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Regulation of transient receptor potential (TRP) channels by phosphoinositides

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Abstract

This review summarizes the modulation of transient receptor potential (TRP) channels, by phosphoinositides. TRP channels are characterized by polymodal activation and a surprising complexity of regulation mechanisms. Possibly, most if not all TRP channels are modulated by phosphoinositides. Modulation by phosphatidylinositol 4,5-biphosphate (PIP2) has been shown in detail for TRP vanilloid (TRPV) 1, TRPV5, TRP melastatin (TRPM) 4, TRPM5, TRPM7, TRPM8, TRP polycystin 2, and the Drosophila TPR-like (TRPL) channels. This review describes mechanisms of modulation of TRP channels mainly by PIP2 and discusses some future challenges of this fascinating topic.

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References

  1. Aarts M, Iihara K, Wei WL, Xiong ZG, Arundine M, Cerwinski W, MacDonald JF, Tymianski M (2003) A key role for TRPM7 channels in anoxic neuronal death. Cell 115:863–877

    Article  PubMed  CAS  Google Scholar 

  2. Abe J, Hosokawa H, Sawada Y, Matsumura K, Kobayashi S (2006) Ca2+-dependent PKC activation mediates menthol-induced desensitization of transient receptor potential M8. Neurosci Lett 397:140–144

    Article  PubMed  CAS  Google Scholar 

  3. Balla T (2001) Pharmacology of phosphoinositides, regulators of multiple cellular functions. Curr Pharm Des 7:475–507

    Article  PubMed  CAS  Google Scholar 

  4. Benedikt J, Teisinger J, Vyklicky L, Vlachova V (2006) Ethanol inhibits cold-menthol receptor TRPM8 by modulating its interaction with membrane phosphatidylinositol 4,5-bisphosphate. J Neurochem 100(1):211

    Article  PubMed  CAS  Google Scholar 

  5. Bezzerides VJ, Ramsey IS, Kotecha S, Greka A, Clapham DE (2004) Rapid vesicular translocation and insertion of TRP channels. Nat Cell Biol 6:709–720

    Article  PubMed  CAS  Google Scholar 

  6. Bhave G, Hu HJ, Glauner KS, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau RW (2003) Protein kinase C phosphorylation sensitizes but does not activate the capsaicin receptor transient receptor potential vanilloid 1 (TRPV1). Proc Natl Acad Sci USA 100:12480–12485

    Article  PubMed  CAS  Google Scholar 

  7. Brady JD, Rich ED, Martens JR, Karpen JW, Varnum MD, Brown RL (2006) Interplay between PIP3 and calmodulin regulation of olfactory cyclic nucleotide-gated channels. Proc Natl Acad Sci USA 103:15635–15640

    Article  PubMed  CAS  Google Scholar 

  8. Brauchi S, Orta G, Salazar M, Rosenmann E, Latorre R (2006) A hot-sensing cold receptor: C-terminal domain determines thermosensation in transient receptor potential channels. J Neurosci 26:4835–4840

    Article  PubMed  CAS  Google Scholar 

  9. Broad LM, Braun FJ, Lievremont JP, Bird GS, Kurosaki T, Putney JW Jr (2001) Role of the phospholipase C-inositol 1,4,5-trisphosphate pathway in calcium release-activated calcium current and capacitative calcium entry. J Biol Chem 276:15945–15952

    Article  PubMed  CAS  Google Scholar 

  10. Caterina MJ, Julius D (2001) The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci 24:487–517

    Article  PubMed  CAS  Google Scholar 

  11. 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

    Article  PubMed  CAS  Google Scholar 

  12. Chen X, Talley EM, Patel N, Gomis A, McIntire WE, Dong B, Viana F, Garrison JC, Bayliss DA (2006) Inhibition of a background potassium channel by Gq protein alpha-subunits. Proc Natl Acad Sci USA 103:3422–3427

    Article  PubMed  CAS  Google Scholar 

  13. Cheng H, Beck A, Launay P, Gross SA, Stokes AJ, Kinet JP, Fleig A, Penner R (2007) TRPM4 controls insulin secretion in pancreatic beta-cells. Cell Calcium 41(1):51–61

    Article  PubMed  CAS  Google Scholar 

  14. Chuang HH, Prescott ED, Kong H, Shields S, Jordt SE, Basbaum AI, Chao MV, Julius D (2001) Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2 mediated inhibition. Nature 411:957–962

    Article  PubMed  CAS  Google Scholar 

  15. Clapham DE (2003) TRP channels as cellular sensors. Nature 426:517–524

    Article  PubMed  CAS  Google Scholar 

  16. Damak S, Rong M, Yasumatsu K, Kokrashvili Z, Perez CA, Shigemura N, Yoshida R, Mosinger B Jr, Glendinning JI, Ninomiya Y, Margolskee RF (2006) Trpm5 null mice respond to bitter, sweet, and umami compounds. Chem Senses 31:253–264

    Article  PubMed  CAS  Google Scholar 

  17. Delmas P, Coste B, Gamper N, Shapiro MS (2005) Phosphoinositide lipid second messengers: new paradigms for calcium channel modulation. Neuron 47:179–182

    Article  PubMed  CAS  Google Scholar 

  18. Dhaka A, Viswanath V, Patapoutian A (2006) Trp ion channels and temperature sensation. Annu Rev Neurosci 29:135–161

    Article  PubMed  CAS  Google Scholar 

  19. Du X, Zhang H, Lopes CM, Mirshahi T, Rohacs T, Logothetis DE (2004) Characteristic interactions with phosphatidylinositol 4,5-bisphosphate determine regulation of Kir channels by diverse modulators. J Biol Chem 279:37271–37281

    Article  PubMed  CAS  Google Scholar 

  20. 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

    Article  PubMed  CAS  Google Scholar 

  21. Estacion M, Sinkins WG, Jones SW, Applegate MA, Schilling WP (2006) Human TRPC6 expressed in HEK 293 cells forms non-selective cation channels with limited Ca2+ permeability. J Physiol 572:359–377

    Article  PubMed  CAS  Google Scholar 

  22. Estacion M, Sinkins WG, Schilling WP (2001) Regulation of Drosophila transient receptor potential-like (TrpL) channels by phospholipase C-dependent mechanisms. J Physiol 530:1–19

    Article  PubMed  CAS  Google Scholar 

  23. Fan Z, Makielski JC (1997) Anionic phospholipids activate ATP-sensitive potassium channels. J Biol Chem 272:5388–5395

    Article  PubMed  CAS  Google Scholar 

  24. Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441:179–185

    Article  PubMed  CAS  Google Scholar 

  25. Flockerzi V, Nilius B (eds) (2007) Transient receptor potential (TRP) channels. Springer, Berlin

    Google Scholar 

  26. Gwanyanya A, Sipido K, Vereecke J, Mubagwa K (2006) ATP- and PIP2-dependence of the magnesium-inhibited, TRPM7-like cation channel in cardiac myocytes. Am J Physiol Cell Physiol 291(4):C627–C635

    Article  PubMed  CAS  Google Scholar 

  27. Hardie RC (2003) Regulation of TRP channels via lipid second messengers. Annu Rev Physiol 65:735–759

    Article  PubMed  CAS  Google Scholar 

  28. Hardie RC (2007) TRP channels and lipids: from Drosophila to mammalian physiology. J Physiol 578(Pt 1):9–24

    PubMed  CAS  Google Scholar 

  29. Hardie RC, Raghu P (2001) Visual transduction in Drosophila. Nature 413:186–193

    Article  PubMed  CAS  Google Scholar 

  30. Hilgemann DW, Ball R (1996) Regulation of cardiac Na+/Ca2+ exchange and KATP potassium channels by PIP2. Science 273:956–959

    Article  PubMed  CAS  Google Scholar 

  31. Hilgemann DW, Feng S, Nasuhoglu C (2001) The complex and intriguing lives of PIP2 with ion channels and transporters. Sci STKE 2001:RE19

    Article  PubMed  CAS  Google Scholar 

  32. Hoenderop JG, Nilius B, Bindels RJ (2005) Calcium absorption across epithelia. Physiol Rev 85:373–422

    Article  PubMed  CAS  Google Scholar 

  33. Hofmann T, Chubanov V, Gudermann T, Montell C (2003) TRPM5 is a voltage-modulated and Ca2+-activated monovalent selective cation channel. Curr Biol 13:1153–1158

    Article  PubMed  CAS  Google Scholar 

  34. Huang CL, Feng S, Hilgemann DW (1998) Direct activation of inward rectifier potassium channels by PIP2 and its stabilization by Gβγ. Nature 391:803–806

    Article  PubMed  CAS  Google Scholar 

  35. Huang GN, Zeng W, Kim JY, Yuan JP, Han L, Muallem S, Worley PF (2006) STIM1 carboxyl-terminus activates native SOC, I(crac) and TRPC1 channels. Nat Cell Biol 8:1003–1010

    Article  PubMed  CAS  Google Scholar 

  36. Inoue T, Heo WD, Grimley JS, Wandless TJ, Meyer T (2005) An inducible translocation strategy to rapidly activate and inhibit small GTPase signaling pathways. Nat Methods 2:415–418

    Article  PubMed  CAS  Google Scholar 

  37. 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

    Article  PubMed  CAS  Google Scholar 

  38. Kiselyov K, Soyombo A, Muallem S (2007) TRPpathies. J Physiol 578(Pt 3):641–653

    Article  PubMed  CAS  Google Scholar 

  39. Kozak JA, Matsushita M, Nairn AC, Cahalan MD (2005) Charge screening by internal pH and polyvalent cations as a mechanism for activation, inhibition, and rundown of TRPM7/MIC channels. J Gen Physiol 126:499–514

    Article  PubMed  CAS  Google Scholar 

  40. Krapivinsky G, Mochida S, Krapivinsky L, Cibulsky SM, Clapham DE (2006) The TRPM7 ion channel functions in cholinergic synaptic vesicles and affects transmitter release. Neuron 52:485–496

    Article  PubMed  CAS  Google Scholar 

  41. Krauter T, Ruppersberg JP, Baukrowitz T (2001) Phospholipids as modulators of KATP channels: distinct mechanisms for control of sensitivity to sulphonylureas, K+ channel openers, and ATP. Mol Pharmacol 59:1086–1093

    PubMed  CAS  Google Scholar 

  42. Kwon Y, Hofmann T, Montell C (2007) Integration of phosphoinositide- and calmodulin-mediated regulation of TRPC6. Mol Cell 25:491–503

    Article  PubMed  CAS  Google Scholar 

  43. Langeslag M, Clark K, Moolenaar WH, van Leeuwen FN, Jalink K (2007) Activation of TRPM7 channels by PLC-coupled receptor agonists. J Biol Chem 282(1):232–239

    Article  PubMed  CAS  Google Scholar 

  44. Launay P, Cheng H, Srivatsan S, Penner R, Fleig A, Kinet JP (2004) TRPM4 regulates calcium oscillations after T cell activation. Science 306:1374–1377

    Article  PubMed  CAS  Google Scholar 

  45. Launay P, Fleig A, Perraud AL, Scharenberg AM, Penner R, Kinet JP (2002) TRPM4 is a Ca2+-activated nonselective cation channel mediating cell membrane depolarization. Cell 109:397–407

    Article  PubMed  CAS  Google Scholar 

  46. Lee AG (2006) Ion channels: a paddle in oil. Nature 444:697

    Article  PubMed  CAS  Google Scholar 

  47. Lee J, Cha SK, Sun TJ, Huang C-L (2005) PIP2 activates TRPV5 and releases its inhibition by intracellular Mg2+. J Gen Physiol 126:439–451

    Article  PubMed  CAS  Google Scholar 

  48. Liu B, Qin F (2005) Functional control of cold- and menthol-sensitive TRPM8 ion channels by phosphatidylinositol 4,5-bisphosphate. J Neurosci 25:1674–1681

    Article  PubMed  CAS  Google Scholar 

  49. Liu B, Zhang C, Qin F (2005) Functional recovery from desensitization of vanilloid receptor TRPV1 requires resynthesis of phosphatidylinositol 4,5-bisphosphate. J Neurosci 25:4835–4843

    Article  PubMed  CAS  Google Scholar 

  50. Liu D, Liman ER (2003) Intracellular Ca2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc Natl Acad Sci USA 100:15160–15165

    Article  PubMed  CAS  Google Scholar 

  51. Lopes CMB, Zhang H, Rohacs T, Jin T, Logothetis DE (2002) Alterations in conserved Kir channel–PIP2 interactions underlie channelopathies. Neuron 34:933–944

    Article  PubMed  CAS  Google Scholar 

  52. Lopez JJ, Salido GM, Pariente JA, Rosado JA (2006) Interaction of STIM1 with endogenously expressed human canonical TRP1 upon depletion of intracellular Ca2+ stores. J Biol Chem 281:28254–28264

    Article  PubMed  CAS  Google Scholar 

  53. Lukacs V, Thyagarajan B, Balla A, Varnai P, Balla T, Rohacs T (2007) Dual regulation of TRPV1 by phosphatidylinositol 4,5-bisphosphate, Biophysical Society Meeting Abstracts. Biophys J Suppl (abstract). Available at http://www.biophysics.org/abstracts/

  54. Ma R, Li WP, Rundle D, Kong J, Akbarali HI, Tsiokas L (2005) PKD2 functions as an epidermal growth factor-activated plasma membrane channel. Mol Cell Biol 25:8285–8298

    Article  PubMed  CAS  Google Scholar 

  55. McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52–58

    Article  PubMed  CAS  Google Scholar 

  56. McLaughlin S (2006) Cell biology. Tools to tamper with phosphoinositides. Science 314:1402–1403

    Article  PubMed  CAS  Google Scholar 

  57. McLaughlin S, Murray D (2005) Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438:605–611

    Article  PubMed  CAS  Google Scholar 

  58. Mohapatra DP, Nau C (2005) Regulation of Ca2+-dependent desensitization in the vanilloid receptor TRPV1 by calcineurin and cAMP-dependent protein kinase. J Biol Chem 280:13424–13432

    Article  PubMed  CAS  Google Scholar 

  59. Monteilh-Zoller MK, Hermosura MC, Nadler MJ, Scharenberg AM, Penner R, Fleig A (2003) TRPM7 provides an ion channel mechanism for cellular entry of trace metal ions. J Gen Physiol 121:49–60

    Article  PubMed  CAS  Google Scholar 

  60. Montell C (2005) The TRP superfamily of cation channels. Sci STKE 2005:RE3

    Article  PubMed  Google Scholar 

  61. Montell C (2006) An exciting release on TRPM7. Neuron 52:395–397

    Article  PubMed  CAS  Google Scholar 

  62. Nakanishi S, Catt KJ, Balla T (1995) A wortmannin-sensitive phosphatidylinositol 4-kinase that regulates hormone-sensitive pools of inositolphospholipids. Proc Natl Acad Sci USA 92:5317–5321

    Article  PubMed  CAS  Google Scholar 

  63. Nilius B (2003) From TRPs to SOCs, CCEs, and CRACs: consensus and controversies. Cell Calcium 33:293–298

    Article  PubMed  CAS  Google Scholar 

  64. Nilius B, Mahieu F (2006) A road map for TR(I)Ps. Mol Cell 22:297–307

    Article  PubMed  CAS  Google Scholar 

  65. Nilius B, Mahieu F, Prenen J, Janssens A, Owsianik G, Vennekens R, Voets T (2006) The Ca2+-activated cation channel TRPM4 is regulated by phosphatidylinositol 4,5-biphosphate. EMBO J 25:467–478

    Article  PubMed  CAS  Google Scholar 

  66. Nilius B, Owsianik G, Voets T, Peters JA (2007) Transient receptor potential channels in disease. Physiol Rev 87:165–217

    Article  PubMed  CAS  Google Scholar 

  67. Nilius B, Talavera K, Owsianik G, Prenen J, Droogmans G, Voets T (2005) Gating of TRP channels: a voltage connection? J Physiol 567:35–44

    Article  PubMed  CAS  Google Scholar 

  68. Nilius B, Vennekens R (2006) From cardiac cation channels to the molecular dissection of the transient receptor potential channel TRPM4. Pflugers Arch 453(3):313–321

    Article  PubMed  CAS  Google Scholar 

  69. Nilius B, Voets T (2005) TRP channels: a TR(I)P through a world of multifunctional cation channels. Pflugers Arch 451:1–10

    Article  PubMed  CAS  Google Scholar 

  70. Nilius B, Voets T, Peters J (2005) TRP channels in disease. Sci STKE 2005:RE8

    Article  PubMed  Google Scholar 

  71. Owsianik G, Talavera K, Voets T, Nilius B (2006) Permeation and selectivity of TRP channels. Annu Rev Physiol 68:685–717

    Article  PubMed  CAS  Google Scholar 

  72. Ozaki S, Dewald DB, Shope JC, Chen J, Prestwich GD (2000) Intracellular delivery of phosphoinositides and inositol phosphates using polyamine carriers. Proc Natl Acad Sci USA 97:11286–11291

    Article  PubMed  CAS  Google Scholar 

  73. Pedersen SF, Owsianik G, Nilius B (2005) TRP channels: an overview. Cell Calcium 38:233–252

    Article  PubMed  CAS  Google Scholar 

  74. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A (2002) A TRP channel that senses cold stimuli and menthol. Cell 108:705–715

    Article  PubMed  CAS  Google Scholar 

  75. Perez 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 5:1169–1176

    Article  PubMed  CAS  Google Scholar 

  76. Prawitt D, Monteilh-Zoller MK, Brixel L, Spangenberg C, Zabel B, Fleig A, Penner R (2003) TRPM5 is a transient Ca2+-activated cation channel responding to rapid changes in [Ca2+]i. Proc Natl Acad Sci USA 100:15166–15171

    Article  PubMed  CAS  Google Scholar 

  77. Premkumar LS, Raisinghani M, Pingle SC, Long C, Pimentel F (2005) Downregulation of transient receptor potential melastatin 8 by protein kinase C-mediated dephosphorylation. J Neurosci 25:11322–11329

    Article  PubMed  CAS  Google Scholar 

  78. Prescott ED, Julius D (2003) A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 300:1284–1288

    Article  PubMed  CAS  Google Scholar 

  79. Proudfoot CJ, Garry EM, Cottrell DF, Rosie R, Anderson H, Robertson DC, Fleetwood-Walker SM, Mitchell R (2006) Analgesia mediated by the TRPM8 cold receptor in chronic neuropathic pain. Curr Biol 16:1591–1605

    Article  PubMed  CAS  Google Scholar 

  80. Putney JW Jr (1990) Capacitative calcium entry revisited. Cell Calcium 11:611–624

    Article  PubMed  CAS  Google Scholar 

  81. Putney JW (2005) Physiological mechanisms of TRPC activation. Pflugers Arch 451:29–34

    Article  PubMed  CAS  Google Scholar 

  82. Rohacs T (2007) Regulation of TRP channels by PIP2. Pflugers Arch 453:753–762

    Article  PubMed  CAS  Google Scholar 

  83. Rohacs T, Chen J, Prestwich GD, Logothetis DE (1999) Distinct specificities of inwardly rectifying K+ channels for phosphoinositides. J Biol Chem 274:36065–36072

    Article  PubMed  CAS  Google Scholar 

  84. Rohacs T, Lopes C, Mirshahi T, Jin T, Zhang H, Logothetis DE (2002) Assaying phosphatidylinositol bisphosphate regulation of potassium channels. Methods Enzymol 345:71–92

    Article  PubMed  Google Scholar 

  85. Rohacs T, Lopes CM, Jin T, Ramdya PP, Molnar Z, Logothetis DE (2003) Specificity of activation by phosphoinositides determines lipid regulation of Kir channels. Proc Natl Acad Sci USA 100:745–750

    Article  PubMed  CAS  Google Scholar 

  86. Rohacs T, Lopes CMB, Michailidis I, Logothetis DE (2005) PI(4,5)P2 regulates the activation and desensitization of TRPM8 channels through the TRP domain. Nat Neurosci 8:626–634

    Article  PubMed  CAS  Google Scholar 

  87. Runnels LW, Yue L, Clapham DE (2002) The TRPM7 channel is inactivated by PIP2 hydrolysis. Nat Cell Biol 4:329–336

    PubMed  CAS  Google Scholar 

  88. Sahni J, Nelson B, Scharenberg AM (2007) SLC41A2 encodes a plasma membrane Mg2+ transporter. Biochem J 401(2):505–513

    Article  PubMed  CAS  Google Scholar 

  89. Sawynok J (2003) Topical and peripherally acting analgesics. Pharmacol Rev 55:1–20

    Article  PubMed  CAS  Google Scholar 

  90. Schmidt D, Jiang QX, MacKinnon R (2006) Phospholipids and the origin of cationic gating charges in voltage sensors. Nature 444:775–779

    Article  PubMed  CAS  Google Scholar 

  91. Schmitz C, Perraud AL, Johnson CO, Inabe K, Smith MK, Penner R, Kurosaki T, Fleig A, Scharenberg AM (2003) Regulation of vertebrate cellular Mg2+ homeostasis by TRPM7. Cell 114:191–200

    Article  PubMed  CAS  Google Scholar 

  92. Shyng SL, Barbieri A, Gumusboga A, Cukras C, Pike L, Davis JN, Stahl PD, Nichols CG (2000) Modulation of nucleotide sensitivity of ATP-sensitive potassium channels by phosphatidylinositol-4-phosphate 5-kinase. Proc Natl Acad Sci USA 97:937–941

    Article  PubMed  CAS  Google Scholar 

  93. 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

    Article  PubMed  CAS  Google Scholar 

  94. Su LT, Agapito MA, Li M, Simonson WT, Huttenlocher A, Habas R, Yue L, Runnels LW (2006) TRPM7 regulates cell adhesion by controlling the calcium-dependent protease calpain. J Biol Chem 281:11260–11270

    Article  PubMed  CAS  Google Scholar 

  95. Suh BC, Hille B (2005) Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate. Curr Opin Neurobiol 15:370–378

    Article  PubMed  CAS  Google Scholar 

  96. Suh BC, Inoue T, Meyer T, Hille B (2006) Rapid chemically induced changes of PtdIns(4,5)P2 gate KCNQ ion channels. Science 314:1454–1457

    Article  PubMed  CAS  Google Scholar 

  97. Sui JL, Petit Jacques J, Logothetis DE (1998) Activation of the atrial KACh channel by the betagamma subunits of G proteins or intracellular Na+ ions depends on the presence of phosphatidylinositol phosphates. Proc Natl Acad Sci USA 95:1307–1312

    Article  PubMed  CAS  Google Scholar 

  98. Takezawa R, Schmitz C, Demeuse P, Scharenberg AM, Penner R, Fleig A (2004) Receptor-mediated regulation of the TRPM7 channel through its endogenous protein kinase domain. Proc Natl Acad Sci USA 101:6009–6014

    Article  PubMed  CAS  Google Scholar 

  99. Talavera K, Yasumatsu K, Voets T, Droogmans G, Shigemura N, Ninomiya Y, Margolskee RF, Nilius B (2005) Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature 438:1022–1025

    Article  PubMed  CAS  Google Scholar 

  100. 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

    Article  PubMed  CAS  Google Scholar 

  101. Tominaga M, Wada M, Masu M (2001) Potentiation of capsaicin receptor activity by metabotropic ATP receptors as a possible mechanism for ATP-evoked pain and hyperalgesia. Proc Natl Acad Sci USA 98:6951–6956

    Article  PubMed  CAS  Google Scholar 

  102. Tseng PH, Lin HP, Hu H, Wang C, Zhu MX, Chen CS (2004) The canonical transient receptor potential 6 channel as a putative phosphatidylinositol 3,4,5-trisphosphate-sensitive calcium entry system. Biochemistry 43:11701–11708

    Article  PubMed  CAS  Google Scholar 

  103. Vanden Abeele F, Zholos A, Bidaux G, Shuba Y, Thebault S, Beck B, Flourakis M, Panchin Y, Skryma R, Prevarskaya N (2006) iPLA2-dependent gating of TRPM8 by lysophospholipids. J Biol Chem 281(52):40174–40182

    Article  CAS  Google Scholar 

  104. Varnai P, Thyagarajan B, Rohacs T, Balla T (2006) Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact cells. J Cell Biol 175:377–382

    Article  PubMed  CAS  Google Scholar 

  105. Vig M, Peinelt C, Beck A, Koomoa DL, Rabah D, Koblan-Huberson M, Kraft S, Turner H, Fleig A, Penner R, Kinet JP (2006) CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312:1220–1223

    Article  PubMed  CAS  Google Scholar 

  106. 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 430:748–754

    Article  PubMed  CAS  Google Scholar 

  107. Voets T, Janssens A, Prenen J, Droogmans G, Nilius B (2003) Mg2+-dependent gating and strong inward rectification of the cation channel TRPV6. J Gen Physiol 121:245–260

    Article  PubMed  CAS  Google Scholar 

  108. Voets T, Talavera K, Owsianik G, Nilius B (2005) Sensing with TRP channels. Nat Chem Biol 1:85–92

    Article  PubMed  CAS  Google Scholar 

  109. Xu H, Delling M, Jun JC, Clapham DE (2006) Oregano, thyme and clove-derived flavors and skin sensitizers activate specific TRP channels. Nat Neurosci 9:628–635

    Article  PubMed  CAS  Google Scholar 

  110. Zhang H, Craciun LC, Mirshahi T, Rohacs T, Lopes CMB, Jin T, Logothetis DE (2003) PIP2 activates KCNQ channels and its hydrolysis underlies receptor-mediated inhibition of M currents. Neuron 37:963–975

    Article  PubMed  CAS  Google Scholar 

  111. Zhang H, Xu Y, Zhang Z, Liman ER, Prestwich GD (2006) Synthesis and biological activity of phospholipase C-resistant analogues of phosphatidylinositol 4,5-bisphosphate. J Am Chem Soc 128:5642–5643

    Article  PubMed  CAS  Google Scholar 

  112. Zhang SL, Yu Y, Roos J, Kozak JA, Deerinck TJ, Ellisman MH, Stauderman KA, Cahalan MD (2005) STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437:902–905

    Article  PubMed  CAS  Google Scholar 

  113. 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 112:293–301

    Article  PubMed  CAS  Google Scholar 

  114. Zhang Z, Okawa H, Wang Y, Liman ER (2005) Phosphatidylinositol 4,5-bisphosphate rescues TRPM4 channels from desensitization. J Biol Chem 280:39185–39192

    Article  PubMed  CAS  Google Scholar 

  115. Zhu X, Jiang M, Peyton M, Boulay G, Hurst R, Stefani E, Birnbaumer L (1996) trp, a novel mammalian gene family essential for agonist-activated capacitative Ca2+ entry. Cell 85:661–671

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

We thank all members or our laboratories for always-helpful discussions. This work was supported by the Human Frontiers Science Programme (HFSP Research Grant Ref. RGP 32/2004), the Belgian Federal Government, the Flemish Government, the Onderzoeksraad KU Leuven (GOA 99/07, F.W.O. G.0214.99, F.W.O. G. 0136.00; F.W.O. G.0172.03, Interuniversity Poles of Attraction Program, Prime Ministers Office (IUAP; BN), and the American Heart Association, the Alexander and Alexandrine Sinsheimer Foundation, and the UMDNJ Foundation (TR).

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Rohacs, T., Nilius, B. Regulation of transient receptor potential (TRP) channels by phosphoinositides. Pflugers Arch - Eur J Physiol 455, 157–168 (2007). https://doi.org/10.1007/s00424-007-0275-6

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  • DOI: https://doi.org/10.1007/s00424-007-0275-6

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