Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity

Molecular and Cellular Neuroscience

Volumn 46, Issue 2, 2011, Pages 409-418

  Lachenal, Gaelle ^a,b   Pernet Gallay, Karin ^a,b   Chivet, Mathilde ^a,b   Hemming, Fiona J ^a,b   Belly, Agnès ^a,b   Bodon, Gilles ^a,b   Blot, Béatrice ^a,b   Haase, Georg ^c   Goldberg, Yves ^a,b   Sadoul, Rémy ^a,b  

^a GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^b UNIV GRENOBLE ALPES   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Exosomes; Multivesicular bodies; Synaptic activity; Tetanus toxin

Indexed keywords

RNA; TETANUS TOXIN;

ARTICLE; BRAIN CELL; CELL MEMBRANE; ELECTRON MICROSCOPY; ENDOCYTOSIS; EXOSOME; MULTIVESICULAR BODY; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM; PRIORITY JOURNAL; SYNAPSE;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; EXOSOMES; GLUTAMINE; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONS; RATS; SYNAPSES;

EID: 78751703517     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2010.11.004     Document Type: Article

References (53)

1. Aguzzi A., Rajendran L. The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 2009, 64:783-790.
2. Arantes R.M., Andrews N.W. A role for synaptotagmin VII-regulated exocytosis of lysosomes in neurite outgrowth from primary sympathetic neurons. J. Neurosci. 2006, 26:4630-4637.
3. Belting M., Wittrup A. Nanotubes, exosomes, and nucleic acid-binding peptides provide novel mechanisms of intercellular communication in eukaryotic cells: implications in health and disease. J. Cell Biol. 2008, 183:1187-1191.
4. Bianco F., Pravettoni E., Colombo A., Schenk U., Moller T., Matteoli M., Verderio C. Astrocyte-derived ATP induces vesicle shedding and IL-1 beta release from microglia. J. Immunol. 2005, 174:7268-7277.
5. Bianco F., Perrotta C., Novellino L., Francolini M., Riganti L., Menna E., Saglietti L., Schuchman E.H., Furlan R., Clementi E., Matteoli M., Verderio C. Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J. 2009, 28:1043-1054.
6. Bordet T., Castelnau-Ptakhine L., Fauchereau F., Friocourt G., Kahn A., Haase G. Neuronal targeting of cardiotrophin-1 by coupling with tetanus toxin C fragment. Mol. Cell. Neurosci. 2001, 17:842-854.
7. Borgonovo B., Cocucci E., Racchetti G., Podini P., Bachi A., Meldolesi J. Regulated exocytosis: a novel, widely expressed system. Nat. Cell Biol. 2002, 4:955-962.
8. Chatellard-Causse C., Blot B., Cristina N., Torch S., Missotten M., Sadoul R. Alix (ALG-2-interacting protein X), a protein involved in apoptosis, binds to endophilins and induces cytoplasmic vacuolization. J. Biol. Chem. 2002, 277:29108-29115.
9. Chiappalone M., Bove M., Vato A., Tedesco M., Martinoia S. Dissociated cortical networks show spontaneously correlated activity patterns during in vitro development. Brain Res. 2006, 1093:41-53.
10. Cooney J.R., Hurlburt J.L., Selig D.K., Harris K.M., Fiala J.C. Endosomal compartments serve multiple hippocampal dendritic spines from a widespread rather than a local store of recycling membrane. J. Neurosci. 2002, 22:2215-2224.
11. Cordero-Erausquin M., Allard S., Dolique T., Bachand K., Ribeiro-da-Silva A., De Koninck Y. Dorsal horn neurons presynaptic to lamina I spinoparabrachial neurons revealed by transynaptic labeling. J. Comp. Neurol. 2009, 517:601-615.
12. Deinhardt K., Berninghausen O., Willison H.J., Hopkins C.R., Schiavo G. Tetanus toxin is internalized by a sequential clathrin-dependent mechanism initiated within lipid microdomains and independent of epsin1. J. Cell Biol. 2006, 174:459-471.
13. Fader C.M., Sanchez D., Furlan M., Colombo M.I. Induction of autophagy promotes fusion of multivesicular bodies with autophagic vacuoles in k562 cells. Traffic 2008, 9:230-250.
14. Faure J., Lachenal G., Court M., Hirrlinger J., Chatellard-Causse C., Blot B., Grange J., Schoehn G., Goldberg Y., Boyer V., Kirchhoff F., Raposo G., Garin J., Sadoul R. Exosomes are released by cultured cortical neurones. Mol. Cell. Neurosci. 2006, 31:642-648.
15. Fevrier B., Vilette D., Laude H., Raposo G. Exosomes: a bubble ride for prions?. Traffic 2005, 6:10-17.
16. Francis J.W., Bastia E., Matthews C.C., Parks D.A., Schwarzschild M.A., Brown R.H., Fishman P.S. Tetanus toxin fragment C as a vector to enhance delivery of proteins to the CNS. Brain Res. 2004, 1011:7-13.
17. Futter C.E., Pearse A., Hewlett L.J., Hopkins C.R. Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J. Cell Biol. 1996, 132:1011-1023.
18. Gerber S.H., Sudhof T.C. Molecular determinants of regulated exocytosis. Diabetes 2002, 51(Suppl 1):S3-S11.
19. Ghidoni R., Paterlini A., Albertini V., Glionna M., Monti E., Schiaffonati L., Benussi L., Levy E., Binetti G. Cystatin C is released in association with exosomes: a new tool of neuronal communication which is unbalanced in Alzheimer's disease. Neurobiol. Aging 2009.
20. Herreros J., Ng T., Schiavo G. Lipid rafts act as specialized domains for tetanus toxin binding and internalization into neurons. Mol. Biol. Cell 2001, 12:2947-2960.
21. Kennedy M.J., Ehlers M.D. Organelles and trafficking machinery for postsynaptic plasticity. Annu. Rev. Neurosci. 2006, 29:325-362.
22. Korkut C., Ataman B., Ramachandran P., Ashley J., Barria R., Gherbesi N., Budnik V. Trans-synaptic transmission of vesicular Wnt signals through Evi/Wntless. Cell 2009, 139:393-404.
23. Krämer-Albers E.M., Bretz N., Tenzer S., Winterstein C., Möbius W., Berger H., Nave K.A., Schild H., Trotter J. Oligodendrocutes secrete exosomes containing major myelin and stress-protective proteins: trophic suppor for axons?. Proteomics Clin. Appl. 2007, 1:1446-1461.
24. Maness P.F., Schachner M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat. Neurosci. 2007, 10:19-26.
25. Marzesco A.M., Janich P., Wilsch-Brauninger M., Dubreuil V., Langenfeld K., Corbeil D., Huttner W.B. Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J. Cell Sci. 2005, 118:2849-2858.
26. Maskos U., Kissa K., St Cloment C., Brulet P. Retrograde trans-synaptic transfer of green fluorescent protein allows the genetic mapping of neuronal circuits in transgenic mice. Proc. Natl Acad. Sci. USA 2002, 99:10120-10125.
27. Mathivanan S., Simpson R.J. ExoCarta: a compendium of exosomal proteins and RNA. Proteomics 2009, 9:4997-5000.
28. Morelli A.E., Larregina A.T., Shufesky W.J., Sullivan M.L., Stolz D.B., Papworth G.D., Zahorchak A.F., Logar A.J., Wang Z., Watkins S.C., Falo L.D., Thomson A.W. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 2004, 104:3257-3266.
29. Newpher T.M., Ehlers M.D. Glutamate receptor dynamics in dendritic microdomains. Neuron 2008, 58:472-497.
30. Ostrowski M., Carmo N.B., Krumeich S., Fanget I., Raposo G., Savina A., Moita C.F., Schauer K., Hume A.N., Freitas R.P., Goud B., Benaroch P., Hacohen N., Fukuda M., Desnos C., Seabra M.C., Darchen F., Amigorena S., Moita L.F., Thery C. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 2010, 12:19-30. sup pp 11-13.
31. 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. 1985, 101:942-948.
32. Popov V.I., Medvedev N.I., Kraev I.V., Gabbott P.L., Davies H.A., Lynch M., Cowley T.R., Berezin V., Bock E., Stewart M.G. A cell adhesion molecule mimetic, FGL peptide, induces alterations in synapse and dendritic spine structure in the dentate gyrus of aged rats: a three-dimensional ultrastructural study. Eur. J. Neurosci. 2008, 27:301-314.
33. Potolicchio I., Carven G.J., Xu X., Stipp C., Riese R.J., Stern L.J., Santambrogio L. Proteomic analysis of microglia-derived exosomes: metabolic role of the aminopeptidase CD13 in neuropeptide catabolism. J. Immunol. 2005, 175:2237-2243.
34. Putz U., Howitt J., Lackovic J., Foot N., Kumar S., Silke J., Tan S.S. Nedd4 family-interacting protein 1 (Ndfip1) is required for the exosomal secretion of Nedd4 family proteins. J. Biol. Chem. 2008, 283:32621-32627.
35. Qu Y., Franchi L., Nunez G., Dubyak G.R. Nonclassical IL-1 beta secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J. Immunol. 2007, 179:1913-1925.
36. Qu Y., Ramachandra L., Mohr S., Franchi L., Harding C.V., Nunez G., Dubyak G.R. P2X7 receptor-stimulated secretion of MHC class II-containing exosomes requires the ASC/NLRP3 inflammasome but is independent of caspase-1. J. Immunol. 2009, 182:5052-5062.
37. Rind H.B., Butowt R., von Bartheld C.S. Synaptic targeting of retrogradely transported trophic factors in motoneurons: comparison of glial cell line-derived neurotrophic factor, brain-derived neurotrophic factor, and cardiotrophin-1 with tetanus toxin. J. Neurosci. 2005, 25:539-549.
38. Savina A., Fader C.M., Damiani M.T., Colombo M.I. Rab11 promotes docking and fusion of multivesicular bodies in a calcium-dependent manner. Traffic 2005, 6:131-143.
39. Simons M., Raposo G. Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 2009, 11:11.
40. Skog J., Wurdinger T., van Rijn S., Meijer D.H., Gainche L., Sena-Esteves M., Curry W.T., Carter B.S., Krichevsky A.M., Breakefield X.O. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 2008, 10:1470-1476.
41. Smalheiser N.R. Exosomal transfer of proteins and RNAs at synapses in the nervous system. Biol. Direct 2007, 2:35.
42. Taylor A.R., Robinson M.B., Gifondorwa D.J., Tytell M., Milligan C.E. Regulation of heat shock protein 70 release in astrocytes: role of signaling kinases. Dev. Neurobiol. 2007, 67:1815-1829.
43. + T cells by dendritic cell-derived exosomes. Nat. Immunol. 2002, 3:1156-1162.
44. Thery C., Ostrowski M., Segura E. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 2009, 9:581-593.
45. Tokuyasu K.T. Application of cryoultramicrotomy to immunocytochemistry. J. Microsc. 1986, 143:139-149.
46. Turrigiano G.G. The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 2008, 135:422-435.
47. Utvik J.K., Haglerod C., Mylonakou M.N., Holen T., Kropf M., Hirling H., Skare O., Laake P., Ottersen O.P., Haug F.M., Davanger S. Neuronal enriched endosomal protein of 21kDa colocalizes with glutamate receptor subunit GLUR2/3 at the postsynaptic membrane. Neuroscience 2009, 158:96-104.
48. Valadi H., Ekstrom K., Bossios A., Sjostrand M., Lee J.J., Lotvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007, 9:654-659.
49. Vella L.J., Greenwood D.L., Cappai R., Scheerlinck J.P., Hill A.F. Enrichment of prion protein in exosomes derived from ovine cerebral spinal fluid. Vet. Immunol. Immunopathol. 2008, 124:385-393.
50. Vella L.J., Sharples R.A., Nisbet R.M., Cappai R., Hill A.F. The role of exosomes in the processing of proteins associated with neurodegenerative diseases. Eur. Biophys. J. 2008, 37:323-332.
51. Vingtdeux V., Hamdane M., Loyens A., Gele P., Drobeck H., Begard S., Galas M.C., Delacourte A., Beauvillain J.C., Buee L., Sergeant N. Alkalizing drugs induce accumulation of amyloid precursor protein by-products in luminal vesicles of multivesicular bodies. J. Biol. Chem. 2007, 282:18197-18205.
52. Yap C.C., Wisco D., Kujala P., Lasiecka Z.M., Cannon J.T., Chang M.C., Hirling H., Klumperman J., Winckler B. The somatodendritic endosomal regulator NEEP21 facilitates axonal targeting of L1/NgCAM. J. Cell Biol. 2008, 180:827-842.
53. Zhang H.G., Liu C., Su K., Yu S., Zhang L., Zhang S., Wang J., Cao X., Grizzle W., Kimberly R.P. A membrane form of TNF-alpha presented by exosomes delays T cell activation-induced cell death. J. Immunol. 2006, 176:7385-7393.