A novel calcium-sensitive switch revealed by the structure of human S100B in the calcium-bound form

Structure

Volumn 6, Issue 2, 1998, Pages 211-222

  Smith, Steven P ^a   Shaw, Gary S ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Calcium binding protein; Conformational change; Human S100B; NMR; Solution structure

Indexed keywords

ANIMALIA; BOS TAURUS;

EID: 0032520214     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(98)00022-7     Document Type: Article

References (86)

1. Kretsinger, R.H. & Nockolds, C.E. (1973). Carp muscle calcium-binding protein. II. Structure determination and general description. J. Biol. Chem. 248, 3313-3326.
2. Ikura, M. (1996). Calcium binding and conformational response in EF-hand proteins. Trends Biochem. Sci. 21, 14-17.
3. Gagné, S.M., Tsuda, S., Li, M.X., Chandra, M., Smillie, L.B. & Sykes, B.D. (1994). Quantification of the calcium-induced secondary structural changes in the regulatory domain of troponin-C. Protein Sci. 3, 1961-1974.
4. Gagné, S.M., Tsuda, S., Li, M.X., Smillie, L.B. & Sykes, B.D. (1995). Structures of the troponin C regulatory domains in the apo and calcium-saturated states. Nat. Struct. Biol. 2, 784-789.
5. Finn, B.E., Evenäs, J., Drakenberg, T., Walthro, J.P., Thulin, E. & Forsén, S. (1995). Calcium-induced structural changes and domain autonomy in calmodulin. Nat. Struct. Biol. 2, 777-783.
6. Ikura, M., Clore, G.M., Gronenborn, A.M., Zhu, G., Klee, C.B. & Bax, A. (1992). Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science 256, 632-638.
7. Kuboniwa, H., Tjandra, N., Grzesiek, S., Ren, H., Klee, C.B. & Bax, A. (1995). Solution structure of calcium-free calmodulin. Nat. Struct. Biol. 2, 768-776.
8. Zhang, M. Tanaka, T. & Ikura, M. (1995). Calcium-induced conformational transition revealed by the solution structure of apo calmodulin. Nat. Struct. Biol. 2, 758-767.
9. Zhang, M., Li, M., Wang, J. & Vogel, H.J. (1994). The effect of Met-Leu mutations on calmodulin's ability to activate cyclic nucleotide phosphodiesterase. J. Biol. Chem. 269, 15546-15552.
10. Yuan, T., Mietzner, T.A., Montelaro, R.C. & Vogel, H.J. (1995). Characterization of the calmodulin binding domain of SIV transmembrane glycoprotein by NMR and CD spectroscopy. Biochemistry 36, 10690-10696.
11. Siivari, K., Zhang, M., Palmer,. A.G., III. & Vogel, H.J. (1995). NMR studies of the methionine methyl groups in calmodulin. FEBS Lett. 366, 104-108.
12. Ames, J.B., Tanaka, T., Stryer, L. & Ikura, M. (1996). Portrait of a myristoyl switch protein. Curr. Opin. Struct. Biol. 6, 432-438.
13. Ames, J.B., Ishima, R., Tanaka, T., Gordon, J.I., Stryer, L. & Ikura, M. (1997). Molecular mechanics of calcium-myristol switches. Nature 389, 198-202.
14. Flaherty, K.M., Zozulya, S., Stryer, L. & McKay, D.B. (1993). Three-dimensional structure of recoverin, a calcium sensor. Cell 75, 709-716.
15. 2+-free state. Nature 376, 444-447.
16. Hilt, D.C. & Kligman, D. (1991). The S-100 protein family: a biochemical and functional overview. In Novel Calcium-Binding Proteins. Fundamentals and Clinical Implications. (Heinzmann, C.W., ed.), pp. 65-103, Springer-Verlag, Berlin.
17. Fanò, G., Biocca, S., Fulle, S., Mariggiò, M., Belia, S. & Calissano, P. (1995). The S100: a protein family in search of a function. Prog. Neurobiol. 46, 71-82.
18. Zimmer, D.B., Cornwall, E.H., Landar, A. & Song, W. (1995). The S100 protein family: history, function, and expression. Brain Res. Bulletin. 37, 417-429.
19. Schäfer, B.W. & Heizmann, C.W. (1996). The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem. Sci. 21, 134-140.
20. 9k by NMR spectroscopy. J. Mol. Biol. 249, 441-462.
21. 9k. J. Mol. Biol. 231, 711-734.
22. Kligman, D. & Hilt, D.C. (1988). The S100 protein family. Trends Biochem. Sci. 13, 437-443.
23. Baudier, J., Glasser, N., Haglid, K., & Gerard, D. (1984). Purification, characterization and ion binding properties of human brain S100b protein. Biochem. Biophys. Acta. 790, 164-173.
24. 2+ binding to S100b protein. J. Biol. Chem. 261, 8192-8203.
25. 2+/S100 regulation of giant protein kinases. Nature 380, 636-639.
26. Van Eldik, L.J. & Zimmer, D.B. (1987). Secretion of S-100 from rat C6 glioma cells. Brain Res. 436, 367-370.
27. Marshak, D.R., Pesce, S.A., Stanley, L.C. & Griffin, W.S.T. (1991). Increased S100β neurotrophic activity in Alzheimer's disease temporal lobe. Neurobiol. Aging. 13, 1-7.
28. Van Eldik, L.J. & Griffin, W.S.T. (1994). S100β expression in Alzheimer's disease: relation to neuropathology in brain regions. Biochim. Biophys. Acta. 1223, 398-403.
29. Griffin, W.S.T., et al., & Araoz, C. (1989). Brain interleukin 1 and S100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc. Natl. Acad. Sci. 86, 7611-7615.
30. Donato, R. (1988). Calcium-independent, pH-regulated effects of S-100 proteins on assembly-disassembly of brain microtubule protein in vitro. J. Biol. Chem. 263, 106-110.
31. Donato, R., Giambanco, I. & Aisa, M.C. (1989). Molecular interaction of S-100 proteins with microtubule proteins in vitro. J. Neurochem. 53, 566-571.
32. 2+-dependent manner. J. Biol. Chem. 268, 12669-12674.
33. Sheu, F.-S., Azmitia, E.C., Marshak, D.R., Parker, P.J. & Routtenberg, A. (1994). Glial-derived S100β protein selectively inhibits recombinant β protein kinase C (PKC) phosphorylation of neuron-specific protein F1/GAP43. Mol. Brain Res. 21, 62-66.
34. Sheu, F.-S., Huang, F.L. & Huang, K.-P. (1995). Differential responses of protein kinase C substrates (MARCKS, neuromodulin and neurogranin) phosphorylation to calmodulin and S100. Arch. Biochem. Biophys. 316, 335-342.
35. Lin, L.-H., Van Eldik, L.J., Osheroff, N. & Norden, J.J. (1994). Inhibition of protein kinase C- and casein kinase II-mediated phosphorylation of GAP-43 by S100β. Mol. Brain Res. 25, 297-304.
36. Baudier, J., Mochly-Rosen, D., Newton, A., Lee, S.-H., Koshland, D.E. & Cole, R.D. (1987). Comparison of S100β with calmodulin: interactions of melittin and microtubule-associated proteins and inhibition of phosphorylation of τ proteins by protein kinase C. Biochemistry 26, 2886-2893.
37. 2+-calmodulin-dependent protein kinase II. J. Biol. Chem. 263, 5876-5883.
38. Drohat, A.C., Amburgey, J.C., Abildgaard, F., Starich, M.R., Baldisseri, D. & Weber, D.J. (1996). Solution structure of rat apo-S100B (ββ) as determined by NMR spectroscopy. Biochemistry 35, 11577-11588.
39. Kilby, P.M. Van Eldik, L.J., & Roberts, G.C.K. (1996). The solution structure of the bovine S100B dimer in the calcium-free state. Structure 4, 1041-1052.
40. 2+-binding proteins. Nat. Struct. Biol. 2, 790-796.
41. Mani, R.S., Shelling, J.G., Sykes, B.D. & Kay, C.M. (1983). Spectral studies on the calcium binding properties of bovine brain S-100b protein. Biochemistry 22, 1734-1740.
42. Smith, S.P., Barber, K.R., Dunn, S.D. & Shaw, G.S. (1996). Structural influence of cation binding to recombinant human brain S100b: evidence for calcium-induced exposure of a hydrophobic surface. Biochemistry 35, 8805-8814.
43. Baudier, J. & Gerard, D. (1986). Ions binding to S100 proteins. II. Conformational studies and calcium-induced conformational changes in S100αα protein: the effect of acidic pH and calcium incubation on subunit exchange in S100a (αβ) protein. J. Biol. Chem. 261, 8402-8212.
44. Baudier, J. & Gerard, D. (1983). Ions binding to S100 proteins: structural changes induced by calcium and zinc on S100a and S100b proteins. Biochemistry 22, 3360-3369.
45. Mani, R.J., Boyes, B.E. & Kay, C.M. (1982). Physiochemical and optical studies on calcium- and potassium-induced conformational changes in bovine brain S-100β protein. Biochemistry 21, 2607-2612.
46. Slupsky, C.M., Kay, C.M., Reinach, F.C., Smillie, L.B. & Sykes, B.D. (1995). Calcium-induced dimerization of troponin C: mode of interaction and use of trifluoroethanol as a denaturant of quaternary structure. Biochemistry 34, 7365-7375.
47. Anglister, J., Grzesiek, S., Ren, H., Klee, C.B. & Bax, A. (1994). Isotope-edited multidimensional NMR of calcineurin B in the presence of the non-deuterated detergent CHAPS. J. Biomol. NMR 3, 121-126.
48. Slupsky, C.M. & Sykes, B.D. (1995). The NMR solution structure of calcium-saturated skeletal muscle troponin-C. Biochemistry 34, 15953-15964.
49. Smith, S.P. & Shaw, G.S. (1997). Assignment and secondary structure of calcium-bound human S100B. J. Biomol. NMR 10, 77-88.
50. Smith, S.P., Barber, K.R. & Shaw, G.S. (1997). Identification and structural influence of a differentially modified N-terminal methionine in human S100b. Protein Sci. 6, 1110-1113.
51. 9k. J. Mol. Biol. 227, 1100-1117.
52. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. (1993). PROCHECK: a program to check stereochemical quality of protein structures. J. Appl. Cryst. 26, 283-290.
53. Harris, N.L., Presnell, S.R. & Cohen, F.E. (1994). Four helix bundle diversity in globular proteins. J. Mol. Biol. 236, 1356-1368.
54. Drohat, A.C., Nenortas, E., Beckett, D. & Weber, D.J. (1997). Oligomerization state of S100B at nanomolar concentration determined by large-zone analytical gel filtration chromatography. Protein Sci. 6, 1577-1582.
55. Vijay-Kumar, S. & Cook, W.J. (1992). Structure of a sarcoplasmic calcium-binding protein from Nereis diversicolor refined at 2.0 Å resolution. J. Mol. Biol. 224, 413-426.
56. Skelton, N.J., Kördel, J., Akke, M., Forsén, S. & Chazin, W. (1994). Signal transduction versus buffering activity in calcium-binding proteins. Nat. Struct. Biol. 1, 239-245.
57. Marsden, B.J., Shaw, G.S. & Sykes, B.D. (1989). Calcium binding proteins. Elucidating the contributions to calcium affinity from analysis of species variants and peptide fragments. Biochem. Cell Biol. 68, 587-601.
58. Satyshur, K.A., Rao, S.T., Pyzalska, D., Drendel, W., Greaser, M. & Sundaralingam, M. (1988). Refined structure of chicken skeletal muscle troponin C in the two-calcium state at 2 Å resolution. J. Biol. Chem. 263, 1628-1647.
59. Strynadka, N.C.J. & James, M.N.G. (1989). Crystal structures of the helix-loop-helix calcium-binding proteins. Annu. Rev. Biochem. 58, 951-998.
60. Baudier, J., Labourette, G. & Gerard, D. (1985). Rat brain S100b protein: purification, characterization and ion binding properties. A comparison with bovine S100b protein. J. Neurochem. 44, 76-84.
61. Baudier, J. & Cole, R.D. (1989). The Ca-binding sequence in bovine brain S100b protein β-subunit. Biochem. J. 264, 79-85.
62. Ivanenkov, V.V., Jamieson, G.A., Gruenstein, E. & Dimlich, R.V.W. (1995). Characterization of S-100b binding epitopes: identification of a novel target, the actin capping protein CapZ. J. Biol. Chem. 270, 14651-14658.
63. Kube, E., Becker, T., Weber, K. & Gerke, V. (1992). Protein-protein interaction studied by site-directed mutagenesis: characterization of the annexin II binding site on p11, a member of the S100 protein family. J. Biol. Chem. 267, 14175-14182.
64. Fohr, U.G., Heizmann, C.W., Engelkamp, D., Shäfer, B.W. & Cox, J.A. (1995). Purification and cation binding properties of the recombinant human S100 calcium-binding protein A3, an EF-hand motif protein with high affinity for zinc. J. Biol. Chem. 270, 21056-21061.
65. Dell'Angelica, E.C., Schleicher, C.H. & Santome, J.A. (1994). Primary structure and binding properties of calgranulin C, a novel S100-like calcium-binding protein from pig granulocytes. J. Biol. Chem. 269, 28929-28936.
66. Donato, H., Jr., Mani, R.S. & Kay, C.M. (1991). Spectral studies on the cadmium-ion-binding properties of bovine brain S-100b protein. Biochem. J. 276, 13-18.
67. Kligman, D. & Marshak, D.R. (1985). Purification and characterization of a neurite extension factor from bovine brain. Proc. Natl. Acad. Sci. USA 82, 7136-7139.
68. Winningham-Major, F., Staecker, J.L., Barger, S.W., Coats, S. & Van Eldik, L.J. (1989). Neurite extension and neuronal survival activities of recombinant S100β proteins that differ in the content and positions of cysteine residues. J. Cell Biol. 109, 3063-3071.
69. Barger, S.W., Wolchok, S.R. & Van Eldik, L.J. (1992). Disulfide-linked S100β dimers and signal transduction. Biochim. Biophys. Acta. 1160, 105-112.
70. Teigelkamp, S., Bhardwaj, R.S., Roth, J., Meinardus-Hager, G., Karas, M. & Sorg, C. (1991). Calcium-dependent complex assembly of the myeloic differentiation proteins MRP-8 and MRP-14. J. Biol. Chem. 266, 13462-13467.
71. 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. J. Magn. Reson. Series B 101, 171-180.
72. Grzesiek, S. & Bax, A. (1992). Correlating backbone amide and sidechain resonances in larger proteins by multiple relayed triple resonance NMR. J. Am. Chem. Soc. 114, 6291-6293.
73. 2O saturation. J. Magn. Reson. Series A 109, 129-133.
74. 15N resonance assignments of the N-terminal SH3 domains of drk in the folded and unfolded states using enhanced-sensitivity pulsed field gradient NMR techniques. J. Biolmol. NMR 4, 845-858.
75. 2O samples of proteins. J. Magn. Reson. Series B 101, 333-337.
76. 2O. J. Magn. Reson Series B 103, 197-201.
77. Macura, S. & Ernst, R.R. (1980). Elucidation of cross relaxation in liquids by two-dimensional NMR spectroscopy. Mol. Phys. 41, 95-117.
78. Jeener, J., Meier, B.H., Bachmann, P. & Ernst, R.R. (1979). Investigation of exchange processes by two dimensional NMR spectroscopy. J. Chem. Phys. 71, 4546-4553.
79. Delaglio, F. (1993). NMRPipe System of Software. National Institutes of Health, Bethesda, MD.
80. Garrett, D.S., Powers, R., Gronenborn, A.M. & Clore, G.M. (1991). A common sense approach to peak picking in two-, three-, and four-dimensional spectra using automatic computer analysis of contour diagrams. J. Magn. Reson. 95, 214-220.
81. Kay, L.E., Keifer, P. & Saarinen, T. (1992). Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved Sensitivity. J. Am. Chem. Soc. 114, 10663-10665.
82. α J couplings in calcium-free calmodulin using new 2D and 3D water-flip-back methods. J. Biomol. NMR 4, 871-878.
83. 15N-enriched proteins. J. Am. Chem. Soc. 115, 7772-7777.
84. Gagné, S.M., Li, M.X. & Sykes, B.D. (1997). Mechanism of direct coupling between binding and induced structural change in regulatory calcium binding proteins. Biochemistry 36, 4386-4392.
85. Brünger, A.T. (1992). X-PLOR version 3.1: A System for X-ray Crystallography and NMR. Columbia University Press. New Haven, CT.
86. Nicholls, A. (1992). GRASP: Graphical Representation and Analysis of Surface Properties. Yale University Press, New York, NY.