Intracellular calcium strongly potentiates agonist-activated TRPC5 channels

Journal of General Physiology

Volumn 133, Issue 5, 2009, Pages 525-546

  Blair, Nathaniel T ^a   Kaczmarek, J Stefan ^a   Clapham, David E ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

TRANSIENT RECEPTOR POTENTIAL CHANNEL 5;

ARTICLE; CALCIUM CELL LEVEL; CELL DENSITY; CONTROLLED STUDY; EMBRYO; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PERMEABILITY; PROTEIN EXPRESSION;

ANIMALS; CALCIUM; CALMODULIN; CARBACHOL; CELL LINE; CELL MEMBRANE PERMEABILITY; CHOLINERGIC AGONISTS; HUMANS; ION CHANNEL GATING; KINETICS; MEMBRANE POTENTIALS; MICE; MICROSCOPY, FLUORESCENCE; PATCH-CLAMP TECHNIQUES; RECEPTOR, MUSCARINIC M1; SIGNAL TRANSDUCTION; TRANSFECTION; TRPC CATION CHANNELS;

EID: 66049141826     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.200810153     Document Type: Article

References (75)

1. Bezzerides, V.J., I.S. Ramsey, S. Kotecha, A. Greka, and D.E. Clapham. 2004. Rapid vesicular translocation and insertion of TRP channels. Nat. Cell Biol. 6:709-720. (Pubitemid 39144476)
2. Biddlecome, G.H., G. Berstein, and E.M. Ross. 1996. Regulation of phospholipase C-beta1 by Gq and m1 muscarinic cholinergic receptor. Steady-state balance of receptor-mediated activation and GTPase-activating protein-promoted deactivation. J. Biol. Chem. 271:7999-8007. (Pubitemid 26108619)
3. 2+ signalling. Nat. Rev. Neurosci. 8:182-193.
4. Chung, M.K., A.D. Guler, and M.J. Caterina. 2005. Biphasic currents evoked by chemical or thermal activation of the heat-gated ion channel, TRPV3. J. Biol. Chem. 280:15928-15941. (Pubitemid 40616716)
5. Chung, M.K., A.D. Guler, and M.J. Caterina. 2008. TRPV1 shows dynamic ionic selectivity during agonist stimulation. Nat. Neurosci. 11:555-564.
6. Colquhoun, D., and A.G. Hawkes. 1995. The principles of the stochastic interpretation of ion-channel mechanisms. In Single- Channel Recording. B. Sakmann and E. Neher, editors. Plenum Press, New York and London. 397-482.
7. + channels. J. Gen. Physiol. 109:647-673.
8. Dattilo, M., N.J. Penington, and K. Williams. 2008. Inhibition of TRPC5 channels by intracellular ATP. Mol. Pharmacol. 73:42-49. (Pubitemid 350294195)
9. Doerner, J.F., G. Gisselmann, H. Hatt, and C.H. Wetzel. 2007. Transient receptor potential channel A1 is directly gated by calcium ions. J. Biol. Chem. 282:13180-13189. (Pubitemid 47100541)
10. Drin, G., and S. Scarlata. 2007. Stimulation of phospholipase Cbeta by membrane interactions, interdomain movement, and G protein binding-how many ways can you activate an enzyme? Cell. Signal. 19:1383-1392. (Pubitemid 46818926)
11. Fowler, M.A., K. Sidiropoulou, E.D. Ozkan, C.W. Phillips, and D.C. Cooper. 2007. Corticolimbic expression of TRPC4 and TRPC5 channels in the rodent brain. PLoS One. 2:e573.
12. Gomez, T.M., and J.Q. Zheng. 2006. The molecular basis for calcium- dependent axon pathfinding. Nat. Rev. Neurosci. 7:115-125. (Pubitemid 43151598)
13. Greka, A., B. Navarro, E. Oancea, A. Duggan, and D.E. Clapham. 2003. TRPC5 is a regulator of hippocampal neurite length and growth cone morphology. Nat. Neurosci. 6:837-845. (Pubitemid 36929705)
14. Hardie, R.C. 2005. Inhibition of phospholipase C activity in Drosophila photoreceptors by 1,2-bis(2-aminophenoxy)ethane N,N,N′,N′- tetraacetic acid (BAPTA) and di-bromo BAPTA. Cell Calcium. 38:547-556. (Pubitemid 41614434)
15. 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.
16. 2+ signaling in dendrites of pyramidal neurons. Biophys. J. 70:1069-1081.
17. 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. (Pubitemid 34568713)
18. 2+ requirement, and regulation of M current. J. Gen. Physiol. 126:243-262.
19. Hui, H., D. McHugh, M. Hannan, F. Zeng, S.Z. Xu, S.U. Khan, R. Levenson, D.J. Beech, and J.L. Weiss. 2006. Calcium-sensing mechanism in TRPC5 channels contributing to retardation of neurite outgrowth. J. Physiol. 572:165-172.
20. Inoue, R., and G. Isenberg. 1990a. Acetylcholine activates nonselective cation channels in guinea pig ileum through a G protein. Am. J. Physiol. 258:C1173-C1178. (Pubitemid 20210369)
21. Inoue, R., and G. Isenberg. 1990b. Effect of membrane potential on acetylcholine-induced inward current in guinea-pig ileum. J. Physiol. 424:57-71. (Pubitemid 20175132)
22. Inoue, R., and G. Isenberg. 1990c. Intracellular calcium ions modulate acetylcholine-induced inward current in guinea-pig ileum. J. Physiol. 424:73-92. (Pubitemid 20175147)
23. Inoue, R., H. Morita, H. Yanagida, and Y. Ito. 1998. Potentiating actions of lanthanum on ACh-induced cation current in guinea-pig ileal smooth muscle cells. J. Smooth Muscle Res. 34:69-81. (Pubitemid 29016849)
24. Jung, S., A. Muhle, M. Schaefer, R. Strotmann, G. Schultz, and T.D. Plant. 2003. Lanthanides potentiate TRPC5 currents by an action at extracellular sites close to the pore mouth. J. Biol. Chem. 278:3562-3571. (Pubitemid 36801079)
25. Kim, M.T., B.J. Kim, J.H. Lee, S.C. Kwon, D.S. Yeon, D.K. Yang, I. So, and K.W. Kim. 2006. Involvement of calmodulin and myosin light chain kinase in activation of mTRPC5 expressed in HEK cells. Am. J. Physiol. Cell Physiol. 290:C1031-C1040.
26. Kim, S.J., Y.S. Kim, J.P. Yuan, R.S. Petralia, P.F. Worley, and D.J. Linden. 2003. Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature. 426:285-291. (Pubitemid 37463146)
27. 2+-binding protein 1 in Xenopus oocytes. Pflugers Arch. 450:345-354.
28. 2+ transients mediated by L-type calcium channels. J. Neurophysiol. 100:2265-2281.
29. 2+)-sensor calmodulin. J. Biol. Chem. 279:28855-28861.
30. Lee, C.R., and J.M. Tepper. 2007. A calcium-activated nonselective cation conductance underlies the plateau potential in rat substantia nigra GABAergic neurons. J. Neurosci. 27:6531-6541. (Pubitemid 46920381)
31. Lee, K.P., J.Y. Jun, I.Y. Chang, S.H. Suh, I. So, and K.W. Kim. 2005. TRPC4 is an essential component of the nonselective cation channel activated by muscarinic stimulation in mouse visceral smooth muscle cells. Mol. Cells. 20:435-441.
32. Lee, Y.M., B.J. Kim, H.J. Kim, D.K. Yang, M.H. Zhu, K.P. Lee, I. So, and K.W. Kim. 2003. TRPC5 as a candidate for the nonselective cation channel activated by muscarinic stimulation in murine stomach. Am. J. Physiol. Gastrointest. Liver Physiol. 284:G604-G616. (Pubitemid 36343210)
33. 2+-dependent regulation of a muscarinic cation current in entorhinal cortex layer II neurons. J. Neurophysiol. 92:1644-1657.
34. McCullar, J.S., S.A. Larsen, R.A. Millimaki, and T.M. Filtz. 2003. Calmodulin is a phospholipase C-beta interacting protein. J. Biol. Chem. 278:33708-33713. (Pubitemid 37553203)
35. Meis, S., T. Munsch, L. Sosulina, and H.C. Pape. 2007. Postsynaptic mechanisms underlying responsiveness of amygdaloid neurons to cholecystokinin are mediated by a transient receptor potential-like current. Mol. Cell. Neurosci. 35:356-367. (Pubitemid 46843571)
36. 2+ channel isoforms in mouse brain. Neuroreport. 9:507-515.
37. Mundell, S.J., G. Pula, R.A. McIlhinney, P.J. Roberts, and E. Kelly. 2004. Desensitization and internalization of metabotropic glutamate receptor 1a following activation of heterologous Gq/11-coupled receptors. Biochemistry. 43:7541-7551. (Pubitemid 38745770)
38. Naraghi, M. 1997. T-jump study of calcium binding kinetics of calcium chelators. Cell Calcium. 22:255-268. (Pubitemid 27490818)
39. 2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron. 20:389-399.
40. Neher, E. 2005. Some quantitative aspects of calcium fluorimetry. In Imaging in Neuroscience and Development. R. Yuste and A. Konnerth, editors. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 245-252.
41. 2+ sensitivity of the nonselective cation channel TRPM4. J. Biol. Chem. 280:6423-6433.
42. Obukhov, A.G., and M.C. Nowycky. 2004. TRPC5 activation kinetics are modulated by the scaffolding protein ezrin/radixin/moesin-binding phosphoprotein-50 (EBP50). J. Cell. Physiol. 201:227-235. (Pubitemid 39305100)
43. 2+ block and regulates inward current amplitude of a transient receptor potential channel. J. Neurosci. 25:1234-1239.
44. Obukhov, A.G., and M.C. Nowycky. 2008. TRPC5 channels undergo changes in gating properties during the activation-deactivation cycle. J. Cell. Physiol. 216:162-171.
45. 2+ channel from mouse brain. J. Biol. Chem. 273:10279-10287.
46. Ordaz, B., J. Tang, R. Xiao, A. Salgado, A. Sampieri, M.X. Zhu, and L. Vaca. 2005. Calmodulin and calcium interplay in the modulation of TRPC5 channel activity. Identification of a novel C-terminal domain for calcium/calmodulin- mediated facilitation. J. Biol. Chem. 280:30788-30796. (Pubitemid 41291809)
47. Otsuguro, K., J. Tang, Y. Tang, R. Xiao, M. Freichel, V. Tsvilovskyy, S. Ito, V. Flockerzi, M.X. Zhu, and A.V. Zholos. 2008. Isoform-specific inhibition of TRPC4 channel by phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem. 283:10026-10036.
48. 2+ transients in dendritic spines of hippocampal pyramidal neurons in brain slice. Neuron. 14:1223-1231.
49. Philipp, S., J. Hambrecht, L. Braslavski, G. Schroth, M. Freichel, M. Murakami, A. Cavalie, and V. Flockerzi. 1998. A novel capacitative calcium entry channel expressed in excitable cells. EMBO J. 17:4274-4282. (Pubitemid 28362618)
50. Plant, T.D., and M. Schaefer. 2005. Receptor-operated cation channels formed by TRPC4 and TRPC5. Naunyn Schmiedebergs Arch. Pharmacol. 371:266-276. (Pubitemid 40905081)
51. Ramsey, I.S., M. Delling, and D.E. Clapham. 2006. An introduction to TRP channels. Annu. Rev. Physiol. 68:619-647.
52. 2+/calmodulin modulates TRPV1 activation by capsaicin. J. Gen. Physiol. 123:53-62.
53. 2+) ions in dendritic spines. Neuron. 33:439-452.
54. Schaefer, M., T.D. Plant, A.G. Obukhov, T. Hofmann, T. Gudermann, and G. Schultz. 2000. Receptor-mediated regulation of the nonselective cation channels TRPC4 and TRPC5. J. Biol. Chem. 275:17517-17526. (Pubitemid 30430793)
55. Schaefer, M., T.D. Plant, N. Stresow, N. Albrecht, and G. Schultz. 2002. Functional differences between TRPC4 splice variants. J. Biol. Chem. 277:3752-3759.
56. Scott, K., Y. Sun, K. Beckingham, and C.S. Zuker. 1997. Calmodulin regulation of Drosophila light-activated channels and receptor function mediates termination of the light response in vivo. Cell. 91:375-383. (Pubitemid 27467968)
57. Shi, J., E. Mori, Y. Mori, M. Mori, J. Li, Y. Ito, and R. Inoue. 2004. Multiple regulation by calcium of murine homologues of transient receptor potential proteins TRPC6 and TRPC7 expressed in HEK293 cell. J. Physiol. 561:415-432. (Pubitemid 39646532)
58. 2+-calmodulin- dependent myosin light chain kinase is essential for activation of TRPC5 channels expressed in HEK293 cells. J. Physiol. 570:219-235.
59. 2+- dependent potentiation of the nonselective cation channel TRPV4 is mediated by a C-terminal calmodulin binding site. J. Biol. Chem. 278:26541-26549.
60. Strubing, C., G. Krapivinsky, L. Krapivinsky, and D.E. Clapham. 2001. TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron. 29:645-655. (Pubitemid 32323938)
61. Strubing, C., G. Krapivinsky, L. Krapivinsky, and D.E. Clapham. 2003. Formation of novel TRPC channels by complex subunit interactions in embryonic brain. J. Biol. Chem. 278:39014-39019. (Pubitemid 37221803)
62. 2+ sensor calmodulin. J. Biol. Chem. 281:9076-9085.
63. Torok, K., D.J. Cowley, B.D. Brandmeier, S. Howell, A. Aitken, and D.R. Trentham. 1998. Inhibition of calmodulin-activated smooth-muscle myosin light-chain kinase by calmodulin-binding peptides and fluorescent (phosphodiesterase-activating) calmodulin derivatives. Biochemistry. 37:6188-6198. (Pubitemid 28196776)
64. Turner, J.H., and J.R. Raymond. 2005. Interaction of calmodulin with the serotonin 5-hydroxytryptamine2A receptor. A putative regulator of G protein coupling and receptor phosphorylation by protein kinase C. J. Biol. Chem. 280:30741-30750. (Pubitemid 41291803)
65. Venkatachalam, K., and C. Montell. 2007. TRP channels. Annu. Rev. Biochem. 76:387-417.
66. Voets, T., G. Droogmans, U. Wissenbach, A. Janssens, V. Flockerzi, and B. Nilius. 2004. The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature. 430:748-754. (Pubitemid 39071340)
67. Wang, Y.Y., R.B. Chang, H.N. Waters, D.D. McKemy, and E.R. Liman. 2008. The nociceptor ion channel TRPA1 is potentiated and inactivated by permeating calcium ions. J. Biol. Chem. 283:32691-32703.
68. Willars, G.B., S.R. Nahorski, and R.A. Challiss. 1998. Differential regulation of muscarinic acetylcholine receptor-sensitive polyphosphoinositide pools and consequences for signaling in human neuroblastoma cells. J. Biol. Chem. 273:5037-5046. (Pubitemid 28108661)
69. Xiao, R., J. Tang, C. Wang, C.K. Colton, J. Tian, and M.X. Zhu. 2008. Calcium plays a central role in the sensitization of TRPV3 channel to repetitive stimulations. J. Biol. Chem. 283:6162-6174.
70. Yamada, H., M. Wakamori, Y. Hara, Y. Takahashi, K. Konishi, K. Imoto, and Y. Mori. 2000. Spontaneous single-channel activity of neuronal TRP5 channel recombinantly expressed in HEK293 cells. Neurosci. Lett. 285:111-114. (Pubitemid 30227632)
71. Zholos, A.V., and T.B. Bolton. 1994. G-protein control of voltage dependence as well as gating of muscarinic metabotropic channels in guinea-pig ileum. J. Physiol. 478:195-202. (Pubitemid 24232192)
72. Zhu, M.H., M. Chae, H.J. Kim, Y.M. Lee, M.J. Kim, N.G. Jin, D.K. Yang, I. So, and K.W. Kim. 2005. Desensitization of canonical transient receptor potential channel 5 by protein kinase C. Am. J. Physiol. Cell Physiol. 289:C591-C600. (Pubitemid 41192668)
73. 2+)- binding proteins in the functional regulation of TRP channels. Pflugers Arch. 451:105-115.
74. Zimmer, S., C. Trost, U. Wissenbach, S. Philipp, M. Freichel, V. Flockerzi, and A. Cavalie. 2000. Modulation of recombinant transient- receptor-potential-like (TRPL) channels by cytosolic Ca2+. Pflugers Arch. 440:409-417. (Pubitemid 30445713)
75. 2+. Nat. Neurosci. 10:277-279.