3D Ultrastructure of the Cochlear Outer Hair Cell Lateral Wall Revealed By Electron Tomography

Triffo, William Jeffrey; Palsdottir, Hildur; Song, Junha; Morgan, David Gene; McDonald, Kent L.; Auer, Manfred; Raphael, Robert M.

doi:10.3389/fncel.2019.00560

Title: 3D Ultrastructure of the Cochlear Outer Hair Cell Lateral Wall Revealed By Electron Tomography

Abstract

Outer Hair Cells (OHCs) in the mammalian cochlea display a unique type of voltage-induced mechanical movement termed electromotility, which amplifies auditory signals and contributes to the sensitivity and frequency selectivity of mammalian hearing. Electromotility occurs in the OHC lateral wall, but it is not fully understood how the supramolecular architecture of the lateral wall enables this unique form of cellular motility. Employing electron tomography of high-pressure frozen and freeze-substituted OHCs, we visualized the 3D structure and organization of the membrane and cytoskeletal components of the OHC lateral wall. The subsurface cisterna (SSC) is a highly prominent feature, and we report that the SSC membranes and lumen possess hexagonally ordered arrays of particles. We also find the SSC is tightly connected to adjacent actin filaments by short filamentous protein connections. Pillar proteins that join the plasma membrane to the cytoskeleton appear as variable structures considerably thinner than actin filaments and significantly more flexible than actin-SSC links. The structurally rich organization and rigidity of the SSC coupled with apparently weaker mechanical connections between the plasma membrane (PM) and cytoskeleton reveal that the membrane-cytoskeletal architecture of the OHC lateral wall is more complex than previously appreciated. These observations are important for our understandingmore »« less

Authors:: Triffo, William Jeffrey; Palsdottir, Hildur; Song, Junha; Morgan, David Gene; McDonald, Kent L.; Auer, Manfred; Raphael, Robert M.

Publication Date:: Fri Dec 20 00:00:00 EST 2019

Research Org.:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC); National Science Foundation (NSF); National Institutes of Health (NIH)

OSTI Identifier:: 1580126

Alternate Identifier(s):: OSTI ID: 1599792

Grant/Contract Number:: AC02-05CH11231; FG02-97ER25308; AC03-76SF00098; 5F30DC009359; 044379; DC009622; DC0008134; DC07680

Resource Type:: Published Article

Journal Name:: Frontiers in Cellular Neuroscience

Additional Journal Information:: Journal Name: Frontiers in Cellular Neuroscience Journal Volume: 13; Journal ID: ISSN 1662-5102

Publisher:: Frontiers Media SA

Country of Publication:: Switzerland

Language:: English

Subject:: 60 APPLIED LIFE SCIENCES; outer hair cell (OHC); subsurface cisternae; cortical cytoskeleton; high pressure freezing and freeze substitution; electron tomography (ET)

Citation Formats


                    Triffo, William Jeffrey, Palsdottir, Hildur, Song, Junha, Morgan, David Gene, McDonald, Kent L., Auer, Manfred, and Raphael, Robert M. 3D Ultrastructure of the Cochlear Outer Hair Cell Lateral Wall Revealed By Electron Tomography.  Switzerland: N. p., 2019. 
Web.  doi:10.3389/fncel.2019.00560.

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                    Triffo, William Jeffrey, Palsdottir, Hildur, Song, Junha, Morgan, David Gene, McDonald, Kent L., Auer, Manfred, & Raphael, Robert M. 3D Ultrastructure of the Cochlear Outer Hair Cell Lateral Wall Revealed By Electron Tomography.  Switzerland.  https://doi.org/10.3389/fncel.2019.00560

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                    Triffo, William Jeffrey, Palsdottir, Hildur, Song, Junha, Morgan, David Gene, McDonald, Kent L., Auer, Manfred, and Raphael, Robert M. Fri .  
"3D Ultrastructure of the Cochlear Outer Hair Cell Lateral Wall Revealed By Electron Tomography".  Switzerland.  https://doi.org/10.3389/fncel.2019.00560.

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@article{osti_1580126,

  title        = {3D Ultrastructure of the Cochlear Outer Hair Cell Lateral Wall Revealed By Electron Tomography},

  author       = {Triffo, William Jeffrey and Palsdottir, Hildur and Song, Junha and Morgan, David Gene and McDonald, Kent L. and Auer, Manfred and Raphael, Robert M.},

  abstractNote = {Outer Hair Cells (OHCs) in the mammalian cochlea display a unique type of voltage-induced mechanical movement termed electromotility, which amplifies auditory signals and contributes to the sensitivity and frequency selectivity of mammalian hearing. Electromotility occurs in the OHC lateral wall, but it is not fully understood how the supramolecular architecture of the lateral wall enables this unique form of cellular motility. Employing electron tomography of high-pressure frozen and freeze-substituted OHCs, we visualized the 3D structure and organization of the membrane and cytoskeletal components of the OHC lateral wall. The subsurface cisterna (SSC) is a highly prominent feature, and we report that the SSC membranes and lumen possess hexagonally ordered arrays of particles. We also find the SSC is tightly connected to adjacent actin filaments by short filamentous protein connections. Pillar proteins that join the plasma membrane to the cytoskeleton appear as variable structures considerably thinner than actin filaments and significantly more flexible than actin-SSC links. The structurally rich organization and rigidity of the SSC coupled with apparently weaker mechanical connections between the plasma membrane (PM) and cytoskeleton reveal that the membrane-cytoskeletal architecture of the OHC lateral wall is more complex than previously appreciated. These observations are important for our understanding of OHC mechanics and need to be considered in computational models of OHC electromotility that incorporate subcellular features.},

  doi          = {10.3389/fncel.2019.00560},

  journal      = {Frontiers in Cellular Neuroscience},

  number       = ,

  volume       = 13,

  place        = {Switzerland},

  year         = {Fri Dec 20 00:00:00 EST 2019},

  month        = {Fri Dec 20 00:00:00 EST 2019}

}

Copy to clipboard

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Title: 3D Ultrastructure of the Cochlear Outer Hair Cell Lateral Wall Revealed By Electron Tomography

Abstract

Citation Formats

A fast motile response in guinea-pig outer hair cells: the cellular basis of the cochlear amplifier. journal, July 1987

Prestin-Based Outer Hair Cell Motility Is Necessary for Mammalian Cochlear Amplification journal, May 2008

Whole cell currents and mechanical responses of isolated outer hair cells journal, September 1988

Outer Hair Cell Electromotility and Otoacoustic Emissions journal, January 1990

Micro- and Nanomechanics of the Cochlear Outer Hair Cell journal, August 2001

Characterization of inner ear sensory hair cells after rapid-freezing and freeze-substitution journal, May 1992

Theory of electrically driven shape changes of cochlear outer hair cells journal, July 1993

A General Approach to Modeling Conduction and Concentration Dynamics in Excitable Cells of Concentric Cylindrical Geometry journal, August 1999

Electrokinetic shape changes of cochlear outer hair cells journal, July 1986

A membrane-based force generation mechanism in auditory sensory cells. journal, September 1992

A cytoskeletal spring in cochlear outer hair cells journal, October 1988

Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier journal, August 2002

Comparative ultrastructure of subsurface cisternae in inner and outer hair cells of the guinea pig cochlea journal, January 1990

Amphipath-Induced Nanoscale Changes in Outer Hair Cell Plasma Membrane Curvature journal, January 2009

Spectrin, actin and the structure of the cortical lattice in mammalian cochlear outer hair cells journal, June 1990

Longitudinal and radial differences in the subsurface cisternal system in the gerbil cochlea journal, April 1995

Mechanical properties of the lateral cortex of mammalian auditory outer hair cells journal, July 1996

Evoked mechanical responses of isolated cochlear outer hair cells journal, January 1985

Motility voltage sensor of the outer hair cell resides within the lateral plasma membrane. journal, December 1994

Excess plasma membrane and effects of ionic amphipaths on mechanics of outer hair cell lateral wall journal, May 2002

Nature of the motor element in electrokinetic shape changes of cochlear outer hair cells journal, March 1991

Structural features of the lateral walls in mammalian cochlear outer hair cells journal, September 1991

UCSF Chimera?A visualization system for exploratory research and analysis journal, January 2004

Mechanisms of movement in outer hair cells and a possible structural basis journal, April 1986

Cochlear Outer Hair Cell Motility journal, January 2008

Tuning in to the Amazing Outer Hair Cell: Membrane Wizardry with a Twist and Shout journal, January 2006

Structure of Ca2+ Release Channel at 14Å Resolution journal, January 2005

The influence of the subsurface cisterna on the electrical properties of the outer hair cell journal, January 1997

A membrane motor model for the fast motility of the outer hair cell journal, October 1994

Controlled microaspiration for high-pressure freezing: a new method for ultrastructural preservation of fragile and sparse tissues for TEM and electron tomography: CONTROLLED MICRO ASPIRATION FOR HIGH-PRESSURE FREEZING journal, April 2008

Concomitant salicylate-induced alterations of outer hair cell subsurface cisternae and electromotility journal, August 1991

Freeze-substitution: the addition of water to polar solvents enhances the retention of structure and acts at temperatures around -60°C: FREEZE-SUBSTITUTION journal, April 2008

Diflunisal inhibits prestin by chloride-dependent mechanism journal, August 2017

Prestin is the motor protein of cochlear outer hair cells journal, May 2000

Visualizing density maps with UCSF Chimera journal, January 2007

Regulation of electromotility in the cochlear outer hair cell: Electromotility in the cochlear outer hair cell journal, September 2006

Action of 2,3-butanedione monoxime on capacitance and electromotility of guinea-pig cochlear outer hair cells journal, March 2001

The location and mechanism of electromotility in guinea pig outer hair cells journal, August 1993

A Membrane Bending Model of Outer Hair Cell Electromotility journal, June 2000

Characterization of cochlear outer hair cell turgor journal, February 1994

Prestin-based outer hair cell electromotility in knockin mice does not appear to adjust the operating point of a cilia-based amplifier journal, July 2007

Cryoimmobilization and three-dimensional visualization of C. elegans ultrastructure journal, October 2003

Freeze substitution of high-pressure frozen samples: the visibility of biological membranes is improved when the substitution medium contains water journal, October 2002

Density of motility-related charge in the outer hair cell of the guinea pig is inversely related to best frequency journal, November 1998

Electromechanical Models of the Outer Hair Cell Composite Membrane journal, January 2006

Current concept of outer hair cell motility journal, October 2000

Ryanodine receptor localisation in the mammalian cochlea: An ultrastructural study journal, September 2006

Integrating the active process of hair cells with cochlear function journal, August 2014

Imaging of the cortical cytoskeleton of guinea pig outer hair cells using atomic force microscopy journal, January 2004

Fluorescence-Imaged Microdeformation of the Outer Hair Cell Lateral Wall journal, January 1998

An Electrical Inspection of the Subsurface Cisternae of the Outer Hair Cell journal, February 2015

Evidence for a Highly Elastic Shell-Core Organization of Cochlear Outer Hair Cells by Local Membrane Indentation journal, April 2005

Automated electron microscope tomography using robust prediction of specimen movements journal, October 2005

High-Pressure Freezing, Cellular Tomography, and Structural Cell Biology journal, August 2006

Structure of the cortical cytoskeleton in mammalian outer hair cells journal, July 1992

Computer Visualization of Three-Dimensional Image Data Using IMOD journal, January 1996

A fast motile response in guinea-pig outer hair cells: the cellular basis of the cochlear amplifier.
journal, July 1987

Prestin-Based Outer Hair Cell Motility Is Necessary for Mammalian Cochlear Amplification
journal, May 2008

Whole cell currents and mechanical responses of isolated outer hair cells
journal, September 1988

Outer Hair Cell Electromotility and Otoacoustic Emissions
journal, January 1990

Micro- and Nanomechanics of the Cochlear Outer Hair Cell
journal, August 2001

Characterization of inner ear sensory hair cells after rapid-freezing and freeze-substitution
journal, May 1992

Theory of electrically driven shape changes of cochlear outer hair cells
journal, July 1993

A General Approach to Modeling Conduction and Concentration Dynamics in Excitable Cells of Concentric Cylindrical Geometry
journal, August 1999

Electrokinetic shape changes of cochlear outer hair cells
journal, July 1986

A membrane-based force generation mechanism in auditory sensory cells.
journal, September 1992

A cytoskeletal spring in cochlear outer hair cells
journal, October 1988

Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier
journal, August 2002

Comparative ultrastructure of subsurface cisternae in inner and outer hair cells of the guinea pig cochlea
journal, January 1990

Amphipath-Induced Nanoscale Changes in Outer Hair Cell Plasma Membrane Curvature
journal, January 2009

Spectrin, actin and the structure of the cortical lattice in mammalian cochlear outer hair cells
journal, June 1990

Longitudinal and radial differences in the subsurface cisternal system in the gerbil cochlea
journal, April 1995

Mechanical properties of the lateral cortex of mammalian auditory outer hair cells
journal, July 1996

Evoked mechanical responses of isolated cochlear outer hair cells
journal, January 1985

Motility voltage sensor of the outer hair cell resides within the lateral plasma membrane.
journal, December 1994

Excess plasma membrane and effects of ionic amphipaths on mechanics of outer hair cell lateral wall
journal, May 2002

Nature of the motor element in electrokinetic shape changes of cochlear outer hair cells
journal, March 1991

Structural features of the lateral walls in mammalian cochlear outer hair cells
journal, September 1991

UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004

Mechanisms of movement in outer hair cells and a possible structural basis
journal, April 1986

Cochlear Outer Hair Cell Motility
journal, January 2008

Tuning in to the Amazing Outer Hair Cell: Membrane Wizardry with a Twist and Shout
journal, January 2006

Structure of Ca2+ Release Channel at 14Å Resolution
journal, January 2005

The influence of the subsurface cisterna on the electrical properties of the outer hair cell
journal, January 1997

A membrane motor model for the fast motility of the outer hair cell
journal, October 1994

Controlled microaspiration for high-pressure freezing: a new method for ultrastructural preservation of fragile and sparse tissues for TEM and electron tomography: CONTROLLED MICRO ASPIRATION FOR HIGH-PRESSURE FREEZING
journal, April 2008

Concomitant salicylate-induced alterations of outer hair cell subsurface cisternae and electromotility
journal, August 1991

Freeze-substitution: the addition of water to polar solvents enhances the retention of structure and acts at temperatures around -60°C: FREEZE-SUBSTITUTION
journal, April 2008

Diflunisal inhibits prestin by chloride-dependent mechanism
journal, August 2017

Prestin is the motor protein of cochlear outer hair cells
journal, May 2000

Visualizing density maps with UCSF Chimera
journal, January 2007

Regulation of electromotility in the cochlear outer hair cell: Electromotility in the cochlear outer hair cell
journal, September 2006

Action of 2,3-butanedione monoxime on capacitance and electromotility of guinea-pig cochlear outer hair cells
journal, March 2001

The location and mechanism of electromotility in guinea pig outer hair cells
journal, August 1993

A Membrane Bending Model of Outer Hair Cell Electromotility
journal, June 2000

Characterization of cochlear outer hair cell turgor
journal, February 1994

Prestin-based outer hair cell electromotility in knockin mice does not appear to adjust the operating point of a cilia-based amplifier
journal, July 2007

Cryoimmobilization and three-dimensional visualization of C. elegans ultrastructure
journal, October 2003

Freeze substitution of high-pressure frozen samples: the visibility of biological membranes is improved when the substitution medium contains water
journal, October 2002

Density of motility-related charge in the outer hair cell of the guinea pig is inversely related to best frequency
journal, November 1998

Electromechanical Models of the Outer Hair Cell Composite Membrane
journal, January 2006

Current concept of outer hair cell motility
journal, October 2000

Ryanodine receptor localisation in the mammalian cochlea: An ultrastructural study
journal, September 2006

Integrating the active process of hair cells with cochlear function
journal, August 2014

Imaging of the cortical cytoskeleton of guinea pig outer hair cells using atomic force microscopy
journal, January 2004

Fluorescence-Imaged Microdeformation of the Outer Hair Cell Lateral Wall
journal, January 1998

An Electrical Inspection of the Subsurface Cisternae of the Outer Hair Cell
journal, February 2015

Evidence for a Highly Elastic Shell-Core Organization of Cochlear Outer Hair Cells by Local Membrane Indentation
journal, April 2005

Automated electron microscope tomography using robust prediction of specimen movements
journal, October 2005

High-Pressure Freezing, Cellular Tomography, and Structural Cell Biology
journal, August 2006

Structure of the cortical cytoskeleton in mammalian outer hair cells
journal, July 1992

Computer Visualization of Three-Dimensional Image Data Using IMOD
journal, January 1996