A microbial platform for rapid and low-cost virus-like particle and capsomere vaccines

Vaccine

Volumn 29, Issue 41, 2011, Pages 7154-7162

  Middelberg, Anton P J ^a   Rivera Hernandez, Tania ^a   Wibowo, Nani ^a   Lua, Linda H L ^a   Fan, Yuanyuan ^a   Magor, Graham ^c   Chang, Cindy ^a   Chuan, Yap P ^a   Good, Michael F ^b,c   Batzloff, Michael R ^b,c  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

Influenza; Manufacture; Particle; Streptococcus; Vaccine; Virus

Indexed keywords

ANTIBODY; J8 PEPTIDE; PEPTIDE DERIVATIVE; PROTEIN VP1; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ARTICLE; BACTERIAL STRAIN; BIOREACTOR; CAPSOMERE; CONTROLLED STUDY; COST EFFECTIVENESS ANALYSIS; DRUG EFFICACY; DRUG FORMULATION; DRUG SAFETY; ESCHERICHIA COLI; FEMALE; FREEZE DRYING; IMMUNIZATION; INFLUENZA; MEDICAL TECHNOLOGY; MICROBIAL PLATFORM; MOUSE; NONHUMAN; POLYOMA VIRUS; PRIORITY JOURNAL; PROTEIN STABILITY; STREPTOCOCCUS GROUP A; VACCINE PRODUCTION; VIRUS CAPSID; VIRUS LIKE AGENT; VIRUS PURIFICATION;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODIES, VIRAL; ANTIGENS, BACTERIAL; BIOTECHNOLOGY; CAPSID PROTEINS; ESCHERICHIA COLI; FEMALE; GENE EXPRESSION; GENETIC ENGINEERING; MICE; POLYOMAVIRUS; RECOMBINANT PROTEINS; STREPTOCOCCUS PYOGENES; TECHNOLOGY, PHARMACEUTICAL; VACCINES, VIROSOME; VIRAL MATRIX PROTEINS; VIROSOMES;

EID: 80052432169     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.05.075     Document Type: Article

References (70)

1. Fenner F. The Florey lecture, 1983 - biological-control, as exemplified by smallpox eradication and myxomatosis. Proceedings of the Royal Society of London Series B, Biological Sciences 1983, 218(1212):259-285.
2. Henderson D.A., Fenner F. Recent events and observations pertaining to smallpox virus destruction in 2002. Clinical Infectious Diseases 2001, 33(7):1057-1059.
3. Fenner F. Risks and benefits of vaccinia vaccine use in the worldwide smallpox eradication campaign. Research in Virology 1989, 140(5):465-466.
4. Heinsbroek E., Ruitenberg E.J. The global introduction of inactivated polio vaccine can circumvent the oral polio vaccine paradox. Vaccine 2010, 28(22):3778-3783.
5. Kew O.M., Sutter R.W., de Gourville E.M., Dowdle W.R., Pallansch M.A. Vaccine-derived polioviruses and the endgame strategy for global polio eradication. Annual Review of Microbiology 2005, 59:587-635.
6. Okonko I.O., Onoja B.A., Adedeji A.O., Ogun A.A., Udeze A.O., Ejembi J., et al. The role of vaccines in elimination and global eradication of measles: a review of literature. African Journal of Pharmacy and Pharmacology 2009, 3(9):413-425.
7. Moss W.J., Griffin D.E. Global measles elimination. Nature Reviews Microbiology 2006, 4(12):900-908.
8. WHO, The global burden of disease. 2004 update. Geneva; 2008.
9. Morens D.M., Folkers G.K., Fauci A.S. The challenge of emerging and re-emerging infectious diseases. Nature 2004, 430(6996):242-249.
10. Kane M.A. Global implementation of human papillomavirus (HPV) vaccine: lessons from hepatitis B vaccine. Gynecologic Oncology 2010, 117(2):S32-S35.
11. Milstien J., Cardenas V., Cheyne J., Brooks A. WHO study policy development processes for a new vaccine: case study of malaria vaccines. Malaria Journal 2010, 9..
12. Massingale S., Pippin T., Davidson S., Butler J. Emergence of a novel swine-origin Influenza A (H1N1) virus in humans. New England Journal of Medicine 2009.
13. Krammer F., Grabherr R. Alternative influenza vaccines made by insect cells. Trends in Molecular Medicine 2010, 16(7):313-320.
14. Frazer I.H. Prevention of cervical cancer through papillomavirus vaccination. Nature Reviews Immunology 2004, 4(1):46-54.
15. Zhou J., Sun X.Y., Stenzel D.J., Frazer I.H. Expression of vaccinia recombinant hpv 16 l1 and l2 ORF proteins in epithelial-cells is sufficient for assembly of HPV virion-like particles. Virology 1991, 185(1):251-257.
16. Roy P., Noad R. Virus-like particles as a vaccine delivery system - myths and facts. Human Vaccines 2008, 4(1):5-12.
17. Palomares L.A., Ramirez O.T. Challenges for the production of virus-like particles in insect cells: the case of rotavirus-like particles. Biochemical Engineering Journal 2009, 45(3):158-167.
18. Pattenden L.K., Middelberg A.P.J., Niebert M., Lipin D.I. Towards the preparative and large-scale precision manufacture of virus-like particles. Trends in Biotechnology 2005, 23(10):523-529.
19. Quan F.S., Vunnava A., Compans R.W., Kang S.M. Virus-like particle vaccine protects against 2009 H1N1 pandemic influenza virus in mice. PLoS One 2010, 5(2).
20. Herbst-Kralovetz M., Mason H.S., Chen Q. Norwalk virus-like particles as vaccines. Expert Review of Vaccines 2010, 9(3):299-307.
21. Ciarlet M., Crawford S.E., Barone C., Bertolotti-Ciarlet A., Ramig R.F., Estes M.K., et al. Subunit rotavirus vaccine administered parenterally to rabbits induces active protective immunity. Journal of Virology 1998, 72(11):9233-9246.
22. Bertolotti-Ciarlet A., Ciarlet M., Crawford S.E., Conner M.E., Estes M.K. Immunogenicity and protective efficacy of rotavirus 2/6-virus-like particles produced by a dual Baculovirus expression vector and administered intramuscularly, intranasally, or orally to mice. Vaccine 2003, 21(25-26):3885-3900.
23. Young K.R., McBurney S.P., Karkhanis L.U., Ross T.M. Virus-like particles: designing an effective AIDS vaccine. Methods 2006, 40(1):98-117.
24. Stanley M.A. Human papillomavirus vaccines. Reviews in Medical Virology 2006, 16(3):139-149.
25. Andrus J.K., Sherris J., Fitzsimmons J.W., Kane M.A., Aguado M.T. Introduction of human papillomavirus vaccines into developing countries - international strategies for funding and procurement. Vaccine 2008, 26:K87-K92.
26. Bundy B.C., Franciszkowicz M.J., Swartz J.R. Escherichia coli-based cell-free synthesis of virus-like particles. Biotechnology and Bioengineering 2008, 100(1):28-37.
27. 2+-triggered switch in the thermodynamic attraction between structural protein capsomeres. Journal of the Royal Society Interface 2010, 7(44):409-421.
28. Salunke D.M., Caspar D.L.D., Garcea R.L. Self-assembly of purified polyomavirus capsid protein-Vp1. Cell 1986, 46(6):895-904.
29. Chuan Y.P., Fan Y.Y., Lua L.H.L., Middelberg A.P.J. Quantitative analysis of virus-like particle size and distribution by field-flow fractionation. Biotechnology and Bioengineering 2008, 99(6):1425-1433.
30. Chuan Y.P, Lua L.H.L., Middelberg A.P.J. High-level expression of soluble viral structural protein in Escherichia coli. Journal of Biotechnology 2008, 134(1-2):64-71.
31. Liew M.W.O., Rajendran A., Middelberg A.P.J. Microbial production of virus-like particle vaccine protein at gram-per-litre levels. Journal of Biotechnology 2010, 150(2):224-231.
32. Lipin D.I., Lua L.H.L., Middelberg A.P.J. Quaternary size distribution of soluble aggregates of glutathione-S-transferase-purified viral protein as determined by asymmetrical flow field flow fractionation and dynamic light scattering. Journal of Chromatography A 2008, 1190(1-2):204-214.
33. Lipin D.I., Raj A., Lua L.H.L., Middelberg A.P.J. Affinity purification of viral protein having heterogeneous quaternary structure: modeling the impact of soluble aggregates on chromatographic performance. Journal of Chromatography A 2009, 1216(30):5696-5708.
34. Rose R.C., White W.I., Li M.L., Suzich J.A., Lane C., Garcea R.L. Human papillomavirus type 11 recombinant L1 capsomeres induce virus-neutralizing antibodies. Journal of Virology 1998, 72(7):6151-6154.
35. Thones N., Herreiner A., Schadlich L., Piuko K., Muller M. A direct comparison of human papillomavirus type 16 L1 particles reveals a lower immunogenicity of capsomeres than viruslike particles with respect to the induced antibody response. Journal of Virology 2008, 82(11):5472-5485.
36. Thones N., Muller M. Oral immunization with different assembly forms of the HPV 16 major capsid protein L1 induces neutralizing antibodies and cytotoxic T-lymphocytes. Virology 2007, 369(2):375-388.
37. Yuan H., Estes P.A., Chen Y., Newsome J., Olcese V.A., Garcea R.L., et al. Immunization with a pentameric L1 fusion protein protects against papillomavirus infection. Journal of Virology 2001, 75(17):7848-7853.
38. Murata Y., Lightfoote P.M., Rose R.C., Walsh E.E. Antigenic presentation of heterologous epitopes engineered into the outer surface-exposed helix 4 loop region of human papillomavirus L1 capsomeres. Virology Journal 2009, 6:p10.
39. Bian T., Wang Y., Lu Z., Ye Z., Zhao L., Ren J., et al. Human papillomavirus type 16 L1E7 chimeric capsomeres have prophylactic and therapeutic efficacy against papillomavirus in mice. Molecular Cancer Therapeutics 2008, 7(5):1329-1335.
40. Carrat F., Flahault A. Influenza vaccine: the challenge of antigenic drift. Vaccine 2007, 25(39-40):6852-6862.
41. Burnet F.M. Influenza virus on the developing egg: I. Changes associated with the development of an egg-passage strain of virus. British Journal of Experimental Pathology 1936, 17(4):282-293.
42. Bommakanti G., Citron M.P., Hepler R.W., Callahan C., Heidecker G.J., Najar T.A., et al. Design of an HA2-based Escherichia coli expressed influenza immunogen that protects mice from pathogenic challenge. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(31):13701-13706.
43. Ionescu R.M., Przysiecki C.T., Liang X., Garsky V.M., Fan J., Wang B., et al. Pharmaceutical and immunological evaluation of human papillomavirus viruslike particle as an antigen carrier. Journal of Pharmaceutical Sciences 2006, 95(1):70-79.
44. Neirynck S., Deroo T., Saelens X., Vanlandschoot P., Jou W.M., Fiers W. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nature Medicine 1999, 5(10):1157-1163.
45. Schotsaert M., De Filette M., Fiers W., Saelens X. Universal M2 ectodomain-based influenza A vaccines: preclinical and clinical developments. Expert Review of Vaccines 2009, 8(4):499-508.
46. Pandey M., Batzloff M.R., Good M.F. Mechanism of protection induced by Group A Streptococcus vaccine candidate J8-DT: contribution of B and T-cells towards protection. PLoS One 2009, 4.(4).
47. Batzloff M.R., Sriprakash K.S., Good M.F. Vaccine development for Group A Streptococcus infections and associated diseases. Current Drug Targets 2004, 5(1):57-69.
48. Carapetis J.R., Steer A.C., Mulholland E.K., Weber M. The global burden of Group A Streptococcal diseases. Lancet Infectious Diseases 2005, 5(11):685-694.
49. Batzloff M.R., Hayman W.A., Davies M.R., Zeng M., Pruksakorn S., Brandt E.R., Good M.F. Protection against Group A Streptococcus by immunization with J8-diphtheria toxoid: contribution of J8- and diphtheria toxoid-specific antibodies to protection. Journal of Infectious Diseases 2003, 187(10):1598-1608.
50. Hayman W.A., Brandt E.R., Relf W.A., Cooper J., Saul A., Good M.F. Mapping the minimal murine T cell and B cell epitopes within a peptide vaccine candidate from the conserved region of the M protein of Group A Streptococcus. International Immunology 1997, 9(11):1723-1733.
51. Pandey M., Sekuloski S., Batzloff M.R. Novel strategies for controlling Streptococcus pyogenes infection and associated diseases: from potential peptide vaccines to antibody immunotherapy. Immunology and Cell Biology 2009, 87(5):391-399.
52. Shaila M.S., Nayak R., Prakash S.S, Georgousakis M., Brandt E., McMillan D.J., et al. Comparative in silico analysis of two vaccine candidates for Group A Streptococcus predicts that they both may have similar safety profiles. Vaccine 2007, 25(18):3567-3573.
53. Sambrook J.a.D.W.R. Molecular cloning: a laboratory manual 2001, Cold Spring Harbor Laboratory Press, NY. 3rd ed.
54. Brandt E.R., Hayman W.A., Currie B., Carapetis J., Wood Y., Jackson D.C., et al. Opsonic human antibodies from an endemic population specific for a conserved epitope on the M protein of Group A Streptococci. Immunology 1996, 89(3):331-337.
55. Brandt E.R., Hayman W.A., Currie B., Pruksakorn S., Good M.F. Human antibodies to the conserved region of the M protein: Opsonization of heterologous strains of Group A Streptococci. Vaccine 1997, 15(16):1805-1812.
56. Lefeber D.J., Benaissa-Trouw B., Vliegenthart J.F.G., Kamerling J.P., Jansen W.T.M., Kraaijeveld K., et al. Th1-directing adjuvants increase the immunogenicity of oligosaccharide-protein conjugate vaccines related to Streptococcus pneumoniae type 3. Infection and Immunity 2003, 71(12):6915-6920.
57. Ravetch J.V, Kinet J.P. Fc receptors. Annual Review of Immunology 1991, 9(1):457-492.
58. Middelberg A.P.J., O'Neill B.K., Bogle I.D.L., Snoswell M.A. A novel technique for the measurement of disruption in high-pressure homogenization - studies on Escherichia coli containing recombinant inclusion-bodies. Biotechnology and Bioengineering 1991, 38(4):363-370.
59. Pease L.F., Lipin D.I., Tsai D.H., Zachariah M.R., Lua L.H.L, Tarlov M.J., Middelberg A.P.J. Quantitative characterization of virus-like particles by asymmetrical flow field flow fractionation, electrospray differential mobility analysis, and transmission electron microscopy. Biotechnology and Bioengineering 2009, 102(3):845-855.
60. Stehle T., Harrison S.C. High-resolution structure of a polyomavirus VP1-oligosaccharide complex: implications for assembly and receptor binding. EMBO Journal 1997, 16(16):5139-5148.
61. Stehle T., Yan Y.W., Benjamin T.L., Harrison S.C. Structure of murine polyomavirus complexed with an oligosaccharide receptor fragment. Nature 1994, 369(6476):160-163.
62. Lua LHL, Middelberg APJ. VLP based vaccine delivery system, WO 2008/040060; 2006.
63. Shin Y.C., Folk W.R. Formation of polyomavirus-like particles with different VP1 molecules that bind the urokinase plasminogen activator receptor. Journal of Virology 2003, 77(21):11491-11498.
64. Skrastina D., Bulavaite A., Sominskaya I., Kovalevska L., Ose V., Priede D., et al. High immunogenicity of a hydrophilic component of the hepatitis B virus preS1 sequence exposed on the surface of three virus-like particle carriers. Vaccine 2008, 26(16):1972-1981.
65. Miller M.A., Viboud C., Balinska M., Simonsen L. The signature features of influenza pandemics-implications for policy. New England Journal of Medicine 2009.
66. Lang R., Winter G., Vogt L., Zurcher A., Dorigo B., Schimmele B. Rational design of a stable freeze-dried virus-like particle-based vaccine formulation. Drug Development and Industrial Pharmacy 2009, 35(1):83-97.
67. Azevedo M.S.P., Gonzalez A.M., Yuan L., Jeong K.I., Iosef C., Van Nguyen T., et al. An oral versus intranasal prime/boost regimen using attenuated human rotavirus or VP2 and VP6 virus-like particles with immunostimulating complexes influences protection and antibody-secreting cell responses to rotavirus in a neonatal gnotobiotic pig model. Clinical and Vaccine Immunology 2010, 17(3):420-428.
68. Pearton M., Kang S.M., Song J.M., Kim Y.C., Quan F.S., Anstey A., et al. Influenza virus-like particles coated onto microneedles can elicit stimulatory effects on Langerhans cells in human skin. Vaccine 2010, 28(37):6104-6113.
69. Barrett P.N., Portsmouth D., Ehrlich H.J. Developing cell culture-derived pandemic vaccines. Current Opinion in Molecular Therapeutics 2010, 12(1):21-30.
70. Ulmer J.B., Valley U., Rappuoli R. Vaccine manufacturing: challenges and solutions. Nature Biotechnology 2006, 24(11):1377-1383.