University of Groningen

Structural studies into ketosteroid dehydrogenases and S-selective ω-transaminasesvan Oosterwijk, Cornelis Christiaan

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References Abul-Hajj YJ (1978) Isolation of vitamin K2(35) from Nocardia restrictus

and Corynebacterium simplex. A natural electron acceptor in microbial steroid ring A dehydrogenations. J.Biol.Chem. 253: 2356–2360

Bamford V, Dobbin PS, Richardson DJ & Hemmings AM (1999) Open conformation of a flavocytochrome c3 fumarate reductase. Nat.Struct.Biol. 6: 1104–1107

Battye TGG, Kontogiannis L, Johnson O, Powell HR & Leslie AGW (2011) iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 67: 271–281

Berkovitch F, Behshad E, Tang K-H, Enns EA, Frey PA & Drennan CL (2004) A locking mechanism preventing radical damage in the absence of substrate, as revealed by the X-ray structure of lysine 5,6-aminomutase. Proc.Natl.Acad.Sci.U.S.A. 101: 15870–15875

Birkenmaier A, Holert J, Erdbrink H, Moeller HM, Friemel A, Schoenenberger R, Suter MJF, Klebensberger J & Philipp B (2007) Biochemical and genetic investigation of initial reactions in aerobic degradation of the bile acid cholate in pseudomonas sp. strain chol1. J.Bacteriol. 189: 7165–7173

Bragin EY, Shtratnikova VY, Dovbnya DV, Schelkunov MI, Pekov YA, Malakho SG, Egorova OV, Ivashina TV, Sokolov SL, Ashapkin VV & Donova MV (2013) Comparative analysis of genes encoding key steroid core oxidation enzymes in fast-growing Mycobacterium spp. strains. J. Steroid Biochem. Mol. Biol. 138: 41–53

Brzostek A, Pawelczyk J, Rumijowska-Galewicz A, Dziadek B & Dziadek J (2009) Mycobacterium tuberculosis is able to accumulate and utilize cholesterol. J.Bacteriol. 191: 6584–6591

Brzostek A, Rumijowska-Galewicz A, Dziadek B, Wojcik EA & Dziadek J (2013) ChoD and HsdD can be dispensable for cholesterol degradation in mycobacteria. J. Steroid Biochem. Mol. Biol. 134: 1–7

Capyk JK, D'Angelo I, Strynadka NC & Eltis LD (2009) Characterization of 3-ketosteroid 9{alpha}-hydroxylase, a Rieske oxygenase in the cholesterol degradation pathway of Mycobacterium tuberculosis. J.Biol.Chem. 284: 9937–9946

118

Carere J, McKenna SE, Kimber MS & Seah SYK (2013) Characterization of an aldolase-dehydrogenase complex from the cholesterol degradation pathway of Mycobacterium tuberculosis. Biochemistry 52: 3502–3511

Casabon I, Swain K, Crowe AM, Eltis LD & Mohn WW (2014) Actinobacterial acyl coenzyme A synthetases involved in steroid side-chain catabolism. J.Bacteriol. 196: 579–587

Casasnovas R, Salvà A, Frau J, Donoso J & Muñoz F (2009) Theoretical study on the distribution of atomic charges in the Schiff bases of 3-hydroxypyridine-4-aldehyde and alanine. The effect of the protonation state of the pyridine and imine nitrogen atoms. Chemical Physics 355: 149–156

Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS & Richardson DC (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66: 12–21

Couñago RM, Davlieva M, Strych U, Hill RE & Krause KL (2009) Biochemical and structural characterization of alanine racemase from Bacillus anthracis (Ames). BMC Struct. Biol. 9: 53

Doherty MK, Pealing SL, Miles CS, Moysey R, Taylor P, Walkinshaw MD, Reid GA & Chapman SK (2000) Identification of the active site acid/base catalyst in a bacterial fumarate reductase: a kinetic and crystallographic study. Biochemistry 39: 10695–10701

Donova MV & Egorova OV (2012) Microbial steroid transformations: current state and prospects. Appl. Microbiol. Biotechnol. 94: 1423–1447

Dresen C, Lin LY-C, D'Angelo I, Tocheva EI, Strynadka N & Eltis LD (2010) A flavin-dependent monooxygenase from Mycobacterium tuberculosis involved in cholesterol catabolism. J.Biol.Chem. 285: 22264–22275

Dunathan HC (1966) Conformation and reaction specificity in pyridoxal phosphate enzymes. Proc.Natl.Acad.Sci.U.S.A. 55: 712–716

Eliot AC & Kirsch JF (2004) Pyridoxal phosphate enzymes: mechanistic, structural, and evolutionary considerations. Annu. Rev. Biochem. 73: 383–415

119

Emsley P, Lohkamp B, Scott WG & Cowtan K (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66: 486–501

Evans P (2006) Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62: 72–82

Fagan RL, Nelson MN, Pagano PM & Palfey BA (2006) Mechanism of flavin reduction in class 2 dihydroorotate dehydrogenases. Biochemistry 45: 14926–14932

Fernandes P, Cruz A, Angelova B, Pinheiro HM & Cabral J (2003) Microbial conversion of steroid compounds: recent developments. Enzyme Microb Tech 32: 688–705

Florin C, Kohler T, Grandguillot M & Plesiat P (1996) Comamonas testosteroni 3-ketosteroid-delta4(5alpha)-dehydrogenase: gene and protein characterization. J.Bacteriol. 178: 3322–3330

Ford GC, Eichele G & Jansonius JN (1980) Three-dimensional structure of a pyridoxal-phosphate-dependent enzyme, mitochondrial aspartate aminotransferase. Proc.Natl.Acad.Sci.U.S.A. 77: 2559–2563

Fraaije MW & Mattevi A (2000) Flavoenzymes: diverse catalysts with recurrent features. Trends Biochem.Sci. 25: 126–132

Fraaije MW, van den Heuvel RH, Van Berkel WJ & Mattevi A (1999) Covalent flavinylation is essential for efficient redox catalysis in vanillyl-alcohol oxidase. J.Biol.Chem. 274: 35514–35520

Fuchs M, Koszelewski D, Tauber K, Kroutil W & Faber K (2010) Chemoenzymatic asymmetric total synthesis of (S)-Rivastigmine using omega-transaminases. Chem. Commun. (Camb.) 46: 5500–5502

Fujii C, Morii S, Kadode M, Sawamoto S, Iwami M & Itagaki E (1999) Essential tyrosine residues in 3-ketosteroid-Delta(1)-dehydrogenase from Rhodococcus rhodochrous. J.Biochem.(Tokyo). 126: 662–667

Galkin A, Kulakova L, Yoshimura T, Soda K & Esaki N (1997) Synthesis of optically active amino acids from alpha-keto acids with Escherichia coli cells expressing heterologous genes. Appl.Environ.Microbiol. 63: 4651–4656

120

García JL, Uhía I & Galán B (2012) Catabolism and biotechnological applications of cholesterol degrading bacteria. Microb Biotechnol 5: 679–699

Ghisla S & Massey V (1989) Mechanisms of flavoprotein-catalyzed reactions. Eur.J.Biochem. 181: 1–17

Ghisla S, Massey V, Lhoste JM & Mayhew SG (1974) Fluorescence and optical characteristics of reduced flavines and flavoproteins. Biochemistry 13: 589–597

Grishin NV, Phillips MA & Goldsmith EJ (1995) Modeling of the spatial structure of eukaryotic ornithine decarboxylases. Protein Sci. 4: 1291–1304

Guan L-J, Ohtsuka J, Okai M, Miyakawa T, Mase T, Zhi Y, Hou F, Ito N, Iwasaki A, Yasohara Y & Tanokura M (2015) A new target region for changing the substrate specificity of amine transaminases. Sci Rep 5: 10753

Hatta T, Wakabayashi T & Itagaki E (1991) 3-keto-5 alpha-steroid-delta 4-dehydrogenase from Nocardia corallina: purification and characterization. J.Biochem.(Tokyo). 109: 581–586

Haußmann U, Wolters DA, Fränzel B, Eltis LD & Poetsch A (2013) Physiological adaptation of the Rhodococcus jostii RHA1 membrane proteome to steroids as growth substrates. J. Proteome Res. 12: 1188–1198

Hirotsu K, Goto M, Okamoto A & Miyahara I (2005) Dual substrate recognition of aminotransferases. Chem Rec 5: 160–172

Holm L & Sander C (1996) Mapping the protein universe. Science 273: 595–603

Horinouchi M, Hayashi T & Kudo T (2012) Steroid degradation in Comamonas testosteroni. J. Steroid Biochem. Mol. Biol. 129: 4–14

Horinouchi M, Hayashi T, Yamamoto T & Kudo T (2003) A new bacterial steroid degradation gene cluster in Comamonas testosteroni TA441 which consists of aromatic-compound degradation genes for seco-steroids and 3-ketosteroid dehydrogenase genes. Appl.Environ.Microbiol. 69: 4421–4430

121

Höhne M & Bornscheuer UT (2009) Biocatalytic Routes to Optically Active Amines. ChemCatChem 1: 42–51

Höhne M, Kühl S, Robins K & Bornscheuer UT (2008) Efficient asymmetric synthesis of chiral amines by combining transaminase and pyruvate decarboxylase. Chembiochem 9: 363–365

Höhne M, Schätzle S, Jochens H, Robins K & Bornscheuer UT (2010) Rational assignment of key motifs for function guides in silico enzyme identification. Nat. Chem. Biol. 6: 807–813

Humble MS, Cassimjee KE, Håkansson M, Kimbung YR, Walse B, Abedi V, Federsel H-J, Berglund P & Logan DT (2012) Crystal structures of the Chromobacterium violaceum ω-transaminase reveal major structural rearrangements upon binding of coenzyme PLP. FEBS J. 279: 779–792

Hyde CC, Ahmed SA, Padlan EA, Miles EW & Davies DR (1988) Three-dimensional structure of the tryptophan synthase alpha 2 beta 2 multienzyme complex from Salmonella typhimurium. J.Biol.Chem. 263: 17857–17871

Ingram CU, Bommer M, Smith MEB, Dalby PA, Ward JM, Hailes HC & Lye GJ (2006) One-pot synthesis of amino-alcohols using a de-novo transketolase and β-alanine: Pyruvate transaminase pathway in Escherichia coli. Biotechnol. Bioeng. 96: 559–569

Itagaki E, Matushita H & Hatta T (1990a) Steroid transhydrogenase activity of 3-Ketosteroid-Delta-1-Dehydrogenase from Nocardia corallina. J.Biochem.(Tokyo). 108: 122–127

Itagaki E, Wakabayashi T & Hatta T (1990b) Purification and characterization of 3-ketosteroid-delta 1-dehydrogenase from Nocardia corallina. Biochim. Biophys. Acta 1038: 60–67

Iverson TM (2002) Crystallographic Studies of the Escherichia coli Quinol-Fumarate Reductase with Inhibitors Bound to the Quinol-binding Site. J.Biol.Chem. 277: 16124–16130

Jackson LK, Goldsmith EJ & Phillips MA (2003) X-ray structure determination of Trypanosoma brucei ornithine decarboxylase bound to D-ornithine and to G418: insights into substrate binding and ODC conformational flexibility. J.Biol.Chem. 278: 22037–22043

122

Jansonius JN (1998) Structure, evolution and action of vitamin B6-dependent enzymes. Curr. Opin. Struct. Biol. 8: 759–769

Jaroszewski L, Rychlewski L, Li Z, Li W & Godzik A (2005) FFAS03: a server for profile-profile sequence alignments. Nucleic Acids Res. 33: W284–8

Kabsch W (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66: 125–132

Kabsch W & Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577–2637

Kariskoga C (2007) Thermostable omega-transaminases.

Kim J, Kyung D, Yun H, Cho B-K, Seo J-H, Cha M & Kim B-G (2007) Cloning and characterization of a novel beta-transaminase from Mesorhizobium sp. strain LUK: a new biocatalyst for the synthesis of enantiomerically pure beta-amino acids. Appl.Environ.Microbiol. 73: 1772–1782

Kisiela M, Skarka A, Ebert B & Maser E (2012) Hydroxysteroid dehydrogenases (HSDs) in bacteria: a bioinformatic perspective. J. Steroid Biochem. Mol. Biol. 129: 31–46

Knol J, Bodewits K, Hessels GI, Dijkhuizen L & van der Geize R (2008) 3-Keto-5alpha-steroid Delta(1)-dehydrogenase from Rhodococcus erythropolis SQ1 and its orthologue in Mycobacterium tuberculosis H37Rv are highly specific enzymes that function in cholesterol catabolism. Biochem. J. 410: 339–346

Kobayashi K, Miyazawa S, Terahara A, Mishima H & Kurihara H (1976) Gabaculine: γ-aminobutyrate aminotransferase inhibitor of microbial origin. Tetrahedron Letters 17: 537–540

Kochhar S & Christen P (1992) Mechanism of racemization of amino acids by aspartate aminotransferase. Eur.J.Biochem. 203: 563–569

Kohls H, Steffen-Munsberg F & Höhne M (2014) Recent achievements in developing the biocatalytic toolbox for chiral amine synthesis. Curr Opin Chem Biol 19: 180–192

123

Konarev PV, Volkov VV & Sokolova AV (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J Appl Crystallogr 36: 1277–1282

Koszelewski D, Göritzer M, Clay D, Seisser B & Kroutil W (2010a) Synthesis of Optically Active Amines Employing Recombinant ω-Transaminases in E. coli Cells. ChemCatChem 2: 73–77

Koszelewski D, Lavandera I, Clay D, Rozzell D & Kroutil W (2008) Asymmetric Synthesis of Optically Pure Pharmacologically Relevant Amines Employing ω-Transaminases. Adv Synth Catal 350: 2761–2766

Koszelewski D, Tauber K, Faber K & Kroutil W (2010b) omega-Transaminases for the synthesis of non-racemic alpha-chiral primary amines. Trends Biotechnol. 28: 324–332

Krissinel E (2010) Crystal contacts as nature's docking solutions. J Comput Chem 31: 133–143

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

Kyte J (1995) Chapter Two - Coenzymes. In Mechanism in Protein chemistry pp 53–62.

Lack N, Lowe ED, Liu J, Eltis LD, Noble MEM, Sim E & Westwood IM (2008) Structure of HsaD, a steroid-degrading hydrolase, from Mycobacterium tuberculosis. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 64: 2–7

Langer GG, Cohen SX, Lamzin VS & Perrakis A (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nature Protocols 3: 1171–1179

Lebedev AA, Young P, Isupov MN, Moroz OV, Vagin AA & Murshudov GN (2012) JLigand: a graphical tool for the CCP4 template-restraint library. Acta Crystallogr. D Biol. Crystallogr. 68: 431–440

Lepore BW, Liu D, Peng Y, Fu M, Yasuda C, Manning JM, Silverman RB & Ringe D (2010) Chiral discrimination among aminotransferases: inactivation by 4-amino-4,5-dihydrothiophenecarboxylic acid. Biochemistry 49: 3138–3147

124

Levy HR & Talalay P (1959a) Bacterial oxidation of steroids I. Ring A dehydrogenations by intact cells. J.Biol.Chem. 234: 2009–2013

Levy HR & Talalay P (1959b) Bacterial oxidation of steroids II. Studies on the enzymatic mechanism of ring A dehydrogenation. J.Biol.Chem. 234: 2014–2021

Leys D, Tsapin AS, Nealson KH, Meyer TE, Cusanovich MA & Van Beeumen JJ (1999) Structure and mechanism of the flavocytochrome c fumarate reductase of Shewanella putrefaciens MR-1. Nat.Struct.Biol. 6: 1113–1117

Li J, Vrielink A, Brick P & Blow DM (1993) Crystal structure of cholesterol oxidase complexed with a steroid substrate: implications for flavin adenine dinucleotide dependent alcohol oxidases. Biochemistry 32: 11507–11515

Lyubimov AY, Heard K, Tang H, Sampson NS & Vrielink A (2007) Distortion of flavin geometry is linked to ligand binding in cholesterol oxidase. Protein Sci. 16: 2647–2656

Malik MS, Park E-S & Shin J-S (2012a) Features and technical applications of ω-transaminases. Appl. Microbiol. Biotechnol. 94: 1163–1171

Malik MS, Park E-S & Shin J-S (2012b) Features and technical applications of ω-transaminases. Appl. Microbiol. Biotechnol. 94: 1163–1171

Martin Hallberg B, Leitner C, Haltrich D & Divne C (2004) Crystal Structure of the 270 kDa Homotetrameric Lignin-degrading Enzyme Pyranose 2-Oxidase. J. Mol. Biol. 341: 781–796

Massey V & Ghisla S (1974) Role of Charge-Transfer Interactions in Flavoprotein Catalysis. Ann Ny Acad Sci 227: 446–465

Matsushita H & Itagaki E (1992) Essential histidine residue in 3-ketosteroid-delta 1-dehydrogenase. J.Biochem.(Tokyo). 111: 594–599

Mattevi A (1998) The PHBH fold: Not only flavoenzymes. Biophys.Chem. 70: 217–222

Mattevi A, Fraaije MW, Mozzarelli A, Olivi L, Coda A & Van Berkel WJ (1997) Crystal structures and inhibitor binding in the octameric flavoenzyme vanillyl-alcohol oxidase: the shape of the active-site cavity controls substrate specificity. Structure 5: 907–920

125

Mattevi A, Tedeschi G, Bacchella L, Coda A, Negri A & Ronchi S (1999) Structure of L-aspartate oxidase: implications for the succinate dehydrogenase/fumarate reductase oxidoreductase family. Structure 7: 745–756

Matthews BW (1968) Solvent content of protein crystals. J. Mol. Biol. 33: 491–497

McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC & Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658–674

McLeod MP, Warren RL, Hsiao WWL, Araki N, Myhre M, Fernandes C, Miyazawa D, Wong W, Lillquist AL, Wang D, Dosanjh M, Hara H, Petrescu A, Morin RD, Yang G, Stott JM, Schein JE, Shin H, Smailus D, Siddiqui AS, et al (2006) The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc.Natl.Acad.Sci.U.S.A. 103: 15582–15587

McPhalen CA, Vincent MG & Jansonius JN (1992) X-ray structure refinement and comparison of three forms of mitochondrial aspartate aminotransferase. J. Mol. Biol. 225: 495–517

Medentsev AG, Arinbasarova AY, Koshcheyenko KA, Akimenko VK & Skryabin GK (1985) Regulation of 3-ketosteroid-1-en-dehydrogenase activity of Arthrobacter globiformis cells by a respiratory chain. J. Steroid Biochem. 23: 365–368

Mehta PK, Hale TI & Christen P (1993) Aminotransferases: demonstration of homology and division into evolutionary subgroups. Eur.J.Biochem. 214: 549–561

Metzler CM, Harris AG & Metzler DE (1988) Spectroscopic studies of quinonoid species from pyridoxal 5'-phosphate. Biochemistry 27: 4923–4933

Miroux B & Walker JE (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260: 289–298

Mohn WW, van der Geize R, Stewart GR, Okamoto S, Liu J, Dijkhuizen L & Eltis LD (2008) The actinobacterial mce4 locus encodes a steroid transporter. J.Biol.Chem. 283: 35368–35374

126

Mohn WW, Wilbrink MH, Casabon I, Stewart GR, Liu J, van der Geize R & Eltis LD (2012) Gene cluster encoding cholate catabolism in Rhodococcus spp. J.Bacteriol. 194: 6712–6719

Molnár I, Choi KP, Yamashita M & Murooka Y (1995) Molecular cloning, expression in Streptomyces lividans, and analysis of a gene cluster from Arthrobacter simplex encoding 3-ketosteroid-delta 1-dehydrogenase, 3-ketosteroid-delta 5-isomerase and a hypothetical regulatory protein. Mol.Microbiol. 15: 895–905

Morii S, Fujii C, Miyoshi T, Iwami M & Itagaki E (1998) 3-Ketosteroid-delta1-dehydrogenase of Rhodococcus rhodochrous: sequencing of the genomic DNA and hyperexpression, purification, and characterization of the recombinant enzyme. J.Biochem.(Tokyo). 124: 1026–1032

Moshides JS (1988) Enzymic determination of the free cholesterol fraction of high-density lipoprotein in plasma with use of 2,4,6-tribromo-3-hydroxybenzoic acid. Clin. Chem. 34: 1799–1804

Murshudov GN, Skubák P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F & Vagin AA (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67: 355–367

Ouellet H, Guan S, Johnston JB, Chow ED, Kells PM, Burlingame AL, Cox JS, Podust LM & de Montellano PRO (2010) Mycobacterium tuberculosis CYP125A1, a steroid C27 monooxygenase that detoxifies intracellularly generated cholest-4-en-3-one. Mol.Microbiol. 77: 730–742

Ouellet H, Johnston JB & de Montellano PRO (2011) Cholesterol catabolism as a therapeutic target in Mycobacterium tuberculosis. 19: 530–539

Pandey AK & Sassetti CM (2008) Mycobacterial persistence requires the utilization of host cholesterol. Proc.Natl.Acad.Sci.U.S.A. 105: 4376–4380

Park E, Kim M & Shin J-S (2010) One-Pot Conversion of L-Threonine into L-Homoalanine: Biocatalytic Production of an Unnatural Amino Acid from a Natural One. Adv Synth Catal 352: 3391–3398

127

Park E-S, Park SR, Han SW, Dong JY & Shin J-S (2014) Structural Determinants for the Non-Canonical Substrate Specificity of the ω-Transaminase from Paracoccus denitrificans. Adv Synth Catal 356: 212–220

Peisach D, Chipman DM, Van Ophem PW, Manning JM & Ringe D (1998) Crystallographic study of steps along the reaction pathway of D-amino acid aminotransferase. Biochemistry 37: 4958–4967

Percudani R & Peracchi A (2003) A genomic overview of pyridoxal-phosphate-dependent enzymes. EMBO Rep. 4: 850–854

Percudani R & Peracchi A (2009) The B6 database: a tool for the description and classification of vitamin B6-dependent enzymatic activities and of the corresponding protein families. BMC Bioinformatics 10: 273

Petrusma M, Hessels G, Dijkhuizen L & van der Geize R (2011) Multiplicity of 3-Ketosteroid-9α-Hydroxylase enzymes in Rhodococcus rhodochrous DSM43269 for specific degradation of different classes of steroids. J.Bacteriol. 193: 3931–3940

Rando RR (1977) Mechanism of the irreversible inhibition of gamma-aminobutyric acid-alpha-ketoglutaric acid transaminase by the neutrotoxin gabaculine. Biochemistry 16: 4604–4610

Rausch C, Lerchner A, Schiefner A & Skerra A (2013) Crystal structure of the ω-aminotransferase from Paracoccus denitrificansand its phylogenetic relationship with other class III amino- transferases that have biotechnological potential. Proteins 81: 774–787

Reibenspies JH, Guo F & Rizzo CJ (2000) X-ray crystal structures of conformationally biased flavin models. Org. Lett. 2: 903–906

Rengarajan J, Bloom BR & Rubin EJ (2005) Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc.Natl.Acad.Sci.U.S.A. 102: 8327–8332

Rhee S, Parris KD, Ahmed SA, Miles EW & Davies DR (1996) Exchange of K+ or Cs+ for Na+ induces local and long-range changes in the three-dimensional structure of the tryptophan synthase alpha2beta2 complex. Biochemistry 35: 4211–4221

128

Richter N, Simon RC, Kroutil W, Ward JM & Hailes HC (2014) Synthesis of pharmaceutically relevant 17-α-amino steroids using an ω-transaminase. Chem. Commun. (Camb.) 50: 6098–6100

Ringold HJ, Stefanovic V & Hayano M (1963) Concerning Stereochemistry and Mechanism of Bacterial C-1,2 Dehydrogenation of Steroids. J.Biol.Chem. 238: 1960–1965

Rohman A, van Oosterwijk N & Dijkstra BW (2012) Purification, crystallization and preliminary X-ray crystallographic analysis of 3-ketosteroid Δ(1)-dehydrogenase from Rhodococcus erythropolis SQ1. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 68: 551–556

Rohman A, van Oosterwijk N, Thunnissen A-MWH & Dijkstra BW (2013) Crystal structure and site-directed mutagenesis of 3-ketosteroid Δ1-dehydrogenase from Rhodococcus erythropolis SQ1 explain its catalytic mechanism. J.Biol.Chem. 288: 35559–35568

Rosas-Magallanes V, Stadthagen-Gomez G, Rauzier J, Barreiro LB, Tailleux L, Boudou F, Griffin R, Nigou J, Jackson M, Gicquel B & Neyrolles O (2007) Signature-tagged transposon mutagenesis identifies novel Mycobacterium tuberculosis genes involved in the parasitism of human macrophages. Infect.Immun. 75: 504–507

Rosłoniec KZ, Wilbrink MH, Capyk JK, Mohn WW, Ostendorf M, van der Geize R, Dijkhuizen L & Eltis LD (2009) Cytochrome P450 125 (CYP125) catalyses C26-hydroxylation to initiate sterol side-chain degradation in Rhodococcus jostii RHA1. Mol.Microbiol. 74: 1031–1043

Ryan A, Keany S, Eleftheriadou O, Ballet R, Cheng H-Y & Sim E (2014) Mechanism-based inhibition of HsaD: a C-C bond hydrolase essential for survival of Mycobacterium tuberculosis in macrophage. FEMS Microbiol. Lett. 350: 42–47

Savile CK, Janey JM, Mundorff EC, Moore JC, Tam S, Jarvis WR, Colbeck JC, Krebber A, Fleitz FJ, Brands J, Devine PN, Huisman GW & Hughes GJ (2010) Biocatalytic Asymmetric Synthesis of Chiral Amines from Ketones Applied to Sitagliptin Manufacture. Science 329: 305–309

Sayer C, Isupov MN & Littlechild JA (2007) Crystallization and preliminary X-ray diffraction analysis of omega-amino acid:pyruvate transaminase from Chromobacterium violaceum. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 63: 117–119

129

Sayer C, Isupov MN, Westlake A & Littlechild JA (2013) Structural studies of Pseudomonas and Chromobacterium ω-aminotransferases provide insights into their differing substrate specificity. Acta Crystallogr. D Biol. Crystallogr. 69: 564–576

Sayer C, Martinez-Torres RJ, Richter N, Isupov MN, Hailes HC, Littlechild JA & Ward JM (2014) The substrate specificity, enantioselectivity and structure of the (R)-selective amine : pyruvate transaminase from Nectria haematococca. FEBS J. 281: 2240–2253

Schrödinger The PyMOL Molecular Graphics System.

Schüttelkopf AW & van Aalten D (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr. D Biol. Crystallogr. 60: 1355–1363

Shaw JP, Petsko GA & Ringe D (1997) Determination of the structure of alanine racemase from Bacillus stearothermophilus at 1.9-A resolution. Biochemistry 36: 1329–1342

Shin J-S & Kim B-G (2002) Exploring the active site of amine:pyruvate aminotransferase on the basis of the substrate structure-reactivity relationship: how the enzyme controls substrate specificity and stereoselectivity. J. Org. Chem. 67: 2848–2853

Sprang SR, Withers SG, Goldsmith EJ, Fletterick RJ & Madsen NB (1991) Structural basis for the activation of glycogen phosphorylase b by adenosine monophosphate. Science 254: 1367–1371

Steffen-Munsberg F, Vickers C, Thontowi A, Schätzle S, Meinhardt T, Svedendahl Humble M, Land H, Berglund P, Bornscheuer UT & Höhne M (2012a) Revealing the Structural Basis of Promiscuous Amine Transaminase Activity. ChemCatChem 5: 154–157

Steffen-Munsberg F, Vickers C, Thontowi A, Schätzle S, Tumlirsch T, Svedendahl Humble M, Land H, Berglund P, Bornscheuer UT & Höhne M (2012b) Connecting Unexplored Protein Crystal Structures to Enzymatic Function. ChemCatChem 5: 150–153

Sugio S, Petsko GA, Manning JM, Soda K & Ringe D (1995) Crystal structure of a D-amino acid aminotransferase: how the protein controls stereoselectivity. Biochemistry 34: 9661–9669

130

Sun F, Huo X, Zhai Y, Wang A, Xu J, Su D, Bartlam M & Rao Z (2005) Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121: 1043–1057

Sun S & Toney MD (1999) Evidence for a two-base mechanism involving tyrosine-265 from arginine-219 mutants of alanine racemase. Biochemistry 38: 4058–4065

Svergun DI, Petoukhov MV & Koch MH (2001) Determination of domain structure of proteins from X-ray solution scattering. Biophys. J. 80: 2946–2953

Taylor P, Pealing SL, Reid GA, Chapman SK & Walkinshaw MD (1999) Structural and mechanistic mapping of a unique fumarate reductase. Nat.Struct.Biol. 6: 1108–1112

Terwilliger TC (2000) Maximum-likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. 56: 965–972

Thomsen M, Skalden L, Palm GJ, Höhne M, Bornscheuer UT & Hinrichs W (2014) Crystallographic characterization of the (R)-selective amine transaminase from Aspergillus fumigatus. Acta Crystallogr. D Biol. Crystallogr. 70: 1086–1093

Toney MD (2005) Reaction specificity in pyridoxal phosphate enzymes. Arch. Biochem. Biophys. 433: 279–287

Toney MD (2011a) Pyridoxal phosphate enzymology. Biochim. Biophys. Acta 1814: 1405–1406

Toney MD (2011b) Controlling reaction specificity in pyridoxal phosphate enzymes. Biochim. Biophys. Acta 1814: 1407–1418

Truppo MD, Rozzell JD & Turner NJ (2009) Efficient production of enantiomerically pure chiral amines at concentrations of 50 g/L using transaminases. Org. Process Res. Dev. 14: 234–237

Tufvesson P, Lima-Ramos J, Jensen JS, Al-Haque N, Neto W & Woodley JM (2011) Process considerations for the asymmetric synthesis of chiral amines using transaminases. Biotechnol. Bioeng. 108: 1479–1493

Vallon O (2000) New sequence motifs in flavoproteins: evidence for common ancestry and tools to predict structure. Proteins 38: 95–114

131

van der Geize R & Dijkhuizen L (2004) Harnessing the catabolic diversity of rhodococci for environmental and biotechnological applications. Curr. Opin. Microbiol. 7: 255–261

van der Geize R, Grommen AWF, Hessels GI, Jacobs AAC & Dijkhuizen L (2011) The steroid catabolic pathway of the intracellular pathogen Rhodococcus equi is important for pathogenesis and a target for vaccine development. PLoS.Pathog. 7: e1002181

van der Geize R, Yam K, Heuser T, Wilbrink MH, Hara H, Anderton MC, Sim E, Dijkhuizen L, Davies JE, Mohn WW & Eltis LD (2007) A gene cluster encoding cholesterol catabolism in a soil actinomycete provides insight into Mycobacterium tuberculosis survival in macrophages. Proc.Natl.Acad.Sci.U.S.A. 104: 1947–1952

van Montfort RLM & Workman P (2009) Structure-based design of molecular cancer therapeutics. Trends Biotechnol. 27: 315–328

van Oosterwijk N, Knol J, Dijkhuizen L, van der Geize R & Dijkstra BW (2011) Cloning, overexpression, purification, crystallization and preliminary X-ray analysis of 3-ketosteroid Δ(4)-(5α)-dehydrogenase from Rhodococcus jostii RHA1. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 67: 1269–1273

van Oosterwijk N, Knol J, Dijkhuizen L, van der Geize R & Dijkstra BW (2012) Structure and catalytic mechanism of 3-ketosteroid-Delta4-(5α)-dehydrogenase from Rhodococcus jostii RHA1 genome. J.Biol.Chem. 287: 30975–30983

Watanabe N, Sakabe K, Sakabe N, Higashi T, Sasaki K, Aibara S, Morita Y, Yonaha K, Toyama S & Fukutani H (1989) Crystal structure analysis of omega-amino acid:pyruvate aminotransferase with a newly developed Weissenberg camera and an imaging plate using synchrotron radiation. J.Biochem.(Tokyo). 105: 1–3

Weiss MS (2001) Global indicators of X-ray data quality. J Appl Crystallogr 34: 130–135

Wierenga RK, de Jong RJ, Kalk KH, Hol WG & Drenth J (1979) Crystal structure of p-hydroxybenzoate hydroxylase. J. Mol. Biol. 131: 55–73

132

Wierenga RK, Drenth J & Schulz GE (1983) Comparison of the three-dimensional protein and nucleotide structure of the FAD-binding domain of p-hydroxybenzoate hydroxylase with the FAD- as well as NADPH-binding domains of glutathione reductase. J. Mol. Biol. 167: 725–739

Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AGW, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A & Wilson KS (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67: 235–242

Winn MD, Isupov MN & Murshudov GN (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D Biol. Crystallogr. 57: 122–133

Wovcha MG, Brooks KE & Kominek LA (1979) Evidence for two steroid 1,2-dehydrogenase activities in Mycobacterium fortuitum. Biochim. Biophys. Acta 574: 471–479

Wybenga GG, Crismaru CG, Janssen DB & Dijkstra BW (2012) Structural Determinants of the β-Selectivity of a Bacterial Aminotransferase. J.Biol.Chem. 287: 28495–28502

Yam KC, D'Angelo I, Kalscheuer R, Zhu H, Wang J-X, Snieckus V, Ly LH, Converse PJ, Jacobs WR, Strynadka N & Eltis LD (2009) Studies of a ring-cleaving dioxygenase illuminate the role of cholesterol metabolism in the pathogenesis of Mycobacterium tuberculosis. PLoS.Pathog. 5: e1000344

Yam KC, Okamoto S, Roberts JN & Eltis LD (2011) Adventures in Rhodococcus - from steroids to explosives. Can. J. Microbiol. 57: 155–168

Yankovskaya V, Horsefield R, Törnroth S, Luna-Chavez C, Miyoshi H, Léger C, Byrne B, Cecchini G & Iwata S (2003) Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299: 700–704

Yoshimoto T, Nagai F, Fujimoto J, Watanabe K, Mizukoshi H, Makino T, Kimura K, Saino H, Sawada H & Omura H (2004) Degradation of estrogens by Rhodococcus zopfii and Rhodococcus equi isolates from activated sludge in wastewater treatment plants. Appl.Environ.Microbiol. 70: 5283–5289

133

Łyskowski A, Gruber C, Steinkellner G, Schürmann M, Schwab H, Gruber K & Steiner K (2014) Crystal Structure of an (R)-Selective ω-Transaminase from Aspergillus terreus. PLOS ONE 9: e87350