A stochastic model of ion channel cluster formation in the plasma membrane

被引:29
|
作者
Sato, Daisuke [1 ]
Hernandez-Hernandez, Gonzalo [2 ]
Matsumoto, Collin [2 ]
Tajada, Sendoa [2 ]
Moreno, Claudia M. [2 ,3 ]
Dixon, Rose E. [2 ]
O'Dwyer, Samantha [2 ]
Navedo, Manuel F. [1 ]
Trimmer, James S. [2 ]
Clancy, Colleen E. [2 ]
Binder, Marc D. [3 ]
Santana, L. Fernando [2 ]
机构
[1] Univ Calif Davis, Sch Med, Dept Pharmacol, Davis, CA 95616 USA
[2] Univ Calif Davis, Sch Med, Dept Physiol & Membrane Biol, Davis, CA 95616 USA
[3] Univ Washington, Sch Med, Dept Physiol & Biophys, Seattle, WA 98195 USA
来源
JOURNAL OF GENERAL PHYSIOLOGY | 2019年 / 151卷 / 09期
基金
美国国家卫生研究院;
关键词
ARTERIAL SMOOTH-MUSCLE; SARCOPLASMIC-RETICULUM; CALCIUM-CHANNELS; SODIUM-CHANNELS; TRPV4; CHANNELS; K+ CHANNELS; LOCALIZATION; EXPRESSION; COMPARTMENTALIZATION; CONTRIBUTES;
D O I
10.1085/jgp.201912327
中图分类号
Q4 [生理学];
学科分类号
071003 ;
摘要
Ion channels are often found arranged into dense clusters in the plasma membranes of excitable cells, but the mechanisms underlying the formation and maintenance of these functional aggregates are unknown. Here, we tested the hypothesis that channel clustering is the consequence of a stochastic self-assembly process and propose a model by which channel clusters are formed and regulated in size. Our hypothesis is based on statistical analyses of the size distributions of the channel clusters we measured in neurons, ventricular myocytes, arterial smooth muscle, and heterologous cells, which in all cases were described by exponential functions, indicative of a Poisson process (i.e., clusters form in a continuous, independent, and memory-less fashion). We were able to reproduce the observed cluster distributions of five different types of channels in the membrane of excitable and tsA-201 cells in simulations using a computer model in which channels are "delivered" to the membrane at randomly assigned locations. The model's three parameters represent channel cluster nucleation, growth, and removal probabilities, the values of which were estimated based on our experimental measurements. We also determined the time course of cluster formation and membrane dwell time for Ca(v)1.2 and TRPV4 channels expressed in tsA-201 cells to constrain our model. In addition, we elaborated a more complex version of our model that incorporated a self-regulating feedback mechanism to shape channel cluster formation. The strong inference we make from our results is that Ca(v)1.2, Ca(v)1.3, BK, and TRPV4 proteins are all randomly inserted into the plasma membranes of excitable cells and that they form homogeneous clusters that increase in size until they reach a steady state. Further, it appears likely that cluster size for a diverse set of membrane-bound proteins and a wide range of cell types is regulated by a common feedback mechanism.
引用
收藏
页码:1116 / 1134
页数:19
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