Synaptotagmin (Syt) IX is an essential determinant for protein sorting to secretory granules in mast cells

Blood

Volumn 109, Issue 8, 2007, Pages 3385-3392

  Haberman, Yael ^a   Ziv, Idit ^a   Gorzalczany, Yaara ^a   Hirschberg, Koret ^a   Mittleman, Leonide ^a   Fukuda, Mitsunori ^b   Sagi Eisenberg, Ronit ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; CLATHRIN; GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; PROTEIN AP1; PROTEIN TGN38; SYNAPTOTAGMIN; SYNAPTOTAGMIN IX; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENDOCYTOSIS; EXOCYTOSIS; MAST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN TARGETING; RAT; SECRETORY GRANULE; TRANS GOLGI NETWORK;

EID: 34147103471     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-07-033126     Document Type: Article

References (41)

1. Griffiths GM. Secretory lysosomes - a special mechanism of regulated secretion in haemopoietic cells. Trends Cell Biol. 1996;6:329-332.
2. Schwartz LB, Austen KF. Enzymes of the mast cell granule. J Invest Dermatol. 1980;74:349-353.
3. Suarez-Quian CA. The distribution of four lysosomal integral membrane proteins (LIMPs) in rat basophilic leukemia cells. Tissue Cell. 1987;19:495-504.
4. Dell'Angelica EC, Mullins C, Caplan S, Bonifacino JS. Lysosome-related organelles. FASEB J. 2000;14:1265-1278.
5. 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.
6. Baram D, Adachi R, Medalia O, et al. Synaptotagmin II negatively regulates Ca2+-triggered exocytosis of lysosomes in mast cells. J Exp Med. 1999;189:1649-1658.
7. Baram D, Mekori YA, Sagi-Eisenberg R. Synaptotagmin regulates mast cell functions. Immunol Rev. 2001;179:25-34.
8. 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.
9. 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.
10. 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.
11. 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.
12. Humphrey JS, Peters PJ, Yuan LC, Bonifacino JS. Localization of TGN38 to the trans-Golgi network: involvement of a cytoplasmic tyrosine-containing sequence. J Cell Biol. 1993;120:1123-1135.
13. 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.
14. 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.
15. Ren M, Xu G, Zeng J, De Lemos-Chiarandini C, 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 U S A. 1998;95:6187-6192.
16. 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.
17. Matlin KS, Simons K. Reduced temperature prevents transfer of a membrane glycoprotein to the cell surface but does not prevent terminal glycosylation. Cell. 1983;34:233-243.
18. Griffiths GD, Kershaw D, Booth AG. Rabbit peroxidase-antiperoxidase complex (PAP) as a model for the uptake of immunoglobulin G by the human placenta. Histochem J. 1985;17:867-881.
19. Lippincott-Schwartz J, Yuan LC, Bonifacino JS, Klausner RD. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell. 1989;56:801-813.
20. Orci L, Tagaya M, Amherdt M, et al. Brefeldin A, a drug that blocks secretion, prevents the assembly of non-clathrin-coated buds on Golgi cisternae. Cell. 1991;64:1183-1195.
21. Sonnichsen B, De Renzis S, Nielsen E, Rietdorf J, Zerial M. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol. 2000;149:901-914.
22. 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(pt 16):2385-2396.
23. 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(pt 4):701-712.
24. Peng Z, Grimberg E, Sagi-Eisenberg R. Suppression of synaptotagmin II restrains phorbolester-induced downregulation of protein kinase Calpha by diverting the kinase from a degradative pathway to the recycling endocytic compartment. J Cell Sci. 2002;115:3083-3092.
25. Sagi-Eisenberg R, Pecht I. Protein kinase C, a coupling element between stimulus and secretion of basophils. Immunol Lett. 1984;8:237-241.
26. Dittie AS, Hajibagheri N, Tooze SA. The AP-1 adaptor complex binds to immature secretory granules from PC12 cells, and is regulated by ADP-ribosylation factor. J Cell Biol. 1996;132:523-536.
27. Austin C, Hinners I, Tooze SA. Direct and GTP-dependent interaction of ADP-ribosylation factor 1 with clathrin adaptor protein AP-1 on immature secretory granules. J Biol Chem. 2000;275:21862-21869.
28. 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.
29. 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.
30. Dascher C, Balch WE. Dominant inhibitory mutants of ARF1 block endoplasmic reticulum to Golgi transport and trigger disassembly of the Golgi apparatus. J Biol Chem. 1994;269:1437-1448.
31. 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.
32. 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.
33. Nichols BJ, Kenworthy AK, Polishchuk RS, et al. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J Cell Biol. 2001;153:529-541.
34. 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.
35. Johannes L, Tenza D, Antony C, Goud B. Retrograde transport of KDEL-bearing B-fragment of Shiga toxin. J Biol Chem. 1997;272:19554-19561.
36. Futter CE, Pearse A, Hewlett LJ, Hopkins CR. Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J Cell Biol. 1996;132:1011-1023.
37. Saint-Pol A, Yelamos B, Amessou M, et al. Clathrin adaptor epsinR is required for retrograde sorting on early endosomal membranes. Dev Cell. 2004;6:525-538.
38. van Dam EM, Stoorvogel W. Dynamin-dependent transferrin receptor recycling by endosome-derived clathrin-coated vesicles. Mol Biol Cell. 2002;13:169-182.
39. Futter CE, Gibson A, Allchin EH, et al. In polarized MDCK cells basolateral vesicles arise from clathrin-gamma-adaptin-coated domains on endosomal tubules. J Cell Biol. 1998;141:611-623.
40. Eaton BA, Haugwitz M, Lau D, Moore HP. Biogenesis of regulated exocytotic carriers in neuroendocrine cells. J Neurosci. 2000;20:7334-7344.
41. Ahras M, Otto GP, Tooze SA. Synaptotagmin IV is necessary for the maturation of secretory granules in PC12 cells. J Cell Biol. 2006;173:241-251.