Detection of two histidyl ligands to CuA of cytochrome oxidase by 35-GHz ENDOR. 14,15N and 63,65Cu ENDOR studies of the CuA site in bovine heart cytochrome aa3 and cytochromes caa3 and ba3 from Thermus thermophilus

Gurbiel, Ryszard J.; Fann, Yang C.; Surerus, Kristene K.; Werst, M.; Musser, Siegfried M.; Doan, Peter E.; Chan, Sunney I.; Fee, James A.; Hoffman, Brian M.

doi:10.1021/ja00076a053

Cited by 65 publications

(45 citation statements)

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“…ET Pathways. Ligand-metal covalency plays an important role in activating ET pathways and increasing k ET through increased donor-acceptor coupling (H DA ) (33,(39)(40)(41). The nature of the ET pathways coupling the Cu A active site with its donor and acceptor has been the subject of much research.…”

Section: Discussionmentioning

confidence: 99%

Axial interactions in the mixed-valent Cu _A active site and role of the axial methionine in electron transfer

Tsai

Hadt

Marshall

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Within Cu-containing electron transfer active sites, the role of the axial ligand in type 1 sites is well defined, yet its role in the binuclear mixed-valent Cu A sites is less clear. Recently, the mutation of the axial Met to Leu in a Cu A site engineered into azurin (Cu A Az) was found to have a limited effect on E 0 relative to this mutation in blue copper (BC). Detailed low-temperature absorption and magnetic circular dichroism, resonance Raman, and electron paramagnetic resonance studies on Cu A Az (WT) and its M123X (X = Q, L, H) axial ligand variants indicated stronger axial ligation in M123L/H. Spectroscopically validated density functional theory calculations show that the smaller ΔE 0 is attributed to H 2 O coordination to the Cu center in the M123L mutant in Cu A but not in the equivalent BC variant. The comparable stabilization energy of the oxidized over the reduced state in Cu A and BC (Cu A ∼ 180 mV; BC ∼ 250 mV) indicates that the S(Met) influences E 0 similarly in both. Electron delocalization over two Cu centers in Cu A was found to minimize the Jahn-Teller distortion induced by the axial Met ligand and lower the inner-sphere reorganization energy. The Cu-S(Met) bond in oxidized Cu A is weak (5.2 kcal/ mol) but energetically similar to that of BC, which demonstrates that the protein matrix also serves an entatic role in keeping the Met bound to the active site to tune down E 0 while maintaining a low reorganization energy required for rapid electron transfer under physiological conditions. spectroscopy | reduction potential | energy transduction pathway L ong-range electron transfer (ET) is vital to a wide range of biological processes, including two key energy transduction pathways essential for life: H 2 O oxidation in photosynthesis and O 2 reduction in respiration (1, 2). Nature has adapted a conserved cupredoxin fold motif (i.e., the Greek-key β barrel) to construct two evolutionarily linked, but structurally distinct Cucontaining ET proteins (3-5). These are the mononuclear type 1 (T1) or blue copper (BC) and binuclear purple Cu A proteins. The first coordination sphere of the classic BC sites [e.g., plastocyanin (Pc) and azurin (Az)] consists of a trigonally distorted tetrahedral environment where Cu resides in an equatorial plane formed by one S(Cys) and two N(His) ligands and has an axial S (Met) ligand (Fig. 1A) (Fig. 1B) (8-11). Both sites carry out rapid, efficient longrange ET with rates on the order of 10 3 -10 5 s −1 (12, 13).Although BC proteins use a Cu + /Cu 2+ redox couple, the binuclear Cu A sites use a (Cu 1+ -Cu 1+ )/(Cu 1.5+ -Cu 1.5+ ) redox cycle. The oxidized form of Cu A is mixed-valent (MV), with a highly covalent Cu 2 S 2 core that gives rise to its unique spectroscopic features. The unpaired electron is fully delocalized over the two Cu centers and exhibits a characteristic seven-line 63,65 Cu hyperfine splitting pattern in electron paramagnetic resonance (EPR) spectroscopy (14, 15). Maintaining valence delocalization even in the presence of a low symmetry protein ...

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Section: Discussionmentioning

confidence: 99%

Axial interactions in the mixed-valent Cu _A active site and role of the axial methionine in electron transfer

Tsai

Hadt

Marshall

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…The authors proposed a model in which a single Cu ion is ligated by two His and two Cys in tetrahedral coordination, often referred to as the Chan model [51]. More recent Q-band ENDOR studies [52] with three different preparations, of which one was labeled with I5N, provided better resolution of the nitrogen hfs. This work confirmed that there were two different His ligands of Cu,.…”

Section: Progress Through Advances In Related Fields Protein Chem-mentioning

confidence: 99%

Copper A of Cytochrome c Oxidase, A Novel, Long‐Embattled, Biological Electron‐Transfer Site

Beinert

1997

European Journal of Biochemistry

124

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This review traces the history of understanding of the CU, site in cytochrome c oxidase (COX) from the beginnings, when few believed that there was any significant Cu in COX, to the verification of three atoms Cu/monomer and to the final identification of the site as a dinuclear, Cys-bridged average valence ... Cu' 5+ structure through spectroscopy, recombinant DNA techniques, and crystallography. The CUM+ critical steps forward in understanding the nature of the Cu, site are recounted and the present state (as of the end of 1996) of our knowledge of the molecular and electronic structure is discussed in some detail. The contributions made through the years by the development of methodology and concepts for solving the enigma of Cu, are emphasized and impediments, often rooted in contemporary preconceptions and attitudes rather than solid data, are mentioned, which discouraged the exploitation of early valuable clues. Finally, analogies in construction principles of polynuclear Cu-S and Fe-S proteins are pointed out.

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“…We have examined the role of the pocket histidine and valine in nitrosyl horse heart myoglobin by observing hyperfine interactions between the paramagnetic center and the protons in the distal residues, using angle-selected EN-DOR spectroscopy. This methodology was first suggested by Rist and Hyde (1970); it permits proton identifications and has been described Hurst et al, 1985) and intensively applied by other authors True et al, 1988;Gurbiel et al, 1993;Moens et al, 1994;Schramm and Rossi, 1999;Tierney et al, 1999;Kappl et al, 1999). The procedures for determining hyperfine tensors with this methodology were developed by Hoffman's group and have been used in this paper .…”

Section: Introductionmentioning

confidence: 99%

Proton Electron Nuclear Double Resonance from Nitrosyl Horse Heart Myoglobin: The Role of His-E7 and Val-E11

Flores

Wajnberg

Bemski

2000

Biophysical Journal

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Electron nuclear double resonance (ENDOR) spectroscopy has been used to study protons in nitrosyl horse heart myoglobin (MbNO). (1)H ENDOR spectra were recorded for different settings of the magnetic field. Detailed analysis of the ENDOR powder spectra, using computer simulation, based on the "orientation-selection" principle, leads to the identification of the available protons in the heme pocket. We observe hyperfine interactions of the N(HisF8)-Fe(2+)-N(NO) complex with five protons in axial and with eight protons in the rhombic symmetry along different orientations, including those of the principal axes of the g-tensor. Protons from His-E7 and Val-E11 residues are identified in the two symmetries, rhombic and axial, exhibited by MbNO. Our results indicate that both residues are present inside the heme pocket and help to stabilize one particular conformation.

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Detection of two histidyl ligands to CuA of cytochrome oxidase by 35-GHz ENDOR. 14,15N and 63,65Cu ENDOR studies of the CuA site in bovine heart cytochrome aa3 and cytochromes caa3 and ba3 from Thermus thermophilus

Cited by 65 publications

References 7 publications

Axial interactions in the mixed-valent Cu _A active site and role of the axial methionine in electron transfer

Axial interactions in the mixed-valent Cu _A active site and role of the axial methionine in electron transfer

Copper A of Cytochrome c Oxidase, A Novel, Long‐Embattled, Biological Electron‐Transfer Site

Proton Electron Nuclear Double Resonance from Nitrosyl Horse Heart Myoglobin: The Role of His-E7 and Val-E11

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Detection of two histidyl ligands to CuA of cytochrome oxidase by 35-GHz ENDOR. 14,15N and 63,65Cu ENDOR studies of the CuA site in bovine heart cytochrome aa3 and cytochromes caa3 and ba3 from Thermus thermophilus

Cited by 65 publications

References 7 publications

Axial interactions in the mixed-valent Cu A active site and role of the axial methionine in electron transfer

Axial interactions in the mixed-valent Cu A active site and role of the axial methionine in electron transfer

Copper A of Cytochrome c Oxidase, A Novel, Long‐Embattled, Biological Electron‐Transfer Site

Proton Electron Nuclear Double Resonance from Nitrosyl Horse Heart Myoglobin: The Role of His-E7 and Val-E11

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Axial interactions in the mixed-valent Cu _A active site and role of the axial methionine in electron transfer

Axial interactions in the mixed-valent Cu _A active site and role of the axial methionine in electron transfer