Protective Vaccination against Infectious Bursal Disease Virus with Whole Recombinant Kluyveromyces lactis Yeast Expressing the Viral VP2 Subunit

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Arnold, Marina ^a   Durairaj, Vijay ^b   Mundt, Egbert ^b,c   Schulze, Katja ^a   Breunig, Karin D ^a   Behrens, Sven Erik ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY OF GEORGIA   (United States)

^c IDT Biologika GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; FUNGAL EXTRACT; FUNGUS VACCINE; KLUYVEROMYCES LACTIS EXTRACT; NEUTRALIZING ANTIBODY; OROTIDINE 5' PHOSPHATE DECARBOXYLASE; PROTEIN VP2; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BURSA FABRICII; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FED BATCH CULTURE; FUNGAL STRAIN; GENE EXPRESSION; HISTOPATHOLOGY; HOMOLOGOUS RECOMBINATION; IMMUNE RESPONSE; INFECTIOUS BURSAL DISEASE; INFECTIOUS BURSAL DISEASE VIRUS; MORTALITY; MOUSE; NONHUMAN; OPEN READING FRAME; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROMOTER REGION; PROTEIN EXPRESSION; VACCINATION; VIRUS CAPSID; YEAST CELL;

ADMINISTRATION, ORAL; ANIMALS; BIRNAVIRIDAE INFECTIONS; CHICKENS; FEMALE; GENE EXPRESSION; GENE ORDER; GENE TARGETING; INFECTIOUS BURSAL DISEASE VIRUS; INJECTIONS, SUBCUTANEOUS; KLUYVEROMYCES; MICE; POULTRY DISEASES; VACCINES, INACTIVATED; VIRAL STRUCTURAL PROTEINS; VIRAL VACCINES;

ANIMALIA; GALLUS GALLUS; INFECTIOUS BURSAL DISEASE VIRUS; KLUYVEROMYCES LACTIS; MIRIDAE; MUS;

EID: 84866385845     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042870     Document Type: Article

References (80)

1. Kibenge FS, Dhillon S, Russell RG, (1988) Biochemistry and immunology of infectious bursal disease virus. J Gen Virol 69: 1757-1775.
2. Coulibaly F, Chevalier C, Gutsche I, Pous J, Navaza J, et al. (2005) The birnavirus crystal structure reveals structural relationships among icosahedral viruses. Cell 120: 761-772.
3. Müller H, (1986) Replication of infectious bursal disease virus in lymphoid cells. Arch Virol 87: 191-203.
4. Petkov DI, Linnemann EG, Kapczynski DR, Sellers HS, (2009) Identification and characterization of two distinct bursal B-cell subpopulations following infectious bursal disease virus infection of White Leghorn chickens. Avian Dis 53: 347-355.
5. Rodríguez-Lecompte JC, Niño-Fong R, Lopez A, Frederick Markham RJ, Kibenge FS, (2005) Infectious bursal disease virus (IBDV) induces apoptosis in chicken B cells. Comp Immunol Microbiol Infect Dis 28: 321-337.
6. Hirai K, Calnek BW, (1979) In vitro replication of infectious bursal disease virus in established lymphoid cell lines and chicken B lymphocytes. Infect Immun 25: 964-970.
7. Okoye JO, Shoyinka SV, (1983) Newcastle disease in a vaccinated flock which had experienced subclinical infectious bursal disease. Trop Anim Health Prod 15: 221-225.
8. Bublot M, Pritchard N, Le Gros FX, Goutebroze S, (2007) Use of a vectored vaccine against infectious bursal disease of chickens in the face of high-titred maternally derived antibody. J Comp Pathol 137: 81-84.
9. Lai SY, (2004) Production and purification of immunogenic virus-like particles formed by the chimeric infectious bursal disease virus structural protein, rVP2H, in insect larvae. Process Biochem 39: 571.
10. Li L, Fang W, Li J, Huang Y, Yu L, (2006) Oral DNA vaccination with the polyprotein gene of infectious bursal disease virus (IBDV) delivered by the attenuated Salmonella elicits protective immune responses in chickens. Vaccine 24: 5919-5927.
11. Lucio B, Hitchner SB, (1979) Response of susceptible versus immune chicks to killed, live-modified, and wild infectious bursal disease virus vaccines. Avian Dis 23: 1037-1050.
12. Wood GW, Muskett JC, Thornton DH, (1983) Use of inactivated oil emulsion infectious bursal disease vaccines in breeder chickens to prevent immunosuppression in progeny chicks. Res Vet Sci 35: 114-115.
13. Müller H, Mundt E, Eterradossi N, Islam MR, (2012) Current status of vaccines against infectious bursal disease. Avian Pathol 41: 133-139.
14. Lucio B, Hitchner SB, (1979) Infectious Bursal Disease Emulsified Vaccine: Effect upon Neutralizing-Antibody Levels in the Dam and Subsequent Protection of the Progeny. Avian Dis 23: 1037-1050.
15. Wyeth PJ, Chettle N, (1982) Comparison of the efficacy of four inactivated infectious bursal disease oil emulsion vaccines. Vet Rec 110: 359-361.
16. Rosenberger JK, Cloud SS (1986) Isolation and characterization of variant infectious bursal disease viruses. Abstracts of the 123rd Meeting of the American Veterinary Medical Association Jul 20-24, Atlanta, Georgia, USA, Abstr. 181.
17. Snyder DB, Vakharia VN, Savage PK, (1992) Naturally occurring-neutralizing monoclonal antibody escape variants define the epidemiology of infectious bursal disease viruses in the United States. Arch Virol 127: 89-101.
18. Box P, (1989) High maternal antibodies help chicks beat virulent strains. World Poultry 53: 17-19.
19. Chettle N, Stuart JC, Wyeth PJ, (1989) Outbreak of virulent infectious bursal disease in East Anglia. Vet Rec 125: 271-272.
20. Kumar K, Singh KCP, Prasad CB, (2000) Immune Responses to Intermediate Strain IBD Vaccine at Different Levels of Maternal Antibody in Broiler Chickens. Trop Anim Health Prod 32: 357-360.
21. Rautenschlein S, Yeh HY, Sharma JM, (2002) The role of T cells in protection by an inactivated infectious bursal disease virus vaccine. Vet Immunol Immunopath 89: 159-167.
22. Tsukamoto K, Tanimura N, Kakita S, Ota K, Mase M, et al. (1995) Efficacy of three live vaccines against highly virulent infectious bursal disease virus in chickens with or without maternal antibodies. Avian Dis 39: 218-229.
23. Azad AA, McKern NM, Macreadie IG, Failla P, Heine HG, et al. (1991) Physicochemical and immunological characterization of recombinant host-protective antigen (VP2) of infectious bursal disease virus. Vaccine 9: 715-722.
24. Becht H, Müller H, Müller HK, (1988) Comparative studies on structural and antigenic properties of two serotypes of infectious bursal disease virus. J Gen Virol 69: 631-640.
25. Fahey KJ, Erny K, Crooks J, (1989) A conformational immunogen on VP-2 of infectious bursal disease virus that induces virus-neutralizing antibodies that passively protect chickens. J Gen Virol 70: 1473-1481.
26. Fahey KJ, McWaters P, Brown MA, Erny K, Murphy VJ, Hewish DR, (1991) Virus-neutralizing and passively protective monoclonal antibodies to infectious bursal disease virus of chickens. Avian Dis 35: 365-373.
27. Heine HG, Boyle DB, (1993) Infectious bursal disease virus structural protein VP2 expressed by a fowlpox virus recombinant confers protection against disease in chickens. Archives Virol 131: 277-292. XXX.
28. Vakharia VN, Snyder DB, Lütticken D, Mengel-Whereat SA, Savage PK, et al. (1994) Active and passive protection against variant and classic infectious bursal disease virus strains induced by baculovirus-expressed structural proteins. Vaccine 12: 452-456.
29. Pitcovski J, Di-Castro D, Shaaltiel Y, Azriel A, Gutter B, et al. (1996) Insect cell-derived VP2 of infectious bursal disease virus confers protection against the disease in chickens. Avian Diseases 40: 753-761.
30. Xu XG, Tong DW, Wang Z S, Zhang Q, Li ZC, et al. (2011) Baculovirus virions displaying infectious bursal disease virus VP2 protein protect chickens against infectious bursal disease virus infection. Avian Dis 55: 223-229.
31. Darteil R, Bublot M, Laplace E, Bouquet JF, Audonnet JC, et al. (1995) Herpesvirus of turkey recombinant viruses expressing infectious bursal disease virus (IBDV) VP2 immunogen induce protection against an IBDV virulent challenge in chickens. Virology 211: 481-490.
32. Tsukamoto K, Kojima C, Komori Y, Tanimura N, Mase M, et al. (1999) Protection of chickens against very virulent infectious bursal disease virus (IBDV) and Marek's disease virus (MDV) with a recombinant MDV expressing IBDV VP2. Virology 257: 352-362.
33. Tsukamoto K, Saito S, Saeki S, Sato T, Tanimura N, et al. (2002) Complete, long-lasting protection against lethal infectious bursal disease virus challenge by a single vaccination with an avian herpesvirus vector expressing VP2 antigens. J Virol 76: 5637-5645.
34. Sheppard M, Werner W, Tsatas E, McCoy R, Prowse S, et al. (1998) Fowl adenovirus recombinant expressing VP2 of infectious bursal disease virus induces protective immunity against bursal disease. Archives Virol 143: 915-930.
35. Francois A, Chevalier C, Delmas B, Eterradossi N, Toquin D, et al. (2004) Avian adenovirus CELO recombinants expressing VP2 of infectious bursal disease virus induce protection against bursal disease in chickens. Vaccine 22: 2351-2360.
36. Shaw I, Davison TF, (2000) Protection from IBDV-induced bursal damage by a recombinant fowlpox vaccine, fpIBD1, is dependent on the titre of challenge virus and chicken genotype. Vaccine 18: 3230-3241.
37. Zhou X, Wang D, Xiong J, Zhang P, Li Y, et al. (2010) Protection of chickens, with or without maternal antibodies, against IBDV infection by a recombinant IBDV-VP2 protein. Vaccine 28: 3990-3996.
38. Wu J, Yu L, Li L, Hu J, Zhou J, et al. (2007) Oral immunization with transgenic rice seeds expressing VP2 protein of infectious bursal disease virus induces protective immune responses in chickens. Plant Biotechnology Journal 5: 570-578.
39. Rong J, Jiang T, Cheng T, Shen M, Du Y, et al. (2007) Large-scale manufacture and use of recombinant VP2 vaccine against infectious bursal disease in chickens. Vaccine 25: 7900-7908.
40. Wu H, Singh NK, Locy RD, Scissum-Gunn K, Giambrone JJ, (2004) Immunization of chickens with VP2 protein of infectious bursal disease virus expressed in Arabidopsis thaliana. Avian Dis 48: 663-668.
41. Pitcovski J, Gutter B, Gallili G, Goldway M, Perelman B, et al. (2003) Development and large-scale use of recombinant VP2 vaccine for the prevention of infectious bursal disease of chickens. Vaccine 21: 4736-4743.
42. Villegas P, Hamoud M, Purvis LB, Perozo F, (2008) Infectious bursal disease subunit vaccination. Avian Dis 52: 670-674.
43. Dey S, Upadhyay C, Madhan MC, Kataria JM, Vakharia VN, (2009) Formation of subviral particles of the capsid protein VP2 of infectious bursal disease virus and its application in serological diagnosis. J Virol Methods 157: 84-89.
44. Krijger JJ, Baumann J, Wagner M, Schulze K, Reinsch C, et al. (2012) A novel, lactase-based selection and strain improvement strategy for recombinant protein expression in Kluyveromyces lactis. Microb Cell Fact: in press.
45. Zenke FT, Zachariae W, Lunkes A, Breunig KD, (1993) Gal80 proteins of Kluyveromyces lactis and Saccharomyces cerevisiae are highly conserved but contribute differently to glucose repression of the galactose regulon. Mol Cell Biol 13: 7566-7576.
46. Jagadish MN, Laughton DL, Azad AA, Macreadie IG, (1991) Stable synthesis of viral protein 2 of infectious bursal disease virus in Saccharomyces cerevisiae. Gene 108: 275-279.
47. Cox JC, Coulter AR, (1997) Adjuvants-a classification and review of their modes of action. Vaccine 15: 248-256.
48. Bathurst IC, (1994) Protein expression in yeast as an approach to production of recombinant malaria antigens. Am J Trop Med Hyg 50: 20-26.
49. Gellissen G, Hollenberg CP, (1997) Application of yeasts in gene expression studies: a comparison of Saccharomyces cerevisiae, Hansenula polymorpha and Kluyveromyces lactis - a review. Gene 190: 87-97.
50. Stubbs AC, Martin KS, Coeshott C, Skaates SV, Kuritzkes DR, et al. (2001) Whole recombinant yeast vaccine activates dendritic cells and elicits protective cell-mediated immunity. Nature Med 7: 625-629.
51. Lu Y, Bellgrau D, Dwyer-Nield LD, Malkinson AM, Duke RC, et al. (2004) Mutation-selective tumor remission with Ras-targeted, whole yeast-based immunotherapy. Cancer Res 64: 5084-5088.
52. Schreuder MP, Deen C, Boersma WJ, Pouwels PH, Klis FM, (1996) Yeast expressing hepatitis B virus surface antigen determinants on its surface: implications for a possible oral vaccine. Vaccine 14: 383-388.
53. Blanquet S, Antonelli R, Laforet L, Denis S, Marol-Bonnin S, et al. (2004) Recombinant Saccharomyces cerevisiae secreting proteins or peptides as a new drug delivery system in the gut. J Biotechnol 110: 37-49.
54. Beier R, Gebert A, (1998) Kinetics of particle uptake in the domes of Peyer's patches. Am J Physiol 275: 130-137.
55. Shin SJ, Bae JL, Cho YW, Lee DY, Kim DH, et al. (2005) Induction of antigen-specific immune responses by oral vaccination with Saccharomyces cerevisiae expressing Actinobacillus pleuropneumoniae ApxIIA. FEMS Immunol Med Microbiol 43: 155-164.
56. van Ooyen AJJ, Dekker P, Huang M, Olsthoorn MMA, Jacobs DI, et al. (2006) Heterologous protein production in the yeast Kluyveromyces lactis. FEMS Yeast Res 6: 381-392.
57. Backhaus K, Buchwald U, Heppeler N, Schmitz HP, Rodicio R, et al. (2011) Milk and sugar: regulation of cell wall synthesis in the milk yeast Kluyveromyces lactis. Eur J Cell Biol 90: 745-750.
58. Uccelletti D, Farina F, Mancini P, Palleschi C, (2004) KlPMR1 inactivation and calcium addition enhance secretion of non-hyperglycosylated heterologous proteins in Kluyveromyces lactis. J Biotechnol 109: 93-101.
59. Mulder W, Scholten IHJM, Grivell LA, (1995) Carbon catabolite regulation of transcription of nuclear genes coding for mitochondrial proteins in the yeast Kluyveromyces lactis. Curr Genet 28: 267-273.
60. Breunig KD, Bolotin-Fukuhara M, Bianchi MM, Bourgarel D, Falcone C, et al. (2000) Regulation of primary carbon metabolism in Kluyveromyces lactis. Enzyme and Microbial Technology 26: 771-780.
61. Donnini C, Farina F, Neglia B, Compagno MC, Uccelletti D, et al. (2004) Improved production of heterologous proteins by a glucose repression-defective mutant of Kluyveromyces lactis. Appl Environ Microbiol 70: 2632-2638.
62. Kuger P, Gödecke A, Breunig KD, (1990) A mutation in the Zn-finger of the GAL4 homolog LAC9 results in glucose repression of its target genes. Nucl Acids Res 18: 745-751.
63. Ardiani A, Higgins JP, Hodge JW, (2010) Vaccines based on whole recombinant Saccharomyces cerevisiae cells. FEMS Yeast Res 10: 1060-1069.
64. Fuller TE, Martin S, Teel JF, Alaniz GR, Kennedy MJ, et al. (2000) Identification of Actinobacillus pleuropneumoniae virulence genes using signature-tagged mutagenesis in a swine infection model. Microb Pathog 29: 39-51.
65. Hensel A, van Leengoed LA, Szostak M, Windt H, Weissenböck H, et al. (1996) Induction of protective immunity by aerosol or oral application of candidate vaccines in a dose-controlled pig aerosol infection model. J Biotechnol 44: 171-181.
66. Prideaux CT, Lenghaus C, Krywult J, Hodgson AL, (1999) Vaccination and protection of pigs against pleuropneumonia with a vaccine strain of Actinobacillus pleuropneumoniae produced by site-specific mutagenesis of the ApxII operon. Infect Immun 67: 1962-1966.
67. Droual R, Bickford AA, Charlton BR, Kuney DR, (1990) Investigation of problems associated with intramuscular breast injection of oil-adjuvanted killed vaccines in chickens. Avian Dis 34: 473-478.
68. Burns KE, Ruiz J, Glisson JR, (2003) Evaluation of the effect of heating an oil-emulsion Pasteurella multocida bacterin on tissue reaction and immunity. Avian Dis 47: 54-58.
69. Cox E, Verdonck F, Vanrompay D, Goddeeris B, (2006) Adjuvants modulating mucosal immune responses or directing systemic responses towards the mucosa. Veterinary Res 37: 511-539.
70. Saugar I, Luque D, Oña A, Rodríguez JF, Carrascosa JL, et al. (2005) Structural polymorphism of the major capsid protein of a double-stranded RNA virus: an amphipathic alpha helix as a molecular switch. Structure 13: 1007-1017.
71. Icard AH, Sellers HS, Mundt E, (2008) Detection of infectious bursal disease virus isolates with unknown antigenic properties by reverse genetics. Avian Dis 52: 590-598.
72. Sherman F, Fink GR, Hicks JB (1986) Methods in yeast genetics: A laboratory course manual. New York: Cold Spring Harbor Press.
73. Raab D, Graf M, Notka F, Schödl T, Wagner R, (2010) The GeneOptimizer Algorithm: using a sliding window approach to cope with the vast sequence space in multiparameter DNA sequence optimization. Syst Synth Biol 4: 215-225.
74. Granzow H, Birghan C, Mettenleiter TC, Beyer J, Köllner B, et al. (1997) A second form of infectious bursal disease virus-associated tubule contains VP4. J Virol 71: 8879-8885.
75. Engler-Blum G, Meier M, Frank J, Müller GA, (1993) Reduction of background problems in nonradioactive northern and Southern blot analyses enables higher sensitivity than 32P-based hybridizations. Anal Biochem 210: 235-244.
76. Hoshi S, Uchino A, Saito N, Kusanagi KI, Ihara T, et al. (1999) Comparison of adjuvants with respect to serum IgG antibody response in orally immunized chickens. Comp Immunol Microbiol Infect Dis 22: 63-69.
77. Snyder DB, Lana DP, Cho BR, Marquardt WW, (1988) Group and strain-specific neutralization sites of infectious bursal disease virus defined with monoclonal antibodies. Avian Dis 32: 527-534.
78. Schröder A, van Loon AA, Goovaerts D, Mundt E, (2000) Chimeras in noncoding regions between serotypes I and II of segment A of infectious bursal disease virus are viable and show pathogenic phenotype in chickens. J Gen Virol 81: 533-540.
79. Perozo F, Villegas P, Estevez C, Alvarado IR, Purvis LB, et al. (2008) Protection against infectious bursal disease virulent challenge conferred by a recombinant avian adeno-associated virus vaccine. Avian Dis 52: 315-319.
80. Rosales AG, Villegas P, Lukert PD, Fletcher OJ, Mohamed MA, et al. (1989) Pathogenicity of recent isolates of infectious bursal disease virus in specific-pathogen-free chickens: protection conferred by an intermediate vaccine strain. Avian Dis 33: 729-734.