Kinetic characterization of methionine γ-lyases from the enteric protozoan parasite Entamoeba histolytica against physiological substrates and trifluoromethionine, a promising lead compound against amoebiasis

FEBS Journal

Volumn 275, Issue 3, 2008, Pages 548-560

  Sato, Dan ^a,c   Yamagata, Wataru ^b   Harada, Shigeharu ^b   Nozaki, Tomoyoshi ^a  

^a GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KYOTO INSTITUTE OF TECHNOLOGY   (Japan)

^c KEIO UNIVERSITY   (Japan)

Author keywords

Amoebiasis; Methionine lyase; Site directed mutagenesis; Sulfur containing amino acid; Trifluoromethionine

Indexed keywords

ANTIAMEBIC AGENT; CYSTEINE; CYSTEINE SYNTHASE; ISOENZYME; METHIONINE DERIVATIVE; METHIONINE GAMMA LYASE; RECOMBINANT ENZYME; SERINE; SULFUR AMINO ACID; TRIFLUOROMETHIONINE; UNCLASSIFIED DRUG;

AMEBIASIS; ARTICLE; CONTROLLED STUDY; CROSS LINKING; ENTAMOEBA HISTOLYTICA; ENZYME ANALYSIS; ENZYME DEGRADATION; ENZYME KINETICS; ENZYME PURIFICATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SITE DIRECTED MUTAGENESIS;

AMEBIASIS; ANIMALS; BASE SEQUENCE; CARBON-SULFUR LYASES; CYSTEINE; ENTAMOEBA HISTOLYTICA; ISOENZYMES; KINETICS; METHIONINE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY;

ENTAMOEBA HISTOLYTICA; MAMMALIA; PROTISTA; PROTOZOA; TRICHOMONAS VAGINALIS;

EID: 38149112907     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.06221.x     Document Type: Article

References (45)

1. Brosnan JT Brosnan ME (2006) The sulfur-containing amino acids: an overview. J Nutr 136, 1636S 1640S.
2. Cellarier E, Durando X, Vasson MP, Farges MC, Demiden A, Maurizis JC, Madelmont JC Chollet P (2003) Methionine dependency and cancer treatment. Cancer Treat Rev 29, 489 499.
3. Ali V Nozaki T (2007) Current therapeutics, their problems, and sulfur-containing-amino-acid metabolism as a novel target against infections by 'amitochondriate' protozoan parasites. Clin Microbiol Rev 20, 164 187.
4. Alexander FW, Sandmeier E, Mehta PK Christen P (1994) Evolutionary relationships among pyridoxal-5′-phosphate-dependent enzymes. Regio-specific alpha, beta and gamma families. Eur J Biochem 219, 953 960.
5. Tanaka H, Esaki N Soda K (1985) A versatile bacterial enzyme: L-methionine γ-lyase. Enzyme Microb Technol 7, 530 537.
6. Nakayama T, Esaki N, Sugie K, Beresov TT, Tanaka H Soda K (1984) Purification of bacterial L-methionine gamma-lyase. Anal Biochem 138, 421 424.
7. Kreis W Hession C (1973) Isolation and purification of L-methionine-alpha-deamino-gamma-mercaptomethane-lyase (L-methioninase) from Clostridium sporogenes. Cancer Res 33, 1862 1865.
8. Faleev NG, Troitskaya MV, Paskonova EA, Saporovskaya MB Belikov VM (1996) L-methionine-γ-lyase in Citrobacter intermedius cells: stereochemical requirements with respect to the thiol structure. Enzyme Microb Technol 19, 590 593.
9. Manukhov IV, Mamaeva DV, Rastorguev SM, Faleev NG, Morozova EA, Demidkina TV Zavilgelsky GB (2005) A gene encoding L-methionine gamma-lyase is present in Enterobacteriaceae family genomes: identification and characterization of Citrobacter freundii L-methionine gamma-lyase. J Bacteriol 187, 3889 3893.
10. Dias B Weimer B (1998) Purification and characterization of L-methionine gamma-lyase from Brevibacterium linens BL2. Appl Environ Microbiol 64, 3327 3331.
11. Yoshimura M, Nakano Y, Yamashita Y, Oho T, Saito T Koga T (2000) Formation of methyl mercaptan from L-methionine by Porphyromonas gingivalis. Infect Immun 68, 6912 6916.
12. Lockwood BC Coombs GH (1991) Purification and characterization of methionine gamma-lyase from Trichomonas vaginalis. Biochem J 279, 675 682.
13. Tokoro M, Asai T, Kobayashi S, Takeuchi T Nozaki T (2003) Identification and characterization of two isoenzymes of methionine gamma-lyase from Entamoeba histolytica: a key enzyme of sulfur-amino acid degradation in an anaerobic parasitic protist that lacks forward and reverse trans-sulfuration pathways. J Biol Chem 278, 42717 42727.
14. Rebeille F, Jabrin S, Bligny R, Loizeau K, Gambonnet B, Van Wilder V, Douce R Ravanel S (2006) Methionine catabolism in arabidopsis cells is initiated by a gamma-cleavage process and leads to S-methylcysteine and isoleucine syntheses. Proc Natl Acad Sci USA 103, 15687 15692.
15. Nozaki T, Ali V Tokoro M (2005) Sulfur-containing amino acid metabolism in parasitic protozoa. Adv Parasitol 60, 1 99.
16. Anderson IJ Loftus BJ (2005) Entamoeba histolytica: observations on metabolism based on the genome sequence. Exp Parasitol 110, 173 177.
17. McKie AE, Edlind T, Walker J, Mottram JC Coombs GH (1998) The primitive protozoon Trichomonas vaginalis contains two methionine gamma-lyase genes that encode members of the gamma-family of pyridoxal 5′-phosphate-dependent enzymes. J Biol Chem 273, 5549 5556.
18. WHO/PAHO/UNESCO report. A consultation with experts on amoebiasis. Mexico City, Mexico 28-29 January, 1997. Epidemiol Bull 13 14.
19. Stanley SL Jr. (2003) Amoebiasis. Lancet 361, 1025 1034.
20. Samarawickrema NA, Brown DM, Upcroft JA, Thammapalerd N Upcroft P (1997) Involvement of superoxide dismutase and pyruvate:ferredoxin oxidoreductase in mechanisms of metronidazole resistance in Entamoeba histolytica. J Antimicrob Chemother 40, 833 840.
21. Wassmann C, Hellberg A, Tannich E Bruchhaus I (1999) Metronidazole resistance in the protozoan parasite Entamoeba histolytica is associated with increased expression of iron-containing superoxide dismutase and peroxiredoxin and decreased expression of ferredoxin 1 and flavin reductase. J Biol Chem 274, 26051 26056.
22. Upcroft P Upcroft JA (2001) Drug targets and mechanisms of resistance in the anaerobic protozoa. Clin Microbiol Rev 14, 150 164.
23. Dannley RL Taborsky RG (1957) Synthesis of DL-S- trifluoromethylhomocysteine (trifluoromethylmethionine). J Organic Chem 22, 1275 1276.
24. Zygmunt WA Tavormina PA (1966) DL-S-Trifluoromethylhomocysteine, a novel inhibitor of microbial growth. Can J Microbiol 12, 143 148.
25. Yoshimura M, Nakano Y Koga T (2002) L-Methionine-gamma-lyase, as a target to inhibit malodorous bacterial growth by trifluoromethionine. Biochem Biophys Res Commun 292, 964 968.
26. Coombs GH Mottram JC (2001) Trifluoromethionine, a prodrug designed against methionine gamma-lyase-containing pathogens, has efficacy in vitro and in vivo against Trichomonas vaginalis. Antimicrob Agents Chemother 45, 1743 1745.
27. Inoue H, Inagaki K, Adachi N, Tamura T, Esaki N, Soda K Tanaka H (2000) Role of tyrosine 114 of L-methionine gamma-lyase from Pseudomonas putida. Biosci Biotechnol Biochem 64, 2336 2343.
28. Kudou D, Misaki S, Yamashita M, Tamura T, Takakura T, Yoshioka T, Yagi S, Hoffman RM, Takimoto A Inagaki K (2007) Structure of the antitumor enzyme L-methionine γ-lyase from Pseudomonas putida at 1.8 Å resolution. J Biochem (Tokyo) 141, 535 544.
29. Northrop DB (1999) So what exactly is V/K, anyway? In Enzymatic Mechanisms (Frey PA Northrop DB, eds Biomed Health Res 250 263.
30. Bakker-Grunwald T, Martin JB Klein G (1995) Characterization of glycogen and amino acid pool of Entamoeba histolytica by 13C-NMR spectroscopy. J Eukaryot Microbiol 42, 346 349.
31. Jakubowski H (2004) Molecular basis of homocysteine toxicity in humans. Cell Mol Life Sci 61, 470 487.
32. Ueland PM Refsum H (1989) Plasma homocysteine, a risk factor for vascular disease: plasma levels in health, disease, and drug therapy. J Lab Clin Med 114, 473 501.
33. Nozaki T, Tokoro M, Imada M, Saito Y, Abe Y, Shigeta Y Takeuchi T (2000) Cloning and biochemical characterization of genes encoding two isozymes of cysteine synthase from Entamoeba dispar. Mol Biochem Parasitol 107, 129 133.
34. Nozaki T, Asai T, Kobayashi S, Ikegami F, Noji M, Saito K Takeuchi T (1998) Molecular cloning and characterization of the genes encoding two isoforms of cysteine synthase in the enteric protozoan parasite Entamoeba histolytica. Mol Biochem Parasitol 97, 33 44.
35. Gilchrist CA, Houpt E, Trapaidze N, Fei Z, Crasta O, Asgharpour A, Evans C, Martino-Catt S, Baba DJ, Stroup S et al. (2006) Impact of intestinal colonization and invasion on the Entamoeba histolytica transcriptome. Mol Biochem Parasitol 147, 163 176.
36. Sato D, Yamagata W, Kamei K, Nozaki T Harada S (2006) Expression, purification and crystallization of L-methionine gamma-lyase 2 from Entamoeba histolytica. Acta Crystallogr F Struct Biol Cryst Commun 62, 1034 1036.
37. Nakayama T, Esaki N, Tanaka H Soda K (1988) Chemical modification of cyseine residues of L-methionine γ-lyase. Agric Biol Chem 52, 177 183.
38. Nakayama T, Esaki N, Tanaka H Soda K (1988) Specific labeling of the essential cysteine residue of L-methionine gamma-lyase with a cofactor analogue, N-(bromoacetyl)pyridoxamine phosphate. Biochemistry 27, 1587 1591.
39. Goyer A, Collakova E, Shachar-Hill Y Hanson AD (2007) Functional characterization of a methionine γ-Lyase in Arabidopsis and its implication in an alternative to the reverse trans-sulfuration pathway. Plant Cell Physiol 48, 232 242.
40. Mamaeva DV, Morozova EA, Nikulin AD, Revtovich SV, Nikonov SV, Garber MB Demidkina TV (2005) Structure of Citrobacter freundii L-methionine gamma-lyase. Acta Crystallogr F Struct Biol Cryst Commun 61, 546 549.
41. Alston TA Bright HJ (1983) Conversion of trifluoromethionine to a cross-linking agent by gamma-cystathionase. Biochem Pharmacol 32, 947 950.
42. Clark CG, Alsmark UCM, Hofer M, Saito-Nakano Y, Ali V, Marion S, Mukherjee C, Bruchhaus I, Tannich E, Leippe M et al. (2007) Structure and content of the Entamoeba histolytica genome. Adv Parasitol 65, 51 190.
43. Colombani F, Cherest H de Robichon-Szulmajster H (1975) Biochemical and regulatory effects of methionine analogues in Saccharomyces cerevisiae. J Bacteriol 122, 375 384.
44. Duewel H, Daub E, Robinson V Honek JF (1997) Incorporation of trifluoromethionine into a phage lysozyme: implications and a new marker for use in protein 19F NMR. Biochemistry 36, 3404 3416.
45. Soda K (1968) Microdetermination of D-amino acids and D-amino acid oxidase activity with 3-methyl-2-benzothiazolone hydrazone hydrochloride. Anal Biochem 25, 228 235.