Miniproteins as phage display-scaffolds for clinical applications

Molecules

Volumn 16, Issue 3, 2011, Pages 2467-2485

  Zoller, Frederic ^a,b   Haberkorn, Uwe ^a,b   Mier, Walter ^b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

In vivo diagnostics; Miniprotein; Phage display; Protein engineering; Scaffold

Indexed keywords

PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIOPHAGE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS;

AMINO ACID SUBSTITUTION; BACTERIOPHAGES; MODELS, MOLECULAR; PROTEINS;

EID: 79953119750     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules16032467     Document Type: Article

References (96)

1. Skerra, A. Imitating the humoral immune response. Curr. Opin. Chem. Biol. 2003, 7, 683-693. (Pubitemid 37486111)
2. Binz, H.K.; Amstutz, P.; Pluckthun, A. Engineering novel binding proteins from nonimmunoglobulin domains. Nat. Biotechnol. 2005, 23, 1257-1268. (Pubitemid 41486853)
3. Descotes, J. Immunotoxicity of monoclonal antibodies. mAbs 2009, 1, 104-111.
4. Wu, A.M.; Senter, P.D. Arming antibodies: Prospects and challenges for immunoconjugates. Nat. Biotechnol. 2005, 23, 1137-1146. (Pubitemid 41486395)
5. Holliger, P.; Hudson, P.J. Engineered antibody fragments and the rise of single domains. Nat. Biotechnol. 2005, 23, 1126-1136. (Pubitemid 41486394)
6. Huang, L.; Muyldermans, S.; Saerens, D. Nanobodies: Proficient tools in diagnostics. Expert Rev Mol Diagn 2010, 10, 777-785.
7. Van Bockstaele, F.; Holz, J.B.; Revets, H. The development of nanobodies for therapeutic applications. Curr. Opin. Investig. Drugs 2009, 10, 1212-1224.
8. Skerra, A. Alternative non-antibody scaffolds for molecular recognition. Curr. Opin. Biotechnol. 2007, 18, 295-304. (Pubitemid 47385180)
9. Skerra, A. Engineered protein scaffolds for molecular recognition. J. Mol. Recognit. 2000, 13, 167-187. (Pubitemid 30613469)
10. Smith, G.P. Filamentous fusion phage: Novel expression vectors that display cloned antigens on the virion surface. Science 1985, 228, 1315-1317. (Pubitemid 15000355)
11. Smith, G.P.; Petrenko, V.A. Phage Display. Chem. Rev. 1997, 97, 391-410. (Pubitemid 127659250)
12. Young, K.H. Yeast two-hybrid: So many interactions, (in) so little time. Biol. Reprod. 1998, 58, 302-311. (Pubitemid 28099093)
13. Roberts, R.W. Totally in vitro protein selection using mRNA-protein fusions and ribosome display. Curr. Opin. Chem. Biol. 1999, 3, 268-273. (Pubitemid 29248622)
14. DeLano, W.L. The PyMol Molecular Graphics System; DeLano Scientific: San Carlos, CA, USA, 2002.
15. Kolmar, H. Engineered cystine-knot miniproteins for diagnostic applications. Expert Rev. Mol. Diagn. 2010, 10, 361-368.
16. Schmidt, M.M.; Wittrup, K.D. A modeling analysis of the effects of molecular size and binding affinity on tumor targeting. Mol. Cancer Ther. 2009, 8, 2861-2871.
17. Batra, S.K.; Jain, M.; Wittel, U.A.; Chauhan, S.C.; Colcher, D. Pharmacokinetics and biodistribution of genetically engineered antibodies. Curr. Opin. Biotechnol. 2002, 13, 603-608. (Pubitemid 35448063)
18. Russeva, M.G.; Adams, G.P. Radioimmunotherapy with engineered antibodies. Expert. Opin. Biol. Ther. 2004, 4, 217-231. (Pubitemid 38200433)
19. Rudin, M.; Weissleder, R. Molecular imaging in drug discovery and development. Nat. Rev. Drug Discov. 2003, 2, 123-131. (Pubitemid 37361644)
20. Tolmachev, V.; Orlova, A.; Nilsson, F.Y.; Feldwisch, J.; Wennborg, A.; Abrahmsen, L. Affibody molecules: Potential for in vivo imaging of molecular targets for cancer therapy. Expert Opin. Biol. Ther. 2007, 7, 555-568. (Pubitemid 46524679)
21. Haberkorn, U.; Eisenhut, M.; Altmann, A.; Mier, W. Endoradiotherapy with peptides - status and future development. Curr. Med. Chem. 2008, 15, 219-234. (Pubitemid 351260492)
22. Zoller, F.; Eisenhut, M.; Haberkorn, U.; Mier, W. Endoradiotherapy in cancer treatment - basic concepts and future trends. Eur. J. Pharmacol. 2009, 625, 55-62.
23. Marshall, G.R. Three-dimensional structure of peptide-protein complexes: Implications for recognition. Curr. Opin. Structl. Biol. 1992, 2, 904-919.
24. Nygren, P.A.; Skerra, A. Binding proteins from alternative scaffolds. J. Immunol. Methods 2004, 290, 3-28. (Pubitemid 38922856)
25. Virnekas, B.; Ge, L.; Pluckthun, A.; Schneider, K.C.; Wellnhofer, G.; Moroney, S.E. Trinucleotide phosphoramidites: Ideal reagents for the synthesis of mixed oligonucleotides for random mutagenesis. Nucl. Acids Res. 1994, 22, 5600-5607.
26. Krumpe, L.R.; Schumacher, K.M.; McMahon, J.B.; Makowski, L.; Mori, T. Trinucleotide cassettes increase diversity of T7 phage-displayed peptide library. BMC Biotechnol. 2007, 7, 65.
27. Rodi, D.J.; Soares, A.S.; Makowski, L. Quantitative assessment of peptide sequence diversity in M13 combinatorial peptide phage display libraries. J. Mol. Biol. 2002, 322, 1039-1052. (Pubitemid 35266511)
28. Pannekoek, H.; Meijer, M.; Gaardsvoll, H.; Zonneveld, A.J. Functional display of proteins, mutant proteins, fragments of proteins and peptides on the surface of filamentous (bacterio) phages: A review. Cytotechnology 1995, 18, 107-112.
29. Hanes, J.; Pluckthun, A. In vitro selection and evolution of functional proteins by using ribosome display. Proc. Natl. Acad. Sci. USA 1997, 94, 4937-4942. (Pubitemid 27214714)
30. McLafferty, M.A.; Kent, R.B.; Ladner, R.C.; Markland, W. M13 bacteriophage displaying disulfide-constrained microproteins. Gene 1993, 128, 29-36. (Pubitemid 23179206)
31. Sidhu, S.S. Engineering M13 for phage display. Biomol. Eng. 2001, 18, 57-63. (Pubitemid 32776595)
32. Roberts, B.L. Directed evolution of a protein: Selection of potent neutrophil elastase inhibitors displayed on M13 fusion phage. Proc. Natl. Acad. Sci. USA 1992, 89, 2429-2433.
33. Sabatino, G.; Papini, A.M. Advances in automatic, manual and microwave-assisted solid-phase peptide synthesis. Curr. Opin. Drug Discov. Devel. 2008, 11, 762-770.
34. Hackenberger, C.P.; Schwarzer, D. Chemoselective ligation and modification strategies for peptides and proteins. Angew. Chem. Int. Ed. Eng. 2008, 47, 10030-10074.
35. Baslé, E.; Joubert, N.; Pucheault, M. Protein chemical modification on endogenous amino acids. Chem. Biol. 2010, 17, 213-227.
36. Brechbiel, M.W. Bifunctional chelates for metal nuclides. Q J. Nucl. Med. Mol. Imaging 2008, 52, 166-173. (Pubitemid 351721937)
37. Walker, J.M. Basic Protein and Peptide Protocols; Springer: Berlin, Germany, 1994; Volume 32, pp. 441-448.
38. Baltzer, L.; Nilsson, H.; Nilsson, J. De novo design of proteins - what are the rules? Chem. Rev. 2001, 101, 3153-3163. (Pubitemid 35377815)
39. Buchner, J.; Moroder, L. Oxidative Folding of Peptides and Proteins; RSC Publishing: Cambridge, UK, 2009.
40. Souriau, C.; Chiche, L.; Irving, R.; Hudson, P. New binding specificities derived from Min-23, a small cystine-stabilized peptidic scaffold. Biochemistry 2005, 44, 7143-7155. (Pubitemid 40656659)
41. Legendre, D. TEM-1 [beta]-lactamase as a scaffold for protein recognition and assay. Protein Sci. 2002, 11, 1506-1518. (Pubitemid 34547221)
42. Schlehuber, S.; Skerra, A. Lipocalins in drug discovery: From natural ligand-binding proteins to [ldquo]anticalins[rdquo]. Drug Discov. Today 2005, 10, 23-33. (Pubitemid 40164816)
43. Nixon, A.E.; Wood, C.R. Engineered protein inhibitors of proteases. Curr. Opin. Drug Discov. Devel. 2006, 9, 261-268.
44. Christmann, A.; Walter, K.; Wentzel, A.; Kratzner, R.; Kolmar, H. The cystine knot of a squashtype protease inhibitor as a structural scaffold for Escherichia coli cell surface display of conformationally constrained peptides. Protein Eng. 1999, 12, 797-806. (Pubitemid 29472087)
45. Silverman, A.P.; Levin, A.M.; Lahti, J.L.; Cochran, J.R. Engineered cystine-knot peptides that bind alpha(v)beta(3) integrin with antibody-like affinities. J. Mol. Biol. 2009, 385, 1064-1075.
46. Vita, C.; Roumestand, C.; Toma, F.; Menez, A. Scorpion toxins as natural scaffolds for protein engineering. Proc. Natl. Acad. Sci. USA 1995, 92, 6404-6408.
47. Vita, C.; Vizzavona, J.; Drakopoulou, E.; Zinn-Justin, S.; Gilquin, B.; Menez, A. Novel miniproteins engineered by the transfer of active sites to small natural scaffolds. Biopolymers 1998, 47, 93-100.
48. Boy, R.G.; Mier, W.; Nothelfer, E.M.; Altmann, A.; Eisenhut, M.; Kolmar, H.; Tomaszowski, M.; Kramer, S.; Haberkorn, U. Sunflower trypsin inhibitor 1 derivatives as molecular scaffolds for the development of novel peptidic radiopharmaceuticals. Mol. Imaging Biol. 2010, 12, 377-385.
49. Korsinczky, M.L.J.; Schirra, H.J.; Rosengren, K.J.; West, J.; Condie, B.A.; Otvos, L.; Anderson, M.A.; Craik, D.J. Solution structures by 1H NMR of the novel cyclic trypsin inhibitor SFTI-1 from sunflower seeds and an acyclic permutant. J. Mol. Biol. 2001, 311, 579-591. (Pubitemid 32816591)
50. Löfblom, J.; Feldwisch, J.; Tolmachev, V.; Carlsson, J.; Ståhl, S.; Frejd, F.Y. Affibody molecules: Engineered proteins for therapeutic, diagnostic and biotechnological applications. FEBS Lett. 2010, 584, 2670-2680.
51. Nord, K.; Gunneriusson, E.; Ringdahl, J.; Stahl, S.; Uhlen, M.; Nygren, P.A. Binding proteins selected from combinatorial libraries of an alpha-helical bacterial receptor domain. Nat. Biotechnol. 1997, 15, 772-777. (Pubitemid 27329481)
52. Bianchi, E.A. Conformationally homogeneous combinatorial peptide library. J. Mol. Biol. 1995, 247, 154-160.
53. Lehtio, J.; Teeri, T.T.; Nygren, P.A. Alpha-amylase inhibitors selected from a combinatorial library of a cellulose binding domain scaffold. Proteins 2000, 41, 316-322.
54. Smith, G.P. Small binding proteins selected from a combinatorial repertoire of knottins displayed on phage. J. Mol. Biol. 1998, 277, 317-332. (Pubitemid 28174971)
55. Dennis, M.S.; Lazarus, R.A. Kunitz domain inhibitors of tissue factor-factor VIIa. II. Potent and specific inhibitors by competitive phage selection. J. Biol. Chem. 1994, 269, 22137-22144.
56. Ley, A.C.; Markland, W.; Ladner, R.C. Obtaining a family of high-affinity, high-specificity protein inhibitors of plasmin and plasma kallikrein. Mol. Divers. 1996, 2, 119-124. (Pubitemid 126817074)
57. Markland, W.; Ley, A.C.; Ladner, R.C. Iterative optimization of high-affinity protease inhibitors using phage display. 2. Plasma kallikrein and thrombin. Biochemistry 1996, 35, 8058-8067. (Pubitemid 26202548)
58. Li, R.; Hoess, R.H.; Bennett, J.S.; DeGrado, W.F. Use of phage display to probe the evolution of binding specificity and affinity in integrins. Protein Eng. 2003, 16, 65-72. (Pubitemid 36407066)
59. McConnell, S.J.; Hoess, R.H. Tendamistat as a scaffold for conformationally constrained phage peptide libraries. J. Mol. Biol. 1995, 250, 460-470.
60. Craik, D.J.; Clark, R.J.; Daly, N.L. Potential therapeutic applications of the cyclotides and related cystine knot mini-proteins. Expert Opin. Investig. Drugs 2007, 16, 595-604. (Pubitemid 46723268)
61. Craik, D.J.; Simonsen, S.; Daly, N.L. The cyclotides: Novel macrocyclic peptides as scaffolds in drug design. Curr. Opin. Drug Discov. Develop. 2002, 5, 251-260. (Pubitemid 35012711)
62. Wentzel, A.; Christmann, A.; Adams, T.; Kolmar, H. Display of passenger proteins on the surface of Escherichia coli K-12 by the enterohemorrhagic E. coli intimin EaeA. J. Bacteriol. 2001, 183, 7273-7284. (Pubitemid 33121862)
63. Le Nguyen, D.; Heitz, A.; Chiche, L.; Castro, B.; Boigegrain, R.A.; Favel, A.; Coletti-Previero, M.A. Molecular recognition between serine proteases and new bioactive microproteins with a knotted structure. Biochimie 1990, 72, 431-435. (Pubitemid 20335939)
64. Craik, D.J.; Cemazar, M.; Daly, N.L. The chemistry and biology of cyclotides. Curr. Opin. Drug Discov. Develop. 2007, 10, 176-184. (Pubitemid 46438647)
65. Craik, D.J.; Cemazar, M.; Wang, C.K.; Daly, N.L. The cyclotide family of circular miniproteins: Nature's combinatorial peptide template. Biopolymers 2006, 84, 250-266.
66. Heitz, A.; Le-Nguyen, D.; Chiche, L. Min-21 and min-23, the smallest peptides that fold like a cystine-stabilized beta-sheet motif: Design, solution structure, and thermal stability. Biochemistry 1999, 38, 10615-10625.
67. Heitz, A.; Chiche, L.; Le-Nguyen, D.; Castro, B. Folding of the Squash Trypsin Inhibitor EETI II. Eur. J. Biochem. 1995, 233, 837-846.
68. Reiss, S.; Sieber, M.; Oberle, V.; Wentzel, A.; Spangenberg, P.; Claus, R.; Kolmar, H.; Losche, W. Inhibition of platelet aggregation by grafting RGD and KGD sequences on the structural scaffold of small disulfide-rich proteins. Platelets 2006, 17, 153-157. (Pubitemid 43791626)
69. Kimura, R.H.; Levin, A.M.; Cochran, F.V.; Cochran, J.R. Engineered cystine knot peptides that bind alphavbeta3, alphavbeta5, and alpha5beta1 integrins with low-nanomolar affinity. Proteins 2009, 77, 359-369.
70. Kimura, R.H.; Cheng, Z.; Gambhir, S.S.; Cochran, J.R. Engineered knottin peptides: A new class of agents for imaging integrin expression in living subjects. Cancer Res. 2009, 69, 2435-2442.
71. Nielsen, C.H.; Kimura, R.H.; Withofs, N.; Tran, P.T.; Miao, Z.; Cochran, J.R.; Cheng, Z.; Felsher, D.; Kjaer, A.; Willmann, J.K.; Gambhir, S.S. PET imaging of tumor neovascularization in a transgenic mouse model with a novel 64Cu-DOTA-knottin peptide. Cancer Res. 2010, 70, 9022-9030.
72. Colgrave, M.L.; Korsinczky, M.J.L.; Clark, R.J.; Foley, F.; Craik, D.J. Sunflower trypsin inhibitor-1, proteolytic studies on a trypsin inhibitor peptide and its analogs. J. Pept. Sci. 2010, 94, 665-672.
73. Nilsson, B.; Moks, T.; Jansson, B.; Abrahmsen, L.; Elmblad, A.; Holmgren, E.; Henrichson, C.; Jones, T.A.; Uhlen, M. A synthetic IgG-binding domain based on staphylococcal protein A. Protein Eng. 1987, 1, 107-113.
74. Nord, K.; Nilsson, J.; Nilsson, B.; Uhlen, M.; Nygren, P.A. A combinatorial library of an alphahelical bacterial receptor domain. Protein Eng. 1995, 8, 601-608.
75. Nygren, P.A. Alternative binding proteins: Affibody binding proteins developed from a small three-helix bundle scaffold. FEBS J. 2008, 275, 2668-2676.
76. Ronnmark, J.; Hansson, M.; Nguyen, T.; Uhlen, M.; Robert, A.; Stahl, S.; Nygren, P.A. Construction and characterization of affibody-Fc chimeras produced in Escherichia coli. J. Immunol. Methods 2002, 261, 199-211. (Pubitemid 34175229)
77. Engfeldt, T.; Renberg, B.; Brumer, H.; Nygren, P.A.; Karlstrom, A.E. Chemical synthesis of triple-labelled three-helix bundle binding proteins for specific fluorescent detection of unlabelled protein. ChemBioChem 2005, 6, 1043-1050. (Pubitemid 40825345)
78. Nissen, F.; Kraft, T.E.; Ruppert, T.; Eisenhut, M.; Haberkorn, U.; Mier, W. Hot or not - the influence of elevated temperature and microwave irradiation on the solid phase synthesis of an affibody. Tetrahedron Lett. 2010, 51, 6216-6219.
79. Tolmachev, V. Imaging of HER-2 overexpression in tumors for guiding therapy. Curr. Pharm. Des. 2008, 14, 2999-3019.
80. Wikman, M.; Steffen, A.C.; Gunneriusson, E.; Tolmachev, V.; Adams, G.P.; Carlsson, J.; Stahl, S. Selection and characterization of HER2/neu-binding affibody ligands. Protein Eng. Des. Sel. 2004, 17, 455-462. (Pubitemid 39294720)
81. Engfeldt, T.; Orlova, A.; Tran, T.; Bruskin, A.; Widstrom, C.; Karlstrom, A.E.; Tolmachev, V. Imaging of HER2-expressing tumours using a synthetic Affibody molecule containing the 99mTc-chelating mercaptoacetyl-glycyl-glycyl- glycyl (MAG3) sequence. Eur. J. Nucl. Med. Mol. Imaging 2007, 34, 722-733. (Pubitemid 46669355)
82. Engfeldt, T.; Tran, T.; Orlova, A.; Widstrom, C.; Feldwisch, J.; Abrahmsen, L.; Wennborg, A.; Karlstrom, A.E.; Tolmachev, V. 99mTc-chelator engineering to improve tumour targeting properties of a HER2-specific Affibody molecule. Eur. J. Nucl. Med. Mol. Imaging 2007, 34, 1843-1853. (Pubitemid 47599054)
83. Orlova, A.; Magnusson, M.; Eriksson, T.L.; Nilsson, M.; Larsson, B.; Hoiden-Guthenberg, I.; Widstrom, C.; Carlsson, J.; Tolmachev, V.; Stahl, S.; Nilsson, F.Y. Tumor imaging using a picomolar affinity HER2 binding affibody molecule. Cancer Res. 2006, 66, 4339-4348.
84. Orlova, A.; Tran, T.; Widstrom, C.; Engfeldt, T.; Eriksson Karlstrom, A.; Tolmachev, V. Preclinical evaluation of [111In]-benzyl-DOTA-Z(HER2:342), a potential agent for imaging of HER2 expression in malignant tumors. Int. J. Mol. Med. 2007, 20, 397-404.
85. Tran, T.; Engfeldt, T.; Orlova, A.; Sandstrom, M.; Feldwisch, J.; Abrahmsen, L.; Wennborg, A.; Tolmachev, V.; Karlstrom, A.E. (99m)Tc-maEEE- Z(HER2:342), an Affibody molecule-based tracer for the detection of HER2 expression in malignant tumors. Bioconjug. Chem. 2007, 18, 1956-1964. (Pubitemid 350219996)
86. Baum, R.P.; Prasad, V.; Muller, D.; Schuchardt, C.; Orlova, A.; Wennborg, A.; Tolmachev, V.; Feldwisch, J. Molecular imaging of HER2-expressing malignant tumors in breast cancer patients using synthetic 111In- or 68Ga-labeled affibody molecules. J. Nucl. Med. 2010, 51, 892-897.
87. Molina, R.; Barak, V.; van Dalen, A.; Duffy, M.J.; Einarsson, R.; Gion, M.; Goike, H.; Lamerz, R.; Nap, M.; Soletormos, G.; Stieber, P. Tumor markers in breast cancer- European Group on Tumor Markers recommendations. Tumour Biol. 2005, 26, 281-293. (Pubitemid 41619458)
88. Zidan, J.; Dashkovsky, I.; Stayerman, C.; Basher, W.; Cozacov, C.; Hadary, A. Comparison of HER-2 overexpression in primary breast cancer and metastatic sites and its effect on biological targeting therapy of metastatic disease. Br. J. Cancer 2005, 93, 552-556. (Pubitemid 43079998)
89. Binz, H.K.; Amstutz, P.; Kohl, A.; Stumpp, M.T.; Briand, C.; Forrer, P.; Grutter, M.G.; Pluckthun, A. High-affinity binders selected from designed ankyrin repeat protein libraries. Nat. Biotechnol. 2004, 22, 575-582. (Pubitemid 38590636)
90. Stumpp, M.T.; Forrer, P.; Binz, H.K.; Pluckthun, A. Designing repeat proteins: Modular leucinerich repeat protein libraries based on the mammalian ribonuclease inhibitor family. J. Mol. Biol. 2003, 332, 471-487. (Pubitemid 37020958)
91. Dennis, M.S.; Lazarus, R.A. Kunitz domain inhibitors of tissue factor-factor VIIa. I. Potent inhibitors selected from libraries by phage display. J. Biol. Chem. 1994, 269, 22129-22136.
92. Garnock-Jones, K.P. Ecallantide: In acute hereditary angioedema. Drugs 2010, 70, 1423-1431.
93. Lehmann, A. Ecallantide (DX-88), a plasma kallikrein inhibitor for the treatment of hereditary angioedema and the prevention of blood loss in on-pump cardiothoracic surgery. Expert Opin. Biol. Ther. 2008, 8, 1187-1199.
94. Williams, A.; Baird, L.G. DX-88 and HAE: A developmental perspective. Transfus. Apher. Sci. 2003, 29, 255-258. (Pubitemid 37315589)
95. Attucci, S.; Gauthier, A.; Korkmaz, B.; Delepine, P.; Martino, M.F.; Saudubray, F.; Diot, P.; Gauthier, F. EPI-hNE4, a proteolysis-resistant inhibitor of human neutrophil elastase and potential anti-inflammatory drug for treating cystic fibrosis. J. Pharmacol. Exp. Ther. 2006, 318, 803-809. (Pubitemid 44061254)
96. Lindner, T.; Kolmar, H.; Haberkorn, U.; Mier, W. DNA libraries for the construction of phage libraries: Statistical and structural requirements and synthetic methods. Molecules 2011, 16, 1625-1641.