An arginine to lysine mutation in the vicinity of the heme propionates affects the redox potentials of the hemes and associated electron and proton transfer in cytochrome c oxidase

by Mills, D. A.; Geren, L.; Hiser, C.; Schmidt, B.; Durham, B.; Millett, F.; Ferguson-Miller, S.

Cytochrome c oxidase pumps protons across a membrane using energy from electron transfer and reduction of oxygen to water. It is postulated that an element of the energy transduction mechanism is the movement of protons to the vicinity of the berries upon reduction, to favor charge neutrality. Possible sites on which protons could reside, in addition to the conserved carboxylate E286, are the propionate groups of heme a and/or heme a3. A highly conserved pair of arginines (R481 and 8482) interact with these propionates through ionic and hydrogen bonds. This study shows that the conservative mutant, R481K, although as fully active as the wild type under many conditions, exhibits a significant decrease in the midpoint redox potential of heme a relative to Cu-A (Delta E-m) of congruent to 40 mV, has lowered activity under conditions of high pH or in the presence of a membrane potential, and has a slowed heme a3 reduction with ditluonite. Another mutant, D132A, which strongly inhibits proton uptake from the internal side of the membrane, has < 4% of the activity of the wild type and appears to be dependent on proton uptake from the outside. A double mutation, D132A/R481 K, is even more strongly inhibited (similar to 1% of that of the wild type). The more-than-additive effect supports the concept that 8481 K not only lowers the midpoint potential of heme a but also limits a supply route for protons from the outside of the membrane used by the D132 mutant. The results are consistent with an important role of 8481 and heme a/a3 propionates in proton movement in a reversible exit path.

Journal
Biochemistry
Volume
44
Issue
31
Year
2005
Start Page
10457-10465
URL
https://dx.doi.org/10.1021/bi050283d
ISBN/ISSN
1520-4995; 0006-2960
DOI
10.1021/bi050283d