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Research Papers

Modeling the Mechanics of Tethers Pulled From the Cochlear Outer Hair Cell Membrane

[+] Author and Article Information
Kristopher R. Schumacher, Aleksander S. Popel, Alexander A. Spector

Department of Biomedical Engineering,  Johns Hopkins University, Baltimore, MD 21205

Bahman Anvari

Department of Bioengineering,  University of California-Riverside, Riverside, CA 92521

William E. Brownell

Bobby R. Alford Department of Otorhinolaryngology and Communicative Sciences,  Baylor College of Medicine, Houston, TX 77030

J Biomech Eng 130(3), 031007 (Apr 28, 2008) (11 pages) doi:10.1115/1.2907758 History: Received January 23, 2007; Revised September 12, 2007; Published April 28, 2008

Cell membrane tethers are formed naturally (e.g., in leukocyte rolling) and experimentally to probe membrane properties. In cochlear outer hair cells, the plasma membrane is part of the trilayer lateral wall, where the membrane is attached to the cytoskeleton by a system of radial pillars. The mechanics of these cells is important to the sound amplification and frequency selectivity of the ear. We present a modeling study to simulate the membrane deflection, bending, and interaction with the cytoskeleton in the outer hair cell tether pulling experiment. In our analysis, three regions of the membrane are considered: the body of a cylindrical tether, the area where the membrane is attached and interacts with the cytoskeleton, and the transition region between the two. By using a computational method, we found the shape of the membrane in all three regions over a range of tether lengths and forces observed in experiments. We also analyze the effects of biophysical properties of the membrane, including the bending modulus and the forces of the membrane adhesion to the cytoskeleton. The model’s results provide a better understanding of the mechanics of tethers pulled from cell membranes.

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Copyright © 2008 by American Society of Mechanical Engineers
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Figures

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Figure 1

Illustration of the cochlear OHC tether experiment, with a particular focus on the modeled region (i.e., where the membrane transitions from the tether and reattaches to the lateral wall). TeR, tether region; TrR, transition region; PAR, pillar attachment region; PM, plasma membrane; DP, detached pillar; AP, attached pillar; C, cytoskeleton.

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Figure 2

Meridional trace of the plasma membrane, including geometric parameters. TeR, tether region; TrR, transition region; PAR, pillar attachment region.

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Figure 3

An excised element of the plasma membrane, along with the relevant internal stresses and moments

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Figure 4

Illustration of the membrane∕cytoskeleton attachment region of the OHC

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Figure 5

The upward force, P1A1, on the plasma membrane is balanced by the downward force P2A2×(No. of pillars)

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Figure 6

An illustration of the maximum deflection before separation, i.e., the point at which Pcritical=kwmax

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Figure 7

The effect of the holding force on the plasma membrane shape. The profiles shown are at holding forces of 30pN, 60pN, and 90pN. (a) Normal deflection over whole domain and (b) normal deflection within the attachment zone only. The direction of the arrow indicates increased holding force.

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Figure 8

The effect of the holding force on the plasma membrane tension. The tension profiles shown in panel (a) are at holding forces of 30pN, 60pN, and 90pN and represent the detachment zone only. Panel (b) shows the radial component of tension at the detachment point (250nm) as it varies with the holding force, the data points represent results from our model, and the dashed line represents the predicted tension from the theoretical relationship, F=2π2BTr. The direction of the arrow indicates increased holding force.

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Figure 9

Effect of the bending modulus on the shape of the plasma membrane. The profiles are shown for bending modulus values of 30kBT, 66kBT, and 100kBT. (a) Normal deflection over whole domain and (b) normal deflection within the attachment zone only. The direction of the arrow indicates increased bending modulus.

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Figure 10

Effect of the adhesion modulus, k, on the shape of the plasma membrane. The profiles are shown for adhesion modulus values of 1.7×107pN∕μm3, 5.7×106pN∕μm3, and 2.8×106pN∕μm3. (a) Normal deflection over whole domain and (b) normal deflection within the attachment zone only. The direction of the arrow indicates increased adhesion modulus.

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Figure 11

Surface plots of the stored adhesion energy (a), and bending energy (b), within the attachment zone, over a range of bending moduli, B, and pillar spring constants, k

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Figure 12

Effect of changing the initial point of membrane-cytoskeleton detachment, Rd,ini, on the shape of the plasma membrane. The profiles are shown for initial radial detachment points of 90nm, 130nm, 170nm, 210nm, and 250nm. (a) Normal deflection over whole domain and (b) normal deflection within the attachment zone only. The direction of the arrow indicates increased detachment radius. Note that the 90nm and 130nm profiles are superimposed due to a membrane-pillar bond breakage in the 90nm case.

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Figure 13

The normal membrane displacement at the detachment point, wd, as a function of tether holding force, FT, at various detachment radius values, Rd,ini

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