The potential of exosomes in immunotherapy

Expert Opinion on Biological Therapy

Volumn 5, Issue 6, 2005, Pages 737-747

  Chaput, Nathalie ^a   Taïeb, Julien ^a,b   André, Fabrice ^a   Zitvogel, Laurence ^a  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

Cross presentation; Exosomes; Immunotherapy; MHC complexes; Tumour

Indexed keywords

CANCER VACCINE; LIPID; PROTEIN;

ANTINEOPLASTIC ACTIVITY; B LYMPHOCYTE; BIOGENESIS; CANCER THERAPY; CROSS PRESENTATION; DENDRITIC CELL; ENDOSOME; EXOCYTOSIS; EXOSOME; EXTRACELLULAR SPACE; HUMAN; IMMUNOGENICITY; IMMUNOREGULATION; IMMUNOSTIMULATION; IMMUNOTHERAPY; LIPID COMPOSITION; MAJOR HISTOCOMPATIBILITY COMPLEX; MEMBRANE VESICLE; MOUSE; NONHUMAN; PROTEIN ANALYSIS; REVIEW;

ANIMALS; ANTIGENS, NEOPLASM; B-LYMPHOCYTES; CANCER VACCINES; CELL LINE, TUMOR; CLINICAL TRIALS; CYTOPLASMIC VESICLES; DENDRITIC CELLS; HUMANS; IMMUNOTHERAPY; MELANOMA; MICE; NEOPLASMS, EXPERIMENTAL; RETICULOCYTES; T-LYMPHOCYTES; VACCINES, SUBUNIT;

EID: 21044443292     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.5.6.737     Document Type: Review

References (58)

1. ANDRE F, SCHARTZ NE, MOVASSAGH M et al.: Malignant effusions and immunogenic tumour-derived exosomes. Lancet (2002) 360(9329):295-305. First observation describing that tumour cell-derived exosomes are founded in vivo in cancer-bearing patients. These TEX could be used as a novel source of tumour antigens.
2. DENZER K, KLEIJMEER MJ, HEIJNEN HF et al.: Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J. Cell Sci. (2000) 113(Pt 19):3365-3374.
3. DENZER K, VAN EIJK M, KLEIJMEER MJ et al.: Follicular dendritic cells carry MHC class II-expressing microvesicles at their surface. J. Immunol. (2000) 165(3):1259-1265.
4. QUAH B, O'NEILL HC: Review: the application of dendritic cell-derived exosomes in tumour immunotherapy. Cancer Biother. Radiopharm. (2000) 15(2):185-194.
5. 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(3):297-303. This work was the first to demonstrate that exosomes secreted by tumour cell lines can have immunological bioactivity in vitro and in vivo.
6. 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(5):594-600. This is the reference article of DEX that highlights the potential antitumour activity of these vesicles.
7. JOHNSTONE RM, ADAM M, HAMMOND JR et al.: Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J. Biol. Chem. (1987) 262(19):9412-9420. This is one of the first descriptions of exosomes as vesicles secreted by living cells.
8. ARNOLD PY, MANNIE MD: Vesicles bearing MHC class II molecules mediate transfer of antigen from antigen-presenting cells to CD4+ T cells. Eur. J. Immunol. (1999) 29(4):1363-1373.
9. ESCOLA JM, KLEIJMEER MJ, STOORVOGEL W et al.: 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(32):20121-20127.
10. GEMINARD C, NAULT F, JOHNSTONE RM et al.: Characteristics of the interaction between Hsc70 and the transferrin receptor in exosomes released during reticulocyte maturation. J. Biol. Chem. (2001) 276(13):9910-9916.
11. HEIJNEN IA, VAN VUGT MJ, FANGER NA et al.: Antigen targeting to myeloid-specific human Fc gamma RI/ CD64 triggers enhanced antibody responses in transgenic mice. J. Clin. Invest. (1996) 97(2):331-338.
12. HESS C, SADALLAH S, HEFTI A et al.: Ectosomes released by human neutrophils are specialized functional units. J. Immunol. (1999) 163(8):4564-4573.
13. PATEL DM, ARNOLD PY, WHITE GA et al.: Class II MHC/peptide complexes are released from APC and are acquired by T cell responders during specific antigen recognition. J. Immunol. (1999) 163(10):5201-5210.
14. RAPOSO G, TENZA D, MECHERI S et al.: Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation. Mol. Biol. Cell (1997) 8(12):2631-2645.
15. SKOKOS D, LE PANSE S, VILLA I et al.: Mast cell-dependent B and T lymphocyte activation is mediated by the secretion of immunologically active exosomes. J. Immunol. (2001) 166(2):868-876.
16. THERY C, ZITVOGEL L, AMIGORENA S: Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. (2002) 2(8):569-579.
17. BLANCHARD N, LANKAR D, FAURE F et al.: TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/zeta complex. J. Immunol. (2002) 168(7):3235-3241.
18. LAULAGNIER K, GRAND D, DUJARDIN A et al.: PLD2 is enriched on exosomes and its activity is correlated to the release of exosomes. FEBS Lett. (2004) 572(1-3):11-14. This work suggests that exosome formation is a regulated mechanism.
19. SAVINA A, VIDAL M, COLOMBO MI: The exosome pathway in K562 cells is regulated by Rab11. J. Cell Sci. (2002) 115(Pt 12):2505-2515.
20. TOLMACHOVA T, ANDERS R, STINCHCOMBE J et al.: A general role for Rab27a in secretory cells. Mol. Biol. Cell (2004) 15(1):332-344.
21. 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(1):53-63.
22. RAPOSO G, MOORE M, INNES D et al.: Human macrophages accumulate HIV-1 particles in MHC II compartments. Traffic (2002) 3(10):718-729.
23. STOORVOGEL W, KLEIJMEER MJ, GEUZE HJ et al.: The biogenesis and functions of exosomes. Traffic (2002) 3(5):321-330.
24. 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(12):7309-7318. This work describes extensively DEX protein composition and demonstrates clearly that they are different from apoptotic bodies.
25. LAULAGNIER K, MOTTA C, HAMDI S et al.: Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem. J. (2004) 380(Pt 1):161-171. The authors show that lipid composition of exosomes could be used as a specific marker for exosome characterisation.
26. + T cells in vivo in a murine model.
27. LAMPARSKI HG, METHA-DAMANI A, YAO JY et al.: Production and characterization of clinical grade exosomes derived from dendritic cells. J. Immunol. Methods (2002) 270(2):211-226. This work describes very extensively how to purify DEX for clinical use. This process was used for the first clinical trial using DEX in cancer patients.
28. ESCUDIER B, DORVAL T, CHAPUT N, et al.: Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of the first phase I clinical trial. J. Transl. Med. (2005) 3(1):10.
29. ESCUDIER B, DORVAL T, ANGEVIN E et al.: Novel approach to immunotherapy of cancer: Phase I trial of dexosome vaccine for patients with advanced melanoma. Proc. Am. Soc. Clin. Oncol. (2002):A1857.
30. HSU DH, PAZ P, VILLAFLOR G et al.: Exosomes as a tumor vaccine: enhancing potency through direct loading of antigenic peptides. J. Immunother. (2003) 26(5):440-450.
31. HARDING C, HEUSER J, STAHL P: Endocytosis and intracellular processing of transferrin and colloidal gold-transferrin in rat reticulocytes: demonstration of a pathway for receptor shedding. Eur. J. Cell Biol. (1984) 35(2):256-263.
32. PAN BT, JOHNSTONE RM: Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell (1983) 33(3):967-978. This was the first description of exosomes as vesicles secreted by living cells.
33. RIEU S, GEMINARD C, RABESANDRATANA H et al.: Exosomes released during reticulocyte maturation bind to fibronectin via integrin alpha4beta1. Eur. J. Biochem. (2000) 267(2):583-590.
34. RAPOSO G, NIJMAN HW, STOORVOGEL W et al.: B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. (1996) 183(3):1161-1172. First work to suggest that exosomes can have immunological activities.
35. CLAYTON A, TURKES A, DEWITT S et al.: Adhesion and signaling by B cell-derived exosomes: the role of integrins. FASEB J. (2004) 18(9):977-979.
36. 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(6):3037-3045.
37. VAN NIEL G, RAPOSO G, CANDALH C et al.: Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology (2001) 121(2):337-349.
38. KARLSSON M, LUNDIN S, DAHLGREN U et al.: 'Tolerosomes' are produced by intestinal epithelial cells. Eur. J. Immunol. (2001) 31(10):2892-2900.
39. VAN NIEL G, HEYMAN M: The epithelial cell cytoskeleton and intracellular trafficking. II. Intestinal epithelial cell exosomes: perspectives on their structure and function. Am. J. Physiol. Gastrointest. Liver Physiol. (2002) 283(2):G251-G255.
40. VAN NIEL G, MALLEGOL J, BEVILACQUA C et al.: Intestinal epithelial exosomes carry MHC class II/peptides able to inform the immune system in mice. Gut (2003) 52(12):1690-1697.
41. HEIJNEN HF, SCHIEL AE, FIJNHEER R et al.: 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(11):3791-3799.
42. JANISZEWSKI M, DO CARMO AO, PEDRO MA et al.: Platelet-derived exosomes of septic individuals possess proapoptotic NAD(P)H oxidase activity: a novel vascular redox pathway. Crit. Care Med. (2004) 32(3):818-825.
43. KELLER R: Dendritic cells: their significance in health and disease. Immunol. Lett. (2001) 78(3):113-122.
44. 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(3):599-610.
45. BANCHEREAU J, BRIERE F, CAUX C et al.: Immunobiology of dendritic cells. Annu. Rev. Immunol. (2000) 18:767-811.
46. PECHE H, HESLAN M, USAL C et al.: Presentation of donor major histocompatibility complex antigens by bone marrow dendritic cell-derived exosomes modulates allograft rejection. Transplantation (2003) 76(10):1503-1510.
47. ALTIERI SL, KHAN AN, TOMASI TB: Exosomes from plasmacytoma cells as a tumor vaccine. J. Immunother. (2004) 27(4):282-288.
48. HEGMANS JP, BARD MP, HEMMES A et al.: Proteomic analysis of exosomes secreted by human mesothelioma cells. Am. J. Pathol. (2004) 164(5):1807-1815.
49. RITEAU B, FAURE F, MENIER C et al.: Exosomes bearing HLA-G are released by melanoma cells. Hum. Immunol. (2003) 64(11):1064-1072.
50. + T cell responses in vitro in normal volunteers and in vivo in a murine model.
51. + T cells leading to tumour regression.
52. FIRAT H, COCHET M, ROHRLICH PS et al.: Comparative analysis of the CD8(+) T cell repertoires of H-2 class I wild-type/HLA-A2.1 and H-2 class I knockout/HLA-A2.1 transgenic mice. Int. Immunol. (2002) 14(8):925-934.
53. CURIEL TJ, COUKOS G, ZOU L et al.: Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. (2004) 10(9):942-949.
54. SAKAGUCHI S: Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. (2004) 22:531-562.
55. VIGUIER M, LEMAITRE F, VEROLA O et al.: Foxp3 expressing CD4+CD25(high) regulatory T cells are overrepresented in human metastatic melanoma lymph nodes and inhibit the function of infiltrating T cells. J. Immunol. (2004) 173(2):1444-1453.
56. GHIRINGHELLI F, LARMONIER N, SCHMITT E et al.: CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur. J. Immunol. (2004) 34(2):336-344.
57. ESCUDIER B, ANGEVIN E, LANTZ O et al.: Preclinical and clinical development of dexosome-based immunotherapy for advanced cancer. Annual Meeting of the American Association for Cancer Research (2003):Abstract #2981, p681.
58. ALINE F, BOUT D, AMIGORENA S et al.: Toxoplasma gondii antigen-pulsed-dendritic cell-derived exosomes induce a protective immune response against T. gondii infection. Infect. Immun. (2004) 72(7):4127-4137.