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Heme-copper/dioxygen adduct formation relevant to cytochrome c oxidase: spectroscopic characterization of [(6L)FeIII-(O22−)-CuII]+

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Abstract

In the further development and understanding of heme-copper dioxygen reactivity relevant to cytochrome c oxidase O2-reduction chemistry, we describe a high-spin, five-coordinate dioxygen (peroxo) adduct of an iron(II)-copper(I) complex, [(6L)FeIICuI](BArF20) (1), where 6L is a tetraarylporphyrinate with a tethered tris(2-pyridylmethyl)amine chelate for copper. Reaction of 1 with O2 in MeCN affords a remarkably stable [t1/2 (rt; MeCN)≈60 min] adduct, [(6L)FeIII-(O22-)-CuII]+ (2) [EPR silent; λmax=418 (Soret), 561 nm], formulated as a peroxo complex based on manometry (1:O2=1:1; spectrophotometric titration, −40 °C, MeCN), mass spectrometry {MALDI-TOF-MS: 16O2, m/z 1191 ([(6L)FeIII-(16O22−)-CuII]+); 18O2, m/z 1195}, and resonance Raman spectroscopy (ν(O-O)=788 cm–1; Δ16O2/18O2=44 cm–1; Δ16O2/16/18O2=22 cm–1). 1H and 2H NMR spectroscopy (−40 °C, MeCN) reveals that 2 is the first heme-copper peroxo complex which is high-spin, with downfield-shifted pyrrole resonances (δpyrrole=75 ppm, s, br) and upfield shifted peaks at δ= −22, −35, and −40 ppm, similar to the pattern observed for the μ-oxo complex [(6L)FeIII-O-CuII](BArF) (3) (known S=2 system, antiferromagnetically coupled high-spin FeIII and CuII). The corresponding magnetic moment measurement (Evans method, CD3CN, −40 °C) also confirms the S=2 spin state, with μB=4.9. Structural insights were obtained from X-ray absorption spectroscopy, showing Fe–O (1.83 Å) and Cu–O (1.882 Å) bonds, and an Fe...Cu distance of 3.35(2) Å, suggestive of a μ-1,2-peroxo ligand present in 2. The reaction of 2 with cobaltocene gives 3, differing from the observed full reduction seen with other heme-Cu peroxo complexes. Finally, thermal decomposition of 2 yields 3, with concomitant release of 0.5 mol O2 per mol 2, as confirmed quantitatively by an alkaline pyrogallol dioxygen scavenging solution.

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Notes

  1. Extremely minor differences exist between the two structures of complex 3. These are due to the use of different counterions and solvent systems employed for crystallization. Here, we crystallized 3 after direct reaction with dioxygen, employing the BarF20– anion [i.e., B(C6F5)4–] and an MeCN/toluene solvent system, yielding [(6L)FeIII-O-CuII][B(C6F5)4]·3toluene. Previously, 3 was formed from an acid–base assembly reaction using a THF/heptane solvent system and employing the (so-called) BArF– anion, yielding [(6L)FeIII-O-CuII][B(C8H3F6)4], with 4–8 disordered heptane molecules (and perhaps some THF) which were not located, but inferred by refinement with PLATON/SQUEEZE. That structure gave Fe–O=1.750(4), Cu–O=1.848(4), and Fe...Cu=3.586 distances (Å), and ∠Fe–O–Cu of 171.1(3)°

  2. As a general feature of MALDI-TOF mass spectrometry, the lack of peak resolution leads to the observed mass numbers being the averaged one of the cluster peaks, different from the base peak. This leads to systematic deviations in the observed peak from the calculated values. For example, an ion of the reduced form [1−BArF20]+ should give the following isotope distribution: m/z 1155 (rel int 6%), 1156 (4), 1157 (100), 1158 (76), 1159 (71), 1160 (40), 1161 (14), 1162 (2). However, we observe one unresolved peak and its peak maximum was m/z=1159. In a similar way, the 16O2 and 18O2 adducts derived from 2 should give the base peaks at m/z=1189 and 1193, respectively. However, the observed data yielded peaks at m/z=1191.5 and 1195.6, respectively. The decomposition product 3 is calculated to give m/z=1173 (16O) and 1175 (18O); observed, 1174.9 and 1177.1 The systematic differences from the calculated values by ~2 mass units could come from the lack of accuracy and peak resolution on the applied mass spectrometric measurement, and we thank a reviewer for bringing this to our attention

  3. See footnote 2

  4. ν(Fe–16OH) (Δ16O/18O) for (6L)FeIII-OH and (F8TPP)FeIII-OH are 636 cm−1 (−29) and 638 cm−1 (−29), respectively (MeCN, rt, 442 nm excitation); unpublished results

  5. The more distant O(peroxide) atom (that bound to Cu) is not resolvable in the EXAFS becasue it is a low Z scatterer and will be obscured also by 2nd shell carbons of the porphyrin ring

  6. This intermediate was ruled out when mass spectrometric analysis of the headspace gas revealed no mixed-isotope dioxygen gas was evolved upon the decomposition of a mixture of 16O2 and 18O2 μ-peroxo adducts

References

  1. Ferguson-Miller S, Babcock GT (1996) Chem Rev 96:2889–2907

    Article  CAS  PubMed  Google Scholar 

  2. Michel H, Behr J, Harrenga A, Kannt A (1998) Annu Rev Biophys Biomol Struct 27:329–356

    Article  CAS  PubMed  Google Scholar 

  3. Iwata S, Ostermeier C, Ludwig B, Michel H (1995) Nature 376:660–669

    Article  CAS  PubMed  Google Scholar 

  4. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S (1995) Science 269:1069–1074

    CAS  PubMed  Google Scholar 

  5. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S (1996) Science 272:1136–1144

    CAS  PubMed  Google Scholar 

  6. Ostermeier C, Harrenga A, Ermler U, Michel H (1997) Proc Natl Acad Sci USA 94:10547–10553

    Article  CAS  PubMed  Google Scholar 

  7. Yoshikawa S, Shinzawa-Itoh K, Nakashima R, Yaono R, Yamashita E, Inoue N, Yao M, Jei-Fei M, Libeu CP, Mizushima T, Yamaguchi H, Tomizaki T, Tsukihara T (1998) Science 280:1723–1729

    Article  CAS  PubMed  Google Scholar 

  8. Harrenga A, Michel H (1999) J Biol Chem 274:33296–33299

    Article  CAS  PubMed  Google Scholar 

  9. Soulimane T, Buse G, Bourenkov GP, Bartunik HD, Huber R, Than ME (2000) EMBO J 19:1766–1776

    Article  CAS  PubMed  Google Scholar 

  10. Abramson J, Riistama S, Larsson G, Jasaitis A, Svensson-Ek M, Laakkonen L, Puustinen A, Iwata S, Wikstrom M (2000) Nat Struct Biol 7:910–917

    Article  CAS  PubMed  Google Scholar 

  11. Svensson-Ek M, Abramson J, Larsson G, Tornroth S, Brzezinski P, Iwata S (2002) J Mol Biol 321:329–339

    Article  CAS  PubMed  Google Scholar 

  12. Babcock GT (1999) Proc Natl Acad Sci USA 96:12971–12973

    Article  CAS  PubMed  Google Scholar 

  13. Fabian M, Wong WW, Gennis RB, Palmer G (1999) Proc Natl Acad Sci USA 96:13114–13117

    Article  CAS  PubMed  Google Scholar 

  14. Proshlyakov DA, Pressler MA, Babcock GT (1998) Proc Natl Acad Sci USA 95:8020–8025

    Article  CAS  PubMed  Google Scholar 

  15. Blomberg MRA, Siegbahn PEM, Wikström M (2003) Inorg Chem 42:5231–5243

    Article  CAS  PubMed  Google Scholar 

  16. Das TK, Pecoraro C, Tomson FL, Gennis RB, Rousseau DL (1998) Biochemistry 37:14471–14476

    Article  CAS  PubMed  Google Scholar 

  17. Okeley NM, Van der Donk WA (2000) Chem Biol 7:R159–R171

    Article  CAS  PubMed  Google Scholar 

  18. Michel H (1998) Proc Natl Acad Sci USA 95:12819–12824

    Article  CAS  PubMed  Google Scholar 

  19. Zaslavsky D, Gennis RB (2000) Biochim Biophys Acta 1458:XXX–XXX

    Google Scholar 

  20. Wikström M, Verkhovsky MI (2002) Biochim Biophys Acta 1555:128–132

    PubMed  Google Scholar 

  21. Szundi I, Van Eps N, Einarsdöttir O (2003) Biochemistry 42:5074–5090

    Article  CAS  PubMed  Google Scholar 

  22. Van Eps N, Szundi I, Einarsdöttir O (2003) Biochemistry 42:5065–5073

    Article  PubMed  Google Scholar 

  23. Kitagawa T (2000) J Inorg Biochem 82:9–18

    Article  CAS  PubMed  Google Scholar 

  24. Verkhovsky MI, Jasaitis A, Verkhovskaya ML, Morgan JE, Wikström M (1999) Nature 400:480–483

    Article  CAS  PubMed  Google Scholar 

  25. Kim E, Chufan EE, Kamaraj K, Karlin KD (2004) Chem Rev 104:1077–1133

    Article  CAS  PubMed  Google Scholar 

  26. Collman JP, Boulatov R, Sunderland CJ, Fu L (2004) Chem Rev 104:561–588

    Article  CAS  PubMed  Google Scholar 

  27. Collman JP, Boulatov R, Sunderland CJ (2003) Porphyrin Handbook 11:1–49

    Google Scholar 

  28. Collman JP, Herrmann PC, Boitrel B, Zhang X, Eberspacher TA, Fu L, Wang J, Rousseau DL, Williams ER (1994) J Am Chem Soc 116:9783–9784

    CAS  Google Scholar 

  29. Sasaki T, Nakamura N, Naruta Y (1998) Chem Lett 351–352

  30. Ghiladi RA, Ju TD, Lee D-H, Moënne-Loccoz P, Kaderli S, Neuhold Y-M, Zuberbühler AD, Woods AS, Cotter RJ, Karlin KD (1999) J Am Chem Soc 121:9885–9886

    Article  CAS  Google Scholar 

  31. Kopf M-A, Karlin KD (1999) Inorg Chem 38:4922–4923

    Article  CAS  PubMed  Google Scholar 

  32. Kopf M-A, Neuhold Y-M, Zuberbühler AD, Karlin KD (1999) Inorg Chem 38:3093–3102

    Article  CAS  Google Scholar 

  33. Naruta Y, Sasaki T, Tani F, Tachi Y, Kawato N, Nakamura N (2001) J Inorg Biochem 83:239–246

    Article  CAS  PubMed  Google Scholar 

  34. Ghiladi RA, Hatwell KR, Karlin KD, Huang H, Moënne-Loccoz P, Krebs C, Huynh BJ, Marzilli LA, Cotter RJ, Kaderli S, Zuberbühler AD (2001) J Am Chem Soc 123:6183–6184

    Article  CAS  PubMed  Google Scholar 

  35. Kim E, Helton ME, Wasser IM, Karlin KD, Lu S, Huang H, Moënne-Loccoz P, Incarvito CD, Rheingold AL, Honecker M, Kaderli S, Zuberbühler AD (2003) Proc Natl Acad Sci USA 100:3623–3628

    Article  CAS  PubMed  Google Scholar 

  36. Collman JP, Sunderland CJ, Berg KE, Vance MA, Solomon EI (2003) J Am Chem Soc 125:6648–6649

    Article  CAS  PubMed  Google Scholar 

  37. Chishiro T, Shimazaki Y, Tani F, Tachi Y, Naruta Y, Karasawa S, Hayami S, Maeda Y (2003) Angew Chem Int Ed 42:2788–2791

    Article  CAS  Google Scholar 

  38. Blackburn NJ, Rhames FC, Ralle M, Jaron S (2000) J Biol Inorg Chem 5:341–353

    CAS  PubMed  Google Scholar 

  39. Karlin KD, Kaderli S, Zuberbühler AD (1997) Acc Chem Res 30:139–147

    Article  CAS  Google Scholar 

  40. Jacobson RR, Tyeklár Z, Karlin KD, Liu S, Zubieta J (1988) J Am Chem Soc 110:3690–3692

    CAS  Google Scholar 

  41. Karlin KD, Wei N, Jung B, Kaderli S, Zuberbühler AD (1991) J Am Chem Soc 113:5868–5870

    CAS  Google Scholar 

  42. Karlin KD, Wei N, Jung B, Kaderli S, Niklaus P, Zuberbühler AD (1993) J Am Chem Soc 115:9506–9514

    CAS  Google Scholar 

  43. Karlin KD, Lee D-H, Kaderli S, Zuberbühler AD (1997) Chem Commun 475–476

  44. Zhang CX, Kaderli S, Costas M, Kim E, Neuhold Y-M, Karlin KD, Zuberbühler AD (2003) Inorg Chem 42:1807–1824

    Article  CAS  PubMed  Google Scholar 

  45. Ghiladi RA, Kretzer RM, Guzei I, Rheingold AL, Neuhold Y-M, Hatwell KR, Zuberbühler AD, Karlin KD (2001) Inorg Chem 40:5754–5767

    Article  CAS  PubMed  Google Scholar 

  46. Ju TD, Ghiladi RA, Lee D-H, van Strijdonck GPF, Woods AS, Cotter RJ, Young VG Jr, Karlin KD (1999) Inorg Chem 38:2244–2245

    Article  CAS  Google Scholar 

  47. Ghiladi RA, Karlin KD (2002) Inorg Chem 41:2400–2407

    Google Scholar 

  48. Tyeklár Z, Jacobson RR, Wei N, Murthy NN, Zubieta J, Karlin KD (1993) J Am Chem Soc 115:2677–2689

    Google Scholar 

  49. Stenkamp RE (1994) Chem Rev 94:715–726

    CAS  Google Scholar 

  50. Mirica LM, Ottenwaelder X, Stack TDP (2004) Chem Rev 104:1013–1045

    Article  CAS  PubMed  Google Scholar 

  51. Kitajima N, Fujisawa K, Fujimoto C, Moro-oka Y, Hashimoto S, Kitagawa T, Toriumi K, Tasumi K, Nakamura A (1992) J Am Chem Soc 114:1277–1291

    CAS  Google Scholar 

  52. Kitajima N, Moro-oka Y (1994) Chem Rev 94:737–757

    CAS  Google Scholar 

  53. Liang H-C, Karlin KD, Dyson R, Kaderli S, Jung B, Zuberbühler AD (2000) Inorg Chem 39:5884–5894

    Article  CAS  PubMed  Google Scholar 

  54. Obias HV, Lin Y, Murthy NN, Pidcock E, Solomon EI, Ralle M, Blackburn NJ, Neuhold Y-M, Zuberbühler AD, Karlin KD (1998) J Am Chem Soc 120:12960–12961

    Article  CAS  Google Scholar 

  55. Pidcock E, Obias HV, Zhang CX, Karlin KD, Solomon EI (1998) J Am Chem Soc 120:7841–7847

    Article  CAS  Google Scholar 

  56. Selke M, Sisemore MF, Valentine JS (1996) J Am Chem Soc 118:2008–2012

    Article  CAS  Google Scholar 

  57. Burstyn JN, Roe JA, Miksztal AR, Shaevitz BA, Lang G, Valentine JS (1988) J Am Chem Soc 110:1382–1388

    CAS  Google Scholar 

  58. Chufán EE, Karlin KD (2003) J Am Chem Soc 125:16160–16161

    Article  PubMed  Google Scholar 

  59. Baldwin MJ, Ross PK, Pate JE, Tyeklár Z, Karlin KD, Solomon EI (1991) J Am Chem Soc 113:8671–8679

    CAS  Google Scholar 

  60. Collman JP, Fu L, Herrmann PC, Zhang X (1997) Science 275:949–951

    Article  CAS  PubMed  Google Scholar 

  61. Kitajima N (1993) In: Karlin KD, Tyeklár Z (eds) Bioinorganic chemistry of copper. Chapman & Hall, New York, pp 251–263

  62. Pidcock E, Obias HV, Abe M, Liang H-C, Karlin KD, Solomon EI (1999) J Am Chem Soc 121:1299–1308

    Article  CAS  Google Scholar 

  63. Kim K, Lippard SJ (1996) J Am Chem Soc 118:4914–4915

    Article  CAS  Google Scholar 

  64. Dong Y, Zang Y, Shu L, Wilkinson EC, Que L Jr (1997) J Am Chem Soc 119:12683–12684

    Article  CAS  Google Scholar 

  65. Dong Y, Yan S, Young VG Jr, Que L Jr (1996) Angew Chem Int Ed Engl 35:618–620

    Article  CAS  Google Scholar 

  66. Obias HV, van Strijdonck GPF, Lee D-H, Ralle M, Blackburn NJ, Karlin KD (1998) J Am Chem Soc 120:9696–9697

    Article  CAS  Google Scholar 

  67. Walker FA, Simonis U (1993) In: Berliner LJ, Reuben J (eds) Biological magnetic resonance. Plenum Press, New York, pp 133–274

  68. Walker FA (2000) In: Kadish KM, Smith KM, Guilard R (eds) The porphyrin handbook. Academic Press, San Diego, pp 81–184

  69. Karlin KD, Nanthakumar A, Fox S, Murthy NN, Ravi N, Huynh BH, Orosz RD, Day EP (1994) J Am Chem Soc 116:4753–4763

    CAS  Google Scholar 

  70. Nanthakumar A, Fox S, Murthy NN, Karlin KD (1997) J Am Chem Soc 119:3898–3906

    Article  CAS  Google Scholar 

  71. Kauffmann KE, Goddard CA, Zang Y, Holm RH, Münck E (1997) Inorg Chem 36:985–993

    Article  CAS  PubMed  Google Scholar 

  72. Suzuki M, Ueda I, Kanatomi H, Murase I (1983) Chem Lett 185–188

  73. Ookubo T, Sugimoto H, Nagayama T, Masuda H, Sato T, Tanaka K, Maeda Y, Okawa H, Hayashi Y, Uehara A, Suzuki M (1996) J Am Chem Soc 118:701–702

    Article  CAS  Google Scholar 

  74. Seo J, Sung N-D, Hynes RC, Chin J (1996) Inorg Chem 35:7472–7473

    Article  CAS  Google Scholar 

  75. Hwang J, Krebs C, Huynh BH, Edmondson DE, Theil EC, Penner-Hahn JE (2000) Science 287:122–125

    Article  CAS  PubMed  Google Scholar 

  76. He C, DuBois JL, Hedman B, Hodgson KO, Lippard SJ (2001) Angew Chem Int Ed 40:1484–1487

    Article  CAS  Google Scholar 

  77. Chin D-H, La Mar GN, Balch AL (1980) J Am Chem Soc 102:4344–4350

    CAS  Google Scholar 

  78. Balch AL (1992) Inorg Chim Acta 198–200:297–307

  79. Feig AL, Becker M, Schindler S, van Eldik R, Lippard SJ (1996) Inorg Chem 35:2590–2601

    Article  CAS  PubMed  Google Scholar 

  80. DuBois JL, Mizoguchi TJ, Lippard SJ (2000) Coord Chem Rev 200:443–485

    Article  Google Scholar 

  81. Collman JP, Fu L, Herrmann PC, Wang Z, Rapta M, Bröring M, Schwenninger R, Boitrel B (1998) Angew Chem Int Ed 37:3397–3400

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to the National Institutes of Health (K.D.K., GM60353; R.J.C., GM54882; P.M.-L., GM18865) for support of this research.

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Author notes

  1. Arnold L. Rheingold

    Present address: Chemistry Department, University of California, San Diego, La Jolla, CA , 92093, USA

Authors and Affiliations

  1. Department of Chemistry, The Johns Hopkins University, Charles & 34th Streets, Baltimore, MD , 21218, USA

    Reza A. Ghiladi & Kenneth D. Karlin

  2. Environmental & Biomolecular Systems, OGI School of Science & Engineering, Oregon Health & Science University, Beaverton, OR , 97006, USA

    Hong-wei Huang, Pierre Moënne-Loccoz, Jay Stasser & Ninian J. Blackburn

  3. Department of Pharmacology and Molecular Sciences, The Johns Hopkins School of Medicine, Baltimore, MD , 21205, USA

    Amina S. Woods & Robert J. Cotter

  4. Crystallography Laboratory, Department of Chemistry, University of Delaware, Newark, DE , 19716, USA

    Christopher D. Incarvito & Arnold L. Rheingold

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  1. Reza A. Ghiladi
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Ghiladi, R.A., Huang, Hw., Moënne-Loccoz, P. et al. Heme-copper/dioxygen adduct formation relevant to cytochrome c oxidase: spectroscopic characterization of [(6L)FeIII-(O22−)-CuII]+. J Biol Inorg Chem 10, 63–77 (2005). https://doi.org/10.1007/s00775-004-0609-1

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