Designing repeat proteins: Well-expressed, soluble and stable proteins from combinatorial libraries of consensus ankyrin repeat proteins

Journal of Molecular Biology

Volumn 332, Issue 2, 2003, Pages 489-503

  Binz, H Kaspar ^a   Stumpp, Michael T ^a   Forrer, Patrik ^a   Amstutz, Patrick ^a   Plückthun, Andreas ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Ankyrin repeat; Combinatorial library; Consensus sequence; Protein design; Scaffold

Indexed keywords

AMINO ACID; ANKYRIN; ANKYRIN REPEAT PROTEIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BIOTECHNOLOGICAL PROCEDURES; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; COMBINATORIAL LIBRARY; CYTOPLASM; ESCHERICHIA COLI; HYDROPHOBICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; THERMOSTABILITY;

ESCHERICHIA COLI;

EID: 0042780350     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00896-9     Document Type: Article

References (55)

1. Andrade M.A., Perez-Iratxeta C., Ponting C.P. Protein repeats: structures, functions, and evolution. J. Struct. Biol. 134:2001;117-131.
2. Kobe B., Kajava A.V. When protein folding is simplified to protein coiling: the continuum of solenoid protein structures. Trends Biochem. Sci. 25:2000;509-515.
3. Forrer P., Stumpp M.T., Binz H.K., Plückthun A. A novel strategy to design binding molecules harnessing the modular nature of repeat proteins. FEBS Letters. 539:2003;2-6.
4. Nygren P.-Å., Uhlén M. Scaffolds for engineering novel binding sites in proteins. Curr. Opin. Struct. Biol. 7:1997;463-469.
5. Skerra A. Engineered protein scaffolds for molecular recognition. J. Mol. Recognit. 13:2000;167-187.
6. Bork P. Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally? Proteins: Struct. Funct. Genet. 17:1993;363-374.
7. Letunic I., Goodstadt L., Dickens N.J., Doerks T., Schultz J., Mott R., et al. Recent improvements to the SMART domain-based sequence annotation resource. Nucl. Acids Res. 30:2002;242-244.
8. Gorina S., Pavletich N.P. Structure of the p53 tumor suppressor bound to the ankyrin and SH3 domains of 53BP2. Science. 274:1996;1001-1005.
9. Sedgwick S.G., Smerdon S.J. The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem. Sci. 24:1999;311-316.
10. Michaely P., Tomchick D.R., Machius M., Anderson R.G. Crystal structure of a 12 ANK repeat stack from human ankyrinR. EMBO J. 21:2002;6387-6396.
11. Suzuki F., Goto M., Sawa C., Ito S., Watanabe H., Sawada J., Handa H. Functional interactions of transcription factor human GA-binding protein subunits. J. Biol. Chem. 273:1998;29302-29308.
12. Malek S., Huxford T., Ghosh G. IκBα functions through direct contacts with the nuclear localization signals and the DNA binding sequences of NF-κB. J. Biol. Chem. 273:1998;25427-25435.
13. Stumpp M.T., Forrer P., Binz H.K., Plückthun A. Designing repeat proteins: modular leucine-rich repeat protein libraries based on the mammalian ribonuclease inhibitor family. J. Mol. Biol. 332:2003;471-487.
14. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22:1994;4673-4680.
15. Breeden L., Nasmyth K. Similarity between cell-cycle genes of budding yeast and fission yeast and the Notch gene of Drosophila. Nature. 329:1987;651-654.
16. Lux S.E., John K.M., Bennett V. Analysis of cDNA for human erythrocyte ankyrin indicates a repeated structure with homology to tissue-differentiation and cell-cycle control proteins. Nature. 344:1990;36-42.
17. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215:1990;403-410.
18. Benson D.A., Karsch-Mizrachi I., Lipman D.J., Ostell J., Rapp B.A., Wheeler D.L. GenBank. Nucl. Acids Res. 28:2000;15-18.
19. Bateman A., Birney E., Durbin R., Eddy S.R., Finn R.D., Sonnhammer E.L. Pfam 3.1: 1313 multiple alignments and profile HMMs match the majority of proteins. Nucl. Acids Res. 27:1999;260-262.
20. Luh F.Y., Archer S.J., Domaille P.J., Smith B.O., Owen D., Brotherton D.H., et al. Structure of the cyclin-dependent kinase inhibitor p19Ink4d. Nature. 389:1997;999-1003.
21. Batchelor A.H., Piper D.E., de la Brousse F.C., McKnight S.L., Wolberger C. The structure of GABPα/β: an ETS domain-ankyrin repeat heterodimer bound to DNA. Science. 279:1998;1037-1041.
22. INK4a: determination of solution structure and analyses of its interaction with cyclin-dependent kinase 4. Mol. Cell. 1:1998;421-431.
23. Huxford T., Huang D.B., Malek S., Ghosh G. The crystal structure of the IκBα/NF-κB complex reveals mechanisms of NF-κB inactivation. Cell. 95:1998;759-770.
24. Jacobs M.D., Harrison S.C. Structure of an IκBα/NF-κB complex. Cell. 95:1998;749-758.
25. Yang Y., Nanduri S., Sen S., Qin J. The structural basis of ankyrin-like repeat function as revealed by the solution structure of myotrophin. Structure. 6:1998;619-626.
26. INK4 mutations. Nature Struct. Biol. 5:1998;74-81.
27. Mandiyan V., Andreev J., Schlessinger J., Hubbard S.R. Crystal structure of the ARF-GAP domain and ankyrin repeats of PYK2-associated protein β EMBO J. 18:1999;6890-6898.
28. Foord R., Taylor I.A., Sedgwick S.G., Smerdon S.J. X-ray structural analysis of the yeast cell cycle regulator Swi6 reveals variations of the ankyrin fold and has implications for Swi6 function. Nature Struct. Biol. 6:1999;157-165.
29. Kohl A., Binz H.K., Forrer P., Stumpp M.T., Plückthun A., Grütter M.G. Designed to be stable: crystal structure of a consensus ankyrin repeat protein. Proc. Natl Acad. Sci. USA. 100:2003;1700-1705.
30. O'Neil K.T., DeGrado W.F. A thermodynamic scale for the helix-forming tendencies of the commonly occurring amino acids. Science. 250:1990;646-651.
31. Rost B. PHD: predicting one-dimensional protein structure by profile-based neural networks. Methods Enzymol. 266:1996;525-539.
32. Rogers S., Wells R., Rechsteiner M. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science. 234:1986;364-368.
33. Womble D.D. GCG: The Wisconsin Package of sequence analysis programs. Methods Mol. Biol. 132:2000;3-22.
34. Virnekäs B., Ge L., Plückthun 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. 22:1994;5600-5607.
35. Mosavi L.K., Williams S., Peng Z.-. Equilibrium folding and stability of myotrophin: a model ankyrin repeat protein. J. Mol. Biol. 320:2002;165-170.
36. Zweifel M.E., Barrick D. Studies of the ankyrin repeats of the Drosophila melanogaster Notch receptor. 1. Solution conformational and hydrodynamic properties. Biochemistry. 40:2001;14344-14356.
37. INK4d. J. Mol. Biol. 315:2002;447-457.
38. INK4. J. Mol. Biol. 299:2000;1121-1132.
39. Zweifel M.E., Barrick D. Studies of the ankyrin repeats of the Drosophila melanogaster Notch receptor. 2. Solution stability and cooperativity of unfolding. Biochemistry. 40:2001;14357-14367.
40. Lehmann M., Pasamontes L., Lassen S.F., Wyss M. The consensus concept for thermostability engineering of proteins. Biochim. Biophys. Acta. 1543:2000;408-415.
41. Knappik A., Ge L., Honegger A., Pack P., Fischer M., Wellnhofer G., et al. Fully synthetic human combinatorial antibody libraries (HuCAL) based on modular consensus frameworks and CDRs randomized with trinucleotides. J. Mol. Biol. 296:2000;57-86.
42. L domain stability. J. Mol. Biol. 291:1999;1119-1128.
43. Steipe B., Schiller B., Plückthun A., Steinbacher S. Sequence statistics reliably predict stabilizing mutations in a protein domain. J. Mol. Biol. 240:1994;188-192.
44. Wang Q., Buckle A.M., Fersht A.R. Stabilization of GroEL minichaperones by core and surface mutations. J. Mol. Biol. 298:2000;917-926.
45. Mosavi L.K., Minor D.L. Jr, Peng Z.-. Consensus-derived structural determinants of the ankyrin repeat motif. Proc. Natl Acad. Sci. USA. 99:2002;16029-16034.
46. Main E.R., Xiong Y., Cocco M.J., D'Andrea L., Regan L. Design of stable alpha-helical arrays from an idealized TPR motif. Structure (Camb.). 11:2003;497-508.
47. Michel F., Soler-Lopez M., Petosa C., Cramer P., Siebenlist U., Müller C.W. Crystal structure of the ankyrin repeat domain of Bcl-3: a unique member of the IκB protein family. EMBO J. 20:2001;6180-6190.
48. Nord K., Gunneriusson E., Ringdahl J., Ståhl S., Uhlén M., Nygren P.-Å. Binding proteins selected from combinatorial libraries of an α-helical bacterial receptor domain. Nature Biotechnol. 15:1997;772-777.
49. Hanes J., Plückthun A. In vitro selection and evolution of functional proteins by using ribosome display. Proc. Natl Acad. Sci. USA. 94:1997;4937-4942.
50. Amstutz P., Forrer P., Zahnd C., Plückthun A. In vitro display technologies: novel developments and applications. Curr. Opin. Biotechnol. 12:2001;400-405.
51. Cattaneo A., Biocca S. The selection of intracellular antibodies. Trends Biotechnol. 17:1999;115-121.
52. Berman H.M., Battistuz T., Bhat T.N., Bluhm W.F., Bourne P.E., Burkhardt K., et al. The Protein Data Bank. Acta Crystallog. sect. D. 58:2002;899-907.
53. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: a Laboratory Manual. 2nd edit. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
54. Koradi R., Billeter M., Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:1996;51-55.
55. Yang F., Forrer P., Dauter Z., Conway J.F., Cheng N., Cerritelli M.E., et al. Novel fold and capsid-binding properties of the lambda-phage display platform protein gpD. Nature Struct. Biol. 7:2000;230-237.