RAL-1 controls multivesicular body biogenesis and exosome secretion

Journal of Cell Biology

Volumn 211, Issue 1, 2015, Pages 27-37

  Hyenne, Vincent ^a,b,c   Apaydin, Ahmet ^a   Rodriguez, David ^a   Spiegelhalter, Coralie ^b   Hoff Yoessle, Sarah ^a   Diem, Maxime ^a   Tak, Saurabh ^a   Lefebvre, Olivier ^b,c   Schwab, Yannick ^b,d   Goetz, Jacky G ^b,c   Labouesse, Michel ^a,e  

^a CNRS   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c Federation de Medecine Translationnelle de Strasbourg FMTS   (France)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^e Sorbonne Universités   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EXOCYST; GUANOSINE TRIPHOSPHATASE; PROTEIN; RAL 1 PROTEIN; SHORT HAIRPIN RNA; SNARE PROTEIN; SYNTAXIN; SYNTAXIN 5; SYX 5 PROTEIN; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; RAL PROTEIN; RAL-1 PROTEIN, C ELEGANS;

ADULT; ANIMAL CELL; ARTICLE; BIOGENESIS; CAENORHABDITIS ELEGANS; CELL MEMBRANE; CENTRIFUGATION; COMPARATIVE STUDY; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME ACTIVITY; EXOSOME; LYSOSOME; MEMBRANE FUSION; MULTIVESICULAR BODY; NONHUMAN; OUTER MEMBRANE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING; ANIMAL; CYTOLOGY; ENZYMOLOGY; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; SECRETION (PROCESS);

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL MEMBRANE; EXOSOMES; MEMBRANE FUSION; MULTIVESICULAR BODIES; PROTEIN TRANSPORT; QA-SNARE PROTEINS; RAL GTP-BINDING PROTEINS;

EID: 84953451639     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201504136     Document Type: Article

References (54)

1. Abrami, L., L. Brandi, M. Moayeri, M.J. Brown, B.A. Krantz, S.H. Leppla, and F. G. van der Goot. 2013. Hijacking multivesicular bodies enables longterm and exosome-mediated long-distance action of anthrax toxin. Cell Reports. 5:986-996. http://dx.doi.org/10.10167j.celrep.2013.10.019
2. Armenti, S.T., E. Chan, and J. Nance. 2014. Polarized exocyst-mediated vesicle fusion directs intracellular lumenogenesis within the C. elegans excretory cell. Dev. Biol. 394:110-121. http://dx.doi.org/10.10167j.ydbio.2014.07.019
3. Baietti, M.F., Z. Zhang, E. Mortier, A. Melchior, G. Degeest, A. Geeraerts, Y. Ivarsson, F. Depoortere, C. Coomans, E. Vermeiren, et al. 2012. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat. Cell Biol. 14:677-685. http://dx.doi.org/10.1038/ncb2502
4. Balklava, Z., S. Pant, H. Fares, and B.D. Grant. 2007. Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat. Cell Biol. 9:1066-1073. http://dx.doi.org/10.1038/ncb1627
5. Bhattacharya, M., A.V. Babwah, C. Godin, PH. Anborgh, L.B. Dale, M.O. Poulter, and S.S. Ferguson. 2004. Ral and phospholipase D2-dependent pathway for constitutive metabotropic glutamate receptor endocytosis. J. Neurosci. 24:8752-8761. http://dx.doi.org/10.1523/JNEUR0SCI.3155-04.2004
6. Bobrie, A., S. Krumeich, F. Reyal, C. Recchi, L.F. Moita, M.C. Seabra, M. Ostrowski, and C. Thery. 2012. Rab27a supports exosome-dependent and -independent mechanisms that modify the tumor microenvironment and can promote tumor progression. Cancer Res. 72:4920-4930. http://dx.doi.org/10.1158/0008-5472.CAN-12-0925
7. Brenner, S. 1974. The genetics of Caenorhabditis elegans. Genetics. 77:71-94.
8. Brymora, A., V.A. Valova, M.R. Larsen, B.D. Roufogalis, and PJ. Robinson. 2001. The brain exocyst complex interacts with RalA in a GTP-dependent manner: identification of a novel mammalian Sec3 gene and a second Sec15 gene. J. Biol. Chem. 276:29792-29797. http://dx.doi.org/10.1074/jbc.C100320200
9. Colombo, M., C. Moita, G. van Niel, J. Kowal, J. Vigneron, P. Benaroch, N. Manel, L.F. Moita, C. Thery, and G. Raposo. 2013. Analysis of ESC RT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J. Cell Sci. 126:5553-5565. http://dx.doi.org/10.1242/jcs.128868
10. Corrotte, M., A.P. Nyguyen, M.L. Harlay, N. Vitale, M.F. Bader, and N.J. Grant. 2010. Ral isoforms are implicated in Fc gamma R-mediated phagocytosis: activation of phospholipase D by RalA. J. Immunol. 185:2942-2950. http://dx.doi.org/10.4049/jimmunol.0903138
11. Dickinson, D.J., J.D. Ward, D.J. Reiner, and B. Goldstein. 2013. Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat. Methods. 10:1028-1034. http://dx.doi.org/10.1038/nmeth.2641
12. Fader, C.M., D.G. Sanchez, M.B. Mestre, and M.I. Colombo. 2009. TI-VAMP/ VAMP7 and VAMP3/cellubrevin: two v-SNARE proteins involved in specific steps of the autophagy/multivesicular body pathways. Biochim. Biophys. Acta. 1793:1901-1916. http://dx.doi.org/10.1016/j.bbamcr.2009.09.011
13. Frand, A.R., S. Russel, and G. Ruvkun. 2005. Functional genomic analysis of C. elegans molting. PLoS Biol. 3:e312.
14. Gentry, L.R., T.D. Martin, D.J. Reiner, and C.J. Der. 2014. Ral small GTPase signaling and oncogenesis: More than just 15 minutes of fame. Biochim. Biophys. Acta. 1843:2976-2988. http://dx.doi.org/10.1016/j.bbamcr.2014.09.004
15. Ghossoub, R., F. Lembo, A. Rubio, C.B. Gaillard, J. Bouchet, N. Vitale, J. Slavik, M. Machala, and P. Zimmermann. 2014. Syntenin-ALIX exosome biogenesis and budding into multivesicular bodies are controlled by ARF6 and PLD2. Nat. Commun. 5:3477. http://dx.doi.org/10.1038/ncomms4477
16. Gilleard, J.S., J.D. Barry, and I.L. Johnstone. 1997. cis Regulatory requirements for hypodermal cell-specific expression of the Caenorhabditis elegans cuticle collagen gene dpy-7. Mol. Cell. Biol. 17:2301-2311.
17. Goi, T., M. Shipitsin, Z. Lu, D.A. Foster, S.G. Klinz, and L.A. Feig. 2000. An EGF receptor/Ral-GTPase signaling cascade regulates c-Src activity and substrate specificity. EMBO J. 19:623-630. http://dx.doi.org/10.1093/emboj/19.4.623
18. Gross, J.C., V. Chaudhary, K. Bartscherer, and M. Boutros. 2012. Active Wnt proteins are secreted on exosomes. Nat. Cell Biol. 14:1036-1045. http://dx.doi.org/10.1038/ncb2574
19. Hardwick, K.G., and H.R. Pelham. 1992. SED5 encodes a 39-kD integral membrane protein required for vesicular transport between the ER and the Golgi complex. J. Cell Biol. 119:513-521. http://dx.doi.org/10.1083/jcb.119.3.513
20. Hase, K., S. Kimura, H. Takatsu, M. Ohmae, S. Kawano, H. Kitamura, M. Ito, H. Watarai, C.C. Hazelett, C. Yeaman, and H. Ohno. 2009. M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex. Nat. Cell Biol. 11:1427-1432. http://dx.doi.org/10.1038/ncb1990
21. Hernandez, J.M., A.J. Kreutzberger, V. Kiessling, L.K. Tamm, and R. Jahn. 2014. Variable cooperativity in SNARE-mediated membrane fusion. Proc. Natl. Acad. Sci. USA. 111:12037-12042. http://dx.doi.org/10.1073/pnas.1407435111
22. Hong, W., and S. Lev. 2014. Tethering the assembly of SNARE complexes. Trends Cell Biol. 24:35-43. http://dx.doi.org/10.1016/j.tcb.2013.09.006
23. Hoshino, D., K.C. Kirkbride, K. Costello, E.S. Clark, S. Sinha, N. Grega-Larson, M.J. Tyska, and A.M. Weaver. 2013. Exosome secretion is enhanced by invadopodia and drives invasive behavior. Cell Reports. 5:1159-1168. http://dx.doi.org/10.1016/j.celrep.2013.10.050
24. Hsu, C., Y. Morohashi, S. Yoshimura, N. Manrique-Hoyos, S. Jung, M.A. Lauterbach, M. Bakhti, M. Grønborg, W. Möbius, J. Rhee, et al, 2010. Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J. Cell Biol. 189:223-232. http://dx.doi.org/10.1083/jcb.200911018
25. Hyenne, V., T. Tremblay-Boudreault, R. Velmurugan, B.D. Grant, D. Loerke, and J.C. Labbé. 2012. RAB-5 controls the cortical organization and dynamics of PAR proteins to maintain C. elegans early embryonic polarity. PLoS ONE. 7:e35286. http://dx.doi.org/10.1371/journal.pone.0035286"
26. Jiang, H., J.Q. Luo, T. Urano, P. Frankel, Z. Lu, D.A. Foster, and L.A. Feig. 1995. Involvement of Ral GTPase in v-Src-induced phospholipase D activation. Nature. 378:409-412. http://dx.doi.org/10.1038/378409a0
27. Jiu, Y., C. Jin, Y Liu, C.I. Holmberg, and J. Jäntti. 2012. Exocyst subunits Exo70 and Exo84 cooperate with small GTPases to regulate behavior and endocytic trafficking in C. elegans. PLoS ONE. 7:e32077. http://dx.doi.org/10.1371/journal.pone.0032077
28. Kalra, H., R.J. Simpson, H. Ji, E. Aikawa, P. Altevogt, P. Askenase, V.C. Bond, F. E. Borràs, X. Breakefield, V. Budnik, et al. 2012. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol. 10:e1001450. http://dx.doi.org/10.1371/journal.pbio.1001450
29. Kamath, R.S., A.G. Fraser, Y. Dong, G. Poulin, R. Durbin, M. Gotta, A. Kanapin, N. Le Bot, S. Moreno, M. Sohrmann, et al. 2003. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature. 421:231-237. http://dx.doi.org/10.1038/nature01278
30. Kawato, M., R. Shirakawa, H. Kondo, T. Higashi, T. Ikeda, K. Okawa, S. Fukai, O. Nureki, T. Kita, and H. Horiuchi. 2008. Regulation of platelet dense granule secretion by the Ral GTPase-exocyst pathway. J. Biol. Chem. 283:166-174. http://dx.doi.org/10.1074/jbc.M705340200
31. Kim, D.K., B. Kang, O.Y. Kim, D.S. Choi, J. Lee, S.R. Kim, G. Go, Y.J. Yoon, J.H. Kim, S.C. Jang, et al. 2013. EVpedia: an integrated database of high-throughput data for systemic analyses of extracellular vesicles. J Extracell Vesicles. 2. http://dx.doi.org/10.3402/jev.v2i0.20384
32. Kinchen, J.M., K. Doukoumetzidis, J. Almendinger, L. Stergiou, A. Tosello-Trampont, C.D. Sifri, M.O. Hengartner, and K.S. Ravichandran. 2008. A pathway for phagosome maturation during engulfment of apoptotic cells. Nat. Cell Biol. 10:556-566. http://dx.doi.org/10.1038/ncb1718
33. Klumperman, J., and G. Raposo. 2014. The complex ultrastructure of the endolysosomal system. Cold Spring Harb. Perspect. Biol. 6:a016857. http://dx.doi.org/10.1101/cshperspect.a016857
34. Kolotuev, I., Y. Schwab, and M. Labouesse. 2010. A precise and rapid mapping protocol for correlative light and electron microscopy of small invertebrate organisms. Biol. Cell. 102:121-132. http://dx.doi.org/10.1042/BC20090096
35. Kowal, J., M. Tkach, and C. Théry. 2014. Biogenesis and secretion of exosomes. Curr Opin. Cell Biol. 29:116-125. http://dx.doi.org/10.1016/j.ceb.2014.05.004
36. Laulagnier, K., D. Grand, A. Dujardin, S. Hamdi, H. Vincent-Schneider, D. Lankar, J.P. Salles, C. Bonnerot, B. Perret, and M. Record. 2004. PLD2 is enriched on exosomes and its activity is correlated to the release of exosomes. FEBS Lett. 572:11-14. http://dx.doi.org/10.1016/j.febslet.2004.06.082
37. Liégeois, S., A. Benedetto, J.M. Garnier, Y. Schwab, and M. Labouesse. 2006. The V0-ATPase mediates apical secretion of exosomes containing Hedgehog-related proteins in Caenorhabditis elegans. J. Cell Biol. 173:949-961. http://dx.doi.org/10.1083/jcb.200511072
38. Lopez, J.A., E.P. Kwan, L. Xie, Y. He, D.E. James, and H.Y. Gaisano. 2008. The RalA GTPase is a central regulator of insulin exocytosis from pancreatic islet beta cells. J. Biol. Chem. 283:17939-17945. http://dx.doi.org/10.1074/jbc.M800321200
39. Luo, J.Q., X. Liu, P. Frankel, T. Rotunda, M. Ramos, J. Flom, H. Jiang, L.A. Feig, A.J. Morris, R.A. Kahn, and D.A. Foster. 1998. Functional association between Arf and RalA in active phospholipase D complex. Proc. Natl. Acad. Sci. USA. 95:3632-3637. http://dx.doi.org/10.1073/pnas.95.7.3632
40. Malsam, J., and T.H. Söllner. 2011. Organization of SNAREs within the Golgi stack. Cold Spring Harb. Perspect. Biol. 3:a005249. http://dx.doi.org/10.1101/cshperspect.a005249
41. Martell, J.D., T.J. Deerinck, Y. Sancak, T.L. Poulos, V.K. Mootha, G.E. Sosinsky, M.H. Ellisman, and A.Y. Ting. 2012. Engineered ascorbate peroxidase as a genetically encoded reporter for electron microscopy. Nat. Biotechnol. 30:1143-1148. http://dx.doi.org/10.1038/nbt.2375
42. Moskalenko, S., D.O. Henry, C. Rosse, G. Mirey, J.H. Camonis, and M.A. White. 2002. The exocyst is a Ral effector complex. Nat. Cell Biol. 4:66-72. http://dx.doi.org/10.1038/ncb728
43. Ohta, Y., N. Suzuki, S. Nakamura, J.H. Hartwig, and T.P. Stossel. 1999. The small GTPase RalA targets filamin to induce filopodia. Proc. Natl. Acad. Sci. USA. 96:2122-2128. http://dx.doi.org/10.1073/pnas.96.5.2122
44. Ostrowski, M., N.B. Carmo, S. Krumeich, I. Fanget, G. Raposo, A. Savina, C.F. Moita, K. Schauer, A.N. Hume, R.P. Freitas, et al., 2010. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 12:19-30, 1-13. http://dx.doi.org/10.1038/ncb200019966785
45. Page, A.P., and I.L. Johnstone. 2007. The cuticle. WormBook. 1-15.
46. Raposo, G., and W. Stoorvogel. 2013. Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol. 200:373-383. http://dx.doi.org/10.1083/jcb.201211138
47. Risselada, H.J., G. Bubnis, and H. Grubmüller. 2014. Expansion of the fusion stalk and its implication for biological membrane fusion. Proc. Natl. Acad. Sci. USA. 111:11043-11048. http://dx.doi.org/10.1073/pnas.1323221111
48. Savina, A., C.M. Fader, M.T. Damiani, and M.I. Colombo. 2005. Rab11 promotes docking and fusion of multivesicular bodies in a calcium-dependent manner. Traffic. 6:131-143. http://dx.doi.org/10.1111/j.1600-0854.2004.00257.x
49. Strauss, K., C. Goebel, H. Runz, W. Möbius, S. Weiss, I. Feussner, M. Simons, and A. Schneider. 2010. Exosome secretion ameliorates lysosomal storage of cholesterol in Niemann-Pick type C disease. J. Biol. Chem. 285:26279-26288. http://dx.doi.org/10.1074/jbc.M110.134775
50. Sugihara, K., S. Asano, K. Tanaka, A. Iwamatsu, K. Okawa, and Y. Ohta. 2002. The exocyst complex binds the small GTPase RalA to mediate filopodia formation. Nat. Cell Biol. 4:73-78. http://dx.doi.org/10.1038/ncb720
51. Tamai, K., N. Tanaka, T. Nakano, E. Kakazu, Y. Kondo, J. Inoue, M. Shiina, K. Fukushima, T. Hoshino, K. Sano, et al. 2010. Exosome secretion of dendritic cells is regulated by Hrs, an ESCRT-0 protein. Biochem. Biophys. Res. Commun. 399:384-390. http://dx.doi.org/10.1016/j.bbrc.2010.07.083
52. Trajkovic, K., C. Hsu, S. Chiantia, L. Rajendran, D. Wenzel, F. Wieland, P. Schwille, B. Brügger, and M. Simons. 2008. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 319:1244-1247. http://dx.doi.org/10.1126/science.1153124
53. Vitale, N., J. Mawet, J. Camonis, R. Regazzi, M.F. Bader, and S. Chasserot-Golaz. 2005. The Small GTPase RalA controls exocytosis of large dense core secretory granules by interacting with ARF6-dependent phospholipase D1. J. Biol. Chem. 280:29921-29928. http://dx.doi.org/10.1074/jbc.M413748200
54. Xu, Y., F. Zhang, Z. Su, J.A. McNew, and YK. Shin. 2005. Hemifusion in SNA RE-mediated membrane fusion. Nat. Struct. Mol. Biol. 12:417-422. http://dx.doi.org/10.1038/nsmb921