Nit1 is a metabolite repair enzyme that hydrolyzes deaminated glutathione

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 16, 2017, Pages E3233-E3242

  Peracchi, Alessio ^a,b,c   Veiga Da Cunha, Maria ^a,b   Kuhara, Tomiko ^d,e   Ellens, Kenneth W ^f   Paczia, Nicole ^f   Stroobant, Vincent ^g   Seliga, Agnieszka K ^a,b   Marlaire, Simon ^a,b   Jaisson, Stephane ^a,b,j   Bommer, Guido T ^a,b   Sun, Jin ^h   Huebner, Kay ^h   Linster, Carole L ^f   Cooper, Arthur J L ⁱ   Van Schaftingen, Emile ^a,b  

^a Welbio (Walloon Excellence in Lifesciences and Biotechnology)   (Belgium)

^b DE DUVE INSTITUTE   (Belgium)

^c UNIVERSITY OF PARMA   (Italy)

^d Japan Clinical Metabolomics Institute   (Japan)

^e KANAZAWA MEDICAL UNIVERSITY   (Japan)

^f UNIVERSITY OF LUXEMBOURG   (Luxembourg)

^g UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^h OHIO STATE UNIVERSITY   (United States)

ⁱ NEW YORK MEDICAL COLLEGE   (United States)

^j HÔPITAL MAISON BLANCHE   (France)

more..

Author keywords

Amidase; Aminotransferases; Deaminated glutathione; Metabolite repair

Indexed keywords

AMIDASE; AMINO ACID OXIDASE; AMINOOXYACETIC ACID; AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; COENZYME A; DISULFIDE; GLUTAMATE DEHYDROGENASE; GLUTAMINE; GLUTAMINE PHENYLPYRUVATE AMINOTRANSFERASE; GLUTATHIONE; GLUTATHIONE SYNTHASE; HYDROLASE; NITRILASE LIKE PROTEIN 1; ORNITHINE OXOACID AMINOTRANSFERASE; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; NITRILASE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CATALYSIS; CATALYTIC EFFICIENCY; CONTROLLED STUDY; CRISPR CAS SYSTEM; CYTOSOL; DERIVATIZATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME PURIFICATION; ESCHERICHIA COLI; GENE INACTIVATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; HYDROLYSIS; ION EXCHANGE CHROMATOGRAPHY; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; YEAST CELL; ANIMAL; DEAMINATION; ENZYME SPECIFICITY; KNOCKOUT MOUSE; METABOLISM; MOUSE; PHYSIOLOGY;

AMINOHYDROLASES; ANIMALS; DEAMINATION; GLUTATHIONE; HUMANS; HYDROLYSIS; MICE; MICE, KNOCKOUT; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY; TRANSAMINASES;

EID: 85017594637     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1613736114     Document Type: Article

References (46)

1. Pekarsky Y, et al. (1998) Nitrilase and Fhit homologs are encoded as fusion proteins in Drosophila melanogaster and Caenorhabditis elegans. Proc Natl Acad Sci USA 95: 8744-8749.
2. Pace HC, et al. (2000) Crystal structure of the worm NitFhit Rosetta Stone protein reveals a Nit tetramer binding two Fhit dimers. Curr Biol 10:907-917.
3. Barglow KT, Cravatt BF (2006) Substrate mimicry in an activity-based probe that targets the nitrilase family of enzymes. Angew Chem Int Ed Engl 45:7408-7411.
4. Barglow KT, et al. (2008) Functional proteomic and structural insights into molecular recognition in the nitrilase family enzymes. Biochemistry 47:13514-13523.
5. Jaisson S, Veiga-da-Cunha M, Van Schaftingen E (2009) Molecular identification of omega-amidase, the enzyme that is functionally coupled with glutamine transaminases, as the putative tumor suppressor Nit2. Biochimie 91:1066-1071.
6. Krasnikov BF, et al. (2009) Identification of the putative tumor suppressor Nit2 as omega-amidase, an enzyme metabolically linked to glutamine and asparagine transamination. Biochimie 91:1072-1080.
7. Meister A, Levintow L, Greenfield RE, Abendschein PA (1955) Hydrolysis and transfer reactions catalyzed by omega-amidase preparations. J Biol Chem 215:441-460.
8. Cooper AJ, Meister A (1977) The glutamine transaminase-omega-amidase pathway. CRC Crit Rev Biochem 4:281-303.
9. Cooper AJ, et al. (2016) ?-Amidase: An underappreciated, but important enzyme in L-glutamine and L-asparagine metabolism; relevance to sulfur and nitrogenmetabolism, tumor biology and hyperammonemic diseases. Amino Acids 48:1-20; erratum in 2015, Amino Acids 47:2671-2672.
10. Galperin MY, Koonin EV (2004) 'Conserved hypothetical' proteins: Prioritization of targets for experimental study. Nucleic Acids Res 32:5452-5463.
11. Galperin MY, Koonin EV (2010) From complete genome sequence to "complete" understanding? Trends Biotechnol 28:398-406.
12. Linster CL, Van Schaftingen E, Hanson AD (2013) Metabolite damage and its repair or pre-emption. Nat Chem Biol 9:72-80.
13. Van Schaftingen E, et al. (2013) Metabolite proofreading, a neglected aspect of intermediary metabolism. J Inherit Metab Dis 36:427-434.
14. Rzem R, et al. (2004) A gene encoding a putative FAD-dependent L-2-hydroxyglutarate dehydrogenase is mutated in L-2-hydroxyglutaric aciduria. Proc Natl Acad Sci USA 101: 16849-16854.
15. Van Schaftingen E, Rzem R, Veiga-da-Cunha M (2009) L-2-Hydroxyglutaric aciduria, a disorder of metabolite repair. J Inherit Metab Dis 32:135-142.
16. Collard F, et al. (2016) A conserved phosphatase destroys toxic glycolytic side products in mammals and yeast. Nat Chem Biol 12:601-607.
17. Gerlt JA, et al. (2011) The enzyme function initiative. Biochemistry 50:9950-9962.
18. Meister A (1953) Preparation and enzymatic reactions of the keto analogues of asparagine and glutamine. J Biol Chem 200:571-589.
19. Meister A, Otani TT (1957) Omega-amide and omega-amino acid derivatives of alphaketoglutaric and oxalacetic acids. J Biol Chem 224:137-148.
20. Hersh LB (1971) Rat liver omega-amidase. Purification and properties. Biochemistry 10:2884-2891.
21. Buell MV, Hansen RE (1960) Reaction of pyridoxal-5-phosphate with aminothiols. J Am Chem Soc 82:6042-6049.
22. Bar-Even A, et al. (2011) The moderately efficient enzyme: Evolutionary and physicochemical trends shaping enzyme parameters. Biochemistry 50:4402-4410.
23. Semba S, et al. (2006) Biological functions of mammalian Nit1, the counterpart of the invertebrate NitFhit Rosetta stone protein, a possible tumor suppressor. J Biol Chem 281:28244-28253.
24. Cooper AJ, et al. (2008) Substrate specificity of human glutamine transaminase K as an aminotransferase and as a cysteine S-conjugate β-lyase. Arch Biochem Biophys 474: 72-81.
25. Donini S, et al. (2009) Recombinant production of eight human cytosolic aminotransferases and assessment of their potential involvement in glyoxylate metabolism. Biochem J 422:265-272.
26. Schiroli D, Peracchi A (2015) A subfamily of PLP-dependent enzymes specialized in handling terminal amines. Biochim Biophys Acta 1854:1200-1211.
27. Malherbe P, Alberati-Giani D, Kohler C, Cesura AM (1995) Identification of a mitochondrial form of kynurenine aminotransferase/glutamine transaminase K from rat brain. FEBS Lett 367:141-144.
28. Korangath P, et al. (2015) Targeting glutamine metabolism in breast cancer with aminooxyacetate. Clin Cancer Res 21:3263-3273.
29. Sun J, et al. (2009) Nit1 and Fhit tumor suppressor activities are additive. J Cell Biochem 107:1097-1106.
30. Marlaire S, Van Schaftingen E, Veiga-da-Cunha M (2014) C7orf10 encodes succinatehydroxymethylglutarate CoA-transferase, the enzyme that converts glutarate to glutaryl-CoA. J Inherit Metab Dis 37:13-19.
31. Liu H, et al. (2013) Structures of enzyme-intermediate complexes of yeast Nit2: Insights into its catalytic mechanism and different substrate specificity compared with mammalian Nit2. Acta Crystallogr D Biol Crystallogr 69:1470-1481.
32. Copley SD, Dhillon JK (2002) Lateral gene transfer and parallel evolution in the history of glutathione biosynthesis genes. Genome Biol 3:research0025.
33. Fahey RC (2013) Glutathione analogs in prokaryotes. Biochim Biophys Acta 1830: 3182-3198.
34. Johnson T, Newton GL, Fahey RC, Rawat M (2009) Unusual production of glutathione in Actinobacteria. Arch Microbiol 191:89-93.
35. Novogrodsky A, Meister A (1964) Control of aspartate beta-decarboxylase activity by transamination. J Biol Chem 239:879-888.
36. Mason JM, et al. (2004) IL-4-induced gene-1 is a leukocyte L-amino acid oxidase with an unusual acidic pH preference and lysosomal localization. J Immunol 173: 4561-4567.
37. Josch C, Klotz LO, Sies H (2003) Identification of cytosolic leucyl aminopeptidase (EC 1.4.11.1) as the major cysteinylglycine-hydrolysing activity in rat liver. Biol Chem 384: 213-218.
38. Cooper AJ (1997) Glutathione in the brain: Disorders of glutathione metabolism. The Molecular and Genetic Basis of Neurological Disease, eds Rosenberg R, Prusiner S, DiMauro S, Barchi R (Butterworth-Heinemann, Boston), 2nd Ed, pp 1195-1230.
39. Keillor JW, Castonguay R, Lherbet C (2005) Gamma-glutamyl transpeptidase substrate specificity and catalytic mechanism. Methods Enzymol 401:449-467.
40. Aoyama K, Watabe M, Nakaki T (2008) Regulation of neuronal glutathione synthesis. J Pharmacol Sci 108:227-238.
41. delCardayre SB, Stock KP, Newton GL, Fahey RC, Davies JE (1998) Coenzyme A disulfide reductase, the primary low molecular weight disulfide reductase from Staphylococcus aureus. Purification and characterization of the native enzyme. J Biol Chem 273:5744-5751.
42. Griffith OW, Meister A (1980) Excretion of cysteine and gamma-glutamylcysteine moieties in human and experimental animal gamma-glutamyl transpeptidase deficiency. Proc Natl Acad Sci USA 77:3384-3387.
43. Wang YA, et al. (2016) Nitrilase 1 modulates lung tumor progression in vitro and in vivo. Oncotarget 7:21381-21392.
44. Mittag S, et al. (2016) A novel role for the tumour suppressor Nitrilase1 modulating the Wnt/β-catenin signalling pathway. Cell Discovery 2:15039.
45. Kitagawa M, et al. (2005) Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): Unique resources for biological research. DNA Res 12:291-299.
46. Gemayel R, et al. (2007) Many fructosamine 3-kinase homologues in bacteria are ribulosamine/erythrulosamine 3-kinases potentially involved in protein deglycation. FEBS J 274:4360-4374.