Influence of methionine oxidation on the aggregation of recombinant human growth hormone

European Journal of Pharmaceutics and Biopharmaceutics

Volumn 85, Issue 1, 2013, Pages 42-52

  Mulinacci, Filippo ^a   Poirier, Emilie ^b   Capelle, Martinus A H ^b   Gurny, Robert ^a   Arvinte, Tudor ^a,b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b Therapeomic Inc   (Switzerland)

Author keywords

Aggregation; Freeze thawing; Human growth hormone; Methionine oxidation; Stability

Indexed keywords

BUFFER; FLUORESCENT DYE; HUMAN GROWTH HORMONE; METHIONINE;

ARTICLE; BIODEGRADATION; CHEMICAL MODIFICATION; FLUORESCENCE SPECTROSCOPY; FREEZE THAWING; GEL PERMEATION CHROMATOGRAPHY; HYDROPHOBICITY; IONIC STRENGTH; LIGHT SCATTERING; OXIDATION; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; THERMOSTABILITY;

1,8-ANS; 1-ANILINONAPHTHALENE-8-SULFONIC ACID; AGGREGATION; FREEZE/THAWING; HUMAN GROWTH HORMONE; METHIONINE OXIDATION; R-HGH; RECOMBINANT HUMAN GROWTH HORMONE; REVERSE PHASE HIGH PRESSURE LIQUID CHROMATOGRAPHY; ROOM TEMPERATURE; RP-HPLC; RT; SEC; SIZE EXCLUSION CHROMATOGRAPHY; STABILITY; ULTRAVIOLET-VISIBLE; UV-VIS;

COLD TEMPERATURE; DRUG STABILITY; DRUG STORAGE; HOT TEMPERATURE; HUMAN GROWTH HORMONE; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; METHIONINE; MICROSCOPY, FLUORESCENCE; MOLECULAR WEIGHT; NEPHELOMETRY AND TURBIDIMETRY; OXIDATION-REDUCTION; PARTICLE SIZE; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN STABILITY; RECOMBINANT PROTEINS; SOLUBILITY; SPECTROMETRY, FLUORESCENCE;

EID: 84883000780     PISSN: 09396411     EISSN: 18733441     Source Type: Journal    
DOI: 10.1016/j.ejpb.2013.03.015     Document Type: Article

References (50)

1. F. Mulinacci, S.E.J. Bell, M.A.H. Capelle, R. Gurny, and T. Arvinte Oxidized recombinant human growth hormone that maintains conformational integrity Journal of Pharmaceutical Sciences 100 2011 110 122
2. F. Mulinacci, M.A.H. Capelle, R. Gurny, A.F. Drake, and T. Arvinte Stability of human growth hormone: influence of methionine oxidation on thermal folding Journal of Pharmaceutical Sciences 100 2011 451 463
3. P.A.C. Cloos, and S. Christgau Non-enzymatic covalent modifications of proteins: mechanisms, physiological consequences and clinical applications Matrix Biology 21 2002 39 52
4. J.E. Visick, and S. Clarke Repair, refold, recycle - how bacteria can deal with spontaneous-damage and environmental-damage to proteins Molecular Microbiology 16 1995 835 845
5. C.M. Smales, D.S. Pepper, and D.C. James Protein modification during anti-viral heat-treatment bioprocessing of factor VIII concentrates, factor IX concentrates, and model proteins in the presence of sucrose Biotechnology and Bioengineering 77 2002 37 48
6. J.L. Cleland, M.F. Powell, and S.J. Shire The development of stable protein formulations - a close look at protein aggregation, deamidation, and oxidation Critical Reviews in Therapeutic Drug Carrier Systems 10 1993 307 377
7. M.L. Xie, D. Vandervelde, M. Morton, R.T. Borchardt, and R.L. Schowen PH-induced change in the rate-determining step for the hydrolysis of the Asp/Asn-derived cyclic-imide intermediate in protein degradation Journal of the American Chemical Society 118 1996 8955 8956
8. M.L. Xie, and R.L. Schowen Secondary structure and protein deamidation Journal of Pharmaceutical Sciences 88 1999 8 13
9. R. Thirumangalathu, S. Krishnan, P. Bondarenko, M. Speed-Ricci, T.W. Randolph, J.F. Carpenter, and D.N. Brems Oxidation of methionine residues in recombinant human interleukin-1 receptor antagonist: implications of conformational stability on protein oxidation kinetics Biochemistry 46 2007 6213 6224
10. W. Vogt Oxidation of methionyl residues in proteins - tools, targets, and reversal Free Radical Biology and Medicine 18 1995 93 105
11. J.E. Zull, S.K. Smith, and R. Wiltshire Effect of methionine oxidation and deletion of amino-terminal residues on the conformation of parathyroid-hormone - circular-dichroism studies Journal of Biological Chemistry 265 1990 5671 5676
12. C.B. Glaser, J. Morser, J.H. Clarke, E. Blasko, K. Mclean, I. Kuhn, R.J. Chang, J.H. Lin, L. Vilander, W.H. Andrews, and D.R. Light Oxidation of a specific methionine in thrombomodulin by activated neutrophil products blocks cofactor activity - a potential rapid mechanism for modulation of coagulation Journal of Clinical Investigation 90 1992 2565 2573
13. D. Liu, D. Ren, H. Huang, J. Dankberg, R. Rosenfeld, M.J. Cocco, L. Li, D.N. Brems, and R.L. Remmele Structure and stability changes of human IgG1 Fc as a consequence of methionine oxidation Biochemistry 47 2008 5088 5100
14. J.L. Liu, K.V. Lu, T. Eris, V. Katta, K.R. Westcott, L.O. Narhi, and H.S. Lu In vitro methionine oxidation of recombinant human leptin Pharmaceutical Research 15 1998 632 640
15. M.C. Gaudiano, M. Colone, C. Bombelli, P. Chistolini, L. Valvo, and M. Diociaiuti Early stages of salmon calcitonin aggregation: effect induced by ageing and oxidation processes in water and in the presence of model membranes Biochimica et Biophysica Acta - Proteins and Proteomics 1750 2005 134 145
16. L.C. Teh, L.J. Murphy, N.L. Huq, A.S. Surus, H.G. Friesen, L. Lazarus, and G.E. Chapman Methionine oxidation in human growth-hormone and human chorionic somatomammotropin - effects on receptor-binding and biological-activities Journal of Biological Chemistry 262 1987 6472 6477
17. G.W. Becker, R.M. Riggin, Derivative of Human Growth Hormone, US Patent 5068317, in: Eli Lilly and Company (Ed.), 208 ed., vol. 168, Indianapolis, USA, 1991.
18. S.M. Van Patten, E. Hanson, R. Bernasconi, K. Zhang, P. Manavalan, E.S. Cole, J.M. McPherson, and T. Edmunds Oxidation of methionine residues in antithrombin - effects on biological activity and heparin binding Journal of Biological Chemistry 274 1999 10268 10276
19. Somatropin, in: European Pharmacopoeia v6.4, 2008, pp. 2931-2937.
20. R.A. Houghten, C.B. Glaser, and C.H. Li Human somatotropin: reaction with hydrogen peroxide Archives of Biochemistry and Biophysics 178 1977 350 355
21. A.M. Devos, M. Ultsch, and A.A. Kossiakoff Human growth-hormone and extracellular domain of its receptor - crystal-structure of the complex Science 255 1992 306 312
22. G. Teshima, and E. Canovadavis Separation of oxidized human growth-hormone variants by reversed-phase high-performance liquid-chromatography - effect of mobile phase ph and organic modifier Journal of Chromatography 625 1992 207 215
23. B. Demeule, R. Gurny, and T. Arvinte Detection and characterization of protein aggregates by fluorescence microscopy International Journal of Pharmaceutics 329 2007 37 45
24. J.R. Lakowicz, and B.R. Masters Principles of fluorescence spectroscopy (Third Edition) Journal of Biomedical Optics 13 2008 029901 029902
25. M.R. Kasimova, S.M. Kristensen, P.W.A. Howe, T. Christensen, F. Matthiesen, J. Petersen, H.H. Sorensen, and J.J. Led NMR studies of the backbone flexibility and structure of human growth hormone: a comparison of high and low pH conformations Journal of Molecular Biology 318 2002 679 695
26. M.R. Defelippis, M.A. Kilcomons, M.P. Lents, K.M. Youngman, and H.A. Havel Acid stabilization of human growth-hormone equilibrium folding intermediates Biochimica et Biophysica Acta - Protein Structure and Molecular Enzymology 1247 1995 35 45
27. L. Dumery, F. Bourdel, Y. Soussan, A. Fialkowsky, S. Viale, P. Nicolas, and M. Reboud-Ravaux Beta-amyloid protein aggregation: its implication in the physiopathology of Alzheimer's disease Pathologie Biologie 49 2001 72 85
28. J. Avila Tau phosphorylation and aggregation in Alzheimer's disease pathology FEBS Letters 580 2006 2922 2927
29. M. Hashimoto, E. Rockenstein, L. Crews, and E. Masliah Role of protein aggregation in mitochondrial dysfunction and neurodegeneration in Alzheimer's and Parkinson's diseases Neuromolecular Medicine 4 2003 21 35
30. K.S.P. McNaught, and C.W. Olanow Protein aggregation in the pathogenesis of familial and sporadic Parkinson's disease Neurobiology of Aging 27 2006 530 545
31. S.B. Prusiner Molecular-biology of Prion diseases Science 252 1991 1515 1522
32. D. Shortle, H.S. Chan, and K.A. Dill Modeling the effects of mutations on the denatured states of proteins Protein Science 1 1992 201 215
33. S. Wicar, M.G. Mulkerrin, G. Bathory, L.H. Khundkar, and B.L. Karger Conformational-changes in the reversed-phase liquid-chromatography of recombinant human growth-hormone as a function of organic-solvent - the molten globule state Analytical Chemistry 66 1994 3908 3915
34. D.L. Sackett, and J. Wolff Nile Red as a polarity-sensitive fluorescent-probe of hydrophobic protein surfaces Analytical Biochemistry 167 1987 228 234
35. A. Hawe, M. Sutter, and W. Jiskoot Extrinsic fluorescent dyes as tools for protein characterization Pharmaceutical Research 25 2008 1487 1499
36. M.A.H. Capelle, R. Gurny, and T. Arvinte A high throughput protein formulation platform: case study of salmon calcitonin Pharmaceutical Research 26 2008 118 128
37. M. Sutter, S. Oliveira, N.N. Sanders, B. Lucas, A. van Hoek, M.A. Hink, A.J.W.G. Visser, S.C. De Smedt, W.E. Hennink, and W. Jiskoot Sensitive spectroscopic detection of large and denatured protein aggregates in solution by use of the fluorescent dye Nile red Journal of Fluorescence 17 2007 181 192
38. B.S. Bhatnagar, R.H. Bogner, and M.J. Pikal Protein stability during freezing: separation of stresses and mechanisms of protein stabilization Pharmaceutical Development and Technology 12 2007 505 523
39. C.F. Lopez, R.K. Darst, and P.J. Rossky Mechanistic elements of protein cold denaturation Journal of Physical Chemistry B 2008
40. K.A. Pikal-Cleland, J.L. Cleland, T.J. Anchordoquy, and J.F. Carpenter Effect of glycine on pH changes and protein stability during freeze-thawing in phosphate buffer systems Journal of Pharmaceutical Sciences 91 2002 1969 1979
41. P.L. Privalov Cold denaturation of proteins Critical Reviews in Biochemistry and Molecular Biology 25 1990 281 305
42. M.C. Heller, J.F. Carpenter, and T.W. Randolph Protein formulation and lyophilization cycle design: prevention of damage due to freeze-concentration induced phase separation Biotechnology and Bioengineering 63 1999 166 174
43. G. Gomez, M.J. Pikal, and N. Rodriguez-Hornedo Effect of initial buffer composition on pH changes during far-from-equilibrium freezing of sodium phosphate buffer solutions Pharmaceutical Research 18 2001 90 97
44. 2O Archives of Biochemistry and Biophysics 81 1959 319 329
45. B.M. Eckhardt, J.Q. Oeswein, and T.A. Bewley Effect of freezing on aggregation of human growth-hormone Pharmaceutical Research 8 1991 1360 1364
46. C. Frieden Protein aggregation processes: in search of the mechanism Protein Science 16 2007 2334 2344
47. E.Y. Chi, S. Krishnan, T.W. Randolph, and J.F. Carpenter Physical stability of proteins in aqueous solution: mechanism and driving forces in nonnative protein aggregation Pharmaceutical Research 20 2003 1325 1336
48. S.Y. Fung, C. Keyes, J. Duhamel, and P. Chen Concentration effect on the aggregation of a self-assembling oligopeptide Biophysical Journal 85 2003 537 548
49. H.C. Mahler, W. Friess, U. Grauschopf, and S. Kiese Protein aggregation: pathways, induction factors and analysis Journal of Pharmaceutical Sciences 98 2009 2909 2934
50. W. Wang Protein aggregation and its inhibition in biopharmaceutics International Journal of Pharmaceutics 289 2005 1 30