His26 protonation in cytochrome c triggers microsecond β-sheet formation and heme exposure: implications for apoptosis

J Am Chem Soc. 2012 Nov 21;134(46):19061-9. doi: 10.1021/ja307100a. Epub 2012 Nov 6.

Abstract

Cytochrome c unfolds locally and reversibly upon heating at pH 3. UV resonance Raman (UVRR) spectra reveal that instead of producing unordered structure, unfolding converts turns and some helical elements to β-sheet. It also disrupts the Met80-heme bond, and has been previously shown to induce peroxidase activity. Aromatic residues that are H-bonded to a heme propionate (Trp59 and Tyr48) alter their orientation, indicating heme displacement. T-jump/UVRR measurements give time constants of 0.2, 3.9, and 67 μs for successive phases of β-sheet formation and concomitant reorientation of Trp59. UVRR spectra reveal protonation of histidines, and specifically of His26, whose H-bond to Pro44 anchors the 40s Ω loop; this loop is known to be the least stable 'foldon' in the protein. His26 protonation is proposed to disrupt its H-bond with Pro44, triggering the extension of a short β-sheet segment at the 'neck' of the 40s Ω loop into the loop itself and back into the 60s and 70s helices. The secondary structure change displaces the heme via H-bonds from residues in the growing β-sheet, thereby exposing it to exogenous ligands, and inducing peroxidase activity. This unfolding mechanism may play a role in cardiolipin peroxidation by cyt c during apoptosis.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Apoptosis*
  • Circular Dichroism
  • Cytochromes c / chemistry*
  • Heme / chemistry*
  • Histidine / chemistry*
  • Models, Molecular
  • Protons
  • Spectrophotometry, Ultraviolet
  • Spectrum Analysis, Raman

Substances

  • Protons
  • Heme
  • Histidine
  • Cytochromes c