Abstract
Protein engineering has brought advances to industrial processes, biomaterials, nanotechnology, biosensors, and biomedical applications. This chapter will focus on the engineering of Src Homology 2 domains (SH2) to act as an antibody mimetic for the recognition of sulfotyrosine-containing peptides or proteins. In comparison to anti-sulfotyrosine antibodies, SH2 mutants have much smaller size and can be heterologously expressed and purified in large quantity at low cost. This chapter will describe the use of phage display to identify a sulfotyrosine-binding SH2 mutant and the subsequent enrichment of sulfotyrosine-containing peptides in complex biological samples.
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References
Pawson T, Gish GD (1992) SH2 and SH3 domains: from structure to function. Cell 71(3):359–362. https://doi.org/10.1016/0092-8674(92)90504-6
Anderson D, Koch CA, Grey L et al (1990) Binding of SH2 domains of phospholipase Cγ1, GAP, and Src to activated growth factor receptors. Science 250(4983):979–982. https://doi.org/10.1126/science.2173144
Moran MF, Koch CA, Anderson D et al (1990) Src homology region 2 domains direct protein-protein interactions in signal transduction. Proc Natl Acad Sci U S A 87(21):8622–8626. https://doi.org/10.1073/pnas.87.21.8622
Filippakopoulos P, Mueller S, Knapp S (2009) SH2 domains: modulators of nonreceptor tyrosine kinase activity. Curr Opin Struct Biol 19(6):643–649. https://doi.org/10.1016/j.sbi.2009.10.001
Wagner MJ, Stacey MM, Liu BA et al (2013) Molecular mechanisms of SH2- and PTB-domain-containing proteins in receptor tyrosine kinase signaling. Cold Spring Harb Perspect Biol 5(12):a008987/008981–a008987/008919. https://doi.org/10.1101/cshperspect.a008987
Machida K, Mayer BJ (2005) The SH2 domain: versatile signaling module and pharmaceutical target. Biochim Biophys Acta, Proteins Proteomics 1747(1):1–25. https://doi.org/10.1016/j.bbapap.2004.10.005
Waksman G, Kumaran S, Lubman O (2004) SH2 domains: role, structure and implications for molecular medicine. Expert Rev Mol Med 6(3):1–18
Songyang Z, Shoelson SE, Chaudhuri M et al (1993) SH2 domains recognize specific phosphopeptide sequences. Cell 72(5):767–778
Kaneko T, Huang H, Cao X et al (2012) Superbinder SH2 domains act as antagonists of cell signaling. Sci Signal 5(243):ra68. https://doi.org/10.1126/scisignal.2003021
Ju T, Niu W, Cerny R et al (2013) Molecular recognition of sulfotyrosine and phosphotyrosine by the Src homology 2 domain. Mol Biosyst 9(7):1829–1832. https://doi.org/10.1039/c3mb70061e
Lawrie J, Waldrop S, Morozov A et al (2021) Engineering of a small protein scaffold to recognize sulfotyrosine with high specificity. ACS Chem Biol 16(8):1508–1517. https://doi.org/10.1021/acschembio.1c00382
Lee RWH, Huttner WB (1983) Tyrosine-O-sulfated proteins of PC12 pheochromocytoma cells and their sulfation by a tyrosylprotein sulfotransferase. J Biol Chem 258(18):11326–11334
Tanaka S, Nishiyori T, Kojo H et al (2017) Structural basis for the broad substrate specificity of the human tyrosylprotein sulfotransferase-1. Sci Rep 7(1):8776–8776. https://doi.org/10.1038/s41598-017-07141-8
Teramoto T, Fujikawa Y, Kawaguchi Y et al (2013) Crystal structure of human tyrosylprotein sulfotransferase-2 reveals the mechanism of protein tyrosine sulfation reaction. Nat Commun 4:1572–1579. https://doi.org/10.1038/ncomms2593
Sherry DM, Murray AR, Kanan Y et al (2010) Lack of protein-tyrosine sulfation disrupts photoreceptor outer segment morphogenesis, retinal function and retinal anatomy. Eur J Neurosci 32:1461–1472. https://doi.org/10.1111/j.1460-9568.2010.07431.x
Farzan M, Mirzabekov T, Kolchinsky P et al (1999) Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 96(5):667–676. https://doi.org/10.1016/S0092-8674(00)80577-2
Sasha Tait A, Dong JF, López JA et al (2002) Site-directed mutagenesis of platelet glycoprotein Ibα demonstrating residues involved in the sulfation of tyrosines 276, 278, and 279. Blood 99:4422–4427. https://doi.org/10.1182/blood.V99.12.4422
Kanan Y, Siefert JC, Kinter M et al (2014) Complement factor H, vitronectin, and opticin are tyrosine-sulfated proteins of the retinal pigment epithelium. PLoS One 9:e105409. https://doi.org/10.1371/journal.pone.0105409
Gao J, Choe H, Bota D et al (2003) Sulfation of tyrosine 174 in the human C3a receptor is essential for binding of C3a anaphylatoxin. J Biol Chem 278:37902–37908. https://doi.org/10.1074/jbc.M306061200
Jiang X, Liu H, Chen X et al (2012) Structure of follicle-stimulating hormone in complex with the entire ectodomain of its receptor. Proc Natl Acad Sci U S A 109:12491–12496. https://doi.org/10.1073/pnas.1206643109
Moore KL (2003) The biology and enzymology of protein tyrosine O-sulfation. J Biol Chem 278:24243–24246. https://doi.org/10.1074/jbc.R300008200
Seibert C, Sakmar TP (2008) Toward a framework for sulfoproteomics: synthesis and characterization of sulfotyrosine-containing peptides. Biopolymers 90(3):459–477. https://doi.org/10.1002/bip.20821
Baeuerle PA, Huttner WB (1987) Tyrosine sulfation is a trans-Golgi-specific protein modification. J Cell Biol 105:2655–2664. https://doi.org/10.1083/jcb.105.6.2655
Hoffhines AJ, Damoc E, Bridges KG et al (2006) Detection and purification of tyrosine-sulfated proteins using a novel anti-sulfotyrosine monoclonal antibody. J Biol Chem 281:37877–37887. https://doi.org/10.1074/jbc.M609398200
Robinson MR, Moore KL, Brodbelt JS (2014) Direct identification of tyrosine sulfation by using ultraviolet photodissociation mass spectrometry. J Am Soc Mass Spectrom 25:1461–1471. https://doi.org/10.1007/s13361-014-0910-3
Balderrama GD, Meneses EP, Orihuela LH et al (2011) Analysis of sulfated peptides from the skin secretion of the Pachymedusa dacnicolor frog using IMAC-Ga enrichment and high-resolution mass spectrometry. Rapid Commun Mass Spectrom 25:1017–1027. https://doi.org/10.1002/rcm.4950
Monigatti F, Hekking B, Steen H (2006) Protein sulfation analysis-a primer. Biochim Biophys Acta 1764. https://doi.org/10.1016/j.bbapap.2006.07.002
Önnerfjord P, Heathfield TF, Heinegård D (2004) Identification of tyrosine sulfation in extracellular leucine-rich repeat proteins using mass spectrometry. J Biol Chem 279:26–33. https://doi.org/10.1074/jbc.M308689200
Ward CM, Andrews RK, Smith AI et al (1996) Mocarhagin, a novel cobra venom metalloproteinase, cleaves the platelet von Willebrand factor receptor glycoprotein Ibalpha. Identification of the sulfated tyrosine/anionic sequence Tyr-276-Glu-282 of glycoprotein Ibalpha as a binding site for von Willebr. Biochemistry 35:4929–4938. https://doi.org/10.1021/bi952456c
Yu Y, Hoffhines AJ, Moore KL et al (2007) Determination of the sites of tyrosine O-sulfation in peptides and proteins. Nat Methods 4:583–588. https://doi.org/10.1038/nmeth1056
Shinde S, Bunschoten A, Kruijtzer JAW et al (2012) Imprinted polymers displaying high affinity for sulfated protein fragments. Angew Chem Int Ed 51(33):8326–8329. https://doi.org/10.1002/anie.201201314
Robinson MR, Brodbelt JS (2016) Integrating weak anion exchange and ultraviolet photodissociation mass spectrometry with strategic modulation of peptide basicity for the enrichment of sulfopeptides. Anal Chem 88(22):11037–11045
Kehoe JW, Velappan N, Walbolt M et al (2006) Using phage display to select antibodies recognizing post-translational modifications independently of sequence context. Mol Cell Proteomics 5(12):2350–2363. https://doi.org/10.1074/mcp.M600314-MCP200
Ju T, Niu W, Guo J (2016) Evolution of Src homology 2 (SH2) domain to recognize sulfotyrosine. ACS Chem Biol 11(9):2551–2557. https://doi.org/10.1021/acschembio.6b00555
Packer MS, Liu DR (2015) Methods for the directed evolution of proteins. Nat Rev Genet 16(7):379–394. https://doi.org/10.1038/nrg3927
Smith GP (1985) Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228(4705):1315–1317
Spriestersbach A, Kubicek J, Schaefer F et al (2015) Purification of His-tagged proteins. Methods Enzymol 559:1–15. https://doi.org/10.1016/bs.mie.2014.11.003. Laboratory methods in enzymology: protein, part D.
Lynch BA, Loiacono KA, Tiong CL et al (1997) A fluorescence polarization based src-SH2 binding assay. Anal Biochem 247(1):77–82. https://doi.org/10.1006/abio.1997.2042
Rossi AM, Taylor CW (2011) Analysis of protein-ligand interactions by fluorescence polarization. Nat Protoc 6(3):365–387. https://doi.org/10.1038/nprot.2011.305
Acknowledgments
This work was supported by National Institute of Health (grant 1R01GM138623 and 1R01GM147785 to J.G. and W.N.).
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Waldrop, S.P., Niu, W., Guo, J. (2023). Engineering of SH2 Domains for the Recognition of Protein Tyrosine O-Sulfation Sites. In: Carlomagno, T., Köhn, M. (eds) SH2 Domains. Methods in Molecular Biology, vol 2705. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-3393-9_16
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DOI: https://doi.org/10.1007/978-1-0716-3393-9_16
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