The glycoprotein of vesicular stomatitis virus promotes release of virus-like particles from tetherin-positive cells

PLoS ONE

Volumn 12, Issue 12, 2017, Pages

  Brinkmann, Constantin ^a   Hoffmann, Markus ^a   Lübke, Anastasia ^a   Nehlmeier, Inga ^a   Krämer Kühl, Annika ^a,b   Winkler, Michael ^a   Pöhlmann, Stefan ^a  

^a GERMAN PRIMATE CENTER   (Germany)

^b Boehringer Ingelheim Veterinary Research Center GmbH and Co KG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; GLYCOPROTEIN; TETHERIN; UNCLASSIFIED DRUG; VESICULAR STOMATITIS VIRUS GLYCOPROTEIN; VIRAL PROTEIN; VPU PROTEIN; BONE MARROW STROMAL ANTIGEN 2; GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ARTICLE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MUTATION; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; VESICULOVIRUS; VIRUS LIKE AGENT; VIRUS LIKE PARTICLE RELEASE; VIRUS RELEASE; ANIMAL; CELL LINE; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PIG; VIRION;

ANIMALS; BONE MARROW STROMAL ANTIGEN 2; CELL LINE; GTP-BINDING PROTEINS; HUMANS; SWINE; VESICULOVIRUS; VIRAL PROTEINS; VIRION;

EID: 85037669016     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0189073     Document Type: Article

References (55)

1. Letchworth GJ, Rodriguez LL, Del cJ. (1999) Vesicular stomatitis. Vet J 157: 239–260. https://doi.org/10.1053/tvjl.1998.0303 PMID: 10328837
2. Mead DG, Ramberg FB, Besselsen DG, Mare CJ. (2000) Transmission of vesicular stomatitis virus from infected to noninfected black flies co-feeding on nonviremic deer mice. Science 287: 485–487. PMID: 10642550
3. Rodriguez LL. (2002) Emergence and re-emergence of vesicular stomatitis in the United States. Virus Res 85: 211–219. PMID: 12034487
4. Lichty BD, Power AT, Stojdl DF, Bell JC. (2004) Vesicular stomatitis virus: re-inventing the bullet. Trends Mol Med 10: 210–216. https://doi.org/10.1016/j.molmed.2004.03.003 PMID: 15121047
5. Balachandran S, Porosnicu M, Barber GN. (2001) Oncolytic activity of vesicular stomatitis virus is effective against tumors exhibiting aberrant p53, Ras, or myc function and involves the induction of apopto-sis. J Virol 75: 3474–3479. https://doi.org/10.1128/JVI.75.7.3474-3479.2001 PMID: 11238874
6. Melzer MK, Lopez-Martinez A, Altomonte J. (2017) Oncolytic Vesicular Stomatitis Virus as a Viro-Immu-notherapy: Defeating Cancer with a "Hammer" and "Anvil". Biomedicines 5.
7. ElSherif MS, Brown C, MacKinnon-Cameron D, Li L, Racine T, Alimonti J, et al. (2017) Assessing the safety and immunogenicity of recombinant vesicular stomatitis virus Ebola vaccine in healthy adults: a randomized clinical trial. CMAJ 189: E819–E827. https://doi.org/10.1503/cmaj.170074 PMID: 28630358
8. Halperin SA, Arribas JR, Rupp R, Andrews CP, Chu L, Das R, et al. (2017) Six-Month Safety Data of Recombinant Vesicular Stomatitis Virus-Zaire Ebola Virus Envelope Glycoprotein Vaccine in a Phase 3 Double-Blind, Placebo-Controlled Randomized Study in Healthy Adults. J Infect Dis.
9. Heppner DG Jr., Kemp TL, Martin BK, Ramsey WJ, Nichols R, Dasen EJ, et al. (2017) Safety and immunogenicity of the rVSVG-ZEBOV-GP Ebola virus vaccine candidate in healthy adults: a phase 1b randomised, multicentre, double-blind, placebo-controlled, dose-response study. Lancet Infect Dis 17: 854–866. https://doi.org/10.1016/S1473-3099(17)30313-4 PMID: 28606591
10. Chow J, Franz KM, Kagan JC. (2015) PRRs are watching you: Localization of innate sensing and signaling regulators. Virology 479–480: 104–109. https://doi.org/10.1016/j.virol.2015.02.051 PMID: 25800355
11. Thompson MR, Kaminski JJ, Kurt-Jones EA, Fitzgerald KA. (2011) Pattern recognition receptors and the innate immune response to viral infection. Viruses 3: 920–940. https://doi.org/10.3390/v3060920PMID: 21994762
12. Schneider WM, Chevillotte MD, Rice CM. (2014) Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol 32: 513–545. https://doi.org/10.1146/annurev-immunol-032713-120231 PMID: 24555472
13. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, et al. (2011) A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472: 481–485. https://doi.org/10.1038/nature09907 PMID: 21478870
14. Ferran MC, Lucas-Lenard JM. (1997) The vesicular stomatitis virus matrix protein inhibits transcription from the human beta interferon promoter. J Virol 71: 371–377. PMID: 8985359
15. Hallum JV, Thacore HR, Youngner JS. (1970) Factors affecting the sensitivity of different viruses to interferon. J Virol 6: 156–162. PMID: 4322869
16. Rieder M, Conzelmann KK. (2009) Rhabdovirus evasion of the interferon system. J Interferon Cytokine Res 29: 499–509. https://doi.org/10.1089/jir.2009.0068 PMID: 19715459
17. Liberatore RA, Mastrocola EJ, Powell C, Bieniasz PD. (2017) Tetherin Inhibits Cell-Free Virus Dissemination and Retards Murine Leukemia Virus Pathogenesis. J Virol 91.
18. Weidner JM, Jiang D, Pan XB, Chang J, Block TM, Guo JT. (2010) Interferon-induced cell membrane proteins, IFITM3 and tetherin, inhibit vesicular stomatitis virus infection via distinct mechanisms. J Virol 84: 12646–12657. https://doi.org/10.1128/JVI.01328-10 PMID: 20943977
19. Neil SJ, Zang T, Bieniasz PD. (2008) Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451: 425–430. https://doi.org/10.1038/nature06553 PMID: 18200009
20. Neil SJ. (2013) The antiviral activities of tetherin. Curr Top Microbiol Immunol 371: 67–104. https://doi.org/10.1007/978-3-642-37765-5_3 PMID: 23686232
21. Perez-Caballero D, Zang T, Ebrahimi A, McNatt MW, Gregory DA, Johnson MC, et al. (2009) Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 139: 499–511. https://doi.org/10.1016/j.cell.2009.08.039 PMID: 19879838
22. Sauter D. (2014) Counteraction of the multifunctional restriction factor tetherin. Front Microbiol 5: 163. https://doi.org/10.3389/fmicb.2014.00163 PMID: 24782851
23. Andrew AJ, Miyagi E, Strebel K. (2011) Differential effects of human immunodeficiency virus type 1 Vpu on the stability of BST-2/tetherin. J Virol 85: 2611–2619. https://doi.org/10.1128/JVI.02080-10 PMID: 21191020
24. Douglas JL, Viswanathan K, McCarroll MN, Gustin JK, Fruh K, Moses AV. (2009) Vpu directs the degradation of the human immunodeficiency virus restriction factor BST-2/Tetherin via a {beta}TrCP-depen-dent mechanism. J Virol 83: 7931–7947. https://doi.org/10.1128/JVI.00242-09 PMID: 19515779
25. Mitchell RS, Katsura C, Skasko MA, Fitzpatrick K, Lau D, Ruiz A, et al. (2009) Vpu antagonizes BST-2mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking. PLoS Pathog 5: e1000450. https://doi.org/10.1371/journal.ppat.1000450 PMID: 19478868
26. Kaletsky RL, Francica JR, Agrawal-Gamse C, Bates P. (2009) Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proc Natl Acad Sci U S A 106: 2886–2891. https://doi.org/10.1073/pnas.0811014106 PMID: 19179289
27. Kühl A, Banning C, Marzi A, Votteler J, Steffen I, Bertram S, et al. (2011) The Ebola virus glycoprotein and HIV-1 Vpu employ different strategies to counteract the antiviral factor tetherin. J Infect Dis 204 Suppl 3: S850–S860.
28. Lopez LA, Yang SJ, Hauser H, Exline CM, Haworth KG, Oldenburg J, et al. (2010) Ebola virus glycoprotein counteracts BST-2/Tetherin restriction in a sequence-independent manner that does not require tetherin surface removal. J Virol 84: 7243–7255. https://doi.org/10.1128/JVI.02636-09 PMID: 20444895
29. Lopez LA, Yang SJ, Exline CM, Rengarajan S, Haworth KG, Cannon PM. (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. https://doi.org/10.1128/JVI.06280-11 PMID: 22398279
30. Barallon R, Bauer SR, Butler J, Capes-Davis A, Dirks WG, Elmore E, et al. (2010) Recommendation of short tandem repeat profiling for authenticating human cell lines, stem cells, and tissues. In Vitro Cell Dev Biol Anim 46: 727–732. https://doi.org/10.1007/s11626-010-9333-z PMID: 20614197
31. Butler JM. (2007) Short tandem repeat typing technologies used in human identity testing. Biotechni-ques 43: ii–iv. PMID: 18019344
32. Brinkmann C, Nehlmeier I, Walendy-Gnirss K, Nehls J, Gonzalez HM, Hoffmann M, et al. (2016) The Tetherin Antagonism of the Ebola Virus Glycoprotein Requires an Intact Receptor-Binding Domain and Can Be Blocked by GP1-Specific Antibodies. J Virol 90: 11075–11086. https://doi.org/10.1128/JVI. 01563-16 PMID: 27707924
33. Hoffmann M, Wu YJ, Gerber M, Berger-Rentsch M, Heimrich B, Schwemmle M, et al. (2010) Fusion-active glycoprotein G mediates the cytotoxicity of vesicular stomatitis virus M mutants lacking host shutoff activity. J Gen Virol 91: 2782–2793. https://doi.org/10.1099/vir.0.023978-0 PMID: 20631091
34. Sauter D, Schindler M, Specht A, Landford WN, Munch J, Kim KA, et al. (2009) Tetherin-driven adaptation of Vpu and Nef function and the evolution of pandemic and nonpandemic HIV-1 strains. Cell Host Microbe 6: 409–421. https://doi.org/10.1016/j.chom.2009.10.004 PMID: 19917496
35. Schnell MJ, Buonocore L, Whitt MA, Rose JK. (1996) The minimal conserved transcription stop-start signal promotes stable expression of a foreign gene in vesicular stomatitis virus. J Virol 70: 2318–2323. PMID: 8642658
36. Hanika A, Larisch B, Steinmann E, Schwegmann-Wessels C, Herrler G, Zimmer G. (2005) Use of influenza C virus glycoprotein HEF for generation of vesicular stomatitis virus pseudotypes. J Gen Virol 86: 1455–1465. https://doi.org/10.1099/vir.0.80788-0 PMID: 15831958
37. Maldarelli F, Chen MY, Willey RL, Strebel K. (1993) Human immunodeficiency virus type 1 Vpu protein is an oligomeric type I integral membrane protein. J Virol 67: 5056–5061. PMID: 8331740
38. Marzi A, Wegele A, Pohlmann S. (2006) Modulation of virion incorporation of Ebolavirus glycoprotein: effects on attachment, cellular entry and neutralization. Virology 352: 345–356. https://doi.org/10.1016/j.virol.2006.04.038 PMID: 16777170
39. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676–682. https://doi.org/10.1038/nmeth. 2019 PMID: 22743772
40. Lawson ND, Stillman EA, Whitt MA, Rose JK. (1995) Recombinant vesicular stomatitis viruses from DNA. Proc Natl Acad Sci U S A 92: 4477–4481. PMID: 7753828
41. Sutter G, Ohlmann M, Erfle V. (1995) Non-replicating vaccinia vector efficiently expresses bacteriophage T7 RNA polymerase. FEBS Lett 371: 9–12. PMID: 7664891
42. Berger RM, Zimmer G. (2011) A vesicular stomatitis virus replicon-based bioassay for the rapid and sensitive determination of multi-species type I interferon. PLoS One 6: e25858. https://doi.org/10.1371/journal.pone.0025858 PMID: 21998709
43. Hoffmann M, Gonzalez HM, Berger E, Marzi A, Pohlmann S. (2016) The Glycoproteins of All Filovirus Species Use the Same Host Factors for Entry into Bat and Human Cells but Entry Efficiency Is Species Dependent. PLoS One 11: e0149651. https://doi.org/10.1371/journal.pone.0149651 PMID: 26901159
44. Goffinet C, Allespach I, Homann S, Tervo HM, Habermann A, Rupp D, et al. (2009) HIV-1 antagonism of CD317 is species specific and involves Vpu-mediated proteasomal degradation of the restriction factor. Cell Host Microbe 5: 285–297. https://doi.org/10.1016/j.chom.2009.01.009 PMID: 19286137
45. Jia B, Serra-Moreno R, Neidermyer W, Rahmberg A, Mackey J, Fofana IB, et al. (2009) Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog 5: e1000429. https://doi.org/10.1371/journal.ppat.1000429 PMID: 19436700
46. McNatt MW, Zang T, Hatziioannou T, Bartlett M, Fofana IB, Johnson WE, et al. (2009) Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog 5: e1000300. https://doi.org/10.1371/journal.ppat.1000300 PMID: 19214216
47. Kopecky SA, Lyles DS. (2003) The cell-rounding activity of the vesicular stomatitis virus matrix protein is due to the induction of cell death. J Virol 77: 5524–5528. https://doi.org/10.1128/JVI.77.9.5524-5528. 2003 PMID: 12692256
48. von Kobbe C, van Deursen JM, Rodrigues JP, Sitterlin D, Bachi A, Wu X, et al. (2000) Vesicular stomatitis virus matrix protein inhibits host cell gene expression by targeting the nucleoporin Nup98. Mol Cell 6: 1243–1252. PMID: 11106761
49. Taylor JK, Coleman CM, Postel S, Sisk JM, Bernbaum JG, Venkataraman T, et al. (2015) Severe Acute Respiratory Syndrome Coronavirus ORF7a Inhibits Bone Marrow Stromal Antigen 2 Virion Tethering through a Novel Mechanism of Glycosylation Interference. J Virol 89: 11820–11833. https://doi.org/10.1128/JVI.02274-15 PMID: 26378163
50. Sun X, Belouzard S, Whittaker GR. (2008) Molecular architecture of the bipartite fusion loops of vesicular stomatitis virus glycoprotein G, a class III viral fusion protein. J Biol Chem 283: 6418–6427. https://doi.org/10.1074/jbc.M708955200 PMID: 18165228
51. Dube M, Paquay C, Roy BB, Bego MG, Mercier J, Cohen EA. (2011) HIV-1 Vpu antagonizes BST-2 by interfering mainly with the trafficking of newly synthesized BST-2 to the cell surface. Traffic 12: 1714–1729. https://doi.org/10.1111/j.1600-0854.2011.01277.x PMID: 21902775
52. Schmidt S, Fritz JV, Bitzegeio J, Fackler OT, Keppler OT. (2011) HIV-1 Vpu blocks recycling and bio-synthetic transport of the intrinsic immunity factor CD317/tetherin to overcome the virion release restriction. MBio 2: e00036–11. https://doi.org/10.1128/mBio.00036-11 PMID: 21610122
53. Cleverley DZ, Lenard J. (1998) The transmembrane domain in viral fusion: essential role for a conserved glycine residue in vesicular stomatitis virus G protein. Proc Natl Acad Sci U S A 95: 3425–3430. PMID: 9520382
54. Hacke M, Bjorkholm P, Hellwig A, Himmels P, Ruiz de AC, Brugger B, et al. (2015) Inhibition of Ebola virus glycoprotein-mediated cytotoxicity by targeting its transmembrane domain and cholesterol. Nat Commun 6: 7688. https://doi.org/10.1038/ncomms8688 PMID: 26158910
55. Lyles DS, McKenzie M, Parce JW. (1992) Subunit interactions of vesicular stomatitis virus envelope glycoprotein stabilized by binding to viral matrix protein. J Virol 66: 349–358. PMID: 1309251