Self-assembling cyclic β3-peptide nanotubes as artificial transmembrane ion channels

Journal of the American Chemical Society

Volumn 120, Issue 4, 1998, Pages 651-656

  Clark, Thomas D ^a   Buehler, Lukas K ^a,b   Ghadiri, M Reza ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b JOHNSON AND JOHNSON PHARMACEUTICAL RESEARCH AND DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPEPTIDE; ION CHANNEL;

ARTICLE; CONDUCTANCE; CONTROLLED STUDY; DRUG SYNTHESIS; HYDROGEN BOND; INFRARED SPECTROSCOPY; ION TRANSPORT; LIPID MEMBRANE; MOLECULAR MODEL; NONHUMAN; SOLUBILITY;

EID: 0032481333     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja972786f     Document Type: Article

References (62)

1. (a) Seebach, D.; Matthews, J.; Meden, A.; Wessels, T.; Baerlocher, C.; McCusker, L. B. Helv. Chim. Acta 1997, 80, 173-182.
2. (b) Seebach, D.; Ciceri, P. E.; Overhand, M.; Jaun, B.; Rigo, D.; Oberer, L.; Hommel, U.; Amstutz, R.; Widmer, H. Helv. Chim. Acta 1996, 79, 2043-2067.
3. (c) Seebach, D.; Overhand, M.; Kühnle, F. N. M.; Martinoni, B.; Oberer, L.; Hommel, U.; Widmer, H. Helv. Chim. Acta 1996, 79, 913-941.
4. (d) Podlech, J.; Seebach, D. Liebigs. Ann. 1995, 1217-1228.
5. (a) Appella, D. H.; Christianson, L. A.; Klein, D. A.; Powell, D. R.; Huang, X.; Barchi, J. J.; Gellman, S. H. Nature 1997, 387, 381-384.
6. (b) Appella, D. H.; Christianson, L. A.; Karle, I. L.; Powell, D. R.; Gellman, S. H. J. Am. Chem. Soc. 1996, 118, 13071-13072.
7. (c) Dado, G. P.; Gellman, S. H. J. Am. Chem. Soc. 1994, 116, 1054-1055.
8. δH → CγH).
9. (a) Hartgerink, J. D.; Granja, J. R.; Milligan, R. A. Ghadiri, M. R. J. Am. Chem. Soc. 1996, 118, 43-50.
10. (b) Khazanovich, N.; Granja, J. R.; McRee, D. E.; Milligan, R. A.; Ghadiri, M. R. J. Am. Chem. Soc. 1994, 116, 6011-6012.
11. (c) Ghadiri, M. R.; Granja, J. R.; Milligan, R. A.; McRee, D. E.; Khazanovich, N. Nature 1993, 366, 324-327.
12. (d) Ghadiri, M. R.; Kobayashi, K.; Granja, J. R.; Chadha, R. K.; McRee, D. E. Angew. Chem., Int. Ed. Engl. 1995, 34, 93-95.
13. (e) Kobayashi, K.; Granja, J. R.; Ghadiri, M. R. Angew. Chem., Int. Ed. Engl. 1995, 34, 95-98.
14. (f) Clark, T. D.; Ghadiri, M. R. J. Am. Chem. Soc. 1995, 117, 12364-12365.
15. (a) Saviano, M.; Lombardi, A.; Pedone, C.; Diblasio, B.; Sun, X. C.; Lorenzi, G. P. J. Include. Phenom. 1994, 18, 27-36.
16. (b) Sun, X. C.; Lorenzi, G. P. Helv. Chim. Acta 1994, 77, 1520-1526.
17. For earlier studies involving cyclic D,L-α-peptides with construction of tubular structures as the stated goal, see: (c) Tomasi, L.; Lorenzi, G. P. Helv. Chim. Acta 1987, 70, 1012-1016.
18. (d) Pavone, V.; Benedetti, E.; Di Blasio, B.; Lombardi, A.; Pedone, C.; Lorenzi, G. P. Biopolymers 1993, 28, 215-223.
19. (a) Engels, M.; Bashford, D.; Ghadiri, M. R. J. Am. Chem. Soc. 1995, 117, 9151-9158.
20. (b) Granja, J. R.; Ghadiri, M. R. J. Am. Chem. Soc. 1994, 116, 10785-10786.
21. (c) Ghadiri, M. R.; Granja, J. R.; Buehler, L. K. Nature 1994, 369, 301-304.
22. (d) Buehler, L. K.; Granja, J. R.; Ghadiri, M. R. Unpublished results.
23. (e) Kim, H. S.; Hartgerink, J. D.; Ghadiri, M. R. Submitted.
24. (a) Hassal, C. H. In Chemistry and Biology of Peptides: Proceedings of the Third American Peptide Symposium; Meinhoffer, J., Ed.; Ann Arbor Sci.; Ann Arbor, MI, 1972; pp 153-157.
25. (b) Karle, I. L.; Handa, B. K.; Hassall, C. H. Acta Crystallogr. 1975, B 31, 555-560.
26. De Santis, P.; Morosetti, S.; Rizzo, R. Macromolecules 1974, 7, 52-58.
27. For a study of backbone dipole effects on channel conductance in a simple α-helical model system see: Kienker, P. K.; DeGrado, W. F.; Lear, J. D. Proc. Natl. Acad. Sci. U.S.A. 1994, 91, 4859-4863.
28. Tryptophan residues of the Gramicidin A channel have been shown to significantly influence channel conductance. For leading references, see: (a) Hu, W.; Lazo, N. D.; Cross, T. A. Biochemistry 1995, 34, 14138-14146.
29. (b) Hu, W.; Crosss, T. A. Biochemisty 1995, 34, 14147-14155.
30. (c) Ketchem, R. R.; Hu, W.; Cross, T. A. Science 1993, 261, 1457-1460.
31. Hintermann, T.; Seebach, D. Chimia 1997, 50, 244-247.
32. The minimum effective radius of the Gramicidin A channel was recently reported as 1.28 Å. Smart, O. S.; Breed, J.; Smith, G. R.; Sanson, M. S. P. Biophys. J. 1997, 72, 1109-1126.
33. Gramicidin A is one example. See refs 10a-c and work cited therein.
34. Carmichael, V. E.; Dutton, P. J.; Fyles, T. M.; James, T. D.; Swan, J. A.; Zojaji, M. J. Am. Chem. Soc. 1989, 111, 769-770.
35. (a) Szoka, F.; Papahadjopoulos, D. Proc. Natl. Acad. Sci. U.S.A. 1978, 75, 4194-4198.
36. (b) Olson, F.; Hunt, C. A.; Szoka, F. C.; Vil, W. J.; Papahadjopoulos, D. Biochim. Biophys. Acta 1979, 557, 9-23.
37. DMSO solutions (1 mM) of peptides 1 and 2 were used in this assay. However, peptide 3 proved insoluble under these conditions and was first dissolved in HFIP (∼7 mM) followed by solvent exchange via gel filtration on an LH-20 column preequilibarated with MeOH. Peptide containing fractions were identified by UV spectroscopy. The resulting MeOH solution of 3 (∼2 mM) was stable at least 24 h at room temperature with no visible signs of precipitation and was either used directly in this assay or first diluted 1:1 v/v with DMSO (∼1 mM final concentration).
38. 5d for peptide 1 or 2). Thus this assay cannot provide comparative information on the actual rate of channel mediated ion transport, which is faster for peptide 1 than for gramicidin A as judged by single channel conductance measurements (see text).
39. Driessen, A. J. M.; van den Hooven, H. W.; Kuiper, W.; van de Kamp, M.; Sahl, H.-G.; Konings, R. N. H.; Konings, W. N. Biochemistry 1995, 34, 1606-1614.
40. (a) Krimm, S.; Bandekar, J. In Advances in Protein Chemistry Afinsen, C. B., Edsall, J. T., Richards, F. M., Eds.; Academic Press: Orlando, Fl, 1986; pp 181-364.
41. (b) Haris, P. I.; Chapman. D. Biopolymers (Peptide Sci.) 1995, 37, 251-263.
42. 3-peptides, see: ref 1c.
43. (a) Suarez-Isla, B. A.; Lindstrom, W. K.; Montal, M. Biochemistry, 1983, 22, 2319-2323.
44. (b) Hille, B. Ionic Channels of Excitable Membranes 2nd ed.; Sinauer Associates: Sunderland, 1992.
45. (a) Hladky, S. B.; Haydon, D. A. Biochim. Biophys. Acta 1972, 274, 294-312.
46. (b) Bamberg, E.; Lauger, P. Biochim. Biophys. Acta 1974, 367, 127-133.
47. (a) Carpino, L. A.; El-Faham.,A. J. Org. Chem. 1994, 59, 695-698.
48. (b) Carpino, L. A. J. Am. Chem. Soc. 1993, 115, 4397-4398.
49. (c) Carpino, L. A.; El-Faham, A.; Minor, C. A.; Albericio, F. J. Chem. Soc., Chem. Commun. 1994, 201-203.
50. (d) Ehlrich, A.; Rothemund, S.; Brudel, M.; Carpino, L. A.; Beinert, M. Tetrahedron Lett. 1993, 34, 4781-4784.
51. Liposomes, New, R. R. C., Ed.; Oxford University Press: New York, 1990.
52. Plucinska, K.; Liberek, B. Tetrahedron Lett. 1987, 43, 3509-3517.
53. Tam, J. P.; Kent, S. B. H.; Wong, T. W.; Merrifield, R. B. Synthesis 1979, 955-957.
54. 2-peptides recently appeared: Guichard, G.; Seebach, D. Chimia 1997, 51, 315-318.
55. Schnolzer, M.; Alewood, P.; Jones, A.; Alewood, D.; Kent, S. B. H. Int. J. Pept. Protein Res. 1992, 40, 180-193.
56. Seebach has investigated solubilization of peptide aggregates with LiCl solutions in organic solvents: (a) Seebach, D.; Thaler, A.; Beck, A. K. Helv. Chim. Acta 1989, 72, 857-867. (b) Thaler, A.; Seebach, D. Helv. Chim. Acta 1991, 74, 616-627. (c) Thaler, A.; Seebach, D. Helv. Chim. Acta 1991, 74, 628-643.
57. Seebach has investigated solubilization of peptide aggregates with LiCl solutions in organic solvents: (a) Seebach, D.; Thaler, A.; Beck, A. K. Helv. Chim. Acta 1989, 72, 857-867. (b) Thaler, A.; Seebach, D. Helv. Chim. Acta 1991, 74, 616-627. (c) Thaler, A.; Seebach, D. Helv. Chim. Acta 1991, 74, 628-643.
58. Seebach has investigated solubilization of peptide aggregates with LiCl solutions in organic solvents: (a) Seebach, D.; Thaler, A.; Beck, A. K. Helv. Chim. Acta 1989, 72, 857-867. (b) Thaler, A.; Seebach, D. Helv. Chim. Acta 1991, 74, 616-627. (c) Thaler, A.; Seebach, D. Helv. Chim. Acta 1991, 74, 628-643.
59. Rance, M.; Sorensen, O.; BodenHausen, G.; Wagner, G.; Ernst, R. R.; Wuthrich, K. Biochem. Biophys. Res. Commun. 1983, 117, 479-485.
60. Merutka, G.; Dyson, H. J.; Wright, P. E. J. Biomol. NMR 1994, 4, 14-24.
61. (a) Benachir, T.; Lafleur, M. Biochim. Biophys. Acta 1995, 1235, 452-460.
62. (b) Portlock, S. H.; Claque, M. J.; Cherry, R. J. Biochim. Biophys. Acta 1990, 1030, 1-10.