The carrying pigeons of the cell: Exosomes and their role in infectious diseases caused by human pathogens

Pathogens and Disease

Volumn 71, Issue 2, 2014, Pages 109-120

  Fleming, Adam ^a   Sampey, Gavin ^a   Chung, Myung Chul ^a   Bailey, Charles ^a   van Hoek, Monique L ^a   Kashanchi, Fatah ^a   Hakami, Ramin M ^a  

^a GEORGE MASON UNIVERSITY   (United States)

Author keywords

Exosome; Human pathogens; Immune response; Infectious diseases; Intercellular communication; Pathogenesis

Indexed keywords

BACTERIUM; EXOSOME; HOST; HUMAN; IMMUNE RESPONSE; INFECTION; NEOPLASM; NONHUMAN; PARASITE; PATHOGENESIS; PRIORITY JOURNAL; PROPHYLAXIS; REVIEW; SYNTHESIS; VIRUS;

EID: 84895488143     PISSN: None     EISSN: 2049632X     Source Type: Journal    
DOI: 10.1111/2049-632X.12135     Document Type: Review

References (76)

1. Ali SA, Huang M, Campbell PE, Roth WW, Campbell T, Kahn M, Newman G, Villinger F, Powell MD & Bond VC (2010) Genetic characterization of HIV type 1 Nef-induced vesicle secretion. AIDS Res Hum Retroviruses 26: 173-192.
2. Aline F, Bout D, Amigorena S, Roingeard P & Dimier-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. Beatty WL, Rhoades ER, Ullrich HJ, Chatterjee D, Heuser JE & Russell DG (2000) Trafficking and release of mycobacterial lipids from infected macrophages. Traffic 1: 235-247.
4. Beatty WL, Ullrich HJ & Russell DG (2001) Mycobacterial surface moieties are released from infected macrophages by a constitutive exocytic event. Eur J Cell Biol 80: 31-40.
5. Beauvillain C, Ruiz S, Guiton R, Bout D & Dimier-Poisson I (2007) A vaccine based on exosomes secreted by a dendritic cell line confers protection against T. gondii infection in syngeneic and allogeneic mice. Microbes Infect 9: 1614-1622.
6. Beauvillain C, Juste MO, Dion S, Pierre J & Dimier-Poisson I (2009) Exosomes are an effective vaccine against congenital toxoplasmosis in mice. Vaccine 27: 1750-1757.
7. Bhatnagar S & Schorey JS (2007) Exosomes released from infected macrophages contain Mycobacterium avium glycopeptidolipids and are proinflammatory. J Biol Chem 282: 25779-25789.
8. Bhatnagar S, Shinagawa K, Castellino FJ & Schorey JS (2007) Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo. Blood 110: 3234-3244.
9. Campbell PE, Isayev O, Ali SA, Roth WW, Huang M-B, Powell MD, Leszczynski J & Bond VC (2012) Validation of a novel secretion modification region (SMR) of HIV-1 Nef using cohort sequence analysis and molecular modeling. J Mol Model 18: 4603-4613.
10. Chen X-M, O'Hara SP, Nelson JB, Splinter PL, Small AJ, Tietz PS, Limper AH & LaRusso NF (2005) Multiple TLRs are expressed in human cholangiocytes and mediate host epithelial defense responses to Cryptosporidium parvum via activation of NF-kappaB. J Immunol 175: 7447-7456.
11. Colino J & Snapper CM (2006) Exosomes from bone marrow dendritic cells pulsed with diphtheria toxoid preferentially induce type 1 antigen-specific IgG responses in naive recipients in the absence of free antigen. J Immunol 177: 3757-3762.
12. Colino J & Snapper CM (2007) Dendritic cell-derived exosomes express a Streptococcus pneumoniae capsular polysaccharide type 14 cross-reactive antigen that induces protective immunoglobulin responses against pneumococcal infection in mice. Infect Immun 75: 220-230.
13. Conde-Vancells J, Rodrigues-Suarez E, Embade N, Gil D, Matthiesen R, Valle M, Elortza F, Lu SC, Mato JM & Falcon-Perez JM (2008) Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes. J Proteome Res 7: 5157-5166.
14. Coppieters K, Barral AM, Juedes A, Wolfe T, Rodrigo E, Théry C, Amigorena S & von Herrath MG (2009) No significant CTL cross-priming by dendritic cell-derived exosomes during murine lymphocytic choriomeningitis virus infection. J Immunol 182: 2213-2220.
15. del Cacho E, Gallego M, Lee SH, Lillehoj HS, Quilez J, Lillehoj EP & Sánchez-Acedo C (2012) Induction of protective immunity against Eimeria tenella, Eimeria maxima, and Eimeria acervulina infections using dendritic cell-derived exosomes. Infect Immun 80: 1909-1916.
16. Dreux M, Garaigorta U, Boyd B, Décembre E, Chung J, Whitten-Bauer C, Wieland S & Chisari FV (2012) Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity. Cell Host Microbe 12: 558-570.
17. Epple LM, Griffiths SG, Dechkovskaia AM, Dusto NL, White J, Ouellette RJ, Anchordoquy TJ, Bemis LT & Graner MW (2012) Medulloblastoma exosome proteomics yield functional roles for extracellular vesicles. PLoS ONE 7: e42064.
18. Fevrier B, Vilette D, Archer F, Loew D, Faigle W, Vidal M, Laude H & Raposo G (2004) Cells release prions in association with exosomes. P Natl Acad Sci USA 101: 9683-9688.
19. Giri PK, Kruh NA, Dobos KM & Schorey JS (2010) Proteomic analysis identifies highly antigenic proteins in exosomes from M. tuberculosis-infected and culture filtrate protein-treated macrophages. Proteomics 10: 3190-3202.
20. Gould SJ, Booth AM & Hildreth JEK (2003) The Trojan exosome hypothesis. P Natl Acad Sci USA 100: 10592-10597.
21. Harding C, Heuser J & Stahl P (1984) Endocytosis and intracellular processing of transferrin and colloidal gold-transferrin in rat reticulocytes: demonstration of a pathway for receptor shedding. Eur J Cell Biol 35: 256-263.
22. Hassani K & Olivier M (2013) Immunomodulatory impact of leishmania-induced macrophage exosomes: a comparative proteomic and functional analysis. PLoS Negl Trop Dis 7: e2185.
23. Hood JL, San RS & Wickline SA (2011) Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res 71: 3792-3801.
24. Hu G, Yao H, Chaudhuri AD, Duan M, Yelamanchili SV, Wen H, Cheney PD, Fox HS & Buch S (2012) Exosome-mediated shuttling of microRNA-29 regulates HIV Tat and morphine-mediated neuronal dysfunction. Cell Death Dis 3: e381.
25. Hu G, Gong A-Y, Roth AL, Huang BQ, Ward HD, Zhu G, Larusso NF, Hanson ND & Chen X-M (2013) Release of luminal exosomes contributes to TLR4-mediated epithelial antimicrobial defense. PLoS Pathog 9: e1003261.
26. Ikeda M & Longnecker R (2007) Cholesterol is critical for Epstein-Barr virus latent membrane protein 2A trafficking and protein stability. Virology 360: 461-468.
27. Izquierdo-Useros N, Naranjo-Gómez M, Erkizia I, Puertas MC, Borràs FE, Blanco J & Martinez-Picado J (2010) HIV and mature dendritic cells: Trojan exosomes riding the Trojan horse? PLoS Pathog 6: e1000740.
28. Johnstone RM, Adam M, Hammond JR, Orr L & Turbide C (1987) Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 262: 9412-9420.
29. Johnstone RM, Mathew A, Mason AB & Teng K (1991) Exosome formation during maturation of mammalian and avian reticulocytes: evidence that exosome release is a major route for externalization of obsolete membrane proteins. J Cell Physiol 147: 27-36.
30. Kadiu I, Narayanasamy P, Dash PK, Zhang W & Gendelman HE (2012) Biochemical and biologic characterization of exosomes and microvesicles as facilitators of HIV-1 infection in macrophages. J Immunol 189: 744-754.
31. Kalra H, Simpson RJ, Ji H et al. (2012) Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol 10: e1001450.
32. Keryer-Bibens C, Pioche-Durieu C, Villemant C, Souquère S, Nishi N, Hirashima M, Middeldorp J & Busson P (2006) Exosomes released by EBV-infected nasopharyngeal carcinoma cells convey the viral latent membrane protein 1 and the immunomodulatory protein galectin 9. BMC Cancer 6: 283.
33. Kharaziha P, Ceder S, Li Q & Panaretakis T (2012) Tumor cell-derived exosomes: a message in a bottle. Biochim Biophys Acta 1826: 103-111.
34. Kim DK, Kang B, Kim OY et al. (2013) EVpedia: an integrated database of high-throughput data for systemic analyses of extracellular vesicles. J Extracell Vesicles 2: 20384.
35. Klibi J, Niki T, Riedel A et al. (2009) Blood diffusion and Th1-suppressive effects of galectin-9-containing exosomes released by Epstein-Barr virus-infected nasopharyngeal carcinoma cells. Blood 113: 1957-1966.
36. Lakhal S & Wood MJA (2011) Exosome nanotechnology: an emerging paradigm shift in drug delivery: exploitation of exosome nanovesicles for systemic in vivo delivery of RNAi heralds new horizons for drug delivery across biological barriers. BioEssays 33: 737-741.
37. Leblanc P, Alais S, Porto-Carreiro I, Lehmann S, Grassi J, Raposo G & Darlix JL (2006) Retrovirus infection strongly enhances scrapie infectivity release in cell culture. EMBO J 25: 2674-2685.
38. Logozzi M, De Milito A, Lugini L et al. (2009) High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS ONE 4: e5219.
39. Luga V, Zhang L, Viloria-Petit AM, Ogunjimi AA, Inanlou MR, Chiu E, Buchanan M, Hosein AN, Basik M & Wrana JL (2012) Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 151: 1542-1556.
40. Mathivanan S, Fahner CJ, Reid GE & Simpson RJ (2012) ExoCarta 2012: database of exosomal proteins. RNA and lipids. Nucleic Acids Res 40 (Database issue): D1241-D1244.
41. Meckes DG Jr & Raab-Traub N (2011) Microvesicles and viral infection. J Virol 85: 12844-12854.
42. Meckes DG Jr, Shair KHY, Marquitz AR, Kung C-P, Edwards RH & Raab-Traub N (2010) Human tumor virus utilizes exosomes for intercellular communication. P Natl Acad Sci USA 107: 20370-20375.
43. Meckes DG Jr, Gunawardena HP, Dekroon RM, Heaton PR, Edwards RH, Ozgur S, Griffith JD, Damania B & Raab-Traub N (2013) Modulation of B-cell exosome proteins by gamma herpesvirus infection. P Natl Acad Sci USA 110: E2925-E2933.
44. Morse MA, Garst J, Osada T et al. (2005) A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. J Transl Med 3: 9.
45. Mu W, Rana S & Zöller M (2013) Host matrix modulation by tumor exosomes promotes motility and invasiveness. Neoplasia 15: 875-887.
46. Narayanan A, Iordanskiy S, Das R et al. (2013) Exosomes derived from HIV-1-infected cells contain trans-activation response element RNA. J Biol Chem 288: 20014-20033.
47. Neumann J, Eis-Hübinger AM & Koch N (2003) Herpes simplex virus type 1 targets the MHC class II processing pathway for immune evasion. J Immunol 171: 3075-3083.
48. Oehmcke S, Westman J, Malmström J, Mörgelin M, Olin AI, Kreikemeyer B & Herwald H (2013) A novel role for pro-coagulant microvesicles in the early host defense against Streptococcus pyogenes. PLoS Pathog 9: e1003529.
49. O'Neill HC & Quah BJC (2008) Exosomes secreted by bacterially infected macrophages are proinflammatory. Sci Signal 1: pe8.
50. Pant S, Hilton H & Burczynski ME (2012) The multifaceted exosome: biogenesis, role in normal and aberrant cellular function, and frontiers for pharmacological and biomarker opportunities. Biochem Pharmacol 83: 1484-1494.
51. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MAJ, Hopmans ES, Lindenberg JL, de Gruijl TD, Würdinger T & Middeldorp JM (2010) Functional delivery of viral miRNAs via exosomes. P Natl Acad Sci USA 107: 6328-6333.
52. Peinado H, Alečković M, Lavotshkin S et al. (2012) Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 18: 883-891.
53. Pestka S, Krause CD, Sarkar D, Walter MR, Shi Y & Fisher PB (2004) Interleukin-10 and related cytokines and receptors. Annu Rev Immunol 22: 929-979.
54. Quah BJC & O'Neill HC (2007) Mycoplasma contaminants present in exosome preparations induce polyclonal B cell responses. J Leukoc Biol 82: 1070-1082.
55. Ramachandra L, Qu Y, Wang Y, Lewis CJ, Cobb BA, Takatsu K, Boom WH, Dubyak GR & Harding CV (2010) Mycobacterium tuberculosis synergizes with ATP to induce release of microvesicles and exosomes containing major histocompatibility complex class II molecules capable of antigen presentation. Infect Immun 78: 5116-5125.
56. Ramakrishnaiah V, Thumann C, Fofana I et al. (2013) Exosome-mediated transmission of hepatitis C virus between human hepatoma Huh7.5 cells. P Natl Acad Sci USA 110: 13109-13113.
57. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ & Geuze HJ (1996) B lymphocytes secrete antigen-presenting vesicles. J Exp Med 183: 1161-1172.
58. Record M, Subra C, Silvente-Poirot S & Poirot M (2011) Exosomes as intercellular signalosomes and pharmacological effectors. Biochem Pharmacol 81: 1171-1182.
59. Rhoades E, Hsu F-F, Torrelles JB, Turk J, Chatterjee D & Russell DG (2003) Identification and macrophage-activating activity of glycolipids released from intracellular Mycobacterium bovis BCG. Mol Microbiol 48: 875-888.
60. Schnitzer JK, Berzel S, Fajardo-Moser M, Remer KA & Moll H (2010) Fragments of antigen-loaded dendritic cells (DC) and DC-derived exosomes induce protective immunity against Leishmania major. Vaccine 28: 5785-5793.
61. Schorey JS & Bhatnagar S (2008) Exosome function: from tumor immunology to pathogen biology. Traffic 9: 871-881.
62. Shelton MN, Huang M-B, Ali SA, Powell MD & Bond VC (2012) Secretion modification region-derived peptide disrupts HIV-1 Nef's interaction with mortalin and blocks virus and Nef exosome release. J Virol 86: 406-419.
63. Simpson RJ, Lim JW, Moritz RL & Mathivanan S (2009) Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics 6: 267-283.
64. Singh PP, LeMaire C, Tan JC, Zeng E & Schorey JS (2011) Exosomes released from M. tuberculosis infected cells can suppress IFN-γ mediated activation of naïve macrophages. PLoS ONE 6: e18564.
65. Singh PP, Smith VL, Karakousis PC & Schorey JS (2012) Exosomes isolated from mycobacteria-infected mice or cultured macrophages can recruit and activate immune cells in vitro and in vivo. J Immunol 189: 777-785.
66. Swirski FK, Nahrendorf M, Etzrodt M et al. (2009) Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 325: 612-616.
67. Temme S, Eis-Hübinger AM, McLellan AD & Koch N (2010) The herpes simplex virus-1 encoded glycoprotein B diverts HLA-DR into the exosome pathway. J Immunol 184: 236-243.
68. Théry C, Amigorena S, Raposo G & Clayton A (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol 60: 3.22.21-3.22.29.
69. Tian T, Wang Y, Wang H, Zhu Z & Xiao Z (2010) Visualizing of the cellular uptake and intracellular trafficking of exosomes by live-cell microscopy. J Cell Biochem 111: 488-496.
70. Torrecilhas AC, Schumacher RI, Alves MJM & Colli W (2012) Vesicles as carriers of virulence factors in parasitic protozoan diseases. Microbes Infect 14: 1465-1474.
71. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ & Lötvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659.
72. van Niel G, Porto-Carreiro I, Simoes S & Raposo G (2006) Exosomes: a common pathway for a specialized function. J Biochem 140: 13-21.
73. Xiao D, Ohlendorf J, Chen Y, Taylor DD, Rai SN, Waigel S, Zacharias W, Hao H & McMasters KM (2012) Identifying mRNA, microRNA and protein profiles of melanoma exosomes. PLoS ONE 7: e46874.
74. Xiu F, Cai Z, Yang Y, Wang X, Wang J & Cao X (2007) Surface anchorage of superantigen SEA promotes induction of specific antitumor immune response by tumor-derived exosomes. J Mol Med 85: 511-521.
75. Yang Y, Xiu F, Cai Z, Wang J, Wang Q, Fu Y & Cao X (2007) Increased induction of antitumor response by exosomes derived from interleukin-2 gene-modified tumor cells. J Cancer Res Clin Oncol 133: 389-399.
76. Yang C, Chalasani G, Ng Y-H & Robbins PD (2012) Exosomes released from Mycoplasma infected tumor cells activate inhibitory B cells. PLoS ONE 7: e36138.