Pflügers Archiv

, Volume 451, Issue 1, pp 19–28 | Cite as

Drosophila TRP channels

Invited Review

Abstract

The transient receptor potential (TRP) superfamily comprises a large group of related cation channels that display surprising diversity in the specific modes of activation and cation selectivities. However, a unifying theme is that many TRP channels play important roles in sensory physiology. The superfamily includes 28 mammalian members, which are subdivided into multiple subfamilies. Each of these subfamilies is represented by at least one of the 13 members in Drosophila, suggesting common evolutionary relationships. In recent years it has become clear that TRP channels in flies and mammals participate in similar sensory modalities. These include, but are not limited to, hearing, thermosensation, and certain specialized types of vision. With the recent flurry of new studies, 9 out of the 13 TRPs have been addressed in various contexts. As a result, the repertoire of biological roles attributed to Drosophila TRPs has increased considerably and is likely to lead to many additional surprises over the next few years.

Keywords

TRP channel Drosophila Calcium Sensory signaling 

References

  1. 1.
    Acharya JK, Jalink K, Hardy RW, Hartenstein V, Zuker CS (1997) InsP3 receptor essential for growth and differentiation but not for vision in Drosophila. Neuron 18:881–887CrossRefPubMedGoogle Scholar
  2. 2.
    Babes A, Zorzon D, Reid G (2004) Two populations of cold-sensitive neurons in rat dorsal root ganglia and their modulation by nerve growth factor. Eur J Neurosci 20:2276–2282PubMedGoogle Scholar
  3. 3.
    Bähner M, Frechter S, Da Silva N, Minke B, Paulsen R, Huber A (2002) Light-regulated subcellular translocation of Drosophila TRPL channels induces long-term adaptation and modifies the light-induced current. Neuron 34:83–93CrossRefPubMedGoogle Scholar
  4. 4.
    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 41:849–857CrossRefPubMedGoogle 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 26:118–123CrossRefPubMedGoogle 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 67:1110–1120Google Scholar
  7. 7.
    Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070–1073CrossRefPubMedGoogle Scholar
  8. 8.
    Bezzerides V, Ramsey S, Greka A, Clapham DE (2004) Rapid vesicular translocation and insertion of TRP channels. Nat Cell Biol 6:709–720CrossRefPubMedGoogle Scholar
  9. 9.
    Boekhoff-Falk G (2005) Hearing in Drosophila: development of Johnston’s organ and emerging parallels to vertebrate ear development. Dev Dyn 232:550–558CrossRefPubMedGoogle Scholar
  10. 10.
    Cayouette S, Lussier MP, Mathieu EL, Bousquet SM, Boulay G (2004) Exocytotic insertion of TRPC6 channel into the plasma membrane upon Gq-protein-coupled receptor activation. J Biol Chem 279:7241–7246CrossRefPubMedGoogle Scholar
  11. 11.
    Chen XZ, Vassilev PM, Basora N, Peng JB, Nomura H, Segal Y, Brown EM, Reeders ST, Hediger MA, Zhou J (1999) Polycystin-L is a calcium-regulated cation channel permeable to calcium ions. Nature 401:383–386CrossRefPubMedGoogle Scholar
  12. 12.
    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 18:95–105CrossRefPubMedGoogle Scholar
  13. 13.
    Chorna-Ornan I, Joel-Almagor T, Ben-Ami HC, Frechter S, Gillo B, Selinger Z, Gill DL, Minke B (2001) A common mechanism underlies vertebrate calcium signaling and Drosophila phototransduction. J Neurosci 21:2622–2629Google Scholar
  14. 14.
    Chyb S, Raghu P, Hardie RC (1999) Polyunsaturated fatty acids activate the Drosophila light-sensitive channels TRP and TRPL. Nature 397:255–259CrossRefPubMedGoogle Scholar
  15. 15.
    Consortium TIPKD (1995) Polycystic kidney disease: the complete structure of the PKD1 gene and its protein. Cell 81:289–298PubMedGoogle Scholar
  16. 16.
    Corey DP, Garcia-Añoveros J, Holt JR, Kwan KY, Lin SY, Vollrath MA, Amalfitano A, Cheung EL, Derfler BH, Duggan A, Gèléoc 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 432:723–730CrossRefPubMedGoogle Scholar
  17. 17.
    Cosens DJ, Manning A (1969) Abnormal electroretinogram from a Drosophila mutant. Nature 224:285–287PubMedGoogle Scholar
  18. 18.
    Cronin MA, Diao F, Tsunoda S (2004) Light-dependent subcellular translocation of Gqa in Drosophila photoreceptors is facilitated by the photoreceptor-specific myosin III NINAC. J Cell Sci 117:4797–4806CrossRefPubMedGoogle Scholar
  19. 19.
    Eberl DF, Hardy RW, Kernan MJ (2000) Genetically similar transduction mechanisms for touch and hearing in Drosophila. J Neurosci 20:5981–5988PubMedGoogle Scholar
  20. 20.
    Foster RG (2005) Neurobiology: bright blue times. Nature 433:698–699CrossRefPubMedGoogle Scholar
  21. 21.
    Gabow PA (1993) Autosomal dominant polycystic kidney disease. N Engl J Med 329:332–342CrossRefPubMedGoogle Scholar
  22. 22.
    Gao Z, Joseph E, Ruden DM, Lu X (2004) Drosophila Pkd2 is haploid-insufficient for mediating optimal smooth muscle contractility. J Biol Chem 279:14225–14231CrossRefPubMedGoogle Scholar
  23. 23.
    Gao Z, Ruden DM, Lu X (2003) PKD2 cation channel is required for directional sperm movement and male fertility. Curr Biol 13:2175–2178CrossRefPubMedGoogle Scholar
  24. 24.
    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 24:9059–9066CrossRefPubMedGoogle Scholar
  25. 25.
    Hardie RC, Minke B (1992) The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors. Neuron 8:643–651CrossRefPubMedGoogle Scholar
  26. 26.
    Hardie RC, Raghu P (1998) Activation of heterologously expressed Drosophila TRPL channels: Ca2+ is not required and InsP3 is not sufficient. Cell Calcium 24:153–163CrossRefPubMedGoogle Scholar
  27. 27.
    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–R226CrossRefPubMedGoogle Scholar
  28. 28.
    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
  29. 29.
    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 274:7325–7333CrossRefPubMedGoogle Scholar
  30. 30.
    Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Hogestätt ED, Meng ID, Julius D (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427:260–265CrossRefPubMedGoogle Scholar
  31. 31.
    Kanzaki M, Zhang YQ, Mashima H, Li L, Shibata H, Kojima I (1999) Translocation of a calcium-permeable cation channel induced by insulin-like growth factor-I. Nat Cell Biol 1:165–170CrossRefPubMedGoogle Scholar
  32. 32.
    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 424:81–84CrossRefPubMedGoogle Scholar
  33. 33.
    Kiselev A, Socolich M, Vinos J, Hardy RW, Zuker CS, Ranganathan R (2000) A molecular pathway for light-dependent photoreceptor apoptosis in Drosophila. Neuron 28:139–152CrossRefPubMedGoogle Scholar
  34. 34.
    Kosloff M, Elia N, Joel-Almagor T, Timberg R, Zars TD, Hyde DR, Minke B, Selinger Z (2003) Regulation of light-dependent Gqa translocation and morphological changes in fly photoreceptors. EMBO J 22:459–468CrossRefPubMedGoogle Scholar
  35. 35.
    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 4:191–197CrossRefPubMedGoogle Scholar
  36. 36.
    Kramer RH, Molokanova E (2001) Modulation of cyclic-nucleotide-gated channels and regulation of vertebrate phototransduction. J Exp Biol 204:2921–2931Google Scholar
  37. 37.
    Lee SJ, Montell C (2004) Light-dependent translocation of visual arrestin regulated by the NINAC myosin III. Neuron 43:95–103CrossRefPubMedGoogle Scholar
  38. 38.
    Lee SJ, Xu H, Kang LW, Amzel LM, Montell C (2003) Light adaptation through phosphoinositide-regulated translocation of Drosophila visual arrestin. Neuron 39:121–132CrossRefPubMedGoogle Scholar
  39. 39.
    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 20:6797–6803Google Scholar
  40. 40.
    Li HS, Montell C (2000) TRP and the PDZ protein, INAD, form the core complex required for retention of the signalplex in Drosophila photoreceptor cells. J Cell Biol 150:1411–1422CrossRefPubMedGoogle Scholar
  41. 41.
    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 103:525–535CrossRefPubMedGoogle Scholar
  42. 42.
    Lo M-VC, Pak WL (1981) Light-induced pigment granule migration in the retinular cells of Drosophila melanogaster. J Gen Physiol 77:155–175CrossRefPubMedGoogle Scholar
  43. 43.
    McClung C, Hirsh J (1999) The trace amine tyramine is essential for sensitization to cocaine in Drosophila. Curr Biol 9:853–860CrossRefPubMedGoogle Scholar
  44. 44.
    McGrath J, Somlo S, Makova S, Tian X, Brueckner M (2003) Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114:61–73CrossRefPubMedGoogle Scholar
  45. 45.
    Mehta D, Ahmmed GU, Paria BC, Holinstat M, Voyno-Yasenetskaya T, Tiruppathi C, Minshall RD, Malik AB (2003) RhoA interaction with inositol 1,4,5-trisphosphate receptor and transient receptor potential channel-1 regulates Ca2+ entry. Role in signaling increased endothelial permeability. J Biol Chem 278:33492–33500Google Scholar
  46. 46.
    Melyan Z, Tarttelin EE, Bellingham J, Lucas RJ, Hankins MW (2005) Addition of human melanopsin renders mammalian cells photoresponsive. Nature 433:741–745CrossRefPubMedGoogle Scholar
  47. 47.
    Michaely P, Tomchick DR, Machius M, Anderson RG (2002) Crystal structure of a 12 ANK repeat stack from human ankyrinR. EMBO J 21:6387–6396CrossRefPubMedGoogle Scholar
  48. 48.
    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 272:1339–1342PubMedGoogle Scholar
  49. 49.
    Montell C (1999) Drosophila visual transduction. Ann Rev Cell Dev Biol 15:231–268CrossRefGoogle Scholar
  50. 50.
    Montell C (2005) The TRP superfamily of cation channels. Sci STKE 2005:re3PubMedGoogle Scholar
  51. 51.
    Montell C, Birnbaumer L, Flockerzi V, Bindels RJ, Bruford EA, Caterina MJ, Clapham DE, Harteneck C, Heller S, Julius D, Mori Y, Penner R, Prawitt D, Scharenberg AM, Schultz G, Shimizu N, Zhu MX (2002) A unified nomenclature for the superfamily of TRP cation channels. Mol Cell 9:229–231PubMedGoogle Scholar
  52. 52.
    Montell C, Jones K, Hafen E, Rubin G (1985) Rescue of the Drosophila phototransduction mutation trp by germline transformation. Science 230:1040–1043PubMedGoogle Scholar
  53. 53.
    Montell C, Rubin GM (1989) Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron 2:1313–1323CrossRefPubMedGoogle Scholar
  54. 54.
    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 93:829–838CrossRefPubMedGoogle Scholar
  55. 55.
    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 33:129–137CrossRefPubMedGoogle Scholar
  56. 56.
    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 85:651–659CrossRefPubMedGoogle Scholar
  57. 57.
    O’Dell KM (1994) The inactive mutation leads to abnormal experience-dependent courtship modification in male Drosophila melanogaster. Behav Genet 24:381–388CrossRefPubMedGoogle Scholar
  58. 58.
    Panda S, Nayak SK, Campo B, Walker JR, Hogenesch JB, Jegla T (2005) Illumination of the melanopsin signaling pathway. Science 307:600–604CrossRefPubMedGoogle Scholar
  59. 59.
    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–R380CrossRefPubMedGoogle Scholar
  60. 60.
    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 8:631–642CrossRefPubMedGoogle Scholar
  61. 61.
    Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD (2000) A novel human opsin in the inner retina. J Neurosci 20:600–605Google Scholar
  62. 62.
    Qiu X, Kumbalasiri T, Carlson SM, Wong KY, Krishna V, Provencio I, Berson DM (2005) Induction of photosensitivity by heterologous expression of melanopsin. Nature 433:745–749CrossRefPubMedGoogle Scholar
  63. 63.
    Raghu P, Colley NJ, Webel R, James T, Hasan G, Danin M, Selinger Z, Hardie RC (2000) Normal phototransduction in Drosophila photoreceptors lacking an InsP3 receptor gene. Mol Cell Neurosci 15:429–445CrossRefPubMedGoogle Scholar
  64. 64.
    Raghu P, Usher K, Jonas S, Chyb S, Polyanovsky A, Hardie RC (2000) Constitutive activity of the light-sensitive channels TRP and TRPL in the Drosophila diacylglycerol kinase mutant, rdgA. Neuron 26:169–179CrossRefPubMedGoogle Scholar
  65. 65.
    Reuss H, Mojet MH, Chyb S, Hardie RC (1997) In vivo analysis of the Drosophila light-sensitive channels, TRP and TRPL. Neuron 19:1249–1259CrossRefPubMedGoogle Scholar
  66. 66.
    Rosenzweig M, Brenman KM, Taylor TD, Phelps P, Patapoutian A, Garrity PA (2005) The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. Genes Dev 19:419–424CrossRefPubMedGoogle Scholar
  67. 67.
    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 31:166–170CrossRefPubMedGoogle Scholar
  68. 68.
    Sekaran S, Foster RG, Lucas RJ, Hankins MW (2003) Calcium imaging reveals a network of intrinsically light-sensitive inner-retinal neurons. Curr Biol 13:1290–1298CrossRefPubMedGoogle Scholar
  69. 69.
    Shieh B-H, Zhu M-Y (1996) Regulation of the TRP Ca2+ channel by INAD in Drosophila photoreceptors. Neuron 16:991–998CrossRefPubMedGoogle Scholar
  70. 70.
    Sidi S, Friedrich RW, Nicolson T (2003) NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 301:96–99CrossRefPubMedGoogle Scholar
  71. 71.
    Singh BB, Lockwich TP, Bandyopadhyay BC, Liu X, Bollimuntha S, Brazer S, Combs C, Das S, Leenders AG, Sheng Z, Knepper MA, Ambudkar SV, Ambudkar IS (2004) VAMP-2-dependent exocytosis regulates plasma membrane insertion of TRPC3 channels and contributes to agonist-stimulated Ca2+ influx. Mol Cell 15:635–646CrossRefPubMedGoogle Scholar
  72. 72.
    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 112:819–829CrossRefPubMedGoogle Scholar
  73. 73.
    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 2:695–702CrossRefPubMedGoogle Scholar
  74. 74.
    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 9:2471–2478CrossRefPubMedGoogle Scholar
  75. 75.
    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 35:307–318CrossRefPubMedGoogle Scholar
  76. 76.
    Tracey WD, Wilson RI, Laurent G, Benzer S (2003) painless, a Drosophila gene essential for nociception. Cell 113:261–273CrossRefPubMedGoogle 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 388:243–249CrossRefPubMedGoogle Scholar
  78. 78.
    Tsunoda S, Sun Y, Suzuki E, Zuker C (2001) Independent anchoring and assembly mechanisms of INAD signaling complexes in Drosophila photoreceptors. J Neurosci 21:150–158Google Scholar
  79. 79.
    Vaca L, Sinkins WG, Hu Y, Kunze DL, Schilling WP (1994) Activation of recombinant trp by thapsigargin in Sf9 insect cells. Am J Physiol 266:C1501–C1505Google Scholar
  80. 80.
    van de Graaf SF, Hoenderop JG, Gkika D, Lamers D, Prenen J, Rescher U, Gerke V, Staub O, Nilius B, Bindels RJ (2003) Functional expression of the epithelial Ca2+ channels (TRPV5 and TRPV6) requires association of the S100A10-annexin 2 complex. EMBO J 22:1478–1487CrossRefPubMedGoogle Scholar
  81. 81.
    Vassilev PM, Guo L, Chen XZ, Segal Y, Peng JB, Basora N, Babakhanlou H, Cruger G, Kanazirska M, Ye C, Brown EM, Hediger MA, Zhou J (2001) Polycystin-2 is a novel cation channel implicated in defective intracellular Ca2+ homeostasis in polycystic kidney disease. Biochem Biophys Res Commun 282:341–350CrossRefPubMedGoogle Scholar
  82. 82.
    Venglarik CJ, Gao Z, Lu X (2004) Evolutionary conservation of Drosophila polycystin-2 as a calcium-activated cation channel. J Am Soc Nephrol 15:1168–1177CrossRefPubMedGoogle Scholar
  83. 83.
    Viswanath V, Story GM, Peier AM, Petrus MJ, Lee VM, Hwang SW, Patapoutian A, Jegla T (2003) Opposite thermosensor in fruitfly and mouse. Nature 423:822–823CrossRefPubMedGoogle Scholar
  84. 84.
    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 31:171–174CrossRefPubMedGoogle Scholar
  85. 85.
    Walker RG, Willingham AT, Zuker CS (2000) A Drosophila mechanosensory transduction channel. Science 287:2229–2234CrossRefPubMedGoogle Scholar
  86. 86.
    Watnick T, Germino GG (1999) Molecular basis of autosomal dominant polycystic kidney disease. Semin Nephrol 19:327–343PubMedGoogle 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 13:2179–2184CrossRefPubMedGoogle Scholar
  88. 88.
    Wes PD, Xu X-ZS, Li H-S, Chien F, Doberstein SK, Montell C (1999) Termination of phototransduction requires binding of the NINAC myosin III and the PDZ protein INAD. Nat Neurosci 2:447–453Google Scholar
  89. 89.
    Wissenbach U, Bödding M, Freichel M, Flockerzi V (2000) Trp12, a novel Trp related protein from kidney. FEBS Lett 485:127–134CrossRefPubMedGoogle Scholar
  90. 90.
    Wu G, Somlo S (2000) Molecular genetics and mechanism of autosomal dominant polycystic kidney disease. Mol Genet Metab 69:1–15CrossRefPubMedGoogle Scholar
  91. 91.
    Xu X-ZS, 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 142:545–555CrossRefPubMedGoogle Scholar
  92. 92.
    Xu X-ZS, Li H-S, Guggino WB, Montell C (1997) Coassembly of TRP and TRPL produces a distinct store-operated conductance. Cell 89:1155–1164CrossRefPubMedGoogle Scholar
  93. 93.
    Xu XZ, Chien F, Butler A, Salkoff L, Montell C (2000) TRPγ, a Drosophila TRP-related subunit, forms a regulated cation channel with TRPL. Neuron 26:647–657CrossRefPubMedGoogle Scholar
  94. 94.
    Xu XZ, Moebius F, Gill DL, Montell C (2001) Regulation of melastatin, a TRP-related protein, through interaction with a cytoplasmic isoform. Proc Natl Acad Sci USA 98:10692–10697PubMedGoogle Scholar
  95. 95.
    Xu XZ, Sternberg PW (2003) A C. elegans sperm TRP protein required for sperm-egg interactions during fertilization. Cell 114:285–297CrossRefPubMedGoogle Scholar
  96. 96.
    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 13:2508–2516CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Department of Biological ChemistryThe Johns Hopkins University School of MedicineBaltimoreUSA

Personalised recommendations