The effect of the cosolvent trifluoroethanol on a tryptophan side chain orientation in the hydrophobic core of troponin C

Protein Science

Volumn 18, Issue 6, 2009, Pages 1165-1174

  Julien, Olivier ^a   Mercier, Pascal ^a   Crane, Melissa L ^a   Sykes, Brian D ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

NMR; Rotamer; Side chain orientation; TFE; Troponin C; Tryptophan

Indexed keywords

TRIFLUOROETHANOL; TROPONIN C; TRYPTOPHAN;

AMINO ACID SEQUENCE; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; NITROGEN NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SOLVENT EFFECT;

HUMANS; HYDROPHOBICITY; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SOLVENTS; TRIFLUOROETHANOL; TROPONIN C; TRYPTOPHAN;

EID: 66349106202     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.121     Document Type: Article

References (50)

1. Khemtemourian L, Sani MA, Bathany K, Grobner G, Dufourc EJ (2006) Synthesis and secondary structure in membranes of the Bcl-2 anti-apoptotic domain BH4. J Pept Sci 12:58-64. (Pubitemid 43033699)
2. Sonnichsen FD, Van Eyk JE, Hodges RS, Sykes BD (1992) Effect of trifluoroethanol on protein secondary structure: an NMR and CD study using a synthetic actin peptide. Biochemistry 31:8790-8798.
3. Santiveri CM, Pantoja-Uceda D, Rico M, Jimenez MA (2005) Beta-hairpin formation in aqueous solution and in the presence of trifluoroethanol: a 1H and 13C nuclear magnetic resonance conformational study of designed peptides. Biopolymers 79:150-162. (Pubitemid 41652911)
4. Calamai M, Chiti F, Dobson CM (2005) Amyloid fibril formation can proceed from different conformations of a partially unfolded protein. Biophys J 89:4201-4210. (Pubitemid 41725639)
5. Pallares I, Vendrell J, Aviles FX, Ventura S (2004) Amyloid fibril formation by a partially structured intermediate state of alpha-chymotrypsin. J Mol Biol 342:321-331. (Pubitemid 39094523)
6. Shanmugam G, Polavarapu PL, Gopinath D, Jayakumar R (2005) The structure of antimicrobial pexiganan peptide in solution probed by Fourier transform infrared absorption, vibrational circular dichroism, and electronic circular dichroism spectroscopy. Biopolymers 80:636-642. (Pubitemid 41665233)
7. Kanno T, Yamaguchi K, Naiki H, Goto Y, Kawai T (2005) Association of thin filaments into thick filaments revealing the structural hierarchy of amyloid fibrils. J Struct Biol 149:213-218. (Pubitemid 40170103)
8. Slupsky CM, Kay CM, Reinach FC, Smillie LB, Sykes BD (1995) Calcium-induced dimerization of troponin C: mode of interaction and use of trifluoroethanol as a denaturant of quaternary structure. Biochemistry 34:7365-7375.
9. Pääkkönen K, Annila A, Sorsa T, Pollesello P, Tilgmann C, Kilpeläinen I, Karisola P, Ulmanen I, Drakenberg T (1998) Solution structure and main chain dynamics of the regulatory domain (Residues 1-91) of human cardiac troponin C. J Biol Chem 273:15633-15638. (Pubitemid 28298178)
10. Julien O, Sun YB, Wang X, Lindhout DA, Thiessen A, Irving M, Sykes BD (2008) Tryptophan mutants of cardiac troponin C: 3D structure, troponin I affinity, and in situ activity. Biochemistry 47:597-606.
11. Slupsky CM, Sykes BD (1995) NMR solution structure of calcium-saturated skeletal muscle troponin C. Biochemistry 34:15953-15964.
12. Buck M (1998) Trifluoroethanol and colleagues: cosolvents come of age. Recent studies with peptides and proteins. Q Rev Biophys 31:297-355.
13. Dong WJ, Xing J, Villain M, Hellinger M, Robinson JM, Chandra M, Solaro RJ, Umeda PK, Cheung HC (1999) Conformation of the regulatory domain of cardiac muscle troponin C in its complex with cardiac troponin I. J Biol Chem 274:31382-31390. (Pubitemid 129501592)
14. Cooke R, Crowder MS, Thomas DD (1982) Orientation of spin labels attached to cross-bridges in contracting muscle fibers. Nature 300:776-778. (Pubitemid 13224364)
15. Pirani A, Vinogradova MV, Curmi PM, King WA, Fletterick RJ, Craig R, Tobacman LS, Xu C, Hatch V, Lehman W (2006) An atomic model of the thin filament in the relaxed and Ca2+-activated states. J Mol Biol 357:707-717.
16. Gagné SM, Tsuda S, Li MX, Smillie LB, Sykes BD (1995) Structures of the troponin C regulatory domains in the apo and calcium-saturated states. Nat Struct Biol 2:784-789.
17. Takeda S, Yamashita A, Maeda K, Maeda Y (2003) Structure of the core domain of human cardiac troponin in the Ca(2+)-saturated form. Nature 424:35-41.
18. Herzberg O, James MN (1985) Structure of the calcium regulatory muscle protein troponin-C at 2.8 A resolution. Nature 313:653-659. (Pubitemid 15172468)
19. Corrie JET, Brandmeier BD, Ferguson RE, Trentham DR, Kendrick-Jones J, Hopkins SC, van der Heide UA, Goldman YE, Sabido-David C, Dale RE, Criddle S, Irving M (1999) Dynamic measurement of myosin light-chain-domain tilt and twist in muscle contraction. Nature 400:425-430. (Pubitemid 29361790)
20. Ferguson RE, Sun YB, Mercier P, Brack AS, Sykes BD, Corrie JE, Trentham DR, Irving M (2003) In situ orientations of protein domains: troponin C in skeletal muscle fibers. Mol Cell 11:865-874.
21. De Simone A, Corrie JET, Dale RE, Irving M, Fraternali F (2008) Conformation and dynamics of a rhodamine probe attached at two sites on a protein: implications for molecular structure determination in situ. J Am Chem Soc 130:17120-17128.
22. Julien O, Mercier P, Spyracopoulos L, Corrie JET, Sykes BD (2008) NMR studies of the dynamics of a bifunctional rhodamine probe attached to troponin C. J Am Chem Soc 130:2602-2609.
23. Lakowicz JR (2000) On spectral relaxation in proteins. Photochem Photobiol 72:421-437.
24. Li MX, Chandra M, Pearlstone JR, Racher KI, Trigo-Gonzalez G, Borgford T, Kay CM, Smillie LB (1994) Properties of isolated recombinant N and C domains of chicken troponin C. Biochemistry 33:917-925. (Pubitemid 24058430)
25. Moncrieffe MC, Eaton S, Bajzer Z, Haydock C, Potter JD, Laue TM, Prendergast FG (1999) Rotational and translational motion of troponin C. J Biol Chem 274:17464-17470. (Pubitemid 129519090)
26. Moncrieffe MC, Venyaminov SY, Miller TE, Guzman G, Potter JD, Prendergast FG (1999) Optical spectroscopic characterization of single tryptophan mutants of chicken skeletal troponin C: evidence for interdomain interaction. Biochemistry 38:11973-11983. (Pubitemid 129515470)
27. Hutnik CM, MacManus JP, Banville D, Szabo AG (1990) Comparison of metal ion-induced conformational changes in parvalbumin and oncomodulin as probed by the intrinsic fluorescence of tryptophan 102. J Biol Chem 265:11456-11464. (Pubitemid 20219301)
28. Moncrieffe MC, Juranic N, Kemple MD, Potter JD, Macura S, Prendergast FG (2000) Structure-fluorescence correlations in a single tryptophan mutant of carp parvalbumin: solution structure, backbone and side-chain dynamics. J Mol Biol 297:147-163.
29. Wang X, Mercier P, Letourneau PJ, Sykes BD (2005) Effects of Phe-to-Trp mutation and fluorotryptophan incorporation on the solution structure of cardiac troponin C, and analysis of its suitability as a potential probe for in situ NMR studies. Protein Sci 14:2447-2460. (Pubitemid 41252813)
30. Zhao X, DeVries JS, McDonald R, Sykes BD (2007) Determination of the 19F NMR chemical shielding tensor and crystal structure of 5-fluoro-dl-tryptophan. J Magn Reson 187:88-96. (Pubitemid 46898865)
31. Richardson RC, King NM, Harrington DJ, Sun H, Royer WE, Nelson DJ (2000) X-Ray crystal structure and molecular dynamics simulations of silver hake parvalbumin (Isoform B). Protein Sci 9:73-82. (Pubitemid 30070941)
32. Nishita K, Tanaka H, Ojima T (1994) Amino acid sequence of troponin C from scallop striated adductor muscle. J Biol Chem 269:3464-3468. (Pubitemid 24237666)
33. Ozkirimli E, Yadav SS, Miller WT, Post CB (2008) An electrostatic network and long-range regulation of Src kinases. Protein Sci 17:1871-1880.
34. Witter R, Nozirov F, Sternberg U, Cross TA, Ulrich AS, Fu R (2008) Solid-state 19F NMR spectroscopy reveals that Trp41 participates in the gating mechanism of the M2 proton channel of influenza A virus. J Am Chem Soc 130:918-924.
35. Willis KJ, Neugebauer W, Sikorska M, Szabo AG (1994) Probing alpha-helical secondary structure at a specific site in model peptides via restriction of tryptophan side-chain rotamer conformation. Biophys J 66:1623-1630. (Pubitemid 2086190)
36. Markley JL, Bax A, Arata Y, Hilbers CW, Kaptein R, Sykes BD, Wright PE, Wuthrich K (1998) Recommendations for the presentation of NMR structures of proteins and nucleic acids-IUPAC-IUBMB-IUPAB Inter-Union Task Group on the standardization of data bases of protein and nucleic acid structures determined by NMR spectroscopy. Eur J Biochem 256:1-15. (Pubitemid 28399089)
37. Lovell SC, Word JM, Richardson JS, Richardson DC (2000) The penultimate rotamer library. Proteins 40:389-408. (Pubitemid 30624447)
38. Dezube B, Dobson CM, Teague CE (1981) Conformational-analysis of tryptophan in solution using nuclear magnetic-resonance methods. J Chem Soc [Perkin 1] 2:730-735.
39. Ross JB, Wyssbrod HR, Porter RA, Schwartz GP, Michaels CA, Laws WR (1992) Correlation of tryptophan fluorescence intensity decay parameters with 1H NMR-determined rotamer conformations: [tryptophan2]oxytocin. Biochemistry 31:1585-1594.
40. Johansson JS, Scharf D, Davies LA, Reddy KS, Eckenhoff RG (2000) A designed four-alpha-helix bundle that binds the volatile general anesthetic halothane with high affinity. Biophys J 78:982-993. (Pubitemid 30211856)
41. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8:477-486. (Pubitemid 126706801)
42. Gagné SM, Tsuda S, Li MX, Chandra M, Smillie LB, Sykes BD (1994) Quantification of the calcium-induced secondary structural changes in the regulatory domain of troponin-C. Protein Sci 3:1961-1974.
43. Li MX, Gagné SM, Tsuda S, Kay CM, Smillie LB, Sykes BD (1995) Calcium binding to the regulatory N-domain of skeletal muscle troponin C occurs in a stepwise manner. Biochemistry 34:8330-8340.
44. Baryshnikova OK, Williams TC, Sykes BD (2008) Internal pH indicators for biomolecular NMR. J Biomol NMR 41:5-7.
45. Zhang OW, Kay LE, Olivier JP, Forman-Kay JD (1994) Backbone H-1 and N-15 resonance assignments of the N-terminal Sh3 domain of Drk in folded and unfolded states using enhanced-sensitivity pulsed-field gradient NMR techniques. J Biomol NMR 4:845-858.
46. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277-293.
47. Slupsky CM, Boyko RF, Booth VK, Sykes BD (2003) Smartnotebook: a semi-automated approach to protein sequential NMR resonance assignments. J Biomol NMR 27:313-321. (Pubitemid 37322105)
48. Graether SP, DeVries JS, McDonald R, Rakovszky ML, Sykes BD (2006) A 1H/19F minicoil NMR probe for solid-state NMR: application to 5-fluoroindoles. J Magn Reson 178:65-71.
49. Guntert P (2004) Automated NMR structure calculation with CYANA. Methods Mol Biol 278:353-378.
50. Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13:289-302. (Pubitemid 29143535)