Abstract
Mechano-gated ion channels are implicated in a variety of key physiological functions ranging from touch sensitivity to arterial pressure regulation. Seminal work in prokaryotes and invertebrates provided strong evidence for the role of specific ion channels in volume regulation, touch sensitivity, or hearing, specifically the mechanosensitive channel subunits of large and small conductances (MscL and MscS), the mechanosensory channel subunits (MEC) and the transient receptor potential channel subunits (TRP). In mammals, recent studies further indicate that members of the TRP channel family may also be considered as possible candidate mechanosensors responding to either tension, flow, or changes in cell volume. However, contradictory results have challenged whether these TRP channels, including TRPC1 and TRPC6, are directly activated by mechanical stimulation. In the present review, we will focus on the mechanosensory function of TRP channels, discuss whether a direct or indirect mechanism is at play, and focus on the proposed role for these channels in the arterial myogenic response to changes in intraluminal pressure.
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Anyatonwu GI, Estrada M, Tian X, Somlo S, Ehrlich BE (2007) Regulation of ryanodine receptor-dependent calcium signaling by polycystin-2. Proc Natl Acad Sci USA 104:6454–6459
Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, Poblete J, Yamoah EN, Basbaum AI, Julius D (2006) TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124:1269–1282
Beech DJ (2005) Emerging functions of 10 types of TRP cationic channel in vascular smooth muscle. Clin Exp Pharmacol Physiol 32:597–603
Beech DJ (2005) TRPC1: store-operated channel and more. Pflugers Arch 451:53–60
Bichet D, Peters D, Patel A, Delmas P, Honoré E (2006) The cardiovascular polycystins: insights from autosomal dominant polycystic kidney disease and transgenic animal models. Trends Cardiovasc Med 16:292–298
Bode F, Sachs F, Franz MR (2001) Tarantula peptide inhibits atrial fibrillation. Nature 409:35–36
Bourque CW, Oliet SH, Richard D (1994) Osmoreceptors, osmoreception, and osmoregulation. Front Neuroendocrinol 15:231–274
Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306–313
Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398:436–441
Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816–824
Christensen AP, Corey DP (2007) TRP channels in mechanosensation: direct or indirect activation? Nat Rev Neurosci 8:510–521
Ciura S, Bourque CW (2006) Transient receptor potential vanilloid 1 is required for intrinsic osmoreception in organum vasculosum lamina terminalis neurons and for normal thirst responses to systemic hyperosmolality. J Neurosci 26:9069–9075
Clapham DE (2003) TRP channels as cellular sensors. Nature 426:517–524
Colbert HA, Smith TL, Bargmann CI (1997) OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J Neurosci 17:8259–8269
Corey DP (2006) What is the hair cell transduction channel? J Physiol 576:23–28
Corey DP, Garcia-Anoveros J, Holt JR, Kwan KY, Lin SY, Vollrath MA, Amalfitano A, Cheung EL, Derfler BH, Duggan A, Geleoc GS, Gray PA, Hoffman MP, Rehm HL, Tamasauskas D, Zhang DS (2004) TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432:723–730
Cuajungco MP, Grimm C, Oshima K, D’Hoedt D, Nilius B, Mensenkamp AR, Bindels RJ, Plomann M, Heller S (2006) PACSINs bind to the TRPV4 cation channel. PACSIN 3 modulates the subcellular localization of TRPV4. J Biol Chem 281:18753–18762
Davis MJ, Hill MA (1999) Signaling mechanisms underlying the vascular myogenic response. Physiol Rev 79:387–423
Delmas P (2005) Polycystins: polymodal receptor/ion-channel cellular sensors. Pflugers Arch 451:264–276
Denis V, Cyert MS (2002) Internal Ca(2+) release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue. J Cell Biol 156:29–34
Dietrich A, Kalwa H, Storch U, Mederos YSM, Salanova B, Pinkenburg O, Dubrovska G, Essin K, Gollasch M, Birnbaumer L, Gudermann T (2007) Pressure-induced and store-operated cation influx in vascular smooth muscle cells is independent of TRPC1. Pflugers Arch 455:465–477
Dietrich A, Mederos YSM, Gollasch M, Gross V, Storch U, Dubrovska G, Obst M, Yildirim E, Salanova B, Kalwa H, Essin K, Pinkenburg O, Luft FC, Gudermann T, Birnbaumer L (2005) Increased vascular smooth muscle contractility in TRPC6 −/− mice. Mol Cell Biol 25:6980–6989
Earley S, Straub SV, Brayden JE (2007) Protein kinase C regulates vascular myogenic tone through activation of TRPM4. Am J Physiol Heart Circ Physiol 292:H2613–2622
Earley S, Waldron BJ, Brayden JE (2004) Critical role for transient receptor potential channel TRPM4 in myogenic constriction of cerebral arteries. Circ Res 95:922–929
Gao X, Wu L, O'Neil RG (2003) Temperature-modulated diversity of TRPV4 channel gating: activation by physical stresses and phorbol ester derivatives through protein kinase C-dependent and -independent pathways. J Biol Chem 278:27129–27137
Giamarchi A, Padilla F, Coste B, Raoux M, Crest M, Honoré E, Delmas P (2006) The versatile nature of the calcium-permeable cation channel TRPP2. EMBO Rep 7:787–793
Giamarchi A, Padilla F, Crest M, Honoré E, Delmas P (2006) TRPP2: calcium permeable cation channel and more. Cell Mol Biol 52:105–114
Gillespie PG, Walker RG (2001) Molecular basis of mechanosensory transduction. Nature 413:194–202
Goodman MB, Schwarz EM (2003) Transducing touch in Caenorhabditis elegans. Annu Rev Physiol 65:429–452
Gottlieb P, Folgering J, Maroto R, Raso A, Wood TG, Kurosky A, Bowman C, Bichet D, Patel A, Sachs F, Martinac B, Hamill OP, Honore E (2007) Revisiting TRPC1 and TRPC6 mechanosensitivity. Pflugers Arch (in press) DOI 10.1007/s00424-007-0359-3
Grimm C, Kraft R, Sauerbruch S, Schultz G, Harteneck C (2003) Molecular and functional characterization of the melastatin-related cation channel TRPM3. J Biol Chem 278:21493–21501
Guharay F, Sachs F (1984) Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. J Physiol 352:685–701
Hamill OP (2006) Twenty odd years of stretch-sensitive channels. Pflugers Arch 453:333–351
Hanaoka K, Qian F, Boletta A, Bhunia AK, Piontek K, Tsiokas L, Sukhatme VP, Guggino WB, Germino GG (2000) Co-assembly of polycystin-1 and -2 produces unique cation-permeable currents. Nature 408:990–994
Hartmannsgruber V, Heyken WT, Kacik M, Kaistha A, Grgic I, Harteneck C, Liedtke W, Hoyer J, Kohler R (2007) Arterial response to shear stress critically depends on endothelial TRPV4 expression. PLoS ONE 2:e827
He Y, Yao G, Savoia C, Touyz RM (2005) Transient receptor potential melastatin 7 ion channels regulate magnesium homeostasis in vascular smooth muscle cells: role of angiotensin II. Circ Res 96:207–215
Hill K, Schaefer M (2007) TRPA1 is differentially modulated by the amphipathic molecules trinitrophenol and chlorpromazine. J Biol Chem 282:7145–7153
Hofmann T, Obukhov AG, Schaefer M, Harteneck C, Gudermann T, Schultz G (1999) Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397:259–263
Hofmann T, Schaefer M, Schultz G, Gudermann T (2002) Subunit composition of mammalian transient receptor potential channels in living cells. Proc Natl Acad Sci USA 99:7461–7466
Honoré E (2007) The neuronal background K2P channels: focus on TREK-1. Nature Rev Neurosci 8:251–261
Honoré E, Patel AJ, Chemin J, Suchyna T, Sachs F (2006) Desensitization of mechano-gated K2P channels. Proc Natl Acad Sci USA 103:6859–6864
Huang AL, Chen X, Hoon MA, Chandrashekar J, Guo W, Trankner D, Ryba NJ, Zuker CS (2006) The cells and logic for mammalian sour taste detection. Nature 442:934–938
Huber TB, Schermer B, Muller RU, Hohne M, Bartram M, Calixto A, Hagmann H, Reinhardt C, Koos F, Kunzelmann K, Shirokova E, Krautwurst D, Harteneck C, Simons M, Pavenstadt H, Kerjaschki D, Thiele C, Walz G, Chalfie M, Benzing T (2006) Podocin and MEC-2 bind cholesterol to regulate the activity of associated ion channels. Proc Natl Acad Sci USA 103:17079–17086
Hughes J, Ward CJ, Peral B, Aspinwall R, Clark K, San Millan JL, Gamble V, Harris PC (1995) The polycystic kidney disease 1 (PKD1) gene encodes a novel protein with multiple cell recognition domains. Nat Genet 10:151–160
Inoue R, Jensen LJ, Shi J, Morita H, Nishida M, Honda A, Ito Y (2006) Transient receptor potential channels in cardiovascular function and disease. Circ Res 99:119–131
Inoue R, Okada T, Onoue H, Hara Y, Shimizu S, Naitoh S, Ito Y, Mori Y (2001) The transient receptor potential protein homologue TRP6 is the essential component of vascular alpha(1)-adrenoceptor-activated Ca(2+)-permeable cation channel. Circ Res 88:325–332
Ishimaru Y, Inada H, Kubota M, Zhuang H, Tominaga M, Matsunami H (2006) Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor. Proc Natl Acad Sci USA 103:12569–12574
Kim J, Chung YD, Park DY, Choi S, Shin DW, Soh H, Lee HW, Son W, Yim J, Park CS, Kernan MJ, Kim C (2003) A TRPV family ion channel required for hearing in Drosophila. Nature 424:81–84
Kindt KS, Viswanath V, Macpherson L, Quast K, Hu H, Patapoutian A, Schafer WR (2007) Caenorhabditis elegans TRPA-1 functions in mechanosensation. Nat Neurosci 10:568–577
Kung C (2005) A possible unifying principle for mechanosensation. Nature 436:647–654
Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, Corey DP (2006) TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50:277–289
Li Q, Montalbetti N, Wu Y, Ramos AJ, Raychowdhury MK, Chen XZ, Cantiello HF (2006) Polycystin-2 cation channel function is under the control of microtubular structures in primary cilia of renal epithelial cells. J Biol Chem 281:37566–37575
Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM, Heller S (2000) Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103:525–535
Liedtke W, Tobin DM, Bargmann CI, Friedman JM (2003) Mammalian TRPV4 (VR-OAC) directs behavioral responses to osmotic and mechanical stimuli in Caenorhabditis elegans. Proc Natl Acad Sci USA 100(Suppl 2):14531–14536
Liu X, Bandyopadhyay B, Nakamoto T, Singh B, Liedtke W, Melvin JE, Ambudkar I (2006) A role for AQP5 in activation of TRPV4 by hypotonicity: concerted involvement of AQP5 and TRPV4 in regulation of cell volume recovery. J Biol Chem 281:15485–15495
Lukacs V, Thyagarajan B, Varnai P, Balla A, Balla T, Rohacs T (2007) Dual regulation of TRPV1 by phosphoinositides. J Neurosci 27:7070–7080
Maroto R, Raso A, Wood TG, Kurosky A, Martinac B, Hamill OP (2005) TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nat Cell Biol 7:179–185
Morita H, Honda A, Inoue R, Ito Y, Abe K, Nelson MT, Brayden JE (2007) Membrane stretch-induced activation of a TRPM4-like nonselective cation channel in cerebral artery myocytes. J Pharmacol Sci 103:417–426
Muraki K, Iwata Y, Katanosaka Y, Ito T, Ohya S, Shigekawa M, Imaizumi Y (2003) TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes. Circ Res 93:829–838
Nadler MJ, Hermosura MC, Inabe K, Perraud AL, Zhu Q, Stokes AJ, Kurosaki T, Kinet JP, Penner R, Scharenberg AM, Fleig A (2001) LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability. Nature 411:590–595
Nauli SM, Alenghat FJ, Luo Y, Williams E, Vassilev P, Li X, Elia AE, Lu W, Brown EM, Quinn SJ, Ingber DE, Zhou J (2003) Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 33:129–137
Nilius B, Owsianik G, Voets T, Peters JA (2007) Transient receptor potential cation channels in disease. Physiol Rev 87:165–217
Nilius B, Prenen J, Droogmans G, Voets T, Vennekens R, Freichel M, Wissenbach U, Flockerzi V (2003) Voltage dependence of the Ca2+-activated cation channel TRPM4. J Biol Chem 278:30813–30820
Nilius B, Prenen J, Wissenbach U, Bodding M, Droogmans G (2001) Differential activation of the volume-sensitive cation channel TRP12 (OTRPC4) and volume-regulated anion currents in HEK-293 cells. Pflugers Arch 443:227–233
Nilius B, Vennekens R (2006) From cardiac cation channels to the molecular dissection of the transient receptor potential channel TRPM4. Pflugers Arch 453:313–321
Nilius B, Vriens J, Prenen J, Droogmans G, Voets T (2004) TRPV4 calcium entry channel: a paradigm for gating diversity. Am J Physiol Cell Physiol 286:C195–205
Numata T, Shimizu T, Okada Y (2007) Direct mechano-stress sensitivity of TRPM7 channel. Cell Physiol Biochem 19:1–8
Numata T, Shimizu T, Okada Y (2007) TRPM7 is a stretch- and swelling-activated cation channel involved in volume regulation in human epithelial cells. Am J Physiol Cell Physiol 292:C460–467
O'Neil RG, Heller S (2005) The mechanosensitive nature of TRPV channels. Pflugers Arch 451:193–203
Oancea E, Wolfe JT, Clapham DE (2006) Functional TRPM7 channels accumulate at the plasma membrane in response to fluid flow. Circ Res 98:245–253
Oliet SH, Bourque CW (1993) Mechanosensitive channels transduce osmosensitivity in supraoptic neurons. Nature 364:341–343
Owsianik G, D'Hoedt D, Voets T, Nilius B (2006) Structure–function relationship of the TRP channel superfamily. Rev Physiol Biochem Pharmacol 156:61–90
Owsianik G, Talavera K, Voets T, Nilius B (2006) Permeation and selectivity of TRP channels. Annu Rev Physiol 68:685–717
Palmer CP, Zhou XL, Lin J, Loukin SH, Kung C, Saimi Y (2001) A TRP homolog in Saccharomyces cerevisiae forms an intracellular Ca(2+)-permeable channel in the yeast vacuolar membrane. Proc Natl Acad Sci USA 98:7801–7805
Patel AJ, Honoré E, Maingret F, Lesage F, Fink M, Duprat F, Lazdunski M (1998) A mammalian two pore domain mechano-gated S-like K+ channel. EMBO J 17:4283–4290
Patel AJ, Lazdunski M, Honoré E (2001) Lipid and mechano-gated 2P domain K+ channels. Curr Opin Cell Biol 13:422–428
Pedersen SA, Nilius B (2007) Transient receptor potential channels in mechanosensing and cell volume regulation. Methods Enzymol 428:183–207
Pedersen SF, Owsianik G, Nilius B (2005) TRP channels: an overview. Cell Calcium 38:233–252
Praetorius HA, Spring KR (2003) The renal cell primary cilium functions as a flow sensor. Curr Opin Nephrol Hypertens 12:517–520
Runnels LW, Yue L, Clapham DE (2001) TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science 291:1043–1047
Runnels LW, Yue L, Clapham DE (2002) The TRPM7 channel is inactivated by PIP2 hydrolysis. Nat Cell Biol 4:329–336
Sachs F (1997) Mechanical transduction by ion channels: how forces reach the channel. Soc Gen Physiol Ser 52:209–218
Sharif Naeini R, Witty MF, Seguela P, Bourque CW (2006) An N-terminal variant of Trpv1 channel is required for osmosensory transduction. Nat Neurosci 9:93–98
Sidi S, Friedrich RW, Nicolson T (2003) NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 301:96–99
Spassova MA, Hewavitharana T, Xu W, Soboloff J, Gill DL (2006) A common mechanism underlies stretch activation and receptor activation of TRPC6 channels. Proc Natl Acad Sci USA 103:16586–16591
Stein AT, Ufret-Vincenty CA, Hua L, Santana LF, Gordon SE (2006) Phosphoinositide 3-kinase binds to TRPV1 and mediates NGF-stimulated TRPV1 trafficking to the plasma membrane. J Gen Physiol 128:509–522
Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant TD (2000) OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2:695–702
Suchyna TM, Tape SE, Koeppe RE 2nd, Andersen OS, Sachs F, Gottlieb PA (2004) Bilayer-dependent inhibition of mechanosensitive channels by neuroactive peptide enantiomers. Nature 430:235–240
Sukharev S, Corey DP (2004) Mechanosensitive channels: multiplicity of families and gating paradigms. Science’s STKE 219:1–24
Takenaka T, Suzuki H, Okada H, Hayashi K, Kanno Y, Saruta T (1998) Mechanosensitive cation channels mediate afferent arteriolar myogenic constriction in the isolated rat kidney. J Physiol 511(Pt 1):245–253
Takenaka T, Suzuki H, Okada H, Hayashi K, Ozawa Y, Saruta T (1998) Biophysical signals underlying myogenic responses in rat interlobular artery. Hypertension 32:1060–1065
Tobin D, Madsen D, Kahn-Kirby A, Peckol E, Moulder G, Barstead R, Maricq A, Bargmann C (2002) Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35:307–318
Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI, Julius D (1998) The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21:531–543
Tsiokas L, Arnould T, Zhu C, Kim E, Walz G, Sukhatme VP (1999) Specific association of the gene product of PKD2 with the TRPC1 channel. Proc Natl Acad Sci USA 96:3934–3939
Tsiokas L, Kim S, Ong EC (2007) Cell biology of polycystin-2. Cell Signal 19:444–453
Vennekens R, Nilius B (2007) Insights into TRPM4 function, regulation and physiological role. Handb Exp Pharmacol 0:269–285
Voets T, Nilius B (2003) TRPs make sense. J Membr Biol 192:1–8
Voets T, Talavera K, Owsianik G, Nilius B (2005) Sensing with TRP channels. Nat Chem Biol 1:85–92
Vriens J, Owsianik G, Fisslthaler B, Suzuki M, Janssens A, Voets T, Morisseau C, Hammock BD, Fleming I, Busse R, Nilius B (2005) Modulation of the Ca2 permeable cation channel TRPV4 by cytochrome P450 epoxygenases in vascular endothelium. Circ Res 97:908–915
Vriens J, Owsianik G, Voets T, Droogmans G, Nilius B (2004) Invertebrate TRP proteins as functional models for mammalian channels. Pflugers Arch 449:213–226
Walker RG, Willingham AT, Zuker CS (2000) A Drosophila mechanosensory transduction channel. Science 287:2229–2234
Watanabe H, Vriens J, Prenen J, Droogmans G, Voets T, Nilius B (2003) Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424:434–438
Welsh DG, Morielli AD, Nelson MT, Brayden JE (2002) Transient receptor potential channels regulate myogenic tone of resistance arteries. Circ Res 90:248–250
Wu Y, Dai XQ, Li Q, Chen CX, Mai W, Hussain Z, Long W, Montalbetti N, Li G, Glynne R, Wang S, Cantiello HF, Wu G, Chen XZ (2006) Kinesin-2 mediates physical and functional interactions between polycystin-2 and fibrocystin. Hum Mol Genet 15:3280–3292
Yao X, Garland CJ (2005) Recent developments in vascular endothelial cell transient receptor potential channels. Circ Res 97:853–863
Zhang Y, Gao F, Popov VL, Wen JW, Hamill OP (2000) Mechanically gated channel activity in cytoskeleton-deficient plasma membrane blebs and vesicles from Xenopus oocytes. J Physiol 523 Pt 1:117–130
Zhou XL, Batiza AF, Loukin SH, Palmer CP, Kung C, Saimi Y (2003) The transient receptor potential channel on the yeast vacuole is mechanosensitive. Proc Natl Acad Sci USA 100:7105–7110
Acknowledgments
We are grateful to the ANR 2005 Cardiovasculaire-obésité-diabète, to the Association for Information and Research on Genetic Kidney Disease France, to the Fondation del Duca, to the Fondation de France, to the Fondation de la Recherche Médicale, to EEC Marie-Curie fellowships, to the Fondation de Recherche sur l’Hypertension Artérielle, to AFM, to INSERM, and to CNRS for support and Human Frontiers Science Program (HFSP Research Grant Ref. RGP 32/2004 BN and a long-term fellowship Ref. LT00555 to Dr. Sharif-Naeini), the Belgian Federal Government, the Flemish Government, the Onderzoeksraad KU Leuven (GOA 2004/07, F.W.O. G. 0136.00; F.W.O. G.0172.03, Interuniversity Poles of Attraction Program, Prime Ministers Office IUAP Nr.3P4/23, Excellentiefinanciering EF/95/010) to BN.
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Sharif-Naeini, R., Dedman, A., Folgering, J.H.A. et al. TRP channels and mechanosensory transduction: insights into the arterial myogenic response. Pflugers Arch - Eur J Physiol 456, 529–540 (2008). https://doi.org/10.1007/s00424-007-0432-y
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DOI: https://doi.org/10.1007/s00424-007-0432-y