JBIC Journal of Biological Inorganic Chemistry

, Volume 12, Issue 7, pp 1029–1053 | Cite as

Electron paramagnetic resonance and Mössbauer spectroscopy of intact mitochondria from respiring Saccharomyces cerevisiae

  • Brandon N. Hudder
  • Jessica Garber Morales
  • Audria Stubna
  • Eckard Münck
  • Michael P. Hendrich
  • Paul A. Lindahl
Original Paper

Abstract

Mitochondria from respiring cells were isolated under anaerobic conditions. Microscopic images were largely devoid of contaminants, and samples consumed O2 in an NADH-dependent manner. Protein and metal concentrations of packed mitochondria were determined, as was the percentage of external void volume. Samples were similarly packed into electron paramagnetic resonance tubes, either in the as-isolated state or after exposure to various reagents. Analyses revealed two signals originating from species that could be removed by chelation, including rhombic Fe3+ (g = 4.3) and aqueous Mn2+ ions (g = 2.00 with Mn-based hyperfine). Three S = 5/2 signals from Fe3+ hemes were observed, probably arising from cytochrome c peroxidase and the a3:Cub site of cytochrome c oxidase. Three Fe/S-based signals were observed, with averaged g values of 1.94, 1.90 and 2.01. These probably arise, respectively, from the [Fe2S2]+ cluster of succinate dehydrogenase, the [Fe2S2]+ cluster of the Rieske protein of cytochrome bc 1, and the [Fe3S4]+ cluster of aconitase, homoaconitase or succinate dehydrogenase. Also observed was a low-intensity isotropic g = 2.00 signal arising from organic-based radicals, and a broad signal with g ave = 2.02. Mössbauer spectra of intact mitochondria were dominated by signals from Fe4S4 clusters (60–85% of Fe). The major feature in as-isolated samples, and in samples treated with ethylenebis(oxyethylenenitrilo)tetraacetic acid, dithionite or O2, was a quadrupole doublet with ΔE Q = 1.15 mm/s and δ = 0.45 mm/s, assigned to [Fe4S4]2+ clusters. Substantial high-spin non-heme Fe2+ (up to 20%) and Fe3+ (up to 15%) species were observed. The distribution of Fe was qualitatively similar to that suggested by the mitochondrial proteome.

Keywords

Iron Sulfur Cluster assembly Heme biosynthesis Non-heme 

Abbreviations

CoQ

Coenzyme Q

DTT

Dithiothreitol

EDTA

Ethylenediaminetetraacetic acid

EGTA

Ethylenebis(oxyethylenenitrilo)tetraacetic acid

EPR

Electron paramagnetic resonance

ETF

Electron transfer flavoprotein

HEPES

N-(2-Hydroxyethyl)piperazine-N′-ethanesulfonic acid

IM

Inner membrane

IMS

Intermembrane space

NHE

Normal hydrogen electrode

OM

Outer membrane

SH buffer

0.6 M sorbitol/20 mM N-(2-hydroxyethyl)piperazine-N′-ethanesulfonic acid buffer pH 7.4

SP buffer

1.2 M sorbitol/20 mM potassium phosphate buffer pH 7.4

Notes

Acknowledgements

We thank the following people: Art Johnson and Holly Cargill (Department of Biochemistry and Biophysics, Texas A&M University) for instructions on isolating mitochondria; Rola Barhoumi (Image Analysis Laboratory, Texas A&M University) and Anne Ellis (Microscopy and Imaging Center, Texas A&M University) for collecting microscopic images; Jinny Johnson (Protein Chemistry Laboratory, Texas A&M University) for performing amino acid analyses; David P. Giedroc (Department of Biochemistry and Biophysics, Texas A&M University) for access to his atomic absorption spectrophotometer; William James (Department of Chemistry, Texas A&M University) for training on and assistance with the inductively coupled plasma mass spectrometer; Shelly Henderson Possi for help in isolating some batches and in measuring O2 consumption; Tanner Freeman for preparing one of the EPR samples; and Roland Lill for helpful discussion.

This study was supported by the Robert A. Welch Foundation (A1170) and The National Institutes of Health [GM077387 (M.P.H.), EB001475 (E.M.) and The Chemistry Biology Interface training program (B.N.H. and J.G)].

Supplementary material

References

  1. 1.
    Lemire BD, Oyedotun KS (2002) Biochim Biophys Acta Bioenerg 1553:102–116CrossRefGoogle Scholar
  2. 2.
    Beinert H (2002) Biochim Biophys Acta Bioenerg 1553:7–22CrossRefGoogle Scholar
  3. 3.
    Maguire JJ, Johnson MK, Morningstar JE, Ackrell BAC, Kearney EB (1985) J Biol Chem 260:10909–10912PubMedGoogle Scholar
  4. 4.
    Fee JA, Findling KL, Yoshida T, Hille R, Tarr GE, Hearshen DO, Dunham WR, Day EP, Kent TA, Münck E (1984) J Biol Chem 259:124–133PubMedGoogle Scholar
  5. 5.
    Emptage MH, Kent TA, Kennedy MC, Beinert H, Munck E (1983) Proc Natl Acad Sci USA 80:4674–4678PubMedCrossRefGoogle Scholar
  6. 6.
    Wallace MA, Liou LL, Martins J, Clement MHS, Bailey S, Longo VD, Valentine JS, Gralla EB (2004) J Biol Chem 279:32055–32062PubMedCrossRefGoogle Scholar
  7. 7.
    Barros MH, Nobrega FG (1999) Gene 233:197–203PubMedCrossRefGoogle Scholar
  8. 8.
    Schiffler B, Bureik M, Reinle W, Muller EC, Hannemann F, Bernhardt R (2004) J Inorg Biochem 98:1229–1237PubMedCrossRefGoogle Scholar
  9. 9.
    Xia B, Cheng H, Bandarian V, Reed GH, Markley JL (1996) Biochemistry 35:9488–9495PubMedCrossRefGoogle Scholar
  10. 10.
    Mitou G, Higgins C, Wittung-Stafshede P, Conover RC, Smith AD, Johnson MK, Gaillard J, Stubna A, Münck E, Meyer J (2003) Biochemistry 42:1354–1364PubMedCrossRefGoogle Scholar
  11. 11.
    Zhang S, Sanyal I, Bulboaca GH, Rich A, Flint DH (1994) Arch Biochem Biophys 309:29–35PubMedCrossRefGoogle Scholar
  12. 12.
    Berkovitch F, Nicolet Y, Wan JT, Jarrett JT, Drennan CL (2004) Science 303:76–79PubMedCrossRefGoogle Scholar
  13. 13.
    Cosper MM, Jameson GNL, Eidsness MK, Huynh BH, Johnson MK (2002) FEBS Lett 529:332–336PubMedCrossRefGoogle Scholar
  14. 14.
    Jameson GN, Cosper MM, Hernandez HL, Johnson MK, Huynh BH (2004) Biochemistry 43:2022–2031PubMedCrossRefGoogle Scholar
  15. 15.
    Hewitson KS, Ollagnier-de Choudens S, Sanakis Y, Shaw NM, Baldwin JE, Münck E, Roach PL, Fontecave M (2002) J Biol Inorg Chem 7:83–93PubMedCrossRefGoogle Scholar
  16. 16.
    Kriek M, Peters L, Takahashi Y, Roach PL (2002) Protein Expr Purif 28:241–245CrossRefGoogle Scholar
  17. 17.
    Miller JR, Busby RW, Jordan SW, Cheek J, Henshaw TF, Ashley GW, Broderick JB, Cronan JE, Marletta MA (2000) Biochemistry 39:15166–15178PubMedCrossRefGoogle Scholar
  18. 18.
    Ollagnier-de Choudens S, Sanakis Y, Hewitson KS, Roach P, Baldwin JE, Münck E, Fontecave M (2000) Biochemistry 39:4165–4173PubMedCrossRefGoogle Scholar
  19. 19.
    Velasco JA, Cansado J, Pena MC, Kawakami T, Laborda J (1993) Gene 137:179–185PubMedCrossRefGoogle Scholar
  20. 20.
    Flint DH, Emptage MH, Finnegan MG, Fu WG, Johnson MK (1993) J Biol Chem 268:14732–14742PubMedGoogle Scholar
  21. 21.
    Mühlenhoff U, Gerber J, Richhardt N, Lill R (2003) EMBO J 22:4815–4825PubMedCrossRefGoogle Scholar
  22. 22.
    Schilke B, Voisine C, Beinert H, Craig E (1999) Proc Natl Acad Sci USA 96:10206–10211PubMedCrossRefGoogle Scholar
  23. 23.
    Jensen LT, Culotta VC (2000) Mol Cell Biol 20:3918–3927PubMedCrossRefGoogle Scholar
  24. 24.
    Tong WH, Jameson GNL, Huynh BH, Rouault TA (2003) Proc Natl Acad Sci USA 100:9762–9767PubMedCrossRefGoogle Scholar
  25. 25.
    Ruzicka FJ, Beinert H (1975) Biochem Biophys Res Comm 66:622–631PubMedCrossRefGoogle Scholar
  26. 26.
    Ruzicka FJ, Beinert H (1975) J Biol Chem 252:8440–8445Google Scholar
  27. 27.
    Paulsen KE, Orville AM, Frerman FE, Lipscomb JD, Stankovich MT (1992) Biochemistry 31:11755–11761PubMedCrossRefGoogle Scholar
  28. 28.
    Hunte C, Koepke J, Lange C, Rossmanith T, Michel H (2000) Structure 8:669–684PubMedCrossRefGoogle Scholar
  29. 29.
    Bonagura CA, Bhaskar B, Shimizu H, Li HY, Sundaramoorthy M, McRee DE, Goodin DB, Poulos TL (2003) Biochemistry 42:5600–5608PubMedCrossRefGoogle Scholar
  30. 30.
    Mowat CG, Miles CS, Munro AW, Cheesman MR, Quaroni LG, Reid GA, Chapman SK (2000) J Biol Inorg Chem 5:584–592PubMedCrossRefGoogle Scholar
  31. 31.
    Kojima N, Palmer G (1983) J Biol Chem 258:4908–4913Google Scholar
  32. 32.
    Brautigan DL, Feinberg BA, Hoffman BM, Margoliash E, Peisach J, Bumberg WE (1977) J Biol Chem 252:574–582PubMedGoogle Scholar
  33. 33.
    Barros MH, Carlson CG, Glerum DM, Tzagoloff A (2001) FEBS Lett 492:133–138PubMedCrossRefGoogle Scholar
  34. 34.
    Hederstedt L, Lewin A, Throne-Holst M (2005) J Bacteriol 187:8361–8369PubMedCrossRefGoogle Scholar
  35. 35.
    Glerum DM, Muroff I, Jin C, Tzagoloff A (1997) J Biol Chem 272:19088–19094PubMedCrossRefGoogle Scholar
  36. 36.
    Bureik M, Schiffler B, Hiraoka Y, Vogel F, Bernhardt R (2002) Biochemistry 41:2311–2321PubMedCrossRefGoogle Scholar
  37. 37.
    Petrova VY, Drescher D, Kujumdzieva AV, Schmitt MJ (2004) Biochem J 380:393–400PubMedCrossRefGoogle Scholar
  38. 38.
    Ding H, Harrison K, Lu J (2005) J Biol Chem 280:30432–30437PubMedCrossRefGoogle Scholar
  39. 39.
    Lesuisse E, Santos R, Matzanke BF, Knight SAB, Camadro JM, Dancis A (2003) Hum Mol Genet 12:879–889PubMedCrossRefGoogle Scholar
  40. 40.
    Sellers VM, Wu CK, Dailey TA, Dailey HA (2001) Biochemistry 40:9821–9827PubMedCrossRefGoogle Scholar
  41. 41.
    Ferreira GC, Franco R, Mangravita A, George GN (2002) Biochemistry 41:4809–4818PubMedCrossRefGoogle Scholar
  42. 42.
    Wu CK, Dailey HA, Rose JP, Burden A, Sellers VM, Wang BC (2001) Nat Struct Biol 8:156–160PubMedCrossRefGoogle Scholar
  43. 43.
    Foury F, Roganti T (2002) J Biol Chem 277:24475–24483PubMedCrossRefGoogle Scholar
  44. 44.
    Li LT, Kaplan J (1997) J Biol Chem 272:28485–28493PubMedCrossRefGoogle Scholar
  45. 45.
    Moraes CT, Diaz F, Barrientos A (2004) Biochim Biophys Acta Bioenerg 1659:153–159CrossRefGoogle Scholar
  46. 46.
    Dumont ME, Cardillo TS, Hayes MK, Sherman F (1991) Mol Cell Biol 11:5487–5496PubMedGoogle Scholar
  47. 47.
    Chloupkova M, LeBard LS, Koeller DM (2003) J Mol Biol 331:155–165PubMedCrossRefGoogle Scholar
  48. 48.
    Lill R, Kispal G (2001) Res Microbiol 152:331–340PubMedCrossRefGoogle Scholar
  49. 49.
    Lange H, Lisowsky T, Gerber J, Mühlenhoff U, Kispal G, Lill R (2001) EMBO Rep 2:715–720PubMedCrossRefGoogle Scholar
  50. 50.
    Stenmark P, Grünler J, Mattsson J, Sindelar PJ, Nordlund P, Berthold DA (2001) J Biol Chem 276:33297–33300PubMedCrossRefGoogle Scholar
  51. 51.
    Berthold DA, Voevodskaya N, Stenmark P, Gräslund A, Nordlund P (2002) J Biol Chem 277:43608–43614PubMedCrossRefGoogle Scholar
  52. 52.
    Neese F, Zumft WG, Antholine WE, Kroneck PMH (1996) J Am Chem Soc 118:8692–8699CrossRefGoogle Scholar
  53. 53.
    Barros MH, Johnson A, Tzagoloff A (2004) J Biol Chem 279:49883–49888PubMedCrossRefGoogle Scholar
  54. 54.
    Palumaa P, Kangur L, Voronova A, Sillard R (2004) Biochem J 382:307–314PubMedCrossRefGoogle Scholar
  55. 55.
    Hiser L, Di Valentin M, Hamer AG, Hosler JP (2000) J Biol Chem 275:619–623PubMedCrossRefGoogle Scholar
  56. 56.
    Sturtz LA, Diekert K, Jensen LT, Lill R, Culotta VC (2001) J Biol Chem 276:38084–38089PubMedGoogle Scholar
  57. 57.
    Cobine PA, Ojeda LD, Rigby KM, Winge DR (2004) J Biol Chem 279:14447–14455PubMedCrossRefGoogle Scholar
  58. 58.
    Luk E, Jensen LT, Culotta VC (2003) J Biol Inorg Chem 8:803–809PubMedCrossRefGoogle Scholar
  59. 59.
    Hirabaya T, Harada T (1971) Biochem Biophys Res Commun 45:1369CrossRefGoogle Scholar
  60. 60.
    Sharp RE, White P, Chapman SK, Reid GA (1994) Biochemistry 33:5115–5120PubMedCrossRefGoogle Scholar
  61. 61.
    Arscott LD, Gromer S, Schirmer RH, Becker K, Williams CH (1997) Proc Natl Acad Sci USA 94:3621–3626PubMedCrossRefGoogle Scholar
  62. 62.
    Staples CR, Ameyibor E, Fu WG, Gardet-Salvi L, Stritt-Etter EL, Knaff DB, Johnson MK (1996) Biochemistry 35:11425–11434PubMedCrossRefGoogle Scholar
  63. 63.
    Garrib A, McMurray WC (1986) J Biol Chem 261:8042–8048PubMedGoogle Scholar
  64. 64.
    Huh WK, Kim ST, Yang KS, Seok YJ, Hah YC, Kang SO (1994) Eur J Biochem 225:1073–1079PubMedCrossRefGoogle Scholar
  65. 65.
    Joo HS, Kim SS (1998) J Biochem Mol Biol 31:37–43Google Scholar
  66. 66.
    Shan XY, Wang LQ, Hoffmaster R, Kruger WD (1999) J Biol Chem 274:32613–32618PubMedCrossRefGoogle Scholar
  67. 67.
    Robinson KM, Lemire BD (1996) J Biol Chem 271:4061–4067PubMedCrossRefGoogle Scholar
  68. 68.
    Gin P, Hsu AY, Rothman SC, Jonassen T, Lee PT, Tzagoloff A, Clarke CF (2003) J Biol Chem 278:25308–25316PubMedCrossRefGoogle Scholar
  69. 69.
    Oxelmark E, Marchini A, Malanchi I, Magherini F, Jaquet L, Hajibagheri MAN, Blight KJ, Jauniaux JC, Tommasino M (2000) Mol Cell Biol 20:7784–7797PubMedCrossRefGoogle Scholar
  70. 70.
    Sands RH, Beinert H (1960) Biochem Biophys Res Commun 3:47–52CrossRefGoogle Scholar
  71. 71.
    Hartzell CR, Beinert H (1974) Biochim Biophys Acta 368:318–338PubMedCrossRefGoogle Scholar
  72. 72.
    Bulteau AL, Ikeda-Saito M, Szweda LI (2003) Biochemistry 42:14846–14855PubMedCrossRefGoogle Scholar
  73. 73.
    Lin CIP, Ohnishi T, Clejan L, Beattie DS (1983) Eur J Biochem 137:179–183PubMedCrossRefGoogle Scholar
  74. 74.
    Phillips JD, Graham LA, Trumpower BL (1993) J Biol Chem 268:11727–11736PubMedGoogle Scholar
  75. 75.
    Merbitz-Zahradnik T, Zwicker K, Nett JH, Link TA, Trumpower BL (2003) Biochemistry 42:13637–13645PubMedCrossRefGoogle Scholar
  76. 76.
    Shergill JK, Cammack R (1994) Biochim Biophys Acta 1185:43–49PubMedCrossRefGoogle Scholar
  77. 77.
    Shergill JK, Cammack R, Chen JH, Fisher MJ, Madden S, Rees HH (1995) Biochem J 307:719–728PubMedGoogle Scholar
  78. 78.
    Albract SPJ, Subramanian J (1977) Biochim Biophys Acta 462:36–48CrossRefGoogle Scholar
  79. 79.
    Gavin CE, Gunter KK, Gunter TE (1999) Neurotoxicology 20:445–453PubMedGoogle Scholar
  80. 80.
    Guldutuna S, Zimmer G, Leuschner M, Bhatti S, Elze A, Beisinger B, Hofmann M, Leuschner U (1999) Biochim Biophys Acta 1453:396–406PubMedGoogle Scholar
  81. 81.
    Tuckey RC, McKinley AJ, Headlam MJ (2001) Eur J Biochem 268:2338–2343PubMedCrossRefGoogle Scholar
  82. 82.
    Albracht SPJ, Leeuwerik FJ, VanSwol B (1979) FEBS Lett 104:197–200PubMedCrossRefGoogle Scholar
  83. 83.
    Albracht SPJ (1980) Biochim Biophys Acta 612:11–28PubMedGoogle Scholar
  84. 84.
    Albracht SPJ, VanVerseveld HW, Hagen WR, Kalkman ML (1980) Biochim Biophys Acta 593:173–186PubMedCrossRefGoogle Scholar
  85. 85.
    Diekert K, de Kroon AIPM, Kispal G, Lill R (2000) In: Pon LA, Schon EA (eds) Methods in yeast genetics, vol 65. Academic, San DiegoGoogle Scholar
  86. 86.
    Cleland WW (1964) Biochemistry 3:480PubMedCrossRefGoogle Scholar
  87. 87.
    Barondeau DP, Roberts LM, Lindahl PA (1994) J Am Chem Soc 116:3442–3448CrossRefGoogle Scholar
  88. 88.
    Wright R (2000) Microsc Res Tech 51:496–510PubMedCrossRefGoogle Scholar
  89. 89.
    Pelley JW, Garner CW, Little GH (1978) Anal Biochem 86:341–343PubMedCrossRefGoogle Scholar
  90. 90.
    Toyoshima S, Wantanabe F, Saido H, Miyatake K, Nakano Y (1995) J Nutr 125:2846–2850PubMedGoogle Scholar
  91. 91.
    Sapan CV, Lundlad RL, Price NC (1999) Biotechnol Appl Biochem 29:99–108PubMedGoogle Scholar
  92. 92.
    Dineley KE, Richards LL, Votyakova TV, Reynolds IJ (2005) Mitochondria 5:55–65CrossRefGoogle Scholar
  93. 93.
    Lund P, Wiggins D (1990) Biochim Biophys Acta 1018:98–102PubMedCrossRefGoogle Scholar
  94. 94.
    Hackenbrock CR (1968) J Cell Biol 37:345–369PubMedCrossRefGoogle Scholar
  95. 95.
    Zischka H, Weber G, Weber PJA, Posch A, Braun RJ, Bühringer D, Schneider U, Nissum M, Meitinger T, Ueffing M, Eckerskorn C (2003) Proteomics 3:906–916PubMedCrossRefGoogle Scholar
  96. 96.
    Shaw JM, Nunnari J (2002) Trends Cell Biol 12:178–184PubMedCrossRefGoogle Scholar
  97. 97.
    Egner A, Jakobs S, Hell SW (2002) Proc Natl Acad Sci USA 99:3370–3375PubMedCrossRefGoogle Scholar
  98. 98.
    Polcic P, Sabova L, Kolarov J (1997) FEBS Lett 412:207–210PubMedCrossRefGoogle Scholar
  99. 99.
    Soubannier V, Vaillier J, Paumard P. Coulary B, Schaeffer J, Velours J (2002) J Biol Chem 277:10739–10745PubMedCrossRefGoogle Scholar
  100. 100.
    Boyle GM, Roucou X, Nagley P, Devenish RJ, Prescott M (1999) Eur J Biochem 262:315–323PubMedCrossRefGoogle Scholar
  101. 101.
    Wickman HH, Klein MP, Shirley DA (1964) Phys Rev 152:345–357CrossRefGoogle Scholar
  102. 102.
    Mayhew SG (1978) Eur J Biochem 85:535–547PubMedCrossRefGoogle Scholar
  103. 103.
    Lindahl PA, Day EP, Kent TA, Orme-Johnson WH, Münck E (1985) J Biol Chem 260:1160–1173Google Scholar
  104. 104.
    Andrew CR, Kemper LJ, Busche TL, Tiwari AM, Kecskes MC, Stafford JM, Croft LC, Lu S, Moenne-Loccoz P, Huston W, Moir JWB, Eady RR (2005) Biochemistry 44:8664–8672PubMedCrossRefGoogle Scholar
  105. 105.
    Miyoshi H, Tokutake N, Imaeda Y, Akagi T, Iwamura H (1995) Biochim Biophys Acta 1229:149–154PubMedCrossRefGoogle Scholar
  106. 106.
    Babcock M, deSilva D, Oaks R, DavisKaplan S, Jiralerspong S, Montermini L, Pandolfo M, Kaplan J (1997) Science 276:1709–1712PubMedCrossRefGoogle Scholar
  107. 107.
    Foury F, Cazzalini O (1997) FEBS Lett 411:373–377PubMedCrossRefGoogle Scholar
  108. 108.
    Tangeras A, Flatmark T, Backstrom D, Ehrenberg A (1980) Biochim Biophys Acta 589:162–175PubMedCrossRefGoogle Scholar
  109. 109.
    Kispal G, Csere P, Prohl C, Lill R (1999) EMBO J 18:3981–3989PubMedCrossRefGoogle Scholar
  110. 110.
    Petrat F, de Groot H, Rauen U (2001) Biochem J 356:61–69PubMedCrossRefGoogle Scholar
  111. 111.
    Petrat F, Weisheit D, Lensen M, de Groot H, Sustmann R, Rauen U (2002) Biochem J 362:137–147PubMedCrossRefGoogle Scholar
  112. 112.
    Sturm B, Bistrich U, Schranzhofer M, Sarsero JP, Rauen U, Scheiber-Mojdehkar B, de Groot H, Ioannou P, Petrat F (2005) J Biol Chem 280:6701–6708PubMedCrossRefGoogle Scholar
  113. 113.
    Lange H, Kispal G, Lill R (1999) J Biol Chem 274:18989–18996Google Scholar
  114. 114.
    Agar JN, Krebs C, Frazzon J, Huynh BH, Dean DR, Johnson MK (2000) Biochemistry 39:7856–7862PubMedCrossRefGoogle Scholar
  115. 115.
    Franco R, Moura JJG, Moura I, Huynh BH, Forbes WS, Ferreira GC (1995) J Biol Chem 270:26352–26357PubMedCrossRefGoogle Scholar
  116. 116.
    Haile DJ, Rouault TA, Harford JB, Kennedy MC, Blondin GA, Beinert H, Klausner RD (1992) Proc Natl Acad Sci USA 89:11735–11739PubMedCrossRefGoogle Scholar
  117. 117.
    Henze K, Martin W (2003) Nature 426:127–128PubMedCrossRefGoogle Scholar
  118. 118.
    Mühlenhoff U, Lill R (2000) Biochim Biophys Acta Bioenerg 1459:370–382CrossRefGoogle Scholar
  119. 119.
    Kilpatrick LK, Kennedy MC, Beinert H, Czernuszewicz RC, Qiu D, Spiro TG (1994) J Am Chem Soc 116:4053–4061CrossRefGoogle Scholar
  120. 120.
    Jackson TA, Karapetian A, Miller AF, Brunold TC (2004) J Am Chem Soc 126:12477–12491PubMedCrossRefGoogle Scholar
  121. 121.
    Un S, Tabares LC, Cortez N, Hiraoka BY, Yamakura F (2004) J Am Chem Soc 126:2720–2726PubMedCrossRefGoogle Scholar
  122. 122.
    Srinivasan C, Liba A, Imlay JA, Valentine JS, Gralla EB (2000) J Biol Chem 275:29187–29192PubMedCrossRefGoogle Scholar
  123. 123.
    Werth MT, Sices H, Cecchini G, Schroder I, Lasage S, Gunsalus RP, Johnson MK (1992) FEBS Lett 299:1–4PubMedCrossRefGoogle Scholar
  124. 124.
    Hirst J, Sucheta A, Ackrell BAC, Armstrong FA (1996) J Am Chem Soc 118:5031–5038CrossRefGoogle Scholar
  125. 125.
    Sucheta A, Ackrell BAC, Cochran B, Armstrong FA (1992) Nature 356:361–362PubMedCrossRefGoogle Scholar
  126. 126.
    Link TA, Hagen WR, Pierik AJ, Assmann C, von Jagow G (1992) Eur J Biochem 208:685–691PubMedCrossRefGoogle Scholar
  127. 127.
    Beinert H, Shaw RW (1977) Biochim Biophys Acta 462:121–130PubMedCrossRefGoogle Scholar
  128. 128.
    Aasa R, Albracht SPJ, Falk KE, Lanne B, Vanngard T (1976) Biochim Biophys Acta 422:260–272PubMedGoogle Scholar
  129. 129.
    Gorbikova EA, Vuorilehto K, Wikstrom M, Verkhovsky MI (2006) Biochemistry 45:5641–5649PubMedCrossRefGoogle Scholar
  130. 130.
    Nicholls P, Elliott WB (1974) In: Worwood M, Jacobs A (eds) Iron in biochemistry and medicine. Academic, New YorkGoogle Scholar
  131. 131.
    Wittenberg BA, Kampa L, Wittenberg JB, Blumberg WE, Peisach J (1968) J Biol Chem 243:1863–1870PubMedGoogle Scholar
  132. 132.
    Coulson AFW, Erman JE, Yonetani T (1971) J Biol Chem 246:917–924PubMedGoogle Scholar
  133. 133.
    Goodin DB, McRee DE (1993) Biochemistry 32:3313–3324PubMedCrossRefGoogle Scholar
  134. 134.
    Bellei M, Jakopitsch C, Battistuzzi G, Sola M, Obinger C (2006) Biochemistry 45:4768–4774PubMedCrossRefGoogle Scholar
  135. 135.
    Cassanova N, O’Brien KM, Stahl BT, McClure T, Poyton RO (2005) J Biol Chem 280:7645–7653PubMedCrossRefGoogle Scholar
  136. 136.
    Reynolds MF, Shelver D, Kerby RL, Parks RB, Roberts GP, Burstyn JN (1998) J Am Chem Soc 120:9080–9081CrossRefGoogle Scholar
  137. 137.
    Lett CM, Guillemette JG (2002) Biochem J 362:281–287PubMedCrossRefGoogle Scholar
  138. 138.
    Yu L, Dong J-H, Yu C-A (1986) Biochim Biophys Acta Bioenerg 852:203–211CrossRefGoogle Scholar
  139. 139.
    Tegoni M, Silvestrini MC, Guigliarelli B, Asso M, Brunori M, Bertrand P (1998) Biochemistry 37:12761–12771PubMedCrossRefGoogle Scholar
  140. 140.
    Anemüller S, Bill E, Schäfer G, Trautwein A, Teixeira M (1992) Eur J Biochem 210:133–138PubMedCrossRefGoogle Scholar
  141. 141.
    Lester RL, Crane FL (1959) J Biol Chem 234:2169–2175PubMedGoogle Scholar
  142. 142.
    Waldeck AR, Stowell MHB, Lee HK, Hung SC, Matsson M, Hederstedt L, Ackrell BAC, Chan SI (1997) J Biol Chem 272:19373–19382PubMedCrossRefGoogle Scholar
  143. 143.
    Lukoyanov D, Berry SM, Lu Y, Antholine WE, Scholes CP (2002) Biophys J 82:2758–2766PubMedCrossRefGoogle Scholar
  144. 144.
    Gamelin DR, Randall DW, Hay MT, Houser RP, Mulder TC, Canters GW, de Vries S, Tolman WB, Lu Y, Solomon EI (1998) J Am Chem Soc 120:5246–5263CrossRefGoogle Scholar
  145. 145.
    Nittis T, George GN, Winge DR (2001) J Biol Chem 276:42520–42526PubMedCrossRefGoogle Scholar
  146. 146.
    Heaton DN, George GN, Garrison G, Winge DR (2001) Biochemistry 40:743–751PubMedCrossRefGoogle Scholar
  147. 147.
    Ludovico P, Sansonetty F, Corte-Real M (2001) Microbiology 147:3335–3343PubMedGoogle Scholar
  148. 148.
    Sickmann A, Reinders J, Wagner Y, Joppich C, Zahedi R, Meyer HE, Schonfisch B, Perschil I, Chacinska A, Guiard B et al (2003) Proc Natl Acad Sci USA 100:13207–13212PubMedCrossRefGoogle Scholar
  149. 149.
    Huh W-K, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O’Shea EK (2003) Nature 425:686–691PubMedCrossRefGoogle Scholar
  150. 150.
    Prokisch H, Scharfe C, Camp DG, Xiao WZ, David L, Andreoli C, Monroe ME, Moore RJ, Gritsenko MA, Kozany C, Hixson KK, Mottaz HM, Zischka H, Ueffing M, Herman ZS, Davis RW, Meitinger T, Oefner PJ, Smith RD, Steinmetz LM (2004) PLoS Biol 2:795–804CrossRefGoogle Scholar
  151. 151.
    Forster J, Famili I, Fu P, Palsson BO, Nielsen J (2003) Genome Res 13(2):244–253PubMedCrossRefGoogle Scholar
  152. 152.
    Ohlmeier S, Kastaniotis AJ, Hiltunen JK, Bergmann U (2004) J Biol Chem 6:3956–3979Google Scholar
  153. 153.
    Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O’Shea EK, Weissman JS (2003) Nature 425:737–741PubMedCrossRefGoogle Scholar
  154. 154.
    Biswas SK, Yamaguchi M, Naoe N, Takashima T, Takeo K (2003) J Electron Microsc 52:133–143CrossRefGoogle Scholar
  155. 155.
    Trumpower B (1990) J Biol Chem 265:11409–11412PubMedGoogle Scholar
  156. 156.
    Murphy MEP, Nall BT, Brayer GD (1992) J Mol Biol 227:160–176PubMedCrossRefGoogle Scholar
  157. 157.
    Daum G et al (1982) J Biol Chem 257:13028–13033PubMedGoogle Scholar
  158. 158.
    Goodin DB, Davidson MG, Roe JA, Mauk AG, Smith M (1991) Biochemistry 30:4953–4962PubMedCrossRefGoogle Scholar
  159. 159.
    Capeillereblandin G, Bray RC, Iwatsubo M, Labeyrie F (1975) Eur J Biochem 54:549–566CrossRefGoogle Scholar
  160. 160.
    Ebert CE, Ghosh M, Wang YD, Beattie DS (2003) Biochim Biophys Acta 1607:65–78PubMedCrossRefGoogle Scholar
  161. 161.
    Orme-Johnson NR, Hansen RE, Beinert H (1971) Biochem Biophys Res Commun 45:871PubMedCrossRefGoogle Scholar
  162. 162.
    Salerno JC (1984) J Biol Chem 259:2331–2336PubMedGoogle Scholar
  163. 163.
    Svensson-Ek M, Abramson J, Larsson G, Tornroth S, Brzezinski P, Iwata S (2002) J Mol Biol 321(2):329–339PubMedCrossRefGoogle Scholar
  164. 164.
    Babcock GT, Vickery LE, Palmer G (1978) J Biol Chem 253:2400–2411PubMedGoogle Scholar
  165. 165.
    Cheesman MR, Oganesyan VS, Watmough NJ, Butler CS, Thomson AJ (2004) J Am Chem Soc 126:4157–4166PubMedCrossRefGoogle Scholar
  166. 166.
    Beinert H, Ackrell BAC, Kearney EB, Singer TP (1974) Biochem Biophys Res Commun 58:564–572PubMedCrossRefGoogle Scholar
  167. 167.
    Peterson J, Vibat C, Gennis RB (1994) FEBS Lett 355:155–156PubMedCrossRefGoogle Scholar
  168. 168.
    Svensson B, Andersson KK, Hederstedt L (1996) Eur J Biochem 238:287–295PubMedCrossRefGoogle Scholar
  169. 169.
    Jonassen T, Proft M, Randez-Gil F, Schultz JR, Marbois BN, Entian KD, Clarke CF (1998) J Biol Chem 273:3351–3357PubMedCrossRefGoogle Scholar
  170. 170.
    Rea S (2001) FEBS Lett 509:389–394PubMedCrossRefGoogle Scholar
  171. 171.
    Liu KE, Lippard SJ (1991) J Biol Chem 266:12836–12839PubMedGoogle Scholar
  172. 172.
    Fox BG, Hendrich MP, Surerus KK, Anderson KK, Froland WA, Lipscomb JD, Münck E (1993) J Am Chem Soc 115:3688–3701CrossRefGoogle Scholar
  173. 173.
    Regev-Rudzki N, Karniely S, Ben-Haim NN, Pines O (2005) Mol Biol Cell 16:4163–4171PubMedCrossRefGoogle Scholar
  174. 174.
    Tong JJ, Feinberg BA (1994) J Biol Chem 269:24920–24927PubMedGoogle Scholar
  175. 175.
    Smith AD, Jameson GNL, Dos Santos PC, Agar JN, Naik S, Krebs C, Frazzon J, Dean DR, Huynh BH, Johnson MK (2005) Biochemistry 44:12955–12969PubMedCrossRefGoogle Scholar
  176. 176.
    Pelzer W, Muhlenhoff U, Diekert K, Siegmund K, Kispal G, Lill R (2000) FEBS Lett 476:134–139PubMedCrossRefGoogle Scholar
  177. 177.
    Picciocchi A, Douce R, Alban C (2003) J Biol Chem 278:24966–24975PubMedCrossRefGoogle Scholar
  178. 178.
    Ugulava NB, Gibney BR, Jarrett JT (2001) Biochemistry 40:8343–8351PubMedCrossRefGoogle Scholar
  179. 179.
    Duin EC, Lafferty ME, Crouse BR, Allen RM, Sanyal I, Flint DH, Johnson MK (1997) Biochemistry 36:11811–11820PubMedCrossRefGoogle Scholar
  180. 180.
    Hoja U, Marthol S, Hofmann J, Stegner S, Schulz R, Meier S, Greiner E, Schweizer E (2004) J Biol Chem 279:21779–21786PubMedCrossRefGoogle Scholar
  181. 181.
    Ollagnier-de Choudens S, Fontecave M (1999) FEBS Lett 453:25–28PubMedCrossRefGoogle Scholar
  182. 182.
    Cosper MM, Jameson GNL, Hernandez HL, Krebs C, Huynh BH, Johnson MK (2004) Biochemistry 43:2007–2021PubMedCrossRefGoogle Scholar
  183. 183.
    Branda SS, Cavadini P, Adamec J, Kalousek F, Taroni F, Isaya G (1999) J Biol Chem 274:22763–22769PubMedCrossRefGoogle Scholar
  184. 184.
    He YN, Alam SL, Proteasa SV, Zhang Y, Lesuisse E, Dancis A, Stemmler TL (2004) Biochemistry 43:16254–16262PubMedCrossRefGoogle Scholar
  185. 185.
    Bou-Abdallah F, Adinolfi S, Pastore A, Laue TM, Chasteen ND (2004) J Mol Biol 341:605–615PubMedCrossRefGoogle Scholar
  186. 186.
    Dawson JH, Bracete AM, Huff AM, Kadkhodayan S, Zeitler CM, Sono M, Chang CK, Loewen PC (1991) FEBS Lett 295:123–126PubMedCrossRefGoogle Scholar
  187. 187.
    Ioannidis N, Cooper CE, Poole RK (1992) Biochem J 288:649–655PubMedGoogle Scholar
  188. 188.
    Macheroux P, Hill S, Austin S, Eydmann T, Jones T, Kim SO, Poole R, Dixon R (1998) Biochem J 332:413–419PubMedGoogle Scholar

Copyright information

© SBIC 2007

Authors and Affiliations

  • Brandon N. Hudder
    • 1
  • Jessica Garber Morales
    • 1
  • Audria Stubna
    • 2
  • Eckard Münck
    • 2
  • Michael P. Hendrich
    • 2
  • Paul A. Lindahl
    • 1
    • 3
  1. 1.Department of ChemistryTexas A&M UniversityCollege StationUSA
  2. 2.Department of ChemistryCarnegie Mellon UniversityPittsburghUSA
  3. 3.Department of Biochemistry and BiophysicsTexas A&M UniversityCollege StationUSA

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