Phenothiazines inhibit hepatitis C virus entry, likely by increasing the fluidity of cholesterol-rich membranes

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 6, 2013, Pages 2571-2581

  Chamoun Emanuelli, Ana M ^a   Pecheur, Eve Isabelle ^c   Simeon, Rudo L ^a   Huang, Da ^d   Cremer, Paul S ^d   Chena, Zhilei ^b  

^a Texas AandM University   (United States)

^b TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^c UNIVERSITÉ DE LYON   (France)

^d TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; CHLORPROMAZINE; FLUPENTIXOL; FLUPHENAZINE; MESORIDAZINE; PHENOTHIAZINE DERIVATIVE; PROCHLORPERAZINE; PROMAZINE; THIORIDAZINE; TRIFLUOPERAZINE; TRIFLUPROMAZINE;

ANTIVIRAL ACTIVITY; ARTICLE; CELL FUSION; CONTROLLED STUDY; HEPATITIS C; HIGH THROUGHPUT SCREENING; LIPID MEMBRANE; MEMBRANE FLUIDITY; NONHUMAN; PRIORITY JOURNAL; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS INHIBITION;

ANTIVIRAL AGENTS; CELL LINE, TUMOR; CELL MEMBRANE; CHOLESTEROL; HEK293 CELLS; HEPACIVIRUS; HEPATOCYTES; HUMANS; MEMBRANE FLUIDITY; PHENOTHIAZINES; VIRUS INTERNALIZATION;

EID: 84877850427     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02593-12     Document Type: Article

References (66)

1. Lauer GM, Walker BD. 2001. Hepatitis C virus infection. N. Engl. J. Med. 345:41-52.
2. Liang TJ, Rehermann B, Seeff LB, Hoofnagle JH. 2000. Pathogenesis, natural history, treatment, and prevention of hepatitis C. Ann. Intern. Med. 132:296-305.
3. Poynard T, Yuen MF, Ratziu V, Lai CL. 2003. Viral hepatitis C. Lancet 362:2095-2100.
4. Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen TL, Liu CC, Maruyama T, Hynes RO, Burton DR, McKeating JA, Rice CM. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623-626.
5. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, Burton DR, Wieland SF, Uprichard SL, Wakita T, Chisari FV. 2005. Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. U. S. A. 102:9294-9299.
6. Pietschmann T, Kaul A, Koutsoudakis G, Shavinskaya A, Kallis S, Steinmann E, Abid K, Negro F, Dreux M, Cosset FL, Bartenschlager R. 2006. Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc. Natl. Acad. Sci. U. S. A. 103:7408-7413.
7. Fried MW. 2002. Side effects of therapy of hepatitis C and their management. Hepatology 36:S237-S244.
8. Welsch C, Jesudian A, Zeuzem S, Jacobson I. 2012. New direct-acting antiviral agents for the treatment of hepatitis C virus infection and perspectives. Gut 61(Suppl 1):i36-i46.
9. Ghany MG, Nelson DR, Strader DB, Thomas DL, Seeff LB, American Association for Study of Liver Diseases. 2011. An update on treatment of genotype 1 chronic hepatitis C virus infection: 2011 practice guideline by the American Association for the Study of Liver Diseases. Hepatology 54:1433-1444.
10. Asselah T, Marcellin P. 2012. Direct acting antivirals for the treatment of chronic hepatitis C: One pill a day for tomorrow. Liver Int. 32(Suppl 1): 88-102.
11. Behrens SE, Tomei L, DeFrancesco R. 1996. Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus. EMBO J. 15:12-22.
12. Lupberger J, Zeisel MB, Xiao F, Thumann C, Fofana I, Zona L, Davis C, Mee CJ, Turek M, Gorke S, Royer C, Fischer B, Zahid MN, Lavillette D, Fresquet J, Cosset FL, Rothenberg SM, Pietschmann T, Patel AH, Pessaux P, Doffoel M, Raffelsberger W, Poch O, McKeating JA, Brino L, Baumert TF. 2011. EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nat. Med. 17:589-595.
13. Samreen B, Khaliq S, Ashfaq UA, Khan M, Afzal N, Shahzad MA, Riaz S, Jahan S. 2012. Hepatitis C virus entry: Role of host and viral factors. Infect. Genet. Evol. 12:1699-1709.
14. Catanese MT, Graziani R, von Hahn T, Moreau M, Huby T, Paonessa G, Santini C, Luzzago A, Rice CM, Cortese R, Vitelli A, Nicosia A. 2007. High-avidity monoclonal antibodies against the human scavenger class B type I receptor efficiently block hepatitis C virus infection in the presence of high-density lipoprotein. J. Virol. 81:8063-8071.
15. Meuleman P, Hesselgesser J, Paulson M, Vanwolleghem T, Desombere I, Reiser H, Leroux-Roels G. 2008. Anti-Cd81 antibodies can prevent a hepatitis C virus infection in vivo. Hepatology 48:1761-1768.
16. Krieger SE, Zeisel MB, Davis C, Thumann C, Harris HJ, Schnober EK, Mee C, Soulier E, Royer C, Lambotin M, Grunert F, Thi VLD, Dreux M, Cosset FL, McKeating JA, Schuster C, Baumert TF. 2010. Inhibition of hepatitis C virus infection by anti-claudin-1 antibodies is mediated by neutralization of E2-CD81-claudin-1 associations. Hepatology 51:1144-1157.
17. Coburn GA, Fisch DN, Moorji SM, de Muys JM, Murga JD, Paul D, Provoncha KP, Rotshteyn Y, Han AQ, Qian D, Maddon PJ, Olson WC. 2012. Novel small-molecule inhibitors of hepatitis C virus entry block viral spread and promote viral clearance in cell culture. PLoS One 7:e35351. doi:10.1371/journal.pone.0035351.
18. Baldick CJ, Wichroski MJ, Pendri A, Walsh AW, Fang J, Mazzucco CE, Pokornowski KA, Rose RE, Eggers BJ, Hsu M, Zhai W, Zhai G, Gerritz SW, Poss MA, Meanwell NA, Cockett MI, Tenney DJ. 2010. A novel small molecule inhibitor of hepatitis C virus entry. PLoS Pathog. 6:e1001086. doi:10.1371/journal.ppat. 1001086.
19. Ciesek S, von Hahn T, Colpitts CC, Schang LM, Friesland M, Steinmann J, Manns MP, Ott M, Wedemeyer H, Meuleman P, Pietschmann T, Steinmann E. 2011. The green tea polyphenol epigallocatechin-3-gallate (EGCG) inhibits hepatitis C virus (HCV) entry. Hepatology 54: 1947-1955.
20. Calland N, Albecka A, Belouzard S, Wychowski C, Duverlie G, Descamps V, Hober D, Dubuisson J, Rouille Y, Seron K. 2012. (?)-Epigallocatechin-3-gallate is a new inhibitor of hepatitis C virus entry. Hepatology 55:720-729.
21. Wagoner J, Negash A, Kane OJ, Martinez LE, Nahmias Y, Bourne N, Owen DM, Grove J, Brimacombe C, McKeating JA, Pecheur EI, Graf TN, Oberlies NH, Lohmann V, Cao F, Tavis JE, Polyak SJ. 2010. Multiple effects of silymarin on the hepatitis C virus lifecycle. Hepatology 51:1912-1921.
22. Haid S, Novodomska A, Gentzsch J, Grethe C, Geuenich S, Bankwitz D, Chhatwal P, Jannack B, Hennebelle T, Bailleul F, Keppler OT, Poenisch M, Bartenschlager R, Hernandez C, Lemasson M, Rosenberg AR, Wong-Staal F, Davioud-Charvet E, Pietschmann T. 2012. A plantderived flavonoid inhibits entry of all HCV genotypes into human hepatocytes. Gastroenterology 143:213-222.
23. Wagoner J, Morishima C, Graf TN, Oberlies NH, Teissier E, Pecheur EI, Tavis JE, Polyak SJ. 2011. Differential in vitro effects of intravenous versus oral formulations of silibinin on the HCV life cycle and inflammation. PLoS One 6:e16464. doi:10.1371/journal.pone.0016464.
24. Teissier E, Zandomeneghi G, Loquet A, Lavillette D, Lavergne JP, Montserret R, Cosset FL, Bockmann A, Meier BH, Penin F, Pecheur EI. 2011. Mechanism of inhibition of enveloped virus membrane fusion by the antiviral drug arbidol. PLoS One 6:e15874. doi:10.1371/journal.pone .0015874.
25. Pluta K, Morak-Mlodawska B, Jelen M. 2011. Recent progress in biological activities of synthesized phenothiazines. Eur. J. Med. Chem. 46:3179-3189.
26. Takacs D, Cerca P, Martins A, Riedl Z, Hajos G, Molnar J, Viveiros M, Couto I, Amaral L. 2011. Evaluation of forty new phenothiazine derivatives for activity against intrinsic efflux pump systems of reference Escherichia coli, Salmonella Enteritidis, Enterococcus faecalis and Staphylococcus aureus strains. In Vivo 25:719-724.
27. Amaral L, Viveiros M, Molnar J. 2004. Antimicrobial activity of phenothiazines. In Vivo 18:725-731.
28. Chockalingam K, Simeon RL, Rice CM, Chen Z. 2010. A cell protection screen reveals potent inhibitors of multiple stages of the hepatitis C virus life cycle. Proc. Natl. Acad. Sci. U. S. A. 107:3764-3769.
29. Gastaminza P, Whitten-Bauer C, Chisari FV. 2010. Unbiased probing of the entire hepatitis C virus life cycle identifies clinical compounds that target multiple aspects of the infection. Proc. Natl. Acad. Sci. U. S. A. 107:291-296.
30. Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, Wolk B, Hatziioannou T, McKeating JA, Bieniasz PD, Rice CM. 2007. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446:801-805.
31. Marukian S, Jones CT, Andrus L, Evans MJ, Ritola KD, Charles ED, Rice CM, Dustin LB. 2008. Cell culture-produced hepatitis C virus does not infect peripheral blood mononuclear cells. Hepatology 48:1843-1850.
32. Lavillette D, Bartosch B, Nourrisson D, Verney G, Cosset FL, Penin F, Pecheur EI. 2006. Hepatitis C virus glycoproteins mediate low pHdependent membrane fusion with liposomes. J. Biol. Chem. 281:3909-3917.
33. Haid S, Pietschmann T, Pecheur EI. 2009. Low pH-dependent hepatitis C virus membrane fusion depends on E2 integrity, target lipid composition, and density of virus particles. J. Biol. Chem. 284:17657-17667.
34. Parasassi T, De Stasio G, d'Ubaldo A, Gratton E. 1990. Phase fluctuation in phospholipid membranes revealed by Laurdan fluorescence. Biophys. J. 57:1179-1186.
35. Takeuchi T, Katsume A, Tanaka T, Abe A, Inoue K, Tsukiyama-Kohara K, Kawaguchi R, Tanaka S, Kohara M. 1999. Real-time detection system for quantification of hepatitisCvirus genome. Gastroenterology 116:636-642.
36. Shulla A, Randall G. 2012. Hepatitis C virus-host interactions, replication, and viral assembly. Curr. Opin. Virol. 2:725-732.
37. Chamoun AM, Chockalingam K, Bobardt M, Simeon R, Chang J, Gallay P, Chen Z. 2012. PD 404,182 is a virocidal small molecule that disrupts hepatitis C virus and human immunodeficiency virus. Antimicrob. Agents Chemother. 56:672-681.
38. Sun X, Yau VK, Briggs BJ, Whittaker GR. 2005. Role of clathrinmediated endocytosis during vesicular stomatitis virus entry into host cells. Virology 338:53-60.
39. Wesolowska O, Michalak K, Hendrich AB. 2011. Direct visualization of phase separation induced by phenothiazine-type antipsychotic drugs in model lipid membranes. Mol. Membr. Biol. 28:103-114.
40. Fadel O, El Kirat K, Morandat S. 2011. The natural antioxidant rosmarinic acid spontaneously penetrates membranes to inhibit lipid peroxidation in situ. Biochim. Biophys. Acta 1808:2973-2980.
41. Parasassi T, Krasnowska EK, Bagatolli L, Gratton E. 1998. LAURDAN andPRODANas polarity-sensitive fluorescent membrane probes. J. Fluoresc. 8:365-373.
42. Pike LJ. 2003. Lipid rafts: Bringing order to chaos. J. Lipid Res. 44:655-667.
43. Freeman BB, Iacono LC, Panetta JC, Gajjar A, Stewart CF. 2006. Using plasma topotecan pharmacokinetics to estimate topotecan exposure in cerebrospinal fluid of children with medulloblastoma. Neuro-Oncol. 8:89-95.
44. Wong-Staal F, Syder AJ, McKelvy JF. 2010. Targeting HCV entry for development of therapeutics. Viruses 2:1718-1733.
45. Teissier E, Pecheur EI. 2007. Lipids as modulators of membrane fusion mediated by viral fusion proteins. Eur. Biophys. J. 36:887-899.
46. Kielian M, Chatterjee PK, Gibbons DL, Lu YE. 2000. Specific roles for lipids in virus fusion and exit. Examples from the alphaviruses. Subcell. Biochem. 34:409-455.
47. Kapadia SB, Barth H, Baumert T, McKeating JA, Chisari FV. 2007. Initiation of hepatitis C virus infection is dependent on cholesterol and cooperativity between CD81 and scavenger receptor B type I. J. Virol. 81:374-383.
48. Aizaki H, Morikawa K, Fukasawa M, Hara H, Inoue Y, Tani H, Saito K, Nishijima M, Hanada K, Matsuura Y, Lai MM, Miyamura T, Wakita T, Suzuki T. 2008. Critical role of virion-associated cholesterol and sphingolipid in hepatitis C virus infection. J. Virol. 82:5715-5724.
49. Sainz B, Jr, Barretto N, Martin DN, Hiraga N, Imamura M, Hussain S, Marsh KA, Yu X, Chayama K, Alrefai WA, Uprichard SL. 2012. Identification of the Niemann-Pick C1-like 1 cholesterol absorption receptor as a new hepatitis C virus entry factor. Nat. Med. 18:281-285.
50. Ge L, Qi W, Wang LJ, Miao HH, Qu YX, Li BL, Song BL. 2011. Flotillins play an essential role in Niemann-Pick C1-like 1-mediated cholesterol uptake. Proc. Natl. Acad. Sci. U. S. A. 108:551-556.
51. Seigneuret M. 2006. Complete predicted three-dimensional structure of the facilitator transmembrane protein and hepatitis C virus receptor CD81: Conserved and variable structural domains in the tetraspanin superfamily. Biophys. J. 90:212-227.
52. Lavillette D, Pecheur EI, Donot P, Fresquet J, Molle J, Corbau R, Dreux M, Penin F, Cosset FL. 2007. Characterization of fusion determinants points to the involvement of three discrete regions of both E1 and E2 glycoproteins in the membrane fusion process of hepatitisCvirus. J. Virol. 81:8752-8765.
53. Rawat SS, Viard M, Gallo SA, Rein A, Blumenthal R, Puri A. 2003. Modulation of entry of enveloped viruses by cholesterol and sphingolipids. Mol. Membr. Biol. 20:243-254.
54. Wennberg CL, van der Spoel D, Hub JS. 2012. Large influence of cholesterol on solute partitioning into lipid membranes. J. Am. Chem. Soc. 134:5351-5361.
55. Spector AA, Yorek MA. 1985. Membrane lipid composition and cellular function. J. Lipid Res. 26:1015-1035.
56. McIntosh TJ. 1978. The effect of cholesterol on the structure of phosphatidylcholine bilayers. Biochim. Biophys. Acta 513:43-58.
57. Stiasny K, Heinz FX. 2004. Effect of membrane curvature-modifying lipids on membrane fusion by tick-borne encephalitis virus. J. Virol. 78: 8536-8542.
58. Pecheur EI, Martin I, Bienvenue A, Ruysschaert JM, Hoekstra D. 2000. Protein-induced fusion can be modulated by target membrane lipids through a structural switch at the level of the fusion peptide. J. Biol. Chem. 275:3936-3942.
59. Rog T, Pasenkiewicz-Gierula M, Vattulainen I, Karttunen M. 2007. What happens if cholesterol is made smoother: Importance of methyl substituents in cholesterol ring structure on phosphatidylcholine-sterol interaction. Biophys. J. 92:3346-3357.
60. Kielian MC, Helenius A. 1984. Role of cholesterol in fusion of Semliki Forest virus with membranes. J. Virol. 52:281-283.
61. Marquardt MT, Phalen T, Kielian M. 1993. Cholesterol is required in the exit pathway of Semliki Forest virus. J. Cell Biol. 123:57-65.
62. Lorusso D, Pietragalla A, Mainenti S, Masciullo V, Di Vagno G, Scambia G. 2010. Role of topotecan in gynaecological cancers: Current indications and perspectives. Crit. Rev. Oncol. Hematol. 74:163-174.
63. Nakashio A, Fujita N, Tsuruo T. 2002. Topotecan inhibits VEGF-and bFGF-induced vascular endothelial cell migration via downregulation of the PI3K-Akt signaling pathway. Int. J. Cancer 98:36-41.
64. Tan C, de Noronha RG, Roecker AJ, Pyrzynska B, Khwaja F, Zhang Z, Zhang H, Teng Q, Nicholson AC, Giannakakou P, Zhou W, Olson JJ, Pereira MM, Nicolaou KC, Van Meir EG. 2005. Identification of a novel small-molecule inhibitor of the hypoxia-inducible factor 1 pathway. Cancer Res. 65:605-612.
65. Shen J, Carcaboso AM, Hubbard KE, Tagen M, Wynn HG, Panetta JC, Waters CM, Elmeliegy MA, Stewart CF. 2009. Compartment-specific roles of ATP-binding cassette transporters define differential topotecan distribution in brain parenchyma and cerebrospinal fluid. Cancer Res. 69:5885-5892.
66. Kohno T, Tsuge M, Hayes CN, Hatakeyama T, Ohnishi M, Abe H, Miki D, Hiraga N, Imamura M, Takahashi S, Ochi H, Tanaka S, Chayama K. 2012. Identification of novel HCV deletion mutants in chronic hepatitis C patients. Antivir. Ther. 17:1551-1561.