Exosomes and other microvesicles in infection biology: Organelles with unanticipated phenotypes

Cellular Microbiology

Volumn 13, Issue 1, 2011, Pages 1-9

  Silverman, Judith Maxwell ^a,b   Reiner, Neil E ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b VANCOUVER COASTAL HEALTH RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ASCOMYCETES; BASIDIOMYCETES; CELL ORGANELLE; CYTOSOL; EXOSOME; GRAM NEGATIVE BACTERIUM; INFECTION; KINETOPLAST; LEISHMANIA; MEMBRANE VESICLE; MOLECULAR MODEL; PARASITE; PHENOTYPE; PRIORITY JOURNAL; REVIEW;

ANIMALS; ASCOMYCOTA; BASIDIOMYCOTA; EXOSOMES; GRAM-NEGATIVE BACTERIA; KINETOPLASTIDA; MAMMALS; PHENOTYPE; VIRULENCE FACTORS;

ASCOMYCOTA; BASIDIOMYCOTA; EUKARYOTA; MAMMALIA; NEGIBACTERIA; PROKARYOTA;

EID: 78650265541     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01537.x     Document Type: Review

References (50)

1. Albuquerque, P.C., Nakayasu, E.S., Rodrigues, M.L., Frases, S., Casadevall, A., Zancope-Oliveira, R.M., et al. (2008) Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell Microbiol 10: 1695-1710.
2. Aline, F., Bout, D., Amigorena, S., Roingeard, P., and mier-Poisson, I. (2004) Toxoplasma gondii antigen-pulsed-dendritic cell-derived exosomes induce a protective immune response against T. gondii infection. Infect Immun 72: 4127-4137.
3. Beauvillain, C., Juste, M.O., Dion, S., Pierre, J., and mier-Poisson, I. (2009) Exosomes are an effective vaccine against congenital toxoplasmosis in mice. Vaccine 27: 1750-1757.
4. 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.
5. Bhatnagar, S., Shinagawa, K., Castellino, F.J., and Schorey, J.S. (2007) Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo. Blood 110: 3234-3244.
6. Bhattacharjee, S., van Ooij, C., Balu, B., Adams, J.H., and Haldar, K. (2008) Maurer's clefts of Plasmodium falciparum are secretory organelles that concentrate virulence protein reporters for delivery to the host erythrocyte. Blood 111: 2418-2426.
7. Brittingham, A., Morrison, C.J., McMaster, W.R., McGwire, B.S., Chang, K.P., and Mosser, D.M. (1995) Role of the Leishmania surface protease gp63 in complement fixation, cell adhesion, and resistance to complement-mediated lysis. J Immunol 155: 3102-3111.
8. Carvalho, L.P., Passos, S., Dutra, W.O., Soto, M., Alonso, C., Gollob, K.J., et al. (2005) Effect of LACK and KMP11 on IFN-gamma production by peripheral blood mononuclear cells from cutaneous and mucosal leishmaniasis patients. Scand J Immunol 61: 337-342.
9. Ellis, T.N., and Kuehn, M.J. (2010) Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol Rev 74: 81-94.
10. Escudier, B., Dorval, T., Chaput, N., Andre, F., Caby, M.P., Novault, S., et al. (2005) Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of thefirst phase I clinical trial. J Transl Med 3: 10.
11. Feng, D., Zhao, W.L., Ye, Y.Y., Bai, X.C., Liu, R.Q., Chang, L.F., et al. (2010) Cellular internalization of exosomes occurs through phagocytosis. Traffic 11: 675-687.
12. Fevrier, B., Vilette, D., Archer, F., Loew, D., Faigle, W., Vidal, M., et al. (2004) Cells release prions in association with exosomes. Proc Natl Acad Sci USA 101: 9683-9688.
13. Galka, F., Wai, S.N., Kusch, H., Engelmann, S., Hecker, M., Schmeck, B., et al. (2008) Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect Immun 76: 1825-1836.
14. Geiger, A., Hirtz, C., Becue, T., Bellard, E., Centeno, D., Gargani, D., et al. (2010) Exocytosis and protein secretion in Trypanosoma. BMC Microbiol 10: 20.
15. Giri, P.K., Kruh, N.A., Dobos, K.M., and Schorey, J.S. (2010) Proteomic analysis identifies highly antigenic proteins in exosomes from M. tuberculosis-infected and culture filtrate protein-treated macrophages. Proteomics 10: 1-13.
16. Gomez, M.A., Contreras, I., Halle, M., Tremblay, M.L., McMaster, R.W., and Olivier, M. (2009) Leishmania GP63 alters host signaling through cleavage-activated protein tyrosine phosphatases. Sci Signal 2: ra58.
17. Goncalves, M.F., Umezawa, E.S., Katzin, A.M., de Souza, W., Alves, M.J., Zingales, B., et al. (1991) Trypanosoma cruzi: shedding of surface antigens as membrane vesicles. Exp Parasitol 72: 43-53.
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. Halle, M., Gomez, M.A., Stuible, M., Shimizu, H., McMaster, W.R., Olivier, M., et al. (2009) The Leishmania surface protease GP63 cleaves multiple intracellular proteins and actively participates in p38 mitogen-activated protein kinase inactivation. J Biol Chem 284: 6893-6908.
20. Hiller, N.L., Bhattacharjee, S., van Ooij, C., Liolios, K., Harrison, T., Lopez-Estrano, C., et al. (2004) A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306: 1934-1937.
21. Hsu, C., Morohashi, Y., Yoshimura, S., Manrique-Hoyos, N., Jung, S., Lauterbach, M.A., et al. (2010) Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J Cell Biol 189: 223-232.
22. Izquierdo-Useros, N., Naranjo-Gomez, M., Erkizia, I., Puertas, M.C., Borras, F.E., Blanco, J., et al. (2010) HIV and mature dendritic cells: Trojan exosomes riding the Trojan horse? PLoS Pathog 6: e1000740.
23. Lenassi, M., Cagney, G., Liao, M., Vaupoti-ì, T., Bartholomeeusen, K., Cheng, Y., et al. (2010) HIV Nef is secreted in exosomes and triggers apoptosis in bystander CD4+ T Cells. Traffic 11: 110-122.
24. McCall, L.I., and Matlashewski, G. (2010) Localization and induction of the A2 virulence factor in Leishmania: evidence that A2 is a stress response protein. Mol Microbiol 77: 518-530.
25. Marti, M., Baum, J., Rug, M., Tilley, L., and Cowman, A.F. (2005) Signal-mediated export of proteins from the malaria parasite to the host erythrocyte. J Cell Biol 171: 587-592.
26. 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.
27. Morse, M.A., Garst, J., Osada, T., Khan, S., Hobeika, A., Clay, T.M., et al. (2005) A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. J Transl Med 3: 9.
28. Nandan, D., Yi, T., Lopez, M., Lai, C., and Reiner, N.E. (2002) Leishmania EF-1alpha activates the Src homology 2 domain containing tyrosine phosphatase SHP-1 leading to macrophage deactivation. J Biol Chem 277: 50190-50197.
29. Nandan, D., Tran, T., Trinh, E., Silverman, J.M., and Lopez, M. (2007) Identification of leishmania fructose-1, 6-bisphosphate aldolase as a novel activator of host macrophage Src homology 2 domain containing protein tyrosine phosphatase SHP-1. Biochem Biophys Res Commun 364: 601-607.
30. Nguyen, D.G., Booth, A., Gould, S.J., and Hildreth, J.E.K. (2003) Evidence that HIV budding in primary macrophages occurs through the exosome release pathway. J Biol Chem 278: 52347-52354.
31. Oliveira, D.L., Freire-de-Lima, C.G., Nosanchuk, J.D., Casadevall, A., Rodrigues, M.L., and Nimrichter, L. (2010) Extracellular vesicles from Cryptococcus neoformans modulate macrophage functions. Infect Immun 78: 1601-1609.
32. Ostrowski, M., Carmo, N.B., Krumeich, S., Fanget, I., Raposo, G., Savina, A., et al. (2010) Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 12: 19-30.
33. Panepinto, J., Komperda, K., Frases, S., Park, Y.D., Djordjevic, J.T., Casadevall, A., et al. (2009) Sec6-dependent sorting of fungal extracellular exosomes and laccase of Cryptococcus neoformans. Mol Microbiol 71: 1165-1176.
34. Pegtel, D.M., Cosmopoulos, K., Thorley-Lawson, D.A., van Eijndhoven, M.A., Hopmans, E.S., Lindenberg, J.L., et al. (2010) Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA 107: 6328-6333.
35. Peruhype-Magalhaes, V., Martins-Filho, O.A., Prata, A., Silva, L.A., Rabello, A., Teixeira-Carvalho, A., et al. (2006) Mixed inflammatory/regulatory cytokine profile marked by simultaneous raise of interferon-gamma and interleukin-10 and low frequency of tumour necrosis factor-alpha(+) monocytes are hallmarks of active human visceral leishmaniasis due to Leishmania chagasi infection. Clin Exp Immunol 146: 124-132.
36. Ranganathan, S., and Garg, G. (2009) Secretome: clues into pathogen infection and clinical applications. Genome Med 1: 113.
37. Reiner, N.E. (2005) Targeting cell regulation promotes pathogen survival in macrophages. Clin Immunol 114: 213-215.
38. Rodrigues, M.L., Nimrichter, L., Oliveira, D.L., Frases, S., Miranda, K., Zaragoza, O., et al. (2007) Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport. Eukaryot Cell 6: 48-59.
39. Rodrigues, M.L., Nakayasu, E.S., Oliveira, D.L., Nimrichter, L., Nosanchuk, J.D., Almeida, I.C., et al. (2008) Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot Cell 7: 58-67.
40. Savina, A., Fader, C.M., Damiani, M.T., and Colombo, M.I. (2005) rab11 promotes docking and fusion of multivesicular bodies in a calcium-dependent manner. Traffic 6: 131-143.
41. Schnitzer, J.K., Berzel, S., Fajardo-Moser, M., Remer, K.A., and Moll, H. (2010) Fragments of antigen-loaded dendritic cells (DC) and DC-derived exosomes induce protective immunity against Leishmania major. Vaccine 28: 5785-5793.
42. Silverman, J.M., Chan, S.K., Robinson, D.P., Dwyer, D.M., Nandan, D., Foster, L.J., et al. (2008) Proteomic analysis of the secretome of Leishmania donovani. Genome Biol 9: R35.
43. Silverman, J.M., Clos, J., Oliveira, C.C., Shirvani, O., Fang, Y., Wang, C., et al. (2010a) An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. J Cell Sci 123: 842-852.
44. Silverman, J.M., Clos, J., Horakova, E., Wang, A.Y., Wiesgigl, M., Kelly, I., et al. (2010b) Leishmania exosomes modulate innate and adaptive immune responses through effects on monocytes and dendritic cells. J Immunol 9: 5011-5022.
45. Simpson, R.J., Jensen, S.S., and Lim, J.W. (2008) Proteomic profiling of exosomes: current perspectives. Proteomics 8: 4083-4099.
46. Tamai, K., Tanaka, N., Nakano, T., Kakazu, E., Kondo, Y., Inoue, J., et al. (2010) Exosome secretion of dendritic cells is regulated by Hrs, an ESCRT-0 protein. Biochem Biophys Res Commun 399: 384-390.
47. Thery, C., Ostrowski, M., and Segura, E. (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9: 581-593.
48. Trajkovic, K., Hsu, C., Chiantia, S., Rajendran, L., Wenzel, D., Wieland, F., et al. (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319: 1244-1247.
49. Trocoli Torrecilhas, A.C., Tonelli, R.R., Pavanelli, W.R., Silva, J.S., Schumacher, R.I., de Souza, W., et al. (2009) Trypanosoma cruzi: parasite shed vesicles increase heart parasitism and generate an intense inflammatory response. Microbes Infect 11: 29-39.
50. Yoshida, N., and Cortez, M. (2008) Trypanosoma cruzi: parasite and host cell signaling during the invasion process. Subcell Biochem 47: 82-91.