The mechanosensitive nature of TRPV channels

Pflugers Archiv European Journal of Physiology

Volumn 451, Issue 1, 2005, Pages 193-203

  O'Neil, Roger G ^a   Heller, Stefan ^b  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

Author keywords

Calcium; Hearing; Mechanosensory; Osmosensory; Pressure; Shear stress; Touch; TRPV channels

Indexed keywords

'5,6' EPOXYEICOSATRIENOIC ACID; ARACHIDONIC ACID; CALCIUM CHANNEL; EPOXYICOSATRIENOIC ACID; HYBRID PROTEIN; HYPOTONIC SOLUTION; IAV PROTEIN; NANCHUNG PROTEIN; OCR 1 PROTEIN; OCR 2 PROTEIN; OCR 3 PROTEIN; OCR 4 PROTEIN; OSM 9 PROTEIN; PHOSPHOLIPASE A; POLYCYSTIN 2; PROTEIN; PROTEIN NOMPC; SEROTONIN; TRANSIENT RECEPTOR PROTEIN VANILLOID 1; TRANSIENT RECEPTOR PROTEIN VANILLOID 2; TRANSIENT RECEPTOR PROTEIN VANILLOID 3; TRANSIENT RECEPTOR PROTEIN VANILLOID 4; TRANSIENT RECEPTOR PROTEIN VANILLOID 5; TRANSIENT RECEPTOR PROTEIN VANILLOID 6; UNCLASSIFIED DRUG; VANILLOID RECEPTOR; VASOPRESSIN;

ANTENNA; ARTERY MUSCLE; AVOIDANCE BEHAVIOR; BIOSYNTHESIS; BREATHING MUSCLE; CAENORHABDITIS ELEGANS; CELL SWELLING; DROSOPHILA; EXTRACELLULAR FLUID; FLUID FLOW; GENETIC SCREENING; HAIR; HEARING; HUMAN; HYPOTHALAMUS; INNER EAR; MEAN ARTERIAL PRESSURE; MECHANORECEPTOR; NERVE CELL; NONHUMAN; ODOR; OSMORECEPTION; OSMORECEPTOR; OSMOREGULATION; OSMOTIC PRESSURE; PRESSORECEPTOR; PRESSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; SENSORY NERVE CELL; SENSORY STIMULATION; SHEAR STRESS; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; VASCULAR ENDOTHELIUM; VASOCONSTRICTION; VASOPRESSIN RELEASE;

ANIMALS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM CHANNELS; DROSOPHILA PROTEINS; HAIR CELLS; HEARING; HUMANS; ION CHANNELS; MECHANORECEPTORS; NERVE TISSUE PROTEINS; OSMOTIC PRESSURE; PRESSORECEPTORS; STRESS, MECHANICAL; TOUCH; TRANSIENT RECEPTOR POTENTIAL CHANNELS; TRPV CATION CHANNELS; ZEBRAFISH PROTEINS;

EID: 26444496051     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-005-1424-4     Document Type: Review

References (94)

1. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ, Patapoutian A (2004) Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41:849-857
2. Basavappa S, Pedersen SF, Jorgensen NK, Ellory JC, Hoffmann EK (1998) Swelling-induced arachidonic acid release via the 85-kDa cPLA2 in human neuroblastoma cells. J Neurophysiol 79:1441-1449
3. Benham CD, Gunthorpe MJ, Davis JB (2003) TRPV channels as temperature sensors. Cell Calcium 33:479-487
4. Blount P (2003) Molecular mechanisms of mechanosensation: big lessons from small cells. Neuron 37:731-734
5. Bourque CW, Oliet SH (1997) Osmoreceptors in the central nervous system. Annu Rev Physiol 59:601-619
6. Brown RC, O'Neil RG (2004) TRPC and TRPV channels in blood-brain barrier endothelial cells: Pathways for calcium entry after stress. Paper presented at the Society for Neuroscience 34th annual meeting, San Diego (program no. 198.14)
7. Calvet JP, Grantham JJ (2001) The genetics and physiology of polycystic kidney disease. Semin Nephrol 21:107-123
8. Chen XZ, Segal Y, Basora N, Guo L, Peng JB, Babakhanlou H, Vassilev PM, Brown EM, Hediger MA, Zhou J (2001) Transport function of the naturally occurring pathogenic polycystin-2 mutant, R742X. Biochem Biophys Res Commun 282:1251-1256
9. Clapham DE (2003) TRP channels as cellular sensors. Nature 426:517-524
10. 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
11. Corey DP (2003) New TRP channels in hearing and mechanosensation. Neuron 39:585-588
12. 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
13. Delany NS, Hurle M, Facer P, Alnadaf T, Plumpton C, Kinghorn I, See CG, Costigan M, Anand P, Woolf CJ, Crowther D, Sanseau P, Tate SN (2001) Identification and characterization of a novel human vanilloid receptor-like protein, VRL-2. Physiol Genomics 4:165-174
14. Delmas P, Padilla F, Osorio N, Coste B, Raoux M, Crest M (2004) Polycystins, calcium signaling, and human diseases. Biochem Biophys Res Commun 322:1374-1383
15. + channel proteins: components of a vascular mechanosensor. Hypertension 44:643-648
16. Drummond HA, Welsh MJ, Abboud FM (2001) ENaC subunits are molecular components of the arterial baroreceptor complex. Ann NY Acad Sci 940:42-47
17. 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
18. Eberl DF, Hardy RW, Kernan MJ (2000) Genetically similar transduction mechanisms for touch and hearing in Drosophila. J Neurosci 20:5981-5988
19. 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
20. Gillespie PG, Walker RG (2001) Molecular basis of mechanosensory transduction. Nature 413:194-202
21. Gong Z, Son W, Chung YD, Kim J, Shin DW, McClung CA, Lee Y, Lee HW, Chang DJ, Kaang BK, Cho H, Oh U, Hirsh J, Kernan MJ, Kim C (2004) Two interdependent TRPV channel subunits, inactive and Nanchung, mediate hearing in Drosophila. J Neurosci 24:9059-9066
22. Goodman MB, Schwarz EM (2003) Transducing touch in Caenorhabditis elegans. Annu Rev Physiol 65:429-452
23. ++ in the receptor lymph of arthropod cuticular mechanoreceptors. J Comp Physiol [A] 161:329-333
24. Guler AD, Lee H, Iida T, Shimizu I, Tominaga M, Caterina M (2002) Heat-evoked activation of the ion channel, TRPV4. J Neurosci 22:6408-6414
25. 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
26. Hardie RC (2003) Regulation of TRP channels via lipid second messengers. Annu Rev Physiol 65:735-759
27. Helmlinger G, Berk BC, Nerem RM (1996) Pulsatile and steady flow-induced calcium oscillations in single cultured endothelial cells. J Vasc Res 33:360-369
28. Hoenderop JG, Nilius B, Bindels RJ (2005) Calcium absorption across epithelia. Physiol Rev 85:373-422
29. Howard J, Bechstedt S (2004) Hypothesis: a helix of ankyrin repeats of the NOMPC-TRP ion channel is the gating spring of mechanoreceptors. Curr Biol 14:R224-R226
30. Hudspeth AJ (1989) How the ear's works work. Nature 341:397-404
31. Hudspeth AJ (2001) How the ear's works work: mechanoelectrical transduction and amplification by hair cells of the internal ear. Harvey Lect 97:41-54
32. Igarashi P, Somlo S (2002) Genetics and pathogenesis of polycystic kidney disease. J Am Soc Nephrol 13:2384-2398
33. Jaquemar D, Schenker T, Trueb B (1999) An ankyrin-like protein with transmembrane domains is specifically lost after oncogenic transformation of human fibroblasts. J Biol Chem 274:7325-7333
34. Jia Y, Wang X, Varty L, Rizzo CA, Yang R, Correll CC, Phelps PT, Egan RW, Hey JA (2004) Functional TRPV4 channels are expressed in human airway smooth muscle cells. Am J Physiol 287:L272-L278
35. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Hogestatt ED, Meng ID, Julius D (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427:260-265
36. Kaplan JM, Horvitz HR (1993) A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. Proc Natl Acad Sci USA 90:2227-2231
37. Kernan M, Cowan D, Zuker C (1994) Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron 12:1195-1206
38. 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
39. Kraske S, Cunningham JT, Hajduczok G, Chapleau MW, Abboud FM, Wachtel RE (1998) Mechanosensitive ion channels in putative aortic baroreceptor neurons. Am J Physiol 275:H1497-H1501
40. Kumada M, Terui N, Kuwaki T (1990) Arterial baroreceptor reflex: its central and peripheral neural mechanisms. Prog Neurobiol 35:331-361
41. 2+ influx in rat endothelial cells. Circ Res 92:286-292
42. 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
43. -/- mice. Proc Natl Acad Sci USA 100:13698-13703
44. 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
45. i response of principal and intercalated cells in cortical collecting duct. Am J Physiol 285:F998-F1012
46. McCarty NA, O'Neil RG (1992) Calcium signaling in cell volume regulation. Physiol Rev 72:1037-1061
47. Mizuno A, Matsumoto N, Imai M, Suzuki M (2003) Impaired osmotic sensation in mice lacking TRPV4. Am J Physiol 285:C96-C101
48. Montell C (2005) The TRP superfamily of cation channels. Sci STKE 2005:re3
49. Montell C (2003) The venerable inveterate invertebrate TRP channels. Cell Calcium 33:409-417
50. Moran MM, Xu H, Clapham DE (2004) TRP ion channels in the nervous system. Curr Opin Neurobiol 14:362-369
51. 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
52. Mutai H, Heller S (2003) Vertebrate and invertebrate TRPV-like mechanoreceptors. Cell Calcium 33:471-478
53. Nakamura T (2000) Cellular and molecular constituents of olfactory sensation in vertebrates. Comp Biochem Physiol A Mol Integr Physiol 126:17-32
54. 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
55. Nauli SM, Zhou J (2004) Polycystins and mechanosensation in renal and nodal cilia. Bioessays 26:844-856
56. Nilius B, Droogmans G, Wondergem R (2003) Transient receptor potential channels in endothelium: solving the calcium entry puzzle? Endothelium 10:5-15
57. 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
58. Nilius B, Voets T (2004) Diversity of TRP channel activation. Novartis Found Symp 258:140-149; discussion 149-159, 263-266
59. Nilius B, Vriens J, Prenen J, Droogmans G, Voets T (2004) TRPV4 calcium entry channel: a paradigm for gating diversity. Am J Physiol 286:C195-C205
60. Okada Y, Maeno E, Shimizu T, Dezaki K, Wang J, Morishima S (2001) Receptor-mediated control of regulatory volume decrease (RVD) and apoptotic volume decrease (AVD). J Physiol 532:3-16
61. O'Neil RG, Brown RC (2003) The vanilloid receptor family of calcium-permeable channels: molecular integrators of microenvironmental stimuli. News Physiol Sci 18:226-231
62. O'Neil RG, Gao X, Wu L (2005) Mechanosensitive nature of the TRPV4 channel in renal epithelia revealed by siRNA gene silencing. FASEB J 19:A1163
63. Pazour GJ, San Agustin JT, Follit JA, Rosenbaum JL, Witman GB (2002) Polycystin-2 localizes to kidney cilia and the ciliary level is elevated in orpk mice with polycystic kidney disease. Curr Biol 12:R378-R380
64. 2+ transport and beyond. J Physiol 551:729-740
65. Praetorius HA, Spring KR (2001) Bending the MDCK cell primary cilium increases intracellular calcium. J Membr Biol 184:71-79
66. Rosenzweig M, Brennan KM, Tayler TD, Phelps PO, Patapoutian A, Garrity PA (2005) The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. Genes Dev 19:419-424
67. Sidi S, Friedrich RW, Nicolson T (2003) NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 301:96-99
68. Snitsarev V, Whiteis CA, Abboud FM, Chapleau MW (2002) Mechanosensory transduction of vagal and baroreceptor afferents revealed by study of isolated nodose neurons in culture. Auton Neurosci 98:59-63
69. Sokolchik I, Tanabe T, Baldi PF, Sze JY (2005) Polymodal sensory function of the Caenorhabditis elegans OCR-2 channel arises from distinct intrinsic determinants within the protein and is selectively conserved in mammalian TRPV proteins. J Neurosci 25:1015-1023
70. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819-829
71. 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
72. Sukharev S, Corey DP (2004) Mechanosensitive channels: multiplicity of families and gating paradigms. Sci STKE 2004:re4
73. 2+ influx through mechanosensitive ion channels in aortic baroreceptor neurons. Circ Res 80:861-867
74. Syntichaki P, Tavernarakis N (2004) Genetic models of mechanotransduction: the nematode Caenorhabditis elegans. Physiol Rev 84:1097-153
75. Tavernarakis N, Driscoll M (2001) Mechanotransduction in Caenorhabditis elegans: the role of DEG/ENaC ion channels. Cell Biochem Biophys 35:1-18
76. Thoroed SM, Lauritzen L, Lambert IH, Hansen HS, Hoffmann EK (1997) Cell swelling activates phospholipase A2 in Ehrlich ascites tumor cells. J Membr Biol 160:47-58
77. Thurm U (1965) An insect mechanoreceptor. I. Fine structure and adequate stimulus. Cold Spring Harb Symp Quant Biol 30:75-82
78. Thurm U (1965) An insect mechanoreceptor. II. Receptor potentials. Cold Spring Harb Symp Quant Biol 30:83-94
79. Tian W, Salanova M, Xu H, Lindsley JN, Oyama TT, Anderson S, Bachmann S, Cohen DM (2004) Renal expression of osmotically responsive cation channel TRPV4 is restricted to water-impermeant nephron segments. Am J Physiol 287:F17-F24
80. Tinel H, Kinne-Saffran E, Kinne RK (2000) Calcium signalling during RVD of kidney cells. Cell Physiol Biochem 10:297-302
81. 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
82. Tominaga M, Caterina MJ (2004) Thermosensation and pain. J Neurobiol 61:3-12
83. Tracey WD Jr, Wilson RI, Laurent G, Benzer S (2003) Painless, a Drosophila gene essential for nociception. Cell 113:261-273
84. Trudeau MC, Zagotta WN (2003) Calcium/calmodulin modulation of olfactory and rod cyclic nucleotide-gated ion channels. J Biol Chem 278:18705-18708
85. Viswanath V, Story GM, Peier AM, Petrus MJ, Lee VM, Hwang SW, Patapoutian A, Jegla T (2003) Opposite thermosensor in fruit fly and mouse. Nature 423:822-823
86. Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T, Nilius B (2004) Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci USA 101:396-401
87. Walker RG, Willingham AT, Zuker CS (2000) A Drosophila mechanosensory transduction channel. Science 287:2229-2234
88. 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
89. Watanabe H, Vriens J, Suh SH, Benham CD, Droogmans G, Nilius B (2002) Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J Biol Chem 277:47044-47051
90. Wissenbach U, Bodding M, Freichel M, Flockerzi V (2000) Trp12, a novel Trp related protein from kidney. FEBS Lett 485:127-134
91. i in rabbit cortical collecting duct. Am J Physiol 283:F437-46
92. Xu GM, Gonzalez-Perrett S, Essafi M, Timpanaro GA, Montalbetti N, Arnaout MA, Cantiello HF (2003) Polycystin-1 activates and stabilizes the polycystin-2 channel. J Biol Chem 278:1457-1462
93. 2+ entry into vascular endothelial cells. FASEB J 14:932-938
94. Yoder BK, Hou X, Guay-Woodford LM (2002) The polycystic kidney disease proteins, polycystin-1, polycystin-2, polaris, and cystin, are co-localized in renal cilia. J Am Soc Nephrol 13:2508-2516