Increasing the potency of an alhydrogel-formulated anthrax vaccine by minimizing antigen-adjuvant interactions

Clinical and Vaccine Immunology

Volumn 20, Issue 11, 2013, Pages 1659-1668

  Watkinson, Allan ^a,g   Soliakov, Andrei ^b   Ganesan, Ashok ^c   Hirst, Karie ^d   LeButt, Chris ^e   Fleetwood, Kelly ^f   Fusco, Peter C ^d   Fuerst, Thomas R ^d   Lakey, Jeremy H ^b  

^a PharmAthene UK   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c XstalBio Ltd   (United Kingdom)

^d PharmAthene Inc   (United States)

^e DEFENCE SCIENCE AND TECHNOLOGY LABORATORY   (United Kingdom)

^f Logan Building   (United Kingdom)

^g GSB Pharma Consultants Ltd   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM HYDROXIDE; ANTHRAX VACCINE; PHOSPHATE; RECOMBINANT ANTIGEN; TRYPTOPHAN;

ANIMAL EXPERIMENT; ARTICLE; BACILLUS ANTHRACIS; BINDING AFFINITY; BINDING SITE; CHEMICAL BINDING; CIRCULAR DICHROISM; CONTROLLED STUDY; DRUG BINDING; DRUG DOSAGE FORM COMPARISON; DRUG EFFECT; DRUG EFFICACY; DRUG FORMULATION; DRUG POTENCY; DRUG STABILITY; FEMALE; FLUORESCENCE ANALYSIS; INFECTION PREVENTION; ISOTHERM; ISOTHERMAL TITRATION CALORIMETRY; LANGMUIR ADSORPTION ISOTHERM; MOUSE; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; SOLID STATE CIRCULAR DICHROISM; SURFACE PROPERTY; SURVIVAL RATE; SURVIVAL TIME; THERMOSTABILITY; VACCINE PRODUCTION; ZETA POTENTIAL;

ADJUVANTS, IMMUNOLOGIC; ALUMINUM HYDROXIDE; ANIMALS; ANTHRAX; ANTHRAX VACCINES; ANTIGENS, BACTERIAL; BUFFERS; CHEMISTRY, PHARMACEUTICAL; DISEASE MODELS, ANIMAL; DRUG STABILITY; FEMALE; MICE; PHOSPHATES; PROTEIN BINDING;

EID: 84886730842     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00320-13     Document Type: Article

References (51)

1. Liljeqvist S, Stahl S. 1999. Production of recombinant subunit vaccines: protein immunogens, live delivery systems and nucleic acid vaccines. J. Biotechnol. 73:1-33.
2. Petosa C, Collier JR, Klimpel KR, Leppla SH, Liddington RC. 1997. Crystal structure of the anthrax toxin protective antigen. Nature 385:833-838.
3. Perrie Y, Mohammed AR, Kirby DJ, McNeil SE, Bramwell VW. 2008. Vaccine adjuvant systems: enhancing the efficacy of sub-unit protein antigens. Int. J. Pharm. 364:272-280.
4. Rinella JV, White JL, Hem SL. 1996. Treatment of aluminium hydroxide adjuvant to optimize the adsorption of basic proteins. Vaccine 14:298-300.
5. Glenny AT, Pope CG, Waddington H, Wallace U. 1926. Immunology notes. XXIII. The antigenic value of toxoid precipitated by potassium alum. J. Pathol. Bacteriol. 29:31-40.
6. Flach TL, Ng G, Hari A, Desrosiers MD, Zhang P, Ward SM, Seamone ME, Vilaysane A, Mucsi AD, Fong Y, Prenner E, Ling CC, Tschopp J, Muruve DA, Amrein MW, Shi Y. 2011. Alum interaction with dendritic cell membrane lipids is essential for its adjuvanticity. Nat. Med. 17:479-487.
7. Levitz SM, Golenbock DT. 2012. Beyond empiricism: informing vaccine development through innate immunity research. Cell 148:1284-1292.
8. Hansen B, Malyala P, Singh M, Sun Y, Srivastava I, Hogenesch H, Hem SL. 2011. Effect of the strength of adsorption of HIV 1 SF162dV2gp140 to aluminum-containing adjuvants on the immune response. J. Pharm. Sci. 100:3245-3250.
9. Hansen B, Belfast M, Soung G, Song L, Egan PM, Capen R, HogenEsch H, Mancinelli R, Hem SL. 2009. Effect of the strength of adsorption of hepatitis B surface antigen to aluminum hydroxide adjuvant on the immune response. Vaccine 27:888-892.
10. Hansen B, Sokolovska A, HogenEsch H, Hem SL. 2007. Relationship between the strength of antigen adsorption to an aluminum-containing adjuvant and the immune response. Vaccine 25:6618-6624.
11. Romero Mendez IZ, Shi Y, HogenEsch H, Hem SL. 2007. Potentiation of the immune response to non-adsorbed antigens by aluminum-containing adjuvants. Vaccine 25:825-833.
12. Jiang DP, Morefield GL, HogenEsch H, Hem SL. 2006. Relationship of adsorption mechanism of antigens by aluminum-containing adjuvants to in vitro elution in interstitial fluid. Vaccine 24:1665-1669.
13. Hutchison S, Benson RA, Gibson VB, Pollock AH, Garside P, Brewer JM. 2012. Antigen depot is not required for alum adjuvanticity. FASEB J. 26:1272-1279.
14. Shirodkar S, Hutchinson RL, Perry DL, White JL, Hem SL. 1990. Aluminum compounds used as adjuvants in vaccines. Pharm. Res. 7:1282-1288.
15. Bruhne S, Gottlieb S, Assmus W, Alig E, Schmidt MU. 2008. Atomic structure analysis of nanocrystalline boehmite AlO(OH). Crystal Growth Design 8:489-493.
16. Yau PK, Schulze DG, Johnston CT, Hem SL. 2006. Aluminum hydroxide adjuvant produced under constant reactant concentration. J. Pharm. Sci. 95:1822-1833.
17. Seeber S, White JJL, Hem SL. 1991. Predicting the adsorption of proteins by aluminium-containing adjuvants. Vaccine 9:201-203.
18. R. Eur. J. Pharm. Biopharm. 80:25-32.
19. Agopian A, Ronzon F, Sauzeat E, Sodoyer R, El Habib R, Buchet R, Chevalier M. 2007. Secondary structure analysis of HIV-1-gp41 in solution and adsorbed to aluminum hydroxide by Fourier transform infrared spectroscopy. Biochim. Biophys. Acta 1774:351-358.
20. Dong A, Jones LS, Kerwin BA, Krishnan S, Carpenter JF. 2006. Secondary structures of proteins adsorbed onto aluminum hydroxide: infrared spectroscopic analysis of proteins from low solution concentrations. Anal. Biochem. 351:282-289.
21. R adjuvant, ultrasonic dispersion and protein binding: a TEM and analytical study. Micron 43:192-200.
22. Soliakov A, Harris JR, Watkinson A, Lakey JH. 2010. The structure of Yersinia pestis Caf1 polymer in free and adjuvant bound states. Vaccine 28:5746-5754.
23. Jones LS, Peek LJ, Power J, Markham A, Yazzie B, Middaugh CR. 2005. Effects of adsorption to aluminum salt adjuvants on the structure and stability of model protein antigens. J. Biol. Chem. 280:13406-13414.
24. Peek LJ, Martin TT, Nation CE, Pegram SA, Middaugh CR. 2007. Effects of stabilizers on the destabilization of proteins upon adsorption to aluminum salt adjuvants. J. Pharm. Sci. 96:547-557.
25. Morefield GL, HogenEsch H, Robinson JP, Hem SL. 2004. Distribution of adsorbed antigen in mono-valent and combination vaccines. Vaccine 22:1973-1984.
26. Hem SL, HogenEsch H. 2007. Relationship between physical and chemical properties of aluminum-containing adjuvants and immunopotentiation. Expert Rev. Vaccines 6:685-698.
27. Wittayanukulluk A, Jiang DP, Regnier FE, Hem SL. 2004. Effect of microenvironment pH of aluminum hydroxide adjuvant on the chemical stability of adsorbed antigen. Vaccine 22:1172-1176.
28. Williamson ED, Hodgson I, Walker NJ, Topping AW, Duchars MG, Mott JM, Estep J, LeButt C, Flick-Smith HC, Jones HE, Li H, Quinn CP. 2005. Immunogenicity of recombinant protective antigen and efficacy against aerosol challenge with anthrax. Infect. Immun. 73:5978-5987.
29. Langmuir I. 1916. The constitution and fundamental properties of solids and liquids: part 1: solids. J. Am. Chem. Soc. 38:2221-2295.
30. Bustamante C, Maestre MF. 1988. Statistical effects in the absorption and optical activity of particulate suspensions. Proc. Natl. Acad. Sci. U. S. A. 85:8482-8486.
31. Ganesan A, Watkinson A, Moore BD. 2012. Biophysical characterisation of thermal-induced precipitates of recombinant anthrax protective antigen: evidence for kinetically trapped unfolding domains in solid-state. Eur. J. Pharm. Biopharm. 82:475-484.
32. Lakey JH, Magetdana R, Ptak M. 1989. The lipopeptide antibiotic A21978C has a specific interaction with DMPC only in the presence of calcium-ions. Biochim. Biophys. Acta 985:60-66.
33. Lindblad EB. 2004. Aluminium compounds for use in vaccines. Immunol. Cell Biol. 82:497-505.
34. Ganesan A, Lyle C, Halling PJ, Kelly S, Price N, Moore BD. 2006. Assessing the structure of immobilised proteins and antigens using circular dichroism. J. Pharm. Pharmacol. 58:9.
35. Chalton DA, Kelly IF, McGregor A, Ridley H, Watkinson A, Miller J, Lakey JH. 2007. Unfolding transitions of Bacillus anthracis protective antigen. Arch. Biochem. Biophys. 465:1-10.
36. Collett D. 2003. Modelling survival data in medical research, 2nd ed. CRC Press, Boca Raton, FL.
37. Food and Drug Administration. 2004. International Conference on Harmonisation: evaluation of stability data: availability: notice. Fed. Regist. 69:32010-32011.
38. Hamid O, Solomon JC, Scotland R, Garcia M, Sian S, Ye W, Groshen SL, Weber JS. 2007. Alum with interleukin-12 augments immunity to a melanoma peptide vaccine: correlation with time to relapse in patients with resected high-risk disease. Clin. Cancer Res. 13:215-222.
39. Cooper A, Johnson CM, Lakey JH, Nollmann M. 2001. Heat does not come in different colours: entropy-enthalpy compensation, free energy windows, quantum confinement, pressure perturbation calorimetry, solvation and the multiple causes of heat capacity effects in biomolecular interactions. Biophys. Chem. 93:215-230.
40. Jelesarov I, Bosshard HR. 1999. Isothermal titration calorimetry and differential scanning calorimetry as complementary tools to investigate the energetics of biomolecular recognition. J. Mol. Recognit. 12:3-18.
41. Svergun DI, Richard S, Koch MHJ, Sayers Z, Kuprin S, Zaccai G. 1998. Protein hydration in solution: experimental observation by x-ray and neutron scattering. Proc. Natl. Acad. Sci. U. S. A. 95:2267-2272.
42. Young JAT, Collier RJ. 2007. Anthrax toxin: receptor binding, internalization, pore formation, and translocation. Annu. Rev. Biochem. 76:243-265.
43. Noe SM, Green MA, HogenEsch H, Hem SL. 2010. Mechanism of immunopotentiation by aluminum-containing adjuvants elucidated by the relationship between antigen retention at the inoculation site and the immune response. Vaccine 28:3588-3594.
44. Lin L, Ibrahim AS, Avanesian V, Edwards JE, Fu Y, Baquir B, Taub R, Spellberg B. 2008. Considerable differences in vaccine immunogenicities and efficacies related to the diluent used for aluminum hydroxide adjuvant. Clin. Vaccine Immunol. 15:582-584.
45. Hunter RL. 2002. Overview of vaccine adjuvants: present and future. Vaccine 20(Suppl 3):S7-S12.
46. Brewer JM, Pollock KGJ, Tetley L, Russell DG. 2004. Vesicle size influences the trafficking, processing, and presentation of antigens in lipid vesicles. J. Immunol. 173:6143-6150.
47. Kool M, Soullie T, van Nimwegen M, Willart MAM, Muskens F, Jung S, Hoogsteden HC, Hammad H, Lambrecht BN. 2008. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J. Exp. Med. 205:869-882.
48. Kuroda E, Ishii KJ, Uematsu S, Ohata K, Coban C, Akira S, Aritake K, Urade Y, Morimoto Y. 2011. Silica crystals and aluminum salts regulate the production of prostaglandin in macrophages via NALP3 inflammasome-independent mechanisms. Immunity 34:514-526.
49. Keele C, Neil E, Joels N. 1984. Samson Wright's applied physiology, 13th ed. Oxford Medical Publications, Oxford, England.
50. Iyer S, HogenEsch H, Hem SL. 2003. Relationship between the degree of antigen adsorption to aluminum hydroxide adjuvant in interstitial fluid and antibody production. Vaccine 21:1219-1223.
51. Bencini DA, Wild JR, O'Donovan GA. 1983. Linear one-step assay for the determination of orthophosphate. Anal. Biochem. 132:254-258. Diseases