CyLoP-1: A novel cysteine-rich cell-penetrating peptide for cytosolic delivery of cargoes

Bioconjugate Chemistry

Volumn 22, Issue 3, 2011, Pages 319-328

  Jha, Deepti ^a   Mishra, Ritu ^a   Gottschalk, Sven ^a   Wiesmüller, Karl Heinz ^b   Ugurbil, Kamil ^a   Maier, Martin E ^c   Engelmann, Jörn ^a  

^a MAX PLANCK INSTITUTE FOR BIOLOGICAL CYBERNETICS   (Germany)

^b EMC MICROCOLLECTIONS GMBH   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CELL PENETRATING PEPTIDE; CYSTEINE; CYSTEINE RICH CELL PENETRATING PEPTIDE CYLOP 1; DISULFIDE; PEPTIDE DERIVATIVE; SMACN7 PEPTIDE; TRYPTOPHAN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL TRANSPORT; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; DRUG DELIVERY SYSTEM; ENDOSOME; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; NONHUMAN; OXIDATION; PARTICLE SIZE; PROTEIN ANALYSIS; PROTEIN INDUCTION; PROTEIN LOCALIZATION;

EID: 79952809889     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc100045s     Document Type: Article

References (55)

1. Vives, E., Schmidt, J., and Pelegrin, A. (2008) Cell-penetrating and cell-targeting peptides in drug delivery Biochim. Biophys. Acta 1786, 126-138
2. Lundberg, P. and Langel, Ü. (2003) A brief introduction to cell-penetrating peptides J. Mol. Recognit. 16, 227-233 (Pubitemid 37231690)
3. Magzoub, M. and Graslund, A. (2004) Cell-penetrating peptides: small from inception to application Q. Rev. Biophys. 37, 147-195 (Pubitemid 40867965)
4. Deshayes, S., Morris, M. C., Divita, G., and Heitz, F. (2005) Cell-penetrating peptides: tools for intracellular delivery of therapeutics Cell. Mol. Life Sci. 62, 1839-1849 (Pubitemid 41188523)
5. Kerkis, A., Hayashi, M. A., Yamane, T., and Kerkis, I. (2006) Properties of cell penetrating peptides (CPPs) IUBMB Life 58, 7-13
6. Snyder, E. L. and Dowdy, S. F. (2004) Cell penetrating peptides in drug delivery Pharm. Res. 21, 389-393 (Pubitemid 38338971)
7. Foerg, C., Ziegler, U., Fernandez-Carneado, J., Giralt, E., Rennert, R., Beck-Sickinger, A. G., and Merkle, H. P. (2005) Decoding the entry of two novel cell-penetrating peptides in HeLa cells: lipid raft-mediated endocytosis and endosomal escape Biochemistry 44, 72-81 (Pubitemid 40095708)
8. Mai, J. C., Shen, H., Watkins, S. C., Cheng, T., and Robbins, P. D. (2002) Efficiency of protein transduction is cell type-dependent and is enhanced by dextran sulfate J. Biol. Chem. 277, 30208-30218
9. Wadia, J. S. and Dowdy, S. F. (2005) Transmembrane delivery of protein and peptide drugs by TAT-mediated transduction in the treatment of cancer Adv. Drug Delivery Rev. 57, 579-596 (Pubitemid 40255562)
10. Gait, M. J. (2003) Peptide-mediated cellular delivery of antisense oligonucleotides and their analogues Cell. Mol. Life Sci. 60, 844-853 (Pubitemid 36735115)
11. Gupta, B., Levchenko, T. S., and Torchilin, V. P. (2005) Intracellular delivery of large molecules and small particles by cell-penetrating proteins and peptides Adv. Drug Delivery Rev. 57, 637-651 (Pubitemid 40255564)
12. Zorko, M. and Langel, Ü. (2005) Cell-penetrating peptides: mechanism and kinetics of cargo delivery Adv. Drug Delivery Rev. 57, 529-545 (Pubitemid 40255559)
13. Mäe, M. and Langel, Ü. (2006) Cell-penetrating peptides as vectors for peptide, protein and oligonucleotide delivery Curr. Opin. Pharmacol. 6, 509-514 (Pubitemid 44340662)
14. Turner, J. J., Arzumanov, A. A., and Gait, M. J. (2005) Synthesis, cellular uptake and HIV-1 Tat-dependent trans-activation inhibition activity of oligonucleotide analogues disulphide-conjugated to cell-penetrating peptides Nucleic Acids Res. 33, 27-42 (Pubitemid 40276926)
15. Melikov, K. and Chernomordik, L. V. (2005) Arginine-rich cell penetrating peptides: from endosomal uptake to nuclear delivery Cell. Mol. Life Sci. 62, 2739-2749 (Pubitemid 41779944)
16. Rothbard, J. B., Jessop, T. C., Lewis, R. S., Murray, B. A., and Wender, P. A. (2004) Role of membrane potential and hydrogen bonding in the mechanism of translocation of guanidinium-rich peptides into cells J. Am. Chem. Soc. 126, 9506-9507 (Pubitemid 39031015)
17. Lundin, P., Johansson, H., Guterstam, P., Holm, T., Hansen, M., Langel, U., and El-Andaloussi, S. (2008) Distinct uptake routes of cell-penetrating peptide conjugates Bioconjugate Chem 19, 2535-2542
18. Richard, J. P., Melikov, K., Vives, E., Ramos, C., Verbeure, B., Gait, M. J., Chernomordik, L. V., and Lebleu, B. (2003) Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake J. Biol. Chem. 278, 585-590 (Pubitemid 36043612)
19. Tréhin, R. and Merkle, H. P. (2004) Chances and pitfalls of cell penetrating peptides for cellular drug delivery Eur. J. Pharm. Biopharm. 58, 209-223 (Pubitemid 39037230)
20. Wender, P. A., Mitchell, D. J., Pattabiraman, K., Pelkey, E. T., Steinman, L., and Rothbard, J. B. (2000) The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: peptoid molecular transporters Proc. Natl. Acad. Sci. U.S.A. 97, 13003-13008
21. Turner, J. J., Ivanova, G. D., Verbeure, B., Williams, D., Arzumanov, A. A., Abes, S., Lebleu, B., and Gait, M. J. (2005) Cell-penetrating peptide conjugates of peptide nucleic acids (PNA) as inhibitors of HIV-1 Tat-dependent trans-activation in cells Nucleic Acids Res. 33, 6837-6849 (Pubitemid 43000315)
22. Wadia, J. S., Stan, R. V., and Dowdy, S. F. (2004) Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis Nat. Med. 10, 310-315 (Pubitemid 38667624)
23. Duchardt, F., Fotin-Mleczek, M., Schwarz, H., Fischer, R., and Brock, R. (2007) A comprehensive model for the cellular uptake of cationic cell-penetrating peptides Traffic 8, 848-866 (Pubitemid 46971632)
24. Oguiura, N., Boni-Mitake, M., and Rádis-Baptista, G. (2005) New view on crotamine, a small basic polypeptide myotoxin from South American rattlesnake venom Toxicon 46, 363-370 (Pubitemid 41218730)
25. Rádis-Baptista, G., Kerkis, A., Prieto-Silva, A. R., Hayashi, M. A. F., Kerkis, I., and Yamane, T. (2008) Membrane-translocating Peptides and Toxins: from Nature to Bedside Journal of Brazilian Chemical Society 19, 211-225
26. Hayashi, M. A., Nascimento, F. D., Kerkis, A., Oliveira, V., Oliveira, E. B., Pereira, A., Rádis-Baptista, G., Nader, H. B., Yamane, T., Kerkis, I., and Tersariol, I. L. (2008) Cytotoxic effects of crotamine are mediated through lysosomal membrane permeabilization Toxicon 52, 508-517
27. Kerkis, A., Kerkis, I., Rádis-Baptista, G., Oliveira, E. B., Vianna-Morgante, A. M., Pereira, L. V., and Yamane, T. (2004) Crotamine is a novel cell-penetrating protein from the venom of rattlesnake Crotalus durissus terrificus FASEB J. 18, 1407-1409 (Pubitemid 39561596)
28. Sarin, V. K., Kent, S. B., Tam, J. P., and Merrifield, R. B. (1981) Quantitative monitoring of solid-phase peptide synthesis by the ninhydrin reaction Anal. Biochem. 117, 147-157
29. Spetzler, J. C. and Meldal, M. (1997) Evaluation of strategies for 'one-pot' deprotection, cleavage and disulfide bond formation in the preparation of cystine-containing peptides Lett. Pept. Sci. 3, 327-332 (Pubitemid 126713549)
30. Su, W., Mishra, R., Pfeuffer, J., Wiesmüller, K. H., Ugurbil, K., and Engelmann, J. (2007) Synthesis and cellular uptake of a MR contrast agent coupled to an antisense peptide nucleic acid-cell-penetrating peptide conjugate Contrast Media Mol. Imaging 2, 42-49 (Pubitemid 46739004)
31. Richards, W. L., Song, M. K., Krutzsch, H., Evarts, R. P., Marsden, E., and Thorgeirsson, S. S. (1985) Measurement of cell proliferation in microculture using Hoechst 33342 for the rapid semiautomated microfluorimetric determination of chromatin DNA Exp. Cell Res. 159, 235-246 (Pubitemid 16247569)
32. Blaheta, R. A., Franz, M., Auth, M. K., Wenisch, H. J., and Markus, B. H. (1991) A rapid non-radioactive fluorescence assay for the measurement of both cell number and proliferation J. Immunol. Methods 142, 199-206
33. Rennert, R., Wespe, C., Beck-Sickinger, A. G., and Neundorf, I. (2006) Developing novel hCT derived cell-penetrating peptides with improved metabolic stability Biochim. Biophys. Acta 1758, 347-354
34. Turner, J. J., Williams, D., Owen, D., and Gait, M. J. (2006) Disulfide conjugation of peptides to oligonucleotides and their analogs Curr. Protoc. Nucleic Acid Chem. 4.28, 1-4.28.21
35. Fling, S. P. and Gregerson, D. S. (1986) Peptide and protein molecular weight determination by electrophoresis using a high-molarity tris buffer system without urea Anal. Biochem. 155, 83-88 (Pubitemid 16034463)
36. Schägger, H. and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa Anal. Biochem. 166, 368-379 (Pubitemid 18004907)
37. Blum, H., Beier, H., and Gross, H. J. (1987) Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels Electrophoresis 8, 93-99
38. Futaki, S., Suzuki, T., Ohashi, W., Yagami, T., Tanaka, S., Ueda, K., and Sugiura, Y. (2001) Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery J. Biol. Chem. 276, 5836-5840
39. Andreu, D., Albericio, F., Solé, N. A., Munson, M. C., Ferrer, M., and Barany, G. (1994) Peptide synthesis protocols, in Methods in Molecular Biology (Pennington, W. and Dunn, B. M., Eds.) pp 91 - 169, Humana Press Inc., Totowa.
40. Siedler, F., Weyher, E., and Moroder, L. (1996) Cysteine racemization in peptide synthesis: a new and easy detection method J. Pept. Sci. 2, 271-275 (Pubitemid 126495406)
41. Huang, H. and Rabenstein, D. L. (1999) A cleavage cocktail for methionine-containing peptides J. Pept. Res. 53, 548-553 (Pubitemid 29287769)
42. Wünsch, E., Jaeger, E., Kisfaludy, L., and Löw., M (1977) Side reactions in peptide synthesis: ter-butylation of tryptophan Angew. Chem., Int. Ed. Engl. 16, 317-318
43. Giraud, M., Cavelier, F., and Martinez, J. (1999) A side-reaction in the SPPS of Trp-containing peptides J. Pept. Sci. 5, 457-461 (Pubitemid 29495473)
44. Angell, Y. M., Alsina, J., Albericio, F., and Barany, G. (2002) Practical protocols for stepwise solid-phase synthesis of cysteine-containing peptides J. Pept. Res. 60, 292-299 (Pubitemid 35246790)
45. Moroder, L. (2005) Isosteric replacement of sulfur with other chalcogens in peptides and proteins J. Pept. Sci. 11, 187-214 (Pubitemid 40542352)
46. Karim, C. B., Paterlini, M. G., Reddy, L. G., Hunter, G. W., Barany, G., and Thomas, D. D. (2001) Role of cysteine residues in structural stability and function of a transmembrane helix bundle J. Biol. Chem. 276, 38814-38819
47. Aubry, S., Burlina, F., Dupont, E., Delaroche, D., Joliot, A., Lavielle, S., Chassaing, G., and Sagan, S. (2009) Cell-surface thiols affect cell entry of disulfide-conjugated peptides FASEB J. 23, 2956-2967
48. Digilio, G., Menchise, V., Gianolio, E., Catanzaro, V., Carrera, C., Napolitano, R., Fedeli, F., and Aime, S. (2010) Exofacial protein thiols as a route for the internalization of Gd(III)-based complexes for magnetic resonance imaging cell labeling. J. Med. Chem. doi: 10.1021/jm901876r.
49. Dom, G., Shaw-Jackson, C., Matis, C., Bouffioux, O., Picard, J. J., Prochiantz, A., Mingeot-Leclercq, M. P., Brasseur, R., and Rezsohazy, R. (2003) Cellular uptake of Antennapedia Penetratin peptides is a two-step process in which phase transfer precedes a tryptophan-dependent translocation Nucleic Acids Res. 31, 556-561 (Pubitemid 36175944)
50. Rueping, M., Mahajan, Y., Sauer, M., and Seebach, D. (2002) Cellular uptake studies with beta-peptides ChemBioChem 3, 257-259
51. Rádis-Baptista, G., De La Torre, B. G., and Andreu, D. (2008) Novel cell-penetrating peptide sequence derived by structural minimization of a snake toxin exhibits preferential nucleolar localization J. Med. Chem. 7041-7044
52. Meade, B. R. and Dowdy, S. F. (2008) Enhancing the cellular uptake of siRNA duplexes following noncovalent packaging with protein transduction domain peptides Adv. Drug Delivery Rev. 60, 530-536
53. Fandy, T. E., Shankar, S., and Srivastava, R. K. (2008) Smac/DIABLO enhances the therapeutic potential of chemotherapeutic drugs and irradiation, and sensitizes TRAIL-resistant breast cancer cells Mol. Cancer 7, 60
54. Heckl, S., Sturzu, A., Regenbogen, M., Beck, A., Feil, G., Gharabaghi, A., and Echner, H. (2008) A novel polyarginine containing Smac peptide conjugate that mediates cell death in tumor and healthy cells Med. Chem. 4, 348-354
55. Lundberg, P., El-Andaloussi, S., Sütlü, T., Johansson, H., and Langel, Ü. (2007) Delivery of short interfering RNA using endosomolytic cell-penetrating peptides FASEB J. 21, 2664-2671 (Pubitemid 47372734)