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Research Article

Picosecond primary structural transition of the heme is retarded after nitric oxide binding to heme proteins

Sergei G. Kruglik, Byung-Kuk Yoo, Stefan Franzen, Marten H. Vos, Jean-Louis Martin, and Michel Negrerie
PNAS August 3, 2010 107 (31) 13678-13683; https://doi.org/10.1073/pnas.0912938107
Sergei G. Kruglik
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  • For correspondence: michel.negrerie@polytechnique.fr sergei.kruglik@upmc.fr
Byung-Kuk Yoo
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Stefan Franzen
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Marten H. Vos
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Jean-Louis Martin
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Michel Negrerie
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  • For correspondence: michel.negrerie@polytechnique.fr sergei.kruglik@upmc.fr
  1. Edited by Robin M. Hochstrasser, University of Pennsylvania, Philadelphia, PA, and approved June 23, 2010 (received for review November 9, 2009)

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Abstract

We investigated the ultrafast structural transitions of the heme induced by nitric oxide (NO) binding for several heme proteins by subpicosecond time-resolved resonance Raman and femtosecond transient absorption spectroscopy. We probed the heme iron motion by the evolution of the iron-histidine Raman band intensity after NO photolysis. Unexpectedly, we found that the heme response and iron motion do not follow the kinetics of NO rebinding. Whereas NO dissociation induces quasi-instantaneous iron motion and heme doming (< 0.6 ps), the reverse process results in a much slower picosecond movement of the iron toward the planar heme configuration after NO binding. The time constant for this primary domed-to-planar heme transition varies among proteins (∼30 ps for myoglobin and its H64V mutant, ∼15 ps for hemoglobin, ∼7 ps for dehaloperoxidase, and ∼6 ps for cytochrome c) and depends upon constraints exerted by the protein structure on the heme cofactor. This observed phenomenon constitutes the primary structural transition in heme proteins induced by NO binding.

  • time-resolved Raman spectroscopy
  • allostery
  • structural dynamics

Footnotes

  • 1To whom correspondence may be addressed. E-mail: michel.negrerie{at}polytechnique.fr or sergei.kruglik{at}upmc.fr.
  • Author contributions: S.G.K., M.H.V., J.-L.M., and M.N. designed research; S.G.K., B.-K.Y., and M.N. performed research; S.F. contributed new reagents/analytic tools; S.G.K., B.-K.Y., S.F., M.H.V., and M.N. analyzed data; and S.G.K., M.H.V., J.-L.M., and M.N. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.0912938107/-/DCSupplemental.

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Picosecond primary structural transition of the heme is retarded after nitric oxide binding to heme proteins
Sergei G. Kruglik, Byung-Kuk Yoo, Stefan Franzen, Marten H. Vos, Jean-Louis Martin, Michel Negrerie
Proceedings of the National Academy of Sciences Aug 2010, 107 (31) 13678-13683; DOI: 10.1073/pnas.0912938107

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Picosecond primary structural transition of the heme is retarded after nitric oxide binding to heme proteins
Sergei G. Kruglik, Byung-Kuk Yoo, Stefan Franzen, Marten H. Vos, Jean-Louis Martin, Michel Negrerie
Proceedings of the National Academy of Sciences Aug 2010, 107 (31) 13678-13683; DOI: 10.1073/pnas.0912938107
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