Functional conservation despite structural divergence in ligand-responsive RNA switches

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 45, 2014, Pages 15952-15957

  Boerneke, Mark A ^a   Dibrov, Sergey M ^a   Gu, Jing ^a   Wyles, David L ^b   Hermann, Thomas ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Hepatitis C virus; IRES elements; RNA viruses; Translation regulation

Indexed keywords

LIGAND; VIRUS RNA; REGULATORY RNA SEQUENCE; VIRUS PROTEIN;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; INTERNAL RIBOSOME ENTRY SITE; LIGAND BINDING; NONHUMAN; NUCLEOTIDE MOTIF; PARTICLE SIZE; PROTEIN SECONDARY STRUCTURE; RIBOSWITCH; RNA ANALYSIS; RNA CONFORMATION; RNA MOTIF; RNA SEQUENCE; RNA STABILITY; RNA STRUCTURE; RNA TRANSLATION; RNA VIRUS; TRANSLATION REGULATION; BIOSYNTHESIS; CELL FREE SYSTEM; CHEMISTRY; CONFORMATION; GENETICS; HEPACIVIRUS; METABOLISM; PHYSIOLOGY; PROTEIN SYNTHESIS; REGULATORY RNA SEQUENCE;

CELL-FREE SYSTEM; HEPACIVIRUS; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA, VIRAL; VIRAL PROTEINS;

EID: 84909595102     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1414678111     Document Type: Article

References (41)

1. Plank TD, Kieft JS (2012) The structures of nonprotein-coding RNAs that drive internal ribosome entry site function. Wiley Interdiscip Rev RNA 3(2):195-212.
2. Hellen CU, Pestova TV (1999) Translation of hepatitis C virus RNA. J Viral Hepat 6(2):79-87.
3. Ji H, Fraser CS, Yu Y, Leary J, Doudna JA (2004) Coordinated assembly of human translation initiation complexes by the hepatitis C virus internal ribosome entry site RNA. Proc Natl Acad Sci USA 101(49):16990-16995.
4. Otto GA, Puglisi JD (2004) The pathway of HCV IRES-mediated translation initiation. Cell 119(3):369-380.
5. Hellen CU, De Breyne S (2007) A distinct group of hepacivirus/pestivirus-like internal ribosomal entry sites in members of diverse picornavirus genera: Evidence for modular exchange of functional noncoding RNA elements by recombination. J Virol 81(11):5850-5863.
6. Kieft JS, et al. (1999) The hepatitis C virus internal ribosome entry site adopts an iondependent tertiary fold. J Mol Biol 292(3):513-529.
7. Dibrov SM, et al. (2014) Hepatitis C virus translation inhibitors targeting the internal ribosomal entry site. J Med Chem 57(5):1694-1707.
8. Pestova TV, Shatsky IN, Fletcher SP, Jackson RJ, Hellen CU (1998) A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNAs. Genes Dev 12(1):67-83.
9. Kolupaeva VG, Pestova TV, Hellen CU (2000) Ribosomal binding to the internal ribosomal entry site of classical swine fever virus. RNA 6(12):1791-1807.
10. Filbin ME, Kieft JS (2011) HCV IRES domain IIb affects the configuration of coding RNA in the 40S subunit's decoding groove. RNA 17(7):1258-1273.
11. Locker N, Easton LE, Lukavsky PJ (2007) HCV and CSFV IRES domain II mediate eIF2 release during 80S ribosome assembly. EMBO J 26(3):795-805.
12. Filbin ME, Vollmar BS, Shi D, Gonen T, Kieft JS (2013) HCV IRES manipulates the ribosome to promote the switch from translation initiation to elongation. Nat Struct Mol Biol 20(2):150-158.
13. Pestova TV, De Breyne S, Pisarev AV, Abaeva IS, Hellen CU (2008) eIF2-dependent and eIF2-independent modes of initiation on the CSFV IRES: A common role of domain II. EMBO J 27(7):1060-1072.
14. Yamamoto H, et al. (2014) Structure of the mammalian 80S initiation complex with initiation factor 5B on HCV-IRES RNA. Nat Struct Mol Biol 21(8):721-727.
15. Dibrov SM, Johnston-Cox H, Weng YH, Hermann T (2007) Functional architecture of HCV IRES domain II stabilized by divalent metal ions in the crystal and in solution. Angew Chem Int Ed Engl 46(1-2):226-229.
16. Lukavsky PJ, Kim I, Otto GA, Puglisi JD (2003) Structure of HCV IRES domain II determined by NMR. Nat Struct Biol 10(12):1033-1038.
17. Spahn CM, et al. (2001) Hepatitis C virus IRES RNA-induced changes in the conformation of the 40s ribosomal subunit. Science 291(5510):1959-1962.
18. Boehringer D, Thermann R, Ostareck-Lederer A, Lewis JD, Stark H (2005) Structure of the hepatitis C virus IRES bound to the human 80S ribosome: Remodeling of the HCV IRES. Structure 13(11):1695-1706.
19. Seth PP, et al. (2005) SAR by MS: Discovery of a new class of RNA-binding small molecules for the hepatitis C virus: Internal ribosome entry site IIA subdomain. J Med Chem 48(23):7099-7102.
20. Parker MA, Satkiewicz E, Hermann T, Bergdahl BM (2011) An efficient new route to dihydropyranobenzimidazole inhibitors of HCV replication. Molecules 16(1):281-290.
21. Dibrov SM, et al. (2012) Structure of a hepatitis C virus RNA domain in complex with a translation inhibitor reveals a binding mode reminiscent of riboswitches. Proc Natl Acad Sci USA 109(14):5223-5228.
22. Carnevali M, Parsons J, Wyles DL, Hermann T (2010) A modular approach to synthetic RNA binders of the hepatitis C virus internal ribosome entry site. ChemBioChem 11(10):1364-1367.
23. Parsons J, et al. (2009) Conformational inhibition of the hepatitis C virus internal ribosome entry site RNA. Nat Chem Biol 5(11):823-825.
24. Puglisi JD, Chen L, Frankel AD, Williamson JR (1993) Role of RNA structure in arginine recognition of TAR RNA. Proc Natl Acad Sci USA 90(8):3680-3684.
25. Kondo J, Westhof E (2011) Classification of pseudo pairs between nucleotide bases and amino acids by analysis of nucleotide-protein complexes. Nucleic Acids Res 39(19):8628-8637.
26. Walberer BJ, Cheng AC, Frankel AD (2003) Structural diversity and isomorphism of hydrogen-bonded base interactions in nucleic acids. J Mol Biol 327(4):767-780.
27. Abu Almakarem AS, Petrov AI, Stombaugh J, Zirbel CL, Leontis NB (2012) Comprehensive survey and geometric classification of base triples in RNA structures. Nucleic Acids Res 40(4):1407-1423.
28. Yarus M (1988) A specific amino acid binding site composed of RNA. Science 240(4860):1751-1758.
29. Zhou S, Rynearson KD, Ding K, Brunn ND, Hermann T (2013) Screening for inhibitors of the hepatitis C virus internal ribosome entry site RNA. Bioorg Med Chem 21(20):6139-6144.
30. Pestova TV, et al. (2001) Molecular mechanisms of translation initiation in eukaryotes. Proc Natl Acad Sci USA 98(13):7029-7036.
31. Willcocks MM, et al. (2011) Structural features of the Seneca Valley virus internal ribosome entry site (IRES) element: A picornavirus with a pestivirus-like IRES. J Virol 85(9):4452-4461.
32. Leontis NB, Westhof E (1998) A common motif organizes the structure of multi-helix loops in 16 S and 23 S ribosomal RNAs. J Mol Biol 283(3):571-583.
33. Reusken CB, Dalebout TJ, Eerligh P, Bredenbeek PJ, Spaan WJ (2003) Analysis of hepatitis C virus/classical swine fever virus chimeric 5'NTRs: Sequences within the hepatitis C virus IRES are required for viral RNA replication. J Gen Virol 84(Pt 7):1761-1769.
34. Blight KJ, McKeating JA, Marcotrigiano J, Rice CM (2003) Efficient replication of hepatitis C virus genotype 1a RNAs in cell culture. J Virol 77(5):3181-3190.
35. Shi ST, Lai M M C (2006) HCV 5' and 3'UTR: When Translation Meets Replication. Hepatitis C Viruses: Genomes and Molecular Biology, ed Tan SL (Horizon Bioscience, Norfolk).
36. Romero-López C, Berzal-Herranz A (2009) A long-range RNA-RNA interaction between the 5' and 3' ends of the HCV genome. RNA 15(9):1740-1752.
37. Berry KE, Waghray S, Mortimer SA, Bai Y, Doudna JA (2011) Crystal structure of the HCV IRES central domain reveals strategy for start-codon positioning. Structure 19(10):1456-1466.
38. Traut TW (1994) Physiological concentrations of purines and pyrimidines. Mol Cell Biochem 140(1):1-22.
39. Seth PP, Jefferson EA, Griffey RH, Swayze EE (2004) Benzimidazoles and analogs thereof as antivirals. World Patent Appl WO2004050035A3.
40. Brunn ND, Garcia Sega E, Kao MB, Hermann T (2012) Targeting a regulatory element in human thymidylate synthase mRNA. ChemBioChem 13(18):2738-2744.
41. Wyles DL, Kaihara KA, Vaida F, Schooley RT (2007) Synergy of small molecular inhibitors of hepatitis C virus replication directed at multiple viral targets. J Virol 81(6):3005-3008.