Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo

Blood

Volumn 110, Issue 9, 2007, Pages 3234-3244

  Bhatnagar, Sanchita ^a   Shinagawa, Kazuhiko ^a   Castellino, Francis J ^a   Schorey, Jeffrey S ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 12; LIPOARABINOMANNAN; LIPOPROTEIN; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL INFECTION; CELL COMMUNICATION; CELL VACUOLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXOSOME; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOSTIMULATION; IMMUNOSURVEILLANCE; INFLAMMATION; LUNG; LUNG LAVAGE; MACROPHAGE; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MACROPHAGE MIGRATION; MOLECULAR BIOLOGY; MOUSE; MYCOBACTERIOSIS; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTOZOAL INFECTION; SALMONELLA TYPHIMURIUM; TOXOPLASMA GONDII;

EID: 36148959342     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2007-03-079152     Document Type: Article

References (50)

1. Schnare M, Barton GM, Holt AC, Takeda K, Akira S, Medzhitov R. Toll-like receptors control activation of adaptive immune responses. Nat Immunol. 2001;2:947-950.
2. Medzhitov R. Toll-like receptors and innate immunity. Nat Rev Immunol. 2001;1:135-145.
3. Barton GM, Medzhitov R. Toll-like receptors and their ligands. Curr Top Microbiol Immunol. 2002;270:81-92.
4. Elson G, Dunn-Siegrist I, Daubeuf B, Pugin J. Contribution of Toll-like receptors to the innate immune response to Gram-negative and Gram-positive bacteria. Blood. 2007;109:1574-1583.
5. Denzer K, Kleijmeer MJ, Heijnen HF, Stoorvogel W, Geuze HJ. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci. 2000;113:3365-3374.
6. van Niel G, Porto-Carreiro I, Simoes S, Raposo G. Exosomes: a common pathway for a specialized function. J Biochem (Tokyo). 2006;140:13-21.
7. Johnstone RM, Bianchini A, Teng K. Reticulocyte maturation and exosome release: transferrin receptor containing exosomes shows multiple plasma membrane functions. Blood. 1989;74:1844-1851.
8. Raposo G, Nijman HW, Stoorvogel W, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med. 1996;183:1161-1172.
9. Mignot G, Roux S, Thery C, Segura E, Zitvogel L. Prospects for exosomes in immunotherapy of cancer. J Cell Mol Med. 2006;10:376-388.
10. Chaput N, Flament C, Viaud S, et al. Dendritic cell derived-exosomes: biology and clinical implementations. J Leukoc Biol. 2006;80:471-478.
11. Andre F, Escudier B, Angevin E, Tursz T, Zitvogel L. Exosomes for cancer immunotherapy. Ann Oncol. 2004;15:iv141-iv144.
12. Chaput N, Schartz NE, Andre F, Zitvogel L. Exosomes for immunotherapy of cancer. Adv Exp Med Biol. 2003;532:215-221.
13. Roach SK, Schorey JS. Differential regulation of the mitogen-activated protein kinases by pathogenic and nonpathogenic mycobacteria. Infect Immun. 2002;70:3040-3052.
14. Bohlson SS, Strasser JA, Bower JJ, Schorey JS. Role of complement in Mycobacterium avium pathogenesis: in vivo and in vitro analyses of the host response to infection in the absence of complement component C3. Infect Immun. 2001;69:7729-7735.
15. Catron DM, Lange Y, Borensztajn J, Sylvester MD, Jones BD, Haldar K. Salmonella enterica serovar Typhimurium requires nonsterol precursors of the cholesterol biosynthetic pathway for intracellular proliferation. Infect Immun. 2004;72:1036-1042.
16. Vidal M, Mangeat P, Hoekstra D. Aggregation reroutes molecules from a recycling to a vesicle-mediated secretion pathway during reticulocyte maturation. J Cell Sci. 1997;110:1867-1877.
17. Vidal M, Sainte-Marie J, Philippot JR, Bienvenue A. Asymmetric distribution of phospholipids in the membrane of vesicles released during in vitro maturation of guinea pig reticulocytes: evidence precluding a role for "aminophospholipid translocase." J Cell Physiol. 1989;140:455-462.
18. Kelley VA, Schorey JS. Mycobacterium's arrest of phagosome maturation in macrophages requires Rab5 activity and accessibility to iron. Mol Biol Cell. 2003;14:3366-3377.
19. Hager KM, Striepen B, Tilney LG, Roos DS. The nuclear envelope serves as an intermediary between the ER and Golgi complex in the intracellular parasite Toxoplasma gondii. J Cell Sci. 1999;112:2631-2638.
20. Schaible UE, Winau F, Sieling PA, et al. Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat Med. 2003;9:1039-1046.
21. Winau F, Weber S, Sad S, et al. Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity. 2006;24:105-117.
22. Katoh N, Kraft S, Wessendorf JH, Bieber T. The high-affinity IgE receptor (FcepsilonRI) blocks apoptosis in normal human monocytes. J Clin Invest. 2000;105:183-190.
23. Ulett GC, Maclean KH, Nekkalapu S, Cleveland JL, Adderson EE. Mechanisms of group B streptococcal-induced apoptosis of murine macrophages. J Immunol. 2005;175:2555-2562.
24. Mohr S, McCormick TS, Lapetina EG. Macrophages resistant to endogenously generated nitric oxide-mediated apoptosis are hypersensitive to exogenously added nitric oxide donors: dichotomous apoptotic response independent of caspase 3 and reversal by the mitogen-activated protein kinase kinase (MEK) inhibitor PD 098059. Proc Natl Acad Sci U S A. 1998;95:5045-5050.
25. Huesmann GR, Clayton DF. Dynamic role of postsynaptic caspase-3 and BIRC4 in zebra finch song-response habituation. Neuron. 2006;52:1061-1072.
26. Thery C, Boussac M, Veron P, et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol. 2001;166:7309-7318.
27. D'Souza-Schorey C, Boshans RL, McDonough M, Stahl PD, Van Aelst L. A role for POR1, a Rac1-interacting protein, in ARF6-mediated cytoskeletal rearrangements. EMBO J. 1997;16:5445-5454.
28. Morelli AE, Larregina AT, Shufesky WJ, et al. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood. 2004;104:3257-3266.
29. Beatty WL, Rhoades ER, Ullrich HJ, Chatterjee D, Heuser JE, Russell DG. Trafficking and release of mycobacterial lipids from infected macrophages. Traffic. 2000;1:235-247.
30. Beatty WL, Ullrich HJ, Russell DG. Mycobacterial surface moieties are released from infected macrophages by a constitutive exocytic event. Eur J Cell Biol. 2001;80:31-40.
31. Rhoades E, Hsu F, Torrelles JB, Turk J, Chatterjee D, Russell DG. Identification and macrophage-activating activity of glycolipids released from intracellular Mycobacterium bovis BCG. Mol Microbiol. 2003;48:875-888.
32. Clayton A, Court J, Navabi H, et al. Analysis of antigen presenting cell derived exosomes, based on immuno-magnetic isolation and flow cytometry. J Immunol Methods. 2001;247:163-174.
33. Fan X, Krahling S, Smith D, Williamson P, Schlegel RA. Macrophage surface expression of annexins I and II in the phagocytosis of apoptotic lymphocytes. Mol Biol Cell. 2004;15:2863-2872.
34. Kang PB, Azad AK, Torrelles JB, et al. The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J Exp Med. 2005;202:987-999.
35. Savina A, Vidal M, Colombo MI. The exosome pathway in K562 cells is regulated by Rab11. J Cell Sci. 2002;115:2505-2515.
36. Mordue DG, Sibley LD. Intracellular fate of vacuoles containing Toxoplasma gondii is determined at the time of formation and depends on the mechanism of entry. J Immunol. 1997;159:4452-4459.
37. Coppens I. Contribution of host lipids to Toxoplasma pathogenesis. Cell Microbiol. 2006;8:1-9.
38. Jones BW, Means TK, Heldwein KA, et al. Different Toll-like receptor agonists induce distinct macrophage responses. J Leukoc Biol. 2001;69:1036-1044.
39. Takeuchi O, Sato S, Horiuchi T, et al. Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins. J Immunol. 2002;169:10-14.
40. Kramer H. Sorting out signals in fly endosomes. Traffic. 2002;3:87-91.
41. Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002;2:569-579.
42. Keller S, Sanderson MP, Stoeck A, Altevogt P. Exosomes: from biogenesis and secretion to biological function. Immunol Lett. 2006;107:102-108.
43. Farsad K. Exosomes: novel organelles implicated in immunomodulation and apoptosis. Yale J Biol Med. 2002;75:95-101.
44. Li XB, Zhang ZR, Schluesener HJ, Xu SQ. Role of exosomes in immune regulation. J Cell Mol Med. 2006;10:364-375.
45. Wolfers J, Lozier A, Raposo G, et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med. 2001;7:297-303.
46. Segura E, Amigorena S, Thery C. Mature dendritic cells secrete exosomes with strong ability to induce antigen-specific effector immune responses. Blood Cells Mol Dis. 2005;35:89-93.
47. Golding H, Aliberti J, King LR, et al. Inhibition of HIV-1 infection by a CCR5-binding cyclophilin from Toxoplasma gondii. Blood. 2003;102:3280-3286.
48. Yarovinsky F, Zhang D, Andersen JF, et al. TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science. 2005;308:1626-1629.
49. Gehring AJ, Rojas RE, Canaday DH, Lakey DL, Harding CV, Boom WH. The Mycobacterium tuberculosis 19-kilodalton lipoprotein inhibits gamma interferon-regulated HLA-DR and Fc gamma R1 on human macrophages through Toll-like receptor 2. Infect Immun. 2003;71:4487-4497.
50. Admyre C, Grunewald J, Thyberg J, et al. Exosomes with major histocompatibility complex class II and co-stimulatory molecules are present in human BAL fluid. Eur Respir J. 2003;22:578-583.