Oxoiron(IV) complexes as synthons for the assembly of heterobimetallic centers such as the Fe/Mn active site of Class Ic ribonucleotide reductases

Abstract

Nonheme oxoiron(IV) complexes can serve as synthons for generating heterobimetallic oxo-bridged dimetal complexes by reaction with divalent metal complexes. The formation of FeIII–O–CrIII and FeIII–O–MnIII complexes is described herein. The latter complexes may serve as models for the FeIII–X–MnIII active sites of an emerging class of Fe/Mn enzymes represented by the Class 1c ribonucleotide reductase from Chlamydia trachomatis and the R2-like ligand-binding oxidase (R2lox) found in Mycobacterium tuberculosis. These synthetic complexes have been characterized by UV–Vis, resonance Raman, and X-ray absorption spectroscopy, as well as electrospray mass spectrometry. The FeIII–O–CrIII complexes exhibit a three-band UV–Vis pattern that differs from the simpler features associated with FeIII–O–FeIII complexes. The positions of these features are modulated by the nature of the supporting polydentate ligand on the iron center, and their bands intensify dramatically in two examples upon the binding of an axial cyanate or thiocyanate ligand trans to the oxo bridge. In contrast, the FeIII–O–MnIII complexes resemble FeIII–O–FeIII complexes more closely. Resonance Raman characterization of the FeIII–O–MIII complexes reveals an 18O-sensitive vibration in the range of 760–890 cm−1. This feature has been assigned to the asymmetric FeIII–O–MIII stretching mode and correlates reasonably with the Fe–O bond distance determined by EXAFS analysis. The likely binding of an acetate as a bridging ligand to the FeIII–O–MnIII complex 12 lays the foundation for further efforts to model the heterobimetallic active sites of Fe/Mn enzymes.

This is a preview of subscription content, log in to check access.

Fig. 1
Chart 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Abbreviations

BnTPEN:

N-benzyl-N,N′,N′-tris(2-pyridylmethyl)-1,2-diaminoethane

Hdpaq:

2-[Bis(pyridin-2-ylmethyl)]amino-N-quinolin-8-yl-acetamide

N4Py:

N,N-bis(2-pyridylmethyl)-N-bis(2-pyridyl)methylamine

TMC:

1,4,8,11-Tetramethylcyclam

TMC-py:

1-(Pyridyl-2′-methyl)-4,8,11-trimethyl-1,4,8,11-tetrazacyclotetradecane

TPA:

Tris(2-pyridylmethyl)amine

H2ICIMP:

2-(N-carboxylmethyl)-[N-(N-methylimidazolyl-2-methyl)aminomethyl]-[6-(N-isopropylmethyl)-[N-(N-methyl-imidazolyl-2-methyl)]aminomethyl-4-methylphenol])

HBPMP:

2,6-Bis[(bis(2-pyridylmethyl)-amino)methyl]-4-methylphenol)

TACN:

1,4,7-Triazacyclononane

Me3TACN:

1,4,7-Trimethyl-1,4,7-triazacyclononane

References

  1. 1.

    Högbom M, Stenmark P, Voevodskaya N, McClarty G, Gräslund A, Nordlund P (2004) Science 305:245–248

    Article  PubMed  Google Scholar 

  2. 2.

    Bollinger JM, Jiang W, Green MT, Krebs C (2008) Curr Opin Struct Biol 18:650–657

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Carboni M, Latour J-M (2011) Coord Chem Rev 255:186–202

    CAS  Article  Google Scholar 

  4. 4.

    Griese JJ, Srinivas V, Högbom M (2014) J Biol Inorg Chem 19:759–774

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Jiang W, Yun D, Saleh L, Barr EW, Xing G, Hoffart LM, Maslak M-A, Krebs C, Bollinger JM (2007) Science 316:1188–1191

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Jiang W, Hoffart LM, Krebs C, Bollinger JM (2007) Biochemistry 46:8709–8716

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Jiang W, Yun D, Saleh L, Bollinger JM Jr, Krebs C (2008) Biochemistry 47:13736–13744

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Younker JM, Krest CM, Jiang W, Krebs C, Bollinger JM, Green MT (2008) J Am Chem Soc 130:15022–15027

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Martinie RJ, Blaesi EJ, Krebs C, Bollinger JM, Silakov A, Pollock CJ (2017) J Am Chem Soc 139:1950–1957

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Andersson CS, Högbom M (2009) Proc Natl Acad Sci USA 106:5633–5638

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Shafaat HS, Griese JJ, Pantazis DA, Roos K, Andersson CS, Popović-Bijelić A, Gråslund A, Siegbahn PE, Neese F, Lubitz W (2014) J Am Chem Soc 136:13399–13409

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Miller EK, Trivelas NE, Maugeri PT, Blaesi EJ, Shafaat HS (2017) Biochemistry 56:3369–3379

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Holman TR, Andersen KA, Anderson OP, Hendrich MP, Juarez-Garcia C, Münck E, Que L Jr (1990) Angew Chem Int Ed Engl 29:921–923

    Article  Google Scholar 

  14. 14.

    Holman TR, Wang Z, Hendrich MP, Que L Jr (1995) Inorg Chem 34:134–139

    CAS  Article  Google Scholar 

  15. 15.

    Carboni M, Clemancey M, Molton F, Pecaut J, Lebrun C, Dubois L, Blondin G, Latour J-M (2012) Inorg Chem 51:10447–104460

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Das B, Daver H, Singh A, Singh R, Haukka M, Demeshko S, Meyer F, Lisensky G, Jarenmark M, Himo F, Nordlander E (2014) Eur J Inorg Chem 2204–2212

  17. 17.

    Hotzelmann R, Wieghardt K, Flörke U, Haupt H-J, Weatherburn DC, Bonvoisin J, Blondin G, Girerd J-J (1992) J Am Chem Soc 114:1681–1696

    CAS  Article  Google Scholar 

  18. 18.

    Zhou A, Kleespies ST, Van Heuvelen KM, Que L Jr (2015) Chem Commun 51:14326–14329

    CAS  Article  Google Scholar 

  19. 19.

    Zhou A, Prakash J, Rohde GT, Klein JEMN, Kleespies ST, Draksharapu A, Fan R, Guo Y, Cramer CJ, Que L Jr (2016) Inorg Chem 56:518–527

    Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Ching W, Zhou A, Klein JEMN, Fan R, Knizia G, Cramer CJ, Guo Y, Que L Jr (2017) Inorg Chem 56:11129–11140

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    Prakash J, Rohde GT, Meier KK, Jasniewski AJ, Van Heuvelen KM, Münck E, Que L Jr (2015) J Am Chem Soc 137:3478–3481

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Draksharapu A, Rasheed W, Klein JEMN, Que L Jr (2017) Angew Chem Int Ed 56:9091–9095

    CAS  Article  Google Scholar 

  23. 23.

    Rohde J-U, Torelli S, Shan X, Lim MH, Klinker EJ, Kaizer J, Chen K, Nam W, Que L Jr (2004) J Am Chem Soc 126:16750–16761

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Sanders-Loehr J, Wheeler WD, Shiemke AK, Averill BA, Loehr TM (1989) J Am Chem Soc 111:8084–8093

    CAS  Article  Google Scholar 

  25. 25.

    Roe AL, Schneider DJ, Mayer RJ, Pyrz JW, Widom J, Que L Jr (1984) J Am Chem Soc 106:1676–1681

    CAS  Article  Google Scholar 

  26. 26.

    Westre TE, Kennepohl P, DeWitt JG, Hedman B, Hodgson KO, Solomon EI (1997) J Am Chem Soc 119:6297–6314

    CAS  Article  Google Scholar 

  27. 27.

    Wijeratne GB, Corzine B, Day VW, Jackson TA (2014) Inorg Chem 53:7622–7634

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Norman RE, Yan S, Que L Jr, Sanders-Loehr J, Backes G, Ling J, Zhang JH, O’Connor CJ (1990) J Am Chem Soc 112:1554–1562

    CAS  Article  Google Scholar 

  29. 29.

    Kurtz DM Jr (1990) Chem Rev 90:585–606

    CAS  Article  Google Scholar 

  30. 30.

    Havare N, Plattner DA (2012) Org Lett 14:5078–5081

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Schardt BC, Hill CL (1983) Inorg Chem 22:1563–1565

    CAS  Article  Google Scholar 

  32. 32.

    Rohde J-U, In J-H, Lim MH, Brennessel WW, Bukowski MR, Stubna A, Münck E, Nam W, Que L Jr (2003) Science 299:1037–1039

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Wang Z-W, Chen Q-Y, Liu Q-S (2014) Transit Met Chem 39:917–924

    Article  Google Scholar 

  34. 34.

    Ward AL, Elbaz L, Kerr JB, Arnold J (2012) Inorg Chem 51:4694–4706

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Zang Y, Kim J, Dong Y, Wilkinson EC, Appelman EH, Que L Jr (1997) J Am Chem Soc 119(18):4197–4205

  36. 36.

    Ankudinov A, Ravel B, Rehr J, Conradson S (1998) Phys Rev B 58:7565–7576

    CAS  Article  Google Scholar 

  37. 37.

    George GN (1990) EXAFSPAK Stanford Synchrotron Radiation Laboratory, Stanford

  38. 38.

    Roelfes G, Lubben M, Chen K, Ho RYN, Meetsma A, Genseberger S, Hermant RM, Hage R, Mandal SK, Young VG, Zang Y, Kooijman H, Spek AL, Que L Jr, Feringa BL (1999) Inorg Chem 38:1929–1936

    CAS  Article  PubMed  Google Scholar 

  39. 39.

    Wojdyr M (2010) J Appl Crystallogr 43:1126–1128

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Institutes of Health (Grant GM-38767 to L.Q.). XAS data were collected at the Stanford Synchrotron Radiation Lightsource, which is supported by the U.S. DOE under Contract No. DE-AC02-76SF00515. Use of Beamline 7–3 is supported by the DOE Office of Biological and Environmental Research and the National Institutes of Health, National Institute of General Medical Sciences (including P41GM103393).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Lawrence Que Jr..

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1927 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhou, A., Crossland, P.M., Draksharapu, A. et al. Oxoiron(IV) complexes as synthons for the assembly of heterobimetallic centers such as the Fe/Mn active site of Class Ic ribonucleotide reductases. J Biol Inorg Chem 23, 155–165 (2018). https://doi.org/10.1007/s00775-017-1517-5

Download citation

Keywords

  • Heterobimetallic Fe–O–M complexes
  • Oxoiron(IV) complexes
  • EXAFS analysis
  • Resonance Raman spectroscopy
  • Ribonucleotide reductase