Solution structure of Ca2+-free rat β-parvalbumin (oncomodulin)

Protein Science

Volumn 16, Issue 9, 2007, Pages 1914-1926

  Henzl, Michael T ^a   Tanner, John J ^a,b  

^a University of Missouri   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

Calcium binding protein; Dynamics; EF hand protein; NMR; Oncomodulin; Parvalbumin; Structure

Indexed keywords

BETA PARVALBUMIN; CALCIUM BINDING PROTEIN; PARVALBUMIN; UNCLASSIFIED DRUG; CALCIUM; ISOPROTEIN; ONCOMODULIN; RECOMBINANT PROTEIN;

ARTICLE; BINDING AFFINITY; ENERGY TRANSFER; HYDROPHOBICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN STRUCTURE; RAT; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; GENETICS; HYDROGEN BOND; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; RAMAN SPECTROMETRY; SOLUTION AND SOLUBILITY;

MAMMALIA; RATTUS;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM; CALCIUM-BINDING PROTEINS; HYDROGEN BONDING; HYDROPHOBICITY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PARVALBUMINS; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RATS; RECOMBINANT PROTEINS; SOLUTIONS; SPECTRUM ANALYSIS, RAMAN;

EID: 34548419772     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.072837307     Document Type: Article

References (69)

1. Ahmed, F.R., Rose, D.R., Evans, S.V., Pippy, M.E., and To, R. 1993. Refinement of recombinant oncomodulin at 1.30 Å resolution. J. Mol. Biol. 230: 1216-1224.
2. Babini, E., Bertini, I., Capozzi, F., Del Bianco, C., Hollender, D., Kiss, O.T., Luchinat, C., and Quattrone, A. 2004. Solution structure of human β-parvalbumin and structural comparison with its paralog α-parvalbumin and with their rat orthologs. Biochemistry 43: 16076-16085.
3. Baig, I., Bertini, I., Del Bianco, C., Gupta, Y.K., Lee, Y.-M., Luchinat, C., and Quattrone, A. 2004. Paramagnetism-based refinement strategy for the solution structure of human α-parvalbumin. Biochemistry 43: 5562-5573.
4. Baryshnikova, O.K. and Sykes, B.D. 2006. Backbone dynamics of SDF-1α determined by NMR: Interpretation in the presence of monomer-dimer equilibrium. Protein Sci. 15: 2568-2578.
5. Bax, A. and Ikura, M. 1991. An efficient 3D NMR technique for correlating the proton and 15N backbone amide resonances with the α-carbon of the preceding residue in uniformly 15N/13C enriched proteins. J. Biomol. NMR 1: 99-104.
6. 2+-binding protein parvalbumin: Molecular cloning and developmental regulation of mRNA abundance. Proc. Natl. Acad. Sci. 82: 1414-1418.
7. Berridge, M.J. 2004. Calcium signal transduction and cellular control mechanisms. Biochim. Biophys. Acta 1742: 3-7.
8. Berridge, M.J. 2005. Unlocking the secrets of cell signaling. Annu. Rev. Physiol. 67: 1-21.
9. Berridge, M.J., Bootman, M.D., and Roderick, H.L. 2003. Calcium signalling: Dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4: 517-529.
10. Bottoms, C.A., Schuermann, J.P., Agah, S., Henzl, M.T., and Tanner, J.J. 2004. Crystal structure of rat α-parvalbumin at 1.05 Å resolution. Protein Sci. 13: 1724-1734.
11. Bracken, C., Carr, P.A., Cavanagh, J., and Palmer III, A.G. 1999. Temperature dependence of intramolecular dynamics of the basic leucine zipper of GCN4: Implications for the entropy association with DNA. J. Mol. Biol. 285: 2133-2146.
12. Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. 1998. Crystallography and NMR System: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54: 905-921.
13. Bryce, D.L. and Bax, A. 2004. Application of correlated residual dipolar couplings to the determination of the molecular alignment tensor magnitude of oriented proteins and nucleic acids. J. Biomol. NMR 28: 273-287. Celio, M.R., Pauls, T., and Schwaller, B. 1996. Guidebook to the calcium-binding proteins. Oxford University Press, Oxford, UK.
14. Clayshulte, T.M., Taylor, D.F., and Henzl, M.T. 1990. Reactivity of cysteine 18 in oncomodulin. J. Biol. Chem. 265: 1800-1805.
15. 1H NMR spectroscopy. Biochemistry 29: 7387-7401.
16. Clore, G.M., Szabo, A., Bax, A., Kay, L.E., Driscoll, P.C., and Gronenborn, A.M. 1990b. Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins. J. Am. Chem. Soc. 112: 4989-4991.
17. Cornilescu, G., Delaglio, F., and Bax, A. 1999. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13: 289-302.
18. Cox, J.A., Milos, M., and MacManus, J.P. 1990. Calcium- and magnesium-binding properties of oncomodulin. Direct binding studies and microcalorimetry. J. Biol. Chem. 265: 6633-6637.
19. DeLano, W.L. 2002. The PyMOL molecular graphics system. DeLano Scientific, San Carlos, CA.
20. Dosset, P., Hus, J.-C., Blackledge, M., and Marion, D. 2000. Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data. J. Biomol. NMR 16: 23-28.
21. Fohr, U.G., Weber, B.R., Muntener, M., Staudenmann, W., Hughes, G.J., Frutiger, S., Banville, D., Schafer, B.W., and Heizmann, C.W. 1993. Human α and β parvalbumins. Structure and tissue-specific expression. Eur. J. Biochem. 215: 719-727.
22. Gillen, M.F., Banville, D., Rutledge, R.G., Narang, S., Seligy, V.L., Whitfield, J.F., and MacManus, J.P. 1987. A complete complementary DNA for the oncodevelopmental calcium-binding protein, oncomodulin. J. Biol. Chem. 262: 5308-5312.
23. 1H NMR and optical stopped-flow studies of the effect on the metal binding properties of an Asp59-Glu59 substitution in the calcium-specific site. J. Biol. Chem. 264: 20314-20319.
24. Goodman, M. and Pechere, J.F. 1977. The evolution of muscular parvalbumins investigated by the maximum parsimony method. J. Mol. Evol. 9: 131-158.
25. Grzesiek, S. and 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.
26. Grzesiek, S., Anglister, J., and Bax, A. 1993. Correlation of backbone amide and aliphatic side-chain resonances in 13C/15N-enriched proteins by isotropic mixing of carbon-13 magnetization. J. Magn. Reson. 101: 114-119.
27. Habeck, M., Rieping, W., Linge, J.P., and Nilges, M. 2004. NOE assignment with ARIA 2.0: The nuts and bolts. Methods Mol. Biol. 278: 379-402.
28. Hapak, R.C., Lammers, P.J., Palmisano, W.A., Birnbaum, E.R., and Henzl, M.T. 1989. Site-specific substitution of glutamate for aspartate at position 59 of rat oncomodulin. J. Biol. Chem. 264: 18751-18760.
29. Heizmann, C.W. and Kagi, U. 1989. Structure and function of parvalbumin. Adv. Ex. Med. Biol. 255: 215-222.
30. Henzl, M.T. and Ndubuka, K. 2006. Low-affinity signature of the rat β-parvalbumin CD site. Evidence for remote determinants. Biochemistry 46: 23-35.
31. Henzl, M.T., Shibasaki, O., Comegys, T.H., Thalmann, I., and Thalmann, R. 1997. Oncomodulin is abundant in the organ of Corti. Hear. Res. 106: 105-111.
32. Henzl, M.T., Larson, J.D., and Agah, S. 2000. Influence of monovalent cations on rat α- and β-parvalbumin stabilities. Biochemistry 39: 5859-5867.
33. 15N nuclear magnetic resonance relaxation studies on rat β-parvalbumin and the pentacarboxylate variants, S55D and G98D. Protein Sci. 11: 158-173.
34. Henzl, M.T., Agah, S., and Larson, J.D. 2004a. Association of the AB and CD-EF domains from rat α- and β-parvalbumin. Biochemistry 43: 10906-10917.
35. Henzl, M.T., Larson, J.D., and Agah, S. 2004b. Influence of monovalent cation identity on parvalbumin divalent ion-binding properties. Biochemistry 43: 2747-2763.
36. 15N spectra of larger proteins: Heteronuclear triple-resonance three-dimensional NMR spectroscopy. Application to calmodulin. Biochemistry 29: 4659-4667.
37. Kawasaki, H. and Kretsinger, R.H. 1995. Calcium-binding proteins 1: EF-hands. Protein Profile 2: 297-490.
38. Kay, L.E., Xu, G.Y., Singer, A.U., Muhandiram, D.R., and Forman-Kay, J.D. 1993. A gradient-enhanced HCCH-TOCSY experiment for recording side-chain proton and carbon-13 correlations in water samples of proteins. J. Magn. Reson. B101: 333-337.
39. 2O saturation. J. Magn. Reson. 109: 129-133.
40. Kretsinger, R.H. 1980. Structure and evolution of calcium-modulated proteins. CRC Crit. Rev. Biochem. 8: 119-174.
41. Kretsinger, R.H. and Nockolds, C.E. 1973. Carp muscle calcium-binding protein. II. Structure determination and general description. J. Biol. Chem. 248: 3313-3326.
42. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M. 1993. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26: 283-291.
43. Linge, J.P., O'Donoghue, S.I., and Nilges, M. 2001. Automated assignment of ambiguous nuclear Overhauser effects with ARIA. Methods Enzymol. 339: 71-90.
44. Lipari, G. and Szabo, A. 1982a. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104: 4546-4559.
45. Lipari, G. and Szabo, A. 1982b. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104: 4559-4570.
46. Lohr, F. and Ruterjans, H. 2005. A new triple-resonance experiment for the sequential assignment of backbone resonances in proteins. J. Biomol. NMR 6: 189-197.
47. MacManus, J.P., Watson, D.C., and Yaguchi, M. 1983. The complete amino acid sequence of oncomodulin - A parvalbumin-like calcium-binding protein from Morris hepatoma 5123tc. Eur. J. Biochem. 136: 9-17.
48. Mandel, A.M., Akke, M., and Palmer III, A.G. 1995. Backbone dynamics of Escherichia coli ribonuclease HI: Correlations with structure and function in an active enzyme. J. Mol. Biol. 246: 144-163.
49. 15N Hartmann-Hahn-multiple quantum coherence and nuclear Overhauser-multiple quantum coherence spectroscopy: Application to interleukin 1β. Biochemistry 28: 6150-6156.
50. Marion, D., Kay, L.E., Sparks, S.W., Torchia, D., and Bax, A. 1989b. Three-dimensional heteronuclear NMR of nitrogen-15 labeled proteins. J. Am. Chem. Soc. 111: 1515-1517.
51. McPhalen, C.A., Sielecki, A.R., Santarsiero, B.D., and James, M.N.G. 1994. Refined crystal structure of rat parvalbumin, a mammalian α-lineage parvalbumin, at 2.0 Å resolution. J. Mol. Biol. 235: 718-732.
52. Moncrief, N.D., Kretsinger, R.H., and Goodman, M. 1990. Evolution of EF-hand calcium-modulated proteins. I. Relationships based on amino acid sequences. J. Mol. Evol. 30: 522-562.
53. Muhandiram, D.R. and Kay, L.E. 1994. Gradient-enhanced triple-resonance three-dimensional NMR experiments with improved sensitivity. J. Magn. Reson. 103: 203-216.
54. 13C labeling. Biochemistry 28: 7510-7516.
55. Ottiger, M., Delaglio, F., and Bax, A. 1998. Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J. Magn. Reson. 131: 373-378.
56. Palmisano, W.A., Trevino, C.L., and Henzl, M.T. 1990. Site-specific replacement of amino acid residues within the CD binding loop of rat oncomodulin. J. Biol. Chem. 265: 14450-14456.
57. 2+-binding proteins parvalbumin and oncomodulin and their genes: New structural and functional findings. Biochim. Biophys. Acta 1306: 39-54.
58. 2+-specific site. Eur. J. Biochem. 242: 249-255.
59. Permyakov, E.A., Kalinichenko, L.P., Medvedkin, V.N., Burstein, E.A., and Gerday, C. 1983. Sodium and potassium binding to parvalbumins measured by means of intrinsic protein fluorescence. Biochim. Biophys. Acta 749: 185-191.
60. Sakaguchi, N., Henzl, M.T., Thalmann, I., Thalmann, R., and Schulte, B.A. 1998. Oncomodulin is expressed exclusively by outer hair cells in the organ of Corti. J. Histochem. Cytochem. 46: 29-39.
61. Schurr, J.M., Babcock, H.P., and Fujimoto, B.S. 1994. A test of the model-free formulas. Effects of anisotropic rotational diffusion and dimerization. J. Magn. Reson. B105: 211-224.
62. Strynadka, N.C.J. and James, M.N.G. 1989. Crystal structures of the helix-loop-helix calcium-binding proteins. Annu. Rev. Biochem. 58: 951-998.
63. Tjandra, N., Feller, S.E., Pastor, R.W., and Bax, A. 1995. Rotational diffusion anisotropy of human ubiquitin from 15N NMR relaxation. J. Am. Chem. Soc. 117: 12562-12566.
64. 2+ ion-binding affinity. J. Biol. Chem. 266: 11301-11308.
65. 15N-enriched proteins. J. Am. Chem. Soc. 115: 7772-7777.
66. Wishart, D.S. and Sykes, B.D. 1994. The 13C chemical-shift index: A simple method for the identification of protein secondary structure using 13C chemical-shift data. J. Biomol. NMR 4: 171-180.
67. 13C-labeled proteins via scalar couplings. J. Am. Chem. Soc. 115: 11054-11055.
68. Yin, Y., Henzl, M.T., Lorber, B., Nakazawa, T., Thomas, T.T., Jiang, F., Langer, R., and Benowitz, L.I. 2006. Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells. Nat. Neurosci. 9: 843-852.
69. Zweckstetter, M. and Bax, A. 2000. Prediction of sterically induced alignment in a dilute liquid crystalline phase: Aid to protein structure determination by NMR. J. Am. Chem. Soc. 122: 3791-3792.