Ab initio structural modeling of and experimental validation for Chlamydia trachomatis protein CT296 reveal structural similarity to Fe(II) 2-Oxoglutarate-dependent enzymes

Journal of Bacteriology

Volumn 193, Issue 23, 2011, Pages 6517-6528

  Kemege, Kyle E ^a   Hickey, John M ^a   Lovell, Scott ^a   Battaile, Kevin P ^b   Zhang, Yang ^c   Hefty, P Scott ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b HAUPTMAN WOODWARD MEDICAL RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CT296 PROTEIN; DIVALENT CATION; IRON; OXOGLUTARATE DEHYDROGENASE; UNCLASSIFIED DRUG;

AB INITIO CALCULATION; ACCURACY; ARTICLE; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; ESCHERICHIA COLI; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA INTERACTION; PROTEIN MOTIF; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS;

CHLAMYDIA; CHLAMYDIA TRACHOMATIS; ESCHERICHIA COLI;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CHLAMYDIA TRACHOMATIS; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA;

EID: 84855369235     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.05488-11     Document Type: Article

References (69)

1. Adams, M. A., M. D. Suits, J. Zheng, and Z. Jia. 2007. Piecing together the structure-function puzzle: experiences in structure-based functional annotation of hypothetical proteins. Proteomics 7:2920-2932.
2. Adams, P. D., et al. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol. Crystallogr 66:213-221.
3. Albrecht, M., C. M. Sharma, R. Reinhardt, J. Vogel, and T. Rudel. 2010. Deep sequencing-based discovery of the Chlamydia trachomatis transcriptome. Nucleic Acids Res. 38:868-877.
4. Blasiak, L. C., F. H. Vaillancourt, C. T. Walsh, and C. L. Drennan. 2006. Crystal structure of the non-haem iron halogenase SyrB2 in syringomycin biosynthesis. Nature 440:368-371.
5. Carlson, J. H., S. F. Porcella, G. McClarty, and H. D. Caldwell. 2005. Comparative genomic analysis of Chlamydia trachomatis oculotropic and genitotropic strains. Infect. Immun. 73:6407-6418.
6. Centers for Disease Control and Prevention. 2010. Sexually transmitted disease surveillance 2009. Centers for Disease Control and Prevention, Atlanta, GA.
7. Chowdhury, R., et al. 2009. Structural basis for binding of hypoxia-inducible factor to the oxygen-sensing prolyl hydroxylases. Structure 17:981-989.
8. Clifton, I. J., et al. 2006. Structural studies on 2-oxoglutarate oxygenases and related double-stranded beta-helix fold proteins. J. Inorg. Biochem. 100:644-669.
9. Daruzzaman, A., I. J. Clifton, R. M. Adlington, J. E. Baldwin, and P. J. Rutledge. 2006. Unexpected oxidation of a depsipeptide substrate analogue in crystalline isopenicillin N synthase. Chembiochem 7:351-358.
10. D'Autreaux, B., et al. 2007. Reversible redox- and zinc-dependent dimerization of the Escherichia coli fur protein. Biochemistry 46:1329-1342.
11. Doublie, S. 2007. Production of selenomethionyl proteins in prokaryotic and eukaryotic expression systems. Methods Mol. Biol. 363:91-108.
12. Dunwell, J. M., A. Purvis, and S. Khuri. 2004. Cupins: the most functionally diverse protein superfamily? Phytochemistry 65:7-17.
13. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
14. Escolar, L., J. Perez-Martin, and V. de Lorenzo. 1999. Opening the iron box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181:6223-6229.
15. Evans, P. 2006. Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62:72-82.
16. Ferrer-Costa, C., H. P. Shanahan, S. Jones, and J. M. Thornton. 2005. HTHquery: a method for detecting DNA-binding proteins with a helix-turnhelix structural motif. Bioinformatics 21:3679-3680.
17. Hantke, K. 1987. Selection procedure for deregulated iron transport mutants (fur) in Escherichia coli K 12: fur not only affects iron metabolism. Mol. Gen. Genet. 210:135-139.
18. Hefty, P. S., and R. S. Stephens. 2007. Chlamydial type III secretion system is encoded on ten operons preceded by sigma 70-like promoter elements. J. Bacteriol. 189:198-206.
19. Hickey, J. M., L. Weldon, and P. S. Hefty. 2011. The atypical OmpR/PhoB response regulator ChxR from Chlamydia trachomatis forms homodimers in vivo and binds a direct repeat of nucleotide sequences. J. Bacteriol. 193:389-398.
20. Holm, L., S. Kaariainen, P. Rosenstrom, and A. Schenkel. 2008. Searching protein structure databases with DaliLite v. 3. Bioinformatics 24:2780-2781.
21. Holm, L., and J. Park. 2000. DaliLite workbench for protein structure comparison. Bioinformatics 16:566-567.
22. Holm, L., and C. Sander. 1993. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233:123-138.
23. Janowski, R., S. Panjikar, A. N. Eddine, S. H. Kaufmann, and M. S. Weiss. 2009. Structural analysis reveals DNA binding properties of Rv2827c, a hypothetical protein from Mycobacterium tuberculosis. J. Struct. Funct. Genomics 10:137-150.
24. Kabsch, W. 1993. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26:795-800.
25. Khare, D., et al. 2010. Conformational switch triggered by alpha-ketoglutarate in a halogenase of curacin A biosynthesis. Proc. Natl. Acad. Sci. U. S. A. 107:14099-14104.
26. Khuri, S., F. T. Bakker, and J. M. Dunwell. 2001. Phylogeny, function, and evolution of the cupins, a structurally conserved, functionally diverse superfamily of proteins. Mol. Biol. Evol. 18:593-605.
27. Kim, H. S., et al. 2010. Crystal structure of Tpa1 from Saccharomyces cerevisiae, a component of the messenger ribonucleoprotein complex. Nucleic Acids Res. 38:2099-2110.
28. Koo, I. C., D. Walthers, P. S. Hefty, L. J. Kenney, and R. S. Stephens. 2006. ChxR is a transcriptional activator in Chlamydia. Proc. Natl. Acad. Sci. U. S. A. 103:750-755.
29. Koski, M. K., et al. 2009. The crystal structure of an algal prolyl 4-hydroxylase complexed with a proline-rich peptide reveals a novel buried tripeptide binding motif. J. Biol. Chem. 284:25290-25301.
30. Lee, J., S. Wu, and Y. Zhang. 2009. Ab initio protein structure prediction, p. 3-25. In J. D. Rigden (ed.), From protein structure to function with bioinformatics. Springer, Dordrecht, Netherlands.
31. Lorenzini, E., et al. 2010. Structure and protein-protein interaction studies on Chlamydia trachomatis protein CT670 (YscO homolog). J. Bacteriol. 192:2746-2756.
32. Mariotti, S. P., D. Pascolini, and J. Rose-Nussbaumer. 2009. Trachoma: global magnitude of a preventable cause of blindness. Br. J. Ophthalmol. 93:563-568.
33. McCoy, A. J., et al. 2007. Phaser crystallographic software. J. Appl. Crystallogr. 40:658-674.
34. McDonough, M. A., et al. 2005. Structure of human phytanoyl-CoA 2-hydroxylase identifies molecular mechanisms of Refsum disease. J. Biol. Chem. 280:41101-41110.
35. McDonough, M. A., et al. 2006. Cellular oxygen sensing: crystal structure of hypoxia-inducible factor prolyl hydroxylase (PHD2). Proc. Natl. Acad. Sci. U. S. A. 103:9814-9819.
36. Michaud-Soret, I., et al. 1997. Electrospray ionization mass spectrometry analysis of the apo- and metal-substituted forms of the Fur protein. FEBS Lett. 413:473-476.
37. Mihalik, S. J., et al. 1997. Identification of PAHX, a Refsum disease gene. Nat. Genet. 17:185-189.
38. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Plainview, NY.
39. Potterton, L., et al. 2004. Developments in the CCP4 molecular-graphics project. Acta Crystallogr. D Biol. Crystallogr. 60:2288-2294.
40. Quatrini, R., C. Lefimil, D. S. Holmes, and E. Jedlicki. 2005. The ferric iron uptake regulator (Fur) from the extreme acidophile Acidithiobacillus ferrooxidans. Microbiology 151:2005-2015.
41. Rau, A., S. Wyllie, J. Whittimore, and J. E. Raulston. 2005. Identification of Chlamydia trachomatis genomic sequences recognized by chlamydial divalent cation-dependent regulator A (DcrA). J. Bacteriol. 187:443-448.
42. Raulston, J. E. 1997. Iron and micronutrients, p. 171-194. In P. M. Bavoil and P. B. Wyrick (ed.), Chlamydia: genomics and pathogenesis. Horizon Bioscience, Wymondham, United Kingdom.
43. Reuter, K., et al. 2010. Synthesis of 5-hydroxyectoine from ectoine: crystal structure of the non-heme iron(II) and 2-oxoglutarate-dependent dioxygenase EctD. PLoS One 5:e10647.
44. Roy, A., A. Kucukural, and Y. Zhang. 2010. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5:725-738.
45. Sim, D. W., et al. 2009. HP0902 from Helicobacter pylori is a thermostable, dimeric protein belonging to an all-beta topology of the cupin superfamily. BMB Rep. 42:387-392.
46. Srivastava, D., et al. 2010. The structure of the proline utilization a proline dehydrogenase domain inactivated by N-propargylglycine provides insight into conformational changes induced by substrate binding and flavin reduction. Biochemistry 49:560-569.
47. Stephens, R. S., et al. 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754-759.
48. Terwilliger, T. C., et al. 2009. Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard. Acta Crystallogr. D Biol. Crystallogr. 65:582-601.
49. Terwilliger, T. C., et al. 2008. Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard. Acta Crystallogr. D Biol. Crystallogr. 64:61-69.
50. Thomson, N. R., et al. 2008. Chlamydia trachomatis: genome sequence analysis of lymphogranuloma venereum isolates. Genome Res. 18:161-171.
51. Tsuchiya, Y., K. Kinoshita, and H. Nakamura. 2005. PreDs: a server for predicting dsDNA-binding site on protein molecular surfaces. Bioinformatics 21:1721-1723.
52. Uebe, R., et al. 2010. Deletion of a fur-like gene affects iron homeostasis and magnetosome formation in Magnetospirillum gryphiswaldense. J. Bacteriol. 192:4192-4204.
53. Unemo, M., et al. 2010. The Swedish new variant of Chlamydia trachomatis: genome sequence, morphology, cell tropism and phenotypic characterization. Microbiology 156:1394-1404.
54. Vajrala, N., L. A. Sayavedra-Soto, P. J. Bottomley, and D. J. Arp. 2011. Role of a Fur homolog in iron metabolism in Nitrosomonas europaea. BMC Microbiol. 11:37.
55. Valegard, K., et al. 2004. The structural basis of cephalosporin formation in a mononuclear ferrous enzyme. Nat. Struct. Mol. Biol. 11:95-101.
56. van Staalduinen, L. M., et al. 2010. Structure-based annotation of a novel sugar isomerase from the pathogenic E. coli O157:H7. J. Mol. Biol. 401:866-881.
57. Vonrhein, C., et al. 2011. Data processing and analysis with the autoPROC toolbox. Acta Crystallogr. D Biol. Crystallogr. 67:293-302.
58. Warshakoon, N. C., et al. 2006. Structure-based design, synthesis, and SAR evaluation of a new series of 8-hydroxyquinolines as HIF-1alpha prolyl hydroxylase inhibitors. Bioorg. Med. Chem. Lett. 16:5517-5522.
59. Wilmouth, R. C., et al. 2002. Structure and mechanism of anthocyanidin synthase from Arabidopsis thaliana. Structure 10:93-103.
60. Wong, C., D. G. Fujimori, C. T. Walsh, and C. L. Drennan. 2009. Structural analysis of an open active site conformation of nonheme iron halogenase CytC3. J. Am. Chem. Soc. 131:4872-4879.
61. Wu, S., J. Skolnick, and Y. Zhang. 2007. Ab initio modeling of small proteins by iterative TASSER simulations. BMC Biol. 5:17.
62. Wu, S., and Y. Zhang. 2007. LOMETS: a local meta-threading-server for protein structure prediction. Nucleic Acids Res. 35:3375-3382.
63. Wyllie, S., and J. E. Raulston. 2001. Identifying regulators of transcription in an obligate intracellular pathogen: a metal-dependent repressor in Chlamydia trachomatis. Mol. Microbiol. 40:1027-1036.
64. Xu, J., and Y. Zhang. 2010. How significant is a protein structure similarity with TM-score = 0.5? Bioinformatics 26:889-895.
65. You, Z., S. Omura, H. Ikeda, D. E. Cane, and G. Jogl. 2007. Crystal structure of the non-heme iron dioxygenase PtlH in pentalenolactone biosynthesis. J. Biol. Chem. 282:36552-36560.
66. Zhang, Y. 2009. I-TASSER: fully automated protein structure prediction in CASP8. Proteins 77(Suppl. 9):100-113.
67. Zhang, Y. 2008. Progress and challenges in protein structure prediction. Curr. Opin. Struct. Biol. 18:342-348.
68. Zhang, Y., and J. Skolnick. 2004. SPICKER: a clustering approach to identify near-native protein folds. J. Comput. Chem. 25:865-871.
69. Zhang, Y., and J. Skolnick. 2005. TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Res. 33:2302-2309.