The history of TRP channels, a commentary and reflection

Invited Review
  • 1.2k Downloads

Abstract

The transient receptor potential (TRP) family of cation channels has redefined our understanding of sensory physiology. In one animal or another, all senses depend on TRP channels. These include vision, taste, smell, hearing, and various forms of touch, including the ability to sense changes in temperature. The first trp gene was identified because it was disrupted in a Drosophila mutant with defective vision. However, there was no clue as to its biochemical function until the cloning, and analysis of the deduced amino acid sequence suggested that trp encoded a cation channel. This concept was further supported by subsequent electrophysiological studies, including alteration of its ion selectivity by an amino acid substitution within the pore loop. The study of TRP channels emerged as a field with the identification of mammalian homologs, some of which are direct sensors of environmental temperature. At least one TRP channel is activated downstream of a thermosensory signaling cascade, demonstrating that there exist two modes of activation, direct and indirect, through which TRP channels respond to changes in temperature. Mutations in many TRP channels result in disease, including a variety of sensory impairments.

Keywords

Transient receptor potential TRP channels Sensory signaling Thermosensation Taste Vision Smell Touch Calcium Drosophila 

References

  1. 1.
    Atkinson NS, Robertson GA, Ganetzky B (1991) A component of calcium-activated potassium channels encoded by the Drosophila slo locus. Science 253:551–555PubMedCrossRefGoogle Scholar
  2. 2.
    Audo I, Kohl S, Leroy BP, Munier FL, Guillonneau X, Mohand-Said S, Bujakowska K, Nandrot EF, Lorenz B, Preising M, Kellner U, Renner AB, Bernd A, Antonio A, Moskova-Doumanova V, Lancelot ME, Poloschek CM, Drumare I, Defoort-Dhellemmes S, Wissinger B, Leveillard T, Hamel CP, Schorderet DF, De Baere E, Berger W, Jacobson SG, Zrenner E, Sahel JA, Bhattacharya SS, Zeitz C (2009) TRPM1 is mutated in patients with autosomal-recessive complete congenital stationary night blindness. Am J Hum Genet 85:720–729PubMedCrossRefGoogle Scholar
  3. 3.
    Auer-Grumbach M, Olschewski A, Papic’ L, Kremer H, McEntagart ME, Uhrig S, Fischer C, Fröhlich E, Balint Z, Tang B, Strohmaier H, Lochmuller H, Schlotter-Weigel B, Senderek J, Krebs A, Dick KJ, Petty R, Longman C, Anderson NE, Padberg GW, Schelhaas HJ, van Ravenswaaij-Arts CM, Pieber TR, Crosby AH, Guelly C (2010) Alterations in the ankyrin domain of TRPV4 cause congenital distal SMA, scapuloperoneal SMA and HMSN2C. Nat Genet 42:160–164PubMedCrossRefGoogle Scholar
  4. 4.
    Bandell M, Macpherson LJ, Patapoutian A (2007) From chills to chilis: mechanisms for thermosensation and chemesthesis via thermoTRPs. Curr Opin Neurobiol 17:490–497PubMedCrossRefGoogle Scholar
  5. 5.
    Bargal R, Avidan N, Ben-Asher E, Olender Z, Zeigler M, Frumkin A, Raas-Rothschild A, Glusman G, Lancet D, Bach G (2000) Identification of the gene causing mucolipidosis type IV. Nat Genet 26:118–123PubMedCrossRefGoogle Scholar
  6. 6.
    Bassi MT, Manzoni M, Monti E, Pizzo MT, Ballabio A, Borsani G (2000) Cloning of the gene encoding a novel integral membrane protein, mucolipidin—and identification of the two major founder mutations causing mucolipidosis type IV. Am J Hum Genet 67:1110–1120PubMedGoogle Scholar
  7. 7.
    Caterina MJ (2007) Transient receptor potential ion channels as participants in thermosensation and thermoregulation. Am J Physiol Regul Integr Comp Physiol 292:R64–R76PubMedCrossRefGoogle Scholar
  8. 8.
    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 389:816–824PubMedCrossRefGoogle Scholar
  9. 9.
    Chevesich J, Kreuz AJ, Montell C (1997) Requirement for the PDZ domain protein, INAD, for localization of the TRP store-operated channel to a signaling complex. Neuron 18:95–105PubMedCrossRefGoogle Scholar
  10. 10.
    Christensen AP, Corey DP (2007) TRP channels in mechanosensation: direct or indirect activation? Nat Rev Neurosci 8:510–521PubMedCrossRefGoogle Scholar
  11. 11.
    Colbert HA, Bargmann CI (1995) Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans. Neuron 14:803–812PubMedCrossRefGoogle Scholar
  12. 12.
    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 17:8259–8269PubMedGoogle Scholar
  13. 13.
    Cosens DJ, Manning A (1969) Abnormal electroretinogram from a Drosophila mutant. Nature 224:285–287PubMedCrossRefGoogle Scholar
  14. 14.
    Deng HX, Klein CJ, Yan J, Shi Y, Wu Y, Fecto F, Yau HJ, Yang Y, Zhai H, Siddique N, Hedley-Whyte ET, Delong R, Martina M, Dyck PJ, Siddique T (2010) Scapuloperoneal spinal muscular atrophy and CMT2C are allelic disorders caused by alterations in TRPV4. Nat Genet 42:165–169PubMedCrossRefGoogle Scholar
  15. 15.
    Ganetzky B, Wu CF (1986) Neurogenetics of membrane excitability in Drosophila. Annu Rev Genet 20:13–44PubMedCrossRefGoogle Scholar
  16. 16.
    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 24:9059–9066PubMedCrossRefGoogle Scholar
  17. 17.
    Göpfert MC, Albert JT, Nadrowski B, Kamikouchi A (2006) Specification of auditory sensitivity by Drosophila TRP channels. Nat Neurosci 9:999–1000PubMedCrossRefGoogle Scholar
  18. 18.
    Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440–3450PubMedGoogle Scholar
  19. 19.
    Hardie RC (1991) Whole-cell recordings of the light induced current in dissociated Drosophila photoreceptors: evidence for feedback by calcium permeating the light-sensitive channels. Proc R Soc Lond B 245:203–210CrossRefGoogle Scholar
  20. 20.
    Hardie RC, Minke B (1992) The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors. Neuron 8:643–651PubMedCrossRefGoogle Scholar
  21. 21.
    Hermosura MC, Cui AM, Go RC, Davenport B, Shetler CM, Heizer JW, Schmitz C, Mocz G, Garruto RM, Perraud AL (2008) Altered functional properties of a TRPM2 variant in Guamanian ALS and PD. Proc Natl Acad Sci USA 105:18029–18034PubMedCrossRefGoogle Scholar
  22. 22.
    Huber A, Sander P, Gobert A, Bähner M, Hermann R, Paulsen R (1996) The transient receptor potential protein (Trp), a putative store-operated Ca2+ channel essential for phosphoinositide-mediated photoreception, forms a signaling complex with NorpA, InaC and InaD. EMBO J 15:7036–7045PubMedGoogle Scholar
  23. 23.
    Kamb A, Iverson LE, Tanouye MA (1987) Molecular characterization of Shaker, a Drosophila gene that encodes a potassium channel. Cell 50:405–413PubMedCrossRefGoogle Scholar
  24. 24.
    Kang L, Gao J, Schafer WR, Xie Z, Xu XZ (2010) C. elegans TRP family protein TRP-4 is a pore-forming subunit of a native mechanotransduction channel. Neuron 67:381–391PubMedCrossRefGoogle Scholar
  25. 25.
    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 424:81–84PubMedCrossRefGoogle Scholar
  26. 26.
    Kim SH, Lee Y, Akitake B, Woodward OM, Guggino WB, Montell C (2010) Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons. Proc Natl Acad Sci USA 107:8440–8445PubMedCrossRefGoogle Scholar
  27. 27.
    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
  28. 28.
    Krakow D, Vriens J, Camacho N, Luong P, Deixler H, Funari TL, Bacino CA, Irons MB, Holm IA, Sadler L, Okenfuss EB, Janssens A, Voets T, Rimoin DL, Lachman RS, Nilius B, Cohn DH (2009) Mutations in the gene encoding the calcium-permeable ion channel TRPV4 produce spondylometaphyseal dysplasia, Kozlowski type and metatropic dysplasia. Am J Hum Genet 84:307–315PubMedCrossRefGoogle Scholar
  29. 29.
    Kremeyer B, Lopera F, Cox JJ, Momin A, Rugiero F, Marsh S, Woods CG, Jones NG, Paterson KJ, Fricker FR, Villegas A, Acosta N, Pineda-Trujillo NG, Ramirez JD, Zea J, Burley MW, Bedoya G, Bennett DL, Wood JN, Ruiz-Linares A (2010) A gain-of-function mutation in TRPA1 causes familial episodic pain syndrome. Neuron 66:671–680PubMedCrossRefGoogle Scholar
  30. 30.
    Kruse M, Schulze-Bahr E, Corfield V, Beckmann A, Stallmeyer B, Kurtbay G, Ohmert I, Brink P, Pongs O (2009) Impaired endocytosis of the ion channel TRPM4 is associated with human progressive familial heart block type I. J Clin Invest 119:2737–2744PubMedCrossRefGoogle Scholar
  31. 31.
    Kwon Y, Kim SH, Ronderos DS, Lee Y, Akitake B, Woodward OM, Guggino WB, Smith DP, Montell C (2010) Drosophila TRPA1 channel Is required to avoid the naturally occurring insect repellent citronellal. Curr Biol 20:1672–1678PubMedCrossRefGoogle Scholar
  32. 32.
    Kwon Y, Shim HS, Wang X, Montell C (2008) Control of thermotactic behavior via coupling of a TRP channel to a phospholipase C signaling cascade. Nat Neurosci 11:871–873PubMedCrossRefGoogle Scholar
  33. 33.
    Landouré G, Zdebik AA, Martinez TL, Burnett BG, Stanescu HC, Inada H, Shi Y, Taye AA, Kong L, Munns CH, Choo SS, Phelps CB, Paudel R, Houlden H, Ludlow CL, Caterina MJ, Gaudet R, Kleta R, Fischbeck KH, Sumner CJ (2010) Mutations in TRPV4 cause Charcot–Marie–Tooth disease type 2C. Nat Genet 42:170–174PubMedCrossRefGoogle Scholar
  34. 34.
    Leung HT, Geng C, Pak WL (2000) Phenotypes of trpl mutants and interactions between the transient receptor potential (TRP) and TRP-like channels in Drosophila. J Neurosci 20:6797–6803PubMedGoogle Scholar
  35. 35.
    Li HS, Xu XZ, Montell C (1999) Activation of a TRPC3-dependent cation current channel through the neurotrophin BDNF. Neuron 24:261–273PubMedCrossRefGoogle Scholar
  36. 36.
    Li Y, Jia YC, Cui K, Li N, Zheng ZY, Wang YZ, Yuan XB (2005) Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor. Nature 434:894–898PubMedCrossRefGoogle Scholar
  37. 37.
    Li Z, Sergouniotis PI, Michaelides M, Mackay DS, Wright GA, Devery S, Moore AT, Holder GE, Robson AG, Webster AR (2009) Recessive mutations of the gene TRPM1 abrogate ON bipolar cell function and cause complete congenital stationary night blindness in humans. Am J Hum Genet 85:711–719PubMedCrossRefGoogle Scholar
  38. 38.
    Liu CH, Wang T, Postma M, Obukhov AG, Montell C, Hardie RC (2007) In vivo identification and manipulation of the Ca2+ selectivity filter in the Drosophila transient receptor potential channel. J Neurosci 27:604–615PubMedCrossRefGoogle Scholar
  39. 39.
    Liu J, Ward A, Gao J, Dong Y, Nishio N, Inada H, Kang L, Yu Y, Ma D, Xu T, Mori I, Xie Z, Xu XZ (2010) C. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog. Nat Neurosci 13:715–722PubMedCrossRefGoogle Scholar
  40. 40.
    Lockwich TP, Liu X, Singh BB, Jadlowiec J, Weiland S, Ambudkar IS (2000) Assembly of Trp1 in a signaling complex associated with caveolin-scaffolding lipid raft domains. J Biol Chem 275:11934–11942PubMedCrossRefGoogle Scholar
  41. 41.
    Loughney K, Kreber R, Ganetzky B (1989) Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell 58:1143–1154PubMedCrossRefGoogle Scholar
  42. 42.
    Minke B (2010) The history of the Drosophila TRP channel: the birth of a new channel superfamily. J Neurogenet 24:216–233PubMedCrossRefGoogle Scholar
  43. 43.
    Minke B, Selinger Z (1991) Inositol lipid pathway in fly photoreceptors, excitation, calcium mobilization and retinal degeneration. In: Osborne NN, Chader GJ (eds) Progress in retinal research, vol 11. Pergamon, Oxford, pp 99–124Google Scholar
  44. 44.
    Minke B, Wu C, Pak WL (1975) Induction of photoreceptor voltage noise in the dark in Drosophila mutant. Nature 258:84–87PubMedCrossRefGoogle Scholar
  45. 45.
    Mochizuki T, Wu G, Hayashi T, Xenophontos SL, Veldhuisen B, Saris JJ, Reynolds DM, Cai Y, Gabow PA, Pierides A, Kimberling WJ, Breuning MH, Deltas CC, Peters DJ, Somlo S (1996) PKD2, a gene for polycystic kidney disease that encodes an integral membrane protein. Science 272:1339–1342PubMedCrossRefGoogle Scholar
  46. 46.
    Montell C (2001) Physiology, phylogeny and functions of the TRP superfamily of cation channels. Sci STKE 2001(90):re1. Available at http://stke.sciencemag.org/cgi/content/full/OC_sigtrans;2001/90/re1
  47. 47.
    Montell C, Jones K, Hafen E, Rubin G (1985) Rescue of the Drosophila phototransduction mutation trp by germline transformation. Science 230:1040–1043PubMedCrossRefGoogle Scholar
  48. 48.
    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
  49. 49.
    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 411:590–595PubMedCrossRefGoogle Scholar
  50. 50.
    Niemeyer BA, Suzuki E, Scott K, Jalink K, Zuker CS (1996) The Drosophila light-activated conductance is composed of the two channels TRP and TRPL. Cell 85:651–659PubMedCrossRefGoogle Scholar
  51. 51.
    Nilius B (2007) TRP channels in disease. Biochim Biophys Acta 1772:805–812PubMedGoogle Scholar
  52. 52.
    Nilius B, Owsianik G (2010) Transient receptor potential channelopathies. Pflugers Arch 460:437–450PubMedCrossRefGoogle Scholar
  53. 53.
    Nilius B, Owsianik G, Voets T (2008) Transient receptor potential channels meet phosphoinositides. EMBO J 27:2809–2816PubMedCrossRefGoogle Scholar
  54. 54.
    Papazian DM, Schwarz TL, Tempel BL, Jan YN, Jan LY (1987) Cloning of genomic and complementary DNA from Shaker, a putative potassium channel gene from Drosophila. Science 237:749–753PubMedCrossRefGoogle Scholar
  55. 55.
    Pérez CA, Huang L, Rong M, Kozak JA, Preuss AK, Zhang H, Max M, Margolskee RF (2002) A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci 5:1169–1176PubMedCrossRefGoogle Scholar
  56. 56.
    Perraud AL, Fleig A, Dunn CA, Bagley LA, Launay P, Schmitz C, Stokes AJ, Zhu Q, Bessman MJ, Penner R, Kinet JP, Scharenberg AM (2001) ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature 411:595–599PubMedCrossRefGoogle Scholar
  57. 57.
    Peterson CCH, Berridge MJ, Borgese MF, Bennett DL (1995) Putative capacitative calcium entry channels: expression of Drosophila trp and evidence for the existence of vertebrate homologues. Biochem J 311:41–44Google Scholar
  58. 58.
    Phillips AM, Bull A, Kelly LE (1992) Identification of a Drosophila gene encoding a calmodulin-binding protein with homology to the trp phototransduction gene. Neuron 8:631–642PubMedCrossRefGoogle Scholar
  59. 59.
    Ramaswami M, Tanouye MA (1989) Two sodium-channel genes in Drosophila: implications for channel diversity. Proc Natl Acad Sci USA 86:2079–2082PubMedCrossRefGoogle Scholar
  60. 60.
    Ramsey IS, Delling M, Clapham DE (2006) An introduction to TRP channels. Annu Rev Physiol 68:619–647PubMedCrossRefGoogle Scholar
  61. 61.
    Ranganathan R, Harris GL, Stevens CF, Zuker CS (1991) A Drosophila mutant defective in extracellular calcium-dependent photoreceptor deactivation and desensitization. Nature 354:230–232PubMedCrossRefGoogle Scholar
  62. 62.
    Reiser J, Polu KR, Moller CC, Kenlan P, Altintas MM, Wei C, Faul C, Herbert S, Villegas I, Avila-Casado C, McGee M, Sugimoto H, Brown D, Kalluri R, Mundel P, Smith PL, Clapham DE, Pollak MR (2005) TRPC6 is a glomerular slit diaphragm-associated channel required for normal renal function. Nat Genet 37:739–744PubMedCrossRefGoogle Scholar
  63. 63.
    Reuss H, Mojet MH, Chyb S, Hardie RC (1997) In vivo analysis of the Drosophila light-sensitive channels, TRP and TRPL. Neuron 19:1249–1259PubMedCrossRefGoogle Scholar
  64. 64.
    Rock MJ, Prenen J, Funari VA, Funari TL, Merriman B, Nelson SF, Lachman RS, Wilcox WR, Reyno S, Quadrelli R, Vaglio A, Owsianik G, Janssens A, Voets T, Ikegawa S, Nagai T, Rimoin DL, Nilius B, Cohn DH (2008) Gain-of-function mutations in TRPV4 cause autosomal dominant brachyolmia. Nat Genet 40:999–1003PubMedCrossRefGoogle Scholar
  65. 65.
    Runnels LW, Yue L, Clapham DE (2001) TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science 291:1043–1047PubMedCrossRefGoogle Scholar
  66. 66.
    Salkoff L (1983) Genetic and voltage-clamp analysis of a Drosophila potassium channel. Cold Spring Harb Symp Quant Biol 48(Pt 1):221–231PubMedGoogle Scholar
  67. 67.
    Salkoff L, Wyman R (1981) Genetic modification of potassium channels in Drosophila Shaker mutants. Nature 293:228–230PubMedCrossRefGoogle Scholar
  68. 68.
    Sano Y, Inamura K, Miyake A, Mochizuki S, Yokoi H, Matsushime H, Furuichi K (2001) Immunocyte Ca2+ influx system mediated by LTRPC2. Science 293:1327–1330PubMedCrossRefGoogle Scholar
  69. 69.
    Schlingmann KP, Weber S, Peters M, Niemann Nejsum L, Vitzthum H, Klingel K, Kratz M, Haddad E, Ristoff E, Dinour D, Syrrou M, Nielsen S, Sassen M, Waldegger S, Seyberth HW, Konrad M (2002) Hypomagnesemia with secondary hypocalcemia is caused by mutations in TRPM6, a new member of the TRPM gene family. Nat Genet 31:166–170PubMedCrossRefGoogle Scholar
  70. 70.
    Shieh B-H, Zhu M-Y (1996) Regulation of the TRP Ca2+ channel by INAD in Drosophila photoreceptors. Neuron 16:991–998PubMedCrossRefGoogle Scholar
  71. 71.
    Sun M, Goldin E, Stahl S, Falardeau JL, Kennedy JC, Acierno JS Jr, Bove C, Kaneski CR, Nagle J, Bromley MC, Colman M, Schiffmann R, Slaugenhaupt SA (2000) Mucolipidosis type IV is caused by mutations in a gene encoding a novel transient receptor potential channel. Hum Mol Genet 9:2471–2478PubMedCrossRefGoogle Scholar
  72. 72.
    Suss-Toby E, Selinger Z, Minke B (1991) Lanthanum reduces the excitation efficiency in fly photoreceptors. J Gen Physiol 98:848–868CrossRefGoogle Scholar
  73. 73.
    Talavera K, Nilius B, Voets T (2008) Neuronal TRP channels: thermometers, pathfinders and life-savers. Trends Neurosci 31:287–295PubMedCrossRefGoogle Scholar
  74. 74.
    Tanouye MA, Ferrus A, Fujita SC (1981) Abnormal action potentials associated with the Shaker complex locus of Drosophila. Proc Natl Acad Sci USA 78:6548–6552PubMedCrossRefGoogle Scholar
  75. 75.
    Tempel BL, Papazian DM, Schwarz TL, Jan YN, Jan LY (1987) Sequence of a probable potassium channel component encoded at Shaker locus of Drosophila. Science 237:770–775PubMedCrossRefGoogle Scholar
  76. 76.
    Tracey WD, Wilson RI, Laurent G, Benzer S (2003) Painless, a Drosophila gene essential for nociception. Cell 113:261–273PubMedCrossRefGoogle Scholar
  77. 77.
    Tsunoda S, Sierralta J, Sun Y, Bodner R, Suzuki E, Becker A, Socolich M, Zuker CS (1997) A multivalent PDZ-domain protein assembles signalling complexes in a G-protein-coupled cascade. Nature 388:243–249PubMedCrossRefGoogle Scholar
  78. 78.
    van Genderen MM, Bijveld MM, Claassen YB, Florijn RJ, Pearring JN, Meire FM, McCall MA, Riemslag FC, Gregg RG, Bergen AA, Kamermans M (2009) Mutations in TRPM1 are a common cause of complete congenital stationary night blindness. Am J Hum Genet 85:730–736PubMedCrossRefGoogle Scholar
  79. 79.
    Venkatachalam K, Long A, Elsaesser R, Nikolaeva D, Broadie K, Montell C (2008) Motor deficit in a Drosophila model of mucolipidosis type IV due to defective clearance of apoptotic cells. Cell 135:838–851PubMedCrossRefGoogle Scholar
  80. 80.
    Venkatachalam K, Montell C (2007) TRP channels. Annu Rev Biochem 76:387–417PubMedCrossRefGoogle Scholar
  81. 81.
    Venugopal B, Browning MF, Curcio-Morelli C, Varro A, Michaud N, Nanthakumar N, Walkley SU, Pickel J, Slaugenhaupt SA (2007) Neurologic, gastric, and opthalmologic pathologies in a murine model of mucolipidosis type IV. Am J Hum Genet 81:1070–1083PubMedCrossRefGoogle Scholar
  82. 82.
    Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, Nilius B (2004) The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430:748–754PubMedCrossRefGoogle Scholar
  83. 83.
    Walder RY, Landau D, Meyer P, Shalev H, Tsolia M, Borochowitz Z, Boettger MB, Beck GE, Englehardt RK, Carmi R, Sheffield VC (2002) Mutation of TRPM6 causes familial hypomagnesemia with secondary hypocalcemia. Nat Genet 31:171–174PubMedCrossRefGoogle Scholar
  84. 84.
    Walker RG, Willingham AT, Zuker CS (2000) A Drosophila mechanosensory transduction channel. Science 287:2229–2234PubMedCrossRefGoogle Scholar
  85. 85.
    Wang GX, Poo MM (2005) Requirement of TRPC channels in netrin-1-induced chemotropic turning of nerve growth cones. Nature 434:898–904PubMedCrossRefGoogle Scholar
  86. 86.
    Warmke J, Drysdale R, Ganetzky B (1991) A distinct potassium channel polypeptide encoded by the Drosophila eag locus. Science 252:1560–1562PubMedCrossRefGoogle Scholar
  87. 87.
    Watnick TJ, Jin Y, Matunis E, Kernan MJ, Montell C (2003) A flagellar polycystin-2 homolog required for male fertility in Drosophila. Curr Biol 13:2179–2184PubMedCrossRefGoogle Scholar
  88. 88.
    Wes PD, Chevesich J, Jeromin A, Rosenberg C, Stetten G, Montell C (1995) TRPC1, a human homolog of a Drosophila store-operated channel. Proc Natl Acad Sci USA 92:9652–9656PubMedCrossRefGoogle Scholar
  89. 89.
    Winn MP, Conlon PJ, Lynn KL, Farrington MK, Creazzo T, Hawkins AF, Daskalakis N, Kwan SY, Ebersviller S, Burchette JL, Pericak-Vance MA, Howell DN, Vance JM, Rosenberg PB (2005) A mutation in the TRPC6 cation channel causes familial focal segmental glomerulosclerosis. Science 308:1801–1804PubMedCrossRefGoogle Scholar
  90. 90.
    Wu CF, Haugland FN (1985) Voltage clamp analysis of membrane currents in larval muscle fibers of Drosophila: alteration of potassium currents in Shaker mutants. J Neurosci 5:2626–2640PubMedGoogle Scholar
  91. 91.
    Xiang Y, Yuan Q, Vogt N, Looger LL, Jan LY, Jan YN (2010) Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 468:921–926PubMedCrossRefGoogle Scholar
  92. 92.
    Xu XZ, Choudhury A, Li X, Montell C (1998) Coordination of an array of signaling proteins through homo- and heteromeric interactions between PDZ domains and target proteins. J Cell Biol 142:545–555PubMedCrossRefGoogle Scholar
  93. 93.
    Yuan JP, Kiselyov K, Shin DM, Chen J, Shcheynikov N, Kang SH, Dehoff MH, Schwarz MK, Seeburg PH, Muallem S, Worley PF (2003) Homer binds TRPC family channels and is required for gating of TRPC1 by IP3 receptors. Cell 114:777–789PubMedCrossRefGoogle Scholar
  94. 94.
    Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D, Zuker CS, Ryba NJ (2003) Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112:293–301PubMedCrossRefGoogle Scholar
  95. 95.
    Zhu X, Chu PB, Peyton M, Birnbaumer L (1995) Molecular cloning of a widely expressed human homologue for the Drosophila trp gene. FEBS Lett 373:193–198PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Departments of Biological Chemistry and Neuroscience, Center for Sensory BiologyThe Johns Hopkins University School of MedicineBaltimoreUSA

Personalised recommendations