Biophysical characterisation of thermal-induced precipitates of recombinant anthrax protective antigen: Evidence for kinetically trapped unfolding domains in solid-state

European Journal of Pharmaceutics and Biopharmaceutics

Volumn 82, Issue 3, 2012, Pages 475-484

  Ganesan, Ashok ^a   Watkinson, Allan ^b,d   Moore, Barry D ^a,c  

^a XstalBio Ltd   (United Kingdom)

^b PharmAthene UK Ltd   (United Kingdom)

^c UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^d GSB Pharma Consultants Ltd   (United Kingdom)

Author keywords

Anthrax protective antigen; Circular dichroism; Differential scanning calorimetry; Fluorescence; Infrared; Protein aggregation

Indexed keywords

ANTHRAX VACCINE;

ARTICLE; BACILLUS ANTHRACIS; BIOPHYSICS; CIRCULAR DICHROISM; DIFFERENTIAL SCANNING CALORIMETRY; DRUG FORMULATION; PRECIPITATION; PROTEIN AGGREGATION; PROTEIN STABILITY; PROTEIN UNFOLDING; SOLID STATE;

ANTIGENS, BACTERIAL; BACTERIAL TOXINS; CHEMICAL PRECIPITATION; CIRCULAR DICHROISM; HOT TEMPERATURE; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS;

EID: 84870501377     PISSN: 09396411     EISSN: 18733441     Source Type: Journal    
DOI: 10.1016/j.ejpb.2012.05.019     Document Type: Article

References (45)

1. S. Frokjaer, and D.E. Otzen Protein drug stability: a formulation challenge Nat. Rev. Drug Discov. 4 2005 298 306
2. H.-C. Mahler, W. Friess, U. Grauschopf, and S. Kiese Protein aggregation: pathways, induction factors and analysis J. Pharm. Sci. 98 2009 2909 2934
3. H. Schellekens Factors influencing the immunogenicity of therapeutic proteins Nephrol. Dial. Transplant. 6 2005 3 9
4. O.C. Tatford, P.T. Gomme, and J. Bertolini Analytical techniques for the evaluation of liquid protein therapeutics Biotechnol. Appl. Biochem. 40 2004 67 81
5. H. Mach, and T. Arvinte Addressing new analytical challenges in protein formulation development Eur. J. Pharm. Biopharm. 78 2011 196 207
6. J.P. den Engelsman, Garidel, R. Smulders, H. Koll, B. Smith, S. Bassarab, A. Seidl, O. Hainzl, and W. Jiskoot Strategies for the assessment of protein aggregates in pharmaceutical biotech product development Pharm. Res. 28 2011 920 933
7. A. Maarschalkerweerd, A. Wolbink, S.O. Stapel, W. Jiskoot, and A. Hawe Comparison of analytical methods to detect instability of etanercept during thermal stress testing Eur. J. Pharm. Biopharm. 78 2011 213 221
8. P.O. Souillac Biophysical characterization of insoluble aggregates of a multi-domain protein: an insight into the role of the various domains J. Pharm. Sci. 94 2005 2070 2083
9. L.L. Chang, and M.J. Pikal Mechanisms of protein stabilization in the solid state J. Pharm. Sci. 98 2009 2886 28908
10. Z.Q. Wen Raman spectroscopy of protein pharmaceuticals J. Pharm. Sci. 96 2007 2861 2878
11. A. Hawe, M. Sutter, and W. Jiskoot Extrinsic fluorescent dyes as tools for protein characterization Pharm. Res. 25 2008 1487 1499
12. A. Ganesan, N.C. Price, S.M. Kelly, I. Petry, B.D. Moore, and P.J. Halling Circular dichroism studies of subtilisin Carlsberg immobilised on micron sized silica particles Biochim. Biophys. Acta 1764 2006 1119 1125
13. A. Ganesan, B.D. Moore, S.M. Kelly, N.C. Price, O.J. Rolinski, D.J.S. Birch, I.R. Dunkin, and P.J. Halling Optical spectroscopic methods for probing the conformational stability of immobilised enzymes Chemphyschem 10 2009 1492 1499
14. C. Petosa, R.J. Collier, K.R. Klimpel, S.H. Leppla, and R.C. Liddington Crystal structure of the anthrax toxin protective antigen Nature 385 1997 833 838
15. R.J. Collier Membrane translocation by anthrax toxin Mol. Aspects Med. 30 2009 413 422
16. R.N. Brey Molecular basis for improved anthrax vaccines Adv. Drug Deliv. Rev. 57 2005 1266 1292
17. S. Singh, A. Singh, M.A. Aziz, S.M. Waheed, R. Bhat, and R. Bhatnagar Thermal inactivation of protective antigen of Bacillus anthracis and its prevention by polyol osmolytes Biochem. Biophys. Res. Commun. 322 2004 1029 1037
18. G. Jiang, S.B. Joshi, L.J. Peek, D.T. Brandau, J. Huang, M.S. Ferriter, W.D. Woodley, B.M. Ford, K.D. Mar, J.A. Mikszta, C.R. Hwang, R. Ulrich, N.G. Harvey, C.R. Middaugh, and V.J. Sullivan Anthrax vaccine powder formulations for nasal mucosal delivery J. Pharm. Sci. 95 2006 80 96
19. D.A. Chalton, I.F. Kelly, A. McGregor, H. Ridley, A. Watkinson, J. Miller, and J.H. Lakey Unfolding transitions of Bacillus anthracis protective antigen Arch. Biochem. Biophys. 465 2007 1 10
20. A.M. Fernandez-Escamilla, F. Rousseau, J. Schymkowitz, and L. Serrano Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins Nat. Biotechnol. 22 2004 1302 1306
21. E.D. Williamson, I. Hodgson, N.J. Walker, A.W. Topping, M.G. Duchars, J.M. Mott, J. Estep, C. LeButt, H.C. Flick-Smith, H.E. Jones, H. Li, and C.P. Quinn Immunogenicity of recombinant protective antigen and efficacy against aerosol challenge with anthrax Infect. Immun. 73 2005 5978 5987
22. F. Weber, and M. Hayer-Hartl Prevention of rhodanese aggregation by the chaperonin GroEL C. Schneider, Methods in Molecular Biology, Chaperonin Protocols vol. 140 2000 Humana Press Inc. Totowa, NJ 111 115
23. H.C. Mahler, R. Muller, W. Frieβ, A. Delille, and S. Matheus Induction and analysis of aggregates in a liquid IgG1-antibody formation Eur. J. Pharm. Biopharm. 59 2005 407 417
24. M.R.H. Krebs, E.H.C. Bromley, and A.M. Donald The binding of thioflavin-T to amyloid fibrils: localisation and implications J. Struct. Biol. 149 2005 30 37
25. S.Y. Venyaminov, and J.T. Yang Determination of protein secondary structure G.D. Fasman, Circular Dichroism and the Conformational Analysis of Biomolecules 1996 Plenum Press New York 69 108
26. N. Sreerama, and R.W. Woody Poly(pro)II helices in globular proteins: identification and circular dichroic analysis Biochemistry 33 1994 10022 10025
27. Z. Shi, K. Chen, Z. Liu, and N.R. Kallenbach Conformation of the backbone in unfolded proteins Chem. Rev. 106 2006 1877 1897
28. S.M. Kelly, T.J. Jess, and N.C. Price How to study proteins by circular dichroism Biochim. Biophys. Acta 1751 2005 119 139
29. C.A. Royer Probing protein folding and conformational transitions with fluorescence Chem. Rev. 106 2006 1769 1784
30. X. Wang, S.K. Singh, and S. Kumar Potential aggregation-prone regions in complementarity-determining regions of antibodies and their contribution towards antigen recognition: a computational analysis Pharm. Res. 27 2010 1512 1529
31. J. Xu, J. Reumers, J.R. Couceiro, F. De Smet, R. Gallardo, S. Rudyak, A. Cornelis, J. Rozenski, A. Zwolinska, J.C. Marine, D. Lambrechts, Y.A. Suh, F. Rousseau, and J. Schymkowitz Gain of function of mutant p53 by coaggregation with multiple tumor suppressors Nat. Chem. Biol. 7 2011 285 295
32. J. Zurdo, J.I. Guijarro, and C.M. Dobson Preparation and characterization of purified amyloid fibrils J. Am. Chem. Soc. 123 2001 8141 8142
33. M.R. Krebs, G.L. Devlin, and A.M. Donald Protein particulates: another generic form of protein aggregation? Biophys. J. 92 2007 1336 1342
34. E.W. Blanch, L.A. Morozova-Roche, D.A.E. Cochran, A.J. Doig, L. Hect, and L.D. Barron Is polyproline II helix the killer conformation? A Raman optical activity study of the amyloidogenic prefibrillar intermediate of human lysozyme J. Mol. Biol. 301 2000 553 563
35. C. Maas, S. Hermeling, B. Bouma, W. Jiskoot, and M.F. Gebbink A role for protein misfolding in immunogenicity of biopharmaceuticals J. Biol. Chem. 282 2007 2229 2236
36. M. Fandrich, M.A. Fletcher, and C.M. Dobson Amyloid fibrils from muscle myoglobin Nature 410 2001 165 166
37. F. Chiti, and C.M. Dobson Amyloid formation by globular proteins under native conditions Nat. Chem. Biol. 5 2009 15 22
38. M. Zhu, S. Han, F. Zhou, S.A. Carter, and A.L. Fink Annular oligomeric amyloid intermediates observed by in situ atomic force microscopy J. Biol. Chem. 273 2004 24452 24459
39. M.K. Joubert, Q. Luo, Y. Nashed-Samuel, J. Wypych, and L.O. Narhi Classification and characterization of therapeutic antibody aggregates J. Biol. Chem. 286 2011 25118 25133
40. R.M. Bhaskara, and N. Srinivasan Stability of domain structures in multi-domain proteins Sci. Rep. 1 2011 40 doi:10.1038/srep00040
41. P.K. Gupta, H. Chandra, R. Gaur, R.K. Kurupati, S. Chowdhury, V. Tandon, Y. Singh, and K. Maithal Conformational fluctuations in anthrax protective antigen: a possible role of calcium in the folding pathway of the protein FEBS Lett. 554 2003 505 510
42. S. Gao-Sheridan, S. Zhang, and R.J. Collier Exchange characteristics of calcium ions bound to anthrax protective antigen Biochem. Biophys. Res. Commun. 300 2003 61 64
43. J. Mogridge, M. Mourez, and R.J. Collier Involvement of domain 3 in oligomerization by the protective antigen moiety of anthrax toxin J. Bacteriol. 183 2003 2111 2116
44. E. Santelli, L.A. Bankston, S.H. Leppla, and R.C. Liddington Crystal structure of a complex between anthrax toxin and its host cell receptor Nature 430 2004 905 908
45. A.S. Williams, S. Lovell, A. Anbanandam, R. El-Chami, and J.G. Bann Domain 4 of the anthrax protective antigen maintains structure and binding to the host receptor CMG2 at low pH Protein Sci. 18 2009 2277 2286