Retroviral Restriction Factors and Their Viral Targets: Restriction Strategies and Evolutionary Adaptations

1973, A new evolutionary law, Evol. Theory, 1, 1

Daugherty, 2012, Rules of engagement: Molecular insights from host-virus arms races, Annu. Rev. Genet., 46, 677, 10.1146/annurev-genet-110711-155522

Feng, 1996, HIV-1 entry cofactor: Functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor, Science, 272, 872, 10.1126/science.272.5263.872

Alkhatib, 1996, CC CKR5: A RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1, Science, 272, 1955, 10.1126/science.272.5270.1955

Dalgleish, 1984, The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus, Nature, 312, 763, 10.1038/312763a0

Gaud, 2018, Regulatory mechanisms in T cell receptor signalling, Nat. Rev. Immunol., 18, 485, 10.1038/s41577-018-0020-8

Huang, 2007, Structures of the CCR5 N terminus and of a tyrosine-sulfated antibody with HIV-1 gp120 and CD4, Science, 317, 1930, 10.1126/science.1145373

Willey, 1994, Sequences present in the cytoplasmic domain of CD4 are necessary and sufficient to confer sensitivity to the human immunodeficiency virus type 1 Vpu protein, J. Virol., 68, 1207, 10.1128/jvi.68.2.1207-1212.1994

Grzesiek, 1996, The CD4 determinant for downregulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR, Biochemistry, 35, 10256, 10.1021/bi9611164

Ramirez, P.W., Sharma, S., Singh, R., Stoneham, C.A., Vollbrecht, T., and Guatelli, J. (2019). Plasma Membrane-Associated Restriction Factors and Their Counteraction by HIV-1 Accessory Proteins. Cells, 8.

Russell, 2019, CD4 receptor diversity in chimpanzees protects against SIV infection, Proc. Natl. Acad. Sci. USA, 116, 3229, 10.1073/pnas.1821197116

Hvilsom, 2008, Genetic subspecies diversity of the chimpanzee CD4 virus-receptor gene, Genomics, 92, 322, 10.1016/j.ygeno.2008.07.003

Zhang, 2008, Rapid evolution by positive Darwinian selection in T-cell antigen CD4 in primates, J. Mol. Evol., 66, 446, 10.1007/s00239-008-9097-1

Wiel, 2017, Genome-scale detection of positive selection in nine primates predicts human-virus evolutionary conflicts, Nucleic Acids Res., 45, 10634, 10.1093/nar/gkx704

Samson, 1996, Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene, Nature, 382, 722, 10.1038/382722a0

Kozak, 2010, The mouse “xenotropic” gammaretroviruses and their XPR1 receptor, Retrovirology, 7, 101, 10.1186/1742-4690-7-101

Kozak, 2011, Naturally Occurring Polymorphisms of the Mouse Gammaretrovirus Receptors CAT-1 and XPR1 Alter Virus Tropism and Pathogenicity, Adv. Virol., 2011, 975801, 10.1155/2011/975801

Martin, 2013, The avian XPR1 gammaretrovirus receptor is under positive selection and is disabled in bird species in contact with virus-infected wild mice, J. Virol., 87, 10094, 10.1128/JVI.01327-13

Yan, 2010, Evolution of functional and sequence variants of the mammalian XPR1 receptor for mouse xenotropic gammaretroviruses and the human-derived XMRV, J. Virol., 84, 11970, 10.1128/JVI.01549-10

Albritton, 1989, A putative murine ecotropic retrovirus receptor gene encodes a multiple membrane-spanning protein and confers susceptibility to virus infection, Cell, 57, 659, 10.1016/0092-8674(89)90134-7

Tailor, 1999, Cloning and characterization of a cell surface receptor for xenotropic and polytropic murine leukemia viruses, Proc. Natl. Acad. Sci. USA, 96, 927, 10.1073/pnas.96.3.927

Kim, 1991, Transport of cationic amino acids by the mouse ecotropic retrovirus receptor, Nature, 352, 725, 10.1038/352725a0

Wang, 1991, Cell-surface receptor for ecotropic murine retroviruses is a basic amino-acid transporter, Nature, 352, 729, 10.1038/352729a0

Giovannini, 2013, Inorganic phosphate export by the retrovirus receptor XPR1 in metazoans, Cell Rep., 3, 1866, 10.1016/j.celrep.2013.05.035

Kozak, 1987, Diverse wild mouse origins of xenotropic, mink cell focus-forming, and two types of ecotropic proviral genes, J. Virol., 61, 3082, 10.1128/jvi.61.10.3082-3088.1987

Eiden, 1993, Characterization of a naturally occurring ecotropic receptor that does not facilitate entry of all ecotropic murine retroviruses, J. Virol., 67, 4056, 10.1128/jvi.67.7.4056-4061.1993

Lu, 2019, Mutational analysis and glycosylation sensitivity of restrictive XPR1 gammaretrovirus receptors in six mammalian species, Virology, 535, 154, 10.1016/j.virol.2019.07.004

Kavanaugh, 1994, Cell-surface receptors for gibbon ape leukemia virus and amphotropic murine retrovirus are inducible sodium-dependent phosphate symporters, Proc. Natl. Acad. Sci. USA, 91, 7071, 10.1073/pnas.91.15.7071

Miller, 1994, Cloning of the cellular receptor for amphotropic murine retroviruses reveals homology to that for gibbon ape leukemia virus, Proc. Natl. Acad. Sci. USA, 91, 78, 10.1073/pnas.91.1.78

Hartley, 1976, Naturally occurring murine leukemia viruses in wild mice: Characterization of a new “amphotropic” class, J. Virol., 19, 19, 10.1128/jvi.19.1.19-25.1976

Rasheed, 1976, Amphotropic host range of naturally occuring wild mouse leukemia viruses, J. Virol., 19, 13, 10.1128/jvi.19.1.13-18.1976

Hartley, 1987, Amphotropic proviral envelope sequences are absent from the Mus germ line, J. Virol., 61, 2225, 10.1128/jvi.61.7.2225-2231.1987

Johnson, 2019, Origins and evolutionary consequences of ancient endogenous retroviruses, Nat. Rev. Microbiol., 17, 355, 10.1038/s41579-019-0189-2

Taylor, 2001, Fv-4: Identification of the defect in Env and the mechanism of resistance to ecotropic murine leukemia virus, J. Virol., 75, 11244, 10.1128/JVI.75.22.11244-11248.2001

Inuzuka, 2005, Serinc, an activity-regulated protein family, incorporates serine into membrane lipid synthesis, J. Biol. Chem., 280, 35776, 10.1074/jbc.M505712200

Rosa, 2015, HIV-1 Nef promotes infection by excluding SERINC5 from virion incorporation, Nature, 526, 212, 10.1038/nature15399

Usami, 2015, SERINC3 and SERINC5 restrict HIV-1 infectivity and are counteracted by Nef, Nature, 526, 218, 10.1038/nature15400

Sharma, S., Lewinski, M.K., and Guatelli, J. (2018). An N-Glycosylated Form of SERINC5 Is Specifically Incorporated into HIV-1 Virions. J. Virol., 92.

Shi, J., Xiong, R., Zhou, T., Su, P., Zhang, X., Qiu, X., Li, H., Li, S., Yu, C., and Wang, B. (2018). HIV-1 Nef Antagonizes SERINC5 Restriction by Downregulation of SERINC5 via the Endosome/Lysosome System. J. Virol., 92.

Ahmad, 2019, The retroviral accessory proteins S2, Nef, and glycoMA use similar mechanisms for antagonizing the host restriction factor SERINC5, J. Biol. Chem., 294, 7013, 10.1074/jbc.RA119.007662

Kmiec, D., Akbil, B., Ananth, S., Hotter, D., Sparrer, K.M.J., Stürzel, C.M., Trautz, B., Ayouba, A., Peeters, M., and Yao, Z. (2018). SIVcol Nef counteracts SERINC5 by promoting its proteasomal degradation but does not efficiently enhance HIV-1 replication in human CD4+ T cells and lymphoid tissue. PLoS Pathog., 14.

Staudt, 2020, Nef Homodimers Downregulate SERINC5 by AP-2-Mediated Endocytosis to Promote HIV-1 Infectivity, J. Biol. Chem., 295, 15540, 10.1074/jbc.RA120.014668

Dai, 2018, A Long Cytoplasmic Loop Governs the Sensitivity of the Anti-viral Host Protein SERINC5 to HIV-1 Nef, Cell Rep., 22, 869, 10.1016/j.celrep.2017.12.082

Stoneham, C.A., Ramirez, P.W., Singh, R., Suarez, M., Debray, A., Lim, C., Jia, X., Xiong, Y., and Guatelli, J. (2020). A Conserved Acidic-Cluster Motif in SERINC5 Confers Partial Resistance to Antagonism by HIV-1 Nef. J. Virol., 94.

Chande, 2016, S2 from equine infectious anemia virus is an infectivity factor which counteracts the retroviral inhibitors SERINC5 and SERINC3, Proc. Natl. Acad. Sci. USA, 113, 13197, 10.1073/pnas.1612044113

Ahi, 2016, Functional Interplay Between Murine Leukemia Virus Glycogag, Serinc5, and Surface Glycoprotein Governs Virus Entry, with Opposite Effects on Gammaretroviral and Ebolavirus Glycoproteins, mBio, 7, e01985-16, 10.1128/mBio.01985-16

Li, S., Ahmad, I., Shi, J., Wang, B., Yu, C., Zhang, L., and Zheng, Y.H. (2019). Murine Leukemia Virus Glycosylated Gag Reduces Murine SERINC5 Protein Expression at Steady-State Levels via the Endosome/Lysosome Pathway to Counteract SERINC5 Antiretroviral Activity. J. Virol., 93.

Beitari, S., Pan, Q., Finzi, A., and Liang, C. (2020). Differential pressures of SERINC5 and IFITM3 on HIV-1 envelope glycoprotein over the course of HIV-1 infection. J. Virol.

Beitari, S., Ding, S., Pan, Q., Finzi, A., and Liang, C. (2017). Effect of HIV-1 Env on SERINC5 Antagonism. J. Virol., 91.

Schulte, 2018, Localization to detergent-resistant membranes and HIV-1 core entry inhibition correlate with HIV-1 restriction by SERINC5, Virology, 515, 52, 10.1016/j.virol.2017.12.005

Sood, 2017, SERINC5 protein inhibits HIV-1 fusion pore formation by promoting functional inactivation of envelope glycoproteins, J. Biol. Chem., 292, 6014, 10.1074/jbc.M117.777714

Chen, 2020, Super-Resolution Fluorescence Imaging Reveals That Serine Incorporator Protein 5 Inhibits Human Immunodeficiency Virus Fusion by Disrupting Envelope Glycoprotein Clusters, ACS Nano, 14, 10929, 10.1021/acsnano.0c02699

Heigele, 2016, The Potency of Nef-Mediated SERINC5 Antagonism Correlates with the Prevalence of Primate Lentiviruses in the Wild, Cell Host Microbe, 20, 381, 10.1016/j.chom.2016.08.004

Abrantes, 2019, The antiviral activity of rodent and lagomorph SERINC3 and SERINC5 is counteracted by known viral antagonists, J. Gen. Virol., 100, 278, 10.1099/jgv.0.001201

Timilsina, U., Umthong, S., Lynch, B., Stablewski, A., and Stavrou, S. (2020). SERINC5 Potently Restricts Retrovirus Infection In Vivo. mBio, 11.

Murrell, 2016, The Evolutionary Histories of Antiretroviral Proteins SERINC3 and SERINC5 Do Not Support an Evolutionary Arms Race in Primates, J. Virol., 90, 8085, 10.1128/JVI.00972-16

Lilly, 1967, Susceptibility to two strains of Friend leukemia virus in mice, Science, 155, 461, 10.1126/science.155.3761.461

Hartley, 1970, Host-range restrictions of murine leukemia viruses in mouse embryo cell cultures, J. Virol., 5, 221, 10.1128/jvi.5.2.221-225.1970

Rowe, 1972, Studies of genetic transmission of murine leukemia virus by AKR mice. I. Crosses with Fv-1 n strains of mice, J. Exp. Med., 136, 1272, 10.1084/jem.136.5.1272

Jung, 2000, A single amino acid change in the murine leukemia virus capsid gene responsible for the Fv1(nr) phenotype, J. Virol., 74, 5385, 10.1128/JVI.74.11.5385-5387.2000

Kozak, 1996, Single amino acid changes in the murine leukemia virus capsid protein gene define the target of Fv1 resistance, Virology, 225, 300, 10.1006/viro.1996.0604

Best, 1996, Positional cloning of the mouse retrovirus restriction gene Fv1, Nature, 382, 826, 10.1038/382826a0

Benit, 1997, Cloning of a new murine endogenous retrovirus, MuERV-L, with strong similarity to the human HERV-L element and with a gag coding sequence closely related to the Fv1 restriction gene, J. Virol., 71, 5652, 10.1128/jvi.71.7.5652-5657.1997

Boso, G., Buckler-White, A., and Kozak, C.A. (2018). Ancient Evolutionary Origin and Positive Selection of the Retroviral Restriction Factor Fv1 in Muroid Rodents. J. Virol., 92.

Sawyer, 2005, Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain, Proc. Natl. Acad. Sci. USA, 102, 2832, 10.1073/pnas.0409853102

Sawyer, S.L., Emerman, M., and Malik, H.S. (2004). Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol., 2.

Laguette, 2012, Evolutionary and functional analyses of the interaction between the myeloid restriction factor SAMHD1 and the lentiviral Vpx protein, Cell Host Microbe, 11, 205, 10.1016/j.chom.2012.01.007

Mitchell, P.S., Young, J.M., Emerman, M., and Malik, H.S. (2015). Evolutionary Analyses Suggest a Function of MxB Immunity Proteins Beyond Lentivirus Restriction. PLoS Pathog., 11.

Sebastian, 2005, TRIM5alpha selectively binds a restriction-sensitive retroviral capsid, Retrovirology, 2, 40, 10.1186/1742-4690-2-40

Vandegraaff, 2006, Requirements for capsid-binding and an effector function in TRIMCyp-mediated restriction of HIV-1, Virology, 351, 404, 10.1016/j.virol.2006.03.023

Kouno, 2015, Structure of the Vif-binding domain of the antiviral enzyme APOBEC3G, Nat. Struct. Mol. Biol., 22, 485, 10.1038/nsmb.3033

Betancor, 2019, The GTPase Domain of MX2 Interacts with the HIV-1 Capsid, Enabling Its Short Isoform to Moderate Antiviral Restriction, Cell Rep., 29, 1923, 10.1016/j.celrep.2019.10.009

Goujon, 2015, A triple-arginine motif in the amino-terminal domain and oligomerization are required for HIV-1 inhibition by human MX2, J. Virol., 89, 4676, 10.1128/JVI.00169-15

Ahn, 2012, HIV/simian immunodeficiency virus (SIV) accessory virulence factor Vpx loads the host cell restriction factor SAMHD1 onto the E3 ubiquitin ligase complex CRL4DCAF1, J. Biol. Chem., 287, 12550, 10.1074/jbc.M112.340711

Jolicoeur, 1976, Effect of Fv-1 gene product on proviral DNA formation and integration in cells infected with murine leukemia viruses, Proc. Natl. Acad. Sci. USA, 73, 2236, 10.1073/pnas.73.7.2236

Li, 2016, Expression levels of Fv1: Effects on retroviral restriction specificities, Retrovirology, 13, 42, 10.1186/s12977-016-0276-7

Stevens, 2004, Retroviral capsid determinants of Fv1 NB and NR tropism, J. Virol., 78, 9592, 10.1128/JVI.78.18.9592-9598.2004

Bishop, 2001, Identification of the regions of Fv1 necessary for murine leukemia virus restriction, J. Virol., 75, 5182, 10.1128/JVI.75.11.5182-5188.2001

Hilditch, 2011, Ordered assembly of murine leukemia virus capsid protein on lipid nanotubes directs specific binding by the restriction factor, Fv1, Proc. Natl. Acad. Sci. USA, 108, 5771, 10.1073/pnas.1100118108

Yan, 2009, Origin, antiviral function and evidence for positive selection of the gammaretrovirus restriction gene Fv1 in the genus Mus, Proc. Natl. Acad. Sci. USA, 106, 3259, 10.1073/pnas.0900181106

Yap, M.W., Colbeck, E., Ellis, S.A., and Stoye, J.P. (2014). Evolution of the retroviral restriction gene Fv1: Inhibition of non-MLV retroviruses. PLoS Pathog., 10.

Young, 2018, Evolutionary journey of the retroviral restriction gene Fv1, Proc. Natl. Acad. Sci. USA, 115, 10130, 10.1073/pnas.1808516115

Steppan, S.J., and Schenk, J.J. (2017). Muroid rodent phylogenetics: 900-species tree reveals increasing diversification rates. PLoS ONE, 12.

Towers, 2000, A conserved mechanism of retrovirus restriction in mammals, Proc. Natl. Acad. Sci. USA, 97, 12295, 10.1073/pnas.200286297

Hatziioannou, 2003, Restriction of multiple divergent retroviruses by Lv1 and Ref1, EMBO J., 22, 385, 10.1093/emboj/cdg042

Stremlau, 2004, The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys, Nature, 427, 848, 10.1038/nature02343

Hatakeyama, 2017, TRIM Family Proteins: Roles in Autophagy, Immunity, and Carcinogenesis, Trends Biochem. Sci., 42, 297, 10.1016/j.tibs.2017.01.002

Sparrer, 2018, TRIM Proteins and Their Roles in Antiviral Host Defenses, Annu. Rev. Virol., 5, 385, 10.1146/annurev-virology-092917-043323

Sardiello, M., Cairo, S., Fontanella, B., Ballabio, A., and Meroni, G. (2008). Genomic analysis of the TRIM family reveals two groups of genes with distinct evolutionary properties. BMC Evol. Biol., 8.

Hatziioannou, 2004, Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha, Proc. Natl. Acad. Sci. USA, 101, 10774, 10.1073/pnas.0402361101

Yap, 2005, A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction, Curr. Biol., 15, 73, 10.1016/j.cub.2004.12.042

Black, 2010, TRIM5alpha disrupts the structure of assembled HIV-1 capsid complexes in vitro, J. Virol., 84, 6564, 10.1128/JVI.00210-10

Chandrasekaran, 2011, Hexagonal assembly of a restricting TRIM5alpha protein, Proc. Natl. Acad. Sci. USA, 108, 534, 10.1073/pnas.1013426108

Li, 2016, Primate TRIM5 proteins form hexagonal nets on HIV-1 capsids, eLife, 5, e16269, 10.7554/eLife.16269

Wagner, 2016, Mechanism of B-box 2 domain-mediated higher-order assembly of the retroviral restriction factor TRIM5alpha, eLife, 5, e16309, 10.7554/eLife.16309

Roganowicz, M.D., Komurlu, S., Mukherjee, S., Plewka, J., Alam, S.L., Skorupka, K.A., Wan, Y., Dawidowski, D., Cafiso, D.S., and Ganser-Pornillos, B.K. (2017). TRIM5alpha SPRY/coiled-coil interactions optimize avid retroviral capsid recognition. PLoS Pathog., 13.

Morger, 2018, The Three-Fold Axis of the HIV-1 Capsid Lattice Is the Species-Specific Binding Interface for TRIM5α, J. Virol., 92, e01541, 10.1128/JVI.01541-17

Stremlau, 2005, Species-specific variation in the B30.2(SPRY) domain of TRIM5alpha determines the potency of human immunodeficiency virus restriction, J. Virol., 79, 3139, 10.1128/JVI.79.5.3139-3145.2005

Kane, 2016, Identification of Interferon-Stimulated Genes with Antiretroviral Activity, Cell Host Microbe, 20, 392, 10.1016/j.chom.2016.08.005

OhAinle, 2018, A virus-packageable CRISPR screen identifies host factors mediating interferon inhibition of HIV, eLife, 7, e39823, 10.7554/eLife.39823

Apolonia, 2019, Immunoproteasome activation enables human TRIM5alpha restriction of HIV-1, Nat. Microbiol., 4, 933, 10.1038/s41564-019-0402-0

Chiramel, 2019, TRIM5alpha Restricts Flavivirus Replication by Targeting the Viral Protease for Proteasomal Degradation, Cell Rep., 27, 3269, 10.1016/j.celrep.2019.05.040

Li, 2006, Rapid turnover and polyubiquitylation of the retroviral restriction factor TRIM5, Virology, 349, 300, 10.1016/j.virol.2005.12.040

Campbell, 2016, TRIM5α-Mediated Ubiquitin Chain Conjugation Is Required for Inhibition of HIV-1 Reverse Transcription and Capsid Destabilization, J. Virol., 90, 1849, 10.1128/JVI.01948-15

Kutluay, S.B., Perez-Caballero, D., and Bieniasz, P.D. (2013). Fates of retroviral core components during unrestricted and TRIM5-restricted infection. PLoS Pathog., 9.

Fletcher, 2015, TRIM5alpha requires Ube2W to anchor Lys63-linked ubiquitin chains and restrict reverse transcription, EMBO J., 34, 2078, 10.15252/embj.201490361

Roa, 2012, RING domain mutations uncouple TRIM5alpha restriction of HIV-1 from inhibition of reverse transcription and acceleration of uncoating, J. Virol., 86, 1717, 10.1128/JVI.05811-11

Sayah, 2004, Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1, Nature, 430, 569, 10.1038/nature02777

Si, 2006, Evolution of a cytoplasmic tripartite motif (TRIM) protein in cows that restricts retroviral infection, Proc. Natl. Acad. Sci. USA, 103, 7454, 10.1073/pnas.0600771103

Ylinen, 2006, Isolation of an active Lv1 gene from cattle indicates that tripartite motif protein-mediated innate immunity to retroviral infection is widespread among mammals, J. Virol., 80, 7332, 10.1128/JVI.00516-06

Sawyer, S.L., Emerman, M., and Malik, H.S. (2007). Discordant evolution of the adjacent antiretroviral genes TRIM22 and TRIM5 in mammals. PLoS Pathog., 3.

Wilson, 2008, Independent evolution of an antiviral TRIMCyp in rhesus macaques, Proc. Natl. Acad. Sci. USA, 105, 3557, 10.1073/pnas.0709003105

Tareen, 2009, An expanded clade of rodent Trim5 genes, Virology, 385, 473, 10.1016/j.virol.2008.12.018

Wu, 2013, Birth, decay, and reconstruction of an ancient TRIMCyp gene fusion in primate genomes, Proc. Natl. Acad. Sci. USA, 110, E583

Mu, 2014, Independent birth of a novel TRIMCyp in Tupaia belangeri with a divergent function from its paralog TRIM5, Mol. Biol. Evol., 31, 2985, 10.1093/molbev/msu238

Boso, 2019, Evolution of the rodent Trim5 cluster is marked by divergent paralogous expansions and independent acquisitions of TrimCyp fusions, Sci. Rep., 9, 11263, 10.1038/s41598-019-47720-5

Águeda-Pinto, A., Lemos de Matos, A., Pinheiro, A., Neves, F., de Sousa-Pereira, P., and Esteves, P.J. (2019). Not so unique to Primates: The independent adaptive evolution of TRIM5 in Lagomorpha lineage. PLoS ONE, 14.

Morrison, J.H., Miller, C., Bankers, L., Crameri, G., Wang, L.F., and Poeschla, E.M. (2020). A Potent Postentry Restriction to Primate Lentiviruses in a Yinpterochiropteran Bat. mBio, 11.

Pertel, 2011, TRIM5 is an innate immune sensor for the retrovirus capsid lattice, Nature, 472, 361, 10.1038/nature09976

Lascano, 2016, TRIM5 Retroviral Restriction Activity Correlates with the Ability to Induce Innate Immune Signaling, J. Virol., 90, 308, 10.1128/JVI.02496-15

Zhu, 2018, Activation of NF-kappaB induced by TRIMCyp showing a discrepancy between owl monkey and northern pig-tailed macaque, Mol. Immunol., 101, 627, 10.1016/j.molimm.2018.08.001

Fletcher, 2018, Trivalent RING Assembly on Retroviral Capsids Activates TRIM5 Ubiquitination and Innate Immune Signaling, Cell Host Microbe, 24, 761, 10.1016/j.chom.2018.10.007

Salter, 2016, The APOBEC Protein Family: United by Structure, Divergent in Function, Trends Biochem. Sci., 41, 578, 10.1016/j.tibs.2016.05.001

Sheehy, 2002, Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein, Nature, 418, 646, 10.1038/nature00939

Larue, 2010, Lentiviral Vif degrades the APOBEC3Z3/APOBEC3H protein of its mammalian host and is capable of cross-species activity, J. Virol., 84, 8193, 10.1128/JVI.00685-10

Yoshikawa, 2016, Small ruminant lentiviral Vif proteins commonly utilize cyclophilin A, an evolutionarily and structurally conserved protein, to degrade ovine and caprine APOBEC3 proteins, Microbiol. Immunol., 60, 427, 10.1111/1348-0421.12387

Su, 2018, Jembrana disease virus Vif antagonizes the inhibition of bovine APOBEC3 proteins through ubiquitin-mediate protein degradation, Virology, 519, 53, 10.1016/j.virol.2018.03.028

Zhao, 2019, CAEV Vif Hijacks ElonginB/C, CYPA and Cullin5 to Assemble the E3 Ubiquitin Ligase Complex Stepwise to Degrade oaA3Z2-Z3, Front. Microbiol., 10, 565, 10.3389/fmicb.2019.00565

Konno, 2018, New World feline APOBEC3 potently controls inter-genus lentiviral transmission, Retrovirology, 15, 31, 10.1186/s12977-018-0414-5

Adolph, 2017, Cytidine deaminase efficiency of the lentiviral viral restriction factor APOBEC3C correlates with dimerization, Nucleic Acids Res., 45, 3378, 10.1093/nar/gkx066

Nakano, Y., Misawa, N., Juarez-Fernandez, G., Moriwaki, M., Nakaoka, S., Funo, T., Yamada, E., Soper, A., Yoshikawa, R., and Ebrahimi, D. (2017). HIV-1 competition experiments in humanized mice show that APOBEC3H imposes selective pressure and promotes virus adaptation. PLoS Pathog., 13.

Anderson, 2018, Natural APOBEC3C variants can elicit differential HIV-1 restriction activity, Retrovirology, 15, 78, 10.1186/s12977-018-0459-5

Mohammadzadeh, 2019, Polymorphisms of the cytidine deaminase APOBEC3F have different HIV-1 restriction efficiencies, Virology, 527, 21, 10.1016/j.virol.2018.11.004

Harris, 2003, DNA deamination mediates innate immunity to retroviral infection, Cell, 113, 803, 10.1016/S0092-8674(03)00423-9

Mangeat, 2003, Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts, Nature, 424, 99, 10.1038/nature01709

Iwatani, 2007, Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G, Nucleic Acids Res., 35, 7096, 10.1093/nar/gkm750

Wang, 2012, The cellular antiviral protein APOBEC3G interacts with HIV-1 reverse transcriptase and inhibits its function during viral replication, J. Virol., 86, 3777, 10.1128/JVI.06594-11

Morse, 2017, Dimerization regulates both deaminase-dependent and deaminase-independent HIV-1 restriction by APOBEC3G, Nat. Commun., 8, 597, 10.1038/s41467-017-00501-y

Takeda, 2008, Mouse APOBEC3 restricts friend leukemia virus infection and pathogenesis in vivo, J. Virol., 82, 10998, 10.1128/JVI.01311-08

Rulli, 2008, Interactions of murine APOBEC3 and human APOBEC3G with murine leukemia viruses, J. Virol., 82, 6566, 10.1128/JVI.01357-07

MacMillan, 2013, APOBEC3 inhibition of mouse mammary tumor virus infection: The role of cytidine deamination versus inhibition of reverse transcription, J. Virol., 87, 4808, 10.1128/JVI.00112-13

Stavrou, S., Zhao, W., Blouch, K., and Ross, S.R. (2018). Deaminase-Dead Mouse APOBEC3 Is an In Vivo Retroviral Restriction Factor. J. Virol., 92.

Stavrou, S., Crawford, D., Blouch, K., Browne, E.P., Kohli, R.M., and Ross, S.R. (2014). Different modes of retrovirus restriction by human APOBEC3A and APOBEC3G in vivo. PLoS Pathog., 10.

Hakata, Y., Li, J., Fujino, T., Tanaka, Y., Shimizu, R., and Miyazawa, M. (2019). Mouse APOBEC3 interferes with autocatalytic cleavage of murine leukemia virus Pr180gag-pol precursor and inhibits Pr65gag processing. PLoS Pathog., 15.

Li, J., Hakata, Y., Takeda, E., Liu, Q., Iwatani, Y., Kozak, C.A., and Miyazawa, M. (2012). Two genetic determinants acquired late in Mus evolution regulate the inclusion of exon 5, which alters mouse APOBEC3 translation efficiency. PLoS Pathog., 8.

Hultquist, 2011, Human and rhesus APOBEC3D, APOBEC3F, APOBEC3G, and APOBEC3H demonstrate a conserved capacity to restrict Vif-deficient HIV-1, J. Virol., 85, 11220, 10.1128/JVI.05238-11

Krisko, 2016, APOBEC3G and APOBEC3F Act in Concert To Extinguish HIV-1 Replication, J. Virol., 90, 4681, 10.1128/JVI.03275-15

Wittkopp, C.J., Adolph, M.B., Wu, L.I., Chelico, L., and Emerman, M. (2016). A Single Nucleotide Polymorphism in Human APOBEC3C Enhances Restriction of Lentiviruses. PLoS Pathog., 12.

Ayyappan Jaguva Vasudevan, A., Balakrishnan, K., Gertzen, C.W.G., Borveto, F., Zhang, Z., Sangwiman, A., Held, U., Kustermann, C., Banerjee, S., and Schumann, G.G. (2020). Loop 1 of APOBEC3C regulates its antiviral activity against HIV-1. J. Mol. Biol.

Zheng, 2004, Human APOBEC3F is another host factor that blocks human immunodeficiency virus type 1 replication, J. Virol., 78, 6073, 10.1128/JVI.78.11.6073-6076.2004

Wiegand, 2004, A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins, EMBO J., 23, 2451, 10.1038/sj.emboj.7600246

Harari, 2009, Polymorphisms and splice variants influence the antiretroviral activity of human APOBEC3H, J. Virol., 83, 295, 10.1128/JVI.01665-08

Mulder, 2010, Moderate influence of human APOBEC3F on HIV-1 replication in primary lymphocytes, J. Virol., 84, 9613, 10.1128/JVI.02630-09

Wang, 2011, Analysis of human APOBEC3H haplotypes and anti-human immunodeficiency virus type 1 activity, J. Virol., 85, 3142, 10.1128/JVI.02049-10

Duggal, 2013, Identification and antiviral activity of common polymorphisms in the APOBEC3 locus in human populations, Virology, 443, 329, 10.1016/j.virol.2013.05.016

Chesarino, N.M., and Emerman, M. (2020). Polymorphisms in Human APOBEC3H Differentially Regulate Ubiquitination and Antiviral Activity. Viruses, 12.

Covino, 2018, Understanding the regulation of APOBEC3 expression: Current evidence and much to learn, J. Leukoc. Biol., 103, 433, 10.1002/JLB.2MR0717-310R

Refsland, 2010, Quantitative profiling of the full APOBEC3 mRNA repertoire in lymphocytes and tissues: Implications for HIV-1 restriction, Nucleic Acids Res., 38, 4274, 10.1093/nar/gkq174

Koning, 2009, Defining APOBEC3 expression patterns in human tissues and hematopoietic cell subsets, J. Virol., 83, 9474, 10.1128/JVI.01089-09

Sanville, B., Dolan, M.A., Wollenberg, K., Yan, Y., Martin, C., Yeung, M.L., Strebel, K., Buckler-White, A., and Kozak, C.A. (2010). Adaptive evolution of Mus Apobec3 includes retroviral insertion and positive selection at two clusters of residues flanking the substrate groove. PLoS Pathog., 6.

Yu, 2003, Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex, Science, 302, 1056, 10.1126/science.1089591

Jager, 2011, Vif hijacks CBF-beta to degrade APOBEC3G and promote HIV-1 infection, Nature, 481, 371, 10.1038/nature10693

Zhang, 2011, T-cell differentiation factor CBF-beta regulates HIV-1 Vif-mediated evasion of host restriction, Nature, 481, 376, 10.1038/nature10718

Hu, 2019, Structural basis of antagonism of human APOBEC3F by HIV-1 Vif, Nat. Struct. Mol. Biol., 26, 1176, 10.1038/s41594-019-0343-6

Miyagi, E., Welbourn, S., Sukegawa, S., Fabryova, H., Kao, S., and Strebel, K. (2020). Inhibition of Vif-Mediated Degradation of APOBEC3G through Competitive Binding of Core-Binding Factor Beta. J. Virol., 94.

Kolokithas, 2010, The glycosylated Gag protein of a murine leukemia virus inhibits the antiretroviral function of APOBEC3, J. Virol., 84, 10933, 10.1128/JVI.01023-10

Stavrou, 2013, Murine leukemia virus glycosylated Gag blocks apolipoprotein B editing complex 3 and cytosolic sensor access to the reverse transcription complex, Proc. Natl. Acad. Sci. USA, 110, 9078, 10.1073/pnas.1217399110

Zhao, W., Akkawi, C., Mougel, M., and Ross, S.R. (2020). Murine Leukemia Virus P50 Protein Counteracts APOBEC3 by Blocking Its Packaging. J. Virol., 94.

Houzet, 2003, A new retroelement constituted by a natural alternatively spliced RNA of murine replication-competent retroviruses, EMBO J., 22, 4866, 10.1093/emboj/cdg450

LaRue, R.S., Jonsson, S.R., Silverstein, K.A., Lajoie, M., Bertrand, D., El-Mabrouk, N., Hotzel, I., Andresdottir, V., Smith, T.P., and Harris, R.S. (2008). The artiodactyl APOBEC3 innate immune repertoire shows evidence for a multi-functional domain organization that existed in the ancestor of placental mammals. BMC Mol. Biol., 9.

Hirano, 2015, Evolution of vertebrate adaptive immunity: Immune cells and tissues, and AID/APOBEC cytidine deaminases, Bioessays, 37, 877, 10.1002/bies.201400178

Munk, C., Willemsen, A., and Bravo, I.G. (2012). An ancient history of gene duplications, fusions and losses in the evolution of APOBEC3 mutators in mammals. BMC Evol. Biol., 12.

Yang, 2020, Retrocopying expands the functional repertoire of APOBEC3 antiviral proteins in primates, eLife, 9, e58436, 10.7554/eLife.58436

LaRue, 2009, Guidelines for naming nonprimate APOBEC3 genes and proteins, J. Virol., 83, 494, 10.1128/JVI.01976-08

Ito, 2020, Retroviruses drive the rapid evolution of mammalian APOBEC3 genes, Proc. Natl. Acad. Sci. USA, 117, 610, 10.1073/pnas.1914183116

Jern, 2007, Role of APOBEC3 in genetic diversity among endogenous murine leukemia viruses, PLoS Genet., 3, 2014, 10.1371/journal.pgen.0030183

Knisbacher, 2016, DNA Editing of LTR Retrotransposons Reveals the Impact of APOBECs on Vertebrate Genomes, Mol. Biol. Evol., 33, 554, 10.1093/molbev/msv239

Renner, 2018, Characterization of molecular attributes that influence LINE-1 restriction by all seven human APOBEC3 proteins, Virology, 520, 127, 10.1016/j.virol.2018.05.015

Treger, 2019, Human APOBEC3G Prevents Emergence of Infectious Endogenous Retrovirus in Mice, J. Virol., 93, e00728, 10.1128/JVI.00728-19

Turelli, 2004, Inhibition of hepatitis B virus replication by APOBEC3G, Science, 303, 1829, 10.1126/science.1092066

Chen, 2017, Heat shock proteins stimulate APOBEC-3-mediated cytidine deamination in the hepatitis B virus, J. Biol. Chem., 292, 13459, 10.1074/jbc.M116.760637

Kanagaraj, 2019, Different antiviral activities of natural APOBEC3C, APOBEC3G, and APOBEC3H variants against hepatitis B virus, Biochem. Biophys. Res. Commun., 518, 26, 10.1016/j.bbrc.2019.08.003

Goldstone, 2011, HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase, Nature, 480, 379, 10.1038/nature10623

Laguette, 2011, SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx, Nature, 474, 654, 10.1038/nature10117

Baldauf, 2012, SAMHD1 restricts HIV-1 infection in resting CD4(+) T cells, Nat. Med., 18, 1682, 10.1038/nm.2964

Hrecka, 2011, Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein, Nature, 474, 658, 10.1038/nature10195

Schott, 2018, Dephosphorylation of the HIV-1 restriction factor SAMHD1 is mediated by PP2A-B55alpha holoenzymes during mitotic exit, Nat. Commun., 9, 2227, 10.1038/s41467-018-04671-1

Cribier, 2013, Phosphorylation of SAMHD1 by cyclin A2/CDK1 regulates its restriction activity toward HIV-1, Cell Rep., 3, 1036, 10.1016/j.celrep.2013.03.017

White, 2013, The retroviral restriction ability of SAMHD1, but not its deoxynucleotide triphosphohydrolase activity, is regulated by phosphorylation, Cell Host Microbe, 13, 441, 10.1016/j.chom.2013.03.005

Welbourn, 2013, Restriction of virus infection but not catalytic dNTPase activity is regulated by phosphorylation of SAMHD1, J. Virol., 87, 11516, 10.1128/JVI.01642-13

Arnold, L.H., Groom, H.C., Kunzelmann, S., Schwefel, D., Caswell, S.J., Ordonez, P., Mann, M.C., Rueschenbaum, S., Goldstone, D.C., and Pennell, S. (2015). Phospho-dependent Regulation of SAMHD1 Oligomerisation Couples Catalysis and Restriction. PLoS Pathog., 11.

Wang, 2016, Phosphorylation of mouse SAMHD1 regulates its restriction of human immunodeficiency virus type 1 infection, but not murine leukemia virus infection, Virology, 487, 273, 10.1016/j.virol.2015.10.024

Lim, 2012, The ability of primate lentiviruses to degrade the monocyte restriction factor SAMHD1 preceded the birth of the viral accessory protein Vpx, Cell Host Microbe, 11, 194, 10.1016/j.chom.2012.01.004

Fregoso, O.I., Ahn, J., Wang, C., Mehrens, J., Skowronski, J., and Emerman, M. (2013). Evolutionary toggling of Vpx/Vpr specificity results in divergent recognition of the restriction factor SAMHD1. PLoS Pathog., 9.

Guo, 2019, Determinants of lentiviral Vpx-CRL4 E3 ligase-mediated SAMHD1 degradation in the substrate adaptor protein DCAF1, Biochem. Biophys. Res. Commun., 513, 933, 10.1016/j.bbrc.2019.04.085

Hosmalin, 1995, Splenic interdigitating dendritic cells in humans: Characterization and HIV infection frequency in vivo, Adv. Exp. Med. Biol., 378, 439, 10.1007/978-1-4615-1971-3_98

Banchereau, 1998, Dendritic cells and the control of immunity, Nature, 392, 245, 10.1038/32588

Schmitz, 2013, Immunopathogenesis of simian immunodeficiency virus infection in nonhuman primates, Curr. Opin. HIV AIDS, 8, 273

Monit, 2019, Positive selection in dNTPase SAMHD1 throughout mammalian evolution, Proc. Natl. Acad. Sci. USA, 116, 18647, 10.1073/pnas.1908755116

Mereby, 2018, Interplay of ancestral non-primate lentiviruses with the virus-restricting SAMHD1 proteins of their hosts, J. Biol. Chem., 293, 16402, 10.1074/jbc.RA118.004567

Wang, 2020, The C-terminal domain of feline and bovine SAMHD1 proteins has a crucial role in lentiviral restriction, J. Biol. Chem., 295, 4252, 10.1074/jbc.RA120.012767

Gramberg, 2013, Restriction of diverse retroviruses by SAMHD1, Retrovirology, 10, 26, 10.1186/1742-4690-10-26

Sze, 2013, Host restriction factor SAMHD1 limits human T cell leukemia virus type 1 infection of monocytes via STING-mediated apoptosis, Cell Host Microbe, 14, 422, 10.1016/j.chom.2013.09.009

Hollenbaugh, J.A., Gee, P., Baker, J., Daly, M.B., Amie, S.M., Tate, J., Kasai, N., Kanemura, Y., Kim, D.H., and Ward, B.M. (2013). Host factor SAMHD1 restricts DNA viruses in non-dividing myeloid cells. PLoS Pathog., 9.

Jeong, 2016, Inhibition of hepatitis B virus replication by a dNTPase-dependent function of the host restriction factor SAMHD1, Virology, 495, 71, 10.1016/j.virol.2016.05.001

Sommer, 2016, Restrictive influence of SAMHD1 on Hepatitis B Virus life cycle, Sci. Rep., 6, 26616, 10.1038/srep26616

Businger, 2019, Human cytomegalovirus overcomes SAMHD1 restriction in macrophages via pUL97, Nat. Microbiol., 4, 2260, 10.1038/s41564-019-0557-8

Sliva, 2019, Interference with SAMHD1 Restores Late Gene Expression of Modified Vaccinia Virus Ankara in Human Dendritic Cells and Abrogates Type I Interferon Expression, J. Virol., 93, e01097, 10.1128/JVI.01097-19

Zhang, 2019, Conserved Herpesvirus Protein Kinases Target SAMHD1 to Facilitate Virus Replication, Cell Rep., 28, 449, 10.1016/j.celrep.2019.04.020

Hu, 2018, Cyclin E2-CDK2 mediates SAMHD1 phosphorylation to abrogate its restriction of HBV replication in hepatoma cells, FEBS Lett., 592, 1893, 10.1002/1873-3468.13105

Gao, 2011, Structure of myxovirus resistance protein a reveals intra- and intermolecular domain interactions required for the antiviral function, Immunity, 35, 514, 10.1016/j.immuni.2011.07.012

Alvarez, 2017, CryoEM structure of MxB reveals a novel oligomerization interface critical for HIV restriction, Sci. Adv., 3, e1701264, 10.1126/sciadv.1701264

Goujon, 2013, Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection, Nature, 502, 559, 10.1038/nature12542

Kane, 2013, MX2 is an interferon-induced inhibitor of HIV-1 infection, Nature, 502, 563, 10.1038/nature12653

Liu, 2013, The interferon-inducible MxB protein inhibits HIV-1 infection, Cell Host Microbe, 14, 398, 10.1016/j.chom.2013.08.015

Bulli, 2016, Complex Interplay between HIV-1 Capsid and MX2-Independent Alpha Interferon-Induced Antiviral Factors, J. Virol., 90, 7469, 10.1128/JVI.00458-16

Xu, 2020, Pro-515 of the dynamin-like GTPase MxB contributes to HIV-1 inhibition by regulating MxB oligomerization and binding to HIV-1 capsid, J. Biol. Chem., 295, 6447, 10.1074/jbc.RA119.012439

Fribourgh, 2014, Structural insight into HIV-1 restriction by MxB, Cell Host Microbe, 16, 627, 10.1016/j.chom.2014.09.021

Fricke, 2014, MxB binds to the HIV-1 core and prevents the uncoating process of HIV-1, Retrovirology, 11, 68, 10.1186/s12977-014-0068-x

Smaga, 2019, MxB Restricts HIV-1 by Targeting the Tri-hexamer Interface of the Viral Capsid, Structure, 27, 1234, 10.1016/j.str.2019.04.015

Melen, 1996, Human MxB protein, an interferon-alpha-inducible GTPase, contains a nuclear targeting signal and is localized in the heterochromatin region beneath the nuclear envelope, J. Biol. Chem., 271, 23478, 10.1074/jbc.271.38.23478

Goujon, 2014, Transfer of the amino-terminal nuclear envelope targeting domain of human MX2 converts MX1 into an HIV-1 resistance factor, J. Virol., 88, 9017, 10.1128/JVI.01269-14

Dicks, M.D.J., Betancor, G., Jimenez-Guardeno, J.M., Pessel-Vivares, L., Apolonia, L., Goujon, C., and Malim, M.H. (2018). Multiple components of the nuclear pore complex interact with the amino-terminus of MX2 to facilitate HIV-1 restriction. PLoS Pathog., 14.

Kane, 2018, Nuclear pore heterogeneity influences HIV-1 infection and the antiviral activity of MX2, eLife, 7, e35738, 10.7554/eLife.35738

Xie, 2020, MxB impedes the NUP358-mediated HIV-1 pre-integration complex nuclear import and viral replication cooperatively with CPSF6, Retrovirology, 17, 16, 10.1186/s12977-020-00524-2

Mitchell, 2012, Evolution-guided identification of antiviral specificity determinants in the broadly acting interferon-induced innate immunity factor MxA, Cell Host Microbe, 12, 598, 10.1016/j.chom.2012.09.005

Braun, 2015, Mx1 and Mx2 key antiviral proteins are surprisingly lost in toothed whales, Proc. Natl. Acad. Sci. USA, 112, 8036, 10.1073/pnas.1501844112

Meier, 2018, Equine MX2 is a restriction factor of equine infectious anemia virus (EIAV), Virology, 523, 52, 10.1016/j.virol.2018.07.024

Ji, 2018, Equine Myxovirus Resistance Protein 2 Restricts Lentiviral Replication by Blocking Nuclear Uptake of Capsid Protein, J. Virol., 92, e00499, 10.1128/JVI.00499-18

Crameri, 2018, MxB is an interferon-induced restriction factor of human herpesviruses, Nat. Commun., 9, 1980, 10.1038/s41467-018-04379-2

Schilling, M., Bulli, L., Weigang, S., Graf, L., Naumann, S., Patzina, C., Wagner, V., Bauersfeld, L., Goujon, C., and Hengel, H. (2018). Human MxB Protein Is a Pan-herpesvirus Restriction Factor. J. Virol., 92.

Yi, 2019, Human MxB Inhibits the Replication of Hepatitis C Virus, J. Virol., 93, e01285, 10.1128/JVI.01285-18

Bahr, 2018, MXB inhibits murine cytomegalovirus, Virology, 522, 158, 10.1016/j.virol.2018.07.017

Wang, 2020, Interferon-inducible MX2 is a host restriction factor of hepatitis B virus replication, J. Hepatol., 72, 865, 10.1016/j.jhep.2019.12.009

Gao, 2002, Inhibition of retroviral RNA production by ZAP, a CCCH-type zinc finger protein, Science, 297, 1703, 10.1126/science.1074276

Karlberg, 2015, Structural basis for lack of ADP-ribosyltransferase activity in poly(ADP-ribose) polymerase-13/zinc finger antiviral protein, J. Biol. Chem., 290, 7336, 10.1074/jbc.M114.630160

Guo, 2004, The zinc finger antiviral protein directly binds to specific viral mRNAs through the CCCH zinc finger motifs, J. Virol., 78, 12781, 10.1128/JVI.78.23.12781-12787.2004

Muller, 2007, Inhibition of filovirus replication by the zinc finger antiviral protein, J. Virol., 81, 2391, 10.1128/JVI.01601-06

Guo, 2007, The zinc-finger antiviral protein recruits the RNA processing exosome to degrade the target mRNA, Proc. Natl. Acad. Sci. USA, 104, 151, 10.1073/pnas.0607063104

Zhu, 2011, Zinc-finger antiviral protein inhibits HIV-1 infection by selectively targeting multiply spliced viral mRNAs for degradation, Proc. Natl. Acad. Sci. USA, 108, 15834, 10.1073/pnas.1101676108

Zhu, 2012, Translational repression precedes and is required for ZAP-mediated mRNA decay, EMBO J., 31, 4236, 10.1038/emboj.2012.271

Takata, 2017, CG dinucleotide suppression enables antiviral defence targeting non-self RNA, Nature, 550, 124, 10.1038/nature24039

Meagher, 2019, Structure of the zinc-finger antiviral protein in complex with RNA reveals a mechanism for selective targeting of CG-rich viral sequences, Proc. Natl. Acad. Sci. USA, 116, 24303, 10.1073/pnas.1913232116

Ficarelli, 2020, CpG Dinucleotides Inhibit HIV-1 Replication through Zinc Finger Antiviral Protein (ZAP)-Dependent and -Independent Mechanisms, J. Virol., 94, e01337, 10.1128/JVI.01337-19

Li, M.M., Lau, Z., Cheung, P., Aguilar, E.G., Schneider, W.M., Bozzacco, L., Molina, H., Buehler, E., Takaoka, A., and Rice, C.M. (2017). TRIM25 Enhances the Antiviral Action of Zinc-Finger Antiviral Protein (ZAP). PLoS Pathog., 13.

Zheng, X., Wang, X., Tu, F., Wang, Q., Fan, Z., and Gao, G. (2017). TRIM25 Is Required for the Antiviral Activity of Zinc Finger Antiviral Protein. J. Virol., 91.

Ficarelli, 2019, KHNYN is essential for the zinc finger antiviral protein (ZAP) to restrict HIV-1 containing clustered CpG dinucleotides, eLife, 8, e46767, 10.7554/eLife.46767

Kerns, J.A., Emerman, M., and Malik, H.S. (2008). Positive selection and increased antiviral activity associated with the PARP-containing isoform of human zinc-finger antiviral protein. PLoS Genet., 4.

Bick, 2003, Expression of the zinc-finger antiviral protein inhibits alphavirus replication, J. Virol., 77, 11555, 10.1128/JVI.77.21.11555-11562.2003

Mao, R., Nie, H., Cai, D., Zhang, J., Liu, H., Yan, R., Cuconati, A., Block, T.M., Guo, J.T., and Guo, H. (2013). Inhibition of hepatitis B virus replication by the host zinc finger antiviral protein. PLoS Pathog., 9.

Goodier, J.L., Pereira, G.C., Cheung, L.E., Rose, R.J., and Kazazian, H.H. (2015). The Broad-Spectrum Antiviral Protein ZAP Restricts Human Retrotransposition. PLoS Genet., 11.

Li, 2015, Zinc finger antiviral protein inhibits coxsackievirus B3 virus replication and protects against viral myocarditis, Antiviral Res., 123, 50, 10.1016/j.antiviral.2015.09.001

Zhu, 2017, Inhibition of avian tumor virus replication by CCCH-type zinc finger antiviral protein, Oncotarget, 8, 58865, 10.18632/oncotarget.19378

Miyazato, 2019, HTLV-1 contains a high CG dinucleotide content and is susceptible to the host antiviral protein ZAP, Retrovirology, 16, 38, 10.1186/s12977-019-0500-3

Chiu, H.P., Chiu, H., Yang, C.F., Lee, Y.L., Chiu, F.L., Kuo, H.C., Lin, R.J., and Lin, Y.L. (2018). Inhibition of Japanese encephalitis virus infection by the host zinc-finger antiviral protein. PLoS Pathog., 14.

Schwarz, 1998, Schlafen, a new family of growth regulatory genes that affect thymocyte development, Immunity, 9, 657, 10.1016/S1074-7613(00)80663-9

Li, 2012, Codon-usage-based inhibition of HIV protein synthesis by human schlafen 11, Nature, 491, 125, 10.1038/nature11433

Mavrommatis, 2013, The schlafen family of proteins and their regulation by interferons, J. Interferon Cytokine Res., 33, 206, 10.1089/jir.2012.0133

Liu, 2018, The Schlafen family: Complex roles in different cell types and virus replication, Cell Biol. Int., 42, 2, 10.1002/cbin.10778

Bustos, 2009, Evolution of the Schlafen genes, a gene family associated with embryonic lethality, meiotic drive, immune processes and orthopoxvirus virulence, Gene, 447, 1, 10.1016/j.gene.2009.07.006

Pranckeviciene, 2011, HIV-1 modulates the tRNA pool to improve translation efficiency, Mol. Biol. Evol., 28, 1827, 10.1093/molbev/msr005

Lin, 2016, Equine schlafen 11 restricts the production of equine infectious anemia virus via a codon usage-dependent mechanism, Virology, 495, 112, 10.1016/j.virol.2016.04.024

Stabell, A.C., Hawkins, J., Li, M., Gao, X., David, M., Press, W.H., and Sawyer, S.L. (2016). Non-human Primate Schlafen11 Inhibits Production of Both Host and Viral Proteins. PLoS Pathog., 12.

Valdez, 2019, Schlafen 11 Restricts Flavivirus Replication, J. Virol., 93, e00104, 10.1128/JVI.00104-19

Olszewski, 2006, In silico genomic analysis of the human and murine guanylate-binding protein (GBP) gene clusters, J. Interferon Cytokine Res., 26, 328, 10.1089/jir.2006.26.328

McLaren, 2015, Identification of potential HIV restriction factors by combining evolutionary genomic signatures with functional analyses, Retrovirology, 12, 41, 10.1186/s12977-015-0165-5

Krapp, 2016, Guanylate Binding Protein (GBP) 5 Is an Interferon-Inducible Inhibitor of HIV-1 Infectivity, Cell Host Microbe, 19, 504, 10.1016/j.chom.2016.02.019

Braun, 2019, Guanylate-Binding Proteins 2 and 5 Exert Broad Antiviral Activity by Inhibiting Furin-Mediated Processing of Viral Envelope Proteins, Cell Rep., 27, 2092, 10.1016/j.celrep.2019.04.063

Hotter, 2017, Guanylate binding protein 5: Impairing virion infectivity by targeting retroviral envelope glycoproteins, Small GTPases, 8, 31, 10.1080/21541248.2016.1189990

Li, 2020, GBP5 is an interferon-induced inhibitor of respiratory syncytial virus, J. Virol., 94, e01407, 10.1128/JVI.01407-20

Goto, 2006, A novel family of membrane-bound E3 ubiquitin ligases, J. Biochem., 140, 147, 10.1093/jb/mvj160

Tada, 2015, MARCH8 inhibits HIV-1 infection by reducing virion incorporation of envelope glycoproteins, Nat. Med., 21, 1502, 10.1038/nm.3956

Zhang, Y., Tada, T., Ozono, S., Kishigami, S., Fujita, H., and Tokunaga, K. (2020). MARCH8 inhibits viral infection by two different mechanisms. eLife, 9.

Yu, C., Li, S., Zhang, X., Khan, I., Ahmad, I., Zhou, Y., Li, S., Shi, J., Wang, Y., and Zheng, Y.H. (2020). MARCH8 Inhibits Ebola Virus Glycoprotein, Human Immunodeficiency Virus Type 1 Envelope Glycoprotein, and Avian Influenza Virus H5N1 Hemagglutinin Maturation. mBio, 11.

Zhang, 2018, MARCH2 is upregulated in HIV-1 infection and inhibits HIV-1 production through envelope protein translocation or degradation, Virology, 518, 293, 10.1016/j.virol.2018.02.003

Zhang, 2019, Membrane-associated RING-CH (MARCH) 1 and 2 are MARCH family members that inhibit HIV-1 infection, J. Biol. Chem., 294, 3397, 10.1074/jbc.AC118.005907

Zhao, 2018, IFITM Genes, Variants, and Their Roles in the Control and Pathogenesis of Viral Infections, Front. Microbiol., 9, 3228, 10.3389/fmicb.2018.03228

Brass, 2009, The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus, Cell, 139, 1243, 10.1016/j.cell.2009.12.017

Perreira, 2013, IFITMs restrict the replication of multiple pathogenic viruses, J. Mol. Biol., 425, 4937, 10.1016/j.jmb.2013.09.024

Compton, 2014, IFITM proteins incorporated into HIV-1 virions impair viral fusion and spread, Cell Host Microbe, 16, 736, 10.1016/j.chom.2014.11.001

Savidis, 2016, The IFITMs Inhibit Zika Virus Replication, Cell Rep., 15, 2323, 10.1016/j.celrep.2016.05.074

Weston, 2016, Alphavirus Restriction by IFITM Proteins, Traffic, 17, 997, 10.1111/tra.12416

Gorman, 2016, The Interferon-Stimulated Gene Ifitm3 Restricts West Nile Virus Infection and Pathogenesis, J. Virol., 90, 8212, 10.1128/JVI.00581-16

Poddar, 2016, The Interferon-Stimulated Gene IFITM3 Restricts Infection and Pathogenesis of Arthritogenic and Encephalitic Alphaviruses, J. Virol., 90, 8780, 10.1128/JVI.00655-16

McMichael, 2018, IFITM3 Restricts Human Metapneumovirus Infection, J. Infect. Dis., 218, 1582

Li, 2018, The Host Restriction Factor Interferon-Inducible Transmembrane Protein 3 Inhibits Vaccinia Virus Infection, Front. Immunol., 9, 228, 10.3389/fimmu.2018.00228

Li, C., Zheng, H., Wang, Y., Dong, W., Liu, Y., Zhang, L., and Zhang, Y. (2019). Antiviral Role of IFITM Proteins in Classical Swine Fever Virus Infection. Viruses, 11.

Londrigan, 2020, IFITM3 and type I interferons are important for the control of influenza A virus replication in murine macrophages, Virology, 540, 17, 10.1016/j.virol.2019.11.003

Lu, 2011, The IFITM proteins inhibit HIV-1 infection, J. Virol., 85, 2126, 10.1128/JVI.01531-10

Tartour, 2014, IFITM proteins are incorporated onto HIV-1 virion particles and negatively imprint their infectivity, Retrovirology, 11, 103, 10.1186/s12977-014-0103-y

Yu, 2015, IFITM Proteins Restrict HIV-1 Infection by Antagonizing the Envelope Glycoprotein, Cell Rep., 13, 145, 10.1016/j.celrep.2015.08.055

Appourchaux, R., Delpeuch, M., Zhong, L., Burlaud-Gaillard, J., Tartour, K., Savidis, G., Brass, A., Etienne, L., Roingeard, P., and Cimarelli, A. (2019). Functional Mapping of Regions Involved in the Negative Imprinting of Virion Particle Infectivity and in Target Cell Protection by Interferon-Induced Transmembrane Protein 3 against HIV-1. J. Virol., 93.

Ahi, 2020, IFITM3 Reduces Retroviral Envelope Abundance and Function and Is Counteracted by glycoGag, mBio, 11, e03088, 10.1128/mBio.03088-19

Spence, 2019, IFITM3 directly engages and shuttles incoming virus particles to lysosomes, Nat. Chem. Biol., 15, 259, 10.1038/s41589-018-0213-2

Buchrieser, 2019, IFITM proteins inhibit placental syncytiotrophoblast formation and promote fetal demise, Science, 365, 176, 10.1126/science.aaw7733

Zani, 2019, Interferon-induced transmembrane proteins inhibit cell fusion mediated by trophoblast syncytins, J. Biol. Chem., 294, 19844, 10.1074/jbc.AC119.010611

Wang, Y., Pan, Q., Ding, S., Wang, Z., Yu, J., Finzi, A., Liu, S.L., and Liang, C. (2017). The V3 Loop of HIV-1 Env Determines Viral Susceptibility to IFITM3 Impairment of Viral Infectivity. J. Virol., 91.

Foster, 2016, Resistance of Transmitted Founder HIV-1 to IFITM-Mediated Restriction, Cell Host Microbe, 20, 429, 10.1016/j.chom.2016.08.006

Zhang, Z., Liu, J., Li, M., Yang, H., and Zhang, C. (2012). Evolutionary dynamics of the interferon-induced transmembrane gene family in vertebrates. PLoS ONE, 7.

Everitt, 2012, IFITM3 restricts the morbidity and mortality associated with influenza, Nature, 484, 519, 10.1038/nature10921

2012, The mannose receptor, J. Leukoc. Biol., 92, 1177, 10.1189/jlb.0512231

Sukegawa, 2018, Mannose Receptor 1 Restricts HIV Particle Release from Infected Macrophages, Cell Rep., 22, 786, 10.1016/j.celrep.2017.12.085

Lubow, 2020, Mannose receptor is an HIV restriction factor counteracted by Vpr in macrophages, eLife, 9, e51035, 10.7554/eLife.51035

Olzmann, 2013, The mammalian endoplasmic reticulum-associated degradation system, Cold Spring Harb. Perspect Biol., 5, a013185, 10.1101/cshperspect.a013185

Zhou, 2014, The mitochondrial translocator protein, TSPO, inhibits HIV-1 envelope glycoprotein biosynthesis via the endoplasmic reticulum-associated protein degradation pathway, J. Virol., 88, 3474, 10.1128/JVI.03286-13

Zhou, 2015, ERManI (Endoplasmic Reticulum Class I alpha-Mannosidase) Is Required for HIV-1 Envelope Glycoprotein Degradation via Endoplasmic Reticulum-associated Protein Degradation Pathway, J. Biol. Chem., 290, 22184, 10.1074/jbc.M115.675207

Frabutt, D.A., Wang, B., Riaz, S., Schwartz, R.C., and Zheng, Y.H. (2018). Innate Sensing of Influenza A Virus Hemagglutinin Glycoproteins by the Host Endoplasmic Reticulum (ER) Stress Pathway Triggers a Potent Antiviral Response via ER-Associated Protein Degradation. J. Virol., 92.

Strebel, 1989, Molecular and biochemical analyses of human immunodeficiency virus type 1 vpu protein, J. Virol., 63, 3784, 10.1128/jvi.63.9.3784-3791.1989

Neil, 2008, Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu, Nature, 451, 425, 10.1038/nature06553

Goto, 1994, A novel membrane antigen selectively expressed on terminally differentiated human B cells, Blood, 84, 1922, 10.1182/blood.V84.6.1922.1922

Erikson, 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. USA, 108, 13688, 10.1073/pnas.1101684108

Kupzig, 2003, Bst-2/HM1.24 is a raft-associated apical membrane protein with an unusual topology, Traffic, 4, 694, 10.1034/j.1600-0854.2003.00129.x

Venkatesh, 2016, Origins and Evolution of tetherin, an Orphan Antiviral Gene, Cell Host Microbe, 20, 189, 10.1016/j.chom.2016.06.007

Zang, 2009, Tetherin inhibits HIV-1 release by directly tethering virions to cells, Cell, 139, 499, 10.1016/j.cell.2009.08.039

Sakuma, 2009, Inhibition of Lassa and Marburg virus production by tetherin, J. Virol., 83, 2382, 10.1128/JVI.01607-08

Weidner, 2010, Interferon-induced cell membrane proteins, IFITM3 and tetherin, inhibit vesicular stomatitis virus infection via distinct mechanisms, J. Virol., 84, 12646, 10.1128/JVI.01328-10

Blondeau, 2013, Tetherin restricts herpes simplex virus 1 and is antagonized by glycoprotein M, J. Virol., 87, 13124, 10.1128/JVI.02250-13

Taylor, 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, 10.1128/JVI.02274-15

Li, 2017, Japanese encephalitis virus counteracts BST2 restriction via its envelope protein E, Virology, 510, 67, 10.1016/j.virol.2017.07.008

Hoffmann, M., Nehlmeier, I., Brinkmann, C., Krahling, V., Behner, L., Moldenhauer, A.S., Kruger, N., Nehls, J., Schindler, M., and Hoenen, T. (2019). Tetherin Inhibits Nipah Virus but Not Ebola Virus Replication in Fruit Bat Cells. J. Virol., 93.

Wan, J.J., Ooi, Y.S., and Kielian, M. (2019). Mechanism of Tetherin Inhibition of Alphavirus Release. J. Virol., 93.

Kelly, J.T., Human, S., Alderman, J., Jobe, F., Logan, L., Rix, T., Gonçalves-Carneiro, D., Leung, C., Thakur, N., and Birch, J. (2019). BST2/Tetherin Overexpression Modulates Morbillivirus Glycoprotein Production to Inhibit Cell-Cell Fusion. Viruses, 11.

Zadeh, V.R., Urata, S., Sakaguchi, M., and Yasuda, J. (2020). Human BST-2/tetherin inhibits Junin virus release from host cells and its inhibition is partially counteracted by viral nucleoprotein. J. Gen. Virol., 101.

Wang, 2019, Severe acute respiratory syndrome coronavirus spike protein counteracts BST2-mediated restriction of virus-like particle release, J. Med. Virol., 91, 1743, 10.1002/jmv.25518

González-Hernández, M., Hoffmann, M., Brinkmann, C., Nehls, J., Winkler, M., Schindler, M., and Pöhlmann, S. (2018). A GXXXA Motif in the Transmembrane Domain of the Ebola Virus Glycoprotein Is Required for Tetherin Antagonism. J. Virol., 92.

Bracq, 2018, Mechanisms for Cell-to-Cell Transmission of HIV-1, Front. Immunol., 9, 260, 10.3389/fimmu.2018.00260

Giese, S., and Marsh, M. (2014). Tetherin can restrict cell-free and cell-cell transmission of HIV from primary macrophages to T cells. PLoS Pathog., 10.

Casartelli, N., Sourisseau, M., Feldmann, J., Guivel-Benhassine, F., Mallet, A., Marcelin, A.G., Guatelli, J., and Schwartz, O. (2010). Tetherin restricts productive HIV-1 cell-to-cell transmission. PLoS Pathog., 6.

Jolly, 2010, Cell-cell spread of human immunodeficiency virus type 1 overcomes tetherin/BST-2-mediated restriction in T cells, J. Virol., 84, 12185, 10.1128/JVI.01447-10

Mitchell, R.S., Katsura, C., Skasko, M.A., Fitzpatrick, K., Lau, D., Ruiz, A., Stephens, E.B., Margottin-Goguet, F., Benarous, R., and Guatelli, J.C. (2009). Vpu antagonizes BST-2-mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking. PLoS Pathog., 5.

Douglas, 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, 10.1128/JVI.00242-09

Song, Y.E., Cyburt, D., Lucas, T.M., Gregory, D.A., Lyddon, T.D., and Johnson, M.C. (2018). βTrCP is Required for HIV-1 Vpu Modulation of CD4, GaLV Env, and BST-2/Tetherin. Viruses, 10.

Dube, M., Roy, B.B., Guiot-Guillain, P., Binette, J., Mercier, J., Chiasson, A., and Cohen, E.A. (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.

Andrew, 2011, Differential effects of human immunodeficiency virus type 1 Vpu on the stability of BST-2/tetherin, J. Virol., 85, 2611, 10.1128/JVI.02080-10

Zhang, 2009, Nef proteins from simian immunodeficiency viruses are tetherin antagonists, Cell Host Microbe, 6, 54, 10.1016/j.chom.2009.05.008

Zhang, F., Landford, W.N., Ng, M., McNatt, M.W., Bieniasz, P.D., and Hatziioannou, T. (2011). SIV Nef proteins recruit the AP-2 complex to antagonize Tetherin and facilitate virion release. PLoS Pathog., 7.

Chen, 2016, Antagonism of BST-2/Tetherin Is a Conserved Function of the Env Glycoprotein of Primary HIV-2 Isolates, J. Virol., 90, 11062, 10.1128/JVI.01451-16

Janaka, S.K., Tavakoli-Tameh, A., Neidermyer, W.J., Serra-Moreno, R., Hoxie, J.A., Desrosiers, R.C., Johnson, R.P., Lifson, J.D., Wolinsky, S.M., and Evans, D.T. (2018). Polymorphisms in Rhesus Macaque Tetherin Are Associated with Differences in Acute Viremia in Simian Immunodeficiency Virus Δ. J. Virol., 92.

Buffalo, 2019, Structural Basis for Tetherin Antagonism as a Barrier to Zoonotic Lentiviral Transmission, Cell Host Microbe, 26, 359, 10.1016/j.chom.2019.08.002

Tavakoli-Tameh, A., Janaka, S.K., Zarbock, K., O’Connor, S., Crosno, K., Capuano, S., Uno, H., Lifson, J.D., and Evans, D.T. (2020). Loss of tetherin antagonism by Nef impairs SIV replication during acute infection of rhesus macaques. PLoS Pathog., 16.

Goffinet, 2010, Endogenous CD317/Tetherin limits replication of HIV-1 and murine leukemia virus in rodent cells and is resistant to antagonists from primate viruses, J. Virol., 84, 11374, 10.1128/JVI.01067-10

Liberatore, 2011, Tetherin is a key effector of the antiretroviral activity of type I interferon in vitro and in vivo, Proc. Natl. Acad. Sci. USA, 108, 18097, 10.1073/pnas.1113694108

Heusinger, 2015, Early Vertebrate Evolution of the Host Restriction Factor Tetherin, J. Virol., 89, 12154, 10.1128/JVI.02149-15

Gupta, R.K., Hue, S., Schaller, T., Verschoor, E., Pillay, D., and Towers, G.J. (2009). Mutation of a single residue renders human tetherin resistant to HIV-1 Vpu-mediated depletion. PLoS Pathog., 5.

Lim, 2010, Ancient adaptive evolution of tetherin shaped the functions of Vpu and Nef in human immunodeficiency virus and primate lentiviruses, J. Virol., 84, 7124, 10.1128/JVI.00468-10

Liu, J., Chen, K., Wang, J.H., and Zhang, C. (2010). Molecular evolution of the primate antiviral restriction factor tetherin. PLoS ONE, 5.

McNatt, M.W., Zang, T., Hatziioannou, T., Bartlett, M., Fofana, I.B., Johnson, W.E., Neil, S.J., and Bieniasz, P.D. (2009). Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog., 5.

Arias, 2016, Tetherin Antagonism by HIV-1 Group M Nef Proteins, J. Virol., 90, 10701, 10.1128/JVI.01465-16

Jager, 2012, Global landscape of HIV-human protein complexes, Nature, 481, 365, 10.1038/nature10719

Matheson, 2015, Cell Surface Proteomic Map of HIV Infection Reveals Antagonism of Amino Acid Metabolism by Vpu and Nef, Cell Host Microbe, 18, 409, 10.1016/j.chom.2015.09.003

Jain, 2018, Large-Scale Arrayed Analysis of Protein Degradation Reveals Cellular Targets for HIV-1 Vpu, Cell Rep., 22, 2493, 10.1016/j.celrep.2018.01.091

Nielsen, R., Bustamante, C., Clark, A.G., Glanowski, S., Sackton, T.B., Hubisz, M.J., Fledel-Alon, A., Tanenbaum, D.M., Civello, D., and White, T.J. (2005). A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol., 3.