Epithelial cell-derived microvesicles activate macrophages and promote inflammation via microvesicle-containing microRNAs

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Lee, Heedoo ^a   Zhang, Duo ^a   Zhu, Ziwen ^a   Dela Cruz, Charles S ^b   Jin, Yang ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA;

BRONCHOALVEOLAR LAVAGE FLUID; CYTOLOGY; EPITHELIUM CELL; HUMAN; INFLAMMATION; MACROPHAGE ACTIVATION; METABOLISM; PATHOPHYSIOLOGY;

BRONCHOALVEOLAR LAVAGE FLUID; EPITHELIAL CELLS; HUMANS; INFLAMMATION; MACROPHAGE ACTIVATION; MICRORNAS;

EID: 84991043221     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep35250     Document Type: Article

References (50)

1. Pitt, J. M., Kroemer, G., Zitvogel, L. Extracellular vesicles: masters of intercellular communication and potential clinical interventions. J Clin Invest 126, 1139-1143, doi: 10. 1172/JCI87316 (2016).
2. Tkach, M., Thery, C. Communication by Extracellular Vesicles: Where We Are and Where We Need to Go. Cell 164, 1226-1232, doi: 10. 1016/j. cell. 2016. 01. 043 (2016).
3. Liu, Y., Cao, X. Organotropic metastasis: role of tumor exosomes. Cell Res 26, 149-150, doi: 10. 1038/cr. 2015. 153 (2016).
4. Hoshino, A. et al. Tumour exosome integrins determine organotropic metastasis. Nature 527, 329-335, doi: 10. 1038/nature15756 (2015).
5. Malda, J., Boere, J., van de Lest, C. H., van Weeren, P. R., Wauben, M. H. Extracellular vesicles-new tool for joint repair and regeneration. Nat Rev Rheumatol 12, 243-249, doi: 10. 1038/nrrheum. 2015. 170 (2016).
6. Nawaz, M. et al. The emerging role of extracellular vesicles as biomarkers for urogenital cancers. Nat Rev Urol 11, 688-701, doi: 10. 1038/nrurol. 2014. 301 (2014).
7. Martin, T. R. Cytokines and the acute respiratory distress syndrome (ARDS): a question of balance. Nat Med 3, 272-273 (1997).
8. Matthay, M. A., Ware, L. B., Zimmerman, G. A. The acute respiratory distress syndrome. J Clin Invest 122, 2731-2740, doi: 10. 1172/JCI60331 (2012).
9. Whitsett, J. A., Alenghat, T. Respiratory epithelial cells orchestrate pulmonary innate immunity. Nat Immunol 16, 27-35, doi: 10. 1038/ni. 3045 (2015).
10. Nold, M. F. et al. IL-37 is a fundamental inhibitor of innate immunity. Nat Immunol 11, 1014-1022, doi: 10. 1038/ni. 1944 (2010).
11. Lamm, W. J., Luchtel, D., Albert, R. K. Sites of leakage in three models of acute lung injury. J Appl Physiol (1985) 64, 1079-1083 (1988).
12. Li, X., Shu, R., Filippatos, G., Uhal, B. D. Apoptosis in lung injury and remodeling. J Appl Physiol (1985) 97, 1535-1542, doi: 10. 1152/japplphysiol. 00519. 2004 (2004).
13. Jiang, D., Liang, J., Noble, P. W. Regulation of non-infectious lung injury, inflammation, and repair by the extracellular matrix glycosaminoglycan hyaluronan. Anat Rec (Hoboken) 293, 982-985, doi: 10. 1002/ar. 21102 (2010).
14. Moon, H. G. et al. Lung epithelial cell-derived extracellular vesicles activate macrophage-mediated inflammatory responses via ROCK1 pathway. Cell Death Dis 6, e2016, doi: 10. 1038/cddis. 2015. 282 (2015).
15. Tao, F., Kobzik, L. Lung macrophage-epithelial cell interactions amplify particle-mediated cytokine release. Am J Respir Cell Mol Biol 26, 499-505, doi: 10. 1165/ajrcmb. 26. 4. 4749 (2002).
16. Matute-Bello, G., Frevert, C. W., Martin, T. R. Animal models of acute lung injury. Am J Physiol Lung Cell Mol Physiol 295, L379-L399, doi: 10. 1152/ajplung. 00010. 2008 (2008).
17. Divangahi, M., King, I. L., Pernet, E. Alveolar macrophages and type I IFN in airway homeostasis and immunity. Trends Immunol 36, 307-314, doi: 10. 1016/j. it. 2015. 03. 005 (2015).
18. Kopf, M., Schneider, C., Nobs, S. P. The development and function of lung-resident macrophages and dendritic cells. Nat Immunol 16, 36-44, doi: 10. 1038/ni. 3052 (2015).
19. Budnik, V., Ruiz-Canada, C., Wendler, F. Extracellular vesicles round off communication in the nervous system. Nat Rev Neurosci 17, 160-172, doi: 10. 1038/nrn. 2015. 29 (2016).
20. Thery, C., Ostrowski, M., Segura, E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9, 581-593, doi: 10. 1038/nri2567 (2009).
21. Lee, Y., El Andaloussi, S., Wood, M. J. Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Hum Mol Genet 21, R125-R134, doi: 10. 1093/hmg/dds317 (2012).
22. Xu, R., Greening, D. W., Zhu, H. J., Takahashi, N., Simpson, R. J. Extracellular vesicle isolation and characterization: toward clinical application. J Clin Invest 126, 1152-1162, doi: 10. 1172/JCI81129 (2016).
23. Crescitelli, R. et al. Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J Extracell Vesicles 2, doi: 10. 3402/jev. v2i0. 20677 (2013).
24. Aliotta, J. M. et al. Alteration of marrow cell gene expression, protein production, and engraftment into lung by lung-derived microvesicles: a novel mechanism for phenotype modulation. Stem Cells 25, 2245-2256, doi: 10. 1634/stemcells. 2007-0128 (2007).
25. Muralidharan-Chari, V. et al. ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Curr Biol 19, 1875-1885, doi: 10. 1016/j. cub. 2009. 09. 059 (2009).
26. Andreu, Z., Yanez-Mo, M. Tetraspanins in extracellular vesicle formation and function. Front Immunol 5, 442, doi: 10. 3389/fimmu. 2014. 00442 (2014).
27. Ratajczak, J. et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20, 847-856, doi: 10. 1038/sj. leu. 2404132 (2006).
28. Mittelbrunn, M., Sanchez-Madrid, F. Intercellular communication: diverse structures for exchange of genetic information. Nat Rev Mol Cell Biol 13, 328-335, doi: 10. 1038/nrm3335 (2012).
29. Kogure, T., Yan, I. K., Lin, W. L., Patel, T. Extracellular Vesicle-Mediated Transfer of a Novel Long Noncoding RNA TUC339: A Mechanism of Intercellular Signaling in Human Hepatocellular Cancer. Genes Cancer 4, 261-272, doi: 10. 1177/1947601913499020 (2013).
30. Ha, M., Kim, V. N. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 15, 509-524, doi: 10. 1038/nrm3838 (2014).
31. Zhang, L. et al. Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth. Nature 527, 100-104, doi: 10. 1038/nature15376 (2015).
32. Tominaga, N. et al. Brain metastatic cancer cells release microRNA-181c-containing extracellular vesicles capable of destructing blood-brain barrier. Nat Commun 6, 6716, doi: 10. 1038/ncomms7716 (2015).
33. Fong, M. Y. et al. Breast-cancer-secreted miR-122 reprograms glucose metabolism in premetastatic niche to promote metastasis. Nat Cell Biol 17, 183-194, doi: 10. 1038/ncb3094 (2015).
34. Chevillet, J. R. et al. Quantitative and stoichiometric analysis of the microRNA content of exosomes. Proc Natl Acad Sci USA 111, 14888-14893, doi: 10. 1073/pnas. 1408301111 (2014).
35. Lo Cicero, A., Stahl, P. D., Raposo, G. Extracellular vesicles shuffling intercellular messages: for good or for bad. Curr Opin Cell Biol 35, 69-77, doi: 10. 1016/j. ceb. 2015. 04. 013 (2015).
36. Pospichalova, V. et al. Simplified protocol for flow cytometry analysis of fluorescently labeled exosomes and microvesicles using dedicated flow cytometer. J Extracell Vesicles 4, 25530, doi: 10. 3402/jev. v4. 25530 (2015).
37. Gong, Y., Hart, E., Shchurin, A., Hoover-Plow, J. Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. J Clin Invest 118, 3012-3024, doi: 10. 1172/JCI32750 (2008).
38. Wong, B. et al. Statins suppress THP-1 cell migration and secretion of matrix metalloproteinase 9 by inhibiting geranylgeranylation. J Leukoc Biol 69, 959-962 (2001).
39. Shubayev, V. I. et al. TNFalpha-induced MMP-9 promotes macrophage recruitment into injured peripheral nerve. Mol Cell Neurosci 31, 407-415, doi: 10. 1016/j. mcn. 2005. 10. 011 (2006).
40. Ji, H. et al. Deep sequencing of RNA from three different extracellular vesicle (EV) subtypes released from the human LIM1863 colon cancer cell line uncovers distinct miRNA-enrichment signatures. PLoS One 9, e110314, doi: 10. 1371/journal. pone. 0110314 (2014).
41. Gibbings, D. J., Ciaudo, C., Erhardt, M., Voinnet, O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 11, 1143-1149, doi: 10. 1038/ncb1929 (2009).
42. Choi, D. S., Kim, D. K., Kim, Y. K., Gho, Y. S. Proteomics of extracellular vesicles: Exosomes and ectosomes. Mass Spectrom Rev 34, 474-490, doi: 10. 1002/mas. 21420 (2015).
43. Liang, X. et al. p62 sequestosome 1/light chain 3b complex confers cytoprotection on lung epithelial cells after hyperoxia. Am J Respir Cell Mol Biol 48, 489-496, doi: 10. 1165/rcmb. 2012-0017OC (2013).
44. Moon, H. G., Yang, J., Zheng, Y., Jin, Y. miR-15a/16 regulates macrophage phagocytosis after bacterial infection. J Immunol 193, 4558-4567, doi: 10. 4049/jimmunol. 1401372 (2014).
45. Jin, Y. et al. Caveolin-1 regulates the secretion and cytoprotection of Cyr61 in hyperoxic cell death. FASEB J 23, 341-350, doi: 10. 1096/fj. 08-108423 (2009).
46. Lazaro-Ibanez, E. et al. Different gDNA content in the subpopulations of prostate cancer extracellular vesicles: apoptotic bodies, microvesicles, and exosomes. Prostate 74, 1379-1390, doi: 10. 1002/pros. 22853 (2014).
47. Zhang, D. et al. Thyroid hormone regulates muscle fiber type conversion via miR-133a1. J Cell Biol 207, 753-766, doi: 10. 1083/jcb. 201406068 (2014).
48. Chen, C. et al. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33, e179, doi: 10. 1093/nar/gni178 (2005).
49. Lee, H. D., Kim, Y. H., Kim, D. S. Exosomes derived from human macrophages suppress endothelial cell migration by controlling integrin trafficking. Eur J Immunol 44, 1156-1169, doi: 10. 1002/eji. 201343660 (2014).
50. Lee, H. D., Koo, B. H., Kim, Y. H., Jeon, O. H., Kim, D. S. Exosome release of ADAM15 and the functional implications of human macrophage-derived ADAM15 exosomes. FASEB J 26, 3084-3095, doi: 10. 1096/fj. 11-201681 (2012).