• This record comes from PubMed

Independent loss events of a functional tetherin gene in galliform birds

. 2023 Oct 31 ; 97 (10) : e0080323. [epub] 20230915

Language English Country United States Media print-electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

Grant support
20-22063S Grantová Agentura České Republiky (GAČR)
SA 2676/1-2 Deutsche Forschungsgemeinschaft (DFG)
Canon Foundation in Europe (CFE)
COVID-19 research grant Ministerium für Wissenschaft, Forschung und Kunst Baden-Württemberg (MWK)

Birds represent important hosts for numerous viruses, including zoonotic viruses and pathogens with the potential to cause major economic losses to the poultry industry. Viral replication and transmission can be inhibited or blocked by the action of antiviral restriction factors (RFs) encoded by the host. One well-characterized RF is tetherin, a protein that directly blocks the release of newly formed viral particles from infected cells. Here, we describe the evolutionary loss of a functional tetherin gene in two galliform birds, turkey (Meleagris gallopavo) and Mikado pheasant (Syrmaticus mikado). Moreover, we demonstrate that the structurally related protein TMCC(aT) exerts antiviral activity in several birds, albeit by a mechanism different from that of tetherin. The evolutionary scenario described here represents the first documented loss-of-tetherin cases in vertebrates.

See more in PubMed

Olsen B, Munster VJ, Wallensten A, Waldenström J, Osterhaus A, Fouchier RAM. 2006. Global patterns of influenza a virus in wild birds. Science 312:384–388. doi:10.1126/science.1122438 PubMed DOI

Hughes LA, Savage C, Naylor C, Bennett M, Chantrey J, Jones R. 2009. Genetically diverse coronaviruses in wild bird populations of northern England. Emerg Infect Dis 15:1091–1094. doi:10.3201/eid1507.090067 PubMed DOI PMC

Chamings A, Nelson TM, Vibin J, Wille M, Klaassen M, Alexandersen S. 2018. Detection and characterisation of coronaviruses in migratory and non-migratory Australian wild birds. Sci Rep 8:5980. doi:10.1038/s41598-018-24407-x PubMed DOI PMC

Reed KD, Meece JK, Henkel JS, Shukla SK. 2003. Birds, migration and emerging zoonoses: west Nile virus, Lyme disease, influenza A and enteropathogens. Clin Med Res 1:5–12. doi:10.3121/cmr.1.1.5 PubMed DOI PMC

Georgopoulou I, Tsiouris V. 2008. The potential role of migratory birds in the transmission of zoonoses. Vet Ital 44:671–677. PubMed

Wille M, Holmes EC. 2020. Wild birds as reservoirs for diverse and abundant gamma- and deltacoronaviruses. FEMS Microbiol Rev 44:631–644. doi:10.1093/femsre/fuaa026 PubMed DOI PMC

Payne LN, Nair V. 2012. The long view: 40 years of avian leukosis research. Avian Pathol 41:11–19. doi:10.1080/03079457.2011.646237 PubMed DOI

Nabi G, Wang Y, Lü L, Jiang C, Ahmad S, Wu Y, Li D. 2021. Bats and birds as viral reservoirs: a physiological and ecological perspective. Sci Total Environ 754:142372. doi:10.1016/j.scitotenv.2020.142372 PubMed DOI PMC

Li L, Feng W, Cheng Z, Yang J, Bi J, Wang X, Wang G. 2019. TRIM62-mediated restriction of avian leukosis virus subgroup J replication is dependent on the SPRY domain. Poult Sci 98:6019–6025. doi:10.3382/ps/pez408 PubMed DOI

Zhou J-R, Liu J-H, Li H-M, Zhao Y, Cheng Z, Hou Y-M, Guo H-J. 2020. Regulatory effects of chicken TRIM25 on the replication of ALV-A and the MDA5-mediated type I interferon response. Vet Res 51:145. doi:10.1186/s13567-020-00870-1 PubMed DOI PMC

Zhu M, Ma X, Cui X, Zhou J, Li C, Huang L, Shang Y, Cheng Z. 2017. Inhibition of avian tumor virus replication by CCCH-type zinc finger antiviral protein. Oncotarget 8:58865–58871. doi:10.18632/oncotarget.19378 PubMed DOI PMC

Greger JG, Katz RA, Ishov AM, Maul GG, Skalka AM. 2005. The cellular protein daxx interacts with avian sarcoma virus integrase and viral DNA to repress viral transcription. J Virol 79:4610–4618. doi:10.1128/JVI.79.8.4610-4618.2005 PubMed DOI PMC

Goossens KE, Karpala AJ, Rohringer A, Ward A, Bean AGD. 2015. Characterisation of chicken viperin. Mol Immunol 63:373–380. doi:10.1016/j.molimm.2014.09.011 PubMed DOI

Schusser B, Reuter A, von der Malsburg A, Penski N, Weigend S, Kaspers B, Staeheli P, Härtle S. 2011. Mx is dispensable for interferon-mediated resistance of chicken cells against influenza A virus. J Virol 85:8307–8315. doi:10.1128/JVI.00535-11 PubMed DOI PMC

Ko J-H, Jin H-K, Asano A, Takada A, Ninomiya A, Kida H, Hokiyama H, Ohara M, Tsuzuki M, Nishibori M, Mizutani M, Watanabe T. 2002. Polymorphisms and the differential antiviral activity of the chicken Mx gene. Genome Res 12:595–601. doi:10.1101/gr.210702 PubMed DOI PMC

Shah M, Bharadwaj MSK, Gupta A, Kumar R, Kumar S. 2019. Chicken viperin inhibits newcastle disease virus infection in vitro: a possible interaction with the viral matrix protein. Cytokine 120:28–40. doi:10.1016/j.cyto.2019.04.007 PubMed DOI

Santhakumar D, Rohaim M, Hussein HA, Hawes P, Ferreira HL, Behboudi S, Iqbal M, Nair V, Arns CW, Munir M. 2018. Chicken interferon-induced protein with tetratricopeptide repeats 5 antagonizes replication of RNA viruses. Sci Rep 8:6794. doi:10.1038/s41598-018-24905-y PubMed DOI PMC

Smith SE, Gibson MS, Wash RS, Ferrara F, Wright E, Temperton N, Kellam P, Fife M. 2013. Chicken interferon-inducible transmembrane protein 3 restricts influenza viruses and lyssaviruses in vitro. J Virol 87:12957–12966. doi:10.1128/JVI.01443-13 PubMed DOI PMC

Chen S, Wang L, Chen J, Zhang L, Wang S, Goraya MU, Chi X, Na Y, Shao W, Yang Z, Zeng X, Chen S, Chen J-L. 2017. Avian interferon-inducible transmembrane protein family effectively restricts avian tembusu virus infection. Front Microbiol 8:672. doi:10.3389/fmicb.2017.00672 PubMed DOI PMC

Neil SJD, Zang T, Bieniasz PD. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425–430. doi:10.1038/nature06553 PubMed DOI

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. doi:10.1016/j.chom.2008.03.001 PubMed DOI PMC

Mansouri M, Viswanathan K, Douglas JL, Hines J, Gustin J, Moses AV, Früh K. 2009. Molecular mechanism of BST2/tetherin downregulation by K5/MIR2 of kaposi's sarcoma-associated herpesvirus. J Virol 83:9672–9681. doi:10.1128/JVI.00597-09 PubMed DOI PMC

Taylor JK, Coleman CM, Postel S, Sisk JM, Bernbaum JG, Venkataraman T, Sundberg EJ, Frieman MB. 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. doi:10.1128/JVI.02274-15 PubMed DOI PMC

Jia B, Serra-Moreno R, Neidermyer W, Rahmberg A, Mackey J, Fofana IB, Johnson WE, Westmoreland S, Evans DT, Emerman M. 2009. Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog 5:e1000429. doi:10.1371/journal.ppat.1000429 PubMed DOI PMC

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. doi:10.1016/j.chom.2009.05.008 PubMed DOI PMC

Le Tortorec A, Neil SJD. 2009. Antagonism to and intracellular sequestration of human tetherin by the human immunodeficiency virus type 2 envelope glycoprotein. J Virol 83:11966–11978. doi:10.1128/JVI.01515-09 PubMed DOI PMC

Sauter D, Schindler M, Specht A, Landford WN, Münch J, Kim K-A, 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. doi:10.1016/j.chom.2009.10.004 PubMed DOI PMC

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. doi:10.1073/pnas.0907075106 PubMed DOI PMC

Heusinger E, Kluge SF, Kirchhoff F, Sauter D. 2015. Early vertebrate evolution of the host restriction factor tetherin. J Virol 89:12154–12165. doi:10.1128/JVI.02149-15 PubMed DOI PMC

Blanco-Melo D, Venkatesh S, Bieniasz PD. 2016. Origins and evolution of tetherin, an orphan antiviral gene. Cell Host Microbe 20:189–201. doi:10.1016/j.chom.2016.06.007 PubMed DOI PMC

Krchlíková V, Fábryová H, Hron T, Young JM, Koslová A, Hejnar J, Strebel K, Elleder D. 2020. Antiviral activity and adaptive evolution of avian tetherins. J Virol 94:e00416-20. doi:10.1128/JVI.00416-20 PubMed DOI PMC

Kumar S, Stecher G, Suleski M, Hedges SB. 2017. Timetree: a resource for timelines, timetrees, and divergence times. Mol Biol Evol 34:1812–1819. doi:10.1093/molbev/msx116 PubMed DOI

Ivashkiv LB, Donlin LT. 2014. Regulation of type I interferon responses. Nat Rev Immunol 14:36–49. doi:10.1038/nri3581 PubMed DOI PMC

Casartelli N, Sourisseau M, Feldmann J, Guivel-Benhassine F, Mallet A, Marcelin A-G, Guatelli J, Schwartz O. 2010. Tetherin restricts productive HIV-1 cell-to-cell transmission. PLoS Pathog 6:e1000955. doi:10.1371/journal.ppat.1000955 PubMed DOI PMC

Murphy L, Varela M, Desloire S, Ftaich N, Murgia C, Golder M, Neil S, Spencer TE, Wootton SK, Lavillette D, Terzian C, Palmarini M, Arnaud F. 2015. The sheep tetherin paralog oBST2B blocks envelope glycoprotein incorporation into nascent retroviral virions. J Virol 89:535–544. doi:10.1128/JVI.02751-14 PubMed DOI PMC

Jolly C, Booth NJ, Neil SJD. 2010. Cell-cell spread of human immunodeficiency virus type 1 overcomes tetherin/BST-2-mediated restriction in T cells. J Virol 84:12185–12199. doi:10.1128/JVI.01447-10 PubMed DOI PMC

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. doi:10.1186/1742-4690-7-115 PubMed DOI PMC

Verhelst J, Hulpiau P, Saelens X. 2013. Mx proteins: antiviral gatekeepers that restrain the uninvited. Microbiol Mol Biol Rev 77:551–566. doi:10.1128/MMBR.00024-13 PubMed DOI PMC

Braun BA, Marcovitz A, Camp JG, Jia R, Bejerano G. 2015. Mx1 and Mx2 key antiviral proteins are surprisingly lost in toothed whales. Proc Natl Acad Sci U S A 112:8036–8040. doi:10.1073/pnas.1501844112 PubMed DOI PMC

Ahn M, Cui J, Irving AT, Wang L-F. 2016. Unique loss of the PYHIN gene family in bats amongst mammals: implications for inflammasome sensing. Sci Rep 6:21722. doi:10.1038/srep21722 PubMed DOI PMC

Lazear HM, Schoggins JW, Diamond MS. 2019. Shared and distinct functions of type I and type III interferons. Immunity 50:907–923. doi:10.1016/j.immuni.2019.03.025 PubMed DOI PMC

Guzzo C, Jung M, Graveline A, Banfield BW, Gee K. 2012. IL-27 increases BST-2 expression in human monocytes and T cells independently of type I IFN. Sci Rep 2:974. doi:10.1038/srep00974 PubMed DOI PMC

Oudshoorn D, van Boheemen S, Sánchez-Aparicio MT, Rajsbaum R, García-Sastre A, Versteeg GA. 2012. HERC6 is the main E3 ligase for global ISG15 conjugation in mouse cells. PLoS One 7:e29870. doi:10.1371/journal.pone.0029870 PubMed DOI PMC

Hayward JA, Tachedjian M, Johnson A, Irving AT, Gordon TB, Cui J, Nicolas A, Smith I, Boyd V, Marsh GA, Baker ML, Wang L-F, Tachedjian G, Lowen AC. 2022. Unique evolution of antiviral tetherin in bats. J Virol 96:e0115222. doi:10.1128/jvi.01152-22 PubMed DOI PMC

Alqutami F, Senok A, Hachim M. 2021. COVID-19 transcriptomic atlas: a comprehensive analysis of COVID-19 related transcriptomics datasets. Front Genet 12:755222. doi:10.3389/fgene.2021.755222 PubMed DOI PMC

Peng Y, Luo X, Chen Y, Peng L, Deng C, Fei Y, Zhang W, Zhao Y. 2020. LncRNA and mRNA expression profile of peripheral blood mononuclear cells in primary Sjögren’s syndrome patients. Sci Rep 10:19629. doi:10.1038/s41598-020-76701-2 PubMed DOI PMC

Buffalo CZ, Stürzel CM, Heusinger E, Kmiec D, Kirchhoff F, Hurley JH, Ren X. 2019. Structural basis for tetherin antagonism as a barrier to zoonotic lentiviral transmission. Cell Host Microbe 26:359–368. doi:10.1016/j.chom.2019.08.002 PubMed DOI PMC

Thomas JM, Allison AB, Holmes EC, Phillips JE, Bunting EM, Yabsley MJ, Brown JD. 2015. Molecular surveillance for lymphoproliferative disease virus in wild turkeys (Meleagris gallopavo) from the eastern United States. PLoS One 10:e0122644. doi:10.1371/journal.pone.0122644 PubMed DOI PMC

MacDonald AM, Barta JR, McKay M, Lair S, Le Net R, Baldwin F, Pople N, Nemeth NM. 2019. Lymphoproliferative disease virus in wild turkeys (Meleagris gallopavo) from Manitoba and Quebec, Canada. Avian Dis 63:506–510. doi:10.1637/aviandiseases-D-19-00102 PubMed DOI

MacDonald AM, Jardine CM, Bowman J, Susta L, Nemeth NM. 2019. Detection of lymphoproliferative disease virus in Canada in a survey for viruses in Ontario wild turkeys (Meleagris gallopavo). J Wildl Dis 55:113–122. doi:10.7589/2018-01-013 PubMed DOI

Hughes SH. 2004. The RCAS vector system. Folia Biol 50:107–119. PubMed

Braun E, Hotter D, Koepke L, Zech F, Groß R, Sparrer KMJ, Müller JA, Pfaller CK, Heusinger E, Wombacher R, Sutter K, Dittmer U, Winkler M, Simmons G, Jakobsen MR, Conzelmann K-K, Pöhlmann S, Münch J, Fackler OT, Kirchhoff F, Sauter D. 2019. Guanylate-binding proteins 2 and 5 exert broad antiviral activity by inhibiting furin-mediated processing of viral envelope proteins. Cell Rep 27:2092–2104. doi:10.1016/j.celrep.2019.04.063 PubMed DOI

Wheeler DL, Church DM, Edgar R, Federhen S, Helmberg W, Madden TL, Pontius JU, Schuler GD, Schriml LM, Sequeira E, Suzek TO, Tatusova TA, Wagner L. 2004. Database resources of the national center for biotechnology information: update. Nucleic Acids Res 32:D35–40. doi:10.1093/nar/gkh073 PubMed DOI PMC

Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580. doi:10.1006/jmbi.2000.4315 PubMed DOI

Lupas A, Van Dyke M, Stock J. 1991. Predicting coiled coils from protein sequences. Science 252:1162–1164. doi:10.1126/science.252.5009.1162 PubMed DOI

Eisenhaber B, Bork P, Eisenhaber F. 1999. Prediction of potential GPI-modification sites in proprotein sequences. J Mol Biol 292:741–758. doi:10.1006/jmbi.1999.3069 PubMed DOI

Pierleoni A, Martelli PL, Casadio R. 2008. Predgpi: a GPI-anchor predictor. BMC Bioinformatics 9:392. doi:10.1186/1471-2105-9-392 PubMed DOI PMC

Kucerová D, Plachy J, Reinisová M, Senigl F, Trejbalová K, Geryk J, Hejnar J. 2013. Nonconserved tryptophan 38 of the cell surface receptor for subgroup J avian leukosis virus discriminates sensitive from resistant avian species. J Virol 87:8399–8407. doi:10.1128/JVI.03180-12 PubMed DOI PMC

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...