1887

Abstract

APOBEC3 (apolipoprotein B mRNA editing enzyme catalytic polypeptide-like 3) proteins are cellular DNA deaminases that restrict a broad spectrum of lentiviruses. This process is counteracted by Vif (viral infectivity factor) of lentiviruses, which binds APOBEC3s and promotes their degradation. CBF-β (core binding factor subunit β) is an essential co-factor for the function of human immunodeficiency virus type 1 Vif to degrade human APOBEC3s. However, the requirement for CBF-β in Vif-mediated degradation of other mammalian APOBEC3 proteins is less clear. Here, we determined the sequence of feline and performed phylogenetic analyses. These analyses revealed that mammalian is under purifying selection. Moreover, we demonstrated that CBF-β is dispensable for feline immunodeficiency virus Vif-mediated degradation of APOBEC3s of its host. These findings suggested that primate lentiviruses have adapted to use CBF-β, an evolutionary stable protein, to counteract APOBEC3 proteins of their hosts after diverging from other lentiviruses.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000027
2015-04-01
2020-01-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/4/887.html?itemId=/content/journal/jgv/10.1099/jgv.0.000027&mimeType=html&fmt=ahah

References

  1. Adya N., Castilla L. H., Liu P. P.. ( 2000;). Function of CBFβ/Bro proteins. . Semin Cell Dev Biol 11:, 361–368. [CrossRef][PubMed]
    [Google Scholar]
  2. Ai Y., Zhu D., Wang C., Su C., Ma J., Ma J., Wang X.. ( 2014;). Core-binding factor subunit beta is not required for non-primate lentiviral Vif-mediated APOBEC3 degradation. . J Virol 88:, 12112–12122. [CrossRef][PubMed]
    [Google Scholar]
  3. Albin J. S., Harris R. S.. ( 2010;). Interactions of host APOBEC3 restriction factors with HIV-1 in vivo: implications for therapeutics. . Expert Rev Mol Med 12:, e4. [CrossRef][PubMed]
    [Google Scholar]
  4. Bravo J., Li Z., Speck N. A., Warren A. J.. ( 2001;). The leukemia-associated AML1 (Runx1)–CBF β complex functions as a DNA-induced molecular clamp. . Nat Struct Biol 8:, 371–378. [CrossRef][PubMed]
    [Google Scholar]
  5. de Bruijn M. F., Speck N. A.. ( 2004;). Core-binding factors in hematopoiesis and immune function. . Oncogene 23:, 4238–4248. [CrossRef][PubMed]
    [Google Scholar]
  6. Desimmie B. A., Delviks-Frankenberrry K. A., Burdick R. C., Qi D., Izumi T., Pathak V. K.. ( 2014;). Multiple APOBEC3 restriction factors for HIV-1 and one Vif to rule them all. . J Mol Biol 426:, 1220–1245. [CrossRef][PubMed]
    [Google Scholar]
  7. Du J., Zhao K., Rui Y., Li P., Zhou X., Zhang W., Yu X. F.. ( 2013;). Differential requirements for HIV-1 Vif-mediated APOBEC3G degradation and RUNX1-mediated transcription by core binding factor beta. . J Virol 87:, 1906–1911. [CrossRef][PubMed]
    [Google Scholar]
  8. Feng Y., Baig T. T., Love R. P., Chelico L.. ( 2014;). Suppression of APOBEC3-mediated restriction of HIV-1 by Vif. . Front Microbiol 5:, 450. [CrossRef][PubMed]
    [Google Scholar]
  9. Gifford R. J.. ( 2012;). Viral evolution in deep time: lentiviruses and mammals. . Trends Genet 28:, 89–100. [CrossRef][PubMed]
    [Google Scholar]
  10. Guindon S., Dufayard J. F., Lefort V., Anisimova M., Hordijk W., Gascuel O.. ( 2010;). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. . Syst Biol 59:, 307–321. [CrossRef][PubMed]
    [Google Scholar]
  11. Guo Y., Dong L., Qiu X., Wang Y., Zhang B., Liu H., Yu Y., Zang Y., Yang M., Huang Z.. ( 2014;). Structural basis for hijacking CBF-β and CUL5 E3 ligase complex by HIV-1 Vif. . Nature 505:, 229–233. [CrossRef][PubMed]
    [Google Scholar]
  12. Han X., Liang W., Hua D., Zhou X., Du J., Evans S. L., Gao Q., Wang H., Viqueira R.. & other authors ( 2014;). Evolutionarily conserved requirement for core binding factor beta in the assembly of the human immunodeficiency virus/simian immunodeficiency virus Vif-cullin 5-RING E3 ubiquitin ligase. . J Virol 88:, 3320–3328. [CrossRef][PubMed]
    [Google Scholar]
  13. Harris R. S., Bishop K. N., Sheehy A. M., Craig H. M., Petersen-Mahrt S. K., Watt I. N., Neuberger M. S., Malim M. H.. ( 2003;). DNA deamination mediates innate immunity to retroviral infection. . Cell 113:, 803–809. [CrossRef][PubMed]
    [Google Scholar]
  14. Hultquist J. F., Binka M., LaRue R. S., Simon V., Harris R. S.. ( 2012a;). Vif proteins of human and simian immunodeficiency viruses require cellular CBFβ to degrade APOBEC3 restriction factors. . J Virol 86:, 2874–2877. [CrossRef][PubMed]
    [Google Scholar]
  15. Hultquist J. F., McDougle R. M., Anderson B. D., Harris R. S.. ( 2012b;). HIV type 1 viral infectivity factor and the RUNX transcription factors interact with core binding factor β on genetically distinct surfaces. . AIDS Res Hum Retroviruses 28:, 1543–1551. [CrossRef][PubMed]
    [Google Scholar]
  16. Ito Y.. ( 2008;). RUNX genes in development and cancer: regulation of viral gene expression and the discovery of RUNX family genes. . Adv Cancer Res 99:, 33–76. [CrossRef][PubMed]
    [Google Scholar]
  17. Jäger S., Kim D. Y., Hultquist J. F., Shindo K., LaRue R. S., Kwon E., Li M., Anderson B. D., Yen L.. & other authors ( 2012;). Vif hijacks CBF-β to degrade APOBEC3G and promote HIV-1 infection. . Nature 481:, 371–375.[PubMed]
    [Google Scholar]
  18. Kim D. Y., Kwon E., Hartley P. D., Crosby D. C., Mann S., Krogan N. J., Gross J. D.. ( 2013;). CBFβ stabilizes HIV Vif to counteract APOBEC3 at the expense of RUNX1 target gene expression. . Mol Cell 49:, 632–644. [CrossRef][PubMed]
    [Google Scholar]
  19. Kitamura S., Ode H., Iwatani Y.. ( 2011;). Structural features of antiviral APOBEC3 proteins are linked to their functional activities. . Front Microbiol 2:, 258. [CrossRef][PubMed]
    [Google Scholar]
  20. Kobayashi T., Koizumi Y., Takeuchi J. S., Misawa N., Kimura Y., Morita S., Aihara K., Koyanagi Y., Iwami S., Sato K.. ( 2014a;). Quantification of deaminase activity-dependent and -independent restriction of HIV-1 replication mediated by APOBEC3F and APOBEC3G through experimental-mathematical investigation. . J Virol 88:, 5881–5887. [CrossRef][PubMed]
    [Google Scholar]
  21. Kobayashi T., Takeuchi J. S., Ren F., Matsuda K., Sato K., Kimura Y., Misawa N., Yoshikawa R., Nakano Y.. & other authors ( 2014b;). Characterization of red-capped mangabey tetherin: implication for the co-evolution of primates and their lentiviruses. . Sci Rep 4:, 5529. [CrossRef][PubMed]
    [Google Scholar]
  22. LaRue R. S., Lengyel J., Jónsson S. R., Andrésdóttir V., Harris R. S.. ( 2010;). Lentiviral Vif degrades the APOBEC3Z3/APOBEC3H protein of its mammalian host and is capable of cross-species activity. . J Virol 84:, 8193–8201. [CrossRef][PubMed]
    [Google Scholar]
  23. Mariani R., Chen D., Schröfelbauer B., Navarro F., König R., Bollman B., Münk C., Nymark-McMahon H., Landau N. R.. ( 2003;). Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. . Cell 114:, 21–31. [CrossRef][PubMed]
    [Google Scholar]
  24. Münk C., Beck T., Zielonka J., Hotz-Wagenblatt A., Chareza S., Battenberg M., Thielebein J., Cichutek K., Bravo I. G.. & other authors ( 2008;). Functions, structure, and read-through alternative splicing of feline APOBEC3 genes. . Genome Biol 9:, R48. [CrossRef][PubMed]
    [Google Scholar]
  25. Münk C., Willemsen A., 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:, 71. [CrossRef][PubMed]
    [Google Scholar]
  26. Penn O., Privman E., Ashkenazy H., Landan G., Graur D., Pupko T.. ( 2010;). guidance: a web server for assessing alignment confidence scores. . Nucleic Acids Res 38: (Web Server issue), W23–W28. [CrossRef][PubMed]
    [Google Scholar]
  27. Pond S. L., Frost S. D.. ( 2005;). Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. . Bioinformatics 21:, 2531–2533. [CrossRef][PubMed]
    [Google Scholar]
  28. Refsland E. W., Harris R. S.. ( 2013;). The APOBEC3 family of retroelement restriction factors. . Curr Top Microbiol Immunol 371:, 1–27.[PubMed]
    [Google Scholar]
  29. Sheehy A. M., Gaddis N. C., Choi J. D., Malim M. H.. ( 2002;). Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. . Nature 418:, 646–650. [CrossRef][PubMed]
    [Google Scholar]
  30. Shimojima M., Miyazawa T., Ikeda Y., McMonagle E. L., Haining H., Akashi H., Takeuchi Y., Hosie M. J., Willett B. J.. ( 2004;). Use of CD134 as a primary receptor by the feline immunodeficiency virus. . Science 303:, 1192–1195. [CrossRef][PubMed]
    [Google Scholar]
  31. Stern M. A., Hu C., Saenz D. T., Fadel H. J., Sims O., Peretz M., Poeschla E. M.. ( 2010;). Productive replication of Vif-chimeric HIV-1 in feline cells. . J Virol 84:, 7378–7395. [CrossRef][PubMed]
    [Google Scholar]
  32. Tahirov T. H., Inoue-Bungo T., Morii H., Fujikawa A., Sasaki M., Kimura K., Shiina M., Sato K., Kumasaka T.. & other authors ( 2001;). Structural analyses of DNA recognition by the AML1/Runx-1 Runt domain and its allosteric control by CBFbeta. . Cell 104:, 755–767. [CrossRef][PubMed]
    [Google Scholar]
  33. Wang J., Zhang W., Lv M., Zuo T., Kong W., Yu X.. ( 2011;). Identification of a Cullin5-ElonginB-ElonginC E3 complex in degradation of feline immunodeficiency virus Vif-mediated feline APOBEC3 proteins. . J Virol 85:, 12482–12491. [CrossRef][PubMed]
    [Google Scholar]
  34. Yan J., Liu Y., Lukasik S. M., Speck N. A., Bushweller J. H.. ( 2004;). CBFbeta allosterically regulates the Runx1 Runt domain via a dynamic conformational equilibrium. . Nat Struct Mol Biol 11:, 901–906. [CrossRef][PubMed]
    [Google Scholar]
  35. Zhang H., Yang B., Pomerantz R. J., Zhang C., Arunachalam S. C., Gao L.. ( 2003;). The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. . Nature 424:, 94–98. [CrossRef][PubMed]
    [Google Scholar]
  36. Zhang W., Du J., Evans S. L., Yu Y., Yu X. F.. ( 2012;). T-cell differentiation factor CBF-β regulates HIV-1 Vif-mediated evasion of host restriction. . Nature 481:, 376–379.[PubMed]
    [Google Scholar]
  37. Zhang W., Wang H., Li Z., Liu X., Liu G., Harris R. S., Yu X. F.. ( 2014;). Cellular requirements for bovine immunodeficiency virus Vif-mediated inactivation of bovine APOBEC3 proteins. . J Virol 88:, 12528–12540. [CrossRef][PubMed]
    [Google Scholar]
  38. Zielonka J., Münk C.. ( 2011;). Cellular restriction factors of feline immunodeficiency virus. . Viruses 3:, 1986–2005. [CrossRef][PubMed]
    [Google Scholar]
  39. Zielonka J., Marino D., Hofmann H., Yuhki N., Löchelt M., Münk C.. ( 2010;). Vif of feline immunodeficiency virus from domestic cats protects against APOBEC3 restriction factors from many felids. . J Virol 84:, 7312–7324. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000027
Loading
/content/journal/jgv/10.1099/jgv.0.000027
Loading

Data & Media loading...

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error