BST-2 expression in human hepatocytes is inducible by all three types of interferons and restricts production of hepatitis C virus

Current Molecular Medicine

Volumn 14, Issue 3, 2014, Pages 349-360

  Amet, T ^a   Byrd, D ^a   Hu, N ^b   Sun, Q ^b   Li, F ^b   Zhao, Y ^b   Hu, S ^a,c   Grantham, A ^a   Yu, Q ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WENZHOU MEDICAL UNIVERSITY   (China)

^c HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

BST 2; HCV; Host restriction factor; Huh7.5.1 cell; Interferon; Lipid droplet

Indexed keywords

ALPHA INTERFERON; ANTIBIOTIC AGENT; BETA ACTIN; BONE MARROW STROMAL CELL ANTIGEN 2; CELL ANTIGEN; CORE PROTEIN; FAT DROPLET; GAMMA INTERFERON; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; LAMBDA INTERFERON; MESSENGER RNA; RIBAVIRIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; VIRUS RNA; BST2 PROTEIN, HUMAN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; INTERFERON; LEUKOCYTE ANTIGEN; SMALL INTERFERING RNA;

ANTIGEN EXPRESSION; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; LIFE CYCLE; LIVER CELL; MULTIPHOTON MICROSCOPY; PLASMID; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS CORE; VIRUS INHIBITION; VIRUS REPLICATION; WESTERN BLOTTING; CELL CULTURE; DRUG EFFECTS; GENETICS; HEPACIVIRUS; HEPG2 CELL LINE; METABOLISM; PATHOGENICITY; TUMOR CELL LINE;

ANTIGENS, CD; CELL LINE, TUMOR; CELLS, CULTURED; GPI-LINKED PROTEINS; HEP G2 CELLS; HEPACIVIRUS; HEPATOCYTES; HUMANS; INTERFERON-ALPHA; INTERFERON-GAMMA; INTERFERONS; RNA, SMALL INTERFERING; VIRUS REPLICATION;

EID: 84897433637     PISSN: 15665240     EISSN: 18755666     Source Type: Journal    
DOI: 10.2174/1566524013666131118111719     Document Type: Article

References (63)

1. National Institutes of Health Consensus Development Conference Statement: Management of hepatitis C 2002 (June 10-12, 2002). Gastroenterology 2002; 123(6): 2082-99.
2. Three broad modalities in the natural history of vertically acquired hepatitis C virus infection. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 2005; 41(1): 45-51.
3. Micallef JM, Kaldor JM, Dore GJ. Spontaneous viral clearance following acute hepatitis C infection: a systematic review of longitudinal studies. J Viral Hepat 2006; 13(1): 34-41.
4. Rauch A, Gaudieri S, Thio C, Bochud PY. Host genetic determinants of spontaneous hepatitis C clearance. Pharmacogenomics 2009; 10(11): 1819-37.
5. Tillmann HL, Thompson AJ, Patel K, et al. A polymorphism near IL28B is associated with spontaneous clearance of acute hepatitis C virus and jaundice. Gastroenterology 2010; 139(5): 1586-92, 92 e1.
6. Grebely J, Petoumenos K, Hellard M, et al. Potential role for interleukin-28B genotype in treatment decision-making in recent hepatitis C virus infection. Hepatology 2010; 52(4): 1216-24.
7. Garten RJ, Lai SH, Zhang JB, Liu W, Chen J, Yu XF. Factors influencing a low rate of hepatitis C viral RNA clearance in heroin users from Southern China. World J Gastroenterol 2008; 14(12): 1878-84.
8. Zhang M, Rosenberg PS, Brown DL, et al. Correlates of spontaneous clearance of hepatitis C virus among people with hemophilia. Blood 2006; 107(3): 892-7.
9. Page K, Hahn JA, Evans J, et al. Acute hepatitis C virus infection in young adult injection drug users: a prospective study of incident infection, resolution, and reinfection. J Infect Dis 2009; 200(8): 1216-26.
10. Wang CC, Krantz E, Klarquist J, et al. Acute hepatitis C in a contemporary US cohort: modes of acquisition and factors influencing viral clearance. J Infect Dis 2007; 196(10): 1474-82.
11. Diepolder HM. New insights into the immunopathogenesis of chronic hepatitis C. Antiviral Res 2009; 82(3): 103-9.
12. Post J, Ratnarajah S, Lloyd AR. Immunological determinants of the outcomes from primary hepatitis C infection. Cell Mol Life Sci 2009; 66(5): 733-56.
13. Rehermann B. Hepatitis C virus versus innate and adaptive immune responses: a tale of coevolution and coexistence. J Clin Invest 2009; 119(7): 1745-54.
14. Lemon SM. Induction and evasion of innate antiviral responses by hepatitis C virus. J Biol Chem 2010; 285(30): 22741-7.
15. Bowen DG, Walker CM. Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature 2005; 436(7053): 946-52.
16. Takaki A, Wiese M, Maertens G, et al. Cellular immune responses persist and humoral responses decrease two decades after recovery from a single-source outbreak of hepatitis C. Nat Med 2000; 6(5): 578-82.
17. Operskalski EA, Mack WJ, Strickler HD, et al. Factors associated with hepatitis C viremia in a large cohort of HIVinfected and-uninfected women. J Clin Virol 2008; 41(4): 255-63.
18. Thomas DL, Astemborski J, Rai RM, et al. The natural history of hepatitis C virus infection: host, viral, and environmental factors. JAMA 2000; 284(4): 450-6.
19. Melendez-Morales L, Konkle BA, Preiss L, et al. Chronic hepatitis B and other correlates of spontaneous clearance of hepatitis C virus among HIV-infected people with hemophilia. AIDS 2007; 21(12): 1631-6.
20. Grebely J, Prins M, Hellard M, et al. Hepatitis C virus clearance, reinfection, and persistence, with insights from studies of injecting drug users: towards a vaccine. Lancet Infect Dis 2012; 12(5): 408-14.
21. Grebely J, Raffa JD, Lai C, Krajden M, Conway B, Tyndall MW. Factors associated with spontaneous clearance of hepatitis C virus among illicit drug users. Can J Gastroenterol 2007; 21(7): 447-51.
22. Piasecki BA, Lewis JD, Reddy KR, et al. Influence of alcohol use, race, and viral coinfections on spontaneous HCV clearance in a US veteran population. Hepatology 2004; 40(4): 892-9.
23. Torriani FJ, Rodriguez-Torres M, Rockstroh JK, et al. Peginterferon Alfa-2a plus ribavirin for chronic hepatitis C virus infection in HIV-infected patients. N Engl J Med 2004; 351(5): 438-50.
24. Mitchell RS, Katsura C, Skasko MA, et al. Vpu antagonizes BST-2-mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking. PLoS Pathog 2009; 5(5): e1000450.
25. Van Damme N, Goff D, Katsura C, et al. The interferoninduced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 2008; 3(4): 245-52.
26. Miyagi E, Andrew AJ, Kao S, Strebel K. Vpu enhances HIV-1 virus release in the absence of Bst-2 cell surface downmodulation and intracellular depletion. Proc Natl Acad Sci U S A 2009; 106(8): 2868-73.
27. Kupzig S, Korolchuk V, Rollason R, Sugden A, Wilde A, Banting G. Bst-2/HM1. 24 is a raft-associated apical membrane protein with an unusual topology. Traffic 2003; 4(10): 694-709.
28. Arias JF, Iwabu Y, Tokunaga K. Structural Basis for the Antiviral Activity of BST-2/Tetherin and Its Viral Antagonism. Front Microbiol 2011; 2: 250.
29. Iwabu Y, Fujita H, Kinomoto M, et al. HIV-1 accessory protein Vpu internalizes cell-surface BST-2/tetherin through transmembrane interactions leading to lysosomes. J Biol Chem 2009; 284(50): 35060-72.
30. Mangeat B, Gers-Huber G, Lehmann M, Zufferey M, Luban J, Piguet V. HIV-1 Vpu neutralizes the antiviral factor Tetherin/BST-2 by binding it and directing its beta-TrCP2-dependent degradation. PLoS Pathog 2009; 5(9): e1000574.
31. Hinz A, Miguet N, Natrajan G, et al. Structural Basis of HIV-1 Tethering to Membranes by the BST-2/Tetherin Ectodomain. Cell Host Microbe 2010; 7(4): 314-23.
32. Zhang J, Liang C. BST-2 diminishes HIV-1 infectivity. J Virol 2010; 84(23): 12336-43.
33. Hauser H, Lopez LA, Yang SJ, et al. HIV-1 Vpu and HIV-2 Env counteract BST-2/tetherin by sequestration in a perinuclear compartment (vol 7, pg 51, 2010). Retrovirology 2011; 8: 85.
34. Gupta RK, Mlcochova P, Pelchen-Matthews A, et al. Simian immunodeficiency virus envelope glycoprotein counteracts tetherin/BST-2/CD317 by intracellular sequestration. Proc Natl Acad Sci U S A 2009; 106(49): 20889-94.
35. Lopez LA, Yang SJ, Hauser H, et al. Ebola virus glycoprotein counteracts BST-2/Tetherin restriction in a sequenceindependent manner that does not require tetherin surface removal. J Virol 2010; 84(14): 7243-55.
36. Sakuma T, Noda T, Urata S, Kawaoka Y, Yasuda J. Inhibition of Lassa and Marburg virus production by tetherin. J Virol 2009; 83(5): 2382-5.
37. Pardieu C, Vigan R, Wilson SJ, et al. The RING-CH ligase K5 antagonizes restriction of KSHV and HIV-1 particle release by mediating ubiquitin-dependent endosomal degradation of tetherin. PLoS Pathog 2010; 6(4): e1000843.
38. Ye L, Wang X, Li J, et al. Tetherin has negligible activity in restricting hepatitis C virus in hepatocytes. Innate Immun 2012; 18(3): 398-405.
39. Dafa-Berger A, Kuzmina A, Fassler M, Yitzhak-Asraf H, Shemer-Avni Y, Taube R. Modulation of hepatitis C virus release by the interferon-induced protein BST-2/tetherin. Virology 2012; 428(2): 98-111.
40. Amet T, Ghabril M, Chalasani N, et al. CD59 incorporation protects hepatitis C virus against complement-mediated destruction. Hepatology 2012; 55(2): 354-63.
41. Rong L, Zhang J, Lu J, et al. The transmembrane domain of BST-2 determines its sensitivity to down-modulation by human immunodeficiency virus type 1 Vpu. J Virol 2009; 83(15): 7536-46.
42. Guo JT, Bichko VV, Seeger C. Effect of alpha interferon on the hepatitis C virus replicon. J Virol 2001; 75(18): 8516-23.
43. Castet V, Fournier C, Soulier A, et al. Alpha interferon inhibits hepatitis C virus replication in primary human hepatocytes infected in vitro. J Virol 2002; 76(16): 8189-99.
44. Camma C, Giunta M, Andreone P, Craxi A. Interferon and prevention of hepatocellular carcinoma in viral cirrhosis: an evidence-based approach. J Hepatol 2001; 34(4): 593-602.
45. Frese M, Schwarzle V, Barth K, et al. Interferon-gamma inhibits replication of subgenomic and genomic hepatitis C virus RNAs. Hepatology 2002; 35(3): 694-703.
46. Katayama K, Kasahara A, Sasaki Y, et al. Immunological response to interferon-gamma priming prior to interferonalpha treatment in refractory chronic hepatitis C in relation to viral clearance. J Viral Hepat 2001; 8(3): 180-5.
47. Pearlman BL, Traub N. Sustained virologic response to antiviral therapy for chronic hepatitis C virus infection: a cure and so much more. Clin Infect Dis 2011; 52(7): 889-900.
48. Thomas DL, Thio CL, Martin MP, et al. Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 2009; 461(7265): 798-801.
49. Marcello T, Grakoui A, Barba-Spaeth G, et al. Interferons alpha and lambda inhibit hepatitis C virus replication with distinct signal transduction and gene regulation kinetics. Gastroenterology 2006; 131(6): 1887-98.
50. Ge D, Fellay J, Thompson AJ, et al. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 2009; 461(7262): 399-401.
51. Suppiah V, Moldovan M, Ahlenstiel G, et al. IL28B is associated with response to chronic hepatitis C interferonalpha and ribavirin therapy. Nat Genet 2009; 41(10): 1100-4.
52. Tanaka Y, Nishida N, Sugiyama M, et al. Genome-wide association of IL28B with response to pegylated interferonalpha and ribavirin therapy for chronic hepatitis C. Nat Genet 2009; 41(10): 1105-9.
53. Hsu NY, Ilnytska O, Belov G, et al. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 2010; 141(5): 799-811.
54. Kotenko SV, Gallagher G, Baurin VV, et al. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 2003; 4(1): 69-77.
55. Sommereyns C, Paul S, Staeheli P, Michiels T. IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog 2008; 4(3): e1000017.
56. Sheppard P, Kindsvogel W, Xu W, et al. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat Immunol 2003; 4(1): 63-8.
57. Lasfar A, Lewis-Antes A, Smirnov SV, et al. Characterization of the mouse IFN-lambda ligand-receptor system: IFNlambdas exhibit antitumor activity against B16 melanoma. Cancer Res 2006; 66(8): 4468-77.
58. Dumoutier L, Lejeune D, Hor S, Fickenscher H, Renauld JC. Cloning of a new type II cytokine receptor activating signal transducer and activator of transcription (STAT)1, STAT2 and STAT3. Biochem J 2003; 370(Pt 2): 391-6.
59. Manns MP, Wedemeyer H, Cornberg M. Treating viral hepatitis C: efficacy, side effects, and complications. Gut 2006; 55(9): 1350-9.
60. Chu H, Wang JJ, Qi M, et al. Tetherin/BST-2 Is Essential for the Formation of the Intracellular Virus-Containing Compartment in HIV-Infected Macrophages. Cell Host Microbe 2012; 12(3): 360-72.
61. Chu H, Wang JJ, Qi M, et al. The intracellular viruscontaining compartments in primary human macrophages are largely inaccessible to antibodies and small molecules. PLoS One 2012; 7(5): e35297.
62. Miyanari Y, Atsuzawa K, Usuda N, et al. The lipid droplet is an important organelle for hepatitis C virus production. Nat Cell Biol 2007; 9(9): 1089-97.
63. Boulant S, Targett-Adams P, McLauchlan J. Disrupting the association of hepatitis C virus core protein with lipid droplets correlates with a loss in production of infectious virus. J Gen Virol 2007; 88(Pt 8): 2204-13.