Effects of sucrose and benzyl alcohol on GCSF conformational dynamics revealed by hydrogen deuterium exchange mass spectrometry

Journal of Pharmaceutical Sciences

Volumn 104, Issue 5, 2015, Pages 1592-1600

  Zhang, Jun ^a   Banks, Douglas D ^a   He, Feng ^a   Treuheit, Michael J ^a   Becker, Gerald W ^a  

^a AMGEN INC   (United States)

Author keywords

Excipients; Granulocyte colony stimulating factor; Hydrogen deuterium exchange; Mass spectrometry; Protein dynamics; Protein formulation

Indexed keywords

BENZYL ALCOHOL; DEUTERIUM; RECOMBINANT GRANULOCYTE COLONY STIMULATING FACTOR; SUCROSE; GRANULOCYTE COLONY STIMULATING FACTOR; RECOMBINANT PROTEIN;

ARTICLE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; DEUTERIUM HYDROGEN EXCHANGE; DRUG CONFORMATION; MICROBIAL GROWTH; MOLECULAR DYNAMICS; PH; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; TANDEM MASS SPECTROMETRY; THERMODYNAMICS; ULTRAVIOLET SPECTROSCOPY; CHEMISTRY; HUMAN; MASS SPECTROMETRY; METABOLISM; PROCEDURES; PROTEIN CONFORMATION; PROTEIN STABILITY;

BENZYL ALCOHOL; DEUTERIUM; DEUTERIUM EXCHANGE MEASUREMENT; GRANULOCYTE COLONY-STIMULATING FACTOR; HUMANS; MASS SPECTROMETRY; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SUCROSE;

EID: 84926662608     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.24384     Document Type: Article

References (43)

1. Frauenfelder H, Sligar SG, Wolynes PG. 1991. The energy landscapes and motions of proteins. Science 254(5038):1598-1603.
2. Vinson VJ. 2009. Proteins in motion. Introduction. Science 324(5924):197.
3. 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.
4. Zhang Z, Smith DL. 1993. Determination of amide hydrogen exchange by mass spectrometry: A new tool for protein structure elucidation. Protein Sci 2(4):522-531.
5. Wales TE, Engen JR. 2006. Hydrogen exchange mass spectrometry for the analysis of protein dynamics. Mass Spectrom Rev 25(1):158-170.
6. Bai Y, Milne JS, Mayne L, Englander SW. 1993. Primary structure effects on peptide group hydrogen exchange. Proteins 17(1):75-86.
7. Englander SW. 2006. Hydrogen exchange and mass spectrometry: A historical perspective. J Am Soc Mass Spectrom 17(11):1481-1489.
8. Kaltashov IA, Bobst CE, Abzalimov RR, Berkowitz SA, Houde D. 2010. Conformation and dynamics of biopharmaceuticals: Transition of mass spectrometry-based tools from academe to industry. J Am Soc Mass Spectrom 21(3):323-337.
9. Houde D, Peng Y, Berkowitz SA, Engen JR. 2010. Post-translational modifications differentially affect IgG1 conformation and receptor binding. Mol Cell Proteomics 9(8):1716-1728.
10. Tang L, Sundaram S, Zhang J, Carlson P, Matathia A, Parekh B, Zhou Q, Hsieh MC. 2013. Conformational characterization of the charge variants of a human IgG1 monoclonal antibody using H/D exchange mass spectrometry. mAbs 5(1):114-125.
11. Houde D, Berkowitz SA, Engen JR. 2011. The utility of hydrogen/deuterium exchange mass spectrometry in biopharmaceutical comparability studies. J Pharm Sci 100(6):2071-2086.
12. Majumdar R, Manikwar P, Hickey JM, Samra HS, Sathish HA, Bishop SM, Middaugh CR, Volkin DB, Weis DD. 2013. Effects of salts from the Hofmeister series on the conformational stability, aggregation propensity, and local flexibility of an IgG1 monoclonal antibody. Biochemistry 52(19):3376-3389.
13. Manikwar P, Majumdar R, Hickey JM, Thakkar SV, Samra HS, Sathish HA, Bishop SM, Middaugh CR, Weis DD, Volkin DB. 2013. Correlating excipient effects on conformational and storage stability of an IgG1 monoclonal antibody with local dynamics as measured by hydrogen/deuterium-exchange mass spectrometry. J Pharm Sci 102(7):2136-2151.
14. Metcalf D, Robb L, Dunn AR, Mifsud S, Di Rago L. 1996. Role of granulocyte-macrophage colony-stimulating factor and granulocyte colony-stimulating factor in the development of an acute neutrophil inflammatory response in mice. Blood 88(10):3755-3764.
15. Hill CP, Osslund TD, Eisenberg D. 1993. The structure of granulocyte-colony-stimulating factor and its relationship to other growth factors. Proc Natl Acad Sci USA 90(11):5167-5171.
16. Krishnan S, Chi EY, Webb JN, Chang BS, Shan D, Goldenberg M, Manning MC, Randolph TW, Carpenter JF. 2002. Aggregation of granulocyte colony stimulating factor under physiological conditions: Characterization and thermodynamic inhibition. Biochemistry 41(20):6422-6431.
17. Thirumangalathu R, Krishnan S, Brems DN, Randolph TW, Carpenter JF. 2006. Effects of pH, temperature, and sucrose on benzyl alcohol-induced aggregation of recombinant human granulocyte colony stimulating factor. J Pharm Sci 95(7):1480-1497.
18. Kendrick BS, Chang BS, Arakawa T, Peterson B, Randolph TW, Manning MC, Carpenter JF. 1997. Preferential exclusion of sucrose from recombinant interleukin-1 receptor antagonist: Role in restricted conformational mobility and compaction of native state. Proc Natl Acad Sci USA 94(22):11917-11922.
19. Zhang Y, Roy S, Jones LS, Krishnan S, Kerwin BA, Chang BS, Manning MC, Randolph TW, Carpenter JF. 2004. Mechanism for benzyl alcohol-induced aggregation of recombinant human interleukin-1 receptor antagonist in aqueous solution. J Pharm Sci 93(12):3076-3089.
20. Alford JR, Fowler AC, Wuttke DS, Kerwin BA, Latypov RF, Carpenter JF, Randolph TW. 2011. Effect of benzyl alcohol on recombinant human interleukin-1 receptor antagonist structure and hydrogen-deuterium exchange. J Pharm Sci 100(10):4215-4224.
21. Zhang Z, Zhang A, Xiao G. 2012. Improved protein hydrogen/deuterium exchange mass spectrometry platform with fully automated data processing. Anal Chem 84(11):4942-4949.
22. Wang L, Pan H, Smith DL. 2002. Hydrogen exchange-mass spectrometry: Optimization of digestion conditions. Mol Cell Proteomics 1(2):132-138.
23. Lapidus LJ. 2013. Understanding protein aggregation from the view of monomer dynamics. Mol Biosyst 9(1):29-35.
24. Thakkar SV, Kim JH, Samra HS, Sathish HA, Bishop SM, Joshi SB, Volkin DB, Middaugh CR. 2012. Local dynamics and their alteration by excipients modulate the global conformational stability of an lgG1 monoclonal antibody. J Pharm Sci 101(12):4444-4457.
25. Kamerzell TJ, Middaugh CR. 2007. Two-dimensional correlation spectroscopy reveals coupled immunoglobulin regions of differential flexibility that influence stability. Biochemistry 46(34):9762-9773.
26. Englander SW, Kallenbach NR. 1983. Hydrogen exchange and structural dynamics of proteins and nucleic acids. Q Rev Biophys 16(4):521-655.
27. Zink T, Ross A, Luers K, Cieslar C, Rudolph R, Holak TA. 1994. Structure and dynamics of the human granulocyte colony-stimulating factor determined by NMR spectroscopy. Loop mobility in a four-helix-bundle protein. Biochemistry 33(28):8453-8463.
28. Chetty PS, Mayne L, Lund-Katz S, Stranz D, Englander SW, Phillips MC. 2009. Helical structure and stability in human apolipoprotein A-I by hydrogen exchange and mass spectrometry. Proc Natl Acad Sci USA 106(45):19005-19010.
29. Lee JC, Timasheff SN. 1981. The stabilization of proteins by sucrose. J Biol Chem 256(14):7193-7201.
30. Coales SJ, E SY, Lee JE, Ma A, Morrow JA, Hamuro Y. 2010. Expansion of time window for mass spectrometric measurement of amide hydrogen/deuterium exchange reactions. Rapid Commun Mass Spectrom 24(24):3585-3592.
31. Goswami D, Devarakonda S, Chalmers MJ, Pascal BD, Spiegelman BM, Griffin PR. 2013. Time window expansion for HDX analysis of an intrinsically disordered protein. J Am Soc Mass Spectrom 24(10):1584-1592.
32. Banks DD, Zhang J, Siska CC. 2014. Relationship between native-state solubility and non-native aggregation of recombinant human granulocyte colony stimulating factor: Practical implications for protein therapeutic development. Mol Pharm 11(10):3431-3442.
33. Roy S, Katayama D, Dong A, Kerwin BA, Randolph TW, Carpenter JF. 2006. Temperature dependence of benzyl alcohol- and 8-anilinonaphthalene-1-sulfonate-induced aggregation of recombinant human interleukin-1 receptor antagonist. Biochemistry 45(12):3898-3911.
34. nd derivative absorbance spectroscopy of aromatic amino acids as a probe of protein dynamics. Protein Sci 18(12):2603-2614.
35. Timasheff SN. 1998. Control of protein stability and reactions by weakly interacting cosolvents: The simplicity of the complicated. Adv Protein Chem 51:355-432.
36. Arakawa T, Timasheff SN. 1982. Stabilization of protein structure by sugars. Biochemistry 21(25):6536-6544.
37. Raso SW, Abel J, Barnes JM, Maloney KM, Pipes G, Treuheit MJ, King J, Brems DN. 2005. Aggregation of granulocyte-colony stimulating factor in vitro involves a conformationally altered monomeric state. Protein Sci 14(9):2246-2257.
38. Bishop B, Koay DC, Sartorelli AC, Regan L. 2001. Reengineering granulocyte colony-stimulating factor for enhanced stability. J Biol Chem 276(36):33465-33470.
39. Hutchings RL, Singh SM, Cabello-Villegas J, Mallela KM. 2013. Effect of antimicrobial preservatives on partial protein unfolding and aggregation. J Pharm Sci 102(2):365-376.
40. Singh SM, Hutchings RL, Mallela KM. 2011. Mechanisms of m-cresol-induced protein aggregation studied using a model protein cytochrome c. J Pharm Sci 100(5):1679-1689.
41. Bis RL, Singh SM, Cabello-Villegas J, Mallela KM. 2014. Role of benzyl alcohol in the unfolding and aggregation of interferon alpha-2a. J Pharm Sci 104(2):407-415.
42. Wang A, Robertson AD, Bolen DW. 1995. Effects of a naturally occurring compatible osmolyte on the internal dynamics of ribonuclease A. Biochemistry 34(46):15096-15104.
43. Sheff JG, Rey M, Schriemer DC. 2013. Peptide-column interactions and their influence on back exchange rates in hydrogen/deuterium exchange-MS. J Am Soc Mass Spectrom 24(7):1006-1015.