1887

Abstract

Bone marrow stromal antigen 2 (BST-2; also known as tetherin or CD317) is an IFN-inducible gene that functions to block the release of a range of nascent enveloped virions from infected host cells. However, the role of BST-2 in viral pathogenesis remains poorly understood. BST-2 plays a multifaceted role in innate immunity, as it hinders retroviral infection and possibly promotes infection with some rhabdo- and orthomyxoviruses. This paradoxical role has probably hindered exploration of BST-2 antiviral function . We reported previously that BST-2 tethers Chikungunya virus (CHIKV)-like particles on the cell plasma membrane. To explore the role of BST-2 in CHIKV replication and host protection, we utilized CHIKV strain 181/25 to examine early events during CHIKV infection in a BST-2 mouse model. We observed an interesting dichotomy between WT and BST-2 mice. BST-2 deficiency increased inoculation site viral load, culminating in higher systemic viraemia and increased lymphoid tissues tropism. A suppressed inflammatory innate response demonstrated by impaired expression of IFN-α, IFN-γ and CD40 ligand was observed in BST-2 mice compared with the WT controls. These findings suggested that, in part, BST-2 protects lymphoid tissues from CHIKV infection and regulates CHIKV-induced inflammatory response by the host.

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2014-11-01
2019-08-25
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References

  1. Arias J. F. , Heyer L. N. , von Bredow B. , Weisgrau K. L. , Moldt B. , Burton D. R. , Rakasz E. G. , Evans D. T. . ( 2014; ). Tetherin antagonism by Vpu protects HIV-infected cells from antibody-dependent cell-mediated cytotoxicity. . Proc Natl Acad Sci U S A 111:, 6425–6430. [CrossRef] [PubMed]
    [Google Scholar]
  2. Blasius A. L. , Giurisato E. , Cella M. , Schreiber R. D. , Shaw A. S. , Colonna M. . ( 2006; ). Bone marrow stromal cell antigen 2 is a specific marker of type I IFN-producing cells in the naive mouse, but a promiscuous cell surface antigen following IFN stimulation. . J Immunol 177:, 3260–3265. [CrossRef] [PubMed]
    [Google Scholar]
  3. Briolant S. , Garin D. , Scaramozzino N. , Jouan A. , Crance J. M. . ( 2004; ). In vitro inhibition of Chikungunya and Semliki Forest viruses replication by antiviral compounds: synergistic effect of interferon-alpha and ribavirin combination. . Antiviral Res 61:, 111–117. [CrossRef] [PubMed]
    [Google Scholar]
  4. Cao W. , Bover L. , Cho M. , Wen X. , Hanabuchi S. , Bao M. , Rosen D. B. , Wang Y. H. , Shaw J. L. . & other authors ( 2009; ). Regulation of TLR7/9 responses in plasmacytoid dendritic cells by BST2 and ILT7 receptor interaction. . J Exp Med 206:, 1603–1614. [CrossRef] [PubMed]
    [Google Scholar]
  5. Chen X. Y. , Zhang H. S. , Wu T. C. , Sang W. W. , Ruan Z. . ( 2013; ). Down-regulation of NAMPT expression by miR-182 is involved in Tat-induced HIV-1 long terminal repeat (LTR) transactivation. . Int J Biochem Cell Biol 45:, 292–298. [CrossRef] [PubMed]
    [Google Scholar]
  6. Couderc T. , Chrétien F. , Schilte C. , Disson O. , Brigitte M. , Guivel-Benhassine F. , Touret Y. , Barau G. , Cayet N. . & other authors ( 2008; ). A mouse model for Chikungunya: young age and inefficient type-I interferon signaling are risk factors for severe disease. . PLoS Pathog 4:, e29. [CrossRef] [PubMed]
    [Google Scholar]
  7. Couderc T. , Khandoudi N. , Grandadam M. , Visse C. , Gangneux N. , Bagot S. , Prost J. F. , Lecuit M. . ( 2009; ). Prophylaxis and therapy for Chikungunya virus infection. . J Infect Dis 200:, 516–523. [CrossRef] [PubMed]
    [Google Scholar]
  8. Das T. , Jaffar-Bandjee M. C. , Hoarau J. J. , Krejbich Trotot P. , Denizot M. , Lee-Pat-Yuen G. , Sahoo R. , Guiraud P. , Ramful D. , Robin S. . ( 2010; ). Chikungunya fever: CNS infection and pathologies of a re-emerging arbovirus. . Prog Neurobiol 91:, 121–129. [CrossRef] [PubMed]
    [Google Scholar]
  9. Douglas J. L. , Gustin J. K. , Viswanathan K. , Mansouri M. , Moses A. V. , Früh K. . ( 2010; ). The great escape: viral strategies to counter BST-2/tetherin. . PLoS Pathog 6:, e1000913. [CrossRef] [PubMed]
    [Google Scholar]
  10. Du S. , Kendall K. , Morris S. , Sweet C. . ( 2010; ). Measuring number-concentrations of nanoparticles and viruses in liquids on-line. . J Chem Technol Biotechnol 85:, 1223–1228. [CrossRef]
    [Google Scholar]
  11. Fan S. X. , Turpin J. A. , Aronovitz J. R. , Meltzer M. S. . ( 1994; ). Interferon-gamma protects primary monocytes against infection with human immunodeficiency virus type 1. . J Leukoc Biol 56:, 362–368.[PubMed]
    [Google Scholar]
  12. Filipe V. , Jiskoot W. , Hawe A. . ( 2011; ). Understanding virus preparations using nanoscale particle characterization. . BioProcess Int 9:, 44–51.[CrossRef]
    [Google Scholar]
  13. Galão R. P. , Le Tortorec A. , Pickering S. , Kueck T. , Neil S. J. . ( 2012; ). Innate sensing of HIV-1 assembly by Tetherin induces NFκB-dependent proinflammatory responses. . Cell Host Microbe 12:, 633–644. [CrossRef] [PubMed]
    [Google Scholar]
  14. Gardner C. L. , Burke C. W. , Higgs S. T. , Klimstra W. B. , Ryman K. D. . ( 2012; ). Interferon-alpha/beta deficiency greatly exacerbates arthritogenic disease in mice infected with wild-type chikungunya virus but not with the cell culture-adapted live-attenuated 181/25 vaccine candidate. . Virology 425:, 103–112. [CrossRef] [PubMed]
    [Google Scholar]
  15. Garten A. , Petzold S. , Körner A. , Imai S. i. , Kiess W. . ( 2009; ). Nampt: linking NAD biology, metabolism and cancer. . Trends Endocrinol Metab 20:, 130–138. [CrossRef] [PubMed]
    [Google Scholar]
  16. Her Z. , Malleret B. , Chan M. , Ong E. K. , Wong S. C. , Kwek D. J. , Tolou H. , Lin R. T. , Tambyah P. A. . & other authors ( 2010; ). Active infection of human blood monocytes by Chikungunya virus triggers an innate immune response. . J Immunol 184:, 5903–5913. [CrossRef] [PubMed]
    [Google Scholar]
  17. Hoarau J. J. , Jaffar Bandjee M. C. , Krejbich Trotot P. , Das T. , Li-Pat-Yuen G. , Dassa B. , Denizot M. , Guichard E. , Ribera A. . & other authors ( 2010; ). Persistent chronic inflammation and infection by Chikungunya arthritogenic alphavirus in spite of a robust host immune response. . J Immunol 184:, 5914–5927. [CrossRef] [PubMed]
    [Google Scholar]
  18. Jones P. H. , Okeoma C. M. . ( 2013; ). Phosphatidylinositol 3-kinase is involved in Toll-like receptor 4-mediated BST-2/tetherin regulation. . Cell Signal 25:, 2752–2761. [CrossRef] [PubMed]
    [Google Scholar]
  19. Jones P. H. , Mehta H. V. , Maric M. , Roller R. J. , Okeoma C. M. . ( 2012; ). Bone marrow stromal cell antigen 2 (BST-2) restricts mouse mammary tumor virus (MMTV) replication in vivo . . Retrovirology 9:, 10. [CrossRef] [PubMed]
    [Google Scholar]
  20. Jones P. H. , Mahauad-Fernandez W. D. , Madison M. N. , Okeoma C. M. . ( 2013a; ). BST-2/tetherin is overexpressed in mammary gland and tumor tissues in MMTV-induced mammary cancer. . Virology 444:, 124–139. [CrossRef] [PubMed]
    [Google Scholar]
  21. Jones P. H. , Maric M. , Madison M. N. , Maury W. , Roller R. J. , Okeoma C. M. . ( 2013b; ). BST-2/tetherin-mediated restriction of chikungunya (CHIKV) VLP budding is counteracted by CHIKV non-structural protein 1 (nsP1). . Virology 438:, 37–49. [CrossRef] [PubMed]
    [Google Scholar]
  22. Kornbluth R. S. , Oh P. S. , Munis J. R. , Cleveland P. H. , Richman D. D. . ( 1989; ). Interferons and bacterial lipopolysaccharide protect macrophages from productive infection by human immunodeficiency virus in vitro . . J Exp Med 169:, 1137–1151. [CrossRef] [PubMed]
    [Google Scholar]
  23. Labadie K. , Larcher T. , Joubert C. , Mannioui A. , Delache B. , Brochard P. , Guigand L. , Dubreil L. , Lebon P. . & other authors ( 2010; ). Chikungunya disease in nonhuman primates involves long-term viral persistence in macrophages. . J Clin Invest 120:, 894–906. [CrossRef] [PubMed]
    [Google Scholar]
  24. Levitt N. H. , Ramsburg H. H. , Hasty S. E. , Repik P. M. , Cole F. E. Jr , Lupton H. W. . ( 1986; ). Development of an attenuated strain of chikungunya virus for use in vaccine production. . Vaccine 4:, 157–162. [CrossRef] [PubMed]
    [Google Scholar]
  25. Liberatore R. A. , Bieniasz P. D. . ( 2011; ). Tetherin is a key effector of the antiretroviral activity of type I interferon in vitro and in vivo . . Proc Natl Acad Sci U S A 108:, 18097–18101. [CrossRef] [PubMed]
    [Google Scholar]
  26. Lopez L. A. , Yang S. J. , Exline C. M. , Rengarajan S. , Haworth K. G. , Cannon P. M. . ( 2012; ). Anti-tetherin activities of HIV-1 Vpu and Ebola virus glycoprotein do not involve removal of tetherin from lipid rafts. . J Virol 86:, 5467–5480. [CrossRef] [PubMed]
    [Google Scholar]
  27. Mackey M. F. , Barth R. J. Jr , Noelle R. J. . ( 1998; ). The role of CD40/CD154 interactions in the priming, differentiation, and effector function of helper and cytotoxic T cells. . J Leukoc Biol 63:, 418–428.[PubMed]
    [Google Scholar]
  28. Malvy D. , Ezzedine K. , Mamani-Matsuda M. , Autran B. , Tolou H. , Receveur M. C. , Pistone T. , Rambert J. , Moynet D. , Mossalayi D. . ( 2009; ). Destructive arthritis in a patient with chikungunya virus infection with persistent specific IgM antibodies. . BMC Infect Dis 9:, 200. [CrossRef] [PubMed]
    [Google Scholar]
  29. Mehta H. V. , Jones P. H. , Weiss J. P. , Okeoma C. M. . ( 2012; ). IFN-α and lipopolysaccharide upregulate APOBEC3 mRNA through different signaling pathways. . J Immunol 189:, 4088–4103. [CrossRef] [PubMed]
    [Google Scholar]
  30. Mills J. , Chanock V. , Chanock R. M. . ( 1971; ). Temperature-sensitive mutants of influenza virus. I. Behavior in tissue culture and in experimental animals. . J Infect Dis 123:, 145–157. [CrossRef] [PubMed]
    [Google Scholar]
  31. Neil S. J. , Zang T. , Bieniasz P. D. . ( 2008; ). Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. . Nature 451:, 425–430. [CrossRef] [PubMed]
    [Google Scholar]
  32. Olagnier D. , Scholte F. E. , Chiang C. , Albulescu I. C. , Nichols C. , He Z. , Lin R. , Snijder E. J. , van Hemert M. J. , Hiscott J. . ( 2014; ). Inhibition of dengue and chikungunya virus infections by RIG-I-mediated type I IFN-independent stimulation of the innate antiviral response. . J Virol 88:, 4180–4194. [CrossRef] [PubMed]
    [Google Scholar]
  33. Otero M. , Lago R. , Gomez R. , Lago F. , Dieguez C. , Gómez-Reino J. J. , Gualillo O. . ( 2006; ). Changes in plasma levels of fat-derived hormones adiponectin, leptin, resistin and visfatin in patients with rheumatoid arthritis. . Ann Rheum Dis 65:, 1198–1201. [CrossRef] [PubMed]
    [Google Scholar]
  34. Ozden S. , Huerre M. , Riviere J. P. , Coffey L. L. , Afonso P. V. , Mouly V. , de Monredon J. , Roger J. C. , El Amrani M. . & other authors ( 2007; ). Human muscle satellite cells as targets of Chikungunya virus infection. . PLoS ONE 2:, e527. [CrossRef] [PubMed]
    [Google Scholar]
  35. Partidos C. D. , Weger J. , Brewoo J. , Seymour R. , Borland E. M. , Ledermann J. P. , Powers A. M. , Weaver S. C. , Stinchcomb D. T. , Osorio J. E. . ( 2011; ). Probing the attenuation and protective efficacy of a candidate chikungunya virus vaccine in mice with compromised interferon (IFN) signaling. . Vaccine 29:,3067–3073. [CrossRef] [PubMed]
    [Google Scholar]
  36. Pham T. N. , Lukhele S. , Hajjar F. , Routy J. P. , Cohen E. A. . ( 2014; ). HIV Nef and Vpu protect HIV-infected CD4+ T cells from antibody-mediated cell lysis through down-modulation of CD4 and BST2. . Retrovirology 11:, 15. [CrossRef] [PubMed]
    [Google Scholar]
  37. Pialoux G. , Gaüzère B. A. , Jauréguiberry S. , Strobel M. . ( 2007; ). Chikungunya, an epidemic arbovirosis. . Lancet Infect Dis 7:, 319–327. [CrossRef] [PubMed]
    [Google Scholar]
  38. Powers A. M. , Logue C. H. . ( 2007; ). Changing patterns of chikungunya virus: re-emergence of a zoonotic arbovirus. . J Gen Virol 88:, 2363–2377. [CrossRef] [PubMed]
    [Google Scholar]
  39. Radoshitzky S. R. , Dong L. , Chi X. , Clester J. C. , Retterer C. , Spurgers K. , Kuhn J. H. , Sandwick S. , Ruthel G. . & other authors ( 2010; ). Infectious Lassa virus, but not filoviruses, is restricted by BST-2/tetherin. . J Virol 84:, 10569–10580. [CrossRef] [PubMed]
    [Google Scholar]
  40. Rizvi M. , Pathak D. , Freedman J. E. , Chakrabarti S. . ( 2008; ). CD40–CD40 ligand interactions in oxidative stress, inflammation and vascular disease. . Trends Mol Med 14:, 530–538. [CrossRef] [PubMed]
    [Google Scholar]
  41. Romacho T. , Azcutia V. , Vázquez-Bella M. , Matesanz N. , Cercas E. , Nevado J. , Carraro R. , Rodríguez-Mañas L. , Sánchez-Ferrer C. F. , Peiró C. . ( 2009; ). Extracellular PBEF/NAMPT/visfatin activates pro-inflammatory signalling in human vascular smooth muscle cells through nicotinamide phosphoribosyltransferase activity. . Diabetologia 52:, 2455–2463. [CrossRef] [PubMed]
    [Google Scholar]
  42. Schilte C. , Couderc T. , Chretien F. , Sourisseau M. , Gangneux N. , Guivel-Benhassine F. , Kraxner A. , Tschopp J. , Higgs S. . & other authors ( 2010; ). Type I IFN controls chikungunya virus via its action on nonhematopoietic cells. . J Exp Med 207:, 429–442. [CrossRef] [PubMed]
    [Google Scholar]
  43. Seymour R. L. , Rossi S. L. , Bergren N. A. , Plante K. S. , Weaver S. C. . ( 2013; ). The role of innate versus adaptive immune responses in a mouse model of O’nyong-nyong virus infection. . Am J Trop Med Hyg 88:, 1170–1179. [CrossRef] [PubMed]
    [Google Scholar]
  44. Sourisseau M. , Schilte C. , Casartelli N. , Trouillet C. , Guivel-Benhassine F. , Rudnicka D. , Sol-Foulon N. , Le Roux K. , Prevost M. C. . & other authors ( 2007; ). Characterization of reemerging chikungunya virus. . PLoS Pathog 3:, e89. [CrossRef] [PubMed]
    [Google Scholar]
  45. Swiecki M. , Wang Y. , Gilfillan S. , Lenschow D. J. , Colonna M. . ( 2012; ). Cutting edge: paradoxical roles of BST2/tetherin in promoting type I IFN response and viral infection. . J Immunol 188:, 2488–2492. [CrossRef] [PubMed]
    [Google Scholar]
  46. Thio C. L. , Yusof R. , Abdul-Rahman P. S. , Karsani S. A. . ( 2013; ). Differential proteome analysis of chikungunya virus infection on host cells. . PLoS ONE 8:, e61444. [CrossRef] [PubMed]
    [Google Scholar]
  47. Tokarev A. , Suarez M. , Kwan W. , Fitzpatrick K. , Singh R. , Guatelli J. . ( 2013; ). Stimulation of NF-κB activity by the HIV restriction factor BST2. . J Virol 87:, 2046–2057. [CrossRef] [PubMed]
    [Google Scholar]
  48. Van den Bergh R. , Morin S. , Sass H. J. , Grzesiek S. , Vekemans M. , Florence E. , Tran H. T. , Imiru R. G. , Heyndrickx L. . & other authors ( 2012; ). Monocytes contribute to differential immune pressure on R5 versus X4 HIV through the adipocytokine visfatin/NAMPT. . PLoS ONE 7:, e35074. [CrossRef] [PubMed]
    [Google Scholar]
  49. Veillette M. , Désormeaux A. , Medjahed H. , Gharsallah N. E. , Coutu M. , Baalwa J. , Guan Y. , Lewis G. , Ferrari G. . & other authors ( 2014; ). Interaction with cellular CD4 exposes HIV-1 envelope epitopes targeted by antibody-dependent cell-mediated cytotoxicity. . J Virol 88:, 2633–2644. [CrossRef] [PubMed]
    [Google Scholar]
  50. Wang P. , Xu T. Y. , Guan Y. F. , Su D. F. , Fan G. R. , Miao C. Y. . ( 2009; ). Perivascular adipose tissue-derived visfatin is a vascular smooth muscle cell growth factor: role of nicotinamide mononucleotide. . Cardiovasc Res 81:, 370–380. [CrossRef] [PubMed]
    [Google Scholar]
  51. Wauquier N. , Becquart P. , Nkoghe D. , Padilla C. , Ndjoyi-Mbiguino A. , Leroy E. M. . ( 2011; ). The acute phase of Chikungunya virus infection in humans is associated with strong innate immunity and T CD8 cell activation. . J Infect Dis 204:, 115–123. [CrossRef] [PubMed]
    [Google Scholar]
  52. Werneke S. W. , Schilte C. , Rohatgi A. , Monte K. J. , Michault A. , Arenzana-Seisdedos F. , Vanlandingham D. L. , Higgs S. , Fontanet A. . & other authors ( 2011; ). ISG15 is critical in the control of Chikungunya virus infection independent of UbE1L mediated conjugation. . PLoS Pathog 7:, e1002322. [CrossRef] [PubMed]
    [Google Scholar]
  53. Whitmire J. K. , Flavell R. A. , Grewal I. S. , Larsen C. P. , Pearson T. C. , Ahmed R. . ( 1999; ). CD40–CD40 ligand costimulation is required for generating antiviral CD4 T cell responses but is dispensable for CD8 T cell responses. . J Immunol 163:, 3194–3201.[PubMed]
    [Google Scholar]
  54. Wikan N. , Sakoonwatanyoo P. , Ubol S. , Yoksan S. , Smith D. R. . ( 2012; ). Chikungunya virus infection of cell lines: analysis of the East, Central and South African lineage. . PLoS ONE 7:, e31102. [CrossRef] [PubMed]
    [Google Scholar]
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