A designed four-α-helix bundle that binds the volatile general anesthetic halothane with high affinity

Biophysical Journal

Volumn 78, Issue 2, 2000, Pages 982-993

  Johansson, Jonas S ^a,b,d   Scharf, Daphna ^a,c   Davies, Lowri A ^a,c   Reddy, Konda S ^b   Eckenhoff, Roderic G ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c Center for Molecular Modeling   (United States)

^d HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARBON 14; HALOTHANE; INHALATION ANESTHETIC AGENT; LEUCINE; METHIONINE;

ANESTHESIA MECHANISM; ARTICLE; BINDING AFFINITY; BINDING SITE; COMPUTER SIMULATION; GAS CHROMATOGRAPHY; GENERAL ANESTHESIA; LIGAND BINDING; MOLECULAR DYNAMICS; PEPTIDE SYNTHESIS; PHOTOAFFINITY LABELING;

EID: 0034077948     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(00)76656-2     Document Type: Article

References (62)

1. Ballew, R. M., J. Sabelko, and M. Gruebele. 1996. Direct observation of fast protein folding: the initial collapse of apomyoglobin. Proc. Natl. Acad. Sci. USA. 93:5759-5764.
2. Basu, G., D. Anglos, and A. Kuki. 1993. Fluorescence quenching in a strongly helical peptide series: the role of noncovalent pathways in modulating electronic interactions. Biochemistry. 32:3067-3076.
3. Bernstein, H. D., M. A. Poritz, K. Strub, P. J. Hoben, S. Brenner, and P. Walter. 1989. Model for signal sequence recognition from amino-acid sequence of 54k subunit of signal recognition particle. Nature. 340: 482-486.
4. Betz, S. F., P. A. Liebman, and W. F. DeGrado. 1997. De novo design of native proteins: characterization of proteins intended to fold into anti-parallel, Rop-like, four-helix bundles. Biochemistry. 36:2450-2458.
5. Bryson, J. W., S. F. Betz, H. S. Lu, D. J. Suich, H. X. Zhou, K. T. O'Neil, and W. F. DeGrado. 1995. Protein design: a hierarchic approach. Science. 270:935-941.
6. Cantor, R. 1997. The lateral pressure profile in membranes: a physical mechanism of general anesthesia. Biochemistry. 36:2339-2344.
7. Cornell, W. D., P. Cieplak, C. I. Bayly, I. R. Gould, K. M. Merz, D. M. Ferguson, D. C. Spellmeyer, T. Fox, J. W. Caldwell, and P. A. Kollman. 1995. A second generation force field for the simulation of proteins and nucleic acids. J. Am. Chem. Soc. 117:5179-5197.
8. Davies, L. A., M. L. Klein, and D. Scharf. 1999a. The vacuum structure of a synthetic four-α-helix bundle which binds halothane. Biophys. J. 76:A383.
9. Davies, L. A., M. L. Klein, and D. Scharf. 1999b. Molecular dynamics simulation of a synthetic four-α-helix bundle that binds the anesthetic halothane. FEBS Lett. 455:332-338.
10. Dougherty, D. A. 1996. Cation-π interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science. 271:163-168.
11. + conduction and selectivity. Science. 280:69-77.
12. 19F-NMR study. Proc. Natl. Acad. Sci. USA. 90:6478-6482.
13. 2) method for characterizing anesthetic binding to proteins: analysis of isoflurane binding to albumin. Biochemistry. 31:7069-7076.
14. Eckenhoff, R. G. 1996a. An inhalational anesthetic binding domain in the nicotinic acetylcholine receptor. Proc. Natl. Acad. Sci. USA. 93: 2807-2810.
15. Eckenhoff, R.G. 1996b. Amino acid resolution of halothane binding sites in serum albumin. J. Biol. Chem. 271:15521-15526.
16. Eckenhoff, R. G. 1998. Do specific or nonspecific interactions with proteins underlie inhalational anesthetic action. Mol. Pharmacol. 54: 610-615.
17. Eckenhoff, R. G., and J. S. Johansson. 1997. Interactions between inhaled anesthetics and proteins. Pharmacol. Rev. 49:343-367.
18. Eckenhoff, R. G., and H. Shuman. 1993. Halothane binding to soluble proteins determined by photoaffinity labeling. Anesthesiology. 79: 96-106.
19. Edelhoch, H. 1967. Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry. 6:1948-1954.
20. Fersht, A. R., and C. Dingwall. 1979. Cysteinyl-tRNA synthetase from Escherichia coli does not need an editing mechanism to reject serine and alanine. High binding energy of small groups in specific molecular interactions. Biochemistry. 18:1245-1249.
21. Franks, N. P., and W. R. Lieb. 1994. Molecular and cellular mechanisms of general anesthesia. Nature. 367:607-614.
22. Gellman, S. H. 1991. On the role of methionine residues in the sequence-independent recognition of nonpolar protein surfaces. Biochemistry. 30:6633-6636.
23. Gibney, B. R., J. S. Johansson, F. Rabanal, J. J. Skalicky, A. J. Wand, and P. L. Dutton. 1997a. Global topology and stability and local structure and dynamics in a synthetic spin-labeled four-helix bundle protein. Biochemistry. 36:2798-2806.
24. Gibney, B. R., S. E. Mulholland, F. Rabanal, and P. L. Dutton. 1996. Ferredoxin and ferredoxin-heme maquettes. Proc. Natl. Acad. Sci. USA. 93:15041-15046.
25. Gibney, B. R., F. Rabanal, J. J. Skalicky, A, J. Wand, and P. L. Dutton. 1997b. Design of a unique protein scaffold for maquettes. J. Am. Chem. Soc. 119:2323-2324.
26. Harris, R. A., S. J. Mihic, J. E. Dildy-Mayfield, and T. K. Machu. 1995. Actions of anesthetics on ligand-gated ion channels: role of receptor subunit composition. FASEB J. 9:1454-1462.
27. Janin, J., S. Wodak, M. Levitt, and B. Maigret. 1978. Conformation of amino acid side-chains in proteins. J. Mol. Biol. 125:357-386.
28. Jasanoff, A., and A. R. Fersht. 1994. Quantitative determination of helical propensities from trifluoroethanol titration curves. Biochemistry. 33: 2129-2135.
29. Jevtovic-Todorovic, V., S. M. Todorovic, S. Mennerick, S. Powell, K. Dikranian, N. Benshoff, C. F. Zorumski, and J. W. Olney. 1998. Nitrous oxide (laughing gas) is an NMDA antagonist, neuroprotectant and neurotoxin. Nature Med. 4:460-463.
30. Johansson, J. S. 1997. Binding of the volatile anesthetic chloroform to albumin demonstrated using tryptophan fluorescence quenching. J. Biol. Chem. 272:17961-17965.
31. Johansson, J. S. 1998. Probing the structural features of volatile anesthetic binding sites with synthetic peptides. Toxicol. Lett. 101:369-375.
32. Johansson, J. S., R. G. Eckenhoff, and P. L. Dutton. 1995. Binding of halothane to serum albumin demonstrated using tryptophan fluorescence. Anesthesiology. 83:316-324.
33. Johansson, J. S., B. R. Gibney, F. Rabanal, K. S. Reddy, and P. L. Dutton. 1998a. A designed cavity in the hydrophobic core of a four-α-helix bundle improves volatile anesthetic binding affinity. Biochemistry. 37: 1421-1429.
34. Johansson, J. S., B. R. Gibney, J. J. Skalicky, A. J. Wand, and P. L. Dutton. 1998b. A native-like three-α-helix bundle protein from structure based redesign: a novel maquette scaffold. J. Am. Chem. Soc. 120:3881-3886.
35. Johansson, J. S., F. Rabanal, and P. L. Dutton. 1996. Binding of the volatile anesthetic halothane to the hydrophobic core of a tetra-α-helix bundle protein. J. Pharmacol. Exp. Ther. 279:56-61.
36. Johansson, J. S., and H. Zou. 1999. Partitioning of four modern volatile general anesthetics into solvents that model buried amino acid side-chains. Biophys. Chem. 79:107-116.
37. Johansson, J. S., H. Zou, and J. T. Tanner. 1999. Bound volatile general anesthetics alter both local protein dynamics and global protein stability. Anesthesiology. 90:235-245.
38. Jorgensen, W. L., J. D. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
39. Lau, S. Y. M., A. K. Taneja, and R. S. Hodges. 1984. Synthesis of a model protein of defined secondary and quaternary structure. J. Biol. Chem. 259:13253-13261.
40. Martyna, G. L., M. E. Tuckerman, D. J. Tobias, and M. L. Klein. 1996. Explicit reversible integrators for extended systems dynamics. Mol. Physiol. 87:1117-1157.
41. McGregor, M. J., S. A. Islam, and M. J. Sternberg. 1987. Analysis of the relationship between side-chain conformation and secondary structure in globular proteins. J. Mol. Biol. 198:295-310.
42. A and glycine receptors. Nature. 389: 385-389.
43. Mok, Y-K., G. De Prat Gay, J. P. Butler, and M. Bycroft. 1996. Equilibrium dissociation and unfolding of the dimeric human papillomavirus strain-16 E2 DNA-binding domain. Protein Sci. 5:310-319.
44. Nozaki, Y., and C. Tanford. 1971. The solubility of amino acids and two glycine peptides in aqueous ethanol and dioxane solutions. J. Biol. Chem. 246:2211-2217.
45. O'Neil, K. T., and W. F. DeGrado. 1990a. A thermodynamic scale for the helix-forming tendencies of the commonly occurring amino acids. Science. 250:646-651.
46. O'Neil, K. T., and W. F. DeGrado. 1990b. How calmodulin binds its targets: sequence independent recognition of amphiphilic α-helices. Trends Biochem. Sci. 15:59-64.
47. Rabanal, F., W. F. DeGrado, and P. L. Dutton. 1996. Toward the synthesis of a photosynthetic reaction center maquette: a cofacial porphrin pair assembled between two subunits of a synthetic four-helix bundle multiheme protein. J. Am. Chem. Soc. 118:473-474.
48. Rees, D. C., H. Komiya, T. O. Yeates, J. P. Allen, and G. Feher. 1989. The bacterial photosynthetic reaction center as a model for membrane proteins. Annu. Rev. Biochem. 58:607-633.
49. Richards, F. M. 1974. The interpretation of protein structures: total volume, group volume distributions and packing density. J. Mol. Biol. 82:1-14.
50. Robertson, D. E., R. S. Farid, C. C. Moser, J. L. Urbauer, S. E. Mulholland, R. Pidikiti, J. D. Lear, A. J. Wand, W. F. DeGrado, and P. L. Dutton. 1994. Design and synthesis of multi-haem proteins. Nature. 368: 425-432.
51. Shibata, A., K. Morita, T. Yamashita, H. Kamaya, and I. Ueda. 1991. Anesthetic-protein interaction: effects of volatile anesthetics on the secondary structure of poly(L-lysine). J. Pharm. Sci. 80:1037-1041.
52. Skalicky, J. J., B. R. Gibney, F. Rabanal, R. J. Bieber Urbauer, P. L. Dutton, and A. J. Wand. 1999. Solution structure of a designed four-α-helix bundle maquette scaffold. J. Am. Chem. Soc. 121:4941-4951.
53. Takenoshita, M., and J. H. Steinbach. 1991. Halothane blocks low-voltage-activated calcium current in rat sensory neurons. J. Neurosci. 11: 1404-1412.
54. Tsao, D. H. H., J. R. Casa-Finet, A. H. Maki, and J. W. Chase. 1989. Triplet state properties of tryptophan residues in complexes of mutated Escherichia coli single-stranded DNA binding proteins with single-stranded polynucleotides. Biophys. J. 55:927-936.
55. Tu, K., M. Tarek, M. L. Klein, and D. Scharf. 1998. Effects of anesthetics on the structure of a phospholipid bilayer: MD investigation of halothane in the hydrated liquid crystal phase of dipalmitoylphosphatidylcholine. Biophys. J. 75:2123-2134.
56. Urry, D. W., D. C. Gowda, T. M. Parker, C. H. Luan, M. C. Reid, C. M. Harris, A. Pattanaik, and R. D. Harris. 1992. Hydrophobicity scale for proteins based on inverse temperature transitions. Biopolymers, 39: 1243-1250.
57. von Heijne, G. 1994. Membrane proteins: from sequence to structure. Annu. Rev. Biophys. Biomol. Struct. 23:167-192.
58. Weiner, S. J., P. A. Kollman, D. A. Case, U. C. Singh, C. Ghio, G. Alagona, S. Profeta, and P. Weiner. 1984. A new force field for molecular mechanics simulation of nucleic acids and proteins. J. Am. Chem. Soc. 106:765-775.
59. Weiner, S. J., P. A. Kollman, D. T. Nguyen, and D. A. Case. 1986. An all atom force field for simulations of proteins and nucleic acids. J. Comp. Chem. 7:230-235.
60. Wimbley, W. C., and S. H. White. 1996. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nature Struct. Biol. 3:842-848.
61. Yuan, T., A. M. Weljie, and H. J. Vogel. 1998. Tryptophan fluorescence quenching by methionine and selenomethionine residues of calmodulin: orientation of peptide and protein binding. Biochemistry. 37:3187-3195.
62. Zhou, N. E., C. M. Kay, and R. S. Hodges. 1992. Synthetic model proteins. Positional effects of interchain hydrophobic interactions on stability of two-stranded α-helical coiled-coils. J. Biol. Chem. 267:2664-2670.