This Article
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Allison, S. L.
Right arrow Articles by Heinz, F. X.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Allison, S. L.
Right arrow Articles by Heinz, F. X.

 Previous Article  |  Next Article 

J. Virol., 02 1995, 695-700, Vol 69, No. 2
Copyright © 1995, American Society for Microbiology

Oligomeric rearrangement of tick-borne encephalitis virus envelope proteins induced by an acidic pH

SL Allison, J Schalich, K Stiasny, CW Mandl, C Kunz and FX Heinz
Institute of Virology, University of Vienna, Austria.

The flavivirus envelope protein E undergoes irreversible conformational changes at a mildly acidic pH which are believed to be necessary for membrane fusion in endosomes. In this study we used a combination of chemical cross-linking and sedimentation analysis to show that the envelope proteins of the flavivirus tick-borne encephalitis virus also change their oligomeric structure when exposed to a mildly acidic environment. Under neutral or slightly alkaline conditions, protein E on the surface of native virions exists as a homodimer which can be isolated by solubilization with the nonionic detergent Triton X-100. Solubilization with the same detergent after pretreatment at an acidic pH, however, yielded homotrimers rather than homodimers, suggesting that exposure to an acidic pH had induced a simultaneous weakening of dimeric contacts and a strengthening of trimeric ones. The pH threshold for the dimer-to-trimer transition was found to be 6.5. Because the pH dependence of this transition parallels that of previously observed changes in the conformation and hydrophobicity of protein E and that of virus-induced membrane fusion, it appears likely that the mechanism of fusion with endosomal membranes involves a specific rearrangement of the proteins in the viral envelope. Immature virions in which protein E is associated with the uncleaved precursor (prM) of the membrane protein M did not undergo a low-pH-induced rearrangement. This is consistent with a protective role of protein prM for protein E during intracellular transport of immature virions through acidic compartments of the trans-Golgi network.


This article has been cited by other articles:

  • Yu, I.-M., Holdaway, H. A., Chipman, P. R., Kuhn, R. J., Rossmann, M. G., Chen, J. (2009). Association of the pr Peptides with Dengue Virus at Acidic pH Blocks Membrane Fusion. J. Virol. 83: 12101-12107 [Abstract] [Full Text]  
  • Mansfield, K. L., Johnson, N., Phipps, L. P., Stephenson, J. R., Fooks, A. R., Solomon, T. (2009). Tick-borne encephalitis virus - a review of an emerging zoonosis. J. Gen. Virol. 90: 1781-1794 [Abstract] [Full Text]  
  • Sultana, H., Foellmer, H. G., Neelakanta, G., Oliphant, T., Engle, M., Ledizet, M., Krishnan, M. N., Bonafe, N., Anthony, K. G., Marasco, W. A., Kaplan, P., Montgomery, R. R., Diamond, M. S., Koski, R. A., Fikrig, E. (2009). Fusion Loop Peptide of the West Nile Virus Envelope Protein Is Essential for Pathogenesis and Is Recognized by a Therapeutic Cross-Reactive Human Monoclonal Antibody. J. Immunol. 183: 650-660 [Abstract] [Full Text]  
  • 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. J. Virol. 83: 4338-4344 [Abstract] [Full Text]  
  • Panyasrivanit, M., Khakpoor, A., Wikan, N., Smith, D. R. (2009). Co-localization of constituents of the dengue virus translation and replication machinery with amphisomes. J. Gen. Virol. 90: 448-456 [Abstract] [Full Text]  
  • Wu, X., Lu, L., Guzman, H., Tesh, R. B., Xiao, S.-Y. (2008). Persistent infection and associated nucleotide changes of West Nile virus serially passaged in hamsters. J. Gen. Virol. 89: 3073-3079 [Abstract] [Full Text]  
  • Fritz, R., Stiasny, K., Heinz, F. X. (2008). Identification of specific histidines as pH sensors in flavivirus membrane fusion. JCB 183: 353-361 [Abstract] [Full Text]  
  • Fischl, W., Elshuber, S., Schrauf, S., Mandl, C. W. (2008). Changing the Protease Specificity for Activation of a Flavivirus, Tick-Borne Encephalitis Virus. J. Virol. 82: 8272-8282 [Abstract] [Full Text]  
  • Kim, J.-M., Yun, S.-I., Song, B.-H., Hahn, Y.-S., Lee, C.-H., Oh, H.-W., Lee, Y.-M. (2008). A Single N-Linked Glycosylation Site in the Japanese Encephalitis Virus prM Protein Is Critical for Cell Type-Specific prM Protein Biogenesis, Virus Particle Release, and Pathogenicity in Mice. J. Virol. 82: 7846-7862 [Abstract] [Full Text]  
  • Yu, I-M., Zhang, W., Holdaway, H. A., Li, L., Kostyuchenko, V. A., Chipman, P. R., Kuhn, R. J., Rossmann, M. G., Chen, J. (2008). Structure of the Immature Dengue Virus at Low pH Primes Proteolytic Maturation. Science 319: 1834-1837 [Abstract] [Full Text]  
  • van der Schaar, H. M., Rust, M. J., Waarts, B.-L., van der Ende-Metselaar, H., Kuhn, R. J., Wilschut, J., Zhuang, X., Smit, J. M. (2007). Characterization of the Early Events in Dengue Virus Cell Entry by Biochemical Assays and Single-Virus Tracking. J. Virol. 81: 12019-12028 [Abstract] [Full Text]  
  • Kanai, R., Kar, K., Anthony, K., Gould, L. H., Ledizet, M., Fikrig, E., Marasco, W. A., Koski, R. A., Modis, Y. (2006). Crystal Structure of West Nile Virus Envelope Glycoprotein Reveals Viral Surface Epitopes. J. Virol. 80: 11000-11008 [Abstract] [Full Text]  
  • Wang, J. P., Liu, P., Latz, E., Golenbock, D. T., Finberg, R. W., Libraty, D. H. (2006). Flavivirus Activation of Plasmacytoid Dendritic Cells Delineates Key Elements of TLR7 Signaling beyond Endosomal Recognition. J. Immunol. 177: 7114-7121 [Abstract] [Full Text]  
  • Samuel, M. A., Diamond, M. S. (2006). Pathogenesis of West Nile Virus Infection: a Balance between Virulence, Innate and Adaptive Immunity, and Viral Evasion. J. Virol. 80: 9349-9360 [Full Text]  
  • Stiasny, K., Kiermayr, S., Holzmann, H., Heinz, F. X. (2006). Cryptic Properties of a Cluster of Dominant Flavivirus Cross-Reactive Antigenic Sites. J. Virol. 80: 9557-9568 [Abstract] [Full Text]  
  • Stiasny, K., Heinz, F. X. (2006). Flavivirus membrane fusion.. J. Gen. Virol. 87: 2755-2766 [Abstract] [Full Text]  
  • Tscherne, D. M., Jones, C. T., Evans, M. J., Lindenbach, B. D., McKeating, J. A., Rice, C. M. (2006). Time- and Temperature-Dependent Activation of Hepatitis C Virus for Low-pH-Triggered Entry. J. Virol. 80: 1734-1741 [Abstract] [Full Text]  
  • Kobayashi, M., Bennett, M. C., Bercot, T., Singh, I. R. (2006). Functional Analysis of Hepatitis C Virus Envelope Proteins, Using a Cell-Cell Fusion Assay. J. Virol. 80: 1817-1825 [Abstract] [Full Text]  
  • Puig-Basagoiti, F., Deas, T. S., Ren, P., Tilgner, M., Ferguson, D. M., Shi, P.-Y. (2005). High-Throughput Assays Using a Luciferase-Expressing Replicon, Virus-Like Particles, and Full-Length Virus for West Nile Virus Drug Discovery. Antimicrob. Agents Chemother. 49: 4980-4988 [Abstract] [Full Text]  
  • Liao, M., Kielian, M. (2005). Domain III from class II fusion proteins functions as a dominant-negative inhibitor of virus membrane fusion. JCB 171: 111-120 [Abstract] [Full Text]  
  • Elshuber, S., Mandl, C. W. (2005). Resuscitating Mutations in a Furin Cleavage-Deficient Mutant of the Flavivirus Tick-Borne Encephalitis Virus. J. Virol. 79: 11813-11823 [Abstract] [Full Text]  
  • Zhao, Z., Date, T., Li, Y., Kato, T., Miyamoto, M., Yasui, K., Wakita, T. (2005). Characterization of the E-138 (Glu/Lys) mutation in Japanese encephalitis virus by using a stable, full-length, infectious cDNA clone. J. Gen. Virol. 86: 2209-2220 [Abstract] [Full Text]  
  • Lin, Y.-J., Wu, S.-C. (2005). Histidine at Residue 99 and the Transmembrane Region of the Precursor Membrane prM Protein Are Important for the prM-E Heterodimeric Complex Formation of Japanese Encephalitis Virus. J. Virol. 79: 8535-8544 [Abstract] [Full Text]  
  • Stiasny, K., Kossl, C., Heinz, F. X. (2005). Differences in the Postfusion Conformations of Full-Length and Truncated Class II Fusion Protein E of Tick-Borne Encephalitis Virus. J. Virol. 79: 6511-6515 [Abstract] [Full Text]  
  • Krey, T., Thiel, H.-J., Rumenapf, T. (2005). Acid-Resistant Bovine Pestivirus Requires Activation for pH-Triggered Fusion during Entry. J. Virol. 79: 4191-4200 [Abstract] [Full Text]  
  • Crill, W. D., Chang, G.-J. J. (2004). Localization and Characterization of Flavivirus Envelope Glycoprotein Cross-Reactive Epitopes. J. Virol. 78: 13975-13986 [Abstract] [Full Text]  
  • Pryor, M. J., Azzola, L., Wright, P. J., Davidson, A. D. (2004). Histidine 39 in the dengue virus type 2 M protein has an important role in virus assembly. J. Gen. Virol. 85: 3627-3636 [Abstract] [Full Text]  
  • Goncalvez, A. P., Purcell, R. H., Lai, C.-J. (2004). Epitope Determinants of a Chimpanzee Fab Antibody That Efficiently Cross-Neutralizes Dengue Type 1 and Type 2 Viruses Map to Inside and in Close Proximity to Fusion Loop of the Dengue Type 2 Virus Envelope Glycoprotein. J. Virol. 78: 12919-12928 [Abstract] [Full Text]  
  • Yoshii, K., Konno, A., Goto, A., Nio, J., Obara, M., Ueki, T., Hayasaka, D., Mizutani, T., Kariwa, H., Takashima, I. (2004). Single point mutation in tick-borne encephalitis virus prM protein induces a reduction of virus particle secretion. J. Gen. Virol. 85: 3049-3058 [Abstract] [Full Text]  
  • Stiasny, K., Heinz, F. X. (2004). Effect of Membrane Curvature-Modifying Lipids on Membrane Fusion by Tick-Borne Encephalitis Virus. J. Virol. 78: 8536-8542 [Abstract] [Full Text]  
  • Kiermayr, S., Kofler, R. M., Mandl, C. W., Messner, P., Heinz, F. X. (2004). Isolation of Capsid Protein Dimers from the Tick-Borne Encephalitis Flavivirus and In Vitro Assembly of Capsid-Like Particles. J. Virol. 78: 8078-8084 [Abstract] [Full Text]  
  • Shmulevitz, M., Epand, R. F., Epand, R. M., Duncan, R. (2004). Structural and Functional Properties of an Unusual Internal Fusion Peptide in a Nonenveloped Virus Membrane Fusion Protein. J. Virol. 78: 2808-2818 [Abstract] [Full Text]  
  • Op De Beeck, A., Voisset, C., Bartosch, B., Ciczora, Y., Cocquerel, L., Keck, Z., Foung, S., Cosset, F.-L., Dubuisson, J. (2004). Characterization of Functional Hepatitis C Virus Envelope Glycoproteins. J. Virol. 78: 2994-3002 [Abstract] [Full Text]  
  • Keelapang, P., Sriburi, R., Supasa, S., Panyadee, N., Songjaeng, A., Jairungsri, A., Puttikhunt, C., Kasinrerk, W., Malasit, P., Sittisombut, N. (2004). Alterations of pr-M Cleavage and Virus Export in pr-M Junction Chimeric Dengue Viruses. J. Virol. 78: 2367-2381 [Abstract] [Full Text]  
  • Hung, J.-J., Hsieh, M.-T., Young, M.-J., Kao, C.-L., King, C.-C., Chang, W. (2004). An External Loop Region of Domain III of Dengue Virus Type 2 Envelope Protein Is Involved in Serotype-Specific Binding to Mosquito but Not Mammalian Cells. J. Virol. 78: 378-388 [Abstract] [Full Text]  
  • Nickells, M., Chambers, T. J. (2003). Neuroadapted Yellow Fever Virus 17D: Determinants in the Envelope Protein Govern Neuroinvasiveness for SCID Mice. J. Virol. 77: 12232-12242 [Abstract] [Full Text]  
  • Allison, S. L., Tao, Y. J., O'Riordain, G., Mandl, C. W., Harrison, S. C., Heinz, F. X. (2003). Two Distinct Size Classes of Immature and Mature Subviral Particles from Tick-Borne Encephalitis Virus. J. Virol. 77: 11357-11366 [Abstract] [Full Text]  
  • Stiasny, K., Koessl, C., Heinz, F. X. (2003). Involvement of Lipids in Different Steps of the Flavivirus Fusion Mechanism. J. Virol. 77: 7856-7862 [Abstract] [Full Text]  
  • Modis, Y., Ogata, S., Clements, D., Harrison, S. C. (2003). A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc. Natl. Acad. Sci. USA 100: 6986-6991 [Abstract] [Full Text]  
  • Lorenz, I. C., Kartenbeck, J., Mezzacasa, A., Allison, S. L., Heinz, F. X., Helenius, A. (2003). Intracellular Assembly and Secretion of Recombinant Subviral Particles from Tick-Borne Encephalitis Virus. J. Virol. 77: 4370-4382 [Abstract] [Full Text]  
  • Elshuber, S., Allison, S. L., Heinz, F. X., Mandl, C. W. (2003). Cleavage of protein prM is necessary for infection of BHK-21 cells by tick-borne encephalitis virus. J. Gen. Virol. 84: 183-191 [Abstract] [Full Text]  
  • Gritsun, T. S., Frolova, T. V., Zhankov, A. I., Armesto, M., Turner, S. L., Frolova, M. P., Pogodina, V. V., Lashkevich, V. A., Gould, E. A. (2002). Characterization of a Siberian Virus Isolated from a Patient with Progressive Chronic Tick-Borne Encephalitis. J. Virol. 77: 25-36 [Abstract] [Full Text]  
  • Wu, S.-F., Lee, C.-J., Liao, C.-L., Dwek, R. A., Zitzmann, N., Lin, Y.-L. (2002). Antiviral Effects of an Iminosugar Derivative on Flavivirus Infections. J. Virol. 76: 3596-3604 [Abstract] [Full Text]  
  • Stiasny, K., Allison, S. L., Schalich, J., Heinz, F. X. (2002). Membrane Interactions of the Tick-Borne Encephalitis Virus Fusion Protein E at Low pH. J. Virol. 76: 3784-3790 [Abstract] [Full Text]  
  • Monath, T. P., Arroyo, J., Levenbook, I., Zhang, Z.-X., Catalan, J., Draper, K., Guirakhoo, F. (2002). Single Mutation in the Flavivirus Envelope Protein Hinge Region Increases Neurovirulence for Mice and Monkeys but Decreases Viscerotropism for Monkeys: Relevance to Development and Safety Testing of Live, Attenuated Vaccines. J. Virol. 76: 1932-1943 [Abstract] [Full Text]  
  • Center, R. J., Schuck, P., Leapman, R. D., Arthur, L. O., Earl, P. L., Moss, B., Lebowitz, J. (2001). Oligomeric structure of virion-associated and soluble forms of the simian immunodeficiency virus envelope protein in the prefusion activated conformation. Proc. Natl. Acad. Sci. USA 98: 14877-14882 [Abstract] [Full Text]  
  • Mackenzie, J. M., Westaway, E. G. (2001). Assembly and Maturation of the Flavivirus Kunjin Virus Appear To Occur in the Rough Endoplasmic Reticulum and along the Secretory Pathway, Respectively. J. Virol. 75: 10787-10799 [Abstract] [Full Text]  
  • Chambers, T. J., Nickells, M. (2001). Neuroadapted Yellow Fever Virus 17D: Genetic and Biological Characterization of a Highly Mouse-Neurovirulent Virus and Its Infectious Molecular Clone. J. Virol. 75: 10912-10922 [Abstract] [Full Text]  
  • Dormitzer, P. R., Greenberg, H. B., Harrison, S. C. (2001). Proteolysis of Monomeric Recombinant Rotavirus VP4 Yields an Oligomeric VP5* Core. J. Virol. 75: 7339-7350 [Abstract] [Full Text]  
  • Stiasny, K., Allison, S. L., Mandl, C. W., Heinz, F. X. (2001). Role of Metastability and Acidic pH in Membrane Fusion by Tick-Borne Encephalitis Virus. J. Virol. 75: 7392-7398 [Abstract] [Full Text]  
  • Hurrelbrink, R. J., McMinn, P. C. (2001). Attenuation of Murray Valley Encephalitis Virus by Site-Directed Mutagenesis of the Hinge and Putative Receptor-Binding Regions of the Envelope Protein. J. Virol. 75: 7692-7702 [Abstract] [Full Text]  
  • Allison, S. L., Schalich, J., Stiasny, K., Mandl, C. W., Heinz, F. X. (2001). Mutational Evidence for an Internal Fusion Peptide in Flavivirus Envelope Protein E. J. Virol. 75: 4268-4275 [Abstract] [Full Text]  
  • Gibbons, D. L., Ahn, A., Chatterjee, P. K., Kielian, M. (2000). Formation and Characterization of the Trimeric Form of the Fusion Protein of Semliki Forest Virus. J. Virol. 74: 7772-7780 [Abstract] [Full Text]  
  • Center, R. J., Earl, P. L., Lebowitz, J., Schuck, P., Moss, B. (2000). The Human Immunodeficiency Virus Type 1 gp120 V2 Domain Mediates gp41-Independent Intersubunit Contacts. J. Virol. 74: 4448-4455 [Abstract] [Full Text]  
  • Aberle, J. H., Aberle, S. W., Allison, S. L., Stiasny, K., Ecker, M., Mandl, C. W., Berger, R., Heinz, F. X. (1999). A DNA Immunization Model Study with Constructs Expressing the Tick-Borne Encephalitis Virus Envelope Protein E in Different Physical Forms. J. Immunol. 163: 6756-6761 [Abstract] [Full Text]  
  • Allison, S. L., Stiasny, K., Stadler, K., Mandl, C. W., Heinz, F. X. (1999). Mapping of Functional Elements in the Stem-Anchor Region of Tick-Borne Encephalitis Virus Envelope Protein E. J. Virol. 73: 5605-5612 [Abstract] [Full Text]  
  • Fleeton, M., Sheahan, B., Gould, E., Atkins, G., Liljestrom, P (1999). Recombinant Semliki Forest virus particles encoding the prME or NS1 proteins of louping ill virus protect mice from lethal challenge. J. Gen. Virol. 80: 1189-1198 [Abstract]  
  • Wang, S., He, R., Anderson, R. (1999). PrM- and Cell-Binding Domains of the Dengue Virus E Protein. J. Virol. 73: 2547-2551 [Abstract] [Full Text]  
  • White, J.M. (1995). Membrane Fusion: The Influenza Paradigm. Cold Spring Harb Symp Quant Biol 60: 581-588 [Abstract]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»