Combinatorial design of an anticalin directed against the extra-domain b for the specific targeting of oncofetal fibronectin

Journal of Molecular Biology

Volumn 425, Issue 4, 2013, Pages 780-802

  Gebauer, Michaela ^a   Schiefner, André ^a   Matschiner, Gabriele ^b   Skerra, Arne ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b Pieris Pharmaceuticals GmbH   (Germany)

Author keywords

lipocalin 2; NGAL; phage display; protein scaffold; X ray analysis

Indexed keywords

ANTICALIN; BINDING PROTEIN; EPITOPE; FIBRONECTIN; MONOMER; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIOPHAGE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN TARGETING; TUMOR CELL;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84873414124     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.12.004     Document Type: Article

References (115)

1. R. Pankov, and K.M. Yamada Fibronectin at a glance J. Cell Sci. 115 2002 3861 3863
2. R.O. Hynes Fibronectins A. Rich, Springer's Series in Molecular Biology 1990 Springer-Verlag New York 546 ff
3. R.O. Hynes The extracellular matrix: not just pretty fibrils Science 326 2009 1216 1219
4. H.P. Erickson, N. Carrell, and J. McDonagh Fibronectin molecule visualized in electron microscopy: a long, thin, flexible strand J. Cell Biol. 91 1981 673 678
5. K.J. Johnson, H. Sage, G. Briscoe, and H.P. Erickson The compact conformation of fibronectin is determined by intramolecular ionic interactions J. Biol. Chem. 274 1999 15473 15479
6. J.E. Schwarzbauer, and D.W. DeSimone Fibronectins, their fibrillogenesis, and in vivo functions Cold Spring Harbor Perspect. Biol. 3 2011 a005041
7. A. Schiefner, M. Gebauer, and A. Skerra Extra-domain B in oncofetal fibronectin structurally promotes fibrillar head-to-tail dimerization of extracellular matrix protein J. Biol. Chem. 287 2012 17578 17588
8. J.R. Potts, and I.D. Campbell Fibronectin structure and assembly Curr. Opin. Cell Biol. 6 1994 648 655
9. J.R. Potts, and I.D. Campbell Structure and function of fibronectin modules Matrix Biol. 15 1996 313 320
10. 2F2 fragment from human fibronectin enhances gelatin binding EMBO J. 20 2001 1519 1529
11. D.J. Leahy, I. Aukhil, and H.P. Erickson 2.0 Å crystal structure of a four-domain segment of human fibronectin encompassing the RGD loop and synergy region Cell 84 1996 155 164
12. R.J. Bingham, E. Rudino-Pinera, N.A. Meenan, U. Schwarz-Linek, J.P. Turkenburg, and M. Hook Crystal structures of fibronectin-binding sites from Staphylococcus aureus FnBPA in complex with fibronectin domains Proc. Natl Acad. Sci. USA 105 2008 12254 12258
13. E. Ruoslahti Fibronectin and its receptors Annu. Rev. Biochem. 57 1988 375 413
14. C. Ffrench-Constant Alternative splicing of fibronectin - many different proteins but few different functions Exp. Cell Res. 1995 261 271
15. H. Kosmehl, A. Berndt, and D. Katenkamp Molecular variants of fibronectin and laminin: structure, physiological occurrence and histopathological aspects Virchows Arch. 429 1996 311 322
16. E.S. White, F.E. Baralle, and A.F. Muro New insights into form and function of fibronectin splice variants J. Pathol. 216 2008 1 14
17. J.E. Schwarzbauer, R.S. Patel, D. Fonda, and R.O. Hynes Multiple sites of alternative splicing of the rat fibronectin gene transcript EMBO J. 6 1987 2573 2580
18. L. Zardi, B. Carnemolla, A. Siri, T.E. Petersen, G. Paolella, G. Sebastio, and F.E. Baralle Transformed human cells produce a new fibronectin isoform by preferential alternative splicing of a previously unobserved exon EMBO J. 6 1987 2337 2342
19. C. Ffrench-Constant, and R.O. Hynes Alternative splicing of fibronectin is temporally and spatially regulated in the chicken embryo Development 106 1989 375 388
20. C. Ffrench-Constant, L. Van de Water, H.F. Dvorak, and R.O. Hynes Reappearance of an embryonic pattern of fibronectin splicing during wound healing in the adult rat J. Cell Biol. 109 1989 903 914
21. P. Castellani, G. Viale, A. Dorcaratto, G. Nicolo, J. Kaczmarek, G. Querze, and L. Zardi The fibronectin isoform containing the ED-B oncofetal domain: a marker of angiogenesis Int. J. Cancer 59 1994 612 618
22. E. Ruoslahti Specialization of tumour vasculature Nat. Rev. Cancer 2 2002 83 90
23. F. Oyama, S. Hirohashi, Y. Shimosato, K. Titani, and K. Sekiguchi Oncodevelopmental regulation of the alternative splicing of fibronectin pre-messenger RNA in human lung tissues Cancer Res. 50 1990 1075 1078
24. + isoforms by human and experimental colorectal cancer. Contribution of cancer cells and tumor-associated myofibroblasts Am. J. Pathol. 148 1996 579 592
25. D.H. Ausprunk, and J. Folkman Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis Microvasc. Res. 14 1977 53 65
26. J. Folkman How is blood vessel growth regulated in normal and neoplastic tissue? Cancer Res. 46 1986 467 473
27. P. Hahnfeldt, D. Panigrahy, J. Folkman, and L. Hlatky Tumor development under angiogenic signaling: a dynamical theory of tumor growth, treatment response, and postvascular dormancy Cancer Res. 59 1999 4770 4775
28. M. Santimaria, G. Moscatelli, G.L. Viale, L. Giovannoni, G. Neri, and F. Viti Immunoscintigraphic detection of the ED-B domain of fibronectin, a marker of angiogenesis, in patients with cancer Clin. Cancer Res. 9 2003 571 579
29. P. Castellani, L. Borsi, B. Carnemolla, A. Biro, A. Dorcaratto, and G.L. Viale Differentiation between high- and low-grade astrocytoma using a human recombinant antibody to the extra domain-B of fibronectin Am. J. Pathol. 161 2002 1695 1700
30. M.T. Birchler, C. Thuerl, D. Schmid, D. Neri, R. Waibel, and A. Schubiger Immunoscintigraphy of patients with head and neck carcinomas, with an anti-angiogenetic antibody fragment Otolaryngol. Head Neck Surg. 136 2007 543 548
31. K. Wagner, P. Schulz, A. Scholz, B. Wiedenmann, and A. Menrad The targeted immunocytokine L19-IL2 efficiently inhibits the growth of orthotopic pancreatic cancer Clin. Cancer Res. 14 2008 4951 4960
32. 131I-L19SIP radioimmunotherapy in Hodgkin lymphoma patients Blood 113 2009 2265 2274
33. R. Fattorusso, M. Pellecchia, F. Viti, P. Neri, D. Neri, and K. Wüthrich NMR structure of the human oncofoetal fibronectin ED-B domain, a specific marker for angiogenesis Structure 7 1999 381 390
34. J.W. Tamkun, and R.O. Hynes Plasma fibronectin is synthesized and secreted by hepatocytes J. Biol. Chem. 258 1983 4641 4647
35. L. Borsi, E. Balza, M. Bestagno, P. Castellani, B. Carnemolla, and A. Biro Selective targeting of tumoral vasculature: comparison of different formats of an antibody (L19) to the ED-B domain of fibronectin Int. J. Cancer 102 2002 75 85
36. M. Kaspar, L. Zardi, and D. Neri Fibronectin as target for tumor therapy Int. J. Cancer 118 2006 1331 1339
37. C. Schliemann, and D. Neri Antibody-based targeting of the tumor vasculature Biochim. Biophys. Acta 1776 2007 175 192
38. 131I-L19-SIP radioimmunotherapy Eur. J. Nucl. Med. Mol. Imaging 36 2009 1235 1244
39. D. Neri, and R. Bicknell Tumour vascular targeting Nat. Rev. Cancer 5 2005 436 446
40. C. Schliemann, A. Palumbo, K. Zuberbuhler, A. Villa, M. Kaspar, and E. Trachsel Complete eradication of human B-cell lymphoma xenografts using rituximab in combination with the immunocytokine L19-IL2 Blood 113 2009 2275 2283
41. L. Tarli, E. Balza, F. Viti, L. Borsi, P. Castellani, and D. Berndorff A high-affinity human antibody that targets tumoral blood vessels Blood 94 1999 192 198
42. C. Halin, S. Rondini, F. Nilsson, A. Berndt, H. Kosmehl, L. Zardi, and D. Neri Enhancement of the antitumor activity of interleukin-12 by targeted delivery to neovasculature Nat. Biotechnol. 20 2002 264 269
43. S. Demartis, L. Tarli, L. Borsi, L. Zardi, and D. Neri Selective targeting of tumour neovasculature by a radiohalogenated human antibody fragment specific for the ED-B domain of fibronectin Eur. J. Nucl. Med. 28 2001 534 539
44. B. Carnemolla, L. Borsi, E. Balza, P. Castellani, R. Meazza, and A. Berndt Enhancement of the antitumor properties of interleukin-2 by its targeted delivery to the tumor blood vessel extracellular matrix Blood 99 2002 1659 1665
45. S.M. Rudman, M.B. Jameson, M.J. McKeage, P. Savage, D.I. Jodrell, and M. Harries A phase 1 study of AS1409, a novel antibody-cytokine fusion protein, in patients with malignant melanoma or renal cell carcinoma Clin. Cancer Res. 17 2011 1998 2005
46. A. Pini, F. Viti, A. Santucci, B. Carnemolla, L. Zardi, P. Neri, and D. Neri Design and use of a phage display library. Human antibodies with subnanomolar affinity against a marker of angiogenesis eluted from a two-dimensional gel J. Biol. Chem. 273 1998 21769 21776
47. L. Borsi, E. Balza, B. Carnemolla, F. Sassi, P. Castellani, and A. Berndt Selective targeted delivery of TNFα to tumor blood vessels Blood 102 2003 4384 4392
48. C. Ebbinghaus, R. Ronca, M. Kaspar, D. Grabulovski, A. Berndt, and H. Kosmehl Engineered vascular-targeting antibody-interferon-γ fusion protein for cancer therapy Int. J. Cancer 116 2005 304 313
49. M. Kaspar, E. Trachsel, and D. Neri The antibody-mediated targeted delivery of interleukin-15 and GM-CSF to the tumor neovasculature inhibits tumor growth and metastasis Cancer Res. 67 2007 4940 4948
50. C. Halin, V. Gafner, M.E. Villani, L. Borsi, A. Berndt, and H. Kosmehl Synergistic therapeutic effects of a tumor targeting antibody fragment, fused to interleukin 12 and to tumor necrosis factor α Cancer Res. 63 2003 3202 3210
51. 131I-labeled antibody L19-SIP for selective targeting of tumor vasculature J. Nucl. Med. 47 2006 1127 1135
52. M. Johannsen, G. Spitaleri, G. Curigliano, J. Roigas, S. Weikert, and C. Kempkensteffen The tumour-targeting human L19-IL2 immunocytokine: preclinical safety studies, phase I clinical trial in patients with solid tumours and expansion into patients with advanced renal cell carcinoma Eur. J. Cancer 46 2010 2926 2935
53. 131I-L19SIP in solid cancers (SC) and lymphoproliferative diseases: final results of the first human trial J. Clin. Oncol. 28 2010 111 Suppl. abstr. 2523
54. M. Gebauer, and A. Skerra Engineered protein scaffolds as next-generation antibody therapeutics Curr. Opin. Chem. Biol. 13 2009 245 255
55. A. Skerra Engineered protein scaffolds for molecular recognition J. Mol. Recognit. 13 2000 167 187
56. A. Skerra Lipocalins as a scaffold Biochim. Biophys. Acta 1482 2000 337 350
57. A. Skerra Imitating the humoral immune response Curr. Opin. Chem. Biol. 7 2003 683 693
58. B. Åkerström, N. Borregaard, D.A. Flower, and J.-S. Salier Lipocalins 2006 Landes Bioscience Georgetown, Texas
59. M. Gebauer, and A. Skerra Anticalins: small engineered binding proteins based on the lipocalin scaffold Methods Enzymol. 503 2012 157 188
60. L. Kjeldsen, J.B. Cowland, and N. Borregaard Human neutrophil gelatinase-associated lipocalin and homologous proteins in rat and mouse Biochim. Biophys. Acta 1482 2000 272 283
61. H.J. Kim, A. Eichinger, and A. Skerra High-affinity recognition of lanthanide(III) chelate complexes by a reprogrammed human lipocalin 2 J. Am. Chem. Soc. 131 2009 3565 3576
62. D. Schönfeld, G. Matschiner, L. Chatwell, S. Trentmann, H. Gille, and M. Hülsmeyer An engineered lipocalin specific for CTLA-4 reveals a combining site with structural and conformational features similar to antibodies Proc. Natl Acad. Sci. USA 106 2009 8198 8203
63. C. Correnti, and R.K. Strong Mammalian siderophores, siderophore-binding lipocalins, and the labile iron pool J. Biol. Chem. 287 2012 13524 13531
64. D.H. Goetz, M.A. Holmes, N. Borregaard, M.E. Bluhm, K.N. Raymond, and R.K. Strong The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition Mol. Cell 10 2002 1033 1043
65. J. Van den Brulle, M. Fischer, T. Langmann, G. Horn, T. Waldmann, and S. Arnold A novel solid phase technology for high-throughput gene synthesis Biotechniques 45 2008 340 343
66. W.O. Bullock, J.M. Fernandez, and J.M. Short XL1-Blue: a high efficiency plasmid transforming recA Escherichia coli strain with β-galactosidase selection Biotechniques 5 1987 376 379
67. T.G. Schmidt, and A. Skerra The Strep-tag system for one-step purification and high-affinity detection or capturing of proteins Nat. Protoc. 2 2007 1528 1535
68. C. Marty, P. Scheidegger, K. Ballmer-Hofer, R. Klemenz, and R.A. Schwendener Production of functionalized single-chain Fv antibody fragments binding to the ED-B domain of the B-isoform of fibronectin in Pichia pastoris Protein Expr. Purif. 21 2001 156 164
69. J. Fogh, J.M. Fogh, and T. Orfeo One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice J. Natl. Cancer Inst. 59 1977 221 226
70. J. Fogh, and G. Trempe New human tumor cell lines J. Fogh, Human Tumor Cells in Vitro 1975 Plenum Publishing New York 115 141
71. I.W. Davis, A. Leaver-Fay, V.B. Chen, J.N. Block, G.J. Kapral, and X. Wang MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Nucleic Acids Res. 35 2007 W375 W383
72. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797
73. J. Janin, F. Rodier, P. Chakrabarti, and R.P. Bahadur Macromolecular recognition in the Protein Data Bank Acta Crystallogr., Sect. D: Biol. Crystallogr. 63 2007 1 8
74. M.C. Lawrence, and P.M. Colman Shape complementarity at protein/protein interfaces J. Mol. Biol. 234 1993 946 950
75. P. Alessi, C. Ebbinghaus, and D. Neri Molecular targeting of angiogenesis Biochim. Biophys. Acta 1654 2004 39 49
76. T.K. Eigentler, B. Weide, F. de Braud, G. Spitaleri, A. Romanini, and A. Pflugfelder A dose-escalation and signal-generating study of the immunocytokine L19-IL2 in combination with dacarbazine for the therapy of patients with metastatic melanoma Clin. Cancer Res. 17 2011 7732 7742
77. S. Schlehuber, and A. Skerra Lipocalins in drug discovery: from natural ligand-binding proteins to "anticalins" Drug Discov. Today 10 2005 23 33
78. Skerra, A., Gebauer, M., Hinz, D., Rauth, S. & Matschiner, G. (2011). Muteins of human lipocalin 2 (Lcn2, hNGAL) with affinity for a given target. WO 2011/069992 A2.
79. Trentmann, S., Matschiner, G. & Skerra, A. (2012). Binding proteins for hepcidin. WO 2012/022742 A1.
80. Matschiner, G. (2012). Muteins of human lipocalin 2 with affinity for glypican-3 (GPC3). WO 2012/065978 A1.
81. F. Viti, L. Tarli, L. Giovannoni, L. Zardi, and D. Neri Increased binding affinity and valence of recombinant antibody fragments lead to improved targeting of tumoral angiogenesis Cancer Res. 59 1999 347 352
82. K.M. Arndt, K.M. Müller, and A. Plückthun Factors influencing the dimer to monomer transition of an antibody single-chain Fv fragment Biochemistry 37 1998 12918 12926
83. y hu3S193 humanized antibody Protein Sci. 12 2003 734 747
84. R.V. Cordoba-Rodriguez Aggregates in MAbs and recombinant therapeutic proteins: a regulatory perspective Biopharm. Int. 21 2008 44ff
85. Y. Wan, S. Vasan, R. Ghosh, G. Hale, and Z. Cui Separation of monoclonal antibody alemtuzumab monomer and dimers using ultrafiltration Biotechnol. Bioeng. 90 2005 422 432
86. V. Kenanova, and A.M. Wu Tailoring antibodies for radionuclide delivery Expert Opin. Drug Deliv. 3 2006 53 70
87. P. Carter Improving the efficacy of antibody-based cancer therapies Nat. Rev. Cancer 1 2001 118 129
88. K.L. Gutbrodt, and D. Neri Immunocytokines Antibodies 1 2012 70 87
89. L domain confirms the structural model J. Mol. Biol. 238 1994 226 244
90. A. Skerra Use of the tetracycline promoter for the tightly regulated production of a murine antibody fragment in Escherichia coli Gene 151 1994 131 135
91. F.W. Studier, and B.A. Moffatt Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes J. Mol. Biol. 189 1986 113 130
92. J. Sambrook, E.F. Fritsch, and T. Maniatis Molecular Cloning: A Laboratory Manual 1989 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
93. A. Skerra A general vector, pASK84, for cloning, bacterial production, and single-step purification of antibody Fab fragments Gene 141 1994 79 84
94. S.C. Gill, and P.H. von Hippel Calculation of protein extinction coefficients from amino acid sequence data Anal. Biochem. 182 1989 319 326
95. ab fragment with improved affinity for the Nogo-A axonal growth inhibitor permits immunochemical detection and shows enhanced neutralizing activity Protein Eng. 15 2002 931 941
96. C. Yanisch-Perron, J. Vieira, and J. Messing Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors Gene 33 1985 103 119
97. M.J. Casadaban Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage Lambda and Mu J. Mol. Biol. 104 1976 541 555
98. M. Schlapschy, S. Grimm, and A. Skerra A system for concomitant overexpression of four periplasmic folding catalysts to improve secretory protein production in Escherichia coli Protein Eng. Des. Sel. 19 2006 385 390
99. W. Schiweck, and A. Skerra Fermenter production of an artificial Fab fragment, rationally designed for the antigen cystatin, and its optimized crystallization through constant domain shuffling Proteins 23 1995 561 565
100. D.A. Breustedt, D.L. Schönfeld, and A. Skerra Comparative ligand-binding analysis of ten human lipocalins Biochim. Biophys. Acta 1764 2006 161 173
101. D.J. O'Shannessy, M. Brigham-Burke, and K. Peck Immobilization chemistries suitable for use in the BIAcore surface plasmon resonance detector Anal. Biochem. 205 1992 132 136
102. D.G. Myszka Improving biosensor analysis J. Mol. Recognit. 12 1999 279 284
103. R. Karlsson, A. Michaelsson, and L. Mattsson Kinetic analysis of monoclonal antibody-antigen interactions with a new biosensor based analytical system J. Immunol. Methods 145 1991 229 240
104. D.G. Myszka, X. He, M. Dembo, T.A. Morton, and B. Goldstein Extending the range of rate constants available from BIACORE: interpreting mass transport-influenced binding data Biophys. J. 75 1998 583 594
105. W. Kabsch XDS Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 125 132
106. D.H. Goetz, S.T. Willie, R.S. Armen, T. Bratt, N. Borregaard, and R.K. Strong Ligand preference inferred from the structure of neutrophil gelatinase associated lipocalin Biochemistry 39 2000 1935 1941
107. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
108. G.N. Murshudov, P. Skubak, A.A. Lebedev, N.S. Pannu, R.A. Steiner, and R.A. Nicholls REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr., Sect. D: Biol. Crystallogr. 67 2011 355 367
109. R.J. Read Improved Fourier coefficients for maps using phases from partial structures with errors Acta Crystallogr., Sect. A: Found. Crystallogr. 42 1986 140 149
110. T.C. Terwilliger Maximum-likelihood density modification Acta Crystallogr., Sect. D: Biol. Crystallogr. 56 2000 965 972
111. A. Vagin, and A. Teplyakov MOLREP: an automated program for molecular replacement J. Appl. Crystallogr. 30 1997 1022 1025
112. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 486 501
113. J. Painter, and E.A. Merritt Optimal description of a protein structure in terms of multiple groups undergoing TLS motion Acta Crystallogr., Sect. D: Biol. Crystallogr. 62 2006 439 450
114. N.A. Baker, D. Sept, S. Joseph, M.J. Holst, and J.A. McCammon Electrostatics of nanosystems: application to microtubules and the ribosome Proc. Natl Acad. Sci. USA 98 2001 10037 10041
115. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612