Hepatitis delta antigen requires a flexible quasi-double-stranded RNA structure to bind and condense hepatitis delta virus RNA in a ribonucleoprotein complex

Journal of Virology

Volumn 88, Issue 13, 2014, Pages 7402-7411

  Griffin, Brittany L ^a   Chasovskikh, Sergey ^a   Dritschilo, Anatoly ^a   Casey, John L ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; HEPATITIS DELTA ANTIGEN; RIBONUCLEOPROTEIN; VIRUS RNA; PROTEIN BINDING;

ACYLATION; ANALYTIC METHOD; ANTIGEN BINDING; ANTIGEN SPECIFICITY; ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; HEPATITIS DELTA VIRUS; HUMAN; IN VITRO STUDY; NONHUMAN; PRIMER EXTENSION; PRIORITY JOURNAL; PROTEIN RNA BINDING; PROTEIN SECONDARY STRUCTURE; RNA SEQUENCE; RNA STRUCTURE; VIRUS REPLICATION; CHEMISTRY; CONFORMATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; SEQUENCE HOMOLOGY;

BASE SEQUENCE; HEPATITIS DELTA ANTIGENS; HUMANS; MICROSCOPY, ATOMIC FORCE; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; RIBONUCLEOPROTEINS; RNA, DOUBLE-STRANDED; RNA, VIRAL; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 84901999766     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00443-14     Document Type: Article

References (53)

1. Rizzetto M. 2009. Hepatitis D: thirty years after. J. Hepatol. 50:1043-1050. http://dx.doi.org/10.1016/j.jhep.2009.01.004.
2. Rizzetto M, Canese MG, Gerin JL, London WT, Sly DL, Purcell RH. 1980. Transmission of the hepatitisBvirus-associated delta antigen to chimpanzees. J. Infect. Dis. 141:590-602. http://dx.doi.org/10.1093/infdis/141.5.590.
3. Bonino F, Hoyer B, Ford E, Shih JW, Purcell RH, Gerin JL. 1981. The delta agent: HBsAg particles with delta antigen and RNA in the serum of an HBV carrier. Hepatology 1:127-131. http://dx.doi.org/10.1002/hep.1840010207.
4. Wang CJ, Chen PJ, Wu JC, Patel D, Chen DS. 1991. Small-form hepatitis B surface antigen is sufficient to help in the assembly of hepatitis delta virus-like particles. J. Virol. 65:6630-6636.
5. Sureau C, Moriarty AM, Thornton GB, Lanford RE. 1992. Production of infectious hepatitis delta virus in vitro and neutralization with antibodies directed against hepatitis B virus pre-S antigens. J. Virol. 66:1241-1245.
6. Ryu WS, Netter HJ, Bayer M, Taylor J. 1993. Ribonucleoprotein complexes of hepatitis delta virus. J. Virol. 67:3281-3287.
7. Kuo MY, Chao M, Taylor J. 1989. Initiation of replication of the human hepatitis delta virus genome from cloned DNA: role of delta antigen. J. Virol. 63:1945-1950.
8. Chang J, Nie X, Chang HE, Han Z, Taylor J. 2008. Transcription of hepatitis delta virus RNA by RNA polymerase II. J. Virol. 82:1118-1127. http://dx.doi.org/10.1128/JVI.01758-07.
9. Taylor J, Pelchat M. 2010. Origin of hepatitis delta virus. Future Microbiol. 5:393-402. http://dx.doi.org/10.2217/fmb.10.15.
10. Tseng CH, Lai MM. 2009. Hepatitis delta virus RNA replication. Viruses 1:818-831. http://dx.doi.org/10.3390/v1030818.
11. Kuo MY, Goldberg J, Coates L, Mason W, Gerin J, Taylor J. 1988. Molecular cloning of hepatitis delta virus RNA from an infected woodchuck liver: sequence, structure, and applications. J. Virol. 62:1855-1861.
12. Wang KS, Choo QL, Weiner AJ, Ou JH, Najarian RC, Thayer RM, Mullenbach GT, Denniston KJ, Gerin JL, Houghton M. 1986. Structure, sequence and expression of the hepatitis delta viral genome. Nature 323: 508-514. http://dx.doi.org/10.1038/323508a0.
13. Bichko VV, Lemon SM, Wang JG, Hwang S, Lai MM, Taylor JM. 1996. Epitopes exposed on hepatitis delta virus ribonucleoproteins. J. Virol. 70: 5807-5811.
14. Chang MF, Chen CH, Lin SL, Chen CJ, Chang SC. 1995. Functional domains of delta antigens and viral RNA required for RNA packaging of hepatitis delta virus. J. Virol. 69:2508-2514.
15. Chou HC, Hsieh TY, Sheu GT, Lai MM. 1998. Hepatitis delta antigen mediates the nuclear import of hepatitis delta virus RNA. J. Virol. 72: 3684-3690.
16. Cunha C, Monjardino J, Cheng D, Krause S, Carmo-Fonseca M. 1998. Localization of hepatitis delta virus RNA in the nucleus of human cells. RNA 4:680-693. http://dx.doi.org/10.1017/S135583829898013X.
17. Lazinski DW, Taylor JM. 1994. Expression of hepatitis delta virus RNA deletions: cis and trans requirements for self-cleavage, ligation, and RNA packaging. J. Virol. 68:2879-2888.
18. Polson AG, Ley HL, III, Bass BL, Casey JL. 1998. Hepatitis delta virus RNA editing is highly specific for the amber/W site and is suppressed by hepatitis delta antigen. Mol. Cell. Biol. 18:1919-1926.
19. Alves C, Cheng H, Roder H, Taylor J. 2010. Intrinsic disorder and oligomerization of the hepatitis delta virus antigen. Virology 407:333-340. http://dx.doi.org/10.1016/j.virol.2010.08.019.
20. Defenbaugh DA, Johnson M, Chen R, Zheng YY, Casey JL. 2009. Hepatitis delta antigen requires a minimum length of the hepatitis delta virus unbranched rod RNA structure for binding. J. Virol. 83:4548-4556. http://dx.doi.org/10.1128/JVI.02467-08.
21. Lin BC, Defenbaugh DA, Casey JL. 2010. Multimerization of hepatitis delta antigen is a critical determinant of RNA binding specificity. J. Virol. 84:1406-1413. http://dx.doi.org/10.1128/JVI.01723-09.
22. Zuccola HJ, Rozzelle JE, Lemon SM, Erickson BW, Hogle JM. 1998. Structural basis of the oligomerization of hepatitis delta antigen. Structure 6:821-830. http://dx.doi.org/10.1016/S0969-2126(98)00084-7.
23. Cornillez-Ty CT, Lazinski DW. 2003. Determination of the multimerization state of the hepatitis delta virus antigens in vivo. J. Virol. 77:10314-10326. http://dx.doi.org/10.1128/JVI.77.19.10314-10326.2003.
24. Wang JG, Lemon SM. 1993. Hepatitis delta virus antigen forms dimers and multimeric complexes in vivo. J. Virol. 67:446-454.
25. Daigh LH, Griffin BL, Soroush A, Mamedov MR, Casey JL. 2013. Arginine-rich motifs are not required for hepatitis delta virus RNA binding activity of the hepatitis delta antigen. J. Virol. 87:8665-8674. http://dx .doi.org/10.1128/JVI.00929-13.
26. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406-3415. http://dx.doi.org/10 .1093/nar/gkg595.
27. Wilkinson KA, Merino EJ, Weeks KM. 2006. Selective 2'-hydroxyl acylation analyzed by primer extension (SHAPE): quantitativeRNAstructure analysis at single nucleotide resolution. Nat. Protoc. 1:1610-1616. http: //dx.doi.org/10.1038/nprot.2006.249.
28. Mortimer SA, Weeks KM. 2009. Time-resolved RNA SHAPE chemistry: quantitative RNA structure analysis in one-second snapshots and at single-nucleotide resolution. Nat. Protoc. 4:1413-1421. http://dx.doi.org/10 .1038/nprot.2009.126.
29. McGinnis JL, Dunkle JA, Cate JH, Weeks KM. 2012. The mechanisms of RNA SHAPE chemistry. J. Am. Chem. Soc. 134:6617-6624. http://dx.doi .org/10.1021/ja2104075.
30. Pang PS, Elazar M, Pham EA, Glenn JS. 2011. Simplified RNA secondary structure mapping by automation of SHAPE data analysis. Nucleic Acids Res. 39:e151. http://dx.doi.org/10.1093/nar/gkr773.
31. Wilkinson KA, Gorelick RJ, Vasa SM, Guex N, Rein A, Mathews DH, Giddings MC, Weeks KM. 2008. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol. 6:e96. http://dx.doi.org/10.1371/journal.pbio .0060096.
32. Deigan KE, Li TW, Mathews DH, Weeks KM. 2009. Accurate SHAPEdirected RNA structure determination. Proc. Natl. Acad. Sci. U. S. A. 106:97-102. http://dx.doi.org/10.1073/pnas.0806929106.
33. McGinnis JL, Duncan CD, Weeks KM. 2009. High-throughput SHAPE and hydroxyl radical analysis of RNA structure and ribonucleoprotein assembly. Methods Enzymol. 468:67-89. http://dx.doi.org /10.1016/S0076-6879(09)68004-6.
34. Chasovskikh S, Dimtchev A, Smulson M, Dritschilo A. 2005. DNA transitions induced by binding of PARP-1 to cruciform structures in supercoiled plasmids. Cytometry A 68:21-27. http://dx.doi.org/10.1002 /cyto.a.20187.
35. Reuter JS, Mathews DH. 2010. RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics 11:129. http: //dx.doi.org/10.1186/1471-2105-11-129.
36. Casey JL. 2002. RNA editing in hepatitis delta virus genotype III requires a branched double-hairpin RNA structure. J. Virol. 76:7385-7397. http: //dx.doi.org/10.1128/JVI.76.15.7385-7397.2002.
37. Linnstaedt SD, Kasprzak WK, Shapiro BA, Casey JL. 2006. The role of a metastable RNA secondary structure in hepatitis delta virus genotype III RNA editing. RNA 12:1521-1533. http://dx.doi.org/10.1261/rna.89306.
38. Ferre-D'Amare AR, Zhou K, Doudna JA. 1998. Crystal structure of a hepatitis delta virus ribozyme. Nature 395:567-574. http://dx.doi.org/10 .1038/26912.
39. Low JT, Weeks KM. 2010. SHAPE-directed RNA secondary structure prediction. Methods 52:150-158. http://dx.doi.org/10.1016/j.ymeth.2010 .06.007.
40. Beard MR, MacNaughton TB, Gowans EJ. 1996. Identification and characterization of a hepatitis delta virusRNAtranscriptional promoter. J. Virol. 70:4986-4995.
41. Virstedt J, Berge T, Henderson RM, Waring MJ, Travers AA. 2004. The influence of DNA stiffness upon nucleosome formation. J. Struct. Biol. 148:66-85. http://dx.doi.org/10.1016/j.jsb.2004.03.007.
42. Bailly C, Waring MJ, Travers AA. 1995. Effects of base substitutions on the binding of a DNA-bending protein. J. Mol. Biol. 253:1-7. http://dx.doi .org/10.1006/jmbi.1995.0530.
43. Grove A, Galeone A, Mayol L, Geiduschek EP. 1996. On the connection between inherent DNA flexure and preferred binding of hydroxymethyluracil-containing DNA by the type II DNA-binding protein TF1. J. Mol. Biol. 260:196-206. http://dx.doi.org/10.1006/jmbi.1996.0392.
44. Grove A, Galeone A, Mayol L, Geiduschek EP. 1996. Localized DNA flexibility contributes to target site selection by DNA-bending proteins. J. Mol. Biol. 260:120-125. http://dx.doi.org/10.1006/jmbi.1996.0386.
45. Hagerman PJ. 1997. Flexibility of RNA. Annu. Rev. Biophys. Biomol. Struct. 26:139-156. http://dx.doi.org/10.1146/annurev.biophys.26.1.139.
46. Bailly C, Payet D, Travers AA, Waring MJ. 1996. PCR-based development ofDNAsubstrates containing modified bases: an efficient system for investigating the role of the exocyclic groups in chemical and structural recognition by minor groove binding drugs and proteins. Proc. Natl. Acad. Sci. U. S. A. 93:13623-13628. http://dx.doi.org/10.1073/pnas.93.24 .13623.
47. Buttinelli M, Minnock A, Panetta G, Waring M, Travers A. 1998. The exocyclic groups of DNA modulate the affinity and positioning of the histone octamer. Proc. Natl. Acad. Sci. U. S. A. 95:8544-8549. http://dx .doi.org/10.1073/pnas.95.15.8544.
48. Tanaka Y, Fujii S, Hiroaki H, Sakata T, Tanaka T, Uesugi S, Tomita K, Kyogoku Y. 1999. A'-form RNA double helix in the single crystal structure of r(UGAGCUUCGGCUC). Nucleic Acids Res. 27:949-955. http: //dx.doi.org/10.1093/nar/27.4.949.
49. Henn A, Medalia O, Shi SP, Steinberg M, Franceschi F, Sagi I. 2001. Visualization of unwinding activity of duplex RNA by DbpA, a DEAD box helicase, at single-molecule resolution by atomic force microscopy. Proc. Natl. Acad. Sci. U. S. A. 98:5007-5012. http://dx.doi.org/10.1073/pnas .071372498.
50. Abrahem A, Pelchat M. 2008. Formation of an RNA polymerase II preinitiation complex on an RNA promoter derived from the hepatitis delta virus RNA genome. Nucleic Acids Res. 36:5201-5211. http://dx.doi.org /10.1093/nar/gkn501.
51. Greco-Stewart VS, Miron P, Abrahem A, Pelchat M. 2007. The human RNA polymerase II interacts with the terminal stem-loop regions of the hepatitis delta virus RNA genome. Virology 357:68-78. http://dx.doi.org /10.1016/j.virol.2006.08.010.
52. Kos A, Dijkema R, Arnberg AC, van der Meide PH, Schellekens H. 1986. The hepatitis delta (delta) virus possesses a circular RNA. Nature 323:558-560. http://dx.doi.org/10.1038/323558a0.
53. Han Z, Alves C, Gudima S, Taylor J. 2009. Intracellular localization of hepatitis delta virus proteins in the presence and absence of viral RNA accumulation. J. Virol. 83:6457-6463. http://dx.doi.org/10.1128/JVI .00008-09.