Protein painting reveals solvent-excluded drug targets hidden within native protein–protein interfaces

Alessandra Luchini; Virginia Espina; Lance A. Liotta

doi:10.1038/ncomms5413

journal article Open Access Jul 22, 2014

Protein painting reveals solvent-excluded drug targets hidden within native protein–protein interfaces

Alessandra Luchini Virginia Espina Lance A. Liotta

Nature Communications Vol. 5 No. 1 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/ncomms5413

Topics

No keywords indexed for this article. Browse by subject →

References

54

[1]

Oncogenic protein interfaces: small molecules, big challenges

Tracy L. Nero, Craig J. Morton, Jessica K. Holien et al.

Nature Reviews Cancer 2014 10.1038/nrc3690

[2]

Johnson, R. & Halder, G. The two faces of Hippo: targeting the Hippo pathway for regenerative medicine and cancer treatment. Nat. Rev. Drug Discov. 13, 63–79 (2014). 10.1038/nrd4161

[3]

Anatomy of hot spots in protein interfaces

Andrew A Bogan, Kurt S Thorn

Journal of Molecular Biology 1998 10.1006/jmbi.1998.1843

[4]

Small-molecule inhibitors of protein–protein interactions: progressing towards the dream

Michelle R. Arkin, James A. Wells

Nature Reviews Drug Discovery 2004 10.1038/nrd1343

[5]

A simple physical model for binding energy hot spots in protein–protein complexes

Tanja Kortemme, David Baker

Proceedings of the National Academy of Sciences 2002 10.1073/pnas.202485799

[6]

Hitting the Hot Spots of Cell Signaling Cascades

Grubb John Joseph Grubb

Science 2006 10.1126/science.1126903

[7]

Unraveling hot spots in binding interfaces: progress and challenges

Warren L DeLano

Current Opinion in Structural Biology 2002 10.1016/s0959-440x(02)00283-x

[8]

Hot Regions in Protein–Protein Interactions: The Organization and Contribution of Structurally Conserved Hot Spot Residues

Ozlem Keskin, Buyong Ma, Ruth Nussinov

Journal of Molecular Biology 2005 10.1016/j.jmb.2004.10.077

[9]

Chemical cross‐linkers for protein structure studies by mass spectrometry

David Paramelle, Guillaume Miralles, Gilles Subra et al.

PROTEOMICS 2013 10.1002/pmic.201200305

[10]

Thomas, C., Bazan, J. F. & Garcia, K. C. Structure of the activating IL-1 receptor signaling complex. Nat. Struct. Mol. Biol. 19, 455–457 (2012). 10.1038/nsmb.2260

[11]

Wang, D. et al. Structural insights into the assembly and activation of IL-1β with its receptors. Nat. Immunol. 11, 905–911 (2010). 10.1038/ni.1925

[12]

Sims, J. E. Accessory to inflammation. Nat. Immunol. 11, 883–885 (2010). 10.1038/ni1010-883

[13]

Nold, M. F. et al. Interleukin-1 receptor antagonist prevents murine bronchopulmonary dysplasia induced by perinatal inflammation and hyperoxia. Proc. Natl Acad. Sci. USA 110, 14384–14389 (2013). 10.1073/pnas.1306859110

[14]

Yılmaz-Eliş, A. S. et al. Inhibition of IL-1 signalling by antisense oligonucleotide-mediated exon skipping of IL-1 receptor accessory protein (IL-1RAcP). Mol. Ther. Nucleic Acids 2, e66 (2013). 10.1038/mtna.2012.58

[15]

Barreyro, L. et al. Overexpression of IL-1 receptor accessory protein in stem and progenitor cells and outcome correlation in AML and MDS. Blood 120, 1290–1298 (2012). 10.1182/blood-2012-01-404699

[16]

Sims, J. E. & Smith, D. E. The IL-1 family: regulators of immunity. Nat. Rev. Immunol. 10, 89–102 (2010). 10.1038/nri2691

[17]

Interleukin-1 Receptor Accessory Protein Organizes Neuronal Synaptogenesis as a Cell Adhesion Molecule

Tomoyuki Yoshida, Tomoko Shiroshima, Sung-Jin Lee et al.

The Journal of Neuroscience 2012 10.1523/jneurosci.4637-11.2012

[18]

Lorenzo, J., Horowitz, M. & Choi, Y. Osteoimmunology: interactions of the bone and immune system. Endocr. Rev. 29, 403–440 (2008). 10.1210/er.2007-0038

[19]

Atomic force microscopy: Determination of unbinding force, off rate and energy barrier for protein–ligand interaction

Chih-Kung Lee, Yu-Ming Wang, Long-Sun Huang et al.

Micron 2007 10.1016/j.micron.2006.06.014

[20]

Chin, J. E. & Horuk, R. Interleukin 1 receptors on rabbit articular chondrocytes: relationship between biological activity and receptor binding kinetics. FASEB J. 4, 1481–1487 (1990). 10.1096/fasebj.4.5.2137805

[21]

Ozbabacan, S. E., Engin, H. B., Gursoy, A. & Keskin, O. Transient protein-protein interactions. Protein Eng. Des. Sel. 24, 635–648 (2011). 10.1093/protein/gzr025

[22]

Tamburro, D. et al. Multifunctional core-shell nanoparticles: discovery of previously invisible biomarkers. J. Am. Chem. Soc 133, 19178–19188 (2011). 10.1021/ja207515j

[23]

Vigers, G. P., Anderson, L. J., Caffes, P. & Brandhuber, B. J. Crystal structure of the type-I interleukin-1 receptor complexed with interleukin-1beta. Nature 386, 190–194 (1997). 10.1038/386190a0

[24]

Blech, M. et al. One target-two different binding modes: structural insights into gevokizumab and canakinumab interactions to interleukin-1β. J. Mol. Biol. 425, 94–111 (2013). 10.1016/j.jmb.2012.09.021

[25]

ASEdb: a database of alanine mutations and their effects on the free energy of binding in protein interactions

Kurt S. Thorn, Andrew A. Bogan

Bioinformatics 2001 10.1093/bioinformatics/17.3.284

[26]

Hot spots—A review of the protein–protein interface determinant amino‐acid residues

Irina S. Moreira, Pedro A. Fernandes, Maria J. Ramos

Proteins: Structure, Function, and Bioinformatics 2007 10.1002/prot.21396

[27]

Morrow, J. K. & Zhang, S. Computational prediction of protein hot spot residues. Curr. Pharm. Des. 18, 1255–1265 (2012). 10.2174/138161212799436412

[28]

Protein structure prediction and analysis using the Robetta server

D. E. Kim, D. Chivian, D. Baker

Nucleic Acids Research 2004 10.1093/nar/gkh468

[29]

Computational Alanine Scanning of Protein-Protein Interfaces

Tanja Kortemme, David E. Kim, David Baker

Science's STKE 2004 10.1126/stke.2192004pl2

[30]

Zhu, X. & Mitchell, J. C. KFC2: a knowledge-based hot spot prediction method based on interface solvation, atomic density, and plasticity features. Proteins 79, 2671–2683 (2011). 10.1002/prot.23094

[31]

Tuncbag, N., Keskin, O. & Gursoy, A. HotPoint: hot spot prediction server for protein interfaces. Nucleic Acids Res. 38, W402–W406 (2010). 10.1093/nar/gkq323

[32]

Towne, J. E., Garka, K. E., Renshaw, B. R., Virca, G. D. & Sims, J. E. Interleukin (IL)-1F6, IL-1F8, and IL-1F9 signal through IL-1Rrp2 and IL-1RAcP to activate the pathway leading to NF-kappaB and MAPKs. J. Biol. Chem. 279, 13677–13688 (2004). 10.1074/jbc.m400117200

[33]

Clegg, C. & Hayes, D. Identification of neighbouring proteins in the ribosomes of Escherichia coli. A topographical study with the cross-linking reagent dimethyl suberimidate. Eur. J. Biochem. 42, 21–28 (1974). 10.1111/j.1432-1033.1974.tb03309.x

[34]

The beginning of a beautiful friendship: Cross-linking/mass spectrometry and modelling of proteins and multi-protein complexes

Juri Rappsilber

Journal of Structural Biology 2011 10.1016/j.jsb.2010.10.014

[35]

MS2Assign, automated assignment and nomenclature of tandem mass spectra of chemically crosslinked peptides

Birgit Schilling, Richard H. Row, Bradford W. Gibson et al.

Journal of the American Society for Mass Spectrome... 2003 10.1016/s1044-0305(03)00327-1

[36]

Mandell, J. G., Baerga-Ortiz, A., Falick, A. M. & Komives, E. A. Measurement of solvent accessibility at protein-protein interfaces. Methods Mol. Biol. 305, 65–80 (2005). 10.1385/1-59259-912-5:065

[37]

Ehring, H. Hydrogen exchange/electrospray ionization mass spectrometry studies of structural features of proteins and protein/protein interactions. Anal. Biochem. 267, 252–259 (1999). 10.1006/abio.1998.3000

[38]

Slysz, G. W. et al. Hydra: software for tailored processing of H/D exchange data from MS or tandem MS analyses. BMC Bioinformatics 10, 162 (2009). 10.1186/1471-2105-10-162

[39]

Hambly, D. M. & Gross, M. L. Laser flash photolysis of hydrogen peroxide to oxidize protein solvent-accessible residues on the microsecond timescale. J. Am. Soc. Mass Spectrom. 16, 2057–2063 (2005). 10.1016/j.jasms.2005.09.008

[40]

Trypsin Cleaves Exclusively C-terminal to Arginine and Lysine Residues

Jesper V. Olsen, Shao-En Ong, Matthias Mann

Molecular & Cellular Proteomics 2004 10.1074/mcp.t400003-mcp200

[41]

Value of Using Multiple Proteases for Large-Scale Mass Spectrometry-Based Proteomics

Danielle L. Swaney, Craig D. Wenger, Joshua J. Coon

Journal of Proteome Research 2010 10.1021/pr900863u

[42]

Conformational changes associated with protein–protein interactions

Chern-Sing Goh, Duncan Milburn, Mark Gerstein

Current Opinion in Structural Biology 2004 10.1016/j.sbi.2004.01.005

[43]

Flores, S. C. & Gerstein, M. B. Predicting protein ligand binding motions with the conformation explorer. BMC Bioinformatics 12, 417 (2011). 10.1186/1471-2105-12-417

[44]

Engelhard, M. & Evans, P. A. Kinetics of interaction of partially folded proteins with a hydrophobic dye: evidence that molten globule character is maximal in early folding intermediates. Protein Sci. 4, 1553–1562 (1995). 10.1002/pro.5560040813

[45]

McCulloch, C. A., Downey, G. P. & El-Gabalawy, H. Signalling platforms that modulate the inflammatory response: new targets for drug development. Nat. Rev. Drug Discov. 5, 864–876 (2006). 10.1038/nrd2109

[46]

Liu, Q. & Li, J. Protein binding hot spots and the residue-residue pairing preference: a water exclusion perspective. BMC Bioinformatics 11, 244 (2010). 10.1186/1471-2105-11-244

[47]

Xia, J. F., Zhao, X. M., Song, J. & Huang, D. S. APIS: accurate prediction of hot spots in protein interfaces by combining protrusion index with solvent accessibility. BMC Bioinformatics 11, 174 (2010). 10.1186/1471-2105-11-174

[48]

Hulme, E. C. & Trevethick, M. A. Ligand binding assays at equilibrium: validation and interpretation. Br. J. Pharmacol. 161, 1219–1237 (2010). 10.1111/j.1476-5381.2009.00604.x

[49]

Munson, P. J. & Rodbard, D. Number of receptor sites from Scatchard and Klotz graphs: a constructive critique. Science 220, 979–981 (1983). 10.1126/science.6302842

[50]

Inference of Macromolecular Assemblies from Crystalline State

Evgeny Krissinel, Kim Henrick

Journal of Molecular Biology 2007 10.1016/j.jmb.2007.05.022

Showing 50 of 54 references

Metrics

60

Citations

54

References

Details

Published: Jul 22, 2014
Vol/Issue: 5(1)
License: View

Authors

A

Alessandra Luchini

From the Departments of Experimental Medicine and Biochemical Sciences and of Clinical and Experimental Medicine, University of Perugia; and the Departments of Chemical Engineering Processes and Oncology and Surgical Sciences, University of Padua, Italy.

Cite This Article

Alessandra Luchini, Virginia Espina, Lance A. Liotta (2014). Protein painting reveals solvent-excluded drug targets hidden within native protein–protein interfaces. Nature Communications, 5(1). https://doi.org/10.1038/ncomms5413

Protein painting reveals solvent-excluded drug targets hidden within native protein–protein interfaces

You May Also Like