The influence of different lipid environments on the structure and function of the hepatitis C virus p7 ion channel protein

References

• Andreyev AY, Fahy E, Guan Z, Kelly S, Li X, McDonald JG, Milne S, Myers D, Park H, Ryan A, Thompson BM, Wang E, Zhao Y, Brown HA, Merrill AH, Raetz CRH, Russell DW, Subramaniam S, Dennis EA. 2010. Subcellular organelle lipidomics in TLR-4-activated macrophages. J Lipid Res 51:2785–2797.
   PubMed Web of Science ®Google Scholar
• Bak M, Bywater RP, Hohwy M, Thomsen JK, Adelhorst K, Jakobsen HJ, Sørensen OW, Nielsen NC. 2001. Conformation of alamethicin in oriented phospholipid bilayers determined by 15N solid-state nuclear magnetic resonance. Biophys J 81:1684–1698.
   PubMed Web of Science ®Google Scholar
• Barrantes F, Bermudez V, Borroni M, Antollini S, Pediconi M, Baier J, Bonini I, Gallegos C, Roccamo A, Valles A, Ayala V, Kamerbeek C. 2010. Boundary lipids in the nicotinic acetylcholine receptor microenvironment. J Mol Neurosci 40:87–90.
   PubMed Web of Science ®Google Scholar
• Bollen IC, Higgins JA. 1980. Phospholipid asymmetry in rough- and smooth-endoplasmic-reticulum membranes of untreated and phenobarbital-treated rat liver. Biochem J 189:475–480.
   PubMed Web of Science ®Google Scholar
• Carrere-Kremer S, Montpellier-Pala C, Cocquerel L, Wychowski C, Penin F, Dubuisson J. 2002. Subcellular localization and topology of the p7 polypeptide of hepatitis C virus. J Virol 76:3720–3730.
   PubMed Web of Science ®Google Scholar
• Chang HM, Reitstetter R, Gruener R. 1995a. Lipid-ion channel interactions: increasing phospholipid headgroup size but not ordering acyl chains alters reconstituted channel behavior. J Membr Biol 145:13–19.
   PubMed Web of Science ®Google Scholar
• Chang HM, Reitstetter R, Mason RP, Gruener R. 1995b. Attenuation of channel kinetics and conductance by cholesterol: An interpretation using structural stress as a unifying concept. J Membr Biol 143:51–63.
   PubMed Web of Science ®Google Scholar
• 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–L12.
   PubMed Web of Science ®Google Scholar
• Clarke D, Griffin S, Beales L, Stgelais C, Burgess S, Harris M, Rowlands D. 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.
   Google Scholar
• Cook G, Opella S. 2010. NMR studies of p7 protein from hepatitis C virus. Eur Biophys J 39:1097–1104.
   PubMed Web of Science ®Google Scholar
• Davison SC, Wills ED. 1974. Studies on the lipid composition of the rat liver endoplasmic reticulum after induction with phenobarbitone and 20-methylcholanthrene. Biochem J 140:461–468.
   PubMedGoogle Scholar
• Di Bisceglie AM. 1997. Hepatitis C and hepatocellular carcinoma. Hepatology 26:34S–38S.
   PubMed Web of Science ®Google Scholar
• Dorwart MR, Wray R, Brautigam CA, Jiang Y, Blount P. 2010. S. aureus MscL is a pentamer in vivo but of variable stoichiometries in vitro: Implications for detergent-solubilized membrane proteins. PLoS Biol 8:e1000555.
   PubMed Web of Science ®Google Scholar
• Duclohier H. 2006. Bilayer lipid composition modulates the activity of dermaseptins, polycationic antimicrobial peptides. Eur Biophys J 35:401–409.
   PubMed Web of Science ®Google Scholar
• Feld JJ, Hoofnagle JH. 2005. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 436:967–972.
   PubMed Web of Science ®Google Scholar
• Fischer WB, Pitkeathly M, Wallace BA, Forrest LR, Smith GR, Sansom MS. 2000. Transmembrane peptide NB of influenza B: A simulation, structure, and conductance study. Biochemistry 39:12708–12716.
   PubMed Web of Science ®Google Scholar
• Gallucci E, Meleleo D, Micelli S, Picciarelli V. 2003. Magainin 2 channel formation in planar lipid membranes: The role of lipid polar groups and ergosterol. Eur Biophys J 32:22–32.
   PubMed Web of Science ®Google Scholar
• Gonzalez ME, Carrasco L. 2003. Viroporins. FEBS Lett 552:28–34.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Griffin SD, Beales LP, Clarke DS, Worsfold O, Evans SD, Jaeger J, Harris MP, Rowlands DJ. 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.
   PubMed Web of Science ®Google Scholar
• Griffin SD, Harvey R, Clarke DS, Barclay WS, Harris M, Rowlands DJ. 2004. A conserved basic loop in hepatitis C virus p7 protein is required for amantadine-sensitive ion channel activity in mammalian cells but is dispensable for localization to mitochondria. J Gen Virol 85:451–461.
   PubMed Web of Science ®Google Scholar
• Hamouda AK, Sanghvi M, Sauls D, Machu TK, Blanton MP. 2006. Assessing the lipid requirements of the Torpedo californica nicotinic acetylcholine receptor. Biochemistry 45:4327–4337.
   PubMed Web of Science ®Google Scholar
• Haqshenas G, Mackenzie JM, Dong X, Gowans EJ. 2007. Hepatitis C virus p7 protein is localized in the endoplasmic reticulum when it is encoded by a replication-competent genome. J Gen Virol 88:134–142.
   PubMed Web of Science ®Google Scholar
• Ismailov II, Berdiev BK, Benos DJ. 1995. Regulation by Na+ and Ca2+ of renal epithelial Na+ channels reconstituted into planar lipid bilayers. J Gen Physiol 106:445–466.
   PubMed Web of Science ®Google Scholar
• Keller SL, Bezrukov SM, Gruner SM, Tate MW, Vodyanoy I, Parsegian VA. 1993. Probability of alamethicin conductance states varies with nonlamellar tendency of bilayer phospholipids. Biophys J 65:23–27.
   PubMed Web of Science ®Google Scholar
• Kolomiytseva IK, Perepelkina NI, Patrushev IV, Popov VI. 2003. Role of lipids in the assembly of endoplasmic reticulum and dictyosomes in neuronal cells from the cerebral cortex of Yakutian ground squirrel (Citellus undulatus) during hibernation. Biochemistry (Mosc) 68:783–794.
   PubMed Web of Science ®Google Scholar
• Lee A. 2009. The effects of lipids on channel function. J Biol 8:86.
   PubMedGoogle Scholar
• Lee AG. 2004. How lipids affect the activities of integral membrane proteins. Biochim Biophys Acta (Biomembranes) 1666:62–87.
   PubMed Web of Science ®Google Scholar
• Lees JG, Smith BR, Wien F, Miles AJ, Wallace BA. 2004. CDtool-an integrated software package for circular dichroism spectroscopic data processing, analysis, and archiving. Anal Biochem 332:285–289.
   PubMed Web of Science ®Google Scholar
• Lin C, Lindenbach BD, Pragai BM, McCourt DW, Rice CM. 1994. Processing in the hepatitis C virus E2-NS2 region: Identification of p7 and two distinct E2-specific products with different C termini. J Virol 68:5063–5073.
   PubMed Web of Science ®Google Scholar
• Luik P, Chew C, Aittoniemi J, Chang J, Wentworth P, Dwek RA, Biggin PC, Venien-Bryan C, Zitzmann N. 2009. The 3-dimensional structure of a hepatitis C virus p7 ion channel by electron microscopy. Proc Natl Acad Sci USA 106:12712–12716.
   PubMed Web of Science ®Google Scholar
• Mehnert T, Routh A, Judge PJ, Lam YH, Fischer D, Watts A, Fischer WB. 2007. Biophysical characterization of Vpu from HIV-1 suggests a channel-pore dualism. Proteins: Struct, Func, Gen 70:1488–1497.
   Web of Science ®Google Scholar
• Melton JV, Ewart G, Weir RC, Board PG, Lee E, Gage PW. 2002. Alphavirus 6K proteins form ion channels. J Biol Chem 277:46923–46931.
   PubMed Web of Science ®Google Scholar
• Miles AJ, Wallace BA. 2006. Synchrotron radiation circular dichroism spectroscopy of proteins and applications in structural and functional genomics. Chem Soc Rev 35:39–51.
   PubMed Web of Science ®Google Scholar
• Myers VB, Haydon DA. 1972. Ion transfer across lipid membranes in the presence of gramicidin A. II. The ion selectivity. Biochim Biophys Acta 274:313–322.
   PubMed Web of Science ®Google Scholar
• Navarro J, Toivio-Kinnucan M, Racker E. 1984. Effect of lipid composition on the calcium/adenosine 5′-triphosphate coupling ratio of the Ca2+-ATPase of sarcoplasmic reticulum. Biochemistry 23:130–135.
   PubMed Web of Science ®Google Scholar
• Neil SJ, Zang T, Bieniasz PD. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425–430.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Pavlovic D, Neville DC, Argaud O, Blumberg B, Dwek RA, Fischer WB, Zitzmann N. 2003. The hepatitis C virus p7 protein forms an ion channel that is inhibited by long-alkyl-chain iminosugar derivatives. Proc Natl Acad Sci USA 100:6104–6108.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Sakai A, Claire MS, Faulk K, Govindarajan S, Emerson SU, Purcell RH, Bukh J. 2003. The p7 polypeptide of hepatitis C virus is critical for infectivity and contains functionally important genotype-specific sequences. Proc Natl Acad Sci USA 100:11646–11651.
   PubMed Web of Science ®Google Scholar
• Savitsky A, Golay M. 1964. Smoothing and differentiation of data by simplified least squares procedures. Anal Chem 36:1627–1639.
   Web of Science ®Google Scholar
• Schmidt D, Jiang Q-X, MacKinnon R. 2006. Phospholipids and the origin of cationic gating charges in voltage sensors. Nature 444:775–779.
   PubMed Web of Science ®Google Scholar
• Schnolzer M, Alewood P, Jones A, Alewood D, Kent SB. 1992. In situ neutralization in Boc-chemistry solid phase peptide synthesis. Rapid, high yield assembly of difficult sequences. Int J Pept Protein Res 40:180–193.
   PubMedGoogle Scholar
• Sreerama N, Venyaminov SY, Woody RW. 1999. Estimation of the number of alpha-helical and beta-strand segments in proteins using circular dichroism spectroscopy. Protein Sci 8:370–380.
   PubMed Web of Science ®Google Scholar
• Sreerama N, Woody RW. 1993. A self-consistent method for the analysis of protein secondary structure from circular dichroism. Anal Biochem 209:32–44.
   PubMed Web of Science ®Google Scholar
• Sreerama N, Woody RW. 2000. Estimation of protein secondary structure from circular dichroism spectra: Comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287:252–260.
   PubMed Web of Science ®Google Scholar
• Steinmann E, Penin F, Kallis S, Patel AH, Bartenschlager R, Pietschmann T. 2007. Hepatitis C virus p7 protein is crucial for assembly and release of infectious virions. PLoS Pathog 3:e103.
   PubMed Web of Science ®Google Scholar
• Stouffer AL, Acharya R, Salom D, Levine AS, Di Costanzo L, Soto CS, Tereshko V, Nanda V, Stayrook S, DeGrado WF. 2008. Structural basis for the function and inhibition of an influenza virus proton channel. Nature 451:596–599.
   PubMed Web of Science ®Google Scholar
• Tillman TS, Cascio M. 2003. Effects of membrane lipids on ion channel structure and function. Cell Biochem Biophys 38:161–190.
   PubMed Web of Science ®Google Scholar
• Turnheim K, Gruber J, Wachter C, Ruiz-Gutierrez V. 1999. Membrane phospholipid composition affects function of potassium channels from rabbit colon epithelium. Am J Physiol 277:C83–C90.
   PubMedGoogle Scholar
• Valiyaveetil FI, Zhou Y, MacKinnon R. 2002. Lipids in the structure, folding, and function of the KcsA K+ channel. Biochemistry 41:10771–10777.
   PubMed Web of Science ®Google Scholar
• van Stokkum IH, Spoelder HJ, Bloemendal M, van Grondelle R, Groen FC. 1990. Estimation of protein secondary structure and error analysis from circular dichroism spectra. Anal Biochem 191:110–118.
   PubMed Web of Science ®Google Scholar
• Wallace BA, Mao D. 1984. Circular dichroism analyses of membrane proteins: An examination of differential light scattering and absorption flattening effects in large membrane vesicles and membrane sheets. Anal Biochem 142:317–328.
   PubMed Web of Science ®Google Scholar
• Weber ME, Elliott EK, Gokel GW. 2006. Activity of synthetic ion channels is influenced by cation-pi interactions with phospholipid headgroups. Org Biomol Chem 4:83–89.
   PubMed Web of Science ®Google Scholar
• White SH. 1978. Formation of ‘solvent-free’ black lipid bilayer membranes from glyceryl monooleate dispersed in squalene. Biophys J 23:337–347.
   PubMed Web of Science ®Google Scholar
• Whitmore L, Wallace BA. 2008. Protein secondary structure analyses from circular dichroism spectroscopy: Methods and reference databases. Biopolymers 89:392–400.
   PubMed Web of Science ®Google Scholar
• Wozniak AL, Griffin S, Rowlands D, Harris M, Yi M, Lemon SM, Weinman SA. 2010. Intracellular proton conductance of the hepatitis C virus p7 protein and its contribution to infectious virus production. PLoS Pathog 6:e1001087.
   PubMed Web of Science ®Google Scholar
• Yang Y, Yan Y, Sigworth FJ. 1997. How does the W434F mutation block current in Shaker potassium channels? J Gen Physiol 109:779–789.
   PubMed Web of Science ®Google Scholar