Influence of carbohydrates on the stability and structure of a hyperglycosylated human interferon alpha mutein

Biochimie

Volumn 92, Issue 8, 2010, Pages 971-978

  Ceaglio, Natalia ^a   Etcheverrigaray, Marina ^a   Kratje, Ricardo ^a   Oggero, Marcos ^a  

^a UNIVERSIDAD NACIONAL DEL LITORAL   (Argentina)

Author keywords

Environmental stresses; Glycosylation engineering; Interferon alpha; Protein stability; Protein structure

Indexed keywords

ALPHA2B INTERFERON; CARBOHYDRATE; HYPERGLYCOSYLATED HUMAN INTERFERON ALPHA MUTEIN; RECOMBINANT HUMAN ALPHA2B INTERFERON; UNCLASSIFIED DRUG;

ACIDITY; ARTICLE; CIRCULAR DICHROISM; CYTOKINE RELEASE; DRUG ACTIVITY; DRUG SOLUBILITY; DRUG STABILITY; ENVIRONMENTAL STRESS; FREEZE THAWING; HEAT TREATMENT; IN VITRO STUDY; MELTING POINT; MICROCALORIMETRY; PH; PLASMA HALF LIFE; PRECIPITATION; PROTEIN DEGRADATION; PROTEIN GLYCOSYLATION; PROTEIN STABILITY; PROTEIN STRUCTURE; TEMPERATURE STRESS; THERMOSTABILITY; ULTRAVIOLET RADIATION;

BLOTTING, WESTERN; CALORIMETRY, DIFFERENTIAL SCANNING; CARBOHYDRATES; CIRCULAR DICHROISM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GLYCOSYLATION; HALF-LIFE; HUMANS; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; INTERFERON-ALPHA; PROTEIN CONFORMATION; SPECTROPHOTOMETRY, ULTRAVIOLET;

MUS;

EID: 77954657941     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2010.04.004     Document Type: Article

References (63)

1. Isaacs A., Lindenmann J. Virus interference I. The interferon. Proc. R. Soc. Lond. B Biol. Sci. 1957, 147:258-267.
2. Gresser I., Bourali C., Levy J.P., Fontaine-Brouty-Boye D., Thomas M.T. Increased survival in mice inoculated with tumor cells and treated with interferon preparations. Proc. Natl. Acad. Sci. U. S. A. 1969, 63:51-57.
3. Borden E.C., Lindner D., Dreicer R., Hussein M., Peereboom D. Second-generation interferon for cancer: clinical targets. Semin. Cancer Biol. 2000, 10:125-144.
4. Ferrantini M., Capone I., Belardelli F. Interferon-α and cancer: mechanisms of action and new perspectives of clinical use. Biochimie 2007, 89:884-893.
5. Gutterman J.U. Cytokine therapeutics: lessons from interferon α. Proc. Natl. Acad. Sci. U. S. A. 1994, 94:1198-1205.
6. Souvignet C., Lejeune O., Trepo C. Interferon-based treatment of chronic hepatitis C. Biochimie 2007, 89:894-898.
7. Bekisz J., Schmeisser H., Hernandez J., Goldman N., Zoon K. Human interferons alpha, beta and omega. Growth Factors 2004, 22(4):243-251.
8. Rachmawati H., Poelstra K., Beljaars L. The use of cytokines and modified cytokines as therapeutic agents: present state and future perspectives. Recent Research Development in Immunology 2004, vol. 6:191-214. Research Signpost, Kerala, India.
9. Ceaglio N., Etcheverrigaray M., Conradt H.S., Grammel N., Kratje R., Oggero M. Highly glycosylated human alpha interferon: an insight into a new therapeutic candidate. J. Biotechnol. 2010, 146:74-83.
10. Manning M.C., Patel K., Borchardt R.T. Stability of protein pharmaceuticals. Pharm. Res. 1989, 6:903-918.
11. Wang W. Instability, stabilization and formulation of liquid protein pharmaceuticals. Int. J. Pharm. 1999, 185:129-188.
12. Ruiz L., Reyes N., Duany L., Franco A., Aroche K., Rando E.H. Long-term stabilization of recombinant human interferon-α2b in aqueous solution without serum albumin. Int. J. Pharm. 2003, 264:57-72.
13. Hermeling S., Aranha L., Damen J.M., et al. Structural characterization and immunogenicity in wild-type and immune tolerant mice of degraded recombinant human interferon alpha 2b. Pharm. Res. 2005, 22(12):1997-2006.
14. Ruiz L., Reyes N., Aroche K., Báez R., Aldana R., Hardy E. Some factors affecting the stability of interferon alpha 2b in solution. Biologicals 2006, 34:15-19.
15. Ceaglio N., Etcheverrigaray M., Kratje R., Oggero M. Novel long-lasting interferon alpha derivatives designed by glycoengineering. Biochimie 2008, 90:437-449.
16. Familletti P.C., Rubinstein S., Petska S. A convenient and rapid cytopathic effect inhibition assay for interferon. Methods Enzymol. 1981, 78:387-394.
17. Rubinstein S., Familletti P.C., Pestka S. Convenient assay for interferons. J. Virol. 1981, 37(2):755-758.
18. 4. Nature 1970, 227:680-685.
19. Carpenter J.F., Kendrick B.S., Chang B.S., Manning M.C., Randolph T.W. Inhibition of stress-induced aggregation of protein therapeutics. Methods Enzymol. 1999, 309:237-255.
20. Arakawa T., Prestrelski S., Kenney W.C., Carpenter J.F. Factors affecting short-term and long-term stabilities of proteins. Adv. Drug Deliv. Rev. 1993, 10:1-28.
21. Wang C., Eufemi M., Turano C., Giartosio A. Influence of the carbohydrate moiety on the stability of glycoproteins. Biochemistry 1996, 35(23):7299-7307.
22. Solá R.J., Griebenow K. Effects of glycosylation on the stability of protein pharmaceuticals. J. Pharm. Sci. 2009, 98(4):1223-1245.
23. D. Shental-Bechor, Y. Levy, Effect of glycosylation on protein folding: a close look at thermodynamic stabilization, Proc. Natl. Acad. Sci. U. S. A. 105 (24) 8256-8261.
24. Fields G.B., Alonso D.O.V., Stigter D., Dill K.A. Theory for the aggregation of proteins and copolymers. J. Phys. Chem. 1992, 96:3974-3981.
25. Sharma V.K., Kalonia D.S. Temperature- and pH-induced multiple partially unfolded states of recombinant human interferon-α2a: possible implications in protein stability. Pharm. Res. 2003, 20(11):1721-1729.
26. Ip A.Y., Arakawa T., Silvers H., Ransone C.M., Niven R.W. Stability of recombinant consensus interferon to air-jet and ultrasonic nebulization. J. Pharm. Sci. 1995, 84(10):1210-1214.
27. Sinclair A.M., Elliott S. Glycoengineering: the effect of glycosylation on the properties of therapeutic proteins. J. Pharm. Sci. 2004, 94(8):1626-1635.
28. Tsuda E., Kawanishi G., Ueda M., Masuda S., Sasaki R. The role of carbohydrate in recombinant human erythropoietin. Eur. J. Biochem. 1990, 188:405-411.
29. Goochee C.F., Gramer M.J., Andersen D.C., Bahr J.B., Rasmussen J.R. The oligosaccharides of glycoproteins: factors affecting their synthesis and their influence on glycoprotein properties. Biotechnology 1992, 9:1347-1355.
30. Beldarraín A., Cruz Y., Cruz O., Navarro M., Gil M. Purification and conformational properties of a human interferon α2b produced in Escherichia coli. Biotechnol. Appl. Biochem. 2001, 33:173-182.
31. Dhalluin C., Ross A., Leuthold L., et al. Structural and biophysical characterization of the 40 kDa PEG-Interferon-α2a and its individual positional isomers. Bioconjug. Chem. 2005, 16:504-517.
32. Pestka S., Kelder B., Familletti P.C., Moscherai J.A., Crowl R., Kempner E.S. Molecular weight of the functional unit of human leukocyte, fibroblast, and immune interferons. J. Biol. Chem. 1983, 258(16):9706-9709.
33. Kontsek P., Borecký L., Novák M., Kontseková E., Máciková I., Krchnák V. Distinct effect of pH 2 on common antigenic structure found in human interferons-alpha 1 and -alpha 2 in the region 30-35. J. Interferon Res. 1991, 11(6):327-332.
34. Kúdela O., Kontseková E., Csabayová M., Záhorová K., Kontsek P. Conformational changes in pH 2-treated human interferon-alpha 2 detected with monoclonal antibodies. Hybridoma 1996, 15(3):185-189.
35. Pikal-Cleland K.A., Rodríguez-Hornedo N., Amidon G.L., Carpenter J.F. Protein denaturation during freezing and thawing in phosphate buffer systems: monomeric and tetrameric β-galactosidase. Arch. Biochem. Biophys. 2000, 384(2):398-406.
36. Lee E.N., Kim Y.M., Lee H.J., et al. Stabilizing peptide fusion for solving the stability and solubility problems of therapeutic proteins. Pharm. Res. 2005, 22(10):1735-1746.
37. Price N.C., Johnson C.M. Proteolytic Enzymes - a Practical Approach 1989, IRL Press, Oxford, UK.
38. Hubbard S.J. The structural aspects of limited proteolysis of native proteins. Biochim. Biophys. Acta 1998, 1382:191-206.
39. Fontana A., Polverino de Laureto P., Spolaore B., Frare E., Picotti P., Zambonin M. Probing protein structure by limited proteolysis. Acta Biochim. Pol. 2004, 51(2):299-321.
40. Parsell D.A., Sauer R.T. The structural stability of a protein is an important determinant of its proteolytic susceptibility in Escherichia coli. J. Biol. Chem. 1989, 264(13):7590-7595.
41. Lumbroso S., Wagschal A., Bourguet W., et al. A new mutation of the androgen receptor, P817A, causing partial androgen insensitivity syndrome: in vitro and structural analysis. J. Mol. Endocrinol. 2004, 32:679-688.
42. Kheterpal I., Williams A., Murphy C., Bledsoe B., Wetzel R. Structural features of the Aβ amyloid fibril elucidated by limited proteolysis. Biochemistry 2001, 40:11757-11767.
43. Kamath N., Karwowska-Desaulniers P., Pflum K.H. Limited proteolysis of human histone deacetylase 1. BMC Biochem. 2006, 7:22.
44. Manalavan P., Curtis Johnson W., Johnston P.D. Prediction structure type for human leukocyte interferon subtype A from circular dichroism. FEBS Lett. 1984, 175(2):227-230.
45. Voss T., Falkner E., Ahorn H., et al. Periplasmic expression of human interferon-α2c in Escherichia coli results in a correctly folded molecule. Biochem. J. 1994, 298:719-725.
46. Cindric M., Galic N., Vuletic M., Klaric M., Drevenkar V. Evaluation of recombinant human interferon α-2b structure and stability by in-gel tryptic digestion, H/D exchange and mass spectrometry. J. Pharm. Biomed. Anal. 2006, 40:781-787.
47. Marshall S.A., Lazar G.A., Chirino A.J., Desjarlais J.R. Rational design and engineering of therapeutic proteins. Drug Discov. Today 2003, 8(5):212-221.
48. Kosman J., Jonas A. Deletion of specific glycan chains affects differentially the stability, local structures, and activity of lecithin-cholesterol acyltransferase. J. Biol. Chem. 2001, 276(40):37230-37236.
49. Purohit S., Shao K., Balasubramanian S.V., Bahl O.P. Mutants of human choriogonadotropin lacking N-glycosyl chains in the α-subunit. 1. Mechanism for the differential action of the N-linked carbohydrates. Biochemistry 1997, 36:12355-12363.
50. Parkins D.A., Lashmar U.T. The formulation of biopharmaceutical products. PSST 2000, 3(4):129-137.
51. Braun A., Kwee L., Labow M.A., Alsenz J. Protein aggregates seem to play a key role among the parameters influencing the antigenicity of interferon alpha (IFN-alpha) in normal and transgenic mice. Pharm. Res. 1997, 14:1472-1478.
52. Schellekens H. Factors influencing the immunogenicity of therapeutic proteins. Nephrol. Dial. Transplant 2005, 20(Suppl. 6):vi3-vi9.
53. Maas C., Hermeling S., Bouma B., Jiskoot W., Gebbink M.F.B.G. A role for protein misfolding in immunogenicity of biopharmaceuticals. J. Biol. Chem. 2007, 282(4):2229-2236.
54. Lis H., Sharon N. Protein glycosylation. Structural and functional aspects. Eur. J. Biochem. 1993, 218:1-27.
55. Varki A. Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 1993, 3(29):97-130.
56. Rudd P.M., Joao H.C., Coghill E., et al. Glycoforms modify the dynamic stability and functional activity of an enzyme. Biochemistry 1994, 33(1):17-22.
57. Kim Y.M., Lee H.J., Lee J.E., Kim H.Y., Kim J. Expression of human interferon α-1 with enhanced stability via the tagging system of a stabilizing peptide. Protein Expr. Purif. 2009, 63:140-146.
58. Osborn B.L., Olsen H.S., Nardelli B., et al. Pharmacokinetic and pharmacodynamic studies of a human serum albumin-interferon-α fusion protein in cynomolgus monkeys. J. Pharmacol. Exp. Ther. 2002, 303(2):540-548.
59. Duttaroy A., Kanakaraj P., Osborn B.L., et al. Development of a long-acting insulin analog using albumin fusion technology. Diabetes 2005, 54(1):251-258.
60. Lo K., Zhang J., Sun Y., et al. Engineering a pharmacologically superior form of leptin for the treatment of obesity. Protein Eng. Des. Sel. 2005, 18(1):1-10.
61. Zhao H.L., Xue C., Wang Y., Sun B., Yao X.Q., Liu Z.M. Elimination of the free sulfhydryl group in the human serum albumin (HSA) moiety of human interferon-α2b and HSA fusion protein increases its stability against mechanical and thermal stresses. Eur. J. Pharm. Biopharm. 2009, 72:405-411.
62. Chennamsetty N., Voynov V., Kayser V., Helk B., Trout B.L. Design of therapeutic proteins with enhanced stability. PNAS 2009, 106(29):11937-11942.
63. Runkel L., Meier W., Pepinsky R.B., et al. Structural and functional differences between glycosylated and non-glycosylated forms of human interferon beta. Pharm. Res. 1998, 15(4):641-649.