Lentivirus restriction by diverse primate APOBEC3A proteins

Virology

Volumn 442, Issue 1, 2013, Pages 82-96

  Schmitt, Kimberly ^a   Guo, Kejun ^b   Katuwal, Miki ^a   Wilson, Darayu ^a   Prochnow, Courtney ^c   Bransteitter, Ronda ^c   Chen, Xiaojiang S ^c   Santiago, Mario L ^b   Stephens, Edward B ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

APOBEC3A; HIV 1; Human immunodeficiency virus type 1; Pathogenesis; SHIV primates; Simian immunodeficiency virus; Virus restriction

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE LIKE 3A; CYTIDINE DEAMINASE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HAPLORHINI; LENTIVIRINAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SEQUENCE ANALYSIS; VIRUS INHIBITION; VIRUS REPLICATION; WILD TYPE;

ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; CYTIDINE DEAMINASE; HIV INFECTIONS; HIV-1; HUMANS; LENTIVIRUS; MACACA MULATTA; PRIMATES; PROTEINS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS REPLICATION;

AOTUS TRIVIRGATUS; CERCOPITHECIDAE; CERCOPITHECUS AETHIOPS; COLOBUS; COLOBUS SP.; HOMINIDAE; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HYLOBATIDAE; LENTIVIRUS; MACACA MULATTA; PLATYRRHINI; PRIMATES; SAIMIRI; SIMIAN IMMUNODEFICIENCY VIRUS; SIMIAN-HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84878947111     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.04.002     Document Type: Article

References (73)

1. Aguiar R.S., Lovsin N., Tanuri A., Peterlin B.M. Vpr.A3A chimera inhibits HIV replication. J. Biol. Chem. 2008, 283:2518-2525.
2. Alke A., Schwantes A., Kido K., Flotenmeyer M., Flügel R.M., Löchelt M. Thebet gene of feline foamy virus is required for virus replication. Virology 2001, 287:310-320.
3. Babushok D.V., Kazazian H.H. Progress in understanding the biology of the human mutagen LINE-1. Hum. Mutat. 2007, 28:527-539.
4. Bailes E., Gao F., Bibollet-Ruche F., Courgnaud V., Peeters M., Marx P.A., Hahn B.H., Sharp P.M. Hybrid origin of SIV in chimpanzees. Science 2003, 300:1713.
5. Bishop K.N., Holmes R.K., Sheehy A.M., Davidson N.O., Cho S.J., Malim M.H. Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr. Biol. 2004, 14:1392-1406.
6. Bogerd H.P., Wiegand H.L., Doehle B.P., Lueders K.K., Cullen B.R. APOBEC3A and APOBEC3B are potent inhibitors of LTR-retrotransposon function in human cells. Nucleic Acids Res. 2006, 34:89-95.
7. Bogerd H.P., Wiegand H.L., Hulme A.E., Garcia-Perez J.L., O'Shea K.S., Moran J.V., Cullen B.R. Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc. Nat. Acad. Sci. U.S.A. 2006, 103:8780-8785.
8. Bourara K., Liegler T.J., Grant R.M. Target cell APOBEC3C can induce limited G-to-A mutation in HIV-1. PLoS Pathog. 2007, 3:1477-1485.
9. Brouha B., Schustak J., Badge R.M., Lutz-Prigge S., Farley A.H., Moran J.V., Kazazian H.H. Hot L1s account for the bulk of retrotransposition in the human population. Proc. Nat. Acad. Sci. U.S.A. 2003, 100:5280-5285.
10. Bulliard T., Narvaiza I., Bertero A., Peddi S., Röhrig U.F., Oritz M., Zoete V., Castro-Diaz N., Turelli P., Telenti A., Michielin O., Weitzman M.D., Trono D. Structure-function analyses point to a polynucleotide-accommodating groove essential for APOBEC3A restriction activities. J. Virol. 2011, 85:1765-1776.
11. Chareza S., Dragana Slavkovic D., Liu Y., Räthe A.M., Münk C., Zabogli E., Pistello M., Löchelt M. Molecular and functional interactions of cat APOBEC3 and feline foam and immunodeficiency virus proteins: different ways to counteract host-encoded restriction. Virology 2012, 424:138-146.
12. Chelico L., Pham P., Calabrese P., Goodman M.F. APOBEC3G DNA deaminase acts processively 3'-5' on single stranded DNA. Nat. Struct. Mol. Bio. 2006, 13:392-399.
13. Chen H., Lilley C.E., Yu Q., Lee D.V., Chou J., Narvaiza I., Landau N.R., Weitzman M.D. APOBEC3A is a potent inhibitor of adeno-associated virus and retrotransposons. Curr. Biol. 2006, 16:480-485.
14. Chiu Y.L., Greene W.C. APOBEC3G: an intracellular centurion. Philos. Trans. R. Soc. London, B. Biol. Sci 2009, 364:689-703.
15. Compton A.A., 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.
16. Courgnaud V., Pourrut X., Bibollet-Ruche F., Mpoudi-Ngole E., Bourgeois A., Delaporte E., Peeters M. Characterization of a novel simian immunodeficiency virus from guereza colobus monkeys (Colobus guereza) in Cameroon: a new lineage in the nonhuman primate lentivirus family. J. Virol. 2001, 75:857-866.
17. Dang Y., Wang X., Esselman W.J., Zheng Y.-H. Identification of APOBEC3DE as another antiretroviral factor from the human APOBEC family. J. Virol. 2007, 80:10522-10533.
18. Derdeyn C.A., Decker J.M., Sfakianos J.N., Wu X., O'Brien W.A., Ratner L., Kappes J.C., Shaw G.M., Hunter E. Sensitivity of human immunodeficiency virus type 1 to the fusion inhibitor T-20 is modulated by coreceptor specificity defined by the V3 loop of gp120. J. Virol. 2000, 74:8358-8367.
19. Doehle B.P., Schafer A., Cullen B.R. Human APOBEC3B is a potent inhibitor of HIV-1 infectivity and is resistant to HIV-1 Vif. Virology 2005, 339:281-288.
20. Goila-Gaur R., Khan M.A., Miyagi E., Kao S., Strebel K. Targeting APOBEC3A to the viral nucleoprotein complex confers antiviral activity. Retrovirology 2007, 4:61.
21. Harari A., Ooms M., Mulder L.C., Simon V. Polymorphisms and splice variants influence the antiretroviral activity of human APOBEC3H. J. Virol. 2009, 83:295-303.
22. Heneine W., SChweizer M., Sandstrom P., Folks T. Human infection with foamy viruses. Curr. Top. Microbiol. Immunol. 2003, 277:181-196.
23. Holden L.G., Prochnow C., Chang Y.P., Bransteitter R., Chelico L., Sen U., Stevens R.C., Goodman M.F., Chen X.S. Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications. Nature 2008, 456:121-124.
24. Hultquist J.F., Lengyel J.A., Refsland E.W., LaRue R.S., Lackey L., Brown W.L., Harris R.S. Human and rhesus APOBEC3D, APOBEC3F, APOBEC3G, and APOBEC3H demonstrate a conserved capacity to restrict Vif-deficient HIV-1. J. Virol. 2011, 85:11220-11234.
25. Hussain A.I., Shanmugam V., Bhullar V.B., Beer B.E., Vallet D., Gautier-Hion A., Wolfe N.D., Karesh W.B., Kilbourn A.M., Tooze Z., Heneine W., Virology Switzer W.M. Screening for simian foamy virus infection by using a combined antigen Western blot assay: evidence for a wide distribution among Old World primates and identification of four new divergent viruses. Virology 2003, 309:248-257.
26. Jäger S., Kim D.Y., Hultquist J.F., Shindo K., LaRue R.S., Kwon E., Li M., Anderson B.D., Yen L., Stanley D., Mahon C., Kane J., Franks-Skiba K., Cimermancic P., Burlingame A., Sali A., Craik C.S., Harris R.S., Gross J.D., Krogan N.J. Vif hijacks CBF-β to degrade APOBEC3G and promote HIV-1 infection. Nature 2011, 481:371-375.
27. 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, 79:285-296.
28. Kahn A.S. Simian foamy virus infection in humans: prevalence and management. Expert Rev. Anti Infect. Ther. 2009, 7:569-580.
29. Kitamura S., Ode H., Nakashima M., Imahashi M., Naganawa Y., Kurosawa T., Yokomaku Y., Yamane T., Watanabe N., Suzuki A., Sugiura W., Iwatani Y. The APOBEC3C crystal structure and the interface for HIV-1 Vif binding. Nat. Struct. Mol. Biol. 2010, 19:1005-1010.
30. Landry S., Narvaiza I., Linfesty D.C., Weitzman M.D. APOBEC3A can activate the DNA damage response and cause cell-cycle arrest. EMBO Rep. 2011, 12:444-455.
31. Langlois M.A., Beale R.C., Conticello S.G., Neuberger M.S. Mutational comparison of the single-domained APOBEC3C and double-domained APOBEC3F/G anti-retroviral cytidine deaminases provides insight into their DNA target site specificities. Nucleic Acids Res. 2005, 33:1913-1923.
32. Leendertz F.H., Zirkel F., Couacy-Hymann E., Ellerbrok H., Morozov V.A., Pauli G., Hedemann C., Formenty P., Jensen S.A., Boesch C., Junglen S. Interspecies transmission of simian foamy virus in a natural predator-prey system. J. Virol. 2008, 82:7741-7744.
33. Li M.M., Wu L.I., Emerman M. The range of human APOBEC3H sensitivity to lentiviral Vif proteins. J. Virol. 2010, 84:88-95.
34. Liu B., Yu X., Luo K., Yu Y., Yu X.F. Influence of primate lentiviral Vif and proteasome inhibitors on human immunodeficiency virus type 1 virion packaging of APOBEC3G. J. Virol. 2004, 78:2072-2081.
35. Liu Z.Q., Muhkerjee S., Sahni M., McCormick-Davis C., Leung K., Li Z., Gattone V.H., Tian C., Doms R.W., Hoffman T.L., Raghavan R., Narayan O., Stephens E.B. Derivation and biological characterization of a molecular clone of SHIV(KU-2) that causes AIDS, neurological disease, and renal disease in rhesus macaques. Virology 1999, 260:295-307.
36. Löchlet M., Romen F., Bastone P., Muckenfuss H., Kirchner N., Kim Y.B., Truyen U., Rosler U., Battenburg M., Saib A., Flory E., Cichutek K., Munk C. The antiretroviral activity of APOBEC3 is inhibited by the foamy virus accessory Bet protein. Proc. Nat. Acad. Sci. U.S.A. 2005, 102:7982-7987.
37. MacGinnitie A.J., Anant S., Davidson N.O. Mutagenesis of apobec-1, the catalytic subunit of the mammalian apolipoprotein B mRNA editing enzyme, reveals distinct domains that mediate cytosine nucleoside deaminase, RNA binding, and RNA editing activity. J. Biol. Chem. 1995, 270:14768-14775.
38. Marin M., Rose K.M., Kozak S.L., Kabat D. HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat. Med. 2003, 9:1398-1403.
39. Mehle A., Strack B., Ancuta P., Zhang C., McPike M., Gabuzda D. Vif overcomes the innate antiviral activity of APOBEC3G by promoting its degradation in the ubiquitin-proteasome pathway. J. Biol. Chem. 2004, 279:7792-7798.
40. Meiering C.D., Linial M.L. Historical perspective of foamy virus epidemiology and infection. Clin. Microbiol. Rev. 2001, 14:165-176.
41. Muckenfuss H., Hamdorf M., Held U., Perkovic M., Lower J., Cichutek K., Flory E., Schumann G.G., Munk C. APOBEC3 proteins inhibit human LINE-1 retrotransposition. J. Biol. Chem. 2006, 281:22161-22172.
42. Narvaiza I., Linfesty D.C., Greener B.N., Hakata Y., Pintel D.J., Logue E., Landau N.R., Weitzman M.D. Deaminase-independent inhibition of parvoviruses by the APOBEC3A cytidine deaminase. PLoS Pathog. 2009, 5:e1000439.
43. OhAinle M., Kerns J.A., Li M.M., Malik H.S., Emerman M. Antiretroelement activity of APOBEC3H was lost twice in recent human evolution. Cell Host Microbe 2008, 11:249-259.
44. Ooms M., Majdak S., Seibert C.W., Harari A., Simon V. The localization of APOBEC3H variants in HIV-1 virions determines their antiviral activity. J. Virol. 2010, 84:7961-7969.
45. Ooms M., Krikoni A., Kress A.K., Simon V., Münk C. APOBEC3A, APOBEC3B, and APOBEC3H haplotype 2 restrict human T-lymphotropic virus type 1. J. Virol. 2012, 86:6097-6108.
46. Rethwilm A. Foamy viruses. Topley & Wilson's Microbiology and Microbial Infections-Virology 2005, 1304-1321. Hodder Arnold, London, (Eds.). 10th edn. B.W.J. Mahy, V. ter Meulen (Eds.).
47. Rethwilm A. Foamy virus vectors: an awaited alternative to gamma retro- and lentiviral vectors. Curr. Gene Ther. 2007, 7:261-271.
48. Russell R.A., Wiegand H.L., Moore M.D., Schafer A., McClure M.O., Cullen B.R. Foamy viruse Bet proteins function as novel inhibitors of the APOBEC3 family of innate antiretroviral defense factors. J. Virol. 2005, 79:8724-8731.
49. Saib A., Koken M.H., van der Spek P., Peries J., de The H. Involvement of a spliced and defective human foamy virus in the establishment of chronic infection. J. Virol. 1995, 69:5261-5268.
50. Santiago M.L., Rodenburg C.M., Kamenya S., Bibollet-Ruche F., Gao F., Bailes E., Meleth S., Soong S.J., Kilby J.M., Moldoveanu Z., Fahey B., Muller M.N., Ayouba A., Nerrienet E., McClure H.M., Heeney J.L., Pusey A.E., Collins D.A., Boesch C., Wrangham R.W., Goodall J., Sharp P.M., Shaw G.M., Hahn B.H. SIVcpz in wild chimpanzees. Science 2002, 295:465.
51. Schmitt K., Hill M.S., Ruiz A., Culley N., Pinson D.M., Wong S.W., Stephens E.B. Mutations in the highly conserved SLQXLA motif of Vif results in a simian-human immunodeficiency virus results in less pathogenic virus and is associated with G to A mutations in the viral genome. Virology 2009, 383:62-72.
52. Schmitt K., Liu Q., Hill M.S., Ruiz A., Culley N., Pinson D.M., Wong S.W., Stephens E.B. Comparison of the pathogenicity of simian-human immunodeficiency viruses expressing Vif proteins with mutation of the SLQYLA and HCCH domains in macaques. Virology 2010, 404:87-203.
53. Schmitt K., Guo K., Algaier M., Ruiz A., Cheng F., Qiu J., Wissing S., Santiago M.L., Stephens E.B. Differential virus restriction patterns of rhesus macaque and human APOBEC3A: implications for lentivirus evolution. Virology 2011, 419:24-42.
54. Schrago C.G. On the time scale of New World primate diversification. Am. J. Phys. Anthropol. 2007, 132:344-354.
55. Schrago C.G., Russo C.A. Timing the origin of New World monkeys. Mol. Biol. Evol. 2003, 20:1620-1625.
56. Schwantes A., Truyen U., Weikel J., Weiss C., Löchelt M. Application of chimeric feline foamy virus-based retroviral vectors for the induction of antiviral immunity in cats. J. Virol. 2003, 77:7830-7842.
57. Sheehy A.M., Gaddis N.C., Choi J.D., Malim M.H. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 2002, 418:646-650.
58. Sheehy A.M., Gaddis N.C., Malim M.H. The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat. Med. 2003, 9:1404-1407.
59. Smith J., Pathak V. Identification of specific determinants of human APOBEC3F, APOBEC3C, and APOBEC3DE and African green monkey APOBEC3F that interact with HIV-1 Vif. J. Virol. 2010, 84:12599-12608.
60. Stenglein M.D., Burns M.B., Li M., Lengyel J., Harris R.S. APOBEC3 proteins mediate the clearance of foreign DNA from human cells. Nat. Struct. Mol. Biol 2010, 17:222-229.
61. Switzer W.M., Bhullar V., Shanmugam V., Cong M.E., Parekh B., Lerche N.W., Yee J.L., Ely J.J., Boneva R., Chapman L.E., Folks T.M., Heneine W. Frequent simian foamy virus infection in persons occupationally exposed to nonhuman primates. J. Virol. 2004, 78:2780-2789.
62. Switzer W.M., Salemi M., Shanmugam V., Gao F., Cong M.E., Kuiken C., Bhullar V., Beer B.E., Vallet D., Gautier-Hion A., Tooze Z., Villinger F., Holmes E.C., Heneine W. Ancient co-speciation of simian foamy viruses and primates. Nature 2005, 434:376-380.
63. Thielen B.K., McNevin J.P., McElrath M.J., Hunt B.V., Klein K.C., Lingappa J.R. Innate immune signaling induces high levels of TC-specific deaminase activity in primary monocyte-derived cells through expression of APOBEC3A isoforms. J. Biol. Chem. 2010, 285:27753-27766.
64. Trobridge G.D. Foamy virus vectors for gene transfer. Expert Opin. Biol. Ther. 2009, 9:1427-1436.
65. Van Heuverswyn F., Li Y., Neel C., Bailes E., Keele B.F., Liu W., Loul S., Butel C., Liegeois F., Bienvenue Y., Ngolle E.M., Sharp P.M., Shaw G.M., Delaporte E., Hahn B.H., Peeters M. Human immunodeficiency viruses: SIV infection in wild gorillas. Nature 2006, 444:164.
66. Virgen C.A., Hatziioannou T. Antiretroviral activity and vif sensitivity of rhesus macaque APOBEC3 proteins. J. Virol. 2007, 81:13932-13937.
67. Wang T., Zhang W., Tian C., Liu B., Yu Y., Ding L., Spearman P., Yu X.F. Distinct viral determinants for the packaging of human cytidine deaminases APOBEC3G and APOBEC3C. Virology 2008, 377:71-79.
68. Wang X., Abudu A., Son S., Dang Y., Venta P.J., Zheng Y.H. Analysis of human APOBEC3H haplotypes and anti-human immunodeficiency virus type-1 activity. J. Virol. 2011, 85:3142-3152.
69. Wei X., Decker J.M., Liu H., Zhang Z., Arani R.B., Kilby J.M., Saag M.S., Wu X., Shaw G.M., Kappes J.C. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob. Agents Chemother. 2002, 46:1896-1905.
70. Wiegand H.L., Doehle B.P., Bogerd H.P., Cullen B.R. A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins. EMBO J. 2004, 23:2451-2458.
71. Yu X., Yu Y., Liu B., Luo K., Kong W., Mao P., Yu X.F. Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 2003, 302:1056-1060.
72. Yu Q., Konig R., Pillai S., Chiles K., Kearney M., Palmer S., Richman D., Coffin J.M., Landau N.R. Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat. Struct. Mol. Biol. 2004, 11:435-442.
73. Zhang W., Du J., Evans S.L., Yu Y., Yu X.F. T-cell differentiation factor CBF-β regulates HIV-1 Vif-mediated evasion of host restriction. Nature 2011, 481:376-379.