New structural and functional contexts of the Dx[DN]xDG linear motif: Insights into evolution of Calcium-binding proteins

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Rigden, Daniel J ^a   Woodhead, Duncan D ^a   Wong, Prudence W H ^a   Galperin, Michael Y ^b  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; BACTERIAL PROTEIN; CALCIUM BINDING PROTEIN; CALCIUM ION; FUNGAL PROTEIN; GLYCINE; SUBTILISIN; CALCIUM; CALMODULIN;

AMINO ACID ANALYSIS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BETA SHEET; CALCIUM CELL LEVEL; CONTROLLED STUDY; MOLECULAR EVOLUTION; NONHUMAN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; SINGLE NUCLEOTIDE POLYMORPHISM; STRUCTURE ANALYSIS; THERMOPHILIC ARCHAEON; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN DATABASE; STRUCTURE ACTIVITY RELATION;

ARCHAEA; BACTERIA (MICROORGANISMS);

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CALCIUM; CALCIUM-BINDING PROTEINS; CALMODULIN; DATABASES, PROTEIN; EVOLUTION, MOLECULAR; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 79959603758     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021507     Document Type: Article

References (94)

1. Smith RJ, (1995) Calcium and bacteria. Adv Microb Physiol 37: 83-133.
2. Carafoli E, (2002) Calcium signaling: A tale for all seasons. Proc Natl Acad Sci U S A 99: 1115-1122.
3. Carafoli E, Klee CB, eds. (1999) Calcium as a cellular regulator New York Oxford University Press.
4. Andreini C, Bertini I, Cavallaro G, Holliday GL, Thornton JM, (2008) Metal ions in biological catalysis: From enzyme databases to general principles. J Biol Inorg Chem 13: 1205-1218.
5. McPhalen CA, Strynadka NC, James MN, (1991) Calcium-binding sites in proteins: A structural perspective. Adv Protein Chem 42: 77-144.
6. Pidcock E, Moore GR, (2001) Structural characteristics of protein binding sites for calcium and lanthanide ions. J Biol Inorg Chem 6: 479-489.
7. Torrance JW, Macarthur MW, Thornton JM, (2008) Evolution of binding sites for zinc and calcium ions playing structural roles. Proteins 71: 813-830.
8. Baumann U, Wu S, Flaherty KM, McKay DB, (1993) Three-dimensional structure of the alkaline protease of pseudomonas aeruginosa: A two-domain protein with a calcium binding parallel beta roll motif. EMBO J 12: 3357-3364.
9. Gifford JL, Walsh MP, Vogel HJ, (2007) Structures and metal-ion-binding properties of the Ca2+-binding helix-loop-helix EF-hand motifs. Biochem J 405: 199-221.
10. Grabarek Z, (2006) Structural basis for diversity of the EF-hand calcium-binding proteins. J Mol Biol 359: 509-525.
11. Kretsinger RH, (1976) Calcium-binding proteins. Annu Rev Biochem 45: 239-266.
12. Strynadka NC, James MN, (1989) Crystal structures of the helix-loop-helix calcium-binding proteins. Annu Rev Biochem 58: 951-998.
13. Kawasaki H, Nakayama S, Kretsinger RH, (1998) Classification and evolution of EF-hand proteins. Biometals 11: 277-295.
14. Dragani B, Aceto A, (1999) About the role of conserved amino acid residues in the calcium-binding site of proteins. Arch Biochem Biophys 368: 211-213.
15. Rigden DJ, Galperin MY, (2004) The DxDxDG motif for calcium binding: Multiple structural contexts and implications for evolution. J Mol Biol 343: 971-984.
16. Rigden DJ, Jedrzejas MJ, Moroz OV, Galperin MY, (2003) Structural diversity of calcium-binding proteins in bacteria: Single-handed EF-hands? Trends Microbiol 11: 295-297.
17. Rigden DJ, Jedrzejas MJ, Galperin MY, (2003) An extracellular calcium-binding domain in bacteria with a distant relationship to EF-hands. FEMS Microbiol Lett 221: 103-110.
18. Ye Y, Shealy S, Lee HW, Torshin I, Harrison R, et al. (2003) A grafting approach to obtain site-specific metal-binding properties of EF-hand proteins. Protein Eng 16: 429-434.
19. Ye Y, Lee HW, Yang W, Shealy SJ, Wilkins AL, et al. (2001) Metal binding affinity and structural properties of an isolated EF-loop in a scaffold protein. Protein Eng 14: 1001-1013.
20. Kurakata Y, Uechi A, Yoshida H, Kamitori S, Sakano Y, et al. (2008) Structural insights into the substrate specificity and function of Escherichia coli K12 YgjK, a glucosidase belonging to the glycoside hydrolase family 63. J Mol Biol 381: 116-128.
21. Suzuki R, Katayama T, Kitaoka M, Kumagai H, Wakagi T, et al. (2009) Crystallographic and mutational analyses of substrate recognition of endo-alpha-N-acetylgalactosaminidase from Bifidobacterium longum. J Biochem 146: 389-398.
22. Li N, Yun P, Nadkarni MA, Ghadikolaee NB, Nguyen KA, et al. (2010) Structure determination and analysis of a haemolytic gingipain adhesin domain from Porphyromonas gingivalis. Mol Microbiol 76: 861-873.
23. Takeuchi Y, Tanaka S, Matsumura H, Koga Y, Takano K, et al. (2009) Requirement of a unique Ca2+-binding loop for folding of Tk-subtilisin from a hyperthermophilic archaeon. Biochemistry 48: 10637-10643.
24. Ochiai A, Itoh T, Maruyama Y, Kawamata A, Mikami B, et al. (2007) A novel structural fold in polysaccharide lyases: Bacillus subtilis family 11 rhamnogalacturonan lyase YesW with an eight-bladed beta-propeller. J Biol Chem 282: 37134-37145.
25. Orans J, Johnson MD, Coggan KA, Sperlazza JR, Heiniger RW, et al. (2010) Crystal structure analysis reveals Pseudomonas PilY1 as an essential calcium-dependent regulator of bacterial surface motility. Proc Natl Acad Sci USA 107: 1065-1070.
26. Cioci G, Mitchell EP, Chazalet V, Debray H, Oscarson S, et al. (2006) Beta-propeller crystal structure of Psathyrella velutina lectin: An integrin-like fungal protein interacting with monosaccharides and calcium. J Mol Biol 357: 1575-1591.
27. Caines ME, Zhu H, Vuckovic M, Willis LM, Withers SG, et al. (2008) The structural basis for T-antigen hydrolysis by Streptococcus pneumoniae: A target for structure-based vaccine design. J Biol Chem 283: 31279-31283.
28. Wilson MA, Brunger AT, (2000) The 1.0 A crystal structure of Ca2+-bound calmodulin: An analysis of disorder and implications for functionally relevant plasticity. J Mol Biol 301: 1237-1256.
29. Harding MM, (2006) Small revisions to predicted distances around metal sites in proteins. Acta Crystallogr D Biol Crystallogr 62: 678-682.
30. Nitz M, Sherawat M, Franz KJ, Peisach E, Allen KN, et al. (2004) Structural origin of the high affinity of a chemically evolved lanthanide-binding peptide. Angew Chem Int Ed Engl 43: 3682-3685.
31. Petosa C, Collier RJ, Klimpel KR, Leppla SH, Liddington RC, (1997) Crystal structure of the anthrax toxin protective antigen. Nature 385: 833-838.
32. Kvansakul M, Adams JC, Hohenester E, (2004) Structure of a thrombospondin C-terminal fragment reveals a novel calcium core in the type 3 repeats. EMBO J 23: 1223-1233.
33. Eddy SR, (1998) Profile hidden markov models. Bioinformatics 14: 755-763.
34. Eddy SR, (2009) A new generation of homology search tools based on probabilistic inference. Genome Inform 23: 205-211.
35. Adany R, Bardos H, (2003) Factor XIII subunit A as an intracellular transglutaminase. Cell Mol Life Sci 60: 1049-1060.
36. Gangola P, Rosen BP, (1987) Maintenance of intracellular calcium in Escherichia coli. J Biol Chem 262: 12570-12574.
37. Bronner F, (2001) Extracellular and intracellular regulation of calcium homeostasis. ScientificWorldJournal 1: 919-925.
38. Chaudhuri I, Soding J, Lupas AN, (2008) Evolution of the beta-propeller fold. Proteins 71: 795-803.
39. Johnson LS, Eddy SR, Portugaly E, (2010) Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinformatics 11: 431.
40. Wheeler DL, Barrett T, Benson DA, Bryant SH, Canese K, et al. (2007) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 35: D5-D12.
41. Li JY, Hollfelder K, Huang KS, Low MG, (1994) Structural features of GPI-specific phospholipase D revealed by proteolytic fragmentation and Ca2+ binding studies. J Biol Chem 269: 28963-28971.
42. Redruello B, Louro B, Anjos L, Silva N, Greenwell RS, et al. (2010) CRTAC1 homolog proteins are conserved from cyanobacteria to man and secreted by the teleost fish pituitary gland. Gene 456: 1-14.
43. Fiscella M, Perry JW, Teng B, Bloom M, Zhang C, et al. (2003) TIP, a T-cell factor identified using high-throughput screening increases survival in a graft-versus-host disease model. Nat Biotechnol 21: 302-307.
44. Harris TW, Antoshechkin I, Bieri T, Blasiar D, Chan J, et al. (2010) WormBase: A comprehensive resource for nematode research. Nucleic Acids Res 38: D463-D467.
45. Liu OW, Chun CD, Chow ED, Chen C, Madhani HD, et al. (2008) Systematic genetic analysis of virulence in the human fungal pathogen Cryptococcus neoformans. Cell 135: 174-188.
46. Bearer EL, (1992) An actin-associated protein present in the microtubule organizing center and the growth cones of PC-12 cells. J Neurosci 12: 750-761.
47. Bearer EL, Abraham MT, (1999) 2E4 (kaptin): A novel actin-associated protein from human blood platelets found in lamellipodia and the tips of the stereocilia of the inner ear. Eur J Cell Biol 78: 117-126.
48. Bearer EL, Chen AF, Chen AH, Li Z, Mark HF, et al. (2000) 2E4/Kaptin (KPTN)-a candidate gene for the hearing loss locus, DFNA4. Ann Hum Genet 64: 189-196.
49. Shah AS, Farmen SL, Moninger TO, Businga TR, Andrews MP, et al. (2008) Loss of Bardet-Biedl syndrome proteins alters the morphology and function of motile cilia in airway epithelia. Proc Natl Acad Sci USA 105: 3380-3385.
50. Seo S, Guo DF, Bugge K, Morgan DA, Rahmouni K, et al. (2009) Requirement of Bardet-Biedl syndrome proteins for leptin receptor signaling. Hum Mol Genet 18: 1323-1331.
51. Bordo D, Argos P, (1991) Suggestions for "safe" residue substitutions in site-directed mutagenesis. J Mol Biol 217: 721-729.
52. Hoskins BE, Thorn A, Scambler PJ, Beales PL, (2003) Evaluation of multiplex capillary heteroduplex analysis: A rapid and sensitive mutation screening technique. Hum Mutat 22: 151-157.
53. Beurg M, Fettiplace R, Nam JH, Ricci AJ, (2009) Localization of inner hair cell mechanotransducer channels using high-speed calcium imaging. Nat Neurosci 12: 553-558.
54. Praetorius HA, Spring KR, (2001) Bending the MDCK cell primary cilium increases intracellular calcium. J Membr Biol 184: 71-79.
55. Mykytyn K, Sheffield VC, (2004) Establishing a connection between cilia and Bardet-Biedl syndrome. Trends Mol Med 10: 106-109.
56. Yadid I, Kirshenbaum N, Sharon M, Dym O, Tawfik DS, (2010) Metamorphic proteins mediate evolutionary transitions of structure. Proc Natl Acad Sci USA 107: 7287-7292.
57. Shinde U, Inouye M, (1996) Propeptide-mediated folding in subtilisin: The intramolecular chaperone concept. Adv Exp Med Biol 379: 147-154.
58. Tanaka S, Saito K, Chon H, Matsumura H, Koga Y, et al. (2007) Crystal structure of unautoprocessed precursor of subtilisin from a hyperthermophilic archaeon: Evidence for Ca2+-induced folding. J Biol Chem 282: 8246-8255.
59. Takeuchi Y, Tanaka S, Matsumura H, Koga Y, Takano K, et al. (2009) Requirement of a unique Ca2+-binding loop for folding of Tk-subtilisin from a hyperthermophilic archaeon. Biochemistry 48: 10637-10643.
60. Li JY, Low MG, (1999) Studies of the role of the integrin EF-hand, Ca2+-binding sites in glycosylphosphatidylinositol-specific phospholipase D: Reduced expression following mutagenesis of residues predicted to bind Ca2+. Arch Biochem Biophys 361: 142-148.
61. Gahmberg CG, Fagerholm SC, Nurmi SM, Chavakis T, Marchesan S, et al. (2009) Regulation of integrin activity and signalling. Biochim Biophys Acta 1790: 431-444.
62. Dutta A, Bahar I, (2010) Metal-binding sites are designed to achieve optimal mechanical and signaling properties. Structure 18: 1140-1148.
63. Neduva V, Linding R, Su-Angrand I, Stark A, de Masi F, et al. (2005) Systematic discovery of new recognition peptides mediating protein interaction networks. PLoS Biol 3: e405.
64. Edwards RJ, Davey NE, Shields DC, (2007) SLiMFinder: A probabilistic method for identifying over-represented, convergently evolved, short linear motifs in proteins. PLoS One 2: e967.
65. Gould CM, Diella F, Via A, Puntervoll P, Gemund C, et al. (2010) ELM: The status of the 2010 eukaryotic linear motif resource. Nucleic Acids Res 38: D167-D180.
66. Wells RD, (1996) Molecular basis of genetic instability of triplet repeats. J Biol Chem 271: 2875-2878.
67. Richard GF, Paques F, (2000) Mini- and microsatellite expansions: The recombination connection. EMBO Rep 1: 122-126.
68. Mar Alba M, Santibanez-Koref MF, Hancock JM, (1999) Amino acid reiterations in yeast are overrepresented in particular classes of proteins and show evidence of a slippage-like mutational process. J Mol Evol 49: 789-797.
69. Yuan P, Leonetti MD, Pico AR, Hsiung Y, MacKinnon R, (2010) Structure of the human BK channel Ca2+-activation apparatus at 3.0 Å resolution. Science 329: 182-186.
70. Sprangers R, Groves MR, Sinning I, Sattler M, (2003) High-resolution X-ray and NMR structures of the SMN Tudor domain: Conformational variation in the binding site for symmetrically dimethylated arginine residues. J Mol Biol 327: 507-520.
71. Graveley BR, (2000) Sorting out the complexity of SR protein functions. RNA 6: 1197-1211.
72. Torrance JW, Macarthur MW, Thornton JM, (2008) Evolution of binding sites for zinc and calcium ions playing structural roles. Proteins 71: 813-830.
73. Brakoulias A, Jackson RM, (2004) Towards a structural classification of phosphate binding sites in protein-nucleotide complexes: An automated all-against-all structural comparison using geometric matching. Proteins 56: 250-260.
74. Kleywegt GJ, (1999) Recognition of spatial motifs in protein structures. J Mol Biol 285: 1887-1897.
75. Kleywegt GJ, (1996) Use of non-crystallographic symmetry in protein structure refinement. Acta Crystallogr D Biol Crystallogr 52: 842-857.
76. Krissinel E, Henrick K, (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 60: 2256-2268.
77. Holm L, Sander C, (1993) Protein structure comparison by alignment of distance matrices. J Mol Biol 233: 123-138.
78. Heinig M, Frishman D, (2004) STRIDE: A web server for secondary structure assignment from known atomic coordinates of proteins. Nucleic Acids Res 32: W500-W502.
79. Andreeva A, Howorth D, Chandonia JM, Brenner SE, Hubbard TJ, et al. (2008) Data growth and its impact on the SCOP database: New developments. Nucleic Acids Res 36: D419-D425.
80. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38: D211-D222.
81. Letunic I, Doerks T, Bork P, (2009) SMART 6: Recent updates and new developments. Nucleic Acids Res 37: D229-D232.
82. UniProt Consortium (2010) The universal protein resource (UniProt) in 2010. Nucleic Acids Res 38: D142-D148.
83. Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH, (2007) UniRef: Comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23: 1282-1288.
84. Edgar RC, (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
85. Gattiker A, Gasteiger E, Bairoch A, (2002) ScanProsite: A reference implementation of a PROSITE scanning tool. Appl Bioinformatics 1: 107-108.
86. Soding J, (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21: 951-960.
87. Rose PW, Beran B, Bi C, Bluhm WF, Dimitropoulos D, et al. (2011) The RCSB protein data bank: Redesigned web site and web services. Nucleic Acids Res 39: D392-D401.
88. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ, (2009) Jalview version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
89. Felsenstein J, (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783-791.
90. Kumar S, Nei M, Dudley J, Tamura K, (2008) MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9: 299-306.
91. Saitou N, Nei M, (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
92. Tanaka S, Matsumura H, Koga Y, Takano K, Kanaya S, (2007) Four new crystal structures of Tk-subtilisin in unautoprocessed, autoprocessed and mature forms: Insight into structural changes during maturation. J Mol Biol 372: 1055-1069.
93. Xiong JP, Stehle T, Diefenbach B, Zhang R, Dunker R, et al. (2001) Crystal structure of the extracellular segment of integrin αVβ3. Science 294: 339-345.
94. Nachury MV, Loktev AV, Zhang Q, Westlake CJ, Peranen J, et al. (2007) A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129: 1201-1213.