Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells

Blood

Volumn 104, Issue 10, 2004, Pages 3257-3266

  Morelli, Adrian E ^a   Larregina, Adriana T ^b   Shufesky, William J ^b   Sullivan, Mara L G ^b   Stolz, Donna Beer ^b   Papworth, Glenn D ^b   Zahorchak, Alan F ^b   Logar, Alison J ^b   Wang, Zhiliang ^b   Watkins, Simon C ^b   Falo Jr , Louis D ^b   Thomson, Angus W ^b  

^a 17043 Biomedical Science Tower   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CD81 ANTIGEN; CD9 ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MILK FAT; PHOSPHATIDYLSERINE;

ARTICLE; CELL MATURATION; DENDRITIC CELL; ENDOCYTOSIS; EPITHELIUM CELL; EXTRACELLULAR FLUID; KUPFFER CELL; LEUKOCYTE; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; T LYMPHOCYTE;

EID: 8644286802     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2004-03-0824     Document Type: Article

References (56)

1. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392:245-252.
2. Gallucci S, Lolkema M, Matzinger P. Natural adjuvants: endogenous activators of dendritic cells. Nat Med. 1999;5:1249-1255.
3. Albert ML, Pearce SF, Francisco LM, et al. Immature dendritic cells phagocytose apoptotic cells via alphavbeta5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J Exp Med. 1998;188:1359-1368.
4. + dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J Exp Med. 2002;195:1289-1302.
5. Morelli AE, Larregina AT, Shufesky WJ, et al. Internalization of circulating apoptotic cells by splenic marginal zone dendritic cells: dependence on complement receptors and effect on cytokine production. Blood. 2003;101:611-620.
6. Harshyne LA, Watkins SC, Gambotto A, Barratt-Boyes SM. Dendritic cells acquire antigens from live cells for cross-presentation to CTL. J Immunol. 2001;166:3717-3723.
7. Russo V, Zhou D, Sartirana C, et al. Acquisition of intact allogeneic human leukocyte antigen molecules by human dendritic cells. Blood. 2000;95:3473-3477.
8. Zitvogel L, Regnault A, Lozier A, et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med. 1998;4:594-600.
9. Andre F, Schartz NEC, Movassagh M, et al. Malignant effusions and immunogenic tumour-derived exosomes. Lancet. 2002;360:295-305.
10. Vincent-Schneider H, Stumptner-Cuvelette P, Lankar D, et al. Exosomes bearing HLA-DR1 molecules need dendritic cells to efficiently stimulate specific T cells. Int Immunol. 2002;14:713-722.
11. + T cells by dendritic cell-derived exosomes. Nat Immunol. 2002;3:1156-1162.
12. Skokos D, Botros HG, Demeure C, et al. Mast cell-derived exosomes induce phenotypic and functional maturation of dendritic cells and elicit specific immune responses in vivo. J Immunol. 2003;170:3037-3045.
13. Raposo G, Nijman HW, Stoorvogel W, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med. 1996;183:1161-1172.
14. 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;19:3365-3374.
15. Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002;2:569-579.
16. Trams EG, Lauter CJ, Salem N, Heine U. Exfoliation of membrane ecto-enzymes in the form of micro-vesicles. Biochim Biophys Acta. 1981;645:63-70.
17. Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol. 1983;97:329-339.
18. Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood. 1999;94:3791-3799.
19. vanNiel G, Raposo G, Candalh C, et al. Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology. 2001;121:337-349.
20. Raposo G, Tenza D, Mecheri S, Peronet R, Bonnerot C, Desaymard C. Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation. Mol Biol Cell. 1997;8:2631-2645.
21. Thery C, Regnault A, Garin J, et al. Molecular characterization of dendritic cell-derived exosomes: selective accumulation of the heat shock protein hsc73. J Cell Biol. 1999;147:599-610.
22. Peters PJ, Borst J, Oorschot V, et al. Cytotoxic T lymphocyte granules are secretory lysosomes, containing both perforin and granzymes. J Exp Med. 1991;173:1099-1109.
23. Gansuvd B, Hagihara M, Higuchi A, et al. Umbilical cord blood dendritic cells are a rich source of soluble HLA-DR: synergistic effect of exosomes and dendritic cells on autologous or allogeneic T-cell proliferation. Hum Immunol. 2003;64:427-439.
24. Andre F, Chaput N, Schartz NEC, et al. Exosomes as potent cell-free peptide-based vaccine, I: dendritic cell-derived exosomes transfer functional MHC class I/peptide complexes to dendritic cells. Blood. 2004;172:2126-2136.
25. Morelli AE, Zahorchak AF, Larregina AT, et al. Regulation of cytokine production by mouse myeloid dendritic cells in relation to differentiation and terminal maturation induced by LPS or CD40 ligation. Blood. 2001;98:1512-1523.
26. Hanayama R, Tanaka M, Miwa K, Shinohara A, Iwamatsu A, Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature. 2002;417:182-187.
27. 52-68 structurally related self-peptide(s) in I-Eα-deficient mice. J Immunol. 2000;164:4627-4634.
28. Murphy DB, Lo D, Rath S, et al. A novel MHC class II epitope expressed in thymic medulla but not cortex. Nature. 1989;338:765-768.
29. Ignatowicz L, Winslow G, Bill J, Kappler J, Marrack P. Cell surface expression of class II MHC proteins bound by a single peptide. J Immunol. 1995;154:3852-3862.
30. Lutz MB, Schuler G. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol. 2002;23:445-449.
31. Wilson NS, El-Sukkari D, Beltz GT, et al. Most lymphoid organ dendritic cell types are phenotypically and functionally immature. Blood. 2003;102:2187-2194.
32. Denzer K, van Eijk M, Kleijmeer MJ, Jakobson E, de Groot C, Geuze HJ. Follicular dendritic cells carry MHC class II-expressing microvesicles at their surface. J Immunol. 2000;165:1259-1265.
33. Martinez-Lorenzo MJ, Anel A, Gamen S, et al. Activated human T cells release bioactive Fas ligand and APO2 ligand in microvesicles. J Immunol. 1999;163:1274-1281.
34. 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.
35. Rieu S, Geminard C, Rabesandratana H, Sainte-Marie J, Vidal M. Exosomes released during reticulocyte maturation bind to fibronectin via integrin alpha4beta1. Eur J Biochem. 2000;267:583-590.
36. Escola JM, Kleijmeer MJ, Stoorvogel W, Griffith JM, Yoshie O, Geuze HJ. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem. 1998;273:20121-20127.
37. Rubinstein E, Le Naour F, Lagaudriere-Gesbert C, Billard M, Conjeaud H, Boucheix C. CD9, CD63, CD81, and CD82 are components of a surface tetraspan network connected to HLA-DR and VLA integrins. Eur J Immunol. 1996;26:2657-2665.
38. Takahashi Y, Bigler D, Ito Y, White JM. Sequence-specific interaction between the disintegrin domain of mouse ADAM 3 and murine eggs: role of beta1 integrin-associated proteins CD9, CD81, and CD98. Mol Biol Cell. 2001;12:809-820.
39. Zhu X, Evans JP. Analysis of the roles of RGD-binding integrins, alpha(4)/alpha(9) integrins, alpha(6) integrins, and CD9 in the interaction of the fertilin beta (ADAM2) disintegrin domain with the mouse egg membrane. Biol Reprod. 2002;66:1193-1202.
40. Verbovetski I, Bychkov H, Trahtemberg U, et al. Opsonization of apoptotic cells by autologous iC3b facilitates clearance by immature dendritic cells, down-regulates DR and CD86, and up-regulates CC chemokine receptor 7. J Exp Med. 2002;196:1553-1561.
41. Clayton A, Harris CL, Court J, Mason MD, Morgan BP. Antigen-presenting cell exosomes are protected from complement-mediated lysis by expression of CD55 and CD59. Eur J Immunol. 2003;33:522-531.
42. Amigorena S, Drake JR, Webster P, Mellman I. Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes. Nature. 1994;369:113-120.
43. Nijman HW, Kleijmeer MJ, Ossevoort MA, et al. Antigen capture and major histocompatibility class II compartments of freshly isolated and cultured human blood dendritic cells. J Exp Med. 1995;182:163-174.
44. Kleijmeer MJ, Ossevoort MA, van Veen CJ, et al. MHC class II compartments and the kinetics of antigen presentation in activated mouse spleen dendritic cells. J Immunol. 1995;154:5715-5724.
45. Geuze HJ. The role of endosomes and lysosomes in MHC class II functioning. Immunol Today. 1998;19:282-287.
46. Felder S, Miller K, Moehren G, Ullrich A, Schlessinger J, Hopkins CR. Kinase activity controls the sorting of the epidermal growth factor receptor within the multivesicular body. Cell. 1990;61:623-634.
47. Kleijmeer M, Ramm G, Schuurhuis D, et al. Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells. J Cell Biol. 2001;155:53-63.
48. Chow A, Toomre D, Garrett W, Mellman I. Dendritic cell maturation triggers retrograde MHC class II transport from lysosomes to the plasma membrane. Nature. 2002;418:988-994.
49. Merad M, Fong L, Bogenberger J, Engelman EG. Differentiation of myeloid dendritic cells into CD8α-positive dendritic cells in vivo. Blood. 2000;96:1865-1872.
50. + dendritic cells originate from the CD8alpha- dendritic cell subset by a maturation process involving CD8alpha, DEC-205, and CD24 up-regulation. Blood. 2002;99:999-1004.
51. - dendritic cell subset. Blood. 2003;102:601-604.
52. Karlsson M, Lundin S, Dahlgren U, Kahu H, Pettersson I, Telemo E. "Tolerosomes" are produced by intestinal epithelial cells. Eur J Immunol. 2001;31:2892-2900.
53. Peche H, Heslam M, Usal C, Amigorena S, Cuturi MC. Presentation of donor major histocompatibility complex antigens by bone marrow dendritic cell-derived exosomes modulates allograft rejection. Transplantation. 2003;76:1503-1510.
54. Stuart LM, Lucas M, Simpson C, Lamb J, Savill J, Lacy-Hulbert A. Inhibitory effects of apoptotic cell ingestion upon endotoxin-driven myeloid dendritic cell maturation. J Immunol. 2002;168:1627-1635.
55. (+) dendritic cell is responsible for inducing peripheral self-tolerance to tissue-associated antigens. J Exp Med. 2002;196:1099-1104.
56. Morelli AE, Thomson AW. Dendritic cells: regulators of alloimmunity and opportunities for tolerance induction. Immunol Rev. 2003;196:125-146.