Differential sensitivities of tetherin isoforms to counteraction by primate lentiviruses

Journal of Virology

Volumn 88, Issue 10, 2014, Pages 5845-5858

  Weinelt, Julia ^a   Neil, Stuart J D ^a  

^a GUY S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; TETHERIN; UNCLASSIFIED DRUG; VPU PROTEIN;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 VPU; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN SENSITIVITY; PROTEIN STRUCTURE, FUNCTION AND VARIABILITY; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SIMIAN IMMUNODEFICIENCY VIRUS; UBIQUITINATION; VIRUS RELEASE; VIRUS RESISTANCE;

ANIMALS; ANTIGENS, CD; HOST-PATHOGEN INTERACTIONS; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; LENTIVIRUSES, PRIMATE; PRIMATES; PROTEIN ISOFORMS; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 84899090611     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03818-13     Document Type: Article

References (62)

1. Neil SJ. 2013. The antiviral activities of tetherin. Curr. Top. Microbiol. Immunol. 371:67-104. http://dx.doi.org/10.1007/978-3-642-37765-5_3.
2. Neil SJ, Zang T, Bieniasz PD. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425-430. http://dx.doi.org /10.1038/nature06553.
3. Jouvenet N, Neil SJ, Zhadina M, Zang T, Kratovac Z, Lee Y, McNatt M, Hatziioannou T, Bieniasz PD. 2009. Broad-spectrum inhibition of retroviral and filoviral particle release by tetherin. J. Virol. 83:1837-1844. http://dx.doi.org/10.1128/JVI.02211-08.
4. Zenner HL, Mauricio R, Banting G, Crump CM. 2013. Herpes simplex virus 1 counteracts tetherin restriction via its virion host shutoff activity. J. Virol. 87:13115-13123. http://dx.doi.org/10.1128/JVI.02167-13.
5. 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. http://dx .doi.org/10.1371/journal.ppat.1000843.
6. 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. http://dx.doi.org/10.1128/JVI.00597-09.
7. Blondeau C, Pelchen-Matthews A, Mlcochova P, Marsh M, Milne RS, Towers GJ. 2013. Tetherin restricts herpes simplex virus 1 and is antagonized by glycoprotein m. J. Virol. 87:13124-13133. http://dx.doi.org/10 .1128/JVI.02250-13.
8. Sakuma T, Noda T, Urata S, Kawaoka Y, Yasuda J. 2009. Inhibition of Lassa and Marburg virus production by tetherin. J. Virol. 83:2382-2385. http://dx.doi.org/10.1128/JVI.01607-08.
9. 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. http://dx.doi.org/10 .1016/j.cell.2009.08.039.
10. Venkatesh S, Bieniasz PD. 2013. Mechanism of HIV-1 virion entrapment by tetherin. PLoS Pathog. 9:e1003483. http://dx.doi.org/10.1371/journal .ppat.1003483.
11. Cocka LJ, Bates P. 2012. Identification of alternatively translated tetherin isoforms with differing antiviral and signaling activities. PLoS Pathog. 8:e1002931. http://dx.doi.org/10.1371/journal.ppat.1002931.
12. Galão 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. http://dx.doi .org/10.1016/j.chom.2012.10.007.
13. 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. http://dx.doi.org/10.1128/JVI.02272-12.
14. Van Damme N, Goff D, Katsura C, Jorgenson RL, Mitchell R, Johnson MC, Stephens EB, Guatelli J. 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. http://dx.doi.org /10.1016/j.chom.2008.03.001.
15. Jia B, Serra-Moreno R, Neidermyer W, Rahmberg A, Mackey J, Fofana IB, Johnson WE, Westmoreland S, Evans DT. 2009. Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/ BST2. PLoS Pathog. 5:e1000429. http://dx.doi.org/10.1371/journal.ppat .1000429.
16. Zhang F, Wilson SJ, Landford WC, Virgen B, Gregory D, Johnson MC, Munch J, Kirchhoff F, Bieniasz PD, Hatziioannou T. 2009. Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell Host Microbe 6:54-67. http://dx.doi.org/10.1016/j.chom.2009.05.008.
17. Gupta RK, Mlcochova P, Pelchen-Matthews A, Petit SJ, Mattiuzzo G, Pillay D, Takeuchi Y, Marsh M, Towers GJ. 2009. Simian immunodeficiency virus envelope glycoprotein counteracts tetherin/BST-2/CD317 by intracellular sequestration. Proc. Natl. Acad. Sci. U. S. A. 106:20889-20894. http://dx.doi.org/10.1073/pnas.0907075106.
18. Le Tortorec A, Neil SJ. 2009. Antagonism to and intracellular sequestration of human tetherin by the human immunodeficiency virus type 2 envelope glycoprotein. J. Virol. 83:11966-11978. http://dx.doi.org/10 .1128/JVI.01515-09.
19. Kaletsky RL, Francica JR, Agrawal-Gamse C, Bates P. 2009. Tetherinmediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proc. Natl. Acad. Sci. U. S. A. 106:2886-2891. http://dx.doi.org /10.1073/pnas.0811014106.
20. Sauter D, Specht A, Kirchhoff F. 2010. Tetherin: holding on and letting go. Cell 141:392-398. http://dx.doi.org/10.1016/j.cell.2010.04.022.
21. Sauter D, Schindler M, Specht A, Landford WN, Munch J, Kim KA, Votteler J, Schubert U, Bibollet-Ruche F, Keele BF, Takehisa J, Ogando Y, Ochsenbauer C, Kappes JC, Ayouba A, Peeters M, Learn GH, Shaw G, Sharp PM, Bieniasz P, Hahn BH, Hatziioannou T, Kirchhoff F. 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. http://dx.doi.org/10.1016/j.chom.2009.10.004.
22. 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. http://dx .doi.org/10.1242/jcs.003343.
23. Dubé M, Roy BB, Guiot-Guillain P, Binette J, Mercier J, Chiasson A, Cohen EA. 2010. Antagonism of tetherin restriction of HIV-1 release by Vpu involves binding and sequestration of the restriction factor in a perinuclear compartment. PLoS Pathog. 6:e1000856. http://dx.doi.org/10 .1371/journal.ppat.1000856.
24. Skasko M, Wang Y, Tian Y, Tokarev A, Munguia J, Ruiz A, Stephens EB, Opella SJ, Guatelli J. 2012. HIV-1 Vpu protein antagonizes innate restriction factor BST-2 via lipid-embedded helix-helix interactions. J. Biol. Chem. 287:58-67. http://dx.doi.org/10.1074/jbc.M111.296772.
25. Vigan R, Neil SJ. 2010. Determinants of tetherin antagonism in the transmembrane domain of the human immunodeficiency virus type 1 Vpu protein. J. Virol. 84:12958 -12970. http://dx.doi.org/10.1128/JVI .01699-10.
26. McNatt MW, Zang T, Bieniasz PD. 2013. Vpu binds directly to tetherin and displaces it from nascent virions. PLoS Pathog. 9:e1003299. http://dx .doi.org/10.1371/journal.ppat.1003299.
27. Dubé 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. http: //dx.doi.org/10.1111/j.1600-0854.2011.01277.x.
28. 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. http://dx.doi.org/10.1128/mBio.00036-11.
29. Kueck T, Neil SJ. 2012. A cytoplasmic tail determinant in HIV-1 Vpu mediates targeting of tetherin for endosomal degradation and counteracts interferon-induced restriction. PLoS Pathog. 8:e1002609. http://dx.doi .org/10.1371/journal.ppat.1002609.
30. 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. http://dx.doi.org/10.1016/j.str.2011.12.013.
31. Janvier K, Pelchen-Matthews A, Renaud JB, Caillet M, Marsh M, Berlioz-Torrent C. 2011. The ESCRT-0 component HRS is required for HIV-1 Vpu-mediated BST-2/tetherin down-regulation. PLoS Pathog. 7:e1001265. http://dx.doi.org/10.1371/journal.ppat.1001265.
32. 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-dependent mechanism. J. Virol. 83:7931-7947. http://dx.doi.org/10.1128/JVI.00242-09.
33. Mitchell RS, Katsura C, Skasko MA, Fitzpatrick K, Lau D, Ruiz A, Stephens EB, Margottin-Goguet F, Benarous R, Guatelli JC. 2009. Vpu antagonizes BST-2-mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking. PLoS Pathog. 5:e1000450. http://dx.doi .org/10.1371/journal.ppat.1000450.
34. Gustin JK, Douglas JL, Bai Y, Moses AV. 2012. Ubiquitination of BST-2 protein by HIV-1 Vpu protein does not require lysine, serine, or threonine residues within the BST-2 cytoplasmic domain. J. Biol. Chem. 287:14837-14850. http://dx.doi.org/10.1074/jbc.M112.349928.
35. Tokarev AA, Munguia J, Guatelli JC. 2011. Serine-threonine ubiquitination mediates downregulation of BST-2/tetherin and relief of restricted virion release by HIV-1 Vpu. J. Virol. 85:51-63. http://dx.doi.org/10.1128 /JVI.01795-10.
36. Zhang F, Landford WN, Ng M, McNatt MW, Bieniasz PD, Hatziioannou T. 2011. SIV Nef proteins recruit the AP-2 complex to antagonize tetherin and facilitate virion release. PLoS Pathog. 7:e1002039. http://dx .doi.org/10.1371/journal.ppat.1002039.
37. Serra-Moreno R, Zimmermann K, Stern LJ, Evans DT. 2013. Tetherin/ BST-2 antagonism by Nef depends on a direct physical interaction between Nef and tetherin, and on clathrin-mediated endocytosis. PLoS Pathog. 9:e1003487. http://dx.doi.org/10.1371/journal.ppat.1003487.
38. Lau D, Kwan W, Guatelli J. 2011. Role of the endocytic pathway in the counteraction of BST-2 by human lentiviral pathogens. J. Virol. 85:9834-9846. http://dx.doi.org/10.1128/JVI.02633-10.
39. Pickering S, Hue S, Kim EY, Reddy S, Wolinsky SM, Neil SJ. 2014. Preservation of tetherin and CD4 counter-activities in circulating Vpu alleles despite extensive sequence variation within HIV-1 infected individuals. PLoS Pathog. 10:e1003895. http://dx.doi.org/10.1371/journal.ppat .1003895.
40. Sharp PM, Hahn BH. 2011. Origins of HIV and the AIDS pandemic. Cold Spring Harb. Perspect. Med. 1:a006841. http://dx.doi.org/10 .1101/cshperspect.a006841.
41. Neil SJ, Eastman SW, Jouvenet N, Bieniasz PD. 2006. HIV-1 Vpu promotes release and prevents endocytosis of nascent retrovirus particles from the plasma membrane. PLoS Pathog. 2:e39. http://dx.doi.org/10 .1371/journal.ppat.0020039.
42. Salazar-Gonzalez JF, Salazar MG, Keele BF, Learn GH, Giorgi EE, Li H, Decker JM, Wang S, Baalwa J, Kraus MH, Parrish NF, Shaw KS, Guffey MB, Bar KJ, Davis KL, Ochsenbauer-Jambor C, Kappes JC, Saag MS, Cohen MS, Mulenga J, Derdeyn CA, Allen S, Hunter E, Markowitz M, Hraber P, Perelson AS, Bhattacharya T, Haynes BF, Korber BT, Hahn BH, Shaw GM. 2009. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J. Exp. Med. 206:1273-1289. http://dx.doi.org/10.1084/jem.20090378.
43. Sauter D, Unterweger D, Vogl M, Usmani SM, Heigele A, Kluge SF, Hermkes E, Moll M, Barker E, Peeters M, Learn GH, Bibollet-Ruche F, Fritz JV, Fackler OT, Hahn BH, Kirchhoff F. 2012. Human tetherin exerts strong selection pressure on the HIV-1 group N Vpu protein. PLoS Pathog. 8:e1003093. http://dx.doi.org/10.1371/journal.ppat.1003093.
44. Miyagi E, Andrew AJ, Kao S, Strebel K. 2009. Vpu enhances HIV-1 virus release in the absence of Bst-2 cell surface down-modulation and intracellular depletion. Proc. Natl. Acad. Sci. U. S. A. 106:2868-2873. http://dx .doi.org/10.1073/pnas.0813223106.
45. Erikson E, Adam T, Schmidt S, Lehmann-Koch J, Over B, Goffinet C, Harter C, Bekeredjian-Ding I, Sertel S, Lasitschka F, Keppler OT. 2011. In vivo expression profile of the antiviral restriction factor and tumor-targeting antigen CD317/BST-2/HM1.24/tetherin in humans. Proc. Natl. Acad. Sci. U. S. A. 108:13688 -13693. http://dx.doi.org/10 .1073/pnas.1101684108.
46. 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. http: //dx.doi.org/10.1128/JVI.06971-11.
47. Lim ES, Malik HS, Emerman M. 2010. Ancient adaptive evolution of tetherin shaped the functions of Vpu and Nef in human immunodeficiency virus and primate lentiviruses. J. Virol. 84:7124-7134. http://dx .doi.org/10.1128/JVI.00468-10.
48. Means RE, Lang SM, Jung JU. 2007. The Kaposi's sarcoma-associated herpesvirus K5 E3 ubiquitin ligase modulates targets by multiple molecular mechanisms. J. Virol. 81:6573-6583. http://dx.doi.org/10.1128/JVI .02751-06.
49. Noble B, Abada P, Nunez-Iglesias J, Cannon PM. 2006. Recruitment of the adaptor protein 2 complex by the human immunodeficiency virus type 2 envelope protein is necessary for high levels of virus release. J. Virol. 80:2924-2932. http://dx.doi.org/10.1128/JVI.80.6.2924-2932.2006.
50. Celestino M, Calistri A, Del Vecchio C, Salata C, Chiuppesi F, Pistello M, Borsetti A, Palu G, Parolin C. 2012. Feline tetherin is characterized by a short N-terminal region and is counteracted by the feline immunodeficiency virus envelope glycoprotein. J. Virol. 86:6688-6700. http://dx.doi .org/10.1128/JVI.07037-11.
51. Dietrich I, Hosie MJ, Willett BJ. 2011. The role of BST2/tetherin in feline retrovirus infection. Vet. Immunol. Immunopathol. 143:255-264. http: //dx.doi.org/10.1016/j.vetimm.2011.06.020.
52. Yin X, Hu Z, Gu Q, Wu X, Zheng YH, Wei P, Wang X. 2014. Equine tetherin blocks retrovirus release and its activity is antagonized by equine infectious anemia virus envelope protein. J. Virol. 88:1259-1270. http: //dx.doi.org/10.1128/JVI.03148-13.
53. Barrett BS, Smith DS, Li SX, Guo K, Hasenkrug KJ, Santiago ML. 2012. A single nucleotide polymorphism in tetherin promotes retrovirus restriction in vivo. PLoS Pathog. 8:e1002596. http://dx.doi.org/10.1371/journal .ppat.1002596.
54. + T cells from antibody-mediated cell lysis through down-modulation of CD4 and BST2. Retrovirology 11:15. http: //dx.doi.org/10.1186/1742-4690-11-15.
55. Cao W, Bover L, Cho M, Wen X, Hanabuchi S, Bao M, Rosen DB, Wang YH, Shaw JL, Du Q, Li C, Arai N, Yao Z, Lanier LL, Liu YJ. 2009. Regulation of TLR7/9 responses in plasmacytoid dendritic cells by BST2 and ILT7 receptor interaction. J. Exp. Med. 206:1603-1614. http://dx.doi .org/10.1084/jem.20090547.
56. Tavano B, Galão RP, Graham DR, Neil SJ, Aquino VN, Fuchs D, Boasso A. 2013. Ig-like transcript 7, but not bone marrow stromal cell antigen 2 (also known as HM1.24, tetherin, or CD317), modulates plasmacytoid dendritic cell function in primary human blood leukocytes. J. Immunol. 190:2622-2630. http://dx.doi.org/10.4049/jimmunol.1202391.
57. Casartelli N, Sourisseau M, Feldmann J, Guivel-Benhassine F, Mallet A, Marcelin AG, Guatelli J, Schwartz O. 2010. Tetherin restricts productive HIV-1 cell-to-cell transmission. PLoS Pathog. 6:e1000955. http://dx.doi .org/10.1371/journal.ppat.1000955.
58. 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. http://dx.doi.org/10.1128/JVI.01447-10.
59. Kuhl BD, Sloan RD, Donahue DA, Bar-Magen T, Liang C, Wainberg MA. 2010. Tetherin restricts direct cell-to-cell infection of HIV-1. Retrovirology 7:115. http://dx.doi.org/10.1186/1742-4690-7-115.
60. Sauter D, Vogl M, Kirchhoff F. 2011. Ancient origin of a deletion in human BST2/tetherin that confers protection against viral zoonoses. Hum. Mutat. 32:1243-1245. http://dx.doi.org/10.1002/humu.21571.
61. Vigan R, Neil SJ. 2011. Separable determinants of subcellular localization and interaction account for the inability of group O HIV-1 Vpu to counteract tetherin. J. Virol. 85:9737-9748. http://dx.doi.org/10.1128/JVI .00479-11.
62. Yang SJ, Lopez LA, Exline CM, Haworth KG, Cannon PM. 2011. Lack of adaptation to human tetherin in HIV-1 group O and P. Retrovirology 8:78. http://dx.doi.org/10.1186/1742-4690-8-78.