Affinity for phosphatidylinositol 4,5-bisphosphate determines muscarinic agonist sensitivity of Kv7 K+ channels

Journal of General Physiology

Volumn 134, Issue 5, 2009, Pages 437-448

  Hernandez, Ciria C ^a,c   Falkenburger, Björn ^b   Shapiro, Mark S ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUSCARINIC M1 RECEPTOR; MUSCARINIC M1 RECEPTOR AGONIST; OXOTREMORINE M; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOLIPASE C; POTASSIUM CHANNEL KCNQ2; POTASSIUM CHANNEL KCNQ3; POTASSIUM CHANNEL KCNQ4;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HETEROLOGOUS EXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PROTEIN BINDING; STIMULATION; VOLTAGE CLAMP;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; HUMANS; KCNQ POTASSIUM CHANNELS; KCNQ2 POTASSIUM CHANNEL; KCNQ3 POTASSIUM CHANNEL; MUSCARINIC AGONISTS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; RECEPTORS, MUSCARINIC;

EID: 70350453776     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.200910313     Document Type: Article

References (52)

1. Balla, A., and T. Balla. 2006. Phosphatidylinositol 4-kinases: old enzymes with emerging functions. Trends Cell Biol. 16:351-361. doi:10.1016/j.tcb.2006.05.003
2. 2+ current and M current in rat sympathetic neurons. Proc. Natl. Acad. Sci. USA. 88:652-656. doi:10.1073/pnas.88.2.652
3. Bender, K., M.C. Wellner-Kienitz, and L. Pott. 2002. Transfection of a phosphatidyl-4-phosphate 5-kinase gene into rat atrial myocytes removes inhibition of GIRK current by endothelin and alpha-adrenergic agonists. FEBS Lett. 529:356-360. doi:10.1016/S0014-5793(02)03426-9
4. 2+ current and M current in rat sympathetic neurons. Proc. Natl. Acad. Sci. USA. 89:9544-9548. doi:10.1073/pnas.89.20.9544
5. + current in a vertebrate neurone. Nature. 283:673-676. doi:10.1038/283673a0
6. Constanti, A., and D.A. Brown. 1981. M-Currents in voltage-clamped mammalian sympathetic neurones. Neurosci. Lett. 24:289-294. doi:10.1016/0304- 3940(81)90173-7 (Pubitemid 11001683)
7. Cooper, E.C., E. Harrington, Y.N. Jan, and L.Y. Jan. 2001. M channel KCNQ2 subunits are localized to key sites for control of neuronal network oscillations and synchronization in mouse brain. J. Neurosci. 21:9529-9540.
8. 2+ stores in rat sympathetic neurons. Proc. Natl. Acad. Sci. USA. 95:7151-7156. doi:10.1073/pnas.95.12.7151
9. Delmas, P., and D.A. Brown. 2005. Pathways modulating neural KCNQ/M (Kv7) potassium channels. Nat. Rev. Neurosci. 6:850-862. doi:10.1038/nrn1785 (Pubitemid 41568727)
10. Etxeberria, A., I. Santana-Castro, M.P. Regalado, P. Aivar, and A. Villarroel. 2004. Three mechanisms underlie KCNQ2/3 heteromeric potassium M-channel potentiation. J. Neurosci. 24:9146-9152. doi:10.1523/JNEUROSCI.3194- 04.2004 (Pubitemid 39372258)
11. Ford, C.P., P.L. Stemkowski, P.E. Light, and P.A. Smith. 2003. Experiments to test the role of phosphatidylinositol 4,5-bisphosphate in neurotransmitter-induced M-channel closure in bullfrog sympathetic neurons. J. Neurosci. 23:4931-4941.
12. 2 on phospholipid membranes by basic/aromatic regions of proteins. Biophys. J. 86:2188-2207. doi:10.1016/S0006-3495(04)74278-2
13. Gamper, N., and M.S. Shapiro. 2007. Regulation of ion transport proteins by membrane phosphoinositides. Nat. Rev. Neurosci. 8:921-934. doi:10.1038/nrn2257
14. Gamper, N., J.D. Stockand, and M.S. Shapiro. 2003. Subunit-specific modulation of KCNQ potassium channels by Src tyrosine kinase. J. Neurosci. 23:84-95. (Pubitemid 36050407)
15. 2+ channels. J. Neurosci. 24:10980-10992. doi:10.1523/JNEUROSCI.3869-04.2004
16. Gamper, N., J.D. Stockand, and M.S. Shapiro. 2005. The use of Chinese hamster ovary (CHO) cells in the study of ion channels. J. Pharmacol. Toxicol. Methods. 51:177-185. doi:10.1016/j.vascn.2004.08.008 (Pubitemid 40615598)
17. Haley, J.E., F.C. Abogadie, J.M. Fernandez-Fernandez, M. Dayrell, Y. Vallis, N.J. Buckley, and D.A. Brown. 2000. Bradykinin, but not muscarinic, inhibition of M-current in rat sympathetic ganglion neurons involves phospholipase C-beta 4. J. Neurosci. 20:RC105.
18. + channels. J. Gen. Physiol. 132:361-381. doi:10.1085/jgp.200810007
19. 2 with ion channels and transporters. Sci. STKE. doi:10.1126/stke.2001.111.re19
20. 2+ requirement, and regulation of M current. J. Gen. Physiol. 126:243-262. doi:10.1085/jgp.200509309
21. + channels. J. Gen. Physiol. 133:347-359. doi:10.1085/jgp.200810075
22. Jentsch, T.J. 2000. Neuronal KCNQ potassium channels: physiology and role in disease. Nat. Rev. Neurosci. 1:21-30. doi:10.1038/35036198
23. + channel mutated in a form of dominant deafness, is expressed in the inner ear and the central auditory pathway. Proc. Natl. Acad. Sci. USA. 97:4333-4338. doi:10.1073/pnas.97.8.4333
24. Koizumi, S., P. Rosa, G.B. Willars, R.A. Challiss, E. Taverna, M. Francolini, M.D. Bootman, P. Lipp, K. Inoue, J. Roder, and A. Jeromin. 2002. Mechanisms underlying the neuronal calcium sensor-1-evoked enhancement of exocytosis in PC12 cells. J. Biol. Chem. 277:30315-30324. doi:10.1074/jbc. M201132200
25. Kubisch, C., B.C. Schroeder, T. Friedrich, B. Lütjohann, A. El- Amraoui, S. Marlin, C. Petit, and T.J. Jentsch. 1999. KCNQ4, a novel potassium channel expressed in sensory outer hair cells, is mutated in dominant deafness. Cell. 96:437-446. doi:10.1016/S0092-8674(00)80556-5 (Pubitemid 29077597)
26. + channels reveals the mechanism of augmentation by a cysteine-modifying reagent. J. Neurosci. 24:5079-5090. doi:10.1523/JNEUROSCI. 0882-04.2004
27. + channel open probability by phosphatidylinositol 4,5-bisphosphate. J. Neurosci. 25:9825-9835. doi:10.1523/JNEUROSCI.2597-05.2005
28. Loew, L.M. 2007. Where does all the PIP2 come from? J. Physiol. 582:945-951. doi:10.1113/jphysiol.2007.132860
29. + channel-mediated cardiac channelopathies. Methods Mol. Biol. 337:167-183.
30. Mackie, A.R., and K.L. Byron. 2008. Cardiovascular KCNQ (Kv7) potassium channels: physiological regulators and new targets for therapeutic intervention. Mol. Pharmacol. 74:1171-1179. doi:10.1124/mol.108.049825
31. McLaughlin, S., G. Hangyás-Mihályné, I. Zaitseva, and U. Golebiewska. 2005. Reversible - through calmodulin - electrostatic interactions between basic residues on proteins and acidic lipids in the plasma membrane. Biochem. Soc. Symp. 72:189-198. (Pubitemid 46126852)
32. Milosevic, I., J.B. Sørensen, T. Lang, M. Krauss, G. Nagy, V. Haucke, R. Jahn, and E. Neher. 2005. Plasmalemmal phosphatidylinositol-4,5- bisphosphate level regulates the releasable vesicle pool size in chromaffin cells. J. Neurosci. 25:2557-2565. doi:10.1523/JNEUROSCI.3761-04.2005
33. Pan, Z., T. Kao, Z. Horvath, J. Lemos, J.Y. Sul, S.D. Cranstoun, V. Bennett, S.S. Scherer, and E.C. Cooper. 2006. A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J. Neurosci. 26:2599-2613. doi:10.1523/JNEUROSCI.4314-05.2006 (Pubitemid 43357843)
34. Peroz, D., N. Rodriguez, F. Choveau, I. Baró, J. Mérot, and G. Loussouarn. 2008. Kv7.1 (KCNQ1) properties and channelopathies. J. Physiol. 586:1785-1789. doi:10.1113/jphysiol.2007.148254
35. Rae, J., K. Cooper, P. Gates, and M. Watsky. 1991. Low access resistance perforated patch recordings using amphotericin B. J. Neurosci. Methods. 37:15-26. doi:10.1016/0165-0270(91)90017-T
36. Rajebhosale, M., S. Greenwood, J. Vidugiriene, A. Jeromin, and S. Hilfiker. 2003. Phosphatidylinositol 4-OH kinase is a downstream target of neuronal calcium sensor-1 in enhancing exocytosis in neuroendocrine cells. J. Biol. Chem. 278:6075-6084. doi:10.1074/jbc.M204702200
37. Robbins, J., S.J. Marsh, and D.A. Brown. 2006. Probing the regulation of M (Kv7) potassium channels in intact neurons with membrane-targeted peptides. J. Neurosci. 26:7950-7961. doi:10.1523/JNEUROSCI.2138-06.2006 (Pubitemid 44315164)
38. + channels. Br. J. Pharmacol. 137:1173-1186. doi:10.1038/sj.bjp.0704989
39. + channel sensitivity to the anticonvulsant retigabine. J. Neurosci. 25:5051-5060. doi:10.1523/JNEUROSCI.0128-05.2005
40. 1 muscarinic acetylcholine receptors. J. Physiol. 522:349-355. doi:10.1111/j.1469-7793.2000.t01-2-00349.x
41. +) channels that underlie the neuronal M current. J. Neurosci. 20:1710-1721.
42. 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. doi:10.1016/S0896-6273(02)00790-0
43. Suh, B.C., L.F. Horowitz, W. Hirdes, K. Mackie, and B. Hille. 2004. Regulation of KCNQ2/KCNQ3 current by G protein cycling: the kinetics of receptor-mediated signaling by Gq. J. Gen. Physiol. 123:663-683. doi:10.1085/jgp.200409029
44. Suh, B.C., T. Inoue, T. Meyer, and B. Hille. 2006. Rapid chemically induced changes of PtdIns(4,5)P2 gate KCNQ ion channels. Science. 314:1454-1457. doi:10.1126/science.1131163
45. Wang, H.S., Z. Pan, W. Shi, B.S. Brown, R.S. Wymore, I.S. Cohen, J.E. Dixon, and D. McKinnon. 1998. KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science. 282:1890-1893. doi:10.1126/science.282.5395.1890
46. 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. doi:10.1523/JNEUROSCI.3231-04.2005
47. Xu, C., J. Watras, and L.M. Loew. 2003. Kinetic analysis of receptor-activated phosphoinositide turnover. J. Cell Biol. 161:779-791. doi:10.1083/jcb.200301070 (Pubitemid 36648761)
48. 2+ signals direct purinergic P2Y receptor regulation of neuronal ion channels. J. Neurosci. 27:8914-8926. doi:10.1523/JNEUROSCI.1739-07.2007
49. + channels governing functional activity. Biophys. J. 95:5121-5137. doi:10.1529/biophysj.108.137604
50. 2) activates KCNQ channels, and its hydrolysis underlies receptor-mediated inhibition of M currents. Neuron. 37:963-975. doi:10.1016/S0896-6273(03)00125-9
51. Zhao, X., P. Várnai, G. Tuymetova, A. Balla, Z.E. Tóth, C. Oker-Blom, J. Roder, A. Jeromin, and T. Balla. 2001. Interaction of neuronal calcium sensor-1 (NCS-1) with phosphatidylinositol 4-kinase beta stimulates lipid kinase activity and affects membrane trafficking in COS-7 cells. J. Biol. Chem. 276:40183-40189. (Pubitemid 33658222)
52. Zheng, Q., J.A. Bobich, J. Vidugiriene, S.C. McFadden, F. Thomas, J. Roder, and A. Jeromin. 2005. Neuronal calcium sensor-1 facilitates neuronal exocytosis through phosphatidylinositol 4-kinase. J. Neurochem. 92:442-451. doi:10.1111/j.1471-4159.2004.02897.x (Pubitemid 40189448)