Rational optimization of conformational effects induced by hydrocarbon staples in peptides and their binding interfaces

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Lama, Dilraj ^a   Quah, Soo T ^b   Verma, Chandra S ^a,c,d   Lakshminarayanan, Rajamani ^e   Beuerman, Roger W ^e   Lane, David P ^b   Brown, Christopher J ^b  

^a BIOINFORMATICS INSTITUTE   (Singapore)

^b AGENCY FOR SCIENCE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^e SINGAPORE EYE RESEARCH INSTITUTE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROCARBON; INITIATION FACTOR 4E; INITIATION FACTOR 4G; PEPTIDE; PROTEIN BINDING;

AMINO ACID SEQUENCE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; HYDROGEN BOND; METABOLISM; PROTEIN CONFORMATION; PROTEIN DOMAIN; REPRODUCIBILITY; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; EUKARYOTIC INITIATION FACTOR-4E; EUKARYOTIC INITIATION FACTOR-4G; HYDROCARBONS; HYDROGEN BONDING; MODELS, MOLECULAR; PEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; REPRODUCIBILITY OF RESULTS;

EID: 84890705499     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep03451     Document Type: Article

References (44)

1. Topisirovic, I., Svitkin, Y. V., Sonenberg, N. & Shatkin, A. J. Cap and cap-binding proteins in the control of gene expression. Wiley Interdiscip Rev RNA 2, 277-298 (2011).
2. Montanaro, L. & Pandolfi, P. P. Initiation of mRNA translation in oncogenesis: the role of eIF4E. Cell Cycle 3, 1387-1389 (2004). (Pubitemid 40310673)
3. Culjkovic, B., Topisirovic, I. & Borden, K. L. Controlling gene expression through RNA regulons: the role of the eukaryotic translation initiation factor eIF4E. Cell Cycle 6, 65-69 (2007). (Pubitemid 46173883)
4. De Benedetti, A. & Graff, J. R. eIF-4E expression and its role in malignancies and metastases. Oncogene 23, 3189-3199 (2004). (Pubitemid 38638830)
5. Gingras, A. C. et al. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev 13, 1422-1437 (1999).
6. Marcotrigiano, J., Gingras, A. C., Sonenberg, N. & Burley, S. K. Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol Cell 3, 707-716 (1999). (Pubitemid 29323049)
7. Fletcher, C. M. et al. 4E binding proteins inhibit the translation factor eIF4E without folded structure. Biochemistry 37, 9-15 (1998). (Pubitemid 28049102)
8. Gross, J. D. et al. Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell 115, 739-750 (2003). (Pubitemid 38030302)
9. Vassilev, L. T. et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303, 844-848 (2004). (Pubitemid 38174664)
10. Sattler, M. et al. Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 275, 983-986 (1997). (Pubitemid 27087715)
11. Kim, Y. W., Grossmann, T. N. & Verdine, G. L. Synthesis of all-hydrocarbon stapled alpha-helical peptides by ring-closing olefin metathesis. Nat Protoc 6, 761-771 (2011).
12. Baek, S. et al. Structure of the stapled p53 peptide bound to Mdm2. J AmChem Soc 134, 103-106 (2012).
13. Walensky, L. D. et al. Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix. Science 305, 1466-1470 (2004). (Pubitemid 39167667)
14. Brown, C. J. et al. Stapled Peptides with Improved Potency and Specificity That Activate p53. ACS Chem Biol, 8, 506-12 (2012).
15. Verdine, G. L. & Hilinski, G. J. Stapled peptides for intracellular drug targets. Methods Enzymol 503, 3-33 (2012).
16. Dastidar, S. G., Lane, D. P. & Verma, C. S. Multiple peptide conformations give rise to similar binding affinities: molecular simulations of p53-MDM2. J Am Chem Soc 130, 13514-13515 (2008).
17. Joseph, T. L., Lane, D. & Verma, C. S. Stapled peptides in the p53 pathway: computer simulations reveal novel interactions of the staples with the target protein. Cell Cycle 9, 4560-4568 (2010).
18. Phillips, C. et al. Design and structure of stapled peptides binding to estrogen receptors. J Am Chem Soc 133, 9696-9699 (2011).
19. Stewart, M. L., Fire, E., Keating, A. E. &Walensky, L. D. The MCL-1 BH3 helix is an exclusive MCL-1 inhibitor and apoptosis sensitizer. Nat Chem Biol 6, 595-601 (2010).
20. Zhou, W. et al. Improved eIF4E binding peptides by phage display guided design: plasticity of interacting surfaces yield collective effects. PLoS One 7, e47235 (2012).
21. Kim, Y. W., Kutchukian, P. S. & Verdine, G. L. Introduction of all-hydrocarbon i, i 1 3 staples into alpha-helices via ring-closing olefin metathesis. Org Lett 12, 3046-3049 (2010).
22. Kutchukian, P. S., Yang, J. S., Verdine, G. L. & Shakhnovich, E. I. All-atom model for stabilization of alpha-helical structure in peptides by hydrocarbon staples. J Am Chem Soc 131, 4622-4627 (2009).
23. Brown, C. J. et al. Stabilizing the eIF4G1 alpha-helix increases its binding affinity with eIF4E: implications for peptidomimetic design strategies. J Mol Biol 405, 736-753 (2011).
24. Brown, C. J., Verma, C. S., Walkinshaw, M. D. & Lane, D. P. Crystallization of eIF4E complexed with eIF4GI peptide and glycerol reveals distinct structural differences around the cap-binding site. Cell Cycle 8, 1905-1911 (2009).
25. Brown, C. J., McNae, I., Fischer, P. M. &Walkinshaw,M. D. Crystallographic and mass spectrometric characterisation of eIF4E with N7-alkylated cap derivatives. J Mol Biol 372, 7-15 (2007). (Pubitemid 47241139)
26. Vanquelef, E. et al. R. E. D. Server: a web service for deriving RESP and ESP charges and building force field libraries for new molecules and molecular fragments. Nucleic Acids Res 39, W511-517 (2011).
27. Hornak, V. et al. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65, 712-725 (2006). (Pubitemid 44583220)
28. Case, D. A. et al. The Amber biomolecular simulation programs. J Comput Chem 26, 1668-1688 (2005). (Pubitemid 43076180)
29. Ponder, J. W. &Case, D. A. Force fields for protein simulations. Adv Protein Chem 66, 27-85 (2003). (Pubitemid 37392314)
30. Schrodinger, L. L. C. The PyMOL Molecular Graphics System, Version 1.3r1 (2010).
31. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W. & Klein, M. L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys 79, 926-935 (1983).
32. Pastor, R. W., Brooks, B. R. & Szabo, A. An analysis of the accuracy of Langevin and molecular dynamics algorithms. Mol. Phys. 65, 1409-1419 (1988).
33. Loncharich, R. J., Brooks, B. R.& Pastor, R. W. Langevin dynamics of peptides: the frictional dependence of isomerization rates of N-acetylalanyl-N9-methylamide. Biopolymers 32, 523-535 (1992).
34. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A. & Haak, J. R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684-3690 (1984).
35. Darden, T., York, D. & Pedersen, L. Particle mesh Ewald: An N [center-dot] log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092 (1993).
36. Ryckaert, J.-P., Ciccotti, G. & Berendsen, H. J. C. Numerical integration of the cartesian equations ofmotion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23, 327-341 (1977).
37. Nymeyer, H., Gnanakaran, S. & Garcia, A. E. Atomic simulations of protein folding, using the replica exchange algorithm. Methods Enzymol 383, 119-149 (2004). (Pubitemid 38401789)
38. Sugita, Y. & Okamoto, Y. Molecular mechanism for stabilizing a short helical peptide studied by generalized-ensemble simulations with explicit solvent. Biophys J 88, 3180-3190 (2005). (Pubitemid 40586571)
39. Gnanakaran, S., Nymeyer, H., Portman, J., Sanbonmatsu, K. Y. & Garcia, A. E. Peptide folding simulations. Curr Opin Struct Biol 13, 168-174 (2003). (Pubitemid 36515144)
40. Sanbonmatsu, K. Y. & Garcia, A. E. Structure of Met-enkephalin in explicit aqueous solution using replica exchange molecular dynamics. Proteins 46, 225-234 (2002). (Pubitemid 34052076)
41. Shao, J., Tanner, S. W., Thompson, N. & Cheatham, T. E. Clustering Molecular Dynamics Trajectories: 1. Characterizing the Performance of Different Clustering Algorithms. J. Chem. Theory Comput. 3, 2312-2334 (2007).
42. Bashford, D. & Case, D. A. Generalized born models of macromolecular solvation effects. Annu Rev Phys Chem 51, 129-152 (2000).
43. Miller, B. R. et al. MMPBSA.py: An Efficient Program for End-State Free Energy Calculations. J. Chem. Theory Comput. 8, 3314-3321 (2012).
44. Onufriev, A., Bashford, D. & Case, D. A. Exploring protein native states and largescale conformational changes with a modified generalized born model. Proteins 55, 383-394 (2004). (Pubitemid 38437495)