Influenza virus-like particles as an antigen-carrier platform for the ESAT-6 epitope of Mycobacterium tuberculosis

Journal of Virological Methods

Volumn 167, Issue 1, 2010, Pages 17-22

  Krammer, Florian ^a   Schinko, Theresa ^a   Messner, Paul ^a   Palmberger, Dieter ^a   Ferko, Boris ^b   Grabherr, Reingard ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b Avir Green Hills Biotechnology AG   (Austria)

Author keywords

Baculovirus expression system; Influenza A; Mycobacterium tuberculosis; Surface display; Virus like particles

Indexed keywords

AMINO ACID; EARLY SECRETORY ANTIGENIC TARGET 6; EPITOPE; HEMAGGLUTININ; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; BACULOVIRUS EXPRESSION SYSTEM; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; FEMALE; HEMAGGLUTINATION; HUMORAL IMMUNITY; IMMUNIZATION; INFLUENZA VIRUS A; INSECT CELL; MOLECULAR CLONING; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY; VIRUS LIKE AGENT; VIRUS STRAIN; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CELL LINE; DRUG CARRIERS; EPITOPES; FEMALE; GENETIC VECTORS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS; MICE; MICE, INBRED BALB C; SPODOPTERA; TUBERCULOSIS VACCINES; VACCINES, VIROSOME;

HEXAPODA; MUS; MYCOBACTERIUM TUBERCULOSIS; ORTHOMYXOVIRIDAE;

EID: 77953028098     PISSN: 01660934     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jviromet.2010.03.003     Document Type: Article

References (65)

1. Amexis G., Young N. Parvovirus B19 empty capsids as antigen carriers for presentation of antigenic determinants of dengue 2 virus. J. Infect. Dis. 2006, 194:790-794.
2. Arap M. Phage display technology-applications and innovations. Genet. Mol. Biol. 2005, 28:1-9.
3. Becker S., Schmoldt H., Adams T., Wilhelm S., Kolmar H. Ultra-high-throughput screening based on cell-surface display and fluorescence-activated cell sorting for the identification of novel biocatalysts. Curr. Opin. Biotechnol. 2004, 15:323-329.
4. Brandt L., Oettinger T., Holm A., Andersen A., Andersen P. Key epitopes on the ESAT-6 antigen recognized in mice during the recall of protective immunity to Mycobacterium tuberculosis. J. Immunol. 1996, 157:3527-3533.
5. Bright R., Carter D., Daniluk S., Toapanta F., Ahmad A., Gavrilov V., Massare M., Pushko P., Mytle N., Rowe T., Smith G., Ross T. Influenza virus-like particles elicit broader immune responses than whole virion inactivated influenza virus or recombinant hemagglutinin. Vaccine 2007, 25:3871-3878.
6. Cox M. Progress on baculovirus-derived influenza vaccines. Curr. Opin. Mol. Ther. 2008, 10:56-61.
7. D'Aoust M., Lavoie P., Couture M., Trépanier S., Guay J., Dargis M., Mongrand S., Landry N., Ward B., Vézina L. Influenza virus-like particles produced by transient expression in Nicotiana benthamiana induce a protective immune response against a lethal viral challenge in mice. Plant Biotechnol. J. 2008, 6:930-940.
8. Dale C., Liu X., De Rose R., Purcell D., Anderson J., Xu Y., Leggatt G., Frazer I., Kent S. Chimeric human papilloma virus-simian/human immunodeficiency virus virus-like-particle vaccines: immunogenicity and protective efficacy in macaques. Virology 2002, 301:176-187.
9. Deml L., Speth C., Dierich M., Wolf H., Wagner R. Recombinant HIV-1 Pr55gag virus-like particles: potent stimulators of innate and acquired immune responses. Mol. Immunol. 2005, 42:259-277.
10. Doan, L., Li, M., Chen, C., Yao, Q., 2005. Virus-like particles as HIV-1 vaccines. Rev. Med. Virol. 15, 75-88.
11. Dormond, E., Perrier, M., Kamen, A., 2009. From the first to the third generation adenoviral vector: what parameters are governing the production yield? Biotechnol. Adv. 27, 133-144.
12. Ernst W., Grabherr R., Wegner D., Borth N., Grassauer A., Katinger H. Baculovirus surface display: construction and screening of a eukaryotic epitope library. Nucleic Acids Res. 1998, 26:1718-1723.
13. Fine P. Variation in protection by BCG: implications of and for heterologous immunity. Lancet 1995, 346:1339-1345.
14. Fotouhi F., Soleimanjahi H., Roostaee M., Behzadian F. Enhancement of protective humoral immune responses against Herpes simplex virus-2 in DNA-immunized guinea-pigs using protein boosting. FEMS Immunol. Med. Microbiol. 2008, 54:18-26.
15. Galarza J., Latham T., Cupo A. Virus-like particle (VLP) vaccine conferred complete protection against a lethal influenza virus challenge. Viral Immunol. 2005, 18:244-251.
16. Gao H., Yue Y., Hu L., Xu W., Xiong S. A novel DNA vaccine containing multiple TB-specific epitopes casted in a natural structure (ECANS) confers protective immunity against pulmonary mycobacterial challenge. Vaccine 2009, 27:5313-5319.
17. Gómez-Puertas P., Albo C., Pérez-Pastrana E., Vivo A., Portela A. Influenza virus matrix protein is the major driving force in virus budding. J. Virol. 2000, 74:11538-11547.
18. Grabherr R., Ernst W., Doblhoff-Dier O., Sara M., Katinger H. Expression of foreign proteins on the surface of Autographa californica nuclear polyhedrosis virus. Biotechniques 1997, 22:730-735.
19. Hall L., Clare S., Pickard D., Clark S., Kelly D., El Ghany M., Hale C., Dietrich J., Andersen P., Marsh P., Dougan G. Characterisation of a live Salmonella vaccine stably expressing the Mycobacterium tuberculosis Ag85B-ESAT6 fusion protein. Vaccine 2009, 27:6894-6904.
20. Harris A., Cardone G., Winkler D., Heymann J., Brecher M., White J., Steven A. Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:19123-19127.
21. Hink W. Established insect cell line from the cabbage looper, Trichoplusia ni. Nature 1970, 226:466-467.
22. Hosse R., Rothe A., Power B. A new generation of protein display scaffolds for molecular recognition. Protein Sci. 2006, 15:14-27.
23. Jegerlehner A., Tissot A., Lechner F., Sebbel P., Erdmann I., Kündig T., Bächi T., Storni T., Jennings G., Pumpens P., Renner W., Bachmann M. A molecular assembly system that renders antigens of choice highly repetitive for induction of protective B cell responses. Vaccine 2002, 20:3104-3112.
24. Jungbauer A., Hahn R. Polymethacrylate monoliths for preparative and industrial separation of biomolecular assemblies. J. Chromatogr. A 2008, 1184:62-79.
25. Kang S., Song J., Quan F., Compans R. Influenza vaccines based on virus-like particles. Virus Res. 2009, 143:140-146.
26. King L., Hitchman R., Possee R. Recombinant baculovirus isolation. Methods Mol. Biol. 2007, 388:77-94.
27. Kirby D., Rosenkrands I., Agger E., Andersen P., Coombes A., Perrie Y. Liposomes act as stronger sub-unit vaccine adjuvants when compared to microspheres. J. Drug Target 2008, 16:543-554.
28. Krammer F., Nakowitsch S., Messner P., Palmberger D., Ferko B., Grabherr R. Swine-origin pandemic H1N1 influenza virus-like particles produced in insect cells induce hemagglutination inhibiting antibodies in BALB/c mice. Biotechnol. J. 2010, 5:17-23.
29. Laemmli U. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
30. Latham T., Galarza J. Formation of wild-type and chimeric influenza virus-like particles following simultaneous expression of only four structural proteins. J. Virol. 2001, 75:6154-6165.
31. Lee S., Choi J., Xu Z. Microbial cell-surface display. Trends Biotechnol. 2003, 21:45-52.
32. Li S., Polonis V., Isobe H., Zaghouani H., Guinea R., Moran T., Bona C., Palese P. Chimeric influenza virus induces neutralizing antibodies and cytotoxic T cells against human immunodeficiency virus type 1. J. Virol. 1993, 67:6659-6666.
33. Liang Y., Wu X., Zhang J., Li N., Yu Q., Yang Y., Bai X., Liu C., Shi Y., Liu Q., Zhang P., Li Z. The treatment of mice infected with multi-drug-resistant Mycobacterium tuberculosis using DNA vaccines or in combination with rifampin. Vaccine 2008, 26:4536-4540.
34. Ludwig C., Wagner R. Virus-like particles-universal molecular toolboxes. Curr. Opin. Biotechnol. 2007, 18:537-545.
35. Mahmood K., Bright R., Mytle N., Carter D., Crevar C., Achenbach J., Heaton P., Tumpey T., Ross T. H5N1 VLP vaccine induced protection in ferrets against lethal challenge with highly pathogenic H5N1 influenza viruses. Vaccine 2008, 26:5393-5399.
36. Mäkelä A., Oker-Blom C. The baculovirus display technology-an evolving instrument for molecular screening and drug delivery. Comb. Chem. High Throughput Screen 2008, 11:86-98.
37. Muster T., Guinea R., Trkola A., Purtscher M., Klima A., Steindl F., Palese P., Katinger H. Cross-neutralizing activity against divergent human immunodeficiency virus type 1 isolates induced by the gp41 sequence ELDKWAS. J. Virol. 1994, 68:4031-4034.
38. Nayak D., Balogun R., Yamada H., Zhou Z., Barman S. Influenza virus morphogenesis and budding. Virus Res. 2009.
39. Notka F., Stahl-Hennig C., Dittmer U., Wolf H., Wagner R. Construction and characterization of recombinant VLPs and Semliki-Forest virus live vectors for comparative evaluation in the SHIV monkey model. Biol. Chem. 1999, 380:341-352.
40. Palmer K., Jenson A., Kouokam J., Lasnik A., Ghim S. Recombinant vaccines for the prevention of human papillomavirus infection and cervical cancer. Exp. Mol. Pathol. 2009, 86:224-233.
41. Peacey M., Wilson S., Baird M., Ward V. Versatile RHDV virus-like particles: incorporation of antigens by genetic modification and chemical conjugation. Biotechnol. Bioeng. 2007, 98:968-977.
42. Pepper L., Cho Y., Boder E., Shusta E. A decade of yeast surface display technology: where are we now?. Comb. Chem. High Throughput Screen 2008, 11:127-134.
43. Perrone L., Ahmad A., Veguilla V., Lu X., Smith G., Katz J., Pushko P., Tumpey T. Intranasal vaccination with 1918 influenza virus-like particles protects mice and ferrets from lethal 1918 and H5N1 influenza virus challenge. J. Virol. 2009, 83:5726-5734.
44. Pumpens P., Grens E. HBV core particles as a carrier for B cell/T cell epitopes. Intervirology 2001, 44:98-114.
45. Pushko P., Tumpey T., Bu F., Knell J., Robinson R., Smith G. Influenza virus-like particles comprised of the HA, NA, and M1 proteins of H9N2 influenza virus induce protective immune responses in BALB/c mice. Vaccine 2005, 23:5751-5759.
46. Quan F., Huang C., Compans R., Kang S. Virus-like particle vaccine induces protective immunity against homologous and heterologous strains of influenza virus. J. Virol. 2007, 81:3514-3524.
47. Quan F., Steinhauer D., Huang C., Ross T., Compans R., Kang S. A bivalent influenza VLP vaccine confers complete inhibition of virus replication in lungs. Vaccine 2008, 26:3352-3361.
48. Ross T., Mahmood K., Crevar C., Schneider-Ohrum K., Heaton P., Bright R. A trivalent virus-like particle vaccine elicits protective immune responses against seasonal influenza strains in mice and ferrets. PLoS One 2009, 4:e6032.
49. Rothe A., Hosse R., Power B. In vitro display technologies reveal novel biopharmaceutics. FASEB J. 2006, 20:1599-1610.
50. Rothe A., Hosse R., Power B. Ribosome display for improved biotherapeutic molecules. Exp. Opin. Biol. Ther. 2006, 6:177-187.
51. Ruedl C., Schwarz K., Jegerlehner A., Storni T., Manolova V., Bachmann M. Virus-like particles as carriers for T-cell epitopes: limited inhibition of T-cell priming by carrier-specific antibodies. J. Virol. 2005, 79:717-724.
52. Sarkar N., Manthey W., Sheffield J. The morphology of murine oncornaviruses following different methods of preparation for electron microscopy. Cancer Res. 1975, 35:740-749.
53. Sedlik C., Saron M., Sarraseca J., Casal I., Leclerc C. Recombinant parvovirus-like particles as an antigen carrier: a novel nonreplicative exogenous antigen to elicit protective antiviral cytotoxic T cells. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:7503-7508.
54. Sereinig S., Stukova M., Zabolotnyh N., Ferko B., Kittel C., Romanova J., Vinogradova T., Katinger H., Kiselev O., Egorov A. Influenza virus NS vectors expressing the mycobacterium tuberculosis ESAT-6 protein induce CD4+ Th1 immune response and protect animals against tuberculosis challenge. Clin. Vac. Immunol. 2006, 13:898-904.
55. Slupetzky K., Shafti-Keramat S., Lenz P., Brandt S., Grassauer A., Sara M., Kirnbauer R. Chimeric papillomavirus-like particles expressing a foreign epitope on capsid surface loops. J. Gen. Virol. 2001, 82:2799-2804.
56. Straume D., Axelsson L., Nes I., Diep D. Improved expression and purification of the correctly folded response regulator PlnC from lactobacilli. J. Microbiol. Methods 2006, 67:193-201.
57. Szécsi J., Boson B., Johnsson P., Dupeyrot-Lacas P., Matrosovich M., Klenk H., Klatzmann D., Volchkov V., Cosset F. Induction of neutralising antibodies by virus-like particles harbouring surface proteins from highly pathogenic H5N1 and H7N1 influenza viruses. Virol. J. 2006, 3:70.
58. Takahashi R., Kanesashi S., Inoue T., Enomoto T., Kawano M., Tsukamoto H., Takeshita F., Imai T., Ochiya T., Kataoka K., Yamaguchi Y., Handa H. Presentation of functional foreign peptides on the surface of SV40 virus-like particles. J. Biotechnol. 2008, 135:385-392.
59. Treanor J., Schiff G., Hayden F., Brady R., Hay C., Meyer A., Holden-Wiltse J., Liang H., Gilbert A., Cox M. Safety and immunogenicity of a baculovirus-expressed hemagglutinin influenza vaccine: a randomized controlled trial. JAMA 2007, 297:1577-1582.
60. Wang B., Quan F., Kang S., Bozja J., Skountzou I., Compans R. Incorporation of membrane-anchored flagellin into influenza virus-like particles enhances the breadth of immune responses. J. Virol. 2008, 82:11813-11823.
61. Wang K., Holtz K., Anderson K., Chubet R., Mahmoud W., Cox M. Expression and purification of an influenza hemagglutinin-one step closer to a recombinant protein-based influenza vaccine. Vaccine 2006, 24:2176-2185.
62. Wickham, T., Davis, T., Granados, R., Shuler, M., Wood, H., 1992. Screening of insect cell lines for the production of recombinant proteins and infectious virus in the baculovirus expression system. Biotechnol. Prog. 8, 391-396.
63. Wiley D., Wilson I., Skehel J. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 1981, 289:373-378.
64. Wu C., Wu T., Kao S., Ko J., Jinn T. Expression and purification of a recombinant Fip-fve protein from Flammulina velutipes in baculovirus-infected insect cells. J Appl Microbiol 2008, 104:1354-1362.
65. Xu J., Xu W., Chen X., Zhao D., Wang Y. Recombinant DNA vaccine of the early secreted antigen ESAT-6 by Mycobacterium tuberculosis and Flt3 ligand enhanced the cell-mediated immunity in mice. Vaccine 2008, 26:4519-4525.