Literature DB >> 25313064

Reaction-diffusion model of hair-bundle morphogenesis.

Adrian Jacobo1, A J Hudspeth2.   

Abstract

The hair bundle, an apical specialization of the hair cell composed of several rows of regularly organized stereocilia and a kinocilium, is essential for mechanotransduction in the ear. Its precise organization allows the hair bundle to convert mechanical stimuli to electrical signals; mutations that alter the bundle's morphology often cause deafness. However, little is known about the proteins involved in the process of morphogenesis and how the structure of the bundle arises through interactions between these molecules. We present a mathematical model based on simple reaction-diffusion mechanisms that can reproduce the shape and organization of the hair bundle. This model suggests that the boundary of the cell and the kinocilium act as signaling centers that establish the bundle's shape. The interaction of two proteins forms a hexagonal Turing pattern--a periodic modulation of the concentrations of the morphogens, sustained by local activation and long-range inhibition of the reactants--that sets a blueprint for the location of the stereocilia. Finally we use this model to predict how different alterations to the system might impact the shape and organization of the hair bundle.

Entities:  

Keywords:  Turing pattern; auditory system; development; hair cell; vestibular system

Mesh:

Year:  2014        PMID: 25313064      PMCID: PMC4217459          DOI: 10.1073/pnas.1417420111

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  27 in total

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Authors:  K Denman-Johnson; A Forge
Journal:  J Neurocytol       Date:  1999 Oct-Nov

Review 2.  Genetic insights into the morphogenesis of inner ear hair cells.

Authors:  Gregory I Frolenkov; Inna A Belyantseva; Thomas B Friedman; Andrew J Griffith
Journal:  Nat Rev Genet       Date:  2004-07       Impact factor: 53.242

3.  Lateral diffusion of membrane proteins.

Authors:  Sivaramakrishnan Ramadurai; Andrea Holt; Victor Krasnikov; Geert van den Bogaart; J Antoinette Killian; Bert Poolman
Journal:  J Am Chem Soc       Date:  2009-09-09       Impact factor: 15.419

4.  Myosin XVa and whirlin, two deafness gene products required for hair bundle growth, are located at the stereocilia tips and interact directly.

Authors:  Benjamin Delprat; Vincent Michel; Richard Goodyear; Yasuhiro Yamasaki; Nicolas Michalski; Aziz El-Amraoui; Isabelle Perfettini; Pierre Legrain; Guy Richardson; Jean-Pierre Hardelin; Christine Petit
Journal:  Hum Mol Genet       Date:  2004-12-08       Impact factor: 6.150

Review 5.  Developmental pattern formation: insights from physics and biology.

Authors:  Anna Kicheva; Michael Cohen; James Briscoe
Journal:  Science       Date:  2012-10-12       Impact factor: 47.728

6.  Positional information and the spatial pattern of cellular differentiation.

Authors:  L Wolpert
Journal:  J Theor Biol       Date:  1969-10       Impact factor: 2.691

Review 7.  The primary cilium: a signalling centre during vertebrate development.

Authors:  Sarah C Goetz; Kathryn V Anderson
Journal:  Nat Rev Genet       Date:  2010-05       Impact factor: 53.242

8.  On the spontaneous emergence of cell polarity.

Authors:  Steven J Altschuler; Sigurd B Angenent; Yanqin Wang; Lani F Wu
Journal:  Nature       Date:  2008-08-14       Impact factor: 49.962

9.  A core cochlear phenotype in USH1 mouse mutants implicates fibrous links of the hair bundle in its cohesion, orientation and differential growth.

Authors:  Gaelle Lefèvre; Vincent Michel; Dominique Weil; Léa Lepelletier; Emilie Bizard; Uwe Wolfrum; Jean-Pierre Hardelin; Christine Petit
Journal:  Development       Date:  2008-03-13       Impact factor: 6.868

Review 10.  Making an effort to listen: mechanical amplification in the ear.

Authors:  A J Hudspeth
Journal:  Neuron       Date:  2008-08-28       Impact factor: 17.173

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  12 in total

1.  Tissue self-organization underlies morphogenesis of the notochord.

Authors:  James Norman; Emma L Sorrell; Yi Hu; Vaishnavi Siripurapu; Jamie Garcia; Jennifer Bagwell; Patrick Charbonneau; Sharon R Lubkin; Michel Bagnat
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2018-09-24       Impact factor: 6.237

Review 2.  Self-organization across scales: from molecules to organisms.

Authors:  Tanumoy Saha; Milos Galic
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2018-05-26       Impact factor: 6.237

3.  A compartmentalized signaling network mediates crossover control in meiosis.

Authors:  Liangyu Zhang; Simone Köhler; Regina Rillo-Bohn; Abby F Dernburg
Journal:  Elife       Date:  2018-03-09       Impact factor: 8.140

4.  Neurog1 can partially substitute for Atoh1 function in hair cell differentiation and maintenance during organ of Corti development.

Authors:  Israt Jahan; Ning Pan; Jennifer Kersigo; Bernd Fritzsch
Journal:  Development       Date:  2015-07-24       Impact factor: 6.868

Review 5.  The mechanical forces that shape our senses.

Authors:  Anh Phuong Le; Jin Kim; Karl R Koehler
Journal:  Development       Date:  2022-03-31       Impact factor: 6.862

Review 6.  Developmental regulation of planar cell polarity and hair-bundle morphogenesis in auditory hair cells: lessons from human and mouse genetics.

Authors:  Xiaowei Lu; Conor W Sipe
Journal:  Wiley Interdiscip Rev Dev Biol       Date:  2015-08-11       Impact factor: 5.814

7.  The GPSM2/LGN GoLoco motifs are essential for hearing.

Authors:  Yoni Bhonker; Amal Abu-Rayyan; Kathy Ushakov; Liat Amir-Zilberstein; Shaked Shivatzki; Ofer Yizhar-Barnea; Tal Elkan-Miller; Einav Tayeb-Fligelman; Sun Myoung Kim; Meytal Landau; Moien Kanaan; Ping Chen; Fumio Matsuzaki; David Sprinzak; Karen B Avraham
Journal:  Mamm Genome       Date:  2015-12-11       Impact factor: 2.957

8.  A Biophysical Model for the Staircase Geometry of Stereocilia.

Authors:  Gilad Orly; Uri Manor; Nir S Gov
Journal:  PLoS One       Date:  2015-07-24       Impact factor: 3.240

9.  Stereocilia-staircase spacing is influenced by myosin III motors and their cargos espin-1 and espin-like.

Authors:  Seham Ebrahim; Matthew R Avenarius; M'hamed Grati; Jocelyn F Krey; Alanna M Windsor; Aurea D Sousa; Angela Ballesteros; Runjia Cui; Bryan A Millis; Felipe T Salles; Michelle A Baird; Michael W Davidson; Sherri M Jones; Dongseok Choi; Lijin Dong; Manmeet H Raval; Christopher M Yengo; Peter G Barr-Gillespie; Bechara Kachar
Journal:  Nat Commun       Date:  2016-03-01       Impact factor: 14.919

Review 10.  Assembly of hair bundles, an amazing problem for cell biology.

Authors:  Peter-G Barr-Gillespie
Journal:  Mol Biol Cell       Date:  2015-08-01       Impact factor: 4.138

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