Home LiteratureArticle Details
PMID: 21436032 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Usher type 1G protein sans is a critical component of the tip-link complex, a structure controlling actin polymerization in stereocilia.

Caberlotto E, Michel V, Foucher I, Bahloul A, Goodyear RJ, Pepermans E, Michalski N, Perfettini I, Alegria-Prévot O, Chardenoux S, Do Cruzeiro M, Hardelin JP, Richardson GP, Avan P, Weil D, Petit C

Abstract

The mechanotransducer channels of auditory hair cells are gated by tip-links, oblique filaments that interconnect the stereocilia of the hair bundle. Tip-links stretch from the tips of stereocilia in the short and middle rows to the sides of neighboring, taller stereocilia. They are made of cadherin-23 and protocadherin-15, products of the Usher syndrome type 1 genes USH1D and USH1F, respectively. In this study we address the role of sans, a putative scaffold protein and product of the USH1G gene. In Ush1g(-/-) mice, the cohesion of stereocilia is disrupted, and both the amplitude and the sensitivity of the transduction currents are reduced. In Ush1g(fl/fl)Myo15-cre(+/-) mice, the loss of sans occurs postnatally and the stereocilia remain cohesive. In these mice, there is a decrease in the amplitude of the total transducer current with no loss in sensitivity, and the tips of the stereocilia in the short and middle rows lose their prolate shape, features that can be attributed to the loss of tip-links. Furthermore, stereocilia from these rows undergo a dramatic reduction in length, suggesting that the mechanotransduction machinery has a positive effect on F-actin polymerization. Sans interacts with the cytoplasmic domains of cadherin-23 and protocadherin-15 in vitro and is absent from the hair bundle in mice defective for either of the two cadherins. Because sans localizes mainly to the tips of short- and middle-row stereocilia in vivo, we conclude that it belongs to a molecular complex at the lower end of the tip-link and plays a critical role in the maintenance of this link.

MeSH Terms
Actins/metabolism Analysis of Variance Animals Cadherin Related Proteins Cadherins/metabolism Cilia/metabolism Electrophysiology Fluorescent Antibody Technique Genetic Vectors/genetics Hair Cells, Auditory/metabolism,ultrastructure Immunohistochemistry Mice Mice, Knockout Microscopy, Electron, Scanning Nerve Tissue Proteins/genetics,metabolism Polymerization Protein Precursors/metabolism Signal Transduction/genetics,physiology
Chemicals
Actins CDHR15 protein, mouse Cadherin Related Proteins Cadherins Cdh23 protein, mouse Nerve Tissue Proteins Protein Precursors Sans protein, mouse
Authors & Affiliations
16 authors, click to expand affiliations / ORCID
Caberlotto Elisa
Unité de Génétique et Physiologie de l'Audition, Institut Pasteur, 75724 Paris cedex 15, France.
Michel Vincent
Foucher Isabelle
Bahloul Amel
Goodyear Richard J
Pepermans Elise
Michalski Nicolas
Perfettini Isabelle
Alegria-Prévot Olinda
Chardenoux Sébastien
Do Cruzeiro Marcio
Hardelin Jean-Pierre
Richardson Guy P
Avan Paul
Weil Dominique
Petit Christine
References (34)
34 references, click to expand
  1. Mutations in a new scaffold protein Sans cause deafness in Jackson shaker mice.
    Hum Mol Genet. 2003 Mar 1;12(5):453-61 PMID: 12588793
  2. Cadherin-23, myosin VIIa and harmonin, encoded by Usher syndrome type I genes, form a ternary complex and interact with membrane phospholipids.
    Hum Mol Genet. 2010 Sep 15;19(18):3557-65 PMID: 20639393
  3. Tonotopic gradient in the developmental acquisition of sensory transduction in outer hair cells of the mouse cochlea.
    J Neurophysiol. 2009 Jun;101(6):2961-73 PMID: 19339464
  4. Harmonin-b, an actin-binding scaffold protein, is involved in the adaptation of mechanoelectrical transduction by sensory hair cells.
    Pflugers Arch. 2009 Nov;459(1):115-30 PMID: 19756723
  5. The tip-link antigen, a protein associated with the transduction complex of sensory hair cells, is protocadherin-15.
    J Neurosci. 2006 Jun 28;26(26):7022-34 PMID: 16807332
  6. Interactions in the network of Usher syndrome type 1 proteins.
    Hum Mol Genet. 2005 Feb 1;14(3):347-56 PMID: 15590703
  7. Stepwise morphological and functional maturation of mechanotransduction in rat outer hair cells.
    J Neurosci. 2007 Dec 12;27(50):13890-902 PMID: 18077701
  8. Myosin VIIa, harmonin and cadherin 23, three Usher I gene products that cooperate to shape the sensory hair cell bundle.
    EMBO J. 2002 Dec 16;21(24):6689-99 PMID: 12485990
  9. Maternally expressed PGK-Cre transgene as a tool for early and uniform activation of the Cre site-specific recombinase.
    Transgenic Res. 1998 Mar;7(2):105-12 PMID: 9608738
  10. Cross-links between stereocilia in the guinea pig cochlea.
    Hear Res. 1985 May;18(2):177-88 PMID: 4044419
  11. Cadherin 23 and protocadherin 15 interact to form tip-link filaments in sensory hair cells.
    Nature. 2007 Sep 6;449(7158):87-91 PMID: 17805295
  12. Dynamic length regulation of sensory stereocilia.
    Semin Cell Dev Biol. 2008 Dec;19(6):502-10 PMID: 18692583
  13. Cadherin 23 is a component of the transient lateral links in the developing hair bundles of cochlear sensory cells.
    Dev Biol. 2005 Apr 15;280(2):281-94 PMID: 15882573
  14. Rapid renewal of auditory hair bundles.
    Nature. 2002 Aug 22;418(6900):837-8 PMID: 12192399
  15. The Usher syndrome proteins cadherin 23 and harmonin form a complex by means of PDZ-domain interactions.
    Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14946-51 PMID: 12407180
  16. The dimensions and structural attachments of tip links in mammalian cochlear hair cells and the effects of exposure to different levels of extracellular calcium.
    Neuroscience. 2008 Jun 12;154(1):10-21 PMID: 18384968
  17. Cochlear outer hair cells undergo an apical circumference remodeling constrained by the hair bundle shape.
    Development. 2010 Apr;137(8):1373-83 PMID: 20332152
  18. Mechanotransduction by hair cells: models, molecules, and mechanisms.
    Cell. 2009 Oct 2;139(1):33-44 PMID: 19804752
  19. Adhesion-mediated mechanosensitivity: a time to experiment, and a time to theorize.
    Curr Opin Cell Biol. 2006 Oct;18(5):472-81 PMID: 16930976
  20. Asymmetric distribution of cadherin 23 and protocadherin 15 in the kinocilial links of avian sensory hair cells.
    J Comp Neurol. 2010 Nov 1;518(21):4288-97 PMID: 20853507
  21. Assembling stable hair cell tip link complex via multidentate interactions between harmonin and cadherin 23.
    Proc Natl Acad Sci U S A. 2009 Apr 7;106(14):5575-80 PMID: 19297620
  22. Physical and functional interaction between protocadherin 15 and myosin VIIa in mechanosensory hair cells.
    J Neurosci. 2006 Feb 15;26(7):2060-71 PMID: 16481439
  23. Cadherin 23 is a component of the tip link in hair-cell stereocilia.
    Nature. 2004 Apr 29;428(6986):950-5 PMID: 15057245
  24. Actin filaments, stereocilia, and hair cells of the bird cochlea. V. How the staircase pattern of stereociliary lengths is generated.
    J Cell Biol. 1988 Feb;106(2):355-65 PMID: 3339095
  25. Cross-links between stereocilia in the guinea pig organ of Corti, and their possible relation to sensory transduction.
    Hear Res. 1984 Aug;15(2):103-12 PMID: 6436216
  26. Linking genes underlying deafness to hair-bundle development and function.
    Nat Neurosci. 2009 Jun;12(6):703-10 PMID: 19471269
  27. Usher I syndrome: unravelling the mechanisms that underlie the cohesion of the growing hair bundle in inner ear sensory cells.
    J Cell Sci. 2005 Oct 15;118(Pt 20):4593-603 PMID: 16219682
  28. The structure of the harmonin/sans complex reveals an unexpected interaction mode of the two Usher syndrome proteins.
    Proc Natl Acad Sci U S A. 2010 Mar 2;107(9):4040-5 PMID: 20142502
  29. A core cochlear phenotype in USH1 mouse mutants implicates fibrous links of the hair bundle in its cohesion, orientation and differential growth.
    Development. 2008 Apr;135(8):1427-37 PMID: 18339676
  30. CD1 hearing-impaired mice. I: Distortion product otoacoustic emission levels, cochlear function and morphology.
    Hear Res. 1998 Jun;120(1-2):37-50 PMID: 9667429
  31. Properties of auditory nerve responses in absence of outer hair cells.
    J Neurophysiol. 1978 Mar;41(2):365-83 PMID: 650272
  32. Localization of inner hair cell mechanotransducer channels using high-speed calcium imaging.
    Nat Neurosci. 2009 May;12(5):553-8 PMID: 19330002
  33. Stereocilin-deficient mice reveal the origin of cochlear waveform distortions.
    Nature. 2008 Nov 13;456(7219):255-8 PMID: 18849963
  34. How the ear's works work: mechanoelectrical transduction and amplification by hair cells.
    C R Biol. 2005 Feb;328(2):155-62 PMID: 15771001
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2011-04-05
Epub
2011-00-21
Pages
5825-30
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3078398
Subset
IM
Grants
Wellcome Trust · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com