Piezo proteins are pore-forming subunits of mechanically activated channels

Nature

Volumn 483, Issue 7388, 2012, Pages 176-181

  Coste, Bertrand ^a   Xiao, Bailong ^a   Santos, Jose S ^b   Syeda, Ruhma ^b   Grandl, Jãrg ^a,d   Spencer, Kathryn S ^a   Kim, Sung Eun ^a   Schmidt, Manuela ^a   Mathur, Jayanti ^c   Dubin, Adrienne E ^a   Montal, Mauricio ^b   Patapoutian, Ardem ^a,c  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATION CHANNEL; CG 8486 PROTEIN; ION CHANNEL; LIPOSOME; MMPIEZO1 PROTEIN; MMPIEZO2 PROTEIN; PIEZO PROTEIN; PORE FORMING CYTOTOXIC PROTEIN; RUTHENIUM RED; UNCLASSIFIED DRUG;

BIOACTIVITY; PHYSIOLOGY; PROTEIN; RUTHENIUM; SENSORY SYSTEM;

ARTICLE; CELLS; CONDUCTANCE; DROSOPHILA MELANOGASTER; ELECTRIC CURRENT; IC 50; LIPID BILAYER; MECHANOTRANSDUCTION; NONHUMAN; PERMEABILITY; PRESSURE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; SENSATION; SENSITIVITY ANALYSIS; SOUND; TOUCH; WAVEFORM;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ELECTRIC CONDUCTIVITY; HEK293 CELLS; HELA CELLS; HUMANS; ION CHANNEL GATING; ION CHANNELS; LIPID BILAYERS; MECHANOTRANSDUCTION, CELLULAR; MICE; MOLECULAR SEQUENCE DATA; NIH 3T3 CELLS; POROSITY; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS;

DROSOPHILA MELANOGASTER;

EID: 84862777142     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature10812     Document Type: Article

References (35)

1. Corey, D. P. & Hudspeth, A. J. Response latency of vertebrate hair cells. Biophys. J. 26, 499-506 (1979). (Pubitemid 9205704)
2. McCarter, G. C., Reichling, D. B. & Levine, J. D. Mechanical transduction by rat dorsal root ganglion neurons in vitro. Neurosci. Lett. 273, 179-182 (1999). (Pubitemid 29430179)
3. Davis, M. J., Donovitz, J. A.&Hood, J. D. Stretch-activated single-channel and whole cell currents in vascular smooth muscle cells. Am. J. Physiol. 262, C1083-C1088 (1992).
4. Praetorius, H. A. & Spring, K. R. Bending the MDCK cell primary cilium increases intracellular calcium. J. Membr. Biol. 184, 71-79 (2001). (Pubitemid 33016173)
5. Chalfie, M. Neurosensory mechanotransduction. Nature Rev. Mol. Cell Biol. 10, 44-52 (2009).
6. Delmas, P., Hao, J. & Rodat-Despoix, L. Molecular mechanisms of mechanotransduction in mammalian sensory neurons. Nature Rev. Neurosci. 12, 139-153 (2011).
7. Hamill, O. P.& Martinac, B. Molecular basis ofmechanotransduction in living cells. Physiol. Rev. 81, 685-740 (2001). (Pubitemid 32267076)
8. Coste, B. et al. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330, 55-60 (2010).
9. Bae, C., Sachs, F. & Gottlieb, P. A. The mechanosensitive ion channel Piezo1 is inhibited by the peptide GsMTx4. Biochemistry 50, 6295-6300 (2011).
10. Reed-Geaghan, E. G. & Maricich, S. M. Peripheral somatosensation: a touch of genetics. Curr. Opin. Genet. Dev. 21, 240-248 (2011).
11. Nilius, B. Pressing and squeezing with Piezos. EMBO Rep. 11, 902-903 (2010).
12. Gong, Z. et al.Two interdependentTRPVchannel subunits, inactive andNanchung, mediate hearing in Drosophila. J. Neurosci. 24, 9059-9066 (2004). (Pubitemid 39377772)
13. Kim, J. et al. A TRPV family ion channel required for hearing in Drosophila. Nature 424, 81-84 (2003). (Pubitemid 36834845)
14. Tracey, W. D. Jr, Wilson, R. I., Laurent, G. & Benzer, S. painless, a Drosophila gene essential for nociception. Cell 113, 261-273 (2003). (Pubitemid 36514976)
15. Walker, R. G., Willingham, A. T. & Zuker, C. S. A Drosophila mechanosensory transduction channel. Science 287, 2229-2234 (2000). (Pubitemid 30177021)
16. Zhong, L., Hwang, R. Y. & Tracey, W. D. Pickpocket is a DEG/ENaC protein required for mechanical nociception in Drosophila larvae. Curr. Biol. 20, 429-434 (2010).
17. Coste, B., Crest, M. & Delmas, P. Pharmacological dissection and distribution of NaN/Nav1.9, T-type Ca21 currents, and mechanically activated cation currents in different populations of DRG neurons. J. Gen. Physiol. 129, 57-77 (2007). (Pubitemid 46036509)
18. Drew, L. J., Wood, J. N. & Cesare, P. Distinct mechanosensitive properties of capsaicin-sensitive and-insensitive sensory neurons. J. Neurosci. 22, RC228 (2002).
19. Kim, S. E., Coste, B., Chadha, A., Cook, B. & Patapoutian, A. The role of Drosophila Piezo inmechanical nociception. Nature http://dx.doi.org/10. 1038/nature10801 (this issue).
20. Voets, T. et al. Molecular determinants of permeation through the cation channel TRPV4. J. Biol. Chem. 277, 33704-33710 (2002).
21. Voets, T. et al. TRPM6 forms the Mg21 influx channel involved in intestinal and renal Mg21 absorption. J. Biol. Chem. 279, 19-25 (2004). (Pubitemid 38044794)
22. Ulbrich, M. H. & Isacoff, E. Y. Subunit counting in membrane-bound proteins. Nature Methods 4, 319-321 (2007). (Pubitemid 46766975)
23. Bayley, H. et al. Droplet interface bilayers. Mol. Biosyst. 4, 1191-1208 (2008).
24. Montal, M. Asymmetric lipid bilayers. Reponse to multivalent ions. Biochim. Biophys. Acta 298, 750-754 (1973).
25. Montal, M. & Mueller, P. Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. Proc. Natl Acad. Sci. USA 69, 3561-3566 (1972).
26. Santos, J. S., Grigoriev, S. M.&Montal, M. Molecular template for a voltage sensor in anovelK1 channel. III. Functional reconstitution of a sensorless poremodule from a prokaryotic Kv channel. J. Gen. Physiol. 132, 651-666 (2008).
27. Leventis, P.A.&Grinstein, S. The distribution andfunction ofphosphatidylserine in cellular membranes. Annu Rev Biophys 39, 407-427 (2010).
28. Ermakov, Y. A., Kamaraju, K., Sengupta, K. & Sukharev, S. Gadolinium ions block mechanosensitive channels by altering the packing and lateral pressure of anionic lipids. Biophys. J. 98, 1018-1027 (2010).
29. Gambale, F. & Montal, M. Characterization of the channel properties of tetanus toxin in planar lipid bilayers. Biophys. J. 53, 771-783 (1988).
30. Oliver, D. et al. Functional conversion between A-type and delayed rectifier K1 channels by membrane lipids. Science 304, 265-270 (2004). (Pubitemid 38452174)
31. Schmidt, D. & MacKinnon, R. Voltage-dependent K1 channel gating and voltage sensor toxin sensitivity depend on the mechanical state of the lipid membrane. Proc. Natl Acad. Sci. USA 105, 19276-19281 (2008).
32. Tao, X. & MacKinnon, R. Functional analysis of Kv1.2 and paddle chimera Kv channels in planar lipid bilayers. J. Mol. Biol. 382, 24-33 (2008).
33. Hartman, N. C. & Groves, J. T. Signaling clusters in the cell membrane. Curr. Opin. Cell Biol. 23, 370-376 (2011).
34. Schagger, H., Cramer, W. A. & von Jagow, G. Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal. Biochem. 217, 220-230 (1994). (Pubitemid 24080754)
35. Gambale, F.& Montal, M. Voltage-gated sodiumchannels expressed in the human cerebellar medulloblastoma cell line TE671. Brain Res. Mol. Brain Res. 7, 123-129 (1990). (Pubitemid 20039551)