Ionization, partitioning, and dynamics of tryptophan octyl ester: Implications for membrane-bound tryptophan residues

Biophysical Journal

Volumn 73, Issue 2, 1997, Pages 839-849

  Chattopadhyay, Amitabha ^a   Mukherjee, Sushmita ^a,b   Rukmini, R ^a   Rawat, Satinder S ^a   Sudha, S ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; TRYPTOPHAN DERIVATIVE;

ARTICLE; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; SPECTROFLUOROMETRY;

EID: 0030749502     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(97)78116-5     Document Type: Article

References (95)

1. Abrams, F. S., A. Chattopadhyay, and E. London. 1992. Determination of the location of fluorescent probes attached to fatty acids using parallax analysis of fluorescence quenching: effect of carboxyl ionization state and environment on depth. Biochemistry. 31:5322-5327.
2. Abrams, F. S., and E. London. 1992. Calibration of the parallax fluorescence quenching method for determination of membrane penetration depth: refinement and comparison of quenching by spin-labeled and brominated lipids. Biochemistry. 31:5312-5322.
3. Abrams, F. S., and E. London. 1993. Extension of the parallax analysis of membrane penetration depth to the polar region of model membranes: use of fluorescence quenching by a spin-label attached to the phospholipid polar headgroup. Biochemistry. 32:10826-10831.
4. Ashcroft, R. G., H. G. L. Coster, and J. R. Smith. 1981. The molecular organisation of bimolecular lipid membranes: the dielectric structure of the hydrophilic/hydrophobic interface. Biochim. Biophys. Acta. 643:191-204.
5. Batzri, S., and E. D. Korn. 1973. Single bilayer liposomes prepared without sonication. Biochim. Biophys. Acta. 298:1015-1019.
6. Becker, M. D., D. V. Greathouse, R. E. Koeppe, and O. S. Andersen. 1991. Amino acid sequence modulation of gramicidin channel function: effects of tryptophan-to-phenylalanine substitutions on the single-channel conductance and duration. Biochemistry. 30:8830-8839.
7. Beddard, G. S. 1983. The photophysics of tryptophan. In Time-Resolved Fluorescence Spectroscopy in Biochemistry and Biology. R. B. Cundall and R. E. Dale, editors. Plenum Press, New York. 629-633.
8. Beechem, J. M. 1989. A second generation global analysis program for the recovery of complex inhomogeneous fluorescence decay kinetics. Chem. Phys. Lipids. 50:237-251.
9. Beechem, J. M. 1992. Global analysis of biochemical and biophysical data. Methods Enzymol. 210:37-54.
10. Beechem, J. M., and L. Brand. 1985. Time-resolved fluorescence of proteins. Annu. Rev. Biochem. 54:43-71.
11. Beechem, J. M., E. Gratton, M. Ameloot, J. R. Knutson, and L. Brand. 1991. The global analysis of fluorescence intensity and anisotropy decay data: second-generation theory and programs. In Topics in Fluorescence Spectroscopy, Vol. 2, Principles. J. R. Lakowicz, editor. Plenum Press, New York. 241-305.
12. Befort, K., L. Tabbara, D. Kling, B. Maigret, and B. L. Kieffer. 1996. Role of aromatic transmembrane residues of the δ-opioid receptor in ligand recognition. J. Biol. Chem. 271:10161-10168.
13. Bevington, P. R. 1969. Data Reduction and Error Analysis for the Physical Sciences. McGraw-Hill, New York.
14. Burley, S. K., and G. A. Petsko. 1985. Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science. 229:23-28.
15. Burley, S. K., and G. A. Petsko. 1988. Weakly polar interactions in proteins. Adv. Protein Chem. 39:125-189.
16. Chattopadhyay, A. 1991. Application of the red edge excitation shift in membranes. Biophys. J. 59:191a.
17. Chattopadhyay, A., and E. London. 1987. Parallax method for direct measurement of membrane penetration depth utilizing fluorescence quenching by spin-labeled phospholipids. Biochemistry. 26:39-45.
18. Chattopadhyay, A., and E. London. 1988. Spectroscopic and ionization properties of N-(7-nitrobenz-2-oxa-1,3-diazol-4-yl)-labeled lipids in model membranes. Biochim. Biophys. Acta. 938:24-34.
19. Chattopadhyay, A., and M. G. McNamee. 1991. Average membrane penetration depth of tryptophan residues of the nicotinic acetylcholine receptor by the parallax method. Biochemistry. 30:7159-7164.
20. Chattopadhyay, A., and S. Mukherjee. 1993. Fluorophore environments in membrane-bound probes: a red edge excitation shift study. Biochemistry. 32:3804-3811.
21. Chattopadhyay, A., and R. Rukmini. 1993. Restricted mobility of the sole tryptophan in membrane-bound melittin. FEBS Lett. 335:341-344.
22. Chattopadhyay, A., R. Rukmini, and S. Mukherjee. 1996. Photophysics of a neurotransmitter: ionization and spectroscopic properties of serotonin. Biophys. J. 71:1952-1960.
23. Chen, R. F., and R. L. Bowman. 1965. Fluorescence polarization: measurement with ultraviolet-polarizing filters in a spectrophotofluorometer. Science. 147:729-732.
24. Cowgill, R. W. 1963. Fluorescence and the structure of proteins. 1. Effects of substituents on the fluorescence of indole and phenol compounds. Arch. Biochem. Biophys. 100:36-44.
25. Dahms, T. E. S., K. J. Willis, and A. G. Szabo. 1995. Conformational heterogeneity of tryptophan in a protein crystal. J. Am. Chem. Soc. 117:2321-2326.
26. De Lauder, W. B., and Ph. Wahl. 1970. pH dependence of the fluorescence decay of tryptuphan. Biochemistry. 9:2750-2754.
27. Deisenhofer, J., and H. Michel. 1989a. The photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis. EMBO J. 8:2149-2170.
28. Deisenhofer, J., and H. Michel. 1989b. The photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis. Science. 245: 1463-1473.
29. Demchenko, A. P. 1988. Site-selective excitation: a new dimension in protein and membrane spectroscopy. Trends Biochem. Sci. 13:374-377.
30. Dittmer, J. C., and R. L. Lester. 1964. A simple, specific spray for the detection of phospholipids on thin-layer chromatograms. J. Lipid Res. 5:126-127.
31. Eftink, M. R. 1991. Fluorescence techniques for studying protein structure. In Methods of Biochemical Analysis, Vol. 35. C. H. Suelter, editor. John Wiley, New York. 127-205.
32. Eftink, M. R., Y. Jia, D. Hu, and C. A. Ghiron. 1995. Fluorescence studies with tryptophan analogues: excited state interactions involving the side chain amino group. J. Phys. Chem. 99:5713-5723.
33. Fauchere, J. L. 1985. How hydrophobic is tryptophan? Trends Biochem. Sci. 10:268.
34. Fauchere, J. L., and V. Pliska. 1983. Hydrophobic parameters π of amino-acid side chains from the partitioning of N-acetyl-amino-acid amides. Eur. J. Med. Chem. 18:369-375.
35. Ferrer-Montiel, A. V., W. Sun, and M. Montal. 1996. A single tryptophan on M2 of glutamate receptor channels confers high permeability to divalent cations. Biophys. J. 71:749-758.
36. Fonseca, V., P. Daumas, L. Ranjalahy-Rasoloarijao, F. Heitz, R. Lazaro, Y. Trudelle, and O. S. Andersen. 1992. Gramicidin channels that have no tryptophan residues. Biochemistry. 31:5340-5350.
37. Galley, W. C., and R. M. Purkey. 1970. Role of heterogeneity of the solvation site in electronic spectra in solution. Proc. Natl. Acad. Sci. USA. 67:1116-1121.
38. Gawrisch, K., J. A. Barry, L. L. Holte, T. Sinnwell, L. D. Bergelson, and J. A. Ferretti. 1995. Role of interactions at the lipid-water interface for domain formation. Mol. Membr. Biol. 12:83-88.
39. Grinvald, A., and I. Z. Steinberg. 1974. On the analysis of fluorescence decay kinetics by the method of least-squares. Anal. Biochem. 59: 583-598.
40. Guha, S., S. S. Rawat, A. Chattopadhyay, and B. Bhattacharyya. 1996. Tubulin conformation and dynamics: a red edge excitation shift study. Biochemistry. 35:13426-13433.
41. Ho, C., and C. D. Stubbs. 1992. Hydration at the membrane-lipid interface. Biophys. J. 63:897-902.
42. Hu, W., and T. A. Cross. 1995. Tryptophan hydrogen bonding and electric dipole moments: functional roles in the gramicidin channel and implications for membrane proteins. Biochemistry: 34:14147-14155.
43. Huang, Z., and R. P. Haugland. 1991. Partition coefficients of fluorescent probes with phospholipid membranes. Biochem. Biophys. Res. Commun. 181:166-171.
44. Ippolito, J. A., R. S. Alexander, and D. W. Christianson. 1990. Hydrogen bond stereochemistry in protein structure and function. J. Mol. Biol. 215:457-471.
45. Jacobs, R. E., and S. H. White. 1989. The nature of the hydrophobic binding of small peptides at the bilayer interface: implications for the insertion of transbilayer helices. Biochemistry: 28:3421-3437.
46. Jain, M. K., J. Rogers, L. Simpson, and L. M. Gierasch. 1985. Effect of tryptophan derivatives on the phase properties of bilayers. Biochim. Biophys. Acta. 816:153-162.
47. Jameson, D. M., and G. Weber. 1981. Resolution of the pH-dependent heterogenous fluorescence decay of tryptophan by phase and modulation measurements. J. Phys. Chem. 85:953-958.
48. Kachel, K., E. Asuncion-Punzalan, and E. London. 1995. Anchoring of tryptophan and tyrosine analogs at the hydrocarbon-polar boundary in model membrane vesicles: parallax analysis of fluorescence quenching induced by nitroxide-labeled phospholipids. Biochemistry. 34: 15475-15479.
49. Kantor, H. L., and J. H. Prestegard. 1978. Fusion of phosphatidylcholine bilayer vesicles: role of free fatty acid. Biochemistry. 17:3592-3597.
50. Killian, J. A., I. Salemink, M. R. R. de Planque, G. Lindblom, R. E. Koeppe, and D. V. Greathouse. 1996. Induction of non bilayer structures in diacylphosphotidylcholine model membranes by transmembrane α-helical peptides: importance of hydrophobic mismatch and proposed role of tryptophans. Biochemistry. 35:1037-1045.
51. Kirby, E. P., and R. F. Steiner. 1970. The influence of solvent and temperature upon the fluorescence of indole derivatives. J. Phys. Chem. 74:4480-4490.
52. Knutson, J. R., J. M. Beechem, and L. Brand. 1983. Simultaneous analysis of multiple fluorescence decay curves: a global approach. Chem. Phys. Lett. 102:501-507.
53. Kremer, J. M. H., M. W. J. Esker, C. Pathmamanoharan, and P. H. Wiersema. 1977. Vesicles of variable diameter prepared by a modified injection method. Biochemistry. 16:3932-3935.
54. Ladokhin, A. S., and P. W. Holloway. 1995. Fluorescence of membrane-bound tryptophan octyl ester: a model for studying intrinsic fluorescence of protein-membrane interactions. Biophys. J. 69:506-517.
55. Ladokhin, A. S., P. W. Holloway, and E. G. Kostrzhevska. 1993. Distribution analysis of membrane penetration of proteins by depth-dependent fluorescence quenching. J. Fluorescence. 3:195-197.
56. Lakowicz, J. R. 1983. Principles of Fluorescence Spectroscopy. Plenum Press, New York.
57. Lampert, R. A., L. A. Chewter, D. Phillips, D. V. O'Connor, A. J. Roberts, and S. R. Meech. 1983. Standards for nanosecond fluorescence decay time measurements. Anal. Chem. 55:68-73.
58. Landolt-Marticorena, C., K. A. Williams, C. M. Deber, and R. A. F. Reithmeier. 1993. Non-random distribution of amino acids in the transmembrane segments of human type I single span membrane proteins. J. Mol. Biol. 229:602-608.
59. Lewis, R. N. A. H., W. Pohle, and R. N. McElhaney. 1996. The interfacial structure of phospholipid bilayers: differential scanning calorimetry and Fourier transform infrared spectroscopic studies of 1,2-dipalmitoyl-sn-glycero-3-phosphorylcholine and its dialkyl and acyl-alkyl analogs. Biophys. J. 70:2736-2746.
60. London, E. 1986. A fluorescence-based detergent binding asssay for protein hydrophobicity. Anal. Biochem. 154:57-63.
61. London, E., and G. W. Feigenson. 1981. Fluorescence quenching in model membranes. 1. Characterization of quenching caused by a spin-labeled phospholipid. Biochemistry. 20:1932-1938.
62. McClare, C. W. F. 1971. An accurate and convenient organic phosphorus assay. Anal. Biochem. 39:527-530.
63. Meers, P. 1990. Location of tryptophans in membrane-bound annexins. Biochemistry. 29:3325-3330.
64. Michel, H., and J. Deisenhofer. 1990. The photosynthetic reaction center from the purple bacterium Rhodopseudomonas viridis: aspects of membrane protein structure. Curr. Top. Membr. Transp. 36:53-69.
65. Mukherjee, S., and A. Chattopadhyay. 1994. Motionally restricted tryptophan environments at the peptide-lipid interface of gramicidin channels. Biochemistry. 33:5089-5097.
66. Mukherjee, S., and A. Chattopadhyay. 1995. Wavelength-selective fluorescence as a novel tool to study organization and dynamics in complex biological systems. J. Fluorescence. 5:237-246.
67. Nemkovich, N. A., A. N. Rubinov, and V. I. Tomin. 1991. Inhomogeneous broadening of electronic spectra of dye molecules in solutions. In Topics in Fluorescence Spectroscopy, Vol. 2. J. R. Lakowicz, editor. Plenum Press, New York. 367-428.
68. O'Connor, D. V., and D. Phillips. 1984. Time-Correlated Single Photon Counting. Academic Press, London. 180-189.
69. Perochon, E., A. Lopez, and J. F. Tocanne. 1992. Polarity of lipid bilayers: a fluorescence investigation. Biochemistry. 31:7672-7682.
70. Ptak, M., M. Egret-Charlier, A. Sanson, and O. Bouloussa. 1980. A NMR study of the ionization of fatty acids, fatty amines and N-acylamino acids incorporated in phosphatidylcholine vesicles. Biochim. Biophys. Acta. 600:387-397.
71. Radzicka, A., and R. Wolfenden. 1988. Comparing the polarities of the amino acids: side-chain distribution coefficients between the vapor phase, cyclohexane, 1-octanol, and neutral aqueous solution. Biochemistry. 27:1664-1670.
72. Rawat, S. S., S. Mukherjee, and A. Chattopadhyay. 1997. Micellar organization and dynamics: a wavelength-selective fluorescence approach. J. Phys. Chem. B. 101:1922-1929.
73. Reithmeier, R. A. F. 1995. Characterization and modeling of membrane proteins using sequence analysis. Curr. Opin. Struct. Biol. 5:491-500.
74. Ricci, R. W. 1970. Deuterium-isotope effect on the fluorescence yields and lifetimes of indole derivatives - including tryptophan and tryptamine. Photochem. Photobiol. 12:67-75.
75. Robbins, R. J., G. R. Fleming, G. S. Beddard, G. W. Robinson, P. J. Thistlethwaite, and G. J. Woolfe. 1980. Photophysics of aqueous tryptophan: pH and temperature effects. J. Am. Chem. Soc. 102:6271-6279.
76. Schiffer, M., C.-H. Chang, and F. J. Stevens. 1992. The functions of tryptophan residues in membrane proteins. Protein Eng. 5:213-214.
77. Slater, S. J., C. Ho, F. J. Taddeo, M. B. Kelly, and C. D. Stubbs. 1993. Contribution of hydrogen bonding to lipid-lipid interactions in membranes and the role of lipid order: effects of cholesterol, increased phospholipid unsaturation, and ethanol. Biochemistry. 32:3714-3721.
78. Stewart, J. M., and J. D. Young. 1984. Laboratory techniques in SPPS. In Solid Phase Peptide Synthesis. Pierce Chemical Co., Rockford, IL. 122.
79. Stubbs, C. D., S. R. Meech, A. G. Lee, and D. Phillips. 1985. Solvent relaxation in lipid bilayers with dansyl probes. Biochim. Biophys. Acta. 815:351-360.
80. Swaminathan, R., G. Krishnamoorthy, and N. Periasamy. 1994. Similarity of fluorescence lifetime distributions for single tryptophan proteins in the random coil state. Biophys. J. 67:2013-2023.
81. Szabo, A. G., and D. M. Rayner. 1980. Fluorescence decay of tryptophan conformers in aqueous solution. J. Am. Chem. Soc. 102:554-563.
82. Venable, R. M., Y. Zhang, B. J. Hardy, and R. W. Pastor. 1993. Molecular dynamics simulations of a lipid bilayer and of hexadecane: an investigation of membrane fluidity. Science. 262:223-226.
83. Vogel, H., L. Nilsson, R. Rigler, K.-P. Voges, and G. Jung. 1988. Structural fluctuations of a helical polypeptide traversing a lipid bilayer. Proc. Natl. Acad. Sci. USA. 85:5067-5071.
84. Weber, G. 1960. Fluorescence-polarization spectrum and electronic energy transfer in tyrosine, tryptophan and related compounds. Biochem. J. 75:335-345.
85. Weiss, M. S., U. Abele, J. Weckesser, W. Welte, E. Schiltz, and G. E. Schultz. 1991. Molecular architecture and electrostatic properties of a bacterial porin. Science. 254:1627-1630.
86. Welti, R., L. J. Mullikin, T. Yoshimura, and G. M. Helmkamp. 1984. Partition of amphiphilic molecules into phospholipid vesicles and human erythrocyte ghosts: measurements by ultraviolet difference spectroscopy. Biochemistry. 23:6086-6091.
87. Wess, J., S. Nanavati, Z. Vogel, and R. Maggio. 1993. Functional role of proline and tryptophan residues highly conserved among G protein-coupled receptors studied by mutational analysis of the m3 muscarinic receptor. EMBO J. 12:331-338.
88. White, A. 1959. Effect of pH on fluorescence of tyrosine, tryptophan and related compounds. Biochem. J. 71:217-220.
89. White, S. H., and W. C. Wimley. 1994. Peptides in lipid bilayers: structural and thermodynamic basis for partitioning and folding. Curr. Opin. Struct. Biol. 4:79-86.
90. Wimley, W. C., and S. H. White. 1992. Partitioning of tryptophan sidechain analogs between water and cyclohexane. Biochemistry. 31: 12813-12818.
91. Wimley, W. C., and S. H. White. 1993. Membrane partitioning: distinguishing bilayer effects from the hydrophobic effect. Biochemistry. 32:6307-6312.
92. Wimley, W. C., and S. H. White. 1996. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nature Struct. Biol. 3:842-848.
93. Wolfenden, R. V., P. M. Cullis, and C. C. F. Southgate. 1979. Water, protein folding, and the genetic code. Science. 206:575-577.
94. Woolf, T. B., and B. Roux. 1994. Molecular dynamics simulation of the gramicidin channel in a phospholipid bilayer. Proc. Natl. Acad. Sci. USA. 91:11631-11635.
95. Yu, H.-T., M. A. Vela, F. R. Fronczek, M. L. McLaughlin, and M. D. Barkley. 1995. Microenvironmental effects on the solvent quenching rate in constrained tryptophan derivatives. J. Am. Chem. Soc. 117: 348-357.