PLC-mediated PI(4,5)P2 hydrolysis regulates activation and inactivation of TRPC6/7 channels

Journal of General Physiology

Volumn 143, Issue 2, 2014, Pages 183-201

  Itsuki, Kyohei ^a,b   Imai, Yuko ^a,b   Hase, Hideharu ^c   Okamura, Yasushi ^d   Inoue, Ryuji ^a   Mori, Masayuki X ^a,c  

^a FUKUOKA UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOLIPASE C; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPC6 PROTEIN, HUMAN; TRPC7 PROTEIN, HUMAN;

ANIMAL; ARTICLE; DOSE RESPONSE; DRUG EFFECT; HEK293 CELL LINE; HUMAN; HYDROLYSIS; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN BINDING;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; HEK293 CELLS; HUMANS; HYDROLYSIS; MICE; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN BINDING; TRPC CATION CHANNELS; TYPE C PHOSPHOLIPASES;

EID: 84893081630     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201311033     Document Type: Article

References (75)

1. Albert, A.P., A.S. Piper, and W.A. Large. 2005. Role of phospholipase D and diacylglycerol in activating constitutive TRPC-like cation channels in rabbit ear artery myocytes. J. Physiol. 566:769-780. http://dx.doi.org/10.1113/jphysiol.2005.090852
2. Ambudkar, I.S., B.C. Bandyopadhyay, X. Liu, T.P. Lockwich, B. Paria, and H.L. Ong. 2006. Functional organization of TRPC-Ca2+ channels and regulation of calcium microdomains. Cell Calcium. 40:495-504. http://dx.doi.org/10.1016/j.ceca.2006.08.011
3. Beech, D.J., K. Muraki, and R. Flemming. 2004. Non-selective cationic channels of smooth muscle and the mammalian homologues of Drosophila TRP. J. Physiol. 559:685-706. http://dx.doi.org/10 .1113/jphysiol.2004.068734
4. Bousquet, S.M., M. Monet, and G. Boulay. 2010. Protein kinase C-dependent phosphorylation of transient receptor potential canonical 6 (TRPC6) on serine 448 causes channel inhibition. J. Biol. Chem. 285:40534-40543. http://dx.doi.org/10.1074/jbc .M110.160051
5. Bousquet, S.M., M. Monet, and G. Boulay. 2011. The serine 814 of TRPC6 is phosphorylated under unstimulated conditions. PLoS ONE. 6:e18121. http://dx.doi.org/10.1371/journal.pone.0018121
6. Brandt, B.L., B.W. Kimes, and F.G. Klier. 1976. Development of a clonal myogenic cell line with unusual biochemical properties. J. Cell. Physiol. 88:255-275. http://dx.doi.org/10.1002/jcp.1040880302
7. Brown, S.A., F. Morgan, J. Watras, and L.M. Loew. 2008. Analysis of phosphatidylinositol-4,5-bisphosphate signaling in cerebellar Purkinje spines. Biophys. J. 95:1795-1812. http://dx.doi.org/10 .1529/biophysj.108.130195
8. Brueggemann, L.I., D.R. Markun, K.K. Henderson, L.L. Cribbs, and K.L. Byron. 2006. Pharmacological and electrophysiological characterization of store-operated currents and capacitative Ca2+ entry in vascular smooth muscle cells. J. Pharmacol. Exp. Ther. 317:488-499. http://dx.doi.org/10.1124/jpet.105.095067
9. Bunce, C.M., P.J. French, P. Allen, J.C. Mountford, B. Moor, M.F. Greaves, R.H. Michell, and G. Brown. 1993. Comparison of the levels of inositol metabolites in transformed haemopoietic cells and their normal counterparts. Biochem. J. 289:667-673.
10. Cao, C., E. Zakharian, I. Borbiro, and T. Rohacs. 2013. Interplay between calmodulin and phosphatidylinositol 4,5-bisphosphate in Ca2+-induced inactivation of transient receptor potential vanilloid 6 channels. J. Biol. Chem. 288:5278-5290. http://dx.doi.org/10 .1074/jbc.M112.409482
11. Dickson, E.J., B.H. Falkenburger, and B. Hille. 2013. Quantitative properties and receptor reserve of the IP3 and calcium branch of Gq-coupled receptor signaling. J. Gen. Physiol. 141:521-535. http:// dx.doi.org/10.1085/jgp.201210886
12. Doerner, J.F., H. Hatt, and I.S. Ramsey. 2011. Voltage-and temperaturedependent activation of TRPV3 channels is potentiated by receptormediated PI(4,5)P2 hydrolysis. J. Gen. Physiol. 137:271-288. http://dx .doi.org/10.1085/jgp.200910388
13. Erickson, M.G., B.A. Alseikhan, B.Z. Peterson, and D.T. Yue. 2001. Preassociation of calmodulin with voltage-gated Ca2+ channels revealed by FRET in single living cells. Neuron. 31:973-985. http://dx .doi.org/10.1016/S0896-6273(01)00438-X
14. Falkenburger, B.H., J.B. Jensen, and B. Hille. 2010. Kinetics of PIP2 metabolism and KCNQ2/3 channel regulation studied with a voltage-sensitive phosphatase in living cells. J. Gen. Physiol. 135:99-114. http://dx.doi.org/10.1085/jgp.200910345
15. Falkenburger, B.H., E.J. Dickson, and B. Hille. 2013. Quantitative properties and receptor reserve of the DAG and PKC branch of Gq-coupled receptor signaling. J. Gen. Physiol. 141:537-555. http:// dx.doi.org/10.1085/jgp.201210887
16. Firth, A.L., C.V. Remillard, and J.X. Yuan. 2007. TRP channels in hypertension. Biochim. Biophys. Acta. 1772:895-906. http://dx.doi.org/10 .1016/j.bbadis.2007.02.009
17. Fujita, A., J. Cheng, K Tauchi-Sato, T. Takenawa, and T. Fujimoto. 2009. A distinct pool of phosphatidylinositol 4,5-bisphosphate in caveolae revealed by a nanoscale labeling technique. Proc. Natl. Acad. Sci. USA. 106:9256-9261.
18. Gamper, N., and M.S. Shapiro. 2007. Regulation of ion transport proteins by membrane phosphoinositides. Nat. Rev. Neurosci. 8:921-934. http://dx.doi.org/10.1038/nrn2257
19. Goel, M., W.G. Sinkins, and W.P. Schilling. 2002. Selective association of TRPC channel subunits in rat brain synaptosomes. J. Biol. Chem. 277:48303-48310. http://dx.doi.org/10.1074/jbc.M207882200
20. Golebiewska, U., M. Nyako, W. Woturski, I. Zaitseva, and S. McLaughlin. 2008. Diffusion coefficient of fluorescent phosphatidylinositol 4,5-bisphosphate in the plasma membrane of cells. Mol. Biol. Cell. 19:1663-1669. http://dx.doi.org/10.1091/mbc.E07-12-1208
21. 2 are essential but independent lipid determinants of membrane identity. Science. 337:727-730. http://dx.doi.org/10.1126/science.1222483
22. Hardie, R.C. 2003. Regulation of TRP channels via lipid second messengers. Annu. Rev. Physiol. 65:735-759. http://dx.doi .org/10.1146/annurev.physiol.65.092101.142505
23. Hartmann, J., E. Dragicevic, H. Adelsberger, H.A. Henning, M. Sumser, J. Abramowitz, R. Blum, A. Dietrich, M. Freichel, V. Flockerzi, et al. 2008. TRPC3 channels are required for synaptic transmission and motor coordination. Neuron. 59:392-398. http://dx.doi.org/10.1016/j.neuron.2008.06.009
24. 2 signals: when, where, and how? Pflugers Arch. 455:55-67. http://dx.doi.org/10.1007/s00424-007-0280-9
25. Hill, A.V. 1910. The possible effects of the aggregation of the molecules of haemoglobin on its oxygen dissociation curve. J. Physiol. 40:iv-vii.
26. Hirose, K., S. Kadowaki, M. Tanabe, H. Takeshima, and M. Iino. 1999. Spatiotemporal dynamics of inositol 1,4,5-trisphosphate that underlies complex Ca2+ mobilization patterns. Science. 284:1527-1530. http://dx.doi.org/10.1126/science.284.5419.1527
27. Hofmann, T., A.G. Obukhov, M. Schaefer, C. Harteneck, T. Gudermann, and G. Schultz. 1999. Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature. 397:259-263. http://dx.doi.org/10.1038/16711
28. Hofmann, T., M. Schaefer, G. Schultz, and T. Gudermann. 2002. Subunit composition of mammalian transient receptor potential channels in living cells. Proc. Natl. Acad. Sci. USA. 99:7461-7466. http://dx.doi.org/10.1073/pnas.102596199
29. 2+ requirement, and regulation of M current. J. Gen. Physiol. 126:243-262. http://dx.doi.org/10.1085/jgp.200509309
30. Imai, Y., K. Itsuki, Y. Okamura, R. Inoue, and M.X. Mori. 2012. A self-limiting regulation of vasoconstrictor-activated TRPC3/C6/ C7 channels coupled to PI(4,5)P2-diacylglycerol signalling. J. Physiol. 590:1101-1119.
31. Inoue, R., and H. Kuriyama. 1993. Dual regulation of cation-selective channels by muscarinic and alpha 1-adrenergic receptors in the rabbit portal vein. J. Physiol. 465:427-448.
32. Inoue, R., L.J. Jensen, J. Shi, H. Morita, M. Nishida, A. Honda, and Y. Ito. 2006. Transient receptor potential channels in cardiovascular function and disease. Circ. Res. 99:119-131. http://dx.doi.org/10 .1161/01.RES.0000233356.10630.8a
33. Irvine, R.F., and M.J. Schell. 2001. Back in the water: the return of the inositol phosphates. Nat. Rev. Mol. Cell Biol. 2:327-338. http://dx.doi.org/10.1038/35073015
34. Itsuki, K., Y. Imai, Y. Okamura, K. Abe, R. Inoue, and M.X. Mori. 2012a. Voltage-sensing phosphatase reveals temporal regulation of TRPC3/ C6/C7 channels by membrane phosphoinositides. Channels (Austin). 6:206-209. http://dx.doi.org/10.4161/chan.20883
35. Itsuki, K., Y. Imai, Y. Okamura, R. Inoue, and M.X. Mori. 2012b. PIP2 dynamics underlying muscarinic or vasopressin receptoractivated TRPC3, C6, and C7 currents. Biophys. J. 104:454a.
36. Jardín, I., P.C. Redondo, G.M. Salido, and J.A. Rosado. 2008. Phosphatidylinositol 4,5-bisphosphate enhances store-operated calcium entry through hTRPC6 channel in human platelets. Biochim. Biophys. Acta. 1783:84-97. http://dx.doi.org/10.1016/ j.bbamcr.2007.07.007
37. Jensen, J.B., J.S. Lyssand, C. Hague, and B. Hille. 2009. Fluorescence changes reveal kinetic steps of muscarinic receptor-mediated modulation of phosphoinositides and Kv7.2/7.3 K+ channels. J. Gen. Physiol. 133:347-359. http://dx.doi.org/10.1085/jgp.200810075
38. Kim, Y.J., M.L. Guzman-Hernandez, and T. Balla. 2011. A highly dynamic ER-derived phosphatidylinositol-synthesizing organelle supplies phosphoinositides to cellular membranes. Dev. Cell. 21:813-824. http://dx.doi.org/10.1016/j.devcel.2011.09.005
39. Koenig, S., M. Schernthaner, H. Maechler, C.O. Kappe, T.N. Glasnov, G. Hoefler, M. Braune, E. Wittchow, and K. Groschner. 2013. A TRPC3 blocker, ethyl-1-(4-(2,3,3-trichloroacrylamide)phenyl)-5-(trifluoromethyl)-1H-pyrazole-4-carboxylate (Pyr3), prevents stentinduced arterial remodeling. J. Pharmacol. Exp. Ther. 344:33-40. http://dx.doi.org/10.1124/jpet.112.196832
40. Kosenko, A., S. Kang, I.M. Smith, D.L. Greene, L.K. Langeberg, J.D. Scott, and N. Hoshi. 2012. Coordinated signal integration at the M-type potassium channel upon muscarinic stimulation. EMBO J. 31:3147-3156. http://dx.doi.org/10.1038/emboj.2012.156
41. Kwon, Y., T. Hofmann, and C. Montell. 2007. Integration of phosphoinositide-and calmodulin-mediated regulation of TRPC6. Mol. Cell. 25:491-503. http://dx.doi.org/10.1016/j.molcel.2007.01.021
42. Lemmon, M.A., K.M. Ferguson, and J. Schlessinger. 1996. PH domains: diverse sequences with a common fold recruit signaling molecules to the cell surface. Cell. 85:621-624. http://dx.doi.org/10 .1016/S0092-8674(00)81022-3
43. Lemonnier, L., M. Trebak, and J.W. Putney Jr. 2008. Complex regulation of the TRPC3, 6 and 7 channel subfamily by diacylglycerol and phosphatidylinositol-4,5-bisphosphate. Cell Calcium. 43:506-514. http://dx.doi.org/10.1016/j.ceca.2007.09.001
44. Lo, M.V., and W.L. Pak. 1981. Light-induced pigment granule migration in the retinular cells of Drosophila melanogaster. Comparison of wild type with ERG-defective mutants. J. Gen. Physiol. 77:155-175. http://dx.doi.org/10.1085/jgp.77.2.155
45. Loew, L.M. 2007. Where does all the PIP2 come from? J. Physiol. 582:945-951. http://dx.doi.org/10.1113/jphysiol.2007.132860
46. Logothetis, D.E., T. Jin, D. Lupyan, and A. Rosenhouse-Dantsker. 2007. Phosphoinositide-mediated gating of inwardly rectifying K+ channels. Pflugers Arch. 455:83-95. http://dx.doi.org/10.1007/ s00424-007-0276-5
47. Maruyama, Y., Y. Nakanishi, E.J. Walsh, D.P. Wilson, D.G. Welsh, and W.C. Cole. 2006. Heteromultimeric TRPC6-TRPC7 channels contribute to arginine vasopressin-induced cation current of A7r5 vascular smooth muscle cells. Circ. Res. 98:1520-1527. http:// dx.doi.org/10.1161/01.RES.0000226495.34949.28
48. McLaughlin, S., and D. Murray. 2005. Plasma membrane phosphoinositide organization by protein electrostatics. Nature. 438: 605-611. http://dx.doi.org/10.1038/nature04398
49. Minke, B. 2010. The history of the Drosophila TRP channel: the birth of a new channel superfamily. J. Neurogenet. 24:216-233. http://dx.doi.org/10.3109/01677063.2010.514369
50. Monet, M., N. Francoeur, and G. Boulay. 2012. Involvement of phosphoinositide 3-kinase and PTEN protein in mechanism of activation of TRPC6 protein in vascular smooth muscle cells. J. Biol. Chem. 287:17672-17681. http://dx.doi.org/10.1074/jbc.M112 .341354
51. Mori, M.X., Y. Imai, K. Itsuki, and R. Inoue. 2011. Quantitative measurement of Ca2+-dependent calmodulin-target binding by Fura-2 and CFP and YFP FRET imaging in living cells. Biochemistry. 50:4685-4696. http://dx.doi.org/10.1021/bi200287x
52. Okada, T., R. Inoue, K. Yamazaki, A. Maeda, T. Kurosaki, T. Yamakuni, I. Tanaka, S. Shimizu, K. Ikenaka, K. Imoto, and Y. Mori. 1999. Molecular and functional characterization of a novel mouse transient receptor potential protein homologue TRP7. Ca2+-permeable cation channel that is constitutively activated and enhanced by stimulation of G protein-coupled receptor. J. Biol. Chem. 274:27359-27370. http://dx.doi.org/10.1074/jbc.274.39.27359
53. Okamura, Y., Y. Murata, and H. Iwasaki. 2009. Voltage-sensing phosphatase: actions and potentials. J. Physiol. 587:513-520. http:// dx.doi.org/10.1113/jphysiol.2008.163097
54. Panda, S., S.K. Nayak, B. Campo, J.R. Walker, J.B. Hogenesch, and T. Jegla. 2005. Illumination of the melanopsin signaling pathway. Science. 307:600-604. http://dx.doi.org/10.1126/science .1105121
55. Petersson, M.E., M. Yoshida, and E.A. Fransén. 2011. Low-frequency summation of synaptically activated transient receptor potential channel-mediated depolarizations. Eur. J. Neurosci. 34:578-593. http://dx.doi.org/10.1111/j.1460-9568.2011.07791.x
56. Prescott, E.D., and D. Julius. 2003. A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science. 300:1284-1288. http://dx.doi.org/10.1126/science.1083646
57. Ramsey, I.S., M. Delling, and D.E. Clapham. 2006. An introduction to TRP channels. Annu. Rev. Physiol. 68:619-647. http://dx.doi.org/ 10.1146/annurev.physiol.68.040204.100431
58. Sinnecker, D., and M. Schaefer. 2004. Real-time analysis of phospholipase C activity during different patterns of receptor-induced Ca2+ responses in HEK293 cells. Cell Calcium. 35:29-38. http:// dx.doi.org/10.1016/S0143-4160(03)00169-6
59. Smedlund, K., J.Y. Tano, and G. Vazquez. 2010. The constitutive function of native TRPC3 channels modulates vascular cell adhesion molecule-1 expression in coronary endothelial cells through nuclear factor kappaB signaling. Circ. Res. 106:1479-1488. http:// dx.doi.org/10.1161/CIRCRESAHA.109.213314
60. Soboloff, J., M. Spassova, T. Hewavitharana, L.P. He, P. Luncsford, W. Xu, K. Venkatachalam, D. van Rossum, R.L. Patterson, and D.L. Gill. 2007. TRPC channels: integrators of multiple cellular signals. Handbook Exp. Pharmacol. 179:575-591. http://dx.doi.org/ 10.1007/978-3-540-34891-7_34
61. Suh, B.C., and B. Hille. 2002. Recovery from muscarinic modulation of M current channels requires phosphatidylinositol 4,5-bisphosphate synthesis. Neuron. 35:507-520. http://dx.doi.org/10.1016/ S0896-6273(02)00790-0
62. Takai, Y., R. Sugawara, H. Ohinata, and A. Takai. 2004. Two types of non-selective cation channel opened by muscarinic stimulation with carbachol in bovine ciliary muscle cells. J. Physiol. 559:899-922. http://dx.doi.org/10.1113/jphysiol.2004.065607
63. Tauseef, M., N. Knezevic, K.R. Chava, M. Smith, S. Sukriti, N. Gianaris, A.G. Obukhov, S.M. Vogel, D.E. Schraufnagel, A. Dietrich, et al. 2012. TLR4 activation of TRPC6-dependent calcium signaling mediates endotoxin-induced lung vascular permeability and inflammation. J. Exp. Med. 209:1953-1968. http:// dx.doi.org/10.1084/jem.20111355
64. Tsvilovskyy, V.V., A.V. Zholos, T. Aberle, S.E. Philipp, A. Dietrich, M.X. Zhu, L. Birnbaumer, M. Freichel, and V. Flockerzi. 2009. Deletion of TRPC4 and TRPC6 in mice impairs smooth muscle contraction and intestinal motility in vivo. Gastroenterology. 137:1415-1424. http://dx.doi.org/10.1053/j.gastro.2009.06.046
65. Ufret-Vincenty, C.A., R.M. Klein, L. Hua, J. Angueyra, and S.E. Gordon. 2011. Localization of the PIP2 sensor of TRPV1 ion channels. J. Biol. Chem. 286:9688-9698. http://dx.doi.org/10.1074/jbc.M110.192526
66. van den Bogaart, G., K. Meyenberg, H.J. Risselada, H. Amin, K.I. Willig, B.E. Hubrich, M. Dier, S.W. Hell, H. Grubmüller, U. Diederichsen, and R. Jahn. 2011. Membrane protein sequestering by ionic protein-lipid interactions. Nature. 479:552-555. http://dx.doi.org/10.1038/nature10545
67. van der Wal, J., R. Habets, P. Várnai, T. Balla, and K. Jalink. 2001. Monitoring agonist-induced phospholipase C activation in live cells by fluorescence resonance energy transfer. J. Biol. Chem. 276:15337-15344. http://dx.doi.org/10.1074/jbc .M007194200
68. van Rossum, D.B., R.L. Patterson, S. Sharma, R.K. Barrow, M. Kornberg, D.L. Gill, and S.H. Snyder. 2005. Phospholipase Cgamma1 controls surface expression of TRPC3 through an intermolecular PH domain. Nature. 434:99-104. http://dx.doi.org/ 10.1038/nature03340
69. Venkatachalam, K., and C. Montell. 2007. TRP channels. Annu. Rev. Biochem. 76:387-417. http://dx.doi.org/10.1146/annurev .biochem.75.103004.142819
70. Violin, J.D., J. Zhang, R.Y. Tsien, and A.C. Newton. 2003. A genetically encoded fluorescent reporter reveals oscillatory phosphorylation by protein kinase C. J. Cell Biol. 161:899-909. http:// dx.doi.org/10.1083/jcb.200302125
71. Weissmann, N., A. Sydykov, H. Kalwa, U. Storch, B. Fuchs, M. Mederos y Schnitzler, R.P. Brandes, F. Grimminger, M. Meissner, M. Freichel, et al. 2012. Activation of TRPC6 channels is essential for lung ischaemia-reperfusion induced oedema in mice. Nat. Commun. 3:649. http://dx.doi.org/10.1038/ncomms1660
72. Winks, J.S., S. Hughes, A.K. Filippov, L. Tatulian, F.C. Abogadie, D.A. Brown, and S.J. Marsh. 2005. Relationship between membrane phosphatidylinositol-4,5-bisphosphate and receptor-mediated inhibition of native neuronal M channels. J. Neurosci. 25:3400-3413. http://dx.doi.org/10.1523/JNEUROSCI.3231-04.2005
73. Xie, J., B. Sun, J. Du, W. Yang, H.C. Chen, J.D. Overton, L.W. Runnels, and L. Yue. 2011. Phosphatidylinositol 4,5-bisphosphate (PIP2) controls magnesium gatekeeper TRPM6 activity. Sci. Rep. 1:146. http://dx.doi.org/10.1038/srep00146
74. Yudin, Y., V. Lukacs, C. Cao, and T. Rohacs. 2011. Decrease in phosphatidylinositol 4,5-bisphosphate levels mediates desensitization of the cold sensor TRPM8 channels. J. Physiol. 589:6007-6027. http://dx.doi.org/10.1113/jphysiol.2011.220228
75. Zacharias, D.A., J.D. Violin, A.C. Newton, and R.Y. Tsien. 2002. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science. 296:913-916. http://dx.doi .org/10.1126/science.1068539