Biophysical comparison of ATP-driven proton pumping mechanisms suggests a kinetic advantage for the rotary process depending on coupling ratio

被引:7
作者
Anandakrishnan, Ramu [1 ,2 ]
Zuckerman, Daniel M. [1 ,3 ,4 ]
机构
[1] Univ Pittsburgh, Dept Computat & Syst Biol, Sch Med, Pittsburgh, PA 15260 USA
[2] Edward Via Coll Osteopath Med, Div Biomed, Blacksburg, VA 24060 USA
[3] Oregon Hlth & Sci Univ, OHSU Ctr Spatial Syst Biomed, Portland, OR 97201 USA
[4] Oregon Hlth & Sci Univ, Dept Biomed Engn, Portland, OR 97201 USA
来源
PLOS ONE | 2017年 / 12卷 / 03期
基金
美国国家科学基金会; 美国国家卫生研究院;
关键词
H+-ATPASE; ROTOR RING; V-ATPASE; STOICHIOMETRY; TONOPLAST; ROTATION; SYNTHASE; PH;
D O I
10.1371/journal.pone.0173500
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
ATP-driven proton pumps, which are critical to the operation of a cell, maintain cytosolic and organellar pH levels within a narrow functional range. These pumps employ two very different mechanisms: an elaborate rotary mechanism used by V-ATPase H+ pumps, and a simpler alternating access mechanism used by P-ATPase H+ pumps. Why are two different mechanisms used to perform the same function? Systematic analysis, without parameter fitting, of kinetic models of the rotary, alternating access and other possible mechanisms suggest that, when the ratio of protons transported per ATP hydrolyzed exceeds one, the oneat- a-time proton transport by the rotary mechanism is faster than other possible mechanisms across a wide range of driving conditions. When the ratio is one, there is no intrinsic difference in the free energy landscape between mechanisms, and therefore all mechanisms can exhibit the same kinetic performance. To our knowledge all known rotary pumps have an H+: ATP ratio greater than one, and all known alternating access ATP-driven proton pumps have a ratio of one. Our analysis suggests a possible explanation for this apparent relationship between coupling ratio and mechanism. When the conditions under which the pump must operate permit a coupling ratio greater than one, the rotary mechanism may have been selected for its kinetic advantage. On the other hand, when conditions require a coupling ratio of one or less, the alternating access mechanism may have been selected for other possible advantages resulting from its structural and functional simplicity.
引用
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页数:14
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