The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals

Nature Neuroscience
Robert O'HaganM B Goodman

Abstract

Transformation of mechanical energy into ionic currents is essential for touch, hearing and nociception. Although DEG/ENaC proteins are believed to form sensory mechanotransduction channels, the evidence for this role remains indirect. By recording from C. elegans touch receptor neurons in vivo, we found that external force evokes rapidly activating mechanoreceptor currents (MRCs) carried mostly by Na(+) and blocked by amiloride-characteristics consistent with direct mechanical gating of a DEG/ENaC channel. Like mammalian Pacinian corpuscles, these neurons depolarized with both positive and negative changes in external force but not with sustained force. Null mutations in the DEG/ENaC gene mec-4 and in the accessory ion channel subunit genes mec-2 and mec-6 eliminated MRCs. In contrast, the genetic elimination of touch neuron-specific microtubules reduced, but did not abolish, MRCs. Our findings link the application of external force to the activation of a molecularly defined metazoan sensory transduction channel.

References

Jun 1, 1979·Biophysical Journal·David P Corey, A J Hudspeth
Jan 1, 1992·Methods in Enzymology·S H Heinemann, F Conti
Apr 1, 1982·The Journal of Cell Biology·Martin Chalfie, J N Thomson
Mar 1, 1981·Developmental Biology·Martin Chalfie, J Sulston
Dec 1, 1994·Journal of Neurophysiology·M JuusolaA S French
Jan 1, 1995·Methods in Cell Biology·R H Plasterk
Oct 27, 1997·Journal of Neurophysiology·U HögerA S French
Apr 1, 2000·Science·R G WalkerC S Zuker
Oct 21, 2000·Journal of Neuroscience Methods·M B Goodman, Shawn R Lockery
Nov 18, 2000·Brain Research·Heather A DrummondMichael J Welsh
Jun 28, 2002·Physiological Reviews·Stephan Kellenberger, Laurent Schild
Nov 14, 2002·Annual Review of Genetics·Glen G Ernstrom, Martin Chalfie
Sep 6, 2003·Current Biology : CB·Joshua A AinsleyWayne A Johnson
Jan 1, 1953·The American Journal of Physiology·R ALVAREZ-BUYLLA, J RAMIREZ DE ARELLANO
Dec 29, 1953·The Journal of Physiology·J A GRAY, M SATO
Jul 14, 1958·The Journal of Physiology·J DIAMONDD R INMAN

Citations

Oct 16, 2009·Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology·Ewan St John Smith, Gary R Lewin
Oct 6, 2006·Pflügers Archiv : European journal of physiology·O P Hamill
Sep 23, 2008·Development Genes and Evolution·Patricia GordonKathleen M Raley-Susman
Jun 19, 2013·Neuroscience Letters·Toshihiro SassaIchi N Maruyama
Aug 2, 2008·Cell Death and Differentiation·W ZhangMonica Driscoll
Oct 31, 2006·Nature·Honeybee Genome Sequencing Consortium
Dec 15, 2006·Nature·Christiane WetzelGary R Lewin
Feb 22, 2012·Nature·Sung Eun KimArdem Patapoutian
Nov 3, 2011·Nature Communications·Anthony W PengAnthony J Ricci
Apr 7, 2010·Nature Methods·Andrea CalixtoMartin Chalfie
Jul 29, 2008·Nature Neuroscience·Daniel RamotM B Goodman
Apr 7, 2010·Nature Neuroscience·Sreekanth H ChalasaniCornelia I Bargmann
Jun 1, 2010·Nature Neuroscience·Marios ChatzigeorgiouWilliam R Schafer
Dec 29, 2004·Nature Neuroscience·Diane Ronan, Peter Gillespie
Apr 24, 2007·Nature Neuroscience·Katie S KindtWilliam R Schafer
Jan 30, 2008·Proceedings of the National Academy of Sciences of the United States of America·Tinsley Davis
Jun 26, 2009·Proceedings of the National Academy of Sciences of the United States of America·Martin Chalfie
Mar 4, 2011·Proceedings of the National Academy of Sciences of the United States of America·Alexander BounoutasMartin Chalfie
Mar 12, 2013·Proceedings of the National Academy of Sciences of the United States of America·Andriy Anishkin, Ching Kung
Feb 18, 2010·The Journal of Biological Chemistry·Stefan DürrnagelStefan Gründer
Jul 27, 2010·The Journal of Biological Chemistry·Dominik Wiemuth, Stefan Gründer
Sep 23, 2011·The Journal of Biological Chemistry·Jeong-Eui LeeYoung-Ki Paik
Oct 4, 2012·The Journal of Biological Chemistry·Nina BoikoBenjamin A Eaton
Aug 31, 2011·The Journal of General Physiology·Diana M Bautista, Ellen A Lumpkin
Sep 26, 2012·The Journal of General Physiology·Stefan DürrnagelStefan Gründer
Jun 12, 2013·Annual Review of Neuroscience·Niels EijkelkampJohn N Wood
Mar 3, 2010·Annual Review of Biophysics·Jóhanna Arnadóttir, Martin Chalfie
Mar 12, 2010·American Journal of Physiology. Regulatory, Integrative and Comparative Physiology·François M Abboud
Jul 15, 2011·American Journal of Physiology. Renal Physiology·Ossama B Kashlan, Thomas R Kleyman
Oct 1, 2010·Journal of Neurophysiology·Marios ChatzigeorgiouWilliam R Schafer
Apr 9, 2005·Molecular Pain·Liam J Drew, John N Wood
Mar 3, 2010·PloS One·Yehuda Ben-ShaharMichael J Welsh
Sep 30, 2010·PloS One·Renate GessmannNektarios Tavernarakis
Feb 6, 2013·PloS One·Kristin A GerholdDiana M Bautista
Jul 16, 2010·The Journal of Neuroscience : the Official Journal of the Society for Neuroscience·Sean E LowLouis Saint-Amant
Jan 18, 2013·The Journal of Neuroscience : the Official Journal of the Society for Neuroscience·Lu HanLaura Bianchi
Sep 2, 2011·The Journal of Neuroscience : the Official Journal of the Society for Neuroscience·Jóhanna ArnadóttirMartin Chalfie
Dec 1, 2007·WormBook : the Online Review of C. Elegans Biology·M B Goodman
Mar 26, 2014·Nature Communications·Kate PooleGary R Lewin
Feb 7, 2007·Proceedings of the National Academy of Sciences of the United States of America·Dattananda S Chelur, Martin Chalfie
Oct 27, 2007·Proceedings of the National Academy of Sciences of the United States of America·Sung-Jin ParkB L Pruitt
Nov 3, 2006·Proceedings of the National Academy of Sciences of the United States of America·Tobias B HuberThomas Benzing
Jun 25, 2014·Proceedings of the National Academy of Sciences of the United States of America·Sanjeev S RanadeArdem Patapoutian
Sep 25, 2007·The International Journal of Developmental Biology·Bernd FritzschGarrett Soukup
Mar 27, 2009·Nature Neuroscience·Shawn R Lockery, M B Goodman
Oct 3, 2012·Physiology·Amy L Eastwood, M B Goodman
Jun 22, 2010·Development Genes and Evolution·Harper C VansteenhouseBirgit Zipser
Apr 20, 2006·Invertebrate Neuroscience : in·Irina VinogradovaLindy Holden-Dye
Oct 29, 2015·Developmental Dynamics : an Official Publication of the American Association of Anatomists·Nicole Gorfinkiel
Oct 20, 2010·The Journal of Cell Biology·Ellen A LumpkinAislyn M Nelson
Dec 3, 2014·Current Biology : CB·Stephanie E MauthnerW Daniel Tracey
Nov 20, 2013·The Journal of Physiology·Alexey KozlenkovEwan St John Smith
Jun 18, 2014·Journal of Molecular Biology·Stephan Kellenberger, Thomas Grutter
Mar 28, 2012·Molecular Pain·Ramin RaoufJohn N Wood
Dec 3, 2015·Proceedings of the National Academy of Sciences of the United States of America·Amy L EastwoodM B Goodman
Sep 2, 2015·Proceedings of the National Academy of Sciences of the United States of America·Yushu ChenMartin Chalfie
Jul 1, 2015·Proceedings of the National Academy of Sciences of the United States of America·Hao-Ching JiangChun-Liang Pan
May 25, 2012·Trends in Neurosciences·Bernd Nilius, Eric Honoré
May 12, 2012·Neurobiology of Aging·Tiffany A TimbersCatharine H Rankin
Aug 16, 2011·Trends in Neurosciences·David H Hall, Millet Treinin
Apr 20, 2011·European Journal of Cell Biology·Liudmilla LapatsinaGary R Lewin
Sep 21, 2010·Current Opinion in Cell Biology·Takeshi Kobayashi, Masahiro Sokabe
Aug 18, 2009·Autonomic Neuroscience : Basic & Clinical·Stuart M Brierley
Mar 18, 2008·Progress in Biophysics and Molecular Biology·Joost H A FolgeringEric Honoré
Nov 23, 2006·Seminars in Cell & Developmental Biology·Johannes S Schlöndorff, Martin R Pollak
Nov 18, 2008·Microscopy Research and Technique·J A VegaJuan M Cobo
Dec 30, 2008·Angewandte Chemie
Mar 31, 2012·Microscopy Research and Technique·M E Del ValleJ A Vega
Mar 16, 2013·Journal of Cellular and Molecular Medicine·Chih-Cheng Chen, Chia-Wen Wong
Aug 2, 2012·The EMBO Journal·Janko BrandOliver Daumke
Apr 18, 2013·The European Journal of Neuroscience·Jiaxin GongZuoren Wang
Apr 9, 2010·Microcirculation : the Official Journal of the Microcirculatory Society, Inc·James C Culver, Mary E Dickinson
Jan 16, 2010·The EMBO Journal·Jing HuGary R Lewin
Jan 20, 2015·BioEssays : News and Reviews in Molecular, Cellular and Developmental Biology·Michael KriegM B Goodman
Jul 19, 2005·Current Opinion in Neurobiology·Ellen A Lumpkin, Diana M Bautista
Nov 14, 2015·Annual Review of Cell and Developmental Biology·Samata KattaM B Goodman
Jul 6, 2014·Neuroscience·E N AllenJ Alcedo
Sep 25, 2015·Neuron·Sanjeev S RanadeArdem Patapoutian
Dec 22, 2014·Neuropharmacology·Damir OmerbašićGary R Lewin
Jan 10, 2012·Current Opinion in Neurobiology·Jennifer K Pirri, Mark J Alkema
Dec 27, 2007·Biochemical and Biophysical Research Communications·Shinya UgawaShoichi Shimada
Jan 17, 2015·Neuropharmacology·François M Abboud, Christopher J Benson
Dec 30, 2014·Peptides·Jason C CampbellWilliam G Bendena
Apr 23, 2015·Biophysical Journal·William GilpinClifford P Brangwynne
Jun 12, 2013·Communicative & Integrative Biology·James D Stockand, Benjamin A Eaton
Jul 11, 2006·Current Biology : CB·William R Schafer
Sep 6, 2005·Current Biology : CB·William R Schafer
Feb 23, 2010·Current Biology : CB·Lixian ZhongW Daniel Tracey
Aug 2, 2011·Current Biology : CB·Sean M MaguireMark J Alkema
Nov 9, 2010·Current Biology : CB·Rui Xiao, X Z Shawn Xu
Oct 18, 2011·Structure·Elizabeth S HaswellDouglas C Rees
Jul 21, 2009·Current Biology : CB·Alexander BounoutasMartin Chalfie
Jan 10, 2006·Developmental Cell·A Wayne OrrMartin A Schwartz
Oct 15, 2013·Cell·Patrick Delmas, Bertrand Coste
Dec 3, 2014·Cell Reports·Yanmeng GuoZuoren Wang
Jul 1, 2014·Seminars in Cell & Developmental Biology·Robert O'HaganMaureen M Barr
Jun 28, 2012·Biophysical Journal·Félix LeboisJean-Marc Di Meglio
Apr 21, 2011·Biophysical Journal·Bryan PetzoldB L Pruitt
Mar 14, 2014·Frontiers in Cellular Neuroscience·M Mar Gámez-Del-EstalManuel Ruiz-Rubio
Dec 20, 2005·Pain·Jing HuGary R Lewin
Jul 2, 2014·Pflügers Archiv : European journal of physiology·Kate PooleGary R Lewin
Jun 4, 2014·Pflügers Archiv : European journal of physiology·Jinfeng TengChing Kung
Sep 23, 2014·Pflügers Archiv : European journal of physiology·Thomas EffertzAnthony J Ricci
Jul 24, 2014·Pflügers Archiv : European journal of physiology·William R Schafer
Jun 9, 2016·Proceedings of the National Academy of Sciences of the United States of America·Chaogu ZhengMartin Chalfie
Jun 15, 2016·Proceedings of the National Academy of Sciences of the United States of America·Yanmeng GuoZuoren Wang
Apr 8, 2015·PloS One·Bing ShenXiaoqiang Yao
Jul 19, 2005·Annual Review of Neuroscience·Mario de Bono, Andres Villu Maricq
Jan 1, 2007·Current Topics in Membranes·Dafne Bazopoulou, Nektarios Tavernarakis
Sep 18, 2007·Pflügers Archiv : European journal of physiology·Martin Fronius, Wolfgang G Clauss
Jun 18, 2017·BioEssays : News and Reviews in Molecular, Cellular and Developmental Biology·Juan Antonio Sánchez-Alcañiz, Richard Benton
Aug 23, 2006·Molecular Pain·Gordon C McCarter, Jon D Levine
Oct 21, 2016·American Journal of Physiology. Cell Physiology·Cristina MatthewmanLaura Bianchi
Sep 16, 2017·Integrative Biology : Quantitative Biosciences From Nano to Macro·Patrick D McClanahanChristopher Fang-Yen
Jun 1, 2018·Journal of Cell Science·Valeria PrystopiukJohannes Fels
Jul 13, 2018·Channels·Alexis S Hill, Yehuda Ben-Shahar
Apr 20, 2013·Integrative Biology : Quantitative Biosciences From Nano to Macro·Bryan PetzoldB L Pruitt
Jul 14, 2006·Journal of Neurobiology·Christian Frøkjaer-JensenWilliam R Schafer
Nov 18, 2008·Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology·Stephan Frings
Jun 23, 2007·Nature Reviews. Neuroscience·Adam P Christensen, David P Corey
Mar 20, 2008·Biological cybernetics·John Bryden, Netta Cohen
Feb 7, 2009·Nature Reviews. Molecular Cell Biology·Martin Chalfie
Jul 2, 2009·Angewandte Chemie·Martin Chalfie
Aug 12, 2005·American Journal of Physiology. Renal Physiology·Lori A Birder
Feb 27, 2009·Journal of the American Society of Nephrology : JASN·Bernhard Schermer, Thomas Benzing
Aug 30, 2008·Journal of the American Society of Nephrology : JASN·Vivek Bhalla, Kenneth R Hallows
Aug 23, 2005·Journal of Neurobiology·Serge FaumontShawn R Lockery
Apr 28, 2006·Pflügers Archiv : European journal of physiology·C BarsantiM Pellegrino
Sep 30, 2005·American Journal of Physiology. Cell Physiology·Heather A DrummondDavid E Stec
Mar 29, 2019·Proceedings of the National Academy of Sciences of the United States of America·Landi SunXin Liang
Feb 8, 2007·Pflügers Archiv : European journal of physiology·Alexander Bounoutas, Martin Chalfie
Feb 25, 2014·Nature Cell Biology·Michael KriegM B Goodman
Jul 20, 2006·American Journal of Physiology. Renal Physiology·Nikki L Jernigan, Heather A Drummond
Jul 18, 2006·American Journal of Physiology. Heart and Circulatory Physiology·Samira C GrifoniHeather A Drummond
Aug 8, 2018·Cold Spring Harbor Perspectives in Medicine·Christopher L Cunningham, Ulrich Müller
May 1, 2010·Expert Review of Clinical Pharmacology·Jacques NoëlEric Lingueglia
Jun 22, 2018·Open Biology·Athanasios MetaxakisNektarios Tavernarakis
Sep 26, 2014·American Journal of Physiology. Cell Physiology·Rachele SangalettiLaura Bianchi
Aug 17, 2019·Science·Hind AbdoPatrik Ernfors
May 26, 2005·American Journal of Physiology. Renal Physiology·Nikki L Jernigan, Heather A Drummond
Apr 26, 2018·American Journal of Physiology. Cell Physiology·Cristina MatthewmanLaura Bianchi
Oct 19, 2007·Journal of Neurophysiology·Carlos Martinez-SalgadoGary R Lewin
Aug 5, 2017·The Journal of Biological Chemistry·Shujie ShiThomas R Kleyman
Sep 20, 2019·The Journal of General Physiology·Samata KattaM B Goodman
Jan 28, 2020·American Journal of Physiology. Renal Physiology·Marcelo D Carattino, Nicolas Montalbetti
Sep 11, 2013·FASEB Journal : Official Publication of the Federation of American Societies for Experimental Biology·Sophie RoyStephan Kellenberger
Nov 18, 2008·Journal of Neurogenetics·Evan L Ardiel, Catharine H Rankin
Nov 28, 2017·Traffic·Parul SoodSandhya P Koushika
Feb 22, 2020·Annual Review of Neuroscience·Peng JinYuh-Nung Jan
Oct 28, 2019·The Journal of General Physiology·Katherine M Perks, Jonathan T Pierce
May 12, 2005·Médecine sciences : M/S·Alex J ParkerChristian Néri
Jul 9, 2016·Physical Review Letters·Benedikt Sabass, Howard A Stone
Jul 22, 2018·Integrative Biology : Quantitative Biosciences From Nano to Macro·E A MazzochetteB L Pruitt
Mar 7, 2019·Scientific Reports·Tomomi ShindouIchiro N Maruyama
May 10, 2019·APL Bioengineering·Johanna Heureaux-TorresAllen P Liu
Nov 27, 2008·The Biochemical Journal·Ivan KadurinStefan Gründer
Mar 2, 2013·G3 : Genes - Genomes - Genetics·Kathleen M ZelleYehuda Ben-Shahar
Sep 28, 2017·Scientific Reports·Muna ElmiMandayam A Srinivasan
Mar 15, 2019·Nature Communications·Luis O RomeroValeria Vásquez
Feb 23, 2007·Nature·Ellen A Lumpkin, Michael J Caterina
May 14, 2016·G3 : Genes - Genomes - Genetics·Yushu ChenMartin Chalfie
May 18, 2016·The Journal of Biological Chemistry·Shujie ShiThomas R Kleyman
Jul 31, 2018·Frontiers in Pediatrics·Henning Hagmann, Paul T Brinkkoetter
Apr 7, 2020·Journal of Neural Transmission·Reza Sharif-Naeini
Jul 26, 2016·Biomedical Optics Express·Michael ShawMandayam A Srinivasan
May 10, 2017·Cell and Tissue Research·Athina Ganner, Elke Neumann-Haefelin
Oct 10, 2020·Nature Communications·Ping LiuZhao-Wen Wang
Dec 17, 2020·Journal of Neurogenetics·Umar Al-Sheikh, Lijun Kang

Related Concepts

Deg-1 protein, C elegans
Mec-4 protein, C elegans
Kaluril
Electric Conductivity
Meissner's Corpuscle
Cell Surface Proteins
Physical Stimulation
Sodium
Touch Sensation
Sodium Channel

Trending Feeds

COVID-19

Coronaviruses encompass a large family of viruses that cause the common cold as well as more serious diseases, such as the ongoing outbreak of coronavirus disease 2019 (COVID-19; formally known as 2019-nCoV). Coronaviruses can spread from animals to humans; symptoms include fever, cough, shortness of breath, and breathing difficulties; in more severe cases, infection can lead to death. This feed covers recent research on COVID-19.

Synthetic Genetic Array Analysis

Synthetic genetic arrays allow the systematic examination of genetic interactions. Here is the latest research focusing on synthetic genetic arrays and their analyses.

Congenital Hyperinsulinism

Congenital hyperinsulinism is caused by genetic mutations resulting in excess insulin secretion from beta cells of the pancreas. Here is the latest research.

Neural Activity: Imaging

Imaging of neural activity in vivo has developed rapidly recently with the advancement of fluorescence microscopy, including new applications using miniaturized microscopes (miniscopes). This feed follows the progress in this growing field.

Chronic Fatigue Syndrome

Chronic fatigue syndrome is a disease characterized by unexplained disabling fatigue; the pathology of which is incompletely understood. Discover the latest research on chronic fatigue syndrome here.

Epigenetic Memory

Epigenetic memory refers to the heritable genetic changes that are not explained by the DNA sequence. Find the latest research on epigenetic memory here.

Cell Atlas of the Human Eye

Constructing a cell atlas of the human eye will require transcriptomic and histologic analysis over the lifespan. This understanding will aid in the study of development and disease. Find the latest research pertaining to the Cell Atlas of the Human Eye here.

Femoral Neoplasms

Femoral Neoplasms are bone tumors that arise in the femur. Discover the latest research on femoral neoplasms here.

STING Receptor Agonists

Stimulator of IFN genes (STING) are a group of transmembrane proteins that are involved in the induction of type I interferon that is important in the innate immune response. The stimulation of STING has been an active area of research in the treatment of cancer and infectious diseases. Here is the latest research on STING receptor agonists.