Rabies virus glycoprotein expression in Drosophila S2 cells. I: Design of expression/selection vectors, subpopulations selection and influence of sodium butyrate and culture medium on protein expression

Journal of Biotechnology

Volumn 143, Issue 2, 2009, Pages 103-110

  Lemos, Marcos Alexandre Nobre ^a   Santos, Alexandra Souza dos ^a   Astray, Renato Mancini ^a   Pereira, Carlos Augusto ^a   Jorge, Soraia Attie Calil ^a  

^a INSTITUTO BUTANTAN   (Brazil)

Author keywords

Drosophila melanogaster S2 cell; Protein expression; Rabies viral glycoprotein (RVGP); Secretion signal BiP

Indexed keywords

CDNA ENCODING; CELL POPULATIONS; CELL SUBPOPULATIONS; CULTURE MEDIUM; DROSOPHILA MELANOGASTER S2 CELL; HYGROMYCIN; METALLOTHIONEINS; PROTEIN EXPRESSION; PROTEIN EXPRESSIONS; RABIES VIRAL GLYCOPROTEIN (RVGP); SECRETION SIGNAL BIP; SODIUM BUTYRATE;

CELL GROWTH; CELL MEMBRANES; CELL PROLIFERATION; FLOW CYTOMETRY; GENE ENCODING; GLYCOPROTEINS; GROWTH KINETICS; SODIUM; VECTORS;

CELL CULTURE;

BUTYRIC ACID; HYGROMYCIN; METALLOTHIONEIN; PLASMID VECTOR; VIRUS GLYCOPROTEIN;

ARTICLE; CELL GROWTH; CELL SUBPOPULATION; CONTROLLED STUDY; CULTURE MEDIUM; DROSOPHILA MELANOGASTER; EXPRESSION VECTOR; GENE EXPRESSION; MOLECULAR CLONING; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANALYSIS OF VARIANCE; ANIMALS; BUTYRIC ACIDS; CELL LINE; CELL PROLIFERATION; CLONING, MOLECULAR; CULTURE MEDIA; DROSOPHILA MELANOGASTER; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GLYCOPROTEINS; KINETICS; MICROSCOPY, CONFOCAL; PLASMIDS; RABIES VIRUS; VIRAL PROTEINS;

DROSOPHILA MELANOGASTER; RABIES VIRUS;

EID: 68349125399     PISSN: 01681656     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2009.07.003     Document Type: Article

References (53)

1. Affleck J.G., and Walker V.K. A role for Drosophila in understanding drug-induced cytotoxicity and teratogenesis. Cytotechnology 57 (2008) 1-9
2. Angelichio M.L., Beck J.A., Johansen H., and Ivey-Hoyle M. Comparison of several promoters and polyadenylation signals for use in heterologous gene expression in cultured Drosophila cells. Nucleic Acids Res. 19 (1991) 5037-5043
3. Astray R.M., Augusto E., Yokomizo A.Y., and Pereira C.A. Analytical approach for the extraction of recombinant membrane viral glycoprotein from stably transfected Drosophila melanogaster cells. Biotechnol. J. 3 (2008) 98-103
4. Bahloul C., Taieb D., Diouani M.F., Ahmed S.B., Chtourou Y., B'Chir B.I., Kharmachi H., and Dellagi K. Field trials of a very potent rabies DNA vaccine which induced long lasting virus neutralizing antibodies and protection in dogs in experimental conditions. Vaccine 24 (2006) 1063-1072
5. Batista F.R., Moraes A.M., Buntemeyer H., and Noll T. Influence of culture conditions on recombinant Drosophila melanogaster S2 cells producing rabies virus glycoprotein cultivated in serum-free medium. Biologicals 37 (2009) 108-118
6. Batista F.R., Pereira C.A., Mendonca R.Z., and Moraes A.M. Formulation of a protein-free medium based on IPL-41 for the sustained growth of Drosophila melanogaster S2 cells. Cytotechnology 57 (2008) 11-22
7. Bovo R., Galesi A.L., Jorge S.A.C., Piccoli R.A., Moraes A.M., Pereira C.A., and Augusto E.F. Kinetic response of a Drosophila melanogaster cell line to different medium formulations and culture conditions. Cytotechnology 57 (2008) 23-35
8. Brillet K., Perret B.G., Klein V., Pattus F., and Wagner R. Using EGFP fusions to monitor the functional expression of GPCRs in the Drosophila Schneider 2 cells. Cytotechnology 57 (2008) 101-109
9. Chen T., Sun H., Lu J., Zhao Y., Tao D., Li X., and Huang B. Histone acetylation is involved in hsp70 gene transcription regulation in Drosophila melanogaster. Arch. Biochem. Biophys. 408 (2002) 171-176
10. Chomczynski P., and Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162 (1987) 156-159
11. Culp J.S., Johansen H., Hellmig B., Beck J., Matthews T.J., Delers A., and Rosenberg M. Regulated expression allows high level production and secretion of HIV-1 gp120 envelope glycoprotein in Drosophila Schneider cells. Biotechnology (NY) 9 (1991) 173-177
12. Deml L., Wolf H., and Wagner R. High level expression of hepatitis B virus surface antigen in stably transfected Drosophila Schneider-2 cells. J. Virol. Methods 79 (1999) 191-203
13. Desmezieres E., Maillard A.P., Gaudin Y., Tordo N., and Perrin P. Differential stability and fusion activity of Lyssavirus glycoprotein trimers. Virus Res. 91 (2003) 181-187
14. Diogo M.M., Ribeiro S.C., Queiroz J.A., Monteiro G.A., Tordo N., Perrin P., and Prazeres D.M. Production, purification and analysis of an experimental DNA vaccine against rabies. J. Gene Med. 3 (2001) 577-584
15. Dorner A.J., Wasley L.C., and Kaufman R.J. Increased synthesis of secreted proteins induces expression of glucose-regulated proteins in butyrate-treated Chinese hamster ovary cells. J. Biol. Chem. 264 (1989) 20602-20607
16. Galesi A.L., Aguiar M.A., Astray R.M., Augusto E.F., and Moraes A.M. Growth of recombinant Drosophila melanogaster Schneider 2 cells producing rabies virus glycoprotein in bioreactor employing serum-free medium. Cytotechnology 57 (2008) 73-81
17. Gaudin Y. Folding of rabies virus glycoprotein: epitope acquisition and interaction with endoplasmic reticulum chaperones. J. Virol. 71 (1997) 3742-3750
18. Hill R.M., Brennan S.O., and Birch N.P. Expression, purification, and functional characterization of the serine protease inhibitor neuroserpin expressed in Drosophila S2 cells. Protein Exp. Purif. 22 (2001) 406-413
19. Iwaki T., and Castellino F.J. A single plasmid transfection that offers a significant advantage associated with puromycin selection in Drosophila Schneider S2 cells expressing heterologous proteins. Cytotechnology 57 (2008) 45-49
20. Jallet C., Jacob Y., Bahloul C., Drings A., Desmezieres E., Tordo N., and Perrin P. Chimeric lyssavirus glycoproteins with increased immunological potential. J. Virol. 73 (1999) 225-233
21. Jorge S.A.C., Santos A.S., Spina A., and Pereira C.A. Expression of the hepatitis B virus surface antigen in Drosophila S2 cells. Cytotechnology 57 (2008) 51-59
22. Kirkpatrick R.B., Ganguly S., Angelichio M., Griego S., Shatzman A., Silverman C., and Rosenberg M. Heavy chain dimers as well as complete antibodies are efficiently formed and secreted from Drosophila via a BiP-mediated pathway. J. Biol. Chem. 270 (1995) 19800-19805
23. Knobel D.L., Cleaveland S., Coleman P.G., Fevre E.M., Meltzer M.I., Miranda M.E., Shaw A., Zinsstag J., and Meslin F.X. Re-evaluating the burden of rabies in Africa and Asia. Bull. World Health Organ. 83 (2005) 360-368
24. Lee J.M., Park J.H., Park J.O., Chang K.H., and Chung I.S. Expression of recombinant erythroprotein in stably transformed Drosophila melanogaster S2 cells. In Vitro Cell. Dev. Biol. 3 (2000) 348-350
25. Li B., Tsing S., Kosaka A.H., Nguyen B., Osen E.G., Bach C., Chan H., and Barnett J. Expression of human dopamine beta-hydroxylase in Drosophila Schneider 2 cells. Biochem. J. 313 Pt. 1 (1996) 57-64
26. Li R.W., and Li C. Butyrate induces profound changes in gene expression related to multiple signal pathways in bovine kidney epithelial cells. BMC Genom. 7 (2006) 234
27. Lodmell D.L. Rabies DNA vaccines for protection and therapeutic treatment. Expert Opin. Invest. Drugs. 8 (1999) 115-122
28. Lodmell D.L., Esposito J.J., and Ewalt L.C. Live vaccinia-rabies virus recombinants, but not an inactivated rabies virus cell culture vaccine, protect B-lymphocyte-deficient A/WySnJ mice against rabies: considerations of recombinant defective poxviruses for rabies immunization of immunocompromised individuals. Vaccine 22 (2004) 3329-3333
29. Mendonça R.Z., Prado J.C.M., and Pereira C.A. Attachment, spreading and growth of VERO cells on microcarriers for the optimization of large scale cultures. Bioprocess Eng. 20 (1999) 565-571
30. Nilsen S.L., and Castellino F.J. Expression of human plasminogen in Drosophila Schneider S2 cells. Protein Exp. Purif. 16 (1999) 136-143
31. Park J.H., Hwang I.S., Kim K.I., Lee J.M., Park Y.M., Park C.H., and Chung I.S. Functional expression of recombinant human ribonuclease/angiogenin inhibitor in stably transformed Drosophila melanogaster S2 cells. Cytotechnology 57 (2008) 93-99
32. Pastoret P.P., Brochier B., Aguilar-Setin A., and Blancou J. Vaccination against rabies. In: Pastoret P.P., Blancou J., Vanner P., and Verschueren C. (Eds). Veterinary Vaccinology (1997), Elsevier, Amsterdan 616
33. Perrin P., Lafon M., and Sureau P. Enzyme linked immuno-sorbent assay (ELISA) for the determination of glycoprotein content of rabies vaccines. In: World Health Organization, Meslin F.X., Kaplan M.M., and Koprowski H. (Eds). Laboratory Techniques in Rabies (1996), World Health Organization, Geneva 383-388
34. Perrin P., Thibodeau L., and Sureau P. Rabies immunosome (subunit vaccine) structure and immunogenicity. Pre- and post-exposure protection studies. Vaccine 3 (1985) 325-332
35. Ping W., Ge J., Li S., Zhou H., Wang K., Feng Y., and Lou Z. Baculovirus-mediated gene expression in chicken primary cells. Avian Dis. 50 (2006) 59-63
36. Rai N., Kaushik P., and Rai A. Development of rabies DNA vaccine using a recombinant plasmid. Acta Virol. 49 (2005) 207-210
37. Rath A., Choudhury S., Batra D., Kapre S.V., Rupprecht C.E., and Gupta S.K. DNA vaccine for rabies: relevance of the trans-membrane domain of the glycoprotein in generating an antibody response. Virus Res. 113 (2005) 143-152
38. Santos M.G., Jorge S.A., Brillet K., and Pereira C.A. Improving heterologous protein expression in transfected Drosophila S2 cells as assessed by EGFP expression. Cytotechnology 54 (2007) 15-24
39. Schamel W.W., Kuppig S., Becker B., Gimborn K., Hauri H.P., and Reth M. A high-molecular-weight complex of membrane proteins BAP29/BAP31 is involved in the retention of membrane-bound IgD in the endoplasmic reticulum. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 9861-9866
40. Schneider I. Cell lines derived from late embryonic stages of Drosophila melanogaster. J. Embryol. Exp. Morphol. 27 (1972) 353-365
41. Schneider M.C., Belotto A., Ade M.P., Hendrickx S., Leanes L.F., Rodrigues M.J., Medina G., and Correa E. Current status of human rabies transmitted by dogs in Latin America. Cad Saude Publica 23 (2007) 2049-2063
42. Sissoeff L., Mousli M., England P., and Tuffereau C. Stable trimerization of recombinant rabies virus glycoprotein ectodomain is required for interaction with the p75NTR receptor. J. Gen. Virol. 86 (2005) 2543-2552
43. Song J., Liang C., and Chen X. Transduction of avian cells with recombinant baculovirus. J. Virol. Methods 135 (2006) 157-162
44. Soulebot J.P., Brun A., Chappuis G., Guillemin F., and Tixier G. Rabies virus pathogenicity and challenge. Influence of the method of preparation, the route of inoculation, and the species. Comparison of the characteristics of the modified, fixed and wild strains. Comp. Immunol. Microbiol. Infect. Dis. 5 (1982) 71-78
45. Sudarshan M.K., Madhusudana S.N., Mahendra B.J., Rao N.S., Ashwath Narayana D.H., Abdul Rahman S., Meslin F.X., Lobo D., Ravikumar K., and Gangaboraiah. Assessing the burden of human rabies in India: results of a national multi-center epidemiological survey. Int. J. Infect. Dis. 11 (2007) 29-35
46. Swiech K., Rossi N., Astray R.M., and Suazo C.A. Enhanced production of recombinant rabies virus glycoprotein (rRVGP) by Drosophila melanogaster S2 cells through control of culture conditions. Cytotechnology 57 (2008) 67-72
47. Swiech K., Rossi N., Silva B.G., Jorge S.A., Astray R.M., and Suazo C.A. Bioreactor culture of recombinant Drosophila melanogaster S2 cells: characterization of metabolic features related to cell growth and production of the rabies virus glycoprotein. Cytotechnology 57 (2008) 61-66
48. Wiktor T.J., Macfarlan R.I., Reagan K.J., Dietzschold B., Curtis P.J., Wunner W.H., Kieny M.P., Lathe R., Lecocq J.P., Mackett M., et al. Protection from rabies by a vaccinia virus recombinant containing the rabies virus glycoprotein gene. Proc. Natl. Acad. Sci. U.S.A. 81 (1984) 7194-7198
49. World Health Organization, 2007. Rabies vaccines. WHO position paper. Wkly Epidemiol. Rec. 82, 425-435.
50. Yokomizo A.Y., Antoniazzi M.M., Galdino P.L., Azambuja Jr. N., Jorge S.A., and Pereira C.A. Rabies virus production in high vero cell density cultures on macroporous microcarriers. Biotechnol. Bioeng. 85 (2004) 506-515
51. Yokomizo A.Y., Jorge S.A., Astray R.M., Fernandes I., Ribeiro O.G., Horton D.S., Tonso A., Tordo N., and Pereira C.A. Rabies virus glycoprotein expression in Drosophila S2 cells. I. Functional recombinant protein in stable co-transfected cell line. Biotechnol. J. 2 (2007) 102-109
52. Zhang Y.Z., Xiong C.L., Xiao D.L., Jiang R.J., Wang Z.X., Zhang L.Z., and Fu Z.F. Human rabies in China. Emerg. Infect. Dis. 11 (2005) 1983-1984
53. Zhao Y.M., Chen X., Sun H., Yuan Z.G., Ren G.L., Li X.X., Lu J., and Huang B.Q. Effects of histone deacetylase inhibitors on transcriptional regulation of the hsp70 gene in Drosophila. Cell Res. 16 (2006) 566-576