593
Views
12
CrossRef citations to date
0
Altmetric
Articles

Structure–function analysis of hepatitis C virus envelope glycoproteins E1 and E2

, , , , &
Pages 1682-1694 | Received 23 May 2014, Accepted 15 Sep 2014, Published online: 15 Oct 2014

References

  • Afzal, S., Idrees, M., & Hussain, M. (2014). De Novo modeling of envelope 2 protein of HCV isolated from Pakistani patient and epitopes prediction for vaccine development. Journal of Translational Medicine, 12, 1–9.10.1186/1479-5876-12-115
  • Ashfaq, U. A., Javed, T., Rehman, S., Nawaz, Z., & Riazuddin, S. (2011). An overview of HCV molecular biology, replication and immune responses. Virology Journal, 8, 1–10.10.1186/1743-422X-8-161
  • Barker, W. C., Mazumder, R., Vasudevan, S., Sagripanti, J. L., & Wu, C. H. (2009). Sequence signatures in envelope protein may determine whether flaviviruses produce hemorrhagic or encephalitic syndromes. Virus Genes, 39, 1–9.10.1007/s11262-009-0343-4
  • Benkert, P., Kunzli, M., & Schwede, T. (2009). QMEAN server for protein model quality estimation. Nucleic Acids Research, 37, W510–W514.10.1093/nar/gkp322
  • Beyene, A., Basu, A., Meyer, K., & Ray, R. (2002). Hepatitis C virus envelope glycoproteins and potential for vaccine development. Vox Sanguinis, 83(Suppl. 1), 27–32.10.1111/j.1423-0410.2002.tb05262.x
  • Bhattacharya, A., Tejero, R., & Montelione, G. T. (2007). Evaluating protein structures determined by structural genomics consortia. Proteins, 66, 778–795.
  • Brown, E. N., & Ramaswamy, S. (2007). Quality of protein crystal structures. Acta Crystallographica Section D: Biological Crystallography, 63, 941–950.10.1107/S0907444907033847
  • Callens, N., Ciczora, Y., Bartosch, B., Vu-Dac, N., Cosset, F. L., Pawlotsky, J. M., … Dubuisson, J. (2005). Basic residues in hypervariable region 1 of hepatitis C virus envelope glycoprotein E2 contribute to virus entry. Journal of Virology, 79, 15331–15341.10.1128/JVI.79.24.15331-15341.2005
  • Chakrabarti, S., & Sowdhamini, R. (2004). Regions of minimal structural variation among members of protein domain superfamilies: Application to remote homology detection and modelling using distant relationships. FEBS Letters, 569, 31–36.10.1016/j.febslet.2004.05.028
  • Christen, M., Hunenberger, P. H., Bakowies, D., Baron, R., Burgi, R., Geerke, D. P., … van Gunsteren, W. F. (2005). The GROMOS software for biomolecular simulation: GROMOS05. Journal of Computational Chemistry, 26, 1719–1751.10.1002/(ISSN)1096-987X
  • Cocquerel, L., Voisset, C., & Dubuisson, J. (2006). Hepatitis C virus entry: Potential receptors and their biological functions. Journal of General Virology, 87, 1075–1084.10.1099/vir.0.81646-0
  • Costin, J. M., Zaitseva, E., Kahle, K. M., Nicholson, C. O., Rowe, D. K., Graham, A. S., … Isern, S. (2013). Mechanistic study of broadly neutralizing human monoclonal antibodies against dengue virus that target the fusion loop. Journal of Virology, 87, 52–66.10.1128/JVI.02273-12
  • Delport, W., Scheffler, K., & Seoighe, C. (2009). Models of coding sequence evolution. Brief Bioinform, 10, 97–109.
  • Drummer, H. E., Boo, I., & Poumbourios, P. (2007). Mutagenesis of a conserved fusion peptide-like motif and membrane-proximal heptad-repeat region of hepatitis C virus glycoprotein E1. Journal of General Virology, 88, 1144–1148.10.1099/vir.0.82567-0
  • DuBois, R. M., Vaney, M. C., Tortorici, M. A., Kurdi, R. A., Barba-Spaeth, G., Krey, T., & Rey, F. A. (2013). Functional and evolutionary insight from the crystal structure of rubella virus protein E1. Nature, 493, 552–556.10.1038/nature11741
  • Dubuisson, J., & Rice, C. M. (1996). Hepatitis C virus glycoprotein folding: Disulfide bond formation and association with calnexin. Journal of Virology, 70, 778–786.
  • Fiser, A., & Sali, A. (2003). Modeller: Generation and refinement of homology-based protein structure models. Methods in Enzymology, 374, 461–491.10.1016/S0076-6879(03)74020-8
  • Flint, M., Maidens, C., Loomis-Price, L. D., Shotton, C., Dubuisson, J., Monk, P., … McKeating, J. A. (1999). Characterization of hepatitis C virus E2 glycoprotein interaction with a putative cellular receptor, CD81. Journal of Virology, 73, 6235–6244.
  • Flint, M., Thomas, J. M., Maidens, C. M., Shotton, C., Levy, S., Barclay, W. S., & McKeating, J. A. (1999). Functional analysis of cell surface-expressed hepatitis C virus E2 glycoprotein. Journal of Virology, 73, 6782–6790.
  • Forns, X., Thimme, R., Govindarajan, S., Emerson, S. U., Purcell, R. H., Chisari, F. V., & Bukh, J. (2000). Hepatitis C virus lacking the hypervariable region 1 of the second envelope protein is infectious and causes acute resolving or persistent infection in chimpanzees. Proceedings of the National Academy of Sciences, 97, 13318–13323.10.1073/pnas.230453597
  • Fournillier, A., Wychowski, C., Boucreux, D., Baumert, T. F., Meunier, J. C., Jacobs, D., … Inchauspe, G. (2001). Induction of hepatitis C virus E1 envelope protein-specific immune response can be enhanced by mutation of N-glycosylation sites. Journal of Virology, 75, 12088–12097.10.1128/JVI.75.24.12088-12097.2001
  • Garry, R. F., & Dash, S. (2003). Proteomics computational analyses suggest that hepatitis C virus E1 and pestivirus E2 envelope glycoproteins are truncated class II fusion proteins. Virology, 307, 255–265.10.1016/S0042-6822(02)00065-X
  • Geiss, B. J., Stahla, H., Hannah, A. M., Gari, A. M., & Keenan, S. M. (2009). Focus on flaviviruses: Current and future drug targets. Future Medicinal Chemistry, 1, 327–344.10.4155/fmc.09.27
  • Gibrat, J. F., Garnier, J., & Robson, B. (1987). Further developments of protein secondary structure prediction using information theory new parameters and consideration of residue pairs. Journal of Molecular Biology, 198, 425–443.
  • Goffard, A., Callens, N., Bartosch, B., Wychowski, C., Cosset, F. L., Montpellier, C., & Dubuisson, J. (2005). Role of N-linked glycans in the functions of hepatitis C virus envelope glycoproteins. Journal of Virology, 79, 8400–8409.10.1128/JVI.79.13.8400-8409.2005
  • Grove, J., Nielsen, S., Zhong, J., Bassendine, M. F., Drummer, H. E., Balfe, P., & McKeating, J. A. (2008). Identification of a residue in hepatitis C virus E2 glycoprotein that determines scavenger receptor BI and CD81 receptor dependency and sensitivity to neutralizing antibodies. Journal of Virology, 82, 12020–12029.10.1128/JVI.01569-08
  • Hart, G. W. (1992). Glycosylation. Current Opinion in Cell Biology, 4, 1017–1023.10.1016/0955-0674(92)90134-X
  • Hebert, D. N., Zhang, J. X., Chen, W., Foellmer, B., & Helenius, A. (1997). The number and location of glycans on influenza hemagglutinin determine folding and association with calnexin and calreticulin. The Journal of Cell Biology, 139, 613–623.10.1083/jcb.139.3.613
  • Helle, F., & Dubuisson, J. (2008). Hepatitis C virus entry into host cells. Cellular and Molecular Life Sciences, 65, 100–112.10.1007/s00018-007-7291-8
  • Helle, F., Duverlie, G., & Dubuisson, J. (2011). The hepatitis C virus glycan shield and evasion of the humoral immune response. Viruses, 3, 1909–1932.10.3390/v3101909
  • Helle, F., Goffard, A., Morel, V., Duverlie, G., McKeating, J., Keck, Z. Y., … Voisset, C. (2007). The neutralizing activity of anti-hepatitis C virus antibodies is modulated by specific glycans on the E2 envelope protein. Journal of Virology, 81, 8101–8111.10.1128/JVI.00127-07
  • Helle, F., Vieyres, G., Elkrief, L., Popescu, C. I., Wychowski, C., Descamps, V., … Dubuisson, J. (2010). Role of N-linked glycans in the functions of hepatitis C virus envelope proteins incorporated into infectious virions. Journal of Virology, 84, 11905–11915.10.1128/JVI.01548-10
  • Houghton, M., & Abrignani, S. (2005). Prospects for a vaccine against the hepatitis C virus. Nature, 436, 961–966.10.1038/nature04081
  • Iacob, R. E., Keck, Z., Olson, O., Foung, S. K., & Tomer, K. B. (2008). Structural elucidation of critical residues involved in binding of human monoclonal antibodies to hepatitis C virus E2 envelope glycoprotein. Biochimica et Biophysica Acta (BBA), 1784, 530–542.10.1016/j.bbapap.2007.12.015
  • Iacob, R. E., Perdivara, I., Przybylski, M., & Tomer, K. B. (2008). Mass spectrometric characterization of glycosylation of hepatitis C virus E2 envelope glycoprotein reveals extended microheterogeneity of N-glycans. Journal of the American Society for Mass Spectrometry, 19, 428–444.10.1016/j.jasms.2007.11.022
  • Ikram, A., Anjum, S., & Tahir, M. (2014). In silico identification and conservation analysis of B-cell and T-cell epitopes of hepatitis C virus 3a genotype enveloped glycoprotein 2 from Pakistan: A step towards heterologous vaccine design. Hepatitis Monthly, 14, e9832.
  • Kachko, A., Kochneva, G., Sivolobova, G., Grazhdantseva, A., Lupan, T., Zubkova, I., … Major, M. E. (2011). New neutralizing antibody epitopes in hepatitis C virus envelope glycoproteins are revealed by dissecting peptide recognition profiles. Vaccine, 30, 69–77.10.1016/j.vaccine.2011.10.045
  • Kanai, R., Kar, K., Anthony, K., Gould, L. H., Ledizet, M., Fikrig, E., … Modis, Y. (2006). Crystal structure of west nile virus envelope glycoprotein reveals viral surface epitopes. Journal of Virology, 80, 11000–11008.10.1128/JVI.01735-06
  • Khan, A. G., Whidby, J., Miller, M. T., Scarborough, H., Zatorski, A. V., Cygan, A., … Marcotrigiano, J. (2014). Structure of the core ectodomain of the hepatitis C virus envelope glycoprotein 2. Nature, 509, 381–384.
  • Kolaskar, A. S., & Tongaonkar, P. C. (1990). A semi-empirical method for prediction of antigenic determinants on protein antigens. FEBS Letters, 276, 172–174.10.1016/0014-5793(90)80535-Q
  • Kong, L., Giang, E., Nieusma, T., Kadam, R. U., Cogburn, K. E., Hua, Y., … Law, M. (2013). Hepatitis C virus E2 envelope glycoprotein core structure. Science, 342, 1090–1094.10.1126/science.1243876
  • Kosakovsky Pond, S. L., & Frost, S. D. (2005). Not so different after all: A comparison of methods for detecting amino acid sites under selection. Molecular Biology and Evolution, 22, 1208–1222.10.1093/molbev/msi105
  • Krekulova, L., Rehak, V., & Riley, L. W. (2006). Structure and functions of hepatitis C virus proteins: 15 years after. Folia Microbiologica, 51, 665–680.10.1007/BF02931636
  • Krey, T., d’Alayer, J., Kikuti, C. M., Saulnier, A., Damier-Piolle, L., Petitpas, I., … Rey, F. A. (2010). The disulfide bonds in glycoprotein E2 of hepatitis C virus reveal the tertiary organization of the molecule. PLoS Pathogens, 6, e1000762.10.1371/journal.ppat.1000762
  • Kumar, S., Nei, M., Dudley, J., & Tamura, K. (2008). MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics, 9, 299–306.10.1093/bib/bbn017
  • Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26, 283–291.10.1107/S0021889892009944
  • Laskowski, R. A., Moss, D. S., & Thornton, J. M. (1993). Main-chain bond lengths and bond angles in protein structures. Journal of Molecular Biology, 231, 1049–1067.10.1006/jmbi.1993.1351
  • Lavie, M., Goffard, A., & Dubuisson, J. (2006). HCV glycoproteins: Assembly of a functional E1–E2 heterodimer. In S. L. Tan (Ed.), Hepatitis C viruses: Genomes and molecular biology (pp. 121–150). Norfolk: Horizon Bioscience.
  • Lavie, M., Sarrazin, S., Montserret, R., Descamps, V., Baumert, T. F., Duverlie, G., … Dubuisson, J. (2014). Identification of conserved residues in hepatitis C virus envelope glycoprotein E2 that modulate virus dependence on CD81 and SRB1 entry factors. Journal of Virology, 88, 10584–10597.10.1128/JVI.01402-14
  • Lavillette, D., Pecheur, E. I., Donot, P., Fresquet, J., Molle, J., Corbau, R., … Cosset, F. L. (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 hepatitis C virus. Journal of Virology, 81, 8752–8765.10.1128/JVI.02642-06
  • Law, J. L., Chen, C., Wong, J., Hockman, D., Santer, D. M., Frey, S. E., … Houghton, M. (2013). A hepatitis C virus (HCV) vaccine comprising envelope glycoproteins gpE1/gpE2 derived from a single isolate elicits broad cross-genotype neutralizing antibodies in humans. PLoS ONE, 8, e59776.10.1371/journal.pone.0059776
  • Li, L., Jose, J., Xiang, Y., Kuhn, R. J., & Rossmann, M. G. (2010). Structural changes of envelope proteins during alphavirus fusion. Nature, 468, 705–708.10.1038/nature09546
  • Lidenbach, B. D., Thiel, H. J., & Rice, C. M. (2007). Flaviviridae: The viruses and their replication. In K. DM & H. PM (Eds.), Fields virology (5th ed., Vol. 1, pp. 1101–1152). Philadelphia, PA: Lippincott-Raven.
  • Marchler-Bauer, A., Anderson, J. B., DeWeese-Scott, C., Fedorova, N. D., Geer, L. Y., He, S., … Bryant, S. H. (2003). CDD: A curated Entrez database of conserved domain alignments. Nucleic Acids Research, 31, 383–387.10.1093/nar/gkg087
  • Maurin, G., Fresquet, J., Granio, O., Wychowski, C., Cosset, F. L., & Lavillette, D. (2011). Identification of interactions in the E1E2 heterodimer of hepatitis C virus important for cell entry. Journal of Biological Chemistry, 286, 23865–23876.10.1074/jbc.M110.213942
  • Mazumder, R., Hu, Z. Z., Vinayaka, C. R., Sagripanti, J. L., Frost, S. D., Kosakovsky Pond, S. L., & Wu, C. H. (2007). Computational analysis and identification of amino acid sites in dengue E proteins relevant to development of diagnostics and vaccines. Virus Genes, 35, 175–186.10.1007/s11262-007-0103-2
  • Mazumder, R., & Vasudevan, S. (2008). Structure-guided comparative analysis of proteins: Principles, tools, and applications for predicting function. PLoS Computational Biology, 4, e1000151.10.1371/journal.pcbi.1000151
  • Mazumder, R., Vasudevan, S., & Nikolskaya, A. N. (2008). Protein functional annotation by homology. Methods in Molecular Biology, 484, 465–490.10.1007/978-1-59745-398-1
  • Meunier, J. C., Russell, R. S., Goossens, V., Priem, S., Walter, H., Depla, E., … Purcell, R. H. (2008). Isolation and characterization of broadly neutralizing human monoclonal antibodies to the E1 glycoprotein of hepatitis C virus. Journal of Virology, 82, 966–973.10.1128/JVI.01872-07
  • Modis, Y., Ogata, S., Clements, D., & Harrison, S. C. (2003). A ligand-binding pocket in the dengue virus envelope glycoprotein. Proceedings of the National Academy of Sciences, 100, 6986–6991.10.1073/pnas.0832193100
  • Murrell, B., Wertheim, J. O., Moola, S., Weighill, T., Scheffler, K., & Kosakovsky Pond, S. L. (2012). Detecting individual sites subject to episodic diversifying selection. PLoS Genetics, 8, e1002764.10.1371/journal.pgen.1002764
  • Nayak, V., Dessau, M., Kucera, K., Anthony, K., Ledizet, M., & Modis, Y. (2009). Crystal structure of dengue virus type 1 envelope protein in the postfusion conformation and its implications for membrane fusion. Journal of Virology, 83, 4338–4344.10.1128/JVI.02574-08
  • NCBI_Resource_Coordinators. (2014). Database resources of the national center for biotechnology information. Nucleic Acids Research, 42, D7–17.
  • Op De Beeck, A., Cocquerel, L., & Dubuisson, J. (2001). Biogenesis of hepatitis C virus envelope glycoproteins. Journal of General Virology, 82, 2589–2595.
  • Pattabiraman, N., Ward, K. B., & Fleming, P. J. (1995). Occluded molecular surface: Analysis of protein packing. Journal of Molecular Recognition, 8, 334–344.10.1002/(ISSN)1099-1352
  • Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera? A visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25, 1605–1612.10.1002/(ISSN)1096-987X
  • Qureshi, S. A. (2007). Hepatitis C virus–biology, host evasion strategies, and promising new therapies on the horizon. Medicinal Research Reviews, 27, 353–373.10.1002/(ISSN)1098-1128
  • Rey, F. A. (2003). Dengue virus envelope glycoprotein structure: New insight into its interactions during viral entry. Proceedings of the National Academy of Sciences, 100, 6899–6901.10.1073/pnas.1332695100
  • Rey, F. A., Heinz, F. X., Mandl, C., Kunz, C., & Harrison, S. C. (1995). The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution. Nature, 375, 291–298.10.1038/375291a0
  • Roussel, A., Lescar, J., Vaney, M. C., Wengler, G., & Rey, F. A. (2006). Structure and interactions at the viral surface of the envelope protein E1 of Semliki Forest virus. Structure, 14, 75–86.10.1016/j.str.2005.09.014
  • Rychlowska, M., Owsianka, A. M., Foung, S. K., Dubuisson, J., Bienkowska-Szewczyk, K., & Patel, A. H. (2011). Comprehensive linker-scanning mutagenesis of the hepatitis C virus E1 and E2 envelope glycoproteins reveals new structure-function relationships. Journal of General Virology, 92, 2249–2261.10.1099/vir.0.034314-0
  • Sabahi, A., Uprichard, S. L., Wimley, W. C., Dash, S., & Garry, R. F. (2014). Unexpected structural features of the hepatitis C virus envelope protein 2 ectodomain. Journal of Virology, 88, 10280–10288.10.1128/JVI.00874-14
  • Sagripanti, J.-L., Mazumder, R., & Wu, C. H. (2011). Amino acid sites in Flavivirus E proteins useful for development of diagnostics and vaccines. USPTO. USA. US7943148 B1.
  • Salimi, N., Fleri, W., Peters, B., & Sette, A. (2012). The immune epitope database: A historical retrospective of the first decade. Immunology, 137, 117–123.10.1111/imm.2012.137.issue-2
  • Schwede, T., Kopp, J., Guex, N., & Peitsch, M. C. (2003). SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Research, 31, 3381–3385.10.1093/nar/gkg520
  • Stadler, K., Allison, S. L., Schalich, J., & Heinz, F. X. (1997). Proteolytic activation of tick-borne encephalitis virus by furin. Journal of Virology, 71, 8475–8481.
  • Stamataki, Z., Coates, S., Abrignani, S., Houghton, M., & McKeating, J. A. (2011). Immunization of human volunteers with hepatitis C virus envelope glycoproteins elicits antibodies that cross-neutralize heterologous virus strains. Journal of Infectious Diseases, 204, 811–813.10.1093/infdis/jir399
  • Stiasny, K., Allison, S. L., Marchler-Bauer, A., Kunz, C., & Heinz, F. X. (1996). Structural requirements for low-pH-induced rearrangements in the envelope glycoprotein of tick-borne encephalitis virus. Journal of Virology, 70, 8142–8147.
  • Stranzl, T., Larsen, M. V., Lundegaard, C., & Nielsen, M. (2010). NetCTLpan: Pan-specific MHC class I pathway epitope predictions. Immunogenetics, 62, 357–368.10.1007/s00251-010-0441-4
  • UniProt_Consortium. (2012). Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Research, 40, D71–75.
  • Vieyres, G., Dubuisson, J., & Pietschmann, T. (2014). Incorporation of hepatitis C virus E1 and E2 glycoproteins: The keystones on a peculiar virion. Viruses, 6, 1149–1187.10.3390/v6031149
  • Voisset, C., & Dubuisson, J. (2004). Functional hepatitis C virus envelope glycoproteins. Biology of the Cell, 96, 413–420.10.1016/j.biolcel.2004.03.008
  • Voss, J. E., Vaney, M. C., Duquerroy, S., Vonrhein, C., Girard-Blanc, C., Crublet, E., … Rey, F. A. (2010). Glycoprotein organization of Chikungunya virus particles revealed by X-ray crystallography. Nature, 468, 709–712.10.1038/nature09555
  • Wahid, A., Helle, F., Descamps, V., Duverlie, G., Penin, F., & Dubuisson, J. (2013). Disulfide bonds in hepatitis C virus glycoprotein E1 control the assembly and entry functions of E2 glycoprotein. Journal of Virology, 87, 1605–1617.10.1128/JVI.02659-12
  • Wengler, G. (1989). Cell-associated west nile flavivirus is covered with E+pre-M protein heterodimers which are destroyed and reorganized by proteolytic cleavage during virus release. Journal of Virology, 63, 2521–2526.
  • Yagnik, A. T., Lahm, A., Meola, A., Roccasecca, R. M., Ercole, B. B., Nicosia, A., & Tramontano, A. (2000). A model for the hepatitis C virus envelope glycoprotein E2. Proteins: Structure, Function, and Genetics, 40, 355–366.10.1002/(ISSN)1097-0134
  • Yi, M., Nakamoto, Y., Kaneko, S., Yamashita, T., & Murakami, S. (1997). Delineation of regions important for heteromeric association of hepatitis C virus E1 and E2. Virology, 231, 119–129.10.1006/viro.1997.8516
  • Yu, X., Qiao, M., Atanasov, I., Hu, Z., Kato, T., Liang, T. J., & Zhou, Z. H. (2007). Cryo-electron microscopy and three-dimensional reconstructions of hepatitis C virus particles. Virology, 367, 126–134.10.1016/j.virol.2007.05.038

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.