Dynamic fluctuations of protein-carbohydrate interactions promote protein aggregation

PLoS ONE

Volumn 4, Issue 12, 2009, Pages

  Voynov, Vladimir ^a   Chennamsetty, Naresh ^a   Kayser, Veysel ^a   Helk, Bernhard ^b   Forrer, Kurt ^b   Zhang, Heidi ^b   Fritsch, Cornelius ^b   Heine, Holger ^b   Trout, Bernhardt L ^a  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC AMINO ACID; CARBOHYDRATE; FC RECEPTOR; GLYCOPROTEIN; IMMUNOGLOBULIN G; AMINO ACID; MUTANT PROTEIN; PEPTIDE;

AMINO ACID SUBSTITUTION; ARTICLE; COMPUTER SIMULATION; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; IMMUNOGENICITY; MOLECULAR INTERACTION; PROTEIN AGGREGATION; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; SITE DIRECTED MUTAGENESIS; STRESS; CARBOHYDRATE ANALYSIS; CARBOHYDRATE METABOLISM; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; HEAT SHOCK RESPONSE; HUMAN; HYDROPHOBICITY; KINETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN QUATERNARY STRUCTURE; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; SURFACE PROPERTY;

AMINO ACIDS; CARBOHYDRATE METABOLISM; CARBOHYDRATE SEQUENCE; CARBOHYDRATES; CELL LINE; COMPUTER SIMULATION; HEAT-SHOCK RESPONSE; HUMANS; HYDROPHOBICITY; IMMUNOGLOBULIN G; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PEPTIDES; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; SURFACE PROPERTIES;

EID: 77049127553     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008425     Document Type: Article

References (39)

1. Arnold JN, Wormald MR, Sim RB, Rudd PM, Dwek RA (2007) The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu Rev Immunol 25: 21-50.
2. Bucior I, Scheuring S, Engel A, Burger MM (2004) Carbohydrate-carbohydrate interaction provides adhesion force and specificity for cellular recognition. J Cell Biol 165: 529-537.
3. Kaneko Y, Nimmerjahn F, Ravetch JV (2006) Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 313: 670-673.
4. Walsh G, Jefferis R (2006) Post-translational modifications in the context oftherapeutic proteins. Nat Biotechnol 24: 1241-1252.
5. Peracaula R, Barrabes S, Sarrats A, Rudd PM, de Llorens R (2008) Altered glycosylation in tumours focused to cancer diagnosis. Dis Markers 25: 207-218.
6. Taylor-Papadimitriou J, Burchell J, Miles DW, Dalziel M (1999) MUC1 and cancer. Biochim Biophys Acta 1455: 301-313.
7. Rege WP, Painter TJ, Watkins WM, Morgan WT (1964) Isolation of Serologically Active Fucose-Containing Oligosaccharides from Human Blood-Group H Substance. Nature 203: 360-363.
8. Painter TJ, Watkins WM, Morgan WT (1965) Serologically active fucose-containing oligosaccharides isolated from human blood-group A and B substances. Nature 206: 594-597.
9. Lloyd KO, Kabat EA, Layug EJ, Gruezo F (1966) Immunochemical studies on blood groups. XXXIV. Structures of some oligosaccharides produced by alkaline degradation of blood group A, B, and H substances. Biochemistry 5:1489-1501.
10. Egrie JC, Browne JK (2001) Development and characterization of novel erythropoiesis stimulating protein (NESP). Br J Cancer 84 Suppl 1: 3-10.
11. Li H, Sethuraman N, Stadheim TA, Zha D, Prinz B, et al. (2006) Optimization of humanized IgGs in glycoengineered Pichia pastoris. Nat Biotechnol 24: 210-215.
12. Mimura Y, Church S, Ghirlando R, Ashton PR, Dong S, et al. (2000) The influence of glycosylation on the thermal stability and effector function expression of human IgG1-Fc: properties of a series of truncated glycoforms. Mol Immunol 37: 697-706.
13. Radaev S, Sun PD (2001) Recognition of IgG by Fcgamma receptor. The role of Fc glycosylation and the binding of peptide inhibitors. J Biol Chem 276: 16478-16483.
14. Carter PJ (2006) Potent antibody therapeutics by design. Nat Rev Immunol 6:343-357.
15. Leader B, Baca QJ, Golan DE (2008) Protein therapeutics: a summary and pharmacological classification. Nat Rev Drug Discov 7: 21-39.
16. Wang W (1999) Instability, stabilization, and formulation of liquid protein pharmaceuticals. Int J Pharm 185: 129-188.
17. Wang W, Singh S, Zeng DL, King K, Nema S (2007) Antibody structure, instability, and formulation. J Pharm Sci 96: 1-26.
18. Cordoba-Rodriguez RV (2008) Aggregates in MAbs and Recombinant Therapeutic Proteins: A Regulatory Perspective. BioPharm International 21: 44-53.
19. Salfeld JG (2007) Isotype selection in antibody engineering. Nat Biotechnol 25: 1369-1372.
20. Garber E, Demarest SJ (2007) A broad range of Fab stabilities within a host of therapeutic IgGs. Biochem Biophys Res Commun 355: 751-757.
21. Ionescu RM, Vlasak J, Price C, Kirchmeier M (2008) Contribution of variable domains to the stability of humanized IgG1 monoclonal antibodies. J Pharm Sci 97: 1414-1426.
22. Quiocho FA (1989) Protein-Carbohydrate Interactions - Basic Molecular-Features. Pure and Applied Chemistry 61: 1293-1306.
23. Taroni C, Jones S, Thornton JM (2000) Analysis and prediction of carbohydrate binding sites. Protein Eng 13: 89-98.
24. Spiwok V, Lipovova P, Skalova T, Vondrackova E, Dohnalek J, et al. (2005) Modelling of carbohydrate-aromatic interactions: ab initio energetics and force field performance. Journal of Computer-Aided Molecular Design 19: 887-901.
25. Deisenhofer J (1981) Crystallographic refinement and atomic models of a human Fc fragment and its complex with fragment B of protein A from Staphylococcus aureus at 2.9- and 2.8-A resolution. Biochemistry 20: 2361-2370.
26. Krapp S, Mimura Y, Jefferis R, Huber R, Sondermann P (2003) Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity. J Mol Biol 325: 979-989.
27. Taves CJ, Kusumi A, Winkelhake JL (1984) Human aglycosyl-IgG exhibits increased hydrophobicity. Binding/fluorescence studies with 8-anilinonaphtha-lene-1-sulfonic acid (ANS). Biochem Biophys Res Commun 124: 605-613.
28. Wormald MR, Rudd PM, Harvey DJ, Chang SC, Scragg IG, et al. (1997) Variations in oligosaccharide-protein interactions in immunoglobulin G determine the site-specific glycosylation profiles and modulate the dynamic motion of the Fc oligosaccharides. Biochemistry 36: 1370-1380.
29. Malhotra R, Wormald MR, Rudd PM, Fischer PB, Dwek RA, et al. (1995) Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein. Nat Med 1: 237-243.
30. Chennamsetty N, Voynov V, Kayser V, Helk B, Trout BL (2009) Design of therapeutic proteins with enhanced stability. PNAS USA 106: 11937-11942.
31. Chennamsetty N, Helk B, Voynov V, Kayser V, Trout BL (2009) Aggregation prone motifs in IgG antibodies. J Mol Biol 391: 404-413.
32. Kayser V, Chennamsetty N, Voynov V, Helk B, Forrer K, et al. (2009) Mechanism of therapeutic monoclonal antibody aggregation. In preparation.
33. Voynov V, Chennamsetty N, Kayser V, Wallny H-J, Helk B, et al. (2009) Design and application of antibody cysteine variants. Submitted.
34. Shields RL, Namenuk AK, Hong K, Meng YG, Rae J, et al. (2001) High resolution mapping of the binding site on human IgG1 for Fc gamma RI, Fcgamma RII, Fc gamma RIII, and FcRn and design of IgG1 variants with improved binding to the Fc gamma R. J Biol Chem 276: 6591-6604.
35. Lund J, Takahashi N, Pound JD, Goodall M, Jefferis R (1996) Multiple interactions of IgG with its core oligosaccharide can modulate recognition by complement and human Fc gamma receptor I and influence the synthesis of its oligosaccharide chains. J Immunol 157: 4963-4969.
36. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, et al. (1983) CHARMM: A program for macromolecular energy, minimization, and dynamics calculations Journal of Computational Chemistry 4: 187-217.
37. MacKerell J.A.D., Bashford D, Bellott M, Dunbrack RL Jr, Evanseck JD, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102.
38. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79: 926-935.
39. Kuttel M, Brady JW, Naidoo KJ (2002) Carbohydrate solution simulations: producing a force field with experimentally consistent primary alcohol rotational frequencies and populations. J Comput Chem 23: 1236-1243.