Immature dendritic cell-derived exosomes rescue septic animals via milk fat globule epidermal growth factor VIII

Journal of Immunology

Volumn 183, Issue 9, 2009, Pages 5983-5990

  Miksa, Michael ^a,b   Wu, Rongqian ^a,b   Dong, Weifeng ^b   Komura, Hidefumi ^b   Amin, Dhruv ^b   Ji, Youxin ^b   Wang, Zhimin ^b   Wang, Haichao ^a   Ravikumar, Thanjavur S ^b   Tracey, Kevin J ^a   Wang, Ping ^a,b  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b NORTH SHORE UNIVERSITY HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; LACTADHERIN; RECOMBINANT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL THERAPY; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; EXOSOME; IN VITRO STUDY; LIGATION; MALE; MORTALITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PUNCTURE; RAT; SEPSIS; SPLEEN; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; TISSUE LEVEL;

ANIMALS; ANTIGENS, SURFACE; APOPTOSIS REGULATORY PROTEINS; CELL DIFFERENTIATION; CELLS, CULTURED; DENDRITIC CELLS; EXOSOMES; INFLAMMATION MEDIATORS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MILK PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; SEPSIS;

EID: 77952094971     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0802994     Document Type: Article

References (45)

1. Thery, C., M. Boussac, P. Veron, P. Ricciardi-Castagnoli, G. Raposo, J. Garin, and S. Amigorena. 2001. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J. Immunol. 166: 7309-7318. (Pubitemid 32525606)
2. Thery, C., A. Regnault, J. Garin, J. Wolfers, L. Zitvogel, P. Ricciardi-Castagnoli, G. Raposo, and S. Amigorena. 1999. Molecular characterization of dendritic cell-derived exosomes: selective accumulation of the heat shock protein hsc73. J. Cell Biol. 147: 599-610.
3. Newburg, D. S., J. A. Peterson, G. M. Ruiz-Palacios, D. O. Matson, A. L. Morrow, J. Shults, M. L. Guerrero, P. Chaturvedi, S. O. Newburg, C. D. Scallan, et al. 1998. Role of human-milk lactadherin in protection against symptomatic rotavirus infection. Lancet 351: 1160-1164.
4. Hanayama, R., M. Tanaka, K. Miyasaka, K. Aozasa, M. Koike, Y. Uchiyama, and S. Nagata. 2004. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science 304: 1147-1150.
5. Degli-Esposti, M. A., and M. J. Smyth. 2005. Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nat. Rev. Immunol. 5: 112-124.
6. Martin, G. S., D. M. Mannino, S. Eaton, and M. Moss. 2003. The epidemiology of sepsis in the United States from 1979 through 2000. N. Engl. J. Med. 348: 1546-1554.
7. Marti-Carvajal, A., G. Salanti, and A. F. Cardona. 2008. Human recombinant activated protein C for severe sepsis. Cochrane Database Syst. Rev. 1: CD004388.
8. Tracey, K. J., Y. Fong, D. G. Hesse, K. R. Manogue, A. T. Lee, G. C. Kuo, S. F. Lowry, and A. Cerami. 1987. Anti-cachectin/TNF monoclonal antibodies prevent septic shock during lethal bacteremia. Nature 330: 662-664.
9. Li, P., H. Allen, S. Banerjee, S. Franklin, L. Herzog, C. Johnston, J. McDowell, M. Paskind, L. Rodman, J. Salfeld, et al. 1995. Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1β and resistant to endotoxic shock. Cell 80: 401-411.
10. Meyer, T. A., J. Wang, G. M. Tiao, C. K. Ogle, J. E. Fischer, and P. O. Hasselgren. 1995. Sepsis and endotoxemia stimulate intestinal interleukin-6 production. Surgery 118: 336-342.
11. Wang, H., O. Bloom, M. Zhang, J. M. Vishnubhakat, M. Ombrellino, J. Che, A. Frazier, H. Yang, S. Ivanova, L. Borovikova, et al. 1999. HMG-1 as a late mediator of endotoxin lethality in mice. Science 285: 248-251.
12. Alves-Filho, J. C., F. A. de, M. Russo, and F. Q. Cunha. 2006. Toll-like receptor 4 signaling leads to neutrophil migration impairment in polymicrobial sepsis. Crit. Care Med. 34: 461-470.
13. Huber-Lang, M. S., E. M. Younkin, J. V. Sarma, S. R. McGuire, K. T. Lu, R. F. Guo, V. A. Padgaonkar, J. T. Curnutte, R. Erickson, and P. A. Ward. 2002. Complement-induced impairment of innate immunity during sepsis. J. Immunol. 169: 3223-3231.
14. Kaufmann, I., A. Hoelzl, F. Schliephake, T. Hummel, A. Chouker, K. Peter, and M. Thiel. 2006. Polymorphonuclear leukocyte dysfunction syndrome in patients with increasing sepsis severity. Shock 26: 254-261.
15. Hallwirth, U., G. Pomberger, D. Zaknun, Z. Szepfalusi, E. Horcher, A. Pollak, E. Roth, and A. Spittler. 2002. Monocyte phagocytosis as a reliable parameter for predicting early-onset sepsis in very low birthweight infants. Early Hum. Dev. 67: 1-9.
16. Gershov, D., S. Kim, N. Brot, and K. B. Elkon. 2000. C-Reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: implications for systemic autoimmunity. J. Exp. Med. 192: 1353-1364.
17. Fink, S. L., and B. T. Cookson. 2005. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect. Immun. 73: 1907-1916.
18. Hanayama, R., M. Tanaka, K. Miwa, A. Shinohara, A. Iwamatsu, and S. Nagata. 2002. Identification of a factor that links apoptotic cells to phagocytes. Nature 417: 182-187.
19. Bell, C. W., W. Jiang, C. F. Reich, III, and D. S. Pisetsky. 2006. The extracellular release of HMGB1 during apoptotic cell death. Am. J. Physiol. 291: C1318-C1325.
20. Scaffidi, P., T. Misteli, and M. E. Bianchi. 2002. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418: 191-195.
21. Muthana, M., B. Fairburn, S. Mirza, L. K. Slack, and A. G. Pockley. 2004. Systematic evaluation of the conditions required for the generation of immature rat bone marrow-derived dendritic cells and their phenotypic and functional characterization. J. Immunol. Methods 294: 165-179.
22. Qin, S., H. Wang, R. Yuan, H. Li, M. Ochani, K. Ochani, M. Rosas-Ballina, C. J. Czura, J. M. Huston, E. Miller, et al. 2006. Role of HMGB1 in apoptosis-mediated sepsis lethality. J. Exp. Med. 203: 1637-1642.
23. Ulloa, L., and D. Messmer. 2006. High-mobility group box 1 (HMGB1) protein: friend and foe. Cytokine Growth Factor Rev. 17: 189-201.
24. Moretta, A. 2002. Natural killer cells and dendritic cells: rendezvous in abused tissues. Nat. Rev. Immunol. 2: 957-964.
25. Riedemann, N. C., and P. A. Ward. 2003. Anti-inflammatory strategies for the treatment of sepsis. Expert. Opin. Biol. Ther. 3: 339-350.
26. Utsugi-Kobukai, S., H. Fujimaki, C. Hotta, M. Nakazawa, and M. Minami. 2003. MHC class I-mediated exogenous antigen presentation by exosomes secreted from immature and mature bone marrow derived dendritic cells. Immunol. Lett. 89: 125-131. (Pubitemid 37222437)
27. Veron, P., E. Segura, G. Sugano, S. Amigorena, and C. Thery. 2005. Accumulation of MFG-E8/lactadherin on exosomes from immature dendritic cells. Blood Cells Mol. Dis. 35: 81-88. (Pubitemid 41267033)
28. Asano, K., M. Miwa, K. Miwa, R. Hanayama, H. Nagase, S. Nagata, and M. Tanaka. 2004. Masking of phosphatidylserine inhibits apoptotic cell engulfment and induces autoantibody production in mice. J. Exp. Med. 200: 459-467.
29. Jinushi, M., Y. Nakazaki, M. Dougan, D. R. Carrasco, M. Mihm, and G. Dranoff. 2007. MFG-E8-mediated uptake of apoptotic cells by APCs links the pro- and antiinflammatory activities of GM-CSF. J. Clin. Invest. 117: 1902-1913.
30. Orozco, H., J. Arch, H. Medina-Franco, J. P. Pantoja, Q. H. Gonzalez, M. Vilatoba, C. Hinojosa, F. Vargas-Vorackova, and J. Sifuentes-Osornio. 2006. Molgramostim (GM-CSF) associated with antibiotic treatment in nontraumatic abdominal sepsis: a randomized, double-blind, placebo-controlled clinical trial. Arch. Surg. 141: 150-153.
31. Presneill, J. J., T. Harris, A. G. Stewart, J. F. Cade, and J. W. Wilson. 2002. A randomized phase II trial of granulocyte-macrophage colony-stimulating factor therapy in severe sepsis with respiratory dysfunction. Am. J Respir. Crit Care Med. 166: 138-143.
32. Rosenbloom, A. J., P. K. Linden, A. Dorrance, N. Penkosky, M. H. Cohen-Melamed, and M. R. Pinsky. 2005. Effect of granulocyte-monocyte colony-stimulating factor therapy on leukocyte function and clearance of serious infection in nonneutropenic patients. Chest 127: 2139-2150.
33. Ahmad, M., H. B. Fleit, M. G. Golightly, and E. F. La Gamma. 2004. In vivo effect of recombinant human granulocyte colony-stimulating factor on phagocytic function and oxidative burst activity in septic neutropenic neonates. Biol. Neonate 86: 48-54. (Pubitemid 39077610)
34. + T lymphocytes during polymicrobial sepsis is mediated by Fas ligand and not endotoxin. Immunology 97: 45-55.
35. Ayala, A., J. L. Lomas, P. S. Grutkoski, and S. Chung. 2003. Fas-ligand mediated apoptosis in severe sepsis and shock. Scand. J. Infect. Dis. 35: 593-600. (Pubitemid 37336878)
36. Ayala, A., X. Y. Xin, C. A. Ayala, D. E. Sonefeld, S. M. Karr, T. A. Evans, and I. H. Chaudry. 1998. Increased mucosal B-lymphocyte apoptosis during polymicrobial sepsis is a Fas ligand but not an endotoxin-mediated process. Blood 91: 1362-1372.
37. Tinsley, K. W., M. H. Grayson, P. E. Swanson, A. M. Drewry, K. C. Chang, I. E. Karl, and R. S. Hotchkiss. 2003. Sepsis induces apoptosis and profound depletion of splenic interdigitating and follicular dendritic cells. J. Immunol. 171: 909-914.
38. Hotchkiss, R. S., K. C. Chang, M. H. Grayson, K. W. Tinsley, B. S. Dunne, C. G. Davis, D. F. Osborne, and I. E. Karl. 2003. Adoptive transfer of apoptotic splenocytes worsens survival, whereas adoptive transfer of necrotic splenocytes improves survival in sepsis. Proc. Natl. Acad. Sci. USA 100: 6724-6729.
39. 2, and PAF. J. Clin. Invest. 101: 890-898.
40. Yang, H., M. Ochani, J. Li, X. Qiang, M. Tanovic, H. E. Harris, S. M. Susarla, L. Ulloa, H. Wang, R. DiRaimo, et al. 2004. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc. Natl. Acad. Sci. USA 101: 296-301.
41. Miksa, M., R. Wu, W. Dong, P. Das, D. Yang, and P. Wang. 2006. Dendritic cell-derived exosomes containing milk fat globule epidermal growth factor-factor VIII attenuate proinflammatory responses in sepsis. Shock 25: 586-593.
42. Lotze, M. T., and K. J. Tracey. 2005. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat. Rev. Immunol. 5: 331-342.
43. Wu, R., W. Dong, M. Zhou, F. Zhang, C. P. Marini, T. S. Ravikumar, and P. Wang. 2007. Ghrelin attenuates sepsis-induced acute lung injury and mortality in rats. Am. J Respir. Crit Care Med. 176: 805-813. (Pubitemid 47598482)
44. Yang, S., C. S. Chung, A. Ayala, I. H. Chaudry, and P. Wang. 2002. Differential alterations in cardiovascular responses during the progression of polymicrobial sepsis in the mouse. Shock 17: 55-60.
45. Raposo, G., H. W. Nijman, W. Stoorvogel, R. Liejendekker, C. V. Harding, C. J. Melief, and H. J. Geuze. 1996. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 183: 1161-1172.