Exploring experimental and computational markers of cyclic peptides: Charting islands of permeability

European Journal of Medicinal Chemistry

Volumn 97, Issue , 2015, Pages 202-213

  Wang, Conan K ^a   Northfield, Susan E ^a   Swedberg, Joakim E ^a   Colless, Barbara ^a   Chaousis, Stephanie ^a   Price, David A ^b   Liras, Spiros ^b   Craik, David J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b PFIZER INC   (United States)

Author keywords

Amide temperature coefficients; Cyclic peptide; Drug design; NMR; Peptide

Indexed keywords

CYCLOPEPTIDE; HEXAPEPTIDE;

ARTICLE; CACO 2 CELL LINE; CELL MEMBRANE PERMEABILITY; CONFORMATIONAL TRANSITION; DRUG BIOAVAILABILITY; HYDROGEN BOND; HYDROPHOBICITY; IN VITRO STUDY; IN VIVO STUDY; LIPOPHILICITY; MOLECULAR DYNAMICS; PEPTIDE SYNTHESIS; PHYSICAL CHEMISTRY; PROTEIN CONFORMATION; QUANTITATIVE STRUCTURE ACTIVITY RELATION; SURFACE AREA; BIOLOGICAL MODEL; CHEMISTRY; HUMAN; SYNTHESIS;

CACO-2 CELLS; HUMANS; MODELS, BIOLOGICAL; MOLECULAR DYNAMICS SIMULATION; PEPTIDES, CYCLIC; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84929084835     PISSN: 02235234     EISSN: 17683254     Source Type: Journal    
DOI: 10.1016/j.ejmech.2015.04.049     Document Type: Article

References (53)

1. D.J. Craik, D.P. Fairlie, S. Liras, D. Price, The future of peptide-based drugs, Chem. Biol. Drug Des. 81 (2013) 136-147.
2. C.A. Lipinski, F. Lombardo, B.W. Dominy, P.J. Feeney, Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings, Adv. Drug Deliv. Rev. 46 (2001) 3-26.
3. K. Valko, J. Butler, P. Eddershaw, Predictive approaches to increase absorption of compounds during lead optimisation, Expert Opin. Drug Discov. 8 (2013) 1225-1238.
4. D.F. Veber, S.R. Johnson, H.Y. Cheng, B.R. Smith, K.W. Ward, K.D. Kopple, Molecular properties that influence the oral bioavailability of drug candidates, J. Med. Chem. 45 (2002) 2615-2623.
5. J.E. Bock, J. Gavenonis, J.A. Kritzer, Getting in shape: controlling peptide bioactivity and bioavailability using conformational constraints, ACS Chem. Biol. 8 (2013) 488-499.
6. C.T. Wong, D.K. Rowlands, C.H. Wong, T.W. Lo, G.K. Nguyen, H.Y. Li, J.P. Tam, Orally active peptidic bradykinin B1 receptor antagonists engineered from a cyclotide scaffold for inflammatory pain treatment, Angew. Chem. Int. Ed. Engl. 51 (2012) 5620-5624.
7. R.J. Clark, J. Jensen, S.T. Nevin, B.P. Callaghan, D.J. Adams, D.J. Craik, The engineering of an orally active conotoxin for the treatment of neuropathic pain, Angew. Chem. Int. Ed. Engl. 49 (2010) 6545-6548.
8. F.W. Okumu, G.M. Pauletti, D.G. Vander Velde, T.J. Siahaan, R.T. Borchardt, Effect of restricted conformational flexibility on the permeation of model hexapeptides across Caco-2 cell monolayers, Pharm. Res. 14 (1997) 169-175.
9. J.G. Beck, J. Chatterjee, B. Laufer, M.U. Kiran, A.O. Frank, S. Neubauer, O. Ovadia, S. Greenberg, C. Gilon, A. Hoffman, H. Kessler, Intestinal permeability of cyclic peptides: common key backbone motifs identified, J. Am. Chem. Soc. 134 (2012) 12125-12133.
10. T. Rezai, B. Yu, G.L. Millhauser, M.P. Jacobson, R.S. Lokey, Testing the conformational hypothesis of passive membrane permeability using synthetic cyclic peptide diastereomers, J. Am. Chem. Soc. 128 (2006) 2510-2511.
11. J.F. Borel, C. Feurer, H.U. Gubler, H. Stahelin, Biological effects of cyclosporin A: a new antilymphocytic agent, Agents Actions 6 (1976) 468-475.
12. J. Chatterjee, C. Gilon, A. Hoffman, H. Kessler, N-methylation of peptides: a new perspective in medicinal chemistry, Acc. Chem. Res. 41 (2008) 1331-1342.
13. E. Biron, J. Chatterjee, O. Ovadia, D. Langenegger, J. Brueggen, D. Hoyer, H.A. Schmid, R. Jelinek, C. Gilon, A. Hoffman, H. Kessler, Improving oral bioavailability of peptides by multiple N-methylation: somatostatin analogues, Angew. Chem. Int. Ed. Engl. 47 (2008) 2595-2599.
14. O. Ovadia, S. Greenberg, J. Chatterjee, B. Laufer, F. Opperer, H. Kessler, C. Gilon, A. Hoffman, The effect of multiple N-methylation on intestinal permeability of cyclic hexapeptides, Mol. Pharm. 8 (2011) 479-487.
15. T.R. White, C.M. Renzelman, A.C. Rand, T. Rezai, C.M. McEwen, V.M. Gelev, R.A. Turner, R.G. Linington, S.S. Leung, A.S. Kalgutkar, J.N. Bauman, Y. Zhang, S. Liras, D.A. Price, A.M. Mathiowetz, M.P. Jacobson, R.S. Lokey, On-resin Nmethylation of cyclic peptides for discovery of orally bioavailable scaffolds, Nat. Chem. Biol. 7 (2011) 810-817.
16. C.K. Wang, S.E. Northfield, B. Colless, S. Chaousis, I. Hamernig, R.J. Lohman, D. Nielsen, C.I. Schroeder, S. Liras, D.A. Price, D.P. Fairlie, D.J. Craik, Rational design and synthesis of orally bioavailable peptides directed by NMR amide temperature coefficients, Proc. Natl. Acad. Sci. 111 (2014) 17504-17509.
17. T. Rezai, J.E. Bock, M.V. Zhou, C. Kalyanaraman, R.S. Lokey, M.P. Jacobson, Conformational flexibility, internal hydrogen bonding, and passive membrane permeability: successful in silico prediction of the relative permeabilities of cyclic peptides, J. Am. Chem. Soc. 128 (2006) 14073-14080.
18. X. Chen, A. Murawski, K. Patel, C.L. Crespi, P.V. Balimane, A novel design of artificial membrane for improving the PAMPA model, Pharm. Res. 25 (2008) 1511-1520.
19. I.A. Lewis, S.C. Schommer, J.L. Markley, rNMR: open source software for identifying and quantifying metabolites in NMR spectra, Magn. Reson. Chem. 47 (Suppl. 1) (2009) S123-S126.
20. W.F. Vranken, W. Boucher, T.J. Stevens, R.H. Fogh, A. Pajon, M. Llinas, E.L. Ulrich, J.L. Markley, J. Ionides, E.D. Laue, The CCPN data model for NMR spectroscopy: development of a software pipeline, Proteins 59 (2005) 687-696.
21. C.K. Wang, S.E. Northfield, J.E. Swedberg, P.J. Harvey, A.M. Mathiowetz, D.A. Price, S. Liras, D.J. Craik, Translational diffusion of cyclic peptides measured using pulsed-field gradient NMR, J. Phys. Chem. B 118 (2014) 11129-11136.
22. T. Herrmann, P. Guntert, K. Wuthrich, Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA, J. Mol. Biol. 319 (2002) 209-227.
23. E. Krieger, G. Koraimann, G. Vriend, Increasing the precision of comparative models with YASARA NOVAea self-parameterizing force field, Proteins 47 (2002) 393-402.
24. W. Humphrey, A. Dalke, K. Schulten, VMD: visual molecular dynamics, J. Mol. Graphics 14 (1996) 33-38, 27-38.
25. K. Vanommeslaeghe, E. Hatcher, C. Acharya, S. Kundu, S. Zhong, J. Shim, E. Darian, O. Guvench, P. Lopes, I. Vorobyov, A.D. Mackerell Jr., CHARMM general force field: a force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields, J. Comput Chem. 31 (2010) 671-690.
26. V. Zoete, M.A. Cuendet, A. Grosdidier, O. Michielin, SwissParam: a fast force field generation tool for small organic molecules, J. Comput. Chem. 32 (2011) 2359-2368.
27. J.C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R.D. Skeel, L. Kale, K. Schulten, Scalable molecular dynamics with NAMD, J. Comput. Chem. 26 (2005) 1781-1802.
28. Z. Liu, G. Wang, Z. Li, R. Wang, Geometrical preferences of the hydrogen bonds on protein-ligand binding interface derived from statistical surveys and quantum mechanics calculations, J. Chem. Theory Comput. 4 (2008) 1959-1973.
29. A. Pedretti, L. Villa, G. Vistoli, VEGAean open platform to develop chemo-bioinformatics applications, using plug-in architecture and script programming, J. Comput. Aided Mol. Des. 18 (2004) 167-173.
30. A.S. Konagurthu, J.C. Whisstock, P.J. Stuckey, A.M. Lesk, MUSTANG: a multiple structural alignment algorithm, Proteins 64 (2006) 559-574.
31. P.G. Arnison, M.J. Bibb, G. Bierbaum, A.A. Bowers, T.S. Bugni, G. Bulaj, J.A. Camarero, D.J. Campopiano, G.L. Challis, J. Clardy, P.D. Cotter, D.J. Craik, M. Dawson, E. Dittmann, S. Donadio, P.C. Dorrestein, K.D. Entian, M.A. Fischbach, J.S. Garavelli, U. Goransson, C.W. Gruber, D.H. Haft, T.K. Hemscheidt, C. Hertweck, C. Hill, A.R. Horswill, M. Jaspars, W.L. Kelly, J.P. Klinman, O.P. Kuipers, A.J. Link, W. Liu, M.A. Marahiel, D.A. Mitchell, G.N. Moll, B.S. Moore, R. Muller, S.K. Nair, I.F. Nes, G.E. Norris, B.M. Olivera, H. Onaka, M.L. Patchett, J. Piel, M.J. Reaney, S. Rebuffat, R.P. Ross, H.G. Sahl, E.W. Schmidt, M.E. Selsted, K. Severinov, B. Shen, K. Sivonen, L. Smith, T. Stein, R.D. Sussmuth, J.R. Tagg, G.L. Tang, A.W. Truman, J.C. Vederas, C.T. Walsh, J.D. Walton, S.C. Wenzel, J.M. Willey, W.A. van der Donk, Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature, Nat. Prod. Rep. 30 (2013) 108-160.
32. M. Bermejo, A. Avdeef, A. Ruiz, R. Nalda, J.A. Ruell, O. Tsinman, I. Gonzalez, C. Fernandez, G. Sanchez, T.M. Garrigues, V. Merino, PAMPAea drug absorption in vitro model 7. Comparing rat in situ, Caco-2, and PAMPA permeability of fluoroquinolones, Eur. J. Pharm. Sci. 21 (2004) 429-441.
33. S.K. Poole, C.F. Poole, Separation methods for estimating octanol-water partition coefficients, J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 797 (2003) 3-19.
34. M. Akamatsu, M. Fujikawa, K. Nakao, R. Shimizu, In silico prediction of human oral absorption based on QSAR analyses of PAMPA permeability, Chem. Biodivers. 6 (2009) 1845-1866.
35. M. Fujikawa, K. Nakao, R. Shimizu, M. Akamatsu, QSAR study on permeability of hydrophobic compounds with artificial membranes, Bioorg Med. Chem. 15 (2007) 3756-3767.
36. V.J. Hruby, in: B. Weinstein (Ed.), Chemistry and Biochemistry of Amino Acids, Peptides and Proteins, Marcel Dekker, New York, 1974, 1-188.
37. T. Cierpicki, J. Otlewski, Amide proton temperature coefficients as hydrogen bond indicators in proteins, J. Biomol. NMR 21 (2001) 249-261.
38. A.C. Rand, S.S. Leung, H. Eng, C.J. Rotter, R. Sharma, A.S. Kalgutkar, Y. Zhang, M.V. Varma, K.A. Farley, B. Khunte, C. Limberakis, D.A. Price, S. Liras, A.M. Mathiowetz, M.P. Jacobson, R.S. Lokey, Optimizing PK properties of cyclic peptides: the effect of side chain substitutions on permeability and clearance, Medchemcomm 3 (2012) 1282-1289.
39. B. Tripet, D. Cepeniene, J.M. Kovacs, C.T. Mant, O.V. Krokhin, R.S. Hodges, Requirements for prediction of peptide retention time in reversed-phase high-performance liquid chromatography: hydrophilicity/hydrophobicity of side-chains at the N- and C-termini of peptides are dramatically affected by the end-groups and location, J. Chromatogr. A 1141 (2007) 212-225.
40. M. Fujikawa, R. Ano, K. Nakao, R. Shimizu, M. Akamatsu, Relationships between structure and high-throughput screening permeability of diverse drugs with artificial membranes: application to prediction of Caco-2 cell permeability, Bioorg. Med. Chem. 13 (2005) 4721-4732.
41. W.M. Hewitt, S.S. Leung, C.R. Pye, A.R. Ponkey, M. Bednarek, M.P. Jacobson, R.S. Lokey, Cell-permeable cyclic peptides from synthetic libraries inspired by natural products, J. Am. Chem. Soc. 137 (2014) 715-721.
42. D.S. Nielsen, H.N. Hoang, R.J. Lohman, T.A. Hill, A.J. Lucke, D.J. Craik, D.J. Edmonds, D.A. Griffith, C.J. Rotter, R.B. Ruggeri, D.A. Price, S. Liras, D.P. Fairlie, Improving on nature: making a cyclic heptapeptide orally bioavailable, Angew. Chem. Int. Ed. Engl. 53 (2014) 12059-12063.
43. P. Thansandote, R.M. Harris, H.L. Dexter, G.L. Simpson, S. Pal, R.J. Upton, K. Valko, Improving the passive permeability of macrocyclic peptides: balancing permeability with other physicochemical properties, Bioorg. Med. Chem. 23 (2015) 322-327.
44. M.J. Waring, Defining optimum lipophilicity and molecular weight ranges for drug candidates-Molecular weight dependent lower logD limits based on permeability, Bioorg. Med. Chem. Lett. 19 (2009) 2844-2851.
45. T.W. Johnson, K.R. Dress, M. Edwards, Using the Golden Triangle to optimize clearance and oral absorption, Bioorg. Med. Chem. Lett. 19 (2009) 5560-5564.
46. K. Goss, Free energy of transfer of a solute and its relation to the partition constant, J. Phys. Chem. B 107 (2003) 14025-14029.
47. N. Ben-Tal, A. Ben-Shaul, A. Nicholls, B. Honig, Free-energy determinants of alpha-helix insertion into lipid bilayers, Biophys. J. 70 (1996) 1803-1812.
48. R.L. Baldwin, The new view of hydrophobic free energy, FEBS Lett. 587 (2013) 1062-1066.
49. M.P. Gleeson, Generation of a set of simple, interpretable ADMET rules of thumb, J. Med. Chem. 51 (2008) 817-834.
50. D.T. Manallack, R.J. Prankerd, G.C. Nassta, O. Ursu, T.I. Oprea, D.K. Chalmers, A chemogenomic analysis of ionization constantseimplications for drug discovery, ChemMedChem 8 (2013) 242-255.
51. P.D. Leeson, B. Springthorpe, The influence of drug-like concepts on decisionmaking in medicinal chemistry, Nat. Rev. Drug Discov. 6 (2007) 881-890.
52. J.D. Hughes, J. Blagg, D.A. Price, S. Bailey, G.A. Decrescenzo, R.V. Devraj, E. Ellsworth, Y.M. Fobian, M.E. Gibbs, R.W. Gilles, N. Greene, E. Huang, T. Krieger-Burke, J. Loesel, T. Wager, L. Whiteley, Y. Zhang, Physiochemical drug properties associated with in vivo toxicological outcomes, Bioorg Med. Chem. Lett. 18 (2008) 4872-4875.
53. F. Giordanetto, J. Kihlberg, Macrocyclic drugs and clinical candidates: what can medicinal chemists learn from their properties? J. Med. Chem. 57 (2014) 278e295.