Identification of calcium-independent and calcium-enhanced binding between S100B and the dopamine D2 receptor

Biochemistry

Volumn 50, Issue 42, 2011, Pages 9056-9065

  Dempsey, Brian R ^a   Shaw, Gary S ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PARTNERS; CALCIUM BINDING; CALCIUM CONCENTRATION; COMPLEX FORMATIONS; CONFORMATIONAL CHANGE; EF-HAND; IN-VIVO; INTERACTING SITES; NMR TITRATION; OPTIMAL INTERACTIONS; PEPTIDE ARRAYS; PROTEIN-BINDING; STRUCTURAL COMPONENT; THIRD INTRACELLULAR LOOPS; TWO-HYBRID SCREENS;

BACTERIOLOGY; BRAIN; EXPERIMENTS; PROTEINS;

CALCIUM;

CALCIUM ION; DOPAMINE 2 RECEPTOR; PROTEIN S100B;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CALCIUM BINDING; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING;

APOPROTEINS; CALCIUM; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; INTRACELLULAR SPACE; NERVE GROWTH FACTORS; PROTEIN ARRAY ANALYSIS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; RECEPTORS, DOPAMINE D2; S100 PROTEINS; TWO-HYBRID SYSTEM TECHNIQUES; UP-REGULATION;

BACTERIA (MICROORGANISMS);

EID: 80054983537     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201054x     Document Type: Article

References (67)

1. Baudier, J. and Gerard, D. (1986) Ions binding to S100 proteins. II. Conformational studies and calcium-induced conformational changes in S100 alpha alpha protein: the effect of acidic pH and calcium incubation on subunit exchange in S100a (alpha beta) protein J. Biol. Chem. 261, 8204-8212 (Pubitemid 17202689)
2. 2+-S100B as examined by NMR and X-ray crystallography J. Mol. Biol. 396, 1227-1243
3. Markowitz, J., Rustandi, R. R., Varney, K. M., Wilder, P. T., Udan, R., Wu, S. L., Horrocks, W. D., and Weber, D. J. (2005) Calcium-binding properties of wild-type and EF-hand mutants of S100B in the presence and absence of a peptide derived from the C-terminal negative regulatory domain of p53 Biochemistry 44, 7305-7314 (Pubitemid 40656674)
4. Garbuglia, M., Verzini, M., and Donato, R. (1998) 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, 177-191 (Pubitemid 28552188)
5. Baudier, J., Delphin, C., Grunwald, D., Khochbin, S., and Lawrence, J. J. (1992) Characterization of the tumor suppressor protein p53 as a protein kinase C substrate and a S100b-binding protein Proc. Natl. Acad. Sci. U. S. A. 89, 11627-11631
6. Huttunen, H. J., Kuja-Panula, J., Sorci, G., Agneletti, A. L., Donato, R., and Rauvala, H. (2000) Coregulation of neurite outgrowth and cell survival by amphoterin and S100 proteins through receptor for advanced glycation end products (RAGE) activation J. Biol. Chem. 275, 40096-40105 (Pubitemid 32064635)
7. Millward, T. A., Heizmann, C. W., Schafer, B. W., and Hemmings, B. A. (1998) Calcium regulation of Ndr protein kinase mediated by S100 calcium- binding proteins EMBO J. 17, 5913-5922 (Pubitemid 28474786)
8. Kleindienst, A., Hesse, F., Bullock, M. R., and Buchfelder, M. (2007) The neurotrophic protein S100B: value as a marker of brain damage and possible therapeutic implications Prog. Brain Res. 161, 317-325 (Pubitemid 47017412)
9. Rothermundt, M., Ponath, G., and Arolt, V. (2004) S100B in schizophrenic psychosis Int. Rev. Neurobiol. 59, 445-470 (Pubitemid 39752424)
10. Sen, J. and Belli, A. (2007) S100B in neuropathologic states: the CRP of the brain? J. Neurosci. Res. 85, 1373-1380 (Pubitemid 46724380)
11. Enjalbert, A. and Bockaert, J. (1983) Pharmacological characterization of the D2 dopamine receptor negatively coupled with adenylate cyclase in rat anterior pituitary Mol. Pharmacol. 23, 576-584 (Pubitemid 13089773)
12. Einhorn, L. C., Gregerson, K. A., and Oxford, G. S. (1991) D2 dopamine receptor activation of potassium channels in identified rat lactotrophs: whole-cell and single-channel recording J. Neurosci. 11, 3727-3737
13. Lledo, P. M., Legendre, P., Israel, J. M., and Vincent, J. D. (1990) Dopamine inhibits two characterized voltage-dependent calcium currents in identified rat lactotroph cells Endocrinology 127, 990-1001 (Pubitemid 20277574)
14. Lukasiewicz, S., Faron-Gorecka, A., Dobrucki, J., Polit, A., and Dziedzicka-Wasylewska, M. (2009) Studies on the role of the receptor protein motifs possibly involved in electrostatic interactions on the dopamine D1 and D2 receptor oligomerization FEBS J. 276, 760-775
15. Bofill-Cardona, E., Kudlacek, O., Yang, Q., Ahorn, H., Freissmuth, M., and Nanoff, C. (2000) Binding of calmodulin to the D2-dopamine receptor reduces receptor signaling by arresting the G protein activation switch J. Biol. Chem. 275, 32672-32680
16. Rustandi, R. R., Baldisseri, D. M., and Weber, D. J. (2000) Structure of the negative regulatory domain of p53 bound to S100B(ββ) Nat. Struct. Biol. 7, 570-574 (Pubitemid 30445914)
17. Bhattacharya, S., Large, E., Heizmann, C. W., Hemmings, B., and Chazin, W. J. (2003) Structure of the Ca2+/S100B/NDR kinase peptide complex: insights into S100 target specificity and activation of the kinase Biochemistry 42, 14416-14426 (Pubitemid 37531986)
18. Ivanenkov, V. V., Jamieson, G. A., Jr., Gruenstein, E., and 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
19. 2+ enhancement of the S100B binding epitope TRTK-12 J. Biol. Chem. 274, 1502-1508
20. 2+ binding protein S100B: role in D2 receptor function Mol. Pharmacol. 74, 371-378
21. Deloulme, J. C., Gentil, B. J., and Baudier, J. (2003) Monitoring of S100 homodimerization and heterodimeric interactions by the yeast two-hybrid system Microsc. Res. Tech. 60, 560-568
22. 2+ in E. coli Biochimie 81, 901-907 (Pubitemid 29520617)
23. 2+ level rises with repellents and falls with attractants in Escherichia coli chemotaxis Proc. Natl. Acad. Sci. U. S. A. 92, 10777-10781 (Pubitemid 3009166)
24. 2+ binding on S100b protein J. Biol. Chem. 261, 8192-8203 (Pubitemid 17202688)
25. Borle, A. B. and Snowdowne, K. W. (1986) Measurement of intracellular ionized calcium with aequorin Methods Enzymol. 124, 90-116 (Pubitemid 16074970)
26. Rescher, U. and Gerke, V. (2008) S100A10/p11: family, friends and functions Pflugers Arch. 455, 575-582 (Pubitemid 350160469)
27. Svenningsson, P., Chergui, K., Rachleff, I., Flajolet, M., Zhang, X., El Yacoubi, M., Vaugeois, J. M., Nomikos, G. G., and Greengard, P. (2006) Alterations in 5-HT1B receptor function by p11 in depression-like states Science 311, 77-80 (Pubitemid 43063061)
28. Smith, S. P., Barber, K. R., Dunn, S. D., and 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 (Pubitemid 26243721)
29. 2+-S100B-TRTK-12 complex J. Biol. Chem. 278, 6251-6257 (Pubitemid 36800881)
30. Deber, C. M., Wang, C., Liu, L. P., Prior, A. S., Agrawal, S., Muskat, B. L., and Cuticchia, A. J. (2001) TM Finder: a prediction program for transmembrane protein segments using a combination of hydrophobicity and nonpolar phase helicity scales Protein Sci. 10, 212-219 (Pubitemid 32221178)
31. Frank, R. and Overwin, H. (1996) SPOT synthesis. Epitope analysis with arrays of synthetic peptides prepared on cellulose membranes Methods Mol. Biol. 66, 149-169
32. Frank, R. (2002) The SPOT-synthesis technique. Synthetic peptide arrays on membrane supports - principles and applications J. Immunol. Methods 267, 13-26 (Pubitemid 34804809)
33. Baryshnikova, O. K., Williams, T. C., and Sykes, B. D. (2008) Internal pH indicators for biomolecular NMR J. Biomol. NMR 41, 5-7
34. Kay, L. E., Keifer, P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity J. Am. Chem. Soc. 114, 10663-10665
35. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-293
36. Johnson, B. A. (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules Methods Mol. Biol. 278, 313-352
37. Shuker, S. B., Hajduk, P. L., Meadows, R. P., and Fesik, S. W. (1996) Discovering high-affinity ligands for proteins:SAR by NMR Science 274, 1531-1534 (Pubitemid 26403929)
38. Chien, E. Y., Liu, W., Zhao, Q., Katritch, V., Han, G. W., Hanson, M. A., Shi, L., Newman, A. H., Javitch, J. A., Cherezov, V., and Stevens, R. C. (2010) Structure of the human dopamine D3 receptor in complex with a D2/D3 selective antagonist Science 330, 1091-1095
39. Baudier, J., Mochly-Rosen, D., Newton, A., Lee, S. H., Koshland, D. E., Jr., and Cole, R. D. (1987) Comparison of S100b protein with calmodulin: interactions with melittin and microtubule-associated tau proteins and inhibition of phosphorylation of tau proteins by protein kinase C Biochemistry 26, 2886-2893 (Pubitemid 17084661)
40. Weiser, A. A., Or-Guil, M., Tapia, V., Leichsenring, A., Schuchhardt, J., Frommel, C., and Volkmer-Engert, R. (2005) SPOT synthesis: reliability of array-based measurement of peptide binding affinity Anal. Biochem. 342, 300-311 (Pubitemid 40884580)
41. Smith, S. P. and Shaw, G. S. (1997) Assignment and secondary structure of calcium-bound human S100B J. Biomol. NMR 10, 77-88 (Pubitemid 127508020)
42. Lee, Y. T., Dimitrova, Y. N., Schneider, G., Ridenour, W. B., Bhattacharya, S., Soss, S. E., Caprioli, R. M., Filipek, A., and Chazin, W. J. (2008) Structure of the S100A6 complex with a fragment from the C-terminal domain of Siah-1 interacting protein: a novel mode for S100 protein target recognition Biochemistry 47, 10921-10932
43. V1.5 J. Mol. Biol. 406, 106-119
44. Houdusse, A., Gaucher, J. F., Krementsova, E., Mui, S., Trybus, K. M., and Cohen, C. (2006) Crystal structure of apo-calmodulin bound to the first two IQ motifs of myosin V reveals essential recognition features Proc. Natl. Acad. Sci. U. S. A. 103, 19326-19331 (Pubitemid 46026031)
45. Rety, S., Sopkova, J., Renouard, M., Osterloh, D., Gerke, V., Tabaries, S., Russo-Marie, F., and Lewit-Bentley, A. (1999) The crystal structure of a complex of p11 with the annexin II N-terminal peptide Nat. Struct. Biol. 6, 89-95 (Pubitemid 29232429)
46. Inman, K. G., Yang, R., Rustandi, R. R., Miller, K. E., Baldisseri, D. M., and Weber, D. J. (2002) Solution NMR structure of S100B bound to the high-affinity target peptide TRTK-12 J. Mol. Biol. 324, 1003-1014 (Pubitemid 41782989)
47. McClintock, K. A. and Shaw, G. S. (2000) A logical sequence search for S100B target proteins Protein Sci. 9, 2043-2046
48. Li, Z. H., Spektor, A., Varlamova, O., and Bresnick, A. R. (2003) Mts1 regulates the assembly of nonmuscle myosin-IIA Biochemistry 42, 14258-14266 (Pubitemid 37499423)
49. Gribenko, A. V., Guzman-Casado, M., Lopez, M. M., and Makhatadze, G. I. (2002) Conformational and thermodynamic properties of peptide binding to the human S100P protein Protein Sci. 11, 1367-1375 (Pubitemid 34547208)
50. Xie, J., Burz, D. S., He, W., Bronstein, I. B., Lednev, I., and Shekhtman, A. (2007) Hexameric calgranulin C (S100A12) binds to the receptor for advanced glycated end products (RAGE) using symmetric hydrophobic target-binding patches J. Biol. Chem. 282, 4218-4231 (Pubitemid 47084493)
51. van Dieck, J., Teufel, D. P., Jaulent, A. M., Fernandez-Fernandez, M. R., Rutherford, T. J., Wyslouch-Cieszynska, A., and Fersht, A. R. (2009) Posttranslational modifications affect the interaction of S100 proteins with tumor suppressor p53 J. Mol. Biol. 394, 922-930
52. Rhoads, A. R. and Friedberg, F. (1997) Sequence motifs for calmodulin recognition FASEB J. 11, 331-340 (Pubitemid 27193937)
53. Cui, Y., Wen, J., Hung Sze, K., Man, D., Lin, D., Liu, M., and Zhu, G. (2003) Interaction between calcium-free calmodulin and IQ motif of neurogranin studied by nuclear magnetic resonance spectroscopy Anal. Biochem. 315, 175-182 (Pubitemid 36407491)
54. Dickerson, J. B., Morgan, M. A., Mishra, A., Slaughter, C. A., Morgan, J. I., and Zheng, J. (2006) The influence of phosphorylation on the activity and structure of the neuronal IQ motif protein, PEP-19 Brain Res. 1092, 16-27 (Pubitemid 43902738)
55. Shah, V. N., Wingo, T. L., Weiss, K. L., Williams, C. K., Balser, J. R., and Chazin, W. J. (2006) Calcium-dependent regulation of the voltage-gated sodium channel hH1: intrinsic and extrinsic sensors use a common molecular switch Proc. Natl. Acad. Sci. U. S. A. 103, 3592-3597 (Pubitemid 43376600)
56. McClintock, K. A., Van Eldik, L. J., and Shaw, G. S. (2002) The C-terminus and linker region of S100B exert dual control on protein-protein interactions with TRTK-12 Biochemistry 41, 5421-5428 (Pubitemid 34429376)
57. Kursula, P., Tikkanen, G., Lehto, V. P., Nishikimi, M., and Heape, A. M. (1999) Calcium-dependent interaction between the large myelin-associated glycoprotein and S100beta J. Neurochem. 73, 1724-1732 (Pubitemid 29440177)
58. Margulis, A., Pozdnyakov, N., and Sitaramayya, A. (1996) Activation of bovine photoreceptor guanylate cyclase by S100 proteins Biochem. Biophys. Res. Commun. 218, 243-247 (Pubitemid 26034519)
59. Girard, C., Tinel, N., Terrenoire, C., Romey, G., Lazdunski, M., and Borsotto, M. (2002) p11, an annexin II subunit, an auxiliary protein associated with the background K+ channel, TASK-1 EMBO J. 21, 4439-4448 (Pubitemid 34984331)
60. Renigunta, V., Yuan, H., Zuzarte, M., Rinne, S., Koch, A., Wischmeyer, E., Schlichthorl, G., Gao, Y., Karschin, A., Jacob, R., Schwappach, B., Daut, J., and Preisig-Muller, R. (2006) The retention factor p11 confers an endoplasmic reticulum-localization signal to the potassium channel TASK-1 Traffic 7, 168-181
61. Huang, Y., Laval, S. H., van Remoortere, A., Baudier, J., Benaud, C., Anderson, L. V., Straub, V., Deelder, A., Frants, R. R., den Dunnen, J. T., Bushby, K., and van der Maarel, S. M. (2007) AHNAK, a novel component of the dysferlin protein complex, redistributes to the cytoplasm with dysferlin during skeletal muscle regeneration FASEB J. 21, 732-742 (Pubitemid 46348249)
62. Lennon, N. J., Kho, A., Bacskai, B. J., Perlmutter, S. L., Hyman, B. T., and Brown, R. H., Jr. (2003) Dysferlin interacts with annexins A1 and A2 and mediates sarcolemmal wound-healing J. Biol. Chem. 278, 50466-50473 (Pubitemid 37548892)
63. Wright, N. T., Cannon, B. R., Wilder, P. T., Morgan, M. T., Varney, K. M., Zimmer, D. B., and Weber, D. J. (2009) Solution structure of S100A1 bound to the CapZ peptide (TRTK12) J. Mol. Biol. 386, 1265-1277
64. Dukhanina, E. A., Dukhanin, A. S., Lomonosov, M. Y., Lukanidin, E. M., and Georgiev, G. P. (1997) Spectral studies on the calcium-binding properties of Mts1 protein and its interaction with target protein FEBS Lett. 410, 403-406 (Pubitemid 27304105)
65. Mons, N. and Cooper, D. M. (1994) Selective expression of one Ca(2+)-inhibitable adenylyl cyclase in dopaminergically innervated rat brain regions Brain Res. Mol. Brain Res. 22, 236-244
66. Cooper, D. M., Mons, N., and Karpen, J. W. (1995) Adenylyl cyclases and the interaction between calcium and cAMP signalling Nature 374, 421-424
67. Malik, S., Revington, M., Smith, S. P., and Shaw, G. S. (2008) Analysis of the structure of human apo-S100B at low temperature indicates a unimodal conformational distribution is adopted by calcium-free S100 proteins Proteins 73, 28-42