EPR and Mössbauer spectroscopy of intact mitochondria isolated from Yah1p-depleted Saccharomyces cerevisiae

Biochemistry

Volumn 47, Issue 37, 2008, Pages 9888-9899

  Miao, Ren ^a   Martinho, Marlène ^b   Morales, Jessica Garber ^a   Kim, Hansoo ^c   Ellis, E Ann ^c   Lill, Roland ^d   Hendrich, Michael P ^b   Münck, Eckard ^b   Lindahl, Paul A ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b CARNEGIE MELLON UNIVERSITY   (United States)

^c Texas AandM University   (United States)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MOLYBDENUM;

SACCHAROMYCES CEREVISIAE; SSBAUER SPECTROSCOPY;

ELECTRON SPIN RESONANCE SPECTROSCOPY;

ARGON; DITHIONITE; FERREDOXIN; IRON; OXYGEN; PEPTONE; SULFUR; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE; UNCLASSIFIED DRUG; YAH1P PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CULTURE MEDIUM; ELECTRON MICROSCOPY; ELECTRON SPIN RESONANCE; FUNGAL CELL CULTURE; ION TRANSPORT; MITOCHONDRION; MOSSBAUER SPECTROSCOPY; NONHUMAN; OXIDATION; OXIDATION REDUCTION STATE; PRECIPITATION; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; WILD TYPE;

ADRENODOXIN; ELECTRON SPIN RESONANCE SPECTROSCOPY; IRON; MITOCHONDRIA; OXYGEN; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPECTROSCOPY, MOSSBAUER;

SACCHAROMYCES CEREVISIAE;

EID: 51849115120     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801047q     Document Type: Article

References (47)

1. Lill, R., and Mühlenhoff, U. (2006) Iron-sulfur protein biogenesis in eukaryotes: Components and mechanisms. Annu. Rev. Cell. Dev. Biol. 22, 457-486.
2. Lill, R., Dutkiewicz, R., Elsasser, H. P., Hausmann, A., Netz, D. J. A., Pierik, A. J., Stehling, O., Urzica, E., and Mühlenhoff, U. (2006) Mechanisms of iron-sulfur protein maturation in mitochondria, cytosol and nucleus of eukaryotes. Biochim. Biophys. Acta Mol. Cell Res. 1763, 652-667.
3. Kwok, E., and Kosman, D. (2006) Iron in yeast: Mechanisms involved in homeostasis, in Molecular Biology of Metal Homeostasis and Detoxification: From Microbes to Man (Tamás, M. J., and Martinoia, E., Eds.), pp 59-99, Springer, Berlin.
4. Rosenfeld, E., and Beauvoit, B. (2003) Role of the non-respiratory pathways in the utilization of molecular oxygen by Saccharomyces cerevisiae. Yeast 20, 1115-1144.
5. Mühlenhoff, U., Stadler, J. A., Richhardt, N., Seubert, A., Eickhorst, T., Schweyen, R. J., Lill, R., and Wiesenberger, G. (2003) A specific role of the yeast mitochondrial carriers Mrs3/4p in mitochondrial iron acquisition under iron-limiting conditions. J. Biol. Chem. 278, 40612-40620.
6. Lange, H., Mühlenhoff, U., Denzel, M., Kispal, G., and Lill, R. (2004) The heme synthesis defect of mutants impaired in mitochondrial iron-sulfur protein biogenesis is caused by reversible inhibition of ferrochelatase. J. Biol. Chem. 279, 29101-29108.
7. Hausmann, A., Samans, B., Lill, R., and Mühlenhoff, U. (2008) Cellular and mitochondrial remodeling upon defects in iron-sulfur protein biogenesis. J. Biol. Chem. 283, 8318-8330.
8. Mühlenhoff, U., Gerber, J., Richhardt, N., and Lill, R. (2003) Components involved in assembly and dislocation of iron-sulfur clusters on the scaffold protein Isu1p. EMBO J. 22, 4815-4825.
9. Barros, M. H., and Nobrega, F. G. (1999) YAH1 of Saccharomyces cerevisiae: a new essential gene that codes for a protein homologous to human adrenodoxin. Gene 233, 197-203.
10. Lange, H., Kaut, A., Kispal, G., and Lill, R. (2000) A mitochondrial ferredoxin is essential for biogenesis of cellular iron-sulfur proteins. Proc. Natl. Acad. Sci. U.S.A. 97, 1050-1055.
11. Barros, M. H., Nobrega, F. G., and Tzagoloff, A. (2002) Mitochondrial ferredoxin is required for heme A synthesis in Saccharomyces cerevisiae. J. Biol. Chem. 277, 9997-10002.
12. Barros, M. H., Carlson, C. G., Glerum, D. M., and Tzagoloff, A. (2001) Involvement of mitochondrial ferredoxin and Cox15p in hydroxylation of heme O. FEBS Lett. 492, 133-138.
13. Babcock, M., deSilva, D., Oaks, R., DavisKaplan, S., Jiralerspong, S., Montermini, L., Pandolfo, M., and Kaplan, J. (1997) Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science 276, 1709-1712.
14. Lesuisse, E., Santos, R., Matzanke, B. F., Knight, S. A. B., Camadro, J. M., and Dancis, A. (2003) Iron use for haeme synthesis is under control of the yeast frataxin homologue (Yfh1). Hum. Mol. Genet. 12, 879-889.
15. Bulteau, A. L., Dancis, A., Gareil, M., Montagne, J. J., Camadro, J. M., and Lesuisse, E. (2007) Oxidative stress and protease dysfunction in the yeast model of Friedreich ataxia. Free Radical Biol. Med. 42, 1561-1570.
16. Aisen, P., Enns, C., and Wessling-Resnick, M. (2001) Chemistry and biology of eukaryotic iron metabolism. Int. J. Biochem. Cell Biol. 33, 940-959.
17. Rotig, A., deLonlay, P., Chretien, D., Foury, F., Koehig, M., Sidi, D., Munnich, A., and Rustin, P. (1997) Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat. Genet. 17, 215-217.
18. Chaston, T. B., and Richardson, D. R. (2003) Iron chelators for the treatment of iron overload disease: Relationship between structure, redox activity, and toxicity. Am. J. Hematol. 73, 200-210.
19. Hudder, B. N., Garber, J. M., Stubna, A., Münck, E., Hendrich, M. P., and Lindahl, P. A. (2007) Electron paramagnetic resonance and Mössbauer spectroscopy of intant mitochondria from respiring Saccharomyces cerevisiae. J. Biol. Inorg. Chem. 12, 1029-1053.
20. Kushnirov, V. V. (2000) Rapid and reliable protein extraction from yeast. Yeast 16, 857-860.
21. Watters, C. (1978) One-step Biuret assay for protein in presence of detergent. Anal. Biochem. 88, 695-698.
22. Parvin, R., Pande, S. V., and Venkitas, Ta. (1965) On colorimetric Biuret method of protein determination. Anal. Biochem. 12, 219-229.
23. Yeast genome database: http://www.yeastgenome.org/straintable. shtml.
24. Dedeken, R. H. (1966) Crabtree effect - a regulatory system in yeast. J. Gen. Microbiol. 44, 149-156.
25. Kwast, K. E., Lai, L. C., Menda, N., James, D. T., Aref, S., and Burke, P. V. (2002) Genomic analyses of anaerobically induced genes in Saccharomyces cerevisiae: Functional roles of Rox1 and other factors in mediating the anoxic response. J. Bacteriol. 184, 250-265.
26. 4. J. Phys. C: Solid State Phys. 15, L919-L924.
27. StPierre, T. G., Chan, P., Bauchspiess, K. R., Webb, J., Betteridge, S., Walton, S., and Dickson, D. P. E. (1996) Synthesis, structure and magnetic properties of ferritin cores with varying composition and degrees of structural order: Models for iron oxide deposits in iron-overload diseases. Coord. Chem. Rev. 151, 125-143.
28. Bauminger, E. R., Cohen, S. G., Dekanter, F. L., Levy, A., Ofer, S., Kessel, M., and Rottem, S. (1980) Iron storage in Mycoplasma capricolum. J. Bacteriol. 141, 378-381.
29. Weir, M. P., Peters, T. J., and Gibson, J. F. (1985) Electron-spin resonance studies of splenic ferritin and hemosiderin. Biochim. Biophys. Acta 828, 298-305.
30. Wajnberg, E., El-Jaick, L. J., Linhares, M. P., and Esquivel, D. M. S. (2001) Ferromagnetic resonance of horse spleen ferritin: Core blocking and surface ordering temperatures. J. Magn. Reson. 153, 69-74.
31. Rauen, U., Springer, A., Weisheit, D., Petrat, F., Korth, H. G., de Groot, H., and Sustmann, R. (2007) Assessment of chelatable mitochondrial iron by using mitochondrion-selective fluorescent iron indicators with different iron-binding affinities. ChemBioChem 8, 341-352.
32. Popescu, B. F. G., Pickering, I. J., George, G. N., and Nichol, H. (2007) The chemical form of mitochondrial iron in Friedreich's ataxia. J. Inorg. Biochem. 101, 957-966.
33. Rauen, U., Petrat, F., Sustmann, R., and de Groot, H. (2004) Iron-induced mitochondrial permeability transition in cultured hepatocytes. J. Hepatol. 40, 607-615.
34. Kalman, E., Radnai, T., Palinkas, G., Hajdu, F., and Vertes, A. (1988) Hydration of iron(II) ion in aqueous-solutions. Electrochim. Acta 33, 1223-1228.
35. Virag, L., Scott, G. S., Antal-Szalmas, P., O'Connor, M., Ohshima, H., and Szabo, C. (1999) Requirement of intracellular calcium mobilization for peroxynitrite-induced poly(ADP-ribose) synthetase activation and cytotoxicity. Mol. Pharmacol. 56, 824-833.
36. Reed, G. H., Leigh, J. S., and Pearson, J. E. (1971) Electron paramagnetic relaxation and epr line shapes of manganous ion complexes in aqueous solutions - frequency and ligand dependence. J. Chem. Phys. 55, 3311-3316.
37. Langner, M., and Hui, S. W. (1993) Dithionite penetration through phospholipid -bilayers as a measure of defects in lipid molecular packing. Chem. Phys. Lipids 65, 23-30.
38. McIntyre, J. C., and Sleight, R. G. (1991) Fluorescence assay for phospholipid membrane asymmetry. Biochemistry 30, 11819-11827.
39. Zagorec, M., Buhler, J. M., Treich, I., Keng, T., Guarente, L., and Labbebois, R. (1988) Isolation, sequence, and regulation by oxygen of the yeast Hem-13 gene coding for coproporphyrinogen oxidase. J. Biol. Chem. 263, 9718-9724.
40. Camadro, J. M., Thome, F., Brouiller, N., and Labbe, P. (1994) Purification and properties of protoporphyrinogen oxidase from the yeast Saccharomyces cerevisiae - mitochondrial location and evidence for a precursor form of the protein. J. Biol. Chem. 269, 32085-32091.
41. Buisson, N., and Labbe-Bois, R. (1998) Flavohemoglobin expression and function in Saccharomyces cerevisiae - No relationship with respiration and complex response to oxidative stress. J. Biol. Chem. 273, 9527-9533.
42. Radisky, D. C., Babcock, M. C., and Kaplan, J. (1999) The yeast frataxin homologue mediates mitochondrial iron efflux - Evidence for a mitochondrial, iron cycle, J. Biol. Chem. 274, 4497-4499.
43. Crisp, R. J., Pollington, A., Galea, C., Jaron, S., Yamaguchi-Iwai, Y., and Kaplan, J. (2003) Inhibition of heme biosynthesis prevents transcription of iron uptake genes in yeast. J. Biol. Chem. 278, 45499-45506.
44. Lange, H., Kispal, G., and Lill, R. (1999) Mechanism of iron transport to the site of heme synthesis inside yeast mitochondria. J. Biol. Chem. 274, 18989-18996.
45. Boukhalfa, H., and Crumbliss, A. L. (2002) Chemical aspects of siderophore mediated iron transport. BioMetals 15, 325-339.
46. Chen, O. S., Hemenway, S., and Kaplan, J. (2002) Inhibition of Fe-S cluster biosynthesis decreases mitochondrial iron export: Evidence that Yfh1p affects Fe-S cluster synthesis. Proc. Natl. Acad. Sci. U.S.A. 99, 12321-12326.
47. Chen, O. S., and Kaplan, J. (2001) YFH1-mediated iron homeostasis is independent of mitochondrial respiration. FEBS Lett. 509, 131-134.