Advertisement

Amino Acids

, Volume 41, Issue 1, pp 7–27 | Cite as

Cysteine S-conjugate β-lyases: important roles in the metabolism of naturally occurring sulfur and selenium-containing compounds, xenobiotics and anticancer agents

  • Arthur J. L. CooperEmail author
  • Boris F. Krasnikov
  • Zoya V. Niatsetskaya
  • John T. Pinto
  • Patrick S. Callery
  • Maria T. Villar
  • Antonio Artigues
  • Sam A. Bruschi
Review Article

Abstract

Cysteine S-conjugate β-lyases are pyridoxal 5′-phosphate-containing enzymes that catalyze β-elimination reactions with cysteine S-conjugates that possess a good leaving group in the β-position. The end products are aminoacrylate and a sulfur-containing fragment. The aminoacrylate tautomerizes and hydrolyzes to pyruvate and ammonia. The mammalian cysteine S-conjugate β-lyases thus far identified are enzymes involved in amino acid metabolism that catalyze β-lyase reactions as non-physiological side reactions. Most are aminotransferases. In some cases the lyase is inactivated by reaction products. The cysteine S-conjugate β-lyases are of much interest to toxicologists because they play an important key role in the bioactivation (toxication) of halogenated alkenes, some of which are produced on an industrial scale and are environmental contaminants. The cysteine S-conjugate β-lyases have been reviewed in this journal previously (Cooper and Pinto in Amino Acids 30:1–15, 2006). Here, we focus on more recent findings regarding: (1) the identification of enzymes associated with high-M r cysteine S-conjugate β-lyases in the cytosolic and mitochondrial fractions of rat liver and kidney; (2) the mechanism of syncatalytic inactivation of rat liver mitochondrial aspartate aminotransferase by the nephrotoxic β-lyase substrate S-(1,1,2,2-tetrafluoroethyl)-l-cysteine (the cysteine S-conjugate of tetrafluoroethylene); (3) toxicant channeling of reactive fragments from the active site of mitochondrial aspartate aminotransferase to susceptible proteins in the mitochondria; (4) the involvement of cysteine S-conjugate β-lyases in the metabolism/bioactivation of drugs and natural products; and (5) the role of cysteine S-conjugate β-lyases in the metabolism of selenocysteine Se-conjugates. This review emphasizes the fact that the cysteine S-conjugate β-lyases are biologically more important than hitherto appreciated.

Keywords

Cysteine S-conjugates Cysteine S-conjugate β-lyases S-(1,2-Dichlorovinyl)-l-cysteine Glutamine transaminase K Mitochondrial aspartate aminotransferase S-(1,1,2,2-tetrafluoroethyl)-l-cysteine 

Abbreviations

AlaAT

Alanine aminotransferase

AGAT II

Alanine-glyoxylate aminotransferase isoenzyme II

BCATc

Cytosolic branched-chain aminotransferase

BCATm

Mitochondrial branched-chain aminotransferase

BCDHC

Branched-chain α-keto acid dehydrogenase complex

BTC

S-(2-Benzothiazolyl)-l-cysteine

cAAT

Cytosolic aspartate aminotransferase

DCVC

S-(1,2-Dichlorovinyl)-l-cysteine

DFTAL

Difluorothioamidyl-lysine

EDAG

γ-Glutamyldehydroalanylglycine

ESI-MS

Electrospray ionization-mass spectrometry

GSH

Glutathione

GST

Glutathione S-transferase

GTK

Glutamine transaminase K

HSP60

Heat shock protein 60 kDa

HSP70i

Heat shock protein 70 kDa (inducible isoform)

Hsc70

Cytosolic HSP70

KAT I

Kynurenine aminotransferase isoenzyme I

KGDHC

α-Ketoglutarate dehydrogenase complex

mAAT

Mitochondrial aspartate aminotransferase

mitACON

Mitochondrial aconitase

mitHSP70

Heat shock protein 70 kDa (mitochondrial isoform)

mitGTK

Mitochondrial GTK

pmAAT

Precursor to mAAT

PDHC

Pyruvate dehydrogenase complex

PLP

Pyridoxal 5′-phosphate

PMP

Pyridoxamine 5′-phosphate

SAC

S-Allyl-l-cysteine

SAMC

S-Allylmercapto-l-cysteine

TCA cycle

Tricarboxylic acid cycle

TFA

Trifluoroacetic acid

TFEC

S-(1,1,2,2-Tetrafluoroethyl)-l-cysteine

THT

Tetrahydrothiophene

THT-A

β-(S-Tetrahydrothiophenium)-l-alanine

Notes

Acknowledgments

Part of the work cited from the authors’ laboratories was supported by NIH grants RO1 ES8421 (AJLC), CA111842 (JTP), GM51916 (SAB) National Institute of Justice Grant IJ-CX-K014 (PSC),University of Kansas Medical Center ROV10525 (AA).

References

  1. Abraham DG, Cooper AJL (1991) Glutamine transaminase K and cysteine S-conjugate β-lyase activity stains. Anal Biochem 197:421–427PubMedCrossRefGoogle Scholar
  2. Abraham DG, Cooper AJL (1996) Cloning and expression of a rat kidney cytosolic glutamine transaminase K that has strong sequence homology to kynurenine-pyruvate aminotransferase. Arch Biochem Biophys 335:311–320PubMedCrossRefGoogle Scholar
  3. Abraham DG, Patel PP, Cooper AJL (1995a) Isolation from rat kidney of a high molecular weight cysteine S-conjugate β-lyase with activity toward leukotriene E4. J Biol Chem 270:180–188PubMedCrossRefGoogle Scholar
  4. Abraham DG, Thomas RJ, Cooper AJL (1995b) Glutamine transaminase K is not a major cysteine S-conjugate β-lyase of rat kidney mitochondria: Evidence that a high-molecular-weight enzyme fulfills this role. Mol Pharmacol 48:855–860PubMedGoogle Scholar
  5. Adams B, Lowpetch K, Thorndycroft F, Whyte SM, Young DW (2005) Stereochemistry of reactions of the inhibitor/substrates l- and d-chloroalanine with β-mercaptoethanol catalysed by l-aspartate aminotransferase and D-amino acid aminotransferase respectively. Org Biomol Med 3:3357–3364CrossRefGoogle Scholar
  6. Adcock HJ, Brophy PM, Teesdale-Spittle PH, Bucknberry LD (1999) Cysteine conjugate β-lyase in three species of parasitic helminth. Int J Parasitol 29:543–548PubMedCrossRefGoogle Scholar
  7. Adcock HJ, Brophy PM, Teesdale-Spittle PH, Bucknberry LD (2000) Purification and characterisation of a novel cysteine conjugate β-lyase from the tapeworm Moniezia expansa. Int J Parasitol 30:56–71CrossRefGoogle Scholar
  8. Amato I (2009) You smell. Chem Eng News 87:50–54CrossRefGoogle Scholar
  9. Anders MW (2004) Glutathione-dependent bioactivation of haloalkanes and haloalkenes. Drug Metab Rev 36:583–594PubMedCrossRefGoogle Scholar
  10. Anders MW (2008) Chemical toxicology of reactive intermediates formed by the glutathione-dependent bioactivation of halogen-containing compounds. Chem Res Toxicol 21:145–159PubMedCrossRefGoogle Scholar
  11. Anders MW, Lash L, Dekant W, Elfarra AA, Dohn DR (1988) Biosynthesis and biotransformation of glutathione S-conjugates to toxic metabolites. Crit Rev Toxicol 18:311–341PubMedCrossRefGoogle Scholar
  12. Anderson PM, Schultze MO (1965) Cleavage of S-(1, 2-dichlorovinyl)-l-cysteine by an enzyme of bovine origin. Arch Biochem Biophys 111:593–602PubMedCrossRefGoogle Scholar
  13. Andreadou I, Menge WMPB, Commandeur JNM, Worthington EA, Vermeulen NPE (1996a) Synthesis of novel Se-substituted selenocysteine derivatives as potential kidney selective prodrugs of biologically active selenol compounds: evaluation of kinetics of β-elimination reactions in rat renal cytosol. J Med Chem 39:2040–2046PubMedCrossRefGoogle Scholar
  14. Andreadou I, van de Water B, Commandeur JNM, Nagelkerke FJ, Vermeulen NPE (1996b) Comparative cytotoxicity of 14 novel selenocysteine Se-conjugates in rat renal proximal tubular cells. Toxicol Appl Pharmacol 141:278–287PubMedGoogle Scholar
  15. Artigues A, Iriarte A, Martinez-Carrion M (2002) Binding to chaperones allows import of a purified mitochondrial precursor into mitochondria. J Biol Chem 277:25047–25055PubMedCrossRefGoogle Scholar
  16. Artigues A, Iriarte A, Martinez-Carrion M (2006) Identification of Hsc70 binding sites in mitochondrial aspartate aminotransferase. Arch Biochem Biophys 450:30–38PubMedCrossRefGoogle Scholar
  17. Bakke JE, Bergman ÅL, Larsen GL (1982) Metabolism of 2, 4’, 5-trichlorobiphenyl by the mercapturic acid pathway. Science 217:645–647PubMedCrossRefGoogle Scholar
  18. Bernström K, Larsen GL, Hammerström S (1989) Metabolism of leukotriene E4 to 5-hydroxy-6-mercapto-7, 9-trans-11, 14-cis-eicosatetraenoic acid by microfloral cysteine conjugate β-lyase and rat cecum contents. Arch Biochem Biophys 275:531–539PubMedCrossRefGoogle Scholar
  19. Bruschi SA, West KA, Crabb JW, Gupta RS, Stevens JL (1993) Mitochondrial HSP60 (P1 protein) and HSP70-like protein (mortalin) are major targets for modification during S-(1, 1, 2, 2-tetrafluoroethyl)-l-cysteine-induced toxicity. J Biol Chem 268:23157–23161PubMedGoogle Scholar
  20. Bruschi SA, Crabb JW, Stevens JL (1994) The E3 subunit of 2-oxoglutarate, branched-chain α-keto acid, and malate dehydrogenase are adducted during nephrotoxic cysteine-conjugate injury. Toxicologist 14:428 (Abstract)Google Scholar
  21. Bruschi SA, Lindsay JG, Crabb JW (1998) Mitochondrial stress protein recognition of inactivated dehydrogenases during mammalian cell death. Proc Natl Acad Sci USA 95:13413–13418PubMedCrossRefGoogle Scholar
  22. Cavallini D, Federici G, Bossa F, Granata F (1973) The protective effect of thiosulfate upon the inactivation of aspartate aminotransferase by aminoacrylic-acid-producing substrates. Eur J Biochem 39:301–304PubMedCrossRefGoogle Scholar
  23. Chasseaud LF (1976) Conjugation with glutathione and mercapturic acid excretion. In: Arias IM, Jakoby WB (eds) Glutathione: metabolism and function. Raven Press, New York, pp 77–114Google Scholar
  24. Chatfield DH, Hunter WH (1973) The metabolism of acetamidothiazoles in the rat. 2-Acetamido-4-chloromethylthiazole. Biochem J 134:879–884PubMedGoogle Scholar
  25. Clausen T, Huber R, Messerschmidt A, Pohlenz HD, Laber B (1997) Slow-binding inhibition of Escherichia coli cystathionine beta-lyase by L-aminoethoxyvinylglycine: a kinetic and X-ray study. Biochemistry 36:12633–12643PubMedCrossRefGoogle Scholar
  26. Colucci DF, Buyske DA (1965) The biotransformation of a sulfonamide to a mercaptan and to mercapturic acid and glucuronide conjugates. Biochem Pharmacol 14:457–466PubMedCrossRefGoogle Scholar
  27. Commandeur JNM, Andreadou I, Rooseboom M, Out M, de Leur LJ, Groot E, Vermeulen NPE (2000) Bioactivation of selenocysteine Se-conjugates by a highly purified rat renal cysteine conjugate β-lyase/glutamine transaminase K. J Pharmacol Exp Ther 294:753–761PubMedGoogle Scholar
  28. Commandeur JNM, Rooseboom M, Vermeulen NPE (2001) Chemistry and biological activity of novel selenium-containing compounds. Adv Exp Med Biol 500:105–112PubMedGoogle Scholar
  29. Cooper AJL, Hanigan MH (2010) Enzymes involved in processing of glutathione conjugates. In: McQueen CA (series ed), Guengerich FP (volume ed), Comprehensive toxicology, vol 4, 2nd edn. Biotransformations. Elsevier Press, Oxford (in press)Google Scholar
  30. Cooper AJL, Pinto JT (2005) Aminotransferase, L-amino acid oxidase and β-lyase reactions involving L-cysteine S-conjugates found in allium extracts. Relevance to biological activity? Biochem Pharmacol 69:209–220PubMedCrossRefGoogle Scholar
  31. Cooper AJL, Pinto JT (2006) Cysteine S-conjugate β-lyases. Amino Acids 30:1–15PubMedCrossRefGoogle Scholar
  32. Cooper AJL, Pinto JT (2008) Role of cysteine S-conjugate β-lyases in the bioactivation of renal toxicants. In: Elfarra AA (ed) Biotechnology: pharmaceutical aspects. Advances in bioactivation research. Springer, New York, pp 323–346Google Scholar
  33. Cooper AJL, Wang J, Gartner CA, Bruschi SA (2001) Co-purification of mitochondrial HSP70 and mature protein disulfide isomerase with a functional rat kidney high-M r cysteine S-conjugate β-lyase. Biochem Pharmacol 62:1345–1353PubMedCrossRefGoogle Scholar
  34. Cooper AJL, Bruschi SA, Anders MW (2002a) Toxic, halogenated cysteine S-conjugates and targeting of mitochondrial enzymes of energy metabolism. Biochem Pharmacol 64:553–564PubMedCrossRefGoogle Scholar
  35. Cooper AJL, Bruschi SA, Iriarte A, Martinez-Carrion M (2002b) Mitochondrial aspartate aminotransferase catalyses cysteine S-conjugate β-lyase reactions. Biochem J 368:253–261PubMedCrossRefGoogle Scholar
  36. Cooper AJL, Bruschi SA, Conway M, Hutson SM (2003) Human mitochondrial and cytosolic branched-chain aminotransferases are cysteine S-conjugate β-lyases, but turnover leads to inactivation. Biochem Pharmacol 65:181–192PubMedCrossRefGoogle Scholar
  37. Cooper AJL, Pinto JT, Krasnikov BF, Niatsetskaya ZV, Han Q, Li J, Vauzour D, Spencer JPE (2008a) Substrate specificity of human glutamine transaminase K as an aminotransferase and as a cysteine S-conjugate β-lyase. Arch Biochem Biophys 474:72–81PubMedCrossRefGoogle Scholar
  38. Cooper AJL, Younis IR, Niatsetskaya ZV, Krasnikov BF, Pinto JT, Petros WP, Callery PS (2008b) Metabolism of the cysteine S-conjugate of busulfan involves a β-lyase reaction. Drug Metab Dispos 36:1546–1552PubMedCrossRefGoogle Scholar
  39. Czerwinski M, Gibbs JP, Slattery JT (1996) Busulfan conjugation by glutathione S-transferases α, μ, and π. Drug Metab Dispos 24:1015–1019PubMedGoogle Scholar
  40. Dekant W (2003) Biosynthesis of toxic glutathione conjugates from halogenated alkenes. Toxicol Lett 144:49–54PubMedCrossRefGoogle Scholar
  41. Dekant W, Vamvakas S, Anders MW (1994) Formation and fate of nephrotoxic and cytotoxic glutathione S-conjugates: Cysteine conjugate β-lyase pathway. Adv Pharmacol 27:115–162PubMedCrossRefGoogle Scholar
  42. Dong Y, Zhang H, Hawthorn L, Ganther HE, Ip C (2003) Delineation of the molecular basis for selenium-induced growth arrest in human prostate cancer cells by oligonucleotide array. Cancer Res 63:52–59PubMedGoogle Scholar
  43. Dowd CA, Sheehan D (1999) Variable expression of glutathione S-transferase isoenzymes in the fungus, Mucor circinelloides. FEMS Microbiol Lett 170:13–17PubMedCrossRefGoogle Scholar
  44. Elfarra AA, Hwang IY (1990) In vivo metabolites of S-(2-benzothiazolyl)-l-cysteine as markers of in vivo cysteine conjugate β-lyase and thiol glucuronosyl transferase activities. Drug Metab Dispos 18:917–922PubMedGoogle Scholar
  45. Elfarra AA, Hwang IY (1993) Targeting of 6-mercaptopurine to the kidneys. Metabolism and kidney-selectivity of S-(6-purinyl)-l-cysteine analogs in rats. Drug Metab Dispos 21:841–845PubMedGoogle Scholar
  46. Elfarra AA, Duescher RJ, Hwang IY, Sicuri AR, Nelson JA (1995) Targeting 6-thioguanine to the kidney with S-(guanin-6-yl)-l-cysteine. J Pharmacol Exp Ther 274:1298–1304PubMedGoogle Scholar
  47. Emter R, Natsch A (2008) The sequential action of a dipeptidase and a β-lyase is required for the release of the human body odorant 3-methyl-3-sulfanylhexan-1-ol from a secreted Cys-Gly-(S) conjugate by Corynebacteria. J Biol Chem 25:20645–20652CrossRefGoogle Scholar
  48. Eng JK, Fischer B, Grossmann J, Maccoss MJ (2008) A fast SEQUEST cross correlation algorithm. J Proteome Res 7:4598–4602PubMedCrossRefGoogle Scholar
  49. Escher S, Niclass Y, van de Waal M, Starkenmann C (2006) Combinatorial synthesis by nature: volatile organic sulfur-containing constituents of Ruta chalepensis L. Chem Biodivers 3:943–957PubMedCrossRefGoogle Scholar
  50. Fisher MB, Hayden PJ, Bruschi SA, Dulik DM, Yang Y, Ward AJ, Stevens JL (1993) Formation, characterization, and immunoreactivity of lysine thioamide adducts from fluorinated nephrotoxic cysteine conjugates in vitro and in vivo. Chem Res Toxicol 6:223–230PubMedCrossRefGoogle Scholar
  51. Gibbs JP, Czerwinski M, Slattery JT (1996) Busulfan-glutathione conjugation catalyzed by human liver cytosolic glutathione S-transferases. Cancer Res 56:3678–3681PubMedGoogle Scholar
  52. Gundimeda U, Schiffman JE, Chhabra D, Wong J, Wu A, Gopalakrishna R (2008) Locally generated methylseleninic acid induces specific inactivation of protein kinase C isoenzymes: relevance to selenium-induced apoptosis in prostate cancer cells. J Biol Chem 283:34519–34531PubMedCrossRefGoogle Scholar
  53. Hafsah Z, Tahara S, Mizutani J (1987) Microbiol metabolism of chlorinated nitrobenzenes. IV. Metabolic pathways of 2, 4-dichloro-1-nitrobenzene in Mucor javanicus. J Pesticide Sci 12:617–625Google Scholar
  54. Hanigan MH, Devarajan P (2003) Cisplatin nephrotoxicity: molecular mechanisms. Cancer Ther 1:47–61PubMedGoogle Scholar
  55. Harris JW, Dekant W, Anders MW (1992) In vivo detection and characterization of protein adducts resulting from bioactivation of haloethene cysteine S-conjugates by 19F NMR: chlorotrifluoroethene and tetrafluoroethene. Chem Res Toxicol 5:34–41PubMedCrossRefGoogle Scholar
  56. Hayden PJ, Stevens JL (1990) Cysteine conjugate toxicity, metabolism and binding to macromolecules in isolated rat kidney mitochondria. Mol Pharmacol 37:468–476PubMedGoogle Scholar
  57. Hayden PJ, Ichimura T, McCann DJ, Pohl LR, Stevens JL (1991) Detection of cysteine conjugate metabolite adduct formation with specific mitochondrial proteins using antibodies raised against halothane metabolite adducts. J Biol Chem 266:18415–18418PubMedGoogle Scholar
  58. Hinchman CA, Ballatori N (1994) Glutathione conjugation and conversion to mercapturic acids can occur as an intrahepatic process. J Toxicol Environ Health 41:387–409PubMedCrossRefGoogle Scholar
  59. Ho HK, Hu Z-H, Tzung S-P, Hockenbery DM, Fausto N, Nelson SD, Bruschi SA (2005) BCL-xL overexpression effectively protects against tetrafluoroethylcysteine-induced intramitochondrial damage and cell death. Biochem Pharmacol 69:147–157PubMedCrossRefGoogle Scholar
  60. Ho HK, Jia Y, Coe KJ, Gao Q, Doneanu CE, Hu ZH, Bammler TK, Beyer RP, Fausto N, Bruschi SA, Nelson SD (2006) Cytosolic heat shock proteins and heme oxygenase-1 are preferentially induced in response to specific and localized intramitochondrial damage by tetrafluoroethylcysteine. Biochem Pharmacol 72:80–90PubMedCrossRefGoogle Scholar
  61. Iciek M, Kwiecień I, Włodek L (2009) Biological properties of garlic and garlic-derived organosulfur compounds. Environ Mol Mutagen 50:247–265PubMedCrossRefGoogle Scholar
  62. Ip C, Zhu Z, Thompson HJ, Lisk D, Ganther HE (1999) Chemoprevention of mammary cancer with Se-allylselenocysteine and other selenoamino acids in the rat. Anticancer Res 19:2875–2880PubMedGoogle Scholar
  63. Ip C, Thompson HJ, Zhu Z, Ganther HE (2000) In vitro and in vivo studies of methylseleninic acid: evidence that a monomethylated selenium metabolite is critical for cancer chemoprevention. Cancer Res 60:2882–2886PubMedGoogle Scholar
  64. Ip C, Dong Y, Ganther HE (2002) New concepts in selenium chemoprevention. Cancer Metastasis Rev 21:281–289PubMedCrossRefGoogle Scholar
  65. Islam MM, Nautiyal M, Wynn RM, Mobley JA, Chunag DT, Hutson SM (2010) Branched-chain amino acid metabolon. Interaction of glutamate dehydrogenase with mitochondrial branched-chain aminotransferase (BCATm). J Biol Chem 285:265–276PubMedCrossRefGoogle Scholar
  66. Iwamoto T, Hiraku Y, Oikawa S, Mizutani H, Kojima M, Kawanishi S (2004) DNA intrastrand cross-link at the 5’-GA-3’ sequence formed by busulfan and its role in the cytotoxic effect. Cancer Sci 95:454–458PubMedCrossRefGoogle Scholar
  67. Jakoby WB, Stevens J (1984) Cysteine conjugate lyase and the thiomethyl shunt. Biochem Soc Trans 12:33–35PubMedGoogle Scholar
  68. James EA, Gygi SP, Adams ML, Pierce RH, Fausto N, Aebersold RH, Nelson SD, Bruschi SA (2002) Mitochondrial aconitase modification, functional inhibition, and evidence for a supramolecular complex of the TCA cycle by the renal toxicant S-(1, 1, 2, 2-tetrafluoroethyl)-l-cysteine. Biochemistry 41:6789–6797PubMedCrossRefGoogle Scholar
  69. Kim HS, Cha SH, Abraham DG, Cooper AJL, Endou H (1997) Intranephron distribution of cysteine-S-conjugate β-lyase activity and implication for hexachloro-1, 3-butadiene-induced nephrotoxicity in rats. Arch Toxicol 71:131–141PubMedCrossRefGoogle Scholar
  70. Kishida K, Saida N, Yamamura N, Iwai Y, Sasabe T (2001) Cysteine conjugate of methazolamide is metabolized by β-lyase. J Pharm Sci 90:224–233PubMedCrossRefGoogle Scholar
  71. Koob M, Dekant W (1991) Bioactivation of xenobiotics by formation of toxic glutathione conjugates. Chem Biol Interact 77:107–136PubMedCrossRefGoogle Scholar
  72. Larsen GL, Bakke JE (1983) Metabolism of mercapturic acid-pathway metabolites of 2-chloro-N-isopropylacetanilide (propachlor) by gastrointestinal bacteria. Xenobiotica 13:115–126PubMedCrossRefGoogle Scholar
  73. Larsen GL, Stevens JL (1986) Cysteine conjugate β-lyase in the gastrointestinal bacterium Eubacterium limosum. Mol Pharmacol 29:97–103PubMedGoogle Scholar
  74. Larsen GL, Larson JD, Gustafsson J-Å (1983) Cysteine conjugate β-lyase in the gastrointestinal bacterium Fusobacterium necrophorum. Xenobiotica 13:689–700PubMedCrossRefGoogle Scholar
  75. Lee J-I, Nian H, Cooper AJL, Sinha R, Dai J, Bisson WH, Dashwood RH, Pinto JT (2009) α-Keto acid metabolites of naturally occurring organoselenium compounds as inhibitors of histone deacetylase in human prostate cancer cells. Cancer Prev Res 2:683–693CrossRefGoogle Scholar
  76. Mattingly JR Jr, Iriarte A, Martinez-Carrion M (1995) Homologous proteins with different affinities for groEL. The refolding of the aspartate aminotransferase isozymes at varying temperatures. J Biol Chem 270:1138–1148PubMedCrossRefGoogle Scholar
  77. Morino Y, Osman AM, Okamoto M (1974) Formate-induced labeling of the active site of aspartate aminotransferase by β-chloro-l-alanine. J Biol Chem 249:6684–6692PubMedGoogle Scholar
  78. Mosca M, Cozzi L, Breton J, Speciale C, Okuno E, Schwarcz R, Benatti L (1994) Molecular cloning of rat kynurenine aminotransferase: identity with glutamine transaminase K. FEBS Lett 353:21–24PubMedCrossRefGoogle Scholar
  79. Musah RA, He Q, Kubec R, Jadhav A (2009) Studies of a novel cysteine sulfoxide lyase from Petiveria alliacea: The first heteromeric alliinase. Plant Physiol 151:1304–1316PubMedCrossRefGoogle Scholar
  80. Nagelkerke JF, Boogaard PJ (1991) Nephrotoxicity of halogenated alkenyl cysteine-S-conjugates. Life Sci 49:1769–1776PubMedCrossRefGoogle Scholar
  81. Nagini S (2008) Cancer chemoprevention by garlic and its organosulfur compounds–panacea or promise? Anticancer Agents Med Chem 8:313–321PubMedCrossRefGoogle Scholar
  82. Natsch A, Schmid J, Flachsmann F (2004) Identification of odiferous sulfanylalkanols in human axilla secretions and their formation through cleavage of cysteine precursors by a C-S lyase isolated from axilla bacteria. Chem Biodiv 1:1058–1072CrossRefGoogle Scholar
  83. Nelson SD, Pearson PG (1990) Covalent and noncovalent interactions in acute lethal cell injury caused by chemicals. Annu Rev Pharmacol Toxicol 30:169–195PubMedCrossRefGoogle Scholar
  84. Nian H, Bisson WH, Dashwood WM, Pinto JT, Dashwood RH (2009) α-Keto acid metabolites of organoselenium compounds inhibit histone deacetylase activity in human colon cancer cells. Carcinogenesis 30:1416–1423PubMedCrossRefGoogle Scholar
  85. Ohta Y, Suzuki KT (2008) Methylation and demethylation of intermediates selenide and methylselenol in the metabolism of selenium. Toxicol Appl Pharmacol 226:169–177PubMedCrossRefGoogle Scholar
  86. Perry SJ, Schofield MA, MacFarlane M, Lock EA, King LJ, Gibson GG, Goldfarb PS (1993) Isolation and expression of a cDNA coding for rat kidney cytosolic cysteine conjugate β-lyase. Mol Pharmacol 43:660–665PubMedGoogle Scholar
  87. Pinto JT, Lapsia S, Shah A, Santiago H, Kim G (2001) Antiproliferative effects of garlic-derived and other allium related compounds. Adv Exp Med Biol 492:83–106PubMedGoogle Scholar
  88. Pinto JT, Krasnikov BF, Cooper AJL (2006) Redox-sensitive proteins are potential targets of garlic derived mercaptocysteine derivatives. J Nutr 136:S835–S841Google Scholar
  89. Pinto JT, Lee JI, Sinha Cooper AJL (2010) Chemopreventive mechanisms of α-keto acid metabolites of naturally occurring organoselenium compounds. this volume, Amino AcidsGoogle Scholar
  90. Ritter CA, Bohnenstengel F, Hofmann U, Kroemer HK, Sperker B (1999) Determination of tetrahydrothiophene formation as a probe of in vitro busulfan metabolism by human glutathione S-transferase A1–1: use of highly sensitive gas chromatographic-mass spectrometric method. J Chromatog B Biomed Sci Appl 730:25–31CrossRefGoogle Scholar
  91. Ritter CA, Sperker B, Grube M, Dressel D, Kunert-Keil C, Kroemer HK (2002) Overexpression of glutathione S-transferase A1–1 in ECV 304 cells protects against busulfan mediated G2-arrest and induces tissue factor expression. Br J Pharmacol 137:1100–1106PubMedCrossRefGoogle Scholar
  92. Roberts JJ, Warwick GP (1961) The mode of action of alkylating agents. III. The formation of 3-hydroxytetrahydrothiophene-1:1-dioxide from 1:4-dimethanesulphonyloxybutane (myleran), S-β-l-alanyl-tetrahydrothiophenium mesylate, tetrahydrothiophene and tetrahydrothiophene-1:1-dioxide in the rat, rabbit and mouse. Biochem Pharmacol 6:217–227Google Scholar
  93. Rooseboom M, Vermeulen NPE, Andreadou I, Commandeur JNM (2000) Evaluation of the kinetics of β-elimination reactions of selenocysteine Se-conjugates in human renal cytosol: possible implications for the use as kidney selective prodrugs. J Pharmacol Exp Ther 294:762–769PubMedGoogle Scholar
  94. Rooseboom M, Vermeulen NPE, Groot EJ, Commandeur JNM (2002a) Tissue distribution of cytosolic β-elimination reactions of selenocysteine Se-conjugates in rat and human. Chem Biol Interact 140:243–264PubMedCrossRefGoogle Scholar
  95. Rooseboom M, Vermeulen NPE, Commandeur JNM (2002b) Enzymatic pathways of β elimination of chemopreventive selenocysteine Se conjugates. Methods Enzymol 348:191–200PubMedCrossRefGoogle Scholar
  96. Rooseboom M, Vermeulen NPE, Durgut F, Commandeur JNM (2002c) Comparative study on the bioactivation, mechanisms and cytotoxicity of Te-phenyl-l-tellurocysteine, Se-phenyl-l-selenocysteine and S-phenyl-l-cysteine. Chem Res Toxicol 15:1610–1618PubMedCrossRefGoogle Scholar
  97. Rossi F, Han Q, Li J, Li J, Rizzi M (2004) Crystal structure of human kynurenine aminotransferase I. J Biol Chem 279:50214–50220PubMedCrossRefGoogle Scholar
  98. Saari JC, Schultze MO (1965) Cleavage of S-(1, 2-dichlorovinyl)-l-cysteine by Escherichia coli B. Arch Biochem Biophys 109:595–602PubMedCrossRefGoogle Scholar
  99. Schwiertz A, Deubel S, Birringer M (2008) Bioactivation of selenocysteine derivatives by β-lyases present in common gastrointestinal bacterial species. Int J Vitam Nutr Res 78:169–174PubMedCrossRefGoogle Scholar
  100. Scott CS, Chiu WA (2006) Trichloroethylene cancer epidemiology: a consideration of select issues. Environ Health Perspect 114:1471–1478PubMedCrossRefGoogle Scholar
  101. Shimomura N, Honma M, Chiba S, Tahara S, Mizutani J (1992) Cysteine-conjugate β-lyase from Mucor javanicus. Biosci Biotech Biochem 56:963–964CrossRefGoogle Scholar
  102. Silbernagl S, Heuner A (1993) Renal transport of mercapturic acids and their precursors, the S-conjugates of glutathione and cysteine. In: Anders MW, Dekant W, Henschler D, Oberleithner H, Silbernagl S (eds) Renal disposition and nephrotoxicity of xenobiotics. Academic Press, Inc., San Diego, pp 135–154Google Scholar
  103. Srere PA (1987) Complexes of sequential metabolic enzymes. Annu Rev Biochem 56:89–124PubMedCrossRefGoogle Scholar
  104. Starkenmann C, Niclass Y, Troccaz M, Clark AJ (2005) Identification of the precursor of (S)-3-methyl-3-sulfanylhexan-1-ol, the sulfury malodour of human axilla sweat. Chem Biodivers 2:705–716PubMedCrossRefGoogle Scholar
  105. Starkenmann C, Luca L, Niclass Y, Praz E, Roguet D (2006) Comparison of volatile constituents of Persicaria odorata (Lour.) Soják (Polygonum odoratum Lour.) and Persicaria hydropiper L. Spach (Polygonum hydropiper L.). J Agric Food Chem 54:3067–3071PubMedCrossRefGoogle Scholar
  106. Starkenmann C, Niclass Y, Escher S (2007) Volatile organic sulfur-containing constituents in Poncirus trifoliata (L.) Raf. (Rutaceae). J Agric Food Chem 55:4511–4517PubMedCrossRefGoogle Scholar
  107. Starkenmann C, Le Calvé B, Niclass Y, Cayeux I, Beccucci S, Troccaz M (2008) Olfactory perception of cysteine-S-conjugates from fruits and vegetables. J Agric Food Chem 56:9575–9580PubMedCrossRefGoogle Scholar
  108. Stevens JL (1985) Isolation and characterization of a rat liver enzyme with both cysteine conjugate β-lyase and kynureninase activity. J Biol Chem 260:7945–7950PubMedGoogle Scholar
  109. Stevens JL, Jones DP (1989) The mercapturic acid pathway: Biosynthesis, intermediary metabolism, and physiological disposition. In: Dolphin D, Poulson R, Avramović O (eds) Glutathione: chemical biochemical and medicinal aspects, Part B. Wiley, New York, pp 45–84Google Scholar
  110. Stevens JL, Robbins JD, Byrd RA (1986) A purified cysteine conjugate β-lyase from rat kidney cytosol. Requirement for an α-keto acid or an amino acid oxidase for activity and identity with soluble glutamine transaminase K. J Biol Chem 261:15529–15537PubMedGoogle Scholar
  111. Suzuki S, Tomisawa H, Ichihara S, Fukuzawa M, Tateishi M (1982) A C-S bond cleavage enzyme of cysteine conjugates in intestinal microorganisms. Biochem Pharmacol 31:2137–2140PubMedCrossRefGoogle Scholar
  112. Suzuki KT, Doi C, Suzuki N (2006) Metabolism of 76Se-methylselenocysteine compared with that of 77Se-selenomethionine and 82Se-selenite. Toxicol Appl Pharmacol 217:185–195Google Scholar
  113. Suzuki KT, Kurasaki K, Suzuki N (2007) Selenocysteine β-lyase and methylselenol demethylase in the metabolism of Se-methylated selenocompounds into selenide. Biochim Biophys Acta 1770:1053–1061PubMedGoogle Scholar
  114. Tateishi M, Suzuki S, Shimizu H (1978a) The metabolism of bromazepam in the rat–identification of mercapturic acid and its conversion in vitro to methylthio-bromazepam. Biochem Pharmacol 27:809–810PubMedCrossRefGoogle Scholar
  115. Tateishi M, Suzuki S, Shimizu H (1978b) Cysteine conjugate β-lyase in rat liver. A novel enzyme catalyzing formation of thiol-containing metabolites of drugs. J Biol Chem 253:8854–8859PubMedGoogle Scholar
  116. Tomisawa H, Suzuki S, Ichihara S, Fukuzawa H, Tateishi M (1984) Purification and characterization of a C-S lyase from Fusobacterium varium. A C-S cleavage enzyme of cysteine conjugates and some S-containing amino acids. J Biol Chem 259:2588–2593PubMedGoogle Scholar
  117. Townsend DM, Tew KD, He L, King JB, Hanigan MH (2009) Role of glutathione S-transferase Pi in cisplatin-induced nephrotoxicity. Biomed Pharmacother 63:79–85PubMedCrossRefGoogle Scholar
  118. Tsuji Y, Suzuki N, Suzuki KT, Ogra Y (2009) Selenium metabolism in rats with long-term ingestion of Se-methylselenocysteine using enriched stable isotopes. J Toxicol Sci 34:191–200Google Scholar
  119. Ueno H, Likos JJ, Metzler DE (1982) Chemistry of the inactivation of cytosolic aspartate aminotransferase by serine O-sulfate. Biochemistry 21:4387–4393PubMedCrossRefGoogle Scholar
  120. Uttamsingh V, Anders MW (1999) Acylase-catalyzed deacetylation of haloalkene-derived mercapturates. Chem Res Toxicol 12:937–942PubMedCrossRefGoogle Scholar
  121. Villar MT, Niatsetskaya ZV, Cooper AJL, Artigues A (2007) Inactivation of rat liver mitochondrial aspartate aminotransferase by a halogenated cysteine S-conjugate. Mol Cell Proteomics 6(Suppl 1) (Abstract #B5, 40)Google Scholar
  122. Wadhwa R, Takano S, Kaur K, Aida S, Yaguchi T, Kaul Z, Hirano T, Taira K, Kaul SC (2005) Identification and characterization of molecular interactions between mortalin/mtHsp70 and HSP60. Biochem J 391:185–190PubMedCrossRefGoogle Scholar
  123. Wakabayashi H, Wakabayashi M, Eisenreich W, Engel KH (2004) Stereochemical course of the generation of 3-mercaptohexanol by β-lyase-catalyzed cleavage of cysteine conjugates. J Agric Food Chem 52:110–116PubMedCrossRefGoogle Scholar
  124. Warrander A, Allen JM, Andrews RS (1985) Incorporation of radiolabelled amino acids into the sulphur-containing metabolites of paracetamol by the hamster. Xenobiotica 15:891–897PubMedCrossRefGoogle Scholar
  125. Wessjohann LA, Schneider A, Abbas M, Brandt W (2007) Selenium in chemistry and biochemistry in comparison to sulfur. Biol Chem 388:997–1006PubMedCrossRefGoogle Scholar
  126. Younis IR, Elliott M, Peer CJ, Cooper AJL, Pinto JT, Konat GW, Kraszpulski M, Petros WP, Callery PS (2008) Dehydroalanine analog of glutathione: an electrophilic busulfan metabolite that binds to human glutathione S-transferase A1–1. J Pharmacol Exp Ther 327:770–776PubMedCrossRefGoogle Scholar
  127. Zhang L, Hanigan MH (2003) Role of cysteine S-conjugate β-lyase in the metabolism of cisplatin. J Pharmacol Exp Ther 306:988–994PubMedCrossRefGoogle Scholar
  128. Zhang L, Cooper AJL, Krasnikov BF, Xu H, Bubber P, Pinto JT, Gibson GE, Hanigan MH (2006) Cisplatin-induced toxicity is associated with platinum deposition in mouse kidney mitochondria in vivo and with selective inactivation of α-ketoglutarate dehydrogenase complex in LLC-PK1 cells. Biochemistry 45:8959–8971PubMedCrossRefGoogle Scholar
  129. Zhu Z, Jiang W, Ganther HE, Ip C, Thompson HJ (2000) In vitro effects of Se-allylselenocysteine and Se-propylselenocysteine on cell growth, DNA integrity, and apoptosis. Biochem Pharmacol 60:1467–1473PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Arthur J. L. Cooper
    • 1
    Email author
  • Boris F. Krasnikov
    • 1
  • Zoya V. Niatsetskaya
    • 2
  • John T. Pinto
    • 1
  • Patrick S. Callery
    • 3
  • Maria T. Villar
    • 4
  • Antonio Artigues
    • 4
  • Sam A. Bruschi
    • 5
  1. 1.Department of Biochemistry and Molecular BiologyNew York Medical CollegeValhallaUSA
  2. 2.Columbia UniversityNew YorkUSA
  3. 3.Department of Basic Pharmaceutical Sciences, School of PharmacyWest Virginia UniversityMorgantownUSA
  4. 4.Department of Biochemistry and Molecular BiologyUniversity of Kansas Medical CenterKansas CityUSA
  5. 5.Laural ConsultingAdelaideAustralia

Personalised recommendations