Dynamic insight into protein structure utilizing red edge excitation shift

Accounts of Chemical Research

Volumn 47, Issue 1, 2014, Pages 12-19

  Chattopadhyay, Amitabha ^a   Haldar, Sourav ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; TRYPTOPHAN;

ARTICLE; CHEMISTRY; COLOR; METHODOLOGY; PROTEIN CONFORMATION; PROTEIN DENATURATION; SPECTROFLUOROMETRY;

COLOR; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEINS; SPECTROMETRY, FLUORESCENCE; TRYPTOPHAN;

EID: 84892745151     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar400006z     Document Type: Article

References (69)

1. Henzler-Wildman, K.; Kern, D. Dynamic personalities of proteins Nature 2007, 450, 964-972
2. Colombo, M. F.; Rau, D. C.; Parsegian, V. A. Protein solvation in allosteric regulation: a water effect on hemoglobin Science 1992, 256, 655-659
3. Xu, F.; Cross, T. A. Water: foldase activity in catalyzing polypeptide conformational rearrangements Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 9057-9061
4. Fenimore, P. W.; Frauenfelder, H.; McMohan, B. H.; Parak, F. G. Slaving: solvent fluctuations dominate protein dynamics and function Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 16047-16051
5. Mattos, C. Protein-water interactions in a dynamic world Trends Biochem. Sci. 2002, 27, 203-208
6. Timasheff, S. N. Protein hydration, thermodynamic binding and preferential hydration Biochemistry 2002, 41, 13473-13482
7. Chaplin, M. Do we underestimate the importance of water in cell biology? Nat. Rev. Mol. Cell Biol. 2006, 7, 861-866
8. Bizzarri, A. R.; Cannistraro, S. Molecular dynamics of water at the protein-solvent interface J. Phys. Chem. B 2002, 106, 6617-6633
9. Bhattacharyya, K.; Bagchi, B. Slow dynamics of constrained water in complex geometries J. Phys. Chem. A 2000, 104, 10603-10613
10. Jha, A.; Ishii, K.; Udgaonkar, J. B.; Tahara, T.; Krishnamoorthy, G. Exploration of the correlation between solvation dynamics and internal dynamics of a protein Biochemistry 2011, 50, 397-408
11. Mukherjee, S.; Chattopadhyay, A. Wavelength-selective fluorescence as a novel tool to study organization and dynamics in complex biological systems J. Fluoresc. 1995, 5, 237-246
12. Demchenko, A. P. The red-edge effects: 30 years of exploration Luminescence 2002, 17, 19-42
13. Demchenko, A. P. Site-selective red-edge effects Methods Enzymol. 2008, 450, 59-78
14. Raghuraman, H.; Kelkar, D. A.; Chattopadhyay, A. Novel insights into protein structure and dynamics utilizing the red edge excitation shift. In Reviews in Fluorescence 2005; Geddes, C. D.; Lakowicz, J. R., Eds.; Springer: NewYork, 2005; pp 199-222.
15. Haldar, S.; Chaudhuri, A.; Chattopadhyay, A. Organization and dynamics of membrane probes and proteins utilizing the red edge excitation shift J. Phys. Chem. B 2011, 115, 5693-5706
16. Haldar, S.; Chattopadhyay, A. Dipolar relaxation within the protein matrix of the green fluorescent protein: a red edge excitation shift study J. Phys. Chem. B 2007, 111, 14436-14439
17. Eftink, M. R. Fluorescence Techniques for Studying Protein Structure. In Methods of Biochemical Analysis; Suelter, C. H., Ed.; John Wiley: New York, 1991; Vol. 35, pp 127-205.
18. Lakowicz, J. R. Principles of fluorescence spectroscopy, 3 rd ed.; Springer: New York, 2006.
19. Ruan, K.; Li, J.; Liang, R.; Xu, C.; Yu, Y.; Lange, R.; Balny, C. A rare protein fluorescence behavior where the emission is dominated by tyrosine: case of the 33-kDa protein from spinach photosystem II Biochem. Biophys. Res. Commun. 2002, 293, 593-597
20. Ross, J. B. A.; Laws, W. R.; Rousslang, K. W.; Wyssbrod, H. R. Tyrosine fluorescence and phosphorescence from proteins and polypeptides. In Topics in Fluorescence Spectroscopy; Lakowicz, J. R., Ed.; Plenum Press: New York, 1992; Vol. 3, pp 1-63.
21. Ruggiero, A. J.; Todd, D. C.; Fleming, G. R. Subpicosecond fluorescence anisotropy studies of tryptophan in water J. Am. Chem. Soc. 1990, 112, 1003-1014
22. Vivian, J. T.; Callis, P. R. Mechanisms of tryptophan fluorescence shifts in proteins Biophys. J. 2001, 80, 2093-2109
23. Broos, J.; Tveen-Jensen, K.; de Waal, E.; Hesp, B. H.; Jackson, J. B.; Canters, G. W.; Callis, P. R. The emitting state of tryptophan in proteins with highly blue-shifted fluorescence Angew. Chem., Int. Ed. 2007, 119, 5229-5231
24. Guha, S.; Rawat, S. S.; Chattopadhyay, A.; Bhattacharyya, B. Tubulin conformation and dynamics: a red edge excitation shift study Biochemistry 1996, 35, 13426-13433
25. Raja, S. M.; Rawat, S. S.; Chattopadhyay, A.; Lala, A. K. Localization and environment of tryptophans in soluble and membrane-bound states of a pore-forming toxin from Staphylococcus aureus Biophys. J. 1999, 76, 1469-1479
26. Chattopadhyay, A.; Rawat, S. S.; Kelkar, D. A.; Ray, S.; Chakrabarti, A. Organization and dynamics of tryptophan residues in erythroid spectrin: novel structural features of denatured spectrin revealed by the wavelength-selective fluorescence approach Protein Sci. 2003, 11, 2389-2403
27. Chakrabarti, A.; Kelkar, D. A.; Chattopadhyay, A. Spectrin organization and dynamics: new insights Biosci. Rep. 2006, 26, 369-386
28. Klein-Seetharaman, J.; Oikawa, M.; Grimshaw, S. B.; Wirmer, J.; Duchardt, E.; Ueda, T.; Imoto, T.; Smith, L. J.; Dobson, C. M.; Schwalbe, H. Long-range interactions within a nonnative protein Science 2002, 295, 1719-1722
29. Neri, D.; Billeter, M.; Wider, G.; Wüthrich, K. NMR determination of residual structure in a urea-denatured protein, the 434-repressor Science 1992, 257, 1559-1563
30. Bhavesh, N. S.; Panchal, S. C.; Hosur, R. V. An efficient high-throughput resonance assignment procedure for structural genomics and protein folding research by NMR Biochemistry 2001, 40, 14727-14735
31. Dyson, H. J.; Wright, P. E. Intrinsically unstructured proteins and their functions Nat. Rev. Mol. Cell Biol. 2005, 6, 197-208
32. Ohgushi, M.; Wada, A. "Molten-globule state": a compact form of globular proteins with mobile side-chains FEBS Lett. 1983, 164, 21-24
33. De Laureto, P. P.; Frare, E.; Gottardo, R.; Van Dael, H.; Fontana, A. Partly folded states of members of the lysozyme/lactalbumin superfamily: a comparative study by circular dichroism spectroscopy and limited proteolysis Protein Sci. 2002, 11, 2932-2946
34. Flynn, G. C.; Beckers, C. J.; Baase, W. A.; Dahlquist, F. W. Individual subunits of bacterial luciferase are molten globules and interact with molecular chaperones Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 10826-10830
35. Booth, D. R.; Sunde, M.; Bellotti, V.; Robinson, C. V.; Hutchinson, W. L.; Fraser, P. E.; Hawkins, P. N.; Dobson, C. M.; Radford, S. E.; Blake, C. C.; Pepys, M. B. Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis Nature 1997, 385, 787-793
36. Ren, J.; Kachel, K.; Kim, H.; Malenbaum, S. E.; Collier, R. J.; London, E. Interaction of diptheria toxin T domain with molten globule-like proteins and its implications for translocation Science 1999, 284, 955-957
37. Kuwajima, K. The molten globule state of α-lactalbumin FASEB J. 1996, 10, 102-109
38. Permyakov, E. A.; Berliner, L. J. α-Lactalbumin: structure and function FEBS Lett. 2000, 473, 269-274
39. Chaudhuri, A.; Haldar, S.; Chattopadhyay, A. Organization and dynamics of tryptophans in the molten globule state of bovine α-lactalbumin utilizing wavelength-selective fluorescence approach: comparisons with native and denatured states Biochem. Biophys. Res. Commun. 2010, 394, 1082-1086
40. Kelkar, D. A.; Chaudhuri, A.; Haldar, S.; Chattopadhyay, A. Exploring tryptophan dynamics in acid-induced molten globule state of bovine α-lactalbumin: a wavelength-selective fluorescence approach Eur. Biophys. J. 2010, 39, 1453-1463
41. Tsien, R. Y. The green fluorescent protein Annu. Rev. Biochem. 1998, 67, 509-544
42. Haldar, S.; Chattopadhyay, A. The green journey J. Fluoresc. 2009, 19, 1-2
43. Haldar, S.; Chattopadhyay, A. Green fluorescent protein: a molecular lantern that illuminates the cellular interior J. Biosci. 2009, 34, 169-172
44. Abbyad, P.; Childs, W.; Shi, X.; Boxer, S. G. Dynamic Stokes shift in green fluorescent protein variants Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 20189-20194
45. Haldar, S.; Chattopadhyay, A. Hydration dynamics of probes and peptides in captivity. In Reviews in Fluorescence 2010; Geddes, C. D., Ed.; Springer: New York, 2012; pp 155-172.
46. Patterson, G. H.; Knobel, S. M.; Sharif, W. D.; Kain, S. R.; Piston, D. W. Use of the green fluorescent protein and its mutants in quantitative fluorescence microscopy Biophys. J. 1997, 73, 2782-2790
47. Drews, J. Drug discovery: a historical perspective Science 2000, 287, 1960-1964
48. Anson, L. Membrane protein biophysics Nature 2009, 459, 343
49. Schiffer, M.; Chang, C. H.; Stevens, F. J. The functions of tryptophan residues in membrane proteins Protein Eng. 1992, 5, 213-214
50. Reithmeier, R. A. F. Characterization and modeling of membrane proteins using sequence analysis Curr. Opin. Struct. Biol. 1995, 5, 491-500
51. Chattopadhyay, A.; Mukherjee, S.; Rukmini, R.; Rawat, S. S.; Sudha, S. Ionization, partitioning, and dynamics of tryptophan octyl ester: implications for membrane-bound tryptophan residues Biophys. J. 1997, 73, 839-849
52. Kelkar, D. A.; Chattopadhyay, A. Membrane interfacial localization of aromatic amino acids and membrane protein function J. Biosci. 2006, 31, 297-302
53. Andersen, O. S. Perspectives on membrane protein insertion, protein-bilayer interactions, and amino acid side hydrophobicity J. Gen. Physiol. 2007, 129, 351-352
54. Koeppe, R. E. Concerning tryptophan and protein-bilayer interactions J. Gen. Physiol. 2007, 130, 223-224
55. Chattopadhyay, A. Exploring membrane organization and dynamics by the wavelength-selective fluorescence approach Chem. Phys. Lipids 2003, 122, 3-17
56. Chothia, C. The nature of the accessible and buried surfaces in proteins J. Mol. Biol. 1976, 105, 1-14
57. Wimley, W. C.; White, S. H. Experimentally determined hydrophobicity scale for proteins at membrane interfaces Nat. Struct. Biol. 1996, 3, 842-848
58. Ghosh, A. K.; Rukmini, R.; Chattopadhyay, A. Modulation of tryptophan environment in membrane-bound melittin by negatively charged phospholipids: implications in membrane organization and function Biochemistry 1997, 36, 14291-14305
59. Raghuraman, H.; Chattopadhyay, A. Interaction of melittin with membrane cholesterol: a fluorescence approach Biophys. J. 2004, 87, 2419-2432
60. Mukherjee, S.; Chattopadhyay, A. Motionally restricted tryptophan environments at the peptide lipid interface of gramicidin channels Biochemistry 1994, 33, 5089-5097
61. Rawat, S. S.; Kelkar, D. A.; Chattopadhyay, A. Monitoring gramicidin conformations in membranes: a fluorescence approach Biophys. J. 2004, 87, 831-843
62. Haldar, S.; Raghuraman, H.; Namani, T.; Rajarathnam, K.; Chattopadhyay, A. Membrane interaction of the N-terminal domain of chemokine receptor CXCR1 Biochim. Biophys. Acta 2010, 1798, 1056-1061
63. Koeppe, R. E.; Andersen, O. S. Engineering the gramicidin channel Annu. Rev. Biophys. Biomol. Struct. 1996, 25, 231-258
64. Kelkar, D. A.; Chattopadhyay, A. The gramicidin ion channel: a model membrane protein Biochim. Biophys. Acta 2007, 1768, 2011-2025
65. Chattopadhyay, A.; Rawat, S. S.; Greathouse, D. V.; Kelkar, D. A.; Koeppe, R. E. Role of tryptophan residues in gramicidin channel organization and function Biophys. J. 2008, 95, 166-175
66. Haldar, S.; Chaudhuri, A.; Gu, H.; Koeppe, R. E.; Kombrabail, M.; Krishnamoorthy, G.; Chattopadhyay, A. Membrane organization and dynamics of "inner pair" and "outer pair" tryptophan residues in gramicidin channels J. Phys. Chem. B 2012, 116, 11056-11064
67. Tory, M. C.; Merrill, A. R. Determination of membrane protein topology by red-edge excitation shift analysis: application to the membrane-bound colicin E1 channel peptide Biochim. Biophys. Acta 2002, 1564, 435-448
68. Qiu, W.; Kao, Y.-T.; Zhang, L.; Yang, Y.; Wang, L.; Stites, W. E.; Zhong, D.; Zewail, A. H. Protein surface hydration mapped by site-specific mutations Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 13979-13984
69. Angel, T. E.; Chance, M. R.; Palczewski, K. Conserved waters mediate structural and functional activation of family A (rhodopsin-like) G protein-coupled receptors Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 8555-8560