A quantitative luciferase-based cell–cell fusion assay to measure four-serotype dengue virus E protein-triggered membrane fusion

References

• Lindenbach BD, Rice CM. Molecular biology of flaviviruses. Adv Virus Res. 2003;59:23–61.
   PubMed Web of Science ®Google Scholar
• Modis Y, Ogata S, Clements D, Harrison SC. Structure of the dengue virus envelope protein after membrane fusion. Nature. 2004;427(6972):313–19. doi:10.1038/nature02165.
   PubMed Web of Science ®Google Scholar
• Rey FA, Heinz FX, Mandl C, Kunz C, Harrison SC. The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature. 1995;375(6529):291–98. doi:10.1038/375291a0.
   PubMed Web of Science ®Google Scholar
• Harrison SC. Viral membrane fusion. Nat Struct Mol Biol. 2008 Jul;15(7):690–98. doi:10.1038/nsmb.1456.
   PubMed Web of Science ®Google Scholar
• White JM, Delos SE, Brecher M, Schornberg K. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit Rev Biochem Mol Biol. 2008;43:189–219. doi:10.1080/10409230802058320.
   PubMed Web of Science ®Google Scholar
• Seligman SJ. Constancy and diversity in the flavivirus fusion peptide. Virol J. 2008;5:27. doi:10.1186/1743-422X-5-27.
   PubMed Web of Science ®Google Scholar
• Zhou Z, Khaliq M, Suk JE, Patkar C, Li L, Kuhn RJ, Post CB. Antiviral compounds discovered by virtual screening of small-molecule libraries against dengue virus E protein. ACS Chem Biol. 2008;3:765–75. doi:10.1021/cb800176t.
   PubMed Web of Science ®Google Scholar
• Kampmann T, Yennamalli R, Campbell P, Stoermer MJ, Fairlie DP, Kobe B, Young PR. In silico screening of small molecule libraries using the dengue virus envelope E protein has identified compounds with antiviral activity against multiple flaviviruses. Antiviral Res. 2009;84:234–41. doi:10.1016/j.antiviral.2009.09.007.
   PubMed Web of Science ®Google Scholar
• Poh MK, Yip A, Zhang S, Priestle JP, Ma NL, Smit JM, Wilschut J, PY S, MR W, Schul W. A small molecule fusion inhibitor of dengue virus. Antiviral Res. 2009;84:260–66.
   PubMed Web of Science ®Google Scholar
• Schmidt AG, Yang PL, Harrison SC. Peptide inhibitors of dengue-virus entry target a late-stage fusion intermediate. PLoS Pathog. 2010;6:e1000851. doi:10.1371/journal.ppat.1000851.
   PubMed Web of Science ®Google Scholar
• Schmidt AG, Lee K, Yang PL, Harrison SC. Small-molecule inhibitors of dengue-virus entry. PLoS Pathog. 2012;8:e1002627. doi:10.1371/journal.ppat.1002627.
   PubMed Web of Science ®Google Scholar
• De Wispelaere M, Lian W, Potisopon S, Li PC, Jang J, Ficarro SB, Clark MJ, Zhu X, Kaplan JB, Pitts JD, et al. Inhibition of flaviviruses by targeting a conserved pocket on the viral envelope protein. Cell Chem Biol. 2018;25(8):1006–1016.e8. doi:10.1016/j.chembiol.2018.05.011.
   PubMed Web of Science ®Google Scholar
• Chao LH, Jang J, Johnson A, Nguyen A, Gray NS, Yang PL, Harrison SC. How small-molecule inhibitors of dengue-virus infection interfere with viral membrane fusion. Elife. 2018;7:ii:e36461. doi:10.7554/eLife.36461.
   Web of Science ®Google Scholar
• Lian W, Jang J, Potisopon S, Li PC, Rahmeh A, Wang J, Kwiatkowski NP, Gray NS, Yang PL. Discovery of immunologically inspired small molecules that target the viral envelope protein. ACS Infect Dis. 2018;4(9):1395–406. doi:10.1021/acsinfecdis.8b00127.
   PubMed Web of Science ®Google Scholar
• Li PC, Jang J, Hsia CY, Groomes PV, Lian W, de Wispelaere M, Pitts JD, Wang J, Kwiatkowski N, Gray NS, et al. Small molecules targeting the flavivirus E protein with broad-spectrum activity and antiviral efficacy in Vivo. ACS Infect Dis. 2019;5(3):460–72. doi:10.1021/acsinfecdis.8b00322.
   PubMed Web of Science ®Google Scholar
• Pitts J, Hsia CY, Lian W, Wang J, Pfeil MP, Kwiatkowski N, Li Z, Jang J, Gray NS, Yang PL. Identification of small molecule inhibitors targeting the Zika virus envelope protein. Antiviral Res. 2019;164:147–53. doi:10.1016/j.antiviral.2019.02.008.
   PubMed Web of Science ®Google Scholar
• Tsai WY, Chen HL, Tsai JJ, Dejnirattisai W, Jumnainsong A, Mongkolsapaya J, Screaton G, Crowe JE Jr, Wang WK. Potent neutralizing human monoclonal antibodies preferentially target mature dengue virus particles: implication for novel strategy for dengue vaccine. J Virol. 2018;92(23):e00556e18. doi:10.1128/JVI.00556-18.
   Web of Science ®Google Scholar
• Tsai WY, Lai CY, Wu YC, Lin HE, Edwards C, Jumnainsong A, Kliks S, Halstead S, Mongkolsapaya J, Screaton GR, et al. High-avidity and potently neutralizing cross-reactive human monoclonal antibodies derived from secondary dengue virus infection. J Virol. 2013;87(23):12562–75. doi:10.1128/JVI.00871-13.
   PubMed Web of Science ®Google Scholar
• Okuma K, Nakamura M, Nakano S, Niho Y, Matsuura Y. Host range of human T-cell leukemia virus type I analyzed by a cell fusion-dependent reporter gene activation assay. Virology. 1999;254(2):235–44. doi:10.1006/viro.1998.9530.
   PubMed Web of Science ®Google Scholar
• Saw WT, Matsuda Z, Eisenberg RJ, Cohen GH, Atanasiu D. Using a split luciferase assay (SLA) to measure the kinetics of cell-cell fusion mediated by herpes simplex virus glycoproteins. Methods. 2015;90:68–75. doi:10.1016/j.ymeth.2015.05.021.
   PubMed Web of Science ®Google Scholar
• Kobayashi M, Bennett MC, Bercot T, Singh IR. Functional analysis of hepatitis C virus envelope proteins, using a cell-cell fusion assay. J Virol. 2006;80(4):1817–25. doi:10.1128/JVI.80.4.1817-1825.2006.
   PubMed Web of Science ®Google Scholar
• Denolly S, Cosset FL, Freitas N. Membrane fusion assays for studying entry hepatitis C virus into cells. Methods Mol Biol. 2019;1911:219–34.
   PubMedGoogle Scholar
• Aoki Y, Aizaki H, Shimoike T, Tani H, Ishii K, Saito I, Matsuura Y, Miyamura T. A human liver cell line exhibits efficient translation of HCV RNAs produced by a recombinant adenovirus expressing T7 RNA polymerase. Virology. 1998;250(1):140–50. doi:10.1006/viro.1998.9361.
   PubMed Web of Science ®Google Scholar
• Su Y, Yang H, Zhang B, Qi X, Tien P. A dual reporter gene based system to quantitate the cell fusion of avian influenza virus H5N1. Biotechnol Lett. 2008;30(1):73–79. doi:10.1007/s10529-007-9521-4.
   PubMed Web of Science ®Google Scholar
• Takikawa S, Ishii K, Aizaki H, Suzuki T, Asakura H, Matsuura Y, Miyamura T. Cell fusion activity of hepatitis C virus envelope proteins. J Virol. 2000;74(11):5066–74. doi:10.1128/JVI.74.11.5066-5074.2000.
   PubMed Web of Science ®Google Scholar
• SC H, IJ L, CC K, GJ C, Wang WK. A strong endoplasmic reticulum retention signal in the stem-anchor region of envelope glycoprotein of dengue virus type 2 affects the production of virus-like particles. Virology. 2008;374(2):338–50. doi:10.1016/j.virol.2007.12.041.
   PubMed Web of Science ®Google Scholar
• Purdy DE, Chang GJ. Secretion of noninfectious dengue virus-like particles and identification of amino acids in the stem region involved in intracellular retention of envelope protein. Virology. 2005;333(2):239–50. doi:10.1016/j.virol.2004.12.036.
   PubMed Web of Science ®Google Scholar
• HP H, SC H, CC K, Wang WK. Characterization of retrovirus-based reporter viruses pseudotyped with the precursor membrane and envelope glycoproteins of four serotypes of dengue viruses. Virology. 2007;368(2):376–87. doi:10.1016/j.virol.2007.06.026.
   PubMed Web of Science ®Google Scholar
• Kostyuchenko VA, Lim EX, Zhang S, Fibriansah G, Ng TS, Ooi JS, Shi J, Lok SM. Structure of the thermally stable Zika virus. Nature. 2016;533(7603):425–28. doi:10.1038/nature17994.
   PubMed Web of Science ®Google Scholar
• Sirohi D, Chen Z, Sun L, Klose T, Pierson TC, Rossmann MG, Kuhn RJ. The 3.8 A resolution cryo-EM structure of Zika virus. Science. 2016;352(6284):467–70. doi:10.1126/science.aaf5316.
   PubMed Web of Science ®Google Scholar