The role of zinc in the S100 proteins: Insights from the X-ray structures

Amino Acids

Volumn 41, Issue 4, 2011, Pages 761-772

  Moroz, Olga V ^a   Wilson, Keith S ^a   Bronstein, Igor B ^b  

^a UNIVERSITY OF YORK   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Extracellular signalling; Keywords S100 proteins; X ray structure; Zinc; Zinc binding site

Indexed keywords

ASPARTIC ACID; CALCIUM; CALGRANULIN A; CALVASCULIN; COPPER; CYSTEINE; HISTIDINE; PROTEIN S 100; PROTEIN S 100A1; PROTEIN S 100A12; PROTEIN S 100A15; PROTEIN S 100A2; PROTEIN S 100A3; PROTEIN S 100A5; PROTEIN S 100A6; PROTEIN S 100A9; PROTEIN S100B; PSORIASIN; UNCLASSIFIED DRUG; ZINC; ZINC BINDING PROTEIN;

BINDING SITE; CALCIUM CELL LEVEL; ENZYME REGULATION; EXTRACELLULAR SPACE; HUMAN; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; X RAY;

AMINO ACID SEQUENCE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; EF HAND MOTIFS; HISTIDINE; MOLECULAR SEQUENCE DATA; S100 PROTEINS; ZINC;

EID: 80855153128     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-010-0540-4     Document Type: Review

References (70)

1. 2+ enhancement of the S100B binding epitope TRTK-12. J Biol Chem 274:1502-1508
2. 2+/calmodulin-dependent protein kinase II. J Biol Chem 263:5876-5883
3. Baudier J, Holtzscherer C, Gerard D (1982) Zinc-dependent affinity chromatography of the S100b protein on phenyl-Sepharose. A rapid purification method. FEBS Lett 148:231-234
4. Baudier J, Glasser N, Haglid K, Gerard D (1984) Purification, characterization and ion binding properties of human brain S100b protein. Biochim Biophys Acta 790:164-173
5. 2+ binding on S100b protein. J Biol Chem 261:8192-8203
6. Bhattacharya S, Bunick CG, Chazin WJ (2004) Target selectivity in EF-hand calcium binding proteins. Biochim Biophys Acta 1742:69-79
7. Bjork P et al (2009) Identification of human S100A9 as a novel target for treatment of autoimmune disease via binding to quinoline-3- carboxamides. PLoS Biol 7:e97
8. Blindauer CA et al (2009) Structure, properties, and engineering of the major zinc binding site on human albumin. J Biol Chem 284:23116-23124
9. Botelho HM, Koch M, Fritz G, Gomes CM (2009) Metal ions modulate the folding and stability of the tumor suppressor protein S100A2. FEBS J 276:1776-1786
10. Bozym RA, Thompson RB, Stoddard AK, Fierke CA (2006) Measuring picomolar intracellular exchangeable zinc in PC-12 cells using a ratiometric fluorescence biosensor. ACS Chem Biol 1:103-111
11. Brand IA, Kleineke J (1996) Intracellular zinc movement and its effect on the carbohydrate metabolism of isolated rat hepatocytes. J Biol Chem 271:1941-1949
12. 2+-free states. Biochemistry 38:1695-1704
13. Castagnetto JM, Hennessy SW, Roberts VA, Getzoff ED, Tainer JA, Pique ME (2002) MDB: the metalloprotein database and browser at The Scripps Research Institute. Nucleic Acids Res 30:379-382
14. Charpentier TH et al (2008) Divalent metal ion complexes of S100B in the absence and presence of pentamidine. J Mol Biol 382:56-73
15. Collaborative Computational Project 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50:760-763
16. Dell'Angelica EC, Schleicher CH, Santome JA (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
17. Deloulme JC, Assard N, Mbele GO, Mangin C, Kuwano R, Baudier J (2000) S100A6 and S100A11 are specific targets of the calciumand zinc-binding S100B protein in vivo. J Biol Chem 275:35302-35310
18. Fohr UG, Heizmann CW, Engelkamp D, Schafer BW, Cox JA (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
19. Frederickson CJ, Koh JY, Bush AI (2005) The neurobiology of zinc in health and disease. Nat Rev Neurosci 6:449-462
20. 2+-binding protein S100A3: spectroscopic investigations of its transition metal ion complexes, and three-dimensional structural model. Biochim Biophys Acta 1448:264-276
21. Fritz G, Mittl PR, Vasak M, Grutter MG, Heizmann CW (2002) The crystal structure of metal-free human EF-hand protein S100A3 at 1.7-A resolution. J Biol Chem 277:33092-33098
22. 2+ homeostasis regulation by S100B. J Biol Chem 276:23253-23261
23. 2+ channels by zinc. J Biol Chem 279:11106-11111
24. 2+/S100 regulation of giant protein kinases. Nature 380:636-639
25. 2+/S100A1- interacting proteins. Biochem J 344(Pt 2):577-583
26. 2+ and regulates ion transport. Proc Natl Acad Sci USA 98:11749-11754
27. Ketterman JK, Li YV (2008) Presynaptic evidence for zinc release at the mossy fiber synapse of rat hippocampus. J Neurosci Res 86:422-434
28. (2+) signaling in neurons induced by the S100A4 protein. Mol Cell Biol 26:3625-3638
29. Klingelhofer J et al (2007) Up-regulation of metastasis-promoting S100A4 (Mts-1) in rheumatoid arthritis: putative involvement in the pathogenesis of rheumatoid arthritis. Arthritis Rheum 56:779-789
30. Koch M et al (2007) Implications on zinc binding to S100A2. Biochim Biophys Acta 1773:457-470
31. 2+ bind to different sites and induce different conformational changes in human calcyclin. Eur J Biochem 253:57-66
32. Korndorfer IP, Brueckner F, Skerra A (2007) The crystal structure of the human (S100A8/S100A9)2 heterotetramer, calprotectin, illustrates how conformational changes of interacting alphahelices can determine specific association of two EF-hand proteins. J Mol Biol 370:887-898
33. Kraemer AM, Saraiva LR, Korsching SI (2008) Structural and functional diversification in the teleost S100 family of calciumbinding proteins. BMC Evol Biol 8:48
34. Krezel A, Maret W (2008) Thionein/metallothionein control Zn(II) availability and the activity of enzymes. J Biol Inorg Chem 13:401-409
35. Landriscina M et al (2001) Copper induces the assembly of a multiprotein aggregate implicated in the release of fibroblast growth factor 1 in response to stress. J Biol Chem 276:25549-25557
36. 2+ binding properties of the alpha-subunit of bovine brain S-100a protein. FEBS Lett 214:35-40
37. (2+)- calcyclin. J Mol Biol 317:279-290
38. Marenholz I, Heizmann CW, Fritz G (2004) S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem Biophys Res Commun 322:1111-1122
39. Marenholz I, Lovering RC, Heizmann CW (2006) An update of the S100 nomenclature. Biochim Biophys Acta 1763:1282-1283
40. Maret W (2009) Molecular aspects of human cellular zinc homeostasis: redox control of zinc potentials and zinc signals. Biometals 22:149-157
41. Maret W, Li Y (2009) Coordination dynamics of zinc in proteins. Chem Rev 109:4684-4707
42. Markowitz J et al (2004) Identification and characterization of small molecule inhibitors of the calcium-dependent S100B-p53 tumor suppressor interaction. J Med Chem 47:5085-5093
43. Marti T, Erttmann KD, Gallin MY (1996) Host-parasite interaction in human onchocerciasis: identification and sequence analysis of a novel human calgranulin. Biochem Biophys Res Commun 221:454-458
44. Mbele GO et al (2002) The zinc- and calcium-binding S100B interacts and co-localizes with IQGAP1 during dynamic rearrangement of cell membranes. J Biol Chem 277:49998-50007
45. Moroz OV et al (2003) Structure of the human S100A12-copper complex: implications for host-parasite defence. Acta Crystallogr D Biol Crystallogr 59:859-867
46. Moroz OV, Blagova EV, Wilkinson AJ, Wilson KS, Bronstein IB (2009a) The crystal structures of human S100A12 in apo form and in complex with zinc: new insights into S100A12 oligomerisation. J Mol Biol 391:536-551
47. 2+ are essential for S100A12 protein oligomerization and function. BMC Biochem 10:11
48. Murakami M, Hirano T (2008) Intracellular zinc homeostasis and zinc signaling. Cancer Sci 99:1515-1522
49. Nakatani Y, Yamazaki M, Chazin WJ, Yui S (2005) Regulation of S100A8/A9 (calprotectin) binding to tumor cells by zinc ion and its implication for apoptosis-inducing activity. Mediators Inflamm 2005:280-292
50. Nishikawa T, Lee IS, Shiraishi N, Ishikawa T, Ohta Y, Nishikimi M (1997) Identification of S100b protein as copper-binding protein and its suppression of copper-induced cell damage. J Biol Chem 272:23037-23041
51. Novitskaya V et al (2000) Oligomeric forms of the metastasis-related Mts1 (S100A4) protein stimulate neuronal differentiation in cultures of rat hippocampal neurons. J Biol Chem 275:41278-41286
52. Oslejskova L, Grigorian M, Gay S, Neidhart M, Senolt L (2008) The metastasis associated protein S100A4: a potential novel link to inflammation and consequent aggressive behaviour of rheumatoid arthritis synovial fibroblasts. Ann Rheum Dis 67:1499-1504
53. Ostendorp T et al (2007) Structural and functional insights into RAGE activation by multimeric S100B. EMBO J 26:3868-3878
54. (2+)-bound states: the calcium sensor mechanism of S100 proteins revealed at atomic resolution. Structure 10:557-567
55. Potterton L et al (2004) Developments in the CCP4 moleculargraphics project. Acta Crystallogr D Biol Crystallogr 60:2288-2294
56. Ravasi T et al (2004) Probing the S100 protein family through genomic and functional analysis. Genomics 84:10-22
57. Santamaria-Kisiel L, Rintala-Dempsey AC, Shaw GS (2006) Calcium- dependent and -independent interactions of the S100 protein family. Biochem J 396:201-214
58. Schäfer BW et al (2000) Brain S100A5 is a novel calcium-, zinc-, and copper ion-binding protein of the EF-hand superfamily. J Biol Chem 275:30623-30630
59. Schaub MC, Heizmann CW (2008) Calcium, troponin, calmodulin, S100 proteins: from myocardial basics to new therapeutic strategies. Biochem Biophys Res Commun 369:247-264
60. Taccioli C et al (2009) Zinc replenishment reverses overexpression of the proinflammatory mediator S100A8 and esophageal preneoplasia in the rat. Gastroenterology 136:953-966
61. Vogl T, Leukert N, Barczyk K, Strupat K, Roth J (2006) Biophysical characterization of S100A8 and S100A9 in the absence and presence of bivalent cations. Biochim Biophys Acta 1763:1298-1306
62. Vogt K, Mellor J, Tong G, Nicoll R (2000) The actions of synaptically released zinc at hippocampal mossy fiber synapses. Neuron 26:187-196
63. Vorum H et al (1996) Expression and divalent cation binding properties of the novel chemotactic inflammatory protein psoriasin. Electrophoresis 17:1787-1796
64. (2+)-binding site on S100B as determined by NMR spectroscopy and site-directed mutagenesis. Biochemistry 42:13410-13421
65. Wolf R et al (2008) Chemotactic activity of S100A7 (Psoriasin) is mediated by the receptor for advanced glycation end products and potentiates inflammation with highly homologous but functionally distinct S100A15. J Immunol 181:1499-1506
66. Xie J, Burz DS, He W, Bronstein IB, Lednev I, 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
67. Yamasaki S et al (2007) Zinc is a novel intracellular second messenger. J Cell Biol 177:637-645
68. Yanamandra K et al (2009) Amyloid formation by the pro-inflammatory S100A8/A9 proteins in the ageing prostate. PLoS One 4:e5562
69. Yousefi R, Imani M, Ardestani SK, Saboury AA, Gheibi N, Ranjbar B (2007) Human calprotectin: effect of calcium and zinc on its secondary and tertiary structures, and role of pH in its thermal stability. Acta Biochim Biophys Sin (Shanghai) 39:795-802
70. Yu WH, Fraser PE (2001) S100beta interaction with tau is promoted by zinc and inhibited by hyperphosphorylation in Alzheimer's disease. J Neurosci 21:2240-2246