Two different conformations in hepatitis C virus p7 protein account for proton transport and dye release

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Gan, Siok Wan ^a   Surya, Wahyu ^a   Vararattanavech, Ardcharaporn ^a   Torres, Jaume ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYFLUORESCEIN; DYE; HEPATITIS C VIRUS P7 PROTEIN; LIPOSOME; MEMBRANE PROTEIN; PROTEIN TM1; PROTEIN TM2; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATION; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; INFRARED SPECTROSCOPY; LIPID BILAYER; MEMBRANE PERMEABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTON TRANSPORT;

BIOLOGICAL TRANSPORT; ELECTRON TRANSPORT; FLUORESCENT DYES; GENE EXPRESSION; HUMANS; LIPID BILAYERS; MASS SPECTROMETRY; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTON PUMPS; PROTONS; RECOMBINANT PROTEINS; VIRAL PROTEINS;

EID: 84896902534     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078494     Document Type: Article

References (54)

1. Lohmann V, Korner F, Koch J, Herian U, Theilmann L, et al. (1999) Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285: 110-113. (Pubitemid 29307577)
2. Sakai A, Claire MS, Faulk K, Govindarajan S, Emerson SU, et al. (2003) The p7 polypeptide of hepatitis C virus is critical for infectivity and contains functionally important genotype-specific sequences. Proc Natl Acad Sci U S A 100: 11646-11651. (Pubitemid 37205990)
3. Steinmann E, Penin F, Kallis S, Patel AH, Bartenschlager R, et al. (2007) Hepatitis C virus p7 protein is crucial for assembly and release of infectious virions. PLoS Path 3: 0962-0971.
4. Griffin SD, Beales LP, Clarke DS, Worsfold O, Evans SD, et al. (2003) The p7 protein of hepatitis C virus forms an ion channel that is blocked by the antiviral drug, Amantadine. FEBS Lett 535: 34-38. (Pubitemid 36126351)
5. Pavlovic D, Neville DC, Argaud O, Blumberg B, Dwek RA, et al. (2003) The hepatitis C virus p7 protein forms an ion channel that is inhibited by long-alkyl-chain iminosugar derivatives. Proc Natl Acad Sci U S A 100: 6104-6108. (Pubitemid 36576938)
6. Premkumar A, Wilson L, Ewart GD, Gage PW (2004) Cation-selective ion channels formed by p7 of hepatitis C virus are blocked by hexamethylene amiloride. FEBS Lett 557: 99-103. (Pubitemid 38115876)
7. StGelais C, Tuthill TJ, Clarke DS, Rowlands DJ, Harris M, et al. (2007) Inhibition of hepatitis C virus p7 membrane channels in a liposome-based assay system. Antiviral Res 76: 48-58. (Pubitemid 47176693)
8. Wozniak AL, Griffin S, Rowlands D, Harris M, Yi M, et al. (2010) Intracellular proton conductance of the hepatitis C virus p7 protein and its contribution to infectious virus production. PLoS Pathog 6: e1001087.
9. Tedbury P, Welbourn S, Pause A, King B, Griffin S, et al. (2011) The subcellular localization of the hepatitis C virus non-structural protein NS2 is regulated by an ion channel-independent function of the p7 protein. J Gen Virol 92: 819-830.
10. Boson B, Granio O, Bartenschlager R, Cosset FL (2011) A Concerted Action of Hepatitis C Virus P7 and Nonstructural Protein 2 Regulates Core Localization at the Endoplasmic Reticulum and Virus Assembly. PLoS Path 7: e1002144.
11. Gentzsch J, Brohm C, Steinmann E, Friesland M, Menzel N, et al. (2013) Hepatitis C Virus p7 is Critical for Capsid Assembly and Envelopment. PLoS Path 9.
12. Montserret R, Saint N, Vanbelle C, Salvay AG, Simorre JP, et al. (2010) NMR structure and ion channel activity of the p7 protein from hepatitis C virus. The Journal of biological chemistry 285: 31446-31461.
13. Cook GA, Opella SJ (2010) Secondary structure, dynamics, and architecture of the p7 membrane protein from hepatitis C virus by NMR spectroscopy. Biochim Biophys Acta 1808: 1448-1453.
14. Cook GA, Zhang H, Park SH, Wang Y, Opella SJ (2010) Comparative NMR studies demonstrate profound differences between two viroporins: p7 of HCV and Vpu of HIV-1. Biochim Biophys Acta 1808: 554-560.
15. Carrere-Kremer S, Montpellier-Pala C, Cocquerel L, Wychowski C, Penin F, et al. (2002) Subcellular localization and topology of the p7 polypeptide of hepatitis C virus. J Virol 76: 3720-3730. (Pubitemid 34250536)
16. Patargias G, Zitzmann N, Dwek R, Fischer WB (2006) Protein-protein interactions: Modeling the hepatitis C virus ion channel p7. J Med Chem 49: 648-655. (Pubitemid 43157494)
17. Chew CF, Vijayan R, Chang J, Zitzmann N, Biggin PC (2009) Determination of pore-lining residues in the hepatitis C virus p7 protein. Biophys J 96: L10-12.
18. Luik P, Chew C, Aittoniemi J, Chang J, Wentworth P, Jr., et al. (2009) The 3-dimensional structure of a hepatitis C virus p7 ion channel by electron microscopy. Proc Natl Acad Sci U S A 106: 12712-12716.
19. Clarke D, Griffin S, Beales L, Gelais CS, Burgess S, et al. (2006) Evidence for the formation of a heptameric ion channel complex by the hepatitis C virus P7 protein in vitro. J Biol Chem 281: 37057-37068. (Pubitemid 46042176)
20. Ouyang B, Xie S, Berardi MJ, Zhao X, Dev J, et al. (2013) Unusual architecture of the p7 channel from hepatitis C virus. Nature 498: 521-525.
21. Griffin S, Clarke D, McCormick C, Rowlands D, Harris M (2005) Signal peptide cleavage and internal targeting signals direct the hepatitis C virus p7 protein to distinct intracellular membranes. J Virol 79: 15525-15536. (Pubitemid 43032334)
22. Isherwood BJ, Patel AH (2005) Analysis of the processing and transmembrane topology of the E2p7 protein of hepatitis C virus. J Gen Virol 86: 667-676. (Pubitemid 40331247)
23. Whitfield T, Miles AJ, Scheinost JC, Offer J, Wentworth P, et al. (2011) The influence of different lipid environments on the structure and function of the hepatitis C virus p7 ion channel protein. Mol Membr Biol 28: 254-264.
24. StGelais C, Tuthill TJ, Clarke DS, Rowlands DJ, Harris M, et al. (2007) Inhibition of hepatitis C virus p7 membrane channels in a liposome-based assay system. Antiviral Res 76: 48-58. (Pubitemid 47176693)
25. Foster TL, Verow M, Wozniak AL, Bentham MJ, Thompson J, et al. (2011) Resistance mutations define specific antiviral effects for inhibitors of the hepatitis C virus p7 ion channel. Hepatology (Baltimore, Md 54: 79-90.
26. Gervais C, Do F, Cantin A, Kukolj G, White PW, et al. (2011) Development and validation of a high-throughput screening assay for the hepatitis C virus p7 viroporin. J Biomol Screen 16: 363-369.
27. Liu H, Naismith J (2008) An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol. BMC Biotechnol 8: 91.
28. Hu J, Qin H, Li C, Sharma M, Cross TA, et al. (2007) Structural biology of transmembrane domains: efficient production and characterization of transmembrane peptides by NMR. Protein Sci 16: 2153-2165. (Pubitemid 47481650)
29. Torres J, Parthasarathy K, Lin X, Saravanan R, Kukol A, et al. (2006) Model of a putative pore: the pentameric a-helical bundle of SARS coronavirus E protein in lipid bilayers. Biophys J 91: 938-947. (Pubitemid 44161926)
30. Hayes DB, Laue T, Philo JS.
31. Parsegian VA, Fuller N, Rand RP (1979) Measured Work of Deformation and Repulsion of Lecithin Bilayers. Proc Nat Acad Sci USA 76: 2750-2754. (Pubitemid 9213158)
32. StGelais C, Foster TL, Verow M, Atkins E, Fishwick CWG, et al. (2009) Determinants of hepatitis C virus p7 ion channel function and drug sensitivity identified in vitro. J Virol 83: 7970-7981.
33. Li H, Atkins E, Bruckner J, McArdle S, Qiu WC, et al. (2012) Genetic and functional heterogeneity of the hepatitis C virus p7 ion channel during natural chronic infection. Virology 423: 30-37.
34. Byler DM, Susi H (1986) Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers 25: 469-487.
35. Litman BJ (1973) Lipid Model Membranes - Characterization of Mixed Phospholipid Vesicles. Biochemistry 12: 2545-2554.
36. Reynolds JA, Mccaslin DR (1985) Determination of Protein Molecular-Weight in Complexes with Detergent without Knowledge of Binding. Methods Enzymol 117: 41-53.
37. Huang CH, Charlton JP (1971) Studies on Phosphatidylcholine Vesicles - Determination of Partial Specific Volumes by Sedimentation Velocity Method. J Biol Chem 246: 2555-&.
38. Perez-Berna AJ, Guillen J, Moreno MR, Bernabeu A, Pabst G, et al. (2008) Identification of the membrane-active regions of hepatitis C virus p7 protein: biophysical characterization of the loop region. J Biol Chem 283: 8089-8101.
39. Arfmann HA, Labitzke R, Wagner KG (1977) Conformational properties of Lleucine, L-isoleucine, and L-norleucine side chains in L-lysine copolymers. Biopolymers 16: 1815-1826. (Pubitemid 8140484)
40. Mutter M, Maser F, Altmann KH, Toniolo C, Bonora GM (1985) Sequence-dependence of secondary structure formation: conformational studies of hostguest peptides in alpha-helix and beta-structure supporting media. Biopolymers 24: 1057-1074.
41. Lopez de la Paz M, Serrano L (2004) Sequence determinants of amyloid fibril formation. Proc Nat Acad Sci USA 101: 87-92.
42. Dawson PE, Muir TW, Clark-Lewis I, Kent SB (1994) Synthesis of proteins by native chemical ligation 22. Science 266: 776-779. (Pubitemid 24359280)
43. Parthasarathy K, Lin X, Tan SM, Law SK, Torres J (2008) Transmembrane helices that form two opposite homodimeric interactions: an asparagine scan study of alphaM and beta2 integrins. Protein Sci 17: 930-938. (Pubitemid 351629587)
44. 18O, in the determination of a structural model of phospholamban in a lipid bilayer. Spatial restraints resolve the ambiguity arising from interpretations of mutagenesis data. J Mol Biol 300: 677-685.
45. Torres J, Kukol A, Arkin IT (2000) Use of a single glycine residue to determine the tilt and orientation of a transmembrane helix. A new structural label for infrared spectroscopy. Biophys J 79: 3139-3143.
46. Gan SW, Tan E, Lin X, Yu D, Wang J, et al. (2012) The small hydrophobic protein of the human respiratory syncytial virus forms pentameric ion channels. J Biol Chem 287: 24671-24689.
47. Cook GA, Opella SJ (2009) NMR studies of p7 protein from hepatitis C virus. Eur Biophys J 39.
48. Lundin M, Monne M, Widell A, Von Heijne G, Persson MA (2003) Topology of the membrane-associated hepatitis C virus protein NS4B. J Virol 77: 5428-5438. (Pubitemid 36460956)
49. Lambert C, Prange R (2001) Dual topology of the hepatitis B virus large envelope protein: determinants influencing post-translational pre-S translocation. J Biol Chem 276: 22265-22272.
50. McGinnes LW, Reitter JN, Gravel K, Morrison TG (2003) Evidence for mixed membrane topology of the newcastle disease virus fusion protein. J Virol 77: 1951-1963. (Pubitemid 36110007)
51. Haqshenas G, Dong X, Ewart G, Bowden S, Gowans EJ (2007) A 2a/1b full-length p7 inter-genotypic chimeric genome of hepatitis C virus is infectious in vitro. Virology 360: 17-26.
52. Yi M, Ma Y, Yates J, Lemon SM (2007) Compensatory mutations in E1, p7, NS2, and NS3 enhance yields of cell culture-infectious intergenotypic chirneric hepatitis C virus. J Virol 81: 629-638. (Pubitemid 46067890)
53. Pietschmann T, Kaul A, Koutsoudakis G, Shavinskaya A, Kallis S, et al. (2006) Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc Nat Acad Sci USA 103: 7408-7413. (Pubitemid 43727846)
54. Tokuriki N, Oldfield CJ, Uversky VN, Berezovsky IN, Tawfik DS (2009) Do viral proteins possess unique biophysical features? Trends Biochem Sci 34: 53-59.