Solution structure and function of YndB, an AHSA1 protein from Bacillus subtilis

Proteins: Structure, Function and Bioinformatics

Volumn 78, Issue 16, 2010, Pages 3328-3340

  Stark, Jaime L ^a   Mercier, Kelly A ^a,b   Mueller, Geoffrey A ^b   Acton, Thomas B ^c   Xiao, Rong ^c   Montelione, Gaetano T ^c,d   Powers, Robert ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c RUTGERS UNIVERSITY   (United States)

^d RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Chalcones; In silico screen; NMR ligand affinity screen; NMR structure; Stress response; Symbiotic relationship; YndB Bacillus subtilis

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ANTIBIOTIC AGENT; BACTERIAL PROTEIN; CHALCONE; FLAVANONE; FLAVONE; FLAVONOL; HEAT SHOCK PROTEIN 90; MICROORGANISM PROTEIN; PROTEIN AHA1; PROTEIN AHSA 1; PROTEIN YNDB; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ARCHEAN; ARTICLE; BACILLUS SUBTILIS; BETA SHEET; ENZYME ACTIVITY; EUKARYOTE; HYDROPHOBICITY; MOLECULAR LIBRARY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PLANT; PRIORITY JOURNAL; PROKARYOTE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STRESS; STRUCTURE ANALYSIS; SYMBIOSIS;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; COMPUTATIONAL BIOLOGY; HUMANS; LIGANDS; LIPIDS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHOLIPID TRANSFER PROTEINS; PROTEIN STRUCTURE, SECONDARY; SOLUTIONS; STRUCTURAL HOMOLOGY, PROTEIN; THERMODYNAMICS; TITRIMETRY; USER-COMPUTER INTERFACE;

BACILLUS SUBTILIS; EUKARYOTA; PROKARYOTA;

EID: 78349285507     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22840     Document Type: Article

References (84)

1. van Loon LC, Rep M, Pieterse CM. Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 2006; 44: 135-162.
2. Gajhede M, Osmark P, Poulsen FM, Ipsen H, Larsen JN, Joost van Neerven RJ, Schou C, Lowenstein H, Spangfort MD. X-ray and NMR structure of Bet v 1, the origin of birch pollen allergy. Nat Struct Biol 1996; 3: 1040-1045.
3. Radauer C, Lackner P, Breiteneder H. The Bet v 1 fold: an ancient, versatile scaffold for binding of large, hydrophobic ligands. BMC Evol Biol 2008; 8: 286.
4. Habe H, Omori T. Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 2003; 67: 225-243.
5. Ponting CP, Aravind L. START: a lipid-binding domain in StAR, HD-ZIP and signalling proteins. Trends Biochem Sci 1999; 24: 130-132.
6. Stocco DM. StAR protein and the regulation of steroid hormone biosynthesis. Annu Rev Physiol 2001; 63: 193-213.
7. Ames BD, Korman TP, Zhang W, Smith P, Vu T, Tang Y, Tsai SC. Crystal structure and functional analysis of tetracenomycin ARO/CYC: implications for cyclization specificity of aromatic polyketides. Proc Natl Acad Sci USA 2008; 105: 5349-5354.
8. Apweiler R, Bairoch A, Wu CH. Protein sequence databases. Curr Opin Chem Biol 2004; 8: 76-80.
9. Lotz GP, Lin H, Harst A, Obermann WM. Aha1 binds to the middle domain of Hsp90, contributes to client protein activation, and stimulates the ATPase activity of the molecular chaperone. J Biol Chem 2003; 278: 17228-17235.
10. Panaretou B, Siligardi G, Meyer P, Maloney A, Sullivan JK, Singh S, Millson SH, Clarke PA, Naaby-Hansen S, Stein R, Cramer R, Mollapour M, Workman P, Piper PW, Pearl LH, Prodromou C. Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1. Mol Cell 2002; 10: 1307-1318.
11. Singh S, Hager MH, Zhang C, Griffith BR, Lee MS, Hallenga K, Markley JL, Thorson JS. Structural insight into the self-sacrifice mechanism of enediyne resistance. ACS Chem Biol 2006; 1: 451-460.
12. Halcomb RL. Organic synthesis and cell biology: partners in controlling gene expression. Proc Natl Acad Sci USA 1994; 91: 9197-9199.
13. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, Bateman A. The Pfam protein families database. Nucleic Acids Res 2008; 36 (Database issue): D281-D288.
14. Andreeva A, Howorth D, Chandonia JM, Brenner SE, Hubbard TJ, Chothia C, Murzin AG. Data growth and its impact on the SCOP database: new developments. Nucleic Acids Res 2008; 36 (Database issue): D419-D425.
15. Mercier KA, Mueller GA, Acton TB, Xiao R, Montelione GT, Powers R. (1)H, (13)C, and (15)N NMR assignments for the Bacillus subtilis yndB START domain. Biomol NMR Assign 2009; 3: 191-194.
16. Liu G, Shen Y, Atreya HS, Parish D, Shao Y, Sukumaran DK, Xiao R, Yee A, Lemak A, Bhattacharya A, Acton TA, Arrowsmith CH, Montelione GT, Szyperski T. NMR data collection and analysis protocol for high-throughput protein structure determination. Proc Natl Acad Sci USA 2005; 102: 10487-10492.
17. Greene LH, Lewis TE, Addou S, Cuff A, Dallman T, Dibley M, Redfern O, Pearl F, Nambudiry R, Reid A, Sillitoe I, Yeats C, Thornton JM, Orengo CA. The CATH domain structure database: new protocols and classification levels give a more comprehensive resource for exploring evolution. Nucleic Acids Res 2007; 35 (Database issue): D291-D297.
18. Montelione GT, Arrowsmith C, Girvin ME, Kennedy MA, Markley JL, Powers R, Prestegard JH, Szyperski T. Unique opportunities for NMR methods in structural genomics. J Struct Funct Genomics 2009; 10: 101-106.
19. del Val C, Mehrle A, Falkenhahn M, Seiler M, Glatting KH, Poustka A, Suhai S, Wiemann S. High-throughput protein analysis integrating bioinformatics and experimental assays. Nucleic Acids Res 2004; 32: 742-748.
20. Joshi T, Chen Y, Becker JM, Alexandrov N, Xu D. Genome-scale gene function prediction using multiple sources of high-throughput data in yeast Saccharomyces cerevisiae. OMICS 2004; 8: 322-333.
21. Lee YH, Moon IJ, Hur B, Park JH, Han KH, Uhm SY, Kim YJ, Kang KJ, Park JW, Seu YB, Kim YH, Park JG. Gene knockdown by large circular antisense for high-throughput functional genomics. Nat Biotechnol 2005; 23: 591-599.
22. Oude Elferink R. One step further towards real high-throughput functional genomics. Trends Biotechnol 2003; 21: 146-147; discussion 147-148.
23. Tucker CL. High-throughput cell-based assays in yeast. Drug Discov Today 2002; 7 (18 Suppl): S125-S130.
24. Mercier KA, Baran M, Ramanathan V, Revesz P, Xiao R, Montelione GT, Powers R. FAST-NMR: functional annotation screening technology using NMR spectroscopy. J Am Chem Soc 2006; 128: 15292-15299.
25. Powers R, Mercier KA, Copeland JC. The application of FAST-NMR for the identification of novel drug discovery targets. Drug Discov Today 2008; 13: 172-179.
26. Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, Belew RK, Olson AJ. Automated docking using a Lamarckian genetic algorithm and an emperical binding free energy function. J Comput Chem 1998; 19: 1639-1662.
27. Stark J, Powers R. Rapid protein-ligand costructures using chemical shift perturbations. J Am Chem Soc 2008; 130: 535-545.
28. Powers R, Copeland JC, Germer K, Mercier KA, Ramanathan V, Revesz P. Comparison of protein active site structures for functional annotation of proteins and drug design. Proteins 2006; 65: 124-135.
29. Fahy E, Sud M, Cotter D, Subramaniam S. LIPID MAPS online tools for lipid research. Nucleic Acids Res 2007; 35 (Web Server issue): W606-W612.
30. Ghosh S, Nie A, An J, Huang Z. Structure-based virtual screening of chemical libraries for drug discovery. Curr Opin Chem Biol 2006; 10: 194-202.
31. Klebe G. Virtual ligand screening: strategies, perspectives and limitations. Drug Discov Today 2006; 11: 580-594.
32. Austin MB, Noel JP. The chalcone synthase superfamily of type III polyketide synthases. Nat Prod Rep 2003; 20: 79-110.
33. Choudhary DK, Johri BN. Interactions of Bacillus spp. and plants-with special reference to induced systemic resistance (ISR). Microbiol Res 2009; 164: 493-513.
34. Acton TB, Gunsalus KC, Xiao R, Ma LC, Aramini J, Baran MC, Chiang YW, Climent T, Cooper B, Denissova NG, Douglas SM, Everett JK, Ho CK, Macapagal D, Rajan PK, Shastry R, Shih LY, Swapna GV, Wilson M, Wu M, Gerstein M, Inouye M, Hunt JF, Montelione GT. Robotic cloning and protein production platform of the northeast structural genomics consortium. Methods Enzymol 2005; 394: 210-243.
35. Herrmann T, Guntert P, Wuthrich K. Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Biol 2002; 319: 209-227.
36. Cornilescu G, Delaglio F, Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 1999; 13: 289-302.
37. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang J-S, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. Crystallography & NMR System: a new software suite for macromolecular structure determination. Acta Crystallogr Sect D 1998; 54: 905-921.
38. Nederveen AJ, Doreleijers JF, Vranken W, Miller Z, Spronk CAEM, Nabuurs SB, Guentert P, Livny M, Markley JL, Nilges M, Ulrich EL, Kaptein R, Bonvin AMJJ. RECOORD: a recalculated coordinate database of 500+ proteins from the PDB using restraints from the BioMagResBank. Proteins 2005; 59: 662-672.
39. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB, Snoeyink J, Richardson JS, Richardson DC. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 2007; 35: W375-W383.
40. Bhattacharya A, Tejero R, Montelione GT. Evaluating protein structures determined by structural genomics consortia. Proteins 2007; 66: 778-795.
41. Dundas J, Ouyang Z, Tseng J, Binkowski A, Turpaz Y, Liang J. CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res 2006; 34 (Web Server issue): W116-W118.
42. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 2004; 25: 1605-1612.
43. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215: 403-410.
44. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25: 3389-3402.
45. Gish W, States DJ. Identification of protein coding regions by database similarity search. Nat Genet 1993; 3: 266-272.
46. Holm L, Kaariainen S, Rosenstrom P, Schenkel A. Searching protein structure databases with DaliLite v.3. Bioinformatics 2008; 24: 2780-2781.
47. Thompson JD, Gibson TJ, Higgins DG. Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics 2002;Chapter 2:Unit 2.3.
48. Fahy E, Subramaniam S, Brown HA, Glass CK, Merrill AH, Jr, Murphy RC, Raetz CR, Russell DW, Seyama Y, Shaw W, Shimizu T, Spener F, van Meer G, VanNieuwenhze MS, White SH, Witztum JL, Dennis EA. A comprehensive classification system for lipids. J Lipid Res 2005; 46: 839-861.
49. Fahy E, Subramaniam S, Murphy RC, Nishijima M, Raetz CR, Shimizu T, Spener F, van Meer G, Wakelam MJ, Dennis EA. Update of the LIPID MAPS comprehensive classification system for lipids. J Lipid Res 2009; 50(Suppl): S9-S14.
50. Bostrom J, Greenwood JR, Gottfries J. Assessing the performance of OMEGA with respect to retrieving bioactive conformations. J Mol Graph Model 2003; 21: 449-462.
51. McGann MR, Almond HR, Nicholls A, Grant JA, Brown FK. Gaussian docking functions. Biopolymers 2003; 68: 76-90.
52. Kellenberger E, Rodrigo J, Muller P, Rognan D. Comparative evaluation of eight docking tools for docking and virtual screening accuracy. Proteins 2004; 57: 225-242.
53. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 1995; 6: 277-293.
54. Johnson BA. Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol Biol 2004; 278: 313-352.
55. Morton CJ, Pugh DJ, Brown EL, Kahmann JD, Renzoni DA, Campbell ID. Solution structure and peptide binding of the SH3 domain from human Fyn. Structure 1996; 4: 705-714.
56. Fielding L. NMR methods for the determination of protein-ligand dissociation constants. Curr Top Med Chem 2003; 3: 39-53.
57. Huey R, Morris GM, Olson AJ, Goodsell DS. A semiempirical free energy force field with charge-based desolvation. J Comput Chem 2007; 28: 1145-1152.
58. Sousa SF, Fernandes PA, Ramos MJ. Protein-ligand docking: current status and future challenges. Proteins 2006; 65: 15-26.
59. Richardson JS, Richardson DC. Natural beta-sheet proteins use negative design to avoid edge-to-edge aggregation. Proc Natl Acad Sci USA 2002; 99: 2754-2759.
60. Arakane F, Sugawara T, Nishino H, Liu Z, Holt JA, Pain D, Stocco DM, Miller WL, Strauss JF, III. Steroidogenic acute regulatory protein (StAR) retains activity in the absence of its mitochondrial import sequence: implications for the mechanism of StAR action. Proc Natl Acad Sci USA 1996; 93: 13731-13736.
61. Feng L, Chan WW, Roderick SL, Cohen DE. High-level expression and mutagenesis of recombinant human phosphatidylcholine transfer protein using a synthetic gene: evidence for a C-terminal membrane binding domain. Biochemistry 2000; 39: 15399-15409.
62. Markwick PRL, Malliavin T, Nilges M. Structural biology by NMR: structure, dynamics, and interactions. PLoS Comput Biol 2008; 4: e1000168.
63. Mercier Kelly A, Cort John R, Kennedy Michael A, Lockert Erin E, Ni S, Shortridge Matthew D, Powers R. Structure and function of Pseudomonas aeruginosa protein PA1324 (21-170). Protein Sci 2009; 18: 606-618.
64. Shortridge MD, Hage DS, Harbison GS, Powers R. Estimating protein-ligand binding affinity using high-throughput screening by NMR. J Comb Chem 2008; 10: 948-958.
65. Rosenfeld RJ, Goodsell DS, Musah RA, Morris GM, Goodin DB, Olson AJ. Automated docking of ligands to an artificial active site: augmenting crystallographic analysis with computer modeling. J Comput Aided Mol Des 2003; 17: 525-536.
66. Roderick SL, Chan WW, Agate DS, Olsen LR, Vetting MW, Rajashankar KR, Cohen DE. Structure of human phosphatidylcholine transfer protein in complex with its ligand. Nat Struct Biol 2002; 9: 507-511.
67. Dove A, Marshall A. Drug screening-beyond the bottleneck. Nat Biotechnol 1999; 17: 859-863.
68. Doman TN, McGovern SL, Witherbee BJ, Kasten TP, Kurumbail R, Stallings WC, Connolly DT, Shoichet BK. Molecular docking and high-throughput screening for novel inhibitors of protein tyrosine phosphatase-1B. J Med Chem 2002; 45: 2213-2221.
69. Konstantinou-Kirtay C, Mitchell JBO, Lumley JA. Scoring functions and enrichment: a case study on Hsp90. BMC Bioinformatics 2007; 8:27.
70. Ghosh S, Nie A, An J, Huang Z. Structure-based virtual screening of chemical libraries for drug discovery. Curr Opin Chem Biol 2006; 10: 194-202.
71. Forkmann G, Martens S. Metabolic engineering and applications of flavonoids. Curr Opin Biotechnol 2001; 12: 155-160.
72. Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, Vierheilig H. Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 2007; 12: 1290-1306.
73. Winkel-Shirley B. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 2001; 126: 485-493.
74. Long SR. Rhizobium-legume nodulation: life together in the underground. Cell 1989; 56: 203-214.
75. Perret X, Staehelin C, Broughton WJ. Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 2000; 64: 180-201.
76. Shen B, Hutchinson CR. Deciphering the mechanism for the assembly of aromatic polyketides by a bacterial polyketide synthase. Proc Natl Acad Sci USA 1996; 93: 6600-6604.
77. Gensheimer M, Mushegian A. Chalcone isomerase family and fold: no longer unique to plants. Protein Sci 2004; 13: 540-544.
78. Bode HB, Muller R. Possibility of bacterial recruitment of plant genes associated with the biosynthesis of secondary metabolites. Plant Physiol 2003; 132: 1153-1161.
79. Versteeg S, Escher A, Wende A, Wiegert T, Schumann W. Regulation of the Bacillus subtilis heat shock gene htpG is under positive control. J Bacteriol 2003; 185: 466-474.
80. Rudrappa T, Bais HP. Arabidopsis thaliana root surface chemistry regulates in planta biofilm formation of Bacillus subtilis. Plant Signal Behav 2007; 2: 349-350.
81. Rudrappa T, Quinn WJ, Stanley-Wall NR, Bais HP. A degradation product of the salicylic acid pathway triggers oxidative stress resulting in down-regulation of Bacillus subtilis biofilm formation on Arabidopsis thaliana roots. Planta 2007; 226: 283-297.
82. Weller DM, Thomashow LS. Current challenges in introducing beneficial microorganisms into the rhizosphere. In: O'Gara F, Dowling DN, Boesten B, editors. Molecular ecology of rhizosphere microorganisms: biotechnology and the release of GMOs. Weinheim: VCH; 1994. pp 1-10.
83. Piggot PJ, Hilbert DW. Sporulation of Bacillus subtilis. Curr Opin Microbiol 2004; 7: 579-586.
84. Mabood F, Jung WJ, Smith DL. Signals in the underground: microbial signaling and plant productivity. molecular mechanisms of plant and microbe coexistence, Vol. 15, Soil Biology. Berlin/Heidelberg: Springer; 2008. pp 291-318.