Proteome adaptations in Ethe1-deficient mice indicate a role in lipid catabolism and cytoskeleton organization via post-translational protein modifications

Bioscience Reports

Volumn 33, Issue 4, 2013, Pages 575-584

  Hildebrandt, Tatjana M ^a   Di Meo, Ivano ^b   Zeviani, Massimo ^b,c   Viscomi, Carlo ^b   Braun, Hans Peter ^a  

^a LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^b DEPARTMENT OF NEUROSURGERY   (Italy)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Branched chain amino acid oxidation; Ethylmalonic encephalopathy; Hydrogen sulfide; Mitochondria; Redox regulation; Sulfur dioxygenase

Indexed keywords

BRANCHED CHAIN AMINO ACID; CYSTEINE; DIOXYGENASE; FATTY ACID; PROTEIN ETHE1; PROTEOME; SULFIDE; SULFURE DIOXYGENASE; UNCLASSIFIED DRUG; ETHE1 PROTEIN, MOUSE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MITOCHONDRIAL PROTEIN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN DISEASE; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVITY; ENZYME REGULATION; ETHYLMALONIC ENCEPHALOPATHY; FEMALE; KIDNEY; LIPOLYSIS; LIVER; MOLECULAR DYNAMICS; MOUSE; MUSCLE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; OXIDATION REDUCTION REACTION; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; SIGNAL TRANSDUCTION; 129 MOUSE; ACTIN FILAMENT; ANIMAL; ANTIBODY SPECIFICITY; C57BL MOUSE; DEFICIENCY; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOLECULAR GENETICS; PROTEIN PROCESSING; SKELETAL MUSCLE;

MUS;

ACTIN CYTOSKELETON; AMINO ACIDS, BRANCHED-CHAIN; ANIMALS; BRAIN; DIOXYGENASES; FATTY ACIDS; FEMALE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE (PHOSPHORYLATING); KIDNEY; LIPOLYSIS; LIVER; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE ANNOTATION; MUSCLE, SKELETAL; ORGAN SPECIFICITY; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; SIGNAL TRANSDUCTION; SULFIDES;

EID: 84881530220     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20130051     Document Type: Article

References (35)

1. Tiranti, V., Viscomi, C., Hildebrandt, T., Di Meo, I., Mineri, R., Tiveron, C., D Levitt, M., Prelle, A., Fagiolari, G., Rimoldi, M. et al. (2009) Loss of ETHE1, a mitochondrial dioxygenase, causes fatal sulfide toxicity in ethylmalonic encephalopathy. Nat. Med. 15, 200-205
2. 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)
3. Kabil, O. and Banerjee, R. (2010) Redox biochemistry of hydrogen sulfide. J. Biol. Chem. 285, 21903-21907
4. Flannigan, K. L., McCoy, K. D. and Wallace, J. L. (2011) Eukaryotic and prokaryotic contributions to colonic hydrogen sulfide synthesis. Am. J. Physiol. Gastrointest. Liver Physiol. 301, G188
5. Li, L., Rose, P. and Moore, P. K. (2011) Hydrogen sulfide and cell signaling. Annu. Rev. Pharmacol. Toxicol. 51, 169-187
6. Predmore, B. L., Lefer, D. J. and Gojon, G. (2012) Hydrogen sulfide in biochemistry and medicine. Antioxid. Redox. Signal. 17, 119-140
7. Burlina, A., Zacchello, F., Dionisi-Vici, C., Bertini, E., Sabetta, G., Bennet, M., Hale, D., Schmidt-Sommerfeld, E. and Rinaldo, P. (1991) New clinical phenotype of branched-chain acyl-CoA oxidation defect. Lancet 338, 1522-1523
8. Mineri, R., Rimoldi, M., Burlina, A. B., Koskull, S., Perletti, C., Heese, B., Dobeln, U. von, Mereghetti, P., Di Meo, I., Invernizzi, F. et al. (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)
9. Giordano, C., Viscomi, C., Orlandi, M., Papoff, P., Spalice, A., Burlina, A., Meo, I., Tiranti, V., Leuzzi, V., d'Amati, G. et al. (2012) Morphologic evidence of diffuse vascular damage in human and in the experimental model of ethylmalonic encephalopathy. J. Inherit. Metab. Dis. 35, 451-458
10. Cooper, C. E. and Brown, G. C. (2008) The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: chemical mechanism and physiological significance. J. Bioenerg. Biomembr. 40, 533-539
11. Di Meo, I., Fagiolari, G., Prelle, A., Viscomi, C., Zeviani, M. and Tiranti, V. (2011) Chronic exposure to sulfide causes accelerated degradation of cytochrome c oxidase in ethylmalonic encephalopathy. Antioxid. Redox. Signal. 15, 353-362
12. Klodmann, J., Senkler, M., Rode, C. and Braun, H.-P. (2011) Defining the protein complex proteome of plant mitochondria. Plant Physiol. 157, 587-598
13. Huang, D. W., Sherman, B. T. and Lempicki, R. A. (2008) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57
14. Finocchiaro, G., Colombo, I., Garavaglia, B., Gellera, C., Valdameri, G., Garbuglio, N. and Didonato, S. (1993) cDNA cloning and mitochondrial import of the beta-subunit of the human electron-transfer flavoprotein. Eur. J. Biochem. 213, 1003-1008 (Pubitemid 23152208)
15. Brosnan, J. T. and Brosnan, M. E. (2006) Branched-chain amino acids: enzyme and substrate regulation. J. Nutr. 136, 2075-2115
16. Mustafa, A. K., Gadalla, M. M., Sen, N., Kim, S., Mu, W., Gazi, S. K., Barrow, R. K., Yang, G., Wang, R. and Snyder, S. H. (2009) H2S Signals through protein S-sulfhydration. Sci. Signal. 2, ra72
17. Hara, M. R., Agrawal, N., Kim, S. F., Cascio, M. B., Fujimuro, M., Ozeki, Y., Takahashi, M., Cheah, J. H., Tankou, S. K., Hester, L. D. et al. (2005) S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat. Cell Biol. 7, 665-674 (Pubitemid 40975747)
18. Yang, J., Gibson, B., Snider, J., Jenkins, C. M., Han, X. and Gross, R. W. (2005) Submicromolar concentrations of palmitoyl-CoA specifically thioesterify cysteine 244 in glyceraldehyde-3-phosphate dehydrogenase inhibiting enzyme activity: a novel mechanism potentially underlying fatty acid induced insulin resistance. Biochemistry 44, 11903-11912 (Pubitemid 41262725)
19. Yap, L., Garcia, J. V., Han, D. S. and Cadenas, E. (2010) Role of nitric oxide-mediated glutathionylation in neuronal function: potential regulation of energy utilization. Biochem. J. 428, 85-93
20. Gregersen, N. (1998) Identification of four new mutations in the short-chain acyl-CoA dehydrogenase (SCAD) gene in two patients: one of the variant alleles, 511C→T, is present at an unexpectedly high frequency in the general population, as was the case for 625G→A, together conferring susceptibility to ethylmalonic aciduria. Hum. Mol. Genet. 7, 619-627 (Pubitemid 28152260)
21. Koeberl, D. D., Young, S. P., Gregersen, N., Vockley, J., Smith, W. E., Benjamin, D. K., An, Y., Weavil, S. D., Chaing, S. H., Bali, D. et al. (2003) Rare disorders of metabolism with elevated butyryland isobutyryl-carnitine detected by tandem mass spectrometry newborn screening. Pediatr. Res. 54, 219-223 (Pubitemid 36918156)
22. Sass, J. O., Ensenauer, R., Röschinger, W., Reich, H., Steuerwald, U., Schirrmacher, O., Engel, K., Häberle, J., Andresen, B. S., Mégarbané, A. et al. (2008) 2-methylbutyryl-coenzyme A dehydrogenase deficiency: functional and molecular studies on a defect in isoleucine catabolism. Mol. Genet. Metab. 93, 30-35 (Pubitemid 350245617)
23. Kabil, O. and Banerjee, R. (2012) Characterization of patient mutations in human persulfide dioxygenase (ETHE1) involved in H2S catabolism. J. Biol. Chem. 287, 44561-44567
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. Suryawan, A., Hawes, J. W., Harris, R. A., Shimomura, Y., Jenkins, A. E. and Hutson, S. M. (1998) A molecular model of human branched-chain amino acid metabolism. Am. J. Clin. Nutr. 68, 72-81 (Pubitemid 28307657)
26. Harris, R. A., Kobayashi, R., Murakami, T. and Shimomura, Y. (2001) Regulation of branched-chain alpha-keto acid dehydrogenase kinase expression in rat liver. J. Nutr. 131, 841S-845S (Pubitemid 32199156)
27. Hirschey, M. D., Shimazu, T., Goetzman, E., Jing, E., Schwer, B., Lombard, D. B., Grueter, C. A., Harris, C., Biddinger, S., Ilkayeva, O. R. et al. (2010) SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 464, 121-125
28. Doulias, P.-T., Tenopoulou, M., Greene, J. L., Raju, K. and Ischiropoulos, H. (2013) Nitric oxide regulates mitochondrial fatty acid metabolism through reversible protein S-nitrosylation. Sci. Signal. 6, rs1
29. Kostiuk, M. A., Corvi, M. M., Keller, B. O., Plummer, G., Prescher, J. A., Hangauer, M. J., Bertozzi, C. R., Rajaiah, G., Falck, J. R. and Berthiaume, L. G. (2007) Identification of palmitoylated mitochondrial proteins using a bio-orthogonal azido-palmitate analogue. FASEB J. 22, 721-732 (Pubitemid 351348125)
30. Whiteman, M., Gooding, K. M., Whatmore, J. L., Ball, C. I., Mawson, D., Skinner, K., Tooke, J. E. and Shore, A. C. (2010) Adiposity is a major determinant of plasma levels of the novel vasodilator hydrogen sulphide. Diabetologia 53, 1722-1726
31. Baiges, I., Palmfeldt, J., Blade, C., Gregersen, N. and Arola, L. (2010) Lipogenesis is decreased by grape seed proanthocyanidins according to liver proteomics of rats fed a high fat diet. Mol. Cell. Proteomics 9, 1499-1513
32. Viscomi, C., Burlina, A. B., Dweikat, I., Savoiardo, M., Lamperti, C., Hildebrandt, T., Tiranti, V. and Zeviani, M. (2010) Combined treatment with oral metronidazole and N-acetylcysteine is effective in ethylmalonic encephalopathy. Nat. Med. 16, 869-871
33. Di Meo, I., Auricchio, A., Lamperti, C., Burlina, A., Viscomi, C. and Zeviani, M. (2012) Effective AAV-mediated gene therapy in a mouse model of ethylmalonic encephalopathy. EMBO Mol. Med. 4, 1008-1014
34. Zhang, L.-J., Tao, B.-B., Wang, M.-J., Jin, H.-M., Zhu, Y.-C. and Yang, C.-M. (2012) PI3K p110α isoform-dependent Rho GTPase Rac1 activation mediates H2S-promoted endothelial cell migration via actin cytoskeleton reorganization. PLoS ONE 7, e44590
35. Palmfeldt, J., Vang, S., Stenbroen, V., Pavlou, E., Baycheva, M., Buchal, G., Monavari, A. A., Augoustides-Savvopoulou, P., Mandel, H. and Gregersen, N. (2011) Proteomics reveals that redox regulation is disrupted in patients with ethylmalonic encephalopathy. J. Proteome Res. 10, 2389-2396