Rab27a and Rab27b control different steps of the exosome secretion pathway

Nature Cell Biology

Volumn 12, Issue 1, 2010, Pages 19-30

  Ostrowski, Matias ^a,b   Carmo, Nuno B ^c   Krumeich, Sophie ^a,b   Fanget, Isabelle ^j   Raposo, Graça ^b,d   Savina, Ariel ^a,b   Moita, Catarina F ^c   Schauer, Kristine ^b,d   Hume, Alistair N ^e   Freitas, Rui P ^c   Goud, Bruno ^b,d   Benaroch, Philippe ^a,b   Hacohen, Nir ^h,i   Fukuda, Mitsunori ^k   Desnos, Claire ^j   Seabra, Miguel C ^e,f,g   Darchen, François ^j   Amigorena, Sebastian ^a,b   Moita, Luis F ^c   Thery, Clotilde ^a,b  

^a PSL RESEARCH UNIVERSITY   (France)

^b INSTITUT CURIE   (France)

^c Avenida Department Egas Moniz   (Portugal)

^d INSTITUT CURIE   (France)

^e NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^f NOVA MEDICAL SCHOOL   (Portugal)

^g INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^h MASSACHUSETTS GENERAL HOSPITAL   (United States)

ⁱ BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^j INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

^k TOHOKU UNIVERSITY   (Japan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

EXOPHILIN 5; MEMBRANE PROTEIN; RAB PROTEIN; RAB27A PROTEIN; RAB27B PROTEIN; SYNAPTOTAGMIN; SYNAPTOTAGMIN LIKE 4; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOSOME; EXOSOME; GENE SILENCING; HELA CELL; MOLECULAR DOCKING; MULTIVESICULAR ENDOSOME; PRIORITY JOURNAL; RNA INTERFERENCE; SECRETION;

CELL COMMUNICATION; CELL MEMBRANE; ENDOSOMES; EXOSOMES; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; HELA CELLS; HUMANS; IMMUNOBLOTTING; RAB GTP-BINDING PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SUBCELLULAR FRACTIONS; VESICULAR TRANSPORT PROTEINS;

EID: 79953136097     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2000     Document Type: Article

References (49)

1. Thery, C., Zitvogel, L. & Amigorena, S. Exosomes: composition, biogenesis and function. Nature Rev. Immunol. 2, 569-579 (2002). (Pubitemid 37328732)
2. Fevrier, B. & Raposo, G. Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr. Opin. Cell Biol. 16, 415-421 (2004). (Pubitemid 38903148)
3. Johnstone, R. M. Exosomes biological significance: a concise review. Blood Cells Mol. Dis. 36, 315-321 (2006).
4. Lakkaraju, A. & Rodriguez-Boulan, E. Itinerant exosomes: emerging roles in cell and tissue polarity. Trends Cell Biol. 18, 199-209 (2008).
5. Raposo, G. et al. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 183, 1161-1172 (1996). (Pubitemid 26113979)
6. Zitvogel, L. et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nature Med. 4, 594-600 (1998). (Pubitemid 28237359)
7. Thery, C. et al. Indirect activation of naive CD4+ T cells by dendritic cell-derived exosomes. Nature Immunol. 3, 1156-1162 (2002). (Pubitemid 35469700)
8. Wiley, R. D. & Gummuluru, S. Immature dendritic cell-derived exosomes can mediate HIV-1 trans infection. Proc. Natl Acad. Sci. USA 103, 738-743 (2006). (Pubitemid 43153095)
9. Fevrier, B. et al. Cells release prions in association with exosomes. Proc. Natl Acad. Sci. USA 101, 9683-9688 (2004). (Pubitemid 38869296)
10. Rajendran, L. et al. Alzheimer's disease β-amyloid peptides are released in association with exosomes. Proc. Natl Acad. Sci. USA 103, 11172-11177 (2006). (Pubitemid 44156491)
11. Wolfers, J. et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nature Med. 7, 297-303 (2001). (Pubitemid 32224344)
12. Iero, M. et al. Tumour-released exosomes and their implications in cancer immunity. Cell Death Differ. 15, 80-88 (2008). (Pubitemid 350286175)
13. Zeelenberg, I. S. et al. Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses. Cancer Res. 68, 1228-1235 (2008). (Pubitemid 351272243)
14. Futter, C. E., Collinson, L. M., Backer, J. M. & Hopkins, C. R. Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J. Cell Biol. 155, 1251-1264 (2001).
15. Pan, B. T., Teng, K., Wu, C., Adam, M. & Johnstone, R. M. Electron. microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J. Cell Biol. 101, 942-948 (1985). (Pubitemid 16256847)
16. Booth, A. M. et al. Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J. Cell Biol. 172, 923-935 (2006).
17. Zerial, M. & McBride, H. Rab proteins as membrane organizers. Nature Rev. Mol. Cell Biol. 2, 107-117 (2001). (Pubitemid 33674039)
18. Seabra, M. C., Mules, E. H. & Hume, A. N. Rab GTPases, intracellular traffic and disease. Trends Mol. Med. 8, 23-30 (2002). (Pubitemid 34044675)
19. Ali, B. R. & Seabra, M. C. Targeting of Rab GTPases to cellular membranes. Biochem. Soc. Trans. 33, 652-656 (2005). (Pubitemid 41160831)
20. Escola, J. M. et al. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J. Biol. Chem. 273, 20121-20127 (1998).
21. Morelli, A. E. et al. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 104, 3257-3266 (2004). (Pubitemid 39507144)
22. Thery, C. et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J. Immunol. 166, 7309-7318 (2001). (Pubitemid 32525606)
23. Ramalho, J. S. et al. Chromosomal mapping, gene structure and characterization of the human and murine RAB27B gene. BMC Genet. 2, 2 (2001).
24. Thery, C., Amigorena, S., Raposo, G. & Clayton, A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. Chapter 3, Unit 3 22 (2006).
25. Desnos, C. et al. Myosin va mediates docking of secretory granules at the plasma membrane. J. Neurosci. 27, 10636-10645 (2007). (Pubitemid 47501995)
26. Huet, S. et al. Analysis of transient behavior in complex trajectories: application to secretory vesicle dynamics. Biophys. J. 91, 3542-3559 (2006). (Pubitemid 44788286)
27. Nofal, S., Becherer, U., Hof, D., Matti, U. & Rettig, J. Primed vesicles can be distinguished from docked vesicles by analyzing their mobility. J. Neurosci. 27, 1386-1395 (2007).
28. Beraud-Dufour, S. & Balch, W. A journey through the exocytic pathway. J. Cell Sci. 115, 1779-1780 (2002). (Pubitemid 34567239)
29. Pereira-Leal, J. B. & Seabra, M. C. Evolution of the Rab family of small GTP-binding proteins. J. Mol. Biol. 313, 889-901 (2001). (Pubitemid 33063434)
30. Buschow, S. I. et al. MHC II in dendritic cells is targeted to lysosomes or T cell-induced exosomes via distinct multivesicular body pathways. Traffic 10, 1528-1542 (2009).
31. Desnos, C. et al. Rab27A and its effector MyRIP link secretory granules to F-actin and control their motion towards release sites. J. Cell Biol. 163, 559-570 (2003). (Pubitemid 37429869)
32. Chen, X. et al. Rab27b localizes to zymogen granules and regulates pancreatic acinar exocytosis. Biochem. Biophys. Res. Commun. 323, 1157-1162 (2004). (Pubitemid 39296546)
33. Imai, A., Yoshie, S., Nashida, T., Shimomura, H. & Fukuda, M. The small GTPase Rab27B regulates amylase release from rat parotid acinar cells. J. Cell Sci. 117, 1945-1953 (2004). (Pubitemid 38745128)
34. Mizuno, K. et al. Rab27b regulates mast cell granule dynamics and secretion. Traffic 8, 883-892 (2007). (Pubitemid 46971634)
35. Tolmachova, T., Abrink, M., Futter, C. E., Authi, K. S. & Seabra, M. C. Rab27b regulates number and secretion of platelet dense granules. Proc. Natl Acad. Sci. USA 104, 5872-5877 (2007). (Pubitemid 47175626)
36. Stinchcombe, J. C. et al. Rab27a is required for regulated secretion in cytotoxic T lymphocytes. J. Cell Biol. 152, 825-834 (2001).
37. Barral, D. C. et al. Functional redundancy of Rab27 proteins and the pathogenesis of Griscelli syndrome. J. Clin. Invest. 110, 247-257 (2002). (Pubitemid 34787362)
38. Strom, M., Hume, A. N., Tarafder, A. K., Barkagianni, E. & Seabra, M. C. A family of Rab27-binding proteins. Melanophilin links Rab27a and myosin Va function in melanosome transport. J. Biol. Chem. 277, 25423-25430 (2002). (Pubitemid 34951855)
39. Seabra, M. C. & Coudrier, E. Rab GTPases and myosin motors in organelle motility. Traffic 5, 393-399 (2004). (Pubitemid 38765434)
40. Savina, A., Vidal, M. & Colombo, M. I. The exosome pathway in K562 cells is regulated by Rab11. J. Cell Sci. 115, 2505-2515 (2002). (Pubitemid 34778068)
41. Kondo, H. et al. Constitutive GDP/GTP exchange and secretion-dependent GTP hydrolysis activity for Rab27 in platelets. J. Biol. Chem. 281, 28657-28665 (2006). (Pubitemid 44507008)
42. Stumptner-Cuvelette, P. et al. HIV-1 Nef impairs MHC class II antigen presentation and surface expression. Proc. Natl Acad. Sci. USA 98, 12144-12149 (2001). (Pubitemid 32959841)
43. Hume, A. N. et al. Rab27a regulates the peripheral distribution of melanosomes in melanocytes. J. Cell Biol. 152, 795-808 (2001). (Pubitemid 34280164)
44. Blott, E. J., Bossi, G., Clark, R., Zvelebil, M. & Griffiths, G. M. Fas ligand is targeted to secretory lysosomes via a proline-rich domain in its cytoplasmic tail. J. Cell Sci. 114, 2405-2416 (2001). (Pubitemid 32684796)
45. Fukuda, M., Kanno, E., Saegusa, C., Ogata, Y. & Kuroda, T. S. Slp4-a/granuphilin-a regulates dense-core vesicle exocytosis in PC12 cells. J. Biol. Chem. 277, 39673-39678 (2002). (Pubitemid 35190949)
46. Shu, X., Shaner, N. C., Yarbrough, C. A., Tsien, R. Y. & Remington, S. J. Novel chromophores and buried charges control color in mFruits. Biochemistry 45, 9639-9647 (2006). (Pubitemid 44257411)
47. Moffat, J. et al. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124, 1283-1298 (2006).
48. Racine, V. et al. Visualization and quantification of vesicle trafficking on a threedimensional cytoskeleton network in living cells. J. Microsc. 225, 214-228 (2007). (Pubitemid 46434873)
49. Steyer, J. A. & Almers, W. Tracking single secretory granules in live chromaffin cells by evanescent-field fluorescence microscopy. Biophys. J. 76, 2262-2271 (1999). (Pubitemid 29266380)