Advertisement

TRP Channels and Mechanical Signals

  • Makoto Suzuki
  • Atsuko Mizuno

Abstract

Transient receptor potential (TRP) channels are a unique cellular mechanism converting a wide variety of signals, including mechanical stress, to cation flow. The protein was first discovered in studies that examined Drosophila phototransduction (Lo and Pak 1981). The photoreceptor cells of wild Drosophila exhibit sustained receptor potential, while a mutant showing a transient receptor potential (trp) in response to continuous light exposure was reported (Cosens and Manning 1969). The ionic basis for the sustained receptor potentials is an influx of Ca2+ from the extracellular space. The trp gene was cloned in 1989 (Montell and Rubin 1989) and was subsequently shown to encode a Ca2+-permeable cation channel (Hardie and Minke 1992). Since then, many channels that bear sequence and structural similarities to the Drosophila TRP have been cloned from flies, worms, and mammals.

Keywords

Transient Receptor Potential Primary Cilium Transient Receptor Potential Channel Mechanosensitive Channel Cortical Collect Duct 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was supported by grants-in-aid for scientific research (17590255, 18590899, 22590291), and grants from Japan Space Forum, JAXA.

References

  1. Allen DG, Whitehead NP, Yeung EW (2005) Mechanisms of stretch-induced muscle damage in normal and dystrophic muscle: role of ionic changes. J Physiol 567  :  723–735PubMedCrossRefGoogle Scholar
  2. Bai CX, Giamarchi A, Rodat-Despoix L, Padilla F, Downs T, Tsiokas L, Delmas P (2008) Formation of a new receptor-operated channel by heteromeric assembly of TRPP2 and TRPC1 subunits. EMBO Rep 9  :  472–479PubMedCrossRefGoogle Scholar
  3. 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  :  1441–1449PubMedGoogle Scholar
  4. 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  :  1269–1282PubMedCrossRefGoogle Scholar
  5. 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  :  816–824Google Scholar
  6. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398  :  436–441PubMedCrossRefGoogle Scholar
  7. 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  :  9069–9075PubMedCrossRefGoogle Scholar
  8. 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  :  723–730PubMedCrossRefGoogle Scholar
  9. Cosens DJ, Manning A (1969) Abnormal electroretinogram from a Drosophila mutant. Nature 224  :  285–287PubMedCrossRefGoogle Scholar
  10. Delmas P (2004) Polycystins: from mechanosensation to gene regulation. Cell 118  :  145–148PubMedCrossRefGoogle Scholar
  11. Delmas P (2005) Polycystins: polymodal receptor/ion-channel cellular sensors. Pflugers Arch 451  :  264–276PubMedCrossRefGoogle Scholar
  12. Delmas P, Nauli SM, Li X, Coste B, Osorio N, Crest M, Brown DA, Zhou J (2004) Gating of the polycystin ion channel signaling complex in neurons and kidney cells. FASEB J 18  :  740–742PubMedGoogle Scholar
  13. Dietrich A, Kalwa H, Storch U, Mederos Y, Schnitzler M, 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  :  465–477PubMedCrossRefGoogle Scholar
  14. Gavva NR, Klionsky L, Qu Y, Shi L, Tamir R, Edenson S, Zhang TJ, Viswanadhan VN, Toth A, Pearce LV, Vanderah TW, Porreca F, Blumberg PM, Lile J, Sun Y, Wild K, Louis JC, Treanor JJ (2004) Molecular determinants of vanilloid sensitivity in TRPV1. J Biol Chem 279  :  20283–20295PubMedCrossRefGoogle Scholar
  15. 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 (2008) Revisiting TRPC1 and TRPC6 mechanosensitivity. Pflugers Arch 455  :  1097–1103PubMedCrossRefGoogle Scholar
  16. 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  :  21493–21501PubMedCrossRefGoogle Scholar
  17. 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  :  990–994PubMedCrossRefGoogle Scholar
  18. Hardie RC, Minke B (1992) The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors. Neuron 8  :  643–651PubMedCrossRefGoogle Scholar
  19. Hernandez M, Burillo SL, Crespo MS, Nieto ML (1998) Secretory phospholipase A2 activates the cascade of mitogen-activated protein kinases and cytosolic phospholipase A2 in the human astrocytoma cell line 1321N1. J Biol Chem 273  :  606–612PubMedCrossRefGoogle Scholar
  20. Hill K, Schaefer M (2007) TRPA1 is differentially modulated by the amphipathic molecules trinitrophenol and chlorpromazine. J Biol Chem 282  :  7145–7153PubMedCrossRefGoogle Scholar
  21. Honore E (2007) The neuronal background K2P channels: focus on TREK1. Nat Rev Neurosci 8  :  251–261PubMedCrossRefGoogle Scholar
  22. 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–R226PubMedCrossRefGoogle Scholar
  23. 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  :  17079–17086PubMedCrossRefGoogle Scholar
  24. Igarashi P, Somlo S (2002) Genetics and pathogenesis of polycystic kidney disease. J Am Soc Nephrol 13  :  2384–2398PubMedCrossRefGoogle Scholar
  25. Iwata Y, Katanosaka Y, Arai Y, Komamura K, Miyatake K, Shigekawa M (2003) A novel mechanism of myocyte degeneration involving the Ca2+-permeable growth factor-regulated channel. J Cell Biol 161  :  957–967PubMedCrossRefGoogle Scholar
  26. 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  :  568–577PubMedCrossRefGoogle Scholar
  27. Kottgen M, Buchholz B, Garcia-Gonzalez MA, Kotsis F, Fu X, Doerken M, Boehlke C, Steffl D, Tauber R, Wegierski T, Nitschke R, Suzuki M, Kramer-Zucker A, Germino GG, Watnick T, Prenen J, Nilius B, Kuehn EW, Walz G (2008) TRPP2 and TRPV4 form a polymodal sensory channel complex. J Cell Biol 182  :  437–447PubMedCrossRefGoogle Scholar
  28. Koulen P, Cai Y, Geng L, Maeda Y, Nishimura S, Witzgall R, Ehrlich BE, Somlo S (2002) Polycystin-2 is an intracellular calcium release channel. Nat Cell Biol 4  :  191–197PubMedCrossRefGoogle Scholar
  29. 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  :  277–289PubMedCrossRefGoogle Scholar
  30. Launay P, Cheng H, Srivatsan S, Penner R, Fleig A, Kinet JP (2004) TRPM4 regulates calcium oscillations after T cell activation. Science 306  :  1374–1377PubMedCrossRefGoogle Scholar
  31. Liedtke W, Friedman JM (2003) Abnormal osmotic regulation in trpv4−/− mice. Proc Natl Acad Sci USA 100  :  13698–13703PubMedCrossRefGoogle Scholar
  32. 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  :  525–535PubMedCrossRefGoogle Scholar
  33. 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)  :  14531–14536PubMedCrossRefGoogle Scholar
  34. Lo MV, Pak WL (1981) Light-induced pigment granule migration in the retinular cells of Drosophila melanogaster. Comparison of wild type with ERG-defective mutants. J Gen Physiol 77  :  155–175PubMedCrossRefGoogle Scholar
  35. Luo Y, Vassilev PM, Li X, Kawanabe Y, Zhou J (2003) Native polycystin 2 functions as a plasma membrane Ca2+-permeable cation channel in renal epithelia. Mol Cell Biol 23  :  2600–2607PubMedCrossRefGoogle Scholar
  36. 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  :  179–185PubMedCrossRefGoogle Scholar
  37. Montell C, Rubin GM (1989) Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron 2  :  1313–1323PubMedCrossRefGoogle Scholar
  38. 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  :  417–426PubMedCrossRefGoogle Scholar
  39. 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  :  829–838PubMedCrossRefGoogle Scholar
  40. Nauli SM, Zhou J (2004) Polycystins and mechanosensation in renal and nodal cilia. Bioessays 26  :  844–856PubMedCrossRefGoogle Scholar
  41. 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  :  129–137PubMedCrossRefGoogle Scholar
  42. 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  :  30813–30820PubMedCrossRefGoogle Scholar
  43. Numata T, Shimizu T, Okada Y (2007) Direct mechano-stress sensitivity of TRPM7 channel. Cell Physiol Biochem 19  :  1–8PubMedCrossRefGoogle Scholar
  44. Patel AJ, Honore 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  :  4283–4290PubMedCrossRefGoogle Scholar
  45. 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–R380PubMedCrossRefGoogle Scholar
  46. Praetorius HA, Spring KR (2001) Bending the MDCK cell primary cilium increases intracellular calcium. J Membr Biol 184  :  71–79PubMedCrossRefGoogle Scholar
  47. Praetorius HA, Spring KR (2003) Removal of the MDCK cell primary cilium abolishes flow sensing. J Membr Biol 191  :  69–76PubMedCrossRefGoogle Scholar
  48. Raychowdhury MK, McLaughlin M, Ramos AJ, Montalbetti N, Bouley R, Ausiello DA, Cantiello HF (2005) Characterization of single channel currents from primary cilia of renal epithelial cells. J Biol Chem 280  :  34718–34722PubMedCrossRefGoogle Scholar
  49. Runnels LW, Yue L, Clapham DE (2002) The TRPM7 channel is inactivated by PIP(2) hydrolysis. Nat Cell Biol 4  :  329–336PubMedGoogle Scholar
  50. Scheffers MS, Le H, van der Bent P, Leonhard W, Prins F, Spruit L, Breuning MH, de Heer E, Peters DJ (2002) Distinct subcellular expression of endogenous polycystin-2 in the plasma membrane and Golgi apparatus of MDCK cells. Hum Mol Genet 11  :  59–67PubMedCrossRefGoogle Scholar
  51. 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  :  93–98PubMedCrossRefGoogle Scholar
  52. Sidhaye VK, Guler AD, Schweitzer KS, D’Alessio F, Caterina MJ, King LS (2006) Transient receptor potential vanilloid 4 regulates aquaporin-5 abundance under hypotonic conditions. Proc Natl Acad Sci USA 103  :  4747–4752PubMedCrossRefGoogle Scholar
  53. Sotomayor M, Corey DP, Schulten K (2005) In search of the hair-cell gating spring elastic properties of ankyrin and cadherin repeats. Structure 13  :  669–682PubMedCrossRefGoogle Scholar
  54. 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  :  16586–16591PubMedCrossRefGoogle Scholar
  55. 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  :  695–702PubMedCrossRefGoogle Scholar
  56. Suchyna TM, Johnson JH, Hamer K, Leykam JF, Gage DA, Clemo HF, Baumgarten CM, Sachs F (2000) Identification of a peptide toxin from Grammostola spatulata spider venom that blocks cation-selective stretch-activated channels. J Gen Physiol 115  :  583–598PubMedCrossRefGoogle Scholar
  57. 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  :  235–240PubMedCrossRefGoogle Scholar
  58. Suzuki M, Mizuno A, Kodaira K, Imai M (2003) Impaired pressure sensation in mice lacking TRPV4. J Biol Chem 278  :  22664–22668PubMedCrossRefGoogle Scholar
  59. Taniguchi J, Takeda M, Yoshitomi K, Imai M (1994) Pressure- and parathyroid-hormone-dependent Ca2+ transport in rabbit connecting tubule: role of the stretch-activated nonselective cation channel. J Membr Biol 140  :  123–132PubMedGoogle Scholar
  60. Taniguchi J, Tsuruoka S, Mizuno A, Sato J, Fujimura A, Suzuki M (2007) TRPV4 as a flow sensor in flow-dependent K+ secretion from the cortical collecting duct. Am J Physiol Renal Physiol 292  :  F667–F673PubMedCrossRefGoogle Scholar
  61. Thodeti CK, Matthews B, Ravi A, Mammoto A, Ghosh K, Bracha AL, Ingber DE (2009) TRPV4 channels mediate cyclic strain-induced endothelial cell reorientation through integrin-to-integrin signaling. Circ Res 104  :  1123–1130PubMedCrossRefGoogle Scholar
  62. 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  :  3934–3939PubMedCrossRefGoogle Scholar
  63. Venkatachalam K, van Rossum DB, Patterson RL, Ma HT, Gill DL (2002) The cellular and molecular basis of store-operated calcium entry. Nat Cell Biol 4  :  E263–E272PubMedCrossRefGoogle Scholar
  64. Venkatachalam K, Zheng F, Gill DL (2003) Regulation of canonical transient receptor potential (TRPC) channel function by diacylglycerol and protein kinase C. J Biol Chem 278  :  29031–29040PubMedCrossRefGoogle Scholar
  65. 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  :  396–401PubMedCrossRefGoogle Scholar
  66. 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  :  908–915PubMedCrossRefGoogle Scholar
  67. 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  :  434–438PubMedCrossRefGoogle Scholar
  68. 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  :  2508–2516PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2011

Authors and Affiliations

  1. 1.Edogawabashi-clinicShinjuku-kuJapan
  2. 2.Department of PharmacologyJichi Medical UniversityShimotsukeJapan

Personalised recommendations