1887

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Volume 99, Issue 5

A naturally occurring feline APOBEC3 variant that loses anti-lentiviral activity by lacking two amino acid residues Free

Abstract

Apolipoprotein B mRNA-editing enzyme catalytic polypeptide-like 3 (APOBEC3) is a mammalian protein that restricts lentiviral replication. Various polymorphisms of mammalian genes have been observed in humans, Old World monkeys and domestic cats; however, the genetic diversity of genes in other mammals remains unaddressed. Here we identify a novel haplotype of the feline gene, an gene that restricts feline immunodeficiency virus (FIV) replication, in a Eurasian lynx (). Compared to the previously identified lynx (haplotype I), the new sequence (haplotype II) harbours two amino acid deletions (Q16 and H17) and a nonsynonymous substitution (R68Q). Interestingly, lynx haplotype II does not suppress FIV infectivity, whereas haplotype I does. Mutagenesis experiments further revealed that deleting two amino acids (Q16 and H17) causes anti-FIV activity loss. This report demonstrates that a naturally occurring APOBEC3 variant loses anti-lentiviral activity through the deletion of two amino acid residues.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): APOBEC3 , evolutionary arms race , felids , FIV , lentivirus and lynx
© 2018 The Authors
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2018-05-01
2024-04-19
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References

  1. Kirchhoff F. Immune evasion and counteraction of restriction factors by HIV-1 and other primate lentiviruses. Cell Host Microbe 2010; 8:55–67 [View Article][PubMed]
     [Google Scholar]
  2. Harris RS, Dudley JP. APOBECs and virus restriction. Virology 2015; 479-480:131–145 [View Article][PubMed]
     [Google Scholar]
  3. Larue RS, Andrésdóttir V, Blanchard Y, Conticello SG, Derse D et al. Guidelines for naming nonprimate APOBEC3 genes and proteins. J Virol 2009; 83:494–497 [View Article][PubMed]
     [Google Scholar]
  4. Zhang J. Evolution by gene duplication: an update. Trends Ecol Evol 2003; 18:292–298 [View Article]
     [Google Scholar]
  5. Sawyer SL, Emerman M, Malik HS. Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2004; 2:e275 [View Article][PubMed]
     [Google Scholar]
  6. Zhang J, Webb DM. Rapid evolution of primate antiviral enzyme APOBEC3G. Hum Mol Genet 2004; 13:1785–1791 [View Article][PubMed]
     [Google Scholar]
  7. Vallender EJ, Lahn BT. Positive selection on the human genome. Hum Mol Genet 2004; 13:R245–R254 [View Article][PubMed]
     [Google Scholar]
  8. Nakano Y, Misawa N, Juarez-Fernandez G, Moriwaki M, Nakaoka S et al. HIV-1 competition experiments in humanized mice show that APOBEC3H imposes selective pressure and promotes virus adaptation. PLoS Pathog 2017; 13:e1006348 [View Article][PubMed]
     [Google Scholar]
  9. 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; 4:249–259 [View Article][PubMed]
     [Google Scholar]
  10. Ooms M, Brayton B, Letko M, Maio SM, Pilcher CD et al. HIV-1 Vif adaptation to human APOBEC3H haplotypes. Cell Host Microbe 2013; 14:411–421 [View Article][PubMed]
     [Google Scholar]
  11. Wang X, Abudu A, Son S, Dang Y, Venta PJ et al. Analysis of human APOBEC3H haplotypes and anti-human immunodeficiency virus type 1 activity. J Virol 2011; 85:3142–3152 [View Article][PubMed]
     [Google Scholar]
  12. Refsland EW, Hultquist JF, Luengas EM, Ikeda T, Shaban NM et al. 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; 10:e1004761 [View Article][PubMed]
     [Google Scholar]
  13. Compton AA, Hirsch VM, Emerman M. The host restriction factor APOBEC3G and retroviral Vif protein coevolve due to ongoing genetic conflict. Cell Host Microbe 2012; 11:91–98 [View Article][PubMed]
     [Google Scholar]
  14. Compton AA, Emerman M. Convergence and divergence in the evolution of the APOBEC3G-Vif interaction reveal ancient origins of simian immunodeficiency viruses. PLoS Pathog 2013; 9:e1003135 [View Article][PubMed]
     [Google Scholar]
  15. de Castro FL, Junqueira DM, de Medeiros RM, da Silva TR, Costenaro JG et al. Analysis of single-nucleotide polymorphisms in the APOBEC3H gene of domestic cats (Felis catus) and their association with the susceptibility to feline immunodeficiency virus and feline leukemia virus infections. Infect Genet Evol 2014; 27:389–394 [View Article][PubMed]
     [Google Scholar]
  16. Yoshikawa R, Izumi T, Yamada E, Nakano Y, Misawa N et al. A naturally occurring domestic cat APOBEC3 variant confers resistance to feline immunodeficiency virus infection. J Virol 2016; 90:474–485 [View Article][PubMed]
     [Google Scholar]
  17. Yamada E, Yoshikawa R, Nakano Y, Misawa N, Kobayashi T et al. A naturally occurring bovine APOBEC3 confers resistance to bovine lentiviruses: implication for the co-evolution of bovids and their lentiviruses. Sci Rep 2016; 6:33988 [View Article][PubMed]
     [Google Scholar]
  18. Irwin DM, Kocher TD, Wilson AC. Evolution of the cytochrome b gene of mammals. J Mol Evol 1991; 32:128–144 [View Article][PubMed]
     [Google Scholar]
  19. Zielonka J, Marino D, Hofmann H, Yuhki N, Löchelt M et al. Vif of feline immunodeficiency virus from domestic cats protects against APOBEC3 restriction factors from many felids. J Virol 2010; 84:7312–7324 [View Article][PubMed]
     [Google Scholar]
  20. Kobayashi T, Takeuchi JS, Ren F, Matsuda K, Sato K et al. Characterization of red-capped mangabey tetherin: implication for the co-evolution of primates and their lentiviruses. Sci Rep 2014; 4:5529 [View Article][PubMed]
     [Google Scholar]
  21. Takeuchi JS, Ren F, Yoshikawa R, Yamada E, Nakano Y et al. Coevolutionary dynamics between tribe Cercopithecini tetherins and their lentiviruses. Sci Rep 2015; 5:16021 [View Article][PubMed]
     [Google Scholar]
  22. Yoshikawa R, Takeuchi JS, Yamada E, Nakano Y, Misawa N et al. Feline immunodeficiency virus evolutionarily acquires two proteins, Vif and protease, capable of antagonizing feline APOBEC3. J Virol 2017; 91:e00250-17 [View Article][PubMed]
     [Google Scholar]
  23. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article][PubMed]
     [Google Scholar]
  24. Nakano Y, Matsuda K, Yoshikawa R, Yamada E, Misawa N et al. Down-modulation of primate lentiviral receptors by Nef proteins of SIVcpz and related SIVs: implication for the evolutionary event on the emergence of SIVcpz. J Gen Virol 2015
     [Google Scholar]
  25. Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G et al. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 2014; 42:W252–W258 [View Article][PubMed]
     [Google Scholar]
  26. Guex N, Peitsch MC, Schwede T. Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: a historical perspective. Electrophoresis 2009; 30:S162–S173 [View Article][PubMed]
     [Google Scholar]
  27. Bordoli L, Kiefer F, Arnold K, Benkert P, Battey J et al. Protein structure homology modeling using SWISS-MODEL workspace. Nat Protoc 2009; 4:1–13 [View Article][PubMed]
     [Google Scholar]
  28. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402 [View Article][PubMed]
     [Google Scholar]
  29. Arnold K, Bordoli L, Kopp J, Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 2006; 22:195–201 [View Article][PubMed]
     [Google Scholar]
  30. Kouno T, Silvas TV, Hilbert BJ, Shandilya SMD, Bohn MF et al. Crystal structure of APOBEC3A bound to single-stranded DNA reveals structural basis for cytidine deamination and specificity. Nat Commun 2017; 8:15024 [View Article][PubMed]
     [Google Scholar]
  31. East JL, Knesek JE, Allen PT, Dmochowski L. Structural characteristics and nucleotide sequence analysis of genomic RNA from RD-114 virus and feline RNA tumor viruses. J Virol 1973; 12:1085–1091[PubMed]
     [Google Scholar]
  32. Okabe H, Gilden RV, Hatanaka M. RD 114 virus-specific sequences in feline cellular RNA: detection and characterization. J Virol 1973; 12:984–994[PubMed]
     [Google Scholar]
  33. Overbaugh J, Donahue PR, Quackenbush SL, Hoover EA, Mullins JI. Molecular cloning of a feline leukemia virus that induces fatal immunodeficiency disease in cats. Science 1988; 239:906–910 [View Article][PubMed]
     [Google Scholar]
  34. Yoshikawa R, Sato E, Igarashi T, Miyazawa T. Characterization of RD-114 virus isolated from a commercial canine vaccine manufactured using CRFK cells. J Clin Microbiol 2010; 48:3366–3369 [View Article][PubMed]
     [Google Scholar]
  35. Fukuma A, Abe M, Morikawa Y, Miyazawa T, Yasuda J. Cloning and characterization of the antiviral activity of feline Tetherin/BST-2. PLoS One 2011; 6:e18247 [View Article][PubMed]
     [Google Scholar]
  36. Izumi T, Io K, Matsui M, Shirakawa K, Shinohara M et al. HIV-1 viral infectivity factor interacts with TP53 to induce G2 cell cycle arrest and positively regulate viral replication. Proc Natl Acad Sci USA 2010; 107:20798–20803 [View Article][PubMed]
     [Google Scholar]
  37. Wei X, Decker JM, Liu H, Zhang Z, Arani RB et al. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 2002; 46:1896–1905 [View Article][PubMed]
     [Google Scholar]
  38. Mariani R, Chen D, Schröfelbauer B, Navarro F, König R et al. Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 2003; 114:21–31 [View Article][PubMed]
     [Google Scholar]
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A naturally occurring feline APOBEC3 variant that loses anti-lentiviral activity by lacking two amino acid residues
J. Gen. Virol. 99, 704 (2018); https://doi.org/10.1099/jgv.0.001046
/content/journal/jgv/10.1099/jgv.0.001046
/content/journal/jgv/10.1099/jgv.0.001046
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