Dengue Virus Glycosylation: What Do We Know?

In many infectious diseases caused by either viruses or bacteria, pathogen glycoproteins play important roles during the infection cycle, ranging from entry to successful intracellular replication and host immune evasion. Dengue is no exception. Dengue virus glycoproteins, envelope protein (E) and non-structural protein 1 (NS1) are two popular sub-unit vaccine candidates. E protein on the virion surface is the major target of neutralizing antibodies. NS1 which is secreted during DENV infection has been shown to induce a variety of host responses through its binding to several host factors. However, despite their critical role in disease and protection, the glycosylated variants of these two proteins and their biological importance have remained understudied. In this review, we seek to provide a comprehensive summary of the current knowledge on protein glycosylation in DENV, and its role in virus biogenesis, host cell receptor interaction and disease pathogenesis.

[1]  M. Diamond,et al.  Secreted NS1 Protects Dengue Virus from Mannose-Binding Lectin–Mediated Neutralization , 2016, The Journal of Immunology.

[2]  Chi‐Huey Wong,et al.  Dengue Virus Infection Is through a Cooperative Interaction between a Mannose Receptor and CLEC5A on Macrophage as a Multivalent Hetero-Complex , 2016, PloS one.

[3]  A. Heck,et al.  Hybrid mass spectrometry approaches in glycoprotein analysis and their usage in scoring biosimilarity , 2016, Nature Communications.

[4]  Frank DiMaio,et al.  Glycan shield and epitope masking of a coronavirus spike protein observed by cryo-electron microscopy , 2016, Nature Structural &Molecular Biology.

[5]  John D. Lambris,et al.  Complement in disease: a defence system turning offensive , 2016, Nature Reviews Nephrology.

[6]  Chen Chen,et al.  Challenges of glycosylation analysis and control: an integrated approach to producing optimal and consistent therapeutic drugs. , 2016, Drug discovery today.

[7]  R. Dwek,et al.  Inhibition of endoplasmic reticulum glucosidases is required for in vitro and in vivo dengue antiviral activity by the iminosugar UV-4 , 2016, Antiviral research.

[8]  R. Dwek,et al.  Iminosugars Inhibit Dengue Virus Production via Inhibition of ER Alpha-Glucosidases—Not Glycolipid Processing Enzymes , 2016, PLoS neglected tropical diseases.

[9]  Nicolle H. Packer,et al.  Maturing Glycoproteomics Technologies Provide Unique Structural Insights into the N-glycoproteome and Its Regulation in Health and Disease* , 2016, Molecular & Cellular Proteomics.

[10]  B. Guy,et al.  Development of the Sanofi Pasteur tetravalent dengue vaccine: One more step forward. , 2015, Vaccine.

[11]  Rana F. Hamdy,et al.  Efficacy of a Tetravalent Dengue Vaccine in Children in Latin America. , 2015, Journal of the Pediatric Infectious Diseases Society.

[12]  I. Wilson,et al.  Parasite Glycobiology: A Bittersweet Symphony , 2015, PLoS pathogens.

[13]  K. Doores,et al.  The HIV glycan shield as a target for broadly neutralizing antibodies , 2015, The FEBS journal.

[14]  Eva Harris,et al.  Dengue virus NS1 triggers endothelial permeability and vascular leak that is prevented by NS1 vaccination , 2015, Science Translational Medicine.

[15]  D. Hume,et al.  Dengue virus NS1 protein activates cells via Toll-like receptor 4 and disrupts endothelial cell monolayer integrity , 2015, Science Translational Medicine.

[16]  H. Yu,et al.  Characterization of N-Glycan Structures on the Surface of Mature Dengue 2 Virus Derived from Insect Cells , 2015, PloS one.

[17]  B. Guy,et al.  Site-specific characterization of envelope protein N-glycosylation on Sanofi Pasteur's tetravalent CYD dengue vaccine. , 2015, Vaccine.

[18]  N. Packer,et al.  Glycomic characterization of basal tears and changes with diabetes and diabetic retinopathy. , 2015, Glycobiology.

[19]  Tao Liu,et al.  The Roles of Direct Recognition by Animal Lectins in Antiviral Immunity and Viral Pathogenesis , 2015, Molecules.

[20]  Cameron P Simmons,et al.  A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus , 2014, Nature Immunology.

[21]  S. Halstead Dengue Antibody-Dependent Enhancement: Knowns and Unknowns , 2014, Microbiology spectrum.

[22]  P. Pitisuttithum,et al.  Clinical efficacy and safety of a novel tetravalent dengue vaccine in healthy children in Asia: a phase 3, randomised, observer-masked, placebo-controlled trial , 2014, The Lancet.

[23]  G. Skiniotis,et al.  Flavivirus NS1 Structures Reveal Surfaces for Associations with Membranes and the Immune System , 2014, Science.

[24]  Weibin Chen,et al.  N- and O-glycosylation analysis of etanercept using liquid chromatography and quadrupole time-of-flight mass spectrometry equipped with electron-transfer dissociation functionality. , 2014, Analytical chemistry.

[25]  Xuping Xie,et al.  Two Distinct Sets of NS2A Molecules Are Responsible for Dengue Virus RNA Synthesis and Virion Assembly , 2014, Journal of Virology.

[26]  Soila Sukupolvi-Petty,et al.  The Potent and Broadly Neutralizing Human Dengue Virus-Specific Monoclonal Antibody 1C19 Reveals a Unique Cross-Reactive Epitope on the bc Loop of Domain II of the Envelope Protein , 2013, mBio.

[27]  M. Larsen,et al.  Structural analysis of glycoprotein sialylation – part II: LC-MS based detection , 2013 .

[28]  Radoslav Goldman,et al.  Exploring site-specific N-glycosylation microheterogeneity of haptoglobin using glycopeptide CID tandem mass spectra and glycan database search. , 2013, Journal of proteome research.

[29]  R. Belshe,et al.  Glycosylations in the Globular Head of the Hemagglutinin Protein Modulate the Virulence and Antigenic Properties of the H1N1 Influenza Viruses , 2013, Science Translational Medicine.

[30]  P. Young,et al.  The flavivirus NS1 protein: molecular and structural biology, immunology, role in pathogenesis and application as a diagnostic biomarker. , 2013, Antiviral research.

[31]  R. Dwek,et al.  An iminosugar with potent inhibition of dengue virus infection in vivo. , 2013, Antiviral research.

[32]  G. Air,et al.  Glycomic Analysis of Human Respiratory Tract Tissues and Correlation with Influenza Virus Infection , 2013, PLoS pathogens.

[33]  G. Hart Thematic Minireview Series on Glycobiology and Extracellular Matrices: Glycan Functions Pervade Biology at All Levels* , 2013, The Journal of Biological Chemistry.

[34]  Lei Li,et al.  CLEC5A is critical for dengue virus-induced inflammasome activation in human macrophages. , 2013, Blood.

[35]  J. Neyts,et al.  Crucial role of the N-glycans on the viral E-envelope glycoprotein in DC-SIGN-mediated dengue virus infection. , 2012, Antiviral research.

[36]  N. Packer,et al.  Comparative structural analysis of the glycosylation of salivary and buccal cell proteins: innate protection against infection by Candida albicans. , 2012, Glycobiology.

[37]  Daniel Kolarich,et al.  Determination of site-specific glycan heterogeneity on glycoproteins , 2012, Nature Protocols.

[38]  D. Fremont,et al.  Evidence for a Genetic and Physical Interaction between Nonstructural Proteins NS1 and NS4B That Modulates Replication of West Nile Virus , 2012, Journal of Virology.

[39]  B. Hankamer,et al.  Structure of the dengue virus glycoprotein non-structural protein 1 by electron microscopy and single-particle analysis. , 2012, The Journal of general virology.

[40]  M. Diamond,et al.  Complement-Mediated Neutralization of Dengue Virus Requires Mannose-Binding Lectin , 2011, mBio.

[41]  A. Barrett,et al.  Next generation dengue vaccines: a review of candidates in preclinical development. , 2011, Vaccine.

[42]  M. Diamond,et al.  N-linked glycosylation of dengue virus NS1 protein modulates secretion, cell-surface expression, hexamer stability, and interactions with human complement. , 2011, Virology.

[43]  Matthew P. Campbell,et al.  N-Glycans Modulate the Function of Human Corticosteroid-Binding Globulin* , 2011, Molecular & Cellular Proteomics.

[44]  J. d'Alayer,et al.  Secreted dengue virus nonstructural protein NS1 is an atypical barrel-shaped high-density lipoprotein , 2011, Proceedings of the National Academy of Sciences.

[45]  M. Diamond,et al.  The lectin pathway of complement activation contributes to protection from West Nile virus infection. , 2011, Virology.

[46]  Anne Dell,et al.  Similarities and Differences in the Glycosylation Mechanisms in Prokaryotes and Eukaryotes , 2011, International journal of microbiology.

[47]  Rosanna W. Peeling,et al.  Dengue: a continuing global threat , 2010, Nature Reviews Microbiology.

[48]  E. Gould,et al.  First cases of autochthonous dengue fever and chikungunya fever in France: from bad dream to reality! , 2010, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[49]  Pauline M Rudd,et al.  A systematic approach to protein glycosylation analysis: a path through the maze. , 2010, Nature chemical biology.

[50]  T. Pierson,et al.  Direct complement restriction of flavivirus infection requires glycan recognition by mannose-binding lectin. , 2010, Cell host & microbe.

[51]  P. Højrup,et al.  Utilizing ion-pairing hydrophilic interaction chromatography solid phase extraction for efficient glycopeptide enrichment in glycoproteomics. , 2010, Analytical chemistry.

[52]  M. Diamond,et al.  Antagonism of the complement component C4 by flavivirus nonstructural protein NS1 , 2010, The Journal of experimental medicine.

[53]  Nichollas E. Scott,et al.  Simultaneous Glycan-Peptide Characterization Using Hydrophilic Interaction Chromatography and Parallel Fragmentation by CID, Higher Energy Collisional Dissociation, and Electron Transfer Dissociation MS Applied to the N-Linked Glycoproteome of Campylobacter jejuni* , 2010, Molecular & Cellular Proteomics.

[54]  S. Leang,et al.  Both E Protein Glycans Adversely Affect Dengue Virus Infectivity but Are Beneficial for Virion Release , 2010, Journal of Virology.

[55]  C. F. Brewer,et al.  Lectins as pattern recognition molecules: the effects of epitope density in innate immunity. , 2010, Glycobiology.

[56]  C. Huang,et al.  The dengue virus type 2 envelope protein fusion peptide is essential for membrane fusion. , 2010, Virology.

[57]  R. Horstkorte,et al.  Increasing the sialylation of therapeutic glycoproteins: the potential of the sialic acid biosynthetic pathway. , 2009, Journal of pharmaceutical sciences.

[58]  M. Rossmann,et al.  Association of the pr Peptides with Dengue Virus at Acidic pH Blocks Membrane Fusion , 2009, Journal of Virology.

[59]  G. Wiederschain,et al.  Essentials of glycobiology , 2009, Biochemistry (Moscow).

[60]  A. D. de Silva,et al.  N-linked glycans on dengue viruses grown in mammalian and insect cells. , 2009, The Journal of general virology.

[61]  J. Michalski,et al.  Glycoproteomics and glycomics investigation of membrane N‐glycosylproteins from human colon carcinoma cells , 2008, Proteomics.

[62]  Chi-Huey Wong,et al.  CLEC5A is critical for dengue-virus-induced lethal disease , 2008, Nature.

[63]  I. Wilson,et al.  The Glycosylation Capacity of Insect Cells , 2008 .

[64]  Wei Zhang,et al.  Structure of the Immature Dengue Virus at Low pH Primes Proteolytic Maturation , 2008, Science.

[65]  M. Rossmann,et al.  The Flavivirus Precursor Membrane-Envelope Protein Complex: Structure and Maturation , 2008, Science.

[66]  S. Tajima,et al.  Characterization of Asn130-to-Ala mutant of dengue type 1 virus NS1 protein , 2008, Virus Genes.

[67]  P. Puthavathana,et al.  Role of Dendritic Cells in Antibody-Dependent Enhancement of Dengue Virus Infection , 2008, Journal of Virology.

[68]  R. Dwek,et al.  The Mannose Receptor Mediates Dengue Virus Infection of Macrophages , 2008, PLoS pathogens.

[69]  M. Diamond,et al.  Secreted NS1 of Dengue Virus Attaches to the Surface of Cells via Interactions with Heparan Sulfate and Chondroitin Sulfate E , 2007, PLoS pathogens.

[70]  C. Huang,et al.  Glycosylation of the dengue 2 virus E protein at N67 is critical for virus growth in vitro but not for growth in intrathoracically inoculated Aedes aegypti mosquitoes. , 2007, Virology.

[71]  D. Jarvis,et al.  Protein N-glycosylation in the baculovirus-insect cell system. , 2007, Current drug targets.

[72]  A. Gamarnik,et al.  Essential Role of Dengue Virus Envelope Protein N Glycosylation at Asparagine-67 during Viral Propagation , 2007, Journal of Virology.

[73]  V. Shepherd,et al.  Virus glycosylation: role in virulence and immune interactions , 2007, Trends in Microbiology.

[74]  Ralf Bartenschlager,et al.  The Non-structural Protein 4A of Dengue Virus Is an Integral Membrane Protein Inducing Membrane Alterations in a 2K-regulated Manner* , 2007, Journal of Biological Chemistry.

[75]  M. Guzmán,et al.  Of cascades and perfect storms: the immunopathogenesis of dengue haemorrhagic fever‐dengue shock syndrome (DHF/DSS) , 2007, Immunology and cell biology.

[76]  D. Rendić,et al.  Reconstitution in vitro of the GDP‐fucose biosynthetic pathways of Caenorhabditis elegans and Drosophila melanogaster , 2006, The FEBS journal.

[77]  Yoshihiro Kawaoka,et al.  Avian flu: Influenza virus receptors in the human airway , 2006, Nature.

[78]  M. Ng,et al.  The glycosylation site in the envelope protein of West Nile virus (Sarafend) plays an important role in replication and maturation processes. , 2006, The Journal of general virology.

[79]  I. Wilson,et al.  Modulation of Neural Carbohydrate Epitope Expression in Drosophila melanogaster Cells* , 2006, Journal of Biological Chemistry.

[80]  M. Rossmann,et al.  Cryo-EM Reconstruction of Dengue Virus in Complex with the Carbohydrate Recognition Domain of DC-SIGN , 2006, Cell.

[81]  J. Gready,et al.  The C‐type lectin‐like domain superfamily , 2005, The FEBS journal.

[82]  H. Gabius,et al.  The asialoglycoprotein receptor clears glycoconjugates terminating with sialic acidα2,6GalNAc , 2005 .

[83]  M. Crabtree,et al.  Deglycosylation of the NS1 protein of dengue 2 virus, strain 16681: Construction and characterization of mutant viruses , 2005, Archives of Virology.

[84]  D. Harvey,et al.  Fragmentation of N-linked glycans with a matrix-assisted laser desorption/ionization ion trap time-of-flight mass spectrometer. , 2004, Rapid communications in mass spectrometry : RCM.

[85]  Timothy S Baker,et al.  Conformational changes of the flavivirus E glycoprotein. , 2004, Structure.

[86]  T. Chambers,et al.  HCV E2 glycoprotein: mutagenesis of N-linked glycosylation sites and its effects on E2 expression and processing. , 2004, Virology.

[87]  Y. Modis,et al.  Structure of the dengue virus envelope protein after membrane fusion , 2004, Nature.

[88]  C. Figdor,et al.  Microdomains of the C-type lectin DC-SIGN are portals for virus entry into dendritic cells , 2004, The Journal of cell biology.

[89]  Alessandra Cambi,et al.  Dual function of C-type lectin-like receptors in the immune system. , 2003, Current opinion in cell biology.

[90]  P. Desprès,et al.  Dendritic‐cell‐specific ICAM3‐grabbing non‐integrin is essential for the productive infection of human dendritic cells by mosquito‐cell‐derived dengue viruses , 2003, EMBO reports.

[91]  R. A. Ezekowitz,et al.  Role of the mannose-binding lectin in innate immunity. , 2003, The Journal of infectious diseases.

[92]  Ying Zhang,et al.  Structures of immature flavivirus particles , 2003, The EMBO journal.

[93]  Y. Modis,et al.  A ligand-binding pocket in the dengue virus envelope glycoprotein , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[94]  R. Steinman,et al.  DC-SIGN (CD209) Mediates Dengue Virus Infection of Human Dendritic Cells , 2003, The Journal of experimental medicine.

[95]  A. Suhrbier,et al.  Suppression of antiviral responses by antibody-dependent enhancement of macrophage infection. , 2003, Trends in immunology.

[96]  A. Helenius,et al.  Folding and Dimerization of Tick-Borne Encephalitis Virus Envelope Proteins prM and E in the Endoplasmic Reticulum , 2002, Journal of Virology.

[97]  J. Roehrig,et al.  Monoclonal Antibodies That Bind to Domain III of Dengue Virus E Glycoprotein Are the Most Efficient Blockers of Virus Adsorption to Vero Cells , 2001, Journal of Virology.

[98]  I. Braakman,et al.  Folding of the human immunodeficiency virus type 1 envelope glycoprotein in the endoplasmic reticulum. , 2001, Biochimie.

[99]  C. Mandl,et al.  Mutational Evidence for an Internal Fusion Peptide in Flavivirus Envelope Protein E , 2001, Journal of Virology.

[100]  R. Contreras,et al.  Ultrasensitive profiling and sequencing of N-linked oligosaccharides using standard DNA-sequencing equipment. , 2001, Glycobiology.

[101]  T. Takegami,et al.  Comparative Sequences of Two Type 1 Dengue Virus Strains Possessing Different Growth Characteristics In Vitro , 2001, Microbiology and immunology.

[102]  J. Bergelson,et al.  Retargeting the Coxsackievirus and Adenovirus Receptor to the Apical Surface of Polarized Epithelial Cells Reveals the Glycocalyx as a Barrier to Adenovirus-Mediated Gene Transfer , 2000, Journal of Virology.

[103]  M. Cadene,et al.  Hybrid and complex glycans are linked to the conserved N-glycosylation site of the third eight-cysteine domain of LTBP-1 in insect cells. , 2000, Biochemistry.

[104]  P. Desprès,et al.  α-Glucosidase Inhibitors Reduce Dengue Virus Production by Affecting the Initial Steps of Virion Morphogenesis in the Endoplasmic Reticulum , 2000, Journal of Virology.

[105]  T. Kishi,et al.  N-glycan structures of murine hippocampus serine protease, neuropsin, produced in Trichoplusia ni cells , 1999, Glycoconjugate Journal.

[106]  J. Lepault,et al.  Dengue Virus Type 1 Nonstructural Glycoprotein NS1 Is Secreted from Mammalian Cells as a Soluble Hexamer in a Glycosylation-Dependent Fashion , 1999, Journal of Virology.

[107]  C. King,et al.  Analysis of the steps involved in Dengue virus entry into host cells. , 1999, Virology.

[108]  J. Dubuisson,et al.  Analysis of the glycosylation sites of hepatitis C virus (HCV) glycoprotein E1 and the influence of E1 glycans on the formation of the HCV glycoprotein complex. , 1999, The Journal of general virology.

[109]  Robert Anderson,et al.  PrM- and Cell-Binding Domains of the Dengue Virus E Protein , 1999, Journal of Virology.

[110]  A. Davidson,et al.  Growth restriction of dengue virus type 2 by site-specific mutagenesis of virus-encoded glycoproteins. , 1998, The Journal of general virology.

[111]  F. Heinz,et al.  Proteolytic activation of tick-borne encephalitis virus by furin , 1997, Journal of virology.

[112]  R. Dwek,et al.  Rapid, sensitive sequencing of oligosaccharides from glycoproteins. , 1997, Current opinion in biotechnology.

[113]  L. Dalgarno,et al.  Changes in the dengue virus major envelope protein on passaging and their localization on the three-dimensional structure of the protein. , 1997, Virology.

[114]  M. Betenbaugh,et al.  Differential N-Glycan Patterns of Secreted and Intracellular IgG Produced in Trichoplusia ni Cells* , 1997, The Journal of Biological Chemistry.

[115]  R. Dwek,et al.  The Glycosylation of the Influenza A Virus Hemagglutinin by Mammalian Cells , 1997, The Journal of Biological Chemistry.

[116]  P. Young,et al.  Immunolocalization of the dengue virus nonstructural glycoprotein NS1 suggests a role in viral RNA replication. , 1996, Virology.

[117]  S. Harrison,et al.  The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution , 1995, Nature.

[118]  C. Mandl,et al.  Oligomeric rearrangement of tick-borne encephalitis virus envelope proteins induced by an acidic pH , 1995, Journal of virology.

[119]  J. Roehrig,et al.  The envelope glycoproteins of dengue 1 and dengue 2 viruses grown in mosquito cells differ in their utilization of potential glycosylation sites. , 1994, Virology.

[120]  P. J. Wright,et al.  Glycosylation mutants of dengue virus NS1 protein. , 1994, The Journal of general virology.

[121]  A. Pletnev,et al.  Chimeric tick-borne encephalitis and dengue type 4 viruses: effects of mutations on neurovirulence in mice , 1993, Journal of virology.

[122]  P. J. Wright,et al.  The effects of site-directed mutagenesis on the dimerization and secretion of the NS1 protein specified by dengue virus. , 1993, Virology.

[123]  J. Vliegenthart,et al.  Primary structures of the N-linked carbohydrate chains from honeybee venom phospholipase A2. , 1993, European journal of biochemistry.

[124]  J. Roehrig,et al.  Selection and partial characterization of dengue 2 virus mutants that induce fusion at elevated pH. , 1993, Virology.

[125]  E. Konishi,et al.  Proper maturation of the Japanese encephalitis virus envelope glycoprotein requires cosynthesis with the premembrane protein , 1993, Journal of virology.

[126]  K. Hård,et al.  α1–6(α1–3)-Difucosylation of the asparagine-boundN-acetylglucosamine in honeybee venom phospholipase A2 , 1992, Glycoconjugate Journal.

[127]  J. Stephenson,et al.  High-level expression of the tick-borne encephalitis virus NS1 protein by using an adenovirus-based vector: protection elicited in a murine model , 1992, Journal of virology.

[128]  M. Bouloy,et al.  Characterization of yellow fever virus proteins E and NS1 expressed in Vero and Spodoptera frugiperda cells. , 1991, The Journal of general virology.

[129]  C. Lai,et al.  Both nonstructural proteins NS2B and NS3 are required for the proteolytic processing of dengue virus nonstructural proteins , 1991, Journal of virology.

[130]  V. Stollar,et al.  Newly synthesized dengue-2 virus nonstructural protein NS1 is a soluble protein but becomes partially hydrophobic and membrane-associated after dimerization. , 1989, Virology.

[131]  P. Mason Maturation of Japanese encephalitis virus glycoproteins produced by infected mammalian and mosquito cells , 1989, Virology.

[132]  A. Nisalak,et al.  Antibody-dependent enhancement of dengue virus growth in human monocytes as a risk factor for dengue hemorrhagic fever. , 1989, The American journal of tropical medicine and hygiene.

[133]  K. Irie,et al.  Functional and antigenic domains of the dengue-2 virus nonstructural glycoprotein NS-1. , 1988, Virology.

[134]  G. Smith,et al.  Synthesis of proteins and glycoproteins in dengue type 2 virus-infected vero and Aedes albopictus cells. , 1985, The Journal of general virology.

[135]  Phillips W. Robbinst,et al.  Regulation of asparagine-linked oligosaccharide processing. Oligosaccharide processing in Aedes albopictus mosquito cells. , 1984, The Journal of biological chemistry.

[136]  R. Cardiff,et al.  Dengue Virions and Antigens in Brain and Serum of Infected Mice , 1970, Journal of virology.

[137]  K. Yoshii,et al.  N-linked glycan in tick-borne encephalitis virus envelope protein affects viral secretion in mammalian cells, but not in tick cells. article (author version) , 2018 .

[138]  M. Wuhrer,et al.  Site-Specific N- and O-Glycopeptide Analysis Using an Integrated C18-PGC-LC-ESI-QTOF-MS/MS Approach. , 2017, Methods in molecular biology.

[139]  R. Bartenschlager,et al.  Revisiting dengue virus-host cell interaction: new insights into molecular and cellular virology. , 2014, Advances in virus research.

[140]  Oscar Nierstrasz,et al.  Journal of Software Maintenance and Evolution: Research and Practice Software Cartography: Thematic Software Visualization with Consistent Layout ‡ , 2022 .

[141]  T. Hase,et al.  Flavivirus entry into cultured mosquito cells and human peripheral blood monocytes , 2005, Archives of Virology.

[142]  E. G. Westaway,et al.  Variation in distribution of the three flavivirus-specified glycoproteins detected by immunofluorescence in infected Vero cells , 2005, Archives of Virology.

[143]  T. Hase,et al.  A comparative study of entry modes into C6/36 cells by Semliki Forest and Japanese encephalitis viruses , 2005, Archives of Virology.

[144]  H. Gabius,et al.  The asialoglycoprotein receptor clears glycoconjugates terminating with sialic acid alpha 2,6GalNAc. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[145]  N. Thielens,et al.  Interaction of C1q and mannan-binding lectin with viruses. , 2002, Immunobiology.

[146]  A. Nisalak,et al.  Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. , 2000, The Journal of infectious diseases.

[147]  F. Altmann,et al.  Structures of the N-linked oligosaccharides of the membrane glycoproteins from three lepidopteran cell lines (Sf-21, IZD-Mb-0503, Bm-N). , 1994, Archives of biochemistry and biophysics.

[148]  K. Hård,et al.  Alpha 1-6(alpha 1-3)-difucosylation of the asparagine-bound N-acetylglucosamine in honeybee venom phospholipase A2. , 1992, Glycoconjugate journal.

[149]  C. Rice,et al.  Flavivirus genome organization, expression, and replication. , 1990, Annual review of microbiology.

[150]  V. Stollar,et al.  Evidence that the mature form of the flavivirus nonstructural protein NS1 is a dimer. , 1988, Virology.