Anticalins Reveal High Plasticity in the Mode of Complex Formation with a Common Tumor Antigen

Structure

Volumn 26, Issue 4, 2018, Pages 649-656.e3

  Schiefner, André ^a   Gebauer, Michaela ^a,b   Richter, Antonia ^a,c   Skerra, Arne ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b XL Protein GmbH   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

extra domain B; fibronectin; lipocalin 2; non Ig scaffold; structural plasticity; X ray structure analysis

Indexed keywords

ANTICALIN; BINDING PROTEIN; FIBRONECTIN; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; EPITOPE; LCN2 PROTEIN, HUMAN; ONCOFETAL FIBRONECTIN; PEPTIDE; PROTEIN BINDING; RECOMBINANT PROTEIN; TUMOR ANTIGEN;

ARTICLE; COMPLEX FORMATION; PHAGE DISPLAY; PLASTICITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY; ALPHA HELIX; AMINO ACID SEQUENCE; BETA SHEET; BINDING SITE; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENE VECTOR; GENETICS; HUMAN; METABOLISM; MOLECULAR CLONING; MOLECULAR MODEL; PEPTIDE LIBRARY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; ANTIGENS, NEOPLASM; BINDING SITES; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; EPITOPES; ESCHERICHIA COLI; FIBRONECTINS; GENE EXPRESSION; GENETIC VECTORS; HUMANS; LIPOCALIN-2; MODELS, MOLECULAR; PEPTIDE LIBRARY; PEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION, ALPHA-HELICAL; PROTEIN CONFORMATION, BETA-STRAND; PROTEIN ENGINEERING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 85042929056     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2018.02.003     Document Type: Article

References (53)

1. Albrecht, V., Richter, A., Pfeiffer, S., Gebauer, M., Lindner, S., Gieser, E., Schüller, U., Schichor, C., Gildehaus, F.J., Bartenstein, P., et al. Anticalins directed against the fibronectin extra domain B as diagnostic tracers for glioblastomas. Int. J. Cancer 138 (2016), 1269–1280.
2. Bachmann, B.J., Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol. Rev. 36 (1972), 525–557.
3. Balza, E., Sassi, F., Ventura, E., Parodi, A., Fossati, S., Blalock, W., Carnemolla, B., Castellani, P., Zardi, L., Borsi, L., A novel human fibronectin cryptic sequence unmasked by the insertion of the angiogenesis-associated extra type III domain B. Int. J. Cancer 125 (2009), 751–758.
4. Barinka, C., Ptacek, J., Richter, A., Novakova, Z., Morath, V., Skerra, A., Selection and characterization of Anticalins targeting human prostate-specific membrane antigen (PSMA). Protein Eng. Des. Sel. 29 (2016), 105–115.
5. Bentley, G.A., The crystal structures of complexes formed between lysozyme and antibody fragments. EXS 75 (1996), 301–319.
6. Binz, H.K., Amstutz, P., Plückthun, A., Engineering novel binding proteins from nonimmunoglobulin domains. Nat. Biotechnol. 23 (2005), 1257–1268.
7. Bond, C.S., Schüttelkopf, A.W., ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments. Acta Crystallogr. D Biol. Crystallogr. 65 (2009), 510–512.
8. Carnemolla, B., Leprini, A., Allemanni, G., Saginati, M., Zardi, L., The inclusion of the type III repeat ED-B in the fibronectin molecule generates conformational modifications that unmask a cryptic sequence. J. Biol. Chem. 267 (1992), 24689–24692.
9. Carnemolla, B., Neri, D., Castellani, P., Leprini, A., Neri, G., Pini, A., Winter, G., Zardi, L., Phage antibodies with pan-species recognition of the oncofoetal angiogenesis marker fibronectin ED-B domain. Int. J. Cancer 68 (1996), 397–405.
10. Connolly, M.L., Analytical molecular surface calculation. J. Appl. Crystallogr. 16 (1983), 548–558.
11. Davis, I.W., Leaver-Fay, A., Chen, V.B., Block, J.N., Kapral, G.J., Wang, X., Murray, L.W., Arendall, W.B. 3rd, Snoeyink, J., Richardson, J.S., et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35 (2007), W375–W383.
12. De Genst, E., Silence, K., Decanniere, K., Conrath, K., Loris, R., Kinne, J., Muyldermans, S., Wyns, L., Molecular basis for the preferential cleft recognition by dromedary heavy-chain antibodies. Proc. Natl. Acad. Sci. USA 103 (2006), 4586–4591.
13. Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K., Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 486–501.
14. Fattorusso, R., Pellecchia, M., Viti, F., Neri, P., Neri, D., Wüthrich, K., NMR structure of the human oncofoetal fibronectin ED-B domain, a specific marker for angiogenesis. Structure 7 (1999), 381–390.
15. Friedrich, L., Kornberger, P., Mendler, C.T., Multhoff, G., Schwaiger, M., Skerra, A., Selection of an Anticalin® against the membrane form of Hsp70 via bacterial surface display and its theranostic application in tumour models. Biol. Chem. 399 (2018), 235–252.
16. Gebauer, M., Schiefner, A., Matschiner, G., Skerra, A., Combinatorial design of an Anticalin directed against the extra-domain B for the specific targeting of oncofetal fibronectin. J. Mol. Biol. 425 (2013), 780–802.
17. Gebauer, M., Skerra, A., Engineered protein scaffolds as next-generation antibody therapeutics. Curr. Opin. Chem. Biol. 13 (2009), 245–255.
18. Gebauer, M., Skerra, A., Anticalins: small engineered binding proteins based on the lipocalin scaffold. Methods Enzymol. 503 (2012), 157–188.
19. Gebauer, M., Skerra, A., Alternative protein scaffolds as novel biotherapeutics. Rosenberg, A., Demeule, B., (eds.) Biobetters – Protein Engineering to Approach the Curative, 2015, Springer, 221–268.
20. Gilbreth, R.N., Koide, S., Structural insights for engineering binding proteins based on non-antibody scaffolds. Curr. Opin. Struct. Biol. 22 (2012), 413–420.
21. Goetz, D.H., Holmes, M.A., Borregaard, N., Bluhm, M.E., Raymond, K.N., Strong, R.K., The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol. Cell 10 (2002), 1033–1043.
22. Jarasch, A., Kopp, M., Eggenstein, E., Richter, A., Gebauer, M., Skerra, A., ANTICALIgn: visualizing, editing and analyzing combined nucleotide and amino acid sequence alignments for combinatorial protein engineering. Protein Eng. Des. Sel. 29 (2016), 263–270.
23. Kabsch, W., XDS. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 125–132.
24. Kim, H.J., Eichinger, A., Skerra, A., High-affinity recognition of lanthanide(III) chelate complexes by a reprogrammed human lipocalin 2. J. Am. Chem. Soc. 131 (2009), 3565–3576.
25. Krissinel, E., Henrick, K., Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372 (2007), 774–797.
26. Lawrence, M.C., Colman, P.M., Shape complementarity at protein/protein interfaces. J. Mol. Biol. 234 (1993), 946–950.
27. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., Read, R.J., Phaser crystallographic software. J. Appl. Crystallogr. 40 (2007), 658–674.
28. Mueller, U., Darowski, N., Fuchs, M.R., Förster, R., Hellmig, M., Paithankar, K.S., Pühringer, S., Steffien, M., Zocher, G., Weiss, M.S., Facilities for macromolecular crystallography at the Helmholtz-Zentrum Berlin. J. Synchrotron Radiat. 19 (2012), 442–449.
29. Murshudov, G.N., Skubak, P., Lebedev, A.A., Pannu, N.S., Steiner, R.A., Nicholls, R.A., Winn, M.D., Long, F., Vagin, A.A., REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67 (2011), 355–367.
30. Muyldermans, S., Nanobodies: natural single-domain antibodies. Annu. Rev. Biochem. 82 (2013), 775–797.
31. Neri, D., Carnemolla, B., Nissim, A., Leprini, A., Querze, G., Balza, E., Pini, A., Tarli, L., Halin, C., Neri, P., et al. Targeting by affinity-matured recombinant antibody fragments of an angiogenesis associated fibronectin isoform. Nat. Biotechnol. 15 (1997), 1271–1275.
32. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., Ferrin, T.E., UCSF Chimera – a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004), 1605–1612.
33. Pini, A., Viti, F., Santucci, A., Carnemolla, B., Zardi, L., Neri, P., Neri, D., 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.
34. Rauth, S., Hinz, D., Börger, M., Uhrig, M., Mayhaus, M., Riemenschneider, M., Skerra, A., High-affinity Anticalins with aggregation-blocking activity directed against the Alzheimer β-amyloid peptide. Biochem. J. 473 (2016), 1563–1578.
35. Richter, A., Eggenstein, E., Skerra, A., Anticalins: exploiting a non-Ig scaffold with hypervariable loops for the engineering of binding proteins. FEBS Lett. 588 (2014), 213–218.
36. Richter, A., Skerra, A., Anticalins directed against vascular endothelial growth factor receptor 3 (VEGFR-3) with picomolar affinities show potential for medical therapy and in vivo imaging. Biol. Chem. 398 (2017), 39–55.
37. Schiefner, A., Gebauer, M., Skerra, A., Extra-domain B in oncofetal fibronectin structurally promotes fibrillar head-to-tail dimerization of extracellular matrix protein. J. Biol. Chem. 287 (2012), 17578–17588.
38. Schiefner, A., Skerra, A., The menagerie of human lipocalins: a natural protein scaffold for molecular recognition of physiological compounds. Acc. Chem. Res. 48 (2015), 976–985.
39. Schiweck, W., Skerra, A., 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.
40. Schönfeld, D., Matschiner, G., Chatwell, L., Trentmann, S., Gille, H., Hülsmeyer, M., Brown, N., Kaye, P.M., Schlehuber, S., Hohlbaum, A.M., et al. 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.
41. Schwarzbauer, J.E., DeSimone, D.W., Fibronectins, their fibrillogenesis, and in vivo functions. Cold Spring Harb. Perspect. Biol., 3, 2011, a005041.
42. Singh, P., Carraher, C., Schwarzbauer, J.E., Assembly of fibronectin extracellular matrix. Annu. Rev. Cell Dev. Biol. 26 (2010), 397–419.
43. Siontorou, C.G., Nanobodies as novel agents for disease diagnosis and therapy. Int. J. Nanomedicine 8 (2013), 4215–4227.
44. Skerra, A., Engineered protein scaffolds for molecular recognition. J. Mol. Recognit. 13 (2000), 167–187.
45. Skerra, A., Lipocalins as a scaffold. Biochim. Biophys. Acta 1482 (2000), 337–350.
46. Skerra, A., Imitating the humoral immune response. Curr. Opin. Chem. Biol. 7 (2003), 683–693.
47. Stanfield, R.L., Gorny, M.K., Williams, C., Zolla-Pazner, S., Wilson, I.A., Structural rationale for the broad neutralization of HIV-1 by human monoclonal antibody 447-52D. Structure 12 (2004), 193–204.
48. Strohl, W.R., Strohl, L.M., Therapeutic Antibody Engineering: Current and Future Advances Driving the Strongest Growth Area in the Pharmaceutical Industry. 2012, Woodhead Publishing.
49. Tóth-Petróczy, A., Tawfik, D.S., The robustness and innovability of protein folds. Curr. Opin. Struct. Biol. 26 (2014), 131–138.
50. Ventura, E., Cordazzo, C., Quarto, R., Zardi, L., Rosano, C., C6: a monoclonal antibody specific for a fibronectin epitope situated at the interface between the oncofoetal extra-domain B and the repeat III8. PLoS One, 11, 2016, e0148103.
51. White, E.S., Baralle, F.E., Muro, A.F., New insights into form and function of fibronectin splice variants. J. Pathol. 216 (2008), 1–14.
52. Whittle, J.R., Zhang, R., Khurana, S., King, L.R., Manischewitz, J., Golding, H., Dormitzer, P.R., Haynes, B.F., Walter, E.B., Moody, M.A., et al. Broadly neutralizing human antibody that recognizes the receptor-binding pocket of influenza virus hemagglutinin. Proc. Natl. Acad. Sci. USA 108 (2011), 14216–14221.
53. Zemlin, M., Klinger, M., Link, J., Zemlin, C., Bauer, K., Engler, J.A., Schroeder, H.W. Jr., Kirkham, P.M., Expressed murine and human CDR-H3 intervals of equal length exhibit distinct repertoires that differ in their amino acid composition and predicted range of structures. J. Mol. Biol. 334 (2003), 733–749.