Redox regulation of mitochondrial sulfide oxidation in the lugworm, Arenicola marina

Journal of Experimental Biology

Volumn 211, Issue 16, 2008, Pages 2617-2623

  Hildebrandt, Tatjana M ^a   Grieshaber, Manfred K ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Alternative oxidase; Arenicola marina; Ascorbate; ATP production; Dehydroascorbate; Glutathione; Redox regulation; Sulfide oxidation

Indexed keywords

ADENOSINE TRIPHOSPHATE; ASCORBIC ACID; DEHYDROASCORBIC ACID; GLUTATHIONE; MALIC ACID; MALIC ACID DERIVATIVE; OXIDOREDUCTASE; OXYGEN; SULFIDE;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CELL RESPIRATION; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; OXYGEN CONSUMPTION; POLYCHAETA;

ADENOSINE TRIPHOSPHATE; ANIMALS; ASCORBIC ACID; CELL RESPIRATION; DEHYDROASCORBIC ACID; GLUTATHIONE; MALATES; MITOCHONDRIA; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; OXIDOREDUCTASES; OXYGEN; OXYGEN CONSUMPTION; POLYCHAETA; SULFIDES;

ARENICOLA MARINA;

EID: 52649125410     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.019729     Document Type: Article

References (46)

1. Andreyev, A. Y., Kushnareva, Y. E. and Starkov, A. A. (2005). Mitochondrial metabolism of reactive oxygen species. Biochem. Mosc. 70, 200-214.
2. Azcon-Bleto, J., Ribas-Carbo, M., Gonzalez-Meler, M. A. and Penuelas, J. (1989). Sulfide-resistant respiration in leaves of Elodea canadensis Michx: comparison with cyanide-resistant respiration. Plant Physiol. 90, 1249-1251.
3. Bagarinao, T. and Vetter, R. D. (1990). Oxidative detoxification of sulfide by mitochondria of the California killifish Fundulus parvipinnis and the speckled sanddab Citharichthys stigmaeus. J. Comp. Physiol. B 160, 519-527.
4. Berthold, D. A., Andersson, M. E. and Nordlund, P. (2000). New insight into the structure and function of the alternative oxidase. Biochim. Biophys. Acta 1460, 241-254.
5. Brigelius, R., Muckel, C., Akerboom, T. P. M. and Sies, H. (1983). Identification and quantitation of glutathione in hepatic protein mixed disulfides and its relationship to glutathione disulfide. Biochem. Pharmacol. 32, 2529-2534.
6. Buchner, T., Abele-Oeschger, D. and Theede, H. (1996). Aspects of antioxidant status in the polychaete Arenicola marina: tissue and subcellular distribution, and reaction to environmental hydrogen peroxide and elevated temperatures. Mar. Ecol. Prog. Ser. 143, 141-150.
7. Damdimopoulos, A. E., Miranda-Vizuete, A., Pelto-Huikko, M., Gustafsson, J. A. and Spyrou, G. (2002). Human mitochondrial thioredoxin-Involvement in mitochondrial membrane potential and cell death. J. Biol. Chem. 277, 33249-33257.
8. 2S generated by heart in rat and its effects on cardiac function. Biochem. Biophys. Res. Commun. 313, 362-368.
9. Ghezzi, P. (2005). Oxidoreduction of protein thiols in redox regulation. Biochem. Soc. Trans. 33, 1378-1381.
10. Gnaiger, E., Steinlechner-Maran, R., Mendez, G., Eberl, T. and Margreiter, R. (1995). Control of mitochondrial and cellular respiration by oxygen. J. Bioenerg. Biomembr. 27, 583-596.
11. Gnaiger, E., Lassnig, B., Kuznetsov, A., Rieger, G. and Margreiter, R. (1998). Mitochondrial oxygen affinity, respiratory flux control and excess capacity of cytochrome c oxidase. J. Exp. Biol. 201, 1129-1139.
12. Goubern, M., Andriamihaja, M., Nubel, T., Blachier, F. and Bouillaud, F. (2007). Sulfide, the first inorganic substrate for human cells. FASEB J. 21, 1699-1706.
13. Grieshaber, M. K. and Völkel, S. (1998). Animal adaptations for tolerance and exploitation of poisonous sulfide. Annu. Rev. Physiol. 60, 33-53.
14. Grieshaber, M. K., Hardewig, I., Kreutzer, U. and Pörtner, H. O. (1994). Physiological and metabolic responses to hypoxia in invertebrates. Rev. Physiol. Biochem. Pharmacol. 125, 43-147.
15. Hahlbeck, E., Arndt, C. and Schiedek, D. (2000). Sulphide detoxification in Hediste diversicolor and Marenzelleria viridis, two dominant polychaete worms within the shallow coastal waters of the southern Baltic Sea. Comp. Biochem. Physiol. 125B, 457-471.
16. Hauschild, K., Weber, W. M., Clauss, W. and Grieshaber, M. K. (1999). Excretion of thiosulphate, the main detoxification product of sulphide, by the lugworm Arenicola marina L. J. Exp. Biol. 202, 855-866.
17. 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.
18. Hinkle, P. C. (2005). P/O ratios of mitochondrial oxidative phosphorylation. Biochim. Biophys. Acta 1706, 1-11.
19. Keller, M., Sommer, A. M., Pörtner, H. O. and Abele, D. (2004). Seasonality of energetic functioning and production of reactive oxygen species by lugworm (Arenicola marina) mitochondria exposed to acute temperature changes. J. Exp. Biol. 207, 2529-2538.
20. Kraus, D. W. and Doeller, J. E. (2004). Sulfide consumption by mussel gill mitochondria is not strictly tied to oxygen reduction: measurements using a novel polarographic sulfide sensor. J. Exp. Biol. 207, 3667-3679.
21. Lee, R. W., Kraus, D. W. and Doeller, J. E. (1996). Sulfide-stimulation of oxygen consumption rate and cytochrome reduction in gills of the estuarine mussel Geukensia demissa. Biol. Bull. 191, 421-430.
22. Li, C. and Jackson, R. M. (2002). Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am. J. Physiol. Cell Physiol. 282, C227-C241.
23. Linster, C. L. and Van Schaftingen, E. (2007). Vitamin C. Biosynthesis, recycling and degradation in mammals. FEBS J. 274, 1-22.
24. May, J. M., Mendiratta, S., Hill, K. E. and Burk, R. F. (1997). Reduction of dehydroascorbate to ascorbate by the selenoenzyme thioredoxin reductase. J. Biol. Chem. 272, 22607-22610.
25. McDonald, A. E. and Vanlerberghe, G. C. (2004). Branched mitochondrial electron transport in the animalia: presence of alternative oxidase in several animal phyla. IUBMB Life 56, 333-341.
26. Millar, A. H., Bergersen, F. J. and Day, D. A. (1994). Oxygen-affinity of terminal oxidases in soybean mitochondria. Plant Physiol. Biochem. 32, 847-852.
27. Millar, A. H., Finnegan, P. M., Whelan, J., Drevon, J. J. and Day, D. A. (1997). Expression and kinetics of the mitochondrial alternative oxidase in nitrogen-fixing nodules of soybean roots. Plant Cell Environ. 20, 1273-1282.
28. Moran, L. K., Gutteridge, J. M. C. and Quinlan, G. J. (2001). Thiols in cellular redox signalling and control. Curr. Med. Chem. 8, 763-772.
29. O'Donovan, D. J. and Fernandes, C. J. (2000). Mitochondrial glutathione and oxidative stress: implications for pulmonary oxygen toxicity in premature infants. Mol. Genet. Metab. 71, 352-358.
30. Parrino, V., Kraus, D. W. and Doeller, J. E. (2000). ATP production from the oxidation of sulfide in gill mitochondria of the ribbed mussel Geukensia demissa. J. Exp. Biol. 203, 2209-2218.
31. 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.
32. Reiber, H., Ruff, M. and Uhr, M. (1993). Ascorbate concentration in human cerebrospinal fluid (CSF) and serum. Intrathecal accumulation and CSF flow rate. Clin. Chim. Acta 217, 163-173.
33. 2 solubility in aqueous media determined by a kinetic method. Anal. Biochem. 145, 406-418.
34. Rhoads, D. M., Umbach, A. L., Sweet, C. R., Lennon, A. M., Rauch, G. S. and Siedow, J. N. (1998). Regulation of the cyanide-resistant alternative oxidase of plant mitochondria - identification of the cysteine residue involved in α-keto acid stimulation and intersubunit disulfide bond formation. J. Biol. Chem. 273, 30750-30756.
35. Siedow, J. N., Umbach, A. L. and Moore, A. L. (1995). The active site of the cyanide-resistant oxidase from plant mitochondria contains a binuclear iron center. FEBS Lett. 362, 10-14.
36. Theissen, U. and Martin, W. (2008). Sulfide:quinone oxidoreductase (SQR) from the lugworm Arenicola marina shows cyanide- and thioredoxin-dependent activity. FEBS J. 275, 1131-1139.
37. Vanlerberghe, G. C. and McIntosh, L. (1997). Alternative oxidase: from gene to function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 703-734.
38. Vanlerberghe, G. C., McIntosh, L. and Yip, J. Y. H. (1998). Molecular localization of a redox-modulated process regulating plant mitochondrial electron transport. Plant Cell 10, 1551-1560.
39. Völkel, S. and Grieshaber, M. K. (1994). Oxygen dependent sulfide detoxification in the lugworm Arenicola marina. Mar. Biol. 118, 137-147.
40. Völkel, S. and Grieshaber, M. K. (1996). Mitochondrial sulfide oxidation in Arenicola marina - evidence for alternative electron pathways. Eur. J. Biochem. 235, 231-237.
41. Völkel, S. and Grieshaber, M. K. (1997). Sulphide oxidation and oxidative phosphorylation in the mitochondria of the lugworm Arenicola marina. J. Exp. Biol. 200, 83-92.
42. 2S be the third endogenous gaseous transmitter? FASEB J. 16, 1792-1798.
43. Whiteman, M., Cheung, N. S., Zhu, Y. Z., Chu, S. H., Slau, J. L., Wong, B. S., Armstrong, J. S. and Moore, P. K. (2005). Hydrogen sulphide: a novel inhibitor of hypochlorous acid-mediated oxidative damage in the brain? Biochem. Biophys. Res. Commun. 326, 794-798.
44. Wu, G., Fang, Y. Z., Yang, S., Lupton, J. R. and Turner, N. D. (2004). Glutathione metabolism and its implications for health. J. Nutr. 134, 489-492.
45. Yong, R. and Searcy, D. G. (2001). Sulfide oxidation coupled to ATP synthesis in chicken liver mitochondria. Comp. Biochem. Physiol. 129B, 129-137.
46. Zuckerbraun, B. S., Chin, B. Y., Bilban, M., de Costa d'Avila, J., Rao, J., Billiar, T. R. and Otterbein, L. E. (2007). Carbon monoxide signals via inhibition of cytochrome c oxidase and generation of mitochondrial reactive oxygen species. FASEB J. 21, 1099-1106.