Anaerobic bacterial metabolism in the ancient eukaryote Giardia duodenalis

International Journal for Parasitology

Volumn 28, Issue 1, 1998, Pages 149-164

  Brown, D M ^a   Upcroft, J A ^a   Edwards, M R ^b   Upcroft, P ^a,c  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

Author keywords

Arginine dihydrolase; Disulphide reductase; Fermentative metabolism; Ferredoxin; Giardia duodenalis; NADH oxidase; Pyruvate:ferredoxin oxidoreductase; Reactive oxygen species; Superoxide dismutase; Thiol

Indexed keywords

AMINO ACID SEQUENCE; CONFERENCE PAPER; ELECTRON TRANSPORT; ENZYME ACTIVITY; FERMENTATION; GIARDIA LAMBLIA; NONHUMAN; OXIDATIVE STRESS; PARASITE DEVELOPMENT; SEQUENCE HOMOLOGY;

AMINO ACIDS; ANIMALS; BACTERIA, ANAEROBIC; ELECTRON TRANSPORT; ENERGY METABOLISM; EVOLUTION; FERMENTATION; GIARDIA; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; OXIDATIVE STRESS; OXYGEN CONSUMPTION;

EID: 0031893062     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0020-7519(97)00172-0     Document Type: Conference Paper

References (128)

1. [1] Adam RD. The biology of Giardia spp. Microbiol Rev 1991; 55: 706-732.
2. [2] Warren KS. In: McAdam PWJ, editor. New strategies in parasitology. Edinburgh: Churchill Livingstone, 1989;217-231.
3. [3] Boreham PFL, Shepherd RW. Giardiasis in child care centres. Med J Aust 1984; 141: 263.
4. [4] Farthing MJG. Giardiasis. Gastroenterol Clin N Am 1996; 25: 493-513.
5. [5] Phillips SC, Mildvan D, Williams DC, Gelb AM, White C. Transmission of enteric protozoa and helminths in a venereal-disease clinic population. N Engl J Med 1981; 305: 603-606.
6. [6] Boreham PFL. Giardiasis and its control. Pharmacol J 1991; 247: 271-274.
7. [7] Upcroft JA, Upcroft P. Drug resistance and Giardia. Parasitol Today 1993; 9: 187-190.
8. [8] Reiner DS, McCaffery M, Gillin FD. Sorting of cyst wall proteins to a regulated secretory pathway during differentiation of the primitive eukaryote, Giardia lamblia. Eur J Cell Biol 1990; 53: 142-153.
9. [9] Gillin FD, Reiner DS, McCaffery M. Organelles of protein transport in Giardia lamblia. Parasitol Today 1991; 7: 113-116.
10. [10] Gillin FD, Reiner DS, McCaffery M. Cell Biology of the primitive eukaryote Giardia lamblia. Annu Rev Microbiol 1996; 50: 679-705.
11. [11] Cavalier-Smith T. The origin of eukaryote and archaebacterial cells, Endocytobiology III. Annu NY Acad Sci 1987; 503: 17-54.
12. [12] Cavalier-Smith T. Kingdom Protozoa and its 18 phyla. Microbiol Rev 1993; 57: 953-994.
13. [13] Sogin ML, Gunderson JH, Elwood HJ, Alonso RA, Peattie DA. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 1989; 243: 75-77.
14. [14] Healey A, Mitchell R, Upcroft JA, Boreham PFL, Upcroft P. Complete nucleotide sequence of the ribosomal RNA tandem repeat unit from Giardia intestinalis. Nucleic Acids Res 1990; 18: 4006.
15. [15] Upcroft P, Chen N, Upcroft P. Telomeric organization of a variable and inducible toxin genefamily in the ancient eukaryote Giardia duodenalis. Genome Res 1997; 7: 37-46.
16. [16] Upcroft JA, Healey A, Mitchell R, Boreham PFL, Upcroft P. Antigen expression from the ribosomal repeat of Giardia intestinalis. Nucleic Acids Res 1990; 18: 7077-8081.
17. [17] Hatefi Y. The mitochondrial electron transport and oxidative phosphorylation system. Annu Rev Biochem 1985; 54: 1015-1069.
18. [18] Müller M. Energy metabolism of protozoa without mitochondria. Annu Rev Microbiol 1988; 42: 465-488.
19. [19] Lindmark DG. Energy metabolism of the anaerobic protozoon Giardia lamblia. Mol Biochem Parasitol 1980; 1: 1-12.
20. [20] Weinbach EC, Elwood-Claggett C, Keister DB, Diamond LS, Kon H. Respiratory metabolism of Giardia lamblia. J Parasitol 1980; 66(3): 47-350.
21. [21] Edwards MR, Gilroy FV, Jimenez BM, O'Sullivan WJ. Alanine is a major end product of metabolism by Giardia lamblia: a proton nuclear magnetic resonance study. Mol Biochem Parasitol 1989; 37: 19-26.
22. [22] Paget TA, Kelly ML, Jarroll EL, Lindmark DG, Lloyd D. The effects of oxygen on fermentation in the intestinal protozoal parasite Giardia lamblia. Mol Biochem Parasitol 1993; 57: 65-72.
23. [23] Jarroll EL, Müller PJ, Meyer EA, Morse SA. Lipid and carbohydrate metabolism of Giardia lamblia. Mol Biochem Parasitol 1981; 2: 187-196.
24. [24] Mertens E. ATP versus pyrophosphate: glycolysis revisited in parasitic protists. Parasitol Today 1993; 9: 122-126.
25. 13C NMR studies of Giardia intestinalis. In: Thompson RCA, Reynoldson JA, Lymbery AJ, editors. Giardia-from molecules to disease, Wallingford: CAB International 1994;185-186.
26. [26] Schofield PJ, Edwards MR, Kranze P. Glucose metabolism in Giardia intestinalis. Mol Biochem Parasitol 1991; 45: 39-48.
27. [27] Hrdy I, Mertens E, Nohýnková E. Giardia intestinalis: detection and characterization of a pyruvate phosphate dikinase. Exp Parasitol 1993; 76: 438-441.
28. [28] CaJacob CA, Gavino GR, Frey PA. Pyruvate dehydrogenase complex of Escherichia coli. Thiamine pyrophosphate and NADH-dependent hydrolysis of acetyl-CoA. J Biol Chem 1985; 260: 14610-14615.
29. [29] Rahmatullah M, Gopalakrishnan S, Andrews PC, Chang CL, Radke GA, Roche TE. Subunit associations in the mammalian pyruvate dehydrogenase complex. Structure and role of protein X and the pyruvate dehydrogenase component binding domain of the dihydrolipoyl transacetylase components. J Biol Chem 1989; 264: 2221-2227.
30. [30] Leach CK, Carr NG. Pyruvate:ferredoxin oxidoreductase and its activation by ATP in the blue-green alga Anabaena variabilis. Biochim Biophys Acta 1971; 245: 165-174.
31. [31] Buchanan BB. Enzymes, 3rd ed. New York: Academic Press, 1972.
32. [32] Gehring U, Arnon DI. Purification and properties of α-ketoglutarate synthase from a photosynthetic bacterium. J Biol Chem 1972; 247: 6963-6969.
33. [33] Blaschkowski HP, Neuer G, Ludwig-Festl M, Knappe J. Routes of flavodoxin and ferredoxin reduction in Escherichia coli CoA-acylating pyruvate:flavodoxin and NADPH:flavodoxin oxidoreductases participating in the activation of pyruvate formate-lyase. Eur J Biochem 1982; 123: 563-569.
34. [34] Neuer G, Bothe H. The pyruvate:ferredoxin oxidoreductase in heterocysts of the cyanobacterium Anabaena cylindrica. Biochim Biophys Acta 1982; 716: 358-365.
35. [35] Reeves RE, Warren LG, Susskind B, Lo H-S. An energy-conserving pyruvate-to-acetate pathway in Entamoeba histolytica. Pyruvate synthase and a new acetate thiokinase. J Biol Chem 1977; 252: 726-731.
36. [36] Townson SM, Hanson GR, Upcroft JA, Upcroft P. Characterisation and purification of pyruvate:ferredoxin oxidoreductase from Giardia duodenalis. Mol Biochem Parasitol 1996; 79: 183-193.
37. [37] Williams K, Lowe PN, Leadlay PF. Purification and characterization of pyruvate:ferredoxin oxidoreductase from the anaerobic protozoon Trichomonas vaginalis. Biochem J 1987; 246: 529-536.
38. [38] Hrdy I, Müller M. Primary structure and eubacterial relationships of the pyruvate:ferredoxin oxidoreductase from the amitochondriate T. vaginalis. J Mol Evol 1995; 41: 388-396.
39. [39] Kletzin A, Adams MWW. Molecular and phylogenetic characterisation of 2-ketoisovalerate ferredoxin oxidoreductases from Pyrococcus furiosus and pyruvate ferredoxin oxidoreductase from Thermotoga maritima. J Bacteriol 1996; 178: 248-257.
40. [40] Mai X, Adams MWW. Characterisation of a fourth type of 2-keto acid-oxidising enzyme from a hyperthermophilic archaeon:2-ketoglutarate ferredoxin oxidoreductase from Thermococcus litoralis. J Bacteriol 1996; 178: 5890-5896.
41. [41] Blamey JM, Adams MWW. Characterization of an ancestral type of pyruvate ferredoxin oxidoreductase from the hyperthermophilic bacterium Thermotoga maritima. Biochemistry 1994; 33: 1000-1007.
42. [42] Lindmark DG, Miller JJ. Wallis PM, Hammond BR, editors. Enzyme activities of Giardia lamblia and Giardia muris trophozoites and cysts. Advances in Giardia research. Calgary: University of Calgary Press, 1988; 187-189.
43. [43] Ellis JE, Cole D, Lloyd D. Influence of oxygen on the fermentative metabolism of metronidazole-sensitive and resistant strains of Trichomonas vaginalis. Mol Biochem Parasitol 1992; 56: 79-88.
44. [44] Mewes HW, Albermann K, Bähr M, et al. Overview of the yeast genome. Nature 1997; 387(Suppl): 5-65.
45. [45] Kerscher L, Osterhelt D. Purification and properties of two 2-oxoacid:ferredoxin oxidoreductases from Halobacterium halobium. Eur J Biochem 1981; 116: 587-594.
46. [46] Sánchez LB, Müller M. Purification and characterization of the acetate forming enzyme, acetyl-CoA synthetase (ADP-forming) from the amitochondriate protist, Giardia lamblia. FEBS Lett 1996; 378: 240-244.
47. [47] Rosenthal B, Mai Z, Caplivski D, et al. Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoan parasite Entamoeba histolytica. J Bacteriol 1997; 179: 3736-3745.
48. [48] Edwards MR, Schofield PJ, O'Sullivan WJ, Costello M. Arginine metabolism during culture of Giardia intestinalis. Mol Biochem Parasitol 1992; 53: 97-104.
49. 2. Parasitology 1990; 42: 63-68.
50. [50] Schofield PJ, Kranz P, Edwards MR. Does Giardia intestinalis need glucose as an energy source? Int J Parasitol 1990; 20: 701-703.
51. [51] Knodler LA, Edwards MR, Schofield PJ. The intracellular amino acid pools of Giardia intestinalis, Trichomonas vaginalis and Crithidia luciliae. Exp Parasitol 1994; 79: 117-125.
52. [52] Park JH, Schofield PJ, Edwards MR. The role of alanine in the acute response of Giardia intestinalis to hypo-osmotic shock. Microbiology 1995; 141: 2455-2462.
53. [53] Park JH, Schofield PJ, Edwards MR. Giardia intestinalis: volume recovery in response to cell swelling. Exp Parasitol 1997; 86: 19-28.
54. [54] Crow VL, Thomas TD. Arginine metabolism in lactic streptococci. J Bacteriol 1982; 150: 1024-1032.
55. [55] Liu SQ, Pritchard GG, Hardman MJ, Pilone GJ. Occurrence of arginine deiminase pathway enzymes in arginine catabolism by wine lactic acid bacteria. App Environ Microbiol 1995; 61: 310-316.
56. [56] Sjostrom KE, Chen KCS, Kenny GE. Detection of end products of the arginine dihydrolase pathway in both fermentative and nonfermentative Mycoplasma species by thin-layer chromatography. Int J Syst Bacteriol 1986; 36: 60-65.
57. [57] Stalon V, Mercenier A. L-Arginine utilization by Pseudomonas species. J Gen Microbiol 1984; 130: 69-76.
58. [58] Linstead D, Cranshaw MA. The pathway of arginine catabolism in the parasitic flagellate Trichomonas vaginalis. Mol Biochem Parasitol 1983; 8: 241-252.
59. [59] Yarlett N, Lindmark DG, Goldberg B, Ali Moharrami M, Bacchic CJ. Subcellular localization of the enzymes of the arginine dihydrolase pathway in Trichomonas vaginalis and Tritrichomonas foetus. J Eukaryot Microbiol 1994; 41: 554-559.
60. [60] Sussenbach JS, Strijkert PJ. Arginine metabolism in Chlamydomonas reinhardtii. FEBS Lett 1969; 3: 166-168.
61. [61] Schofield PJ, Costello M, Edwards MR, O'Sullivan WJ. The arginine dihydrolase pathway is present in Giardia intestinalis. Int J Parasitol 1990; 20: 697-699.
62. [62] Schofield PJ, Edwards MR, Matthews J, Wilson JR. The pathway of arginine catabolism in Giardia intestinalis. Mol Biochem Parasitol 1992; 51: 29-36.
63. [63] Knodler LA, Schofield PJ, Edwards MR. L-Arginine transport and metabolism in Giardia intestinalis support its position as a transition between the prokaryotic and eukaryotic kingdoms. Microbiology 1995; 141: 2063-2070.
64. [64] Driessen AJM, Poolman B, Kiewiet R, Konings WN. Arginine transport in Streptococcus lactis is catalysed by a cationic exchanger. Proc Natl Acad Sci USA 1987; 84: 6093-6097.
65. [65] Bourdineaud JP, Heierli D, Gamper M, et al. Characterization of the arcD arginine: ornithine exchanger of Pseudomonas aeruginosa. J Biol Chem 1993; 268: 5417-5424.
66. [66] Christensen HN. Organic ion transport during seven decades. The amino acids. Biochim Biophys Acta 1984; 779: 225-269.
67. [67] Anraku Y. Bacterial electron transport chains. Annu Rev Biochem 1988; 57: 101-132.
68. [68] Vignais PM, Colbeau A, Willison JC, Jouanneau Y. Hydrogenase, nitrogenase, and hydrogen metabolism in the photosynthetic bacteria. Adv Microb Physiol 1985; 26: 155-234.
69. [69] Mason JR, Cammack R. The electron-transport proteins of hydroxylating bacterial dioxygenases. Annu Rev Microbiol 1992; 46: 277-305.
70. [70] Townson SM, Hanson GR, Upcroft JA, Upcroft P. A purified ferredoxin from Giardia duodenalis. Eur J Biochem 1994; 220: 439-446.
71. [71] Müller M. Biochemical cytology of trichomonad flagellates I. Subcetlular localisation of hydroxylases, dehydrogenases and catalase in Tritrichomonas foetus. J Cell Biol 1973; 57: 453-474.
72. [72] Ellis JE, Williams R, Cole D, Cammack R, Lloyd D. Electron transport components of the parasitic protozoan Giardia lamblia. FEBS Lett 1993; 325: 196-200.
73. [73] Brown DM, Upcroft JA, Upcroft P. Free radical detoxification in Giardia duodenalis. Mol Biochem Parasitol 1995; 72: 47-56.
74. 2O-producing NADH oxidase from the protozoan parasite Giardia duodenalis. Eur J Biochem 1996; 241: 155-161.
75. [75] Saeki K, Suetsugu Y, Tokuda K, et al. Genetic analysis of functional differences among distinct ferredoxins in Rhodobacter capsulatus. J Biol Chem 1991; 266: 12889-12895.
76. [76] Klipp W, Reiländer H, Schlüter A, Krey R, Pühler A. The Rhizobium meliloti fdxN gene encoding a ferredoxin-like protein is necessary for nitrogen fixation and is cotranscribed with nifA and nifB. Mol Gen Genet 1989; 216: 293-302.
77. [77] Ogata M, Kondo S, Okawara N, Yagi T. Purification and characterization of ferredoxin from Desulfovibrio vulgaris Miyazaki. J Biochem 1988; 103: 121-125.
78. [78] Bult CJ, White O, Olsen GJ, et al. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 1996; 273: 1058-1073.
79. [79] Huber M, Garfinkel L, Gitler C, Mirelman D, Revel M, Rozenblatt S. Nucleotide sequence of an Entamoeba histolytica ferredoxin gene. Mol Biochem Parasitol 1988; 31: 27-34.
80. [80] Quinkal I, Kyritsis P, Kohzuma T, Im SC, Sykes AG, Moulis JM. The influence of conserved aromatic residues on the electron transfer reactivity of 2[4Fe-4S] ferredoxins. Biochim Biophys Acta 1996; 1295: 210-218.
81. [81] Gorrell TE, Yarlett N, Müller M. Isolation and characterisation of Trichomonas vaginalis ferredoxin. Carlsberg Res Commun 1984; 49: 259-268.
82. [82] Marczak R, Gorrell TE, Müller M. Hydrogenosomal ferredoxin of the anaerobic protozoan, Tritrichomonas foetus. J Biol Chem 1983; 258: 12427-12433.
83. [83] Steinbüchel A, Müller M. Anaerobic pyruvate metabolism of Tritrichomonas foetus and Trichomonas vaginalis hydrogenosomes. Mol Biochem Parasitol 1986; 20: 57-65.
84. [84] Odom JM, Peck HD Jr. Hydrogenase, electron transfer proteins, and energy coupling in the sulfate-reducing bacteria Desulfovibrio, Annu Rev Microbiol 1984; 38: 551-592.
85. [85] Yarlett N, Lloyd D, Williams G. Respiration of the rumen ciliate Dasytricha ruminantium Schuberg. Biochem J 1982; 206: 259-266.
86. [86] Lloyd D, Williams J, Yarlett N, Williams AG. Oxygen affinities of the hydrogenosome-containing protozoa Tritrichomonas foetus and Dasytricha ruminantium, and two aerobic protozoa, determined by bacterial bioluminescence. J Gen Microbiol 1982; 128: 1019-1022.
87. [87] Müller M, Gorrell TE. Metabolism and metronidazole uptake in Trichomonas vaginalis isolates with different metronidazole susceptibilities. Antimicrob Agents Chemother 1983; 24: 667-673.
88. [88] Lloyd D, Ohnishi T, Lindmark DG, Müller M. Respiration of Tritrichomonas foetus. Wiad Parazytol 1983; 29: 37-39.
89. 2O-forming NADH oxidase from Streptococcus faecalis. Eur J Biochem 1986; 156: 149-155.
90. [90] Ahmed SA, Claiborne A. The streptococcal flavoprotein NADH oxidase. I. Evidence linking NADH oxidase and NADH peroxidase cysteinyl redox centers. J Biol Chem 1989; 264: 19856-19863.
91. [91] Ohnishi K, Niimura Y, Yokoyama K, et al. Purification and analysis of a flavoprotein functional as NADH oxidase from Amphibacillus xylanus overexpressed in Escherichia coli. J Biol Chem 1994; 269: 31418-31423.
92. [92] Shah VK, Stacey G, Brill WJ. Electron transport to nitrogenase. Purification and characterization of pyruvate-flavodoxin oxidoreductase, the nifJ gene product. J Biol Chem 1983; 258: 12064-12068.
93. [93] Lo H-S, Reeves RE. Purification and properties of NADPH: flavin oxidoreductase from Entamoeba histolytica. Mol Biochem Parasitol 1980; 2: 23-30.
94. [94] Linstead DJ, Bradley S. The purification and properties of two soluble reduced nicotinamide: acceptor oxidoreductases from Trichomonas vaginali. Mol Biochem Parasitol 1988; 27: 125-134.
95. [95] Cerkasovová A, Cerkasov J. Location of NADH oxidase activity in fractions of Tritrichomonas foetus homogenate. Folia Parasitol (Prague) 1974; 21: 193-203.
96. [96] Prins RA, Prast ER. Oxidation of NADH in a coupled oxidase-peroxidase reaction and its significance for the fermentation in the rumen protozoa of the genus Isotricha. J Protozool 1973; 20: 471-477.
97. [97] Cadenas E. Biochemistry of oxygen toxicity. Annu Rev Biochem 1989; 58: 79-110.
98. [98] Malmström BG. Enzymology of oxygen. Annu Rev Biochem 1982; 51: 21-59.
99. [99] Biaglow JE, Varnes ME, Roizen-Towle L, et al. Biochemistry of reduction of nitro heterocycles. Biochem Pharmacol 1986; 35: 77-90.
100. [100] Gralla EB, Kosman D. Molecular genetics of superoxide dismutases in yeast and related fungi. Adv Genet 1992; 30: 252-319.
101. [101] Tannich E, Bruchhaus I, Walter RD, Horstman RD. Pathogenic and nonpathogenic Entamoeba histolytica: identification and molecular cloning of an iron-containing superoxide dismutase. Mol Biochem Parasitol 1991; 49: 61-72.
102. [102] Ellis JE, Yarlett N, Cole D, Humphreys MJ, Lloyd D. Antioxidant defences in the microaerophilic protozoan Trichomonas vaginalis: comparison of metronidazole-resistant and sensitive strains. Microbiology 1994; 140: 2489-2494.
103. [103] James ER. Superoxide dismutase. Parasitol Today 1994; 10: 481-484.
104. [104] Mehlotra RK. Antioxidant defence mechanisms in parasitic protozoa. Crit Rev Microbiol 1996; 22: 295-314.
105. [105] Müller M. The hydrogenosome. J Gen Microbiol 1993; 139: 2879-2889.
106. [106] Mendis AHW, Schofield P.J. Discussants report: Giardia biochemistry. In: Thompson RCA, Reynoldson JA, Lymbery AJ, editors. Giardia: from molecules to disease. Wallingford: CAB International, 1994; 205-213.
107. [107] Thompson RCA, Reynoldson JA. Mendis AHW Giardia and giardiasis. Adv Parasitol 1993; 32: 71-160.
108. [108] Privalle CT, Fridovich I. Inductions of superoxide dismutases in Escherichia coli under anaerobic conditions. J Biol Chem 1988; 263: 4274-4279.
109. [109] Privalle CT, Kong SE, Fridovich I. Induction of manganese-containing superoxide dismutase in anaerobic Escherichia coli by diamide and 1,10-phenanthroline: sites of transcriptional regulation. Proc Natl Acad Sci USA 1993; 90: 2310-2314.
110. [110] Bruchhaus I, Tannich E. Induction of the iron-containing superoxide dismutase in Entamoeba histolytica by a superoxide anion-generating system or by iron chelation. Mol Biochem Parasitol 1994; 67: 281-288.
111. [111] Brown DM, Upcroft JA, Upcroft P. Cysteine is the major low molecular weight thiol in Giardia duodenalis. Mol Biochem Parasitol 1993; 61: 155-158.
112. [112] Fahey RC, Newton GL, Arrick B, Overdank-Bogart T, Aley SB. Entamoeba histolytica: a eukaryote without glutathione metabolism. Science 1984; 224: 69-72.
113. [113] Fairlamb AH. Novel biochemical pathways in parasitic protozoa. Parasitology 1989; 99S: 93-112.
114. [114] Fairlamb AH, Cerami A. Metabolism and functions of trypanothione in the kinetoplastida. Annu Rev Microbiol 1992; 46: 659-729.
115. [115] Turner E, Hager LJ, Shapiro BM. Ovothiol replaces glutathione peroxidase as a hydrogen peroxide scavenger in sea urchin eggs. Science 1988; 242: 939-941.
116. [116] Fahey RC, Sundquist AR. Evolution of glutathione metabolism. Adv Enzymol Relat Areas Mol Biol 1991; 64: 1-53.
117. [117] Williams CH, Jr. Flavin-containing dehydrogenases. In: Boyer PD, editor. The enzymes. New York: Academic Press 1976; 13: 89-173.
118. [118] Russel M, Model P. Sequence of thioredoxin reductase from Escherichia coli. Relationship to other flavoprotein disulfide oxidoreductases. J Biol Chem 1988; 263: 9015-9019.
119. [119] Williams CH, Jr. Lipoamide dehydrogenase, glutathione reductase, thioredoxin reductase and mercuric ion reductase. A family of flavoenzyme transhydrogenases In: Müller F, editor. Chemistry and biochemistry of flavoenzymes, vol. III. Boca Raton, FL: CRC Press, 1992; 121-211.
120. [120] Kuriyan J, Krishna TSR, Wong L, et al. Convergent evolution of similar function in two structurally divergent enzymes. Nature 1991; 352: 172-174.
121. [121] Holmgren A. Thioredoxin. Annu Rev Biochem 1985; 54: 237-271.
122. [122] Schallreuter KU, Wood JM. The role of thioredoxin reductase in the reduction of free radicals at the surface of the epidermis. Biochem Biophys Res Commun 1986; 136: 630-637.
123. [123] Smith NC, Bryant C, Boreham PFL. Possible role for pyruvate:ferredoxin oxidoreductase and thiol-dependent peroxidase and reductase activities in resistance to nitroheterocyclic drugs in Giardia intestinalis. Int J Parasitol 1988; 18: 991-997.
124. [124] Brown DM, Upcroft JA, Upcroft P. Thiol redox management by disulphide reductase in the protozoan parasite Giardia duodenalis. Mol Biochem Parasitol 1996; 83: 211-220.
125. [125] Aharonowitz Y, Av-Gay Y, Schreiber R, Cohen G. Characterisation of a broad-range disulfide reductase from Streptomyces clavulgerus and its possible role in β-lactam antibiotic biosynthesis. J Bacteriol 1993; 175: 623-629.
126. [126] Cohen G, Argamen A, Schreiber R, Mislovati M, Aharonowitz Y. The thioredoxin system of Penicillium chrysogenum and its possible role in penicillin biosynthesis. J Bacteriol 1994; 176: 973-984.
127. [127] Bruchhaus I, Tannich E. Identification of an Entamoeba histolytica gene encoding a protein homologous to prokaryotic disulphide oxidoreductases. Mol Biochem Parasitol 1995; 70: 187-191.
128. [128] Gupta RS, Golding GB. The origin of the eukaryotic cell. Trends Biochem Sci 1996; 21: 166-171.