Solvent-induced differentiation of protein backbone hydrogen bonds in calmodulin

Protein Science

Volumn 16, Issue 7, 2007, Pages 1329-1337

  Juranić, Nenad ^a   Atanasova, Elena ^a   Streiff, John H ^b   Macura, Slobodan ^a   Prendergast, Franklyn G ^a  

^a MAYO CLINIC   (United States)

^b DEPARTMENT OF UROLOGY   (United States)

Author keywords

h3JNC couplings; Calmodulin; Hydrogen bonding; Proteins

Indexed keywords

CALMODULIN; CELL ADHESION MOLECULE; PROTEIN; SOLVENT; WATER;

ARTICLE; CORRELATION ANALYSIS; DIFFERENTIATION; GEOMETRY; HUMAN; HYDROGEN BOND; PRIORITY JOURNAL; PROTEIN STRUCTURE; SOLUTION AND SOLUBILITY;

CALMODULIN; HUMANS; HYDROGEN BONDING; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS, PROTEIN; SOLVENTS;

EID: 34250868555     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.062689807     Document Type: Article

References (60)

1. Alexandrescu, A.T., Snyder, D.R., and Abildgaard, F. 2001. NMR of hydrogen bonding in cold-shock protein A and an analysis of the influence of crystallographic resolution on comparisons of hydrogen bond lengths. Protein Sci. 10: 1856-1868.
2. Assadi-Porter, F.M., Abildgaard, F., Blad, H., and Markley, J.L. 2003. Correlation of the sweetness of variants of the protein brazzein with patterns of hydrogen bonds detected by NMR spectroscopy. J. Biol. Chem. 278: 31331-31339.
3. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: The central helix is flexible. Biochemistry 31: 5269-5278.
4. 1H chemical shifts in the hydrogen bonding regions of proteins. J. Am. Chem. Soc. 124: 4158-4168.
5. Bouvignies, G., Bernado, P., Meier, S., Cho, K., Grzesiek, S., Bruschweiler, R., and Blackledge, M. 2005. Identification of slow correlated motions in proteins using residual dipolar and hydrogen-bond scalar couplings. Proc. Natl. Acad. Sci. 102: 13885-13890.
6. Brzeska, H., Venyaminov, S.Vu., Grabarek, Z., and Drabikowski, W. 1983. Comparative studies on thermostability of calmodulin, skeletal muscle troponin C and their fragments. FEBS Lett. 153: 169-173.
7. Carafoli, E. and Klee, C. 1999. Calcium as cellular regulator. Oxford University Press, New York.
8. Chattopadhyaya, R., Meador, W.E., Means, A.R., and Quiocho, F.A. 1992. Calmodulin structure refined at 1.7 angstrom resolution. J. Mol. Biol. 228: 1177-1192.
9. Cheung, W.Y. 1980. Calmodulin plays a pivotal role in cellular regulation. Science 207: 19-27.
10. 2+-calmodulin reveals flexible hand-like properties of its domains. Nat. Struct. Biol. 8: 990-997.
11. NC′ scalar couplings. J. Am. Chem. Soc. 121: 1601-1602.
12. Cordier, F. and Grzesiek, S. 2004. Quantitative comparison of the hydrogen bond network of A-state and native ubiquitin by hydrogen bond scalar couplings. Biochemistry 43: 11295-11301.
13. Cornilescu, G., Hu, J.S., and Bax, A. 1999. Identification of the hydrogen bonding network in a protein by scalar couplings. J. Am. Chem. Soc. 121: 2949-2950.
14. Dannenberg, J.J. 2006. The importance of cooperative interactions and a solid-state paradigm to proteins: What peptide chemists can learn from molecular crystals. Adv. Protein Chem. 72: 227.
15. Derrick, J.P. and Wigley, D.B. 1994. The 3rd igg-binding domain from streptococcal protein-G - An analysis by X-ray crystallography of the structure alone and in a complex with Fab. J. Mol. Biol. 243: 906-918.
16. Evenas, J., Malmendal, A., and Akke, M. 2001. Dynamics of the transition between open and closed conformations in a calmodulin C-terminal domain mutant. Structure 9: 185-195.
17. Falke, J.J., Drake, S.K., Hazard, A.L., and Peersen, O.B. 1994. Molecular tuning of ion-binding to calcium signaling proteins. Q. Rev. Biophys. 27: 219-290.
18. 2+-calmodulin. Structure 11: 1303-1307.
19. Grzesiek, S., Cordier, F., Jaravine, V., and Barfielfd, M. 2004. Insight into biomolecular hydrogen bonds from hydrogen bond scalar couplings. Prog. Nucl. Magn. Reson. Spectrosc. 45: 275-300.
20. Hee-chul, A., Juranić, N., Macura, S., and Markley, J.L. 2006. Three-dimensional structure of the water-insoluble protein crambin in dodecylphosphocholine micelles and its minimal solvent-exposed surface. J. Am. Chem. Soc. 128: 4398-4404.
21. Ikura, M. 1996. Calcium binding and conformational response in EF-hand proteins. Trends Biochem. Sci. 21: 14-17.
22. Ikura, M. and Ames, J.B. 2006. Genetic polymorphism and protein conformational plasticity in the calmodulin superfamily: Two ways to promote multifunctionality. Proc. Natl. Acad. Sci. 103: 1159-1164.
23. Ikura, M., Clore, G.M., Gronenborn, A.M., Zhu, G., Klee, C., and Bax, A. 1992. Solution structure of calmodulin-target peptide complex by multidimensional NMR. Science 256: 632-638.
24. Ishima, R. and Torchia, D.A. 2003. Extending the range of amide proton relaxation dispersion experiments in proteins using a constant-time relaxation-compensated CPMG approach. J. Biomol. NMR 25: 243-248.
25. Ishima, R., Baber, J., Louis, J.M., and Torchia, D.A. 2004. Carbonyl carbon transverse relaxation dispersion measurements and ms-μs timescale motion in a protein hydrogen bond network. J. Biomol. NMR 29: 187-198.
26. Jelsch, C., Teeter, M.M., Lamzin, V., Pichon-Pesme, V., Blessing, R.H., and Lecomte, C. 2000. Accurate protein crystallography at ultra-high resolution: Valence electron distribution in crambin. Proc. Natl. Acad. Sci. 97: 3171-3176.
27. Jurado, L.A., Chockalingam, P.S., and Jarrett, H.W. 1999. Apocalmodulin. Physiol. Rev. 79: 661-682.
28. NC′ coupling constants in the hydrogen-bonding network of human ubiquitin. J. Am. Chem. Soc. 123: 4099-4100.
29. NC′ coupling constant determination and molecular dynamics simulations. J. Am. Chem. Soc. 118: 7859-7860.
30. NC′ scalar coupling in protein H-bond chains. J. Am. Chem. Soc. 124: 14221-14226.
31. Juranić, N., Macura, S., and Prendergast, F.G. 2003. H-bonding mediates polarization of peptide groups in folded proteins. Protein Sci. 12: 2633-2636.
32. Karplus, M. and McCammon, J.A. 2002. Molecular dynamics simulations of biomolecules. Nat. Struct. Biol. 9: 646-652; Erratum 9: 788.
33. Kuboniwa, H., Tjandra, N., Grzesiek, S., Ren, H., Klee, C.B., and Bax, A. 1995. Solution structure of calcium-free calmodulin. Nat. Struct. Biol. 2: 768-776.
34. Kumar, V.D., Lee, L., and Edwards, B.F. 1990. Refined crystal structure of calcium-liganded carp parvalbumin 4.25 at 1.5-Å resolution. Biochemistry 29: 1404-1412.
35. Malmendal, A., Evenas, J., Forsen, S., and Akke, M. 1999. Structural dynamics in the C-terminal domain of calmodulin at low calcium levels. J. Mol. Biol. 293: 883-899.
36. Manas, E.S., Getahun, Z., Wright, W.W., DeGrado, W.F., and Vanderkooi, J.M. 2000. Infrared spectra of amide groups in α-helical proteins: Evidence for hydrogen bonding between helices and water. J. Am. Chem. Soc. 122: 9883-9890.
37. Markwick, P.R., Sprangers, R., and Sattler, M. 2003. Dynamic effects on J-couplings across hydrogen bonds in proteins. J. Am. Chem. Soc. 125: 644-645; Erratum 125: 6336.
38. Marley, J., Lu, M., and Bracken, C. 2001. A method for efficient isotopic labeling of recombinant proteins. J. Biomol. NMR 20: 71-75.
39. Meador, W.E., Means, A.R., and Quiocho, F.A. 1993. Modulation of calmodulin plasticity in molecular recognition on the basis of X-ray structures. Science 262: 1718-1721.
40. Meador, W.E., George, S.E., Means, A.R., and Quiocho, F.A. 1995. X-ray-analysis reveals conformational adaptation of the linker in functional calmodulin mutants. Nat. Struct. Biol. 2: 943-945.
41. Morozov, A.V., Kortemme, T., Tsemekhman, K., and Baker, D. 2004. Close agreement between the orientation dependence of hydrogen bonds observed in protein structures and quantum mechanical calculations. Proc. Natl. Acad. Sci. 101: 6946-6951.
42. 2+ sensor proteins. Protein Sci. 7: 270-282.
43. Nelson, M.R., Thulin, E., Fagan, P.A., Forsen, S., and Chazin, W.J. 2002. The EF-hand domain: A globally cooperative structural unit. Protein Sci. 11: 198-205.
44. 2+ binding and implications for kinase activation. Protein Sci. 6: 794-807.
45. Pelupessy, P., Ravindranathan, S., and Bodenhausen, G. 2003. Correlated motions of successive amide N-H bonds in proteins. J. Biomol. NMR 25: 265-280.
46. Putkey, J.A., Slaughter, G.R., and Means, A.R. 1985. Bacterial expression and characterization of proteins derived from the chicken calmodulin cDNA and calmodulin processed gene. J. Biol. Chem. 260: 4704-4712.
47. Sacchettini, J.C., Gordon, J.I., and Banaszak, L.J. 1989. Refined apoprotein structure of rat intestinal fatty acid binding protein produced in Escherichia coli. Proc. Natl. Acad. Sci. 86: 7736-7740.
48. Schumacher, M.A., Crum, M., and Miller, M.C. 2004. Crystal structures of apocalmodulin and an apocalmodulin/SK potassium channel gating domain complex. Structure 12: 849-860.
49. Shenkarev, Z.O., Balashova, T.A., Yakimenko, Z.A., Ovchinnikova, T.V., and Arseniev, A.S. 2004. Peptaibol zervamicin IIB structure and dynamics refinement from transhydrogen bond J couplings. Biophys. J. 86: 3687-3699.
50. Sheu, S.Y., Yang, D.Y., Selzle, H.L., and Schlag, E.W. 2003. Energetics of hydrogen bonds in peptides. Proc. Natl. Acad. Sci. 100: 12683-12687.
51. Slaughter, B.D., Unruh, J.R., Allen, M.W., Urbauer, R.J.B., and Johnson, C.K. 2005. Conformational substates of calmodulin revealed by single-pair fluorescence resonance energy transfer: Influence of solution conditions and oxidative modification. Biochemistry 44: 3694-3707.
52. 15N-NMR relaxation measurements. Eur. J. Biochem. 230: 1014-1024.
53. Vetter, S.W. and Leclerc, E. 2003. Novel aspects of calmodulin target recognition and activation. Eur. J. Biochem. 270: 404-414.
54. Vijay-Kumar, S., Bugg, C.E., and Cook, W.J. 1987. Structure of ubiquitin refined at 1.8 Å resolution. J. Mol. Biol. 194: 531-544.
55. Walsh, S.T., Cheng, R.P., Wright, W.W., Alonso, D.O., Daggett, V., Vanderkooi, J.M., and DeGrado, W.F. 2003. The hydration of amides in helices; a comprehensive picture from molecular dynamics, IR, and NMR. Protein Sci. 12: 520-531; Erratum 12: 1303.
56. Wieczorek, R. and Dannenberg, J.J. 2005. Enthalpies of hydrogen-bonds in α-helical peptides. An ONIOM DFT/AM1 study. J. Am. Chem. Soc. 127: 14534-14535.
57. 2+-bound calmodulin: An analysis of disorder and implications for functionally relevant plasticity. J. Mol. Biol. 301: 1237-1256.
58. Yang, W., Lee, H.W., Hellinga, H., and Yang, J.J. 2002. Structural analysis, identification, and design of calcium-binding sites in proteins. Protein Struct. Funct. Genet. 47: 344-356.
59. Zhang, M., Tanaka, T., and Ikura, M. 1995a. Calcium-induced conformational transition revealed by the solution structure of apo calmodulin. Nat. Struct. Biol. 2: 758-767.
60. Zhang, M.J., Tanaka, T., Farrow, N.A., Kay, L.E., and Ikura, M. 1995b. Multidimensional NMR-studies of the structure and dynamics of calcium-free calmodulin. Protein Eng. 8: 30.