Stability of human growth hormone: Influence of methionine oxidation on thermal folding

Journal of Pharmaceutical Sciences

Volumn 100, Issue 2, 2011, Pages 451-463

  Mulinacci, Filippo ^a   A H Capelle, Martinus ^a   Gurny, Robert ^a   F Drake, Alex ^b   Arvinte, Tudor ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Calorimetry; Circular dichroism; Human growth hormone; Melting temperature; Oxidation; Spectroscopy; Stability; Thermal analysis

Indexed keywords

HUMAN GROWTH HORMONE; METHIONINE; RECOMBINANT GROWTH HORMONE;

ARTICLE; DRUG FORMULATION; IONIC STRENGTH; MELTING POINT; OXIDATION; PH; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; THERMOSTABILITY;

EID: 78650528867     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.22293     Document Type: Article

References (76)

1. Strobl JS, Thomas MJ. 1994. Human growth-hormone. Pharmacol Rev 46:1-34.
2. Zhan XQ, Giorgianni F, Desiderio DM. 2005. Proteomics analysis of growth hormone isoforms in the human pituitary. Proteomics 5:1228-1241.
3. Giorgianni F, Beranova-Giorgianni S, Desiderio DM. 2004. Identification and characterization of phosphorylated proteins in the human pituitary. Proteomics 4:587-598.
4. Garcia-Barros M, Costoya JA, Rios R, Arce VM, Devesa J. 2000. N-glycosylated variants of growth hormone in human pituitary extracts. Horm Res 53:40-45.
5. Haro LS, Lewis UJ, Garcia M, Bustamante J, Martinez AO, Ling NC. 1996. Glycosylated human growth hormone (hGH): A novel 24 kDa hGH-N variant. Biochem Biophys Res Commun 228:549-556.
6. Giustina A, Veldhuis JD. 1998. Pathophysiology of the neuroregulation of growth hormone secretion in experimental animals and the human. Endocr Rev. 19:717-797.
7. Sakharov DA, Thevis M, Tonevitsky AG. 2008. Analysis of major isoforms of human growth hormone before and after intensive physical exercise. Bull Exp Biol Med 146:466- 469.
8. Hindmarsh PC, Fall CHD, Pringle PJ, Osmond C, Brook CGD. 1997. Peak and trough growth hormone concentrations have different associations with the insulin-like growth factor axis, body composition, and metabolic parameters. J Clin Endocrinol Metab 82:2172-2176.
9. Veldhuis JD, Liem AY, South S, Weltman A, Weltman J, Clemmons DA, Abbott R, Mulligan T, Johnson ML, Pincus S. 1995. Differential impact of age, sex steroid hormones, and obesity on basal versus pulsatile growth hormone secretion in men as assessed in an ultrasensitive chemiluminescence assay. J Clin Endocrinol Metab 80:3209-3222.
10. Doga M, Bonadonna S, Gola M, Mazziotti G, Giustina A. 2006. Growth hormone deficiency in the adult. Pituitary 9:305-311.
11. Casanueva FF, Castro AI, Micic D, Kelestimur F, Dieguez C. 2009. New guidelines for the diagnosis of growth hormone deficiency in adults. Horm Res 71:112-115.
12. Schwenk WF. 2006. Growth hormone therapy-established uses in short children. Acta Paediatr 95:6-8.
13. Corpas E, Harman SM, Blackman MR. 1993. Human growth-hormone and human aging. Endocr Rev 14:20-39.
14. Bartke A, Brown-Borg HM, Bode AM, Carlson J, Hunter WS, Bronson RT. 1998. Does growth hormone prevent or accelerate aging? Exp Gerontol 33:675-687.
15. Burgess W, Liu Q, Zhou JH, Tang QS, Ozawa A, VanHoy R, Arkins S, Dantzer R, Kelley KW. 1999. The immune-endocrine loop during aging: Role of growth hormone and insulin-like growth factor-I. Neuroimmunomodulation 6:56-68.
16. Brown-Borg HM, Bode AM, Bartke A. 1999. Antioxidative mechanisms and plasma growth hormone levels-potential relationship in the aging process. Endocrine 11:41-48.
17. Lyle WG. 2002. Human growth hormone and anti-aging. Plast Reconstr Surg 110:1585-1589.
18. Mahmud K. 2003. Human growth hormone and aging. N Engl J Med 348:2256.
19. Vance ML. 2003. Retrospective-can growth hormone prevent aging? N Engl J Med 348:779-780.
20. Perls TT, Reisman NR, Olshansky SJ. 2005. Provision or distribution of growth hormone for "antiaging": Clinical and legal issues. JAMA 294:2086-2090.
21. Blackman MR. 2008. Use of growth hormone secretagogues to prevent or treat the effects of aging: Not yet ready for prime time. Ann Intern Med 149:677-679.
22. Melmed GY, Devlin SM, Vlotides G, Dhall D, Ross S, Yu R, Melvied S. 2008. Anti-aging therapy with human growth hormone associated with metastatic colon cancer in a patient with Crohn's colitis. Clin Gastroenterol Hepatol 6:360- 363.
23. Rudman D, Feller AG, Nagraj HS, Gergans GA, Lalitha PY, Goldberg AF, Schlenker RA, Cohn L, Rudman IW, Mattson DE. 1990. Effects of human growth-hormone in men over 60 years old. N Engl J Med 323:1-6.
24. Perls TT. 2004. Anti-aging quackery: Human growth hormone and tricks of the trade-more dangerous than ever. J Gerontol A Biol Sci Med Sci 59:682-691.
25. Reisman NR. 2004. Legal issues associated with the current and future practice of anti-aging medicine. J Gerontol A Biol Sci Med Sci 59:674-681.
26. Siddiqui NA, Nychis WG. 2007. Detention without physical examination of human growth hormone (hGH), also known as somatropin. FDA Import Alert 66-71.
27. 21 U.S.C.§ 333 (e)(f) 9a Prohibited distribution of human growth hormone.
28. La Merie Business Intelligence 2008. Competitor analysis: Human growth hormone (hGH). Barcelona:La Merie S.L.
29. Leitner VM, Guggi D, Krauland AH, Bernkop A. 2004. Nasal delivery of human growth hormone: in vitro and in vivo evaluation of a thiomer/glutathione microparticulate delivery system. J Control Release 100:87-95.
30. Il Choi W, Kim M, Tae G, Kim YH. 2008. Sustained release of human growth hormone from heparin-based hydrogel. Biomacromolecules 9:1698-1704.
31. Yoo HS. 2007. Photo-cross-linkable and thermo-responsive hydrogels containing chitosan and Pluronic for sustained release of human growth hormone (hGH). J Biomater Sci Polym Ed 18:1429-1441.
32. Bidlingmaier M, Kim J, Savoy C, Kim MJ, Ebrecht N, de la Motte S, Strasburger CJ. 2006. Comparative pharmacokinetics and pharmacodynamics of a new sustained-release growth hormone (GH), LB03002, versus daily GH in adults with GH deficiency. J Clin Endocrinol Metab 91:2926-2930.
33. Kim HK, Chung HJ, Park TG. 2006. Biodegradable polymeric microspheres with "open/closed" pores for sustained release of human growth hormone. J Control Release 112:167- 174.
34. Brodbeck KJ, Pushpala S, Mchugh AJ. 1999. Sustained release of human growth hormone from PLGA solution depots. Pharm Res 16:1825-1829.
35. Takada S, Yamagata Y, Misaki M, Taira K, Kurokawa T. 2003. Sustained release of human growth hormone from microcapsules prepared by a solvent evaporation technique. J Control Release 88:229-242.
36. Cleland JL, Powell MF, Shire SJ. 1993. The development of stable protein formulations-a close look at protein aggregation, deamidation, and oxidation. Crit Rev Ther Drug Carrier Syst 10:307-377.
37. Lai MC, Topp EM. 1999. Solid-state chemical stability of proteins and peptides. J Pharm Sci 88:489-500.
38. Manning MC, Patel K, Borchardt RT. 1989. Stability of protein pharmaceuticals. Pharm Res 6:903-918.
39. Maa YF, Hsu CC. 1996. Aggregation of recombinant human growth hormone induced by phenolic compounds. Int J Pharm 140:155-168.
40. Eckhardt BM, Oeswein JQ, Bewley TA. 1991. Effect of freezing on aggregation of human growth-hormone. Pharm Res 8:1360-1364.
41. Bam NB, Cleland JL, Yang J, Manning MC, Carpenter JF, Kelley RF, Randolph JW. 1998. Tween protects recombinant human growth hormone against agitation-induced damage via hydrophobic interactions. J Pharm Sci 87:1554-1559.
42. Tavornvipas S, Tajiri S, Hirayama F, Arima H, Uekama K. 2004. Effects of hydrophilic cyclodextrins on aggregation of recombinant human growth hormone. Pharm Res 21:2369-2376.
43. Battersby JE, Hancock WS, Canovadavis E, Oeswein J, Oconnor B. 1994. Diketopiperazine formation and N-terminal degradation in recombinant human growth-hormone. Int J Pept Protein Res 44:215-222.
44. Houghten RA, Glaser CB, Li CH. 1977. Human somatotropin: Reaction with hydrogen peroxide. Arch Biochem Biophys 178:350-355.
45. Teshima G, Canovadavis E. 1992. Separation of oxidized human growth-hormone variants by reversed-phase high-performance liquid-chromatography-effect of mobile phase pH and organic modifier. J Chromatogr 625:207-215.
46. Zhao F, GhezzoSchoneich E, Aced GI, Hong JY, Milby T, Schoneich C. 1997. Metal-catalyzed oxidation of histidine in human growth hormone-mechanism, isotope effects, and inhibition by a mild denaturing alcohol. J Biol Chem 272:9019-9029.
47. Chang SH, Teshima GM, Milby T, GilleceCastro B, Canovadavis E. 1997. Metal-catalyzed photooxidation of histidine in human growth hormone. Anal Biochem 244:221- 227.
48. Hovorka SW, Hong JY, Cleland JL, Schoneich C. 2001. Metal-catalyzed oxidation of human growth hormone: Modulation by solvent-induced changes of protein conformation. J Pharm Sci 90:58-69.
49. Hepner F, Cszasar E, Roitinger E, Lubec G. 2005. Mass spectrometrical analysis of recombinant human growth hormone (Genotropin(R)) reveals amino acid substitutions in 2% of the expressed protein. Proteome Sci 3:1.
50. Hepner F, Csaszar E, Roitinger E, Pollak A, Lubec G. 2006. Massspectrometrical analysis of recombinant human growth hormone Norditropin (R) reveals amino acid exchange at M14_V14 rhGH. Proteomics 6:775-784.
51. Jiang HT, Wu SL, Karger BL, Hancock WS. 2009. Mass spectrometric analysis of innovator, counterfeit, and follow-on recombinant human growth hormone. Biotechnol Prog 25:207-218.
52. Jespersen AM, Christensen T, Klausen NK, Nielsen PF, Sorensen HH. 1994. Characterization of A trisulfide derivative of biosynthetic human growth-hormone produced in Escherichia-coli. Eur J Biochem 219:365-373.
53. Mulinacci F, Bell SEJ, Capelle MAH, Gurny R, Arvinte T. 2010. Oxidized recombinant human growth hormone that maintains conformational integrity. J Pharm Sci 10.1002/jps.22268
54. Karlsson G, Gellerfors P, Persson A, Noren B, Edlund PO, Sandberg C, Birnbaum S. 1999. Separation of oxidized and deamidated human growth hormone variants by isocratic reversed-phase high-performance liquid chromatography. J Chromatogr A 855:147-155.
55. Teh LC, Murphy LJ, Huq NL, Surus AS, Friesen HG, Lazarus L, Chapman GE. 1987. Methionine oxidation in human growth-hormone and human chorionic somatomammotropin-effects on receptor-binding and biological-activities. J Biol Chem 262:6472-6477.
56. Greenfield NJ. 2006. Using circular dichroism collected as a function of temperature to determine the thermodynamics of protein unfolding and binding interactions. Nat Protoc 1:2527-2535.
57. Pace CN, McGrath T. 1980. Substrate stabilization of lysozyme to thermal and guanidine-hydrochloride denaturation. J Biol Chem 255:3862-3865.
58. Yadav S, Ahmad F. 2000. A new method for the determination of stability parameters of proteins from their heat-induced denaturation curves. Anal Biochem 283:207-213.
59. Idicula-Thomas S, Balaji PV. 2007. Protein aggregation: A perspective from amyloid and inclusion-body formation. Curr Sci 92:758-767.
60. Rosenberg AS. 2006. Effects of protein aggregates: An immunologic perspective. AAPS J 8:E501-E507.
61. Carpenter JF, Randolph TW, Jiskoot W, Crommelin DJA, Middaugh CR, Winter G, Fan YX, Kirshner S, Verthelyi D, Kozlowski S, Clouse KA, Swann PG, Rosenberg A, Cherney B. 2009. Overlooking subvisible particles in therapeutic protein products: Gaps that may compromise product quality. J Pharm Sci 98:1201-1205.
62. Baglioni S, Casamenti F, Bucciantini M, Luheshi LM, Taddei N, Chiti F, Dobson CM, Stefani M. 2006. Prefibrillar amyloid aggregates could be generic toxins in higher organisms. J Neurosci 26:8160-8167.
63. Mirzaei H, Regnier F. 2008. Protein Protein aggregation induced by protein oxidation. J Chromatogr B Analyt Technol Biomed Life Sci 873:8-14.
64. Jayaraman S, Gantz DL, Gursky O. 2008. Effects of protein oxidation on the structure and stability of model discoidal high-density lipoproteins. Biochem 47:3875-3882.
65. Gao J, Yin DH, Yao YH, Sun HY, Qin ZH, Schoneich C, Williams TD, Squier TC. 1998. Loss of conformational stability in calmodulin upon methionine oxidation. Biophys J 74:1115-1134.
66. Wood MJ, Prieto JH, Komives EA. 2005. Structural and functional consequences of methionine oxidation in thrombomodulin. Biochim Biophys Acta 1703:141-147.
67. Gaza-Bulseco G, Faidu S, Hurkmans K, Chumsae C, Liu HC. 2008. Effect of methionine oxidation of a recombinant monoclonal antibody on the binding affinity to protein A and protein G. J Chromatogr B Analyt Technol Biomed Life Sci 870:55-62.
68. Chumsae C, Gaza-Bulseco G, Sun J, Liu H. 2007. Comparison of methionine oxidation in thermal stability and chemically stressed samples of a fully human monoclonal antibody. J Chromatogr B 850:285-294.
69. Turner C, Cary PD, Grego B, Hearn MTW, Chapman GE. 1983. A proton-nuclear-magnetic-resonance study of human somatotropin (growth-hormone)-assignment and properties of the histidine-residues. Biochem J 213:107-113.
70. Kasimova MR, Kristensen SM, Howe PWA, Christensen T, Matthiesen F, Petersen J, Sorensen HH, Led JJ. 2002. NMR studies of the backbone flexibility and structure of human growth hormone: A comparison of high and low pH conformations. J Mol Biol 318:679-695.
71. Abildgaard F, Jorgensen AMM, Led JJ, Christensen T, Jensen EB, Junker F, Dalboge H. 1992. Characterization of tertiary interactions in A folded protein by NMR methods-studies of pH-induced structural-changes in human growth-hormone. Biochemistry 31:8587-8596.
72. Gomez-Orellana I, Variano B, Miura-Fraboni J, Milstein S, Paton DR. 1998. Thermodynamic characterization of an intermediate state of human growth hormone. Protein Sci 7:1352-1358.
73. Claudy P, Letoffe JM, Bayol A, Bonnet MC, Maurizot JC. 1992. Denaturation versus pH of lysozyme and biosynthetic human growth-hormone by differential scanning calorimetry and circular-dichroism-a comparative-study. Thermochim Acta 207:227-237.
74. Chan HS, Bromberg S, Dill KA. 1995. Models of cooperativity in protein-folding. Philos Trans R Soc Lond B Biol Sci 348:61-70.
75. Zhou HX. 2005. Interactions of macromolecules with salt ions: An electrostatic theory for the Hofmeister effect. Proteins 61:69-78.
76. Creighton T. 1992. Proteins: Structures and molecular properties. New York: W. H. Freeman.