Discovery of a widespread prokaryotic 5-oxoprolinase that was hiding in plain sight

Journal of Biological Chemistry

Volumn 292, Issue 39, 2017, Pages 16360-16367

  Niehaus, Thomas D ^a   Elbadawi Sidhu, Mona ^b   De Crécy Lagard, Valérie ^a   Fiehn, Oliver ^b   Hanson, Andrew D ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BACTERIOLOGY; BIOMOLECULES; ESCHERICHIA COLI; GENE ENCODING; RECOMBINANT PROTEINS;

BACILLUS SUBTILIS; COMPARATIVE ANALYSIS; DAMAGE CONTROL SYSTEMS; DISPOSAL SYSTEMS; MODEL ORGANISMS; NITROGEN SOURCES; PROKARYOTIC GENOMES; SPONTANEOUS FORMATION;

METABOLITES;

5 OXOPROLINASE; 5 OXOPROLYL PEPTIDASE; ADENOSINE TRIPHOSPHATE; ALLOPHANATE HYDROLASE; PXPA PROTEIN; PXPB PROTEIN; PXPC PROTEIN; UNCLASSIFIED DRUG; 5-OXOPROLINASE (ATP-HYDROLYZING); AMIDASE; BACTERIAL PROTEIN; ESCHERICHIA COLI PROTEIN; PROTEIN SUBUNIT; PYROGLUTAMIC ACID; RECOMBINANT PROTEIN;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENE; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE OVEREXPRESSION; GENOMICS; MICROBIAL GENOME; NONHUMAN; PRIORITY JOURNAL; PXPA GENE; PXPB GENE; PXPC GENE; ENZYMOLOGY; GENE DELETION; GENE INACTIVATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MULTIGENE FAMILY; MUTATION; PROCEDURES; PROTEIN SUBUNIT;

ALLOPHANATE HYDROLASE; AMIDOHYDROLASES; BACILLUS SUBTILIS; BACTERIAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; GENE KNOCKOUT TECHNIQUES; GENOMICS; MULTIGENE FAMILY; MUTATION; PROTEIN SUBUNITS; PYRROLIDONECARBOXYLIC ACID; RECOMBINANT PROTEINS;

EID: 85030028835     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M117.805028     Document Type: Article

References (51)

1. Orlowski, M., and Meister, A. (1970) The -glutamyl cycle: a possible transport system for amino acids. Proc. Natl. Acad. Sci. U.S.A. 67, 1248–1255
2. Griffith, O. W., Bridges, R. J., and Meister, A. (1978) Evidence that the -glutamyl cycle functions in vivo using intracellular glutathione: effects of amino acids and selective inhibition of enzymes. Proc. Natl. Acad. Sci. U.S.A. 75, 5405–5408
3. Van der Werf, P., Orlowski, M., and Meister, A. (1971) Enzymatic conversion of 5-oxo-L-proline (L-pyrrolidone carboxylate) to L-glutamate coupled with cleavage of adenosine triphosphate to adenosine diphosphate, a reaction in the -glutamyl cycle. Proc. Natl. Acad. Sci. U.S.A. 68, 2982–2985
4. Paulose, B., Chhikara, S., Coomey, J., Jung, H. I., Vatamaniuk, O., and Dhankher, O. P. (2013) A -glutamyl cyclotransferase protects Arabidopsis plants from heavy metal toxicity by recycling glutamate to maintain glutathione homeostasis. Plant Cell 25, 4580 – 4595
5. Ohkama-Ohtsu, N., Oikawa, A., Zhao, P., Xiang, C., Saito, K., and Oliver, D. J. (2008) A -glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis. Plant Physiol. 148, 1603–1613
6. Kumar, A., and Bachhawat, A. K. (2010) OXP1/YKL215c encodes an ATP-dependent 5-oxoprolinase in Saccharomyces cerevisiae: functional characterization, domain structure, and identification of actin-like ATP-binding motifs in eukaryotic 5-oxoprolinases. FEMS Yeast Res. 10, 394 – 401
7. Okada, T., Suzuki, H., Wada, K., Kumagai, H., and Fukuyama, K. (2006) Crystal structures of -glutamyltranspeptidase from Escherichia coli, a key enzyme in glutathione metabolism, and its reaction intermediate. Proc. Natl. Acad. Sci. U.S.A. 103, 6471– 6476
8. Newton, G.L., Rawat, M., La Clair, J.J., Jothivasan, V.K., Budiarto, T., Hamilton, C.J., Claiborne, A., Helmann, J.D., and Fahey, R.C. (2009) Bacillithiol is an antioxidant thiol produced in Bacilli. Nat. Chem. Biol. 5, 625– 627
9. Tritsch, G. L., and Moore, G. E. (1962) Spontaneous decomposition of glutamine in cell culture media. Exp. Cell Res. 28, 360 –364
10. Park, C. B., Lee, S. B., and Ryu, D. D. (2001) L-Pyroglutamate spontaneously formed from L-glutamate inhibits growth of the hyperthermo-philic archaeon Sulfolobus solfataricus. Appl. Environ. Microbiol. 67, 3650 –3654
11. Orlowski, M., and Meister, A. (1971) Partial reactions catalyzed by -glu-tamylcysteine synthetase and evidence for an activated glutamate intermediate. J. Biol. Chem. 246, 7095–7105
12. Schilling, S., Wasternack, C., and Demuth, H. U. (2008) Glutaminyl cyclases from animals and plants: a case of functionally convergent protein evolution. Biol. Chem. 389, 983–991
13. Carrillo, D. R., Parthier, C., Jänckel, N., Grandke, J., Stelter, M., Schilling, S., Boehme, M., Neumann, P., Wolf, R., Demuth, H. U., Stubbs, M. T., and Rahfeld, J. U. (2010) Kinetic and structural characterization of bacterial glutaminyl cyclases from Zymomonas mobilis and Myxococcus xanthus. Biol. Chem. 391, 1419 –1428
14. Awadé, A., Cleuziat, P., Gonzalès, T., and Robert-Baudouy, J. (1992) Characterization of the pcp gene encoding the pyrrolidone carboxyl peptidase of Bacillus subtilis. FEBS Lett. 305, 67–73
15. Pedrotti, E. L., Jay-Allemand, C., Doumas, P., and Cornu, D. (1994) Effect of autoclaving amino acids on in vitro rooting response of wild cherry shoot. Scientia Horticulturae 57, 89 –98
16. Silva, A. R., Silva, C. G., Ruschel, C., Helegda, C., Wyse, A. T., Wannmacher, C. M., Wajner, M., and Dutra-Filho, C. S. (2001) L-Pyroglutamic acid inhibits energy production and lipid synthesis in cerebral cortex of young rats in vitro. Neurochem. Res. 26, 1277–1283
17. Pederzolli, C. D., Sgaravatti, A. M., Braum, C. A., Prestes, C. C., Zorzi, G. K., Sgarbi, M. B., Wyse, A. T., Wannmacher, C. M., Wajner, M., and Dutra-Filho, C. S. (2007) 5-Oxoproline reduces non-enzymatic antioxidant defenses in vitro in rat brain. Metab. Brain Dis. 22, 51– 65
18. Ristoff, E., and Larsson, A. (2007) Inborn errors in the metabolism of glutathione. Orphanet. J. Rare Dis. 2, 16
19. Sass, J. O., Gemperle-Britschgi, C., Tarailo-Graovac, M., Patel, N., Walter, M., Jordanova, A., Alfadhel, M., Barić, I., Çoker, M., Damli-Huber, A., Faqeih, E. A., García Segarra, N., Geraghty, M. T., Jåtun, B. M., Kalkan Uçar, S., et al. (2016) Unravelling 5-oxoprolinuria (pyroglutamic aciduria) due to bi-allelic OPLAH mutations: 20 new mutations in 14 families. Mol. Genet. Metab. 119, 44 – 49
20. Nishimura, A., Ozaki, Y., Oyama, H., Shin, T., and Murao, S. (1999) Purification and characterization of a novel 5-oxoprolinase (without ATP-hydrolyzing activity) from Alcaligenes faecalis N-38A. Appl. Environ. Microbiol. 65, 712–717
21. Nishimura, A., Oyama, H., Hamada, T., Nobuoka, K., Shin, T., Murao, S., and Oda, K. (2000) Molecular cloning, sequencing, and expression in Escherichia coli of the gene encoding a novel 5-oxoprolinase without ATP-hydrolyzing activity from Alcaligenes faecalis N-38A. Appl. Environ. Microbiol. 66, 3201–3205
22. Van der Werf, P., and Meister, A. (1974) Isolation of 5-oxoprolinase from a prokaryote. Biochem. Biophys. Res. Commun. 56, 90 –96
23. Seddon, A. P., Li, L. Y., and Meister, A. (1984) Resolution of 5-oxo-L-prolinase into a 5-oxo-l-proline-dependent ATPase and a coupling protein. J. Biol. Chem. 259, 8091– 8094
24. Seddon, A. P., and Meister, A. (1986) Trapping of an intermediate in the reaction catalyzed by 5-oxoprolinase. J. Biol. Chem. 261, 11538 –11543
25. Li, L. Y., Seddon, A. P., and Meister, A. (1988) Interaction of the protein components of 5-oxoprolinase. Substrate-dependent enzyme complex formation. J. Biol. Chem. 263, 6495– 6501
26. Overbeek, R., Begley, T., Butler, R. M., Choudhuri, J.V., Chuang, H. Y., Cohoon, M., de Crécy-Lagard, V., Diaz, N., Disz, T., Edwards, R., Fonstein, M., Frank, E. D., Gerdes, S., Glass, E. M., Goesmann, A., et al. (2005) The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 33, 5691–5702
27. Niehaus, T. D., Gerdes, S., Hodge-Hanson, K., Zhukov, A., Cooper, A. J., ElBadawi-Sidhu, M., Fiehn, O., Downs, D. M., and Hanson, A. D. (2015) Genomic and experimental evidence for multiple metabolic functions in the RidA/YjgF/YER057c/UK114 (Rid) protein family. BMC Genomics 16, 382
28. Hanson, A. D., Pribat, A., Waller, J. C., and de Crécy-Lagard, V. (2009) “Unknown” proteins and “orphan” enzymes: the missing half of the engineering parts list and how to find it. Biochem. J. 425, 1–11
29. Bochner, B. R., Gadzinski, P., and Panomitros, E. (2001) Phenotype mi-croarrays for high-throughput phenotypic testing and assay of gene function. Genome Res. 11, 1246 –1255
30. Koo, B.M., Kritikos, G., Farelli, J.D., Todor, H., Tong, K., Kimsey, H., Wapinski, I., Galardini, M., Cabal, A., Peters, J. M., Hachmann, A. B., Rudner, D. Z., Allen, K. N., Typas, A., and Gross, C. A. (2017) Construction and analysis of two genome-scale deletion libraries for Bacillus subtilis. Cell Syst. 4, 291–305
31. Jacques, D. A., Langley, D. B., Kuramitsu, S., Yokoyama, S., Trewhella, J., and Guss, J. M. (2011) The structure of TTHA0988 from Thermus thermophilus, a KipI-KipA homologue incorrectly annotated as an allophanate hydrolase. Acta Crystallogr. D. Biol. Crystallogr. 67, 105–111
32. Mazelis, M., and Creveling, R. K. (1978) 5-Oxoprolinase (L-pyroglutamate hydrolase) in higher plants: partial purification and characterization of the wheat germ enzyme. Plant Physiol. 62, 798 – 801
33. Jaspers, C. J., Gigot, D., and Penninckx, M. J. (1985) Pathways of glutathione degradation in the yeast Saccharomyces cerevisiae. Phytochemistry 24, 703–707
34. Yu, A. C., Loo, J. F., Yu, S., Kong, S. K., and Chan, T. F. (2014) Monitoring bacterial growth using tunable resistive pulse sensing with a pore-based technique. Appl. Microbiol. Biotechnol. 98, 855– 862
35. Marbaix, A. Y., Noël, G., Detroux, A. M., Vertommen, D., Van Schaftingen, E., and Linster, C. L. (2011) Extremely conserved ATP- or ADP-dependent enzymatic system for nicotinamide nucleotide repair. J. Biol. Chem. 286, 41246 – 41252
36. Lambrecht, J. A., Flynn, J. M., and Downs, D. M. (2012) Conserved YjgF protein family deaminates reactive enamine/imine intermediates of pyri-doxal 5-phosphate (PLP)-dependent enzyme reactions. J. Biol. Chem. 287, 3454 –3461
37. Peracchi, A., Veiga-da-Cunha, M., Kuhara, T., Ellens, K. W., Paczia, N., Stroobant, V., Seliga, A. K., Marlaire, S., Jaisson, S., Bommer, G. T., Sun, J., and Huebner, K., and Linster, C. L., et al. (2017) Nit1 is a metabolite repair enzyme that hydrolyzes deaminated glutathione. Proc. Natl. Acad. Sci. U.S.A. 114, E3233–E3242
38. Gray, M. W. (2017) Lynn Margulis and the endosymbiont hypothesis: 50 years later. Mol. Biol. Cell 28, 1285–1287
39. Ouzounis, C. A., Kunin, V., Darzentas, N., and Goldovsky, L. (2006) A minimal estimate for the gene content of the last universal common ancestor: exobiology from a terrestrial perspective. Res. Microbiol. 157, 57–68
40. Juttukonda, L. J., Chazin, W. J., and Skaar, E. P. (2016) Acinetobacter bau-mannii coordinates urea metabolism with metal import to resist host-mediated metal limitation. MBio. 7, e01475–16
41. Wang, L., Grau, R., Perego, M., and Hoch, J. A. (1997) A novel histidine kinase inhibitor regulating development in Bacillus subtilis. Genes Dev. 11, 2569 –2579
42. Jacques, D. A., Langley, D. B., Hynson, R. M., Whitten, A. E., Kwan, A., Guss, J. M., and Trewhella, J. (2011) A novel structure of an antikinase and its inhibitor. J. Mol. Biol. 405, 214 –226
43. Lin, Y., Boese, C. J., and St Maurice, M. (2016) The urea carboxylase and allophanate hydrolase activities of urea amidolyase are functionally independent. Protein Sci. 25, 1812–1824
44. Zhang, Y., Kiba, A., Hikichi, Y., and Ohnishi, K. (2011) prhKLM genes of Ralstonia solanacearum encode novel activators of hrp regulon and are required for pathogenesis in tomato. FEMS Microbiol. Lett. 317, 75– 82
45. Meister, A. (1973) On the enzymology of amino acid transport. Science 180, 33–39
46. Golubev, A. G. (1996) The other side of metabolism. Biokhimiia 61, 2018–2039
47. Golubev, A., Hanson, A. D., and Gladyshev, V. N. (2017) Non-enzymatic molecular damage as a prototypic driver of aging. J. Biol. Chem. 292, 6029–6038
48. Blattner, F. R., Plunkett, G., 3rd, Bloch, C. A., Perna, N. T., Burland, V., Riley, M., Collado-Vides, J., Glasner, J. D., Rode, C. K., Mayhew, G. F., Gregor, J., Davis, N. W., Kirkpatrick, H. A., Goeden, M. A., Rose, D. J., Mau, B., and Shao, Y. (1997) The complete genome sequence of Escherichia coli K-12. Science 277, 1453–1462
49. Kunst, F., Ogasawara, N., Moszer, I., Albertini, A. M., Alloni, G., Azevedo, V., Bertero, M. G., Bessières, P., Bolotin, A., Borchert, S., Borriss, R., Boursier, L., Brans, A., Braun, M., and Brignell, S. C., et al. (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390, 249 –256
50. Harwood, C. R., and Cutting, S. M. (1990) Molecular Biological Methods for Bacillus, pp. 27–74, John Wiley & Sons Ltd, Chichester, England
51. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248 –254