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Spin cascade and doming in ferric hemes: Femtosecond X-ray absorption and X-ray emission studies

September 8, 2020

The structure-function relationship is at the heart of biology: specific structural changes in proteins are usually associated with specific functions. This is particularly the case with hemoproteins, which have a wide range of functions, such as oxygen fixation and transport, and neurotransmission.

In humans, the most important protein involved in electron transfer is Cytochrome c, which is involved in cellular respiration in the respiratory chain, transporting one electron per molecule. As such, it is associated with the inner mitochondrial membrane.

Like all heme proteins, the active center of cytochrome c is the so-called “heme porphyrin”. The electron transfer properties of cytochrome c have been associated to the “ruffled” deformation of its heme. In contrast, the “domed” deformation of the heme is the hallmark of respiratory proteins such as hemoglobin and myoglobin.

In a new experiment, a team of scientists led by Majed Chergui at EPFL’s School of Basic Sciences, with Chris MIlne and colleagues at the Paul-Scherrer Institut and the European X-ray Free Electron Laser (Hamburg) have found that Cytochrome c also undergoes doming.

To carry out their study, the researchers used cutting-edge ultrafast X-ray spectroscopic techniques. They activated the heme using ultrashort, energizing laser pulses, and monitored its evolution using another ultrashort X-ray pulse from an X-ray free-electron laser to record X-ray absorption and X-ray emission as a function of time.

X-ray absorption is sensitive to the structure of heme, while X-ray emission offers a fingerprint of its electronic states. By combining the two, the scientists have unambiguously determined that the system undergoes doming and goes back to its initial state via a cascade among spin states.

“The conclusions of our work show that doming is a universal feature of all heme proteins and is not limited to respiratory ones (hemoglobin and myoglobin),” says Majed Chergui. “The question that arises now is the extent to which doming intervenes in the electron transfer function of cytochrome c.”



Fig. 1. Crystal structure of ferric Cyt c. The heme and the Met80, His18, and Tyr67 amino acid residues ligated to the Fe heme are highlighted as sticks (Fe [orange], C [teal], N [blue], O [red], S [yellow]). The structure was obtained from the Protein Data Bank, under ID code 1HRC (18). The Fe atom at the center of the porphyrin is coordinated by four pyrrole (Np) atoms and by the distal Met80 and the proximal His18 ligands.

See also:
 
Reference: Bacellar, C., Kinschel, D., Mancini, G.F., Ingle, R.A., Rouxel, J., Cannelli, O., Cirelli, C., Knopp, G., Szlachetko, J., Lima, F.A., Menzi, S., Pamfilidis, G., Kubicek, K., Khakhulin, D., Gawelda, W., Rodriguez-Fernandez, A., Biednov, M., Bressler, C., Arrell, C.A., Johnson, P.J.M., Milne, C.J., and Chergui, M. (2020). Spin cascade and doming in ferric hemes: Femtosecond X-ray absorption and X-ray emission studies. Proc Natl Acad Sci USA 117, 21914 (10.1073/pnas.2009490117)

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