Herpes simplex virus 1 counteracts tetherin restriction via its virion host shutoff activity

Journal of Virology

Volumn 87, Issue 24, 2013, Pages 13115-13123

  Zenner, Helen L ^a   Mauricio, Rui ^a   Banting, George ^b   Crump, Colin M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MESSENGER RNA; RIBONUCLEASE; TETHERIN; UNCLASSIFIED DRUG; VIRION HOST SHUTOFF PROTEIN;

ANTIVIRAL ACTIVITY; ARTICLE; CELL STRAIN CACO 2; CELL STRAIN COS7; CONTROLLED STUDY; HELA CELL; HERPES SIMPLEX VIRUS 1; IMMUNE EVASION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA DEGRADATION; VERO CELL; VIRUS RELEASE; VIRUS REPLICATION;

ANTIGENS, CD; GPI-LINKED PROTEINS; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN BINDING; RIBONUCLEASES; VIRAL PROTEINS; VIRUS RELEASE; VIRUS REPLICATION;

EID: 84888048397     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02167-13     Document Type: Article

References (50)

1. Le Tortorec A, Willey S, Neil SJ. 2011. Antiviral inhibition of enveloped virus release by tetherin/BST-2:action and counteraction. Viruses 3:520-540.
2. Swiecki M, Omattage NS, Brett TJ. 2013. BST-2/tetherin:structural biology, viral antagonism, and immunobiology of a potent host antiviral factor. Mol. Immunol. 54:132-139.
3. Hinz A, Miguet N, Natrajan G, Usami Y, Yamanaka H, Renesto P, Hartlieb B, McCarthy AA, Simorre JP, Gottlinger H, Weissenhorn W. 2010. Structural basis of HIV-1 tethering to membranes by the BST-2/ tetherin ectodomain. Cell Host Microbe 7:314-323.
4. Perez-Caballero D, Zang T, Ebrahimi A, McNatt MW, Gregory DA, Johnson MC, Bieniasz PD. 2009. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 139:499-511.
5. Venkatesh S, Bieniasz PD. 2013. Mechanism of HIV-1 virion entrapment by tetherin. PLoS Pathog. 9:e1003483. doi:10.1371/journal.ppat.1003483.
6. Galao RP, Le Tortorec A, Pickering S, Kueck T, Neil SJ. 2012. Innate sensing of HIV-1 assembly by tetherin induces NFkappaB-dependent proinflammatory responses. Cell Host Microbe 12:633-644.
7. Tokarev A, Suarez M, Kwan W, Fitzpatrick K, Singh R, Guatelli J. 2013. Stimulation of NF-kappaB activity by the HIV restriction factor BST2. J. Virol. 87:2046-2057.
8. Rollason R, Korolchuk V, Hamilton C, Schu P, Banting G. 2007. Clathrin-mediated endocytosis of a lipid-raft-associated protein is mediated through a dual tyrosine motif. J. Cell Sci. 120:3850-3858.
9. Hollinshead M, Johns HL, Sayers CL, Gonzalez-Lopez C, Smith GL, Elliott G. 2012. Endocytic tubules regulated by Rab GTPases 5 and 11 are used for envelopment of herpes simplex virus. EMBO J. 31:4204-4220.
10. Johnson DC, Baines JD. 2011. Herpesviruses remodel host membranes for virus egress. Nat. Rev. Microbiol. 9:382-394.
11. Mettenleiter TC, Klupp BG, Granzow H. 2009. Herpesvirus assembly:an update. Virus Res. 143:222-234.
12. Mansouri M, Viswanathan K, Douglas JL, Hines J, Gustin J, Moses AV, Fruh K. 2009. Molecular mechanism of BST2/tetherin downregulation by K5/MIR2 of Kaposi's sarcoma-associated herpesvirus. J. Virol. 83:9672-9681.
13. Pardieu C, Vigan R, Wilson SJ, Calvi A, Zang T, Bieniasz P, Kellam P, Towers GJ, Neil SJ. 2010. The RING-CH ligase K5 antagonizes restriction of KSHV and HIV-1 particle release by mediating ubiquitin-dependent endosomal degradation of tetherin. PLoS Pathog. 6:e1000843. doi:10.1371/journal.ppat.1000843.
14. Viswanathan K, Smith MS, Malouli D, Mansouri M, Nelson JA, Fruh K. 2011. BST2/tetherin enhances entry of human cytomegalovirus. PLoS Pathog. 7:e1002332. doi:10.1371/journal.ppat.1002332.
15. Jolly C, Booth NJ, Neil SJ. 2010. Cell-cell spread of human immunodeficiency virus type 1 overcomes tetherin/BST-2-mediated restriction in T cells. J. Virol. 84:12185-12199.
16. Liberatore RA, Bieniasz PD. 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.
17. Swiecki M, Wang Y, Gilfillan S, Lenschow DJ, Colonna M. 2012. Cutting edge:paradoxical roles of BST2/tetherin in promoting type I IFN response and viral infection. J. Immunol. 188:2488-2492.
18. Agromayor M, Soler N, Caballe A, Kueck T, Freund SM, Allen MD, Bycroft M, Perisic O, Ye Y, McDonald B, Scheel H, Hofmann K, Neil SJ, Martin-Serrano J, Williams RL. 2012. The UBAP1 subunit of ESCRT-I interacts with ubiquitin via a SOUBA domain. Structure 20:414-428.
19. Smiley JR. 2004. Herpes simplex virus virion host shutoff protein:immune evasion mediated by a viral RNase? J. Virol. 78:1063-1068.
20. Taddeo B, Roizman B. 2006. The virion host shutoff protein (UL41) of herpes simplex virus 1 is an endoribonuclease with a substrate specificity similar to that of RNase A. J. Virol. 80:9341-9345.
21. Cotter CR, Kim WK, Nguyen ML, Yount JS, Lopez CB, Blaho JA, Moran TM. 2011. The virion host shutoff protein of herpes simplex virus 1 blocks the replication-independent activation of NF-kappaB in dendritic cells in the absence of type I interferon signaling. J. Virol. 85:12662-12672.
22. Pasieka TJ, Cilloniz C, Carter VS, Rosato P, Katze MG, Leib DA. 2011. Functional genomics reveals an essential and specific role for Stat1 in protection of the central nervous system following herpes simplex virus corneal infection. J. Virol. 85:12972-12981.
23. Tigges MA, Leng S, Johnson DC, Burke RL. 1996. Human herpes simplex virus (HSV)-specific CD8+ CTL clones recognize HSV-2-infected fibroblasts after treatment with IFN-gamma or when virion host shutoff functions are disabled. J. Immunol. 156:3901-3910.
24. Duerst RJ, Morrison LA. 2004. Herpes simplex virus 2 virion host shutoff protein interferes with type I interferon production and responsiveness. Virology 322:158-167.
25. Pasieka TJ, Lu B, Crosby SD, Wylie KM, Morrison LA, Alexander DE, Menachery VD, Leib DA. 2008. Herpes simplex virus virion host shutoff attenuates establishment of the antiviral state. J. Virol. 82:5527-5535.
26. Strelow LI, Leib DA. 1995. Role of the virion host shutoff (Vhs) of herpes simplex virus type 1 in latency and pathogenesis. J. Virol. 69:6779-6786.
27. Pasieka TJ, Cilloniz C, Lu B, Teal TH, Proll SC, Katze MG, Leib DA. 2009. Host responses to wild-type and attenuated herpes simplex virus infection in the absence of Stat1. J. Virol. 83:2075-2087.
28. Tischer BK, Smith GA, Osterrieder N. 2010. En passant mutagenesis:a two step markerless red recombination system. Methods Mol. Biol. 634:421-430.
29. Gierasch WW, Zimmerman DL, Ward SL, Vanheyningen TK, Romine JD, Leib DA. 2006. Construction and characterization of bacterial artificial chromosomes containing HSV-1 strains 17 and KOS. J. Virol. Methods 135:197-206.
30. Svobodova S, Bell S, Crump CM. 2012. Analysis of the interaction between the essential herpes simplex virus 1 tegument proteins VP16 and VP1/2. J. Virol. 86:473-483.
31. Zenner HL, Yoshimura S, Barr FA, Crump CM. 2011. Analysis of Rab GTPase-activating proteins indicates that Rab1a/b and Rab43 are important for herpes simplex virus 1 secondary envelopment. J. Virol. 85:8012-8021.
32. Neil SJ, Zang T, Bieniasz PD. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425-430.
33. Campadelli G, Brandimarti R, Di Lazzaro C, Ward PL, Roizman B, Torrisi MR. 1993. Fragmentation and dispersal of Golgi proteins and redistribution of glycoproteins and glycolipids processed through the Golgi apparatus after infection with herpes simplex virus 1. Proc. Natl. Acad. Sci. U.S.A. 90:2798-2802.
34. Dauber B, Pelletier J, Smiley JR. 2011. The herpes simplex virus 1 Vhs protein enhances translation of viral true late mRNAs and virus production in a cell type-dependent manner. J. Virol. 85:5363-5373.
35. Emeny JM, Morgan MJ. 1979. Regulation of the interferon system:evidence that Vero cells have a genetic defect in interferon production. J. Gen. Virol. 43:247-252.
36. Rollason R, Korolchuk V, Hamilton C, Jepson M, Banting G. 2009. A CD317/tetherin-RICH2 complex plays a critical role in the organization of the subapical actin cytoskeleton in polarized epithelial cells. J. Cell Biol. 184:721-736.
37. Dafa-Berger A, Kuzmina A, Fassler M, Yitzhak-Asraf H, Shemer-Avni Y, Taube R. 2012. Modulation of hepatitis C virus release by the interferon-induced protein BST-2/tetherin. Virology 428:98-111.
38. Radoshitzky SR, Dong L, Chi X, Clester JC, Retterer C, Spurgers K, Kuhn JH, Sandwick S, Ruthel G, Kota K, Boltz D, Warren T, Kranzusch PJ, Whelan SP, Bavari S. 2010. Infectious Lassa virus, but not filoviruses, is restricted by BST-2/tetherin. J. Virol. 84:10569-10580.
39. Billcliff PG, Rollason R, Prior I, Owen DM, Gaus K, Banting G. 2013. CD317/tetherin is an organiser of membrane microdomains. J. Cell Sci. 126:1553-1564.
40. Kupzig S, Korolchuk V, Rollason R, Sugden A, Wilde A, Banting G. 2003. Bst-2/HM1.24 is a raft-associated apical membrane protein with an unusual topology. Traffic 4:694-709.
41. Page HG, Read GS. 2010. The virion host shutoff endonuclease (UL41) of herpes simplex virus interacts with the cellular cap-binding complex eIF4F. J. Virol. 84:6886-6890.
42. Shiflett LA, Read GS. 2013. mRNA decay during herpes simplex virus (HSV) infections:mutations that affect translation of an mRNA influence the sites at which it is cleaved by the HSVvirion host shutoff (Vhs) protein. J. Virol. 87:94-109.
43. Taylor KE, Mossman KL. 2013. Recent advances in understanding viral evasion of type I interferon. Immunology 138:190-197.
44. Smibert CA, Johnson DC, Smiley JR. 1992. Identification and characterization of the virion-induced host shutoff product of herpes simplex virus gene UL41. J. Gen. Virol. 73:467-470.
45. Bego MG, Mercier J, Cohen EA. 2012. Virus-activated interferon regulatory factor 7 upregulates expression of the interferon-regulated BST2 gene independently of interferon signaling. J. Virol. 86:3513-3527.
46. Liu MQ, Zhou DJ, Wang X, Zhou W, Ye L, Li JL, Wang YZ, Ho WZ. 2012. IFN-lambda3 inhibits HIV infection of macrophages through the JAK-STAT pathway. PLoS One 7:e35902. doi:10.1371/journal.pone.0035902.
47. Mossman KL, Smiley JR. 2002. Herpes simplex virus ICP0 and ICP34.5 counteract distinct interferon-induced barriers to virus replication. J. Virol. 76:1995-1998.
48. Blondeau C, Pelchen-Matthews A, Mlcochova P, Marsh M, Milne RSB, Towers GJ. 2013. Tetherin restricts herpes simplex virus 1 and is antagonized by glycoprotein M. J. Virol. 87:13124-13133.
49. Crump CM, Bruun B, Bell S, Pomeranz LE, Minson T, Browne HM. 2004. Alphaherpesvirus glycoprotein M causes the relocalization of plasma membrane proteins. J. Gen. Virol. 85:3517-3527.
50. Ren Y, Bell S, Zenner HL, Lau SY, Crump CM. 2012. Glycoprotein M is important for the efficient incorporation of glycoprotein H-L into herpes simplex virus type 1 particles. J. Gen. Virol. 93:319-329.