Forces between clustered stereocilia minimize friction in the ear on a subnanometre scale

被引:62
作者
Kozlov, Andrei S. [1 ,2 ]
Baumgart, Johannes [3 ]
Risler, Thomas [4 ,5 ,6 ]
Versteegh, Corstiaen P. C. [1 ,2 ,7 ]
Hudspeth, A. J. [1 ,2 ]
机构
[1] Rockefeller Univ, Howard Hughes Med Inst, New York, NY 10065 USA
[2] Rockefeller Univ, Lab Sensory Neurosci, New York, NY 10065 USA
[3] Tech Univ Dresden, Dept Math, Inst Comp Sci, D-01062 Dresden, Germany
[4] Inst Curie, Ctr Rech, F-75005 Paris, France
[5] Univ Paris 06, UMR 168, F-75005 Paris, France
[6] CNRS, UMR 168, F-75005 Paris, France
[7] Wageningen Univ, Expt Zool Grp, NL-6709 PG Wageningen, Netherlands
关键词
HAIR CELL STEREOCILIA; TRANSDUCTION CHANNELS; MECHANICAL AMPLIFICATION; COHERENT MOTION; BUNDLE; MEMBRANE;
D O I
10.1038/nature10073
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 detection of sound begins when energy derived from an acoustic stimulus deflects the hair bundles on top of hair cells(1). As hair bundles move, the viscous friction between stereocilia and the surrounding liquid poses a fundamental physical challenge to the ear's high sensitivity and sharp frequency selectivity. Part of the solution to this problem lies in the active process that uses energy for frequency-selective sound amplification(2,3). Here we demonstrate that a complementary part of the solution involves the fluid-structure interaction between the liquid within the hair bundle and the stereocilia. Using force measurement on a dynamically scaled model, finite-element analysis, analytical estimation of hydrodynamic forces, stochastic simulation and high-resolution interferometric measurement of hair bundles, we characterize the origin and magnitude of the forces between individual stereocilia during small hair-bundle deflections. We find that the close apposition of stereocilia effectively immobilizes the liquid between them, which reduces the drag and suppresses the relative squeezing but not the sliding mode of stereociliary motion. The obliquely oriented tip links couple the mechanotransduction channels to this least dissipative coherent mode, whereas the elastic horizontal top connectors that stabilize the structure further reduce the drag. As measured from the distortion products associated with channel gating at physiological stimulation amplitudes of tens of nanometres, the balance of viscous and elastic forces in a hair bundle permits a relative mode of motion between adjacent stereocilia that encompasses only a fraction of a nanometre. A combination of high-resolution experiments and detailed numerical modelling of fluid-structure interactions reveals the physical principles behind the basic structural features of hair bundles and shows quantitatively how these organelles are adapted to the needs of sensitive mechanotransduction.
引用
收藏
页码:376 / 379
页数:4
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