Ouachee-Chardin M., Chedeville G., Tamary H., Minard-Colin V., Vilmer E., Blanche S., Le Deist F., Fischer A., and de Saint Basile G. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell 115 (2003) 461-473
42. Feng L., Seymour A.B., Jiang S., To A., Peden A.A., Novak E.K., Zhen L., Rusiniak M.E., Eicher E.M., Robinson M.S., Gorin M.B., and Swank R.T. The beta3A subunit gene (Ap3b1) of the AP-3 adaptor complex is altered in the mouse hypopigmentation mutant pearl, a model for Hermansky-Pudlak syndrome and night blindness. Hum. Mol. Genet. 8 (1999) 323-330
43. Feng L., Rigatti B.W., Novak E.K., Gorin M.B., and Swank R.T. Genomic structure of the mouse Ap3b1 gene in normal and pearl mice. Genomics 69 (2000) 370-379
44. Fernandez-Chacon R., Konigstorfer A., Gerber S.H., Garcia J., Matos M.F., Stevens C.F., Brose N., Rizo J., Rosenmund C., and Sudhof T.C. Synaptotagmin I functions as a calcium regulator of release probability. Nature 410 (2001) 41-49
45. Fingerhut A., von Figura K., and Honing S. Binding of AP2 to sorting signals is modulated by AP2 phosphorylation. J. Biol. Chem. 276 (2001) 5476-5482
46. Fowler K.T., Andrews N.W., and Huleatt J.W. Expression and function of synaptotagmin VII in CTLs. J. Immunol. 178 (2007) 1498-1504
47. Fukuda M. RNA interference-mediated silencing of synaptotagmin IX, but not synaptotagmin I, inhibits dense-core vesicle exocytosis in PC12 cells. Biochem. J. 380 (2004) 875-879
48. Fukuda M. Versatile role of Rab27 in membrane trafficking: focus on the Rab27 effector families. J. Biochem. (Tokyo) 137 (2005) 9-16
49. Fukuda M., Aruga J., Niinobe M., Aimoto S., and Mikoshiba K. Inositol-1,3,4,5-tetrakisphosphate binding to C2B domain of IP4BP/synaptotagmin II. J. Biol. Chem. 269 (1994) 29206-29211
50. Fukuda M., Kowalchyk J.A., Zhang X., Martin T.F., and Mikoshiba K. Synaptotagmin IX regulates Ca2+-dependent secretion in PC12 cells. J. Biol. Chem. 277 (2002) 4601-4604
51. Geiger B., Rosen D., and Berke G. Spatial relationships of microtubule-organizing centers and the contact area of cytotoxic T lymphocytes and target cells. J. Cell. Biol. 95 (1982) 137-143
52. Geppert M., Archer B.D., and Sudhof T.C. Synaptotagmin II. A novel differentially distributed form of synaptotagmin. J. Biol. Chem. 266 (1991) 13548-13552
53. Geppert M., Goda Y., Hammer R.E., Li C., Rosahl T.W., Stevens C.F., and Sudhof T.C. Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell 79 (1994) 717-727
54. Ghosh P., and Kornfeld S. Phosphorylation-induced conformational changes regulate GGAs 1 and 3 function at the trans-Golgi network. J. Biol. Chem. 278 (2003) 14543-14549
55. Goishi K., Mizuno K., Nakanishi H., and Sasaki T. Involvement of Rab27 in antigen-induced histamine release from rat basophilic leukemia 2H3 cells. Biochim. Biophys. Res. Commun. 324 (2004) 294-301
56. Gomi H., Mizutani S., Kasai K., Itohara S., and Izumi T. Granuphilin molecularly docks insulin granules to the fusion machinery. J. Cell Biol. 171 (2005) 99-109
57. Gomi H., Mori K., Itohara S., and Izumi T. Rab27b is expressed in a wide range of exocytic cells and involved in the delivery of secretory granules near the plasma membrane. Mol. Biol. Cell 18 (2007) 4377-4386
58. Griffiths G.M. Secretory lysosomes - a special mechanism of regulated secretion in haemopoietic cells. Trends Cell Biol. 6 (1996) 329-332
59. Grimberg E., Peng Z., Hammel I., and 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. 116 (2003) 145-154
60. Griscelli C., Durandy A., Guy-Grand D., Daguillard F., Herzog C., and Prunieras M. A syndrome associating partial albinism and immunodeficiency. Am. J. Med. 65 (1978) 691-702
61. Grote E., Hao J.C., Bennett M.K., and Kelly R.B. A targeting signal in VAMP regulating transport to synaptic vesicles. Cell 81 (1995) 581-589
62. Haberman Y., Grimberg E., Fukuda M., and Sagi-Eisenberg R. Synaptotagmin IX, a possible linker between the perinuclear endocytic recycling compartment and the microtubules. J. Cell Sci. 116 (2003) 4307-4318
63. Haberman Y., Ziv I., Gorzalczany Y., Fukuda M., and Sagi-Eisenberg R. Classical protein kinase C(s) regulates targeting of synaptotagmin IX to the endocytic recycling compartment. J. Cell Sci. 118 (2005) 1641-1649
64. Haberman Y., Ziv I., Gorzalczany Y., Hirschberg K., Mittleman L., Fukuda M., and Sagi-Eisenberg R. Synaptotagmin (Syt) IX is an essential determinant for protein sorting to secretory granules in mast cells. Blood 109 (2007) 3385-3392
65. Han W., Rhee J.S., Maximov A., Lao Y., Mashimo T., Rosenmund C., and Sudhof T.C. N-glycosylation is essential for vesicular targeting of synaptotagmin 1. Neuron 41 (2004) 85-99
66. Hart G.W. Dynamic O-linked glycosylation of nuclear and cytoskeletal proteins. Annu. Rev. Biochem. 66 (1997) 315-335
67. Hartwell D.W., Mayadas T.N., Berger G., Frenette P.S., Rayburn H., Hynes R.O., and Wagner D.D. Role of P-Selectin cytoplasmic domain in granular targeting in vivo and in early inflammatory responses. J. Cell Biol. 143 (1998) 1129-1141
68. Hepp R., Puri N., Hohenstein A.C., Crawford G.L., Whiteheart S.W., and Roche P.A. Phosphorylation of SNAP-23 regulates exocytosis from mast cells. J. Biol. Chem. 280 (2005) 6610-6620
69. Hicke L., and Riezman H. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84 (1996) 277-287
70. Holt O., Kanno E., Bossi G., Booth S., Daniele T., Santoro A., Arico M., Saegusa C., Fukuda M., and Griffiths G.M. Slp1 and Slp2-a localize to the plasma membrane of CTL and contribute to secretion from the immunological synapse. Traffic 9 (2008) 446-457
71. Honing S., Sandoval I., and von Figura K. A di-leucine-based motif in the cytoplasmic tail of LIMP-II and tyrosinase mediates selective binding of AP-3. EMBO J. 17 (1998) 1304-1314
72. Hurley J.H., Lee S., and Prag G. Ubiquitin-binding domains. Biochem. J. 399 (2006) 361-372
73. Iezzi M., Kouri G., Fukuda M., and Wollheim C.B. Synaptotagmin V and IX isoforms control Ca2+-dependent insulin exocytosis. J. Cell Sci. 117 (2004) 3119-3127
74. Johnston P.A., Cameron P.L., Stukenbrok H., Jahn R., De C.P., and Sudhof T.C. Synaptophysin is targeted to similar microvesicles in CHO and PC12 cells. EMBO J. 8 (1989) 2863-2872
75. Jordens I., Fernandez-Borja M., Marsman M., Dusseljee S., Janssen L., Calafat J., Janssen H., Wubbolts R., and Neefjes J. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr. Biol. 11 (2001) 1680-1685
76. Kantheti P., Qiao X., Diaz M.E., Peden A.A., Meyer G.E., Carskadon S.L., Kapfhamer D., Sufalko D., Robinson M.S., Noebels J.L., and Burmeister M. Mutation in AP-3 delta in the mocha mouse links endosomal transport to storage deficiency in platelets, melanosomes, and synaptic vesicles. Neuron 21 (1998) 111-212
77. Katzmann D.J., Babst M., and Emr S.D. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106 (2001) 145-155
78. Kaur J., and Cutler D.F. P-selectin targeting to secretory lysosomes of Rbl-2H3 cells. J. Biol. Chem. 277 (2002) 10498-10505
79. Kim H.L., and Kim J.A. Purification of clathrin assembly protein from rat liver. Exp. Mol. Med. 32 (2000) 222-226
80. Kinet J.P. The high-affinity IgE receptor (Fc epsilon RI): from physiology to pathology. Annu. Rev. Immunol. 17 (1999) 931-972
81. Kirchhausen T. Adaptors for clathrin-mediated traffic. Annu. Rev. Cell Dev. Biol. 15 (1999) 705-732
82. Kirchhausen T. Clathrin adaptors really adapt. Cell 109 (2002) 413-416
83. Klausner R.D., Donaldson J.G., and Lippincott-Schwartz J. Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116 (1992) 1071-1080
84. Kuroda T.S., and Fukuda M. Rab27A-binding protein Slp2-a is required for peripheral melanosome distribution and elongated cell shape in melanocytes. Nat. Cell Biol. 6 (2004) 1195-1203
85. Kzhyshkowska J., Gratchev A., Martens J.H., Pervushina O., Mamidi S., Johansson S., Schledzewski K., Hansen B., He X., Tang J., Nakayama K., and Goerdt S. Stabilin-1 localizes to endosomes and the trans-Golgi network in human macrophages and interacts with GGA adaptors. J. Leukoc. Biol. 76 (2004) 1151-1161
86. Laporte S.A., Oakley R.H., Holt J.A., Barak L.S., and Caron M.G. The interaction of beta-arrestin with the AP-2 adaptor is required for the clustering of beta 2-adrenergic receptor into clathrin-coated pits. J. Biol. Chem. 275 (2000) 23120-23126
87. Le Borgne R., Schmidt A., Mauxion F., Griffiths G., and Hoflack B. Binding of AP-1 Golgi adaptors to membranes requires phosphorylated cytoplasmic domains of the mannose 6-phosphate/insulin-like growth factor II receptor. J. Biol. Chem. 268 (1993) 22552-22556
88. Lewin D.A., and Mellman I. Sorting out adaptors. Biochim. Biophys. Acta 1401 (1998) 129-145
89. Lindmark I.M., Karlsson A., Serrander L., Francois P., Lew D., Rasmusson B., Stendahl O., and Nue O. Synaptotagmin II could confer Ca2+ sensitivity to phagocytosis in human neutrophils. Biochim. Biophys. Acta 1590 (2002) 159-166
90. Lippert U., Ferrari D.M., and Jahn R. Endobrevin/VAMP8 mediates exocytotic release of hexosaminidase from rat basophilic leukaemia cells. FEBS Lett. 581 (2007) 3479-3484
91. Logan M.R., Lacy P., Bablitz B., and Moqbel R. Expression of eosinophil target SNAREs as potential cognate receptors for vesicle-associated membrane protein-2 in exocytosis. J. Allergy Clin. Immunol. 109 (2002) 299-306
92. Martin-Martin B., Nabokina S.M., Blasi J., Lazo P.A., and Mollinedo F. Involvement of SNAP-23 and syntaxin 6 in human neutrophil exocytosis. Blood 96 (2000) 2574-2583
93. Martin-Verdeaux S., Pombo I., Iannascoli B., Roa M., Varin-Blank N., Rivera J., and Blank U. Evidence of a role for Munc18-2 and microtubules in mast cell granule exocytosis. J. Cell Sci. 116 (2003) 325-334
94. Martina J.A., Bonangelino C.J., Aguilar R.C., and Bonifacino J.S. Stonin 2: an adaptor-like protein that interacts with components of the endocytic machinery. J. Cell Biol. 153 (2001) 1111-1120
95. Martinez I., Chakrabarti S., Hellevik T., Morehead J., Fowler K., and Andrews N.W. Synaptotagmin VII regulates Ca2+-dependent exocytosis of lysosomes in fibroblasts. J. Cell Biol. 148 (2000) 1141-1150
96. Masuda E.S., Luo Y., Young C., Shen M., Rossi A.B., Huang B.C., Yu S., Bennett M.K., Payan D.G., and Scheller R.H. Rab37 is a novel mast cell specific GTPase localized to secretory granules. FEBS Lett. 470 (2000) 61-64
97. Masztalerz A., Zeelenberg I.S., Wijnands Y.M., de Bruijn R., Drager A.M., Janssen H., and Roos E. Synaptotagmin 3 deficiency in T cells impairs recycling of the chemokine receptor CXCR4 and thereby inhibits CXCL12 chemokine-induced migration. J. Cell Sci. 120 (2007) 219-228
98. Mauxion F., Le Borgne R., Munier-Lehmann H., and Hoflack B. A casein kinase II phosphorylation site in the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor determines the high affinity interaction of the AP-1 Golgi assembly proteins with membranes. J. Biol. Chem. 271 (1996) 2171-2178
99. Mc Dermott R., Ziylan U., Spehner D., Bausinger H., Lipsker D., Mommaas M., Cazenave J.P., Raposo G., Goud B., de la Salle H., Salamero J., and Hanau D. Birbeck granules are subdomains of endosomal recycling compartment in human epidermal langerhans cells, which form where langerin accumulates. Mol. Biol. Cell 13 (2002) 317-335
100. McVey Ward D., Griffiths G.M., Stinchcombe J.C., and Kaplan J. Analysis of the lysosomal storage disease Chediak-Higashi syndrome. Traffic 1 (2000) 816-822
101. Mehrotra B., Myszka D.G., and Prestwich G.D. Binding kinetics, ligand specificity for the interactions of the C2B domain of synaptogmin II with inositol polyphosphates and phosphoinositides. Biochemistry 39 (2000) 9679-9686
102. Menager M.M., Menasche G., Romao M., Knapnougel P., Ho C.H., Garfa M., Raposo G., Feldmann J., Fischer A., and de Saint Basile G. Secretory cytotoxic granule maturation and exocytosis require the effector protein hMunc13-4. Nat. Immunol. 8 (2007) 257-267
103. Menasche G., Pastural E., Feldmann J., Certain S., Ersoy F., Dupuis S., Wulffraat N., Bianchi D., Fischer A., Le Deist F., and de Saint Basile G. Mutations in RAB27A cause Griscelli syndrome associated with haemophagocytic syndrome. Nat. Genet. 25 (2000) 173-176
104. Menasche G., Feldmann J., Houdusse A., Desaymard C., Fischer A., Goud B., and de Saint Basile G. Biochemical and functional characterization of Rab27a mutations occurring in Griscelli syndrome patients. Blood 101 (2003) 2736-2742
105. Mizuno K., Tolmachova T., Ushakov D.S., Romao M., Abrink M., Ferenczi M.A., Raposo G., and Seabra M.C. Rab27b regulates mast cell granule dynamics and secretion. Traffic 8 (2007) 883-892
106. Mizutani A., Fukuda M., Niinobe M., and Mikoshiba K. Regulation of AP-2-synaptotagmin interaction by inositol high polyphosphates. Biochem. Biophys. Res. Commun. 240 (1997) 128-131
107. Mousavi S.A., Malerod L., Berg T., and Kjeken R. Clathrin-dependent endocytosis. Biochem. J. 377 (2004) 1-16
108. Munafó D.B., Jennifer J.L., Ellis B.A., Rutschmann S., Beutler B., and Catz S.D. Rab27a is a key component of the secretory machinery of azurophilic granules in granulocytes. Biochem. J. 402 (2007) 229-239
109. Nagle D.L., Karim M.A., Woolf E.A., Holmgren L., Bork P., Misumi D.J., McGrail S.H., Dussault B.J., Perou C.M., Boissy R.E., Duyk G.M., Spritz R.A., and Moore K.J. Identification and mutation analysis of the complete gene for Chediak-Higashi syndrome. Nat. Genet. 14 (1996) 307-311
110. Neeft M., Weiffer M., de Jong A.S., Negroiu G., Metz C.H., van Loon A., Groffith J., Krijgsveld J., Wulffraat N., Koch H., Heck A.J., Brose N., Kleojmeer M., and van der Sluijs P. Munc13-4 is an effector of Rab27a and controls secretion of lysosomes inhematopoietic cells. Mol. Biol. 16 (2005) 731-741
111. Nishida K., Yamasaki S., Ito Y., Kabu K., Hattori K., Tezuka T., Nishizumi H., Kitamura D., Goitsuka R., Geha R.S., Yamamoto T., Yagi T., and Hirano T. Fcε{lunate} RI-mediated mast cell degranulation requires calcium-independent microtubule-dependent translocation of granules to the plasma membrane. J. Cell Biol. 170 (2005) 115-126
112. Nonet M.L., Grundahl K., Meyer B.J., and Rand J.B. Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73 (1993) 1291-1305
113. Ohno H. Clathrin-associated adaptor protein complexes. J. Cell Sci. 119 (2006) 3719-3721
114. Olszewski M.B., Trzaska D., Knol E.F., Adamczewska V., and Dastych J. Efficient sorting of TNF-alpha to rodent mast cell granules is dependent on N-linked glycosylation. Eur. J. Immunol. 36 (2006) 997-1008
115. Ooi C.E., Dell'Angelica E.C., and Bonifacino J.S. ADP-Ribosylation Factor 1(ARF1) regulates recruitment of the AP-3 adaptor complex to membranes. J. Cell Biol. 142 (1998) 391-402
116. Peden A.A., Oorschot V., Hesser B.A., Austin C.D., Scheller R.H., and Klumperman J. Localization of the AP-3 adaptor complex defines a novel endosomal exit site for lysosomal membrane proteins. J. Cell Biol. 164 (2004) 1065-1076
117. Pelham H.R. Membrane traffic: GGAs sort Ubiquitin. Curr. Biol. 14 (2004) R357
118. Perin M.S., Fried V.A., Mignery G.A., Jahn R., and Sudhof T.C. Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature 345 (1990) 260-263
119. Piper R.C., and Luzio J.P. Ubiquitin-dependent sorting of integral membrane proteins for degradation in lysosomes. Curr. Opin. Cell Biol. 19 (2007) 459-465
120. Polgar J., Lane W.S., Chung S.H., Houng A.K., and Reed G.L. Phosphorylation of SNAP-23 in activated human platelets. J. Biol. Chem. 278 (2003) 44369-44376
121. Poupon V., Girard M., Legendre-Guillemin V., Thomas S., Bourbonniere L., Philie J., Bright N.A., and McPherson P.S. Clathrin light chains function in mannose phosphate receptor trafficking via regulation of actin assembly. Proc. Natl. Acad. Sci. USA 105 (2008) 168-173
122. Puertollano R., Aguilar R.C., Gorshkova I., Crouch R.J., and Bonifacino J. Sorting of mannose 6-phosphate receptors mediated by the GGAs. Science 292 (2001) 1712-1716
123. Puri N., and Roche P.A. Mast cells possess distinct secretory granule subsets whose exocytosis is regulated by different SNARE isoforms. Proc. Natl. Acad. Sci. USA 105 (2008) 2580-2585
124. Puri N., Kruhlak M.J., Whiteheart S.W., and Roche P.A. Mast cell degranulation requires N-ethylmaleimide-sensitive factor-mediated SNARE disassembly. J. Immunol. 171 (2003) 5345-5352
125. Raiborg C., and Stenmark H. Hrs and endocytic sorting of ubiquitinated membrane proteins. Cell Struct. Funct. 27 (2002) 403-408
126. Ramalho J.S., Tolmachova T., Hume A.N., McGuigan A., Gregory-Evans C.Y., Huxley C., and Seabra M.C. Chromosomal mapping, gene structure and characterization of the human and murine RAB27B gene. BMC Genet. 2 (2001) 2
127. Raposo G., Tenza D., Mecheri S., Peronet R., Bonnerot C., and Desaymard C. Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation. Mol. Biol. Cell 8 (1997) 2631-2645
128. Reales E., Mora-Lopez F., Rivas V., Garcia-Poley A., Brieva J.A., and Campos-Caro A. Identification of soluble N-ethylmaleimide-sensitive factor attachment protein receptor exocytotic machinery in human plasma cells: SNAP-23 is essential for antibody secretion. J. Immunol. 175 (2005) 6686-6693
129. Regnier V.A., Tooze S.A., and Huttner W.B. Newly synthesized synaptophysin is transported to synaptic-like microvesicles via constitutive secretory vesicles and the plasma membrane. EMBO J. 10 (1991) 3589-3601
130. Roa M., Paumet F., Le Mao J., David B., and Blank U. Involvement of the ras-like GTPase rab3d in RBL-2H3 mast cell exocytosis following stimulation via high affinity IgE receptors (Fc epsilonRI). J. Immunol. 159 (1997) 2815-2823
131. Robinson M.S., and Bonifacino J.S. Adaptor-related proteins. Curr. Opin. Cell Biol. 13 (2001) 444-453
132. Rouille Y., Rohn W., and Hoflack B. Targeting of lysosomal proteins. Semin. Cell Dev. Biol. 11 (2000) 165-171
133. Rous B.A., Reaves B.J., Ihrke G., Briggs J.A., Gray S.R., Stephens D.J., Banting G., and Luzio J.P. Role of adaptor complex AP-3 in targeting wild-type and mutated CD63 to lysosomes. Mol. Biol. Cell 13 (2002) 1071-1082
134. Salazar G., Craige B., Styers M.L., Newell-Litwa K.A., Doucette M.M., Wainer B.H., Falcon-Perez J.M., Dell'Angelica E.C., Peden A.A., Werner E., and Faundez V. BLOC-1 complex deficiency alters the targeting of adaptor protein complex-3 cargoes. Mol. Biol. Cell 17 (2006) 4014-4026
135. Salinas E., Rodriguez G., and Quintanar J.L. Presence of SNAP-23 and syntaxin 4 in mouse and hamster peritoneal mast cells. Acta Histochem. 109 (2007) 454-460
136. Sander L.E., Frank S.P., Bolat S., Galli T., Bigalke H., Bischoff S.C., and Lorens A. 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. 38 (2008) 855-863
137. Sannes P.L., and Spicer S.S. The heterophagic granules of mast cells: dipeptidyl aminopeptidase II activity and resistance to exocytosis. Am. J. Pathol. 94 (1979) 447-457
138. Santoro A., Cannella S., Bossi G., Gallo F., Trizzino A., Pende D., Dieli F., Bruno G., Stinchcombe J.C., Micalizzi C., De Fusco C., Danesino C., Moretta L., Notarangelo L.D., Griffiths G.M., and Arico M. Novel Munc13-4 mutations in children and young adult patients with haemophagocytic lymphohistiocytosis. J. Med. Genet. 43 (2006) 953-960
139. Schwartz L.B., and Austen K.F. Enzymes of the mast cell granule. J. Invest. Dermatol. 74 (1980) 349-353
140. Seabra M.C., and Coudrier E. Rab GTPases and myosin motors in organelle motility. Traffic 5 (2004) 393-399
141. Setty S.R.G., Tenza D., Truschel S.T., Chou E., Sviderskaya E.V., Theos A.C., Lamoreux M.L., Di Pietro S.M., Starcevic M., Bennett D.C., Dell'Angelica E.C., Raposo G., and Marks M.S. BLOC-1 is required for cargo-specific sorting from vacuolar early endosomes toward lysosome-related organelles. Mol. Biol. Cell 18 (2007) 768-780
142. Shi G., Faundez V., Roos J., Dell'Angelica E.C., and Kelly R.B. Neuroendocrine synaptic vesicles are formed in vitro by both clathrin-dependent and clathrin-independent pathways. J. Cell Biol. 143 (1998) 947-955
143. Shiba T., Kametaka S., Kawasaki M., Shibata M., Waguri S., Uchiyama Y., and Wakatsuki S. Insights into the phosphoregulation of beta-secretase sorting signal by the VHS domain of GGA1. Traffic 5 (2004) 437-448
144. Smith A.J., Pfeiffer J.R., Zhang J., Martinez A.M., Griffiths G.M., and Wilson B.S. Microtubule-dependent transport of secretory vesicles in RBL-2H3 cells. Traffic 4 (2003) 302-312
145. Starcevic M., Nazarian R., and Dell'Angelica E.C. The molecular machinery for the biogenesis of lysosome-related organelles: lessons from Hermansky-Pudlak syndrome. Semin. Cell Dev. Biol. 13 (2002) 271-278
146. Stinchcombe J., Bossi G., and Griffiths G.M. Linking albinism and immunity: the secrets of secretory lysosomes. Science 305 (2004) 55-59
147. Stinchcombe J.C., Bossi G., Booth S., and Griffiths G.M. The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 15 (2001) 751-761
148. Stinchcombe J.C., Majorovits E., Bossi G., Fuller S., and Griffiths G.M. Centrosome polarization delivers secretory granules to the immunological synapse. Nature 443 (2006) 462-465
149. Sugita M., Cao X., Watts G.F., Rogersm R.A., Bonifacino J.S., and Brenner M.B. Failure of trafficking and antigen presentation by CD1 in AP-3-deficient cells. Immunity 16 (2002) 697-706
150. Sulimenko V., Draberova E., Sulimenko T., Macurek L., Richterova V., Draber P., and Draber P. Regulation of microtubule formation in activated mast cells by complexes of {gamma}-tubulin with Fyn and Syk kinases. J. Immunol. 176 (2006) 7243-7253
151. Swank R.T., Novak E.K., McGarry M.P., Zhang Y., Li W., Zhang Q., and Feng L. Abnormal vesicular trafficking in mouse models of Hermansky-Pudlak syndrome. Pigment. Cell Res. 13 Suppl. 8 (2000) 59-67
152. Takei K., Mundigl O., Daniell L., and De C.P. The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J. Cell Biol. 133 (1996) 1237-1250
153. Tiwari N., Wang C.C., Brochetta C., Ke G., Vita F., Qi Z., Rivera J., Soranzo M.R., Zabucchi G., Hong W., and Blank U. VAMP-8 segregates mast cell-preformed mediator exocytosis from cytokine trafficking pathways. Blood 111 (2008) 3665-3674
154. Tolmachova T., Anders R., Stinchcombe J., Bossi G., Griffiths G.M., Huxley C., and Seabra M.C. A general role for Rab27a in secretory cells. Mol. Biol. Cell 15 (2004) 332-344
155. Tooze J., and Tooze S.A. Clathrin-coated vesicular transport of secretory proteins during the formation of ACTH-containing secretory granules in AtT20 cells. J. Cell Biol. 103 (1986) 839-850
156. Tooze S.A. Biogenesis of secretory granules in the trans-Golgi network of neuroendocrine and endocrine cells. Biochim. Biophys. Acta 1404 (1998) 231-244
157. Traub L.M. Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection. J. Cell Biol. 163 (2003) 203-208
158. Traub L.M. Common principles in clathrin-mediated sorting at the Golgi and the plasma membrane. Biochim. Biophys. Acta 1744 (2005) 415-437
159. Tuvim M.J., Adachi R., Chocano J.F., Moore R.H., Lampert R.M., Zera E., Romero E., Knoll B.J., and Dickey B.F. 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. 20 (1999) 79-89
160. Ullrich B., Li C., Zhang J.Z., McMahon H., Anderson R.G., Geppert M., and Sudhof T.C. Functional properties of multiple synaptotagmins in brain. Neuron 13 (1994) 1281-1291
161. Uzan-Gafsou S., Bausinger H., Proamer F., Monier S., Lipsker D., Cazenave J.P., Goud B., de la Salle H., Hanau D., and Salamero J. Rab11A controls the biogenesis of Birbeck granules by regulating langerin recycling and stability. Mol. Biol. Cell 18 (2007) 3169-3179
162. Vaidyanathan V.V., Puri N., and Roche P.A. The last exon of SNAP-23 regulates granule exocytosis from mast cells. J. Biol. Chem. 276 (2001) 25101-25106
163. Valladeau J., Ravel O., Dezutter-Dambuyant C., Moore K., Kleijmeer M., Liu Y., Duvert-Frances V., Vincent C., Schmitt D., Davoust J., Caux C., Lebecque S., and Saeland S. Langerin, a novel C-type lectin specific to langerhans cells, is an endocytic receptor that induces the formation of Birbeck granules. Immunity 12 (2000) 71-81
164. Van den Steen P., Rudd P.M., Dwek R.A., and Opdenakker G. Concepts and principles of O-linked glycosylation. Crit. Rev. Biochem. Mol. Biol. 33 (1998) 151-208
165. Vincent-Schneider H., Thery C., Mazzeo D., Tenza D., Raposo G., and Bonnerot C. Secretory granules of mast cells accumulate mature and immature MHC class II molecules. J. Cell Sci. 114 (2001) 323-334
166. Walther K., Diril M.K., Jung N., and Haucke V. Functional dissection of the interactions of stonin 2 with the adaptor complex AP-2 and synaptotagmin. Proc. Natl. Acad. Sci. USA 101 (2004) 964-969
167. Wang T., and Hong W. Assay and functional properties of Rab34 interaction with RILP in lysosome morphogenesis. Methods Enzymol. 403 (2005) 675-687
168. Ward D.M., Griffiths G.M., Stinchcombe J.C., and Kaplan J. Analysis of the lysosomal storage disease Chediak-Higashi syndrome. Traffic 1 (2000) 816-822
169. Wilson S.M., Yip R., Swing D.A., O'Sullivan T.N., Zhang Y., Novak E.K., Swank R.T., Russell L.B., Copeland N.G., and Jenkins N.A. A mutation in Rab27a causes the vesicle transport defects observed in ashen mice. Proc. Natl. Acad. Sci. USA 97 (2000) 7933-7938
170. Wu M., Baumgart T., Hammond S., Holowka D., and Baird B. Differential targeting of secretory lysosomes and recycling endosomes in mast cells revealed by patterned antigen arrays. J. Cell Sci. 120 (2007) 3147-3154
171. Yoshihara M., Adolfsen B., and Littleton J.T. Is synaptotagmin the calcium sensor?. Curr. Opin. Neurobiol. 13 (2003) 315-323
172. Yu M., Kasai K., Nagashima K., Torii S., Yokota-Hashimoto H., Okamoto K., Takeuchi T., Gomi H., and Izumi T. Exophilin4/Slp2-a targets glucagon granules to the plasma membrane through unique Ca2+-inhibitory phospholipid-binding activity of the C2A domain. Mol. Biol. Cell 18 (2007) 688-696
173. Zhang J.Z., Davletov B.A., Sudhof T.C., and Anderson R.G. Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling. Cell 78 (1994) 751-760
174. Zhu Y., Traub L.M., and Kornfeld S. ADP-Ribosylation factor 1 transiently activates high-affinity adaptor protein complex AP-1 binding sites on Golgi membranes. Mol. Biol. Cell 9 (1998) 1323-1337
175. Zuccato E., Blott E.J., Holt O., Sigismund S., Shaw M., Bossi G., and Griffiths G.M. Sorting of Fas ligand to secretory lysosomes is regulated by mono-ubiquitylation and phosphorylation. J. Cell Sci. 120 (2007) 191-199