Muscarinic acetylcholine receptors activate TRPC6 channels in PC12D cells via Ca2+ store-independent mechanisms

Journal of Biochemistry

Volumn 139, Issue 3, 2006, Pages 459-470

  Zhang, Lei ^a,d   Guo, Feifan ^a,e   Kim, Ju Young ^b,f   Saffen, David ^a,b,c  

^a UNIVERSITY OF TOKYO   (Japan)

^b OHIO STATE UNIVERSITY   (United States)

^c THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

^e PENNSYLVANIA STATE UNIVERSITY   (United States)

^f JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Barium; Calcium; Muscarinic acetylcholine receptor; PC12; TRPC6

Indexed keywords

BARIUM; CALCIUM; CALCIUM CHANNEL; CARBACHOL; COMPLEMENTARY RNA; DIACYLGLYCEROL; GLYCEROL 2 ACETATE 1 OLEATE; MUSCARINIC RECEPTOR; NICOTINIC RECEPTOR; PROTEIN KINASE C; THAPSIGARGIN;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL ACTIVATION; CONTROLLED STUDY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT;

ANIMALS; BARIUM; CALCIUM; CARBACHOL; CHOLINERGIC AGONISTS; ION CHANNEL GATING; PC12 CELLS; RATS; RECEPTORS, MUSCARINIC; TRPC CATION CHANNELS;

ANIMALIA;

EID: 33646368934     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/jb/mvj065     Document Type: Article

References (49)

1. Schilling, W.P., Rajan, L., and Strobl-Jager, E. (1989) Characterization of the bradykinin-stimulated calcium influx pathway of cultured vascular endothelial cells. Saturability, selectivity, and kinetics. J. Biol. Chem. 264, 12838-12848
2. 2+ of agonist-stimulated divalent cation entry from the refilling of the agonist-sensitive intracellular pool. J. Biol. Chem. 265, 678-684
3. Yamaguchi, D.T., Green, J., Kleeman, C.R., and Muallem, S. (1989) Properties of the depolarization-activated calcium and barium entry in osteoblast-like cells. J. Biol. Chem. 264, 197-204
4. Montell, C. (2003) The venerable inveterate invertebrate TRP channels. Cell Calcium 33, 409-417
5. Montell, C., Birnbaumer, L., and Flockerzi, V. (2002) The TRP channels, a remarkably functional family. Cell 108, 595-598
6. Nilius, B. (2003) From TRPs to SOCs, CCEs, and CRACs: consensus and controversies. Cell Calcium 33, 293-298
7. Clapham, D.E. (2003) TRP channels as cellular sensors. Nature 426, 517-524
8. Montell, C., Birnbaumer, L., Flockerzi, V., Bindels, R.J., Bruford, E.A., Caterina, M.J., Clapham, D.E., Harteneck, C., Heller, S., Julius, D., Kojima, I., Mori, Y., Penner, R., Prawitt, D., Scharenberg, A.M., Schultz, G., Shimizu, N., and Zhu, M.X. (2002) A unified nomenclature for the superfamily of TRP cation channels. Mol. Cell 9, 229-231
9. Zitt, C., Zobel, A., Obukhov, A.G., Harteneck, C., Kalkbrenner, F., Luckhoff, A., and Schultz, G. (1996) Cloning and functional expression of a human Ca2+-permeable cation channel activated by calcium store depletion. Neuron 16, 1189-1196
10. 2+ release from endoplasmic reticulum in B lymphocytes. J. Exp. Med. 195, 673-681
11. Vazquez, G., Lievremont, J.P., St, J.B.G., and Putney, J.W., Jr. (2001) Human Trp3 forms both inositol trisphosphate receptor-dependent and receptor-independent store-operated cation channels in DT40 avian B lymphocytes. Proc. Natl. Acad. Sci. USA 98, 11777-11782
12. Trebak, M., Bird, G.S., McKay, R.R., and Putney, J.W., Jr. (2002) Comparison of human TRPC3 channels in receptor-activated and store-operated modes. Differential sensitivity to channel blockers suggests fundamental differences in channel composition. J. Biol. Chem. 277, 21617-21623
13. Vazquez, G., Wedel, B.J., Trebak, M., St John Bird, G., and Putney, J.W., Jr. (2003) Expression level of the canonical transient receptor potential 3 (TRPC3) channel determines its mechanism of activation. J. Biol. Chem. 278, 21649-21654
14. 2+-like channels in adrenal cells. J. Biol Chem. 275, 23965-23972
15. Zeng, F., Xu, S.Z., Jackson, P.K., McHugh, D., Kumar, B., Fountain, S.J., and Beech, D.J. (2004) Human TRPC5 channel activated by a multiplicity of signals in a single cell. J. Physiol.
16. 2+ influx. J. Biol. Chem. 277, 12302-12309
17. Venkatachalam, K., Ma, H.T., Ford, D.L., and Gill, D.L. (2001) Expression of functional receptor-coupled TRPC3 channels in DT40 triple receptor InsP3 knockout cells. J. Biol. Chem. 276, 33980-33985
18. 2+ accumulation, storage, and release. J. Biol. Chem. 266, 20159-20167
19. 2+-permeable nonselective cation channels. Cell Calcium 33, 441-450
20. Boulay, G., Zhu, X., Peyton, M., Jiang, M., Hurst, R., Stefani, E., and Birnbaumer, L. (1997) Cloning and expression of a novel mammalian homolog of Drosophila transient receptor potential (Trp) involved in calcium entry secondary to activation of receptors coupled by the Gq class of G protein. J. Biol. Chem. 272, 29672-29680
21. 2+ channel isoforms. Molecular structures and functional characterization. J. Biol. Chem. 276, 13331-13339
22. 2+-permeable cation channel that is constitutively activated and enhanced by stimulation of G protein-coupled receptor. J. Biol. Chem. 274, 27359-27370
23. Hofmann, T., Obukhov, A.G., Schaefer, M., Harteneck, C., Gudermann, T., and Schultz, G. (1999) Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397, 259-263
24. Ebihara, T. and Saffen, D. (1997) Muscarinic acetylcholine receptor-mediated induction of zif268 mRNA in PC12D cells requires protein kinase C and the influx of extracellular calcium. J. Neurochem. 68, 1001-1010
25. 2+ channel triggers transmitter release in PC12 cells. FEBS Lett. 342, 209-213
26. 2+ channels in rat phaeochromocytoma cell lines. J. Physiol. 426, 95-116
27. 2+ channels in PC12 cells. J. Neurosci. 16, 7557-7565
28. Crespo, L.M., Grantham, C.J., and Carmell, M.B. (1990) Kinetics, stoichiometry and role of the Na-Ca exchange mechanism in isolated cardiac myocytes. Nature 345, 618-621
29. 2+ exchanger. J. Biol. Chem. 279, 13696-13704
30. Reeves, J.P., Chernaya, G., and Condrescu, M. (1996) Sodium-calcium exchange and calcium homeostasis in transfected Chinese hamster ovary cells. Ann. NY Acad. Sci 779, 73-85
31. Condrescu, M., Chernaya, G., Kalaria, V., and Reeves, J.P. (1997) Barium influx mediated by the cardiac sodium-calcium exchanger in transfected Chinese hamster ovary cells. J. Gen. Physiol. 109, 41-51
32. van Koppen, C.J. and Kaiser, B. (2003) Regulation of muscarinic acetylcholine receptor signaling. Pharmacol. Ther. 98, 197-220
33. Smith, R.J., Sam, L.M., Justen, J.M., Bundy, G.L., Bala, G.A., and Bleasdale, J.E. (1990) Receptor-coupled signal transduction in human polymorphonuclear neutrophils: effects of a novel inhibitor of phospholipase C-dependent processes on cell responsiveness. J. Pharmacol. Exp. Ther. 253, 688-697
34. Thompson, A.K., Mostafapour, S.P., Denlinger, L.C., Bleasdale, J.E., and Fisher, S.K. (1991) The aminosteroid U-73122 inhibits muscarinic receptor sequestration and phosphoinositide hydrolysis in SK-N-SH neuroblastoma cells. A role for Gp in receptor compartmentation. J. Biol. Chem. 266, 23856-23862
35. Grynkiewicz, G., Poenie, M., and Tsien, R.Y. (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450
36. Merritt, J.E., Armstrong, W.P., Benham, C.D., Hallam, T.J., Jacob, R., Jaxa-Chamiec, A., Leigh, B.K., McCarthy, S.A., Moores, K.E., and Rink, T.J. (1990) SK&F 96365, a novel inhibitor of receptor-mediated calcium entry. Biochem. J. 271, 515-522
37. 2+ channel in PC12 cells (an adrenal chromaffin cell line) correlates with expression of the TRP-6 (transient receptor potential) protein. Biochem. J. 358, 717-726
38. 2+ influx. Two independently regulated mechanisms of influx stimulation coexist in neurosecretory PC12 cells. J. Biol. Chem. 267, 2164-2172
39. Almers, W. and McCleskey, E.W. (1984) Non-selective conductance in calcium channels of frog muscle: calcium selectivity in a single-file pore. J. Physiol. 353, 585-608
40. Almers, W., McCleskey, E.W., and Palade, P.T. (1984) A non-selective cation conductance in frog muscle membrane blocked by micromolar external calcium ions. J. Physiol. 353, 565-583
41. Hofmann, T., Schaefer, M., Schultz, G., and Gudermann, T. (2002) Subunit composition of mammalian transient receptor potential channels in living cells. Proc. Natl. Acad. Sci. USA 99, 7461-7466
42. Goel, M., Sinkins, W.G., and Schilling, W.P. (2002) Selective association of TRPC channel subunits in rat brain synaptosomes. J. Biol. Chem. 277, 48303-48310
43. Venkatachalam, K., Zheng, F., and Gill, D.L. (2003) Regulation of TRPC channel function by diacylglycerol and protein kinase C. J. Biol. Chem. 278, 29031-29340
44. Trebak, M., Hempel, N., Wedel, B.J., Smyth, J.T., Bird, G.S., and Putney, J.W., Jr. (2005) Negative regulation of TRPC3 channels by protein kinase C-mediated phosphorylation of serine 712. Mol. Pharmacol. 67, 558-563
45. Kim, J.Y. and Saffen, D. (2005) Activation of M1 muscarinic acetylcholine receptors stimulates the formation of a multiprotein complex centered on TRPC6 channels. J. Biol. Chem. 280, 32035-32047
46. Delmas, P., Wanaverbecq, N., Abogadie, F.C., Mistry, M., and Brown, D.A. (2002) Signaling microdomains define the specificity of receptor-mediated InsP(3) pathways in neurons. Neuron 34, 209-220
47. Strubing, C., Krapivinsky, G., Krapivinsky, L., and Clapham, D.E. (2003) Formation of novel TRPC channels by complex subunit interactions in embryonic brain. J. Biol. Chem. 278, 39014-39019
48. Mizuno, N., Kitayama, S., Saishin, Y., Shimada, S., Morita, K., Mitsuhata, C., Kurihara, H., and Dohi, T. (1999) Molecular cloning and characterization of rat trp homologues from brain. Brain Res. Mol. Brain Res. 64, 41-51
49. Volpicelli, L.A. and Levey, A.I. (2004) Muscarinic acetylcholine receptor subtypes in cerebral cortex and hippocampus. Prog. Brain Res. 145, 59-66 471-482