Isolation of monobodies that bind specifically to the SH3 domain of the Fyn tyrosine protein kinase

New Biotechnology

Volumn 29, Issue 5, 2012, Pages 526-533

  Huang, Renhua ^a   Fang, Pete ^a   Kay, Brian K ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFFINITY REAGENTS; CROSS-REACTIVITY; DISSOCIATION CONSTANT; FIBRONECTIN TYPE III; INFLAMMATORY PROCESS; ISOTHERMAL TITRATION CALORIMETRY; KINASE FAMILY; NEURONAL FUNCTION; PHAGE-DISPLAY; PROTEIN KINASE; PROTEIN TYROSINE KINASE; SRC FAMILY; SRC HOMOLOGY 3; SRC-FAMILY KINASE;

AMINO ACIDS; DISSOCIATION; ENZYMES; PROBES;

BINDERS;

FIBRONECTIN; FIBRONECTIN TYPE 3 MONOBODY; G9 MONOBODY; LIGAND; PROLINE; PROTEIN KINASE FYN; PROTEIN SH3; REAGENT; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING COMPETITION; CONTROLLED STUDY; CROSS REACTION; DISSOCIATION CONSTANT; ENZYME ANALYSIS; ENZYME BINDING; ENZYME STRUCTURE; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANTIBODIES; BINDING SITES; BIOMIMETIC MATERIALS; CALORIMETRY; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; KINETICS; MOLECULAR SEQUENCE DATA; PEPTIDE LIBRARY; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTO-ONCOGENE PROTEINS C-FYN; SEQUENCE ALIGNMENT; SRC HOMOLOGY DOMAINS;

EID: 84862020561     PISSN: 18716784     EISSN: 18764347     Source Type: Journal    
DOI: 10.1016/j.nbt.2011.11.015     Document Type: Article

References (60)

1. Gebauer M., Skerra A. Engineered protein scaffolds as next-generation antibody therapeutics. Curr. Opin. Chem. Biol. 2009, 13:245-255.
2. Nilsson F.Y., Tolmachev V. Affibody molecules: new protein domains for molecular imaging and targeted tumor therapy. Curr Opin. Drug Discov. Dev. 2007, 10:167-175.
3. Silverman J., et al. Multivalent avimer proteins evolved by exon shuffling of a family of human receptor domains. Nat. Biotechnol. 2005, 23:1556-1561.
4. Kolmar H. Alternative binding proteins: biological activity and therapeutic potential of cystine-knot miniproteins. FEBS J. 2008, 275:2684-2690.
5. Dai M., et al. Using T7 phage display to select GFP-based binders. Protein Eng. Des. Sel. 2008, 21:413-424.
6. Skerra A. Alternative binding proteins: anticalins - harnessing the structural plasticity of the lipocalin ligand pocket to engineer novel binding activities. FEBS J. 2008, 275:2677-2683.
7. Muyldermans S., et al. Camelid immunoglobulins and nanobody technology. Vet. Immunol. Immunopathol. 2009, 128:178-183.
8. Boersma Y.L., Pluckthun A. DARPins and other repeat protein scaffolds: advances in engineering and applications. Curr. Opin. Biotechnol. 2011.
9. Xiong J.P., et al. Crystal structure of the extracellular segment of integrin alpha Vbeta3 in complex with an Arg-Gly-Asp ligand. Science 2002, 296:151-155.
10. Batori V., et al. Exploring the potential of the monobody scaffold: effects of loop elongation on the stability of a fibronectin type III domain. Protein Eng. 2002, 15:1015-1020.
11. Koide A., et al. Probing protein conformational changes in living cells by using designer binding proteins: application to the estrogen receptor. Proc Natl. Acad. Sci. U.S.A. 2002, 99:1253-1258.
12. Richards J., et al. Engineered fibronectin type III domain with a RGDWXE sequence binds with enhanced affinity and specificity to human alphavbeta3 integrin. J. Mol. Biol. 2003, 326:1475-1488.
13. Hackel B.J., et al. Picomolar affinity fibronectin domains engineered utilizing loop length diversity, recursive mutagenesis, and loop shuffling. J. Mol. Biol. 2008, 381:1238-1252.
14. Olson C.A., et al. mRNA display selection of a high-affinity, modification-specific phospho-IkappaBalpha-binding fibronectin. ACS Chem. Biol. 2008, 3:480-485.
15. Gilbreth R.N., et al. Isoform-specific monobody inhibitors of small ubiquitin-related modifiers engineered using structure-guided library design. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:7751-7756.
16. Karatan E., et al. Molecular recognition properties of FN3 monobodies that bind the Src SH3 domain. Chem. Biol. 2004, 11:835-844.
17. Xu L., et al. Directed evolution of high-affinity antibody mimics using mRNA display. Chem. Biol. 2002, 9:933-942.
18. Koide A., et al. The fibronectin type III domain as a scaffold for novel binding proteins. J. Mol. Biol. 1998, 284:1141-1151.
19. Parker M.H., et al. Antibody mimics based on human fibronectin type three domain engineered for thermostability and high-affinity binding to vascular endothelial growth factor receptor two. Protein Eng. Des. Sel. 2005, 18:435-444.
20. Huang J., et al. Design of protein function leaps by directed domain interface evolution. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:6578-6583.
21. Huang J., et al. Structural basis for exquisite specificity of affinity clamps, synthetic binding proteins generated through directed domain-interface evolution. J. Mol. Biol. 2009, 392:1221-1231.
22. Mayer B.J. SH3 domains: complexity in moderation. J. Cell Sci. 2001, 114:1253-1263.
23. Li S.S. Specificity and versatility of SH3 and other proline-recognition domains: structural basis and implications for cellular signal transduction. Biochem. J. 2005, 390:641-653.
24. Buday L., et al. The Nck family of adapter proteins: regulators of actin cytoskeleton. Cell Signal. 2002, 14:723-731.
25. McPherson P.S. Regulatory role of SH3 domain-mediated protein-protein interactions in synaptic vesicle endocytosis. Cell Signal. 1999, 11:229-238.
26. Engen J.R., et al. Structure and dynamic regulation of Src-family kinases. Cell Mol. Life Sci. 2008, 65:3058-3073.
27. Salmond R.J., et al. T-cell receptor proximal signaling via the Src-family kinases, Lck and Fyn, influences T-cell activation, differentiation, and tolerance. Immunol. Rev. 2009, 228:9-22.
28. Vatish M., et al. Fyn kinase function in lipid utilization: a new upstream regulator of AMPK activity?. Arch. Physiol. Biochem. 2009, 115:191-198.
29. Levi M., Shalgi R. The role of Fyn kinase in the release from metaphase in mammalian oocytes. Mol. Cell. Endocrinol. 2010, 314:228-233.
30. Siraganian R.P., et al. Mast cell signaling: the role of protein tyrosine kinase Syk, its activation and screening methods for new pathway participants. FEBS Lett. 2010, 584:4933-4940.
31. Saito Y.D., et al. Fyn: a novel molecular target in cancer. Cancer 2010, 116:1629-1637.
32. Schenone S., et al. Fyn kinase in brain diseases and cancer: the search for inhibitors. Curr. Med. Chem. 2011.
33. Gulyani A., et al. A biosensor generated via high-throughput screening quantifies cell edge Src dynamics. Nat. Chem. Biol. 2011, 7:437-444.
34. Thomas S.M., Brugge J.S. Cellular functions regulated by Src family kinases. Annu. Rev. Cell Dev. Biol. 1997, 13:513-609.
35. Kunkel T.A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:488-492.
36. Weiss G.A., et al. Rapid mapping of protein functional epitopes by combinatorial alanine scanning. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:8950-8954.
37. Pershad K., et al. Drop-out phagemid vector for switching from phage displayed affinity reagents to expression formats. Anal. Biochem. 2011, 412:210-216.
38. Steiner D., et al. Signal sequences directing cotranslational translocation expand the range of proteins amenable to phage display. Nat. Biotechnol. 2006, 24:823-831.
39. Rickles R.J., et al. Phage display selection of ligand residues important for Src homology 3 domain binding specificity. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:10909-10913.
40. Lu B., et al. The SH2 domain-containing proteins in 21 extant species establish the provenance and scope of phosphotyrosine signaling in Eukaryotes. Sci. Signal 2011, 4:ra83.
41. Manning G., et al. The protein kinase complement of the human genome. Science 2002, 298:1912-1934.
42. Parsons S.J., Parsons J.T. Src family kinases, key regulators of signal transduction. Oncogene 2004, 23:7906-7909.
43. Parsons H.L., et al. Directing phage selections towards specific epitopes. Protein Eng. 1996, 9:1043-1049.
44. Tonikian R., et al. Identifying specificity profiles for peptide recognition modules from phage-displayed peptide libraries. Nat. Protoc. 2007, 2:1368-1386.
45. Sparks A.B., et al. Mapping the specificity of SH3 domains with phage-displayed random-peptide libraries. Methods Mol. Biol. 1998, 84:87-103.
46. Lim W.A., Richards F.M. Critical residues in an SH3 domain from Sem-5 suggest a mechanism for proline-rich peptide recognition. Nat. Struct. Biol. 1994, 1:221-225.
47. Berry D.M., et al. A high-affinity Arg-X-X-Lys SH3 binding motif confers specificity for the interaction between Gads and SLP-76 in T cell signaling. Curr. Biol. 2002, 12:1336-1341.
48. Karkkainen S., et al. Identification of preferred protein interactions by phage-display of the human Src homology-3 proteome. EMBO Rep. 2006, 7:186-191.
49. Schlesinger M.J., Andersen L. Multiple molecular forms of the alkaline phosphatase of Escherichia coli. Ann. N. Y. Acad. Sci. 1968, 151:159-170.
50. Sicheri F., et al. Crystal structure of the Src family tyrosine kinase Hck. Nature 1997, 385:602-609.
51. Williams J.C., et al. The 2.35Å crystal structure of the inactivated form of chicken Src: a dynamic molecule with multiple regulatory interactions. J. Mol. Biol. 1997, 274:757-775.
52. Xu W., et al. Three-dimensional structure of the tyrosine kinase c-Src. Nature 1997, 385:595-602.
53. Yamaguchi H., Hendrickson W.A. Structural basis for activation of human lymphocyte kinase Lck upon tyrosine phosphorylation. Nature 1996, 384:484-489.
54. Lim W.A., et al. Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains. Nature 1994, 372:375-379.
55. Yu H., et al. Structural basis for the binding of proline-rich peptides to SH3 domains. Cell 1994, 76:933-945.
56. Musacchio A., et al. High-resolution crystal structures of tyrosine kinase SH3 domains complexed with proline-rich peptides. Nat. Struct. Biol. 1994, 1:546-551.
57. Pershad K., et al. Generating a panel of highly specific antibodies to 20 human SH2 domains by phage display. Protein Eng. Des. Sel. 2010, 23:279-288.
58. Wojcik J., et al. A potent and highly specific FN3 monobody inhibitor of the Abl SH2 domain. Nat. Struct. Mol. Biol. 2010, 17:519-527.
59. DeLano W. The PYMOL Molecular Graphics System 2002.
60. Main A.L., et al. The three-dimensional structure of the tenth type III module of fibronectin: an insight into RGD-mediated interactions. Cell 1992, 71:671-678.