Modulation of TRESK Background K+ Channel by Membrane Stretch

被引:29
作者
Callejo, Gerard [1 ,2 ]
Giblin, Jonathan P. [1 ,2 ]
Gasull, Xavier [1 ,2 ]
机构
[1] Univ Barcelona, Sch Med, Dept Physiol Sci 1, Neurophysiol Lab, Barcelona, Spain
[2] Inst Invest Biomed August Pi i Sunyer IDIBAPS, Barcelona, Spain
关键词
MOLECULAR-MECHANISMS; POTASSIUM CHANNEL; SENSORY NEURONS; RAT SKIN; TRAAK; NOCICEPTORS; ACTIVATION; PRESSURE; TREK-2; SENSITIZATION;
D O I
10.1371/journal.pone.0064471
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
The two-pore domain K+ channel TRESK is expressed in dorsal root ganglion and trigeminal sensory neurons where it is a major contributor to background K+ current. TRESK acts as a break to prevent excessive sensory neuron activation and decreases in its expression or function have been involved in neuronal hyperexcitability after injury/inflammation, migraine or altered sensory perception (tingling, cooling and pungent burning sensations). All these effects have implicated this channel in nociception and mechanotransduction. To determine the role of TRESK in sensory transduction, we studied its sensitivity to changes in membrane tension (stretch) in heterologous systems, F-11 cells and trigeminal neurons. Laminar shear stress increased TRESK currents by 22-30%. An increase in membrane tension induced by cell swelling (hypotonic medium) produced a reversible elevation of TRESK currents (39.9%). In contrast, cell shrinkage (hypertonic solution) produced the opposite effect. Membrane crenators or cup-formers produced equivalent effects. In trigeminal sensory neurons, TRESK channels were mechanically stimulated by negative pressure, which led to a 1.51-fold increase in channel open probability. TRESK-like currents in trigeminal neurons were additively inhibited by arachidonic acid, acidic pH and hypertonic stimulation, conditions usually found after tissue inflammation. Our results show that TRESK is modulated by changes in cell membrane tension and/or cell volume. Several key players released during inflammation or tissue injury could modulate sensory neuron activation through small changes in membrane tension.
引用
收藏
页数:12
相关论文
共 67 条
[11]   TRESK Background K+ Channel Is Inhibited by PAR-1/MARK Microtubule Affinity-Regulating Kinases in Xenopus Oocytes [J].
Braun, Gabriella ;
Nemcsics, Balazs ;
Enyedi, Peter ;
Czirjak, Gabor .
PLOS ONE, 2011, 6 (12)
[12]   TASK-3 two-pore domain potassium channels enable sustained high-frequency firing in cerebellar granule neurons [J].
Brickley, Stephen G. ;
Aller, M. Isabel ;
Sandu, Cristina ;
Veale, Emma L. ;
Alder, Felicity G. ;
Sambi, Harvinder ;
Mathie, Alistair ;
Wisden, William .
JOURNAL OF NEUROSCIENCE, 2007, 27 (35) :9329-9340
[13]  
Brierley SM, 2011, J PHYSIOL-LONDON, DOI [10.1113/jphysiol.2011.206789, DOI 10.1113/JPHY-SI0L.2011.206789]
[14]   Crystal Structure of the Human K2P TRAAK, a Lipid- and Mechano-Sensitive K+ Ion Channel [J].
Brohawn, Stephen G. ;
del Marmol, Josefina ;
MacKinnon, Roderick .
SCIENCE, 2012, 335 (6067) :436-441
[15]   Alkylamides that produce tingling paresthesia activate tactile and thermal trigeminal neurons [J].
Bryant, BP ;
Mezine, I .
BRAIN RESEARCH, 1999, 842 (02) :452-460
[16]   Drug therapy: Mechanisms of actions of inhaled anesthetics [J].
Campagna, JA ;
Miller, KW ;
Forman, SA .
NEW ENGLAND JOURNAL OF MEDICINE, 2003, 348 (21) :2110-2124
[17]   A phospholipid sensor controls mechanogating of the K+ channel TREK-1 [J].
Chemin, J ;
Patel, AJ ;
Duprat, F ;
Lauritzen, I ;
Lazdunski, M ;
Honoré, E .
EMBO JOURNAL, 2005, 24 (01) :44-53
[18]   Piezo proteins are pore-forming subunits of mechanically activated channels [J].
Coste, Bertrand ;
Xiao, Bailong ;
Santos, Jose S. ;
Syeda, Ruhma ;
Grandl, Joerg ;
Spencer, Kathryn S. ;
Kim, Sung Eun ;
Schmidt, Manuela ;
Mathur, Jayanti ;
Dubin, Adrienne E. ;
Montal, Mauricio ;
Patapoutian, Ardem .
NATURE, 2012, 483 (7388) :176-U72
[19]   Piezo1 and Piezo2 Are Essential Components of Distinct Mechanically Activated Cation Channels [J].
Coste, Bertrand ;
Mathur, Jayanti ;
Schmidt, Manuela ;
Earley, Taryn J. ;
Ranade, Sanjeev ;
Petrus, Matt J. ;
Dubin, Adrienne E. ;
Patapoutian, Ardem .
SCIENCE, 2010, 330 (6000) :55-60
[20]   Human ASIC3 channel dynamically adapts its activity to sense the extracellular pH in both acidic and alkaline directions [J].
Delaunay, Anne ;
Gasull, Xavier ;
Salinas, Miguel ;
Noel, Jacques ;
Friend, Valerie ;
Lingueglia, Eric ;
Deval, Emmanuel .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2012, 109 (32) :13124-13129