Exosomes derived from Rab27a-overexpressing tumor cells elicit efficient induction of antitumor immunity

Molecular Medicine Reports

Volumn 8, Issue 6, 2013, Pages 1876-1882

  Li, Wenhai ^a   Mu, Deguang ^b   Tian, Feng ^a   Hu, Yunsheng ^a   Jiang, Tao ^a   Han, Yong ^a   Chen, Jiakuan ^a   Han, Guoliang ^a   Li, Xiaofei ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Exosomes; Non small cell lung cancer; Rab27a; Tumor immunotherapy

Indexed keywords

B7 ANTIGEN; CANCER VACCINE; CD63 ANTIGEN; CD86 ANTIGEN; CD9 ANTIGEN; EXOSOME CANCER VACCINE; GAMMA INTERFERON; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; INTERLEUKIN 1BETA; INTERLEUKIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; RAB27A PROTEIN; RANTES; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYTOKINE; RAB PROTEIN; RAB27A PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER SIZE; CD4+ T LYMPHOCYTE; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DENDRITIC CELL; EXOSOME; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNIZATION; IN VITRO STUDY; IN VIVO STUDY; LUNG NON SMALL CELL CANCER; LYMPHOCYTE PROLIFERATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; SPLEEN CELL; TUMOR IMMUNITY; UPREGULATION; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL DIFFERENTIATION; IMMUNITY; IMMUNOLOGY; METABOLISM; NEOPLASM; PATHOLOGY; SPLEEN;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOKINES; DENDRITIC CELLS; EXOSOMES; HUMANS; IMMUNITY; MICE; MICE, INBRED BALB C; NEOPLASMS; RAB GTP-BINDING PROTEINS; SPLEEN;

EID: 84893786295     PISSN: 17912997     EISSN: 17913004     Source Type: Journal    
DOI: 10.3892/mmr.2013.1738     Document Type: Article

References (41)

1. Jemal A, Siegel R, Ward E, et al: Cancer statistics, 2007. CA Cancer J Clin 57: 43-66, 2007.
2. Schiller JH, Harrington D, Belani CP, et al: Comparison of four chemotherapy regimens for advanced non-small-cell lung cancer. N Engl J Med 346: 92-98, 2002.
3. Thomas L: On immunosurveillance in human cancer. Yale J Biol Med 55: 329-333, 1982.
4. Kaplan DH, Shankaran V, Dighe AS, et al: Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci USA 95: 7556-7561, 1998.
5. Shankaran V, Ikeda H, Bruce AT, et al: IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410: 1107-1111, 2001.
6. 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 7: 297-303, 2001.
7. Navabi H, Croston D, Hobot J, et al: Preparation of human ovarian cancer ascites-derived exosomes for a clinical trial. Blood Cells Mol Dis 35: 149-152, 2005.
8. Pan BT and Johnstone RM: Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell 33: 967-978, 1983.
9. Harding C, Heuser J and Stahl P: Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol 97: 329-339, 1983.
10. Pan BT, Teng K, Wu C, Adam M and Johnstone RM: Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol 101: 942-948, 1985.
11. Yang C and Robbins PD: The roles of tumor-derived exosomes in cancer pathogenesis. Clin Dev Immunol 2011: 842849, 2011.
12. Stoorvogel W, Kleijmeer MJ, Geuze HJ and Raposo G: The biogenesis and functions of exosomes. Traffic 3: 321-330, 2002.
13. Mignot G, Roux S, Thery C, Ségura E and Zitvogel L: Prospects for exosomes in immunotherapy of cancer. J Cell Mol Med 10: 376-388, 2006.
14. Valadi H, Ekström K, Bossios A, et al: Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659, 2007.
15. Subra C, Laulagnier K, Perret B and Record M: Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies. Biochimie 89: 205-212, 2007.
16. Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A and Ratajczak MZ: Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 20: 1487-1495, 2006.
17. 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 4: 594-600, 1998.
18. Raposo G, Nijman HW, Stoorvogel W, et al: B lymphocytes secrete antigen-presenting vesicles. J Exp Med 183: 1161-1172, 1996.
19. Ostrowski M, Carmo NB, Krumeich S, et al: Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 12: 19-30; sup pp 11-13, 2010.
20. Zerial M and McBride H: Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2: 107-117, 2001.
21. Johnson JL, Brzezinska AA, Tolmachova T, et al: Rab27a and Rab27b regulate neutrophil azurophilic granule exocytosis and NADPH oxidase activity by independent mechanisms. Traffic 11: 533-547, 2010.
22. Griscelli C, Durandy A, Guy-Grand D, et al: A syndrome associating partial albinism and immunodeficiency. Am J Med 65: 691-702, 1978.
23. Klein C, Philippe N, Le Deist F, et al: Partial albinism with immunodeficiency (Griscelli syndrome). J Pediatr 125: 886-895, 1994.
24. Munafó DB, Johnson JL, Ellis BA, et al: Rab27a is a key component of the secretory machinery of azurophilic granules in granulocytes. Biochem J 402: 229-239, 2007.
25. Guo J, Wang B, Zhang M, et al: Macrophage-derived chemokine gene transfer results in tumor regression in murine lung carcinoma model through efficient induction of antitumor immunity. Gene Ther 9: 793-803, 2002.
26. Chaput N, Taïeb J, Schartz NE, et al: Exosome-based immunotherapy. Cancer Immunol Immunother 53: 234-239, 2004.
27. Chen W, Wang J, Shao C, et al: Efficient induction of antitumor T cell immunity by exosomes derived from heat-shocked lymphoma cells. Eur J Immunol 36: 1598-1607, 2006.
28. Lv LH, Wan YL, Lin Y, et al: Anticancer drugs cause release of exosomes with heat shock proteins from human hepatocellular carcinoma cells that elicit effective natural killer cell antitumor responses in vitro. J Biol Chem 287: 15874-15885, 2012.
29. Desnos C, Schonn JS, Huet S, et al: Rab27A and its effector MyRIP link secretory granules to F-actin and control their motion towards release sites. J Cell Biol 163: 559-570, 2003.
30. Stinchcombe JC, Barral DC, Mules EH, et al: Rab27a is required for regulated secretion in cytotoxic T lymphocytes. J Cell Biol 152: 825-834, 2001.
31. Barral DC, Ramalho JS, Anders R, et al: Functional redundancy of Rab27 proteins and the pathogenesis of Griscelli syndrome. J Clin Invest 110: 247-257, 2002.
32. Bobrie A, Krumeich S, Reyal F, et al: Rab27a supports exosome-dependent and -independent mechanisms that modify the tumor microenvironment and can promote tumor progression. Cancer Res 72: 4920-4930, 2012.
33. Peinado H, Ale-kovi? M, Lavotshkin S, et al: Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 18: 883-891, 2012.
34. Cho BK, Palliser D, Guillen E, et al: A proposed mechanism for the induction of cytotoxic T lymphocyte production by heat shock fusion proteins. Immunity 12: 263-272, 2000.
35. Fowler DW, Copier J, Wilson N, Dalgleish AG and Bodman-Smith MD: Mycobacteria activate γ? T-cell anti-tumour responses via cytokines from type 1 myeloid dendritic cells: a mechanism of action for cancer immunotherapy. Cancer Immunol Immunother 61: 535-547, 2012.
36. Tan A, De La Peña H and Seifalian AM: The application of exosomes as a nanoscale cancer vaccine. Int J Nanomedicine 5: 889-900, 2010.
37. Morse MA, Garst J, Osada T, et al: A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. J Transl Med 3: 9, 2005.
38. Dai S, Wei D, Wu Z, et al: Phase I clinical trial of autologous ascites-derived exosomes combined with GM-CSF for colorectal cancer. Mol Ther 16: 782-790, 2008.
39. Guo F, Chang CK, Fan HH, et al: Anti-tumour effects of exosomes in combination with cyclophosphamide and polyinosinic-polycytidylic acid. J Int Med Res 36: 1342-1353, 2008.
40. Hao S, Ye Z, Yang J, Bai O and Xiang J: Intradermal vaccination of dendritic cell-derived exosomes is superior to a subcutaneous one in the induction of antitumor immunity. Cancer Biother Radiopharm 21: 146-154, 2006.
41. Hao S, Bai O, Yuan J, Qureshi M and Xiang J: Dendritic cell-derived exosomes stimulate stronger CD8+ CTL responses and antitumor immunity than tumor cell-derived exosomes. Cell Mol Immunol 3: 205-211, 2006.