The contributions of TLR2, TLR8 and TLR3 to direct and antibody-dependent enhancement of dengue virus serotype 2 infection

The contributions of TLR2, TLR8 and TLR3 to direct and antibody-dependent enhancement of dengue virus serotype 2 infection

  • Bhatt, S. et al. The global distribution and burden of dengue. Nature https://doi.org/10.1038/nature12060 (2013).

  • World Health Organization. Dengue control 2018. http://www.who.int/denguecontrol/disease/en/).

  • De La Cruz Hernández, S. I. et al. Primary dengue virus infections induce differential cytokine production in Mexican patients. Mem. Inst. Oswaldo Cruz 111, 161–167 (2016).

    Article 

    Google Scholar
     

  • Dalrymple, N. A. & Mackow, E. R. Endothelial cells elicit immune-enhancing responses to dengue virus infection. J. Virol. 86, 6408–6415 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Guzman, M. G., Gubler, D. J., Izquierdo, A., Martinez, E. & Halstead, S. B. Dengue infection. Nat. Rev. Dis. Primer https://doi.org/10.1038/nrdp.2016.55 (2016).

  • Aguilar-Briseño, J. A., Moser, J. & Rodenhuis-Zybert, I. A. Understanding immunopathology of severe dengue: lessons learnt from sepsis. Curr. Opin. Virol. 43, 41–49 (2020).

    Article 
    PubMed 

    Google Scholar
     

  • Flipse, J., Wilschut, J. & Smit, J. M. Molecular mechanisms involved in antibody-dependent enhancement of dengue virus infection in humans. Traffic 14, 25–35 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ayala-Nunez, N. V. et al. How antibodies alter the cell entry pathway of dengue virus particles in macrophages. Sci Rep 6, 28768 (2016). https://doi.org/10.1038/srep28768.

  • Narayan, R. & Tripathi, S. Intrinsic ADE: the dark side of antibody dependent enhancement during dengue infection. Front. Cell. Infect. Microbiol. 10, (2020).

  • Bournazos, S., Gupta, A. & Ravetch, J. V. The role of IgG Fc receptors in antibody-dependent enhancement. Nat. Rev. Immunol. 20 (2020).

  • Kou, Z. et al. Monocytes, but not T or B cells, are the principal target cells for dengue virus (DV) infection among human peripheral blood mononuclear cells. J. Med. Virol. 80 (2008).

  • Durbin, A. P. et al. Phenotyping of peripheral blood mononuclear cells during acute dengue illness demonstrates infection and increased activation of monocytes in severe cases compared to classic dengue fever. Virology 376 (2008).

  • Kwissa, M. et al. Dengue virus infection induces expansion of a CD14(+)CD16(+) monocyte population that stimulates plasmablast differentiation. Cell Host Microbe 16, 115–127 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Aguilar-Briseño, J. A. et al. TLR2 on blood monocytes senses dengue virus infection and its expression correlates with disease pathogenesis. Nat. Commun. 11 (2020).

  • Castillo, J. A., Naranjo, J. S., Rojas, M., Castaño, D. & Velilla, P. A. Role of monocytes in the pathogenesis of dengue. Arch. Immunol. Ther. Exp.) 67, 27–40 (2019).

    Article 
    CAS 

    Google Scholar
     

  • Anderson, K. B. et al. A shorter time interval between first and second dengue infections is associated with protection from clinical illness in a school-based cohort in Thailand. J. Infect. Dis. 209, 360–368 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Anderson, R., Wang, S., Osiowy, C. & Issekutz, A. C. Activation of endothelial cells via antibody-enhanced dengue virus infection of peripheral blood monocytes. J. Virol. 71, 4226–4232 (1997).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yamin, R. et al. Human FcγRIIIa activation on splenic macrophages drives dengue pathogenesis in mice. Nat. Microbiol. https://doi.org/10.1038/s41564-023-01421-y (2023).

  • Tassaneetrithep, B. et al. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 197, 823–829 (2003).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Upasani, V., Rodenhuis-Zybert, I. & Cantaert, T. Antibody-independent functions of B cells during viral infections. PLoS Pathog 17, e1009708 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Upasani, V. et al. Direct Infection of B cells by dengue virus modulates B cell responses in a Cambodian pediatric cohort. Front. Immunol. 11, 594813 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gebo, C. et al. B cell receptor dependent enhancement of dengue virus infection. PLoS Pathog. 20, e1012683 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stiasny, K., Fritz, R., Pangerl, K. & Heinz, F. X. Molecular mechanisms of flavivirus membrane fusion. Amino Acids 41, 1159–1163 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Aguilar Briseño, J. A. et al. TLR2 axis on peripheral blood mononuclear cells regulates inflammatory responses to non-infectious immature dengue virus particles. PLoS Pathog. 18, e1010499 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tsai, T.T. et al. Antibody-dependent enhancement infection facilitates dengue virus-regulated signaling of IL-10 production in monocytes. PLoS Negl. Trop. Dis. 8, e3320 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Boonnak, K., Slike, B. M., Donofrio, G. C. & Marovich, M. A. Human FcγRII cytoplasmic domains differentially influence antibody-mediated dengue virus infection. J. Immunol. 190, 5659–5665 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sun, P. et al. Infection and activation of human peripheral blood monocytes by dengue viruses through the mechanism of antibody-dependent enhancement. Virology 421, 245–252 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen, S.T. et al. CLEC5A is critical for dengue-virus-induced lethal disease. Nature 453, 672–676 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ong, E. Z. et al. Dengue virus compartmentalization during antibody-enhanced infection. Sci. Rep. 7 (2017).

  • Chan, K. R. et al. Leukocyte immunoglobulin-like receptor B1 is critical for antibody-dependent dengue. Proc. Natl. Acad. Sci. USA 111 (2014).

  • Kawai, T. & Akira, S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637–650 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hoepel, W. et al. FcγR-TLR cross-talk enhances TNF production by human monocyte-derived DCs via IRF5-dependent gene transcription and glycolytic reprogramming. Front. Immunol. 10, 739 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, W., Li, M., Anthony, S. M. & Yu, Y. Spatial organization of FcγR and TLR2/1 on phagosome membranes differentially regulates their synergistic and inhibitory receptor crosstalk. Sci. Rep. 11, 13430 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, M. et al. Immobile ligands enhance FcγR-TLR2/1 crosstalk by promoting interface overlap of receptor clusters. Biophys. J. 121, 966–976 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Heit, B. et al. Multimolecular signaling complexes enable Syk-mediated signaling of CD36 internalization. Dev. Cell 24, 372–383 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Castillo, R. Innate Immune Responses of Monocytes/Macrophages to DENV-2 infection (University of Groningen, 2023).

  • Mistry, P. et al. Inhibition of TLR2 signaling by small molecule inhibitors targeting a pocket within the TLR2 TIR domain. Proc. Natl. Acad. Sci. USA 112, 5455–5460 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Triantafilou, M. et al. Membrane sorting of toll-like receptor (TLR)-2/6 and TLR2/1 heterodimers at the cell surface determines heterotypic associations with CD36 and intracellular targeting. J. Biol. Chem. 281, 31002–31011 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Stuart, L. M. et al. Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J. Cell Biol. 170, 477–485 (2005).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nilsen, N. et al. Cellular trafficking of lipoteichoic acid and Toll-like receptor 2 in relation to signaling; role of CD14 and CD36. J. Leukoc. Biol. 84, 280–291 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Spiropoulou, C. F. & Srikiatkhachorn, A. The role of endothelial activation in dengue hemorrhagic fever and hantavirus pulmonary syndrome. Virulence 4, 525–536 (2013).

  • Kawasaki, T. & Kawai, T. Toll-like receptor signaling pathways. Front. Immunol. https://doi.org/10.3389/fimmu.2014.00461 (2014).

  • El-Zayat, S. R., Sibaii, H. & Mannaa, F. A. Toll-like receptors activation, signaling, and targeting: an overview. Bull. Natl. Res. Cent. 43, 187 (2019).

    Article 

    Google Scholar
     

  • Shah, P. et al. Toll-like receptor 2 ligands regulate monocyte fcγ receptor expression and function. J. Biol. Chem. 288, 12345–12352 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, M., Wang, H., Li, W., Xu, X. G. & Yu, Y. Macrophage activation on “phagocytic synapse” arrays: Spacing of nanoclustered ligands directs TLR1/2 signaling with an intrinsic limit. Sci. Adv. 6, eabc8482 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Simmons, C. P. et al. Maternal antibody and viral factors in the pathogenesis of dengue virus in infants. J. Infect. Dis. 196, 416–424 (2007).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Brandt, K. J., Fickentscher, C., Kruithof, E. K. O. & de Moerloose, P. TLR2 ligands induce NF-κB activation from endosomal compartments of human monocytes. PLoS ONE 8, e80743 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Barbalat, R., Lau, L., Locksley, R. M. & Barton, G. M. Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat. Immunol. 10, 1200–1207 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ip, W. K. E., Takahashi, K., Moore, K. J., Stuart, L. M. & Ezekowitz, R. A. B. Mannose-binding lectin enhances Toll-like receptors 2 and 6 signaling from the phagosome. J. Exp. Med. 205, 169–181 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zahoor, A. et al. MerTK negatively regulates Staphylococcus aureus induced inflammatory response via Toll-like receptor signaling in the mammary gland. Mol. Immunol. 122, 1–12 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Seo, J. Y., Choi, J. W., Lee, J. Y., Park, Y. S. & Park, Y. I. Enzyme hydrolysates of ginseng marc polysaccharides promote the phagocytic activity of macrophages via activation of TLR2 and Mer tyrosine kinase. 28, 860–873 (2018).

  • Zizzo, G. & Cohen, P. L. Antibody cross-linking of CD14 activates MerTK and promotes human macrophage clearance of apoptotic neutrophils: the dual role of CD14 at the crossroads between M1 and M2c polarization. Inflammation 41, 2206–2221 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li, W., Yan, J. & Yu, Y. Geometrical reorganization of Dectin-1 and TLR2 on single phagosomes alters their synergistic immune signaling. Proc. Natl. Acad. Sci. USA 116, 25106–25114 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, Y., Hoppe, A. D. & Swanson, J. A. Coordination of Fc receptor signaling regulates cellular commitment to phagocytosis. Proc. Natl. Acad. Sci. USA 107, 19332–19337 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Crowley, M. T. et al. A critical role for Syk in signal transduction and phagocytosis mediated by Fcgamma receptors on macrophages. J. Exp. Med. 186, 1027–1039 (1997).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fitzer-Attas, C. J. et al. Fcgamma receptor-mediated phagocytosis in macrophages lacking the Src family tyrosine kinases Hck, Fgr, and Lyn. J. Exp. Med. 191, 669–682 (2000).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Aouar, B. et al. Dual role of the tyrosine kinase Syk in regulation of toll-like receptor signaling in plasmacytoid dendritic cells. PLoS ONE 11, e0156063 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhai, N. et al. Hepatitis C virus induces MDSCs-like monocytes through TLR2/PI3K/AKT/STAT3 signaling. PLoS ONE 12, e0170516 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lin, Y.C., Huang, D.Y., Chu, C.L., Lin, Y.L. & Lin, W.W. The tyrosine kinase Syk differentially regulates toll-like receptor signaling downstream of the adaptor molecules TRAF6 and TRAF3. Sci. Signal. 6, ra71 (2013).

    Article 
    PubMed 

    Google Scholar
     

  • Fang, L., Wu, H.M., Ding, P.S. & Liu, R.Y. TLR2 mediates phagocytosis and autophagy through JNK signaling pathway in Staphylococcus aureus-stimulated RAW264.7 cells. Cell. Signal. 26, 806–814 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhao, G. et al. Toll-like receptor 2 signaling pathway activation contributes to a highly efficient inflammatory response in Japanese encephalitis virus-infected mouse microglial cells by proteomics. Front. Microbiol. 13, 989183 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Belmont, L. et al. Functional genomics screens reveal a role for TBC1D24 and SV2B in antibody-dependent enhancement of dengue virus infection. J. Virol. 98, e01582–24 (2024).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Junjhon, J. et al. Influence of pr-M cleavage on the heterogeneity of extracellular dengue virus particles. J. Virol. 84, 8353–8358 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Martinez, J., Huang, X. & Yang, Y. Toll-like receptor 8-mediated activation of murine plasmacytoid dendritic cells by vaccinia viral DNA. Proc. Natl. Acad. Sci. USA 107, 6442–6447 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Triantafilou, K. et al. Human cardiac inflammatory responses triggered by Coxsackie B viruses are mainly Toll-like receptor (TLR) 8-dependent. Cell. Microbiol. 7, 1117–1126 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Paul, A. M. et al. TLR8 couples SOCS-1 and restrains TLR7-mediated antiviral immunity exacerbating West Nile virus infection in mice. J. Immunol. 197, 4425–4435 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wang, J. P. et al. Toll-like receptor–mediated activation of neutrophils by influenza A virus. Blood 112, 2028–2034 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Huo, C. et al. Lethal influenza A virus preferentially activates TLR3 and triggers a severe inflammatory response. Virus Res. 257, 102–112 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Daffis, S., Samuel, M. A., Suthar, M. S., Gale, M. & Diamond, M. S. Toll-like receptor 3 has a protective role against West Nile Virus Infection. J. Virol. 82, 10349–10358 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Posadas-Mondragón, A. et al. Association of genetic polymorphisms in TLR3, TLR4, TLR7, and TLR8 with the clinical forms of dengue in patients from Veracruz, Mexico. Viruses 12, 1230 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Alagarasu, K., Bachal, R. V., Memane, R. S., Shah, P. S. & Cecilia, D. Polymorphisms in RNA sensing toll like receptor genes and its association with clinical outcomes of dengue virus infection. Immunobiology 220, 164–168 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sengupta, S., Mukherjee, S., Bhattacharya, N. & Tripathi, A. Differential genotypic signatures of Toll-like receptor polymorphisms among dengue-chikungunya mono- and co-infected Eastern Indian patients. Eur. J. Clin. Microbiol. Infect. Dis. 40, 1369–1381 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Torres, S. et al. Differential expression of toll-like receptors in dendritic cells of patients with dengue during early and late acute phases of the disease. PLoS Negl. Trop. Dis. 7, e2060 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tsai, Y.T., Chang, S.Y., Lee, C.N. & Kao, C.L. Human TLR3 recognizes dengue virus and modulates viral replication in vitro. Cell. Microbiol. 11, 604–615 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Liang, Z. et al. Activation of Toll-like receptor 3 impairs the dengue virus serotype 2 replication through induction of IFN-β in cultured hepatoma cells. PLoS ONE 6, e23346 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lien, T.S. et al. Dengue virus and antiplatelet autoantibodies synergistically induce haemorrhage through Nlrp3-inflammasome and FcγRIII. Thromb. Haemost. 113, 1060–1070 (2015).

    Article 
    PubMed 

    Google Scholar
     

  • Hsu, Y.L., Wang, M.Y., Ho, L.J. & Lai, J.H. Dengue virus infection induces interferon-lambda1 to facilitate cell migration. Sci. Rep. 6, 24530 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bösl, K. et al. Coactivation of TLR2 and TLR8 in primary human monocytes triggers a distinct inflammatory signaling response. Front. Physiol. 9, 618 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, W.W. et al. Ubiquitination of TLR3 by TRIM3 signals its ESCRT-mediated trafficking to the endolysosomes for innate antiviral response. Proc. Natl. Acad. Sci. USA 117, 23707–23716 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nanaware, N., Banerjee, A., Mullick Bagchi, S., Bagchi, P. & Mukherjee, A. Dengue virus infection: a tale of viral exploitations and host responses. Viruses 13, 1967 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nishiya, T., Kajita, E., Miwa, S. & DeFranco, A. L. TLR3 and TLR7 are targeted to the same intracellular compartments by distinct regulatory elements*. J. Biol. Chem. 280, 37107–37117 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mielcarska, M. B. et al. Participation of endosomes in toll-like receptor 3 transportation pathway in murine astrocytes. Front. Cell. Neurosci. 14 (2020).

  • McGettrick, A. F. & O’Neill, L. A. J. Localisation and trafficking of Toll-like receptors: an important mode of regulation. Curr. Opin. Immunol. 22, 20–27 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kagan, J. C. Infection infidelities drive innate immunity. Science 379, 333–335 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Callaway, J. B. et al. Spleen tyrosine kinase (Syk) mediates IL-1β induction by primary human monocytes during antibody-enhanced dengue virus infection. J. Biol. Chem. 290, 17306–17320 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Baronti, C., Pastorino, B., Charrel, R. & de Lamballerie, X. Mycoplasma removal: simple curative methods for viral supernatants. J. Virol. Methods https://doi.org/10.1016/j.jviromet.2012.09.014 (2013).

  • Rodenhuis-Zybert, I. A. et al. Immature dengue virus: a veiled pathogen? PLoS Pathog. https://doi.org/10.1371/journal.ppat.1000718 (2010).

  • van der Schaar, H. M. et al. Characterization of the early events in dengue virus cell entry by biochemical assays and single-virus tracking. J. Virol. https://doi.org/10.1128/JVI.00300-07 (2007).

  • Zybert, I. A., van der Ende-Metselaar, H., Wilschut, J. & Smit, J. M. Functional importance of dengue virus maturation: Infectious properties of immature virions. J. Gen. Virol. https://doi.org/10.1099/vir.0.2008/002535-0 (2008).

  • Van Duijl-Richter, M. K. S., Blijleven, J. S., van Oijen, A. M. & Smit, J. M. Chikungunya virus fusion properties elucidated by single-particle and bulk approaches. J. Gen. Virol. https://doi.org/10.1099/vir.0.000144 (2015).

  • Lhermusier, T. et al. The Syk-kinase inhibitor R406 impairs platelet activation and monocyte tissue factor expression triggered by heparin-PF4 complex directed antibodies. J. Thromb. Haemost. 9, 2067–2076 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhang, S. et al. Small-molecule inhibition of TLR8 through stabilization of its resting state. Nat. Chem. Biol. 14, 58–64 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pierson, T. C. et al. The stoichiometry of antibody-mediated neutralization and enhancement of West Nile virus infection. Cell Host Microbe 1, 135–145 (2007).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lux, A., Yu, X., Scanlan, C. N. & Nimmerjahn, F. Impact of immune complex size and glycosylation on IgG binding to human FcγRs. J. Immunol. 190, 4315–4323 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lu, L. L., Suscovich, T. J., Fortune, S. M. & Alter, G. Beyond binding: antibody effector functions in infectious diseases. Nat. Rev. Immunol. 18, 46–61 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sarker, A., Dhama, N. & Gupta, R. D. Dengue virus neutralizing antibody: a review of targets, cross-reactivity, and antibody-dependent enhancement. Front. Immunol. 14 (2023).