Selection of a hepatitis C virus with altered entry factor requirements reveals a genetic interaction between the E1 glycoprotein and claudins

Hepatology

Volumn 62, Issue 4, 2015, Pages 1059-1069

  Hopcraft, Sharon E ^a   Evans, Matthew J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN; CLAUDIN 6; CLAUDIN 9; GLYCOPROTEIN E1; UNCLASSIFIED DRUG; CLAUDIN 1; E1 PROTEIN, HEPATITIS C VIRUS; VIRUS ENVELOPE PROTEIN;

ARTICLE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; GENE INTERACTION; GENOTYPE; HEPATITIS C; HEPATITIS C VIRUS; HOST CELL; HUMAN; HUMAN CELL; PHENOTYPE; PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS MUTATION; CELL CULTURE; GENETICS; HEPACIVIRUS; VIRUS ENTRY;

CELLS, CULTURED; CLAUDIN-1; HEPACIVIRUS; HUMANS; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

EID: 84942552545     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.27815     Document Type: Article

References (34)

1. Messina JP, Humphreys I, Flaxman A, Brown A, Cooke GS, Pybus OG, Barnes E. Global distribution and prevalence of hepatitis C virus genotypes. Hepatology 2015;61:77-87.
2. Brown RS, Jr. Hepatitis C and liver transplantation. Nature 2005;436:973-978.
3. Ploss A, Evans MJ. Hepatitis C virus host cell entry. Curr Opin Virol 2012;2:14-19.
4. Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, Wolk B, et al. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 2007;446:801-805.
5. Zheng A, Yuan F, Li Y, Zhu F, Hou P, Li J, et al. Claudin-6 and claudin-9 function as additional coreceptors for hepatitis C virus. J Virol 2007;81:12465-12471.
6. Meertens L, Bertaux C, Cukierman L, Cormier E, Lavillette D, Cosset FL, Dragic T. The tight junction proteins claudin-1, -6, and -9 are entry cofactors for hepatitis C virus. J Virol 2008;82:3555-3560.
7. Fofana I, Zona L, Thumann C, Heydmann L, Durand SC, Lupberger J, et al. Functional analysis of claudin-6 and claudin-9 as entry factors for hepatitis C virus infection of human hepatocytes by using monoclonal antibodies. J Virol 2013;87:10405-10410.
8. Haid S, Grethe C, Dill MT, Heim M, Kaderali L, Pietschmann T. Isolate-dependent use of claudins for cell entry by hepatitis C virus. Hepatology 2014;59:24-34.
9. Yang W, Qiu C, Biswas N, Jin J, Watkins SC, Montelaro RC, et al. Correlation of the tight junction-like distribution of Claudin-1 to the cellular tropism of hepatitis C virus. J Biol Chem 2008;283:8643-8653.
10. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, et al. RNA-guided human genome engineering via Cas9. Science 2013;339:823-826.
11. Michta ML, Hopcraft SE, Narbus CM, Kratovac Z, Israelow B, Sourisseau M, Evans MJ. Species-specific regions of occludin required by hepatitis C virus for cell entry. J Virol 2010;84:11696-11708.
12. Sirven A, Ravet E, Charneau P, Zennou V, Coulombel L, Guetard D, et al. Enhanced transgene expression in cord blood CD34(+)-derived hematopoietic cells, including developing T cells and NOD/SCID mouse repopulating cells, following transduction with modified trip lentiviral vectors. Mol Ther 2001;3:438-448.
13. Zennou V, Petit C, Guetard D, Nerhbass U, Montagnier L, Charneau P. HIV-1 genome nuclear import is mediated by a central DNA flap. Cell 2000;101:173-185.
14. Sabo MC, Luca VC, Prentoe J, Hopcraft SE, Blight KJ, Yi M, et al. Neutralizing monoclonal antibodies against hepatitis C virus E2 protein bind discontinuous epitopes and inhibit infection at a postattachment step. J Virol 2011;85:7005-7019.
15. Blight KJ, McKeating JA, Rice CM. Highly permissive cell lines for hepatitis C virus genomic and subgenomic RNA replication. J Virol 2002;76:13001-13014.
16. Hotzel I, Chiang V, Diao J, Pantua H, Maun HR, Kapadia SB. Efficient production of antibodies against a mammalian integral membrane protein by phage display. Protein Eng Des Sel 2011;24:679-689.
17. Vieyres G, Pietschmann T. Entry and replication of recombinant hepatitis C viruses in cell culture. Methods 2013;59:233-248.
18. Gottwein JM, Scheel TK, Jensen TB, Lademann JB, Prentoe JC, Knudsen ML, et al. Development and characterization of hepatitis C virus genotype 1-7 cell culture systems: role of CD81 and scavenger receptor class B type I and effect of antiviral drugs. Hepatology 2009;49:364-377.
19. Ploss A, Evans MJ, Gaysinskaya VA, Panis M, You H, de Jong YP, Rice CM. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 2009;457:882-886.
20. Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen TL, Liu CC, et al. Complete replication of hepatitis C virus in cell culture. Science 2005;309:623-626.
21. Carroll SS, Tomassini JE, Bosserman M, Getty K, Stahlhut MW, Eldrup AB, et al. Inhibition of hepatitis C virus RNA replication by 2'-modified nucleoside analogs. J Biol Chem 2003;278:11979-11984.
22. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 2012;337:816-821.
23. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, et al. Multiplex genome engineering using CRISPR/Cas systems. Science 2013;339:819-823.
24. Pietschmann T, Kaul A, Koutsoudakis G, Shavinskaya A, Kallis S, Steinmann E, et al. Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc Natl Acad Sci U S A 2006;103:7408-7413.
25. Bitzegeio J, Bankwitz D, Hueging K, Haid S, Brohm C, Zeisel MB, et al. Adaptation of hepatitis C virus to mouse CD81 permits infection of mouse cells in the absence of human entry factors. PLoS Pathog 2010;6:e1000978.
26. Bukh J, Miller RH, Purcell RH. Genetic heterogeneity of hepatitis C virus: Quasispecies and genotypes. Semin Liver Dis 1995;15:41-63.
27. Sourisseau M, Michta ML, Zony C, Israelow B, Hopcraft SE, Narbus CM, et al. Temporal analysis of hepatitis C virus cell entry with occludin directed blocking antibodies. PLoS Pathog 2013;9:e1003244.
28. Haid S, Windisch MP, Bartenschlager R, Pietschmann T. Mouse-specific residues of claudin-1 limit hepatitis C virus genotype 2a infection in a human hepatocyte cell line. J Virol 2010;84:964-975.
29. Chhatwal P, Bankwitz D, Gentzsch J, Frentzen A, Schult P, Lohmann V, Pietschmann T. Bile acids specifically increase hepatitis C virus RNA-replication. PLoS One 2012;7:e36029.
30. Goffard A, Dubuisson J. Glycosylation of hepatitis C virus envelope proteins. Biochimie 2003;85:295-301.
31. Douam F, Dao Thi VL, Maurin G, Fresquet J, Mompelat D, Zeisel MB, Baumert TF, et al. Critical interaction between E1 and E2 glycoproteins determines binding and fusion properties of hepatitis C virus during cell entry. Hepatology 2014;59:776-788.
32. Krieger SE, Zeisel MB, Davis C, Thumann C, Harris HJ, Schnober EK, et al. Inhibition of hepatitis C virus infection by anti-claudin-1 antibodies is mediated by neutralization of E2-CD81-claudin-1 associations. Hepatology 2010;51:1144-1157.
33. Fofana I, Krieger SE, Grunert F, Glauben S, Xiao F, Fafi-Kremer S, et al. Monoclonal anti-claudin 1 antibodies prevent hepatitis C virus infection of primary human hepatocytes. Gastroenterology 2010;139:953-964, 964.e1-4.
34. Mailly L, Xiao F, Lupberger J, Wilson GK, Aubert P, Duong FH, et al. Clearance of persistent hepatitis C virus infection in humanized mice using a claudin-1-targeting monoclonal antibody. Nat Biotechnol 2015. doi: 10.1038/nbt.3179 [Epub ahead of print].