A systematic approach toward stabilization of CagL, a protein antigen from Helicobacter pylori that is a candidate subunit vaccine

Journal of Pharmaceutical Sciences

Volumn 102, Issue 8, 2013, Pages 2508-2519

  Choudhari, Shyamal P ^a   Pendleton, Kirk P ^a   Ramsey, Joshua D ^b   Blanchard, Thomas G ^c   Picking, William D ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

^b Oklahoma State University   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Light scattering (static); PH; Physical stability; Protein aggregation; Protein formulation; Stabilization; Temperature; Vaccines

Indexed keywords

8 ANILINO 1 NAPHTHALENESULFONIC ACID; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; PROTEIN CAGL; SUBUNIT VACCINE; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5;

ARTICLE; BACTERIUM ADHERENCE; CIRCULAR DICHROISM; CONTROLLED STUDY; HELICOBACTER PYLORI; LIGHT SCATTERING; NONHUMAN; PH; PROTEIN AGGREGATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; THERMOSTABILITY; TRANSITION TEMPERATURE; TYPE IV SECRETION SYSTEM; ULTRAVIOLET SPECTROSCOPY;

EID: 84881002741     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.23643     Document Type: Article

References (51)

1. Warren JR, Marshall BJ. 1983. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet 321:1273-1275.
2. Marshall BJ, Warren JR. 1984. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1(8390):1311-1315.
3. NIH CC. 1994. Helicobacter pylori in peptic ulcer disease. JAMA 272:65-69.
4. World Health Organization. 1994. Infection with Helicobacter pylori. Schistosomes, liver flukes and Helicobacter pylori. Lyon, France: International Agency for Research on Cancer, pp 177-241.
5. Rupnow MF, Shachter RD, Owens DK, Parsonnet J. 2001. Quantifying the population impact of a prophylactic Helicobacter pylori vaccine. Vaccine 20(5-6):879-885.
6. Blanchard TG, Nedrud JG. 2010. Helicobacter pylori vaccines. In Helicobacter pylori in the 21st century; P, Hazel M, Eds. Wallingford, UK: CABI, pp 167-189.
7. Czinn SJ, Blanchard T. 2011. Vaccinating against Helicobacter pylori infection. Nat Rev Gastroenterol Hepatol 8(3):133-140.
8. Ferrero RL, Thiberge J-M, Kansau I, Wuscher N, Huerre M, Labigne A. 1995. The groES homolog of Helicobacter pylori confers protective immunity against mucosal infection in mice. Proc Natl Acad Sci USA 92:6499-6503.
9. Fischer W, Puls J, Buhrdorf R, Gebert B, Odenbreit S, Haas R. 2001. Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: Essential genes for CagA translocation in host cells and induction of interleukin-8. Mol Microbiol 42(5):1337-1348.
10. Segal ED, Cha J, Lo J, Falkow S, Tompkins LS. 1999. Altered states: Involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc Natl Acad Sci USA 96(25):14559-14564.
11. Asahi M, Azuma T, Ito S, Ito Y, Suto H, Nagai Y, Tsubokawa M, Tohyama Y, Maeda S, Omata M, Suzuki T, Sasakawa C. 2000. Helicobacter pylori CagA protein can be tyrosine phosphorylated in gastric epithelial cells. J Exp Med 191(4):593-602.
12. Backert S, Ziska E, Brinkmann V, Zimny-Arndt U, Fauconnier A, Jungblut PR, Naumann M, Meyer TF. 2000. Translocation of the Helicobacter pylori CagA protein in gastric epithelial cells by a type IV secretion apparatus. Cell Microbiol 2(2):155-164.
13. Odenbreit S, Puls J, Sedlmaier B, Gerland E, Fischer W, Haas R. 2000. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287(5457):1497-1500.
14. Stein M, Rappuoli R, Covacci A. 2000. Tyrosine phosphorylation of the Helicobacter pylori CagA antigen after cag-driven host cell translocation. Proc Natl Acad Sci USA 97(3):1263-1268.
15. Kwok T, Zabler D, Urman S, Rohde M, Hartig R, Wessler S, Misselwitz R, Berger J, Sewald N, Konig W, Backert S. 2007. Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449(7164):862-866.
16. Jimenez-Soto LF, Kutter S, Sewald X, Ertl C, Weiss E, Kapp U, Rohde M, Pirch T, Jung K, Retta SF, Terradot L, Fischer W, Haas R. 2009. Helicobacter pylori type IV secretion apparatus exploits beta1 integrin in a novel RGD-independent manner. PLoS Pathog 5(12):e1000684.
17. Maddux NR, Joshi SB, Volkin DB, Ralston JP, Middaugh CR. 2011. Multidimensional methods for the formulation of biopharmaceuticals and vaccines. J Pharm Sci 100:4171-4197.
18. Johnson WC. 1988. Secondary structure of proteins through circular dichroism spectroscopy. Annu Rev Biophys Biophys Chem 17:145-166.
19. Wilson WW. 2003. Light scattering as a diagnostic for protein crystal growth-A practical approach. J Struct Biol 142(1):56-65.
20. Liu T, Chu B. 2002. Light-scattering by proteins. In Encyclopedia of surface and colloid science; Somasundaran P, Ed. 2nd ed. New York: Marcel Dekker, pp 3326-3346.
21. Hawe A, Sutter M, Jiskoot W. 2008. Extrinsic fluorescent dyes as tools for protein characterization. Pharm Res 25(7):1487-1499.
22. Brandau DT, Jones LS, Wiethoff CM, Rexroad J, Middaugh CR. 2003. Thermal stability of vaccines. J Pharm Sci 92(2):218-231.
23. Kelly SM, Price NC. 2000. The use of circular dichroism in the investigation of protein structure and function. Curr Protein Pept Sci 1(4):349-384.
24. Johnson WC. 1990. Protein secondary structure and circular dichroism: A practical guide. Proteins 7(3):205-214.
25. Strickland EH. 1974. Aromatic contributions to circular dichroism spectra of proteins. CRC Crit Rev Biochem 2(1):113-175.
26. Kelly SM, Jess TJ, Price NC. 2005. How to study proteins by circular dichroism. Biochim Biophys Acta 1751(2):119-139.
27. Semisotnov GV, Rodionova NA, Razgulyaev OI, Uversky VN, Gripas AF, Gilmanshin RI. 1991. Study of the molten globule intermediate state in protein folding by a hydrophobic fluorescent-probe. Biopolymers 31(1):119-128.
28. Dougherty DA. 1996. Cation-pi interactions in chemistry and biology: A new view of benzene, Phe, Tyr, and Trp. Science 271(5246):163-168.
29. Crowley PB, Golovin A. 2005. Cation-pi interactions in protein-protein interfaces. Proteins 59(2):231-239.
30. Ohtake S, Kita Y, Arakawa T. 2011. Interactions of formulation excipients with proteins in solution and in the dried state. Adv Drug Deliv Rev 63(13):1053-1073.
31. Miller R, Fainerman VB, Makievski AV, Kragel J, Grigoriev DO, Kazakov VN, Sinyachenko OV. 2000. Dynamics of protein and mixed protein/surfactant adsorption layers at the water/fluid interface. Adv Colloid Interface Sci 86(1-2):39-82.
32. Kamerzell TJ, Esfandiary R, Joshi SB, Middaugh CR, Volkin DB. 2011. Protein-excipient interactions: Mechanisms and biophysical characterization applied to protein formulation development. Adv Drug Deliv Rev 63(13):1118-1159.
33. Lee JC, Timasheff SN. 1981. The stabilization of proteins by sucrose. J Biol Chem 256(14):7193-7201.
34. Peek LJ, Brandau DT, Jones LS, Joshi SB, Middaugh CR. 2006. A systematic approach to stabilizing EBA-175 RII-NG for use as a malaria vaccine. Vaccine 24(31-32):5839-5851.
35. Barrett PN, Schober-Bendixen S, Ehrlich HJ. 2003. History of TBE vaccines. Vaccine 21 Suppl 1:S41-S49.
36. Hu L, Joshi SB, Liyanage MR, Pansalawatta M, Alderson MR, Tate A, Robertson G, Maisonneuve J, Volkin DB, Middaugh CR. 2013. Physical characterization and formulation development of a recombinant pneumolysoid protein-based pneumococcal vaccine. J Pharm Sci 102(2):387-400.
37. Evans RK, Nawrocki DK, Isopi LA, Williams DM, Casimiro DR, Chin S, Chen M, Zhu DM, Shiver JW, Volkin DB. 2004. Development of stable liquid formulations for adenovirus-based vaccines. J Pharm Sci 93(10):2458-2475.
38. Blanchard TG, Czinn SJ, Redline RW, Sigmund N, Harriman G, Nedrud JG. 1999. Antibody-independent protective mucosal immunity to gastric helicobacter infection in mice. Cell Immunol 191(1):74-80.
39. Ermak TH, Giannasca PJ, Nichols R, Myers GA, Nedrud J, Weltzin R, Lee CK, Kleanthous H, Monath TP. 1998. Immunization of mice with urease vaccine affords protection against Helicobacter pylori infection in the absence of antibodies and is mediated by MHC class II-restricted responses. J Exp Med 188(12):2277-2288.
40. P, Wilson J, Kosaka T, Wolowczuk I, Lee A. 2000. Therapeutic immunization against Helicobacter pylori infection in the absence of antibodies. Immunol Cell Biol 78(1):28-30.
41. Cuenca R, Blanchard TG, Czinn SJ, Nedrud JG, Monath TP, Lee CK, Redline RW. 1996. Therapeutic immunization against Helicobacter mustelae in naturally infected ferrets. Gastroenterology 110(6):1770-1775.
42. Gottwein JM, Blanchard TG, Targoni OS, Eisenberg JC, Zagorski BM, Redline RW, Nedrud JG, Tary-Lehmann M, Lehmann PV, Czinn SJ. 2001. Protective anti-Helicobacter immunity is induced with aluminum hydroxide or complete Freund's adjuvant by systemic immunization. J Infect Dis 184(3):308-314.
43. Guy B, Hessler C, Fourage S. 1997. Mucosal, systemic, or combined therapeutic immunizations in cynomolgus monkeys naturally infected with Gastrospirillum hominis-like organisms. Vaccine Res 6:141-150.
44. Guy B, Hessler C, Fourage S, Haensler J, Vialon-Lafay E, Rokbi B, Millet MJ. 1998. Systemic immunization with urease protects mice against Helicobacter pylori infection. Vaccine 16(8):850-856.
45. Lee CK, Soike K, Giannasca P, Hill J, Weltzin R, Kleanthous H, Blanchard J, Monath TP. 1999. Immunization of rhesus monkeys with a mucosal prime, parenteral boost strategy protects against infection with Helicobacter pylori. Vaccine 17(23-24):3072-3082.
46. Salnikova MS, Joshi SB, Rytting JH, Warny M, Middaugh CR. 2008. Preformulation studies of Clostridium difficile toxoids A and B. J Pharm Sci 97(10):4194-4207.
47. 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(14):13406-13414.
48. Peek LJ, Martin TT, Elk Nation C, Pegram SA, Middaugh CR. 2007. Effects of stabilizers on the destabilization of proteins upon adsorption to aluminum salt adjuvants. J Pharm Sci 96(3):547-557.
49. Sjokvist Ottsjo L, Flach CF, Clements J, Holmgren J, Raghavan S. 2013. A double mutant heat-labile toxin from Escherichia coli, LT(R192G/L211A), is an effective mucosal adjuvant for vaccination against Helicobacter pylori infection. Infect Immun 81(5):1532.
50. Norton EB, Lawson LB, Freytag LC, Clements JD. 2011. Characterization of a mutant Escherichia coli heat-labile toxin, LT(R192G/L211A), as a safe and effective oral adjuvant. Clin Vaccine Immunol 18(4):546-551.
51. Baldridge JR, Crane RT. 1999. Monophosphoryl lipid A (MPL) formulations for the next generation of vaccines. Methods 19(1):103-107.