Macrophage-derived extracellular vesicles induce long-lasting immunity against hepatitis C virus which is blunted by polyunsaturated fatty acids

Frontiers in Immunology

Volumn 9, Issue APR, 2018, Pages

  Cai, Chengcong ^a   Koch, Benjamin ^a   Morikawa, Kenichi ^b   Suda, Goki ^b   Sakamoto, Naoya ^b   Rueschenbaum, Sabrina ^a   Akhras, Sami ^c   Dietz, Julia ^a   Hildt, Eberhard ^c   Zeuzem, Stefan ^a   Welsch, Christoph ^a   Lange, Christian M ^a,d  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^b HOKKAIDO UNIVERSITY HOSPITAL   (Japan)

^c PAUL EHRLICH INSTITUT   (Germany)

^d UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

Arachidonic acid; Exosomes; Innate immunity; Interferon; Omega 3 fatty acids

Indexed keywords

ALPHA INTERFERON; GAMMA INTERFERON; INTERFERON; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PEGINTERFERON ALPHA; RIBAVIRIN;

ADAPTIVE IMMUNITY; ANTIVIRAL ACTIVITY; ANTIVIRAL THERAPY; ARTICLE; CAUCASIAN; CHRONIC HEPATITIS C; CONTROLLED STUDY; ELECTRON MICROSCOPY; EXOSOME; FLOW CYTOMETRY; HEPATITIS C VIRUS; HUH-7.5 CELL LINE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; JAPANESE (PEOPLE); MACROPHAGE; MACROPHAGE CULTURE; PERIPHERAL BLOOD MONONUCLEAR CELL; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; RNA SEQUENCE; THP-1 CELL LINE; TRANSMISSION ELECTRON MICROSCOPY; VIRUS IMMUNITY;

EID: 85045317248     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2018.00723     Document Type: Article

References (32)

1. Kalunian KC, Merrill JT, Maciuca R, McBride JM, Townsend MJ, Wei X, et al. A phase II study of the efficacy and safety of rontalizumab (rhuMAb interferon-alpha) in patients with systemic lupus erythematosus (ROSE). Ann Rheum Dis (2016) 75:196-202. doi:10.1136/annrheumdis-2014-206090
2. Heim MH, Thimme R. Innate and adaptive immune responses in HCV infections. J Hepatol (2014) 61:S14-25. doi:10.1016/j.jhep.2014.06.035
3. Schindler C, Levy DE, Decker T. JAK-STAT signaling: from interferons to cytokines. J Biol Chem (2007) 282:20059-63. doi:10.1074/jbc. R700016200
4. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, et al. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature (2011) 472:481-5. doi:10.1038/nature09907
5. Xu R, Greening DW, Zhu HJ, Takahashi N, Simpson RJ. Extracellular vesicle isolation and characterization: toward clinical application. J Clin Invest (2016) 126:1152-62. doi:10.1172/JCI81129
6. Pitt JM, Kroemer G, Zitvogel L. Extracellular vesicles: masters of intercellular communication and potential clinical interventions. J Clin Invest (2016) 126:1139-43. doi:10.1172/JCI87316
7. Lemoinne S, Thabut D, Housset C, Moreau R, Valla D, Boulanger CM, et al. The emerging roles of microvesicles in liver diseases. Nat Rev Gastroenterol Hepatol (2014) 11:350-61. doi:10.1038/nrgastro.2014.7
8. Robbins PD, Dorronsoro A, Booker CN. Regulation of chronic inflammatory and immune processes by extracellular vesicles. J Clin Invest (2016) 126:1173-80. doi:10.1172/JCI81131
9. Schorey JS, Harding CV. Extracellular vesicles and infectious diseases: new complexity to an old story. J Clin Invest (2016) 126:1181-9. doi:10.1172/JCI81132
10. Whiteside TL. Exosomes and tumor-mediated immune suppression. J Clin Invest (2016) 126:1216-23. doi:10.1172/JCI81136
11. Masyuk AI, Masyuk TV, Larusso NF. Exosomes in the pathogenesis, diagnostics and therapeutics of liver diseases. J Hepatol (2013) 59:621-5. doi:10.1016/j.jhep.2013.03.028
12. Giugliano S, Kriss M, Golden-Mason L, Dobrinskikh E, Stone AE, Soto-Gutierrez A, et al. Hepatitis C virus infection induces autocrine interferon signaling by human liver endothelial cells and release of exosomes, which inhibits viral replication. Gastroenterology (2015) 148:392-402.e313. doi:10.1053/j.gastro.2014.10.040
13. Li J, Liu K, Liu Y, Xu Y, Zhang F, Yang H, et al. Exosomes mediate the cell-to-cell transmission of IFN-alpha-induced antiviral activity. Nat Immunol (2013) 14:793-803. doi:10.1038/ni.2647
14. Buckley CD, Gilroy DW, Serhan CN. Proresolving lipid mediators and mechanisms in the resolution of acute inflammation. Immunity (2014) 40:315-27. doi:10.1016/j.immuni.2014.02.009
15. Henson PM. Dampening inflammation. Nat Immunol (2005) 6:1179-81. doi:10.1038/ni1205-1179
16. Blight KJ, Kolykhalov AA, Rice CM. Efficient initiation of HCV RNA replication in cell culture. Science (2000) 290:1972-4. doi:10.1126/science.290.5498.1972
17. Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol (2006) Chapter 3:Unit322. doi:10.1002/0471143030.cb0322s30
18. Cantin R, Diou J, Belanger D, Tremblay AM, Gilbert C. Discrimination between exosomes and HIV-1: purification of both vesicles from cell-free supernatants. J Immunol Methods (2008) 338:21-30. doi:10.1016/j.jim.2008.07.007
19. Lange CM, Gouttenoire J, Duong FH, Morikawa K, Heim MH, Moradpour D. Vitamin D receptor and Jak-STAT signaling crosstalk results in calcitriol-mediated increase of hepatocellular response to IFN-alpha. J Immunol (2014) 192:6037-44. doi:10.4049/jimmunol.1302296
20. Xue J, Schmidt SV, Sander J, Draffehn A, Krebs W, Quester I, et al. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity (2014) 40:274-88. doi:10.1016/j.immuni.2014.01.006
21. Irons R, Fritsche KL. Omega-3 polyunsaturated fatty acids impair in vivo interferon-gamma responsiveness via diminished receptor signaling. J Infect Dis (2005) 191:481-6. doi:10.1086/427264
22. Lange CM, Jacobson IM, Rice CM, Zeuzem S. Emerging therapies for the treatment of hepatitis C. EMBO Mol Med (2014) 6:4-15. doi:10.1002/emmm.201303131
23. Sugano M, Hirahara F. Polyunsaturated fatty acids in the food chain in Japan. Am J Clin Nutr (2000) 71:189S-96S. doi:10.1093/ajcn/71.1.189S
24. Thimme R, Binder M, Bartenschlager R. Failure of innate and adaptive immune responses in controlling hepatitis C virus infection. FEMS Microbiol Rev (2012) 36:663-83. doi:10.1111/j.1574-6976.2011.00319.x
25. Park SH, Rehermann B. Immune responses to HCV and other hepatitis viruses. Immunity (2014) 40:13-24. doi:10.1016/j.immuni.2013.12.010
26. Horner SM, Gale M Jr. Regulation of hepatic innate immunity by hepatitis C virus. Nat Med (2013) 19:879-88. doi:10.1038/nm.3253
27. Dill MT, Makowska Z, Trincucci G, Gruber AJ, Vogt JE, Filipowicz M, et al. Pegylated IFN-alpha regulates hepatic gene expression through transient Jak/STAT activation. J Clin Invest (2014) 124:1568-81. doi:10.1172/JCI70408
28. Bertola A, Mathews S, Ki SH, Wang H, Gao B. Mouse model of chronic and binge ethanol feeding (the NIAAA model). Nat Protoc (2013) 8:627-37. doi:10.1038/nprot.2013.032
29. Yanez-Mo M, Siljander PR, Andreu Z, Zavec AB, Borras FE, Buzas EI, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles (2015) 4:27066. doi:10.3402/jev.v4.27066
30. Gajewski TF, Schreiber H, Fu YX. Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol (2013) 14:1014-22. doi:10.1038/ni.2703
31. Wang X, Breeze A, Kulka M. N-3 polyunsaturated fatty acids inhibit IFN-gamma-induced IL-18 binding protein production by prostate cancer cells. Cancer Immunol Immunother (2015) 64:249-58. doi:10.1007/s00262-014-1630-z
32. Calder PC. The relationship between the fatty acid composition of immune cells and their function. Prostaglandins Leukot Essent Fatty Acids (2008) 79:101-8. doi:10.1016/j.plefa.2008.09.016