Structural parameters modulating the cellular uptake of disulfide-rich cyclic cell-penetrating peptides: MCoTI-II and SFTI-1

European Journal of Medicinal Chemistry

Volumn 88, Issue , 2014, Pages 10-18

  Dg'Souza, Charlotte ^a   Henriques, Sónia Troeira ^a   Wang, Conan K ^a   Craik, David J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Cell penetrating peptides; Flow cytometry; Nuclear magnetic resonance spectroscopy; Peptides; Solid phase peptide synthesis; Surface plasmon resonance

Indexed keywords

CELL PENETRATING PEPTIDE; DISULFIDE; MOMORDICA COCHINCHINENSIS TRYPSIN INHIBITOR 2; MOMORDICA COCHINCHINENSIS TRYPSIN INHIBITOR 3; MOMORDICA COCHINCHINENSIS TRYPSIN INHIBITOR 4; MOMORDICA COCHINCHINENSIS TRYPSIN INHIBITOR 5; SUNFLOWER TRYPSIN INHIBITOR 1; TRYPSIN INHIBITOR; UNCLASSIFIED DRUG; CELL-PENETRATING PEPTIDES; CYCLOTIDES; DISULFIDES; PEPTIDES, CYCLIC; SFTI-1 PEPTIDE, SUNFLOWER; TRYPSIN INHIBITOR MCOTI-II;

AMINO ACID SEQUENCE; ARTICLE; CANCER CELL; CELL SURFACE; CONTROLLED STUDY; CYTOTOXICITY; ENDOCYTOSIS; GENE MUTATION; HUMAN; HUMAN CELL; INTERNALIZATION; MEMBRANE BINDING; PEPTIDE SYNTHESIS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LIPID INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SURFACE PLASMON RESONANCE; SURFACE PROPERTY; CHEMICAL SYNTHESIS; CHEMISTRY; HELA CELLS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION;

AMINO ACID SEQUENCE; CELL-PENETRATING PEPTIDES; CYCLOTIDES; DISULFIDES; HELA CELLS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES, CYCLIC; PROTEIN CONFORMATION;

EID: 84911496240     PISSN: 02235234     EISSN: 17683254     Source Type: Journal    
DOI: 10.1016/j.ejmech.2014.06.047     Document Type: Article

References (52)

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. P. Vlieghe, V. Lisowski, J. Martinez, M. Khrestchatisky, Synthetic therapeutic peptides: science and market, Drug. Discov. Today 15 (2010) 40-56.
3. P. Jarver, U. Langel, Cell-penetrating peptides-a brief introduction, Biochim. Biophys. Acta 1758 (2006) 260-263.
4. S.T. Henriques, M.N. Melo, M.A.R.B. Castanho, Cell-penetrating peptides and antimicrobial peptides: how different are they? Biochem. J. 399 (2006) 1-7.
5. F. Madani, S. Lindberg, U. Langel, S. Futaki, A. Graslund, Mechanisms of cellular uptake of cell-penetrating peptides, J. Biophys. 2011 (2011) 414729.
6. G.L. Bidwell 3rd, D. Raucher, Therapeutic peptides for cancer therapy. Part I - peptide inhibitors of signal transduction cascades, Expert Opin. Drug. Deliv. 6 (2009) 1033-1047.
7. A. Lalatsa, A.G. Schatzlein, I.F. Uchegbu, Strategies to deliver peptide drugs to the brain, Mol. Pharm. 11 (2014) 1081-1093.
8. J.S. Orange, M.J. May, Cell penetrating peptide inhibitors of nuclear factorkappa B, Cell. Mol. Life Sci. CMLS 65 (2008) 3564-3591.
9. L. Cascales, S.T. Henriques, M.C. Kerr, Y.H. Huang, M.J. Sweet, N.L. Daly, D.J. Craik, Identification and characterization of a new family of cellpenetrating peptides: cyclic cell-penetrating peptides, J. Biol. Chem. 286 (2011) 36932-36943.
10. J.F. Hernandez, J. Gagnon, L. Chiche, T.M. Nguyen, J.P. Andrieu, A. Heitz, T. Trinh Hong, T.T. Pham, D. Le Nguyen, Squash trypsin inhibitors from Momordica cochinchinensis exhibit an atypical macrocyclic structure, Biochemistry 39 (2000) 5722-5730.
11. M.E. Felizmenio-Quimio, N.L. Daly, D.J. Craik, Circular proteins in plants: solution structure of a novel macrocyclic trypsin inhibitor from Momordica cochinchinensis, J. Biol. Chem. 276 (2001) 22875-22882.
12. O. Saether, D.J. Craik, I.D. Campbell, K. Sletten, J. Juul, D.G. Norman, Elucidation of the primary and three-dimensional structure of the uterotonic polypeptide kalata B1, Biochemistry 34 (1995) 4147-4158.
13. S. Luckett, R.S. Garcia, J.J. Barker, A.V. Konarev, P.R. Shewry, A.R. Clarke, R.L. Brady, High-resolution structure of a potent, cyclic proteinase inhibitor from sunflower seeds, J. Mol. Biol. 290 (1999) 525-533.
14. M.L. Colgrave, D.J. Craik, Thermal, chemical, and enzymatic stability of the cyclotide kalata B1: the importance of the cyclic cystine knot, Biochemistry 43 (2004) 5965-5975.
15. M.L. Colgrave, M.J.L. Korsinczky, R.J. Clark, F. Foley, D.J. Craik, Sunflower trypsin inhibitor-1, proteolytic studies on a trypsin inhibitor peptide and its analogs, Biopolymers 94 (2010) 665-672.
16. D.G. Barry, N.L. Daly, R.J. Clark, L. Sando, D.J. Craik, Linearization of a naturally occurring circular protein maintains structure but eliminates hemolytic activity, Biochemistry 42 (2003) 6688-6695.
17. D. Mandal, A.N. Shirazi, K. Parang, Cell-Penetrating homochiral cyclic peptides as nuclear-targeting molecular transporters, Angew. Chem. Int. Ed. 50 (2011) 9633-9637.
18. K.P. Greenwood, N.L. Daly, D.L. Brown, J.L. Stow, D.J. Craik, The cyclic cystine knot miniprotein MCoTI-II is internalized into cells by macropinocytosis, Int. J. Biochem. Cell. Biol. 39 (2007) 2252-2264.
19. J. Contreras, A.Y. Elnagar, S.F. Hamm-Alvarez, J.A. Camarero, Cellular uptake of cyclotide MCoTI-I follows multiple endocytic pathways, J. Control Release 155 (2011) 134-143.
20. S.E. Northfield, C.K. Wang, C.I. Schroeder, T. Durek, M. Kan, J.E. Swedberg, D.J. Craik, Disulfide-rich macrocyclic peptides as templates in drug design, Eur. J. Med. Chem. 77 (2014) 248-257.
21. T.L. Aboye, H. Ha, S. Majumder, F. Christ, Z. Debyser, A. Shekhtman, N. Neamati, J.A. Camarero, Design of a novel cyclotide-based CXCR4 antagonist with anti-human immunodeficiency virus (HIV)-1 activity, J. Med. Chem. 55 (2012) 10729-10734.
22. L.Y. Chan, S. Gunasekera, S.T. Henriques, N.F. Worth, S.J. Le, R.J. Clark, J.H. Campbell, D.J. Craik, N.L. Daly, Engineering pro-angiogenic peptides using stable, disulfide-rich cyclic scaffolds, Blood 118 (2011) 6709-6717.
23. P. Thongyoo, C. Bonomelli, R.J. Leatherbarrow, E.W. Tate, Potent inhibitors of beta-tryptase and human leukocyte elastase based on the MCoTI-II scaffold, J. Med. Chem. 52 (2009) 6197-6200.
24. S. Gunasekera, F.M. Foley, R.J. Clark, L. Sando, L.J. Fabri, D.J. Craik, N.L. Daly, Engineering stabilized vascular endothelial growth factor-A antagonists: synthesis, structural characterization, and bioactivity of grafted analogues of cyclotides, J. Med. Chem. 51 (2008) 7697-7704.
25. C.K. Wang, C.W. Gruber, M. Cemazar, C. Siatskas, P. Tagore, N. Payne, G. Sun, S. Wang, C.C. Bernard, D.J. Craik, Molecular grafting onto a stable framework yields novel cyclic peptides for the treatment of multiple sclerosis, ACS Chem. Biol. 9 (2014) 156-163.
26. A.G. Poth, L.Y. Chan, D.J. Craik, Cyclotides as grafting frameworks for protein engineering and drug design applications, Biopolymers 100 (2013) 480-491.
27. J.A. Camarero, Optimizing the future for biotechnology therapies, the key role of protein engineering, Adv. Drug. Deliv. Rev. 61 (2009) 897-898.
28. Y. Ji, S. Majumder, M. Millard, R. Borra, T. Bi, A.Y. Elnagar, N. Neamati, A. Shekhtman, J.A. Camarero, In vivo activation of the p53 tumor suppressor pathway by an engineered cyclotide, J. Am. Chem. Soc. 135 (2013) 11623-11633.
29. H.L. Amand, K. Fant, B. Norden, E.K. Esbjorner, Stimulated endocytosis in penetratin uptake: effect of arginine and lysine, Biochem. Biophys. Res. Commun. 371 (2008) 621-625.
30. H.A. Rydberg, M. Matson, H.L. Amand, E.K. Esbjorner, B. Norden, Effects of tryptophan content and backbone spacing on the uptake efficiency of cellpenetrating peptides, Biochemistry 51 (2012) 5531-5539.
31. H. Brooks, B. Lebleu, E. Vives, Tat peptide-mediated cellular delivery: back to basics, Adv. Drug. Deliv. Rev. 57 (2005) 559-577.
32. P.A. Wender, D.J. Mitchell, K. Pattabiraman, E.T. Pelkey, L. Steinman, J.B. Rothbard, The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: peptoid molecular transporters, Proc. Natl. Acad. Sci. USA 97 (2000) 13003-13008.
33. K. Wüthrich, NMR of Proteins and Nucleic Acids, Wiley Interscience, New York, 1986.
34. N.L. Daly, Y.K. Chen, F.M. Foley, P.S. Bansal, R. Bharathi, R.J. Clark, C.P. Sommerhoff, D.J. Craik, The absolute structural requirement for a proline in the P3'-position of Bowman-Birk protease inhibitors is surmounted in the minimized SFTI-1 scaffold, J. Biol. Chem. 281 (2006) 23668-23675.
35. M.R. Plan, U. Goransson, R.J. Clark, N.L. Daly, M.L. Colgrave, D.J. Craik, The cyclotide fingerprint in Oldenlandia affinis: elucidation of chemically modified, linear and novel macrocyclic peptides, Chembiochem 8 (2007) 1001-1011.
36. I.M. Torcato, Y.H. Huang, H.G. Franquelim, D.D. Gaspar, D.J. Craik, M.A.R.B. Castanho, S.T. Henriques, The antimicrobial activity of Sub3 is dependent on membrane binding and cell-penetrating ability, Chembiochem 14 (2013) 2013-2022.
37. M. Benincasa, S. Pacor, R. Gennaro, M. Scocchi, Rapid and reliable detection of antimicrobial peptide penetration into gram-negative bacteria based on fluorescence quenching, Antimicrob. Agents Chemother. 53 (2009) 3501-3504.
38. S.T. Henriques, J. Costa, M.A.R.B. Castanho, Re-evaluating the role of strongly charged sequences in amphipathic cell-penetrating peptides e a fluorescence study using Pep-1, FEBS Lett. 579 (2005) 4498-4502.
39. L. Fei, L. Ren, J.L. Zaro, W.C. Shen, The influence of net charge and charge distribution on cellular uptake and cytosolic localization of arginine-rich peptides, J. Drug Target 19 (2011) 675-680.
40. A. Ziegler, Thermodynamic studies and binding mechanisms of cellpenetrating peptides with lipids and glycosaminoglycans, Adv. Drug. Deliv. Rev. 60 (2008) 580-597.
41. D.L. Daleke, Regulation of phospholipid asymmetry in the erythrocyte membrane, Curr. Opin. Hematol. 15 (2008) 191-195.
42. S.T. Henriques, Y.H. Huang, K.J. Rosengren, H.G. Franquelim, F.A. Carvalho, A. Johnson, S. Sonza, G. Tachedjian, M.A.R.B. Castanho, N.L. Daly, D.J. Craik, Decoding the membrane activity of the cyclotide kalata B1: the importance of phosphatidylethanolamine phospholipids and lipid organization on hemolytic and anti-HIV activities, J. Biol. Chem. 286 (2011) 24231-24241.
43. H.H. Szeto, P.W. Schiller, K.S. Zhao, G.X. Luo, Fluorescent dyes alter intracellular targeting and function of cell-penetrating tetrapeptides, FASEB J. 19 (2004) 118-120.
44. S.D. Conner, S.L. Schmid, Regulated portals of entry into the cell, Nature 422 (2003) 37-44.
45. S.T. Henriques, J. Costa, M.A.R.B. Castanho, Translocation of beta-galactosidase mediated by the cell-penetrating peptide pep-1 into lipid vesicles and human HeLa cells is driven by membrane electrostatic potential, Biochemistry 44 (2005) 10189-10198.
46. S. Boisseau, K. Mabrouk, N. Ram, N. Garmy, V. Collin, A. Tadmouri, M. Mikati, J.-M. Sabatier, M. Ronjat, J. Fantini, M. De Waard, Cell penetration properties of maurocalcine, a natural venom peptide active on the intracellular ryanodine receptor, Biochim. Biophys. Acta 1758 (2006) 308-319.
47. M. Mano, A. Henriques, A. Paiva, M. Prieto, F. Gavilanes, S. Simoes, M.C. Pedroso de Lima, Cellular uptake of S413-PV peptide occurs upon conformational changes induced by peptide-membrane interactions, Biochim. Biophys. Acta 1758 (2006) 336-346.
48. O. Cheneval, C.I. Schroeder, T. Durek, P. Walsh, Y.H. Huang, S. Liras, D.A. Price, D.J. Craik, Fmoc-based synthesis of disulfide-rich cyclic peptides, J. Org. Chem. 79 (2014) 5538-5544.
49. 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.
50. B. Chen, M.L. Colgrave, C. Wang, D.J. Craik, Cycloviolacin H4, a hydrophobic cyclotide from Viola hederaceae, J. Nat. Prod. 69 (2006) 23-28.
51. S.T. Henriques, Y.H. Huang, M.A.R.B. Castanho, L.A. Bagatolli, S. Sonza, G. Tachedjian, N.L. Daly, D.J. Craik, Phosphatidylethanolamine binding is a conserved feature of cyclotide-membrane interactions, J. Biol. Chem. 287 (2012) 33629-33643.
52. S.T. Henriques, L.K. Pattenden, M.I. Aguilar, M.A.R.B. Castanho, PrP(106-126) does not interact with membranes under physiological conditions, Biophys. J. 95 (2008) 1877-1889.