Fluorescence resonance energy transfer-based intracellular assay for the conformation of hepatitis C virus drug target NS5A

Journal of Virology

Volumn 86, Issue 15, 2012, Pages 8277-8286

  Bhattacharya, Dipankar ^b   Ansari, Israrul H ^b   Mehle, Andrew ^c   Striker, Rob ^a,b  

^a WILLIAM S MIDDLETON MEMORIAL VETERANS HOSPITAL   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NONSTRUCTURAL PROTEIN 5A; QUERCETIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOCHEMICAL COMPOSITION; CARBOXY TERMINAL SEQUENCE; CELL ASSAY; CELL CULTURE; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEPATITIS C VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN UNFOLDING; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; VIRUS PARTICLE;

ANTIVIRAL AGENTS; CELL LINE; DRUG DELIVERY SYSTEMS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEPACIVIRUS; HEPATITIS C; HUMANS; PROTEIN STRUCTURE, TERTIARY; VIRAL NONSTRUCTURAL PROTEINS;

HEPATITIS C VIRUS;

EID: 84864386121     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00645-12     Document Type: Article

References (38)

1. Adams SR, et al. 2002. New biarsenical ligands and tetracysteine motifs for protein labeling in vitro and in vivo: synthesis and biological applications. J. Am. Chem. Soc. 124:6063-6076.
2. Appel N, Pietschmann T, Bartenschlager R. 2005. Mutational analysis of hepatitis C virus nonstructural protein 5A: potential role of differential phosphorylation in RNA replication and identification of a genetically flexible domain. J. Virol. 79:3187-3194.
3. Appel N, et al. 2008. Essential role of domain III of nonstructural protein 5A for hepatitis C virus infectious particle assembly. PLoS Pathog. 4:e1000035. doi:10.1371/journal.ppat.1000035.
4. Brass V, et al. 2002. An amino-terminal amphipathic alpha-helix mediates membrane association of the hepatitis C virus nonstructural protein 5A. J. Biol. Chem. 277:8130-8139.
5. Brzostowski JA, Meckel T, Hong J, Chen A, Jin T. 2009. Imaging protein-protein interactions by Forster resonance energy transfer (FRET) microscopy in live cells. Curr. Protoc. Protein Sci. Chapter 19:Unit19.5.
6. Coelmont L., et al. 2010. DEB025 (Alisporivir) inhibits hepatitis C virus replication by preventing a cyclophilin A induced cis-trans isomerisation in domain II of NS5A. PLoS One 5:e13687. doi:10.1371/journal.pone.0013687.
7. Counihan NA, Rawlinson SM, Lindenbach BD. 2011. Trafficking of hepatitisCvirus core protein during virus particle assembly. PLoS Pathog. 7:e1002302. doi:10.1371/journal.ppat.1002302.
8. dos Remedios CG, Moens PD. 1995. Fluorescence resonance energy transfer spectroscopy is a reliable "ruler" for measuring structural changes in proteins. Dispelling the problem of the unknown orientation factor. J. Struct. Biol. 115:175-185.
9. Enomoto N, et al. 1996. Mutations in the nonstructural protein 5A gene and response to interferon in patients with chronic hepatitis C virus 1b infection. N. Engl. J. Med. 334:77-81.
10. Fernandes F, Ansari IU, Striker R. 2010. Cyclosporine inhibits a direct interaction between cyclophilins and hepatitis C NS5A. PLoS One 5:e9815. doi:10.1371/journal.pone.0009815.
11. Gao M, et al. 2010. Chemical genetics strategy identifies an HCV NS5A inhibitor with a potent clinical effect. Nature 465:96-100.
12. Gonzalez O, et al. 2009. The heat shock protein inhibitor Quercetin attenuates hepatitis C virus production. Hepatology 50:1756-1764.
13. Griffin BA, Adams SR, Jones J, Tsien RY. 2000. Fluorescent labeling of recombinant proteins in living cells with FlAsH. Methods Enzymol. 327: 565-578.
14. Griffin BA, Adams SR, Tsien RY. 1998. Specific covalent labeling of recombinant protein molecules inside live cells. Science 281:269-272.
15. Hanoulle X, et al. 2009. Hepatitis C virus NS5A protein is a substrate for the peptidyl-prolyl cis/trans isomerase activity of cyclophilins A and B. J. Biol. Chem. 284:13589-13601.
16. Hanoulle X, et al. 2009. Domain 3 of non-structural protein 5A from hepatitis C virus is natively unfolded. Biochem. Biophys. Res. Commun. 381:634-638.
17. Heidecker M, Yan-Marriott Y, Marriott G. 1995. Proximity relationships and structural dynamics of the phalloidin binding site of actin filaments in solution and on single actin filaments on heavy meromyosin. Biochemistry 34:11017-11025.
18. Hoffmann C, et al. 2005. A FlAsH-based FRET approach to determine G protein-coupled receptor activation in living cells. Nat. Methods 2:171-176.
19. Kang J, Lee MS, Gorenstein DG. 2007. Application of RNase in the purification of RNA-binding proteins. Anal. Biochem. 365:147-148.
20. Khachatoorian R, et al. 20 December 2011. A cell-permeable hairpin peptide inhibits hepatitis C viral nonstructural protein 5A-mediated translation and virus production. Hepatology [Epub ahead of print.] doi: 10.1002/hep.25533.
21. Lakowicz JR. 2009. Principles of fluorescence spectroscopy, 3rd ed, p 443-475. Springer Science, New York, NY.
22. Li X, Romero P, Rani M, Dunker AK, Obradovic Z. 1999. Predicting protein disorder for N-, C-, and internal regions. Genome Inform. Ser. Workshop Genome Inform. 10:30-40.
23. Love RA, Brodsky O, Hickey MJ, Wells PA, Cronin CN. 2009. Crystal structure of a novel dimeric form of NS5A domain I protein from hepatitis C virus. J. Virol. 83:4395-4403.
24. Miyawaki A, Tsien RY. 2000. Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein. Methods Enzymol. 327:472-500.
25. Nagai T, Yamada S, Tominaga T, Ichikawa M, Miyawaki A. 2004. Expanded dynamic range of fluorescent indicators for Ca(2+) by circularly permuted yellow fluorescent proteins. Proc. Natl. Acad. Sci. U. S. A. 101:10554-10559.
26. Penin F, et al. 2004. Structure and function of the membrane anchor domain of hepatitis C virus nonstructural protein 5A. J. Biol. Chem. 279: 40835-40843.
27. Romero P, et al. 2001. Sequence complexity of disordered protein. Proteins 42:38-48.
28. Sapay N, et al. 2006. NMR structure and molecular dynamics of the in-plane membrane anchor of nonstructural protein 5A from bovine viral diarrhea virus. Biochemistry 45:2221-2233.
29. Stankova K, et al. 2012. Conformational transitions of proteins engaged in DNA double strand break repair, analyzed by tryptophan fluorescence emission and FRET. Biochem. J. 443:701-709.
30. Sudo K, et al. 2005. High-throughput screening of low molecular weight NS3-NS4A protease inhibitors using a fluorescence resonance energy transfer substrate. Antivir. Chem. Chemother. 16:385-392.
31. Tellinghuisen TL, Foss KL, Treadaway J. 2008. Regulation of hepatitis C virion production via phosphorylation of the NS5A protein. PLoS Pathog. 4:e1000032. doi:10.1371/journal.ppat.1000032.
32. Tellinghuisen TL, Foss KL, Treadaway JC, Rice CM. 2008. Identification of residues required for RNA replication in domains II and III of the hepatitis C virus NS5A protein. J. Virol. 82:1073-1083.
33. Tellinghuisen TL, Marcotrigiano J, Gorbalenya AE, Rice CM. 2004. The NS5A protein of hepatitis C virus is a zinc metalloprotein. J. Biol. Chem. 279:48576-48587.
34. Tellinghuisen TL, Marcotrigiano J, Rice CM. 2005. Structure of the zinc-binding domain of an essential component of the hepatitis C virus replicase. Nature 435:374-379.
35. Uversky VN. 2002. Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 11:739-756.
36. Verdegem D, et al. 2011. Domain 3 of NS5A protein from the hepatitis C virus has intrinsic alpha-helical propensity and is a substrate of cyclophilin A. J. Biol. Chem. 286:20441-20454.
37. World Health Organization. 2011. Fact sheet, p N 166. World Health Organization, Geneva, Switzerland.
38. Yu X, Sainz B, Jr, Uprichard SL. 2009. Development of a cell-based hepatitis C virus infection fluorescent resonance energy transfer assay for high-throughput antiviral compound screening. Antimicrob. Agents Chemother. 53:4311-4319.