New perspectives on s100 proteins: A multi-functional Ca2+-, Zn2+- and Cu2+-binding protein family

BioMetals

Volumn 11, Issue 4, 1998, Pages 383-397

  Heizmann, Claus W ^a   Cox, Jos A ^b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Ca2+; Ca2+ binding S100 proteins; Cu2+; EF hand; Protein structures; Zn2+

Indexed keywords

CALCIUM BINDING PROTEIN; CALCIUM ION; COPPER ION; METALLOPROTEIN; PROTEIN S 100; ZINC ION;

ALLERGY; CANCER; CARBOXY TERMINAL SEQUENCE; CARDIOMYOPATHY; CELLULAR DISTRIBUTION; DEGENERATIVE DISEASE; DIABETES MELLITUS; DIMERIZATION; HUMAN; HYDROPHOBICITY; INFLAMMATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PROCESSING; PROTEIN TERTIARY STRUCTURE; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM; CALCIUM-BINDING PROTEINS; CARRIER PROTEINS; COPPER; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; S100 PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; ZINC; ZINC FINGERS;

EID: 0032453876     PISSN: 09660844     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1009212521172     Document Type: Review

References (104)

1. 2+-binding properties of calgizzarin (S100C) isolated from chicken gizzard smooth muscle. Biochem Cell Biol 74, 687-694.
2. Ames JB, Ishima R, Tanaka T, Gordon JI, Stryer L, Ikura M. 1997 Molecular mechanics of calcium-myristoyl switches. Nature 389, 198-202.
3. Barger SW, Wolchok SR, Van Eldik EL. 1992 Disulfide-linked S100 beta dimers and signal transduction. Biochem Biophys Acta 1160, 105-112.
4. Baudier J, Glasser N, Gerard DJ. 1986 Ion binding to S100 proteins. J Biol Chem 261, 8192-8203.
5. 2+ stimulates disulfide cross-linking between the S100b beta-subunit and the microtubule-associated tau(2) protein. Biochemistry 27, 2728-2738.
6. Baudier J, Delphin C, Grunwald D, Khochbin S, Laurence JJ. 1992 Characterizartion of the tumor suppressor protein p53 as a protein kinase C substrate and a S100B-binding protein. Proc Natl Acad Sci USA 89, 11627-1163.
7. 2+ binding S100 proteins in normal human skin and melanocytic lesions. Br J Dermatol 137, 39-43.
8. 2+-binding proteins S100A6 and S100B in primary cutaneous melanoma. J Cutaneous Pathol 24, 76-80.
9. Brodersen DE, Etzerodt M, Madsen P, et al. 1998 EF-hands at atomic resolution: the structure of human psoriasin (S100A7) solved by MAD phasing. Structure 6, 477-489.
10. Brown DR, Qin K, Herms JW et al. 1997 The cellular prion protein binds copper in vivo. Nature 390, 684-687.
11. Camby I, Nagy N, Lopes M-B et al. 1999 Supratentorial pilocytic astrocytomas, astrocytomas, anaplastic astrocytomas and glioblastomas are characteristized by a differential expression of S100 proteins. Brain Pathol, in press.
12. Chaudhuri D, Horrocks DW, Amburgey JC, Weber DJ. 1997 Characterization of lanthanide ion binding to the EF-hand protein S100β by luminescence spectroscopy. Biochemistry 36, 9674-9680.
13. Clohessy PA, Golden BE. 1996 His-X-X-X-His motif in S100 protein, calprotectin: relation to microbiostatic activity. J Leukocyte Biol 60, 674.
14. Cohen P, Klee CB, eds. 1988 Molecular Aspects of Cellular Regulation. Amsterdam: Elsevier: Vol. 5.
15. Crivici A, Ikura M. 1995 Molecular and structural basis of target recognition by calmodulin. Annu Rev Biophys Biomol Struct 24, 85-116.
16. Donato R, Michetti F, Miani N. 1975 Soluble and membrane-bound S-100 protein in cerebral cortex synaptosomes. Properties of the S-100 receptor. Brain Res 98, 561-573.
17. Donato R. 1982 The specific interaction of S-100 protein with synaptosomal particulate fractions. Modulation of binding by fractional occupancy of sites and by the physical state of membranes. J Neurochem 39, 125-131.
18. Donato R. 1991 Perspectives in S-100 protein biology. Cell Calcium 12, 713-726.
19. Drohat AC, Amburgey JC, Abildgaard F, Starich MR, Baldisseri D, Weber DJ. 1996 Solution structure of rat apo-S100B(ββ) as determined by NMR spectroscopy. Biochemistry 35, 11577-11588.
20. Drohat AC, Nenortas E, Beckett D, Weber DJ. 1997 Oligomerization state of S100B(ββ) at nanomolar concentration determined by large-zone analytical gel filtration chromatography. Protein Sci 6, 1577-1582.
21. Drohat AC, Baldisseri DM, Rustandi RR, Weber DJ. 1998 Solution structure of calcium-bound rat S100b(ββ) as determined by nuclear magnetic resonance spectroscopy. Biochemistry 37, 2729-2740.
22. 2+ site I. Biochim Biophys Acta 1343, 139-143.
23. Edgeworth J, Freemont P, Hogg N. 1989 Ionomycin-regulated phosphorylation of the myeloid calcium-binding protein p14. Nature 342, 189-192.
24. Eide D. 1997 Molecular biology of iron and zinc uptake in eukaryotes. Curr Opin Cell Biol 9, 573-577.
25. Filipek A, Heizmann CW, Kuznicki J. 1990 Calcyclin is a calcium and zinc binding protein. J FEBS Lett 264, 263-266.
26. Finn BE, Evenäs J, Drakenberg T, Waltho JP, Thulin E, Forsén S. 1995 Calcium-induced structural changes and domain autonomy in calmodulin. Nat Struct Biol 2, 777-783.
27. Föhr U, Heizmann CW, Engelkamp D, Schäfer 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.
28. 2+ to human nuclear S100A2 and mutant proteins. J Biol Chem. 273, 18826-18834.
29. Frederickson CJ. 1989 Neurobiology of zinc and zinc-containing neurons. Int Rev Neurobiol 31, 145-238.
30. 2+-binding protein S100A3: spectroscopic investigations of its transition metal ion complexes, and 3-D structural model. Biochem Biophys Acta, in press.
31. Gerke V. 1991 p11, a member of the S-100 protein family, is associated with the tyrosine kinase substrate p36 (annexin II). In: Heizmann CW, ed. Novel Calcium-Binding Proteins. Fundamentals and Clinical Implications. Berlin: Springer-Verlag: 139-155.
32. Glenney JR, Kindy MS, Zokas L. 1989 Isolation of a new member of the S100 protein family: amino acid sequence, tissue, and subcellular distribution. J Cell Biol 108, 569-578.
33. Goebeler M, Roth J, Burwinkel F, Vollmer E, Böcker W, Sorg C. 1994 Expression and complex formation of S100-like proteins MRP8 and MRP14 by macrophages during renal allograft rejection. Transplantation 58, 355-361.
34. Guignard F, Mauel J, Markert M. 1996 Phosporylation of myeloid-related proteins MRP-14 and MRP-8 during human neutrophil activation. Eur J Biochem 241, 265-271.
35. 2+/S100 regulation of giant protein kinases. Nature 380, 636-639.
36. 2+-binding proteins. Eur J Biochem 249, 127-133.
37. Heizmann CW, Hunziker W. 1991 Intracellular calcium-binding proteins: more sites than insights. Trends Biochem Sci 16, 98-103.
38. Heizmann CW, Braun K. 1995 Calcium Regulation by Calcium-Binding Proteins in Neurodegenerative Disorders. Neuroscience Intelligence Unit. New York Berlin: Springer-Verlag and Austin: R.G. Landes Company.
39. Heizmann CW, Braun K. 1997 Neuroprotection by calcium-binding proteins. In: Bär PR, Flint Beal M, eds. Neuroprotection in CS Diseases. New York: Marcel Dekker, Inc: 53-69.
40. Heizmann CW. 1996 Multistep calcium signalling in health and disease. Molec Cells 6, 629-636.
41. Higaki JN, Fletterick RJ, Craik SC 1992 Engineered metalloregulation in enzymes. Trends Biol Sci 17, 100-104.
42. 2+-binding Proteins. Fundamentals and Clinical Implications. Berlin: Springer Verlag: 65-103.
43. 2+-binding S-100 proteins S-100A1, S-100A2, S-100A4, S-100A6 and S-100B in salivary gland tumors. J Oral Pathol Med 25, 547-555.
44. Hunter MJ, Chazin WJ. 1998 High level expression and dimer characterization of the S100 EF-hand proteins, migration inhibitory factor-related proteins 8 and 14. J Biol Chem 273, 12427-12485.
45. Ilg EC, Schäfer BW, Heizmann CW. 1996a Expression pattern of S100 calcium-binding proteins in human tumors. Int J Cancer 68, 325-332.
46. Ilg EC, Troxler H, Bürgisser DM, et al. 1996b Amino acid sequence determination of human S100A12 (P6, calgranulin C, CGRP, CAAF1) by tandem mass spectrometry. Biochem Biophys Res Commun 225, 146-150.
47. Ivanenkov VV, Jamieson GA, Gruenstein E, Dimlich RVW. 1995 Characterization of S-100b binding epitopes. J Biol Chem 270, 14651-14658.
48. Jacob C, Maret W, Vallee BL. (1998) Control of zinc transfer between thionein, metallothionein, and zinc proteins. Proc Natl Acad Sci USA 95, 3489-3494.
49. Jiang L-J, Maret W, Vallee BL. (1998) The glutathione redox couple modulates zinc transfer from metallothionein to zinc-depleted sorbitol dehydrogenase. Proc Natl Acad Sci USA 95, 3483-3488.
50. 9k into a normal EF-hand. Eur J Biochem 202, 1283-1290.
51. 9k's, as determined by NMR, show that the calcum-binding site can adopt different folds. Biochemistry 32, 8429-8438.
52. Johnson WC Jr, Palczewski K, Gorczyca WA, Riazance-Lawrence JH, Witkowska D, Polans AS. 1997 Calcium binding to recoverin: implications for secondary structure and membrane association. Biochim Biophys Acta 1342, 164-174.
53. Johnsson N, Weber K. 1990 Alkylation of cysteine 82 of p11 abolishes the complex formation with the tyrosine-protein kinase substrate p36. J Biol Chem 265, 14464-14468.
54. Kilby PM, Van Eldik LJ, Roberts GCK. 1996 The solution structure of the bovine S100B protein dimer in the calcium-free state. Structure 4, 1041-1052.
55. Kizawa K, Uchiwa H, Murakami U. 1996 Highly-expressed S100A3, a calcium-binding protein, in human hair cuticle. Biochim Biophys Acta 1313, 94-98.
56. 2+-binding proteins MRP8 and MRP14 binds arachidonic acid. FEBS Lett 408, 81-84.
57. Kobe B, Heierhorst J, Feil SC et al. 1996 Giant protein kinases: domain interactions and structural basis of autoregulation. EMBO J 15, 6810-6821.
58. Kocher M, Kenny PA, Farram E, Abdul Majid KB, Finlay-Jones JJ, Geczy CL. 1996 Functional chemotactic factor CP-10 and MRP-14 are abundant in murine abscesses. Infect Immun 64, 1342-1350.
59. Komada T, Araki R, Nakatani K, Yada I, Tanaka T. 1996 Novel specific chemotactic receptor for S100L protein on guinea pig eosinophils. Biochem Biophys Res Commun 220, 871-874.
60. 2+ bind to different sites and induce different conformational changes in human calcyclin. Eur J Biochem 253, 57-66.
61. Krebs J, Quadroni M, Van Eldik LJ. 1995 Dance of the dimers. Nature Struct Biol 2, 711-714.
62. Kriajevska M, Tarabykina S, Bronstein I et al. 1998 Metastasis-associated Mts1 (S100A4) protein modulates protein kinase C phosphorylation of the heavy chain of nonmuscle myosin. J Biol Chem 273, 9852-9856.
63. Kuboniwa H, Tijandra N, Grzesiek S, Ren H, Klee CB, Bax A. 1995 Solution structure of calcium-free calmodulin. Nat Struct Biol 2, 768-776.
64. Landar A, Hall TL, Cornwall EH et al. 1997 The role of cysteine residues in S100B dimerization and regulation of target protein activity. Biochem Biophys Acta 1343, 117-129.
65. Maelandsmo GM, Florenes VA, Mellingsaeter T, Hovig E, Kerbel RS, Fodstad O. 1997 Differential expression patterns of S100A2, S100A4 and S100A6 during progression of human malignant melanoma. Int J Cancer 74, 464-469.
66. Mandinova A, Atar D, Schäfer BW, Spiess M, Aebi U, Heizmann CW. 1998 Distinct subcellular localization of calcium binding S100 proteins in human smooth muscle cells and their relocation in response to rises in intracellular calcium. J Cell Sci 111, 2043-2054.
67. 2+-binding protein from smooth muscle. Biochemistry 29, 1398-1404.
68. Maret W, Vallee BL. 1998 Thiolate ligands in metallothionein confer redox activity on zinc clusters. Proc Natl Acad Sci USA 95, 3478-3482.
69. Matsumura H, Shiba T, Inoue T, Harada S, Kai Y. 1998 A novel mode of target recognition suggested by the 2.0 Å structure of holo S100B from bovine brain. Structure 6, 233-241.
70. Moore BW. 1965 A soluble protein characteristic of the nervous system. Biochem Biophys Res Commun 19, 739-744.
71. Multhaup G, Schlicksupp A, Hesse L, et al. 1996 The amyloid precursor protein of Alzheimer's disease in the reduction of copper(II) to copper(I). Science 271, 1406-1409.
72. Nakatani K, Kawanabe Y, Kato A, Tanaka T. 1996 Interaction of propanolol with S100 proteins of the cardiac muscle. Eur J Pharmacol 315, 335-338.
73. Nishikawa T, Lee ISM, 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.
74. Nonato MC, Garratt RC, Schleicher CH, Santome JA, Oliva G. 1997 Crystallization and preliminary crystallographic studies of calgranulin C, a S100-like calcium-binding protein from pig granulocytes. Acta Cryst D53, 200-202.
75. Oyama Y, Shishibori T, Yamashita K et al. 1997 Two distinct anti-allergic drugs, Amlexanox and Cromolyn, bind to the same kinds of calcium binding proteins, except calmodulin, in bovine lung extract. Biochem Biophys Res Commun 240, 341-347.
76. Pedrocchi M, Schäfer BW, Durussel I, Cox JA, Heizmann CW. 1994 Purification and characterization of the recombinant human calcium-binding S100 proteins CAPL and CACY. Biochemistry 33, 6732-6738.
77. 2+-binding proteins. Nature Struct Biol 2, 790-796.
78. 9k and S100β. Protein Science 5, 2162-2174.
79. Presland RB, Bassuk JA, Kimball JR, Dale BA. 1995 Characterization of two distinct calcium-binding sites in the amino-terminus of human profilaggrin. J Invest Dermatol 104, 218-223.
80. Raftery MJ, Harrison CA, Alewood P, Jones A, Geczy CL. 1996 Isolation of the murine S100 protein MRP14 (14 kDa migration-inhibitory-factor-related protein) from activated spleen cells: characterization of post-translational modifications and zinc binding. Biochem J 316, 285-293.
81. Rammes A, Roth J, Goebeler M, Klempt M, Hartmann M, Sorg C. 1997 Myeloid-related protein (MRP)8 and MRP14, calcium-binding proteins of the S100 family, are secreted by activated monocytes via a novel, tubulin-dependent pathway. J Biol Chem 272, 9496-9502.
82. 2+-binding protein S100A1 in human cardiomyopathy. Biochim Biophys Acta 1313, 253-257.
83. Réty S, Sopkova J, Renouard M et al. 1999 Crystal structure of a complex of p11, the ligand of annexin II, with the annexin N-terminal peptide. Nature Struct Biol, in press.
84. Reyes JG. 1996 Zinc transport in mammalian cells. Am J Physiol 39, C401-C410.
85. Ridinger K, Ilg EC, Niggli FK, Heizmann CW, Schäfer BW. 1998 Clustered organization of S100 genes in human and mouse. Biochem Biophys Acta, in press.
86. Robinson NA, Eckert RL. 1998 Identification of transglutaminase-reactive residues in S100A11. J Biol Chem 273, 2721-2728.
87. 2+-dependent interaction of S100B(ββ) with a peptide derived from p53. Biochemistry 37, 1951-1960.
88. 2+-signal transduction by S100 proteins. Structure 6, 223-231.
89. Schäfer BW, Wicki R, Engelkamp D, Mattei MG, Heizmann CW. 1995 Isolation of a YAC clone covering a cluster of nine S100 genes on human chromosome 1q21: rationale for a new nomenclature of the S100 calcium-binding protein family. Genomics 25, 638-643.
90. Schäfer BW, Heizmann CW. 1996 The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem Sci 21, 134-140.
91. Scotto C, Mély Y, Ohshima H et al. 1998 Cysteine oxidation in the mitogenic S100B protein leads to changes in phosphorylation by catalytic CKII-α subunit. J Biol Chem 273, 3901-3908.
92. Siegenthaler G, Roulin K, Chatelard-Gruaz D et al. 1997 A heterocomplex formed by the calcium-binding proteins MRP8 (S100A8) and MRP14 (S100A9) binds unsaturated fatty acids with high affinity. J Biol Chem 272, 9371-9377.
93. Smith SP, Barber KR, Shaw GS. 1997 Identification and structural influence of a differentially modified N-terminal methionine in human S100b. Protein Sci 6, 1110-1113.
94. Smith SP, Shaw GS. 1998 A novel calcium-sensitive switch revealed by the structure of human S100B in the calcium-bound form. Structure 6, 211-222.
95. Usui A, Kato K, Abe T, Murase M, Tanaka M, Takeuchi E. 1989 S-100ao protein in blood and urine during open-heart surgery. Clin Chem 35, 1942-1944.
96. Weterman MAJ, Wilbrink M, Dijkhuizen T, van den Berg E, van Kessel AG. 1996 Fine mapping of the 1q21 breakpoint of the papillary renal cell carcinoma-associated (X;1) translocation. Hum Genet 98, 16-21.
97. Wicki R, Schäfer BW, Erne P, Heizmann CW. 1996a Characterization of the human and mouse cDNAs coding for S100A13, a new member of the S100 protein family. Biochem Biophys Res Commun 227, 594-599.
98. Wicki R, Marenholz I, Mischke D, Schäfer BW, Heizmann CW. 1996b Characterization of the human S100A12 (calgranulin C, p6, CAAFI, CGRP) gene, a new member of the S100 gene cluster on chromosome 1q21. Cell Calcium 20, 459-464.
99. Wicki R, Franz C, Scholl FA, Heizmann CW, Schäfer BW. 1997 Repression of the candidate tumor suppressor gene S100A2 in breast cancer is mediated by site-specific hypermethylation. Cell Calcium 22, 243-254.
100. 2+-dependent manner. Prot Sci 7, 794-798.
101. Yang Z, de Veer MJ, Gardiner EE et al. 1996 Rabbit polymorphonuclear neutrophils from 35S-labeled S-sulfocalgranulin C when incubated with inorganic [35S]sulfate. J Biol Chem 271, 19802-19809.
102. Yao Y, Yin D, Jas GS et al. 1996 Oxidative modification of a carboxyl-terminal vicinal methionine in calmodulin by hydrogen peroxide inhibits calmodulin-dependent activation of the plasma membrane Ca-ATPase. Biochemistry 35, 2767-2787.
103. 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.
104. Zimmer DB, Chessher J, Wilson GL, Zimmer WE. 1997 S100A1 and S100B expression and target proteins in type I diabetes. Endocrin 138, 5176-5183