Identification of oxidation sites and covalent cross-links in metal catalyzed oxidized interferon beta-1a: Potential implications for protein aggregation and immunogenicity

Molecular Pharmaceutics

Volumn 10, Issue 6, 2013, Pages 2311-2322

  Torosantucci, Riccardo ^a,b   Sharov, Victor S ^b   Van Beers, Miranda ^c   Brinks, Vera ^d   Schöneich, Christian ^b   Jiskoot, Wim ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF KANSAS   (United States)

^c AGENCY FOR SCIENCE   (Singapore)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

covalent aggregation; Cu2+ ascorbate; IFN 1a; immunogenicity; metal catalyzed oxidation; tyrosine oxidation products

Indexed keywords

BETA1A INTERFERON; COPPER; DISULFIDE; HISTIDINE; METHIONINE; PHENYLALANINE; SCHIFF BASE; TRYPTOPHAN; TYROSINE;

ADDITION REACTION; ALKYLATION; ARTICLE; CATALYSIS; CIRCULAR DICHROISM; CONTROLLED STUDY; CROSS LINKING; DERIVATIZATION; ELECTROSPRAY MASS SPECTROMETRY; FLUORESCENCE SPECTROSCOPY; GEL PERMEATION CHROMATOGRAPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOGENICITY; OXIDATION; PRIORITY JOURNAL; PROTEIN AGGREGATION;

ASCORBIC ACID; BENZENE DERIVATIVES; CHROMATOGRAPHY, GEL; CIRCULAR DICHROISM; COPPER; HUMANS; INTERFERON-BETA; METHYLAMINES; MOLECULAR STRUCTURE; SPECTROMETRY, FLUORESCENCE; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 84878643485     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp300665u     Document Type: Article

References (51)

1. Kaynor, C.; Xin, M.; Wakefield, J.; Barsoum, J.; Qin, X. Q. Direct evidence that IFN-beta functions as a tumor-suppressor protein J. Interferon Cytokine Res. 2002, 22, 1089-1098
2. Calabresi, P. A. Diagnosis and management of multiple sclerosis Am. Fam. Physician. 2004, 70, 1935-1944
3. Runkel, L.; Meier, W.; Pepinsky, R. B.; Karpusas, M.; Whitty, A.; Kimball, K.; Brickelmaier, M.; Muldowney, C.; Jones, W.; Goelz, S. E. Structural and functional differences between glycosylated and non-glycosylated forms of human interferon-beta (IFN-beta) Pharm. Res. 1998, 15, 641-649
4. Nelissen, I.; Martens, E.; Van Den Steen, P. E.; Proost, P.; Ronsse, I.; Opdenakker., G. Gelatinase B/matrix metalloproteinase-9 cleaves interferon-beta and is a target for immunotherapy Brain 2003, 126, 1371-1381
5. Kagawa, Y.; Takasaki, S.; Utsumi, J.; Hosoi, K.; Shimizu, H.; Kochibe, N.; Kobata, A. Comparative-Study of the Asparagine-Linked Sugar Chains of Natural Human Interferon-Beta-1 and Recombinant Human Interferon-Beta-1 Produced by 3 Different Mammalian-Cells J. Biol. Chem. 1988, 263, 17508-17515
6. Conradt, H. S.; Egge, H.; Peter-Katalinic, J.; Reiser, W.; Siklosi, T.; Schaper, K. Structure of the carbohydrate moiety of human interferon-beta secreted by a recombinant Chinese hamster ovary cell line J. Biol. Chem. 1987, 262, 14600-14605
7. Karpusas, M.; Nolte, M.; Benton, C. B.; Meier, W.; Lipscomb, W. N.; Goelz., S. The crystal structure of human interferon beta at 2.2-angstrom resolution Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 11813-11818
8. van Beers, M. M.; Sauerborn, M.; Gilli, F.; Brinks, V.; Schellekens, H.; Jiskoot, W. Oxidized and aggregated recombinant human interferon beta is immunogenic in human interferon beta transgenic mice Pharm. Res. 2011, 28, 2393-2402
9. van Beers, M. M.; Sauerborn, M.; Gilli, F.; Brinks, V.; Schellekens, H.; Jiskoot, W. Aggregated recombinant human interferon Beta induces antibodies but no memory in immune-tolerant transgenic mice Pharm. Res. 2010, 27, 1812-1824
10. Rifkin, R. A.; Maggio, E. T.; Dike, S.; Kerr, D. A.; Levy, M. n-Dodecyl-beta-d-Maltoside Inhibits Aggregation of Human Interferon-beta-1b and Reduces Its Immunogenicity J. Neuroimmune Pharmacol. 2011, 6, 158-162
11. Seefeldt, M. B.; Rosendahl, M. S.; Cleland, J. L.; Hesterberg, L. K. Application of high hydrostatic pressure to dissociate aggregates and refold proteins Curr. Pharm. Biotechnol. 2009, 10, 447-455
12. Bertolotto, A.; Malucchi, S.; Sala, A.; Orefice, G.; Carrieri, P. B.; Capobianco, M.; Milano, E.; Melis, F.; Giordana, M. T. Differential effects of three interferon betas on neutralising antibodies in patients with multiple sclerosis: a follow up study in an independent laboratory J. Neurol., Neurosurg. Psychiatry 2002, 73, 148-153
13. Scagnolari, C.; Bellomi, F.; Turriziani, O.; Bagnato, F.; Tomassini, V.; Lavolpe, V.; Ruggieri, M.; Bruschi, F.; Meucci, G.; Dicuonzo, G.; Antonelli, G. Neutralizing and binding antibodies to IFN-beta: relative frequency in relapsing-remitting multiple sclerosis patients treated with different IFN-beta preparations J. Interferon Cytokine Res. 2002, 22, 207-213
14. Hermeling, S.; Aranha, L.; Damen, J. M. A.; Slijper, M.; Schellekens, H.; Crommelin, D. J. A.; Jiskoot, W. Structural characterization and immunogenicity in wild-type and immune tolerant mice of degraded recombinant human interferon alpha2b Pharm. Res. 2005, 22, 1997-2006
15. Hermeling, S.; Schellekens, H.; Maas, C.; Gebbink, M. F.; Crommelin, D. J.; Jiskoot, W. Antibody response to aggregated human interferon alpha2b in wild-type and transgenic immune tolerant mice depends on type and level of aggregation J. Pharm. Sci. 2006, 95, 1084-1096
16. Filipe, V.; Jiskoot, W.; Basmeleh, A. H.; Halim, A.; Schellekens, H. Immunogenicity of different stressed IgG monoclonal antibody formulations in immune tolerant transgenic mice mAbs 2012, 4, 740-752
17. Torosantucci, R.; Mozziconacci, O.; Sharov, V.; Schöneich, C.; Jiskoot, W. Chemical Modifications in Aggregates of Recombinant Human Insulin Induced by Metal-Catalyzed Oxidation: Covalent Cross-Linking via Michael Addition to Tyrosine Oxidation Products Pharm. Res. 2012, 29, 2276-2293
18. Gallo-Rodriguez, C.; Ji, X. D.; Melman, N.; Siegman, B. D.; Sanders, L. H.; Orlina, J.; Fischer, B.; Pu, Q.; Olah, M. E.; van Galen, P. J. Structure-activity relationships of N6-benzyladenosine-5′-uronamides as A3-selective adenosine agonists J. Med. Chem. 1994, 37, 636-646
19. Torosantucci, R.; Kukrer, B.; Mero, A.; Van Winsen, M.; Tantipolphan, R.; Jiskoot., W. Plain and mono-pegylated recombinant human insulin exhibit similar stress-induced aggregation profiles J. Pharm. Sci. 2011, 100, 2574-2585
20. Giulivi, C.; Davies., K. J. Dityrosine: a marker for oxidatively modified proteins and selective proteolysis Methods. Enzymol. 1994, 233, 363-371
21. Ikehata, K.; Duzhak, T. G.; Galeva, N. A.; Ji, T.; Koen, Y. M.; Hanzlik, R. P. Protein targets of reactive metabolites of thiobenzamide in rat liver in vivo Chem. Res. Toxicol. 2008, 21, 1432-1442
22. Xu, H.; Freitas., M. A. A mass accuracy sensitive probability based scoring algorithm for database searching of tandem mass spectrometry data BMC Bioinf. 2007, 8, 133
23. Xu, H.; Freitas., M. A. MassMatrix: a database search program for rapid characterization of proteins and peptides from tandem mass spectrometry data Proteomics 2009, 9, 1548-1555
24. Xu, H.; Yang, L.; Freitas., M. A. A robust linear regression based algorithm for automated evaluation of peptide identifications from shotgun proteomics by use of reversed-phase liquid chromatography retention time BMC Bioinf. 2008, 9, 347
25. Xu, H.; Zhang, L.; Freitas, M. A. Identification and characterization of disulfide bonds in proteins and peptides from tandem MS data by use of the MassMatrix MS/MS search engine J. Proteome Res. 2008, 7, 138-144
26. Paizs, B.; Suhai, S. Fragmentation pathways of protonated peptides Mass Spectrom. Rev. 2005, 24, 508-548
27. Sharov, V. S.; Dremina, E. S.; Galeva, N. A.; Gerstenecker, G. S.; Li, X.; Dobrowsky, R. T.; Stobaugh, J. F.; Schöneich., C. Fluorogenic Tagging of Peptide and Protein 3-Nitrotyrosine with 4-(Aminomethyl)-benzenesulfonic Acid for Quantitative Analysis of Protein Tyrosine Nitration Chromatographia 2010, 71, 37-53
28. Sharov, V. S.; Dremina, E. S.; Pennington, J.; Killmer, J.; Asmus, C.; Thorson, M.; Hong, S. J.; Li, X.; Stobaugh, J. F.; Schöneich, C. Selective fluorogenic derivatization of 3-nitrotyrosine and 3,4-dihydroxyphenylalanine in peptides: a method designed for quantitative proteomic analysis Methods Enzymol. 2008, 441, 19-32
29. Bobst, C. E.; Abzalimov, R. R.; Houde, D.; Kloczewiak, M.; Mhatre, R.; Berkowitz, S. A.; Kaltashov, I. A. Detection and characterization of altered conformations of protein pharmaceuticals using complementary mass spectrometry-based approaches Anal. Chem. 2008, 80, 7473-7481
30. Kelly, S. M.; Jess, T. J.; Price, N. C. How to study proteins by circular dichroism Biochim. Biophys. Acta 2005, 1751, 119-139
31. Orru, S.; Amoresano, A.; Siciliano, R.; Napoleoni, R.; Finocchiaro, O.; Datola, A.; De Luca, E.; Sirna, A.; Pucci, P. Structural analysis of modified forms of recombinant IFN-beta produced under stress-simulating conditions Biol. Chem. 2000, 381, 7-17
32. Sharov, V. S.; Galeva, N. A.; Dremina, E. S.; Williams, T. D.; Schöneich, C. Inactivation of rabbit muscle glycogen phosphorylase b by peroxynitrite revisited: does the nitration of Tyr613 in the allosteric inhibition site control enzymatic function? Arch. Biochem. Biophys. 2009, 484, 155-166
33. O'Hair, R. A. J.; Reid, G. E. Neighboring group versus cis-elimination mechanisms for side chain loss from protonated methionine, methionine sulfoxide and their peptides Eur. Mass Spectrom. 1999, 5, 325-334
34. 2+ Eur. J. Biochem. 1994, 223, 759-764
35. 2+ J. Pharm. Sci. 2007, 96, 1844-1847
36. 2+ insulin to metal-catalyzed oxidation: Detection of 2-oxo-histidine by tandem mass spectrometry Pharm. Res. 2002, 19, 530-537
37. Stadtman, E. R. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions Annu. Rev. Biochem. 1993, 62, 797-821
38. Anderson, L. B.; Maderia, M.; Ouellette, A. J.; Putnam-Evans, C.; Higgins, L.; Krick, T.; MacCoss, M. J.; Lim, H.; Yates, J. R., 3rd; Barry, B. A. Posttranslational modifications in the CP43 subunit of photosystem II Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 14676-14681
39. Taylor, S. W.; Fahy, E.; Murray, J.; Capaldi, R. A.; Ghosh, S. S. Oxidative post-translational modification of tryptophan residues in cardiac mitochondrial proteins J. Biol. Chem. 2003, 278, 19587-19590
40. Palmisano, G.; Melo-Braga, M. N.; Engholm-Keller, K.; Parker, B. L.; Larsen, M. R. Chemical Deamidation: A Common Pitfall in Large-Scale N-Linked Glycoproteomic Mass Spectrometry-Based Analyses J. Proteome Res. 2012, 11, 1949-1957
41. Koriatopoulou, K.; Karousis, N.; Varvounis, G. Novel synthesis of the pyrrolo[2,1-c][1,4]benzodiazocine ring system via a Dieckmann condensation Tetrahedron 2008, 64, 10009-10013
42. Hovorka, S. W.; Hong, J. Y.; Cleland, J. L.; Schöneich, C. Metal-catalyzed oxidation of human growth hormone: Modulation by solvent-induced changes of protein conformation J. Pharm. Sci. 2001, 90, 58-69
43. Luo, Q. Z.; Joubert, M. K.; Stevenson, R.; Ketchem, R. R.; Narhi, L. O.; Wypych, J. Chemical Modifications in Therapeutic Protein Aggregates Generated under Different Stress Conditions J. Biol. Chem. 2011, 286, 25134-25144
44. Li, S.; Nguyen, T. H.; Schöneich, C.; Borchardt, R. T. Aggregation and precipitation of human relaxin induced by metal-catalyzed oxidation Biochemistry 1995, 34, 5762-5772
45. Requena, J. R.; Groth, D.; Legname, G.; Stadtman, E. R.; Prusiner, S. B.; Levine, R. L. Copper-catalyzed oxidation of the recombinant SHa(29-231) prion protein Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 7170-7175
46. Rakhit, R.; Cunningham, P.; Furtos-Matei, A.; Dahan, S.; Qi, X. F.; Crow, J. P.; Cashman, N. R.; Kondejewski, L. H.; Chakrabartty., A. Oxidation-induced misfolding and aggregation of superoxide dismutase and its implications for amyotrophic lateral sclerosis J. Biol. Chem. 2002, 277, 47551-47556
47. Rauniyar, N.; Prokai, L. Detection and identification of 4-hydroxy-2-nonenal Schiff-base adducts along with products of Michael addition using data-dependent neutral loss-driven MS3 acquisition: method evaluation through an in vitro study on cytochrome c oxidase modifications Proteomics 2009, 9, 5188-5193
48. Dohno, C.; Okamoto, A.; Saito., I. Stable, specific, and reversible base pairing via Schiff base J. Am. Chem. Soc. 2005, 127, 16681-16684
49. Kato, Y.; Kitamoto, N.; Kawai, Y.; Osawa., T. The hydrogen peroxide/copper ion system, but not other metal-catalyzed oxidation systems, produces protein-bound dityrosine Free Radical Biol. Med. 2001, 31, 624-632
50. Schöneich, C. Mechanisms of metal-catalyzed oxidation of histidine to 2-oxo-histidine in peptides and proteins J. Pharm. Biomed. Anal. 2000, 21, 1093-1097
51. Greenfield, N.; Fasman, G. D. Computed circular dichroism spectra for the evaluation of protein conformation Biochemistry 1969, 8, 4108-4116