Abstract
Sulfite oxidase (sulfite: ferricytochrome c oxidoreductase; EC 1.8.2.1) has been detected in Drosophila melanogaster and some of its properties have been studied. In most respects this enzyme resembles the mammalian sulfite oxidases except for its molecular weight (148,000), which is somewhat higher than that of rat sulfite oxidase (116,000). Cytochrome c, potassium-ferricyanide, and oxygen can serve as electron acceptors in the oxidation of sulfite by the enzyme. Although definite evidence can be obtained only through the analysis of the pure enzyme, experiments involving tungstate feeding suggest that Drosophila sulfite oxidase is most probably a molybdoenzyme. Extracts of mal flies show normal levels of sulfite oxidase, whereas lxd flies have only 5–10% of the activity of wild type, and in cin flies the enzyme is apparently absent. While it is possible that the lxd and cin mutations are at some level responsible for the defective synthesis of a molybdenum-containing cofactor (supposed to be present in most molybdoenzymes), the evidence accumulated so far by several authors and the results of the present investigation argue against the involvement of a Mo cofactor in the multiple enzyme deficiencies observed in mal flies.
Similar content being viewed by others
References
Andres, R. Y. (1976). Aldehyde oxidase and xanthine dehydrogenase from wild type Droxophila melanogaster and immunologically cross-reacting material from ma-1 mutants. Eur. J. Biochem. 62591.
Bailey, J. L. (1967). Techniques in Protein Chemistry. Elsevier, Amsterdam, p. 341.
Baker, B. S. (1973). The maternal and zygotic control of development by cinnamon. A new mutant in Drosophila melanogaster. Dev. Biol. 33429.
Bewley, G. C., and Lucchesi, J. C. (1975). Lethal effects of low and “null” activity allels of 6-phosphogluconate dehydrogenase in Drosophila melanogaster. Genetics 79451.
Cohen, H. J., and Fridovich, I. (1971). Hepatic sulfite oxidase. Purification and properties. J. Biol. Chem. 246359.
Cohen, H. J., and Fridovich, I. (1971a). Hepatic sulfite oxidase. The nature and function of the heme prosthetic groups. J. Biol. Chem. 246367.
Cohen, H. J., Fridovich, I., and Rajagopalan, K. V. (1971). Hepatic sulfite oxidase. A functional role for molybdenum. J. Biol. Chem. 246374.
Cohen, H. J., Betcher-Lange, S., Kessler, D. L., and Rajagopalan, K. V. (1972). Hepatic sulfite oxidase. Congruency in mitochondria of prosthetic groups and activity. J. Biol. Chem. 2477759.
Collins, J. F., and Glassman, E. (1969). A third locus (lpo) affecting pyridoxal oxidase in Drosophila melanogaster. Genetics 61833.
Courtright, J. B. (1967). Polygenic control of aldehyde oxidase in Drosophila. Genetics 5725.
Courtright, J. B. (1975). Evidence for a new type of complementation among the cin, lxd and ma-1 loci in Drosophila melanogaster. Mol. Gen. Genet. 142231.
David, J., Bocquet, Ch., Herrewege, J. van, Fouillet, P., and Arens, M. F. (1978). Alcohol metabolism in Drosophila melanogaster: Uselessness of the most active aldehyde oxidase produced by the aldox locus. Biochem. Genet. 16203.
Dickinson, W. J. (1970). The genetics of aldehyde oxidase in Drosophila melanogaster. Genetics 66487.
Dubourdieu, M., Andrade, E., and Puig, J. (1976). Molybdenum and chlorate resistant mutants in Escherichia coli K 12. Biochem. Biophys. Res. Commun. 70766.
Duke, E. J., Rushing, D. R., and Glassman, E. (1975). Nutritional control of xanthine dehydrogenase. II. Effects on xanthine dehydrogenase and aldehyde oxidase of culturing wild-type and mutant Drosophila on different levels of molybdenum. Biochem. Genet. 1353.
Duran, M., Beemer, F. A., Heiden, C. v. d., Korteland, J. de Bree, P. K., Brink, M., Wadman, S. K., and Lombeck, J. (1978). Combined deficiency of xanthine oxidase and sulphite oxidase: A defect of molybdenum metabolism or transport? J. Inher. Metab. Dis. 1175.
Duran, M., Beemer, F. A., Wadman, S. K., Johnson, J. L., Waud, W. R., and Rajagopalan, K. V. (1980). Pediat. Res. 14177 (abstr. 77).
Edwards, T. C. R., Candido, E. P. M., and Chovnik, A. (1977). Xanthine dehydrogenase from Drosophila melanogaster. Mol. Gen. Genet. 1541.
Finnerty, V. (1976). Genetic units of Drosophila—simple cistrons. In Ashburner, M., and Novitski, E. (eds.), The Genetics and Biology of Drosophila Academic Press, New York, Vol. 1b, Chap. 18.
Forrest, H. S., Glassman, E., and Mitchell, H. K. (1956). Conversion of 2-amino-4-hydroxypteridine to isoxanthopterin in D. melanogaster. Science 124725.
Glassman, E. (1962). Convenient assay of xanthine dehydrogenase in single Drosophila melanogaster. Science 137990.
Glassman, E., and Mitchell, H. K. (1959). Maternal effect of mal+ on xanthine dehydrogenase of Drosophila melanogaster. Genetics 44547.
Glassman, E., Shinoda, T., Duke, E. J., and Collins, J. F. (1968). Multiple molecular forms of xanthine dehydrogenase and related enzymes. Ann. N.Y. Acad. Sci. 151263.
Goa, J. (1953). A micro biuret method for protein determination. Scand. J. Clin. Lab. Invest. 5218.
Guilbault, G. G., Kramer, D. N., and Hackley, E. (1967). A new substrate for fluorometric determination of oxidative enzymes. Anal. Chem. 39271.
Guilbault, G. G., Brignac, P., Jr., and Zimmer, M. (1968). Homovanillic acid as a fluorometric substrate for oxidative enzymes. Anal. Chem. 40190.
Higgins, E. S., Richert, D. A., and Westerfeld, W. W. (1956). Molybdenum deficiency and tungstate inhibition studies. J. Nutr. 59539.
Irreverre, F., Mudd, S. H., Heizer, W. D., and Laster, L. (1967). Sulfite oxidase deficiency: Studies of a patient with mental retardation, dislocated ocular lenses and abnormal urinary excretion of S-sulfo-L-cysteine, sulfite and thiosulfate. Biochem. Med. 1187.
Johnson, J. L., Cohen, H. J., and Rajagopalan, K. V. (1974a). Molecular basis of the biological function of molybdenum. Molybdenum free sulfite oxidase from livers of tungsten treated rats. J. Biol. Chem. 2495046.
Johnson, J. L., Rajagopalan, K. V., and Cohen, H. J. (1974b). Molecular basis of the biological function of molybdenum. Effect of tungsten on xanthine oxidase and sulphite oxidase in the rat. J. Biol. Chem. 249859.
Johnson, J. L., Waud, W. R., Cohen, H. J., and Rajagopalan, K. V. (1974c). Molecular basis of the biological function of molybdenum. Molybdenum-free xanthine oxidase from livers of tungsten treated rats. J. Biol. Chem. 2495056.
Keller, E. C., and Glassman, E. (1964). A third locus (lxd) affecting xanthine dehydrogenase in Drosophila melanogaster. Genetics 49663.
Kessler, D. L., and Rajagopalan, K. V. (1972). Purification and properties of sulfite oxidase from chicken liver. Presence of molybdenum in sulfite oxidase from diverse sources. J. Biol. Chem. 2476566.
Ketchum, P. A., Cambier, H. Y., Frazier, W. A., III, Madansky, C. H., and Nason, A. (1970). In vitro assembly of Neurospora assimilatory nitrate reductase from protein subunits of a Neurospora mutant and the xanthine oxidizing or aldehyde oxidase systems of higher animals. Proc. Natl. Acad. Sci. USA 661016.
Kraus, A. P., and Neeley, C. L., Jr. (1964). Human erythrocyte lactate dehydrogenase: Four genetically determined variants (Note 7). Science 145595.
Lee, K. Y., Pan, S. S., Erickson, R., and Nason, A. (1974). Involvement of molybdenum and iron in the in vitro assembly of assimilatory nitrate reductase utilizing Neurospora mutant nit-1. J. Biol. Chem. 2493941.
Lyric, R. M., and Suzuki, I. (1970a). Enzymes involved in the metabolism of thiosulfate by Thiobacillus thioparus. I. Survey of enzymes and properties of sulfite: cytochrome c oxidoreductase. Can. J. Biochem. 48334.
Lyric, R. M., and Suzuki, I. (1970b). Enzymes involved in the metabolism of thiosulfate by Thiobacillus thioparus. II. Properties of adenosine-5′-phosphosulfate reductase. Can J. Biochem. 48344.
MacCarron, M., Gelbart, W., and Chovnick, A. (1974). Intracistronic mapping of electrophoretic sites in Drosophila melanogaster: Fidelity of information transfer by gene conversion. Genetics 76289.
MacIntyre, R. J., and O'Brien, S. J. (1976). Interacting gene-enzyme systems in Drosophila. Annu. Rev. Genet. 10281.
MacLeod, R. M., Farkas, W., Fridovich, I., and Handler, P. (1961). Purification and properties of hepatic sulfite oxidase. J. Biol. Chem. 2361841.
Möllering, H., Wahlefeld, A. W., and Michal, G. (1974). Visualization of NAD(P) dependent reactions. In Bergmeyer, H. U. (ed.), Methods in Enzymatic Analysis. Vol 1 Verlag Chemie Weinheim (Academic Press, New York, London), p. 139.
Mudd, S. H., Irreverre, F., and Laster, L. (1967). Sulfite oxidase deficiency in man: Demonstration of the enzymatic defect. Science 1561599.
Nason, A., Lee, K. Y., Pan, S. S., Ketchum, P. A., Lamberti, A., and de Vries, J. (1971). In vitro formation of assimilatory reduced nicotinamide adenine dinucleotide phosphate: Nitrate reductase from a Neurospora mutant and a component of molybdo-enzymes. Proc. Natl. Acad. Sci. USA 683242.
Owen, E. C., and Proudfoot, R. (1968). The effect of tungstate ingestion on xanthine oxidase in milk and liver. Br. J. Nutr. 22331.
Pateman, J. A., Cove, D. J., Rever, B. M., and Roberts, D. B. (1964). A common co-factor for nitrate reductase and xanthine dehydrogenase which also regulates the synthesis of nitrate reductase. Nature 20158.
Sofer, W., and Ursprung, H. (1968). Drosophila alcohol dehydrogenase. Purification and partial characterization. J. Biol. Chem. 2433110.
Thatcher, D. R. (1977). Enzyme instability and proteolysis during the purification of an alcohol dehydrogenase from Drosophila melanogaster. Biochem. J. 163317.
van Bezooyen, C. F. A., Noord, M. J. van, and Knook D. L. (1974). The viability of parenchymal liver cells isolated from young and old rats. Mech. Age. Dev. 3107.
Wattiaux-de Coninck, S., and Wattiaux, R. (1971). Subcellular distribution of sulfite cytochrome c reductase in rat liver tissue. Eur. J. Biochem. 19552.
World Health Organization (1967). Standardization of procedures for the study of glucose-6-phosphate dehydrogenase. W.H.O. Tech. Rep. Ser. 366.
Author information
Authors and Affiliations
Additional information
This investigation is part of a doctoral thesis to be submitted to the Faculty of Medicine of the University of Leiden, the Netherlands.
Rights and permissions
About this article
Cite this article
Bogaart, A.M., Bernini, L.F. The molybdoenzyme system of Drosophila melanogaster. I. Sulfite oxidase: Identification and properties. Expression of the enzyme in maroon-like (mal), low-xanthine dehydrogenase (lxd), and cinnamon (cin) flies. Biochem Genet 19, 929–946 (1981). https://doi.org/10.1007/BF00504258
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00504258