Literature DB >> 29109250

Molecular basis of tactile specialization in the duck bill.

Eve R Schneider1, Evan O Anderson1, Marco Mastrotto1,2,3, Jon D Matson1, Vincent P Schulz4, Patrick G Gallagher4,5, Robert H LaMotte2,6, Elena O Gracheva7,2,3, Sviatoslav N Bagriantsev7.   

Abstract

Tactile-foraging ducks are specialist birds known for their touch-dependent feeding behavior. They use dabbling, straining, and filtering to find edible matter in murky water, relying on the sense of touch in their bill. Here, we present the molecular characterization of embryonic duck bill, which we show contains a high density of mechanosensory corpuscles innervated by functional rapidly adapting trigeminal afferents. In contrast to chicken, a visually foraging bird, the majority of duck trigeminal neurons are mechanoreceptors that express the Piezo2 ion channel and produce slowly inactivating mechano-current before hatching. Furthermore, duck neurons have a significantly reduced mechano-activation threshold and elevated mechano-current amplitude. Cloning and electrophysiological characterization of duck Piezo2 in a heterologous expression system shows that duck Piezo2 is functionally similar to the mouse ortholog but with prolonged inactivation kinetics, particularly at positive potentials. Knockdown of Piezo2 in duck trigeminal neurons attenuates mechano current with intermediate and slow inactivation kinetics. This suggests that Piezo2 is capable of contributing to a larger range of mechano-activated currents in duck trigeminal ganglia than in mouse trigeminal ganglia. Our results provide insights into the molecular basis of mechanotransduction in a tactile-specialist vertebrate.

Entities:  

Keywords:  Piezo2; mechano-gating; mechanoreception; mechanosensitivity; trigeminal ganglia

Mesh:

Substances:

Year:  2017        PMID: 29109250      PMCID: PMC5724259          DOI: 10.1073/pnas.1708793114

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


  68 in total

1.  Transduction of Repetitive Mechanical Stimuli by Piezo1 and Piezo2 Ion Channels.

Authors:  Amanda H Lewis; Alisa F Cui; Malcolm F McDonald; Jörg Grandl
Journal:  Cell Rep       Date:  2017-06-20       Impact factor: 9.423

2.  Piezo1, a mechanically activated ion channel, is required for vascular development in mice.

Authors:  Sanjeev S Ranade; Zhaozhu Qiu; Seung-Hyun Woo; Sung Sik Hur; Swetha E Murthy; Stuart M Cahalan; Jie Xu; Jayanti Mathur; Michael Bandell; Bertrand Coste; Yi-Shuan J Li; Shu Chien; Ardem Patapoutian
Journal:  Proc Natl Acad Sci U S A       Date:  2014-06-23       Impact factor: 11.205

3.  Mechanosensitive units in the upper bill and in the tongue of the domestic duck.

Authors:  L M Leitner; M Roumy
Journal:  Pflugers Arch       Date:  1974-02-04       Impact factor: 3.657

4.  Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels.

Authors:  Bertrand Coste; Jayanti Mathur; Manuela Schmidt; Taryn J Earley; Sanjeev Ranade; Matt J Petrus; Adrienne E Dubin; Ardem Patapoutian
Journal:  Science       Date:  2010-09-02       Impact factor: 47.728

5.  Comparative analysis of Meissner's corpuscles in the fingertips of primates.

Authors:  Andrey Verendeev; Christian Thomas; Shannon C McFarlin; William D Hopkins; Kimberley A Phillips; Chet C Sherwood
Journal:  J Anat       Date:  2015-06-05       Impact factor: 2.610

6.  Xerocytosis is caused by mutations that alter the kinetics of the mechanosensitive channel PIEZO1.

Authors:  Chilman Bae; Radhakrishnan Gnanasambandam; Chris Nicolai; Frederick Sachs; Philip A Gottlieb
Journal:  Proc Natl Acad Sci U S A       Date:  2013-03-04       Impact factor: 11.205

7.  The Role of PIEZO2 in Human Mechanosensation.

Authors:  Alexander T Chesler; Marcin Szczot; Diana Bharucha-Goebel; Marta Čeko; Sandra Donkervoort; Claire Laubacher; Leslie H Hayes; Katharine Alter; Cristiane Zampieri; Christopher Stanley; A Micheil Innes; Jean K Mah; Carla M Grosmann; Nathaniel Bradley; David Nguyen; A Reghan Foley; Claire E Le Pichon; Carsten G Bönnemann
Journal:  N Engl J Med       Date:  2016-09-21       Impact factor: 91.245

8.  Piezo1 ion channel pore properties are dictated by C-terminal region.

Authors:  Bertrand Coste; Swetha E Murthy; Jayanti Mathur; Manuela Schmidt; Yasmine Mechioukhi; Patrick Delmas; Ardem Patapoutian
Journal:  Nat Commun       Date:  2015-05-26       Impact factor: 14.919

9.  Developmental waves of mechanosensitivity acquisition in sensory neuron subtypes during embryonic development.

Authors:  Stefan G Lechner; Henning Frenzel; Rui Wang; Gary R Lewin
Journal:  EMBO J       Date:  2009-03-26       Impact factor: 11.598

10.  Tuning Piezo ion channels to detect molecular-scale movements relevant for fine touch.

Authors:  Kate Poole; Regina Herget; Liudmila Lapatsina; Ha-Duong Ngo; Gary R Lewin
Journal:  Nat Commun       Date:  2014-03-24       Impact factor: 14.919

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  12 in total

1.  Piezo2 integrates mechanical and thermal cues in vertebrate mechanoreceptors.

Authors:  Wang Zheng; Yury A Nikolaev; Elena O Gracheva; Sviatoslav N Bagriantsev
Journal:  Proc Natl Acad Sci U S A       Date:  2019-08-14       Impact factor: 11.205

2.  Dabbling with Piezo2 for mechanosensation.

Authors:  Ruhma Syeda
Journal:  Proc Natl Acad Sci U S A       Date:  2017-11-21       Impact factor: 11.205

3.  Quantitative Evaluation of Tactile Foraging Behavior in Pekin and Muscovy Ducks.

Authors:  Aaron K West; Emily M Xu; Mitchell D Nelson; Thomas R Hart; Emelia M Stricker; Alexandra G Cones; Grace M Martin; Kourtney Strickland; Devin L Lambert; Lainey Burman; Bailey H Zhu; Eve R Schneider
Journal:  Front Physiol       Date:  2022-06-14       Impact factor: 4.755

Review 4.  Tactile sensation in birds: Physiological insights from avian mechanoreceptors.

Authors:  Luke H Ziolkowski; Elena O Gracheva; Sviatoslav N Bagriantsev
Journal:  Curr Opin Neurobiol       Date:  2022-04-27       Impact factor: 7.070

5.  Piezo2 Mediates Low-Threshold Mechanically Evoked Pain in the Cornea.

Authors:  Jorge Fernández-Trillo; Danny Florez-Paz; Almudena Íñigo-Portugués; Omar González-González; Ana Gómez Del Campo; Alejandro González; Félix Viana; Carlos Belmonte; Ana Gomis
Journal:  J Neurosci       Date:  2020-10-14       Impact factor: 6.167

6.  TMEM150C/Tentonin3 Is a Regulator of Mechano-gated Ion Channels.

Authors:  Evan O Anderson; Eve R Schneider; Jon D Matson; Elena O Gracheva; Sviatoslav N Bagriantsev
Journal:  Cell Rep       Date:  2018-04-17       Impact factor: 9.423

7.  Piezo1 forms a slowly-inactivating mechanosensory channel in mouse embryonic stem cells.

Authors:  Josefina Inés Del Mármol; Kouki K Touhara; Gist Croft; Roderick MacKinnon
Journal:  Elife       Date:  2018-08-22       Impact factor: 8.140

8.  A hydrophobic gate in the inner pore helix is the major determinant of inactivation in mechanosensitive Piezo channels.

Authors:  Wang Zheng; Elena O Gracheva; Sviatoslav N Bagriantsev
Journal:  Elife       Date:  2019-01-10       Impact factor: 8.140

9.  A Cross-Species Analysis Reveals a General Role for Piezo2 in Mechanosensory Specialization of Trigeminal Ganglia from Tactile Specialist Birds.

Authors:  Eve R Schneider; Evan O Anderson; Viktor V Feketa; Marco Mastrotto; Yury A Nikolaev; Elena O Gracheva; Sviatoslav N Bagriantsev
Journal:  Cell Rep       Date:  2019-02-19       Impact factor: 9.423

10.  Innocuous pressure sensation requires A-type afferents but not functional ΡΙΕΖΟ2 channels in humans.

Authors:  Laura K Case; Jaquette Liljencrantz; Nicholas Madian; Aaron Necaise; Justin Tubbs; Micaela McCall; Megan L Bradson; Marcin Szczot; Mark H Pitcher; Nima Ghitani; Eleni Frangos; Jonathan Cole; Diana Bharucha-Goebel; Dimah Saade; Tracy Ogata; Sandra Donkervoort; A Reghan Foley; Carsten G Bönnemann; Håkan Olausson; M Catherine Bushnell; Alexander T Chesler
Journal:  Nat Commun       Date:  2021-01-28       Impact factor: 14.919

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