Infectivity of hepatitis C virus correlates with the amount of envelope protein E2: Development of a new aptamer-based assay system suitable for measuring the infectious titer of HCV

Virology

Volumn 439, Issue 1, 2013, Pages 13-22

  Park, Ji Hoon ^a   Jee, Min Hyeok ^a   Kwon, Oh Sung ^a   Keum, Sun Ju ^a   Jang, Sung Key ^a  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

Author keywords

Aptamer; Detection; E2; ELASA; ELISA; HCV; Hepatitis C virus; Infectious HCV particles; Infectivity measurement; SELEX

Indexed keywords

ALPHA INTERFERON; APTAMER; DACLATASVIR; GLYCOPROTEIN E2; VIRUS RNA;

ARTICLE; CELL CULTURE; CONTROLLED STUDY; DRUG EFFECT; ENZYME LINKED APTOSORBENT ASSAY; GENOTYPE; HEPATITIS C VIRUS; IMMUNOASSAY; IN VITRO STUDY; LIMIT OF DETECTION; NONHUMAN; PRIORITY JOURNAL; PROCESS DEVELOPMENT; QUANTITATIVE ANALYSIS; SENSITIVITY ANALYSIS; VIRUS INFECTIVITY; VIRUS PARTICLE;

APTAMERS, NUCLEOTIDE; HEPACIVIRUS; HUMANS; SELEX APTAMER TECHNIQUE; VIRAL ENVELOPE PROTEINS; VIRAL LOAD;

HEPATITIS C VIRUS;

EID: 84874971734     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.01.014     Document Type: Article

References (61)

1. Armstrong G.L., Wasley A., Simard E.P., McQuillan G.M., Kuhnert W.L., Alter M.J. The prevalence of hepatitis C virus infection in the United States, 1999 through 2002. Ann. Intern. Med. 2006, 144:705-714.
2. Bartosch B., Dubuisson J., Cosset F.L Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J. Exp. Med. 2003, 197:633-642.
3. Bianchi A., Crotta S., Brazzoli M., Foung S.K., Merola M. Hepatitis C virus e2 protein ectodomain is essential for assembly of infectious virions. Int. J. Hepatol. 2011, 968161.
4. Brimacombe C.L., Grove J., Meredith L.W., Hu K., Syder A.J., Flores M.V., Timpe J.M., Krieger S.E., Baumert T.F., Tellinghuisen T.L., Wong-Staal F., Balfe P., McKeating J.A. Neutralizing antibody-resistant hepatitis C virus cell-to-cell transmission. J. Virol. 2011, 85:596-605.
5. Brody E.N., Gold L. Aptamers as therapeutic and diagnostic agents. J. Biotechnol. 2000, 74:5-13.
6. Bukh J. A critical role for the chimpanzee model in the study of hepatitis C. Hepatology 2004, 39:1469-1475.
7. Chen F., Hu Y., Li D., Chen H., Zhang X.L. CS-SELEX generates high-affinity ssDNA aptamers as molecular probes for hepatitis C virus envelope glycoprotein E2. PLoS One 2009, 4:e8142.
8. Cuesta A.M., Sainz-Pastor N., Bonet J., Oliva B., Alvarez-Vallina L. Multivalent antibodies: when design surpasses evolution. Trends Biotechnol. 2010, 28:355-362.
9. Dubuisson J., Helle F., Cocquerel L. Early steps of the hepatitis C virus life cycle. Cell. Microbiol. 2008, 10:821-827.
10. Dubuisson J., Rice C.M. Hepatitis C virus glycoprotein folding: disulfide bond formation and association with calnexin. J. Virol. 1996, 70:778-786.
11. Ellington A.D. RNA selection. Aptamers achieve the desired recognition. Curr. Biol. 1994, 4:427-429.
12. Ellington A.D., Szostak J.W. In vitro selection of RNA molecules that bind specific ligands. Nature 1990, 346:818-822.
13. Engvall E., Perlmann P. Enzyme-linked immunosorbent assay (ELISA). Quant. Assay Immunoglobulin G. Immunochem. 1971, 8:871-874.
14. Esteban J.I., Sauleda S., Quer J. The changing epidemiology of hepatitis C virus infection in Europe. J. Hepatol. 2008, 48:148-162.
15. Evans M.J., von Hahn T., Tscherne D.M., Syder A.J., Panis M., Wolk B., Hatziioannou T., McKeating J.A., Bieniasz P.D., Rice C.M. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 2007, 446:801-805.
16. Falkowska E., Kajumo F., Garcia E., Reinus J., Dragic T. Hepatitis C virus envelope glycoprotein E2 glycans modulate entry, CD81 binding, and neutralization. J. Virol. 2007, 81:8072-8079.
17. Famulok M., Hartig J.S., Mayer G. Functional aptamers and aptazymes in biotechnology, diagnostics, and therapy. Chem. Rev. 2007, 107:3715-3743.
18. Fenouillet E., Lavillette D., Loureiro S., Krashias G., Maurin G., Cosset F.L., Jones I.M., Barbouche R Contribution of redox status to hepatitis C virus E2 envelope protein function and antigenicity. J. Biol. Chem. 2008, 283:26340-26348.
19. Fried M.W., Shiffman M.L., Reddy K.R., Smith C., Marinos G., Goncales F.L., Haussinger D., Diago M., Carosi G., Dhumeaux D., Craxi A., Lin A., Hoffman J., Yu J. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N. Engl. J. Med. 2002, 347:975-982.
20. Gao M., Nettles R.E., Belema M., Snyder L.B., Nguyen V.N., Fridell R.A., Serrano-Wu M.H., Langley D.R., Sun J.H., O'Boyle D.R., Lemm J.A., Wang C., Knipe J.O., Chien C., Colonno R.J., Grasela D.M., Meanwell N.A., Hamann L.G. Chemical genetics strategy identifies an HCV NS5A inhibitor with a potent clinical effect. Nature 2010, 465:96-100.
21. Gastaminza P., Dryden K.A., Boyd B., Wood M.R., Law M., Yeager M., Chisari F.V. Ultrastructural and biophysical characterization of hepatitis C virus particles produced in cell culture. J. Virol. 2010, 84:10999-11009.
22. Gastaminza P., Kapadia S.B., Chisari F.V. Differential biophysical properties of infectious intracellular and secreted hepatitis C virus particles. J. Virol. 2006, 80:11074-11081.
23. Goffard A., Callens N., Bartosch B., Wychowski C., Cosset F.L., Montpellier C., Dubuisson J Role of N-linked glycans in the functions of hepatitis C virus envelope glycoproteins. J. Virol. 2005, 79:8400-8409.
24. Goffard A., Dubuisson J. Glycosylation of hepatitis C virus envelope proteins. Biochimie 2003, 85:295-301.
25. Gold L. Oligonucleotides as research, diagnostic, and therapeutic agents. J. Biol. Chem. 1995, 270:13581-13584.
26. Gold L., Ayers D., Bertino J., Bock C., Bock A., Brody E.N., Carter J., Dalby A.B., Eaton B.E., Fitzwater T., Flather D., Forbes A., Foreman T., Fowler C., Gawande B., Goss M., Gunn M., Gupta S., Halladay D., Heil J., Heilig J., Hicke B., Husar G., Janjic N., Jarvis T., Jennings S., Katilius E., Keeney T.R., Kim N., Koch T.H., Kraemer S., Kroiss L., Le N., Levine D., Lindsey W., Lollo B., Mayfield W., Mehan M., Mehler R., Nelson S.K., Nelson M., Nieuwlandt D., Nikrad M., Ochsner U., Ostroff R.M., Otis M., Parker T., Pietrasiewicz S., Resnicow D.I., Rohloff J., Sanders G., Sattin S., Schneider D., Singer B., Stanton M., Sterkel A., Stewart A., Stratford S., Vaught J.D., Vrkljan M., Walker J.J., Watrobka M., Waugh S., Weiss A., Wilcox S.K., Wolfson A., Wolk S.K., Zhang C., Zichi D. Aptamer-based multiplexed proteomic technology for biomarker discovery. PLoS One 2010, 5:e15004.
27. Gold L., Polisky B., Uhlenbeck O., Yarus M. Diversity of oligonucleotide functions. Annu. Rev. Biochem. 1995, 64:763-797.
28. Gottwein J.M., Bukh J. Cutting the gordian knot-development and biological relevance of hepatitis C virus cell culture systems. Adv. Virus. Res. 2008, 71:51-133.
29. Grove J., Nielsen S., Zhong J., Bassendine M.F., Drummer H.E., Balfe P., McKeating J.A. Identification of a residue in hepatitis C virus E2 glycoprotein that determines scavenger receptor BI and CD81 receptor dependency and sensitivity to neutralizing antibodies. J. Virol. 2008, 82:12020-12029.
30. Hadlock K.G., Lanford R.E., Perkins S., Rowe J., Yang Q., Levy S., Pileri P., Abrignani S., Foung S.K. Human monoclonal antibodies that inhibit binding of hepatitis C virus E2 protein to CD81 and recognize conserved conformational epitopes. J. Virol. 2000, 74:10407-10416.
31. Hoofnagle J.H. Course and outcome of hepatitis C. Hepatology 2002, 36:S21-29.
32. Keum S.J., Park S.M., Park J.H., Jung J.H., Shin E.J., Jang S.K. The specific infectivity of hepatitis C virus changes through its life cycle. Virology 2012, 433:462-470.
33. Kim C.S., Jung J.H., Wakita T., Yoon S.K., Jang S.K. Monitoring the antiviral effect of alpha interferon on individual cells. J. Virol. 2007, 81:8814-8820.
34. Krey T., d'Alayer J., Kikuti C.M., Saulnier A., Damier-Piolle L., Petitpas I., Johansson D.X., Tawar R.G., Baron B., Robert B., England P., Persson M.A., Martin A., Rey F.A. The disulfide bonds in glycoprotein E2 of hepatitis C virus reveal the tertiary organization of the molecule. PLoS Pathog. 2010, 6:e1000762.
35. Li P., Wan Q., Feng Y., Liu M., Wu J., Chen X., Zhang X.L. Engineering of N-glycosylation of hepatitis C virus envelope protein E2 enhances T cell responses for DNA immunization. Vaccine 2007, 25:1544-1551.
36. Lindenbach B.D., Evans M.J., Syder A.J., Wolk B., Tellinghuisen T.L., Liu C.C., Maruyama T., Hynes R.O., Burton D.R., McKeating J.A., Rice C.M. Complete replication of hepatitis C virus in cell culture. Science 2005, 309:623-626.
37. Liu Z., Tian Y., Machida K., Lai M.M., Luo G., Foung S.K., Ou J.H. Transient activation of the PI3K-AKT pathway by HCV to enhance viral entry. J. Biol. Chem 2012.
38. Mazumdar B., Banerjee A., Meyer K., Ray R. Hepatitis C virus E1 envelope glycoprotein interacts with apolipoproteins in facilitating entry into hepatocytes. Hepatology 2011, 54:1149-1156.
39. McCaffrey K., Boo I., Tewierek K., Edmunds M.L., Poumbourios P., Drummer H.E. Role of conserved cysteine residues in hepatitis C virus glycoprotein e2 folding and function. J. Virol. 2012, 86:3961-3974.
40. Mellor J., Hawkins A., Simmonds P. Genotype dependence of hepatitis C virus load measurement in commercially available quantitative assays. J. Clin. Microbiol. 1999, 37:2525-2532.
41. Memon M.I., Memon M.A. Hepatitis C: an epidemiological review. J. Viral. Hepatitis. 2002, 9:84-100.
42. Merz A., Long G., Hiet M.S., Brugger B., Chlanda P., Andre P., Wieland F., Krijnse-Locker J., Bartenschlager R. Biochemical and morphological properties of hepatitis C virus particles and determination of their lipidome. J. Biol. Chem. 2011, 286:3018-3032.
43. Op De Beeck A., Cocquerel L., Dubuisson J. Biogenesis of hepatitis C virus envelope glycoproteins. J. Gen. Virol. 2001, 82:2589-2595.
44. Op De Beeck A., Montserret R., Duvet S., Cocquerel L., Cacan R., Barberot B., Le Maire M., Penin F., Dubuisson J. The transmembrane domains of hepatitis C virus envelope glycoproteins E1 and E2 play a major role in heterodimerization. J. Biol. Chem. 2000, 275:31428-31437.
45. Patel D.J., Suri A.K., Jiang F., Jiang L., Fan P., Kumar R.A., Nonin S. Structure, recognition and adaptive binding in RNA aptamer complexes. J. Mol. Biol. 1997, 272:645-664.
46. Pileri P., Uematsu Y., Campagnoli S., Galli G., Falugi F., Petracca R., Weiner A.J., Houghton M., Rosa D., Grandi G., Abrignani S. Binding of hepatitis C virus to CD81. Science 1998, 282:938-941.
47. Ploss A., Evans M.J., Gaysinskaya V.A., Panis M., You H., de Jong Y.P., Rice C.M Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 2009, 457:882-886.
48. Reed K.E., Rice C.M. Overview of hepatitis C virus genome structure, polyprotein processing, and protein properties. Curr. Top. Microbiol. Immunol. 2000, 242:55-84.
49. Roingeard P., Hourioux C., Blanchard E., Brand D., Ait-Goughoulte M. Hepatitis C virus ultrastructure and morphogenesis. Biology of the cell/ under the auspices of the European Cell Biology Organization 2004, 96:103-108.
50. Scarselli E., Ansuini H., Cerino R., Roccasecca R.M., Acali S., Filocamo G., Traboni C., Nicosia A., Cortese R., Vitelli A. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J. 2002, 21:5017-5025.
51. Simmonds P., Bukh J., Combet C., Deleage G., Enomoto N., Feinstone S., Halfon P., Inchauspe G., Kuiken C., Maertens G., Mizokami M., Murphy D.G., Okamoto H., Pawlotsky J.M., Penin F., Sablon E., Shin I.T., Stuyver L.J., Thiel H.J., Viazov S., Weiner A.J., Widell A. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 2005, 42:962-973.
52. Slater-Handshy T., Droll D.A., Fan X., Di Bisceglie A.M., Chambers T.J. HCV E2 glycoprotein: mutagenesis of N-linked glycosylation sites and its effects on E2 expression and processing. Virology 2004, 319:36-48.
53. Tanaka E., Ohue C., Aoyagi K., Yamaguchi K., Yagi S., Kiyosawa K., Alter H.J. Evaluation of a new enzyme immunoassay for hepatitis C virus (HCV) core antigen with clinical sensitivity approximating that of genomic amplification of HCV RNA. Hepatology 2000, 32:388-393.
54. Tuerk C., Gold L. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 1990, 249:505-510.
55. Vaught J.D., Bock C., Carter J., Fitzwater T., Otis M., Schneider D., Rolando J., Waugh S., Wilcox S.K., Eaton B.E. Expanding the chemistry of DNA for in vitro selection. J. Am. Chem. Soc. 2010, 132:4141-4151.
56. Vermehren J., Sarrazin C. New HCV therapies on the horizon. Clinical microbiology and infection. (the official publication). Eur. Soc. Clin. Microbiol. Infect. Dis. 2011, 17:122-134.
57. Vieyres G., Thomas X., Descamps V., Duverlie G., Patel A.H., Dubuisson J. Characterization of the envelope glycoproteins associated with infectious hepatitis C virus. J. Virol. 2010, 84:10159-10168.
58. Yi M., Ma Y., Yates J., Lemon S.M. Compensatory mutations in E1, p7, NS2, and NS3 enhance yields of cell culture-infectious intergenotypic chimeric hepatitis C virus. J. Virol. 2007, 81:629-638.
59. Yi, M., Villanueva, R.A., Thomas, D.L., Wakita, T., Lemon, S.M., 2006. Production of infectious genotype 1a hepatitis C virus (Hutchinson strain) in cultured human hepatoma cells. In: Proceedings of the National Academy of Sciences of the United States of America 103, pp. 2310-2315.
60. Zeuzem S. Heterogeneous virologic response rates to interferon-based therapy in patients with chronic hepatitis C: who responds less well?. Ann. Intern. Med. 2004, 140:370-381.
61. Zhong J., Gastaminza P., Cheng G., Kapadia S., Kato T., Burton D.R., Wieland S.F., Uprichard S.L., Wakita T., Chisari F.V. Robust hepatitis C virus infection in vitro. PNAS 2005, 102:9294-9299.