Promiscuous RNA Binding Ensures Effective Encapsidation of APOBEC3 Proteins by HIV-1

PLoS Pathogens

Volumn 11, Issue 1, 2015, Pages 1-22

  Apolonia, Luis ^a   Schulz, Reiner ^a   Curk, Tomaž ^b   Rocha, Paula ^c   Swanson, Chad M ^a   Schaller, Torsten ^a,f   Ule, Jernej ^d,e   Malim, Michael H ^d  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B MRNA EDITING ENZYME CATALYTIC POLYPEPTIDE LIKE 3 PROTEIN; APOLIPOPROTEIN B MRNA EDITING ENZYME CATALYTIC POLYPEPTIDE LIKE 3 PROTEIN F; APOLIPOPROTEIN B MRNA EDITING ENZYME CATALYTIC POLYPEPTIDE LIKE 3 PROTEIN G; CYTIDINE DEAMINASE; MESSENGER RNA; SMALL UNTRANSLATED RNA; UNCLASSIFIED DRUG; 7SL RNA; APOBEC3 PROTEIN, HUMAN; APOBEC3F PROTEIN, HUMAN; APOBEC3G PROTEIN, HUMAN; AUTOANTIGEN; CYTOSINE DEAMINASE; PROTEIN BINDING; RIBONUCLEOPROTEIN; SIGNAL RECOGNITION PARTICLE; SMALL CYTOPLASMIC RNA; TROVE2 PROTEIN, HUMAN;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; AUTORADIOGRAPHY; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CONTROLLED STUDY; ENCAPSIDATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOPRECIPITATION; OPEN READING FRAME; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION; RNA BINDING; VIRION; VIRUS NUCLEOCAPSID; VIRUS PARTICLE; CELL CULTURE; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PHYSIOLOGY; VIRUS ASSEMBLY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

AUTOANTIGENS; CELLS, CULTURED; CYTIDINE DEAMINASE; CYTOSINE DEAMINASE; HEK293 CELLS; HELA CELLS; HIV-1; HUMANS; PROTEIN BINDING; RIBONUCLEOPROTEINS; RNA, SMALL CYTOPLASMIC; RNA, SMALL UNTRANSLATED; SIGNAL RECOGNITION PARTICLE; VIRUS ASSEMBLY;

EID: 84923839045     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004609     Document Type: Article

References (69)

1. Holmes RK, Malim MH, Bishop KN, (2007) APOBEC-mediated viral restriction: not simply editing? Trends Biochem Sci 32: 118–128. 17303427
2. Desimmie B a, Delviks-Frankenberrry K a, Burdick RC, Qi D, Izumi T, et al. (2013) Multiple APOBEC3 Restriction Factors for HIV-1 and One Vif to Rule Them All. J Mol Biol: 1–26.
3. LaRue RS, Andrésdóttir V, Blanchard Y, Conticello SG, Derse D, et al. (2009) Guidelines for naming nonprimate APOBEC3 genes and proteins. J Virol 83: 494–497. doi: 10.1128/JVI.01976-08 18987154
4. Sheehy AM, Gaddis NC, Choi JD, Malim MH, (2002) Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418: 4–8. 12167863
5. Mangeat B, Turelli P, Caron G, Friedli M, Perrin L, et al. (2003) Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424: 99–103. 12808466
6. Gaddis NC, Sheehy AM, Ahmad KM, Swanson M, Bishop KN, et al. (2004) Further Investigation of Simian Immunodeficiency Virus Vif Function in Human Cells. J Virol 78: 12041–12046. 15479843
7. Harris RS, Bishop KN, Sheehy AM, Craig HM, Petersen-mahrt SK, et al. (2003) DNA deamination mediates innate immunity to retroviral infection. Cell 113: 803–809. 12809610
8. Okeoma CM, Lovsin N, Peterlin BM, Ross SR, (2007) APOBEC3 inhibits mouse mammary tumour virus replication in vivo. Nature 445: 927–930. 17259974
9. Turelli P, Mangeat B, Jost S, Vianin S, Trono D, (2004) Inhibition of hepatitis B virus replication by APOBEC3G. Science 303: 1829.
10. Narvaiza I, Linfesty DC, Greener BN, Hakata Y, Pintel DJ, et al. (2009) Deaminase-independent inhibition of parvoviruses by the APOBEC3A cytidine deaminase. PLoS Pathog 5: e1000439. doi: 10.1371/journal.ppat.1000439 19461882
11. Esnault C, Heidmann O, Delebecque F, Dewannieux M, Ribet D, et al. (2005) APOBEC3G cytidine deaminase inhibits retrotransposition of endogenous retroviruses. Nature 433: 430–433. 15674295
12. Marin M, Rose KM, Kozak SL, Kabat D, (2003) HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat Med 9: 1398–1403. 14528301
13. Yu X, Yu Y, Liu B, Luo K, Kong W, et al. (2003) Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302: 1056–1060. 14564014
14. Sheehy AM, Gaddis NC, Malim MH, (2003) The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat Med 9: 1404–1407. 14528300
15. Guo Y, Dong L, Qiu X, Wang Y, Zhang B, et al. (2014) Structural basis for hijacking CBF-β and CUL5 E3 ligase complex by HIV-1 Vif. Nature 505: 229–233. doi: 10.1038/nature12884 24402281
16. Zhang H, Yang B, Pomerantz RJ, Zhang C, Arunachalam SC, et al. (2003) The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424: 94–98. 12808465
17. Bishop KN, Verma M, Kim E-Y, Wolinsky SM, Malim MH, (2008) APOBEC3G inhibits elongation of HIV-1 reverse transcripts. PLoS Pathog 4: e1000231. 19057663
18. Iwatani Y, Chan DSB, Wang F, Maynard KS, Sugiura W, et al. (2007) Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G. Nucleic Acids Res 35: 7096–7108. 17942420
19. Gillick K, Pollpeter D, Phalora P, Kim E-Y, Wolinsky SM, et al. (2013) Suppression of HIV-1 infection by APOBEC3 proteins in primary human CD4(+) T cells is associated with inhibition of processive reverse transcription as well as excessive cytidine deamination. J Virol 87: 1508–1517. doi: 10.1128/JVI.02587-12 23152537
20. Navarro F, Bollman B, Chen H, König R, Yu Q, et al. (2005) Complementary function of the two catalytic domains of APOBEC3G. Virology 333: 374–386. 15721369
21. Iwatani Y, Takeuchi H, Strebel K, Levin JG, (2006) Biochemical activities of highly purified, catalytically active human APOBEC3G: correlation with antiviral effect. J Virol 80: 5992–6002. 16731938
22. Huthoff H, Autore F, Gallois-Montbrun S, Fraternali F, Malim MH, (2009) RNA-dependent oligomerization of APOBEC3G is required for restriction of HIV-1. PLoS Pathog 5: e1000330. 19266078
23. Chiu Y-L, Soros VB, Kreisberg JF, Stopak K, Yonemoto W, et al. (2005) Cellular APOBEC3G restricts HIV-1 infection in resting CD4+ T cells. Nature 435: 108–114. 15829920
24. Kozak SL, Marin M, Rose KM, Bystrom C, Kabat D, (2006) The anti-HIV-1 editing enzyme APOBEC3G binds HIV-1 RNA and messenger RNAs that shuttle between polysomes and stress granules. J Biol Chem 281: 29105–29119. 16887808
25. Wichroski MJ, Robb GB, Rana TM, (2006) Human retroviral host restriction factors APOBEC3G and APOBEC3F localize to mRNA processing bodies. PLoS Pathog 2: e41. 16699599
26. Gallois-Montbrun S, Kramer B, Swanson CM, Byers H, Lynham S, et al. (2007) Antiviral protein APOBEC3G localizes to ribonucleoprotein complexes found in P bodies and stress granules. J Virol 81: 2165–2178. 17166910
27. Phalora PK, Sherer NM, Wolinsky SM, Swanson CM, Malim MH, (2012) HIV-1 replication and APOBEC3 antiviral activity are not regulated by P bodies. J Virol 86: 11712–11724. 22915799
28. Izumi T, Burdick R, Shigemi M, Plisov S, Hu W-S, et al. (2013) Mov10 and APOBEC3G localization to processing bodies is not required for virion incorporation and antiviral activity. J Virol 87: 11047–11062. doi: 10.1128/JVI.02070-13 23926332
29. Soros VB, Yonemoto W, Greene WC, (2007) Newly synthesized APOBEC3G is incorporated into HIV virions, inhibited by HIV RNA, and subsequently activated by RNase H. PLoS Pathog 3: e15. 17291161
30. Luo K, Liu B, Xiao Z, Yu Y, Gorelick R, et al. (2004) Amino-Terminal Region of the Human Immunodeficiency Virus Type 1 Nucleocapsid Is Required for Human APOBEC3G Packaging. J Virol 78: 11841–11852. 15479826
31. Schäfer A, Bogerd HP, Cullen BR, (2004) Specific packaging of APOBEC3G into HIV-1 virions is mediated by the nucleocapsid domain of the gag polyprotein precursor. Virology 328: 163–168. 15464836
32. Svarovskaia ES, Xu H, Mbisa JL, Barr R, Gorelick RJ, et al. (2004) Human apolipoprotein B mRNA-editing enzyme-catalytic polypeptide-like 3G (APOBEC3G) is incorporated into HIV-1 virions through interactions with viral and nonviral RNAs. J Biol Chem 279: 35822–35828. 15210704
33. Zennou V, Perez-caballero D, Bieniasz PD, (2004) APOBEC3G Incorporation into Human Immunodeficiency Virus Type 1 Particles. J Virol 78: 12058–12061. 15479846
34. Khan MA, Kao S, Miyagi E, Goila-gaur R, Opi S, et al. (2005) Viral RNA Is Required for the Association of APOBEC3G with Human Immunodeficiency Virus Type 1 Nucleoprotein Complexes. J Virol 79: 5870–5874. 15827203
35. Wang T, Tian C, Zhang W, Luo K, Sarkis PTN, et al. (2007) 7SL RNA mediates virion packaging of the antiviral cytidine deaminase APOBEC3G. J Virol 81: 13112–13124. 17881443
36. Chiu Y, Witkowska HE, Hall SC, Santiago M, Soros VB, et al. (2006) High-molecular-mass APOBEC3G complexes restrict Alu retrotransposition. Proc Natl Acad Sci USA 103: 15588–15593. 17030807
37. Berkowitz R, Fisher J, Goff SP, (1996) RNA Packaging. In: Kräusslich H-G, editor. Morphogenesis and Maturation of Retroviruses SE - 6. Springer Berlin Heidelberg, Vol. 214. pp. 177–218.
38. Ule J, Jensen KB, Ruggiu M, Mele A, Ule A, et al. (2003) CLIP identifies Nova-regulated RNA networks in the brain. Science 302: 1212–1215. 14615540
39. König J, Zarnack K, Rot G, Curk T, Kayikci M, et al. (2010) iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat Struct Mol Biol 17: 909–915.
40. Chi SW, Zang JB, Mele A, Darnell RB, (2009) Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460: 479–486. doi: 10.1038/nature08170 19536157
41. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25. doi: 10.1186/gb-2009-10-3-r25 19261174
42. Smit Afa Green (n.d.) Repeat Masker. Available: http://repeatmasker.org.
43. Zufferey R, Nagy D, Mandel R, Naldini L, Trono D, (1997) Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 15: 871–875. 9306402
44. Demaison C, Parsley K, Brouns G, Scherr M, Battmer K, et al. (2002) High-level transduction and gene expression in hematopoietic repopulating cells using a human immunodeficiency virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter. Hum Gene Ther 13: 803–813. 11975847
45. Accola MA, Strack B, Göttlinger HG, (2000) Efficient Particle Production by Minimal Gag Constructs Which Retain the Carboxy-Terminal Domain of Human Immunodeficiency Virus Type 1 Capsid-p2 and a Late Assembly Domain. J Virol 74: 5395–5402. 10823843
46. Luban J, Goff SP, (1994) Mutational Analysis of cis-Acting Packaging Signals in Human Immunodeficiency Virus Type 1 RNA. J Virol 68: 3784–3793. 8189516
47. Onafuwa-Nuga A a, Telesnitsky A, King SR, (2006) 7SL RNA, but not the 54-kd signal recognition particle protein, is an abundant component of both infectious HIV-1 and minimal virus-like particles. RNA 12: 542–546. 16489186
48. Khan M a, Goila-Gaur R, Opi S, Miyagi E, Takeuchi H, et al. (2007) Analysis of the contribution of cellular and viral RNA to the packaging of APOBEC3G into HIV-1 virions. Retrovirology 4: 48. 17631688
49. Onafuwa-nuga AA, King SR, Telesnitsky A, (2005) Nonrandom Packaging of Host RNAs in Moloney Murine Leukemia Virus. J Virol 79: 13528–13537. 16227273
50. Gallois-Montbrun S, Holmes RK, Swanson CM, Fernández-Ocaña M, Byers HL, et al. (2008) Comparison of cellular ribonucleoprotein complexes associated with the APOBEC3F and APOBEC3G antiviral proteins. J Virol 82: 5636–5642. doi: 10.1128/JVI.00287-08 18367521
51. Bach D, Peddi S, Mangeat B, Lakkaraju A, Strub K, et al. (2008) Characterization of APOBEC3G binding to 7SL RNA. Retrovirology 5: 54. doi: 10.1186/1742-4690-5-54 18597676
52. Sherer NM, Lehmann MJ, Jimenez-Soto LF, Ingmundson A, Horner SM, et al. (2003) Visualization of retroviral replication in living cells reveals budding into multivesicular bodies. Traffic 4: 785–801. 14617360
53. Müller B, Daecke J, Fackler OT, Dittmar T, Zentgraf H, et al. (2004) Construction and Characterization of a Fluorescently Labeled Infectious Human Immunodeficiency Virus Type 1 Derivative. J Virol 78: 10803–10813.
54. Lerner MR, Boyle JA, Hardin JA, Steitz JA, Science S, et al. (1981) Two Novel Classes of Small Ribonucleoproteins Detected by Antibodies Associated with Lupus Erythematosus. Science (80) 211: 400–402. 6164096
55. Hendrick JP, Wolin SL, Rinke J, Steitz JA, (1981) Ro small cytoplasmic ribonucleoproteins are a subclass of La ribonucleoproteins : further characterization of the Ro and La Small ribonucleoproteins from uninfected mammalian cells. Mol Cell Biol 12: 1138–1149. 6180298
56. Garcia EL, Onafuwa-Nuga A, Sim S, King SR, Wolin SL, et al. (2009) Packaging of host mY RNAs by murine leukemia virus may occur early in Y RNA biogenesis. J Virol 83: 12526–12534. doi: 10.1128/JVI.01219-09 19776129
57. Swanson MS, Dreyfuss G, (1988) heterogeneous nuclear ribonucleoprotein Classification and Purification of Proteins of Heterogeneous Nuclear Ribonucleoprotein Particles by RNA-Binding Specificities. Mol Cell Biol 8: 2237–2241.
58. Makeyev A V, Liebhaber SA, (2002) The poly (C) -binding proteins: a multiplicity of functions and a search for mechanisms. RNA 8: 265–278. 12003487
59. Pandit S, Zhou Y, Shiue L, Coutinho-Mansfield G, Li H, et al. (2013) Genome-wide analysis reveals SR protein cooperation and competition in regulated splicing. Mol Cell 50: 223–235. doi: 10.1016/j.molcel.2013.03.001 23562324
60. Saunders LR, Barber GN, (2003) The dsRNA binding protein family: critical roles, diverse cellular functions. FASEB J 17: 961–983. 12773480
61. De Lucas S, Oliveros JC, Chagoyen M, Ortín J, (2014) Functional signature for the recognition of specific target mRNAs by human Staufen1 protein. Nucleic Acids Res 42: 4516–4526. doi: 10.1093/nar/gku073 24470147
62. Wilson a C, Peterson MG, Herr W, (1995) The HCF repeat is an unusual proteolytic cleavage signal. Genes Dev 9: 2445–2458. 7590226
63. Simon JH, Southerling TE, Peterson JC, Meyer BE, Malim MH, (1995) Complementation of vif-defective human immunodeficiency virus type 1 by primate, but not nonprimate, lentivirus vif genes. J Virol 69: 4166–4172. 7769676
64. Ratner L, Haseltine W, Patarca R, Livak KJ, Starcich B, et al. (1985) Complete nucleotide sequence of the AIDS virus, HTLV-III. Nature 313: 277–284. 2578615
65. Swanson CM, Puffer B a, Ahmad KM, Doms RW, Malim MH, (2004) Retroviral mRNA nuclear export elements regulate protein function and virion assembly. EMBO J 23: 2632–2640. 15201866
66. Newman ENC, Holmes RK, Craig HM, Klein KC, Lingappa JR, et al. (2005) Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity. Curr Biol 15: 166–170. 15668174
67. 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. 17121840
68. Shlyakhtenko LS, Lushnikov AY, Li M, Lackey L, Harris RS, et al. (2011) Atomic force microscopy studies provide direct evidence for dimerization of the HIV restriction factor APOBEC3G. J Biol Chem 286: 3387–3395. doi: 10.1074/jbc.M110.195685 21123176
69. Gaddis NC, Chertova E, Sheehy AM, Henderson LE, Malim MH, (2003) Comprehensive investigation of the molecular defect in vif-deficient human immunodeficiency virus type 1 virions. J Virol 77: 5810–5820. 12719574