Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis

Journal of Cell Science

Volumn 124, Issue 3, 2011, Pages 447-458

  Fitzner, Dirk ^a,b   Schnaars, Mareike ^a   Van Rossum, Denise ^b   Krishnamoorthy, Gurumoorthy ^c   Dibaj, Payam ^b   Bakhti, Mostafa ^a   Regen, Tommy ^b   Hanisch, Uwe Karsten ^b   Simons, Mikael ^a,b  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

Exosomes; Macropinocytosis; Microglia; Myelin; Oligodendrocytes

Indexed keywords

GAMMA INTERFERON; LIPOSOME; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PHOSPHATIDYLSERINE;

ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; CELL SUBPOPULATION; CONTROLLED STUDY; DEGRADATION; DOWN REGULATION; ENDOSOME; EXOSOME; INFLAMMATION; INTERNALIZATION; LYSOSOME; MACROPHAGE ACTIVATION; MACROPINOCYTOSIS; MEMBRANE VESICLE; MICROGLIA; MOUSE; NONHUMAN; OLIGODENDROGLIA; PINOCYTOSIS; PRIORITY JOURNAL; UPREGULATION;

ANIMALS; BIOLOGICAL TRANSPORT; EXOSOMES; GENES, MHC CLASS II; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; OLIGODENDROGLIA; PINOCYTOSIS; T-LYMPHOCYTES;

EID: 79551542416     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.074088     Document Type: Article

References (67)

1. Bettelli, E., Pagany, M., Weiner, H. L., Linington, C., Sobel, R. A. and Kuchroo, V. K. (2003). Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J. Exp. Med. 197, 1073-1081.
2. Beyer, M., Gimsa, U., Eyupoglu, I. Y., Hailer, N. P. and Nitsch, R. (2000). Phagocytosis of neuronal or glial debris by microglial cells: upregulation of MHC class II expression and multinuclear giant cell formation in vitro. Glia 31, 262-266.
3. Bhatnagar, S. and Schorey, J. S. (2007). Exosomes released from infected macrophages contain Mycobacterium avium glycopeptidolipids and are proinflammatory. J Biol. Chem. 282, 25779-25789.
4. Bianco, F., Perrotta, C., Novellino, L., Francolini, M., Riganti, L., Menna, E., Saglietti, L., Schuchman, E. H., Furlan, R., Clementi, E. et al. (2009). Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J. 28, 1043-1054.
5. Booth, A. M., Fang, Y., Fallon, J. K., Yang, J. M., Hildreth, J. E. and Gould, S. J. (2006). Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J. Cell Biol. 172, 923-935.
6. Cella, M., Engering, A., Pinet, V., Pieters, J. and Lanzavecchia, A. (1997). Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature 388, 782-787.
7. Cocucci, E., Racchetti, G. and Meldolesi, J. (2009). Shedding microvesicles: artefacts no more. Trends Cell Biol. 9, 43-51.
8. Cohen, G., Makranz, C., Spira, M., Kodama, T., Reichert, F. and Rotshenker, S. (2006). Non-PKC DAG/phorbol-ester receptor(s) inhibit complement receptor-3 and nPKC inhibit scavenger receptor-AI/II-mediated myelin phagocytosis but cPKC, PI3k, and PLCgamma activate myelin phagocytosis by both. Glia 53, 538-550.
9. Court, F. A., Hendriks, W. T., Macgillavry, H. D., Alvarez, J. and van Minnen, J. (2008). Schwann cell to axon transfer of ribosomes: toward a novel understanding of the role of glia in the nervous system. J. Neurosci. 28, 11024-11029.
10. Davalos, D., Grutzendler, J., Yang, G., Kim, J. V., Zuo, Y., Jung, S., Littman, D. R., Dustin, M. L. and Gan, W. B. (2005). ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 8, 752-758.
11. DeJong, B. A. and Smith, M. E. (1997). A role for complement in phagocytosis of myelin. Neurochem. Res. 22, 491-498.
12. Fevrier, B. and Raposo, G. (2004). Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr. Opin. Cell Biol. 16, 415-421. (Pubitemid 38903148)
13. Floden, A. M. and Combs, C. K. (2006). Beta-amyloid stimulates murine postnatal and adult microglia cultures in a unique manner. J. Neurosci. 26, 4644-4648.
14. Fomina, A. F., Deerinck, T. J., Ellisman, M. H. and Cahalan, M. D. (2003). Regulation of membrane trafficking and subcellular organization of endocytic compartments revealed with FM1-43 in resting and activated human T cells. Exp. Cell Res. 291, 150-166.
15. Garrett, W. S., Chen, L. M., Kroschewski, R., Ebersold, M., Turley, S., Trombetta, S., Galan, J. E. and Mellman, I. (2000). Developmental control of endocytosis in dendritic cells by Cdc42. Cell 102, 325-334.
16. Gaultier, A., Wu, X., Le Moan, N., Takimoto, S., Mukandala, G., Akassoglou, K., Campana, W. M. and Gonias, S. L. (2009). Low-density lipoprotein receptor-related protein 1 is an essential receptor for myelin phagocytosis. J. Cell Sci. 122, 1155-1162.
17. Gonzales, P. A., Pisitkun, T., Hoffert, J. D., Tchapyjnikov, D., Star, R. A., Kleta, R., Wang, N. S. and Knepper, M. A. (2009). Large-scale proteomics and phosphoproteomics of urinary exosomes. J. Am. Soc. Nephrol. 20, 363-379.
18. Gould, S. J., Booth, A. M. and Hildreth, J. E. (2003). The Trojan exosome hypothesis. Proc. Natl. Acad. Sci. USA 100, 10592-10597.
19. Hanisch, U. K. and Kettenmann, H. (2007). Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 10, 1387-1394.
20. Hanisch, U. K., Johnson, T. V. and Kipnis, J. (2008). Toll-like receptors: roles in neuroprotection? Trends Neurosci. 31, 176-182.
21. Hsu, C., Morohashi, Y., Yoshimura, S., Manrique-Hoyos, N., Jung, S., Lauterbach, M. A., Bakhti, M., Gronborg, M., Mobius, W., Rhee, J. et al. (2010). Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J. Cell Biol. 189, 223-232.
22. Jung, S., Aliberti, J., Graemmel, P., Sunshine, M. J., Kreutzberg, G. W., Sher, A. and Littman, D. R. (2000). Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 20, 4106-4114.
23. Keller, S., Rupp, C., Stoeck, A., Runz, S., Fogel, M., Lugert, S., Hager, H. D., Abdel-Bakky, M. S., Gutwein, P. and Altevogt, P. (2007). CD24 is a marker of exosomes secreted into urine and amniotic fluid. Kidney Int. 72, 1095-1102.
24. Kerr, M. C. and Teasdale, R. D. (2009). Defining macropinocytosis. Traffic 10, 364-371.
25. Koenigsknecht, J. and Landreth, G. (2004). Microglial phagocytosis of fibrillar beta-amyloid through a beta1 integrin-dependent mechanism. J. Neurosci. 24, 9838-9846.
26. Krämer-Albers, E.M., Bretz, N., Tenzer, S., Winterstein, C., Möbius, W., Berger, H., Nave, K.A., Schild, H. and Trotter J. (2007). Oligodendrocytes secrete exosomes containing major myelin and stress-protective proteins: Trophic support for axons? Proteomics Clin. Appl. 1, 1446-1461.
27. Kreutzberg, G. W. (1996). Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19, 312-318.
28. Krishnamoorthy, G., Lassmann, H., Wekerle, H. and Holz, A. (2006). Spontaneous opticospinal encephalomyelitis in a double-transgenic mouse model of autoimmune T cell/B cell cooperation. J. Clin. Invest. 116, 2385-2392.
29. Laulagnier, K., Motta, C., Hamdi. S., Roy. S., Fauvelle, F., Pageaux, J. F., Kobayashi, T., Salles, J. P., Perret, B., Bonnerot, C. et al. (2004). Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem. J. 380,161-171.
30. Lehnardt, S., Schott, E., Trimbuch, T., Laubisch, D., Krueger, C., Wulczyn, G., Nitsch, R. and Weber, J. R. (2008). A vicious cycle involving release of heat shock protein 60 from injured cells and activation of toll-like receptor 4 mediates neurodegeneration in the CNS. J. Neurosci. 28, 2320-2331.
31. Liu, Y., Walter, S., Stagi, M., Cherny, D., Letiembre, M., Schulz-Schaeffer, W., Heine, H., Penke, B., Neumann, H. and Fassbender, K. (2005). LPS receptor (CD14): a receptor for phagocytosis of Alzheimer's amyloid peptide. Brain 128, 1778-1789.
32. Liu, Y., Hao, W., Letiembre, M., Walter, S., Kulanga, M., Neumann, H. and Fassbender, K. (2006). Suppression of microglial inflammatory activity by myelin phagocytosis: role of p47-PHOX-mediated generation of reactive oxygen species. J. Neurosci. 26, 12904-12913. (Pubitemid 44954610)
33. Magnus, T., Chan, A., Grauer, O., Toyka, K. V. and Gold, R. (2001). Microglial phagocytosis of apoptotic inflammatory T cells leads to down-regulation of microglial immune activation. J. Immunol. 167, 5004-5010.
34. Mandrekar, S., Jiang, Q., Lee, C. Y., Koenigsknecht-Talboo, J., Holtzman, D. M. and Landreth, G. E. (2009). Microglia mediate the clearance of soluble Abeta through fluid phase macropinocytosis. J. Neurosci. 29, 4252-4262.
35. Mercer, J. and Helenius, A. (2008). Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320, 531-535.
36. Mercer, J. and Helenius, A. (2009). Virus entry by macropinocytosis. Nat. Cell Biol. 11, 510-520.
37. Miyanishi, M., Tada, K., Koike, M., Uchiyama, Y., Kitamura, T. and Nagata, S. (2007). Identification of Tim4 as a phosphatidylserine receptor. Nature 450, 435-439.
38. 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. et al. (2004). Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 104, 3257-3266.
39. Mui, B., Chow, L. and Hope, M. J. (2003). Extrusion technique to generate liposomes of defined size. Methods Enzymol. 367, 3-14.
40. Napoli, I. and Neumann, H. (2009). Microglial clearance function in health and disease. Neuroscience 158, 1030-1038.
41. Nimmerjahn, A., Kirchhoff, F. and Helmchen, F. (2005). Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308, 1314-1318. (Pubitemid 40746128)
42. Ostrowski, M., Carmo, N. B., Krumeich, S., Fanget, I., Raposo, G., Savina, A., Moita, C. F., Schauer, K., Hume, A. N., Freitas, R. P. et al. (2010). Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 12, 19-30.
43. Pan, B. T. and Johnstone, R. (1984). Selective externalization of the transferrin receptor by sheep reticulocytes in vitro. Response to ligands and inhibitors of endocytosis. J. Biol. Chem. 259, 9776-9782.
44. Pfeiffer, S. E., Warrington, A. E. and Bansal, R. (1993). The oligodendrocyte and its many cellular processes. Trends Cell Biol. 3, 191-197.
45. Pierre, P., Turley, S. J., Gatti, E., Hull, M., Meltzer, J., Mirza, A., Inaba, K., Steinman, R. M. and Mellman, I. (1997). Developmental regulation of MHC class II transport in mouse dendritic cells. Nature 388, 787-792. (Pubitemid 27375159)
46. Raposo, G., Nijman, H. W., Stoorvogel, W., Liejendekker, R., Harding, C. V., Melief, C. J. and Geuze, H. J. (1996). B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 183, 1161-1172.
47. Ravichandran, K. S. and Lorenz, U. (2007). Engulfment of apoptotic cells: signals for a good meal. Nat. Rev. Immunol. 7, 964-974.
48. Reichert, F. and Rotshenker, S. (2003). Complement-receptor-3 and scavenger-receptor-AI/II mediated myelin phagocytosis in microglia and macrophages. Neurobiol. Dis. 12, 65-72.
49. Sallusto, F., Cella, M., Danieli, C. and Lanzavecchia, A. (1995). Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J. Exp. Med. 182, 389-400.
50. Savina, A. and Amigorena, S. (2007). Phagocytosis and antigen presentation in dendritic cells. Immunol. Rev. 219, 143-156.
51. Schorey, J. S. and Bhatnagar, S. (2008). Exosome function: from tumor immunology to pathogen biology. Traffic 9, 871-881.
52. Simons, M. and Raposo, G. (2009). Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 21, 575-581.
53. Smith, M. E. (2001). Phagocytic properties of microglia in vitro: implications for a role in multiple sclerosis and EAE. Microsc. Res. Tech. 54, 81-94.
54. Sospedra, M. and Martin, R. (2005). Immunology of multiple sclerosis. Annu. Rev. Immunol. 23, 683-747.
55. Steinman, L. (2001). Multiple sclerosis: a two-stage disease. Nat. Immunol. 2, 762-764.
56. Thery, C., Ostrowski, M. and Segura, E. (2009). Membrane vesicles as conveyors of immune responses. Nat. Rev Immunol. 9, 581-593.
57. Tian, T., Wang, Y., Wang, H., Zhu, Z. and Xiao, Z. (2010). Visualizing of the cellular uptake and intracellular trafficking of exosomes by live-cell microscopy. J. Cell. Biochem. 111, 488-496.
58. Trajkovic, K., Dhaunchak, A. S., Goncalves, J. T., Wenzel, D., Schneider, A., Bunt, G., Nave, K. A. and Simons, M. (2006). Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites. J. Cell Biol. 172, 937-948.
59. Trajkovic, K., Hsu, C., Chiantia, S., Rajendran, L., Wenzel, D., Wieland, F., Schwille, P., Brugger, B. and Simons, M. (2008). Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319, 1244-1247. (Pubitemid 351323020)
60. van Niel, G., Porto-Carreiro, I., Simoes, S. and Raposo, G. (2006). Exosomes: a common pathway for a specialized function. J. Biochem. 140, 13-21.
61. van Rossum, D., Hilbert, S., Strassenburg, S., Hanisch, U. K. and Bruck, W. (2008). Myelin-phagocytosing macrophages in isolated sciatic and optic nerves reveal a unique reactive phenotype. Glia 56, 271-283.
62. Wake, H., Moorhouse, A. J., Jinno, S., Kohsaka, S. and Nabekura, J. (2009). Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 29, 3974-3980.
63. Walker, J. D., Maier, C. L. and Pober, J. S. (2009). Cytomegalovirus- infected human endothelial cells can stimulate allogeneic CD4+ memory T cells by releasing antigenic exosomes. J. Immunol. 182, 1548-1559.
64. Weiner, H. L. (2004). Multiple sclerosis is an inflammatory T-cell-mediated autoimmune disease. Arch. Neurol. 61, 1613-1615. (Pubitemid 39350279)
65. West, M. A., Prescott, A. R., Eskelinen, E. L., Ridley, A. J. and Watts, C. (2000). Rac is required for constitutive macropinocytosis by dendritic cells but does not control its downregulation. Curr. Biol. 10, 839-848.
66. Zeelenberg, I. S., Ostrowski, M., Krumeich, S., Bobrie, A., Jancic, C., Boissonnas, A., Delcayre, A., Le Pecq, J. B., Combadiere, B., Amigorena, S. et al. (2008). Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses. Cancer Res. 68, 1228-1235. (Pubitemid 351272243)
67. Zitvogel, L., Regnault, A., Lozier, A., Wolfers, J., Flament, C., Tenza, D., Ricciardi-Castagnoli, P., Raposo, G. and Amigorena, S. (1998). Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat. Med. 4, 594-600.