Aromatic interactions in homeodomains contribute to the low quantum yield of a conserved, buried tryptophan

Proteins: Structure, Function and Genetics

Volumn 40, Issue 1, 2000, Pages 112-125

  Nanda, Vikas ^a   Brand, Ludwig ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Fibronectin type III; Fluorescence; NH ... hydrogen bond; Protein unfolding; Quenching

Indexed keywords

AROMATIC AMINO ACID; BENZENE; FIBRONECTIN; HOMEODOMAIN PROTEIN; INDOLE; TRYPTOPHAN;

ARTICLE; CONTROLLED STUDY; DROSOPHILA; FLUORESCENCE; HYDROGEN BOND; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE; QUANTUM CHEMISTRY;

ANIMALS; ANTENNAPEDIA HOMEODOMAIN PROTEIN; BENZENE; DATABASES, FACTUAL; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; ELECTROSTATICS; FIBRONECTINS; HOMEODOMAIN PROTEINS; HUMANS; HYDROGEN BONDING; INDOLES; NUCLEAR PROTEINS; PROTEIN DENATURATION; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, FLUORESCENCE; TRANSCRIPTION FACTORS; TRYPTOPHAN;

EID: 0034237284     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0134(20000701)40:1<112::AID-PROT130>3.0.CO;2-C     Document Type: Article

References (57)

1. Qian Y, Billeter M, Otting G, Müller M, Gehring W, Wüthrich K. The structure of the Antennapedia homeodomain determined by NMR spectroscopy in solution: Comparison with prokaryotic repressors. Cell 1989;59:573-580.
2. Passner JM, Ryoo HD, Shen L, Mann RS, Aggarwal AK. Structure of a DNA-bound Ultrabithorax-Extradenticle homeodomain complex. Nature 1999;397:714-719.
3. Clarke ND, Kissinger CR, Desjarlais J, Gilliland GL, Pabo CO. Structural studies of the engrailed homeodomain. Protein Sci 1994;3:1779-1787.
4. Li T, Stark MR, Johnson AD, Wolberger C. Crystal structure of the MATa1/MATa2 homeodomain heterodimer bound to DNA. Science 1995;270:262-269.
5. Li H, Tejero R, Monleon D, et al. Homology modeling using simulated annealing of restrained molecular dynamics and conformational search calculations with CONGEN: application in predicting the three-dimensional structure of murine homeodomain MSX-1. Protein Sci 1997;6:956-970.
6. Laughon A. DNA binding specificity of homeodomains. Biochemistry 1991;30:11358-11367.
7. Gehring WJ, Affolter M, Bürglin T. Homeodomain proteins. Annu Rev Biochem 1994;63:487-526.
8. Subramaniam V, Rivera-Pomar R, Jovin TM. Su-Pos447: the conserved tryptophan in the recognition helix of the bicoid homeodomain is a sensitive probe of structure and folding. Biophys J 1999;76:A108.
9. Shang Z, Issac VE, Li H, et al. Design of a "minimAL" homeodomain: the N-terminal arm modulates DNA binding affinity and stabilizes homeodomain structure. Proc Natl Acad Sci 1994;94: 8373-8377.
10. Sanchez M, Jennings PA, Murre C. Conformational changes induced in Hoxb-8/Pbx-1 heterodimers in solution and upon interaction with specific DNA. Mol Cell Bio 1997;17:5369-5376.
11. Bürglin TR. Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Irogquois, TGIF) reveals a novel domain conserved between plants and animals. Nucl Acids Res 1997;25:4173-4180.
12. Chen Y, Liu B, Yu H-T, Barkley MD. The peptide bond quenches indole fluorescence. J Am Chem Soc 1996;118:9271-9278.
13. Chen Y, Barkley MD. Towards understanding tryptophan fluorescence in proteins. Biochemistry 1998;37:9976-9982.
14. Harris DL, Hudson BS. Photophysics of tryptophan in bacteriophage T4 lysozyme. Biochemistry 1990;29:5276-5285.
15. Cowgill RW. Fluorescence and the structure of proteins. XVIII. Spatial requirements for quenching by disulfide groups. Biochim Biophys Acta 1970;207:556-559.
16. Ekker SC, von Kessler DP, Beachy PA. Differential DNA sequence recognition is a determinant of specificity in homeotic gene action. EMBO J 1992;11:4059-4072.
17. Toptygin D, Rodgers ME, Brand L. Tu-Pos490: Non-exponential fluorescence decay of photobleached indole and tryptophan. Biophys J 1999;76:A361.
18. Grinvald A, Steinberg IZ. On the analysis of fluorescence decay kinetics by the method of least-squares. Anal Biochem 1974;59: 583-598.
19. Donzel B, Gauduchon P, Wahl P. Study of the conformation in the excited-state of two tryptophanyl diketopiperazines. J Am Chem Soc 1974;96:801-808.
20. Knutson JR, Walbridge DG, Brand L. Decay-associated fluorescence spectra and the heterogeneous emission of alcohol dehydrogenase. Biochemistry 1982;21:4671-4679.
21. Ross JBA, Schmidt CJ, Brand L. Time-resolved fluorescence of the two tryptophans in horse liver alcohol dehydrogenase. Biochemistry 1981;20:4369-4377.
22. Lakowicz JR. Principles of fluorescence spectroscopy. New York: Plenum Press; 1983.
23. Levitt M, Perutz MF. Aromatic rings act as hydrogen bond acceptors. J Mol Biol 1988;201:751-754.
24. Muiño PL, Harris D, Berryhill J, Hudson B, Callis PR. Simulation of solvent dynamics effects on the fluorescence of 3-methylindole in water. SPIE - Time-resolved laser spectroscopy in biochemistry III 1992;1640:240-251.
25. Bolis G, Clementi E. Analytical potentials from "ab initio" computations for the interaction between biomolecules. 3. Reliability and transferability of the pair potentials. J Am Chem Soc 1977;99: 5550-5557.
26. Bernstein FC, Koetzle TF, Williams GJB, et al. The protein data bank: a computer-based archival file for macromolecular structure. J Mol Biol 1977;112:535-542.
27. Strickler SJ, Berg RA. Relationship between absorption intensity and fluorescence lifetime of molecules. J Chem Phys 1962;37:814-822.
28. Van Duuren BL. Solvent effects in the fluorescence of indole and substituted indoles. J Org Chem 1961;26:2954-2960.
29. Suwaiyan A, Klein KA. Picosecond study of solute-solvent interaction of the excited-state of indole. Chem Phys Lett 1989;159:244-250.
30. Hager J, Ivanco M, Smith MA, Wallace SC. Two-color threshold photoionization spectroscopy of jet-cooled indole clusters. Chem Phys 1986;105:397-416.
31. Braun JE, Grebner ThL, Neusser HJ. van der Waals versus hydrogen-bonding in complexes of indole with argon, water and benzene by mass-analyzed pulsed field threshold ionization. J Phys Chem 1998;102:3273-3278.
32. Isaacs ED, Shukla A, Platzman PM, Hamann DR, Barbiellini B, TuIk CA. Covalency of the hydrogen bond in ice: a direct x-ray measurement. Phys Rev Lett 1999;82:600-603.
33. 3hJNC. connectivities across hydrogen bonds in a 30 kDa protein. J Biomol NMR 1999:14:181-184.
34. Hunter CA, Singh J, Thornton JM. π-π interactions: the geometry and energetics of phenylalanine-phenylalanine interactions in proteins. J Mol Biol 1991;218:837-846.
35. Pimentel GC. Hydrogen bonding and electronic transitions: the role of the Franck-Condon principle. J Am Chem Soc 1957;79:3323-3326.
36. Insight95.0. San Diego: MSI/Biosym; 1995.
37. Gallay J, Vekshin N, Sopkova J, Vincent M. Evidences for picosecond excited state reactions of indole derivatives in alcoholic solvents, reverse micelles and proteins. SPIE - time-resolved laser spectroscopy in biochemistry III 1994;2137:390-399.
38. Silva ND, Prendergast FG. Tryptophan dynamics of the FK506 binding protein: time-resolved fluorescence and simulations. Biophys J 1996;70:1122-1137.
39. Chen RF. Fluorescence quantum yields of tryptophan and tyrosine. Anal Lett 1967;1:35-42.
40. Egan DA, Logan TM, Liang H, Mtayoshi E, Fesik SW, Holzman TF. Equilibrium denaturation of recombinant Human FK Binding Protein in Urea. Biochemistry 1993;32:1920-1927.
41. Craescu CT, Rouvière N, Popescu A, Cerpolini E, Lebeau M-C, Baulieu E-E, Mispelter J. Three-dimensional structure of the immunophilin-like domain of FKBP59 in solution. Biochemistry 1996;34:11045-11052.
42. Rouvière N, Vincent M, Craescu CT, Gallay J. Immunosupressor binding to the immunophilin FKBP59 affects the local structure dynamics of a surface β-strand: time-resolved fluorescence study. Biochemistry 1997;36:7339-7352.
43. McCammon JA, Wolynes PG, Karplus M. Picosecond dynamics of tyrosine side chains in proteins. Biochemistry 1979;18:927-942.
44. Pierce DW, Boxer SG. Stark effect spectroscopy of tryptophan. Biophys J 1995;68:1583-1591.
45. Dryden D, Weir MP. Evidence for an acid-induced molten-globule state in interleukin-2; a fluorescence and circular dichroism study. Biochim Biophys Acta 1991;1078:94-100.
46. Weir MP, Chaplin MA, Wallace DM, Dykes CW, Hobden AN. Structure-activity relationships of recombinant human interleukin 2. Biochemistry 1988;27:6883-6892.
47. Litvinovich SV, Novokhatny W, Brew SA, Ingham KC. Reversible unfolding of an isolated heparin and DNA binding fragment, the first type III module from fibronectin. Biochim Biophys Acta 1992;1119:57-62.
48. Knee JL, Khundkar LR, Zewail AH. Picosecond photofragment spectroscopy. III. Vibrational predissociation of van der Waal's clusters. J Chem Phys 1987;87:115-127.
49. Mitchell JBO, Nandi CL, McDonald IK, Thornton JM, Price SL. Amino/aromatic interactions in proteins: is the evidence stacked against hydrogen bonding? J Mol Biol 1994;239:315-331.
50. Armstrong KM, Fairman R, Baldwin RL. The (i, i + 4) Phe-His interaction studied in a alanine-based α-helix. J Mol Biol 1993;230: 284-291.
51. Perutz MF. The role of aromatic rings as hydrogen-bond acceptors in molecular recognition. Phi Trans R Soc A 1993;345:105-112.
52. Burley SK, Petsko GA. Amino-aromatic interactions in proteins. FEBS Lett 1986;203:139-143.
53. Parkinson G, Gunasekera A, Vojtechovsky J, Zhang X, Kunkel TA, Berman H, Ebright RH. Aromatic hydrogen bond in sequence specific DNA recognition. Nat Struct Biol 1996;3:837-841.
54. Pace NC. Conformational stability of globular proteins. Trends Biochem Sci 1990;15:14-17.
55. Burley SK, Petsko GA. Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science 1985;229:23-28.
56. Bazan JF. Structural design and molecular evolution of a cytokine receptor subfamily. Proc Natl Acad Sci 1990;87:6934-6938.
57. Nanda V, Brand L. WPos277 Fluorescence characterization of homeodomains: Quenching of a buried tryptophan by aromatic hydrogen bonding associations. Biophys J 1999;76:A448.