Skip to main content
Top
Published in: Virology Journal 1/2017

Open Access 01-12-2017 | Short Report

The effect of bovine BST2A1 on the release and cell-to-cell transmission of retroviruses

Authors: Zhibin Liang, Yang Zhang, Jie Song, Hui Zhang, Suzhen Zhang, Yue Li, Juan Tan, Wentao Qiao

Published in: Virology Journal | Issue 1/2017

Login to get access

Abstract

Background

Human BST2 (hBST2, also called Tetherin) is a host restriction factor that blocks the release of various enveloped viruses. BST2s from different mammals also possess antiviral activity. Bovine BST2s (bBST2s), bBST2A1 and bBST2A2, reduce production of cell-free bovine leukemia virus (BLV) and vesicular stomatitis virus (VSV). However, the effect of bBST2 on other retroviruses remains unstudied.

Results

Here, we studied the antiviral activity of wildtype and mutant bBST2A1 proteins on retroviruses including human immunodeficiency virus type 1 (HIV-1), prototypic foamy virus (PFV), bovine foamy virus (BFV) and bovine immunodeficiency virus (BIV). The results showed that wildtype bBST2A1 suppressed the release of HIV-1, PFV and BFV. We also generated bBST2A1 mutants, and found that GPI anchor and dimerization, but not glycosylation, are essential for antiviral activity of bBST2A1. Moreover, unlike hBST2, bBST2A1 displayed no inhibitory effect on cell-to-cell transmission of PFV, BFV and BIV.

Conclusions

Our data suggested that bBST2A1 inhibited retrovirus release, however, had no effect on cell-to-cell transmission of retroviruses.
Literature
1.
go back to reference Arnaud F, Black SG, Murphy L, Griffiths DJ, Neil SJ, Spencer TE, Palmarini M. Interplay between ovine bone marrow stromal cell antigen 2/tetherin and endogenous retroviruses. J Virol. 2010;84:4415–25.CrossRefPubMedPubMedCentral Arnaud F, Black SG, Murphy L, Griffiths DJ, Neil SJ, Spencer TE, Palmarini M. Interplay between ovine bone marrow stromal cell antigen 2/tetherin and endogenous retroviruses. J Virol. 2010;84:4415–25.CrossRefPubMedPubMedCentral
2.
go back to reference Casartelli N, Sourisseau M, Feldmann J, Guivel-Benhassine F, Mallet A, Marcelin AG, Guatelli J, Schwartz O. Tetherin restricts productive HIV-1 cell-to-cell transmission. PLoS Pathog. 2010;6:e1000955.CrossRefPubMedPubMedCentral Casartelli N, Sourisseau M, Feldmann J, Guivel-Benhassine F, Mallet A, Marcelin AG, Guatelli J, Schwartz O. Tetherin restricts productive HIV-1 cell-to-cell transmission. PLoS Pathog. 2010;6:e1000955.CrossRefPubMedPubMedCentral
3.
go back to reference Chu H, Wang JJ, Qi M, Yoon JJ, Chen X, Wen X, Hammonds J, Ding L, Spearman P. Tetherin/BST-2 is essential for the formation of the intracellular virus-containing compartment in HIV-infected macrophages. Cell host microbe. 2012;12:360–72.CrossRefPubMedPubMedCentral Chu H, Wang JJ, Qi M, Yoon JJ, Chen X, Wen X, Hammonds J, Ding L, Spearman P. Tetherin/BST-2 is essential for the formation of the intracellular virus-containing compartment in HIV-infected macrophages. Cell host microbe. 2012;12:360–72.CrossRefPubMedPubMedCentral
4.
go back to reference Coleman CM, Spearman P, Wu L. Tetherin does not significantly restrict dendritic cell-mediated HIV-1 transmission and its expression is upregulated by newly synthesized HIV-1 Nef. Retrovirology. 2011;8:26.CrossRefPubMedPubMedCentral Coleman CM, Spearman P, Wu L. Tetherin does not significantly restrict dendritic cell-mediated HIV-1 transmission and its expression is upregulated by newly synthesized HIV-1 Nef. Retrovirology. 2011;8:26.CrossRefPubMedPubMedCentral
6.
go back to reference Dietrich I, McMonagle EL, Petit SJ, Vijayakrishnan S, Logan N, Chan CN, Towers GJ, Hosie MJ, Willett BJ. Feline tetherin efficiently restricts release of feline immunodeficiency virus but not spreading of infection. J Virol. 2011;85:5840–52.CrossRefPubMedPubMedCentral Dietrich I, McMonagle EL, Petit SJ, Vijayakrishnan S, Logan N, Chan CN, Towers GJ, Hosie MJ, Willett BJ. Feline tetherin efficiently restricts release of feline immunodeficiency virus but not spreading of infection. J Virol. 2011;85:5840–52.CrossRefPubMedPubMedCentral
7.
go back to reference Durocher Y, Perret S, Kamen A. High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic acids res. 2002;30:E9.CrossRefPubMedPubMedCentral Durocher Y, Perret S, Kamen A. High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic acids res. 2002;30:E9.CrossRefPubMedPubMedCentral
8.
go back to reference Fukuma A, Abe M, Morikawa Y, Miyazawa T, Yasuda J. Cloning and characterization of the antiviral activity of feline Tetherin/BST-2. PLoS one. 2011;6:e18247.CrossRefPubMedPubMedCentral Fukuma A, Abe M, Morikawa Y, Miyazawa T, Yasuda J. Cloning and characterization of the antiviral activity of feline Tetherin/BST-2. PLoS one. 2011;6:e18247.CrossRefPubMedPubMedCentral
9.
go back to reference Giese S, Marsh M. Tetherin can restrict cell-free and cell-cell transmission of HIV from primary macrophages to T cells. PLoS Pathog. 2014;10:e1004189.CrossRefPubMedPubMedCentral Giese S, Marsh M. Tetherin can restrict cell-free and cell-cell transmission of HIV from primary macrophages to T cells. PLoS Pathog. 2014;10:e1004189.CrossRefPubMedPubMedCentral
10.
go back to reference Gnirss K, Zmora P, Blazejewska P, Winkler M, Lins A, Nehlmeier I, Gartner S, Moldenhauer AS, Hofmann-Winkler H, Wolff T, Schindler M, Pohlmann S. Tetherin sensitivity of influenza a viruses is strain specific: role of Hemagglutinin and neuraminidase. J Virol. 2015;89:9178–88.CrossRefPubMedPubMedCentral Gnirss K, Zmora P, Blazejewska P, Winkler M, Lins A, Nehlmeier I, Gartner S, Moldenhauer AS, Hofmann-Winkler H, Wolff T, Schindler M, Pohlmann S. Tetherin sensitivity of influenza a viruses is strain specific: role of Hemagglutinin and neuraminidase. J Virol. 2015;89:9178–88.CrossRefPubMedPubMedCentral
11.
go back to reference Goffinet C, Schmidt S, Kern C, Oberbremer L, Keppler OT. Endogenous CD317/Tetherin limits replication of HIV-1 and murine leukemia virus in rodent cells and is resistant to antagonists from primate viruses. J Virol. 2010;84:11374–84.CrossRefPubMedPubMedCentral Goffinet C, Schmidt S, Kern C, Oberbremer L, Keppler OT. Endogenous CD317/Tetherin limits replication of HIV-1 and murine leukemia virus in rodent cells and is resistant to antagonists from primate viruses. J Virol. 2010;84:11374–84.CrossRefPubMedPubMedCentral
12.
go back to reference Guo HY, Liang ZB, Li Y, Tan J, Chen QM, Qiao WT. A new indicator cell line established to monitor bovine foamy virus infection. Virol sin. 2011;26:315–23.CrossRefPubMed Guo HY, Liang ZB, Li Y, Tan J, Chen QM, Qiao WT. A new indicator cell line established to monitor bovine foamy virus infection. Virol sin. 2011;26:315–23.CrossRefPubMed
13.
go back to reference Gupta RK, Mlcochova P, Pelchen-Matthews A, Petit SJ, Mattiuzzo G, Pillay D, Takeuchi Y, Marsh M, Towers GJ. Simian immunodeficiency virus envelope glycoprotein counteracts tetherin/BST-2/CD317 by intracellular sequestration. Proc Natl Acad Sci U S a. 2009;106:20889–94.CrossRefPubMedPubMedCentral Gupta RK, Mlcochova P, Pelchen-Matthews A, Petit SJ, Mattiuzzo G, Pillay D, Takeuchi Y, Marsh M, Towers GJ. Simian immunodeficiency virus envelope glycoprotein counteracts tetherin/BST-2/CD317 by intracellular sequestration. Proc Natl Acad Sci U S a. 2009;106:20889–94.CrossRefPubMedPubMedCentral
14.
go back to reference Ilinskaya, A., Derse, D., Hill, S., Princler, G., Heidecker, G., 2013. Cell-cell transmission allows human T-lymphotropic virus 1 to circumvent tetherin restriction. Virology 436, 201-209. Ilinskaya, A., Derse, D., Hill, S., Princler, G., Heidecker, G., 2013. Cell-cell transmission allows human T-lymphotropic virus 1 to circumvent tetherin restriction. Virology 436, 201-209.
15.
go back to reference Jia B, Serra-Moreno R, Neidermyer W, Rahmberg A, Mackey J, Fofana IB, Johnson WE, Westmoreland S, Evans DT. Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog. 2009;5:e1000429.CrossRefPubMedPubMedCentral Jia B, Serra-Moreno R, Neidermyer W, Rahmberg A, Mackey J, Fofana IB, Johnson WE, Westmoreland S, Evans DT. Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog. 2009;5:e1000429.CrossRefPubMedPubMedCentral
16.
go back to reference Jolly C, Booth NJ, Neil SJ. Cell-cell spread of human immunodeficiency virus type 1 overcomes tetherin/BST-2-mediated restriction in T cells. J Virol. 2010;84:12185–99.CrossRefPubMedPubMedCentral Jolly C, Booth NJ, Neil SJ. Cell-cell spread of human immunodeficiency virus type 1 overcomes tetherin/BST-2-mediated restriction in T cells. J Virol. 2010;84:12185–99.CrossRefPubMedPubMedCentral
17.
go back to reference Jouvenet N, Neil SJ, Zhadina M, Zang T, Kratovac Z, Lee Y, McNatt M, Hatziioannou T, Bieniasz PD. Broad-spectrum inhibition of retroviral and filoviral particle release by tetherin. J Virol. 2009;83:1837–44.CrossRefPubMed Jouvenet N, Neil SJ, Zhadina M, Zang T, Kratovac Z, Lee Y, McNatt M, Hatziioannou T, Bieniasz PD. Broad-spectrum inhibition of retroviral and filoviral particle release by tetherin. J Virol. 2009;83:1837–44.CrossRefPubMed
18.
go back to reference Kaletsky RL, Francica JR, Agrawal-Gamse C, Bates P. Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proc Natl Acad Sci U S a. 2009;106:2886–91.CrossRefPubMedPubMedCentral Kaletsky RL, Francica JR, Agrawal-Gamse C, Bates P. Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proc Natl Acad Sci U S a. 2009;106:2886–91.CrossRefPubMedPubMedCentral
19.
go back to reference Kuhl BD, Sloan RD, Donahue DA, Bar-Magen T, Liang C, Wainberg MA. Tetherin restricts direct cell-to-cell infection of HIV-1. Retrovirology. 2010;7:115.CrossRefPubMedPubMedCentral Kuhl BD, Sloan RD, Donahue DA, Bar-Magen T, Liang C, Wainberg MA. Tetherin restricts direct cell-to-cell infection of HIV-1. Retrovirology. 2010;7:115.CrossRefPubMedPubMedCentral
20.
go back to reference 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;4:694–709.CrossRefPubMed 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;4:694–709.CrossRefPubMed
21.
go back to reference Le Tortorec A, Neil SJ. Antagonism to and intracellular sequestration of human tetherin by the human immunodeficiency virus type 2 envelope glycoprotein. J Virol. 2009;83:11966–78.CrossRefPubMedPubMedCentral Le Tortorec A, Neil SJ. Antagonism to and intracellular sequestration of human tetherin by the human immunodeficiency virus type 2 envelope glycoprotein. J Virol. 2009;83:11966–78.CrossRefPubMedPubMedCentral
22.
go back to reference Liberatore RA, Bieniasz PD. 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. 2011;108:18097–101.CrossRefPubMedPubMedCentral Liberatore RA, Bieniasz PD. 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. 2011;108:18097–101.CrossRefPubMedPubMedCentral
23.
go back to reference Lv M, Zhang B, Shi Y, Han Z, Zhang Y, Zhou Y, Zhang W, Niu J, Yu XF. Identification of BST-2/tetherin-induced hepatitis B virus restriction and hepatocyte-specific BST-2 inactivation. Sci rep. 2015;5:11736.CrossRefPubMedPubMedCentral Lv M, Zhang B, Shi Y, Han Z, Zhang Y, Zhou Y, Zhang W, Niu J, Yu XF. Identification of BST-2/tetherin-induced hepatitis B virus restriction and hepatocyte-specific BST-2 inactivation. Sci rep. 2015;5:11736.CrossRefPubMedPubMedCentral
24.
go back to reference Mansouri M, Viswanathan K, Douglas JL, Hines J, Gustin J, Moses AV, Fruh K. Molecular mechanism of BST2/tetherin downregulation by K5/MIR2 of Kaposi's sarcoma-associated herpesvirus. J Virol. 2009;83:9672–81.CrossRefPubMedPubMedCentral Mansouri M, Viswanathan K, Douglas JL, Hines J, Gustin J, Moses AV, Fruh K. Molecular mechanism of BST2/tetherin downregulation by K5/MIR2 of Kaposi's sarcoma-associated herpesvirus. J Virol. 2009;83:9672–81.CrossRefPubMedPubMedCentral
25.
go back to reference Mattiuzzo G, Ivol S, Takeuchi Y. Regulation of porcine endogenous retrovirus release by porcine and human tetherins. J Virol. 2010;84:2618–22.CrossRefPubMed Mattiuzzo G, Ivol S, Takeuchi Y. Regulation of porcine endogenous retrovirus release by porcine and human tetherins. J Virol. 2010;84:2618–22.CrossRefPubMed
26.
go back to reference Neil SJ, Zang T, Bieniasz PD. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature. 2008;451:425–30.CrossRefPubMed Neil SJ, Zang T, Bieniasz PD. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature. 2008;451:425–30.CrossRefPubMed
27.
go back to reference Pardieu C, Vigan R, Wilson SJ, Calvi A, Zang T, Bieniasz P, Kellam P, Towers GJ, Neil SJ. 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:e1000843.CrossRefPubMedPubMedCentral Pardieu C, Vigan R, Wilson SJ, Calvi A, Zang T, Bieniasz P, Kellam P, Towers GJ, Neil SJ. 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:e1000843.CrossRefPubMedPubMedCentral
28.
go back to reference Perez-Caballero D, Zang T, Ebrahimi A, McNatt MW, Gregory DA, Johnson MC, Bieniasz PD. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell. 2009;139:499–511.CrossRefPubMedPubMedCentral Perez-Caballero D, Zang T, Ebrahimi A, McNatt MW, Gregory DA, Johnson MC, Bieniasz PD. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell. 2009;139:499–511.CrossRefPubMedPubMedCentral
29.
go back to reference Sakuma T, Noda T, Urata S, Kawaoka Y, Yasuda J. Inhibition of Lassa and Marburg virus production by tetherin. J Virol. 2009;83:2382–5.CrossRefPubMed Sakuma T, Noda T, Urata S, Kawaoka Y, Yasuda J. Inhibition of Lassa and Marburg virus production by tetherin. J Virol. 2009;83:2382–5.CrossRefPubMed
30.
go back to reference Simon V, Bloch N, Landau NR. Intrinsic host restrictions to HIV-1 and mechanisms of viral escape. Nat Immunol. 2015;16:546–53.CrossRefPubMed Simon V, Bloch N, Landau NR. Intrinsic host restrictions to HIV-1 and mechanisms of viral escape. Nat Immunol. 2015;16:546–53.CrossRefPubMed
31.
go back to reference Takeda E, Nakagawa S, Nakaya Y, Tanaka A, Miyazawa T, Yasuda J. Identification and functional analysis of three isoforms of bovine BST-2. PLoS one. 2012;7:e41483.CrossRefPubMedPubMedCentral Takeda E, Nakagawa S, Nakaya Y, Tanaka A, Miyazawa T, Yasuda J. Identification and functional analysis of three isoforms of bovine BST-2. PLoS one. 2012;7:e41483.CrossRefPubMedPubMedCentral
32.
go back to reference Van Damme N, Goff D, Katsura C, Jorgenson RL, Mitchell R, Johnson MC, Stephens EB, Guatelli J. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell host microbe. 2008;3:245–52.CrossRefPubMedPubMedCentral Van Damme N, Goff D, Katsura C, Jorgenson RL, Mitchell R, Johnson MC, Stephens EB, Guatelli J. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell host microbe. 2008;3:245–52.CrossRefPubMedPubMedCentral
33.
go back to reference Wang W, Wang J, Qu M, Li X, Zhang J, Zhang H, Wu J, Yu B, Wu H, Kong W, Yu X. Viral restriction activity of feline BST2 is independent of its N-Glycosylation and induction of NF-kappaB activation. PLoS one. 2015;10:e0138190.CrossRefPubMedPubMedCentral Wang W, Wang J, Qu M, Li X, Zhang J, Zhang H, Wu J, Yu B, Wu H, Kong W, Yu X. Viral restriction activity of feline BST2 is independent of its N-Glycosylation and induction of NF-kappaB activation. PLoS one. 2015;10:e0138190.CrossRefPubMedPubMedCentral
35.
go back to reference Xu FX, Li D, Wang S, Qiao MW. A quantitative assay for measuring of prototypic foamy virus using a Luciferase-based indicator cell line. Acta Scientiarum Naturalium Universitatis Nankaiensis. 2011;44:80-84. Xu FX, Li D, Wang S, Qiao MW. A quantitative assay for measuring of prototypic foamy virus using a Luciferase-based indicator cell line. Acta Scientiarum Naturalium Universitatis Nankaiensis. 2011;44:80-84.
36.
go back to reference Yao X, Guo HY, Liu C, Xu X, Du JS, Liang HY, Geng YQ, Qiao WT. A quantitative assay for measuring of bovine immunodeficiency virus using a luciferase-based indicator cell line. Virol sin. 2010;25:137–44.CrossRefPubMed Yao X, Guo HY, Liu C, Xu X, Du JS, Liang HY, Geng YQ, Qiao WT. A quantitative assay for measuring of bovine immunodeficiency virus using a luciferase-based indicator cell line. Virol sin. 2010;25:137–44.CrossRefPubMed
37.
go back to reference Yin X, Hu Z, Gu Q, Wu X, Zheng YH, Wei P, Wang X. Equine tetherin blocks retrovirus release and its activity is antagonized by equine infectious anemia virus envelope protein. J Virol. 2014;88:1259–70.CrossRefPubMedPubMedCentral Yin X, Hu Z, Gu Q, Wu X, Zheng YH, Wei P, Wang X. Equine tetherin blocks retrovirus release and its activity is antagonized by equine infectious anemia virus envelope protein. J Virol. 2014;88:1259–70.CrossRefPubMedPubMedCentral
38.
go back to reference Zhang F, Wilson SJ, Landford WC, Virgen B, Gregory D, Johnson MC, Munch J, Kirchhoff F, Bieniasz PD, Hatziioannou T. Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell Host Microbe. 2009;6:54–67.CrossRefPubMedPubMedCentral Zhang F, Wilson SJ, Landford WC, Virgen B, Gregory D, Johnson MC, Munch J, Kirchhoff F, Bieniasz PD, Hatziioannou T. Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell Host Microbe. 2009;6:54–67.CrossRefPubMedPubMedCentral
Metadata
Title
The effect of bovine BST2A1 on the release and cell-to-cell transmission of retroviruses
Authors
Zhibin Liang
Yang Zhang
Jie Song
Hui Zhang
Suzhen Zhang
Yue Li
Juan Tan
Wentao Qiao
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2017
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-017-0835-0

Other articles of this Issue 1/2017

Virology Journal 1/2017 Go to the issue