The liver X receptor agonist LXR 623 restricts flavivirus replication

References

• Bäck AT, Lundkvist A. Dengue viruses – an overview. Infect Ecol Epidemiol. 2013;3:1–21. DOI:https://doi.org/10.3402/iee.v3i0.19839.
   Google Scholar
• Bhatt S. The global distribution and burden of dengue. Nature. 2013;496:504–507. DOI:https://doi.org/10.1038/nature12060.
   PubMed Web of Science ®Google Scholar
• Guarner J, Hale GL. Four human diseases with significant public health impact caused by mosquito-borne flaviviruses: West Nile, Zika, dengue and yellow fever. Semin Diagn Pathol. 2019;36:170–176. DOI:https://doi.org/10.1053/j.semdp.2019.04.009.
   PubMed Web of Science ®Google Scholar
• Mlakar J. Zika virus associated with microcephaly. N Engl J Med. 2016;374:951–958. DOI:https://doi.org/10.1056/NEJMoa1600651.
   PubMed Web of Science ®Google Scholar
• Nascimento OJM, da Silva IRF. Guillain-Barré syndrome and Zika virus outbreaks. Curr Opin Neurol. 2017;30:500–507. DOI:https://doi.org/10.1097/wco.0000000000000471.
   Web of Science ®Google Scholar
• Gritsun TS, Lashkevich VA, Gould EA. Tick-borne encephalitis. Antiviral Res. 2003;57:129–146.
   PubMed Web of Science ®Google Scholar
• Hermance ME, Thangamani S. Powassan virus: an emerging arbovirus of public health concern in North America. Vector Borne Zoon Dis. 2017. DOI:https://doi.org/10.1089/vbz.2017.2110
   Google Scholar
• Apte-Sengupta S, Sirohi D, Kuhn RJ. Coupling of replication and assembly in flaviviruses. Curr Opin Virol. 2014;9:134–142. DOI:https://doi.org/10.1016/j.coviro.2014.09.020.
   PubMed Web of Science ®Google Scholar
• Smit JM, Moesker B, Rodenhuis-Zybert I, et al. Flavivirus cell entry and membrane fusion. Viruses. 2011;3:160–171. DOI:https://doi.org/10.3390/v3020160.
   PubMed Web of Science ®Google Scholar
• Aktepe TE, Mackenzie JM. Shaping the flavivirus replication complex: It is curvaceous!. Cell Microbiol. 2018;20:e12884. DOI:https://doi.org/10.1111/cmi.12884.
   Web of Science ®Google Scholar
• Offerdahl DK, Dorward DW, Hansen BT, et al. A three-dimensional comparison of tick-borne flavivirus infection in mammalian and tick cell lines. PLoS One. 2012;7:e47912. DOI:https://doi.org/10.1371/journal.pone.0047912.
   PubMed Web of Science ®Google Scholar
• Mackenzie JM, Jones MK, Young PR. Improved membrane preservation of flavivirus-infected cells with cryosectioning. J Virol Methods. 1996;56:67–75. DOI:https://doi.org/10.1016/0166-0934(95)01916-2.
   Web of Science ®Google Scholar
• Offerdahl DK, Dorward DW, Hansen BT, et al. Cytoarchitecture of Zika virus infection in human neuroblastoma and Aedes albopictus cell lines. Virology. 2017;501:54–62. DOI:https://doi.org/10.1016/j.virol.2016.11.002.
   PubMed Web of Science ®Google Scholar
• Neufeldt CJ, Cortese M, Acosta EG, et al. Rewiring cellular networks by members of the Flaviviridae family. Nat Rev Microbiol. 2018;16:125–142. DOI:https://doi.org/10.1038/nrmicro.2017.170.
   PubMed Web of Science ®Google Scholar
• Leier HC, Messer WB, Tafesse FG. Lipids and pathogenic flaviviruses: an intimate union. PLoS Pathog. 2018;14:e1006952–e1006952. DOI:https://doi.org/10.1371/journal.ppat.1006952.
   Web of Science ®Google Scholar
• Villareal VA, Rodgers MA, Costello DA, et al. Targeting host lipid synthesis and metabolism to inhibit dengue and hepatitis C viruses. Antiviral Res. 2015;124:110–121. DOI:https://doi.org/10.1016/j.antiviral.2015.10.013.
   PubMed Web of Science ®Google Scholar
• Zhang J. Flaviviruses exploit the lipid droplet protein AUP1 to trigger lipophagy and drive virus production. Cell Host Microbe. 2018;23:819–831. DOI:https://doi.org/10.1016/j.chom.2018.05.005.
   PubMed Web of Science ®Google Scholar
• Mlera L. Peromyscus leucopus mouse brain transcriptome response to Powassan virus infection. J Neurovirol. 2017. DOI:https://doi.org/10.1007/s13365-017-0596-y
   Google Scholar
• Zelcer N, Tontonoz P. Liver X receptors as integrators of metabolic and inflammatory signaling. J Clin Invest. 2006;116:607–614. DOI:https://doi.org/10.1172/JCI27883.
   PubMed Web of Science ®Google Scholar
• Peet DJ. Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXRα. Cell. 1998;93:693–704. DOI:https://doi.org/10.1016/S0092-8674(00)81432-4.
   PubMed Web of Science ®Google Scholar
• Mlera L, Meade-White K, Saturday G, et al. Modeling Powassan virus infection in Peromyscus leucopus, a natural host. PLoS Negl Trop Dis. 2017;11:e0005346. DOI:https://doi.org/10.1371/journal.pntd.0005346.
   Web of Science ®Google Scholar
• Yu L, Takeda K, Gao Y. Characterization of virus-specific vesicles assembled by West Nile virus non-structural proteins. Virology. 2017;506:130–140. DOI:https://doi.org/10.1016/j.virol.2017.03.016.
   Web of Science ®Google Scholar
• He Z. NLRP3 inflammasome activation mediates Zika virus – associated inflammation. J Infect Dis. 2018;217:1942–1951. DOI:https://doi.org/10.1093/infdis/jiy129.
   PubMed Web of Science ®Google Scholar
• Wang W. Zika virus infection induces host inflammatory responses by facilitating NLRP3 inflammasome assembly and interleukin-1β secretion. Nat Commun. 2018;9:106. DOI:https://doi.org/10.1038/s41467-017-02645-3.
   Web of Science ®Google Scholar
• Im S-S, Osborne TF. Liver x receptors in atherosclerosis and inflammation. Circ Res. 2011;108:996–1001. DOI:https://doi.org/10.1161/CIRCRESAHA.110.226878.
   PubMed Web of Science ®Google Scholar
• Hanners NW. Western Zika virus in human fetal neural progenitors persists long term with partial cytopathic and limited immunogenic effects. Cell Rep. 2016;15:2315–2322. DOI:https://doi.org/10.1016/j.celrep.2016.05.075.
   PubMed Web of Science ®Google Scholar
• Chen J. Zika virus infects renal proximal tubular epithelial cells with prolonged persistency and cytopathic effects. Emerg Microb Infect. 2017;6:e77. DOI:https://doi.org/10.1038/emi.2017.67, https://www.nature.com/articles/emi201767#supplementary-information
   Web of Science ®Google Scholar
• Souza BSF. Zika virus infection induces mitosis abnormalities and apoptotic cell death of human neural progenitor cells. Sci Rep. 2016;6:39775. DOI:https://doi.org/10.1038/srep39775.
   Web of Science ®Google Scholar
• Fukuchi J, Kokontis JM, Hiipakka RA, et al. Antiproliferative effect of liver X receptor agonists on LNCaP human prostate cancer cells. Cancer Res. 2004;64:7686–7689. DOI:https://doi.org/10.1158/0008-5472.Can-04-2332.
   PubMed Web of Science ®Google Scholar
• Martín-Acebes MA, Vázquez-Calvo Á, Saiz J-C. Lipids and flaviviruses, present and future perspectives for the control of dengue, Zika, and West Nile viruses. Prog Lipid Res. 2016;64:123–137. DOI:https://doi.org/10.1016/j.plipres.2016.09.005.
   PubMed Web of Science ®Google Scholar
• Zhang J, Lan Y, Sanyal S. Modulation of lipid droplet metabolism – a potential target for therapeutic intervention in Flaviviridae infections. Front Microbiol. 2017;8:2286–2286. DOI:https://doi.org/10.3389/fmicb.2017.02286.
   PubMed Web of Science ®Google Scholar
• Osuna-Ramos JF, Reyes-Ruiz JM, Del Ángel RM. The role of host cholesterol during flavivirus infection. Front Cell Infect Microbiol. 2018;8:388–388. DOI:https://doi.org/10.3389/fcimb.2018.00388.
   PubMed Web of Science ®Google Scholar
• Leier HC, Messer WB, Tafesse FG. Lipids and pathogenic flaviviruses: An intimate union. PLoS Pathog. 2018;14:e1006952. DOI:https://doi.org/10.1371/journal.ppat.1006952.
   Web of Science ®Google Scholar
• Mackenzie JM, Khromykh AA, Parton RG. Cholesterol manipulation by West Nile virus perturbs the cellular immune response. Cell Host Microbe. 2007;2:229–239. DOI:https://doi.org/10.1016/j.chom.2007.09.003.
   PubMed Web of Science ®Google Scholar
• Rothwell C. Cholesterol biosynthesis modulation regulates dengue viral replication. Virology. 2009;389:8–19. DOI:https://doi.org/10.1016/j.virol.2009.03.025.
   PubMed Web of Science ®Google Scholar
• Merino-Ramos T. Modification of the host cell lipid metabolism induced by hypolipidemic drugs targeting the acetyl coenzyme A carboxylase impairs West Nile virus replication. Antimicrob Agents Chemother. 2016;60:307–315. DOI:https://doi.org/10.1128/aac.01578-15.
   Web of Science ®Google Scholar
• Mazar J. Zika virus as an oncolytic treatment of human neuroblastoma cells requires CD24. PLoS One. 2018;13:e0200358. DOI:https://doi.org/10.1371/journal.pone.0200358.
   Web of Science ®Google Scholar
• Sánchez-San Martín C. Differentiation enhances Zika virus infection of neuronal brain cells. Sci Rep. 2018;8:14543–14543. DOI:https://doi.org/10.1038/s41598-018-32400-7.
   Web of Science ®Google Scholar
• Biedler JL, Roffler-Tarlov S, Schachner M, et al. Multiple neurotransmitter synthesis by human neuroblastoma cell lines and clones. Cancer Res. 1978;38:3751–3757.
   PubMed Web of Science ®Google Scholar
• Sidell N, Sarafian T, Kelly M, et al. Retinoic acid-induced differentiation of human neuroblastoma: a cell variant system showing two distinct responses. Exp. Cell Biol.. 1986;54:287–300. DOI:https://doi.org/10.1159/000163368.
   PubMedGoogle Scholar
• Lazear HM. A mouse model of Zika virus pathogenesis. Cell Host Microbe. 2016;19:720–730. DOI:https://doi.org/10.1016/j.chom.2016.03.010.
   PubMed Web of Science ®Google Scholar
• Shresta S. 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. DOI:https://doi.org/10.1128/jvi.78.6.2701-2710.2004.
   PubMed Web of Science ®Google Scholar
• Best SM. Inhibition of interferon-stimulated JAK-STAT signaling by a tick-borne flavivirus and identification of NS5 as an interferon antagonist. J Virol. 2005;79:12828–12839. DOI:https://doi.org/10.1128/JVI.79.20.12828-12839.2005.
   PubMed Web of Science ®Google Scholar
• Ngono AE, Shresta S. Immune response to dengue and zika. Annu Rev Immunol. 2018;36:279–308. DOI:https://doi.org/10.1146/annurev-immunol-042617-053142.
   PubMed Web of Science ®Google Scholar
• González N, Castrillo A. Liver X receptors as regulators of macrophage inflammatory and metabolic pathways. Biochim Biophys Acta. 2011;1812:982–994. DOI:https://doi.org/https://doi.org/10.1016/j.bbadis.2010.12.015.
   Web of Science ®Google Scholar
• Pourcet B. The nuclear receptor LXR modulates interleukin-18 levels in macrophages through multiple mechanisms. Sci Rep. 2016;6:25481. DOI:https://doi.org/10.1038/srep25481, https://www.nature.com/articles/srep25481#supplementary-information
   Web of Science ®Google Scholar
• Schulman IG. Liver X receptors link lipid metabolism and inflammation. FEBS Lett. 2017;591:2978–2991. DOI:https://doi.org/10.1002/1873-3468.12702.
   PubMed Web of Science ®Google Scholar
• Birrell MA. Novel role for the Liver X nuclear receptor in the suppression of lung inflammatory responses. J Biol Chem. 2007;282:31882–31890. DOI:https://doi.org/10.1074/jbc.M703278200.
   PubMed Web of Science ®Google Scholar
• Yu S. Dissociated sterol-based liver X receptor agonists as therapeutics for chronic inflammatory diseases. FASEB J. 2016;30:2570–2579. DOI:https://doi.org/10.1096/fj.201600244R.
   Web of Science ®Google Scholar
• Pascual-García M. Reciprocal negative cross-talk between liver X receptors (LXRs) and STAT1: effects on IFN-γ–induced inflammatory responses and LXR-dependent gene expression. J Immunol. 2013;190:6520–6532. DOI:https://doi.org/10.4049/jimmunol.1201393.
   Web of Science ®Google Scholar
• Nakajima S. Fungus-derived neoechinulin B as a novel antagonist of liver X receptor, identified by chemical genetics using a hepatitis C virus cell culture system. J Virol. 2016;90:9058–9074. DOI:https://doi.org/10.1128/JVI.00856-16.
   Web of Science ®Google Scholar
• Sirtori CR. The pharmacology of statins. Pharmacol Res. 2014;88:3–11. DOI:https://doi.org/10.1016/j.phrs.2014.03.002.
   PubMed Web of Science ®Google Scholar
• Martínez-Gutierrez M, Castellanos JE, Gallego-Gómez JC. Statins reduce dengue virus production via decreased virion assembly. Intervirology. 2011;54:202–216. DOI:https://doi.org/10.1159/000321892.
   PubMed Web of Science ®Google Scholar
• Martinez-Gutierrez M, Correa-Londoño LA, Castellanos JE, et al. Lovastatin delays infection and increases survival rates in AG129 mice infected with dengue virus serotype 2. PLoS One. 2014;9:e87412. DOI:https://doi.org/10.1371/journal.pone.0087412.
   PubMed Web of Science ®Google Scholar
• Lange PT. Type I interferon counteracts antiviral effects of statins in the context of gammaherpesvirus infection. J Virol. 2016;90:3342–3354. DOI:https://doi.org/10.1128/jvi.02277-15.
   Web of Science ®Google Scholar
• Giannarelli C. Synergistic effect of liver X receptor activation and simvastatin on plaque regression and stabilization: an magnetic resonance imaging study in a model of advanced atherosclerosis. Eur Heart J. 2012;33:264–273. DOI:https://doi.org/10.1093/eurheartj/ehr136.
   Web of Science ®Google Scholar
• Dang J. Zika virus depletes neural progenitors in human cerebral organoids through activation of the innate immune receptor TLR3. Cell Stem Cell. 2016;19:258–265. DOI:https://doi.org/10.1016/j.stem.2016.04.014.
   PubMed Web of Science ®Google Scholar
• Onorati M. Zika virus disrupts phospho-TBK1 localization and mitosis in human neuroepithelial stem cells and radial glia. Cell Rep. 2016;16:2576–2592. DOI:https://doi.org/10.1016/j.celrep.2016.08.038.
   PubMed Web of Science ®Google Scholar
• Bayless NL, Greenberg RS, Swigut T, et al. Zika virus infection induces cranial neural crest cells to produce cytokines at levels detrimental for neurogenesis. Cell Host Microbe. 2016;20:423–428. DOI:https://doi.org/10.1016/j.chom.2016.09.006.
   PubMed Web of Science ®Google Scholar
• Hwang J, Wang Y, Fikrig E. Inhibition of Chikungunya virus replication in Primary human fibroblasts by liver X receptor agonist. Antimicrob Agents Chemother. 2019;63:e01220–e01219. DOI:https://doi.org/10.1128/AAC.01220-19.
   Web of Science ®Google Scholar