Distinct usage of three C-type lectins by Japanese encephalitis virus: DC-SIGN, DC-SIGNR, and LSECtin

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Abstract

Infection with West Nile virus and dengue virus, two mosquito-borne flaviviruses, is enhanced by two calcium-dependent lectins: dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin (DC-SIGN), and its related molecule (DC-SIGNR). The present study examined the relationship between Japanese encephalitis virus (JEV) infection and three lectins: DC-SIGN, DC-SIGNR, and liver sinusoidal endothelial cell lectin (LSECtin). Expression of DC-SIGNR resulted in robust JEV proliferation in a lymphoid cell line, Daudi cells, which was otherwise non-permissive to infection. DC-SIGN expression caused moderate JEV proliferation, with effects that varied according to the cells in which JEV was prepared. LSECtin expression had comparatively minor, but consistent, effects, in all cell types used in JEV preparation. While DC-SIGN/DC-SIGNR-mediated JEV infection was inhibited by yeast mannan, LSECtin-mediated infection was inhibited by N-acetylglucosamine β1-2 mannose. Although involvement of DC-SIGN/DC-SIGNR in infection seems to be a common characteristic, this is the first report on usage of LSECtin in mosquito-borne flavivirus infection.

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CD209L (L-SIGN) is a receptor for severe acute respiratory syndrome coronavirus.

Scott A Jeffers, Sonia M Tusell, Laura Gillim-Ross … (2004)

Angiotensin-converting enzyme 2 (ACE2) is a receptor for SARS-CoV, the novel coronavirus that causes severe acute respiratory syndrome [Li, W. Moore, M. J., Vasilieva, N., Sui, J., Wong, S. K., Berne, M. A., Somasundaran, M., Sullivan, J. L., Luzuriaga, K., Greenough, T. C., et al. (2003) Nature 426, 450-454]. We have identified a different human cellular glycoprotein that can serve as an alternative receptor for SARS-CoV. A human lung cDNA library in vesicular stomatitis virus G pseudotyped retrovirus was transduced into Chinese hamster ovary cells, and the cells were sorted for binding of soluble SARS-CoV spike (S) glycoproteins, S(590) and S(1180). Clones of transduced cells that bound SARS-CoV S glycoprotein were inoculated with SARS-CoV, and increases in subgenomic viral RNA from 1-16 h or more were detected by multiplex RT-PCR in four cloned cell lines. Sequencing of the human lung cDNA inserts showed that each of the cloned cell lines contained cDNA that encoded human CD209L, a C-type lectin (also called L-SIGN). When the cDNA encoding CD209L from clone 2.27 was cloned and transfected into Chinese hamster ovary cells, the cells expressed human CD209L glycoprotein and became susceptible to infection with SARS-CoV. Immunohistochemistry showed that CD209L is expressed in human lung in type II alveolar cells and endothelial cells, both potential targets for SARS-CoV. Several other enveloped viruses including Ebola and Sindbis also use CD209L as a portal of entry, and HIV and hepatitis C virus can bind to CD209L on cell membranes but do not use it to mediate virus entry. Our data suggest that the large S glycoprotein of SARS-CoV may use both ACE2 and CD209L in virus infection and pathogenesis.

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DC-SIGN (CD209) Mediates Dengue Virus Infection of Human Dendritic Cells

Boonrat Tassaneetrithep, Timothy H. Burgess, Angela Granelli-Piperno … (2003)

Dengue virus is a single-stranded, enveloped RNA virus that productively infects human dendritic cells (DCs) primarily at the immature stage of their differentiation. We now find that all four serotypes of dengue use DC-SIGN (CD209), a C-type lectin, to infect dendritic cells. THP-1 cells become susceptible to dengue infection after transfection of DC-specific ICAM-3 grabbing nonintegrin (DC-SIGN), or its homologue L-SIGN, whereas the infection of dendritic cells is blocked by anti–DC-SIGN antibodies and not by antibodies to other molecules on these cells. Viruses produced by dendritic cells are infectious for DC-SIGN– and L-SIGN–bearing THP-1 cells and other permissive cell lines. Therefore, DC-SIGN may be considered as a new target for designing therapies that block dengue infection.

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Dendritic-cell-specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses.

Erika Navarro-Sánchez, Ralf Altmeyer, Ali Amara … (2003)

Dengue virus (DV) is a mosquito-borne flavivirus that causes haemorrhagic fever in humans. DV primarily targets immature dendritic cells (DCs) after a bite by an infected mosquito vector. Here, we analysed the interactions between DV and human-monocyte-derived DCs at the level of virus entry. We show that the DC-specific ICAM3-grabbing non-integrin (DC-SIGN) molecule, a cell-surface, mannose-specific, C-type lectin, binds mosquito-cell-derived DVs and allows viral replication. Conclusive evidence for the involvement of DC-SIGN in DV infection was obtained by the inhibition of viral infection by anti-DC-SIGN antibodies and by the soluble tetrameric ectodomain of DC-SIGN. Our data show that DC-SIGN functions as a DV-binding lectin by interacting with the DV envelope glycoprotein. Mosquito-cell-derived DVs may have differential infectivity for DC-SIGN-expressing cells. We suggest that the differential use of DC-SIGN by viral envelope glycoproteins may account for the immunopathogenesis of DVs.

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Author and article information

Contributors

Masayuki Shimojima: +81-42-8487020 , +81-42-5612039 , shimoji-@nih.go.jp

Atsushi Takenouchi: m014gc@yamaguchi-u.ac.jp

Hiroshi Shimoda: hshimoda@yamguchi-u.ac.jp

Naho Kimura: k012gc@yamaguchi-u.ac.jp

Ken Maeda: kmaeda@yamaguchi-u.ac.jp

Journal

Journal ID (nlm-ta): Arch Virol

Journal ID (iso-abbrev): Arch. Virol

Title: Archives of Virology

Publisher: Springer Vienna (Vienna )

ISSN (Print): 0304-8608

ISSN (Electronic): 1432-8798

Publication date (Electronic): 13 March 2014

Publication date (Print): 2014

Volume: 159

Issue: 8

Pages: 2023-2031

Affiliations

[1 ]GRID grid.268397.1, ISNI 0000000106607960, Laboratory of Veterinary Microbiology, Faculty of Agriculture, , Yamaguchi University, ; 1677-1 Yoshida, Yamaguchi, 753-8515 Japan

[2 ]GRID grid.410795.e, ISNI 0000000122201880, Present Address: Special Pathogens Laboratory, Department of Virology I, , National Institute of Infectious Diseases, ; 4-7-1 Gakuen, Musashimurayama, Tokyo 208-0011 Japan

Article

Publisher ID: 2042

DOI: 10.1007/s00705-014-2042-2

PMC ID: 7087284

PubMed ID: 24623090

SO-VID: e301edf9-cef6-4b0b-a795-f21ce8dc02a7

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This article is made available via the PMC Open Access Subset for unrestricted research re-use and secondary analysis in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the World Health Organization (WHO) declaration of COVID-19 as a global pandemic.

History

Date received : 30 November 2013

Date accepted : 28 February 2014

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ScienceOpen disciplines: Microbiology & Virology

Keywords: west nile virus,dengue virus,japanese encephalitis virus,japanese encephalitis

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ScienceOpen disciplines: Microbiology & Virology

Keywords: west nile virus, dengue virus, japanese encephalitis virus, japanese encephalitis

Distinct usage of three C-type lectins by Japanese encephalitis virus: DC-SIGN, DC-SIGNR, and LSECtin

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Decoding Infection and Transmission

Most cited references 23

CD209L (L-SIGN) is a receptor for severe acute respiratory syndrome coronavirus.

DC-SIGN (CD209) Mediates Dengue Virus Infection of Human Dendritic Cells

Dendritic-cell-specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses.

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