A cryo-tomography-based volumetric model of the actin core of mouse vestibular hair cell stereocilia lacking plastin 1.


Journal

Journal of structural biology
ISSN: 1095-8657
Titre abrégé: J Struct Biol
Pays: United States
ID NLM: 9011206

Informations de publication

Date de publication:
01 04 2020
Historique:
received: 05 12 2019
revised: 11 01 2020
accepted: 14 01 2020
pubmed: 22 1 2020
medline: 20 7 2021
entrez: 22 1 2020
Statut: ppublish

Résumé

Electron cryo-tomography allows for high-resolution imaging of stereocilia in their native state. Because their actin filaments have a higher degree of order, we imaged stereocilia from mice lacking the actin crosslinker plastin 1 (PLS1). We found that while stereocilia actin filaments run 13 nm apart in parallel for long distances, there were gaps of significant size that were stochastically distributed throughout the actin core. Actin crosslinkers were distributed through the stereocilium, but did not occupy all possible binding sites. At stereocilia tips, protein density extended beyond actin filaments, especially on the side of the tip where a tip link is expected to anchor. Along the shaft, repeating density was observed that corresponds to actin-to-membrane connectors. In the taper region, most actin filaments terminated near the plasma membrane. The remaining filaments twisted together to make a tighter bundle than was present in the shaft region; the spacing between them decreased from 13 nm to 9 nm, and the apparent filament diameter decreased from 6.4 to 4.8 nm. Our models illustrate detailed features of distinct structural domains that are present within the stereocilium.

Identifiants

pubmed: 31962158
pii: S1047-8477(20)30020-4
doi: 10.1016/j.jsb.2020.107461
pmc: PMC7067663
mid: NIHMS1555692
pii:
doi:

Substances chimiques

Actins 0
Membrane Glycoproteins 0
Microfilament Proteins 0
plastin 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

107461

Subventions

Organisme : NIGMS NIH HHS
ID : P01 GM051487
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01 DC011034
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM062968
Pays : United States

Informations de copyright

Copyright © 2020 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Références

Methods. 2017 Feb 15;115:80-90
pubmed: 27713081
J Neurosci. 2004 Jun 9;24(23):5445-56
pubmed: 15190118
J Neurobiol. 2002 Feb 5;50(2):81-92
pubmed: 11793356
J Neurosci. 2012 Mar 28;32(13):4600-9
pubmed: 22457506
Dev Biol. 2006 Mar 1;291(1):83-95
pubmed: 16413524
Elife. 2016 Jun 08;5:
pubmed: 27269051
J Neurosci. 1983 May;3(5):962-76
pubmed: 6601694
Proc Natl Acad Sci U S A. 2018 Jun 26;115(26):E5916-E5925
pubmed: 29891682
Cold Spring Harb Symp Quant Biol. 1990;55:547-61
pubmed: 1983446
Cell Rep. 2018 Oct 30;25(5):1268-1280.e4
pubmed: 30380417
Curr Biol. 2012 Feb 21;22(4):320-5
pubmed: 22264607
PLoS One. 2011;6(4):e14807
pubmed: 21625653
Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):13958-63
pubmed: 14610277
Biophys J. 2007 Aug 15;93(4):1124-33
pubmed: 17526588
J Mol Biol. 1997 Feb 21;266(2):331-42
pubmed: 9047367
J Comput Chem. 2004 Oct;25(13):1605-12
pubmed: 15264254
J Cell Biol. 1997 Jun 16;137(6):1287-307
pubmed: 9182663
J Cell Biol. 2018 Aug 6;217(8):2691-2708
pubmed: 29794031
J Cell Biol. 2016 Nov 21;215(4):467-482
pubmed: 27811163
J Neurosci. 2010 Jul 21;30(29):9683-94
pubmed: 20660251
J Cell Biol. 2004 Mar 15;164(6):887-97
pubmed: 15024034
J Neurosci. 2016 Mar 9;36(10):2945-56
pubmed: 26961949
J Cell Biol. 2004 Aug 16;166(4):559-70
pubmed: 15314067
Cell. 2000 Jan 21;100(2):221-8
pubmed: 10660045
Nat Commun. 2015 Apr 21;6:6855
pubmed: 25897778
Hear Res. 1980 Jan;2(1):39-43
pubmed: 7351390
Nature. 2017 Mar 9;543(7644):261-264
pubmed: 28241138
Hear Res. 1987;26(1):45-64
pubmed: 3558143
JCI Insight. 2019 Jun 20;4(12):
pubmed: 31217345
Cell. 2009 Oct 2;139(1):33-44
pubmed: 19804752
Elife. 2017 Mar 28;6:
pubmed: 28350294
Cold Spring Harb Symp Quant Biol. 1982;46 Pt 2:525-40
pubmed: 6955098
Biophys J. 2014 Jun 3;106(11):2519-28
pubmed: 24896132
Cytoskeleton (Hoboken). 2014 Jan;71(1):61-78
pubmed: 24285636
Elife. 2015 Aug 24;4:
pubmed: 26302205
Semin Cell Dev Biol. 2017 Nov;71:30-41
pubmed: 28851599
Curr Opin Struct Biol. 2017 Oct;46:149-156
pubmed: 28915442
Hear Res. 1985;20(3):245-60
pubmed: 3910630
Hear Res. 1993 Sep;69(1-2):163-75
pubmed: 8226337
Nature. 1995 Dec 14;378(6558):748-51
pubmed: 7501026
J Neurosci. 1998 Jun 15;18(12):4603-15
pubmed: 9614235
Elife. 2016 Aug 15;5:
pubmed: 27525485
J Struct Biol. 2019 May 1;206(2):149-155
pubmed: 30822456
Dev Biol. 1986 Jul;116(1):100-18
pubmed: 3732601
J Neurosci. 2003 Oct 8;23(27):9208-19
pubmed: 14534255
Annu Rev Neurosci. 1991;14:301-33
pubmed: 2031573
Biophys J. 2012 Jan 18;102(2):201-10
pubmed: 22339856
Am J Hum Genet. 2010 Mar 12;86(3):378-88
pubmed: 20170899
Cell Tissue Res. 1982;224(1):15-24
pubmed: 7201348
Cell Rep. 2015 Nov 17;13(7):1287-1294
pubmed: 26549442
Annu Rev Cell Biol. 1988;4:63-92
pubmed: 2461723
Cell Motil Cytoskeleton. 2002 Dec;53(4):326-36
pubmed: 12378542
Dev Biol. 1986 Jul;116(1):119-29
pubmed: 3732602
J Neurosci. 1998 Nov 1;18(21):8637-47
pubmed: 9786971
J Cell Biol. 1989 Oct;109(4 Pt 1):1711-23
pubmed: 2677026
Phys Rev Lett. 2009 Dec 4;103(23):238102
pubmed: 20366178
Neuron. 1991 Dec;7(6):985-94
pubmed: 1764247
J Neurosci. 2006 Oct 4;26(40):10188-98
pubmed: 17021174
J Cell Biol. 1997 Nov 3;139(3):683-93
pubmed: 9348285
Hear Res. 1982 Apr;6(3):277-89
pubmed: 6806231
Acta Otolaryngol. 1980 Nov-Dec;90(5-6):385-90
pubmed: 6163314
J Neurosci. 2013 May 8;33(19):8114-21
pubmed: 23658152
Nat Neurosci. 2013 Mar;16(3):365-74
pubmed: 23334578
Proc Natl Acad Sci U S A. 2013 Dec 17;110(51):20521-6
pubmed: 24306931
Sci Data. 2015 Sep 15;2:150047
pubmed: 26401315
Annu Rev Biochem. 2017 Jun 20;86:873-896
pubmed: 28426242
Acta Otolaryngol. 1983 Nov-Dec;96(5-6):407-12
pubmed: 6356776
Proc Natl Acad Sci U S A. 2004 Feb 24;101(8):2601-6
pubmed: 14983055
Nature. 1980 Sep 25;287(5780):291-6
pubmed: 6893482
Nature. 2012 Jan 15;481(7382):520-4
pubmed: 22246323
Molecules. 2018 Apr 11;23(4):
pubmed: 29641472
J Cell Biol. 1980 Jul;86(1):244-59
pubmed: 6893452
J Neurosci. 2006 Oct 4;26(40):10243-52
pubmed: 17021180
Cell. 2000 Aug 4;102(3):377-85
pubmed: 10975527
J Cell Biol. 1983 Mar;96(3):822-34
pubmed: 6682111
Physiol Rev. 2014 Jul;94(3):951-86
pubmed: 24987009
Biochem Soc Trans. 2018 Dec 17;46(6):1771
pubmed: 30514773
J Neurosci. 2008 Jun 18;28(25):6342-53
pubmed: 18562604
J Struct Biol. 1996 Jan-Feb;116(1):71-6
pubmed: 8742726
J Neurosci. 2017 Nov 29;37(48):11632-11646
pubmed: 29066559
Hear Res. 1985 May;18(2):177-88
pubmed: 4044419
Cell. 2010 May 28;141(5):786-98
pubmed: 20510926
Bioinformatics. 2011 Feb 15;27(4):582-3
pubmed: 21172911
Neuron. 2004 Oct 14;44(2):309-20
pubmed: 15473969
Nat Cell Biol. 2005 Feb;7(2):148-56
pubmed: 15654330

Auteurs

Junha Song (J)

Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Roma Patterson (R)

Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Zoltan Metlagel (Z)

Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Jocelyn F Krey (JF)

Oregon Hearing Research Center & Vollum Institute, Oregon Health & Science University, Portland, OR, USA.

Samantha Hao (S)

Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Linshanshan Wang (L)

Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Brian Ng (B)

Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.

Salim Sazzed (S)

Department of Computer Science, Old Dominion University, Norfolk, VA, USA.

Julio Kovacs (J)

Department of Mechanical and Aerospace Engineering, Old Dominion University, Norfolk, VA, USA.

Willy Wriggers (W)

Department of Mechanical and Aerospace Engineering, Old Dominion University, Norfolk, VA, USA.

Jing He (J)

Department of Computer Science, Old Dominion University, Norfolk, VA, USA.

Peter G Barr-Gillespie (PG)

Oregon Hearing Research Center & Vollum Institute, Oregon Health & Science University, Portland, OR, USA. Electronic address: gillespp@ohsu.edu.

Manfred Auer (M)

Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA. Electronic address: mauer@lbl.gov.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH