Production and Purification of Filovirus Glycoproteins in Insect and Mammalian Cell Lines

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Clarke, Elizabeth C ^a   Collar, Amanda L ^a   Ye, Chunyan ^a   Caì, Yíngyún ^b   Anaya, Eduardo ^a   Rinaldi, Derek ^a   Martinez, Britney ^c   Yarborough, Sarah ^c   Merle, Christine ^d   Theisen, Manfred ^d   Wada, Jiro ^b   Kuhn, Jens H ^b   Bradfute, Steven B ^a  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c UNIVERSITY OF NEW MEXICO   (United States)

^d Proteodynamics SARL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; VIRAL PROTEIN; VIRUS ANTIBODY;

ANIMAL; FILOVIRIDAE; GENE EXPRESSION REGULATION; GENE VECTOR; GENETICS; HEK293 CELL LINE; HUMAN; IMMUNOLOGY; METABOLISM; PATHOGENICITY; RNA EDITING; SF9 CELL LINE; SPODOPTERA; VIRION; VIRULENCE;

ANIMALS; ANTIBODIES, VIRAL; FILOVIRIDAE; GENE EXPRESSION REGULATION, VIRAL; GENETIC VECTORS; GLYCOPROTEINS; HEK293 CELLS; HUMANS; RNA EDITING; SF9 CELLS; SPODOPTERA; VIRAL PROTEINS; VIRION; VIRULENCE;

EID: 85033381839     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-15416-3     Document Type: Article

References (43)

1. Bukreyev, A. A. et al. Discussions and decisions of the 2012-2014 International Committee on Taxonomy of Viruses (ICTV) Filoviridae Study Group, January 2012-June 2013. Archives of virology 159, 821-830, https://doi.org/10.1007/s00705-013-1846-9 (2014).
2. Kuhn, J. H. In Harrison's Principles of Internal Medicine (eds Dennis L. Kasper et al.) Ch. 234, 1323-1329 (McGraw-Hill Education, 2015).
3. Negredo, A. et al. Discovery of an ebolavirus-like filovirus in europe. PLoS pathogens 7, e1002304, https://doi.org/10.1371/journal.ppat.1002304 (2011).
4. Cote, M. et al. Small molecule inhibitors reveal Niemann-Pick C1 is essential for Ebola virus infection. Nature 477, 344-348, https://doi.org/10.1038/nature10380 (2011).
5. Carette, J. E. et al. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 477, 340-343, https://doi.org/10.1038/nature10348 (2011).
6. Corti, D. et al. Protective monotherapy against lethal Ebola virus infection by a potently neutralizing antibody. Science 351, 1339-1342, https://doi.org/10.1126/science.aad5224 (2016).
7. Howell, K. A. et al. Antibody treatment of Ebola and Sudan virus infection via a uniquely exposed epitope within the glycoprotein receptor-binding site. Cell Rep 15, 1514-1526, https://doi.org/10.1016/j.celrep.2016.04.026 (2016).
8. Lee, J. E. et al. Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature 454, 177-182, https://doi.org/10.1038/nature07082 (2008).
9. Maruyama, J. et al. Characterization of the envelope glycoprotein of a novel filovirus, lloviu virus. Journal of virology 88, 99-109, https://doi.org/10.1128/JVI.02265-13 (2014).
10. Mehedi, M. et al. A new Ebola virus nonstructural glycoprotein expressed through RNA editing. Journal of virology 85, 5406-5414, https://doi.org/10.1128/JVI.02190-10 (2011).
11. Sanchez, A., Trappier, S. G., Mahy, B. W. J., Peters, C. J. & Nichol, S. T. The virion glycoproteins of Ebola viruses are encoded in two reading frames and are expressed through transcriptional editing. Proc Natl Acad Sci USA 93, 3602-3607 (1996).
12. Volchkov, V. E. et al. GP mRNA ofEbola virus is edited by the Ebola virus polymerase and by T7 and vaccinia virus polymerases. Virology 214, 421-430 (1995).
13. Volchkov, V. E., Feldmann, H., Volchkova, V. A. & Klenk, H.-D. Processing of the Ebola virus glycoprotein by the proprotein convertase furin. Proc Natl Acad Sci USA 95, 5762-5767 (1998).
14. Volchkov, V. E. et al. Proteolytic processing of Marburg virus glycoprotein. Virology 268, 1-6, https://doi.org/10.1006/viro.1999.0110 (2000).
15. Burk, R. et al. Neglected filoviruses. FEMS microbiology reviews 40, 494-519, https://doi.org/10.1093/femsre/fuw010 (2016).
16. Anthony, S. M. & Bradfute, S. B. Filoviruses: One of These Things is (not) Like the Other. Viruses 7, 5172-5190, https://doi.org/10.3390/v7102867 (2015).
17. Vu, H. et al. Quantitative serology assays for determination of antibody responses to Ebola virus glycoprotein and matrix protein in nonhuman primates and humans. Antiviral Res 126, 55-61, https://doi.org/10.1016/j.antiviral.2015.11.012 (2016).
18. Wang, H. et al. Ebola viral glycoprotein bound to its endosomal receptor Niemann-Pick C1. Cell 164, 258-268, https://doi.org/10.1016/j.cell.2015.12.044 (2016).
19. Hashiguchi, T. et al. Structural basis for Marburg virus neutralization by a cross-reactive human antibody. Cell 160, 904-912 (2015).
20. Stanley, D. A. et al. Chimpanzee adenovirus vaccine generates acute and durable protective immunity against ebolavirus challenge. Nature medicine 20, 1126-1129, https://doi.org/10.1038/nm.3702 (2014).
21. Falzarano, D. et al. Single immunization with a monovalent vesicular stomatitis virus-based vaccine protects nonhuman primates against heterologous challenge with Bundibugyo ebolavirus. The Journal of infectious diseases 204(suppl. 3), S1082-1089, https://doi.org/10.1093/infdis/jir350 (2011).
22. Daddario-DiCaprio, K. M. et al. Cross-protection against Marburg virus strains by using a live, attenuated recombinant vaccine. Journal of virology 80, 9659-9666, https://doi.org/10.1128/JVI.00959-06 (2006).
23. Warfield, K. L. et al. Filovirus-like particles produced in insect cells: immunogenicity and protection in rodents. The Journal of infectious diseases 196(Suppl 2), S421-429, https://doi.org/10.1086/520612 (2007).
24. Hahn, T. e. a. Rapid Manufacture and Release of a GMP Batch of Zaire Ebolavirus Glycoprotein Vaccine Made Using Recombinant Baculovirus-Sf9 Insect Cell Culture Technology. BioProcess Journal 14, 6-14, https://doi.org/10.12665/J141.Hahn (2015).
25. Bengtsson, K. L. et al. Matrix-M adjuvant enhances antibody, cellular and protective immune responses of a Zaire Ebola/Makona virus glycoprotein (GP) nanoparticle vaccine in mice. Vaccine 34, 1927-1935, https://doi.org/10.1016/j.vaccine.2016.02.033 (2016).
26. Melen, K. et al. Production, purification and immunogenicity of recombinant Ebola virus proteins- A comparison of Freund's adjuvant and adjuvant system 03. Journal of virological methods 242, 35-45 (2017).
27. Collar, A. L. et al. Comparison of N- and O-linked glycosylation patterns of ebolavirus glycoproteins. Virology 502, 39-47, https://doi.org/10.1016/j.virol.2016.12.010 (2016).
28. Wilde, M., Klausberger, M., Palmberger, D., Ernst, W. & Grabherr, R. Tnao38, high five and Sf9 - evaluation of host-virus interactions in three different insect cell lines: baculovirus production and recombinant protein expression. Biotechnol Lett 36, 743-749, https://doi.org/10.1007/s10529-013-1429-6 (2014).
29. Hevey, M., Negley, D., Geisbert, J., Jahrling, P. & Schmaljohn, A. Antigenicity and vaccine potential of Marburg virus glycoprotein expressed by baculovirus recombinants. Virology 239, 206-216, doi:S0042-6822(97)98883-8 [pii]10.1006/viro.1997.8883 (1997).
30. Shi, X. & Jarvis, D. L. Protein N-glycosylation in the baculovirus-insect cell system. Curr Drug Targets 8, 1116-1125 (2007).
31. Lennemann, N. J., Walkner, M., Berkebile, A. R., Patel, N. & Maury, W. The role of conserved n-linked glycans on ebola virus glycoprotein 2. The Journal of infectious diseases 212, S204-S209 (2015).
32. Gallaher, W. R. & Garry, R. F. Modeling of the Ebola virus delta peptide reveals a potential lytic sequence motif. Viruses 7, 285-305, https://doi.org/10.3390/v7010285 (2015).
33. Volchkova, V. A., Dolnik, O., Martinez, M. J., Reynard, O. & Volchkov, V. E. RNA editing of the GP gene of Ebola virus is an important pathogenicity factor. The Journal of infectious diseases 212(suppl. 2), S226-233, https://doi.org/10.1093/infdis/jiv309 (2015).
34. Volchkov, V. E. et al. Recovery of infectious Ebola virus from complementary DNA: RNA editing of the GP gene and viral cytotoxicity. Science 291, 1965-1969, https://doi.org/10.1126/science.1057269 (2001).
35. Hacke, M. et al. Inhibition of Ebola virus glycoprotein-mediated cytotoxicity by targeting its transmembrane domain and cholesterol. Nat Commun 6, 7688, https://doi.org/10.1038/ncomms8688 (2015).
36. Kost, T. A., Condreay, J. P. & Jarvis, D. L. Baculovirus as versatile vectors for protein expression in insect and mammalian cells. Nat Biotechnol 23, 567-575, https://doi.org/10.1038/nbt1095 (2005).
37. Towner, J. S. et al. Marburgvirus genomics and association with a large hemorrhagic fever outbreak in Angola. Journal of virology 80, 6497-6516, https://doi.org/10.1128/JVI.00069-06 (2006).
38. Marchal, I., Jarvis, D. L., Cacan, R. & Verbert, A. Glycoproteins from insect cells: sialylated or not? Biological chemistry 382, 151-159 (2001).
39. Lehmann, F., Tiralongo, E. & Tiralongo, J. Sialic acid-specific lectins: occurrence, specificity and function. Cellular and molecular life sciences 63, 1331-1354 (2006).
40. Gaunitz, S. et al. Mucin-type proteins produced in the Trichoplusia ni and Spodoptera frugiperda insect cell lines carry novel O-glycans with phosphocholine and sulfate substitutions. Glycobiology 23, 778-796 (2013).
41. Mehedi, M. et al. Ebola virus RNA editing depends on the primary editing site sequence and an upstream secondary structure. PLoS Pathog 9, e1003677, https://doi.org/10.1371/journal.ppat.1003677 (2013).
42. Neumann, G. et al. Proteolytic processing of the Ebola virus glycoprotein is not critical for Ebola virus replication in nonhuman primates. Journal of virology 81, 2995-2998, https://doi.org/10.1128/JVI.02486-06 (2007).
43. Morelle, W. & Michalski, J. C. Analysis of protein glycosylation by mass spectrometry. Nature protocols 2, 1585-1602, https://doi.org/10.1038/nprot.2007.227 (2007).