Structural investigations of a human calcitonin-derived carrier peptide in a membrane environment by solid-state NMR

Biochemistry

Volumn 43, Issue 39, 2004, Pages 12459-12468

  Wagner, Kerstin ^a   Beck Sickinger, Annette G ^a   Huster, Daniel ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANISOTROPY; DNA; FATTY ACIDS; FLUORESCENCE; NUCLEAR MAGNETIC RESONANCE; PARAMAGNETISM; PHOSPHOLIPIDS; PLASMAS; POLARIZATION; POWDERS;

CHEMICAL SHIFT ANISOTROPY; GREEN FLUORESCENT PROTEIN; HUMAN CALCITONIN (HCT); LIPID MEMBRANES;

PROTEINS;

ALANINE; AMINO ACID; CALCITONIN; CARRIER PROTEIN; DRUG; FATTY ACID; GLYCINE; GREEN FLUORESCENT PROTEIN; LIPID; PEPTIDE; PHENYLALANINE; PHOSPHOLIPID; PLASMID DNA; VALINE;

ANISOTROPY; ARTICLE; BETA SHEET; CELL MEMBRANE; DEUTERON NUCLEAR MAGNETIC RESONANCE; HUMAN; LIPID MEMBRANE; NOSE MUCOSA; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; CALCITONIN; CARBON ISOTOPES; CARRIER PROTEINS; HUMANS; MEMBRANE LIPIDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NASAL MUCOSA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES; PHOSPHATIDYLGLYCEROLS; PHOSPHORUS ISOTOPES; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; THERMODYNAMICS;

EID: 4744363014     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049181y     Document Type: Article

References (68)

1. Krauss, U., and Beck-Sickinger, A. (2002) Carrier peptides are promising tools for a broad range of applications, in Membrane interacting proteins and peptides (Heitz, F., Ed.) pp 25-42, Research Signpost, Trivandrum.
2. Lindgren, M., Hallbrink, M., Prochiantz, A., and Langel, U. (2000) Cell-penetrating peptides, Trends Pharmacol. Sci. 21, 99-103.
3. 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.
4. Derossi, D., Chassaing, G., and Prochiantz, A. (1998) Trojan peptides: the penetratin system for intracellular delivery, Trends Cell Biol. 8, 84-87.
5. Morris, M. C., Vidal, P., Chaloin, L., Heitz, F., and Divita, G. (1997) A new peptide vector for efficient delivery of oligonucleotides into mammalian cells, Nucleic Acids Res. 25, 2730-2736.
6. Pooga, M., Hallbrink, M., Zorko, M., and Langel, U. (1998) Cell penetration by transportan, FASEB J. 12, 67-77.
7. Schmidt, M. C., Rothen-Rutishauser, B., Rist, B., Beck-Sickinger, A., Wunderli-Allenspach, H., Rubas, W., Sadee, W., and Merkle, H. P. (1998) Translocation of human calcitonin in respiratory nasal epithelium is associated with self-assembly in lipid membrane, Biochemistry 37, 16582-16590.
8. Lang, S., Rothen-Rutishauser, B., Perriard, J. C., Schmidt, M. C., and Merkle, H. P. (1998) Permeation and pathways of human calcitonin (hCT) across excised bovine nasal mucosa, Peptides 19, 599-607.
9. Pontiroli, A. E., Alberetto, M., and Pozza, G. (1985) Intranasal calcitonin and plasma calcium concentrations in normal subjects, Br. Med. J. 290, 1390-1391.
10. Silverman, S. L. (1997) Calcitonin, Am. J. Med. Sci. 313, 13-16.
11. Stroop, S. D., Nakamuta, H., Kuestner, R. E., Moore, E. E., and Epand, R. M. (1996) Determinants for calcitonin analog interaction with the calcitonin receptor N-terminus and transmembrane-loop regions, Endocrinology 137, 4752-4756.
12. Machova, Z., Muhle, C., Krauss, U., Trehin, R., Koch, A., Merkle, H. P., and Beck-Sickinger, A. G. (2002) Cellular internalization of enhanced green fluorescent protein ligated to a human calcitonin-based carrier peptide, ChemBioChem 3, 672-677.
13. Krauss, U., Kratz, F., and Beck-Sickinger, A. G. (2003) Novel daunorubicin-carrier peptide conjugates derived from human calcitonin segments, J. Mol. Recognit. 16, 280-287.
14. Krauss, U., Muller, M., Stahl, M., and Beck-Sickinger, A. G. (2004) In vitro gene delivery by a novel human calcitonin (hCT)-derived carrier peptide, Bioorg. Med. Chem. Lett. 14, 51-54.
15. Binder, H., and Lindblom, G. (2003) Charge-dependent translocation of the Trojan peptide penetratin across lipid membranes, Biophys. J. 85, 982-995.
16. Bauer, H. H., Muller, M., Goette, J., Merkle, H. P., and Fringeli, U. P. (1994) Interfacial adsorption and aggregation associated changes in secondary structure of human calcitonin monitored by ATR-FTIR spectroscopy, Biochemistry 33, 12276-12282.
17. 13C NMR, J. Biol. Chem. 278, 2859-2865.
18. Arvinte, T., Cudd, A., and Drake, A. F. (1993) The structure and mechanism of formation of human calcitonin fibrils, J. Biol. Chem. 268, 6415-6422.
19. Arvinte, T., and Drake, A. F. (1993) Comparative study of human and salmon calcitonin secondary structure in solutions with low dielectric constants, J. Biol. Chem. 268, 6408-6414.
20. Epand, R. M., Epand, R. F., and Orlowski, R. C. (1985) Presence of an amphipathic helical segment and its relationship to biological potency of calcitonin analogs, Int. J. Pept. Protein Res. 25, 105-111.
21. Epand, R. M., Epand, R. F., Orlowski, R. C., Schlueter, R. J., Boni, L. T., and Hui, S. W. (1983) Amphipathic helix and its relationship to the interaction of calcitonin with phospholipids, Biochemistry 22, 5074-5084.
22. Hashimoto, Y., Toma, K., Nishikido, J., Yamamoto, K., Haneda, K., Inazu, T., Valentine, K. G., and Opella, S. J. (1999) Effects of glycosylation on the structure and dynamics of eel calcitonin in micelles and lipid bilayers determined by nuclear magnetic resonance spectroscopy, Biochemistry 38, 8377-8384.
23. Motta, A., Pastore, A., Goud, N. A., and Castiglione Morelli, M. A. (1991) Solution conformation of salmon calcitonin in sodium dodecyl sulfate micelles as determined by two-dimensional NMR and distance geometry calculations, Biochemistry 30, 10444-10450.
24. Motta, A., Andreotti, G., Amodeo, P., Strazzullo, G., and Castiglione Morelli, M. A. (1998) Solution structure of human calcitonin in membrane-mimetic environment: the role of the amphipathic helix, Proteins 32, 314-323.
25. 1H NMR study of human calcitonin in solution, Biochemistry, 30, 2364-2371.
26. Epand, R. M., Epand, R. F., and Orlowski, R. C. (1988) Biologically active calcitonin analogs which have minimal interactions with phospholipids, Biochem. Biophys. Res. Commun. 152, 203-207.
27. Wagner, K., Van Mau, N., Boichot, S., Kajava, A. V., Krauss, U., Le Grimellec, C., Beck-Sickinger, A., and Heitz, F. (2004) Interactions of human calcitonin fragment 9-32 with phospholipids: a monolayer study, Biophys. J. 87, 386-395.
28. Marsh, D. (1996) Lateral pressure in membranes, Biochim. Biophys. Acta 1286, 183-223.
29. Stejskal, E. O., and Schaefer, J. (1976) Carbon-13 nuclear magnetic resonance of polymers spinning at the magic angle, J. Am. Chem. Soc. 98, 1031-1032.
30. Torres, J., Stevens, T. J., and Samso, M. (2003) Membrane proteins: the 'Wild West' of structural biology, Trends Biochem. Sci. 28, 137-144.
31. Luca, S., White, J. F., Sohal, A. K., Filippov, D. V., van Boom, J. H., Grisshammer, R., and Baldus, M. (2003) The conformation of neurotensin bound to its G protein-coupled receptor, Proc. Natl. Acad. Sci. U.S.A. 100, 10706-10711.
32. Ketchem, R. R., Hu, W., and Cross, T. A. (1993) High-resolution conformation of gramicidin A in a lipid bilayer by solid-state NMR, Science 261, 1457-1460.
33. Barré, P., Zschörnig, O., Arnold, K., and Huster, D. (2003) Structural and Dynamical Changes of the Bindin B18 Peptide upon Binding to Lipid Membranes. A Solid-State NMR Study, Biochemistry 42, 8377-8386.
34. Lam, Y. H., Wassall, S. R., Morton, C. J., Smith, R., and Separovic, F. (2001) Solid-state NMR structure determination of melittin in a lipid environment, Biophys. J. 81, 2752-2761.
35. Yang, J., Gabrys, C. M., and Weliky, D. P. (2001) Solid-state nuclear magnetic resonance evidence for an extended β strand conformation of the membrane-bound HIV-1 fusion peptide, Biochemistry 40, 8126-8137.
36. Hirsh, D. J., Hammer, J., Maloy, W. L., Blazyk, J., and Schaefer, J. (1996) Secondary structure and location of a magainin analogue in synthetic phospholipid bilayers, Biochemistry 35, 12733-12741.
37. Zeri, A. C., Mesleh, M. F., Nevzorov, A. A., and Opella, S. J. (2003) Structure of the coat protein in fd filamentous bacteriophage particles determined by solid-state NMR spectroscopy, Proc. Natl. Acad. Sci. U.S.A. 100, 6458-6463.
38. Kaiser, E., Colescott, R. L., Bossinger, C. D., and Cook, P. I. (1970) Color test for detection of free terminal amino groups in the solid-phase synthesis of peptides, Anal. Biochem. 34, 595-598.
39. Huster, D., Arnold, K., and Gawrisch, K. (1998) Influence of docosahexaenoic acid and cholesterol on lateral lipid organization in phospholipid membranes, Biochemistry 37, 17299-17308.
40. Bennett, A. E., Rienstra, C. M., Auger, M., Lakshmi, K. V., and Griffin, R. G. (1995) Heteronuclear decoupling in rotating solids, J. Chem. Phys. 103, 6951-6958.
41. Morcombe, C. R., and Zilm, K. W. (2003) Chemical shift referencing in MAS solid state NMR, J. Magn. Reson. 162,479-486.
42. Torchia, D. A., and Szabo, A. (1982) Spin-lattice relaxation in solids, J. Magn. Reson. 49, 107-121.
43. Vogel, A., Scheidt, H. A., and Huster, D. (2003) The distribution of lipid attached EPR probes in bilayers. Application to membrane protein topology, Biophys. J. 85, 1691-1701.
44. 13C cross polarization magic-angle spinning, J. Magn. Reson. 47, 462-475.
45. Munowitz, M. G., Griffin, R. G., Bodenhausen, G., and Huang, T. H. (1981) Two-dimensional rotational spin-echo nuclear magnetic resonance in solids: correlation of chemical shift and dipolar interactions, J. Am. Chem. Soc. 103, 2529-2533.
46. 13C-NMR of polymers, J. Magn. Reson. 52, 123-129.
47. Hong, M., Gross, J. D., and Griffin, R. G. (1997) Site-resolved determination of peptide torsion angle Φ from relative orientations of backbone N-H and C-H bonds by solid-state NMR, J. Phys. Chem. 101, 5869-5874.
48. Bielecki, A., Kolbert, A. C., and Levitt, M. H. (1989) Frequency-switched pulse sequences: homonuclear decoupling and dilute spin NMR in solids, Chem. Phys. Lett. 155, 341-345.
49. Schmidt-Rohr, K., and Spiess, H. W. (1994) Multidimensional solid-state NMR and polymers, Academic Press, San Diego.
50. Russell, Y., Evans, P., and Dodd, G. H. (1989) Characterization of the total lipid and fatty acid composition of rat olfactory mucosa, J. Lipid Res. 30, 877-884.
51. Huster, D., Yao, X., Jakes, K. S., and Hong, M. (2002) Conformational changes of colicin Ia channel-forming domain upon membrane binding: a solid-state NMR study, Biochim. Biophys. Acta 1561, 159-170.
52. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1991) Relationship between nuclear magnetic resonance chemical shift and protein secondary structure, J. Mol. Biol. 222, 311-333.
53. Wishart, D. S., and Sykes, B. D. (1994) Chemical shifts as a tool for structure determination, Methods Enzymol. 239, 363-392.
54. 13C nuclear magnetic resonance chemical shifts, J. Am. Chem. Soc. 113, 5490-5492.
55. Castellani, F., van Rossum, B., Diehl, A., Schubert, M., Rehbein, K., and Oschkinat, H. (2002) Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy, Nature 420, 98-102.
56. Saito, H., Tuzi, S., and Naito, A. (2001) Empirical versus nonempirical evaluation of secondary structure of fibrous and membrane proteins by solid-state NMR: a practical approach, Annu. Rep. NMR Spectrosc. 38, 79-121.
57. Luca, S., Filippov, D. V., van Boom, J. H., Oschkinat, H., de Groot, H. J., and Baldus, M. (2001) Secondary chemical shifts in immobilized peptides and proteins: a qualitative basis for structure refinement under magic angle spinning, J. Biomol. NMR 20, 325-331.
58. Creighton, T. E. (1993) Proteins. Structures and molecular properties, W. H. Freeman and Company, New York.
59. Scherer, P. G., and Seelig, J. (1989) Electric charge effects on phospholipid headgroups. Phosphatidylcholine in mixtures with cationic and anionic amphiphiles, Biochemistry 28, 7720-7728.
60. 2H NMR and ESR study using designed transmembrane α-helical peptides and gramicidin A, Biochemistry 37, 9333-9345.
61. Wimley, W. C., and White, S. H. (1996) Experimentally determined hydrophobicity scale for proteins at membrane interfaces, Nat. Struct. Biol. 3, 842-848.
62. 13C solid-state NMR spectroscopy, Magn. Reson. Chem. 42, 247-257.
63. Kanaori, K., and Nosaka, A. Y. (1995) Study of human calcitonin fibrillation by proton nuclear magnetic resonance spectroscopy, Biochemistry 34, 12138-12143.
64. 13C NMR, Protein Sci. 9, 867-877.
65. Tycko, R. (2003) Insights into the amyloid folding problem from solid-state NMR, Biochemistry 42, 3151-3159.
66. Petkova, A. T., Ishii, Y., Balbach, J. J., Antzutkin, O. N., Leapman, R. D., Delaglio, F., and Tycko, R. (2002) A structural model for Alzheimer's β-amyloid fibrils based on experimental constraints from solid-state NMR, Proc. Natl. Acad. Sci. U.S.A. 99, 16742-16747.
67. Trehin, R., Krauss, U., Muff, R., Meinecke, M., Beck-Sickinger, A. G., and Merkle, H. P. (2004) Cellular internalization of human calcitonin derived peptides in MDCK monolayers: a comparative study with Tat(47-57) and penetratin(43-58), Pharm. Res. 21, 33-42.
68. http://www.bmrb.wisc.edu/index.html.