Usutu Virus escapes langerin-induced restriction to productively infect human Langerhans cells, unlike West Nile virus

References

• Poidinger M, Hall RA, Mackenzie JS. Molecular characterization of the Japanese encephalitis serocomplex of the flavivirus genus. Virology. 1996;218:417–421.
   PubMed Web of Science ®Google Scholar
• Weissenböck H, Kolodziejek J, Url A, et al. Emergence of Usutu virus, an African mosquito-borne flavivirus of the Japanese encephalitis virus group, central Europe. Emerg Infect Dis. 2002;8:652–656.
   PubMed Web of Science ®Google Scholar
• Clé M, Beck C, Salinas S, et al. Usutu virus: A new threat? Epidemiol Infect. 2019;147:e232.
   PubMed Web of Science ®Google Scholar
• Roesch F, Fajardo A, Moratorio G, et al. Usutu virus: An arbovirus on the rise. Viruses. 2019;11; doi:10.3390/v11070640.
   PubMed Web of Science ®Google Scholar
• Pierson TC, Diamond MS. The continued threat of emerging flaviviruses. Nat Microbiol. 2020;5:796–812.
   PubMed Web of Science ®Google Scholar
• Suthar MS, Diamond MS, Gale M. West Nile virus infection and immunity. Nat Rev Microbiol. 2013;11:115–128.
   PubMed Web of Science ®Google Scholar
• Gill CM, Kapadia RK, Beckham JD, et al. Usutu virus disease: a potential problem for North America? J Neurovirol. 2020;26:149–154.
   PubMed Web of Science ®Google Scholar
• Nisole S. [Usutu, that which does not kill us, makes us stronger]. Virologie (Montrouge). 2018;22:231–232.
   PubMedGoogle Scholar
• Pfeffer M, Dobler G. Emergence of zoonotic arboviruses by animal trade and migration. Parasit Vectors. 2010;3:35.
   PubMed Web of Science ®Google Scholar
• Kashem SW, Haniffa M, Kaplan DH. Antigen-presenting cells in the skin. Annu Rev Immunol. 2017;35:469–499.
   PubMed Web of Science ®Google Scholar
• Malissen B, Tamoutounour S, Henri S. The origins and functions of dendritic cells and macrophages in the skin. Nat Rev Immunol. 2014;14:417–428.
   PubMed Web of Science ®Google Scholar
• Bermejo-Jambrina M, Eder J, Helgers LC, et al. C-type lectin receptors in antiviral immunity and viral escape. Front Immunol. 2018;9; doi:10.3389/fimmu.2018.00590.
   PubMed Web of Science ®Google Scholar
• Valladeau J, Ravel O, Dezutter-Dambuyant C, et al. Langerin, a novel C-type lectin specific to Langerhans cells, is an endocytic receptor that induces the formation of Birbeck granules. Immunity. 2000;12:71–81.
   PubMed Web of Science ®Google Scholar
• Mc Dermott R, Ziylan U, Spehner D, et al. Birbeck granules are subdomains of endosomal recycling compartment in human epidermal Langerhans cells, which form where langerin accumulates. Mol Biol Cell. 2002;13:317–335.
   PubMed Web of Science ®Google Scholar
• de Witte L, Nabatov A, Pion M, et al. Langerin is a natural barrier to HIV-1 transmission by Langerhans cells. Nat Med. 2007;13:367–371.
   PubMed Web of Science ®Google Scholar
• Ribeiro CMS, Sarrami-Forooshani R, Setiawan LC, et al. Receptor usage dictates HIV-1 restriction by human TRIM5α in dendritic cell subsets. Nature. 2016;540:448–452.
   PubMed Web of Science ®Google Scholar
• Geijtenbeek TB, Torensma R, van Vliet SJ, et al. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell. 2000;100:575–585.
   PubMed Web of Science ®Google Scholar
• Geijtenbeek TBH, Kwon DS, Torensma R, et al. DC-SIGN, a dendritic cell–specific HIV-1-binding protein that enhances trans-infection of T cells. Cell. 2000;100:587–597.
   PubMed Web of Science ®Google Scholar
• Halary F, Amara A, Lortat-Jacob H, et al. Human cytomegalovirus binding to DC-SIGN is required for dendritic cell infection and target cell trans-infection. Immunity. 2002;17:653–664.
   PubMed Web of Science ®Google Scholar
• Alvarez CP, Lasala F, Carrillo J, et al. C-type lectins DC-SIGN and L-SIGN mediate cellular entry by Ebola virus in cis and in trans. J Virol. 2002;76:6841–6844.
   PubMed Web of Science ®Google Scholar
• Tassaneetrithep B, Burgess TH, Granelli-Piperno A, et al. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med. 2003;197:823–829.
   PubMed Web of Science ®Google Scholar
• Davis CW, Nguyen H-Y, Hanna SL, et al. West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection. J Virol. 2006;80:1290–1301.
   PubMed Web of Science ®Google Scholar
• Carbaugh DL, Lazear HM. Flavivirus envelope protein glycosylation: impacts on viral infection and pathogenesis. J Virol. 2020;94:e00104–20.
   PubMed Web of Science ®Google Scholar
• Ng WC, Londrigan SL, Nasr N, et al. The C-type lectin langerin functions as a receptor for attachment and infectious entry of influenza A virus. J Virol. 2016;90:206–221.
   PubMed Web of Science ®Google Scholar
• Wu SJ, Grouard-Vogel G, Sun W, et al. Human skin Langerhans cells are targets of dengue virus infection. Nat Med. 2000;6:816–820.
   PubMed Web of Science ®Google Scholar
• Duangkhae P, Erdos G, Ryman KD, et al. Interplay between keratinocytes and myeloid cells drives dengue virus spread in human skin. J Investig Dermatol. 2018;138:618–626.
   PubMed Web of Science ®Google Scholar
• Cerny D, Haniffa M, Shin A, et al. Selective susceptibility of human skin antigen presenting cells to productive dengue virus infection. PLoS Pathog. 2014;10:e1004548.
   PubMed Web of Science ®Google Scholar
• Garcia M, Wehbe M, Lévêque N, et al. Skin innate immune response to flaviviral infection. Eur Cytokine Netw. 2017;28:41–51.
   PubMed Web of Science ®Google Scholar
• Briant L, Desprès P, Choumet V, et al. Role of skin immune cells on the host susceptibility to mosquito-borne viruses. Virology. 2014;464–465:26–32.
   PubMed Web of Science ®Google Scholar
• Styer LM, Kent KA, Albright RG, et al. Mosquitoes inoculate high doses of West Nile virus as they probe and feed on live hosts. PLoS Pathog. 2007;3:1262–1270.
   PubMed Web of Science ®Google Scholar
• Lim P-Y, Behr MJ, Chadwick CM, et al. Keratinocytes are cell targets of West Nile virus in vivo. J Virol. 2011;85:5197–5201.
   PubMed Web of Science ®Google Scholar
• Martina BEE, Koraka P, van den Doel P, et al. DC-SIGN enhances infection of cells with glycosylated West Nile virus in vitro and virus replication in human dendritic cells induces production of IFN-α and TNF-α. Virus Res. 2008;135:64–71.
   PubMed Web of Science ®Google Scholar
• Zimmerman MG, Bowen JR, McDonald CE, et al. West Nile virus infection blocks inflammatory response and T cell costimulatory capacity of human monocyte-derived dendritic cells. J Virol. 2019;93:e00664-19.
   PubMed Web of Science ®Google Scholar
• Rawle DJ, Setoh YX, Edmonds JH, et al. Comparison of attenuated and virulent West Nile virus strains in human monocyte-derived dendritic cells as a model of initial human infection. Virol J. 2015;12:46.
   PubMed Web of Science ®Google Scholar
• Johnston LJ, Halliday GM, King NJ. Langerhans cells migrate to local lymph nodes following cutaneous infection with an arbovirus. J Invest Dermatol. 2000;114:560–568.
   PubMed Web of Science ®Google Scholar
• Kärber G. Beitrag zur kollektiven behandlung pharmakologischer reihenversuche. Arch Experiment Pathol u Pharmakol. 1931;162:480–483.
   Google Scholar
• Arrighi J-F, Pion M, Wiznerowicz M, et al. Lentivirus-mediated RNA interference of DC-SIGN expression inhibits human immunodeficiency virus transmission from dendritic cells to T cells. J Virol. 2004;78:10848–10855.
   PubMed Web of Science ®Google Scholar
• Maarifi G, Lagisquet J, Hertel Q, et al. Alarmin S100A9 restricts retroviral infection by limiting reverse transcription in human dendritic cells. EMBO J. 2021: e106540.
   PubMed Web of Science ®Google Scholar
• Lucas-Hourani M, Dauzonne D, Munier-Lehmann H, et al. Original chemical series of pyrimidine biosynthesis inhibitors that boost the antiviral interferon response. Antimicrob Agents Chemother. 2017;61; doi:10.1128/AAC.00383-17.
   PubMed Web of Science ®Google Scholar
• Cavrini F, Gaibani P, Longo G, et al. Usutu virus infection in a patient who underwent orthotropic liver transplantation, Italy, August-September 2009. Eurosurveillance. 2009;14:19448.
   Web of Science ®Google Scholar
• Pacenti M, Sinigaglia A, Martello T, et al. Clinical and virological findings in patients with Usutu virus infection, northern Italy, 2018. Euro Surveill. 2019;24; doi:10.2807/1560-7917.ES.2019.24.47.1900180.
   Google Scholar
• Hernández-Triana LM, Jeffries CL, Mansfield KL, et al. Emergence of west Nile virus lineage 2 in Europe: a review on the introduction and spread of a mosquito-borne disease. Front Public Health. 2014;2:271.
   PubMedGoogle Scholar
• Haller O, Staeheli P, Schwemmle M, et al. Mx GTPases: dynamin-like antiviral machines of innate immunity. Trends Microbiol. 2015;23:154–163.
   PubMed Web of Science ®Google Scholar
• Girard M, Nelson CB, Picot V, et al. Arboviruses: A global public health threat. Vaccine. 2020;38:3989–3994.
   PubMed Web of Science ®Google Scholar
• Kawamura T, Ogawa Y, Aoki R, et al. Innate and intrinsic antiviral immunity in skin. J Dermatol Sci. 2014;75:159–166.
   PubMed Web of Science ®Google Scholar
• Bertram KM, Truong NR, Smith JB, et al. Herpes simplex virus type 1 infects Langerhans cells and the novel epidermal dendritic cell, Epi-cDC2s, via different entry pathways. PLoS Pathog. 2021;17:e1009536.
   PubMed Web of Science ®Google Scholar
• Puttur FK, Fernandez MA, White R, et al. Herpes simplex virus infects skin gamma delta T cells before Langerhans cells and impedes migration of infected Langerhans cells by inducing apoptosis and blocking E-cadherin downregulation. J Immunol. 2010;185:477–487.
   PubMed Web of Science ®Google Scholar
• Clé M, Constant O, Barthelemy J, et al. Differential neurovirulence of Usutu virus lineages in mice and neuronal cells. J Neuroinflammation. 2021;18:11.
   PubMed Web of Science ®Google Scholar
• Mukhopadhyay S, Kim B-S, Chipman PR, et al. Structure of West Nile virus. Science. 2003;302:248–248.
   PubMed Web of Science ®Google Scholar
• Kuhn RJ, Zhang W, Rossmann MG, et al. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell. 2002;108:717–725.
   PubMed Web of Science ®Google Scholar
• Davis CW, Mattei LM, Nguyen H-Y, et al. The location of asparagine-linked glycans on West Nile virions controls their interactions with CD209 (dendritic cell-specific ICAM-3 grabbing nonintegrin)*. J Biol Chem. 2006;281:37183–37194.
   PubMed Web of Science ®Google Scholar
• Lozach P-Y, Burleigh L, Staropoli I, et al. Dendritic cell-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN)-mediated enhancement of dengue virus infection is independent of DC-SIGN internalization signals. J Biol Chem. 2005;280:23698–23708.
   PubMed Web of Science ®Google Scholar
• Maarifi G, Czubala MA, Lagisquet J, et al. Langerin (CD207) represents a novel interferon-stimulated gene in Langerhans cells. Cell Mol Immunol. 2020;17:547–549.
   PubMed Web of Science ®Google Scholar
• Cacciotti G, Caputo B, Selvaggi C, et al. Variation in interferon sensitivity and induction between Usutu and West Nile (lineages 1 and 2) viruses. Virology. 2015;485:189–198.
   PubMed Web of Science ®Google Scholar
• Martin M-F, Nisole S. West Nile virus restriction in mosquito and human cells: A virus under confinement. Vaccines (Basel). 2020;8; doi:10.3390/vaccines8020256.
   Web of Science ®Google Scholar
• García-Nicolás O, Lewandowska M, Ricklin ME, et al. Monocyte-Derived Dendritic Cells as model to evaluate species tropism of mosquito-borne flaviviruses. Front Cell Infect Microbiol. 2019;9:5.
   PubMed Web of Science ®Google Scholar