Rab27-Dependent exosome production inhibits chronic inflammation and enables acute responses to inflammatory stimuli

Journal of Immunology

Volumn 199, Issue 10, 2017, Pages 3559-3570

  Alexander, Margaret ^a   Ramstead, Andrew G ^a   Bauer, Kaylyn M ^a   Lee, Soh Hyun ^a   Runtsch, Marah C ^a   Wallace, Jared ^a   Huffaker, Thomas B ^a   Larsen, Dane K ^a   Tolmachova, Tanya ^b   Seabra, Miguel C ^b   Round, June L ^a   Ward, Diane M ^a   O'Connell, Ryan M ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; ENDOTOXIN; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 3; MICRORNA 155; NUCLEOTIDE BINDING PROTEIN; RAB27A PROTEIN; RAB27B PROTEIN; SHC SIGNALING ADAPTOR PROTEIN; SRC HOMOLOGY 2 DOMAIN CONTAINING INOSITOL 5 PHOSPHATASE 1; UNCLASSIFIED DRUG; AUTACOID; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; MICRORNA; MIRN155 MICRORNA, MOUSE; RAB PROTEIN; RAB27A PROTEIN, MOUSE; RAB27B PROTEIN, MOUSE; RAS RELATED PROTEIN RAB 27A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CELLULAR SECRETION; CHRONIC INFLAMMATION; CONTROLLED STUDY; EXOSOME; FEMALE; HEMATOPOIETIC CELL; HEMATOPOIETIC SYSTEM; HOMEOSTASIS; KNOCKOUT MOUSE; MALE; MOUSE; MYELOPROLIFERATIVE DISORDER; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STIMULUS; UPREGULATION; WILD TYPE; ACUTE DISEASE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL PROLIFERATION; CHRONIC DISEASE; COMPARATIVE STUDY; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; INFLAMMATION; METABOLISM; PATHOLOGY;

ACUTE DISEASE; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CHRONIC DISEASE; CYTOKINES; EXOSOMES; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; IMMUNE TOLERANCE; INFLAMMATION; INFLAMMATION MEDIATORS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; MYELOID CELLS; RAB GTP-BINDING PROTEINS; RAB27 GTP-BINDING PROTEINS;

EID: 85033407954     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1700904     Document Type: Article

References (44)

1. Xu, H., G. T. Barnes, Q. Yang, G. Tan, D. Yang, C. J. Chou, J. Sole, A. Nichols, J. S. Ross, L. A. Tartaglia, and H. Chen. 2003. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 112: 1821-1830.
2. Alexander, M., and R. M. OConnell. 2015. Noncoding RNAs and chronic inflammation: micro-managing the fire within. BioEssays 37: 1005-1015.
3. Hu, R., D. A. Kagele, T. B. Huffaker, M. C. Runtsch, M. Alexander, J. Liu, E. Bake, W. Su, M. A. Williams, D. S. Rao, et al. 2014. miR-155 promotes T follicular helper cell accumulation during chronic, low-grade inflammation. Immunity 41: 605-619.
4. Mittelbrunn, M., and F. Sánchez-Madrid. 2012. Intercellular communication: diverse structures for exchange of genetic information. Nat. Rev. Mol. Cell Biol. 13: 328-335.
5. Ramachandran, S., and V. Palanisamy. 2012. Horizontal transfer of RNAs: exosomes as mediators of intercellular communication. Wiley Interdiscip. Rev. RNA 3: 286-293.
6. Robbins, P. D., and A. E. Morelli. 2014. Regulation of immune responses by extracellular vesicles. Nat. Rev. Immunol. 14: 195-208.
7. Valadi, H., K. Ekström, A. Bossios, M. Sjöstrand, J. J. Lee, and J. O. Lötvall. 2007. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9: 654-659.
8. Stoorvogel, W., M. J. Kleijmeer, H. J. Geuze, and G. Raposo. 2002. The biogenesis and functions of exosomes. Traffic 3: 321-330.
9. Okoye, I. S., S. M. Coomes, V. S. Pelly, S. Czieso, V. Papayannopoulos, T. Tolmachova, M. C. Seabra, and M. S. Wilson. 2014. MicroRNA-containing T-regulatory-cell-derived exosomes suppress pathogenic T helper 1 cells. Immunity 41: 89-103.
10. Kosaka, N., H. Iguchi, Y. Yoshioka, F. Takeshita, Y. Matsuki, and T. Ochiya. 2010. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J. Biol. Chem. 285: 17442-17452.
11. Alexander, M., R. Hu, M. C. Runtsch, D. A. Kagele, T. L. Mosbruger, T. Tolmachova, M. C. Seabra, J. L. Round, D. M. Ward, and R. M. OConnell. 2015. Exosome-delivered microRNAs modulate the inflammatory response to endotoxin. Nat. Commun. 6: 7321-7337.
12. Montecalvo, A., A. T. Larregina, W. J. Shufesky, D. B. Stolz, M. L. G. Sullivan, J. M. Karlsson, C. J. Baty, G. A. Gibson, G. Erdos, Z. Wang, et al. 2012. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 119: 756-766.
13. Mittelbrunn, M., C. Gutiérrez-Vázquez, C. Villarroya-Beltri, S. González, F. Sánchez-Cabo, M. A . González, A. Bernad, and F. Sánchez-Madrid. 2011. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigenpresenting cells. Nat. Commun. 2: 282-292.
14. Li, J., K. Liu, Y. Liu, Y. Xu, F. Zhang, H. Yang, J. Liu, T. Pan, J. Chen, M. Wu, et al. 2013. Exosomes mediate the cell-To-cell transmission of IFN-A-induced antiviral activity. Nat. Immunol. 14: 793-803.
15. Balusu, S., E. Van Wonterghem, R. De Rycke, K. Raemdonck, S. Stremersch, K. Gevaert, M. Brkic, D. Demeestere, V. Vanhooren, A. Hendrix, et al. 2016. Identification of a novel mechanism of blood-brain communication during peripheral inflammation via choroid plexus-derived extracellular vesicles. EMBO Mol. Med. 8: 1162-1183.
16. Hornick, N. I., B. Doron, S. Abdelhamed, J. Huan, C. A. Harrington, R. Shen, X. A. Cambronne, S. Chakkaramakkil Verghese, and P. Kurre. 2016. AML suppresses hematopoiesis by releasing exosomes that contain microRNAs targeting c-MYB. Sci. Signal. 9: ra88.
17. Ostrowski, M., N. B. Carmo, S. Krumeich, I. Fanget, G. Raposo, A. Savina, C. F. Moita, K. Schauer, A. N. Hume, R. P. Freitas, et al. 2010. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 12: 19-30, 1-13.
18. Tolmachova, T., M. Abrink, C. E. Futter, K. S. Authi, and M. C. Seabra. 2007. Rab27b regulates number and secretion of platelet dense granules. Proc. Natl. Acad. Sci. USA 104: 5872-5877.
19. Singh, R. K., R. C. Furze, M. A. Birrell, S. M. Rankin, A. N. Hume, and M. C. Seabra. 2014. A role for Rab27 in neutrophil chemotaxis and lung recruitment. BMC Cell Biol. 15: 39-48.
20. Johnson, J. L., A. A. Brzezinska, T. Tolmachova, D. B. Munafo, B. A. Ellis, M. C. Seabra, H. Hong, and S. D. Catz. 2010. Rab27a and Rab27b regulate neutrophil azurophilic granule exocytosis and NADPH oxidase activity by independent mechanisms. Traffic 11: 533-547.
21. Biswas, S. K., and E. Lopez-Collazo. 2009. Endotoxin tolerance: new mechanisms, molecules and clinical significance. Trends Immunol. 30: 475-487.
22. Fang, H., R. A. Pengal, X. Cao, L. P. Ganesan, M. D. Wewers, C. B. Marsh, and S. Tridandapani. 2004. Lipopolysaccharide-induced macrophage inflammatory response is regulated by SHIP. J. Immunol. 173: 360-366.
23. OConnell, R. M., A. A. Chaudhuri, D. S. Rao, and D. Baltimore. 2009. Inositol phosphatase SHIP1 is a primary target of miR-155. Proc. Natl. Acad. Sci. USA 106: 7113-7118.
24. Sly, L.M., M. J. Rauh, J. Kalesnikoff, C. H. Song, and G. Krystal. 2004. LPS-induced upregulation of SHIP is essential for endotoxin tolerance. Immunity 21: 227-239.
25. Théry, C., A. Clayton, S. Amigorena, and G. Raposo. 2006. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. Chapter 3: Unit 3.22.
26. Bala, S., M. Marcos, K. Kodys, T. Csak, D. Catalano, P. Mandrekar, and G. Szabo. 2011. Up-regulation of microRNA-155 in macrophages contributes to increased tumor necrosis factor a (TNFa) production via increased mRNA halflife in alcoholic liver disease. J. Biol. Chem. 286: 1436-1444.
27. An, H., H. Xu, M. Zhang, J. Zhou, T. Feng, C. Qian, R. Qi, and X. Cao. 2005. Src homology 2 domain-containing inositol-5-phosphatase 1 (SHIP1) negatively regulates TLR4-mediated LPS response primarily through a phosphatase activity-And PI-3K-independent mechanism. Blood 105: 4685-4692.
28. Bala, S., T. Csak, K. Kodys, D. Catalano, A. Ambade, I. Furi, P. Lowe, Y. Cho, A. Iracheta-Vellve, and G. Szabo. 2017. Alcohol-induced miR-155 and HDAC11 inhibit negative regulators of the TLR4 pathway and lead to increased LPS responsiveness of Kupffer cells in alcoholic liver disease. J. Leukoc. Biol. 102: 487-498.
29. Théry, C., M. Ostrowski, and E. Segura. 2009. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9: 581-593.
30. Iborra, M., F. Bernuzzi, C. Correale, S. Vetrano, G. Fiorino, B. Beltrán, F. Marabita, M. Locati, A. Spinelli, P. Nos, et al. 2013. Identification of serum and tissue micro-RNA expression profiles in different stages of inflammatory bowel disease. Clin. Exp. Immunol. 173: 250-258.
31. Taylor, D. D., and C. Gercel-Taylor. 2008. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 110: 13-21.
32. Wu, L., X. Dai, J. Zhan, Y. Zhang, H. Zhang, H. Zhang, S. Zeng, and W. Xi. 2015. Profiling peripheral microRNAs in obesity and type 2 diabetes mellitus. APMIS 123: 580-585.
33. Zeelenberg, I. S., M. Ostrowski, S. Krumeich, A. Bobrie, C. Jancic, A. Boissonnas, A. Delcayre, J. B. Le Pecq, B. Combadière, S. Amigorena, and C. Théry. 2008. Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses. Cancer Res. 68: 1228-1235.
34. Stinchcombe, J. C., D. C. Barral, E. H. Mules, S. Booth, A. N. Hume, L. M. Machesky, M. C. Seabra, and G. M. Griffiths. 2001. Rab27a is required for regulated secretion in cytotoxic T lymphocytes. J. Cell Biol. 152: 825-834.
35. Shimada-Sugawara, M., E. Sakai, K. Okamoto, M. Fukuda, T. Izumi, N. Yoshida, and T. Tsukuba. 2015. Rab27A regulates transport of cell surface receptors modulating multinucleation and lysosome-related organelles in osteoclasts. Sci. Rep. 5: 9620-9631.
36. Jancic, C., A. Savina, C. Wasmeier, T. Tolmachova, J. El-Benna, P. M. Dang, S. Pascolo, M. A. Gougerot-Pocidalo, G. Raposo, M. C. Seabra, and S. Amigorena. 2007. Rab27a regulates phagosomal pH and NADPH oxidase recruitment to dendritic cell phagosomes. Nat. Cell Biol. 9: 367-378.
37. Johnson, J. L., H. Hong, J. Monfregola, and S. D. Catz. 2011. Increased survival and reduced neutrophil infiltration of the liver in Rab27a-but not Munc13-4-deficient mice in lipopolysaccharide-induced systemic inflammation. Infect. Immun. 79: 3607-3618.
38. 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.
39. Zitvogel, L., A. Regnault, A. Lozier, J. Wolfers, C. Flament, D. Tenza, P. Ricciardi-Castagnoli, G. Raposo, and S. Amigorena. 1998. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat. Med. 4: 594-600.
40. Viaud, S., M. Terme, C. Flament, J. Taieb, F. André, S. Novault, B. Escudier, C. Robert, S. Caillat-Zucman, T. Tursz, et al. 2009. Dendritic cell-derived exosomes promote natural killer cell activation and proliferation: A role for NKG2D ligands and IL-15Ralpha. PLoS One 4: e4942.
41. Bala, S., J. Petrasek, S. Mundkur, D. Catalano, I. Levin, J. Ward, H. Alao, K. Kodys, and G. Szabo. 2012. Circulating microRNAs in exosomes indicate hepatocyte injury and inflammation in alcoholic, drug-induced, and inflammatory liver diseases. Hepatology 56: 1946-1957.
42. Shurtleff, M. J., M. M. Temoche-Diaz, K. V. Karfilis, S. Ri, and R. Schekman. 2016. Y-box protein 1 is required to sort microRNAs into exosomes in cells and in a cell-free reaction. eLife 5: e19276.
43. Villarroya-Beltri, C., C. Gutiérrez-Vázquez, F. Sánchez-Cabo, D. Pérez-Hernández, J. Vázquez, N. Martin-Cofreces, D. J. Martinez-Herrera, A. Pascual-Montano, M. Mittelbrunn, and F. Sánchez-Madrid. 2013. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat. Commun. 4: 2980-2990.
44. Santangelo, L., G. Giurato, C. Cicchini, C. Montaldo, C. Mancone, R. Tarallo, C. Battistelli, T. Alonzi, A. Weisz, and M. Tripodi. 2016. The RNA-binding protein SYNCRIP is a component of the hepatocyte exosomal machinery controlling microRNA sorting. Cell Reports 17: 799-808.