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Evolution of enzymatic activities in the enolase superfamily: crystallographic and mutagenesis studies of the reaction catalyzed by D-glucarate dehydratase from Escherichia coli.

Gulick AM, Hubbard BK, Gerlt JA, Rayment I
Biochemistry 39 4590-602 (2000)
Related entries: 1ec7, 1ec9, 1ecq

Cited: 24 times
EuropePMC logo PMID: 10769114

Abstract

D-Glucarate dehydratase (GlucD) from Escherichia coli catalyzes the dehydration of both D-glucarate and L-idarate as well as their interconversion via epimerization. GlucD is a member of the mandelate racemase (MR) subgroup of the enolase superfamily, the members of which catalyze reactions that are initiated by abstraction of the alpha-proton of a carboxylate anion substrate. Alignment of the sequence of GlucD with that of MR reveals a conserved Lys-X-Lys motif and a His-Asp dyad homologous to the S- and R-specific bases in the active site of MR. Crystals of GlucD have been obtained into which the substrate D-glucarate and two competitive inhibitors, 4-deoxy-D-glucarate and xylarohydroxamate, could be diffused; D-glucarate is converted to the dehydration product, 5-keto-4-deoxy-D-glucarate (KDG). The structures of these complexes have been determined and reveal the identities of the ligands for the required Mg(2+) (Asp(235), Glu(266), and Asn(289)) as well as confirm the expected presence of Lys(207) and His(339), the catalytic bases that are properly positioned to abstract the proton from C5 of L-idarate and D-glucarate, respectively. Surprisingly, the C6 carboxylate group of KDG is a bidentate ligand to the Mg(2+), with the resulting geometry of the bound KDG suggesting that stereochemical roles of Lys(207) and His(339) are reversed from the predictions made on the basis of the established structure-function relationships for the MR-catalyzed reaction. The catalytic roles of these residues have been examined by characterization of mutant enzymes, although we were unable to use these to demonstrate the catalytic independence of Lys(207) and His(339) as was possible for the homologous Lys(166) and His(297) in the MR-catalyzed reaction.

Articles - 1ec8 mentioned but not cited (1)

  1. Loss of quaternary structure is associated with rapid sequence divergence in the OSBS family. Odokonyero D, Sakai A, Patskovsky Y, Malashkevich VN, Fedorov AA, Bonanno JB, Fedorov EV, Toro R, Agarwal R, Wang C, Ozerova ND, Yew WS, Sauder JM, Swaminathan S, Burley SK, Almo SC, Glasner ME. Proc Natl Acad Sci U S A 111 8535-8540 (2014)


Reviews citing this publication (3)

  1. Divergent evolution of enzymatic function: mechanistically diverse superfamilies and functionally distinct suprafamilies. Gerlt JA, Babbitt PC. Annu Rev Biochem 70 209-246 (2001)
  2. Divergent evolution in the enolase superfamily: the interplay of mechanism and specificity. Gerlt JA, Babbitt PC, Rayment I. Arch Biochem Biophys 433 59-70 (2005)
  3. Structure and function of aldopentose catabolism enzymes involved in oxidative non-phosphorylative pathways. Ren Y, Eronen V, Blomster Andberg M, Koivula A, Hakulinen N. Biotechnol Biofuels Bioprod 15 147 (2022)

Articles citing this publication (20)

  1. Crystal structure of the Escherichia coli RNA degradosome component enolase. Kühnel K, Luisi BF. J Mol Biol 313 583-592 (2001)
  2. Evolution of structure and function in the o-succinylbenzoate synthase/N-acylamino acid racemase family of the enolase superfamily. Glasner ME, Fayazmanesh N, Chiang RA, Sakai A, Jacobson MP, Gerlt JA, Babbitt PC. J Mol Biol 360 228-250 (2006)
  3. Superfamily active site templates. Meng EC, Polacco BJ, Babbitt PC. Proteins 55 962-976 (2004)
  4. Evolution of enzymatic activities in the enolase superfamily: L-rhamnonate dehydratase. Rakus JF, Fedorov AA, Fedorov EV, Glasner ME, Hubbard BK, Delli JD, Babbitt PC, Almo SC, Gerlt JA. Biochemistry 47 9944-9954 (2008)
  5. New insights into the alternative D-glucarate degradation pathway. Aghaie A, Lechaplais C, Sirven P, Tricot S, Besnard-Gonnet M, Muselet D, de Berardinis V, Kreimeyer A, Gyapay G, Salanoubat M, Perret A. J Biol Chem 283 15638-15646 (2008)
  6. Discovery of function in the enolase superfamily: D-mannonate and d-gluconate dehydratases in the D-mannonate dehydratase subgroup. Wichelecki DJ, Balthazor BM, Chau AC, Vetting MW, Fedorov AA, Fedorov EV, Lukk T, Patskovsky YV, Stead MB, Hillerich BS, Seidel RD, Almo SC, Gerlt JA. Biochemistry 53 2722-2731 (2014)
  7. Structure of mandelate racemase with bound intermediate analogues benzohydroxamate and cupferron. Lietzan AD, Nagar M, Pellmann EA, Bourque JR, Bearne SL, St Maurice M. Biochemistry 51 1160-1170 (2012)
  8. Structural basis for catalytic racemization and substrate specificity of an N-acylamino acid racemase homologue from Deinococcus radiodurans. Wang WC, Chiu WC, Hsu SK, Wu CL, Chen CY, Liu JS, Hsu WH. J Mol Biol 342 155-169 (2004)
  9. Transient knockdown and overexpression reveal a developmental role for the zebrafish enosf1b gene. Finckbeiner S, Ko PJ, Carrington B, Sood R, Gross K, Dolnick B, Sufrin J, Liu P. Cell Biosci 1 32 (2011)
  10. Divergent evolution of ligand binding in the o-succinylbenzoate synthase family. Odokonyero D, Ragumani S, Lopez MS, Bonanno JB, Ozerova ND, Woodard DR, Machala BW, Swaminathan S, Burley SK, Almo SC, Glasner ME. Biochemistry 52 7512-7521 (2013)
  11. Identification of the in vivo function of the high-efficiency D-mannonate dehydratase in Caulobacter crescentus NA1000 from the enolase superfamily. Wichelecki DJ, Graff DC, Al-Obaidi N, Almo SC, Gerlt JA. Biochemistry 53 4087-4089 (2014)
  12. A convenient preparation of aldonohydroxamic acids in water and crystal structure of L-erythronohydroxamic acid. Salmon L, Prost E, Merienne C, Hardré R, Morgant G. Carbohydr Res 335 195-204 (2001)
  13. Investigating the physiological roles of low-efficiency D-mannonate and D-gluconate dehydratases in the enolase superfamily: pathways for the catabolism of L-gulonate and L-idonate. Wichelecki DJ, Vendiola JA, Jones AM, Al-Obaidi N, Almo SC, Gerlt JA. Biochemistry 53 5692-5699 (2014)
  14. Comparison of Alicyclobacillus acidocaldarius o-Succinylbenzoate Synthase to Its Promiscuous N-Succinylamino Acid Racemase/ o-Succinylbenzoate Synthase Relatives. Odokonyero D, McMillan AW, Ramagopal UA, Toro R, Truong DP, Zhu M, Lopez MS, Somiari B, Herman M, Aziz A, Bonanno JB, Hull KG, Burley SK, Romo D, Almo SC, Glasner ME. Biochemistry 57 3676-3689 (2018)
  15. Crystal structure of N-acylamino acid racemase from Thermus thermophilus HB8. Hayashida M, Kim SH, Takeda K, Hisano T, Miki K. Proteins 71 519-523 (2008)
  16. Identification and characterization of two new 5-keto-4-deoxy-D-Glucarate Dehydratases/Decarboxylases. Pick A, Beer B, Hemmi R, Momma R, Schmid J, Miyamoto K, Sieber V. BMC Biotechnol 16 80 (2016)
  17. The Birth of Genomic Enzymology: Discovery of the Mechanistically Diverse Enolase Superfamily. Allen KN, Whitman CP. Biochemistry 60 3515-3528 (2021)
  18. Predicting enzyme-substrate specificity with QM/MM methods: a case study of the stereospecificity of (D)-glucarate dehydratase. Tian B, Wallrapp F, Kalyanaraman C, Zhao S, Eriksson LA, Jacobson MP. Biochemistry 52 5511-5513 (2013)
  19. Hydroxamates as substrates and inhibitors for FMN-dependent 2-hydroxy acid dehydrogenases. Amar D, North P, Miskiniene V, Cénas N, Lederer F. Bioorg Chem 30 145-162 (2002)
  20. Crystal structure analysis of 3,6-anhydro-l-galactonate cycloisomerase suggests emergence of novel substrate specificity in the enolase superfamily. Lee S, Kim KH, Kim HY, Choi IG. Biochem Biophys Res Commun 491 217-222 (2017)


Related citations provided by authors (1)

  1. Evolution of Enzymative Activities in the Enolase Superfamily: Crystal Structure of (D)-glucarate Dehydratase from Pseudomonas putida. Gulick AM, Palmer DR, Babbitt PC, Gerlt JA, Rayment I Biochemistry 37 14358-14368 (1998)

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