Sequence-Structure-Function Classification of a Catalytically Diverse Oxidoreductase Superfamily in Mycobacteria

Journal of Molecular Biology

Volumn 427, Issue 22, 2015, Pages 3554-3571

  Ahmed, F Hafna ^a   Carr, Paul D ^a   Lee, Brendon M ^a   Afriat Jurnou, Livnat ^a   Mohamed, A Elaaf ^a   Hong, Nan Sook ^a   Flanagan, Jack ^b   Taylor, Matthew C ^c   Greening, Chris ^c   Jackson, Colin J ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c CSIRO   (Australia)

Author keywords

biliverdin reductase; F420; flavin deazaflavin oxidoreductase (FDOR); mycobacteria; pyridoxamine pyridoxine 5 phosphate oxidase (PnPOx)

Indexed keywords

BILIVERDIN; BINDING PROTEIN; CUTINASE; FATTY ACID; FLAVIN DEAZAFLAVIN OXIDOREDUCTASE; FLAVINE ADENINE NUCLEOTIDE; FLAVINE MONONUCLEOTIDE; HEME OXYGENASE; LIPOPROTEIN; LONG CHAIN FATTY ACID COENZYME A LIGASE; OXIDOREDUCTASE; PYRIDOXAMINE PHOSPHATE OXIDASE; QUINONE DERIVATIVE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; HEME; PROTEIN BINDING;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CATALYSIS; CONCEPTUAL FRAMEWORK; CRYSTAL STRUCTURE; ENZYME DEGRADATION; ENZYME STRUCTURE; GENE SEQUENCE; MYCOBACTERIUM; NONHUMAN; PATHOGENESIS; PHENOTYPIC PLASTICITY; PHYLOGENETIC TREE; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SPECTROSCOPY; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; ENZYME SPECIFICITY; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; FLAVIN MONONUCLEOTIDE; FLAVIN-ADENINE DINUCLEOTIDE; HEME; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM; OXIDOREDUCTASES; PHYLOGENY; PROTEIN BINDING; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY;

EID: 84952865220     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.09.021     Document Type: Article

References (110)

1. P. Hemmerich, G. Nagelschneider, and C. Veeger Chemistry and molecular biology of flavins and flavoproteins FEBS Lett. 8 1970 69 83
2. L. Daniels, N. Bakhiet, and K. Harmon Widespread Distribution of a 5-deazaflavin Cofactor in Actinomyces and Related Bacteria Syst. Appl. Microbiol. 6 1985 12 17
3. P. Cheeseman, A. Toms-Wood, and R.S. Wolfe Isolation and Properties of a Fluorescent Compound, Factor420, from Methanobacterium Strain M.o.H J. Bacteriol. 112 1972 527 531
4. C. Walsh Naturally occurring 5-deazaflavin coenzymes: biological redox roles Acc. Chem. Res. 19 1986 216 221
5. R.K. Thauer, A.K. Kaster, H. Seedorf, W. Buckel, and R. Hedderich Methanogenic archaea: ecologically relevant differences in energy conservation Nat. Rev. Microbiol. 6 2008 579 591
6. 420 biosynthesis Arch. Microbiol. 180 2003 455 464
7. 420-dependent glucose-6-phosphate dehydrogenase FGD1 involved in the activation of the anti-tuberculosis drug candidate PA-824 reveal the basis of coenzyme and substrate binding J. Biol. Chem. 283 2008 17531 17541
8. 2-dependent reductases from Mycobacteria that catalyse aflatoxin degradation Mol. Microbiol. 78 2010 561 575
9. 2-Dependent Degradation of Aflatoxin and other Furanocoumarins Is Widespread throughout the Actinomycetales PLoS One 7 2012 e30114
10. 420-dependent anti-oxidant mechanism protects Mycobacterium tuberculosis against oxidative stress and bactericidal agents Mol. Microbiol. 8 2013 744 755
11. 420-Dependent Enzymes in Mycobacterium tuberculosis and Other Actinobacteria J. Bacteriol. 192 2010 5788 5798
12. M.R. Hasan, M. Rahman, S. Jaques, E. Purwantini, and L. Daniels Glucose 6-Phosphate Accumulation in Mycobacteria J. Biol. Chem. 285 2010 19135 19144
13. 420 biosynthesis Microbiology 153 2007 2724 2732
14. 420 protects mycobacteria from nitrosative damage Proc. Natl. Acad. Sci. U. S. A. 106 2009 6333 6338
15. 420-dependent reductases enables them to catalyse both oxidation and reduction of the same substrate Catal. Sci. Technol. 2 2012 1560 1567
16. S.E. Cellitti, J. Shaffer, D.H. Jones, T. Mukherjee, M. Gurumurthy, B. Bursulaya, H.I. Boshoff, I. Choi, A. Nayyar, Y.S. Lee, J. Cherian, P. Niyomrattanakit, T. Dick, U.H. Manjunatha, C.E. Barry III, G. Spraggon, and B.H. Geierstanger Structure of Ddn, the Deazaflavin-Dependent Nitroreductase from Mycobacterium tuberculosis Involved in Bioreductive Activation of PA-824 Structure 20 2012 101 112
17. 420 to the conserved protein Rv1155 from Mycobacterium tuberculosis Protein Sci. 24 2015 729 740
18. R. Singh, U. Manjunatha, H.I.M. Boshoff, Y.H. Ha, P. Niyomrattanakit, R. Ledwidge, C.S. Dowd, I.Y. Lee, P. Kim, L. Zhang, S. Kang, T.H. Keller, J. Jiricek, and C.E. Barry PA-824 Kills Nonreplicating Mycobacterium tuberculosis by Intracellular NO Release Science 322 2008 1392 1395
19. M. Gurumurthy, T. Mukherjee, C.S. Dowd, R. Singh, P. Niyomrattanakit, J.A. Tay, A. Nayyar, Y.S. Lee, J. Cherian, H.I. Boshoff, T. Dick, C.E. Barry, and U.H. Manjunatha Substrate specificity of the deazaflavin-dependent nitroreductase from Mycobacterium tuberculosis responsible for the bioreductive activation of bicyclic nitroimidazoles FEBS J. 279 2012 113 125
20. E.H. Mashalidis, T. Mukherjee, P. ͆ledź, D. Matak-Vinković, H. Boshoff, C. Abell, and C.E. Barry III Rv2607 from Mycobacterium tuberculosis Is a Pyridoxine 5′-Phosphate Oxidase with Unusual Substrate Specificity PLoS One 6 2011 e27643
21. M.L. Salvo, M.K. Safo, F.N. Musayev, F. Bossa, and V. Schirch Structure and mechanism of Escherichia coli pyridoxine 5′-phosphate oxidase Biochim. Biophys. Acta 1647 2003 76 82
22. F.N. Musayev, M.L. Di Salvo, T.-P. Ko, V. Schirch, and M.K. Safo Structure and properties of recombinant human pyridoxine 5′-phosphate oxidase Protein Sci. 12 2003 1455 1463
23. Y. Hu, F. Jiang, Y. Guo, X. Shen, Y. Zhang, R. Zhang, G. Guo, X. Mao, Q. Zou, and D.-C. Wang Crystal Structure of HugZ, a Novel Heme Oxygenase from Helicobacter pylori J. Biol. Chem. 286 2011 1537 1544
24. R. Zhang, J. Zhang, G. Guo, X. Mao, W. Tong, Y. Zhang, D.-C. Wang, Y. Hu, and Q. Zou Crystal structure of Campylobacter jejuni ChuZ: A split-barrel family heme oxygenase with a novel heme-binding mode Biochem. Biophys. Res. Commun. 415 2011 82 87
25. R. Stocker, Y. Yamamoto, A. McDonagh, A. Glazer, and B. Ames Bilirubin is an antioxidant of possible physiological importance Science 235 1987 1043 1046
26. L.C. Mireles, M.A. Lum, and P.A. Dennery Antioxidant and Cytotoxic Effects of Bilirubin on Neonatal Erythrocytes Pediatr. Res. 45 1999 355 362
27. D.E. Barañano, M. Rao, C.D. Ferris, and S.H. Snyder Biliverdin reductase: A major physiologic cytoprotectant Proc. Natl. Acad. Sci. U. S. A. 99 2002 16093 16098
28. T. Jansen, and A. Daiber Direct antioxidant properties of bilirubin and biliverdin. Is there a role for biliverdin reductase? Front. Pharmacol. 3 2012 30
29. M.Y. Abdalla, I.M. Ahmad, B. Switzer, and B.E. Britigan Induction of heme oxygenase-1 contributes to survival of Mycobacterium abscessus in human macrophages-like THP-1 cells Redox Biol. 4 2015 328 339
30. S.T. Mashiyama, M.M. Malabanan, E. Akiva, R. Bhosle, M.C. Branch, B. Hillerich, K. Jagessar, J. Kim, Y. Patskovsky, R.D. Seidel, M. Stead, R. Toro, M.W. Vetting, S.C. Almo, R.N. Armstrong, and P.C. Babbitt Large-Scale Determination of Sequence, Structure, and Function Relationships in Cytosolic Glutathione Transferases across the Biosphere PLoS Biol. 12 2014 e1001843
31. R. Uberto, and E.W. Moomaw Protein Similarity Networks Reveal Relationships among Sequence, Structure, and Function within the Cupin Superfamily PLoS One 8 2013 e74477
32. S.D. Brown, and P.C. Babbitt New Insights about Enzyme Evolution from Large Scale Studies of Sequence and Structure Relationships J. Biol. Chem. 289 2014 30221 30228
33. H.J. Atkinson, J.H. Morris, T.E. Ferrin, and P.C. Babbitt Using Sequence Similarity Networks for Visualization of Relationships Across Diverse Protein Superfamilies PLoS One 4 2009 e4345
34. A.J.M. Martin, I. Walsh, T.D. Domenico, I. Mičetić, and S.C.E. Tosatto PANADA: Protein Association Network Annotation, Determination and Analysis PLoS One 8 2013 e78383
35. M.J. Sanderson, and A.C. Driskell The challenge of constructing large phylogenetic trees Trends Plant Sci. 8 2003 374 379
36. W.P. Maddison Gene Trees in Species Trees Syst. Biol. 46 1997 523 536
37. A. Som Causes, consequences and solutions of phylogenetic incongruence Brief. Bioinform. 16 2015 536 548
38. S.F. Altschul, W. Gish, W. Miller, E.W. Myers, and D.J. Lipman Basic local alignment search tool J. Mol. Biol. 215 1990 403 410
39. S.F. Altschul, T.L. Madden, A.A. Schäffer, J. Zhang, Z. Zhang, W. Miller, and D.J. Lipman Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res. 25 1997 3389 3402
40. B.K. Biswal, K. Au, M.M. Cherney, C. Garen, and M.N.G. James The molecular structure of Rv2074, a probable pyridoxine 5'-phosphate oxidase from Mycobacterium tuberculosis, at 1.6 A resolution Acta Crystallogr. Sect. F: Struct. Biol. Cryst. Commun. 62 2006 735 742
41. R.D. Finn, A. Bateman, J. Clements, P. Coggill, R.Y. Eberhardt, S.R. Eddy, A. Heger, K. Hetherington, L. Holm, J. Mistry, E.L.L. Sonnhammer, J. Tate, and M. Punta Pfam: the protein families database Nucleic Acids Res. 42 2014 D222 D230
42. J.F. Parsons, K. Calabrese, E. Eisenstein, and J.E. Ladner Structure of the phenazine biosynthesis enzyme PhzG Acta Crystallogr. D Biol. Crystallogr. 60 2004 2110 2113
43. N. Xu, E.G. Ahuja, P. Janning, D.V. Mavrodi, L.S. Thomashow, and W. Blankenfeldt Trapped intermediates in crystals of the FMN-dependent oxidase PhzG provide insight into the final steps of phenazine biosynthesis Acta Crystallogr. D Biol. Crystallogr. 69 2013 1403 1413
44. Y. Guo, G. Guo, X. Mao, W. Zhang, J. Xiao, W. Tong, T. Liu, B. Xiao, X. Liu, Y. Feng, and Q. Zou Functional identification of HugZ, a heme oxygenase from Helicobacter pylori BMC Microbiol. 8 2008 226
45. A.L. Oldham, T.A. Wood, and D.P. Henderson Plesiomonas shigelloides hugZ encodes an iron-regulated heme binding protein required for heme iron utilization Can. J. Microbiol. 54 2008 97 102
46. M.K. Safo, I. Mathews, F.N. Musayev, M.L. di Salvo, D.J. Thiel, D.J. Abraham, and V. Schirch X-ray structure of Escherichia coli pyridoxine 5′-phosphate oxidase complexed with FMN at 1.8 Å resolution Structure 8 2000 751 762
47. A.S. Konagurthu, C.F. Reboul, J.W. Schmidberger, J.A. Irving, A.M. Lesk, P.J. Stuckey, J.C. Whisstock, and A.M. Buckle MUSTANG-MR Structural Sieving Server: Applications in Protein Structural Analysis and Crystallography PLoS One 5 2010 e10048
48. K. Suto, K. Kawagoe, N. Shibata, Y. Morimoto, Y. Higuchi, M. Kitamura, T. Nakaya, and N. Yasuoka How do the X-ray structure and the NMR structure of FMN-binding protein differ? Acta Crystallogr. D Biol. Crystallogr. 56 2000 368 371
49. H.-K.S. Leiros, S. Kozielski-Stuhrmann, U. Kapp, L. Terradot, G.A. Leonard, and S.M. McSweeney Structural Basis of 5-Nitroimidazole Antibiotic Resistance: The crystal structure of NimA from Deinococcus radiodurans J. Biol. Chem. 279 2004 55840 55849
50. S. Canaan, G. Sulzenbacher, V. Roig-Zamboni, L. Scappuccini-Calvo, F. Frassinetti, D. Maurin, C. Cambillau, and Y. Bourne Crystal structure of the conserved hypothetical protein Rv1155 from Mycobacterium tuberculosis FEBS Lett. 579 2005 215 221
51. J.-D. Pédelacq, B.-S. Rho, C.-Y. Kim, G.S. Waldo, T.P. Lekin, B.W. Segelke, B. Rupp, L.-W. Hung, S.-I. Kim, and T.C. Terwilliger Crystal structure of a putative pyridoxine 5′-phosphate oxidase (Rv2607) from Mycobacterium tuberculosis Proteins 62 2006 563 569
52. X. Liu, J. Gong, T. Wei, Z. Wang, Q. Du, D. Zhu, Y. Huang, S. Xu, and L. Gu Crystal structure of HutZ, a heme storage protein from Vibrio cholerae: A structural mismatch observed in the region of high sequence conservation BMC Struct. Biol. 12 2012 23
53. E. Hilario, Y. Li, D. Niks, and L. Fan The structure of a Xanthomonas general stress protein involved in citrus canker reveals its flavin-binding property Acta Crystallogr. D Biol. Crystallogr. 68 2012 846 853
54. A. Wilks, and M.P. Schmitt Expression and Characterization of a Heme Oxygenase (Hmu O) from Corynebacterium diphtheriae: iron acquisition requires oxidative cleavage of the heme macrocycle J. Biol. Chem. 273 1998 837 841
55. H. Zhiguo, and J.D. Buck Cell wall proteome analysis of Mycobacterium smegmatis strain MC2 155 BMC Microbiol. 10 2010 121
56. K.G. Mawuenyega, C.V. Forst, K.M. Dobos, J.T. Belisle, J. Chen, E.M. Bradbury, A.R.M. Bradbury, and X. Chen Mycobacterium tuberculosis Functional Network Analysis by Global Subcellular Protein Profiling Mol. Biol. Cell 16 2005 396 404
57. G.A. De Souza, N.A. Leversen, H. Målen, and H.G. Wiker Bacterial proteins with cleaved or uncleaved signal peptides of the general secretory pathway J. Proteome 75 2011 502 510
58. A. Franceschini, D. Szklarczyk, S. Frankild, M. Kuhn, M. Simonovic, A. Roth, J. Lin, P. Minguez, P. Bork, C. von Mering, and L.J. Jensen STRING v9.1: protein-protein interaction networks, with increased coverage and integration Nucleic Acids Res. 41 2013 D808 D815
59. J.A. McGarvey, and L.E. Bermudez Phenotypic and Genomic Analyses of the Mycobacterium avium Complex Reveal Differences in Gastrointestinal Invasion and Genomic Composition Infect. Immun. 69 2001 7242 7249
60. S.M. Behar, M. Divangahi, and H.G. Remold Evasion of innate immunity by Mycobacterium tuberculosis: is death an exit strategy? Nat. Rev. Microbiol. 8 2010 668 674
61. B.K. Biswal, M.M. Cherney, M. Wang, C. Garen, and M.N.G. James Structures of Mycobacterium tuberculosis pyridoxine 5'-phosphate oxidase and its complexes with flavin mononucleotide and pyridoxal 5'-phosphate Acta Crystallogr. D Biol. Crystallogr. 61 2005 1492 1499
62. D.F. Xiang, P. Kolb, A.A. Fedorov, C. Xu, E.V. Fedorov, T. Narindoshivili, H.J. Williams, B.K. Shoichet, S.C. Almo, and F.M. Raushel Structure-Based Function Discovery of an Enzyme for the Hydrolysis of Phosphorylated Sugar Lactones Biochemistry 51 2012 1762 1773
63. G.Q. Dong, S. Calhoun, H. Fan, C. Kalyanaraman, M.C. Branch, S.T. Mashiyama, N. London, M.P. Jacobson, P.C. Babbitt, B.K. Shoichet, R.N. Armstrong, and A. Sali Prediction of Substrates for Glutathione Transferases by Covalent Docking J. Chem. Inf. Model. 54 2014 1687 1699
64. J.C. Hermann, E. Ghanem, Y. Li, F.M. Raushel, J.J. Irwin, and B.K. Shoichet Predicting Substrates by Docking High-Energy Intermediates to Enzyme Structures J. Am. Chem. Soc. 128 2006 15882 15891
65. M. Unno, T. Matsui, and M. Ikeda-Saito Structure and catalytic mechanism of heme oxygenase Nat. Prod. Rep. 24 2007 553 570
66. Liam J. Smith, S. Browne, Adrian J. Mulholland, and Timothy J. Mantle Computational and experimental studies on the catalytic mechanism of biliverdin-IXβ reductase 411 2008 475 484
67. T.L. Bailey, and C. Elkan Fitting a mixture model by expectation maximization to discover motifs in biopolymers Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology 1994 AAAI Press Menlo Park, CA 28 36
68. T.L. Bailey, M. Boden, F.A. Buske, M. Frith, C.E. Grant, L. Clementi, J. Ren, W.W. Li, and W.S. Noble MEME Suite: tools for motif discovery and searching Nucleic Acids Res. 37 2009 W202 W208
69. M.K. Safo, F.N. Musayev, M.L. di Salvo, and V. Schirch X-ray structure of Escherichia coli pyridoxine 5′-phosphate oxidase complexed with pyridoxal 5′-phosphate at 2.0 Å resolution J. Mol. Biol. 310 2001 817 826
70. J.T. Lennon, and S.E. Jones Microbial seed banks: the ecological and evolutionary implications of dormancy Nat. Rev. Microbiol. 9 2011 119 130
71. M.S. Rappé, and S.J. Giovannoni The Uncultured Microbial Majority Annu. Rev. Microbiol. 57 2003 369 394
72. R.J. Whittington, D.J. Marshall, P.J. Nicholls, I.B. Marsh, and L.A. Reddacliff Survival and Dormancy of Mycobacterium avium subsp. Paratuberculosis in the Environment Appl. Environ. Microbiol. 70 2004 2989 3004
73. M. Berney, C. Greening, R. Conrad, W.R. Jacobs, and G.M. Cook An obligately aerobic soil bacterium activates fermentative hydrogen production to survive reductive stress during hypoxia Proc. Natl. Acad. Sci. U. S. A. 111 2014 11479 11484
74. M.J. Smeulders, J. Keer, R.A. Speight, and H.D. Williams Adaptation of Mycobacterium smegmatis to Stationary Phase J. Bacteriol. 181 1999 270 283
75. E. Purwantini, and L. Daniels Purification of a novel coenzyme F420-dependent glucose-6-phosphate dehydrogenase from Mycobacterium smegmatis J. Bacteriol. 178 1996 2861 2866
76. S.T. Cole, K. Eiglmeier, J. Parkhill, K.D. James, N.R. Thomson, P.R. Wheeler, N. Honore, T. Garnier, C. Churcher, D. Harris, K. Mungall, D. Basham, D. Brown, T. Chillingworth, R. Connor, R.M. Davies, K. Devlin, S. Duthoy, T. Feltwell, A. Fraser, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, C. Lacroix, J. Maclean, S. Moule, L. Murphy, K. Oliver, M.A. Quail, M.A. Rajandream, K.M. Rutherford, S. Rutter, K. Seeger, S. Simon, M. Simmonds, J. Skelton, R. Squares, S. Squares, K. Stevens, K. Taylor, S. Whitehead, J.R. Woodward, and B.G. Barrell Massive gene decay in the leprosy bacillus Nature 409 2001 1007 1011
77. T. Yamaguchi, Y. Komoda, and H. Nakajima Biliverdin-IX alpha reductase and biliverdin-IX beta reductase from human liver Purification and characterization J. Biol. Chem. 269 1994 24343 24348
78. W.M. Schluchter, and A.N. Glazer Biliverdin Reductase: conversion of biliverdin to bilirubin is important for normal phycobiliprotein biosynthesis J. Biol. Chem. 272 1997 13562 13569
79. H. Målen, F.S. Berven, K.E. Fladmark, and H.G. Wiker Comprehensive analysis of exported proteins from Mycobacterium tuberculosis H37Rv Proteomics 7 2007 1702 1718
80. G. Bashiri, E.F. Perkowski, A.P. Turner, M.E. Feltcher, M. Braunstein, and E.N. Baker Tat-Dependent Translocation of an F(420)-Binding Protein of Mycobacterium tuberculosis PLoS One 7 2012 e45003
81. S. Nambu, T. Matsui, C.W. Goulding, S. Takahashi, and M. Ikeda-Saito A new way to degrade heme: the mycobacterium tuberculosis enzyme mhud catalyzes heme degradation without generating CO J. Biol. Chem. 288 2013 10101 10109
82. A.B. Graves, R.P. Morse, A. Chao, A. Iniguez, C.W. Goulding, and M.D. Liptak Crystallographic and Spectroscopic Insights into Heme Degradation by Mycobacterium tuberculosis MhuD Inorg. Chem. 53 2014 5931 5940
83. G.M. Cook, C. Greening, K. Hards, and M. Berney Chapter One - Energetics of Pathogenic Bacteria and Opportunities for Drug Development K.P. Robert, Adv. Microb. Physiol. 65 2014 Academic Press 1 62
84. J. Daniel, H. Maamar, C. Deb, T.D. Sirakova, and P.E. Kolattukudy Mycobacterium tuberculosis uses host triacylglycerol to accumulate lipid droplets and acquires a dormancy-like phenotype in lipid-loaded macrophages PLoS Pathog. 7 2011 e1002093
85. J.E. Galagan, P. Sisk, C. Stolte, B. Weiner, M. Koehrsen, F. Wymore, T.B.K. Reddy, J.D. Zucker, R. Engels, M. Gellesch, J. Hubble, H. Jin, L. Larson, M. Mao, M. Nitzberg, J. White, Z.K. Zachariah, G. Sherlock, C.A. Ball, and G.K. Schoolnik TB database 2010: Overview and update Tuberculosis 90 2010 225 235
86. J. Pei, B.-H. Kim, and N.V. Grishin PROMALS3D: a tool for multiple protein sequence and structure alignments Nucleic Acids Res. 36 2008 2295 2300
87. K. Tamura, G. Stecher, D. Peterson, A. Filipski, and S. Kumar MEGA6: Molecular Evolutionary Genetics Analysis version 6.0 Mol. Biol. Evol. 30 2013 2725 2729
88. L. Fu, B. Niu, Z. Zhu, S. Wu, and W. Li CD-HIT: accelerated for clustering the next-generation sequencing data Bioinformatics 28 2012 3150 3152
89. P. Shannon, A. Markiel, O. Ozier, N.S. Baliga, J.T. Wang, D. Ramage, N. Amin, B. Schwikowski, and T. Ideker Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Genome Res. 13 2003 2498 2504
90. D.G. Gibson, L. Young, R.-Y. Chuang, J.C. Venter, C.A. Hutchison, and H.O. Smith Enzymatic assembly of DNA molecules up to several hundred kilobases Nat. Methods 6 2009 343 345
91. K.D. Tartof, and C.A. Hobbs Improved media for growing plasmid and cosmid clones Focus 9 1987 12
92. M.H. Hefti, F.J. Milder, S. Boeren, J. Vervoort, and W.J.H. van Berkel A His-tag based immobilization method for the preparation and reconstitution of apoflavoproteins Biochimi. Biophys. Acta 1619 2003 139 143
93. W. Kabsch XDS. Acta Crystallogr. D Biol. Crystallogr. 66 2010 125 132
94. N. Collaborative Computational Project The CCP4 Suite: Programs for Protein Crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
95. P.R. Evans, and G.N. Murshudov How good are my data and what is the resolution? Acta Crystallogr. D Biol. Crystallogr. 69 2013 1204 1214
96. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
97. K. Cowtan Fitting molecular fragments into electron density Acta Crystallogr. D Biol. Crystallogr. 64 2008 83 89
98. C.G. Carolan, and V.S. Lamzin Automated identification of crystallographic ligands using sparse-density representations Acta Crystallogr. D Biol. Crystallogr. 70 2014 1844 1853
99. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
100. G.N. Murshudov, P. Skubak, A.A. Lebedev, N.S. Pannu, R.A. Steiner, R.A. Nicholls, M.D. Winn, F. Long, and A.A. Vagin REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr. D Biol. Crystallogr. 67 2011 355 367
101. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.-W. Hung, G.J. Kapral, R.W. Grosse-Kunstleve, A.J. McCoy, N.W. Moriarty, R. Oeffner, R.J. Read, D.C. Richardson, J.S. Richardson, T.C. Terwilliger, and P.H. Zwart PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
102. M.H.M. Olsson, C.R. Søndergaard, M. Rostkowski, and J.H. Jensen PROPKA3: Consistent Treatment of Internal and Surface Residues in Empirical pKa Predictions J. Chem. Theory Comput. 7 2011 525 537
103. J.J. Irwin, T. Sterling, M.M. Mysinger, E.S. Bolstad, and R.G. Coleman ZINC: A Free Tool to Discover Chemistry for Biology J. Chem. Inf. Model. 52 2012 1757 1768
104. M.L. Verdonk, J.C. Cole, M.J. Hartshorn, C.W. Murray, and R.D. Taylor Improved protein-ligand docking using GOLD Proteins 52 2003 609 623
105. O. Trott, and A.J. Olson AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading J. Comput. Chem. 31 2010 455 461
106. G.M. Morris, R. Huey, W. Lindstrom, M.F. Sanner, R.K. Belew, D.S. Goodsell, and A.J. Olson AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility J. Comput. Chem. 30 2009 2785 2791
107. 420 production in Mycobacterium smegmatis PLoS One 5 2010 e15803
108. 420-5,6 by using Mycobacterium smegmatis Appl. Environ. Microbiol. 68 2002 5750 5755
109. 420 and related compounds Anal. Biochem. 205 1992 342 350
110. D.B. Chen, D. Jason, Y. Kawasaki, J. Bommer, and J.Y. Takemoto Scalable production of biliverdin IXα by Escherichia coli BMC Biochem. 12 2012 89