The dual role of exosomes in hepatitis A and C virus transmission and viral immune activation

Viruses

Volumn 7, Issue 12, 2015, Pages 6707-6715

  Longatti, Andrea ^a  

^a MEDIMMUNE   (United States)

Author keywords

Exosomes; Hepatitis A virus; Hepatitis C virus; Immune evasion; Infection; Innate immunity; Interferon; Plasmacytoid dendritic cells; Transmission

Indexed keywords

TOLL LIKE RECEPTOR 7; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; VIRUS RNA;

ENDOSOME; EXOSOME; HEPATITIS A; HEPATITIS A VIRUS; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; IMMUNE ACTIVATION; IMMUNE EVASION; IMMUNE RESPONSE; INNATE IMMUNITY; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; NONHUMAN; PLASMACYTOID DENDRITIC CELL; REVIEW; VIRION; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS TRANSMISSION; DENDRITIC CELL; HEPACIVIRUS; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; VIROLOGY; VIRUS ENTRY; VIRUS RELEASE;

DENDRITIC CELLS; EXOSOMES; HEPACIVIRUS; HEPATITIS A VIRUS; HUMANS; VIRUS INTERNALIZATION; VIRUS RELEASE;

EID: 84951012428     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7122967     Document Type: Review

References (66)

1. Johnstone, R.M.; Adam, M.; Hammond, J.R.; Orr, L.; Turbide, C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J. Biol. Chem. 1987, 262, 9412-9420. [PubMed]
2. 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, 256-263. [PubMed]
3. Harding, C.; Heuser, J.; Stahl, P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J. Cell Biol. 1983, 97, 329-339. [CrossRef] [PubMed]
4. Meckes, D.G., Jr.; Raab-Traub, N. Microvesicles and viral infection. J. Virol. 2011, 85, 12844-12854. [CrossRef] [PubMed]
5. Keller, S.; Sanderson, M.P.; Stoeck, A.; Altevogt, P. Exosomes: From biogenesis and secretion to biological function. Immunol. Lett. 2006, 107, 102-108. [CrossRef] [PubMed]
6. Van Niel, G.; Porto-Carreiro, I.; Simoes, S.; Raposo, G. Exosomes: A common pathway for a specialized function. J. Biochem. 2006, 140, 13-21. [CrossRef] [PubMed]
7. Stuffers, S.; SemWegner, C.; Stenmark, H.; Brech, A. Multivesicular endosome biogenesis in the absence of ESCRTs. Traffic 2009, 10, 925-937. [CrossRef] [PubMed]
8. Van Niel, G.; Charrin, S.; Simoes, S.; Romao, M.; Rochin, L.; Saftig, P.; Marks, M.S.; Rubinstein, E.; Raposo, G. The tetraspanin CD63 regulates ESCRT-independent and-dependent endosomal sorting during melanogenesis. Dev. Cell 2011, 21, 708-721. [CrossRef] [PubMed]
9. Henne, W.M.; Stenmark, H.; Emr, S.D. Molecular mechanisms of the membrane sculpting ESCRT pathway. Cold Spring Harbor Perspect. Biol. 2013, 5. [CrossRef] [PubMed]
10. Hsu, C.; Morohashi, Y.; Yoshimura, S.; Manrique-Hoyos, N.; Jung, S.; Lauterbach, M.A.; Bakhti, M.; Grønborg, M.; Möbius, W.; Rhee, J. Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C.J. Cell Biol. 2010, 189, 223-232. [CrossRef] [PubMed]
11. Chahar, H.S.; Bao, X.; Casola, A. Exosomes and their role in the life cycle and pathogenesis of RNA viruses. Viruses 2015, 7, 3204-3225. [CrossRef] [PubMed]
12. Thery, C.; Zitvogel, L.; Amigorena, S. Exosomes: Composition, biogenesis and function. Nat. Rev. Immunol. 2002, 2, 569-579. [PubMed]
13. Conde-Vancells, J.; Rodriguez-Suarez, E.; Embade, N.; Gil, D.; Matthiesen, R.; Valle, M.; Elortza, F.; Lu, S.C.; Mato, J.M.; Falcon-Perez, J.M. Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes. J. Proteome Res. 2008, 7, 5157-5166. [CrossRef] [PubMed]
14. Shepard, C.W.; Finelli, L.; Alter, M.J. Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis. 2005, 5, 558-567. [CrossRef]
15. Negro, F.; Alberti, A. The global health burden of hepatitis C virus infection. Liver Int. 2011, 31, S1-S3. [CrossRef] [PubMed]
16. Meylan, E.; Curran, J.; Hofmann, K.; Moradpour, D.; Binder, M.; Bartenschlager, R.; Tschopp, J. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005, 437, 1167-1172. [CrossRef] [PubMed]
17. Loo, Y.M.; Owen, D.M.; Li, K.; Erickson, A.K.; Johnson, C.L.; Fish, P.M.; Carney, D.S.; Wang, T.; Ishida, H.; Yoneyama, M.; et al. Viral and therapeutic control of IFN-beta promoter stimulator 1 during hepatitis C virus infection. Proc. Natl. Acad. Sci. USA 2006, 103, 6001-6006. [CrossRef] [PubMed]
18. Cheng, G.; Zhong, J.; Chisari, F.V. Inhibition of dsRNA-induced signaling in hepatitis C virus-infected cells by NS3 protease-dependent and-independent mechanisms. Proc. Natl. Acad. Sci. USA 2006, 103, 8499-8504. [CrossRef] [PubMed]
19. Takahashi, K.; Asabe, S.; Wieland, S.; Garaigorta, U.; Gastaminza, P.; Isogawa, M.; Chisari, F.V. Plasmacytoid dendritic cells sense hepatitis C virus-infected cells, produce interferon, and inhibit infection. Proc. Natl. Acad. Sci. USA 2010, 107, 7431-7436. [CrossRef] [PubMed]
20. Dreux, M.; Garaigorta, U.; Boyd, B.; Décembre, E.; Chung, J.; Whitten-Bauer, C.; Wieland, S.; Chisari, F.V. Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity. Cell Host Microbe 2012, 12, 558-570. [CrossRef] [PubMed]
21. Park, H.; Serti, E.; Eke, O.; Muchmore, B.; Prokunina-Olsson, L.; Capone, S.; Folgori, A.; Rehermann, B. IL-29 is the dominant type III interferon produced by hepatocytes during acute hepatitis C virus infection. Hepatology 2012, 56, 2060-2070. [CrossRef] [PubMed]
22. Stone, A.E.; Giugliano, S.; Schnell, G.; Cheng, L.; Leahy, K.F.; Golden-Mason, L.; Gale, M., Jr.; Rosen, H.R. Hepatitis C virus pathogen associated molecular pattern (PAMP) triggers production of lambda-interferons by human plasmacytoid dendritic cells. PLoS Pathog. 2013, 9. [CrossRef]
23. Giugliano, S.; Kriss, M.; Golden-Mason, L.; Dobrinskikh, E.; Stone, A.E.; Soto-Gutierrez, A.; Mitchell, A.; Khetani, S.R.; Yamane, D.; Stoddard, M.; 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. [CrossRef] [PubMed]
24. Zhang, S.; Kodys, K.; Li, K.; Szabo, G. Human type 2 myeloid dendritic cells produce interferon-Λ and amplify interferon-Λ in response to hepatitis C virus infection. Gastroenterology 2013, 144, 414-425. [CrossRef] [PubMed]
25. Longatti, A.; Boyd, B.; Chisari, F.V. Virion-independent transfer of replication-competent hepatitis C virus RNA between permissive cells. J. Virol. 2015, 89, 2956-2961. [CrossRef] [PubMed]
26. Bukong, T.N.; Momen-Heravi, F.; Kodys, K.; Bala, S.; Szabo, G. Exosomes from hepatitis C infected patients transmit HCV infection and contain replication competent viral RNA in complex with Ago2-miR122-HSP90. PLoS Pathog. 2014, 10. [CrossRef] [PubMed]
27. Ramakrishnaiah, V.; Thumann, C.; Fofana, I.; Habersetzer, F.; Pan, Q.; de Ruiter, P.E.; Willemsen, R.; Demmers, J.A.; Stalin Raj, V.; Jenster, G.; et al. Exosome-mediated transmission of hepatitis C virus between human hepatoma Huh7. 5 cells. Proc. Natl. Acad. Sci. USA 2013, 110, 13109-13113. [CrossRef] [PubMed]
28. Liu, Z.; Zhang, X.; Yu, Q.; He, J.J. Exosome-associated hepatitis C virus in cell cultures and patient plasma. Biochem. Biophys. Res. Commun. 2014, 455, 218-222. [CrossRef] [PubMed]
29. Shiina, M.; Rehermann, B. Cell culture-produced hepatitis C virus impairs plasmacytoid dendritic cell function. Hepatology 2008, 47, 385-395. [CrossRef] [PubMed]
30. Kanto, T.; Inoue, M.; Miyatake, H.; Sato, A.; Sakakibara, M.; Yakushijin, T.; Oki, C.; Itose, I.; Hiramatsu, N.; Takehara, T.; et al. Reduced numbers and impaired ability of myeloid and plasmacytoid dendritic cells to polarize T helper cells in chronic hepatitis C virus infection. J. Infect. Dis. 2004, 190, 1919-1926. [CrossRef] [PubMed]
31. Florentin, J.; Aouar, B.; Dental, C.; Thumann, C.; Firaguay, G.; Gondois-Rey, F.; Soumelis, V.; Baumert, T.F.; Nunès, J.A.; Olive, D.; et al. HCV glycoprotein E2 is a novel BDCA-2 ligand and acts as an inhibitor of IFN production by plasmacytoid dendritic cells. Blood 2012, 120, 4544-4551. [CrossRef] [PubMed]
32. Qu, L.; Feng, Z.; Yamane, D.; Liang, Y.; Lanford, R.E.; Li, K.; Lemon, S.M. Disruption of TLR3 signaling due to cleavage of TRIF by the hepatitis A virus protease-polymerase processing intermediate, 3CD. PLoS Pathog. 2011, 7. [CrossRef] [PubMed]
33. Yang, Y.; Liang, Y.; Qu, L.; Chen, Z.; Yi, M.; Li, K.; Lemon, S.M. Disruption of innate immunity due to mitochondrial targeting of a picornaviral protease precursor. Proc. Natl. Acad. Sci. USA 2007, 104, 7253-7258. [CrossRef] [PubMed]
34. Li, K.; Foy, E.; Ferreon, J.C.; Nakamura, M.; Ferreon, A.C.; Ikeda, M.; Ray, S.C.; Gale, M., Jr.; Lemon, S.M. Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc. Natl. Acad. Sci. USA 2005, 102, 2992-2997. [CrossRef] [PubMed]
35. Martin, A.; Lemon, S.M. Hepatitis A virus: From discovery to vaccines. Hepatology 2006, 43, S164-S172. [CrossRef] [PubMed]
36. Lemon, S.M. Type A viral hepatitis. New developments in an old disease. N. Engl. J. Med. 1985, 313, 1059-1067. [CrossRef] [PubMed]
37. Lanforda, R.E.; Fengc, Z.; Chaveza, D.; Guerraa, B.; Braskyb, K.M.; Zhoud, Y.; Yamanec, D.; Perelsone, A.S.; Walkerd, C.M.; Lemonc, S.M. Acute hepatitis A virus infection is associated with a limited type I interferon response and persistence of intrahepatic viral RNA. Proc. Natl. Acad. Sci. USA 2011, 108, 11223-11228. [CrossRef] [PubMed]
38. Feng, Z.; Hensley, L.; McKnight, K.L.; Hu, F.; Madden, V.; Ping, L.; Jeong, S.H.; Walker, C.; Lanford, R.E.; Lemon, S.M. A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature 2013, 496, 367-371. [CrossRef] [PubMed]
39. Victor, J.C.; Monto, A.S.; Surdina, T.Y.; Suleimenova, S.Z.; Vaughan, G.; Nainan, O.V.; Favorov, M.O.; Margolis, H.S.; Bell, B.P. Hepatitis A vaccine versus immune globulin for postexposure prophylaxis. N. Engl. J. Med. 2007, 357, 1685-1694. [CrossRef] [PubMed]
40. Feng, Z.; Li, Y.; McKnight, K.L.; Hensley, L.; Lanford, R.E.; Walker, C.M.; Lemon, S.M. Human pDCs preferentially sense enveloped hepatitis A virions. J. Clin. Invest. 2015, 125, 169-176. [CrossRef] [PubMed]
41. Kato, T.; Date, T.; Miyamoto, M.; Furusaka, A.; Tokushige, K.; Mizokami, M.; Wakita, T. Efficient replication of the genotype 2a hepatitis C virus subgenomic replicon. Gastroenterology 2003, 125, 1808-1817. [CrossRef] [PubMed]
42. Pietschmann, T.; Lohmann, V.; Kaul, A.; Krieger, N.; Rinck, G.; Rutter, G.; Strand, D.; Bartenschlager, R. Persistent and transient replication of full-length hepatitis C virus genomes in cell culture. J. Virol. 2002, 76, 4008-4021. [CrossRef] [PubMed]
43. Assil, S.; Webster, B.; Dreux, M. Regulation of the host antiviral state by intercellular communications. Viruses 2015, 7, 4707-4733. [CrossRef] [PubMed]
44. Tamai, K.; Shiina, M.; Tanaka, N.; Nakano, T.; Yamamoto, A.; Kondo, Y.; Kakazu, E.; Inoue, J.; Fukushima, K.; Sano, K.; et al. Regulation of hepatitis C virus secretion by the Hrs-dependent exosomal pathway. Virology 2012, 422, 377-385. [CrossRef] [PubMed]
45. Alenquer, M.; Amorim, M.J. Exosome biogenesis, regulation, and function in viral infection. Viruses 2015, 7, 5066-5083. [CrossRef] [PubMed]
46. Tian, T.; Zhu, Y.L.; Zhou, Y.Y.; Liang, G.F.; Wang, Y.Y.; Hu, F.H.; Xiao, Z.D. Exosome uptake through clathrin-mediated endocytosis and macropinocytosis and mediating miR-21 delivery. J. Biol. Chem. 2014, 289, 22258-22267. [CrossRef] [PubMed]
47. Svensson, K.J.; Christianson, H.C.; Wittrup, A.; Bourseau-Guilmain, E.; Lindqvist, E.; Svensson, L.M.; Mörgelin, M.; Belting, M. Exosome uptake depends on ERK1/2-heat shock protein 27 signaling and lipid Raft-mediated endocytosis negatively regulated by caveolin-1. J. Biol. Chem. 2013, 288, 17713-17724. [CrossRef] [PubMed]
48. Feng, D.; Zhao, W.L.; Ye, Y.Y.; Bai, X.C.; Liu, R.Q.; Chang, L.F.; Zhou, Q.; Sui, S.F. Cellular internalization of exosomes occurs through phagocytosis. Traffic 2010, 11, 675-687. [CrossRef] [PubMed]
49. Barres, C.; Blanc, L.; Bette-Bobillo, P.; André, S.; Mamoun, R.; Gabius, H.J.; Vidal, M. Galectin-5 is bound onto the surface of rat reticulocyte exosomes and modulates vesicle uptake by macrophages. Blood 2010, 115, 696-705. [CrossRef] [PubMed]
50. Escrevente, C.; Keller, S.; Altevogt, P.; Costa, J. Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer 2011, 11. [CrossRef] [PubMed]
51. Sagar, G.; Sah, R.P.; Javeed, N.; Dutta, S.K.; Smyrk, T.C.; Lau, J.S.; Giorgadze, N.; Tchkonia, T.; Kirkland, J.L.; Chari, S.T.; et al. Pathogenesis of pancreatic cancer exosome-induced lipolysis in adipose tissue. Gut 2015. [CrossRef] [PubMed]
52. Nakase, I.; Kobayashi, N.B.; Takatani-Nakase, T.; Yoshida, T. Active macropinocytosis induction by stimulation of epidermal growth factor receptor and oncogenic Ras expression potentiates cellular uptake efficacy of exosomes. Sci. Rep. 2015, 5. [CrossRef] [PubMed]
53. Masciopinto, F.; Giovani, C.; Campagnoli, S.; Galli-Stampino, L.; Colombatto, P.; Brunetto, M.; Yen, T.S.; Houghton, M.; Pileri, P.; Abrignani, S. Association of hepatitis C virus envelope proteins with exosomes. Eur. J. Immunol. 2004, 34, 2834-2842. [CrossRef] [PubMed]
54. Shimakami, T.; Yamane, D.; Welsch, C.; Hensley, L.; Jangra, R.K.; Lemon, S.M. Base pairing between hepatitis C virus RNA and microRNA 122 3' of its seed sequence is essential for genome stabilization and production of infectious virus. J. Virol. 2012, 86, 7372-7383. [CrossRef] [PubMed]
55. Shimakami, T.; Yamane, D.; Jangra, R.K.; Kempf, B.J.; Spaniel, C.; Barton, D.J.; Lemon, S.M. Stabilization of hepatitis C virus RNA by an Ago2-miR-122 complex. Proc. Natl. Acad. Sci. USA 2012, 109, 941-946. [CrossRef] [PubMed]
56. Okamoto, T.; Nishimura, Y.; Ichimura, T.; Suzuki, K.; Miyamura, T.; Suzuki, T.; Moriishi, K.; Matsuura, Y. Hepatitis C virus RNA replication is regulated by FKBP8 and Hsp90. EMBO J. 2006, 25, 5015-5025. [CrossRef] [PubMed]
57. Wilson, J.A.; Zhang, C.; Huys, A.; Richardson, C.D. Human Ago2 is required for efficient microRNA 122 regulation of hepatitis C virus RNA accumulation and translation. J. Virol. 2011, 85, 2342-2350. [CrossRef] [PubMed]
58. Jopling, C.L.; Schutz, S.; Sarnow, P. Position-dependent function for a tandem microRNA miR-122-binding site located in the hepatitis C virus RNA genome. Cell Host Microbe 2008, 4, 77-85. [CrossRef] [PubMed]
59. Jopling, C.L.; Yi, M.; Lancaster, A.M.; Lemon, S.M.; Sarnow, P. Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 2005, 309, 1577-1581. [CrossRef] [PubMed]
60. Jangra, R.K.; Yi, M.; Lemon, S.M. Regulation of hepatitis C virus translation and infectious virus production by the microRNA miR-122. J. Virol. 2010, 84, 6615-6625. [CrossRef] [PubMed]
61. Henke, J.I.; Goergen, D.; Zheng, J.; Song, Y.; Schüttler, C.G.; Fehr, C.; Jünemann, C.; Niepmann, M. microRNA-122 stimulates translation of hepatitis C virus RNA. EMBO J. 2008, 27, 3300-3310. [CrossRef] [PubMed]
62. Teijaro, J.R.; Ng, C.; Lee, A.M.; Sullivan, B.M.; Sheehan, K.C.F.; Welch, M.; Schreiber, R.D.; de la Torre, J.D.; Oldstone, M.B.A. Persistent LCMV infection is controlled by blockade of type I interferon signaling. Science 2013, 340, 207-211. [CrossRef] [PubMed]
63. Odorizzi, P.M.; Wherry, E.J. Immunology. An interferon paradox. Science 2013, 340, 155-156. [CrossRef] [PubMed]
64. Wilson, E.B.; Yamada, D.H.; Elsaesser, H.; Herskovitz, J.; Deng, J.; Cheng, G.; Aronow, B.J.; Karp, C.L.; Brooks, D.G. Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science 2013, 340, 202-207. [CrossRef] [PubMed]
65. Wieland, S.F.; Takahashi, K.; Boyd, B.; Whitten-Bauer, C.; Ngo, N.; de la Torre, J.C.; Chisari, F.V. Human plasmacytoid dendritic cells sense lymphocytic choriomeningitis virus-infected cells in vitro. J. Virol. 2014, 88, 752-757. [CrossRef] [PubMed]
66. Lepelley, A.; Louis, S.; Sourisseau, M.; Law, H.K.; Pothlichet, J.; Schilte, C.; Chaperot, L.; Plumas, J.; Randall, R.E.; Si-Tahar, M.; et al. Innate sensing of HIV-infected cells. PLoS Pathog. 2011, 7. [CrossRef] [PubMed]