Iron-ascorbate cleavable malic enzyme from hydrogenosomes of Trichomonas vaginalis: Purification and characterization

Molecular and Biochemical Parasitology

Volumn 83, Issue 2, 1996, Pages 221-234

  Drmota, Tomáš ^a,d   Proost, Paul ^b   Van Ranst, Marc ^b   Weyda, František ^c   Kulda, Jaroslav ^a   Tachezy, Jan ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^c INSTITUTE OF ENTOMOLOGY   (Czech Republic)

^d INSTITUTE OF PHYSIOLOGY   (Czech Republic)

Author keywords

hydrogenosome; iron ascorbate cleavable metal binding site; malic enzyme; Trichomonas vaginalis

Indexed keywords

ASCORBIC ACID; IRON; MALATE DEHYDROGENASE (DECARBOXYLATING);

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME PURIFICATION; IMMUNOCYTOCHEMISTRY; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN PROCESSING; TRICHOMONAS VAGINALIS;

AMINO ACID SEQUENCE; ANIMALS; ASCORBIC ACID; CELL FRACTIONATION; CHLORIDES; FERROUS COMPOUNDS; HYDROGEN-ION CONCENTRATION; INTRACELLULAR MEMBRANES; ISOENZYMES; KINETICS; MALATE DEHYDROGENASE; MANGANESE COMPOUNDS; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; NAD; ORGANELLES; SEQUENCE ANALYSIS; TRICHOMONAS VAGINALIS;

ORYCTOLAGUS CUNICULUS; TRICHOMONAS VAGINALIS;

EID: 0030596212     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-6851(96)02777-6     Document Type: Article

References (49)

1. [1] Müller, M. (1993) The hydrogenosome. J. Gen. Microbiol. 139, 2879-2889.
2. [2] Steinbüchel, A. and Müller, M. (1986) Glyoerol, a metabolic end product of Trichomonas vaginalis and Tritrichomonas foetus. Mol. Biochem. Parasitol. 20, 45-55.
3. [3] Chapman, A., Linstead, D.J., Lloyd, D. and Williams, J. (1985) 13C-NMR reveals glycerol as an unexpected major metabolite of the protozoan parasite Trichomonas vaginalis. FEBS Lett. 191, 287-292.
4. [4] Čerkasovová, A., Novák, J., Čerkasov, J., Kulda, J. and Tachezy, J. (1986) Metabolic properties of Trichomonas vaginalis resistant to metronidazole under anaerobic conditions. Acta Univ. Carol., Biol. 30, 505-512.
5. [5] Čerkasov, J., Čerkasovová, A., Kulda, J. and Vilhelmová, D. (1978) Respiration of hydrogenosomes of Tritrichomonas foetus. J. Biol. Chem. 253, 1207-1214.
6. [6] Frenkel, R. (1975) Regulation and physiological functions of malic enzyme. Curr. Top. Cell. Regul. 9, 157-181.
7. [7] Chang, G.G., Huang, T.M., Lee, H.J., Chou, W.Y. and Chang, T.C. (1994) Pigeon liver malic enzyme: quarternary structure and reversible dissociation of the subunits. Biotechnol. Appl. Biochem. 19, 17-29.
8. +-malic enzyme from Lupinus luteus leaves. Physiol. Plant. 59, 641-646.
9. [9] Cannata, J.J.B. and Cazzulo, J.J. (1984) The aerobic fermentation of glucose by Trypanosoma cruzi. Comp. Biochem. Physiol. 79B, 297-308.
10. +-dependent enzyme. Biochim. Biophys. Acta 916, 446-454.
11. [11] Biegniewska, A. and Skorkowski, E.F. (1987) Mitochondrial NADP-dependent malic enzyme of cod heart. Rate of forward and reverse reaction. Comp. Biochem. Physiol. 86B, 731-735.
12. 4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim. Biophys. Acta 895, 81-106.
13. + -dependent malic enzyme. J. Biol. Chem. 259, 6215-6221.
14. [14] Teller, J.K., Fahien, L.A. and Davis, J.W. (1992) Kinetics and regulation of hepatoma mitochondrial NAD(P) malic enzyme. J. Biol. Chem. 267, 10423-10432.
15. 4 photosynthetic NAD-dependent malic enzyme of amaranth mitochondria. J. Biol. Chem. 269, 2827-2833.
16. [16] Hrdý, I. and Mertens, E. (1993) Purification and partial characterization of malate dehydrogenase (decarboxylating) from Tritrichomonas foetus hydrogenosomes. Parasitology 107, 379-385.
17. [17] Marvin Sikkema, F.D., Pedro Gomes, T.M., Grivet, J.P., Gottschal, J.C. and Prins, R.A. (1993) Characterization of hydrogenosomes and their role in glucose metabolism of Neocallimastix sp. L2. Arch. Microbiol. 160, 388-396.
18. [18] Kobayashi, K., Doi, S., Negoro, S., Urabe, I. and Okada, H. (1989) Structure and properties of malic enzyme from Bacillus stearothermophilus. J. Biol. Chem. 264, 3200-3205.
19. [19] Rutter, W.J. and Lardy, H.A. (1958) Purification and properties of pigeon liver malic enzyme. J. Biol. Chem. 233, 374-382.
20. [20] Wei, C.H., Chou, W.Y., Huang, S.M., Lin, C.C. and Chang, G.G. (1994) Affinity cleavage at the putative metal-binding site of pigeon liver malic enzyme by the Fe(2+)-ascorbate system. Biochemistry 33, 7931-7936.
21. 258 as the metal coordinate of pigeon liver malic enzyme by site-specific mutagenesis. Biochemistry 34, 7949-7954.
22. [22] Steinbüchel, A. and Müller, M. (1986) Anaerobic pyruvate metabolism of Tritrichomonas foetus and Trichomonas vaginalis hydrogenosomes. Mol. Biochem. Parasitol. 20, 57-65.
23. [23] Coombs, H.G., Hackstein, J.H.P., Konig, H., et al. (1995) Anaerobic protists and anaerobic ecosystems. In: Protistological Actualities (Brugerolle, G. and Mignot, J.-P., eds.), pp. 90-101. Laboratoire de Biologie des Protistes, U.R.A.-C.N.R.S. 1944, Aubiere.
24. [24] Marvin Sikkema, F.D., Driessen, A.J.M., Gottschal, J.C. and Prins, R.A. (1994) Metabolic energy generation in hydrogenosomes of the anaerobic fungus Neocallimastix: evidence for a functional relationship with mitochondria. Mycol. Res. 98, 205-212.
25. [25] Brugerolle, G. and Metenier, G. (1973) Intracellular localization and characterization of 2 types of malate dehydrogenases in Trichomonas vaginalis Donne, 1836. J. Protozool. 20, 320-327.
26. +-linked malic enzymes. Jap. J. Parasit. 29, 19-26.
27. [27] Hrdý, I. and Müller, M. (1995) Primary structure of the hydrogenosomal malic enzyme of Trichomonas vaginalis and its relationship to homologous enzymes. J. Euk. Microbiol. 42, 593-603.
28. [28] Alderete, J.F., O'Brien, J.L., Arroyo, R., Engbring, J.A., Musatovova, O., Lopez, O., Lauriano, C. and Nguyen, J. (1995) Cloning and molecular characterization of two genes encoding adhesion proteins involved in Trichomonas vaginalis cytoadherence. Mol. Microbiol. 17, 69-83.
29. [29] Rappelli, P., Rocchigiani, A.M., Erre, G., Colombo, M.M., Cappuccinelli, P. and Fiori, P.L. (1995) Sequence of cDNA coding for a 65 kDa adhesive protein for the specific detection of Trichomonas vaginalis by PCR. FEMS Microbiol. Lett. 129, 21-26.
30. [30] Kulda, J., Vojtěchovská, M., Tachezy, J., Demeš, P. and Kunzová, E. (1982) Metronidazole resistance of Trichomonas vaginalis as a cause of treatment failure in trichomoniasis: A case report. Br. J. Vener. Dis. 58, 394-399.
31. [31] Diamond, L.S. (1957) The establishment of various trichomonads of animals and man in axenic cultures. J. Parasitol. 43, 488-490.
32. [32] Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951) Protein measurement with the folin phenol reagent. J. Biol. Chem. 193, 265-275.
33. [33] Lahti, C.J., d'Oliveira, C.E. and Johnson, P.J. (1992) Beta-succinyl-coenzyme A synthetase from Trichomonas vaginalis is a soluble hydrogenosomal protein with an amino-terminal sequence that resembles mitochondrial presequences. J. Bacteriol. 174, 6822-6830.
34. [34] Merril, C.R. (1990) Gel staining techniques. In: Guide to Protein Purification (Deutscher, M.P., ed.), pp. 477-488. Academic Press, San Diego.
35. [35] Johnson, P.J., Lahti, C.J. and Bradley, P.J. (1993) Biogenesis of the hydrogenosome in the anaerobic protist Trichomonas vaginalis. J. Parasitol. 79, 664-670.
36. [36] Scrutton, N.S., Berry, A. and Perham, R.N. (1990) Redesign of the coenzyme specificity of a dehydrogenase by protein engineering. Nature 343, 38-43.
37. [37] Willeford, K.O. and Wedding, R.T. (1987) pH effects on the activity and regulation of the NAD malic enzyme. Plant. Physiol. 84, 1084-1087.
38. [38] Farber, J.M. and Levine, R.L. (1986) Sequence of a peptide susceptible to mixed-function oxidation. Probable cation binding site in glutamine syntetase. J. Biol. Chem. 261, 4574-4578.
39. [39] Stadtman, E.R. and Oliver, C.N. (1991) Metal-catalyzed oxidation of proteins. J. Biol. Chem. 266, 2005-2008.
40. [40] Stadtman, E.R. (1986) Oxidation of proteins by mixed-function oxidation system: implication in protein turover, ageing and neutrophil function. TIBS 11, 11-12.
41. [41] Stadtman, E.R. (1992) Protein oxidation and aging. Science 257, 1220-1224.
42. [42] Gorrel, T.E., Yarlett, N. and Müller, M. (1984) Isolation and characterization of Trichomonas vaginalis ferredoxin. Carlsberg. Res. Commun. 49, 259-268.
43. [43] Williams, K., Lowe, P.N. and Leadlay, P.F. (1987) Purification and characterization of pyruvate: ferredoxin oxidoreductase from the anaerobic protozoon Trichomonas vaginalis. Biochem. J. 246, 529-536.
44. [44] Chapman, A., Cammack, R., Linstead, D.J. and Lloyd, D. (1986) Respiration of Trichomonas vaginalis. Components detected by electron paramagnetic resonance spectroscopy. Eur. J. Biochem. 156, 193-198.
45. [45] Payne, M.J., Chapman, A. and Cammack, R. (1993) Evidence for an [Fe]-type hydrogenase in the parasitic protozoan Trichomonas vaginalis. FEBS Lett. 317, 101-104.
46. [46] Lindmark, D.G. and Müller, M. (1974) Superoxide dismutase in the anaerobic flagellates, Tritrichomonas foetus and Monocercomonas sp. J. Biol. Chem. 249, 4634-4637.
47. [47] Arroyo, R., Engbring, J. and Alderete, J.F. (1992) Molecular basis of host epithelial cell recognition by Trichomonas vaginalis. Mol. Microbiol. 6, 853-862.
48. [48] Lindmark, D.G., Müller, M. and Shio, H. (1975) Hydrogenosomes in Trichomonas vaginalis. J. Parasitol. 61, 552-524.
49. [49] Lehker, M.W., Arroyo, R. and Alderete, J.F. (1991) The regulation by iron of the synthesis of adhesins and cytoadherence levels in the protozoan Trichomonas vaginalis. J. Exp. Med. 174, 311-318.