Unusual fluorescence of W168 in Plasmodium falciparum triosephosphate isomerase, probed by single-tryptophan mutants

European Journal of Biochemistry

Volumn 270, Issue 4, 2003, Pages 745-756

  Pattanaik, Priyaranjan ^a   Ravindra, Gudihal ^b   Sengupta, Chandana ^b   Maithal, Kapil ^b   Balaram, Padmanabhan ^b   Balaram, Hemalatha ^a  

^a JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

^b INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

Fluorescence lifetime; Plasmodium falciparum; Red edge excitation shift; Single tryptophan mutant; Triosephosphate isomerase

Indexed keywords

2 PHOSPHOGLYCOLIC ACID; GLYCOLIC ACID DERIVATIVE; GUANIDINE; TRIOSEPHOSPHATE ISOMERASE; TRYPTOPHAN; UNCLASSIFIED DRUG; UREA;

ARTICLE; CHROMATOPHORE; CRYSTAL STRUCTURE; ELECTRICITY; ENZYME ACTIVITY; FLUORESCENCE; HYDROGEN BOND; MUTAGENESIS; MUTANT; PH; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE;

ANIMALS; CIRCULAR DICHROISM; FLUORESCENCE; GLYCOLATES; GUANIDINE; MASS SPECTROMETRY; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DENATURATION; SPECTROMETRY, FLUORESCENCE; TRIOSE-PHOSPHATE ISOMERASE; TRYPTOPHAN; UREA;

PLASMODIUM FALCIPARUM; PROTOZOA;

EID: 0037293775     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03436.x     Document Type: Article

References (55)

1. Velanker, S.S., Ray, S.S., Gokhale, R.S., Suma, S., Balaram, H., Balaram, P. & Murthy, M.R.N. (1997) Triosephosphate isomerase from Plasmodium falciparum: the crystal structure provides insights into antimalarial drug design. Structure 5, 751-761.
2. Wierenga, R.K. (2001) The TIM-barrel fold: a versatile framework for efficient enzymes. FEBS Lett. 492, 193-198.
3. Farber, G.K. & Petsko, G.A. (1990) The evolution of alpha/beta barrel enzymes. Trends Biochem. Sci. 6, 228-234.
4. Reardon, D. & Farber, G.K. (1996) The structure and evolution of alpha/beta barrel proteins. FASEB J. 10, 184.
5. Pujadas, G. & Palau, J. (1999) TIM barrel fold: structural, functional and evolutionary characteristics in natural and designed molecules. Biologia Bratislava 53, 231-254.
6. Gerstein, M. (1997) A structural census of genomes: comparing bacterial, eukaryotic, and archaeal genomes in terms of protein structure. J. Mol. Biol. 274, 562-576.
7. Hegyi, H. & Gerstein, M. (1999) The relationship between protein structure and function: a comprehensive survey with application to the yeast genome. J. Mol. Biol. 288, 147-164.
8. Mainfroid, V., Terpstra, P., Beauregard, M., Frere, J.M., Mande, S.C., Hol, W.G., Martial, J.A. & Goraj, K. (1996) Three human TIM mutants that provide new insights on why TIM is a dimer. J. Mol. Biol. 257, 441-456.
9. Kursula, I., Partanen, S., Lambeir, A.M., Antonov, D.M., Augustyns, K. & Wierenga, R.K. (2001) Structural determinants for ligand binding and catalysis of triosephosphate isomerase. Eur. J. Biochem. 268, 5189-5196.
10. Borchert, T.V., Abagyan, R., Jaenicke, R. & Wierenga, R.K. (1994) Design, creation, and characterization of a stable, monomeric triosephosphate isomerase. Proc. Natl. Acad. Sci. USA 91, 1515-1518.
11. Gokhale, R.S., Ray, S.S., Balaram, H. & Balaram, P. (1999) Unfolding of Plasmodium falciparum triosephosphate isomerase in urea and guanidinium chloride: evidence for a novel disulfide exchange reaction in a covalently cross-linked mutant. Biochemistry 38, 423-431.
12. Gopal, B., Ray, S.S., Gokhale, R.S., Balaram, H., Murthy, M.R.N. & Balaram, P. (1999) Cavity-creating mutation at the dimer interface of Plasmodium falciparum triosephosphate isomerase: restoration of stability by disulfide cross-linking of subunits. Biochemistry 38, 478-486.
13. Zabori, S., Rudolf, R. & Jaenicke, R. (1980) Folding and association of triose phosphate isomerase from rabbit muscle. Z. Naturforsch. 35, 999-1004.
14. Waley, S.G. (1973) Refolding of triose phosphate isomerase. Biochem. J. 135, 165-172.
15. Pompliano, D.L., Peyman, A. & Knowles, J.R. (1990) Stabilization of a reaction intermediate as a catalytic device: definition of the functional role of the flexible loop in triosephosphate isomerase. Biochemistry 29, 3186-3194.
16. Rozovsky, S., Jogl, G., Tong, L. & McDermott, A.E. (2001) Solution-state NMR investigations of triosephosphate isomerase active site loop motion: ligand release in relation to active site loop dynamics. J. Mol. Biol. 310, 271-280.
17. Rozovsky, S. & McDermott, A.E. (2001) The time scale of the catalytic loop motion in triosephosphate isomerase. J. Mol. Biol. 310, 259-270.
18. Demchenko, A.P., Gryczynski, I., Gryczynski, Z., Wiczk, W., Malak, H. & Fishman, M. (1993) Intramolecular dynamics in the environment of the single tryptophan residue in staphylococcal nuclease. Biophys. Chem. 48, 39-48.
19. Tcherkasskaya, O., Bychkova, V.E., Uversky, V.N. & Gronenborn, A.M. (2000) Multisite fluorescence in proteins with multiple tryptophan residues. Apomyoglobin natural variants and site-directed mutants. J. Biol. Chem. 275, 36285-36294.
20. Shen, W.H. (1993) Fluorescence lifetimes of the tryptophan residues in ornithine transcarbamoylase. Biochemistry 32, 13925-13932.
21. Nath, U. & Udgaonkar, J.B. (1997) Folding of tryptophan mutants of barstar: evidence for an initial hydrophobic collapse on the folding pathway. Biochemistry 36, 8602-8610.
22. Martensson, L., Jonasson, P., Freskgard, P., Svensson, M., Carlsson, V. & Jonsson, B. (1995) Contribution of individual tryptophan residues to the fluorescence spectrum of native and denatured forms of human carbonic anhydrase II. Biochemistry 34, 1101-1121.
23. Soulages, J.L. & Arrese, E.L. (2000) Fluorescence spectroscopy of single tryptophan mutants of apolipophorin-III in discoidal lipoproteins of dimyristoylphosphatidylcholine. Biochemistry 39, 10674-10580.
24. Engelborghs, Y. & Fersht, A. (2000) Barnase: fluorescence analysis of a three tryptophan protein. In Topics in Fluorescence Spectroscopy (Lakowicz, J. R., ed.), Vol. 6, pp. 83-102. Kluwer Academic, New York, USA.
25. Vivian, J.T. & Callis, P.R. (2001) Mechanisms of tryptophan fluorescence shifts in proteins. Biophys. J. 80, 2093-2109.
26. Callis, P.R. (1997) 1La and 1Lb transitions of tryptophan: applications of theory and experimental observations to fluorescence of proteins. Methods Enzymol. 278, 113-150.
27. Ranie, J., Kumar, V.P. & Balaram, H. (1993) Cloning of the triosephosphate isomerase gene of Plasmodium falciparum and expression in Escherichia coli. Mol. Biochem. Parasitol. 61, 159-170.
28. Sarkar, G. & Sommer, S.S. (1995) The megaprimer method of site directed mutagenesis. Biotechniques, 8, 404-407.
29. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
30. Plaut, B. & Knowles, J.R. (1972) pH-dependence of the triose phosphate isomerase reaction. Biochem. J. 129, 311-320.
31. Sampson, N.S. & Knowles, J.R. (1992) Segmental movement: definition of the structural requirements for loop closure in catalysis by triosephosphate isomerase. Biochemistry 31, 8482-8487.
32. Demchenko, A.P. (1988) Red-edge-excitation fluorescence spectroscopy of single-tryptophan proteins. Eur. Biophys. J. 16, 121-129.
33. Demchenko, A.P. & Ladokhin, A.S. (1988) Red-edge-excitation fluorescence spectroscopy of indole and tryptophan. Eur. Biophys. J. 15, 369-379.
34. Demchenko, A.P. (1986) Ultraviolet Spectroscopy of Proteins. Springer-Verlag, Berlin, Germany.
35. Mukherjee, S. & Chattopadhyay, A. (1995) Wavelength-selective fluorescence as a novel tool to study organization and dynamics in complex biological systems. J. Fluorescence 5, 237-246.
36. Chen, Y. & Barkley, M.D. (1998) Toward understanding tryptophan fluorescence in proteins. Biochemistry 37, 9976-9982.
37. Nanda, V. & Brand, L. (2000) Aromatic interactions in homeodomains contribute to the low quantum yield of a conserved, buried tryptophan. Proteins 40, 112-125.
38. Eftink, M.R. (1991) Fluorescence techniques for studying protein structure. Methods Biochem. Anal. 35, 127-205.
39. Gilardi, G., Mei, G., Rosato, N., Canters, G.W. & Finazzi-Agro, A. (1994) Unique environment of Trp48 in Pseudomonas aeruginosa azurin as probed by site-directed mutagenesis and dynamic fluorescence spectroscopy. Biochemistry 33, 1425-1432.
40. Hammann, C., Messerschmidt, A., Huber, R., Nar, H., Gilardi, G. & Canters, G.W. (1996) X-ray crystal structure of the two site-specific mutants Ile7Ser and Phe110Ser of azurin from Pseudomonas aeruginosa. J. Mol. Biol. 255, 362-366.
41. Axelsen, P.H. & Prendergast, F.G. (1989) Molecular dynamics of tryptophan in ribonuclease-T1. II. Correlations with fluorescence. Biophys. J. 56, 43-66.
42. Hubbard, S.J. & Thornton, J.M. (1993) 'Naccess', Computer Program. Department of Biochemistry and Molecular Biology, University College, London, UK.
43. Ray, S.S., Singh, S.K. & Balaram, P. (2001) An electrospray ionisation mass spectrometry investigation of 1-anilino-8-naphthalene-sulfonate (ANS) binding to proteins. J. Am. Soc. Mass. Spetrom. 4, 428-438.
44. Parthasarathy, S. (2001) Structural studies on Plasmodium Falciparum triosephosphate isomerase and analysis of atomic displacement parameters in high resolution protein structures. PhD Thesis, Indian Institute of Science, Bangalore, India.
45. Baldwin, E.P. & Matthews, B.W. (1994) Core-packing constraints, hydrophobicity and protein design. Curr. Opin. Biotechnol. 5, 396-402.
46. Varadarajan, R. & Richards, F.M. (1992) Crystallographic structures of ribonuclease S variants with nonpolar substitution at position 13: packing and cavities. Biochemistry 31, 12315-12327.
47. Jackson, S.E., Moracci, M., el Masry, N., Johnson, C.M. & Fersht, A.R. (1993) Effect of cavity-creating mutations in the hydrophobic core of chymotrypsin inhibitor 2. Biochemistry 32, 11259-11269.
48. Stites, W.E., Gittis, A.G., Lattman, E.E. & Shortle, D. (1991) In a staphylococcal nuclease mutant the side-chain of a lysine replacing valine 66 is fully buried in the hydrophobic core. J. Mol. Biol. 221, 7-14.
49. Hubbard, S.J. & Argos, P. (1995) Evidence on close packing and cavities in proteins. Curr. Opin. Biotechnol. 6, 375-381.
50. Chanez-Cardenas, M.E. Fernandez-Velasco, D.A., Vazquez-Contreras, A., Coria, R., Saab-Rincon, G. & Perez-Montfort, R. (2002) Unfolding of triosephosphate isomerase from Trypanosoma brucei: identification of intermediates and insight into the denaturation pathway using tryptophan mutants. Arch. Biochem. Biophys. 399, 117-129.
51. Demchenko, A.P. (1991) Fluorescence and dynamics in proteins. In Topics in Fluorescence Spectroscopy (Lakowicz, J.R., ed.), Vol. 3, pp. 65-112. Plenum press, New York, USA.
52. Lakowicz, J.R. (2000) On spectral relaxation in proteins. Photochem. Photobiol. 72, 421-437.
53. Eftink, M.R. (2000) Intrinsic fluorescence of proteins. In Topics in Fluorescence Spectroscopy (Lakowicz, J.R., ed.), Vol. 6, pp. 1-16. Kluwer Academic, New York, USA.
54. Kraulis, P.J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-953.
55. Guex, N. & Peitsch, M.C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modelling. Electrophoresis 18, 2714-2723.