Identification of a Dimeric Intermediate in the Unfolding Pathway for the Calcium-Binding Protein S100B

Journal of Molecular Biology

Volumn 382, Issue 4, 2008, Pages 1075-1088

  Shaw, Gary S ^a   Marlatt, Nicole M ^a   Ferguson, Peter L ^a   Barber, Kathryn R ^a   Bottomley, Stephen P ^b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b MONASH UNIVERSITY   (Australia)

Author keywords

calcium binding; chemical denaturation; fluorescence; NMR spectroscopy

Indexed keywords

4,4 DIANILINO 1,1' BINAPHTHYL 5,5' DISULFONIC ACID; CALCIUM BINDING PROTEIN; CYTOSKELETON PROTEIN; GUANIDINE; PROTEIN S100B; SULFONIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM BINDING; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIMERIZATION; FLUORESCENCE; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS;

EID: 51249083442     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.07.083     Document Type: Article

References (83)

1. Santamaria-Kisiel L., Rintala-Dempsey A.C., and Shaw G.S. Calcium-dependent and-independent interactions of the S100 protein family. Biochem. J. 396 (2006) 201-214
2. Heizmann C.W., Fritz G., and Schafer B.W. S100 proteins: structure, functions and pathology. Front. Biosci. 7 (2002) d1356-d1368
3. Drohat A.C., Baldisseri D.M., Rustandi R.R., and Weber D.J. Solution structure of calcium-bound rat S100B(betabeta) as determined by nuclear magnetic resonance spectroscopy. Biochemistry 37 (1998) 2729-2740
4. Smith S.P., and Shaw G.S. A change-in-hand mechanism for S100 Signalling. Biochem. Cell. Biol. 76 (1998) 324-333
5. Smith S.P., and Shaw G.S. A novel calcium-sensitive switch revealed by the structure of human S100B in the calcium-bound form. Structure 6 (1998) 211-222
6. Sorci G., Agneletti A.L., and Donato R. Effects of S100A1 and S100B on microtubule stability. An in vitro study using triton-cytoskeletons from astrocyte and myoblast cell lines. Neurosci. 99 (2000) 773-783
7. Frizzo J.K., Tramontina A.C., Tramontina F., Gottfried C., Leal R.B., Donato R., and Goncalves C.A. Involvement of the S100B in cAMP-induced cytoskeleton remodeling in astrocytes: a study using TRTK-12 in digitonin-permeabilized cells. Cell Mol. Neurobiol. 24 (2004) 833-840
8. Garbuglia M., Verzini M., Dimlich R.V.W., Jamieson Jr. G.A., and Donato R. Characterization of type III intermediate filament regulatory protein target epitopes: S100 (b and/or a) binds the N-terminal head domain; annexin II2-p112 binds rod domain. Biochim. Biophys. Acta 1313 (1996) 268-276
9. Garbuglia M., Verzini M., and Donato R. Annexin VI binds S100A1 and S100B and blocks the ability of S100A1 and S100B to inhibit desmin and GFAP assemblies into intermediate filaments. Cell Calcium 24 (1998) 177-191
10. Frizzo J.K., Tramontina F., Bortoli E., Gottfried C., Leal R.B., Lengyel I., et al. S100B-mediated inhibition of the phosphorylation of GFAP is prevented by TRTK-12. Neurochem. Res. 29 (2004) 735-740
11. Bichsel S.J., Tamaskovic R., Stegert M.R., and Hemmings B.A. Mechanism of activation of NDR (nuclear Dbf2-related) protein kinase by the hMOB1 protein. J. Biol. Chem. 279 (2004) 35228-35235
12. Lin L.-H., Van Eldik L.J., Osheroff N., and Norden J.J. Inhibition of protein kinase C- and casein kinase II-mediated phosphorylation of GAP-43 by S100β. Mol. Brain Res. 25 (1994) 297-304
13. 2+/calmodulin-dependent protein kinase II. J. Biol. Chem. 263 (1988) 5876-5883
14. Kilby P.M., Van Eldik L.J., and Roberts G.C. The solution structure of the bovine S100B protein dimer in the calcium-free state. Structure 4 (1996) 1041-1052
15. Drohat A.C., Tjandra N., Baldisseri D.M., and Weber D.J. The use of dipolar couplings for determining the solution structure of rat apo-S100B(ββ). Protein Sci. 8 (1999) 800-809
16. Malik, S., Revington, M., Smith, S. P. & Shaw, G. S. Analysis of the structure of human apo-S100B at low temperature indicates a unimodal conformational distribution is adopted by calcium-free S100 proteins. Proteins: Struct. Funct. Bioinf. In press. doi:10.1002/prot.22037.
17. Matsumura H., Shiba T., Inoue T., Harada S., and Kai Y. A novel mode of target recognition suggested by the 2.0 Å structure of holo S100B from bovine brain. Structure 6 (1998) 233-241
18. Ferguson P.L., and Shaw G.S. Role of the N-terminal Helix I for dimerization and stability of the calcium-binding protein S100B. Biochemistry 41 (2002) 3637-3646
19. Tsalkova T.N., and Privalov P.L. Stability of troponin C. Biochim. Biophys. Acta 624 (1980) 196-204
20. Mercier P., Spyracopoulos L., and Sykes B.D. Structure, dynamics, and thermodynamics of the structural domain of troponin C in complex with the regulatory peptide 1-40 of troponin I. Biochemistry 40 (2001) 10063-10077
21. Gagne S.M., Tsuda S., Spyrocopoulos L., Kay L.E., and Sykes B.D. 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 (1998) 667-686
22. Spyracopoulos L., Lavigne P., Crump M.P., Gagne S.M., Kay C.M., and Sykes B.D. Temperature dependence of dynamics and thermodynamics of the regulatory domain of human cardiac troponin C. Biochemistry 40 (2001) 12541-12551
23. 9k. J. Mol. Biol. 227 (1992) 1100-1117
24. 15N NMR spectroscopy. Biochemistry 31 (1992) 4856-4866
25. 1H NMR. Biochemistry 29 (1990) 5925-5934
26. 15N NMR relaxation. Biochemistry 32 (1993) 9832-9844
27. Marlatt N.M., and Shaw G.S. Amide exchange shows calcium-induced conformational changes are transmitted to the dimer interface of S100B. Biochemistry 46 (2007) 7478-7487
28. Aitio H., Laakso T., Pihlajamaa T., Torkkeli M., Kilpelainen I., Drakenberg T., et al. Characterization of apo and partially saturated states of calerythrin, an EF-hand protein from S. erythraea: a molten globule when deprived of Ca(2+). Protein Sci. 10 (2001) 74-82
29. Yamniuk A.P., Silver D.M., Anderson K.L., Martin S.R., and Vogel H.J. Domain stability and metal-induced folding of calcium- and integrin-binding protein 1. Biochemistry 46 (2007) 7088-7098
30. 2+-calmodulin reveals flexible hand-like properties of its domains. Nat. Struct. Biol. 8 (2001) 990-997
31. Evenas J., Malmendal A., and Akke M. Dynamics of the transition between open and closed conformations in a calmodulin C-terminal domain mutant. Structure 9 (2001) 185-195
32. Yokouchi T., Izumi Y., Matsufuji T., Jinbo Y., and Yoshino H. Unfolding intermediate of a multidomain protein, calmodulin, in urea as revealed by small-angle X-ray scattering. FEBS Lett. 551 (2003) 119-122
33. Ramos C.H., Lima Jr. M.V., Silva S.L., Borin P.F., Regis W.C., and Santoro M.M. Stability and folding studies of the N-domain of troponin C. Evidence for the formation of an intermediate. Arch. Biochem. Biophys. 427 (2004) 135-142
34. Pan J., Rintala-Dempsey A.C., Li Y., Shaw G.S., and Konermann L. Folding kinetics of the S100A11 protein dimer studied by time-resolved electrospray mass spectrometry and pulsed hydrogen-deuterium exchange. Biochemistry 45 (2006) 3005-3013
35. Yang Q., O'Hanlon D., Heizmann C.W., and Marks A. Demonstration of heterodimer formation between S100B and S100A6 in the yeast two-hybrid system and human melanoma. Exp. Cell Res. 246 (1999) 501-509
36. Deloulme J.C., Assard N., Mbele G.O., Mangin C., Kuwano R., and Baudier J. S100A6 and S100A11 are specific targets of the calcium- and zinc-binding S100B protein in vivo. J. Biol. Chem. 275 (2000) 35302-35310
37. Deloulme J.C., Gentil B.J., and Baudier J. Monitoring of S100 homodimerization and heterodimeric interactions by the yeast two-hybrid system. Microsc. Res. Tech. 60 (2003) 560-568
38. 2+-binding protein S100P. J. Mol. Biol. 325 (2003) 785-794
39. Tarabykina S., Scott D.J., Herzyk P., Hill T.J., Tame J.R., Kriajevska M., et al. The dimerization interface of the metastasis-associated protein S100A4 (Mts1): in vivo and in vitro studies. J. Biol. Chem. 276 (2001) 24212-24222
40. Drohat A.C., Nenortas E., Beckett D., and Weber D.J. Oligomerization state of S100B at nanomolar concentration determined by large-zone analytical gel filtration chromatography. Protein Sci. 6 (1997) 1577-1582
41. Maler L., Potts B.C., and Chazin W.J. High resolution solution structure of apo calcyclin and structural variations in the S100 family of calcium-binding proteins. J. Biomol. NMR 13 (1999) 233-247
42. 2+-binding proteins. Nat. Struct. Biol. 2 (1995) 790-796
43. Otterbein L.R., Kordowska J., Witte-Hoffmann C., Wang C.L., and Dominguez R. Crystal structures of S100A6 in the Ca(2+)-free and Ca(2+)-bound states: the calcium sensor mechanism of S100 proteins revealed at atomic resolution. Structure (Camb) 10 (2002) 557-567
44. Fritz G., Mittl P.R.E., Vasak M., Grutters M.G., and Heizmann C.W. The crystal structure of metal-free human EF-hand protein S100A3 at 1.7-Å resolution. J. Biol. Chem. 277 (2002) 33092-33098
45. Lee Y.C., Volk D.E., Thiviyanathan V., Kleerekoper Q., Gribenko A.V., Zhang S., et al. NMR structure of the Apo-S100P protein. J. Biomol. NMR 29 (2004) 399-402
46. Chen Y., and Barkley M.D. Toward understanding tryptophan fluorescence in proteins. Biochemistry 37 (1998) 9976-9982
47. Spudich G., and Marqusee S. A change in the apparent m value reveals a populated intermediate under equilibrium conditions in Escherichia coli ribonuclease HI. Biochemistry 39 (2000) 11677-11683
48. Soulages J.L. Chemical denaturation: potential impact of undetected intermediates in the free energy of unfolding and m-values obtained from a two-state assumption. Biophys. J. 75 (1998) 484-492
49. Mallam A.L., and Jackson S.E. Folding studies on a knotted protein. J. Mol. Biol. 346 (2005) 1409-1421
50. Hobart S.A., Meinhold D.W., Osuna R., and Colon W. From two-state to three-state: the effect of the P61A mutation on the dynamics and stability of the factor for inversion stimulation results in an altered equilibrium denaturation mechanism. Biochemistry 41 (2002) 13744-13754
51. Horton N., and Lewis M. Calculation of the free energy of association for protein complexes. Protein Sci. 1 (1992) 169-181
52. Karplus P.A. Hydrophobicity regained. Protein Sci. 6 (1997) 1302-1307
53. Yamniuk A.P., Nguyen L.T., Hoang T.T., and Vogel H.J. Metal ion binding properties and conformational states of calcium- and integrin-binding protein. Biochemistry 43 (2004) 2558-2568
54. Ames J.B., Dizhoor A.M., Ikura M., Palczewski K., and Stryer L. Three-dimensional structure of guanylyl cyclase activating protein-2, a calcium-sensitive modulator of photoreceptor guanylyl cyclases. J. Biol. Chem. 274 (1999) 19329-19337
55. Gagne S.M., Tsuda S., Li M.X., Smillie L.B., and Sykes B.D. Structures of the troponin C regulatory domains in the apo and calcium-saturated states. Nat. Struct. Biol. 2 (1995) 784-789
56. Ikura M., Clore G.M., Gronenborn A.M., Zhu G., Klee C.B., and Bax A. Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science 256 (1992) 632-638
57. Weljie A.M., and Vogel H.J. Tryptophan fluorescence of calmodulin binding domain peptides interacting with calmodulin containing unnatural methionine analogues. Protein Eng. 13 (2000) 59-66
58. Yuan T., Ouyang H., and Vogel H.J. Surface exposure of the methionine side chain of calmodulin in solution. J. Biol. Chem. 274 (1999) 8411-8520
59. 1H NMR structural evidence. Science 249 (1990) 280-283
60. Lakowski T.M., Lee G.M., Lelj-Garolla B., Okon M., Reid R.E., and McIntosh L.P. Peptide binding by a fragment of calmodulin composed of EF-hands 2 and 3. Biochemistry 46 (2007) 8525-8536
61. Lakowski T.M., Lee G.M., Okon M., Reid R.E., and McIntosh L.P. Calcium-induced folding of a fragment of calmodulin composed of EF-hands 2 and 3. Protein Sci. 16 (2007) 1119-1132
62. 9k: stability, calcium binding and NMR studies. Protein Sci. 2 (1993) 985-1000
63. Baudier J., Haglid K., Haiech J., and Gerard D. Zinc ion binding to human brain calcium binding proteins, calmodulin and s100b protein. Biochem. Biophys. Res. Commun. 114 (1983) 1138-1146
64. Baudier J., and Gerard D. Ions binding to S100 proteins: structural changes induced by calcium and zinc on s100a and s100b proteins. Biochemistry 22 (1983) 3360-3369
65. 2+-signal transduction by S100 proteins. Structure 6 (1998) 223-231
66. Smith S.P., and Shaw G.S. Assignment and secondary structure of calcium-bound human S100B. J. Biomol. NMR 10 (1997) 77-88
67. Kuznetsova I.M., Stepanenko O.V., Turoverov K.K., Zhu L., Zhou J.M., Fink A.L., and Uversky V.N. Unraveling multistate unfolding of rabbit muscle creatine kinase. Biochim. Biophys. Acta 1596 (2002) 138-155
68. Shao X., Hensley P., and Matthews C.R. Construction and characterization of monomeric tryptophan repressor: a model for an early intermediate in the folding of a dimeric protein. Biochemistry 36 (1997) 9941-9949
69. Gloss L.M., and Matthews C.R. Urea and thermal equilibrium denaturation studies on the dimerization domain of Escherichia coli Trp repressor. Biochemistry 36 (1997) 5612-5623
70. Mann C.J., and Matthews C.R. Structure and stability of an early folding intermediate of Escherichia coli trp aporepressor measured by far-UV stopped-flow circular dichroism and 8-anilino-1-naphthalene sulfonate binding. Biochemistry 32 (1993) 5282-5290
71. Ke H., Zhang S., Li J., Howlett G.J., and Wang C.C. Folding of Escherichia coli DsbC: characterization of a monomeric folding intermediate. Biochemistry 45 (2006) 15100-15110
72. Doyle S.M., Braswell E.H., and Teschke C.M. SecA folds via a dimeric intermediate. Biochemistry 39 (2000) 11667-11676
73. Grimsley J.K., Scholtz J.M., Pace C.N., and Wild J.R. Organophosphorus hydrolase is a remarkably stable enzyme that unfolds through a homodimeric intermediate. Biochemistry 36 (1997) 14366-14374
74. Chanez-Cardenas M.E., Fernandez-Velasco D.A., Vazquez-Contreras E., Coria R., Saab-Rincon G., and Perez-Montfort R. Unfolding of triosephosphate isomerase from Trypanosoma brucei: identification of intermediates and insight into the denaturation pathway using tryptophan mutants. Arch. Biochem. Biophys. 399 (2002) 117-129
75. Chanez-Cardenas M.E., Perez-Hernandez G., Sanchez-Rebollar B.G., Costas M., and Vazquez-Contreras E. Reversible equilibrium unfolding of triosephosphate isomerase from Trypanosoma cruzi in guanidinium hydrochloride involves stable dimeric and monomeric intermediates. Biochemistry 44 (2005) 10883-10892
76. Louzada P.R., Sebollela A., Scaramello M.E., and Ferreira S.T. Predissociated dimers and molten globule monomers in the equilibrium unfolding of yeast glutathione reductase. Biophys. J. 85 (2003) 3255-3261
77. Smith S.P., Barber K.R., Dunn S.D., and Shaw G.S. Structural influence of cation binding to recombinant human brain S100b: evidence for calcium-induced exposure of a hydrophobic surface. Biochemistry 35 (1996) 8805-8814
78. Santoro M.M., and Bolen D.W. Unfolding free energy changes determined by the linear extrapolation method.1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry 27 (1988) 8063-8068
79. Reece L.J., Nichols R., Ogden R.C., and Howell E.E. Construction of a synthetic gene for an R-plasmid-encoded dihydrofolate reductase and studies on the role of the N-terminus in the protein. Biochemistry 30 (1991) 10895-10904
80. Kay L.E., Keifer P., and Saarinen T. Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114 (1992) 10663-10665
81. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (1995) 277-293
82. Johnson B.A., and Belvins R.A. NMRView: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4 (1994) 603-614
83. Altieri A.S., Hinton D.P., and Byrd R.A. Association of biomolecular systems via pulsed field gradient NMR self-diffusion measurements. J. Am. Chem. Soc. 117 (1995) 7566-7567