Prediction of EF-hand calcium-binding proteins and analysis of bacterial EF-hand proteins

Proteins: Structure, Function and Genetics

Volumn 65, Issue 3, 2006, Pages 643-655

  Zhou, Yubin ^a   Yang, Wei ^a   Kirberger, Michael ^a   Lee, Hsiau Wei ^a   Ayalasomayajula, Gayatri ^a   Yang, Jenny J ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Bacterial genomes; EF hand; Evolution; Pattern search; Prediction; S100

Indexed keywords

BACTERIAL PROTEIN; CALCIUM BINDING PROTEIN; CALCIUM ION; CALCYCLIN; CALVASCULIN; HELIX LOOP HELIX PROTEIN; HORNERIN; PROTEIN S 100; PROTEIN S100A1; PROTEIN S100A10; PROTEIN S100A11; PROTEIN S100A11P; PROTEIN S100A12; PROTEIN S100A13; PROTEIN S100A14; PROTEIN S100A15; PROTEIN S100A16; PROTEIN S100A17; PROTEIN S100A2; PROTEIN S100A3; PROTEIN S100A5; PROTEIN S100A8; PROTEIN S100A9; PROTEIN S100B; PROTEIN S100G; PROTEIN S100H; PROTEIN S100P; PROTEIN S100Z; PSORIASIN; UNCLASSIFIED DRUG; UNINDEXED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENOME; CALCIUM BINDING; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; GENOMICS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN STRUCTURE; SENSITIVITY AND SPECIFICITY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; CALCIUM-BINDING PROTEINS; EF HAND MOTIFS; EVOLUTION, MOLECULAR; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ALIGNMENT;

BACTERIA (MICROORGANISMS);

EID: 33750046332     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21139     Document Type: Article

References (97)

1. Carafoli E. Calcium signaling: a tale for all seasons. Proc Natl Acad Sci USA 2002;99:1115-1122.
2. Ermak G, Davies KJ. Calcium and oxidative stress: from cell signaling to cell death. Mol Immunol 2002;38:713-721.
3. Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 2003;4:552-565.
4. Dowd DR. Calcium regulation of apoptosis. Adv Second Messenger Phosphoprotein Res 1995;30:255-280.
5. Means AR, Rasmussen CD. Calcium, calmodulin and cell proliferation. Cell Calcium 1988;9:313-319.
6. Tsien RW, Tsien RY. Calcium channels, stores, and oscillations. Annu Rev Cell Biol 1990;6:715-760.
7. Levine BA, Dalgarno DC, Esnouf MP, Klevit RE, Scott GM, Williams RJ. The mobility of calcium-trigger proteins and its function. Ciba Found Symp 1983;93:72-97.
8. 2+ ions in pig duodenal enterocytes. J Physiol 1996;492(Part 3):715-722.
9. Buchanan JD, Corbett RJ, Roche RS. The thermodynamics of calcium binding to thermolysin. Biophys Chem 1986;23:183-199.
10. Henikoff S, Greene EA, Pietrokovski S, Bork P, Attwood TK, Hood L. Gene families: the taxonomy of protein paralogs and chimeras. Science 1997;278:609-614.
11. Kawasaki H, Nakayama S, Kretsinger RH. Classification and evolution of EF-hand proteins. Biometals 1998;11:277-295.
12. Kretsinger RH, Nockolds CE. Carp muscle calcium-binding protein. II. Structure determination and general description. J Biol Chem 1973;248:3313-3326.
13. Ravasi T, Hsu K, Goyette J, Schroder K, Yang Z, Rahimi F, Miranda LP, Alewood PF, Hume DA, Geczy C. Probing the S100 protein family through genomic and functional analysis. Genomics 2004;84:10-22.
14. Schuster-Bockler B, Schultz J, Rahmann S. HMM Logos for visualization of protein families. BMC Bioinformatics 2004;5:7.
15. Pal GP, Elce JS, Jia Z. Dissociation and aggregation of calpain in the presence of calcium. J Biol Chem 2001;276:47233-47238.
16. Raser KJ, Buroker-Kilgore M, Wang KK. Binding and aggregation of human mu-calpain by terbium ion. Biochim Biophys Acta 1996;1292:9-14.
17. Ravulapalli R, Diaz BG, Campbell RL, Davies PL. Homodimerization of calpain 3 penta-EF-hand domain. Biochem J 2005;388(Part 2): 585-591.
18. Hunter MJ, Chazin WJ. High level expression and dimer characterization of the S100 EF-hand proteins, migration inhibitory factor-related proteins 8 and 14. J Biol Chem 1998;273:12427-12435.
19. Yap KL, Ames JB, Swindells MB, Ikura M. Diversity of conformational states and changes within the EF-hand protein superfamily. Proteins 1999;37:499-507.
20. Rigden DJ, Jedrzejas MJ, Galperin MY. An extracellular calcium-binding domain in bacteria with a distant relationship to EF-hands. FEMS Microbiol Lett 2003;221:103-110.
21. Rigden DJ, Jedrzejas MJ, Moroz OV, Galperin MY. Structural diversity of calcium-binding proteins in bacteria: single-handed EF-hands? Trends Microbiol 2003;11:295-297.
22. Vyas NK, Vyas MN, Quiocho FA. A novel calcium binding site in the galactose-binding protein of bacterial transport and chemotaxis. Nature 1987;327:635-638.
23. 2+ in bacteria: a role for EF-hand proteins? Trends Microbiol 2002;10:87-93.
24. Rigden DJ, Galperin MY. The DxDxDG motif for calcium binding: multiple structural contexts and implications for evolution. J Mol Biol 2004;343:971-984.
25. Yang K. Prokaryotic calmodulins: recent developments and evolutionary implications. J Mol Microbiol Biotechnol 2001;3:457-459.
26. Momma K, Mikami B, Mishima Y, Hashimoto W, Murata K. Crystal structure of AlgQ2, a macromolecule (alginate)-binding protein of Sphingomonas sp. A1 at 2.0A resolution. J Mol Biol 2002; 316:1051-1059.
27. Petosa C, Collier RJ, Klimpel KR, Leppla SH, Liddington RC. Crystal structure of the anthrax toxin protective antigen. Nature 1997;385:833-838.
28. Lytle BL, Volkman BF, Westler WM, Heckman MP, Wu JH. Solution structure of a type I dockerin domain, a novel prokaryotic, extracellular calcium-binding domain. J Mol Biol 2001;307: 745-753.
29. Ye Y, Shealy S, Lee HW, Torshin I, Harrison R, Yang JJ. A grafting approach to obtain site-specific metal-binding properties of EF-hand proteins. Protein Eng 2003;16:429-434.
30. Ye Y, Lee HW, Yang W, Shealy S, Yang JJ. Probing site-specific calmodulin calcium and lanthanide affinity by grafting. J Am Chem Soc 2005;127:3743-3750.
31. Ye Y, Lee HW, Yang W, Yang JJ. Calcium and lanthanide affinity of the EF-loops from the C-terminal domain of calmodulin. J Inorg Biochem 2005;99:1376-1383.
32. ++-binding by EF-hand proteins. J Mol Microbiol Biotechnol 1999;1:175-182.
33. Dragani B, Aceto A. About the role of conserved amino acid residues in the calcium-binding site of proteins. Arch Biochem Biophys 1999;368:211-213.
34. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994;22:4673-4680.
35. Page RD. TreeView. an application to display phylogenetic trees on personal computers. Comput Appl Biosci 1996;12:357, 358.
36. Eddy SR. Profile hidden markov models. Bioinformatics 1998;14: 755-763.
37. Krieg P, Schuppler M, Koesters R, Mincheva A, Lichter P, Marks F. Repetin (Rptn), a new member of the "fused gene" subgroup within the S100 gene family encoding a murine epidermal differentiation protein. Genomics 1997;43:339-348.
38. Makino T, Takaishi M, Morohashi M, Huh NH. Hornerin, a novel profilaggrin-like protein and differentiation-specific marker isolated from mouse skin. J Biol Chem 2001;276:47445-47452.
39. Huber M, Siegenthaler G, Mirancea N, Marenholz I, Nizetic D, Breitkreutz D, Mischke D, Hohl D. Isolation and characterization of human repetin, a member of the fused gene family of the epidermal differentiation complex. J Invest Dermatol 2005;124:998-1007.
40. Lee SC, Kim IG, Marekov LN, O'Keefe EJ, Parry DA, Steinert PM. The structure of human trichohyalin. Potential multiple roles as a functional EF-hand-like calcium-binding protein, a cornified cell envelope precursor, and an intermediate filament-associated (cross-linking) protein. J Biol Chem 1993;268:12164-12176.
41. Donato R. Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim Biophys Acta 1999;1450: 191-231.
42. Donato R. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol 2001;33:637-668.
43. 2+-binding protein family. Biometals 1998;11:383-397.
44. Tanaka T, Miwa N, Kawamura S, Sohma H, Nitta K, Matsushima N. Molecular modeling of single polypeptide chain of calcium-binding protein p26olf from dimeric S100B(ββ). Protein Eng 1999; 12:395-405.
45. Miwa N, Kobayashi M, Takamatsu K, Kawamura S. Purification and molecular cloning of a novel calcium-binding protein, p26olf, in the frog olfactory epithelium. Biochem Biophys Res Commun 1998;251:860-867.
46. Leung AK, Duewel HS, Hohek JF, Berghuis AM. Crystal structure of the lytic transglycosylase from bacteriophage lambda in complex with hexa-N-acetylchitohexaose. Biochemistry 2001;40: 5665-5673.
47. van Asselt EJ, Dijkstra BW. Binding of calcium in the EF-hand of Escherichia coli lytic transglycosylase Slt35 is important for stability. FEBS Lett 1999;458:429-435.
48. Wu CH, Yeh LS, Huang H, Arminski L, Castro-Alvear J, Chen Y, Hu Z, Kourtesis P, Ledley RS, Suzek BE, Vinayaka CR, Zhang J, Barker WC. The protein information resource. Nucleic Acids Res 2003;31:345-347.
49. Aitio H, Annila A, Heikkinen S, Thulin E, Drakenberg T, Kilpelainen I. NMR assignments, secondary structure, and global fold of calerythrin, an EF-hand calcium-binding protein from Saccharopolyspora erythraea. Protein Sci 1999;8:2580-2588.
50. Gangola P, Rosen BP. Maintenance of intracellular calcium in Escherichia coli. J Biol Chem 1987;262:12570-12574.
51. Herbaud ML, Guiseppi A, Denizot F, Haiech J, Kilhoffer MC. Calcium signalling in Bacillus subtilis. Biochim Biophys Acta 1998;1448:212-226.
52. Kalckar HM. The periplasmic galactose receptor protein of Escherichia coli in relation to galactose chemotaxis. Biochimie 1976;58: 81-85.
53. Tisa LS, Adler J. Calcium ions are involved in Escherichia coli chemotaxis. Proc Natl Acad Sci USA 1992;89:11804-11808.
54. Carvalho AL, Dias FM, Prates JA, Nagy T, Gilbert HJ, Davies GJ, Ferreira LM, Romao MJ, Fontes CM. Cellulosome assembly revealed by the crystal structure of the cohesin-dockerin complex. Proc Natl Acad Sci USA 2003;100:13809-13814.
55. Lin J, Ficht TA. Protein synthesis in Brucella abortus induced during macrophage infection. Infect Immun 1995;63:1409-1414.
56. Teixeira-Gomes AP, Cloeckaert A, Zygmunt MS. Characterization of heat, oxidative, and acid stress responses in Brucella melitensis. Infect Immun 2000;68:2954-2961.
57. Leadly PF, Roberts G, Walker JE. Isolation of a novel calcium-binding protein from Streptomyces erythreus. FEBS Lett 1984;178: 157-160.
58. Natsume M, Yasui K, Marumo S. Calcium ion regulates aerial mycelium formation in actinomycetes. J Antibiot (Tokyo) 1989;42: 440-447.
59. Tossavainen H, Permi P, Annila A, Kilpelainen I, Drakenberg T. NMR solution structure of calerythrin, an EF-hand calcium-binding protein from Saccharopolyspora erythraea. Eur J Biochem 2003;270:2505-2512.
60. Yonekawa T, Ohnishi Y, Horinouchi S. A calmodulin-like protein in the bacterial genus Streptomyces. FEMS Microbiol Lett 2005; 244:315-321.
61. Xi C, Schoeters E, Vanderleyden J, Michiels J. Symbiosis-specific expression of Rhizobium etli casA encoding a secreted calmodulin-related protein. Proc Natl Acad Sci USA 2000;97:11114-11119.
62. Spurway TD, Morland C, Cooper A, Sumner I, Hazlewood GP, O'Donnell AG, Pickersgill RW, Gilbert HJ. Calcium protects a mesophilic xylanase from proteinase inactivation and thermal unfolding. J Biol Chem. 1997;272:17523- 17530.
63. Chen L, Liu MY, Le Gall J. Calcium is required for the reduction of sulfite from hydrogen in a reconstituted electron transfer chain from the sulfate reducing bacterium, Desulfovibrio gigas. Biochem Biophys Res Commun 1991;180:238-242.
64. Lytle BL, Volkman BF, Westler WM, Wu JH. Secondary structure and calcium-induced folding of the Clostridium thermocellum dockerin domain determined by NMR spectroscopy. Arch Biochem Biophys 2000;379:237-244.
65. Kohler U, Cerff R, Brinkmann H. Transaldolase genes from the cyanobacteria Anabaena variabilis and Synechocystis sp. PCC 6803: comparison with other eubacterial and eukaryotic homologues. Plant Mol Biol 1996;30:213-218.
66. Laarmann S, Schmidt MA The Escherichia coli AIDA autotransporter adhesin recognizes an integral membrane glycoprotein as receptor. Microbiology 2003;149(Part 7):1871-1882.
67. Dean M, Allikmets R. Evolution of ATP-binding cassette transporter genes. Curr Opin Genet Dev 1995;5:779-785.
68. Higgins CF. ABC transporters: from microorganisms to man. Annu Rev Cell Biol 1992;8:67-113.
69. van Veen HW, Konings WN. Multidrug transporters from bacteria to man: similarities in structure and function. Semin Cancer Biol 1997;8:183-191.
70. 3+ siderophore transporter from gram-positive pathogenic bacteria. Genome Biol 2002;3:research0047.1.
71. Bates CS, Montanez GE, Woods CR, Vincent RM, Eichenbaum Z. Identification and characterization of a Streptococcus pyogenes operon involved in binding of hemoproteins and acquisition of iron. Infect Immun 2003;71:1042-1055.
72. Day IS, Reddy VS, Shad Ali G, Reddy AS. Analysis of EF-hand-containing proteins in Arabidopsis. Genome Biol 2002;3: research0056.1.
73. Julenius K, Robblee J, Thulin E, Finn BE, Fairman R, Linse S. Coupling of ligand binding and dimerization of helix-loop-helix peptides: spectroscopic and sedimentation analyses of calbindin D9k EF-hands. Proteins 2002;47:323-333.
74. Kawasaki H, Kretsinger RH. Calcium-binding proteins 1: EF-hands. Protein Profile 1995;2:297-490.
75. Lee HW, Yang W, Ye Y, Liu ZR, Glushka J, Yang JJ. Isolated EF-loop III of calmodulin in a scaffold protein remains unpaired in solution using pulsed-field-gradient NMR spectroscopy. Biochim Biophys Acta 2002;1598:80-87.
76. Franchini PL, Reid RE. A model for circular dichroism monitored dimerization and calcium binding in an EF-hand synthetic peptide. J Theor Biol 1999;199:199-211.
77. Berggard T, Julenius K, Ogard A, Drakenberg T, Linse S. Fragment complementation studies of protein stabilization by hydrophobic core residues. Biochemistry 2001;40:1257-1264.
78. Wojcik J, Goral J, Pawlowski K, Bierzynski A. Isolated calcium-binding loops of EF-hand proteins can dimerize to form a native-like structure. Biochemistry 1997;36:680-687.
79. Berggard T, Thulin E, Akerfeldt KS, Linse S. Fragment complementation of calbindin D28k. Protein Sci 2000;9:2094-2108.
80. Kretsinger RH. Evolution and function of calcium-binding proteins. Int Rev Cytol 1976;46:323-393.
81. Kretsinger RH, Moncrief ND. Evolution of calcium modulated proteins. Va Explor 1989;5:7-9.
82. Nakayama S, Kretsinger RH. Evolution of the EF-hand family of proteins. Annu Rev Biophys Biomol Struct 1994;23:473-507.
83. Ridinger K, Ilg EC, Niggli FK, Heizmann CW, Schafer BW. Clustered organization of S100 genes in human and mouse. Biochim Biophys Acta 1998;1448:254-263.
84. 2+ to human nuclear S100A2 and mutant proteins. J Biol Chem 1998;273:18826-18834.
85. Fohr UG, Heizmann CW, Engelkamp D, Schafer BW, Cox JA. 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 1995;270:21056-21061.
86. Schafer BW, Fritschy JM, Murmann P, Troxler H, Durussel I, Heizmann CW, Cox JA. Brain S100A5 is a novel calcium-, zinc-, and copper ion-binding protein of the EF-hand superfamily. J Biol Chem 2000;275:30623-30630.
87. Filipek A, Heizmann CW, Kuznicki J. Calcyclin is a calcium and zinc binding protein. FEBS Lett 1990;264:263-266.
88. Heizmann CW. The multifunctional S100 protein family. Methods Mol Biol 2002;172:69-80.
89. Clohessy PA, Golden BE. His-X-X-X-His motif in S100 protein, calprotectin: relation to microbiostatic activity. J Leukoc Biol 1996; 60:674.
90. Contzler R, Favre B, Huber M, Hohl D. Cornulin, a new member of the "fused gene" family, is expressed during epidermal differentiation. J Invest Dermatol 2005;124:990-997.
91. 2+-binding proteins with five EF-hand motifs. Biochem J 1997; 328(Part 2):718-720.
92. Palczewska M, Groves P, Batta G, Heise B, Kuznicki J. Calretinin and calbindin D28k have different domain organizations. Protein Sci 2003;12:180-184.
93. Swan DG, Hale RS, Dhillon N, Leadlay PF. A bacterial calcium-binding protein homologous to calmodulin. Nature 1987;329:84-85.
94. Yonekawa T, Ohnishi Y, Horinouchi S. A calcium-binding protein with four EF-hand motifs in Streptomyces ambofaciens. Biosci Biotechnol Biochem 2001;65:156-160.
95. Grishin NV. Fold change in evolution of protein structures. J Struct Biol 2001;134:167-185.
96. 2+-binding protein S100A3: spectroscopic investigations of its transition metal ion complexes, and three-dimensional structural model. Biochim Biophys Acta 1998;1448:264-276.
97. Fritz G, Mittl PR, Vasak M, Grutter MG, Heizmann CW. The crystal structure of metal-free human EF-hand protein S100A3 at 1.7-A resolution. J Biol Chem 2002;277:33092-33098.