Directed Evolution of Streptavidin Variants Using In Vitro Compartmentalization

Chemistry and Biology

Volumn 15, Issue 9, 2008, Pages 979-989

  Levy, Matthew ^a   Ellington, Andrew D ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

CHEMBIO

Indexed keywords

DNA; STREPTAVIDIN;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; GENETIC VARIABILITY; GENETICS; KINETICS; METABOLISM; PROTEIN BINDING;

DNA; KINETICS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTEIN BINDING; STREPTAVIDIN; SUBSTRATE SPECIFICITY; VARIATION (GENETICS);

EID: 51649085576     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2008.07.017     Document Type: Article

References (60)

1. Aharoni A., Amitai G., Bernath K., Magdassi S., and Tawfik D.S. High-throughput screening of enzyme libraries: thiolactonases evolved by fluorescence-activated sorting of single cells in emulsion compartments. Chem. Biol. 12 (2005) 1281-1289
2. Aslan F.M., Yu Y., Mohr S.C., and Cantor C.R. Engineered single-chain dimeric streptavidins with an unexpected strong preference for biotin-4-fluorescein. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 8507-8512
3. Bayer E.A., and Wilchek M. Application of avidin-biotin technology to affinity-based separations. J. Chromatogr. 510 (1990) 3-11
4. Bertschinger J., Grabulovski D., and Neri D. Selection of single domain binding proteins by covalent DNA display. Protein Eng. Des. Sel. 20 (2007) 57-68
5. Boder E.T., Midelfort K.S., and Wittrup K.D. Directed evolution of antibody fragments with monovalent femtomolar antigen-binding affinity. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 10701-10705
6. Chilkoti A., and Stayton P.S. Molecular origins of the slow streptavidin-biotin dissociation kinetics. J. Am. Chem. Soc. 117 (1995) 10622-10628
7. Chilkoti A., Tan P.H., and Stayton P.S. Site-directed mutagenesis studies of the high-affinity streptavidin-biotin complex: contributions of tryptophan residues 79, 108, and 120. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 1754-1758
8. Cohen J.D., Sadowski J.P., and Dervan P.B. Programming multiple protein patterns on a single DNA nanostructure. J. Am. Chem. Soc. 130 (2008) 402-403
9. DeChancie J., and Houk K.N. The origins of femtomolar protein-ligand binding: hydrogen-bond cooperativity and desolvation energetics in the biotin-(strept)avidin binding site. J. Am. Chem. Soc. 129 (2007) 5419-5429
10. Dixon R.W., Radmer R.J., Kuhn B., Kollman P.A., Yang J., Raposo C., Wilcox C.S., Klumb L.A., Stayton P.S., Behnke C., et al. Theoretical and experimental studies of biotin analogues that bind almost as tightly to streptavidin as biotin. J. Org. Chem. 67 (2002) 1827-1837
11. Doi N., and Yanagawa H. STABLE: protein-DNA fusion system for screening of combinatorial protein libraries in vitro. FEBS Lett. 457 (1999) 227-230
12. Freitag S., Le Trong I., Klumb L., Stayton P.S., and Stenkamp R.E. Structural studies of the streptavidin binding loop. Protein Sci. 6 (1997) 1157-1166
13. Freitag S., Le Trong I., Chilkoti A., Klumb L.A., Stayton P.S., and Stenkamp R.E. Structural studies of binding site tryptophan mutants in the high-affinity streptavidin-biotin complex. J. Mol. Biol. 279 (1998) 211-221
14. Gao C., Mao S., Lo C.H., Wirsching P., Lerner R.A., and Janda K.D. Making artificial antibodies: a format for phage display of combinatorial heterodimeric arrays. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 6025-6030
15. Ghadessy F.J., Ong J.L., and Holliger P. Directed evolution of polymerase function by compartmentalized self-replication. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 4552-4557
16. Ghadessy F.J., Ramsay N., Boudsocq F., Loakes D., Brown A., Iwai S., Vaisman A., Woodgate R., and Holliger P. Generic expansion of the substrate spectrum of a DNA polymerase by directed evolution. Nat. Biotechnol. 22 (2004) 755-759
17. Green N.M. Spectrophotometric determination of avidin and biotin. Methods Enzymol. 18A (1970) 418-424
18. Green N.M. Avidin and streptavidin. Methods Enzymol. 184 (1990) 51-67
19. Griffiths A.D., and Tawfik D.S. Directed evolution of an extremely fast phosphotriesterase by in vitro compartmentalization. EMBO J. 22 (2003) 24-35
20. Hanes J., and Pluckthun A. In vitro selection and evolution of functional proteins by using ribosome display. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 4937-4942
21. Hidalgo-Fernandez P., Ayet E., Canal I., and Farrera J.A. Avidin and streptavidin ligands based on the glycoluril bicyclic system. Org. Biomol. Chem. 4 (2006) 3147-3154
22. Hirsch J.D., Eslamizar L., Filanoski B.J., Malekzadeh N., Haugland R.P., Beechem J.M., and Haugland R.P. Easily reversible desthiobiotin binding to streptavidin, avidin, and other biotin-binding proteins: uses for protein labeling, detection, and isolation. Anal. Biochem. 308 (2002) 343-357
23. Howarth M., Chinnapen D.J., Gerrow K., Dorrestein P.C., Grandy M.R., Kelleher N.L., El-Husseini A., and Ting A.Y. A monovalent streptavidin with a single femtomolar biotin binding site. Nat. Methods 3 (2006) 267-273
24. Hyre D.E., Le Trong I., Merritt E.A., Eccleston J.F., Green N.M., Stenkamp R.E., and Stayton P.S. Cooperative hydrogen bond interactions in the streptavidin-biotin system. Protein Sci. 15 (2006) 459-467
25. James L.C., and Tawfik D.S. The specificity of cross-reactivity: promiscuous antibody binding involves specific hydrogen bonds rather than nonspecific hydrophobic stickiness. Protein Sci. 12 (2003) 2183-2193
26. Jung S.T., Jeong K.J., Iverson B.L., and Georgiou G. Binding and enrichment of Escherichia coli spheroplasts expressing inner membrane tethered scFv antibodies on surface immobilized antigens. Biotechnol. Bioeng. 98 (2007) 39-47
27. Kayushin A.L., Korosteleva M.D., Miroshnikov A.I., Kosch W., Zubov D., and Piel N. A convenient approach to the synthesis of trinucleotide phosphoramidites-synthons for the generation of oligonucleotide/peptide libraries. Nucleic Acids Res. 24 (1996) 3748-3755
28. Klumb L.A., Chu V., and Stayton P.S. Energetic roles of hydrogen bonds at the ureido oxygen binding pocket in the streptavidin-biotin complex. Biochemistry 37 (1998) 7657-7663
29. Korndorfer I.P., and Skerra A. Improved affinity of engineered streptavidin for the Strep-tag II peptide is due to a fixed open conformation of the lid-like loop at the binding site. Protein Sci. 11 (2002) 883-893
30. Kranz D.M., Herron J.N., and Voss Jr. E.W. Mechanisms of ligand binding by monoclonal anti-fluorescyl antibodies. J. Biol. Chem. 257 (1982) 6987-6995
31. Le Trong I., Freitag S., Klumb L.A., Chu V., Stayton P.S., and Stenkamp R.E. Structural studies of hydrogen bonds in the high-affinity streptavidin-biotin complex: mutations of amino acids interacting with the ureido oxygen of biotin. Acta Crystallogr. D Biol. Crystallogr. 59 (2003) 1567-1573
32. Lee J., Govorov A.O., and Kotov N.A. Bioconjugated superstructures of CdTe nanowires and nanoparticles: multistep cascade Forster resonance energy transfer and energy channeling. Nano Lett. 5 (2005) 2063-2069
33. Mastrobattista E., Taly V., Chanudet E., Treacy P., Kelly B.T., and Griffiths A.D. High-throughput screening of enzyme libraries: in vitro evolution of a beta-galactosidase by fluorescence-activated sorting of double emulsions. Chem. Biol. 12 (2005) 1291-1300
34. Miyamoto S., and Kollman P.A. Absolute and relative binding free energy calculations of the interaction of biotin and its analogs with streptavidin using molecular dynamics/free energy perturbation approaches. Proteins 16 (1993) 226-245
35. Moll D., Huber C., Schlegel B., Pum D., Sleytr U.B., and Sara M. S-layer-streptavidin fusion proteins as template for nanopatterned molecular arrays. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 14646-14651
36. Park S.H., Yin P., Liu Y., Reif J.H., LaBean T.H., and Yan H. Programmable DNA self-assemblies for nanoscale organization of ligands and proteins. Nano Lett. 5 (2005) 729-733
37. Pei R., Taylor S.K., Stefanovic D., Rudchenko S., Mitchell T.E., and Stojanovic M.N. Behavior of polycatalytic assemblies in a substrate-displaying matrix. J. Am. Chem. Soc. 128 (2006) 12693-12699
38. Peluso P., Wilson D.S., Do D., Tran H., Venkatasubbaiah M., Quincy D., Heidecker B., Poindexter K., Tolani N., Phelan M., et al. Optimizing antibody immobilization strategies for the construction of protein microarrays. Anal. Biochem. 312 (2003) 113-124
39. Qureshi M.H., Yeung J.C., Wu S.C., and Wong S.L. Development and characterization of a series of soluble tetrameric and monomeric streptavidin muteins with differential biotin binding affinities. J. Biol. Chem. 276 (2001) 46422-46428
40. Reznik G.O., Vajda S., Sano T., and Cantor C.R. A streptavidin mutant with altered ligand-binding specificity. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 13525-13530
41. Sabanayagam C.R., Smith C.L., and Cantor C.R. Oligonucleotide immobilization on micropatterned streptavidin surfaces. Nucleic Acids Res. 28 (2000) E33
42. Salem A.K., Chen M., Hayden J., Leong K.W., and Searson P.C. Directed assembly of multisegment Au/Pt/Au nanowires. Nano Lett. 4 (2004) 1163-1165
43. Sano T., Pandori M.W., Chen X., Smith C.L., and Cantor C.R. Recombinant core streptavidins. A minimum-sized core streptavidin has enhanced structural stability and higher accessibility to biotinylated macromolecules. J. Biol. Chem. 270 (1995) 28204-28209
44. Sano T., Vajda S., Smith C.L., and Cantor C.R. Engineering subunit association of multisubunit proteins: a dimeric streptavidin. Proc. Natl. Acad. Sci. USA. 94 (1997) 6153-6158
45. Sepp A., and Choo Y. Cell-free selection of zinc finger DNA-binding proteins using in vitro compartmentalization. J. Mol. Biol. 354 (2005) 212-219
46. Sepp A., Tawfik D.S., and Griffiths A.D. Microbead display by in vitro compartmentalisation: selection for binding using flow cytometry. FEBS Lett. 532 (2002) 455-458
47. Shin J.S., and Pierce N.A. A synthetic DNA walker for molecular transport. J. Am. Chem. Soc. 126 (2004) 10834-10835
48. Stayton P.S., Freitag S., Klumb L.A., Chilkoti A., Chu V., Penzotti J.E., To R., Hyre D., Le Trong I., Lybrand T.P., et al. Streptavidin-biotin binding energetics. Biomol. Eng. 16 (1999) 39-44
49. Stemmer W.P. Rapid evolution of a protein in vitro by DNA shuffling. Nature 370 (1994) 389-391
50. Szafranski P., Mello C.M., Sano T., Smith C.L., Kaplan D.L., and Cantor C.R. A new approach for containment of microorganisms: dual control of streptavidin expression by antisense RNA and the T7 transcription system. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 1059-1063
51. Tawfik D.S., and Griffiths A.D. Man-made cell-like compartments for molecular evolution. Nat. Biotechnol. 16 (1998) 652-656
52. Voss S., and Skerra A. Mutagenesis of a flexible loop in streptavidin leads to higher affinity for the Strep-tag II peptide and improved performance in recombinant protein purification. Protein Eng. 10 (1997) 975-982
53. Weber P.C., Ohlendorf D.H., Wendoloski J.J., and Salemme F.R. Structural origins of high-affinity biotin binding to streptavidin. Science 243 (1989) 85-88
54. Weber P.C., Pantoliano M.W., Simons D.M., and Salemme F.R. Structure-based design of synthetic azobenzene ligands for streptavidin. J. Am. Chem. Soc. 116 (1994) 2717-2724
55. Wu S.C., and Wong S.L. Engineering soluble monomeric streptavidin with reversible biotin binding capability. J. Biol. Chem. 280 (2005) 23225-23231
56. Xavier K.A., and Willson R.C. Association and dissociation kinetics of anti-hen egg lysozyme monoclonal antibodies HyHEL-5 and HyHEL-10. Biophys. J. 74 (1998) 2036-2045
57. Yan H., Park S.H., Finkelstein G., Reif J.H., and LaBean T.H. DNA-templated self-assembly of protein arrays and highly conductive nanowires. Science 301 (2003) 1882-1884
58. Yonezawa M., Doi N., Kawahashi Y., Higashinakagawa T., and Yanagawa H. DNA display for in vitro selection of diverse peptide libraries. Nucleic Acids Res. 31 (2003) e118
59. Yurke B., Turberfield A.J., Mills Jr. A.P., Simmel F.C., and Neumann J.L. A DNA-fuelled molecular machine made of DNA. Nature 406 (2000) 605-608
60. Zhang D.Y., Turberfield A.J., Yurke B., and Winfree E. Engineering entropy-driven reactions and networks catalyzed by DNA. Science 318 (2007) 1121-1125