Interdomain orientation of cardiac troponin C characterized by paramagnetic relaxation enhancement NMR reveals a compact state

Protein Science

Volumn 21, Issue 9, 2012, Pages 1376-1387

  Cordina, Nicole M ^a   Liew, Chu Kong ^b,d   Gell, David A ^b,e   Fajer, Piotr G ^c   Mackay, Joel P ^b   Brown, Louise J ^a  

^a MACQUARIE UNIVERSITY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c FLORIDA STATE UNIVERSITY   (United States)

^d VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^e UNIVERSITY OF TASMANIA   (Australia)

Author keywords

Cardiac troponin C; Ensemble states; Paramagnetic relaxation enhancement; Site directed spin labeling; Solution NMR

Indexed keywords

TROPONIN C;

ARTICLE; CONTRAST ENHANCEMENT; DATA ANALYSIS; HEART FUNCTION; NUCLEAR MAGNETIC RESONANCE; PARAMAGNETIC RELAXATION ENHANCEMENT NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; REGULATORY MECHANISM; SPECTROSCOPY;

EID: 84865416690     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2124     Document Type: Article

References (50)

1. 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)
2. Li MX, Robertson IM, Sykes BD (2008) Interaction of cardiac troponin with cardiotonic drugs: a structural perspective. Biochem Biophys Res Commun 369:88-99.
3. Sundaralingam M, Bergstrom R, Strasburg G, Rao ST, Roychowdhury P, Greaser M, Wang BC (1985) Molecular structure of troponin C from chicken skeletal muscle at 3-angstrom resolution. Science 227:945-948. (Pubitemid 15090458)
4. Metzler WJ, Constantine KL, Friedrichs MS, Bell AJ, Ernst EG, Lavoie TB, Mueller L (1993) Characterization of the three-dimensional solution structure of human profilin: proton, carbon-13, and nitrogen-15 NMR assignments and global folding pattern. Biochemistry 32:13818-13829. (Pubitemid 24018232)
5. Gordon AM, Homsher E, Regnier M (2000) Regulation of contraction in striated muscle. Physiol Rev 80:853-924. (Pubitemid 30164950)
6. Heidorn DB, Trewhella J (1988) Comparison of the crystal and solution structures of calmodulin and troponin C. Biochemistry 27:909-915. (Pubitemid 18052986)
7. Slupsky CM, Sykes BD (1995) NMR solution structure of calcium-saturated skeletal muscle troponin C. Biochemistry 34:15953-15964.
8. Blumenschein TMA, Stone DB, Fletterick RJ, Mendelson RA, Sykes BD (2005) Calcium-dependent changes in the flexibility of the regulatory domain of troponin C in the troponin complex. J Biol Chem 280:21924-21932. (Pubitemid 40827844)
9. Anthis NJ, Doucleff M, Clore GM (2011) Transient, sparsely populated compact states of apo and calcium-loaded calmodulin probed by paramagnetic relaxation enhancement: interplay of conformational selection and induced fit. J Am Chem Soc 133:18966-18974.
10. Baber JL, Szabo A, Tjandra N (2001) Analysis of slow interdomain motion of macromolecules using NMR relaxation data. J Am Chem Soc 123:3953-3959. (Pubitemid 32899482)
11. Abbott MB, Gaponenko V, Abusamhadneh E, Finley N, Li G, Dvoretsky A, Rance M, Solaro RJ, Rosevear PR (2000) Regulatory domain conformational exchange and linker region flexibility in cardiac troponin C bound to cardiac troponin I. J Biol Chem 275:20610-20617. (Pubitemid 30457646)
12. Gaponenko V, Abusamhadneh E, Abbott MB, Finley N, Gasmi-Seabrook G, Solaro RJ, Rance M, Rosevear PR (1999) Effects of troponin I phosphorylation on conformational exchange in the regulatory domain of cardiac troponin C. J Biol Chem 274:16681-16684.
13. 2+ switch in muscular contraction. J Biol Chem 268:19232-19238.
14. Dobrowolski Z, Xu GQ, Hitchcock-DeGregori SE (1991) Modified calcium-dependent regulatory function of troponin C central helix mutants. J Biol Chem 266:5703-5710. (Pubitemid 21909551)
15. Ramakrishnan S, Hitchcock-DeGregori SE (1995) Investigation of the structural requirements of the troponin C central helix for function. Biochemistry 34:16789-16796. (Pubitemid 26011804)
16. Zheng D, Aramini JM, Montelione GT (2004) Validation of helical tilt angles in the solution NMR structure of the Z domain of Staphylococcal protein A by combined analysis of residual dipolar coupling and NOE data. Protein Sci 13:549-554. (Pubitemid 38124976)
17. Deshmukh MV, John M, Coles M, Peters J, Baumeister W, Kessler H (2006) Inter-domain orientation and motions in VAT-N explored by residual dipolar couplings and 15N backbone relaxation. Magn Reson Chem 44:S89-S100. (Pubitemid 44090394)
18. Sia SK, Li MX, Spyracopoulos L, Gagne SM, Liu W, Putkey JA, Sykes BD (1997) Structure of cardiac muscle troponin C unexpectedly reveals a closed regulatory domain. J Biol Chem 272:18216-18221. (Pubitemid 27306409)
19. 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)
20. Battiste JL, Wagner G (2000) Utilization of site-directed spin labeling and high-resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear overhauser effect data. Biochemistry 39:5355-5365. (Pubitemid 30257075)
21. Clore GM, Iwahara J (2009) Theory, practice, and applications of paramagnetic relaxation enhancement for the characterization of transient low-population states of biological macromolecules and their complexes. Chem Rev 109:4108-4139.
22. 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. (Pubitemid 36834832)
23. Farmer BT, Constantine KL, Goldfarb V, Friedrichs MS, Wittekind M, Yanchunas J, Robertson JG, Mueller L (1996) Localizing the NADP+ binding site on the MurB enzyme by NMR. Nat Struct Mol Biol 3:995-997. (Pubitemid 27014626)
24. Nakamura M, Ueki S, Hara H, Arata T (2005) Calcium structural transition of human cardiac troponin C in reconstituted muscle fibres as studied by site-directed spin labelling. J Mol Biol 348:127-137. (Pubitemid 40461845)
25. Dong W-j, Wang C-K, Gordon AM, Cheung HC (1997) Disparate fluorescence properties of 2-[4′-(iodoacetamido)anilino]-naphthalene-6-sulfonic acid attached to Cys-84 and Cys-35 of troponin C in cardiac muscle troponin. Biophys J 72:850-857. (Pubitemid 27044890)
26. Putkey JA, Dotson DG, Mouawad P (1993) Formation of inter- and intramolecular disulfide bonds can activate cardiac troponin C. J Biol Chem 268:6827-6830. (Pubitemid 23105554)
27. Wishart DS, Arndt D, Berjanskii M, Tang P, Zhou J, Lin G (2008) CS23D: a web server for rapid protein structure generation using NMR chemical shifts and sequence data. Nucleic Acids Res 36:W496-W502.
28. Kleerekoper Q, Howarth JW, Guo X, Solaro RJ, Rosevear PR (1995) Cardiac Troponin I induced conformational changes in cardiac troponin C as monitored by NMR using site-directed spin and isotope labeling. Biochemistry 34:13343-13352.
29. Tang C, Schwieters CD, Clore GM (2007) Open-to-closed transition in apo maltose-binding protein observed by paramagnetic NMR. Nature 449:1078-1082. (Pubitemid 350014601)
30. Bertini I, Luchinat C, Nagulapalli M, Parigi G, Ravera E (2012) Paramagnetic relaxation enhancement for the characterization of the conformational heterogeneity in two-domain proteins. Phys Chem Chem Phys 14:9149-9156.
31. Dong W-J, Robinson JM, Xing JUN, Umeda PK, Cheung HC (2000) An interdomain distance in cardiac troponin C determined by fluorescence spectroscopy. Protein Sci 9:280-289. (Pubitemid 30127001)
32. Heller WT, Abusamhadneh E, Finley N, Rosevear PR, Trewhella J (2002) The solution structure of a cardiac troponin C-troponin I-troponin T complex shows a somewhat compact troponin C interacting with an extended troponin I-troponin Tcomponent. Biochemistry 41:15654-15663. (Pubitemid 36062470)
33. Vinogradova MV, Stone DB, Malanina GG, Karatzaferi C, Cooke R, Mendelson RA, Fletterick RJ (2005) Ca(2+)-regulated structural changes in troponin. Proc Natl Acad Sci USA 102:5038-5043.
34. Brown LJ, Sale KL, Hills R, Rouviere C, Song L, Zhang X, Fajer PG (2002) Structure of the inhibitory region of troponin by site directed spin labeling electron paramagnetic resonance. Proc Natl Acad Sci USA 99:12765-12770.
35. Sambrook J, Fritsch EF, Maniatis T.1989. Molecular cloning: a laboratory manual. New York: Cold Spring Harbor Laboratory Press.
36. Studier FW, Rosenberg AH, Dunn JJ, Dubendorff JW (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 185:60-89. (Pubitemid 20219811)
37. Donaldson LW, Skrynnikov NR, Choy WY, Muhandiram DR, Sarkar B, Forman-Kay JD, Kay LE (2001) Structural characterization of proteins with an attached ATCUN motif by paramagnetic relaxation enhancement NMR spectroscopy. J Am Chem Soc 123:9843-9847. (Pubitemid 32929390)
38. Goddard TD, Kneller DG (2007) SPARKY 3. San Francisco: University of California.
39. Grzesiek S, Bax A (1992) Correlating backbone amide and side chain resonances in larger proteins by multiple relayed triple resonance NMR. J Am Chem Soc 114:6291-6293.
40. Ikura M, Kay LE, Bax A (1990) A novel approach for sequential assignment of proton, carbon-13, and nitrogen-15 spectra of larger proteins: heteronuclear tripleresonance three-dimensional NMR spectroscopy. Application to calmodulin. Biochemistry 29:4659-4667. (Pubitemid 20172684)
41. Wittekind M, Mueller L (1993) HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha- and beta-carbon resonances in proteins. J Magn Reson B 101:201-205.
42. Volkov AN, Worrall JAR, Holtzmann E, Ubbink M (2006) Solution structure and dynamics of the complex between cytochrome c and cytochrome c peroxidase determined by paramagnetic NMR. Proc Natl Acad Sci USA 103:18945-18950. (Pubitemid 350002808)
43. Liang B, Bushweller JH, Tamm LK (2006) Site-directed parallel spin-labeling and paramagnetic relaxation enhancement in structure determination of membrane proteins by solution NMR spectroscopy. J Am Chem Soc 128:4389-4397.
44. Iwahara J, Schwieters CD, Clore GM (2004) Ensemble approach for NMR structure refinement against (1)H paramagnetic relaxation enhancement data arising from a flexible paramagnetic group attached to a macromolecule. J Am Chem Soc 126:5879-5896. (Pubitemid 38621427)
45. Cantor CR, Schimmel PR (1980) Biophysical chemistry. New York: W. H. Freeman & Co. pp461.
46. Li H-C, Fajer PG (1994) Orientational changes of troponin C associated with thin filament activation. Biochemistry 33:14324-14332. (Pubitemid 24382380)
47. Gagné SM, Tsuda S, Spyracopoulos L, Kay LE, Sykes BD (1998) Backbone and methyl dynamics of the regulatory domain of troponin C: anisotropic rotational diffusion and contribution of conformational entropy to calcium affinity. J Mol Biol 278:667-686. (Pubitemid 28224863)
48. Guo Z, Cascio D, Hideg K, Hubbell WL (2008) Structural determinants of nitroxide motion in spin-labeled proteins: solvent-exposed sites in helix B of T4 lysozyme. Protein Sci 17:228-239. (Pubitemid 351171835)
49. Cornilescu G, Marquardt JL, Ottiger M, Bax A (1998) Validation of Protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase. J Am Chem Soc 120:6836-6837. (Pubitemid 28347351)
50. Bermejo GA, Strub M-P, Ho C, Tjandra N (2009) Determination of the solution-bound conformation of an amino acid binding protein by NMR paramagnetic relaxation enhancement: use of a single flexible paramagnetic probe with improved estimation of its sampling space. J Am Chem Soc 131:9532-9537.