The sheep tetherin paralog oBST2B blocks envelope glycoprotein incorporation into nascent retroviral virions

Journal of Virology

Volumn 89, Issue 1, 2015, Pages 535-544

  Murphy, Lita ^a   Varela, Mariana ^a   Desloire, Sophie ^b   Ftaich, Najate ^b   Murgia, Claudio ^a   Golder, Matthew ^a   Neil, Stuart ^c   Spencer, Thomas E ^d   Wootton, Sarah K ^e   Lavillette, Dimitri ^f   Terzian, Christophe ^b   Palmarini, Massimo ^a   Arnaud, Frédérick ^b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b University Lyon i   (France)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d WASHINGTON STATE UNIVERSITY   (United States)

^e UNIVERSITY OF GUELPH   (Canada)

^f UNIVERSITÉ LYON 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MARROW STROMAL CELL ANTIGEN 2; CELL ANTIGEN; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; MEMBRANE PROTEIN; VIRUS ENVELOPE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; GOLGI COMPLEX; JAAGSIEKTE SHEEP RETROVIRUS; NONHUMAN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RETROVIRUS INFECTION; SHEEP; VIRION; VIRUS ENVELOPE; VIRUS PARTICLE; VIRUS TRANSMISSION; ANIMAL; ANTAGONISTS AND INHIBITORS; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; VIRUS ASSEMBLY;

JAAGSIEKTE SHEEP RETROVIRUS; OVIS ARIES; VESICULAR STOMATITIS VIRUS;

ANIMALS; GOLGI APPARATUS; JAAGSIEKTE SHEEP RETROVIRUS; MEMBRANE GLYCOPROTEINS; PROTEIN TRANSPORT; SHEEP; VIRAL ENVELOPE PROTEINS; VIRION; VIRUS ASSEMBLY;

EID: 84919431401     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02751-14     Document Type: Article

References (46)

1. 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.
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. 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.
4. Weinelt J, Neil SJ. 2014. Differential sensitivities of tetherin isoforms to counteraction by primate lentiviruses. J Virol 88:5845-5858. http://dx.doi.org/10.1128/JVI.03818-13.
5. 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.
6. 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.
7. 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.
8. 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.
9. 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. http://dx.doi.org/10.1034/j.1600-0854.2003.00129.x.
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. 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.
12. 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. http://dx.doi.org/10.3390/v3050520.
13. Arias JF, Iwabu Y, Tokunaga K. 2012. Sites of action of HIV-1 Vpu in BST-2/tetherin downregulation. Curr HIV Res 10:283-291. http://dx.doi.org/10.2174/157016212800792423.
14. 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 USA 106:20889-20894. http://dx.doi.org/10.1073/pnas.0907075106.
15. 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.
16. Murgia C, Caporale M, Ceesay O, Di Francesco G, Ferri N, Varasano V, de Las Heras M, Palmarini M. 2011. Lung adenocarcinoma originates from retrovirus infection of proliferating type 2 pneumocytes during pulmonary post-natal development or tissue repair. PLoS Pathog 7:e1002014. http://dx.doi.org/10.1371/journal.ppat.1002014.
17. Palmarini M, Cousens C, Dalziel RG, Bai J, Stedman K, DeMartini JC, Sharp JM. 1996. The exogenous form of Jaagsiekte retrovirus is specifically associated with a contagious lung cancer of sheep. J Virol 70:1618-1623.
18. Palmarini M, Fan H. 2001. Retrovirus-induced ovine pulmonary adenocarcinoma, an animal model for lung cancer. J Natl Cancer Inst 93:1603-1614. http://dx.doi.org/10.1093/jnci/93.21.1603.
19. Palmarini M, Sharp JM, de Las Heras M, Fan H. 1999. Jaagsiekte sheep retrovirus is necessary and sufficient to induce a contagious lung cancer in sheep. J Virol 73:6964-6972.
20. Arnaud F, Caporale M, Varela M, Biek R, Chessa B, Alberti A, Golder M, Mura M, Zhang YP, Yu L, Pereira F, Demartini JC, Leymaster K, Spencer TE, Palmarini M. 2007. A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses. PLoS Pathog 3:e170. http://dx.doi.org/10.1371/journal.ppat.0030170.
21. Chessa B, Pereira F, Arnaud F, Amorim A, Goyache F, Mainland I, Kao RR, Pemberton JM, Beraldi D, Stear MJ, Alberti A, Pittau M, Iannuzzi L, Banabazi MH, Kazwala RR, Zhang YP, Arranz JJ, Ali BA, Wang Z, Uzun M, Dione MM, Olsaker I, Holm LE, Saarma U, Ahmad S, Marzanov N, Eythorsdottir E, Holland MJ, Ajmone-Marsan P, Bruford MW, Kantanen J, Spencer TE, Palmarini M. 2009. Revealing the history of sheep domestication using retrovirus integrations. Science 324:532-536. http://dx.doi.org/10.1126/science.1170587.
22. Black SG, Arnaud F, Burghardt RC, Satterfield MC, Fleming JA, Long CR, Hanna C, Murphy L, Biek R, Palmarini M, Spencer TE. 2010. Viral particles of endogenous betaretroviruses are released in the sheep uterus and infect the conceptus trophectoderm in a transspecies embryo transfer model. J Virol 84:9078-9085. http://dx.doi.org/10.1128/JVI.00950-10.
23. Dunlap KA, Palmarini M, Varela M, Burghardt RC, Hayashi K, Farmer JL, Spencer TE. 2006. Endogenous retroviruses regulate periimplantation placental growth and differentiation. Proc Natl Acad Sci USA 103:14390-14395. http://dx.doi.org/10.1073/pnas.0603836103.
24. Palmarini M, Hallwirth C, York D, Murgia C, de Oliveira T, Spencer T, Fan H. 2000. Molecular cloning and functional analysis of three type D endogenous retroviruses of sheep reveal a different cell tropism from that of the highly related exogenous jaagsiekte sheep retrovirus. J Virol 74: 8065-8076. http://dx.doi.org/10.1128/JVI.74.17.8065-8076.2000.
25. Mura M, Murcia P, Caporale M, Spencer TE, Nagashima K, Rein A, Palmarini M. 2004. Late viral interference induced by transdominant Gag of an endogenous retrovirus. Proc Natl Acad Sci USA 101:11117-11122. http://dx.doi.org/10.1073/pnas.0402877101.
26. Arnaud F, Black SG, Murphy L, Griffiths DJ, Neil SJ, Spencer TE, Palmarini M. 2010. Interplay between ovine bone marrow stromal cell antigen 2/tetherin and endogenous retroviruses. J Virol 84:4415-4425. http://dx.doi.org/10.1128/JVI.00029-10.
27. Takeda E, Nakagawa S, Nakaya Y, Tanaka A, Miyazawa T, Yasuda J. 2012. Identification and functional analysis of three isoforms of bovine BST-2. PLoS One 7:e41483. http://dx.doi.org/10.1371/journal.pone.0041483.
28. Palmarini M, Sharp JM, Lee C, Fan H. 1999. In vitro infection of ovine cell lines by Jaagsiekte sheep retrovirus. J Virol 73:10070-10078.
29. Maeda N, Palmarini M, Murgia C, Fan H. 2001. Direct transformation of rodent fibroblasts by jaagsiekte sheep retrovirus DNA. Proc Natl Acad Sci USA 98:4449-4454. http://dx.doi.org/10.1073/pnas.071547598.
30. Zavala G, Pretto C, Chow YH, Jones L, Alberti A, Grego E, De Las Heras M, Palmarini M. 2003. Relevance of Akt phosphorylation in cell transformation induced by Jaagsiekte sheep retrovirus. Virology 312:95-105. http://dx.doi.org/10.1016/S0042-6822(03)00205-8.
31. Varela M, Chow YH, Sturkie C, Murcia P, Palmarini M. 2006. Association of RON tyrosine kinase with the Jaagsiekte sheep retrovirus envelope glycoprotein. Virology 350:347-357. http://dx.doi.org/10.1016/j.virol.2006.01.040.
32. Murcia PR, Arnaud F, Palmarini M. 2007. The transdominant endogenous retrovirus enJS56A1 associates with and blocks intracellular trafficking of Jaagsiekte sheep retrovirus Gag. J Virol 81:1762-1772. http://dx.doi.org/10.1128/JVI.01859-06.
33. Wootton SK, Metzger MJ, Hudkins KL, Alpers CE, York D, DeMartini JC, Miller AD. 2006. Lung cancer induced in mice by the envelope protein of jaagsiekte sheep retrovirus (JSRV) closely resembles lung cancer in sheep infected with JSRV. Retrovirology 3:94. http://dx.doi.org/10.1186/1742-4690-3-94.
34. Arnaud F, Murcia PR, Palmarini M. 2007. Mechanisms of late restriction induced by an endogenous retrovirus. J Virol 81:11441-11451. http://dx.doi.org/10.1128/JVI.01214-07.
35. Douam F, Dao Thi VL, Maurin G, Fresquet J, Mompelat D, Zeisel MB, Baumert TF, Cosset FL, Lavillette D. 2014. Critical interaction between E1 and E2 glycoproteins determines binding and fusion properties of hepatitis C virus during cell entry. Hepatology 59:776-788. http://dx.doi.org/10.1002/hep.26733.
36. Fujiwara T, Oda K, Yokota S, Takatsuki A, Ikehara Y. 1988. Brefeldin A causes disassembly of the Golgi complex and accumulation of secretory proteins in the endoplasmic reticulum. J Biol Chem 263:18545-18552.
37. Yap AS, Crampton MS, Hardin J. 2007. Making and breaking contacts: the cellular biology of cadherin regulation. Curr Opin Cell Biol 19:508-514. http://dx.doi.org/10.1016/j.ceb.2007.09.008.
38. Helenius A, Aebi M. 2004. Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73:1019-1049. http://dx.doi.org/10.1146/annurev.biochem.73.011303.073752.
39. Sfakianos JN, Hunter E. 2003. M-PMV capsid transport is mediated by Env/Gag interactions at the pericentriolar recycling endosome. Traffic 4:671-680. http://dx.doi.org/10.1034/j.1600-0854.2003.00126.x.
40. Sfakianos JN, LaCasse RA, Hunter E. 2003. The M-PMV cytoplasmic targeting-retention signal directs nascent Gag polypeptides to a pericentriolar region of the cell. Traffic 4:660-670. http://dx.doi.org/10.1034/j.1600-0854.2003.00125.x.
41. 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 USA 106:2886-2891. http://dx.doi.org/10.1073/pnas.0811014106.
42. 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.
43. 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.
44. Palmarini M, Fan H. 2003. Molecular biology of jaagsiekte sheep retrovirus. Curr Top Microbiol Immunol 275:81-115. http://dx.doi.org/10.1007/978-3-642-55638-8_4.
45. Caporale M, Cousens C, Centorame P, Pinoni C, De Las Heras M, Palmarini M. 2006. Expression of the jaagsiekte sheep retrovirus envelope glycoprotein is sufficient to induce lung tumors in sheep. J Virol 80:8030-8037. http://dx.doi.org/10.1128/JVI.00474-06.
46. Wootton SK, Halbert CL, Miller AD. 2005. Sheep retrovirus structural protein induces lung tumours. Nature 434:904-907. http://dx.doi.org/10.1038/nature03492.