Influenza a virus does not encode a tetherin antagonist with Vpu-like activity and induces IFN-dependent tetherin expression in infected cells

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Winkler, Michael ^a   Bertram, Stephanie ^a   Gnirß, Kerstin ^a,b   Nehlmeier, Inga ^a   Gawanbacht, Ali ^c   Kirchhoff, Frank ^c   Ehrhardt, Christina ^d   Ludwig, Stephan ^d   Kiene, Miriam ^b   Moldenhauer, Anna Sophie ^a   Goedecke, Ulrike ^a   Karsten, Christina B ^a,b   Kühl, Annika ^a,b   Pöhlmann, Stefan ^a,b  

^a GERMAN PRIMATE CENTER   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY HOSPITAL ULM   (Germany)

^d UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; NONSTRUCTURAL PROTEIN 1; SMALL INTERFERING RNA; TETHERIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; INFLUENZA VIRUS A; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; TARGET CELL; UPREGULATION; VIRION; VIRUS RELEASE;

ANTIGENS, CD; CELL LINE, TUMOR; CELL MEMBRANE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, VIRAL; GPI-LINKED PROTEINS; HEK293 CELLS; HELA CELLS; HIV-1; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; INFLUENZA A VIRUS; INTERFERONS; PLASMIDS; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRION;

EID: 84865413706     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043337     Document Type: Article

References (46)

1. Versteeg GA, Garcia-Sastre A, (2010) Viral tricks to grid-lock the type I interferon system. Current opinion in microbiology 13: 508-516.
2. Neil SJ, Zang T, Bieniasz PD, (2008) Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451: 425-430.
3. Van Damme N, Goff D, Katsura C, Jorgenson RL, Mitchell R, et al. (2008) 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 3: 245-252.
4. Bartee E, McCormack A, Fruh K, (2006) Quantitative membrane proteomics reveals new cellular targets of viral immune modulators. PLoS pathogens 2: e107.
5. Jia B, Serra-Moreno R, Neidermyer W, Rahmberg A, Mackey J, et al. (2009) Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS pathogens 5: e1000429.
6. Jouvenet N, Neil SJ, Zhadina M, Zang T, Kratovac Z, et al. (2009) Broad-spectrum inhibition of retroviral and filoviral particle release by tetherin. Journal of virology 83: 1837-1844.
7. Kaletsky RL, Francica JR, Agrawal-Gamse C, Bates P, (2009) Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proceedings of the National Academy of Sciences of the United States of America 106: 2886-2891.
8. Radoshitzky SR, Dong L, Chi X, Clester JC, Retterer C, et al. (2010) Infectious Lassa virus, but not filoviruses, is restricted by BST-2/tetherin. Journal of virology 84: 10569-10580.
9. Sakuma T, Noda T, Urata S, Kawaoka Y, Yasuda J, (2009) Inhibition of Lassa and Marburg virus production by tetherin. Journal of virology 83: 2382-2385.
10. Zhang F, Wilson SJ, Landford WC, Virgen B, Gregory D, et al. (2009) Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell host & microbe 6: 54-67.
11. Kühl A, Banning C, Marzi A, Votteler J, Steffen I, et al. (2011) The Ebola virus glycoprotein and HIV-1 Vpu employ different strategies to counteract the antiviral factor tetherin. The Journal of infectious diseases 204Suppl 3: S850-860.
12. Lopez LA, Yang SJ, Hauser H, Exline CM, Haworth KG, et al. (2010) Ebola virus glycoprotein counteracts BST-2/Tetherin restriction in a sequence-independent manner that does not require tetherin surface removal. Journal of virology 84: 7243-7255.
13. Perez-Caballero D, Zang T, Ebrahimi A, McNatt MW, Gregory DA, et al. (2009) Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 139: 499-511.
14. Kupzig S, Korolchuk V, Rollason R, Sugden A, Wilde A, et al. (2003) Bst-2/HM1.24 is a raft-associated apical membrane protein with an unusual topology. Traffic 4: 694-709.
15. Goffinet C, Allespach I, Homann S, Tervo HM, Habermann A, 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.
16. Mitchell RS, Katsura C, Skasko MA, Fitzpatrick K, Lau D, et al. (2009) Vpu antagonizes BST-2-mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking. PLoS pathogens 5: e1000450.
17. Lopez LA, Yang SJ, Exline CM, Rengarajan S, Haworth KG, et al. (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.
18. Chen BJ, Leser GP, Morita E, Lamb RA, (2007) Influenza virus hemagglutinin and neuraminidase, but not the matrix protein, are required for assembly and budding of plasmid-derived virus-like particles. Journal of virology 81: 7111-7123.
19. Rossman JS, Jing X, Leser GP, Lamb RA, (2010) Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142: 902-913.
20. Rossman JS, Lamb RA, (2011) Influenza virus assembly and budding. Virology 411: 229-236.
21. Yondola MA, Fernandes F, Belicha-Villanueva A, Uccelini M, Gao Q, et al. (2011) Budding capability of the influenza virus neuraminidase can be modulated by tetherin. Journal of virology 85: 2480-2491.
22. Watanabe R, Leser GP, Lamb RA, (2011) Influenza virus is not restricted by tetherin whereas influenza VLP production is restricted by tetherin. Virology 417: 50-56.
23. Kühl A, Münch J, Sauter D, Bertram S, Glowacka I, et al. (2010) Calcium-modulating cyclophilin ligand does not restrict retrovirus release. Nature medicine 16: 155-156; author reply 157.
24. Bruce EA, Abbink TE, Wise HM, Rollason R, Galao RP, et al. (2012) Release of filamentous and spherical influenza A virus is not restricted by tetherin. The Journal of general virology 93: 963-9.
25. Emeny JM, Morgan MJ, (1979) Regulation of the interferon system: evidence that Vero cells have a genetic defect in interferon production. The Journal of general virology 43: 247-252.
26. Douglas JL, Gustin JK, Viswanathan K, Mansouri M, Moses AV, et al. (2010) The great escape: viral strategies to counter BST-2/tetherin. PLoS pathogens 6: e1000913.
27. Evans DT, Serra-Moreno R, Singh RK, Guatelli JC, (2010) BST-2/tetherin: a new component of the innate immune response to enveloped viruses. Trends in microbiology 18: 388-396.
28. Hammonds J, Wang JJ, Yi H, Spearman P, (2010) Immunoelectron microscopic evidence for Tetherin/BST2 as the physical bridge between HIV-1 virions and the plasma membrane. PLoS Pathog 6: e1000749.
29. Goto H, Kawaoka Y, (1998) A novel mechanism for the acquisition of virulence by a human influenza A virus. Proc Natl Acad Sci U S A 95: 10224-10228.
30. Schmidt S, Fritz JV, Bitzegeio J, Fackler OT, Keppler OT, (2011) HIV-1 Vpu blocks recycling and biosynthetic transport of the intrinsic immunity factor CD317/tetherin to overcome the virion release restriction. mBio 2: e00036-00011.
31. Goffinet C, Homann S, Ambiel I, Tibroni N, Rupp D, et al. (2010) Antagonism of CD317 restriction of human immunodeficiency virus type 1 (HIV-1) particle release and depletion of CD317 are separable activities of HIV-1 Vpu. Journal of virology 84: 4089-4094.
32. Erikson E, Adam T, Schmidt S, Lehmann-Koch J, Over B, et al. (2011) In vivo expression profile of the antiviral restriction factor and tumor-targeting antigen CD317/BST-2/HM1.24/tetherin in humans. Proceedings of the National Academy of Sciences of the United States of America 108: 13688-13693.
33. Ehrhardt C, Seyer R, Hrincius ER, Eierhoff T, Wolff T, et al. (2010) Interplay between influenza A virus and the innate immune signaling. Microbes and infection/Institut Pasteur 12: 81-87.
34. Mosca JD, Pitha PM, (1986) Transcriptional and posttranscriptional regulation of exogenous human beta interferon gene in simian cells defective in interferon synthesis. Molecular and cellular biology 6: 2279-2283.
35. Cao W, Bover L, Cho M, Wen X, Hanabuchi S, et al. (2009) Regulation of TLR7/9 responses in plasmacytoid dendritic cells by BST2 and ILT7 receptor interaction. The Journal of experimental medicine 206: 1603-1614.
36. Khurana S, Krementsov DN, de Parseval A, Elder JH, Foti M, et al. (2007) Human immunodeficiency virus type 1 and influenza virus exit via different membrane microdomains. Journal of virology 81: 12630-12640.
37. Mangeat B, Cavagliotti L, Lehmann M, Gers-Huber G, Kaur I, et al. (2012) Influenza virus partially counteracts a restriction imposed by tetherin/BST-2. J Biol Chem 287: 22015-29.
38. Gao F, Li Y, Decker JM, Peyerl FW, Bibollet-Ruche F, et al. (2003) Codon usage optimization of HIV type 1 subtype C gag, pol, env, and nef genes: in vitro expression and immune responses in DNA-vaccinated mice. AIDS research and human retroviruses 19: 817-823.
39. Nguyen KL, Llano M, Akari H, Miyagi E, Poeschla EM, et al. (2004) Codon optimization of the HIV-1 vpu and vif genes stabilizes their mRNA and allows for highly efficient Rev-independent expression. Virology 319: 163-175.
40. Marzi A, Akhavan A, Simmons G, Gramberg T, Hofmann H, et al. (2006) The signal peptide of the ebolavirus glycoprotein influences interaction with the cellular lectins DC-SIGN and DC-SIGNR. Journal of virology 80: 6305-6317.
41. Sauter D, Schindler M, Specht A, Landford WN, Munch J, 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.
42. Jiang D, Guo H, Xu C, Chang J, Gu B, et al. (2008) Identification of three interferon-inducible cellular enzymes that inhibit the replication of hepatitis C virus. J Virol 82: 1665-1678.
43. Bertram S, Glowacka I, Blazejewska P, Soilleux E, Allen P, et al. (2010) TMPRSS2 and TMPRSS4 facilitate trypsin-independent spread of influenza virus in Caco-2 cells. J Virol 84: 10016-10025.
44. Matrosovich M, Matrosovich T, Garten W, Klenk HD, (2006) New low-viscosity overlay medium for viral plaque assays. Virology journal 3: 63.
45. Kawai S, Yoshimura Y, Iida S, Kinoshita Y, Koishihara Y, et al. (2006) Antitumor activity of humanized monoclonal antibody against HM1.24 antigen in human myeloma xenograft models. Oncology reports 15: 361-367.
46. Chesebro B, Wehrly K, Nishio J, Perryman S, (1992) Macrophage-tropic human immunodeficiency virus isolates from different patients exhibit unusual V3 envelope sequence homogeneity in comparison with T-cell-tropic isolates: definition of critical amino acids involved in cell tropism. Journal of virology 66: 6547-6554.