Site-specific PEGylation of protein bisulfide bonds using a three-carbon bridge

Bioconjugate Chemistry

Volumn 18, Issue 1, 2007, Pages 61-76

  Balan, Sibu ^a   Choi, Ji Won ^b   Godwin, Antony ^a   Teo, Ian ^b   Laborde, Carlos M ^a   Heidelberger, Sibylle ^a   Zloh, Mire ^a   Shaunak, Sunil ^b   Brocchini, Steve ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATION; BIOACTIVITY; COVALENT BONDS; ISOMERS; MOLECULES; PEPTIDES; POLYETHYLENE GLYCOLS; REDUCTION; SULFUR COMPOUNDS;

% REDUCTIONS; CARBON BRIDGE; DISULPHIDE BONDS; FUNCTIONALIZED; L-ASPARAGINASE; PEGYLATED; PEGYLATION; PROPERTY; SITE-SPECIFIC; STERIC SHIELDING;

AMINO ACIDS;

ALPHA2B INTERFERON; ASPARAGINASE; GLUTATHIONE; MACROGOL; PROTEIN; SOMATOSTATIN;

ALKYLATION; ARTICLE; CHEMICAL STRUCTURE; CONJUGATION; DISULFIDE BOND; REACTION ANALYSIS; REDUCTION; STEREOSPECIFICITY; SYNTHESIS;

EID: 33846406038     PISSN: 10431802     EISSN: None     Source Type: Journal    
DOI: 10.1021/bc0601471     Document Type: Article

References (72)

1. Harris, J., and Chess, R. (2003) Effect of Pegylation on pharmaceuticals. Nat. Rev. Drug Discovery 2 (3), 214-221.
2. Zalipsky, S. (1995) Chemistry of poly(ethylene glycol) conjugates with biologically active molecules. Adv. Drug Delivery Rev. 16, 157-182.
3. Greenwald, R., Choe, Y., McGuire, J., and Conover, C. (2003) Effective drug delivery by PEGylated drug conjugates. Adv. Drug Delivery Rev. 55, 217-250.
4. Pasut, G., Guiotto, A., and Veronese F. (2004) Protein, peptide and non-peptide drug PEGylation for therapeutic application. Expert Opin. Ther. Pat. 14 (5), 1-36.
5. Veronese, F., and Pasut G. (2005) PEGylation, successful approach to drug delivery. Drug Discovery Today 10 (21), 1451-1458.
6. Grace, M., Lee, S., Bradshaw, S., Chapman, J., Spond, J., Cox, S., DeLorenzo, M., Brassard, D., Wylie, D., Cannon-Carlson, S., Cullen, C., Indelicato, S., Voloch, M., and Bordens, R. (2005) Site of pegylation and polyethylene glycol molecule size attenuate interferon-a antiviral and antiproliferative activities through the JAK/STAT signaling pathway. J. Biol. Chem. 280 (8), 6327-6336.
7. Woghiren, C., Sharma, B., and Stein S. (1993) Protected thio-poly(ethylene glycol): A new activated polymer for reversible protein modification. Bioconjugate Chem. 4 (5), 314-318.
8. Kinstler, O., Brems, D., Lauren, S., Paige, A., Hamburger, J., and Treuheit, M. (1996) Characterization and stability of N-terminally PEGylated rhG-CSF. Pharm. Res. 13 (7), 996-1002.
9. Kinstler, O., Molineux, G., Treuheit, M., Ladd, D., and Gegg, C. (2002) Mono-N-terminal poly(ethylene glycol)-protein conjugates. Adv. Drug Delivery Rev. 54 (4), 477-485.
10. Chapman, A. (2002) PEGylated antibodies and antibody fragments for improved therapy: a review. Adv. Drug Delivery Rev. 54, 531-545.
11. Wylie, D., Voloch, M., Lee, S., Liu, Y., Cannon-Carlson, S., Cutler, C., and Pramanik, B. (2001) Carboxyalkylated histidine is a pH-dependent product of pegylation with SC-PEG. Pharm. Res. 18, 1354-1360.
12. Manjula, B., Tsai, A., Upadhya, R., Perumalsamy, K., Smith, P., Malavalli, A., Vandegriff, I., Winslow, R., Intaglietta, I., Prabhakaran, M., Friedman, J., and Acharya, A. (2003) Site-specific PEGylation of hemoglobin at cys-93: Correlation between the colligative properties of the PEGylated protein and the length of the conjugated PEG chain. Bioconjugate Chem. 14, 464-472.
13. Lee, H., Jang, H., Ryu, S., and Park, T. (2003) N-terminal site-specific mono-PEGylation of epidermal growth factor. Pharm. Res. 20 (5), 818-825.
14. Yamamoto, Y., Tsutsumi, Y., Yoshioka, Y., Nishibata, T., Kobayashi, K., Okamoto, T., Mukai, Y., Shimizu, T., Nakagawa, S., Nagata, S., and Mayumi, T. (2003) Site-specific PEGylation of a lysine-deficient TNF-alpha with full bioactivity. Nat. Biotechnol. 21, 546-552.
15. Gentle, I., DeSouza, D., and Baca, M. (2004) Direct production of proteins with N-terminal cysteine for site-specific conjugation. Bioconjugate Chem. 15, 658-663.
16. Edwards, C., Martin, S., Seely, J., Kinstler, O., Buckel, S., Bendele, A., Cosenza, M., Feige, U., and Kohno, T. (2003) Design of PEGylated soluble tumor necrosis factor receptor type I (PEG sTNF-RI) for chronic inflammatory diseases. Adv. Drug Delivery Rev. 55(10), 1315-1336.
17. Sato, H., Yamamoto, K., Hayashi, E., and Takahara, Y. (2000) Transflutaminase-mediated dual and site-specific incorporation of poly(ethylene glycol) derivatives into a chimeric interleukin-2. Bioconjugate Chem. 11, 502-509.
18. Sato, H. (2002) Enzymatic procedure for site-specific pegylation of proteins. Adv. Drug Delivery Rev. 54, 487-504.
19. Rosendahl, M., Doherty, D., Smith, S., Carlson, S., Chlipala, E., and Cox, G. (2005) A long-acting, highly potent interferon a-2 conjugate created using site-specific PEGylation. Bioconjugate Chem. 16, 200-207.
20. Pavlou, A., and Reichert, J. (2004) Recombinant protein therapeutics-success rates, market trends and values to 2010. Nat. Biotechnol. 22, 1513-1519.
21. Thornton, J. (1981) Disulphide bridges in globular proteins. J. Mol. Biol. 151, 261-287.
22. Petersen, M., Jonson, P., and Petersen S. (1999) Amino acid neighbours and detailed conformational analysis of cysteines in proteins. Protein Eng. 12 (7), 535-548.
23. Leung, H., Xu, G., Narayan, M., and Scheraga, H. (2005) Impact of an easily reducible disulfide bond on the oxidative folding rate of multi-disulfide-containing proteins. J. Peptide Res. 65, 47-54.
24. Betz, S. (1993) Disulfide bonds and the stability of globular proteins. Protein Sci. 2, 1551-1558.
25. Saunders, A., Young, G., and Pielak, G. (1993) Polarity of disulfide bonds. Protein Sci. 2, 1183-1184.
26. Bewley, T., Brovetto-Cruz, J., and Li, C. (1969) Human pituitary growth hormone. Physicochemical investigations of the native and reduced-alkylated protein. Biochemistry 8 (12), 4701-4708.
27. Wedemeyer, W., Welker, E., Narayan, M., and Scheraga, H. (2000) Disulfide bonds and protein folding. Biochemistry 39, 4207-4216.
28. Rajarathnam, K., Sykes, B., Dewald, B., Baggiolini, M., and Clark-Lewis, I. (1999) Disulfide bridges in interleukin-8 probed using nono-natural disulfide analogues: dissociation of roles in structure from function. Biochemistry 38, 7653-7658.
29. Zhu, H., Dupureur, C., Zhang, B., and Tsai, M. (1995) Phospholipase A2 engineering. The roles of disulfide bonds in structure, conformational stability, and catalytic function? Biochemistry 34, 15307-15314.
30. Morehead, H., Johnston, P., and Wetzel, R. (1984) Roles of the 29-138 disulfide bond of subtype A of human a interferon in its antiviral activity and conformational stability. Biochemistry 23, 2500-2507.
31. Todokoro, K., Saito, T., Obata, M., Yamazaki, S., and Tamaura, Y. (1975) Studies on conformation and antigenicity of reduced S-methylated asparaginase in comparison with asparaginase. FEBS Lett. 60, 259-262.
32. Godwin, A., Choi, J., Pedone, E., Balan, S., Jumnah, R., Shaunak, S., Brocchini, S., and Zloh, M. (2006) Molecular dyamics simulations of proteins with chemically modified disulfide bonds. Theor. Chem. Ace. DOI: 10.1007/s00214-006-0134-0.
33. Shaunak, S., Godwin, A., Choi, J., Balan, S., Pedone, E., Vijayarangam, D., Heidelberger, S., Teo, I., Zloh, M., and Brocchini, S. (2006) Site-specific PEGylation of native disulfide bonds in therapeutic proteins. Nat. Chem. Biol 2, 312-313.
34. Meager, A., Gaines, D., Zoon, K., and Mire-Sluis, A. (2001) Establishment of new and replacement World Health Organization international biological standards for human interferon alpha and omega. J. Immunol. Methods 257, 17-33.
35. Liberatore, F., Comeau, R., McKearin, J., Pearson, D., Belonga, B., Brocchini, S., Kath, J., Phillips, T., Oswell, K., and Lawton, R. (1990) Site directed modification and cross-linking of a monoclonal antibody with equilibrium transfer alkylating cross-link reagents. Bioconjugate Chem. 1, 36-50.
36. de Rosario, R., Brocchini, S., Lawton, R., Wahl, R., and Smith, R. (1990) Sulfydral site-specific cross-linking of a monoclonal antibody by a fluorescent equilibrium transfer alkylating cross-link reagent. Bioconjugate Chem. 1, 51-65.
37. Burns, J., Butler, J., Moran, J., and Whitesides, G. (1991) Selective reduction of disulfides by tris(2-carboxyethyl)phosphine. J. Org. Chem. 56, 2648-2650.
38. Fahey, E., Chaudhuri, J., and Binding, P. (2000) Refolding of low molecular weight urokinase plasminogen activator by dilution and size exlusion chromatography. A comparative study. Sep. Sci. Technol. 55(11), 1743-1760.
39. Wüthrich, K. (1986) NMR of the Proteins and Nucleic Acids, Wiley, New York.
40. Bax, A., and Davis, D. (1985) MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 65, 355-360.
41. Jeener, J., Meier, B., Ernst, B., and Ernst, R. (1979) Investigation of exchange processes by 2-dimensional NMR-spectroscopy. J. Chem. Phys. 71, 4546-4553.
42. Mashburn, L., and Wriston, J. (1964) Tumor inhibitory effect of L-asparaginase from Escherichia coli. Arch. Biochem. Biophys. 105, 450-452.
43. Soares, A., Guimaraes, G., Polakiewicz, B., Pitombo, R., and Abrahao-Neto, J. (2002) Effects of polyethylene glycol attachment on physicochemical and biological stability of E. coli L-asparaginase. Int. J. Pharm. 237, 163-170.
44. Mohamadi, F., Richards, N., Guida, W., Liskamp, R., Lipton, M., Caufield, C., Chang, G., Hendrickson, T., and Still, W. (1990) Macromodel - an integrated software system for modeling organic and bioorganic molecules using molecular mechanics. J. Comput. Chem. 11, 440-467.
45. Jorgensen, W., Maxwell D., and Tirado-Rives (1996) Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 118, 11225-11236.
46. Still, W., Tempczyk, A., Hawley, R., and Hendrickson, T. (1990) Semianalytical treatment of solvation for molecular mechanics and dynamics. J. Am. Chem. Soc. 112 (16), 6127-6129.
47. McLachlan, A. (1982) Rapid comparison of protein structures. Acta Crystallogr., Sect. A 38, 871-873.
48. Martin A. (2005) Profit, version 1.8; http://www.bioinf.org.uk/ software/profit/.
49. Mitra, S., and Lawton, R. (1979) Reagents for the cross-linking of proteins by equilibrium transfer alkylation. J. Am. Chem. Soc. 101 (11), 3097-3110.
50. Brocchini, S., Eberle, M., and Lawton, R. (1988) Molecular yardsticks. Synthesis of extended equilibrium transfer alkylating cross-link reagents and their use in the formation of macrocycles. J. Am. Chem. Soc. 110, 5211.
51. Wilbur, D., Stray, J., Hamlin, D., Curtis, D., and Vessella, R. (1994) Monoclonal antibody Fab′ fragment cross-linking using equilibrium transfer alkylation reagents. A strategy for site-specific conjugation of diagnostic and therapeutic agents with F(ab′)2 fragments. Bioconjugate Chem. 5, 220-235.
52. Kim, S., and Lim, C. (2002) Tin-free radical-mediated C-C bond formations with alkyl allyl sulfones as radical precursors. Angew. Chem., Int. Ed. 41 (17), 3265-3267.
53. Pan, Y., Hutchinson, D., Nantz, M., and Fuchs, P. (1989) Synthesis via vinyl sulfones. 34. Sn2′ additions of cuprates to sulfone and esterpolarized cyclopentenylic systems. Tetrahedron 45 (2), 467-478.
54. Seebach, D., and Knochel, P. (1984) 2′-nitro-2′-propen-l-yl 2, 2-dimethylpropanoate (NPP), a multiple coupling reagent. Helv. Chim. Acta 67 (1), 261-283.
55. Nelson, R., and Lawton, R. (1966) On the α,α′ annelation of cyclic ketones. J. Am. Chem. Soc. 88 (16), 3884-3885.
56. Padwa, A., Kline, D., Murphree, S., and Yeske, P. (1992) Use of 2,3-bis(phenylsulfonyl)-1-propene as a multicoupling reagent. J. Org. Chem. 57, 298-306.
57. Casey, J., Pedley, R., King, D., Boden, R., Chapman, A., Yarranton, G., and Begent, R. (2000) Improved tumour targeting of di-Fab′ fragments modified with polyethylene glycol. Tumor Targeting 4, 235-244.
58. Shafer, D., Inman, J., and Lees, A. (2000) Reaction of Tris(2-carboxyethyl)phosphine (TCEP) with Maleimide and a-Haloacyl Groups: Anomalous Elution of TCEP by Gel Filtration. Anal. Biochem. 282, 161-164.
59. Ho, P., Milikin, E., Bobbitt, J., Grinnan, E., Burck, P., Frank, B., Boeck, L., and Squires, R. (1970) Crystalline L-asparaginase from Escherichia coli B. I. Purification and chemical characterisation. J. Biol. Chem. 245, 3708-3715.
60. Swain, A., Jaskolski, M., Housset, D., Rao, J., and Wlodawer, A. (1993) Crystal-structure of Escherichia coli L-asparaginase, an enzyme used in cancer-therapy. Proc. Natl. Acad. Sci. U.S.A. 90, 1474-1478.
61. Palm, G., Lubkowski, J., Derst, C., Schleper, S., Rohm, K., and Wlodawer, A. (1996) A covalently bound catalytic intermediate in Escherichia coli asparaginase: crystal structure of a Thr-89-Val mutant. FEBS Lett. 390, 211-216.
62. Killander, D., Dohlwitz, A., Engstedt, L., Franzen, S., Gahrton, G., Gullbring, B., Holm, G., Holmgren, A., Hoglund, S., Killander, A., Lockner, D., Mellstedt, H., Moe, P., Palmblad, J., Reizenstein, P., Skarberg, K., Swedberg, B., Uden, A., Wadman, B., Wide, L., and Ahstrom, L. (1976) Hypersensitive reactions and antibody formation during L-asparaginase treatment of children and adults with acute leukemia. Cancer 37, 220-228.
63. Kamisaki, Y., Wada, H., Yagura, T., Matsushima, A., and Inada, Y. (1981) Reduction in immunogenicity and clearance rate of Escherichia coli L-asparaginase by modification with monomethoxy-polyethylene glycol. J. Pharmacol. Exp. Ther. 216, 410-414.
64. Yoshimoto, T., Nishimura, H., Saito, Y., Sakurai, K., Kamisaki, Y., Wada, H., Sako, M., Tsujino, G., and Inada, Y. (1986) Characterization of Polyethylene Glycol-Modified L-Asparaginase from Escherichia coli and Its Application to Therapy of Leukemia. Jpn. J. Cancer Res. 77, 1264-1270.
65. Bailon, P., Palleroni, A., Schaffer, C., Spence, C., Fung, W., Porter, J. E., Ehrlich, G., Pan, W., Xu, Z., Modi, M., Farid, A., and Berthold, W. (2001) Rational design of a potent, long-lasting form of interferon: A 40 kDa branched polyethylene glycol-conjugated interferon α-2a for the treatment of Hepatitis C. Bioconjugate Chem. 12, 195-202.
66. Grace, M., Youngster, S., Gitlin, G., Sydor, W., Xie, L., Westreich, L., Jacobs, S., Brassard, D., Bausch, J., and Bordens, R. (2001) Structural and biologic characterization of pegylated recombinant IFN-a2b. J. Interferon Cytokine Res. 21, 1103-1115.
67. Rajender, R., Modi, M., and Pedder, S. (2002) Use of peginterferon alfa-2a (40 KD) (Pegasys) for the treatment of Hepatitis C. Adv. Drug Delivery Rev. 54, 571-586.
68. Youngster, S., Wang, Y., Grace, M., Bausch, J., Bordens, R., and Wyss, D. (2002) Structure, biology, and therapeutic implications of pegylated interferon alpha-2b. Curr. Pharm. Des. 8, 2139-2157.
69. Dhalluin, C., Ross, A., Huber, W., Gerber, P., Brugger, D., Gsell, B., and Senn, H. (2005) Structural, kinetic, and thermodynamic analysis of the binding of the 40 kDa PEG-interferon-alpha 2a and its individual positional isomers to the extracellular domain of the receptor IFNAR2. Bioconjugate Chem. 16, 518-527.
70. Piehler, J., Roisman, L., and Schreiber, G. (2000) New structural and functional aspects of the type I interferon-receptor interaction revealed by comprehensive mutational analysis of the binding interface. J. Biol. Chem. 275, 40425-40433.
71. Kubetzko, S., Sarkar, C., and Pluckthun, A. (2005) Protein PEGylation decreases observed target association rates via a dual blocking mechanism. Mol. Pharmacol. 68, 1439-1454.
72. Dhalluin, C., Ross, A., Leuthold, L., Foser, S., Gsell, B., Muller, F., and Senn, H. (2005) Structural and biophysical characterization of the 40 kDa PEG-interferon-α2a and its individual positional isomers. Bioconjugate Chem. 16, 504-517.