Restriction of equine infectious anemia virus by equine APOBEC3 cytidine deaminases.
Abstract: The mammalian APOBEC3 (A3) proteins comprise a multigene family of cytidine deaminases that act as potent inhibitors of retroviruses and retrotransposons. The A3 locus on the chromosome 28 of the horse genome contains multiple A3 genes: two copies of A3Z1, five copies of A3Z2, and a single copy of A3Z3, indicating a complex evolution of multiple gene duplications. We have cloned and analyzed for expression the different equine A3 genes and examined as well the subcellular distribution of the corresponding proteins. Additionally, we have tested the functional antiretroviral activity of the equine and of several of the human and nonprimate A3 proteins against the Equine infectious anemia virus (EIAV), the Simian immunodeficiency virus (SIV), and the Adeno-associated virus type 2 (AAV-2). Hematopoietic cells of horses express at least five different A3s: A3Z1b, A3Z2a-Z2b, A3Z2c-Z2d, A3Z2e, and A3Z3, whereas circulating macrophages, the natural target of EIAV, express only part of the A3 repertoire. The five A3Z2 tandem copies arose after three consecutive, recent duplication events in the horse lineage, after the split between Equidae and Carnivora. The duplicated genes show different antiviral activities against different viruses: equine A3Z3 and A3Z2c-Z2d are potent inhibitors of EIAV while equine A3Z1b, A3Z2a-Z2b, A3Z2e showed only weak anti-EIAV activity. Equine A3Z1b and A3Z3 restricted AAV and all equine A3s, except A3Z1b, inhibited SIV. We hypothesize that the horse A3 genes are undergoing a process of subfunctionalization in their respective viral specificities, which might provide the evolutionary advantage for keeping five copies of the original gene.
Publication Date: 2009-05-20 PubMed ID: 19458006PubMed Central: PMC2708611DOI: 10.1128/JVI.00015-09Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The study investigates how certain proteins in the horse genome inhibit certain viruses including the equine infectious anemia virus (EIAV). It also investigates why horses have multiple copies of these antiviral proteins and how these influence their response to different viruses.
Study Overview
- The researchers focused on a group of proteins known as mammalian APOBEC3 (A3), which are known to prevent infection by retroviruses and retrotransposons – a type of jumping gene that can move around the genome.
- These proteins are found on chromosome 28 of the horse genome. There are multiple A3 genes present in this region, including two copies of A3Z1, five of A3Z2, and a single copy of A3Z3. This suggested a fascinating evolution of these genes with considerable duplications.
Analyzing Gene Expression and Functionality
- The research team cloned various equine A3 genes and evaluated their expression and the subcellular location of the related proteins. They also tested these genes’ capabilities to inhibit particular viruses: EIAV, Simian immunodeficiency virus (SIV), and Adeno-associated virus type 2 (AAV-2).
- The results showed that hematopoietic cells (blood cell producing cells) of horses expressed at least five A3s. Circulating macrophages, a type of white blood cell targeted by EIAV, only expressed part of the A3 repertoire.
Discovering Antiviral Activities and Evolution of A3 Genes
- They discovered that the five A3Z2 gene copies came about after three consecutive duplications in the horse lineage, following the split between Equidae (horse family) and Carnivora (meat-eating animals).
- The team noted that the duplicated genes exhibited different antiviral properties against different viruses. For instance, the equine A3Z3 and A3Z2c-Z2d effectively inhibited EIAV, but other A3 genes displayed only weak anti-EIAV activity.
- The researchers proposed that horse A3 genes may be undergoing a process of subfunctionalization in which each gene adapts to counteract specific viruses. This might offer an evolutionary advantage in maintaining numerous copies of the original gene.
Cite This Article
APA
Zielonka J, Bravo IG, Marino D, Conrad E, Perković M, Battenberg M, Cichutek K, Münk C.
(2009).
Restriction of equine infectious anemia virus by equine APOBEC3 cytidine deaminases.
J Virol, 83(15), 7547-7559.
https://doi.org/10.1128/JVI.00015-09 Publication
Researcher Affiliations
- Division of Medical Biotechnology, Paul Ehrlich Institut, Langen, Germany.
MeSH Terms
- APOBEC Deaminases
- Animals
- Cell Line
- Cytidine Deaminase / genetics
- Cytidine Deaminase / metabolism
- Cytosine Deaminase / genetics
- Cytosine Deaminase / metabolism
- Equine Infectious Anemia / enzymology
- Equine Infectious Anemia / virology
- Gene Expression
- HeLa Cells
- Horses
- Humans
- Infectious Anemia Virus, Equine / genetics
- Infectious Anemia Virus, Equine / physiology
- Molecular Sequence Data
- Multigene Family
References
This article includes 100 references
- Balaggan KS, Binley K, Esapa M, Iqball S, Askham Z, Kan O, Tschernutter M, Bainbridge JW, Naylor S, Ali RR. Stable and efficient intraocular gene transfer using pseudotyped EIAV lentiviral vectors.. J Gene Med 2006 Mar;8(3):275-85.
- Benton MJ, Donoghue PC. Paleontological evidence to date the tree of life.. Mol Biol Evol 2007 Jan;24(1):26-53.
- Bininda-Emonds OR, Cardillo M, Jones KE, MacPhee RD, Beck RM, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A. The delayed rise of present-day mammals.. Nature 2007 Mar 29;446(7135):507-12.
- Bishop KN, Holmes RK, Malim MH. Antiviral potency of APOBEC proteins does not correlate with cytidine deamination.. J Virol 2006 Sep;80(17):8450-8.
- Bishop KN, Holmes RK, Sheehy AM, Davidson NO, Cho SJ, Malim MH. Cytidine deamination of retroviral DNA by diverse APOBEC proteins.. Curr Biol 2004 Aug 10;14(15):1392-6.
- Bogerd HP, Tallmadge RL, Oaks JL, Carpenter S, Cullen BR. Equine infectious anemia virus resists the antiretroviral activity of equine APOBEC3 proteins through a packaging-independent mechanism.. J Virol 2008 Dec;82(23):11889-901.
- Bogerd HP, Wiegand HL, Doehle BP, Cullen BR. The intrinsic antiretroviral factor APOBEC3B contains two enzymatically active cytidine deaminase domains.. Virology 2007 Aug 1;364(2):486-93.
- Browne EP, Allers C, Landau NR. Restriction of HIV-1 by APOBEC3G is cytidine deaminase-dependent.. Virology 2009 May 10;387(2):313-21.
- Browne EP, Littman DR. Species-specific restriction of apobec3-mediated hypermutation.. J Virol 2008 Feb;82(3):1305-13.
- Craigo JK, Durkin S, Sturgeon TJ, Tagmyer T, Cook SJ, Issel CJ, Montelaro RC. Immune suppression of challenged vaccinates as a rigorous assessment of sterile protection by lentiviral vaccines.. Vaccine 2007 Jan 15;25(5):834-45.
- Dang Y, Wang X, Esselman WJ, Zheng YH. Identification of APOBEC3DE as another antiretroviral factor from the human APOBEC family.. J Virol 2006 Nov;80(21):10522-33.
- Derse D, Hill SA, Princler G, Lloyd P, Heidecker G. Resistance of human T cell leukemia virus type 1 to APOBEC3G restriction is mediated by elements in nucleocapsid.. Proc Natl Acad Sci U S A 2007 Feb 20;104(8):2915-20.
- Doehle BP, Schäfer A, Wiegand HL, Bogerd HP, Cullen BR. Differential sensitivity of murine leukemia virus to APOBEC3-mediated inhibition is governed by virion exclusion.. J Virol 2005 Jul;79(13):8201-7.
- Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees.. BMC Evol Biol 2007 Nov 8;7:214.
- Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity.. BMC Bioinformatics 2004 Aug 19;5:113.
- Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput.. Nucleic Acids Res 2004;32(5):1792-7.
- Elder JH, Lerner DL, Hasselkus-Light CS, Fontenot DJ, Hunter E, Luciw PA, Montelaro RC, Phillips TR. Distinct subsets of retroviruses encode dUTPase.. J Virol 1992 Mar;66(3):1791-4.
- Emi N, Friedmann T, Yee JK. Pseudotype formation of murine leukemia virus with the G protein of vesicular stomatitis virus.. J Virol 1991 Mar;65(3):1202-7.
- Fagerness AJ, Flaherty MT, Perry ST, Jia B, Payne SL, Fuller FJ. The S2 accessory gene of equine infectious anemia virus is essential for expression of disease in ponies.. Virology 2006 May 25;349(1):22-30.
- Fidalgo-Carvalho I, Craigo JK, Barnes S, Costa-Ramos C, Montelaro RC. Characterization of an equine macrophage cell line: application to studies of EIAV infection.. Vet Microbiol 2009 Apr 14;136(1-2):8-19.
- Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations.. Genetics 1999 Apr;151(4):1531-45.
- Haché G, Liddament MT, Harris RS. The retroviral hypermutation specificity of APOBEC3F and APOBEC3G is governed by the C-terminal DNA cytosine deaminase domain.. J Biol Chem 2005 Mar 25;280(12):10920-4.
- Hakata Y, Landau NR. Reversed functional organization of mouse and human APOBEC3 cytidine deaminase domains.. J Biol Chem 2006 Dec 1;281(48):36624-31.
- Harari A, Ooms M, Mulder LC, Simon V. Polymorphisms and splice variants influence the antiretroviral activity of human APOBEC3H.. J Virol 2009 Jan;83(1):295-303.
- Harris RS, Bishop KN, Sheehy AM, Craig HM, Petersen-Mahrt SK, Watt IN, Neuberger MS, Malim MH. DNA deamination mediates innate immunity to retroviral infection.. Cell 2003 Jun 13;113(6):803-9.
- Hatziioannou T, Perez-Caballero D, Yang A, Cowan S, Bieniasz PD. Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha.. Proc Natl Acad Sci U S A 2004 Jul 20;101(29):10774-9.
- Holmes RK, Koning FA, Bishop KN, Malim MH. APOBEC3F can inhibit the accumulation of HIV-1 reverse transcription products in the absence of hypermutation. Comparisons with APOBEC3G.. J Biol Chem 2007 Jan 26;282(4):2587-95.
- Holmes RK, Malim MH, Bishop KN. APOBEC-mediated viral restriction: not simply editing?. Trends Biochem Sci 2007 Mar;32(3):118-28.
- Hughes T, Liberles DA. The pattern of evolution of smaller-scale gene duplicates in mammalian genomes is more consistent with neo- than subfunctionalisation.. J Mol Evol 2007 Nov;65(5):574-88.
- Iwatani Y, Chan DS, Wang F, Stewart-Maynard K, Sugiura W, Gronenborn AM, Rouzina I, Williams MC, Musier-Forsyth K, Levin JG. Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G.. Nucleic Acids Res 2007;35(21):7096-108.
- Jarmuz A, Chester A, Bayliss J, Gisbourne J, Dunham I, Scott J, Navaratnam N. An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22.. Genomics 2002 Mar;79(3):285-96.
- Jern P, Stoye JP, Coffin JM. Role of APOBEC3 in genetic diversity among endogenous murine leukemia viruses.. PLoS Genet 2007 Oct;3(10):2014-22.
- Jónsson SR, Haché G, Stenglein MD, Fahrenkrug SC, Andrésdóttir V, Harris RS. Evolutionarily conserved and non-conserved retrovirus restriction activities of artiodactyl APOBEC3F proteins.. Nucleic Acids Res 2006;34(19):5683-94.
- Katzourakis A, Tristem M, Pybus OG, Gifford RJ. Discovery and analysis of the first endogenous lentivirus.. Proc Natl Acad Sci U S A 2007 Apr 10;104(15):6261-5.
- Kobayashi M, Takaori-Kondo A, Shindo K, Abudu A, Fukunaga K, Uchiyama T. APOBEC3G targets specific virus species.. J Virol 2004 Aug;78(15):8238-44.
- Kummerfeld SK, Teichmann SA. Relative rates of gene fusion and fission in multi-domain proteins.. Trends Genet 2005 Jan;21(1):25-30.
- LaRue RS, Andrésdóttir V, Blanchard Y, Conticello SG, Derse D, Emerman M, Greene WC, Jónsson SR, Landau NR, Löchelt M, Malik HS, Malim MH, Münk C, O'Brien SJ, Pathak VK, Strebel K, Wain-Hobson S, Yu XF, Yuhki N, Harris RS. Guidelines for naming nonprimate APOBEC3 genes and proteins.. J Virol 2009 Jan;83(2):494-7.
- LaRue RS, Jónsson SR, Silverstein KA, Lajoie M, Bertrand D, El-Mabrouk N, Hötzel I, Andrésdóttir V, Smith TP, Harris RS. 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 2008 Nov 18;9:104.
- Lecossier D, Bouchonnet F, Clavel F, Hance AJ. Hypermutation of HIV-1 DNA in the absence of the Vif protein.. Science 2003 May 16;300(5622):1112.
- Leroux C, Cadoré JL, Montelaro RC. Equine Infectious Anemia Virus (EIAV): what has HIV's country cousin got to tell us?. Vet Res 2004 Jul-Aug;35(4):485-512.
- Leroux C, Craigo JK, Issel CJ, Montelaro RC. Equine infectious anemia virus genomic evolution in progressor and nonprogressor ponies.. J Virol 2001 May;75(10):4570-83.
- Li F, Leroux C, Craigo JK, Cook SJ, Issel CJ, Montelaro RC. The S2 gene of equine infectious anemia virus is a highly conserved determinant of viral replication and virulence properties in experimentally infected ponies.. J Virol 2000 Jan;74(1):573-9.
- Li F, Puffer BA, Montelaro RC. The S2 gene of equine infectious anemia virus is dispensable for viral replication in vitro.. J Virol 1998 Oct;72(10):8344-8.
- Löchelt M, Romen F, Bastone P, Muckenfuss H, Kirchner N, Kim YB, Truyen U, Rösler U, Battenberg M, Saib A, Flory E, Cichutek K, Münk C. The antiretroviral activity of APOBEC3 is inhibited by the foamy virus accessory Bet protein.. Proc Natl Acad Sci U S A 2005 May 31;102(22):7982-7.
- Low A, Okeoma CM, Lovsin N, de las Heras M, Taylor TH, Peterlin BM, Ross SR, Fan H. Enhanced replication and pathogenesis of Moloney murine leukemia virus in mice defective in the murine APOBEC3 gene.. Virology 2009 Mar 15;385(2):455-63.
- Luo K, Wang T, Liu B, Tian C, Xiao Z, Kappes J, Yu XF. Cytidine deaminases APOBEC3G and APOBEC3F interact with human immunodeficiency virus type 1 integrase and inhibit proviral DNA formation.. J Virol 2007 Jul;81(13):7238-48.
- Lynch M, Force A. The probability of duplicate gene preservation by subfunctionalization.. Genetics 2000 Jan;154(1):459-73.
- Mangeat B, Turelli P, Caron G, Friedli M, Perrin L, Trono D. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts.. Nature 2003 Jul 3;424(6944):99-103.
- Mariani R, Chen D, Schröfelbauer B, Navarro F, König R, Bollman B, Münk C, Nymark-McMahon H, Landau NR. Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif.. Cell 2003 Jul 11;114(1):21-31.
- Marin M, Rose KM, Kozak SL, Kabat D. HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation.. Nat Med 2003 Nov;9(11):1398-403.
- Matsushita T, Elliger S, Elliger C, Podsakoff G, Villarreal L, Kurtzman GJ, Iwaki Y, Colosi P. Adeno-associated virus vectors can be efficiently produced without helper virus.. Gene Ther 1998 Jul;5(7):938-45.
- Maury W. Monocyte maturation controls expression of equine infectious anemia virus.. J Virol 1994 Oct;68(10):6270-9.
- Mazarakis ND, Azzouz M, Rohll JB, Ellard FM, Wilkes FJ, Olsen AL, Carter EE, Barber RD, Baban DF, Kingsman SM, Kingsman AJ, O'Malley K, Mitrophanous KA. Rabies virus glycoprotein pseudotyping of lentiviral vectors enables retrograde axonal transport and access to the nervous system after peripheral delivery.. Hum Mol Genet 2001 Sep 15;10(19):2109-21.
- Mbisa JL, Barr R, Thomas JA, Vandegraaff N, Dorweiler IJ, Svarovskaia ES, Brown WL, Mansky LM, Gorelick RJ, Harris RS, Engelman A, Pathak VK. Human immunodeficiency virus type 1 cDNAs produced in the presence of APOBEC3G exhibit defects in plus-strand DNA transfer and integration.. J Virol 2007 Jul;81(13):7099-110.
- Mitrophanous K, Yoon S, Rohll J, Patil D, Wilkes F, Kim V, Kingsman S, Kingsman A, Mazarakis N. Stable gene transfer to the nervous system using a non-primate lentiviral vector.. Gene Ther 1999 Nov;6(11):1808-18.
- Miyagi E, Opi S, Takeuchi H, Khan M, Goila-Gaur R, Kao S, Strebel K. Enzymatically active APOBEC3G is required for efficient inhibition of human immunodeficiency virus type 1.. J Virol 2007 Dec;81(24):13346-53.
- Muckenfuss H, Hamdorf M, Held U, Perković M, Löwer J, Cichutek K, Flory E, Schumann GG, Münk C. APOBEC3 proteins inhibit human LINE-1 retrotransposition.. J Biol Chem 2006 Aug 4;281(31):22161-22172.
- Münk C, Beck T, Zielonka J, Hotz-Wagenblatt A, Chareza S, Battenberg M, Thielebein J, Cichutek K, Bravo IG, O'Brien SJ, Löchelt M, Yuhki N. Functions, structure, and read-through alternative splicing of feline APOBEC3 genes.. Genome Biol 2008;9(3):R48.
- Münk C, Zielonka J, Constabel H, Kloke BP, Rengstl B, Battenberg M, Bonci F, Pistello M, Löchelt M, Cichutek K. Multiple restrictions of human immunodeficiency virus type 1 in feline cells.. J Virol 2007 Jul;81(13):7048-60.
- Navarro F, Bollman B, Chen H, König R, Yu Q, Chiles K, Landau NR. Complementary function of the two catalytic domains of APOBEC3G.. Virology 2005 Mar 15;333(2):374-86.
- Newman EN, Holmes RK, Craig HM, Klein KC, Lingappa JR, Malim MH, Sheehy AM. Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity.. Curr Biol 2005 Jan 26;15(2):166-70.
- OhAinle M, Kerns JA, Li MM, Malik HS, Emerman M. Antiretroelement activity of APOBEC3H was lost twice in recent human evolution.. Cell Host Microbe 2008 Sep 11;4(3):249-59.
- OhAinle M, Kerns JA, Malik HS, Emerman M. Adaptive evolution and antiviral activity of the conserved mammalian cytidine deaminase APOBEC3H.. J Virol 2006 Apr;80(8):3853-62.
- Okeoma CM, Lovsin N, Peterlin BM, Ross SR. APOBEC3 inhibits mouse mammary tumour virus replication in vivo.. Nature 2007 Feb 22;445(7130):927-30.
- Okeoma CM, Low A, Bailis W, Fan HY, Peterlin BM, Ross SR. Induction of APOBEC3 in vivo causes increased restriction of retrovirus infection.. J Virol 2009 Apr;83(8):3486-95.
- Okeoma CM, Petersen J, Ross SR. Expression of murine APOBEC3 alleles in different mouse strains and their effect on mouse mammary tumor virus infection.. J Virol 2009 Apr;83(7):3029-38.
- O'Rourke JP, Hiraragi H, Urban K, Patel M, Olsen JC, Bunnell BA. Analysis of gene transfer and expression in skeletal muscle using enhanced EIAV lentivirus vectors.. Mol Ther 2003 May;7(5 Pt 1):632-9.
- Radcliffe PA, Sion CJ, Wilkes FJ, Custard EJ, Beard GL, Kingsman SM, Mitrophanous KA. Analysis of factor VIII mediated suppression of lentiviral vector titres.. Gene Ther 2008 Feb;15(4):289-97.
- Rohll JB, Mitrophanous KA, Martin-Rendon E, Ellard FM, Radcliffe PA, Mazarakis ND, Kingsman SM. Design, production, safety, evaluation, and clinical applications of nonprimate lentiviral vectors.. Methods Enzymol 2002;346:466-500.
- Ross SR. Are viruses inhibited by APOBEC3 molecules from their host species?. PLoS Pathog 2009 Apr;5(4):e1000347.
- Russell RA, Wiegand HL, Moore MD, Schäfer A, McClure MO, Cullen BR. Foamy virus Bet proteins function as novel inhibitors of the APOBEC3 family of innate antiretroviral defense factors.. J Virol 2005 Jul;79(14):8724-31.
- Saenz DT, Teo W, Olsen JC, Poeschla EM. Restriction of feline immunodeficiency virus by Ref1, Lv1, and primate TRIM5alpha proteins.. J Virol 2005 Dec;79(24):15175-88.
- Santiago ML, Montano M, Benitez R, Messer RJ, Yonemoto W, Chesebro B, Hasenkrug KJ, Greene WC. Apobec3 encodes Rfv3, a gene influencing neutralizing antibody control of retrovirus infection.. Science 2008 Sep 5;321(5894):1343-6.
- Schröfelbauer B, Chen D, Landau NR. A single amino acid of APOBEC3G controls its species-specific interaction with virion infectivity factor (Vif).. Proc Natl Acad Sci U S A 2004 Mar 16;101(11):3927-32.
- Schumacher AJ, Haché G, Macduff DA, Brown WL, Harris RS. The DNA deaminase activity of human APOBEC3G is required for Ty1, MusD, and human immunodeficiency virus type 1 restriction.. J Virol 2008 Mar;82(6):2652-60.
- Sellon DC, Fuller FJ, McGuire TC. The immunopathogenesis of equine infectious anemia virus.. Virus Res 1994 May;32(2):111-38.
- Sellon DC, Perry ST, Coggins L, Fuller FJ. Wild-type equine infectious anemia virus replicates in vivo predominantly in tissue macrophages, not in peripheral blood monocytes.. J Virol 1992 Oct;66(10):5906-13.
- Sheehy AM, Gaddis NC, Choi JD, Malim MH. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein.. Nature 2002 Aug 8;418(6898):646-50.
- Sheehy AM, Gaddis NC, Malim MH. The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif.. Nat Med 2003 Nov;9(11):1404-7.
- Shimodaira H, Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 161114-1116.
- Sonnhammer EL, Koonin EV. Orthology, paralogy and proposed classification for paralog subtypes.. Trends Genet 2002 Dec;18(12):619-20.
- Sponseller BA, Sparks WO, Wannemuehler Y, Li Y, Antons AK, Oaks JL, Carpenter S. Immune selection of equine infectious anemia virus env variants during the long-term inapparent stage of disease.. Virology 2007 Jun 20;363(1):156-65.
- Stamatakis A. Phylogenetic models of rate heterogeneity: a high performance computing perspective. p. 278. In Proceedings of the 20th IEEE International Parallel and Distributed Processing Symposium, Rhodes, Greece. IEEE Computer Society, Washington, DC.
- Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.. Bioinformatics 2006 Nov 1;22(21):2688-90.
- Stamatakis A, Ludwig T, Meier H. RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees.. Bioinformatics 2005 Feb 15;21(4):456-63.
- Suchard MA, Weiss RE, Sinsheimer JS. Bayesian selection of continuous-time Markov chain evolutionary models.. Mol Biol Evol 2001 Jun;18(6):1001-13.
- Suspène R, Henry M, Guillot S, Wain-Hobson S, Vartanian JP. Recovery of APOBEC3-edited human immunodeficiency virus G->A hypermutants by differential DNA denaturation PCR.. J Gen Virol 2005 Jan;86(Pt 1):125-129.
- Suyama M, Torrents D, Bork P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments.. Nucleic Acids Res 2006 Jul 1;34(Web Server issue):W609-12.
- Takeda E, Tsuji-Kawahara S, Sakamoto M, Langlois MA, Neuberger MS, Rada C, Miyazawa M. Mouse APOBEC3 restricts friend leukemia virus infection and pathogenesis in vivo.. J Virol 2008 Nov;82(22):10998-1008.
- Threadgill DS, Steagall WK, Flaherty MT, Fuller FJ, Perry ST, Rushlow KE, Le Grice SF, Payne SL. Characterization of equine infectious anemia virus dUTPase: growth properties of a dUTPase-deficient mutant.. J Virol 1993 May;67(5):2592-600.
- Wiegand HL, Doehle BP, Bogerd HP, Cullen BR. A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins.. EMBO J 2004 Jun 16;23(12):2451-8.
- Wolf D, Goff SP. Host restriction factors blocking retroviral replication.. Annu Rev Genet 2008;42:143-63.
- Xiao X, Li J, Samulski RJ. Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus.. J Virol 1998 Mar;72(3):2224-32.
- Yu X, Yu Y, Liu B, Luo K, Kong W, Mao P, Yu XF. Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex.. Science 2003 Nov 7;302(5647):1056-60.
- Yu Y, Xiao Z, Ehrlich ES, Yu X, Yu XF. Selective assembly of HIV-1 Vif-Cul5-ElonginB-ElonginC E3 ubiquitin ligase complex through a novel SOCS box and upstream cysteines.. Genes Dev 2004 Dec 1;18(23):2867-72.
- Zhang B, Jin S, Jin J, Li F, Montelaro RC. A tumor necrosis factor receptor family protein serves as a cellular receptor for the macrophage-tropic equine lentivirus.. Proc Natl Acad Sci U S A 2005 Jul 12;102(28):9918-23.
- Zhang F, Hatziioannou T, Perez-Caballero D, Derse D, Bieniasz PD. Antiretroviral potential of human tripartite motif-5 and related proteins.. Virology 2006 Sep 30;353(2):396-409.
- Zhang H, Yang B, Pomerantz RJ, Zhang C, Arunachalam SC, Gao L. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA.. Nature 2003 Jul 3;424(6944):94-8.
- Zhang W, Zhang X, Tian C, Wang T, Sarkis PT, Fang Y, Zheng S, Yu XF, Xu R. Cytidine deaminase APOBEC3B interacts with heterogeneous nuclear ribonucleoprotein K and suppresses hepatitis B virus expression.. Cell Microbiol 2008 Jan;10(1):112-21.
- Zheng YH, Irwin D, Kurosu T, Tokunaga K, Sata T, Peterlin BM. Human APOBEC3F is another host factor that blocks human immunodeficiency virus type 1 replication.. J Virol 2004 Jun;78(11):6073-6.
Citations
This article has been cited 25 times.- Wang XF, Zhang X, Ma W, Li J, Wang X. Host cell restriction factors of equine infectious anemia virus.. Virol Sin 2023 Aug;38(4):485-496.
- Shilova ON, Tsyba DL, Shilov ES. Mutagenic Activity of AID/APOBEC Deaminases in Antiviral Defense and Carcinogenesis.. Mol Biol 2022;56(1):46-58.
- Christofi T, Zaravinos A. RNA editing in the forefront of epitranscriptomics and human health.. J Transl Med 2019 Sep 23;17(1):319.
- de Pablo-Maiso L, Doménech A, Echeverría I, Gómez-Arrebola C, de Andrés D, Rosati S, Gómez-Lucia E, Reina R. Prospects in Innate Immune Responses as Potential Control Strategies against Non-Primate Lentiviruses.. Viruses 2018 Aug 17;10(8).
- Milewska A, Kindler E, Vkovski P, Zeglen S, Ochman M, Thiel V, Rajfur Z, Pyrc K. APOBEC3-mediated restriction of RNA virus replication.. Sci Rep 2018 Apr 13;8(1):5960.
- Ai Y, Ma J, Wang X. Clues for two-step virion infectivity factor regulation by core binding factor beta.. J Gen Virol 2017 May;98(5):1113-1121.
- Nakano Y, Aso H, Soper A, Yamada E, Moriwaki M, Juarez-Fernandez G, Koyanagi Y, Sato K. A conflict of interest: the evolutionary arms race between mammalian APOBEC3 and lentiviral Vif.. Retrovirology 2017 May 8;14(1):31.
- Zhang Z, Gu Q, Jaguva Vasudevan AA, Hain A, Kloke BP, Hasheminasab S, Mulnaes D, Sato K, Cichutek K, Häussinger D, Bravo IG, Smits SH, Gohlke H, Münk C. Determinants of FIV and HIV Vif sensitivity of feline APOBEC3 restriction factors.. Retrovirology 2016 Jul 1;13(1):46.
- Nakaya Y, Stavrou S, Blouch K, Tattersall P, Ross SR. In Vivo Examination of Mouse APOBEC3- and Human APOBEC3A- and APOBEC3G-Mediated Restriction of Parvovirus and Herpesvirus Infection in Mouse Models.. J Virol 2016 Sep 1;90(17):8005-12.
- Refsland EW, Hultquist JF, Luengas EM, Ikeda T, Shaban NM, Law EK, Brown WL, Reilly C, Emerman M, Harris RS. Natural polymorphisms in human APOBEC3H and HIV-1 Vif combine in primary T lymphocytes to affect viral G-to-A mutation levels and infectivity.. PLoS Genet 2014 Nov;10(11):e1004761.
- Yin X, Lin Y, Cai W, Wei P, Wang X. Comprehensive analysis of the overall codon usage patterns in equine infectious anemia virus.. Virol J 2013 Dec 20;10:356.
- Yin X, Hu Z, Gu Q, Wu X, Zheng YH, Wei P, Wang X. Equine tetherin blocks retrovirus release and its activity is antagonized by equine infectious anemia virus envelope protein.. J Virol 2014 Jan;88(2):1259-70.
- Horn AV, Klawitter S, Held U, Berger A, Vasudevan AA, Bock A, Hofmann H, Hanschmann KM, Trösemeier JH, Flory E, Jabulowsky RA, Han JS, Löwer J, Löwer R, Münk C, Schumann GG. Human LINE-1 restriction by APOBEC3C is deaminase independent and mediated by an ORF1p interaction that affects LINE reverse transcriptase activity.. Nucleic Acids Res 2014 Jan;42(1):396-416.
- Stavrou S, Nitta T, Kotla S, Ha D, Nagashima K, Rein AR, Fan H, Ross SR. Murine leukemia virus glycosylated Gag blocks apolipoprotein B editing complex 3 and cytosolic sensor access to the reverse transcription complex.. Proc Natl Acad Sci U S A 2013 May 28;110(22):9078-83.
- Münk C, Jensen BE, Zielonka J, Häussinger D, Kamp C. Running loose or getting lost: how HIV-1 counters and capitalizes on APOBEC3-induced mutagenesis through its Vif protein.. Viruses 2012 Nov 14;4(11):3132-61.
- Münk C, Willemsen A, Bravo IG. An ancient history of gene duplications, fusions and losses in the evolution of APOBEC3 mutators in mammals.. BMC Evol Biol 2012 May 28;12:71.
- Denner J, Tönjes RR. Infection barriers to successful xenotransplantation focusing on porcine endogenous retroviruses.. Clin Microbiol Rev 2012 Apr;25(2):318-43.
- Smith HC, Bennett RP, Kizilyer A, McDougall WM, Prohaska KM. Functions and regulation of the APOBEC family of proteins.. Semin Cell Dev Biol 2012 May;23(3):258-68.
- Li MM, Emerman M. Polymorphism in human APOBEC3H affects a phenotype dominant for subcellular localization and antiviral activity.. J Virol 2011 Aug;85(16):8197-207.
- Dörrschuck E, Fischer N, Bravo IG, Hanschmann KM, Kuiper H, Spötter A, Möller R, Cichutek K, Münk C, Tönjes RR. Restriction of porcine endogenous retrovirus by porcine APOBEC3 cytidine deaminases.. J Virol 2011 Apr;85(8):3842-57.
- Albin JS, Haché G, Hultquist JF, Brown WL, Harris RS. Long-term restriction by APOBEC3F selects human immunodeficiency virus type 1 variants with restored Vif function.. J Virol 2010 Oct;84(19):10209-19.
- Qi X, Wang X, Wang S, Lin Y, Jiang C, Ma J, Zhao L, Lv X, Shen R, Wang F, Kong X, Su Z, Zhou J. Genomic analysis of an effective lentiviral vaccine-attenuated equine infectious anemia virus vaccine EIAV FDDV13.. Virus Genes 2010 Aug;41(1):86-98.
- Ooms M, Majdak S, Seibert CW, Harari A, Simon V. The localization of APOBEC3H variants in HIV-1 virions determines their antiviral activity.. J Virol 2010 Aug;84(16):7961-9.
- Larue RS, Lengyel J, Jónsson SR, Andrésdóttir V, Harris RS. Lentiviral Vif degrades the APOBEC3Z3/APOBEC3H protein of its mammalian host and is capable of cross-species activity.. J Virol 2010 Aug;84(16):8193-201.
- Zielonka J, Marino D, Hofmann H, Yuhki N, Löchelt M, Münk C. Vif of feline immunodeficiency virus from domestic cats protects against APOBEC3 restriction factors from many felids.. J Virol 2010 Jul;84(14):7312-24.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists