Intramitochondrial hydrogen sulfide production by 3-mercaptopyruvate sulfurtransferase maintains mitochondrial electron flow and supports cellular bioenergetics

FASEB Journal

Volumn 27, Issue 2, 2013, Pages 601-611

  Módis, Katalin ^a   Coletta, Ciro ^a   Erdélyi, Katalin ^a   Papapetropoulos, Andreas ^a   Szabo, Csaba ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b SHRINERS HOSPITALS FOR CHILDREN   (United States)

Author keywords

ATP; Gasotransmitter; Hepatocyte

Indexed keywords

3 MERCAPTOPYRUVIC ACID; HYDROGEN SULFIDE; SMALL INTERFERING RNA; SULFURTRANSFERASE;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; BIOENERGY; CITRIC ACID CYCLE; ELECTRON TRANSPORT; GENE SILENCING; HEPATOMA CELL; ISOLATED LIVER; MITOCHONDRIAL ENERGY TRANSFER; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; RAT; WESTERN BLOTTING;

ANIMALS; BASE SEQUENCE; CELL LINE; CITRIC ACID CYCLE; CYSTEINE; ELECTRON TRANSPORT; ENERGY METABOLISM; HYDROGEN SULFIDE; MALE; MICE; MITOCHONDRIA, LIVER; MODELS, BIOLOGICAL; OXIDATIVE PHOSPHORYLATION; QUINONE REDUCTASES; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; SULFURTRANSFERASES;

EID: 84873467050     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-216507     Document Type: Article

References (48)

1. Nelson, D. L., and Cox, M., eds (2008) Lehninger Principles of Biochemistry, W. H. Freeman, New York
2. Voet, D., Viet, J.G., and Pratt, C. W., eds (2008) Fundamentals of Biochemistry, Wiley, New York
3. Stipanuk, M. H., and Beck, P. W. (1982) Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat. Biochem. J. 206, 267-277
4. Chen, X., Jhee, K.-H., and Kruger, W. D. (2004) Production of the neuromodulator H2S by cystathionine ?-synthase via the condensation of cysteine and homocysteine. J. Biol. Chem. 279, 52082-52086
5. Banerjee, R., and Zou, C. G. (2005) Redox regulation and reaction mechanism of human cystathionine-beta-synthase: A PLP-dependent heme sensor protein. Arch. Biochem. Biophys. 433, 144-156
6. Singh, S., Padovani, D., Leslie, R. A., Chiku, T., and Banerjee, R. (2009) Relative contributions of cystathionine beta-synthase and gamma-cystathionase to H2S biogenesis via alternative transsulfuration reactions. J. Biol. Chem. 284, 22457-22466
7. Shibuya, N., Tanaka, M., Yoshida, M., Ogasawara, Y., Togawa, T., Ishii, K., and Kimura, H. (2009) 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid. Redox Signal. 11, 703-714
8. Szabo, C. (2007) Hydrogen sulphide and its therapeutic potential. Nat. Rev. Drug Discov. 6, 917-935
9. Wang, R. (2012) Physiological implications of hydrogen sulfide: A whiff exploration that blossomed. Physiol. Rev. 92, 791-896
10. Goubern, M., Andriamihaja, M., Nübel, T., Blachier, F., and Bouillaud, F. (2007) Sulfide, the first inorganic substrate for human cells. FASEB J. 21, 1699-1706
11. Lagoutte, E., Mimoun, S., Andriamihaja, M., Chaumontet, C., Blachier, F., and Bouillaud, F. (2010) Oxidation of hydrogen sulfide remains a priority in mammalian cells and causes reverse electron transfer in colonocytes. Biochim. Biophys. Acta 1797, 1500-1511
12. Bouillaud, F., and Blachier, F. (2011) Mitochondria and sulfide: A very old story of poisoning, feeding, and signaling? Antioxid. Redox Signal. 15, 379-391
13. Nicholls, P. (1975) Inhibition of cytochrome c oxidase by sulphide. Biochem. Soc. Trans. 3, 316-319
14. Khan, A. A., Schuler, M. M., Prior, M. G., Yong, S., Coppock, R. W., Florence, L. Z., and Lillie, L. E. (1990) Effects of hydrogen sulfide exposure on lung mitochondrial respiratory chain enzymes in rats. Toxicol. Appl. Pharmacol. 103, 482-490
15. Collman, J. P., Ghosh, S., Dey, A., and Decreau, R. A. (2009) Using a functional enzyme model to understand the chemistry behind hydrogen sulfide induced hibernation. Proc. Natl. Acad. Sci. U. S. A. 106, 22090-22095
16. Tanizawa, K. (2011) Production of H2S by 3-mercaptopyruvate sulphurtransferase. J. Biochem. 149, 357-359
17. Nagahara, N., Ito, T., Kitamura, H., and Nishino, T. (1998) Tissue and subcellular distribution of mercaptopyruvate sulfurtransferase in the rat: Confocal laser fluorescence and immunoelectron microscopic studies combined with biochemical analysis. Histochem. Cell Biol. 110, 243-250
18. Rogers, G. W., Brand, M. D., Petrosyan, S., Ashok, D., Elorza, A. A., Ferrick, D. A., and Murphy, A. N. (2011) High throughput microplate respiratory measurements using minimal quantities of isolated mitochondria. PLoS One 6, e21746
19. Frezza, C., Cipolat, S., and Scorrano, L. (2007) Organelle isolation: Functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nat. Protoc. 2, 287-295
20. Módis, K., Gero, D., Nagy, N., Szoleczky, P., Tóth, Z. D., and Szabo, C. (2009) Cytoprotective effects of adenosine and inosine in an in vitro model of acute tubular necrosis. Br. J. Pharmacol. 158, 1565-1578
21. Erdelyi, K., Bai, P., Kovacs, I., Szabo, E., Mocsar, G., Kakuk, A., Szabo, C., Gergely, P., and Virag, L. (2009) Dual role of poly(ADP-ribose) glycohydrolase in the regulation of cell death in oxidatively stressed A549 cells. FASEB J. 23, 3553-3563
22. Coletta, C., Papapetropoulos, A., Erdelyi, K., Olah, G., Módis, K., Panopoulos, P., Asimakopoulou, A., Gero, D., Sharina, I., Martin, E., and Szabo, C. (2012) Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation. Proc. Natl. Acad. Sci. U. S. A. 109, 9161-9166
23. Módis, K., Gerö, D., Erdélyi, K., Szoleczky, P., DeWitt, D., and Szabo, C. (2012) Cellular bioenergetics is regulated by PARP1 under resting conditions and during oxidative stress. Biochem. Pharmacol. 83, 633-643
24. Suzuki, K., Olah, G., Modis, K., Coletta, C., Kulp, G., Gerö, D., Szoleczky, P., Chang, T., Zhou, Z., Wu, L., Wang, R., Papapetropoulos, A., and Szabo, C. (2011) Hydrogen sulfide replacement therapy protects the vascular endothelium in hyperglycemia by preserving mitochondrial function. Proc. Natl. Acad. Sci. U. S. A. 108, 13829-13834
25. Ferrick, D. A., Neilson, A., and Beeson, C. (2008) Advances in measuring cellular bioenergetics using extracellular flux. Drug Discov. Today 13, 268-274
26. Zhao, D., Liu, T. Z., Chan, E. C., Fein, H., and Zhang, X. (2007) A novel enzymatic method for determination of homocysteine using electrochemical hydrogen sulfide sensor. Front. Biosci. 12, 3774-3780
27. Stachowska, E., Bober, J., Chlubek, D., and Machoy, Z. (2000) Number of fluoride ions binding to succinate dehydrogenase during mixed inhibition. Fluoride 3, 115-120
28. Dranka, B. P., Hill, B. G., and Darley-Usmar, V. M. (2010) Mitochondrial reserve capacity in endothelial cells: The impact of nitric oxide and reactive oxygen species. Free Radic. Biol. Med. 48, 905-914
29. Powell, M. A., and Somero, G. N. (1986) Hydrogen sulfide oxidation is coupled to oxidative phosphorylation in mitochondria of Solemya reidi. Science 233, 563-566
30. Völkel, S., and Grieshaber, M. K. (1996) Mitochondrial sulfide oxidation in Arenicola marina. Evidence for alternative electron pathways. Eur. J. Biochem. 235, 231-237
31. Grieshaber, M. K., and Völkel, S. (1998) Animal adaptations for tolerance and exploitation of poisonous sulfide. Annu. Rev. Physiol. 60, 33-53
32. Olson, K. R. (2012) Mitochondrial adaptations to utilize hydrogen sulfide for energy and signaling. J. Comp. Physiol. B 182, 881-897
33. Yong, R., and Searcy, D. G. (2001) Sulfide oxidation coupled to ATP synthesis in chicken liver mitochondria. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 129, 129-137
34. Mimoun, S., Andriamihaja, M., Chaumontet, C., Atanasiu, C., Benamouzig, R., Blouin, J. M., Tomé, D., Bouillaud, F., and Blachier, F. (2012) Detoxification of H2S by differentiated colonic epithelial cells: Implication of the sulfide oxidizing unit and of the cell respiratory capacity. Antioxid. Redox Signal. 17, 1-10
35. Groeger, M., Matallo, J., McCook, O., Wagner, F., Wachter, U., Bastian, O., Gierer, S., Reich, V., Stahl, B. M. H. L., Szabo, C., Georgieff, M., Radermacher, P., Calzia, E., and Wagner, K. (2012) Temperature and cell-type dependency of sulfide-effects on mitochondrial respiration. Shock 38, 367-374
36. Blackstone, E., Morrison, M., and Roth, M. B. (2005) H2S induces a suspended animation-like state in mice. Science 308, 518
37. Aslami, H., Schultz, M. J., and Juffermans, N. P. (2009) Potential applications of hydrogen sulfide-induced suspended animation. Curr. Med. Chem. 16, 1295-1303
38. Wagner, F., Asfar, P., Calzia, E., Radermacher, P., and Szabo, C. (2009) Bench-to-bedside review: Hydrogen sulfide-the third gaseous transmitter: Applications for critical care. Crit. Care 13, 213
39. Fu, M., Zhang, W., Wu, L., Yang, G., Li, H., and Wang, R. (2012) Hydrogen sulfide (H2S) metabolism in mitochondria and its regulatory role in energy production. Proc. Natl. Acad. Sci. U. S. A. 109, 2943-2948
40. Madden, J. A., Madden, J. A., Ahlf, S. B., Dantuma, M. W., Olson, K. R., and Roerig, D. L. (2012) Precursors and inhibitors of hydrogen sulfide synthesis affect acute hypoxic pulmonary vasoconstriction in the intact lung. J. Appl. Physiol. 112, 411-418
41. Shibuya, N., Mikami, Y., Kimura, Y., Nagahara, N., and Kimura, H. (2009) Vascular endothelium expresses 3-mercaptopyruvate sulfurtransferase and produces hydrogen sulfide. J. Biochem. 146, 623-626
42. Kimura, Y., Goto, Y., and Kimura, H. (2010) Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochondria. Antioxid. Redox Signal. 12, 1-13
43. Ohta, J., and Ubuka, T. (1989) Reduction of 3-mercaptopyruvate in rat liver is catalyzed by lactate dehydrogenase. Acta Med. Okayama 43, 89-95
44. Martensson, J., Nilsson, L., and Sorbo, B. (1984) The decarboxylation of 3-mercaptopyruvate to 2-mercaptoacetate. FEBS Lett. 176, 334-336
45. Thangaraju, M., Carswell, K. N., Prasad, P. D., and Ganapathy, V. (2009) Colon cancer cells maintain low levels of pyruvate to avoid cell death caused by inhibition of HDAC1/HDAC3. Biochem. J. 417, 379-389
46. Zhu, A., Romero, R., and Petty, H. R. (2010) A sensitive fluorimetric assay for pyruvate. Anal. Biochem. 396, 146-151
47. Kannampuzha, J. V., Tupy, J. H., and Pritzker, K. P. (2009) Mercaptopyruvate inhibits tissue-nonspecific alkaline phosphatase and calcium pyrophosphate dihydrate crystal dissolution. (2009) J. Rheumatol. 12, 2758-2765
48. Wlodek, P., Marcykiewicz, B., Iciek, M., Suliga, M., Smolénski, O., and Kowalczyk-Pachel, D. (2010) Thiol levels, protein carbonylation and anaerobic sulfur metabolism in erythrocytes of peritoneal dialysis and predialysis patients. Nephrology 8, 755-761