Tailoring small proteins towards biomedical applications

Current Pharmaceutical Biotechnology

Volumn 12, Issue 11, 2011, Pages 1792-1798

  Zakrzewska, Malgorzata ^a   Szlachcic, Anna ^a   Otlewski, Jacek ^a  

^a UNIVERSITY OF WROC AW   (Poland)

Author keywords

Bpti; Fgf1; Protease inhibitors; Protein engineering; Protein stability; Protein therapeutics; Squash inhibitors

Indexed keywords

APROTININ; BLOOD CLOTTING FACTOR 10; BLOOD CLOTTING FACTOR 12; BOVINE PANCREATIC TRYPSIN INHIBITOR; FIBROBLAST GROWTH FACTOR 1; HEPARIN; PLASMA KALLIKREIN; PLASMIN; PROTEIN C; SERINE PROTEINASE INHIBITOR; THROMBIN; UNCLASSIFIED DRUG;

CRYSTALLOGRAPHY; ENZYME ASSAY; HUMAN; MEASUREMENT; MUTAGENESIS; MUTATION; NONHUMAN; PHYSICAL CHEMISTRY; PLANT SEED; PROTEIN FUNCTION; PROTEIN VARIANT; REVIEW; SQUASH; SYNTHESIS;

EID: 83455210941     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920111798376905     Document Type: Review

References (61)

1. Marshall, S. A.; Lazar, G. A.; Chirino, A. J.; Desjarlais, J. R. Rational design and engineering of therapeutic proteins. Drug. Discov. Today, 2003, 8, 212-221.
2. Lazar, G. A.; Marshall, S. A.; Plecs, J. J.; Mayo, S. L.; Desjarlais, J. R. Designing proteins for therapeutic applications. Curr. Opin. Struct. Biol., 2003, 13, 513-518.
3. Rustgi, V. K. Albinterferon alfa-2b, a novel fusion protein of human albumin and human interferon alfa-2b, for chronic hepatitis C. Curr. Med. Res. Opin., 2009, 25, 991-1002.
4. Schmidt, S. R. Fusion-proteins as biopharmaceuticals-applications and challenges. Curr. Opin. Drug Discov. Devel., 2009, 12, 284-295.
5. Sola, R. J.; Griebenow, K. Effects of glycosylation on the stability of protein pharmaceuticals. J. Pharm. Sci., 2009, 98, 1223-1245.
6. Zakrzewska, M.; Krowarsch, D.; Wiedlocha, A.; Otlewski, J. Design of fully active FGF-1 variants with increased stability. Protein Eng. Des. Sel., 2004, 17, 603-611.
7. Drevelle, A.; Urvoas, A.; Hamida-Rebai, M. B.; Van Vooren, G.; Nicaise, M.; Valerio-Lepiniec, M.; Desmadril, M.; Robert, C. H.; Minard, P. Disulfide bond substitution by directed evolution in an engineered binding protein. ChemBioChem, 2009, 10, 1349-1359.
8. 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-a2b and HSA fusion protein increases its stability against mechanical and thermal stress. Eur. J. Pharm. Biopharm., 2009, 72, 405-411.
9. Huang, Z.; Ni, C.; Chu, Y.; Wang, S.; Yang, S.; Wu, X.; Wang, X.; Li, X.; Feng, W.; Lin, S. Chemical modification of recombinant human keratinocyte growth factor 2 with polyethylene glycol improves biostability and reduces animal immunogenicity. J. Biotechnol., 2009, 142, 242-249.
10. Veronese, F. M.; Mero, A. The impact of PEGylation on biological therapies. BioDrugs, 2008, 22, 315-329.
11. Rawlings, N. D.; Morton, F. R.; Kok, C. Y.; Kong, J.; Barrett, A. J. MEROPS: the peptidase database. Nucleic Acids Res., 2008, 36, D320-325.
12. Schechter, I.; Berger, A. On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun., 1967, 27, 157-162.
13. Dipiro, J. T.; Matzke, G. R.; Posey, L. M.; Wells, B. G.; Talbert, R. L.; Yee, G. C. Enzymes and Their Inhibition: Drug Development. 2005.
14. Polanowski, A.; Wilusz, T.; Nienartowicz, B.; Cieslar, E.; Slominska, A.; Nowak, K. Isolation and partial amino acid sequence of the trypsin inhibitor from the seeds of Cucurbita maxima. Acta Biochim. Pol., 1980, 27, 371-382.
15. Otlewski, J.; Whatley, H.; Polanowski, A.; Wilusz, T. Amino-acid sequences of trypsin inhibitors from watermelon (Citrullus vulgaris) and red bryony (Bryonia dioica) seeds. Biol. Chem. Hoppe Seyler, 1987, 368, 1505-1507.
16. Otlewski, J.; Zbyryt, T.; Krokoszynska, I.; Wilusz, T. Inhibition of serine proteinases by squash inhibitors. Biol. Chem. Hoppe Seyler, 1990, 371, 589-594.
17. Hojima, Y.; Pierce, J. V.; Pisano, J. J. Pumpkin seed inhibitor of human factor XIIa (activated Hageman factor) and bovine trypsin. Biochemistry, 1982, 21, 3741-3746.
18. Bode, W.; Greyling, H. J.; Huber, R.; Otlewski, J.; Wilusz, T. The refined 2.0 A X-ray crystal structure of the complex formed between bovine beta-trypsin and CMTI-I, a trypsin inhibitor from squash seeds (Cucurbita maxima). Topological similarity of the squash seed inhibitors with the carboxypeptidase A inhibitor from potatoes. FEBS Lett., 1989, 242, 285-292.
19. Holak, T. A.; Gondol, D.; Otlewski, J.; Wilusz, T. Determination of the complete three-dimensional structure of the trypsin inhibitor from squash seeds in aqueous solution by nuclear magnetic resonance and a combination of distance geometry and dynamical simulated annealing. J. Mol. Biol., 1989, 210, 635-648.
20. Otlewski, J.; Krowarsch, D. Squash inhibitor family of serine proteinases. Acta Biochim. Pol., 1996, 43, 431-444.
21. Chiche, L.; Heitz, A.; Gelly, J. C.; Gracy, J.; Chau, P. T.; Ha, P. T.; Hernandez, J. F.; Le-Nguyen, D. Squash inhibitors: from structural motifs to macrocyclic knottins. Curr. Protein Pept. Sci., 2004, 5, 341-349.
22. Helland, R.; Berglund, G. I.; Otlewski, J.; Apostoluk, W.; Andersen, O. A.; Willassen, N. P.; Smalas, A. O. High-resolution structures of three new trypsin-squash-inhibitor complexes: a detailed comparison with other trypsins and their complexes. Acta Crystallogr. D Biol. Crystallogr., 1999, 55, 139-148.
23. Ay, J.; Hilpert, K.; Krauss, N.; Schneider-Mergener, J.; Hohne, W. Structure of a hybrid squash inhibitor in complex with porcine pancreatic elastase at 1.8 A resolution. Acta Crystallogr. D Biol. Crystallogr., 2003, 59, 247-254.
24. Kratzner, R.; Debreczeni, J. E.; Pape, T.; Schneider, T. R.; Wentzel, A.; Kolmar, H.; Sheldrick, G. M.; Uson, I. Structure of Ecballium elaterium trypsin inhibitor II (EETI-II): a rigid molecular scaffold. Acta Crystallogr. D Biol. Crystallogr., 2005, 61, 1255-1262.
25. Rolka, K.; Kupryszewski, G.; Ragnarsson, U.; Otlewski, J.; Wilusz, T.; Polanowski, A. Synthesis of an elastase inhibitor by monosubstitution of arginine-5 with valine at the reactive site in a trypsin inhibitor from squash seeds (CMTI III). Biol. Chem. Hoppe Seyler, 1989, 370, 499-502.
26. Rolka, K.; Kupryszewski, G.; Ragnarsson, U.; Otlewski, J.; Krokoszynska, I.; Wilusz, T. Chemical synthesis of new trypsin, chymotrypsin and elastase inhibitors by amino-acid substitutions in a trypsin inhibitor from squash seeds (CMTI III). Biol. Chem. Hoppe Seyler, 1991, 372, 63-68.
27. Grzesiak, A.; Buczek, O.; Petry, I.; Szewczuk, Z.; Otlewski, J. Inhibition of serine proteinases from human blood clotting system by squash inhibitor mutants. Biochim. Biophys. Acta, 2000, 1478, 318-324.
28. Gracy, J.; Le-Nguyen, D.; Gelly, J. C.; Kaas, Q.; Heitz, A.; Chiche, L. KNOTTIN: the knottin or inhibitor cystine knot scaffold in 2007. Nucleic Acids Res., 2008, 36, D314-319.
29. Kolmar, H. Biological diversity and therapeutic potential of natural and engineered cystine knot miniproteins. Curr. Opin. Pharmacol., 2009, 9, 608-614.
30. Ascenzi, P.; Bocedi, A.; Bolognesi, M.; Spallarossa, A.; Coletta, M.; De Cristofaro, R.; Menegatti, E. The bovine basic pancreatic trypsin inhibitor (Kunitz inhibitor): a milestone protein. Curr. Protein Pept. Sci., 2003, 4, 231-251.
31. Addlagatta, A.; Krzywda, S.; Czapinska, H.; Otlewski, J.; Jaskolski, M. Ultrahigh-resolution structure of a BPTI mutant. Acta Crystallogr. D Biol. Crystallogr., 2001, 57, 649-663.
32. Helland, R.; Otlewski, J.; Sundheim, O.; Dadlez, M.; Smalas, A. O. The crystal structures of the complexes between bovine betatrypsin and ten P1 variants of BPTI. J. Mol. Biol., 1999, 287, 923-942.
33. Helland, R.; Czapinska, H.; Leiros, I.; Olufsen, M.; Otlewski, J.; Smalas, A. O. Structural consequences of accommodation of four non-cognate amino acid residues in the S1 pocket of bovine trypsin and chymotrypsin. J. Mol. Biol., 2003, 333, 845-861.
34. Czapinska, H.; Helland, R.; Smalas, A. O.; Otlewski, J. Crystal structures of five bovine chymotrypsin complexes with P1 BPTI variants. J. Mol. Biol., 2004, 344, 1005-1020.
35. Krowarsch, D.; Dadlez, M.; Buczek, O.; Krokoszynska, I.; Smalas, A. O.; Otlewski, J. Interscaffolding additivity: binding of P1 variants of bovine pancreatic trypsin inhibitor to four serine proteases. J. Mol. Biol., 1999, 289, 175-186.
36. Polanowska, J.; Krokoszynska, I.; Czapinska, H.; Watorek, W.; Dadlez, M.; Otlewski, J. Specificity of human cathepsin G. Biochim. Biophys. Acta, 1998, 1386, 189-198.
37. Grzesiak, A.; Helland, R.; Smalas, A. O.; Krowarsch, D.; Dadlez, M.; Otlewski, J. Substitutions at the P(1) position in BPTI strongly affect the association energy with serine proteinases. J. Mol. Biol., 2000, 301, 205-217.
38. Grzesiak, A.; Krokoszynska, I.; Krowarsch, D.; Buczek, O.; Dadlez, M.; Otlewski, J. Inhibition of six serine proteinases of the human coagulation system by mutants of bovine pancreatic trypsin inhibitor. J. Biol. Chem., 2000, 275, 33346-33352.
39. Kiczak, L.; Kasztura, M.; Koscielska-Kasprzak, K.; Dadlez, M.; Otlewski, J. Selection of potent chymotrypsin and elastase inhibitors from M13 phage library of basic pancreatic trypsin inhibitor (BPTI). Biochim. Biophys. Acta, 2001, 1550, 153-163.
40. Burgess, W. H.; Maciag, T. The heparin-binding (fibroblast) growth factor family of proteins. Annu. Rev. Biochem., 1989, 58, 575-606.
41. Goldfarb, M. Functions of fibroblast growth factors in vertebrate development. Cytokine Growth Factor Rev., 1996, 7, 311-325.
42. Vasiliauskas, D.; Stern, C. D. Patterning the embryonic axis: FGF signaling and how vertebrate embryos measure time. Cell, 2001, 106, 133-136.
43. Eswarakumar, V. P.; Lax, I.; Schlessinger, J. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev., 2005, 16, 139-149.
44. Zakrzewska, M.; Marcinkowska, E.; Wiedlocha, A. FGF-1: from biology through engineering to potential medical applications. Crit. Rev. Clin. Lab. Sci., 2008, 45, 91-135.
45. Ornitz, D. M.; Itoh, N. Fibroblast growth factors. Genome Biol., 2001, 2, 3005.
46. Bernett, M. J.; Somasundaram, T.; Blaber, M. An atomic resolution structure for human fibroblast growth factor 1. Proteins, 2004, 57, 626-634.
47. Schlessinger, J.; Lax, I.; Lemmon, M. Regulation of growth factor activation by proteoglycans: what is the role of the low affinity receptors? Cell, 1995, 83, 357-360.
48. Powers, C. J.; McLeskey, S. W.; Wellstein, A. Fibroblast growth factors, their receptors and signaling. Endocr. Relat. Cancer, 2000, 7, 165-197.
49. Culajay, J. F.; Blaber, S. I.; Khurana, A.; Blaber, M. Thermodynamic characterization of mutants of human fibroblast growth factor 1 with an increased physiological half-life. Biochemistry, 2000, 39, 7153-7158.
50. Zakrzewska, M.; Krowarsch, D.; Wiedlocha, A.; Olsnes, S.; Otlewski, J. Highly stable mutants of human fibroblast growth factor- 1 exhibit prolonged biological action. J. Mol. Biol., 2005, 352, 860-875.
51. Hubbard, S. J.; Beynon, R. J.; Thornton, J. M. Assessment of conformational parameters as predictors of limited proteolytic sites in native protein structures. Protein Eng., 1998, 11, 349-359.
52. Steipe, B.; Schiller, B.; Pluckthun, A.; Steinbacher, S. Sequence statistics reliably predict stabilizing mutations in a protein domain. J. Mol. Biol., 1994, 240, 188-192.
53. Szlachcic, A.; Zakrzewska, M.; Krowarsch, D.; Os, V.; Helland, R.; Smalas, A. O.; Otlewski, J. Structure of a highly stable mutant of human fibroblast growth factor 1. Acta Crystallogr. D Biol. Crystallogr., 2009, 65, 67-73.
54. Zakrzewska, M.; Wiedlocha, A.; Szlachcic, A.; Krowarsch, D.; Otlewski, J.; Olsnes, S. Increased protein stability of FGF1 can compensate for its reduced affinity for heparin. J. Biol. Chem., 2009, 284, 25388-25403.
55. Gospodarowicz, D.; Cheng, J. Heparin protects basic and acidic FGF from inactivation. J. Cell. Physiol., 1986, 128, 475-484.
56. Damon, D. H.; Lobb, R. R.; D'Amore, P. A.; Wagner, J. A. Heparin potentiates the action of acidic fibroblast growth factor by prolonging its biological half-life. J. Cell. Physiol., 1989, 138, 221-226.
57. DiGabriele, A. D.; Lax, I.; Chen, D. I.; Svahn, C. M.; Jaye, M.; Schlessinger, J.; Hendrickson, W. A. Structure of a heparin-linked biologically active dimer of fibroblast growth factor. Nature, 1998, 393, 812-817.
58. Harper, J. W.; Lobb, R. R. Reductive methylation of lysine residues in acidic fibroblast growth factor: effect on mitogenic activity and heparin affinity. Biochemistry, 1988, 27, 671-678.
59. Zhu, X.; Komiya, H.; Chirino, A.; Faham, S.; Fox, G. M.; Arakawa, T.; Hsu, B. T.; Rees, D. C. Three-dimensional structures of acidic and basic fibroblast growth factors. Science, 1991, 251, 90-93.
60. Klingenberg, O.; Wiedlocha, A.; Rapak, A.; Munoz, R.; Falnes, P.; Olsnes, S. Inability of the acidic fibroblast growth factor mutant K132E to stimulate DNA synthesis after translocation into cells. J. Biol. Chem., 1998, 273, 11164-11172.
61. Klingenberg, O.; Wiedlocha, A.; Olsnes, S. Effects of mutations of a phosphorylation site in an exposed loop in acidic fibroblast growth factor. J. Biol. Chem., 1999, 274, 18081-18086.