Genetic analysis of the localization of APOBEC3F to human immunodeficiency virus type 1 virion cores

Journal of Virology

Volumn 89, Issue 4, 2015, Pages 2415-2424

  Donahue, John P ^a   Levinson, Rebecca T ^b   Sheehan, Jonathan H ^a   Sutton, Lorraine ^a   Taylor, Harry E ^c   Meiler, Jens ^a   D'Aquila, Richard T ^c   Song, Chisu ^c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3F; CYTIDINE DEAMINASE; LEUCINE; MUTANT PROTEIN; PHENYLALANINE; APOBEC3F PROTEIN, HUMAN; BETA GALACTOSIDASE; CYTOSINE DEAMINASE; LUCIFERASE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENETIC ANALYSIS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PROTEIN DOMAIN; PROTEIN LOCALIZATION; VIRAL GENETICS; VIRION; VIRUS CORE; VIRUS INHIBITION; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; DNA MUTATIONAL ANALYSIS; GENETICS; IMMUNOLOGY; MISSENSE MUTATION; PHYSIOLOGY; REPORTER GENE; SITE DIRECTED MUTAGENESIS; STAINING; VIRUS ASSEMBLY;

AQUILA; HUMAN IMMUNODEFICIENCY VIRUS 1;

BETA-GALACTOSIDASE; CELL LINE; CYTOSINE DEAMINASE; DNA MUTATIONAL ANALYSIS; GENES, REPORTER; HIV-1; HUMANS; LUCIFERASES; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; STAINING AND LABELING; VIRUS ASSEMBLY;

EID: 84921694996     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01981-14     Document Type: Article

References (55)

1. Bogerd HP, Wiegand HL, Hulme AE, Garcia-Perez JL, O'Shea KS, Moran JV, Cullen BR. 2006. Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc Natl Acad Sci USA 103:8780-8785. http://dx.doi.org/10.1073/pnas.0603313103.
2. Chiu YL, Witkowska HE, Hall SC, Santiago M, Soros VB, Esnault C, Heidmann T, Greene WC. 2006. High-molecular-mass APOBEC3G complexes restrict Alu retrotransposition. Proc Natl Acad Sci USA 103: 15588-15593. http://dx.doi.org/10.1073/pnas.0604524103.
3. Dutko JA, Schafer A, Kenny AE, Cullen BR, Curcio MJ. 2005. Inhibition of a yeast LTR retrotransposon by human APOBEC3 cytidine deaminases. Curr Biol 15:661-666. http://dx.doi.org/10.1016/j.cub.2005.02.051.
4. Esnault C, Millet J, Schwartz O, Heidmann T. 2006. Dual inhibitory effects of APOBEC family proteins on retrotransposition of mammalian endogenous retroviruses. Nucleic Acids Res 34:1522-1531. http://dx.doi.org/10.1093/nar/gkl054.
5. Muckenfuss H, Hamdorf M, Held U, Perkovic M, Lower J, Cichutek K, Flory E, Schumann GG, Munk C. 2006. APOBEC3 proteins inhibit human LINE-1 retrotransposition. J Biol Chem 281:22161-22172. http://dx.doi.org/10.1074/jbc.M601716200.
6. Schumacher AJ, Hache G, Macduff DA, Brown WL, Harris RS. 2008. The DNA deaminase activity of human APOBEC3G is required for Ty1, MusD, and human immunodeficiency virus type 1 restriction. J Virol 82:2652-2660. http://dx.doi.org/10.1128/JVI.02391-07.
7. Schumacher AJ, Nissley DV, Harris RS. 2005. APOBEC3G hypermutates genomicDNAandinhibitsTy1retrotransposition in yeast. Proc NatlAcadSci USA 102:9854-9859. http://dx.doi.org/10.1073/pnas.0501694102.
8. Stenglein MD, Harris RS. 2006. APOBEC3B and APOBEC3F inhibit L1 retrotransposition by a DNA deamination-independent mechanism. J Biol Chem 281:16837-16841. http://dx.doi.org/10.1074/jbc.M602367200.
9. Armitage AE, Katzourakis A, de Oliveira T, Welch JJ, Belshaw R, Bishop KN, Kramer B, McMichael AJ, Rambaut A, Iversen AK. 2008. Conserved footprints of APOBEC3G on hypermutated human immunodeficiency virus type 1 and human endogenous retrovirus HERV-K(HML2) sequences. J Virol 82:8743-8761. http://dx.doi.org/10.1128/JVI.00584-08.
10. Esnault C, Heidmann O, Delebecque F, Dewannieux M, Ribet D, Hance AJ, Heidmann T, Schwartz O. 2005. APOBEC3G cytidine deaminase inhibits retrotransposition of endogenous retroviruses. Nature 433:430-433. http://dx.doi.org/10.1038/nature03238.
11. Lee YN, Malim MH, Bieniasz PD. 2008. Hypermutation of an ancient human retrovirus by APOBEC3G. J Virol 82:8762-8770. http://dx.doi.org/10.1128/JVI.00751-08.
12. Delebecque F, Suspene R, Calattini S, Casartelli N, Saib A, Froment A, Wain-Hobson S, Gessain A, Vartanian JP, Schwartz O. 2006. Restriction of foamy viruses by APOBEC cytidine deaminases. J Virol 80:605-614. http://dx.doi.org/10.1128/JVI.80.2.605-614.2006.
13. Jonsson SR, LaRue RS, Stenglein MD, Fahrenkrug SC, Andresdottir V, Harris RS. 2007. The restriction of zoonotic PERV transmission by human APOBEC3G. PLoS One 2:e893. http://dx.doi.org/10.1371/journal.pone.0000893.
14. Mangeat B, Turelli P, Caron G, Friedli M, Perrin L, Trono D. 2003. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424:99-103. http://dx.doi.org/10.1038/nature01709.
15. Takeda E, Tsuji-Kawahara S, Sakamoto M, Langlois MA, Neuberger MS, Rada C, Miyazawa M. 2008. Mouse APOBEC3 restricts friend leukemia virus infection and pathogenesis in vivo. J Virol 82:10998-11008. http://dx.doi.org/10.1128/JVI.01311-08.
16. Low A, Okeoma CM, Lovsin N, de las Heras M, Taylor TH, Peterlin BM, Ross SR, Fan H. 2009. Enhanced replication and pathogenesis of Moloney murine leukemia virus in mice defective in the murine APOBEC3 gene. Virology 385:455-463. http://dx.doi.org/10.1016/j.virol.2008.11.051.
17. Okeoma CM, Low A, Bailis W, Fan HY, Peterlin BM, Ross SR. 2009. Induction of APOBEC3 in vivo causes increased restriction of retrovirus infection. J Virol 83:3486-3495. http://dx.doi.org/10.1128/JVI.02347-08.
18. Okeoma CM, Petersen J, Ross SR. 2009. Expression of murine APOBEC3 alleles in different mouse strains and their effect on mouse mammary tumor virus infection. J Virol 83:3029-3038. http://dx.doi.org/10.1128/JVI.02536-08.
19. Chen H, Lilley CE, Yu Q, Lee DV, Chou J, Narvaiza I, Landau NR, Weitzman MD. 2006. APOBEC3A is a potent inhibitor of adenoassociated virus and retrotransposons. Curr Biol 16:480-485. http://dx.doi.org/10.1016/j.cub.2006.01.031.
20. Narvaiza I, Linfesty DC, Greener BN, Hakata Y, Pintel DJ, Logue E, Landau NR, Weitzman MD. 2009. Deaminase-independent inhibition of parvoviruses by the APOBEC3A cytidine deaminase. PLoS Pathog 5:e1000439. http://dx.doi.org/10.1371/journal.ppat.1000439.
21. Baumert TF, Rosler C, Malim MH, von Weizsacker F. 2007. Hepatitis B virus DNA is subject to extensive editing by the human deaminase APOBEC3C. Hepatology 46:682-689. http://dx.doi.org/10.1002/hep.21733.
22. Rosler C, Kock J, Kann M, Malim MH, Blum HE, Baumert TF, von Weizsacker F. 2005. APOBEC-mediated interference with hepadnavirus production. Hepatology 42:301-309. http://dx.doi.org/10.1002/hep.20801.
23. Suspene R, Guetard D, Henry M, Sommer P, Wain-Hobson S, Vartanian JP. 2005. Extensive editing of both hepatitis B virus DNA strands by APOBEC3 cytidine deaminases in vitro and in vivo. Proc Natl Acad Sci USA 102:8321-8326. http://dx.doi.org/10.1073/pnas.0408223102.
24. Song C, Sutton L, Johnson M, D'Aquila R, Donahue J. 2012. Signals in APOBEC3F N-terminal and C-terminal deaminase domains each contribute to encapsidation in HIV-1 virions and are both required for HIV-1 restriction. J Biol Chem 287:16965-16974. http://dx.doi.org/10.1074/jbc.M111.310839.
25. MacMillan AL, Kohli RM, Ross SR. 2013. APOBEC3 inhibition of mouse mammary tumor virus infection: the role of cytidine deamination versus inhibition of reverse transcription. J Virol 87:4808-4817. http://dx.doi.org/10.1128/JVI.00112-13.
26. Rulli SJ, Jr, Mirro J, Hill SA, Lloyd P, Gorelick RJ, Coffin JM, Derse D, Rein A. 2008. Interactions of murine APOBEC3 and human APOBEC3G with murine leukemia viruses. J Virol 82:6566-6575. http://dx.doi.org/10.1128/JVI.01357-07.
27. Zhang L, Li X, Ma J, Yu L, Jiang J, Cen S. 2008. The incorporation of APOBEC3 proteins into murine leukemia viruses. Virology 378:69-78. http://dx.doi.org/10.1016/j.virol.2008.05.006.
28. Aguiar RS, Lovsin N, Tanuri A, Peterlin BM. 2008. Vpr.A3A chimera inhibits HIV replication. J Biol Chem 283:2518-2525. http://dx.doi.org/10.1074/jbc.M706436200.
29. Goila-Gaur R, Khan M, Miyagi E, Kao S, Strebel K. 2007. Targeting APOBEC3A to the viral nucleoprotein complex confers antiviral activity. Retrovirology 4:61. http://dx.doi.org/10.1186/1742-4690-4-61.
30. Zheng YH, Irwin D, Kurosu T, Tokunaga K, Sata T, Peterlin BM. 2004. Human APOBEC3F is another host factor that blocks human immunodeficiency virus type 1 replication. J Virol 78:6073-6076. http://dx.doi.org/10.1128/JVI.78.11.6073-6076.2004.
31. Song C, Dubay SR, Hunter E. 2003. A tyrosine motif in the cytoplasmic domain of Mason-Pfizer monkey virus is essential for the incorporation of glycoprotein into virions. J Virol 77:5192-5200. http://dx.doi.org/10.1128/JVI.77.9.5192-5200.2003.
32. Holmes RK, Koning FA, Bishop KN, Malim MH. 2007. APOBEC3F can inhibit the accumulation of HIV-1 reverse transcription products in the absence of hypermutation. Comparisons with APOBEC3G. J Biol Chem 282:2587-2595. http://dx.doi.org/10.1074/jbc.M607298200.
33. Durocher Y, Perret S, Kamen A. 2002. High-level and high-throughput recombinant protein production by transient transfection of suspensiongrowing human 293-EBNA1 cells. Nucleic Acids Res 30:E9. http://dx.doi.org/10.1093/nar/30.2.e9.
34. Taylor HE, Khatua AK, Popik W. 2014. The innate immune factor apolipoprotein L1 restricts HIV-1 infection. J Virol 88:592-603. http://dx.doi.org/10.1128/JVI.02828-13.
35. Kotov A, Zhou J, Flicker P, Aiken C. 1999. Association of Nef with the human immunodeficiency virus type 1 core. J Virol 73:8824-8830.
36. Leaver-Fay A, Tyka M, Lewis SM, Lange OF, Thompson J, Jacak R, Kaufman K, Renfrew PD, Smith CA, Sheffler W, Davis IW, Cooper S, Treuille A, Mandell DJ, Richter F, Ban YE, Fleishman SJ, Corn JE, Kim DE, Lyskov S, Berrondo M, Mentzer S, Popovic Z, Havranek JJ, Karanicolas J, Das R, Meiler J, Kortemme T, Gray JJ, Kuhlman B, Baker D, Bradley P. 2011. ROSETTA3: an object-oriented software suite for the simulation and design of macromolecules. Methods Enzymol 487:545-574. http://dx.doi.org/10.1016/B978-0-12-381270-4.00019-6.
37. Li M, Shandilya SM, Carpenter MA, Rathore A, Brown WL, Perkins AL, Harki DA, Solberg J, Hook DJ, Pandey KK, Parniak MA, Johnson JR, Krogan NJ, Somasundaran M, Ali A, Schiffer CA, Harris RS. 2012. First-in-class small molecule inhibitors of the single-strand DNA cytosine deaminase APOBEC3G. ACS Chem Biol 7:506-517. http://dx.doi.org/10.1021/cb200440y.
38. Bohn M-F, Shandilya S, Albin J, Kouno T, Anderson B, McDougle R, Carpenter M, Rathore A, Evans L, Davis A, Zhang J, Lu Y, Somasundaran M, Matsuo H, Harris R, Schiffer C. 2013. Crystal structure of the DNA cytosine deaminase APOBEC3F: the catalytically active and HIV-1 Vif-binding domain. Structure 21:1042-1050. http://dx.doi.org/10.1016/j.str.2013.04.010.
39. Combs SA, Deluca SL, Deluca SH, Lemmon GH, Nannemann DP, Nguyen ED, Willis JR, Sheehan JH, Meiler J. 2013. Small-molecule ligand docking into comparative models with Rosetta. Nat Protoc 8:1277-1298. http://dx.doi.org/10.1038/nprot.2013.074.
40. Shandilya SM, Nalam MN, Nalivaika EA, Gross PJ, Valesano JC, Shindo K, Li M, Munson M, Royer WE, Harjes E, Kono T, Matsuo H, Harris RS, Somasundaran M, Schiffer CA. 2010. Crystal structure of the APOBEC3G catalytic domain reveals potential oligomerization interfaces. Structure 18:28-38. http://dx.doi.org/10.1016/j.str.2009.10.016.
41. Shlyakhtenko L, Lushnikov A, Miyagi A, Li M, Harris R, Lyubchenko Y. 2012. Nanoscale structure and dynamics of ABOBEC3G complexes with single-stranded DNA. Biochemistry 51:6432-6440. http://dx.doi.org/10.1021/bi300733d.
42. Chen KM, Harjes E, Gross PJ, Fahmy A, Lu Y, Shindo K, Harris RS, Matsuo H. 2008. Structure of the DNA deaminase domain of the HIV-1 restriction factor APOBEC3G. Nature 452:116-119. http://dx.doi.org/10.1038/nature06638.
43. Burdick RC, Hu WS, Pathak VK. 2013. Nuclear import of APOBEC3Flabeled HIV-1 preintegration complexes. Proc Natl Acad Sci USA 110: E4780-E4789. http://dx.doi.org/10.1073/pnas.1315996110.
44. Hache G, Liddament MT, Harris RS. 2005. The retroviral hypermutation specificity of APOBEC3F and APOBEC3G is governed by the C-terminal DNA cytosine deaminase domain. J Biol Chem 280:10920-10924. http://dx.doi.org/10.1074/jbc.M500382200.
45. Wang T, Tian C, Zhang W, Sarkis PT, Yu XF. 2008. Interaction with 7SL RNA but not with HIV-1 genomic RNA or P bodies is required for APOBEC3F virion packaging. J Mol Biol 375:1098-1112. http://dx.doi.org/10.1016/j.jmb.2007.11.017.
46. Sanchez-Martinez S, Aloia AL, Harvin D, Mirro J, Gorelick RJ, Jern P, Coffin JM, Rein A. 2012. Studies on the restriction of murine leukemia viruses by mouse APOBEC3. PLoS One 7:e38190. http://dx.doi.org/10.1371/journal.pone.0038190.
47. Ara A, Love RP, Chelico L. 2014. Different mutagenic potential of HIV-1 restriction factors APOBEC3G and APOBEC3F is determined by distinct single-stranded DNA scanning mechanisms. PLoS Pathog 10:e1004024. http://dx.doi.org/10.1371/journal.ppat.1004024.
48. Zennou V, Bieniasz PD. 2006. Comparative analysis of the antiretroviral activity of APOBEC3G and APOBEC3F from primates. Virology 349:31-40. http://dx.doi.org/10.1016/j.virol.2005.12.035.
49. Haché G, Shindo K, Albin J, Harris R. 2008. Evolution of HIV-1 isolates that use a novel Vif-independent mechanism to resist restriction by human APOBEC3G. Curr Biol 18:819-824. http://dx.doi.org/10.1016/j.cub.2008.04.073.
50. Hache G, Abbink TE, Berkhout B, Harris RS. 2009. Optimal translation initiation enables Vif-deficient human immunodeficiency virus type 1 to escape restriction by APOBEC3G. J Virol 83:5956-5960. http://dx.doi.org/10.1128/JVI.00045-09.
51. Nguyen DH, Gummuluru S, Hu J. 2007. Deamination-independent inhibition of hepatitis B virus reverse transcription by APOBEC3G. J Virol 81:4465-4472. http://dx.doi.org/10.1128/JVI.02510-06.
52. Li D, Liu J, Kang F, Guan W, Gao X, Wang Y, Sun D. 2011. Core-APOBEC3C chimerical protein inhibits hepatitis B virus replication. J Biochem 150:371-374. http://dx.doi.org/10.1093/jb/mvr086.
53. Turelli P, Mangeat B, Jost S, Vianin S, Trono D. 2004. Inhibition of hepatitis B virus replication by APOBEC3G. Science 303:1829. http://dx.doi.org/10.1126/science.1092066.
54. Rosler C, Kock J, Malim MH, Blum HE, von Weizsacker F. 2004. Comment on "Inhibition of hepatitis B virus replication by APOBEC3G." Science 305:1403. (Reply.) http://dx.doi.org/10.1126/science.1100464.
55. Noguchi C, Hiraga N, Mori N, Tsuge M, Imamura M, Takahashi S, Fujimoto Y, Ochi H, Abe H, Maekawa T, Yatsuji H, Shirakawa K, Takaori-Kondo A, Chayama K. 2007. Dual effect of APOBEC3G on hepatitis B virus. J Gen Virol 88:432-440. http://dx.doi.org/10.1099/vir.0.82319-0.