Transient Blockade of Type I Interferon Signalling Promotes Replication of Dengue Virus Strain D2Y98P in Adult Wild-Type Mice
Abstract
:1. Introduction
2. Materials and Methods
2.1. Ethics Statement
2.2. Mice
2.3. Cells and Virus
2.4. Mouse Infections
2.5. Virus Titrations
2.6. Neutralisation Assay
2.7. Viral RNA Quantification
2.8. Statistical Analysis
3. Results
3.1. D2Y98P Infection Is Asymptomatic in Adult Wild-Type Mice Treated with IFNAR1-Blocking Antibody
3.2. Infectious Virus Is Undetectable in Sera and Organs of D2Y98P-Infected Adult Wild-Type Mice Treated with IFNAR1-Blocking Antibody
3.3. High Levels of Viral RNA Are Present in Sera and Organs of D2Y98P-Infected Adult Wild-Type Mice Treated with IFNAR1-Blocking Antibody
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Bhatt, S.; Gething, P.W.; Brady, O.J.; Messina, J.P.; Farlow, A.W.; Moyes, C.L.; Drake, J.M.; Brownstein, J.S.; Hoen, A.G.; Sankoh, O.; et al. The global distribution and burden of dengue. Nature 2013, 496, 504–507. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martina, B.E.E.; Koraka, P.; Osterhaus, A.D.M.E. Dengue virus pathogenesis: An integrated view. Clin. Microbiol. Rev. 2009, 22, 564–581. [Google Scholar] [CrossRef] [Green Version]
- OhAinle, M.; Balmaseda, A.; Macalalad, A.R.; Tellez, Y.; Zody, M.C.; Saborío, S.; Nuñez, A.; Lennon, N.J.; Birren, B.W.; Gordon, A.; et al. Dynamics of dengue disease severity determined by the interplay between viral genetics and serotype-specific immunity. Sci. Transl. Med. 2011, 3, 114ra128. [Google Scholar] [CrossRef] [Green Version]
- Vaughn, D.W.; Green, S.; Kalayanarooj, S.; Innis, B.L.; Nimmannitya, S.; Suntayakorn, S.; Endy, T.P.; Raengsakulrach, B.; Rothman, A.L.; Ennis, F.A.; et al. Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J. Infect. Dis. 2000, 181, 2–9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boonnak, K.; Slike, B.M.; Burgess, T.H.; Mason, R.M.; Wu, S.-J.; Sun, P.; Porter, K.; Rudiman, I.F.; Yuwono, D.; Puthavathana, P.; et al. Role of dendritic cells in antibody-dependent enhancement of dengue virus infection. J. Virol. 2008, 82, 3939–3951. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Halstead, S.B.; O’Rourke, E.J. Antibody-enhanced dengue virus infection in primate leukocytes. Nature 1977, 265, 739–741. [Google Scholar] [CrossRef] [PubMed]
- Katzelnick, L.C.; Gresh, L.; Halloran, M.E.; Mercado, J.C.; Kuan, G.; Gordon, A.; Balmaseda, A.; Harris, E. Antibody-dependent enhancement of severe dengue disease in humans. Science 2017, 358, 929–932. [Google Scholar] [CrossRef] [Green Version]
- Balsitis, S.J.; Williams, K.L.; Lachica, R.; Flores, D.; Kyle, J.L.; Mehlhop, E.; Johnson, S.; Diamond, M.S.; Beatty, P.R.; Harris, E. Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog. 2010, 6, e1000790. [Google Scholar] [CrossRef] [Green Version]
- Dejnirattisai, W.; Jumnainsong, A.; Onsirisakul, N.; Fitton, P.; Vasanawathana, S.; Limpitikul, W.; Puttikhunt, C.; Edwards, C.; Duangchinda, T.; Supasa, S.; et al. Cross-reacting antibodies enhance dengue virus infection in humans. Science 2010, 328, 745–748. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hadinegoro, S.R.; Arredondo-García, J.L.; Capeding, M.R.; Deseda, C.; Chotpitayasunondh, T.; Dietze, R.; Hj Muhammad Ismail, H.I.; Reynales, H.; Limkittikul, K.; Rivera-Medina, D.M.; et al. Efficacy and long-term safety of a dengue vaccine in regions of endemic disease. N. Engl. J. Med. 2015, 373, 1195–1206. [Google Scholar] [CrossRef] [Green Version]
- Sridhar, S.; Luedtke, A.; Langevin, E.; Zhu, M.; Bonaparte, M.; Machabert, T.; Savarino, S.; Zambrano, B.; Moureau, A.; Khromava, A.; et al. Effect of dengue serostatus on dengue vaccine safety and efficacy. N. Engl. J. Med. 2018, 379, 327–340. [Google Scholar] [CrossRef] [PubMed]
- Halstead, S.B. Dengvaxia sensitizes seronegatives to vaccine enhanced disease regardless of age. Vaccine 2017, 35, 6355–6358. [Google Scholar] [CrossRef] [PubMed]
- Chen, R.E.; Diamond, M.S. Dengue mouse models for evaluating pathogenesis and countermeasures. Curr. Opin. Virol. 2020, 43, 50–58. [Google Scholar] [CrossRef] [PubMed]
- Johnson, A.J.; Roehrig, J.T. New mouse model for dengue virus vaccine testing. J. Virol. 1999, 73, 783–786. [Google Scholar] [CrossRef] [Green Version]
- Ashour, J.; Morrison, J.; Laurent-Rolle, M.; Belicha-Villanueva, A.; Plumlee, C.R.; Bernal-Rubio, D.; Williams, K.L.; Harris, E.; Fernandez-Sesma, A.; Schindler, C.; et al. Mouse STAT2 restricts early dengue virus replication. Cell Host Microbe 2010, 8, 410–421. [Google Scholar] [CrossRef] [Green Version]
- Aguirre, S.; Maestre, A.M.; Pagni, S.; Patel, J.R.; Savage, T.; Gutman, D.; Maringer, K.; Bernal-Rubio, D.; Shabman, R.S.; Simon, V.; et al. DENV inhibits Type I IFN production in infected cells by cleaving human STING. PLoS Pathog. 2012, 8, e1002934. [Google Scholar] [CrossRef] [Green Version]
- Shresta, S.; Kyle, J.L.; Snider, H.M.; Basavapatna, M.; Beatty, P.R.; Harris, E. Interferon-dependent immunity is essential for resistance to primary dengue virus infection in mice, whereas T- and B-cell-dependent immunity are less critical. J. Virol. 2004, 78, 2701–2710. [Google Scholar] [CrossRef] [Green Version]
- Tan, G.K.; Ng, J.K.W.; Trasti, S.L.; Schul, W.; Yip, G.; Alonso, S. A non mouse-adapted dengue virus strain as a new model of severe dengue infection in AG129 mice. PLoS Negl. Trop. Dis. 2010, 4, e672. [Google Scholar] [CrossRef]
- Orozco, S.; Schmid, M.A.; Parameswaran, P.; Lachica, R.; Henn, M.R.; Beatty, R.; Harris, E. Characterization of a model of lethal dengue virus 2 infection in C57BL/6 mice deficient in the alpha/beta interferon receptor. J. Gen. Virol. 2012, 93, 2152–2157. [Google Scholar] [CrossRef]
- Sarathy, V.V.; Infante, E.; Li, L.; Campbell, G.A.; Wang, T.; Paessler, S.; Beatty, P.R.; Harris, E.; Milligan, G.N.; Bourne, N.; et al. Characterization of lethal dengue virus type 4 (DENV-4) TVP-376 infection in mice lacking both IFN-α/β and IFN-γ receptors (AG129) and comparison with the DENV-2 AG129 mouse model. J. Gen. Virol. 2015, 96, 3035–3048. [Google Scholar] [CrossRef]
- Sarathy, V.V.; White, M.; Li, L.; Gorder, S.R.; Pyles, R.B.; Campbell, G.A.; Milligan, G.N.; Bourne, N.; Barrett, A.D.T. A lethal murine infection model for dengue virus 3 in AG129 mice deficient in Type I and II interferon receptors leads to systemic disease. J. Virol. 2015, 89, 1254–1266. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Milligan, G.N.; Sarathy, V.V.; White, M.M.; Greenberg, M.B.; Campbell, G.A.; Pyles, R.B.; Barrett, A.D.T.; Bourne, N. A lethal model of disseminated dengue virus type 1 infection in AG129 mice. J. Gen. Virol. 2017, 98, 2507–2519. [Google Scholar] [CrossRef] [PubMed]
- Fink, K.; Lang, K.S.; Manjarrez-Orduno, N.; Junt, T.; Senn, B.M.; Holdener, M.; Akira, S.; Zinkernagel, R.M.; Hengartner, H. Early type I interferon-mediated signals on B cells specifically enhance antiviral humoral responses. Eur. J. Immunol. 2006, 36, 2094–2105. [Google Scholar] [CrossRef] [PubMed]
- Heer, A.K.; Shamshiev, A.; Donda, A.; Uematsu, S.; Akira, S.; Kopf, M.; Marsland, B.J. TLR signaling fine-tunes anti-influenza B cell responses without regulating effector T cell responses. J. Immunol. 2007, 178, 2182–2191. [Google Scholar] [CrossRef] [Green Version]
- Le Bon, A.; Schiavoni, G.; D’Agostino, G.; Gresser, I.; Belardelli, F.; Tough, D.F. Type I interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo. Immunity 2001, 14, 461–470. [Google Scholar] [CrossRef] [Green Version]
- Bach, P.; Kamphuis, E.; Odermatt, B.; Sutter, G.; Buchholz, C.J.; Kalinke, U. Vesicular stomatitis virus glycoprotein displaying retrovirus-like particles induce a Type I IFN receptor-dependent switch to neutralizing IgG antibodies. J. Immunol. 2007, 178, 5839–5847. [Google Scholar] [CrossRef] [Green Version]
- Le Bon, A.; Durand, V.; Kamphuis, E.; Thompson, C.; Bulfone-Paus, S.; Rossmann, C.; Kalinke, U.; Tough, D.F. Direct stimulation of T cells by Type I IFN enhances the CD8+ T cell response during cross-priming. J. Immunol. 2006, 176, 4682–4689. [Google Scholar] [CrossRef] [Green Version]
- Lapenta, C.; Santini, S.M.; Spada, M.; Donati, S.; Urbani, F.; Accapezzato, D.; Franceschini, D.; Andreotti, M.; Barnaba, V.; Belardelli, F. IFN-α-conditioned dendritic cells are highly efficient in inducing cross-priming CD8+ T cells against exogenous viral antigens. Eur. J. Immunol. 2006, 36, 2046–2060. [Google Scholar] [CrossRef]
- Le Bon, A.; Etchart, N.; Rossmann, C.; Ashton, M.; Hou, S.; Gewert, D.; Borrow, P.; Tough, D.F. Cross-priming of CD8+ T cells stimulated by virus-induced type I interferon. Nat. Immunol. 2003, 4, 1009–1015. [Google Scholar] [CrossRef]
- Havenar-Daughton, C.; Kolumam, G.A.; Murali-Krishna, K. Cutting edge: The direct action of Type I IFN on CD4 T cells is critical for sustaining clonal expansion in response to a viral but not a bacterial infection. J. Immunol. 2006, 176, 3315–3319. [Google Scholar] [CrossRef] [Green Version]
- Le Bon, A.; Thompson, C.; Kamphuis, E.; Durand, V.; Rossmann, C.; Kalinke, U.; Tough, D.F. Cutting edge: Enhancement of antibody responses through direct stimulation of B and T Cells by Type I IFN. J. Immunol. 2006, 176, 2074–2078. [Google Scholar] [CrossRef] [Green Version]
- Kolumam, G.A.; Thomas, S.; Thompson, L.J.; Sprent, J.; Murali-Krishna, K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J. Exp. Med. 2005, 202, 637–650. [Google Scholar] [CrossRef] [Green Version]
- Curtsinger, J.M.; Valenzuela, J.O.; Agarwal, P.; Lins, D.; Mescher, M.F. Cutting edge: Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J. Immunol. 2005, 174, 4465–4469. [Google Scholar] [CrossRef] [Green Version]
- Pinto, A.K.; Daffis, S.; Brien, J.D.; Gainey, M.D.; Yokoyama, W.M.; Sheehan, K.C.F.; Murphy, K.M.; Schreiber, R.D.; Diamond, M.S. A temporal role of type I interferon signaling in CD8 + T cell maturation during acute West Nile virus infection. PLoS Pathog. 2011, 7, e1002407. [Google Scholar] [CrossRef] [Green Version]
- Züst, R.; Toh, Y.-X.; Valdés, I.; Cerny, D.; Heinrich, J.; Hermida, L.; Marcos, E.; Guillén, G.; Kalinke, U.; Shi, P.-Y.; et al. Type I interferon signals in macrophages and dendritic cells control dengue virus infection: Implications for a new mouse model to test dengue vaccines. J. Virol. 2014, 88, 7276–7285. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pinto, A.K.; Brien, J.D.; Lam, C.Y.K.; Johnson, S.; Chiang, C.; Hiscott, J.; Sarathy, V.V.; Barrett, A.D.; Shresta, S.; Diamond, M.S. Defining new therapeutics using a more immunocompetent mouse model of antibody-enhanced dengue virus infection. MBio 2015, 6, e01316-15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sheehan, K.C.F.; Lai, K.S.; Dunn, G.P.; Bruce, A.T.; Diamond, M.S.; Heutel, J.D.; Dungo-Arthur, C.; Carrero, J.A.; White, J.M.; Hertzog, P.J.; et al. Blocking monoclonal antibodies specific for mouse IFN-α/β receptor subunit 1 (IFNAR-1) from mice immunized by in vivo hydrodynamic transfection. J. Interf. Cytokine Res. 2006, 26, 804–819. [Google Scholar] [CrossRef]
- Lazear, H.M.; Govero, J.; Smith, A.M.; Platt, D.J.; Fernandez, E.; Miner, J.J.; Diamond, M.S. A mouse model of Zika virus pathogenesis. Cell Host Microbe 2016, 19, 720–730. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Smith, D.R.; Hollidge, B.; Daye, S.; Zeng, X.; Blancett, C.; Kuszpit, K.; Bocan, T.; Koehler, J.W.; Coyne, S.; Minogue, T.; et al. Neuropathogenesis of Zika virus in a highly susceptible immunocompetent mouse model after antibody blockade of Type I interferon. PLoS Negl. Trop. Dis. 2017, 11, e0005296. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gorman, M.J.; Caine, E.A.; Zaitsev, K.; Begley, M.C.; Weger-Lucarelli, J.; Uccellini, M.B.; Tripathi, S.; Morrison, J.; Yount, B.L.; Dinnon, K.H.; et al. An immunocompetent mouse model of Zika Virus infection. Cell Host Microbe 2018, 23, 672–685. [Google Scholar] [CrossRef] [Green Version]
- Roth, C.; Cantaert, T.; Colas, C.; Prot, M.; Casadémont, I.; Levillayer, L.; Thalmensi, J.; Langlade-Demoyen, P.; Gerke, C.; Bahl, K.; et al. A modified mRNA vaccine targeting immunodominant NS epitopes protects against dengue virus infection in HLA Class I transgenic mice. Front. Immunol. 2019, 10, 1424. [Google Scholar] [CrossRef]
- Sheehan, K.C.; Calderon, J.; Schreiber, R.D. Generation and characterization of monoclonal antibodies specific for the human IFN-gamma receptor. J. Immunol. 1988, 140, 4231–4237. [Google Scholar] [CrossRef] [PubMed]
- McNab, F.; Mayer-Barber, K.; Sher, A.; Wack, A.; O’Garra, A. Type I interferons in infectious disease. Nat. Rev. Immunol. 2015, 15, 87–103. [Google Scholar] [CrossRef] [PubMed]
- Zuest, R.; Valdes, I.; Skibinski, D.; Lin, Y.; Toh, Y.X.; Chan, K.; Hermida, L.; Connolly, J.; Guillen, G.; Fink, K. Tetravalent dengue DIIIC protein together with alum and ODN elicits a Th1 response and neutralizing antibodies in mice. Vaccine 2015, 33, 1474–1482. [Google Scholar] [CrossRef] [PubMed]
- Lee, P.X.; Ting, D.H.R.; Boey, C.P.H.; Tan, E.T.X.; Chia, J.Z.H.; Idris, F.; Oo, Y.; Ong, L.C.; Chua, Y.L.; Hapuarachchi, C.; et al. Relative contribution of nonstructural protein 1 in dengue pathogenesis. J. Exp. Med. 2020, 217, e20191548. [Google Scholar] [CrossRef] [PubMed]
- Aaskov, J.; Buzacott, K.; Thu, H.M.; Lowry, K.; Holmes, E.C. Long-term transmission of defective RNA viruses in humans and aedes mosquitoes. Science 2006, 311, 236–238. [Google Scholar] [CrossRef]
- Bates, T.A.; Chuong, C.; Hawks, S.A.; Rai, P.; Duggal, N.K.; Weger-Lucarelli, J. Development and characterization of infectious clones of two strains of Usutu virus. Virology 2021, 554, 28–36. [Google Scholar] [CrossRef]
- Chuong, C.; Bates, T.A.; Akter, S.; Werre, S.R.; LeRoith, T.; Weger-Lucarelli, J. Nutritional status impacts dengue virus infection in mice. BMC Biol. 2020, 18, 106. [Google Scholar] [CrossRef]
- Zellweger, R.M.; Prestwood, T.R.; Shresta, S. Enhanced infection of liver sinusoidal endothelial cells in a mouse model of antibody-induced severe dengue disease. Cell Host Microbe 2010, 7, 128–139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wilken, L.; Stelz, S.; Prajeeth, C.K.; Rimmelzwaan, G.F. Transient Blockade of Type I Interferon Signalling Promotes Replication of Dengue Virus Strain D2Y98P in Adult Wild-Type Mice. Viruses 2023, 15, 814. https://doi.org/10.3390/v15040814
Wilken L, Stelz S, Prajeeth CK, Rimmelzwaan GF. Transient Blockade of Type I Interferon Signalling Promotes Replication of Dengue Virus Strain D2Y98P in Adult Wild-Type Mice. Viruses. 2023; 15(4):814. https://doi.org/10.3390/v15040814
Chicago/Turabian StyleWilken, Lucas, Sonja Stelz, Chittappen Kandiyil Prajeeth, and Guus F. Rimmelzwaan. 2023. "Transient Blockade of Type I Interferon Signalling Promotes Replication of Dengue Virus Strain D2Y98P in Adult Wild-Type Mice" Viruses 15, no. 4: 814. https://doi.org/10.3390/v15040814
APA StyleWilken, L., Stelz, S., Prajeeth, C. K., & Rimmelzwaan, G. F. (2023). Transient Blockade of Type I Interferon Signalling Promotes Replication of Dengue Virus Strain D2Y98P in Adult Wild-Type Mice. Viruses, 15(4), 814. https://doi.org/10.3390/v15040814