Exosomes and nanotubes: Control of immune cell communication

International Journal of Biochemistry and Cell Biology

Volumn 71, Issue , 2016, Pages 44-54

  McCoy Simandle, Kessler ^a   Hanna, Samer J ^a   Cox, Dianne ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Cell cell communication; Exosomes; Multivesicular bodies; Tunneling nanotubes

Indexed keywords

NANOTUBE;

ANTIGEN PRESENTATION; BIOGENESIS; CELL COMMUNICATION; CELL ORGANELLE; CHEMICAL STRUCTURE; EXOSOME; GENE EXPRESSION; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IN VITRO STUDY; MEMBRANE VESICLE; REVIEW; SIGNAL TRANSDUCTION; HUMAN; IMMUNOLOGY; METABOLISM;

CELL COMMUNICATION; EXOSOMES; HUMANS;

EID: 84952012402     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2015.12.006     Document Type: Review

References (109)

1. S. Abounit, and C. Zurzolo Wiring through tunneling nanotubes - from electrical signals to organelle transfer J Cell Sci 125 2012 1089 1098
2. C. Admyre, S.M. Johansson, S. Paulie, and S. Gabrielsson Direct exosome stimulation of peripheral human T cells detected by ELISPOT Eur J Immunol 36 2006 1772 1781
3. M. Alexander, R. Hu, M.C. Runtsch, D.A. Kagele, T.L. Mosbruger, and et al. Exosome-delivered microRNAs modulate the inflammatory response to endotoxin Nat Commun 6 2015 7321
4. G. Andreola, L. Rivoltini, C. Castelli, V. Huber, P. Perego, and et al. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles J Exp Med 195 2002 1303 1316
5. P.D. Arkwright, F. Luchetti, J. Tour, C. Roberts, R. Ayub, and et al. Fas stimulation of T lymphocytes promotes rapid intercellular exchange of death signals via membrane nanotubes Cell Res 20 2010 72 88
6. P.Y. Arnold, and M.D. Mannie Vesicles bearing MHC class II molecules mediate transfer of antigen from antigen-presenting cells to CD4+ T cells Eur J Immunol 29 1999 1363 1373
7. M. Babst A protein's final ESCRT Traffic 6 2005 2 9
8. P. Bedford, K. Garner, and S.C. Knight MHC class II molecules transferred between allogeneic dendritic cells stimulate primary mixed leukocyte reactions Int Immunol 11 1999 1739 1744
9. S. Bhatnagar, and J.S. Schorey Exosomes released from infected macrophages contain Mycobacterium avium glycopeptidolipids and are proinflammatory J Biol Chem 282 2007 25779 25789
10. N. Blanchard, D. Lankar, F. Faure, A. Regnault, C. Dumont, and et al. TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/zeta complex J Immunol 168 2002 3235 3241
11. E.J. Blott, and G.M. Griffiths Secretory lysosomes Nature Rev Mol Cell Biol 3 2002 122 131
12. M. Boudsocq, M.R. Willmann, M. McCormack, H. Lee, L. Shan, and et al. Differential innate immune signalling via Ca(2+) sensor protein kinases Nature 464 2010 418 422
13. S.I. Buschow, J.M. Liefhebber, R. Wubbolts, and W. Stoorvogel Exosomes contain ubiquitinated proteins Blood Cells Mol Dis 35 2005 398 403
14. S.I. Buschow, E.N. Nolte-'t Hoen, G. van Niel, M.S. Pols, T. ten Broeke, and et al. MHC II in dendritic cells is targeted to lysosomes or T cell-induced exosomes via distinct multivesicular body pathways Traffic 10 2009 1528 1542
15. T. Carandini, F. Colombo, A. Finardi, G. Casella, L. Garzetti, and et al. Microvesicles: What is the Role in Multiple Sclerosis? Front Neurol 6 2015 111
16. A. Chauveau, A. Aucher, P. Eissmann, E. Vivier, and D.M. Davis Membrane nanotubes facilitate long-distance interactions between natural killer cells and target cells Pro Natl Acad Sci U S A 107 2010 5545 5550
17. A. Clayton, J. Court, H. Navabi, M. Adams, M.D. Mason, and et al. Analysis of antigen presenting cell derived exosomes, based on immuno-magnetic isolation and flow cytometry J Immunol Methods 247 2001 163 174
18. A. Clayton, J.P. Mitchell, J. Court, S. Linnane, M.D. Mason, and Z. Tabi Human tumor-derived exosomes down-modulate NKG2D expression J Immunol 180 2008 7249 7258
19. A. Clayton, J.P. Mitchell, J. Court, M.D. Mason, and Z. Tabi Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2 Cancer Res 67 2007 7458 7466
20. J. Conde-Vancells, E. Rodriguez-Suarez, N. Embade, D. Gil, R. Matthiesen, and et al. Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes J Proteome Res 7 2008 5157 5166
21. D.M. Davis, and M.L. Dustin What is the importance of the immunological synapse? Trends Immunol 25 2004 323 327
22. D.M. Davis, and S. Sowinski Membrane nanotubes: dynamic long-distance connections between animal cells Nature Rev Mol Cell Biol 9 2008 431 436
23. J.Q. Davis, D. Dansereau, R.M. Johnstone, and V. Bennett Selective externalization of an ATP-binding protein structurally related to the clathrin-uncoating ATPase/heat shock protein in vesicles containing terminal transferrin receptors during reticulocyte maturation J Biol Chem 261 1986 15368 15371
24. J.M. Escola, M.J. Kleijmeer, W. Stoorvogel, J.M. Griffith, O. Yoshie, and H.J. Geuze Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes J Biol Chem 273 1998 20121 20127
25. E.A. Eugenin, P.J. Gaskill, and J.W. Berman Tunneling nanotubes (TNT): A potential mechanism for intercellular HIV trafficking Commun Integr Biol 2 2009 243 244
26. S. Feske Calcium signalling in lymphocyte activation and disease Nat Rev Immunol 7 2007 690 702
27. B. Fevrier, and G. Raposo Exosomes: endosomal-derived vesicles shipping extracellular messages Curr Opin Cell Biol 16 2004 415 421
28. S.I. Galkina, V.I. Stadnichuk, J.G. Molotkovsky, J.M. Romanova, G.F. Sud'ina, and T. Klein Microbial alkaloid staurosporine induces formation of nanometer-wide membrane tubular extensions (cytonemes, membrane tethers) in human neutrophils Cell Adh Migr 4 2010 32 38
29. K. Gousset, and C. Zurzolo Tunnelling nanotubes: a highway for prion spreading? Prion 3 2009 94 98
30. J. Gruenberg, and F.R. Maxfield Membrane transport in the endocytic pathway Curr Opin Cell Biol 7 1995 552 563
31. N. Gupta, and A.L. DeFranco Visualizing lipid raft dynamics and early signaling events during antigen receptor-mediated B-lymphocyte activation Mol Biol Cell 14 2003 432 444
32. C. Harding, J. Heuser, and P. Stahl Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes J Cell Biology 97 1983 329 339
33. K. Hase, S. Kimura, H. Takatsu, M. Ohmae, S. Kawano, and et al. M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex Nature Cell Biol 11 2009 1427 1432
34. L. Hicke A new ticket for entry into budding vesicles-ubiquitin Cell 106 2001 527 530
35. J.L. Hood, H. Pan, G.M. Lanza, and S.A. Wickline Consortium for Translational Research in Advanced I, Nanomedicine. 2009. Paracrine induction of endothelium by tumor exosomes Lab Invest 89 2009 1317 1328
36. V. Huber, S. Fais, M. Iero, L. Lugini, P. Canese, and et al. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape Gastroenterology 128 2005 1796 1804
37. T.B. Huffaker, R. Hu, M.C. Runtsch, E. Bake, X. Chen, and et al. Epistasis between microRNAs 155 and 146a during T cell-mediated antitumor immunity Cell Rep 2 2012 1697 1709
38. R.M. Johnstone, M. Adam, J.R. Hammond, L. Orr, and C. Turbide Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes) J Biol Chem 262 1987 9412 9420
39. I. Kadiu, and H.E. Gendelman Macrophage bridging conduit trafficking of HIV-1 through the endoplasmic reticulum and Golgi network J Proteome Res 10 2011 3225 3238
40. D.J. Katzmann, M. Babst, and S.D. Emr Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I Cell 106 2001 145 155
41. S. Kimura, K. Hase, and H. Ohno The molecular basis of induction and formation of tunneling nanotubes Cell Tissue Res 352 2013 67 76
42. M.J. Kleijmeer, G. Raposo, and H.J. Geuze Characterization of MHC Class II Compartments by Immunoelectron Microscopy Methods 10 1996 191 207
43. S.C. Knight, S. Iqball, M.S. Roberts, S. Macatonia, and P.A. Bedford Transfer of antigen between dendritic cells in the stimulation of primary T cell proliferation Eur J Immunol 28 1998 1636 1644
44. S. Lachambre, C. Chopard, and B. Beaumelle Preliminary characterisation of nanotubes connecting T-cells and their use by HIV-1 Biol Cell 106 2014 394 404
45. C. Liu, S. Yu, K. Zinn, J. Wang, L. Zhang, and et al. Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function J Immunol 176 2006 1375 1385
46. J. Lotvall, A.F. Hill, F. Hochberg, E.I. Buzas, D. Di Vizio, and et al. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles J Extracell Vesicles 3 2014 26913
47. L. Marzo, K. Gousset, and C. Zurzolo Multifaceted roles of tunneling nanotubes in intercellular communication Front Physiol 3 2012 72
48. S. Mathivanan, and R.J. Simpson ExoCarta: A compendium of exosomal proteins and RNA Proteomics 9 2009 4997 5000
49. X. Michelet, A. Djeddi, and R. Legouis Developmental and cellular functions of the ESCRT machinery in pluricellular organisms Biol Cell 102 2010 191 202
50. M. Mineo, S.H. Garfield, S. Taverna, A. Flugy, G. De Leo, and et al. Exosomes released by K562 chronic myeloid leukemia cells promote angiogenesis in a Src-dependent fashion Angiogenesis 15 2012 33 45
51. M. Mittelbrunn, C. Gutierrez-Vazquez, C. Villarroya-Beltri, S. Gonzalez, F. Sanchez-Cabo, and et al. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells Nat Commun 2 2011 282
52. A. Montecalvo, A.T. Larregina, W.J. Shufesky, D.B. Stolz, M.L. Sullivan, and et al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes Blood 119 2012 756 766
53. A. Montecalvo, W.J. Shufesky, D.B. Stolz, M.G. Sullivan, Z. Wang, and et al. Exosomes as a short-range mechanism to spread alloantigen between dendritic cells during T cell allorecognition J Immunol 180 2008 3081 3090
54. J. Mukerji, K.C. Olivieri, V. Misra, K.A. Agopian, and D. Gabuzda Proteomic analysis of HIV-1 Nef cellular binding partners reveals a role for exocyst complex proteins in mediating enhancement of intercellular nanotube formation Retrovirology 9 2012 33
55. A. Muntasell, A.C. Berger, and P.A. Roche T cell-induced secretion of MHC class II-peptide complexes on B cell exosomes EMBO J 26 2007 4263 4272
56. D.S. Nikolic, M. Lehmann, R. Felts, E. Garcia, F.P. Blanchet, and et al. HIV-1 activates Cdc42 and induces membrane extensions in immature dendritic cells to facilitate cell-to-cell virus propagation Blood 118 2011 4841 4852
57. C. Nobile, D. Rudnicka, M. Hasan, N. Aulner, F. Porrot, and et al. HIV-1 Nef inhibits ruffles, induces filopodia, and modulates migration of infected lymphocytes J Virol 84 2010 2282 2293
58. E.N. Nolte-'t Hoen, S.I. Buschow, S.M. Anderton, W. Stoorvogel, and M.H. Wauben Activated T cells recruit exosomes secreted by dendritic cells via LFA-1 Blood 113 2009 1977 1981
59. S. Nourshargh, and R. Alon Leukocyte migration into inflamed tissues Immunity 41 2014 694 707
60. R.M. O'Connell, K.D. Taganov, M.P. Boldin, G. Cheng, and D. Baltimore MicroRNA-155 is induced during the macrophage inflammatory response Proc Natl Acad Sci U S A 104 2007 1604 1609
61. B. Onfelt, S. Nedvetzki, R.K. Benninger, M.A. Purbhoo, S. Sowinski, and et al. Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria J Immunol 177 2006 8476 8483
62. B. Onfelt, S. Nedvetzki, K. Yanagi, and D.M. Davis Cutting edge: Membrane nanotubes connect immune cells J Immunol 173 2004 1511 1513
63. B.T. Pan, K. Teng, C. Wu, M. Adam, and R.M. Johnstone Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes J Cell Biology 101 1985 942 948
64. D.M. Patel, P.Y. Arnold, G.A. White, J.P. Nardella, and M.D. Mannie Class II MHC/peptide complexes are released from APC and are acquired by T cell responders during specific antigen recognition J Immunol 163 1999 5201 5210
65. D.M. Pegtel, K. Cosmopoulos, D.A. Thorley-Lawson, M.A. van Eijndhoven, E.S. Hopmans, and et al. Functional delivery of viral miRNAs via exosomes Proc Natl Acad Sci U S A 107 2010 6328 6333
66. R. Polak, B. de Rooij, R. Pieters, and M.L. den Boer B-cell precursor acute lymphoblastic leukemia cells use tunneling nanotubes to orchestrate their microenvironment Blood 2015
67. N. Rainy, D. Chetrit, V. Rouger, H. Vernitsky, O. Rechavi, and et al. H-Ras transfers from B to T cells via tunneling nanotubes Cell Death Dis 4 2013 e726
68. G. Raposo, H.W. Nijman, W. Stoorvogel, R. Liejendekker, C.V. Harding, and et al. B lymphocytes secrete antigen-presenting vesicles The J Exp Med 183 1996 1161 1172
69. G. Raposo, and W. Stoorvogel Extracellular vesicles: exosomes, microvesicles, and friends J Cell Biology 200 2013 373 383
70. G. Raposo, D. Tenza, S. Mecheri, R. Peronet, C. Bonnerot, and C. Desaymard Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation Mol Biol Cell 8 1997 2631 2645
71. J. Ratajczak, M. Wysoczynski, F. Hayek, A. Janowska-Wieczorek, and M.Z. Ratajczak Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication Leukemia 20 2006 1487 1495
72. C.R. Rinaldo HIV-1 Trans Infection of CD4(+) T Cells by Professional Antigen Presenting Cells Scientifica 2013 2013 164203
73. G.G. Romagnoli, B.B. Zelante, P.A. Toniolo, I.K. Migliori, and J.A. Barbuto Dendritic Cell-Derived Exosomes may be a Tool for Cancer Immunotherapy by Converting Tumor Cells into Immunogenic Targets Front Immunol 5 2014 692
74. A. Rustom, R. Saffrich, I. Markovic, P. Walther, and H.H. Gerdes Nanotubular highways for intercellular organelle transport Science 303 2004 1007 1010
75. J.C. Saez, V.M. Berthoud, M.C. Branes, A.D. Martinez, and E.C. Beyer Plasma membrane channels formed by connexins: their regulation and functions Physiol Rev 83 2003 1359 1400
76. R.D. Salter, and S.C. Watkins Dynamic properties of antigen uptake and communication between dendritic cells Immunol Res 36 2006 211 220
77. C. Schiller, K.N. Diakopoulos, I. Rohwedder, E. Kremmer, C. von Toerne, and et al. LST1 promotes the assembly of a molecular machinery responsible for tunneling nanotube formation J Cell Sci 126 2013 767 777
78. E. Segura, C. Guerin, N. Hogg, S. Amigorena, and C. Thery CD8+ dendritic cells use LFA-1 to capture MHC-peptide complexes from exosomes in vivo J Immunol 179 2007 1489 1496
79. J.M. Silverman, J. Clos, E. Horakova, A.Y. Wang, M. Wiesgigl, and et al. Leishmania exosomes modulate innate and adaptive immune responses through effects on monocytes and dendritic cells J Immunol 185 2010 5011 5022
80. S. Sowinski, J.M. Alakoskela, C. Jolly, and D.M. Davis Optimized methods for imaging membrane nanotubes between T cells and trafficking of HIV-1 Methods 53 2011 27 33
81. S. Sowinski, C. Jolly, O. Berninghausen, M.A. Purbhoo, A. Chauveau, and et al. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission Nature Cell Biol 10 2008 211 219
82. P. Sundd, E. Gutierrez, E.K. Koltsova, Y. Kuwano, S. Fukuda, and et al. 'Slings' enable neutrophil rolling at high shear Nature 488 2012 399 403
83. D.D. Taylor, C. Gercel-Taylor, K.S. Lyons, J. Stanson, and T.L. Whiteside T-cell apoptosis and suppression of T-cell receptor/CD3-zeta by Fas ligand-containing membrane vesicles shed from ovarian tumors Clin Cancer Res 9 2003 5113 5119
84. V. Thayanithy, E.L. Dickson, C. Steer, S. Subramanian, and E. Lou Tumor-stromal cross talk: direct cell-to-cell transfer of oncogenic microRNAs via tunneling nanotubes Transl Res 164 2014 359 365
85. C. Thery, S. Amigorena, G. Raposo, and A. Clayton Isolation and characterization of exosomes from cell culture supernatants and biological fluids Curr Protoc Cell Biol Chapter 3: Unit 3 2006 22
86. C. Thery, M. Boussac, P. Veron, P. Ricciardi-Castagnoli, G. Raposo, and et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles J Immunol 166 2001 7309 7318
87. C. Thery, L. Duban, E. Segura, P. Veron, O. Lantz, and S. Amigorena Indirect activation of naive CD4+ T cells by dendritic cell-derived exosomes Nat Immunol 3 2002 1156 1162
88. C. Thery, M. Ostrowski, and E. Segura Membrane vesicles as conveyors of immune responses Nat Rev Immunol 9 2009 581 593
89. C. Thery, A. Regnault, J. Garin, J. Wolfers, L. Zitvogel, and et al. Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73 J Cell Biology 147 1999 599 610
90. T. Tian, Y. Wang, H. Wang, Z. Zhu, and Z. Xiao Visualizing of the cellular uptake and intracellular trafficking of exosomes by live-cell microscopy J Cell Biochem 111 2010 488 496
91. M.L. Turner, F.M. Schnorfeil, and T. Brocker MicroRNAs regulate dendritic cell differentiation and function J Immunol 187 2011 3911 3917
92. H. Valadi, K. Ekstrom, A. Bossios, M. Sjostrand, J.J. Lee, and J.O. Lotvall Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells Nature Cell Biol 9 2007 654 659
93. H. Vallhov, C. Gutzeit, K. Hultenby, R. Valenta, H. Gronlund, and A. Scheynius Dendritic cell-derived exosomes carry the major cat allergen Fel d 1 and induce an allergic immune response Allergy 2015
94. B. van Deurs, P.K. Holm, L. Kayser, K. Sandvig, and S.H. Hansen Multivesicular bodies in HEp-2 cells are maturing endosomes EJCB 61 1993 208 224
95. N. Van Prooyen, H. Gold, V. Andresen, O. Schwartz, K. Jones, and et al. Human T-cell leukemia virus type 1 p8 protein increases cellular conduits and virus transmission Proc Natl Acad Sci U S A 107 2010 20738 20743
96. P. Veranic, M. Lokar, G.J. Schutz, J. Weghuber, S. Wieser, and et al. Different types of cell-to-cell connections mediated by nanotubular structures Biophys J 95 2008 4416 4425
97. E. Vigorito, S. Kohlhaas, D. Lu, and R. Leyland miR-155: an ancient regulator of the immune system Immunol Rev 253 2013 146 157
98. H. Vincent-Schneider, P. Stumptner-Cuvelette, D. Lankar, S. Pain, G. Raposo, and et al. Exosomes bearing HLA-DR1 molecules need dendritic cells to efficiently stimulate specific T cells Int Immunol 14 2002 713 722
99. J.D. Walker, C.L. Maier, and J.S. Pober Cytomegalovirus-infected human endothelial cells can stimulate allogeneic CD4+ memory T cells by releasing antigenic exosomes J Immunol 182 2009 1548 1559
100. X. Wang, and H.H. Gerdes Long-distance electrical coupling via tunneling nanotubes Biochim Biophys Acta 1818 2012 2082 2086
101. X. Wang, and H.H. Gerdes Transfer of mitochondria via tunneling nanotubes rescues apoptotic PC12 cells Cell Death Differ 22 2015 1181 1191
102. X. Wang, M.L. Veruki, N.V. Bukoreshtliev, E. Hartveit, and H.H. Gerdes Animal cells connected by nanotubes can be electrically coupled through interposed gap-junction channels Proc Natl Acad Sci U S A 107 2010 17194 17199
103. S.C. Watkins, and R.D. Salter Functional connectivity between immune cells mediated by tunneling nanotubules Immunity 23 2005 309 318
104. Y. Wei, M. Nazari-Jahantigh, L. Chan, M. Zhu, K. Heyll, and et al. The microRNA-342-5p fosters inflammatory macrophage activation through an Akt1- and microRNA-155-dependent pathway during atherosclerosis Circulation 127 2013 1609 1619
105. R. Wubbolts, R.S. Leckie, P.T. Veenhuizen, G. Schwarzmann, W. Mobius, and et al. Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation J Biol Chem 278 2003 10963 10972
106. W. Xu, P.A. Santini, J.S. Sullivan, B. He, M. Shan, and et al. HIV-1 evades virus-specific IgG2 and IgA responses by targeting systemic and intestinal B cells via long-range intercellular conduits Nat Immunol 10 2009 1008 1017
107. C.R. Zaccard, S.C. Watkins, P. Kalinski, R.J. Fecek, A.L. Yates, and et al. CD40L induces functional tunneling nanotube networks exclusively in dendritic cells programmed by mediators of type 1 immunity J Immunol 194 2015 1047 1056
108. J. Zhang, and Y. Zhang Membrane nanotubes: novel communication between distant cells Sci China Life Sci 56 2013 994 999
109. L. Zitvogel, A. Regnault, A. Lozier, J. Wolfers, C. Flament, and et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes Nat Med 4 1998 594 600