Co-evolution of HAD phosphatase and hotdog-fold thioesterase domain function in the menaquinone-pathway fusion proteins BF1314 and PG1653

FEBS Letters

Volumn 587, Issue 17, 2013, Pages 2851-2859

  Wang, Min ^a   Song, Feng ^a,c   Wu, Rui ^b,d   Allen, Karen N ^b   Mariano, Patrick S ^a   Dunaway Mariano, Debra ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

^b USA   (United States)

^c SYNGENTA CROP PROTECTION   (United States)

^d IMMUNOGEN INC   (United States)

Author keywords

14 Dihroxynapthoyl coenzyme; A Enzyme evolution; Bacteroides fragilis; Enzyme superfamily; Haloacid dehalogenase; Porphyromonas gingivalis

Indexed keywords

1,4 DIHYDROXYNAPTHOYL COENZYME A; COENZYME A; HALOACID DEHALOGENASE PHOSPHATASE; HOTDOG FOLD THIOESTERASE; HYBRID PROTEIN; MENAQUINONE; PHOSPHATASE; THIOL ESTER HYDROLASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENOME; BACTEROIDES FRAGILIS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME MECHANISM; ENZYME SUBSTRATE COMPLEX; GENE MUTATION; HYDROLYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY;

14-DIHROXYNAPTHOYL-COENZYME A; 2-(N-MORPHOLINO)ETHANESULFONATE; BACTEROIDES FRAGILIS; COA; COENZYME A; ENZYME EVOLUTION; ENZYME SUPERFAMILY; HAD; HALOACID DEHALOGENASE; HEPES; IPTG; ISOPROPYL-1-THIO-Β-D-GALACTOPYRANOSIDE; MES; N-(2-HYDROXYETHYL)PIPERAZINE-N′-2-ETHANESULFONATE; PORPHYROMONAS GINGIVALIS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BACTEROIDETES; BIOSYNTHETIC PATHWAYS; CATALYTIC DOMAIN; EVOLUTION, MOLECULAR; HYDROLASES; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT FUSION PROTEINS; THIOLESTER HYDROLASES; VITAMIN K 2;

BACTEROIDES FRAGILIS; BACTEROIDETES; PORPHYROMONAS GINGIVALIS;

EID: 84883053117     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2013.07.009     Document Type: Article

References (55)

1. G. Ferland Vitamin K, an emerging nutrient in brain function BioFactors 38 2012 151 157
2. M.J. Shearer, and P. Newman Metabolism and cell biology of vitamin K Thromb. Haemost. 100 2008 530 547
3. M.J. Shearer, X. Fu, and S.L. Booth Vitamin K nutrition metabolism, and requirements: current concepts and future research Adv. Nutr: Int. Rev. J. 3 2012 182 195
4. S. Bugel Vitamin K and bone health in adult humans in vitamin K 2008 Elsevier Academic Press Inc San Diego 393 416
5. M.K. Shea, and R.M. Holden Vitamin K status and vascular calcification: evidence from observational and clinical studies Adv. Nutr: Int. Rev. J. 3 2012 158 165
6. G. Ferland Vitamin K and the nervous system: an overview of its actions Adv. Nutr. 3 2012 204 212
7. B. Nowicka, and J. Kruk Occurrence, biosynthesis and function of isoprenoid quinones Biochim. Biophys. Acta (BBA) - Bioenerg. 1797 2010 1587 1605
8. P. Sharma, M.J. Teixeira de Mattos, K.J. Hellingwerf, and M. Bekker On the function of the various quinone species in Escherichia coli FEBS J. 279 2012 3364 3373
9. R. Bentley, and R. Meganathan Biosynthesis of vitamin K (menaquinone) in bacteria Microbiol. Rev. 46 1982 241 280
10. M. Kurosu, and E. Begari Vitamin K2 in electron transport system: are enzymes involved in vitamin K2 biosynthesis promising drug targets? Molecules 15 2010 1531 1553
11. X. Li, N. Liu, H. Zhang, S.E. Knudson, H.J. Li, C.T. Lai, C. Simmerling, R.A. Slayden, and P.J. Tonge CoA adducts of 4-oxo-4-phenylbut-2-enoates: inhibitors of MenB from the M. tuberculosis menaquinone biosynthesis pathway ACS Med. Chem. Lett. 2 2011 818 823
12. X. Lu, R. Zhou, I. Sharma, X. Li, G. Kumar, S. Swaminathan, P.J. Tonge, and D.S. Tan Stable analogues of OSB-AMP: potent inhibitors of MenE, the o-succinylbenzoate-CoA synthetase from bacterial menaquinone biosynthesis ChemBioChem 13 2012 129 136
13. X. Lu, H. Zhang, P.J. Tonge, and D.S. Tan Mechanism-based inhibitors of MenE, an acyl-CoA synthetase involved in bacterial menaquinone biosynthesis Bioorg. Med. Chem. Lett. 18 2008 5963 5966
14. J. Debnath, S. Siricilla, B. Wan, D.C. Crick, A.J. Lenaerts, S.G. Franzblau, and M. Kurosu Discovery of selective menaquinone biosynthesis inhibitors against Mycobacterium tuberculosis J. Med. Chem. 55 2012 3739 3755
15. L. Heide, S. Arendt, and E. Leistner Enzymatic synthesis, characterization, and metabolism of the coenzyme A ester of o-succinylbenzoic acid, an intermediate in menaquinone (vitamin K2) biosynthesis J. Biol. Chem. 257 1982 7396 7400
16. R. Meganathan, and R. Bentley Thiamine pyrophosphate requirement for o-succinylbenzoic acid synthesis in Escherichia coli and evidence for an intermediate J. Bacteriol. 153 1983 739 746
17. C. Palaniappan, V. Sharma, M.E. Hudspeth, and R. Meganathan Menaquinone (vitamin K2) biosynthesis: evidence that the Escherichia coli menD gene encodes both 2-succinyl-6-hydroxy-2,4-cyclohexadiene-1-carboxylic acid synthase and alpha-ketoglutarate decarboxylase activities J. Bacteriol. 174 1992 8111 8118
18. V. Sharma, R. Meganathan, and M.E. Hudspeth Menaquinone (vitamin K2) biosynthesis: cloning, nucleotide sequence, and expression of the menC gene from Escherichia coli J. Bacteriol. 175 1993 4917 4921
19. R. Daruwala, O. Kwon, R. Meganathan, and M.E. Hudspeth A new isochorismate synthase specifically involved in menaquinone (vitamin K2) biosynthesis encoded by the menF gene FEMS Microbiol. Lett. 140 1996 159 163
20. R. Meganathan Biosynthesis of menaquinone (vitamin K2) and ubiquinone (coenzyme Q): a perspective on enzymatic mechanisms Vitam. Horm. 61 2001 173 218
21. V.A. Klenchin, E.A. Taylor Ringia, J.A. Gerlt, and I. Rayment Evolution of enzymatic activity in the enolase superfamily: structural and mutagenic studies of the mechanism of the reaction catalyzed by o-succinylbenzoate synthase from Escherichia coli Biochemistry 42 2003 14427 14433
22. M. Jiang, Y. Cao, Z.-F. Guo, M. Chen, X. Chen, and Z. Guo Menaquinone biosynthesis in Escherichia coli: identification of 2-succinyl-5-enolpyruvyl-6- hydroxy-3-cyclohexene-1-carboxylate as a novel intermediate and re-evaluation of MenD activity Biochemistry 46 2007 10979 10989
23. M. Jiang, X. Chen, Z.-F. Guo, Y. Cao, M. Chen, and Z. Guo Identification and characterization of (1R,6R)-2-succinyl-6-hydroxy-2,4-cyclohexadiene-1- carboxylate synthase in the menaquinone biosynthesis of Escherichia coli Biochemistry 47 2008 3426 3434
24. H.-J. Li, X. Li, N. Liu, H. Zhang, J.J. Truglio, S. Mishra, C. Kisker, M. Garcia-Diaz, and P.J. Tonge Mechanism of the intramolecular Claisen condensation reaction catalyzed by MenB, a crotonase superfamily member Biochemistry 50 2011 9532 9544
25. J.M. Johnston, M. Jiang, Z. Guo, and E.N. Baker Crystal sructures of E. coli native MenH and two active site mutants PLoS One 8 2013 e61325
26. R. Meganathan, R. Bentley, and H. Taber Identification of Bacillus subtilis men mutants which lack O-succinylbenzoyl-coenzyme A synthetase and dihydroxynaphthoate synthase J. Bacteriol. 145 1981 328 332
27. B. Rowland, K. Hill, P. Miller, J. Driscoll, and H. Taber Structural organization of a Bacillus subtilis operon encoding menaquinone biosynthetic enzymes Gene 167 1995 105 109
28. T. Dairi A.H. David, Chapter Six Menaquinone Biosyntheses in Microorganisms in Methods in Enzymology 2012 Academic Press 107 122
29. T. Dairi An alternative menaquinone biosynthetic pathway operating in microorganisms: an attractive target for drug discovery to pathogenic Helicobacter and Chlamydia strains J. Antibiot. 62 2009 347 352
30. J.R. Widhalm, C. van Oostende, F. Furt, and G.J. Basset A dedicated thioesterase of the Hotdog-fold family is required for the biosynthesis of the naphthoquinone ring of vitamin K1 Proc. Natl. Acad. Sci. USA 106 2009 5599 5603
31. J.A. Latham Structure to function: case studies of hotdog-fold superfamily thioesterases from Escherichia coli 2012 University of New Mexico
32. M. Chen, X. Ma, X. Chen, M. Jiang, H. Song, and Z. Guo Identification of a hotdog fold thioesterase involved in the biosynthesis of menaquinone in Escherichia coli J. Bacteriol. 195 2013 2768 2775
33. K. Suvarna, D. Stevenson, R. Meganathan, and M.E.S. Hudspeth Menaquinone (vitamin K2) biosynthesis: localization and characterization of the menA gene from Escherichia coli J. Bacteriol. 180 1998 2782 2787
34. A. Koike-Takeshita, T. Koyama, and K. Ogura Identification of a novel gene cluster participating in menaquinone (vitamin K2) biosynthesis. Cloning and sequence determination of the 2-heptaprenyl-1,4-naphthoquinone methyltransferase gene of Bacillus stearothermophilus J. Biol. Chem. 272 1997 12380 12383
35. L. Michaelis, and M.L. Menten Die Kinetik der Invertinwirkung Biochem. Z. 49 1913 333 369
36. K.A. Johnson, and R.S. Goody The original michaelis constant: translation of the 1913 Michaelis-Menten Paper Biochemistry 50 2011 8264 8269
37. Z. Zhuang, F. Song, H. Zhao, L. Li, J. Cao, E. Eisenstein, O. Herzberg, and D. Dunaway-Mariano Divergence of function in the hot dog fold enzyme superfamily: the bacterial thioesterase YciA Biochemistry 47 2008 2789 2796
38. F. Song, Z. Zhuang, L. Finci, D. Dunaway-Mariano, R. Kniewel, J.A. Buglino, V. Solorzano, J. Wu, and C.D. Lima Structure, function, and mechanism of the phenylacetate pathway hot dog-fold thioesterase PaaI J. Biol. Chem. 281 2006 11028 11038
39. L. Luo, K.L. Taylor, H. Xiang, Y. Wei, W. Zhang, and D. Dunaway-Mariano Role of active site binding interactions in 4-chlorobenzoyl-coenzyme A dehalogenase catalysis Biochemistry 40 2001 15684 15692
40. S.M. Merkel, A.E. Eberhard, J. Gibson, and C.S. Harwood Involvement of coenzyme A thioesters in anaerobic metabolism of 4-hydroxybenzoate by Rhodopseudomonas palustris J. Bacteriol. 171 1989 1 7
41. H. Huang, Y. Patskovsky, R. Toro, J.D. Farelli, C. Pandya, S.C. Almo, K.N. Allen, and D. Dunaway-Mariano Divergence of structure and function in the haloacid dehalogenase enzyme superfamily: Bacteroides thetaiotaomicron BT2127 is an inorganic pyrophosphatase Biochemistry 50 2011 8937 8949
42. Z. Lu, D. Dunaway-Mariano, and K.N. Allen The X-ray crystallographic structure and specificity profile of HAD superfamily phosphohydrolase BT1666: comparison of paralogous functions in B. thetaiotaomicron Proteins: Struct., Funct., Bioinf. 79 2011 3099 3107
43. Z. Lu, D. Dunaway-Mariano, and K.N. Allen HAD superfamily phosphotransferase substrate diversification: structure and function analysis of HAD subclass IIB sugar phosphatase BT4131 Biochemistry 44 2005 8684 8696
44. A. Roberts, S.-Y. Lee, E. McCullagh, R.E. Silversmith, and D.E. Wemmer Ybiv from Escherichia coli K12 is a HAD phosphatase Proteins: Struct., Funct., Bioinf. 58 2005 790 801
45. Z. Lu, D. Dunaway-Mariano, and K.N. Allen The catalytic scaffold of the haloalkanoic acid dehalogenase enzyme superfamily acts as a mold for the trigonal bipyramidal transition state Proc. Natl. Acad. Sci. USA 105 2008 5687 5692
46. H.H. Nguyen, L. Wang, H. Huang, E. Peisach, D. Dunaway-Mariano, and K.N. Allen Structural determinants of substrate recognition in the HAD superfamily member d-glycero-d-manno-heptose-1,7-bisphosphate phosphatase (GmhB) Biochemistry 49 2010 1082 1092
47. K. Walldén, A. Rinaldo-Matthis, B. Ruzzenente, C. Rampazzo, V. Bianchi, and P. Nordlund Crystal structures of human and murine deoxyribonucleotidases: insights into recognition of substrates and nucleotide analogues Biochemistry 46 2007 13809 13818
48. E. Kuznetsova, M. Proudfoot, C.F. Gonzalez, G. Brown, M.V. Omelchenko, I. Borozan, L. Carmel, Y.I. Wolf, H. Mori, A.V. Savchenko, C.H. Arrowsmith, E.V. Koonin, A.M. Edwards, and A.F. Yakunin Genome-wide analysis of substrate specificities of the Escherichia coli haloacid dehalogenase-like phosphatase family J. Biol. Chem. 281 2006 36149 36161
49. M. Wang Evolution of structure and function among hotdog-fold thioesterase and HAD family phosphates 2011 University of New Mexico
50. K.N. Allen, and D. Dunaway-Mariano Markers of fitness in a successful enzyme superfamily Curr. Opin. Struct. Biol. 19 2009 658 665
51. J.B. Thoden, H.M. Holden, Z. Zhuang, and D. Dunaway-Mariano X-ray crystallographic analyses of inhibitor and substrate complexes of wild-type and mutant 4-hydroxybenzoyl-CoA thioesterase J. Biol. Chem. 277 2002 27468 27476
52. J.B. Thoden, Z. Zhuang, D. Dunaway-Mariano, and H.M. Holden The structure of 4-hydroxybenzoyl-CoA thioesterase from Arthrobacter sp. strain SU J. Biol. Chem. 278 2003 43709 43716
53. A.D. Mccarthy, and D.G. Hardie Fatty-acid synthase - an example of protein evolution by gene fusion Trends Biochem. Sci. 9 1984 60 63
54. M. Long A new function evolved from gene fusion Genome Res. 10 2000 1655 1657
55. L.A. Kelley, and M.J. Sternberg Protein structure prediction on the Web: a case study using the Phyre server Nat. Protoc. 4 2009 363 371