Bovine pancreatic polypeptide (bPP) undergoes significant changes in conformation and dynamics upon binding to DPC micelles

Journal of Molecular Biology

Volumn 322, Issue 5, 2002, Pages 1117-1133

  Lerch, Mirjam ^a   Gafner, Verena ^a   Bader, Reto ^a   Christen, Barbara ^a   Folkers, Gerd ^a   Zerbe, Oliver ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Dynamics; Membrane; NMR; Pancreatic polypeptide; Structure

Indexed keywords

POLYPEPTIDE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CORRELATION ANALYSIS; HYDROPHOBICITY; MEASUREMENT; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PANCREAS; PRIORITY JOURNAL; PROTEIN STRUCTURE; RECEPTOR BINDING; RIGIDITY;

BOVINAE;

EID: 0036409123     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)00889-6     Document Type: Article

References (89)

1. Schwartz, T. W. & Tager, H. S. (1981). Isolation and biogenesis of a new peptide from pancreatic islets. Nature, 294, 589-591.
2. Katsuura, G., Asakawa, A. & Inui, A. (2002). Roles of pancreatic polypeptide in regulation of food intake. Peptides, 23, 323-329.
3. Clark, J. T., Kalra, P. S., Crowley, W. R. & Kalra, S. P. (1984). Neuropeptide Y and human pancreatic polypeptide stimulate feeding behavior in rats. Endocrinology, 115, 427-429.
4. Inui, A., Okita, M., Nakajima, M., Inoue, T., Sakatani, N., Oya, M. et al. (1991). Neuropeptide regulation of feeding in dogs. Am. J. Physiol. 261, R588-R594.
5. Michel, M. C., Beck-Sickinger, A. G., Cox, H., Doods, H. N., Herzog, H., Larhammar, D. et al. (1998). XVI International Union of Pharmacology recommendations for the nomenclature of neuropeptide Y, peptide YY, and pancreatic polypeptide receptors. Pharmacol. Rev. 50, 143-150.
6. Berglund, M. M., Lundell, I., Eriksson, H., Söll, R., Beck-Sickinger, A. G. & Larhammar, D. (2001). Studies of the human, rat, and guinea pig Y4 receptors using neuropeptide Y analogues and two distinct radioligands. Peptides, 22, 351-356.
7. Voisin, T., Goumain, M., Lorinet, A. M., Maoret, J. J. & Laburthe, M. (2000). Functional and molecular properties of the human recombinant Y4 receptor: resistance to agonist-promoted desensitization. J. Pharmacol. Exp. Ther. 292, 638-646.
8. Cabrele, C., Wieland, H. A., Langer, M., Stidsen, C. E. & Beck-Sickinger, A. G. (2001). Y-receptor affinity modulation by the design of pancreatic polypeptide/neuropeptide Y chimera led to Y(5)-receptor ligands with picomolar affinity. Peptides, 22, 365-378.
9. Cabrele, C. & Beck-Sickinger, A. G. (2000). Molecular characterization of the ligand-receptor interaction of the neuropeptide Y family. J. Pept. Sci. 6, 97-122.
10. Blundell, T. L., Pitts, J. E., Tickle, I. J., Wood, S. P. & Wu, C.-W. (1981). X-ray analysis (1.4 Å resolution) of avian pancreatic polypeptide: small globular protein hormone. Proc. Natl Acad. Sci. USA, 78, 4175-4179.
11. 1H NMR assignments and solution structure of bovine pancreatic polypeptide. Biochemistry, 31, 1245-1253.
12. Chin, J. W., Grotzfeld, R. M., Fabian, M. A. & Schepartz, A. (2001). Methodology for optimizing functional miniature proteins based on avian pancreatic polypeptide using phage display. Bioorg. Med. Chem. Letters, 11, 1501-1505.
13. Zondlo, N. J. & Schepartz, A. (1999). Highly specific DNA recognition by a designed miniature protein. J. Am. Chem. Soc. 121, 6938-6939.
14. Chin, J. W. & Schepartz, A. (2001). Conc erted evolution of structure and function in a miniature protein. J. Am. Chem. Soc. 123, 2929-2930.
15. 1H nuclear magnetic resonance and restrained molecular dynamics. Eur. J. Biochem. 209, 765-771.
16. Monks, S. A., Karagianis, G., Howlett, G. J. & Norton, R. S. (1996). Solution structure of human neuropeptide Y. J. Biomol. NMR, 8, 379-390.
17. Cowley, D. J., Hoflack, J. M., Pelton, J. T. & Saudek, V. (1992). Structure of neuropeptide Y dimer in solution. Eur. J. Biochem. 205, 1099-1106.
18. Bader, R., Bettio, A., Beck-Sickinger, A. G. & Zerbe, O. (2001). Structure and dynamics of micelle-bound neuropeptide Y: comparison with unligated NPY and implications for receptor selection. J. Mol. Biol. 305, 307-329.
19. Kaiser, E. T. & Kézdy, F. J. (1984). Amphiphilic secondary structure: design of peptide hormones. Science, 223, 249-255.
20. Sargent, D. F. & Schwyzer, R. (1986). Membrane lipid phase as catalyst for peptide-receptor interactions. Proc. Natl Acad. Sci. USA, 83, 5774-5778.
21. Schwyzer, R. (1986). Molecular mechanism of opioid receptor selection. Biochemistry, 25, 6335-6342
22. Moroder, L., Romano, R., Guba, W., Mierke, D. F., Kessler, H., Delporte, C. et al. (1993). New evidence for a membrane-bound pathway in hormone receptor binding. Biochemistry, 32, 13551-13559.
23. Inooka, H., Ohtaki, T., Kitahara, O., Ikegami, T., Endo, S., Kitada, C. et al. (2001). Conformation of a peptide ligand bound to its G-protein coupled receptor. Nature Struct. Biol. 8, 161-165.
24. Bader, R., Rytz, G., Lerch, M., Beck-Sickinger, A. G. & Zerbe, O. (2002). Key motif to gain selectivity at the neuropeptide Y5-receptor: solution structure and dynamics of [Ala31,Pro32]-NPY. Biochemistry, 41, 8031-8042.
25. Wüthrich, K. (1986). NMR of Proteins and Nucleic Acids, Wiley, New York.
26. Henry, G. D. & Brian, D. S. (1990). Methods to study membrane protein structure in solution. In Methods in Enzymology (James, T. L. & Oppenheimer, N. J., eds), part C, vol. 293, pp. 515-535.
27. Güntert, P., Mumenthaler, C. & Wüthrich, K. (1997). Torsion angle dynamics for NMR structure calculation with the new program Dyana. J. Mol. Biol. 273, 283-298.
28. Case, D. A., Pearlman, D. A., Caldwell, J. W., Cheatham, T. E., III, Ross, W. S., Simmerling, C. L., et al. (1999). AMBER 6, University of California, San Francisco.
29. Pearlman, D. A., Case, D. A., Caldwell, J. W., Ross, W. S., Cheatham, T. E., DeBolt, S. et al. (1995). AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energectic properties of molecules. Comput. Phys. Commun. 91, 1-41.
30. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R. & Thornton, J. M. (1996). AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR, 8, 477-486.
31. Wüthrich, K., Billeter, M. & Braun, W. (1984). Polypeptide secondary structure determination by nuclear magnetic resonance observation of short proton-proton distances. J. Mol. Biol. 180, 715-740.
32. 1H nuclear magnetic resonance spectra. Computation of sterically allowed proton-proton distances and statistical analysis of proton-proton distances in single crystal protein conformations. J. Mol. Biol. 155, 321-346.
33. Shao, H., Jao, S., Ma, K. & Zagorski, M. G. (1999). Solution structures of micelle-bound amyloid beta-(1-40) and beta-(1-42) peptides of Alzheimer's disease. J. Mol. Biol. 285, 755-773.
34. Brown, L. R., Bösch, C. & Wüthrich, K. (1981). Location and orientation relative to the micelle surface for glucagon in mixed micelles with dodecylphosphocholine: EPR and NMR studies. Biochim. Biophys. Acta, 642, 296-312.
35. Lipari, G. & Szabo, A. (1982). Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104, 4546-4559.
36. Lipari, G. & Szabo, A. (1982). Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104, 4559-4570.
37. 1H NMR spectroscopy. Biochemistry, 29, 7387-7401.
38. 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry, 28, 8972-8979.
39. Mandel, A. M., Akke, M. & Palmer, A. G., 3rd (1995). Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J. Mol. Biol. 246, 144-163.
40. 1H NMR relaxation. Prog. NMR Spectrosc. 31, 63-105.
41. Chang, P. J., Noelken, M. E. & Kimmel, J. R. (1980). Reversible dimerization of avian pancreatic polypeptide. Biochemistry, 19, 1844-1849.
42. Noelken, M. E., Chang, P. J. & Kimmel, J. R. (1980). Conformation and association of pancreatic polypeptide from three species. Biochemistry, 19, 1838-1843.
43. Burley, S. K. & Petsko, G. A. (1985). Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science, 229, 23-28.
44. Hunter, C. A. & Sanders, J. K. M. (1998). The nature of π-π interactions. J. Am. Chem. Soc. 112, 5525-5534.
45. Monne, M., Nilsson, I., Johansson, M., Elmhed, N. & von Heijne, G. (1998). Positively and negatively charged residues have different effects on the position in the membrane of a model transmembrane helix. J. Mol. Biol. 284, 1177-1183.
46. Killian, J. A. & von Heijne, G. (2000). How proteins adapt to a membrane-water interface. Trends Biochem. Sci. 25, 429-434.
47. White, S. H. & Wimley, W. C. (1998). Hydrophobic interactions of peptides with membrane interfaces. Biochim. Biophys. Acta, 1376, 339-352.
48. McLean, L. R., Buck, S. H. & Krstenansky, J. L. (1990). Examination of the role of the amphipathic alpha-helix in the interaction of neuropeptide Y and active cyclic analogues with cell membrane receptors and dimyristoylphosphatidylcholine. Biochemistry, 29, 2016-2022.
49. McLean, L. R., Baron, B. M., Buck, S. H. & Krstenansky, J. L. (1990). Lipid and membrane interactions of neuropeptide Y. Biochim. Biophys. Acta, 1024, 1-4.
50. Beck-Sickinger, A. G., Wieland, H. A., Wittneben, H., Willim, K. D., Rudolf, K. & Jung, G. (1994). Complete L-alanine scan of neuropeptide Y reveals ligands binding to Y1 and Y2 receptors with distinguished conformations. Eur. J. Biochem. 225, 947-958.
51. McCrea, K., Wisialowski, T., Cabrele, C., Church, B., Beck-Sickinger, A. G., Kraegen, E. & Herzog, H. (2000). 2-36[K4,RYYSA(19-23)]PP a novel Y5-receptor preferring ligand with strong stimulatory effect on food intake. Regul. Pept. 87, 47-58.
52. Eckard, C. P., Cabrele, C., Wieland, H. A. & Beck-Sickinger, A. G. (2001). Molecular characterisation of NPY receptors using synthetic peptides and anti-receptor antibodies. Molecules, 6, 448-467.
53. Walker, P., Munoz, M., Martinez, R. & Peitsch, M. C. (1994). Acidic residues in extracellular loops of the human Y1 neuropeptide Y receptor are essential for ligand binding. J. Biol. Chem. 269, 2863-2869.
54. Munch, G., Walker, P., Shine, J. & Herzog, H. (1995). Ligand binding analysis of human neuropeptide Y1 receptor mutants expressed in E. coli. Recept. Channels, 3, 291-297.
55. Robin-Jagerschmidt, C., Sylte, I., Bihoreau, C., Hendricksen, L., Calvet, A., Dahl, S. G. & Benicourt, C. (1998). The ligand binding site of NPY at the rat Y1 receptor investigated by site-directed mutagenesis and molecular modeling. Mol. Cell. Endocrinol. 139, 187-198.
56. Parker, M. S., Lundell, I. & Parker, S. L. (2002). Pancreatic polypeptide receptors: affinity, sodium sensitivity and stability of agonist binding. Peptides, 23, 291-303.
57. Gregor, P., Millham, M. L., Feng, Y., DeCarr, L. B., McCaleb, M. L. & Cornfield, L. J. (1996). Cloning and characterization of a novel receptor to pancreatic polypeptide, a member of the neuropeptide Y receptor family. FEBS Letters, 381, 58-62.
58. Keire, D. A., Bowers, C. W., Solomon, T. E. & Reeve, J. R., Jr (2002). Structure and receptor binding of PYY analogs. Peptides, 23, 305-321.
59. 125I]Leu31, Pro34-PYY is a high affinity radio-ligand for rat PP1/Y4 and Y1 receptors: evidence for heterogeneity in pancreatic polypeptide receptors. Peptides, 18, 397-401.
60. Eriksson, H., Berglund, M. M., Holmberg, S. K., Kahl, U., Gehlert, D. R. & Larhammar, D. (1998). The cloned guinea pig pancreatic polypeptide receptor Y4 resembles more the human Y4 than does the rat Y4. Regul. Pept. 75-76, 29-37.
61. Gehlert, D. R., Schober, D. A., Beavers, L., Gadski, R., Hoffman, J. A., Smiley, D. L. et al. (1996). Characterization of the peptide binding requirements for the cloned human pancreatic polypeptide-preferring receptor. Mol. Pharmacol. 50, 112-118.
62. Gingerich, R. L., Akpan, J. O., Gilbert, W. R., Leith, K. M., Hoffmann, J. A. & Chance, R. E. (1991). Structural requirements of pancreatic polypeptide receptor binding. Am. J. Physiol. 261, E319-E324.
63. Bard, J. A., Walker, M. W., Branchek, T. A. & Weinshank, R. L. (1995). Cloning and functional expression of a human Y4 subtype receptor for pancreatic polypeptide, neuropeptide Y, and peptide YY. J. Biol. Chem. 270, 26762-26765.
64. Lundell, I., Blomqvist, A. G., Berglund, M. M., Schober, D. A., Johnson, D., Statnick, M. A. et al. (1995). Cloning of a human receptor of the NPY receptor family with high affinity for pancreatic polypeptide and peptide YY. J. Biol. Chem. 270, 29123-29128.
65. Walker, M. W., Smith, K. E., Bard, J., Vaysse, P. J., Gerald, C., Daouti, S. et al. (1997). A structure-activity analysis of the cloned rat and human Y4 receptors for pancreatic polypeptide. Peptides, 18, 609-612.
66. Lundell, I., Statnick, M. A., Johnson, D., Schober, D. A., Starback, P., Gehlert, D. R. & Larhammar, D. (1996). The cloned rat pancreatic polypeptide receptor exhibits profound differences to the orthologous receptor. Proc. Natl Acad. Sci. USA, 93, 5111-5115.
67. Cabrele, C., Langer, M., Bader, R., Wieland, H. A., Doods, H. N., Zerbe, O. & Beck-Sickinger, A. G. (2000). The first selective agonist for the neuropeptide Y5 receptor increases food intake in rats. J. Biol. Chem. 275, 36043-36048.
68. Larhammar, D. (1996). Structural diversity of receptors for neuropeptide Y, peptide YY and pancreatic polypeptide. Regul. Pept. 65, 165-174.
69. 13C. J. Biomol. NMR, 12, 109-121.
70. Marley, J., Lu, M. & Bracken, C. (2001). A method for efficient isotopic labeling of recombinant proteins. J. Biomol. NMR, 20, 71-75.
71. 15N Hartmann-Hahn multiple-quantum coherence and nuclear Overhauser-multiple quantum coherence spectroscopy: application to interleukin 1β. Biochemistry, 28, 6150-6156.
72. 1H multiple quantum coherence spectroscopy. FEBS Letters, 243, 93-98.
73. 15N NMR via proton-detected multiple-quantum coherences: studies of large peptides. J. Am. Chem. Soc. 106, 6104-6105.
74. Meiboom, S. & Gill, D. (1958). Modified spin-echo method for measuring spin-relaxation rates. Rev. Sci. Instrum. 29, 688-691.
75. Vold, R. L., Waugh, J. S., Klein, M. P. & Phelps, D. E. (1968). Measurement of spin relaxation rates in complex systems. J. Chem. Phys. 48, 3831-3832.
76. Noggle, J. H. & Schirmer, R. E. (1971). The Nuclear Overhauser Effect - Chemical Applications, Academic Press, New York.
77. 1H spin system identification in macromolecules. J. Am. Chem. Soc. 110, 7870-7872.
78. Otting, G. (1990). Zero-quantum suppression in NOESY and experiments with a z-filter. J. Magn. Reson. 86, 496-508.
79. Hurd, R. E. (1990). Gradient-enhanced spectroscopy. J. Magn. Reson. 87, 422.
80. Keeler, J., Clowes, R. T., Davis, A. L. & Laue, E. D. (1994). Pulsed-field gradients: theory and practice. Methods Enzymol. 239, 145-207.
81. Bartels, C., Xia, T.-h., Billeter, M., Güntert, P. & Wüthrich, K. (1995). The program XEASY for computer-supported spectral analysis of biological macromolecules. J. Biomol. NMR, 6, 1-10.
82. Szyperski, T., Güntert, P., Otting, G. & Wüthrich, K. (1992). Determination of scalar coupling constants by inverse Fourier transfomation of in-phase multiplets. J. Magn. Reson. 99, 552-560.
83. Griesinger, C., Sørensen, O. & Ernst, R. R. (1987). Practical aspects of the E.COSY technique. Measurement of scalar spin-spin coupling constants in peptides. J. Magn. Reson. 75, 474-492.
84. Weiner, P. K., Kollman, P. A., Nguyen, D. T. & Case, D. A. (1986). An all-atom force field for simulations of proteins and nucleic acids. J. Comput. Chem. 7, 230-252.
85. Koradi, R., Billeter, M. & Wüthrich, K. (1996). MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14, 29-32.
86. Kabsch, W. & Sander, C. (1983). Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577-2637.
87. Press, W. H., Teukolsky, S. A., Vetterling, W. T. & Flannery, B. P. (1992). Numerical Recipes. The Art of Scientific Computing, 2nd edit., Cambridge University Press, Cambridge.
88. 13C heteronuclear NMR spectroscopy. J. Am. Chem. Soc. 113, 4371-4380.
89. 15N NMR relaxation. J. Am. Chem. Soc, 117, 12562-12566.