X-ray absorption spectroscopic investigation of the electronic structure differences in solution and crystalline oxyhemoglobin

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 41, 2013, Pages 16333-16338

  Wilson, Samuel A ^a,b   Green, Evan ^b,c   Mathews, Irimpan I ^b   Benfatto, Maurizio ^d   Hodgson, Keith O ^a,b   Hedman, Britt ^b   Sarangi, Ritimukta ^b  

^a STANFORD UNIVERSITY   (United States)

^b SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^c Reed College   (Portugal)

^d INFN LABORATORI NAZIONALI DI FRASCATI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

FERRIC OXIDE; FERRIC SUPEROXIDE; OXYHEMOGLOBIN; OZONE; UNCLASSIFIED DRUG;

ARTICLE; CALCULATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; CRYSTALLOGRAPHY; DENSITY FUNCTIONAL THEORY; DIPOLE; ELECTRONICS; GEOMETRY; HYDROGEN BOND; PRIORITY JOURNAL; SOLVATION; THEORETICAL STUDY; X RAY ABSORPTION SPECTROSCOPY;

CRYSTALLOGRAPHY, X-RAY; MOLECULAR STRUCTURE; OXYHEMOGLOBINS; PROTEIN CONFORMATION; X-RAY ABSORPTION SPECTROSCOPY;

EID: 84885360031     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1315734110     Document Type: Article

References (38)

1. Hsia CC (1998) Respiratory function of hemoglobin. N Engl J Med 338(4):239-247.
2. Hoppe-Seylor F (1866) Uber die oxydation in lebendemblute. Med-chem Untersuch Lab 1:133-140.
3. Funke O (1851) Über das milzvenenblut. Z Rat Med 1:172-218.
4. Pauling L, Coryell CD (1936) The magnetic properties and structure of hemoglobin, oxyhemoglobin and carbonmonoxyhemoglobin. Proc Natl Acad Sci USA 22(4): 210-216.
5. Perutz MF, et al. (1960) Structure of haemoglobin: A three-dimensional Fourier synthesis at 5.5-A. resolution, obtained by X-ray analysis. Nature 185(4711):416-422.
6. Collman JP, Gagne RR, Reed CA, Robinson WT, Rodley GA (1974) Structure of an iron (II) dioxygen complex; a model for oxygen carrying hemeproteins. Proc Natl Acad Sci USA 71(4):1326-1329.
7. Pauling L (1977) Magnetic properties and structure of oxyhemoglobin. Proc Natl Acad Sci USA 74(7):2612-2613.
8. Weiss JJ (1964) Nature of the iron-oxygen bond in oxyhaemoglobin. Nature 202: 83-84.
9. McClure DS (1960) Electronic structure of transition-metal complex ions. Radiat Res Suppl 2:218-224.
10. Goddard WA, 3rd, Olafson BD (1975) Ozone model for bonding of an O2 to heme in oxyhemoglobin. Proc Natl Acad Sci USA 72(6):2335-2339.
11. Chen H, Ikeda-Saito M, Shaik S (2008) Nature of the Fe-O2 bonding in oxy-myoglobin: Effect of the protein. J Am Chem Soc 130(44):14778-14790.
12. Oshtrakh MJ (1999) Mössbauer spectroscopy of iron containing biomolecules and model compounds in biomedical research. J Mol Struct 480-481:109-120.
13. Das TK, Couture M, Ouellet Y, Guertin M, Rousseau DL (2001) Simultaneous observation of the O-O and Fe-O2 stretching modes in oxyhemoglobins. Proc Natl Acad Sci USA 98(2):479-484.
14. Park SY, Yokoyama T, Shibayama N, Shiro Y, Tame JR (2006) 1.25 A resolution crystal structures of human haemoglobin in the oxy, deoxy and carbonmonoxy forms. J Mol Biol 360(3):690-701.
15. Bianconi A, et al. (1986) Local Fe site structure in the tense-to-relaxed transition in carp deoxyhemoglobin: A XANES (x-ray absorption near edge structure) study. Proc Natl Acad Sci USA 83(20):7736-7740.
16. Durham P, et al. (1983) X-ray absorption near edge structure (XANES) for CO, CN and deoxyhaemoglobin: geometrical information. EMBO J 2(9):1441-1443.
17. Eisenberger P, Shulman RG, Brown GS, Ogawa S (1976) Structure-function relations in hemoglobin as determined by x-ray absorption spectroscopy. Proc Natl Acad Sci USA 73(2):491-495.
18. Della Longa S, et al. (2001) Structure of the Fe-heme in the hemodimeric hemoglobin from Scapharca inaequivalvis and in the T721 mutant: An X-ray absorption spectroscopic study at low temperature. Eur Biophys J 29(8):559-568.
19. Zijlstra WG, Buursma A (1997) Spectrophotometry of hemoglobin:absorption spectra of bovine oxyhemoglobin, deoxyhemoglobin, carboxyhemoglobin and methemoglobin. Comp Biochem Physiol A: Physiol 118B:743-749.
20. Westre TE, et al. (1997) A multiplet analysis of Fe K-edge 1s->3d pre-edge features of iron complexes. J Am Chem Soc 119(27):6297-6314.
21. Cartier C, et al. (1992) X-Ray absorption spectroscopy of Iron-(11) and-(111) baskethandle porphyrins. J Chem Soc, Dalton Trans 609:609-618.
22. Bianconi A, Dell'Ariccia M, Gargano A, Natoli CR (1983) Bond length determination using XANES. EXAFS and Near Edge Structure, Springer Series in Chemical Physics, eds Bianconi A, Incoccia A, Stipcich S (Springer, Berlin), Vol 27, pp 57-61.
23. Della Longa S, Pin S, Cortès R, Soldatov AV, Alpert B (1998) Fe-heme conformations in ferric myoglobin. Biophys J 75(6):3154-3162.
24. Sarangi R, et al. (2006) X-ray absorption edge spectroscopy and computational studies on LCuO2 species: Superoxide-Cu(II) versus peroxide-Cu(III) bonding. J Am Chem Soc 128(25):8286-8296.
25. DeBeer George S, Petrenko T, Neese F (2008) Prediction of iron K-edge absorption spectra using time-dependent density functional theory. J Phys Chem A 112(50): 12936-12943.
26. Rehr JJ, Zabinsky SI, Albers RC, Albers RC; Mustre de Leon J (1991) Ab initio curvedwave x-ray-absorption fine structure. Phys Rev B Condens Matter 44(9):4146-4156.
27. Rehr JJ, Ankudinov AL (2003) New developments in the theory and interpretation of X-ray spectra based on fast parallel calculations. J Synchrotron Radiat 10(Pt 1):43-45.
28. Rehr JJ, Mustre de Leon J, Zabinsky SI, Albers RC (1991) Theoretical X-ray absorption fine structure standards. J Am Chem Soc 113(14):5135-5140.
29. Cramer CJ, Tolman WB, Theopold KH, Rheingold AL (2003) Variable character of O-O and M-O bonding in side-on (eta(2)) 1:1 metal complexes of O2. Proc Natl Acad Sci USA 100(7):3635-3640.
30. Cho J, Sarangi R, Nam W (2012) Mononuclear metal-o2 complexes: Crystallographic and spectroscopic characterization and reactivity. Acc Chem Res 45:1321-1330.
31. Wilson SA, et al. (2013) Iron L-edge X-ray absorption spectroscopy of oxy-picket fence porphyrin: experimental insight into Fe-O2 bonding. J Am Chem Soc 135(3): 1124-1136.
32. Shaik S, Chen H (2011) Lessons on O2 and NO bonding to heme from ab initio multireference/ multiconfiguration and DFT calculations. J Biol Inorg Chem 16:841-855.
33. Jameson GB, et al. (1980) Models for the active site of oxygen-binding hemoproteins. Dioxygen binding properties and the structures of(2-Methylimidazole)-meso-tetra (α,α,α,α-o- pivalamidophenyl)porphyrinatoiron(II)-ethanol and Its dioxygen adduct. J Am Chem Soc 102:3224-3237.
34. Yano J, et al. (2005) X-ray damage to the Mn4Ca complex in single crystals of photosystem II: A case study for metalloprotein crystallography. Proc Natl Acad Sci USA 102(34):12047-12052.
35. George GN, et al. (2012) X-ray-induced photo-chemistry and X-ray absorption spectroscopy of biological samples. J Synchrotron Radiat 19(Pt 6):875-886.
36. Tenderholt A (2007) Pyspline and QMForge (Stanford Univ Press, Stanford, CA).
37. George GN (2000) EXAFSPAK and EDG-FIT (Stanford Synchrotron Radiation Laboratory, Stanford Linear Accelerator Center, Stanford, CA).
38. Neese F (2008) ORCA: An ab initio, DFT and semiempirical electronic structure package. Version 2.6.35 (Univ of Bonn, Bonn).