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PMID: 30382938 Published · epublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

OSCA/TMEM63 are an Evolutionarily Conserved Family of Mechanically Activated Ion Channels.

eLife ·Vol. 7 ·2018-00-01

Murthy SE, Dubin AE, Whitwam T, Jojoa-Cruz S, Cahalan SM, Mousavi SAR, Ward AB, Patapoutian A

Abstract

Mechanically activated (MA) ion channels convert physical forces into electrical signals, and are essential for eukaryotic physiology. Despite their importance, few bona-fide MA channels have been described in plants and animals. Here, we show that various members of the OSCA and TMEM63 family of proteins from plants, flies, and mammals confer mechanosensitivity to naïve cells. We conclusively demonstrate that OSCA1.2, one of the Arabidopsis thaliana OSCA proteins, is an inherently mechanosensitive, pore-forming ion channel. Our results suggest that OSCA/TMEM63 proteins are the largest family of MA ion channels identified, and are conserved across eukaryotes. Our findings will enable studies to gain deep insight into molecular mechanisms of MA channel gating, and will facilitate a better understanding of mechanosensory processes in vivo across plants and animals.

Keywords
<i>a. thaliana</i> D. melanogaster OSCA evolutionary biology human ion channels mechanically activated mechanotransduction molecular biophysics mouse structural biology
MeSH Terms
Animals Arabidopsis Biophysical Phenomena Conserved Sequence Evolution, Molecular Gadolinium/pharmacology HEK293 Cells Humans Ion Channel Gating Ion Channels/genetics,metabolism Liposomes Mechanotransduction, Cellular Osmolar Concentration
Chemicals
Ion Channels Liposomes Gadolinium
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Murthy Swetha E ORCID
Department of Neuroscience, Dorris Neuroscience Center, The Scripps Research Institute, California, United States.
Dubin Adrienne E ORCID
Department of Neuroscience, Dorris Neuroscience Center, The Scripps Research Institute, California, United States.
Whitwam Tess
Department of Neuroscience, Dorris Neuroscience Center, The Scripps Research Institute, California, United States.
Jojoa-Cruz Sebastian ORCID
Department of Integrative Structural and Computational Biology, The Scripps Research Institute, Howard Hughes Medical Institute, California, United States.
Cahalan Stuart M
Department of Neuroscience, Dorris Neuroscience Center, The Scripps Research Institute, California, United States.
Mousavi Seyed Ali Reza
Department of Neuroscience, Dorris Neuroscience Center, The Scripps Research Institute, California, United States.
Ward Andrew B ORCID
Department of Integrative Structural and Computational Biology, The Scripps Research Institute, Howard Hughes Medical Institute, California, United States.
Patapoutian Ardem ORCID
Department of Neuroscience, Dorris Neuroscience Center, The Scripps Research Institute, California, United States.
Conflict of Interest

SM, AD, TW, SJ, SC, SM, AW, AP No competing interests declared

References (33)
33 references, click to expand
  1. Co-expression of mouse TMEM63A, TMEM63B and TMEM63C confers hyperosmolarity activated ion currents in HEK293 cells.
    Cell Biochem Funct. 2016 Jun;34(4):238-41 PMID: 27045885
  2. Widespread mechanosensing controls the structure behind the architecture in plants.
    Curr Opin Plant Biol. 2013 Oct;16(5):654-60 PMID: 23830994
  3. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels.
    Science. 2010 Oct 1;330(6000):55-60 PMID: 20813920
  4. Common evolutionary origins of mechanosensitive ion channels in Archaea, Bacteria and cell-walled Eukarya.
    Archaea. 2002 Mar;1(1):35-44 PMID: 15803657
  5. Piezo1 ion channel pore properties are dictated by C-terminal region.
    Nat Commun. 2015 May 26;6:7223 PMID: 26008989
  6. Structural relationship between the putative hair cell mechanotransduction channel TMC1 and TMEM16 proteins.
    Elife. 2018 Jul 31;7: PMID: 30063209
  7. Activation of the mechanosensitive ion channel MscL by mechanical stimulation of supported Droplet-Hydrogel bilayers.
    Sci Rep. 2017 Mar 27;7:45180 PMID: 28345591
  8. Mechanically Activated Ion Channels.
    Neuron. 2015 Sep 23;87(6):1162-1179 PMID: 26402601
  9. Impaired PIEZO1 function in patients with a novel autosomal recessive congenital lymphatic dysplasia.
    Nat Commun. 2015 Sep 21;6:8329 PMID: 26387913
  10. Piezo1 links mechanical forces to red blood cell volume.
    Elife. 2015 May 22;4:null PMID: 26001274
  11. Examination of subconductance levels arising from a single ion channel.
    J Theor Biol. 1991 Dec 7;153(3):401-23 PMID: 1724679
  12. Piezo1 Channels Are Inherently Mechanosensitive.
    Cell Rep. 2016 Nov 8;17(7):1739-1746 PMID: 27829145
  13. Stretch-activated ion channels: what are they?
    Physiology (Bethesda). 2010 Feb;25(1):50-6 PMID: 20134028
  14. Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination.
    Science. 2015 Oct 23;350(6259):438-41 PMID: 26494758
  15. Cryo-EM structure of the mechanically activated ion channel OSCA1.2.
    Elife. 2018 Nov 01;7: PMID: 30382939
  16. Piezo proteins are pore-forming subunits of mechanically activated channels.
    Nature. 2012 Feb 19;483(7388):176-81 PMID: 22343900
  17. Structure of the mechanosensitive OSCA channels.
    Nat Struct Mol Biol. 2018 Sep;25(9):850-858 PMID: 30190597
  18. TMEM16 chloride channels are two-faced.
    J Gen Physiol. 2016 Nov;148(5):367-373 PMID: 27799317
  19. DUF221 proteins are a family of osmosensitive calcium-permeable cation channels conserved across eukaryotes.
    Cell Res. 2014 May;24(5):632-5 PMID: 24503647
  20. Feeling the hidden mechanical forces in lipid bilayer is an original sense.
    Proc Natl Acad Sci U S A. 2014 Jun 3;111(22):7898-905 PMID: 24850861
  21. Anoctamins/TMEM16 Proteins: Chloride Channels Flirting with Lipids and Extracellular Vesicles.
    Annu Rev Physiol. 2017 Feb 10;79:119-143 PMID: 27860832
  22. TMC1 Forms the Pore of Mechanosensory Transduction Channels in Vertebrate Inner Ear Hair Cells.
    Neuron. 2018 Aug 22;99(4):736-753.e6 PMID: 30138589
  23. Eukaryotic mechanosensitive channels.
    Annu Rev Biophys. 2010;39:111-37 PMID: 20192782
  24. Mechanically Gated Ion Channels in Mammalian Hair Cells.
    Front Cell Neurosci. 2018 Apr 11;12:100 PMID: 29755320
  25. Endogenous Piezo1 Can Confound Mechanically Activated Channel Identification and Characterization.
    Neuron. 2017 Apr 19;94(2):266-270.e3 PMID: 28426961
  26. Life behind the wall: sensing mechanical cues in plants.
    BMC Biol. 2017 Jul 11;15(1):59 PMID: 28697754
  27. Piezos thrive under pressure: mechanically activated ion channels in health and disease.
    Nat Rev Mol Cell Biol. 2017 Dec;18(12):771-783 PMID: 28974772
  28. The evolutionary 'tinkering' of MscS-like channels: generation of structural and functional diversity.
    Pflugers Arch. 2015 Jan;467(1):3-13 PMID: 24819593
  29. OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis.
    Nature. 2014 Oct 16;514(7522):367-71 PMID: 25162526
  30. Purification and functional reconstitution of the recombinant large mechanosensitive ion channel (MscL) of Escherichia coli.
    J Biol Chem. 1995 Aug 4;270(31):18329-34 PMID: 7543101
  31. Structure of the mechanically activated ion channel Piezo1.
    Nature. 2018 Feb 22;554(7693):481-486 PMID: 29261642
  32. Open-state substructure of single chloride channels from Torpedo electroplax.
    Philos Trans R Soc Lond B Biol Sci. 1982 Dec 1;299(1097):401-11 PMID: 6130538
  33. Mechanosensitivity is mediated directly by the lipid membrane in TRAAK and TREK1 K+ channels.
    Proc Natl Acad Sci U S A. 2014 Mar 4;111(9):3614-9 PMID: 24550493
Article Info
Journal
eLife
Abbr.
Elife
ISSN
2050-084X
Published
2018-00-01
Epub
2018-00-01
Language
English
Region
England
NLM ID
101579614
PMCID
PMC6235560
Subset
IM
Grants
Howard Hughes Medical Institute · United States
NINDS NIH HHS · R35 NS105067 · United States
NINDS NIH HHS · R35NS105067 · United States
NIH HHS · R21DE025329 · United States
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