Characterization of patient mutations in human persulfide dioxygenase (ETHE1) involved in H2S catabolism

Journal of Biological Chemistry

Volumn 287, Issue 53, 2012, Pages 44561-44667

  Kabil, Omer ^a   Banerjee, Ruma ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL CHARACTERIZATION; CELLULAR PROCESS; CENTRAL NERVOUS SYSTEMS; DIOXYGENASES; ELECTRON-TRANSFER CHAIN; GASTROINTESTINAL TRACT; GLUTATHIONES; IRON CONTENT; KINETIC PROPERTIES; MUTATION RESULTS; OXIDOREDUCTASES; SIGNALING MOLECULES; STEADY-STATE KINETICS; STEADY-STATE LEVEL; SULFITE OXIDASE; SYNTHASES; WILD-TYPE ENZYMES;

CARDIOVASCULAR SYSTEM; ENZYMES; HYDROGEN SULFIDE;

METABOLISM;

ASPARAGINE; ASPARTIC ACID; DIOXYGENASE; HYDROGEN SULFIDE; IRON; ISOLEUCINE; PROTEIN ETHE1; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; BIOCHEMISTRY; CATABOLISM; CONTROLLED STUDY; DEGRADATION KINETICS; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME SUBSTRATE; GENETIC ASSOCIATION; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; OXIDATION KINETICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEADY STATE; WILD TYPE;

BRAIN DISEASES, METABOLIC, INBORN; HUMANS; HYDROGEN SULFIDE; KINETICS; MITOCHONDRIAL PROTEINS; MUTATION, MISSENSE; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; PURPURA;

EID: 84871786683     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.407411     Document Type: Article

References (28)

1. Burlina, A., Zacchello, F., Dionisi-Vici, C., Bertini, E., Sabetta, G., Bennet, M. J., Hale, D. E., Schmidt-Sommerfeld, E., and Rinaldo, P. (1991) New clinical phenotype of branched-chain acyl-CoA oxidation defect. Lancet 338, 1522-1523
2. García-Silva, M. T., Campos, Y., Ribes, A., Briones, P., Cabello, A., Santos Borbujo, J., Arenas, J., and Garavaglia, B. (1994) Encephalopathy, petechiae, and acrocyanosis with ethylmalonic aciduria associated with muscle cytochrome c oxidase deficiency. J. Pediatr. 125, 843-844 (Pubitemid 24350203)
3. Tiranti, V., D'Adamo, P., Briem, E., Ferrari, G., Mineri, R., Lamantea, E., Mandel, H., Balestri, P., Garcia-Silva, M. T., Vollmer, B., Rinaldo, P., Hahn, S. H., Leonard, J., Rahman, S., Dionisi-Vici, C., Garavaglia, B., Gasparini, P., and Zeviani, M. (2004) Ethylmalonic encephalopathy is caused by mutations in ETHE1, a gene encoding a mitochondrial matrix protein. Am. J. Hum. Genet. 74, 239-252 (Pubitemid 38168612)
4. Daiyasu, H., Osaka, K., Ishino, Y., and Toh, H. (2001) Expansion of the zinc metallohydrolase family of the β-lactamase fold. FEBS Lett. 503, 1-6 (Pubitemid 32769945)
5. McCoy, J. G., Bingman, C. A., Bitto, E., Holdorf, M. M., Makaroff, C. A., and Phillips, G. N., Jr. (2006) Structure of an ETHE1-like protein from Arabidopsis thaliana. Acta Crystallogr. D Biol. Crystallogr. 62, 964-970 (Pubitemid 44337369)
6. Cameron, A. D., Ridderström, M., Olin, B., and Mannervik, B. (1999) Crystal structure of human glyoxalase II and its complex with a glutathione thiolester substrate analogue. Structure 7, 1067-1078 (Pubitemid 29436504)
7. Crowder, M. W., Maiti, M. K., Banovic, L., and Makaroff, C. A. (1997) Glyoxalase II from A. thaliana requires Zn(II) for catalytic activity. FEBS Lett. 418, 351-354 (Pubitemid 27515955)
8. Zang, T. M., Hollman, D. A., Crawford, P. A., Crowder, M. W., and Makaroff, C. A. (2001) Arabidopsis glyoxalase II contains a zinc/iron binuclear metal center that is essential for substrate binding and catalysis. J. Biol. Chem. 276, 4788-4795
9. Wenzel, N. F., Carenbauer, A. L., Pfiester, M. P., Schilling, O., Meyer- Klaucke, W., Makaroff, C. A., and Crowder, M. W. (2004) The binding of iron and zinc to glyoxalase II occurs exclusively as di-metal centers and is unique within the metallo-β-lactamase family. J. Biol. Inorg. Chem. 9, 429-438 (Pubitemid 38855553)
10. Marasinghe, G. P., Sander, I. M., Bennett, B., Periyannan, G., Yang, K. W., Makaroff, C. A., and Crowder, M. W. (2005) Structural studies on a mitochondrial glyoxalase II. J. Biol. Chem. 280, 40668-40675 (Pubitemid 41780558)
11. Tiranti, V., Viscomi, C., Hildebrandt, T., Di Meo, I., Mineri, R., Tiveron, C., Levitt, M. D., Prelle, A., Fagiolari, G., Rimoldi, M., and Zeviani, M. (2009) Loss of ETHE1, a mitochondrial dioxygenase, causes fatal sulfide toxicity in ethylmalonic encephalopathy. Nat. Med. 15, 200-205
12. Hildebrandt, T. M., and Grieshaber, M. K. (2008) Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria. FEBS J. 275, 3352-3361 (Pubitemid 351813547)
13. Furne, J., Saeed, A., and Levitt, M. D. (2008) Whole tissue hydrogen sulfide concentrations are orders of magnitude lower than presently accepted values. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R1479-1485
14. Levitt, M. D., Abdel-Rehim, M. S., and Furne, J. (2011) Free and acid-labile hydrogen sulfide concentrations in mouse tissues: anomalously high free hydrogen sulfide in aortic tissue. Antioxid. Redox Signal. 15, 373-378
15. Bouillaud, F., and Blachier, F. (2011) Mitochondria and sulfide: a very old story of poisoning, feeding and signaling? Antioxid. Redox Signal. 15, 379-391
16. Leschelle, X., Goubern, M., Andriamihaja, M., Blottière, H. M., Couplan, E., Gonzalez-Barroso, M. D., Petit, C., Pagniez, A., Chaumontet, C., Mignotte, B., Bouillaud, F., and Blachier, F. (2005) Adaptative metabolic response of human colonic epithelial cells to the adverse effects of the luminal compound sulfide. Biochim. Biophys. Acta 1725, 201-212 (Pubitemid 41253930)
17. Olson, K. R., Dombkowski, R. A., Russell, M. J., Doellman, M. M., Head, S. K., Whitfield, N. L., and Madden, J. A. (2006) Hydrogen sulfide as an oxygen sensor/transducer in vertebrate hypoxic vasoconstriction and hypoxic vasodilation. J. Exp. Biol. 209, 4011-4023 (Pubitemid 44769370)
18. Olson, K. R., and Whitfield, N. L. (2010) Hydrogen sulfide and oxygen sensing in the cardiovascular system. Antioxid. Redox Signal. 12, 1219-1234
19. Hegg, E. L., and Que, L., Jr. (1997) The 2-His-1-carboxylate facial triad: an emerging structural motif in mononuclear nonheme iron(II) enzymes. Eur. J. Biochem. 250, 625-629 (Pubitemid 28022477)
20. Holdorf, M. M., Bennett, B., Crowder, M. W., and Makaroff, C. A. (2008) Spectroscopic studies on Arabidopsis ETHE1, a glyoxalase II-like protein. J. Inorg. Biochem. 102, 1825-1830
21. Mineri, R., Rimoldi, M., Burlina, A. B., Koskull, S., Perletti, C., Heese, B., von Dobeln, U., Mereghetti, P., Di Meo, I., Invernizzi, F., Zeviani, M., Uziel, G., and Tiranti, V. (2008) Identification of new mutations in the ETHE1 gene in a cohort of 14 patients presenting with ethylmalonic encephalopathy. J. Med. Genet. 45, 473-478 (Pubitemid 351977139)
22. Wood, J. L. (1987) Sulfane sulfur. Methods Enzymol. 143, 25-29
23. Williamson, G., Engel, P. C., Mizzer, J. P., Thorpe, C., and Massey, V. (1982) Evidence that the greening ligand in native butyryl-CoA dehydrogenase is a CoA persulfide. J. Biol. Chem. 257, 4314-4320
24. Shaw, L., and Engel, P. C. (1987) CoA-persulphide: a possible in vivo inhibitor of mammalian short-chain acyl-CoA dehydrogenase. Biochim. Biophys. Acta 919, 171-174 (Pubitemid 17076677)
25. 35S]Thiosulphate oxidation by rat liver mitochondria in the presence of glutathione. Biochem. J. 103, 791-795
26. Jackson, M. R., Melideo, S. L., and Jorns, M. S. (2012) Human sulfide: quinone oxidoreductase catalyzes the first step in hydrogen sulfide metabolism and produces a sulfane sulfur metabolite. Biochemistry 51, 6804-6815
27. McCoy, J. G., Bailey, L. J., Bitto, E., Bingman, C. A., Aceti, D. J., Fox, B. G., and Phillips, G. N., Jr. (2006) Structure and mechanism of mouse cysteine dioxygenase. Proc. Natl. Acad. Sci. U.S.A. 103, 3084-3089 (Pubitemid 43346428)
28. Vitvitsky, V., Kabil, O., and Banerjee, R. (2012) High turnover rates for hydrogen sulfide allow for rapid regulation of its tissue concentrations. Antioxid. Redox Signal. 17, 22-31