Modulation of ion channels by protein phosphorylation and dephosphorylation

Annual Review of Physiology

Volumn 56, Issue , 1994, Pages 193-212

  Levitan, Irwin B ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

ATP modulation; channel gating; channel inactivation; phosphoprotein phosphatase; protein kinase

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMATE RECEPTOR; NICOTINIC RECEPTOR; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE;

CHANNEL GATING; DEPHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW;

EID: 0028324395     PISSN: 00664278     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.ph.56.030194.001205     Document Type: Review

References (148)

1. Abdul-Ghani M, Kravitz EA, Meiri H, Rahamimoff R. 1991. Protein phosphatase inhibitor okadaic acid enhances transmitter release at neuromuscular junctions. Proc. Natl. Acad. Sci. USA 88:1803-7
2. Adelman JP, Shen K-Z, Kavanaugh MP, Warren RA, Wu YN, el al. 1992. Calcium-activated potassium channels expressed from cloned complementary DNAs. Neuron 9:209-16
3. Anderson MP, Berger HA, Rich DP, Gregory RJ, Smith AE, Welsh MJ. 1991. Nucleoside triphosphates are required to open the CFTR chloride channel. Cell 67:775-84
4. Andersen MP, Gregory RJ, Thompson S, Souza DW, Sucharita P, et al. 1991. Demonstration that CFTR is a chloride channel by alteration of its anion selectivity. Science 253:202-5
5. Anderson MP, Rich DP, Gregory RJ, Smith AE, Welsh MJ. 1991. Generation of cAMP-activated chloride currents by expression of CFTR. Science 251:679-82
6. Anderson MP, Welsh MJ. 1992. Regulation by ATP and ADP of CFTR chloride channels that contain mutant nucleotide-binding domains. Science 257:1701-4
7. Angelotti TP, Uhler MD, Madconald RL. 1993. Enhancement of a recombinant α1β1-γ2S GABA A receptor currents by chronic elevation of cAMP-dependent protein kinase is mediated by phosphorylation of the βl subunit. J. Neurosci. In press
8. 2+ activated phosphatase in mammalian brain. Trends Neuro. Sci. 12:1-10
9. Armstrong DL, Rossier MF, Shcherbatko AD, White RE. 1991. Enzymatic gating of voltage-activated calcium channels. Ann. NY Acad. Sci. 635:26-34
10. Armstrong DL, White RE. 1992. An enzymatic mechanism for potassium channel stimulation through pertussis toxin-sensitive G proteins. Trends Neuro. Sci. 15:403-8
11. Atkinson NS, Robertson GA, Ganetzky B. 1991. A component of calcium-activated potassium channels encoded by the Drosophila slo locus. Science 253: 551-55
12. Auld VJ, Goldin AL, Krafte DS, Marshall J, Dunn JM, et al. 1988. A rat brain Na channel α subunit with novel gating properties. Neuron 1:449-61
13. Baraban JM, Snyder SH, Alger B. 1985. Protein kinase C regulates ionic conductance in hippocampal pyramidal neurons: electrophysiological effects of phorbol esters. Proc. Natl. Acad. Sci. USA 82:2538-42
14. Blumenthal EM, Kaczmarek LK. 1992. Modulation by cAMP of a slowly activating potassium channel expressed in Xenopus oocytes. J. Neurosci. 12: 290-96
15. Boyle MB, Azhderian EM, MacLusky NJ, Naftolin F, Kaczmarek LK. 1987. Xenopus oocytes injected with rat uterine RNA express very slowly activating potassium currents. Science 235:1221-24
16. Browning MD, Bureau M, Dudek EM, Olsen RW. 1990. Protein kinase C and cAMP-dependent protein kinase phosphorylate the β subunit of the purified γ-aminobutyric acid A receptor. Proc. Natl. Acad. Sci. USA 87: 1315-18
17. Brum G, Flockerzi V, Hofmann F, Osterrieder W, Trautwein W. 1983. Injection of catalytic subunit of cAMP-dependent protein kinase into isolated cardiac myocytes. Pflügers Arch. 398: 147-54
18. Busch AE, Varnum MD, North RA, Adelman JP. 1992. An amino acid mutation in a potassium channel that prevents inhibition by protein kinase C. Science 255:1705-07
19. Butler AG, Tsunoda SL, McCobb DP, Wei AD, Salkoff LB. 1993. mSlo, a complex mouse gene encoding high conductance calcium-activated potassium channels. Science 261:221-24
20. Catterall WA. 1988. Structure and function of voltage-sensitive ion channels. Science 242:50-61
21. Catterall WA. 1991. Functional subunit structure of voltage-gated calcium channels. Science 253:1499-500
22. 2+ block of NMDA-receptor channels as a mechanism of modulation. Nature 356:521-23
23. A receptor function is regulated by phosphorylation in acutely dissociated guinea-pig hippocampal neurones. J. Physiol. 420:207-21
24. Cheng SH, Rich DP, Marshall J, Gregory RJ, Welsh MJ, Smith AE. 1991. Phosphorylation of the R domain by cAMP-dependent protein kinase regulates the CFTR chloride channel. Cell 66:1027-36
25. Chung SK, Reinhart PH, Martin BL, Brautigan D, Levitan IB. 1991. Protein kinase activity closely associated with a reconstituted calcium-activated potassium channel. Science 253:560-62
26. Cohen P. 1988. Protein phosphorylation and hormone action. Proc. R. Soc. London Ser. B B234:115-44
27. Cohen P. 1992. Signal integration at the level of protein kinases, protein phosphatases and their substrates. Trends Biochem. Sci. 17:408-13
28. Collins FS. 1992. Cystic fibrosis: Molecular biology and therapeutic implications. Science 256:774-79
29. Cooper E, Couturier S, Ballivet M. 1991. Pentameric structure and subunit stoichiometry of a neuronal nicotinic acetylcholine receptor. Nature 350:235-38
30. Costa MR, Casnellie JE, Catterall WA. 1982. Selective phosphorylation of the a subunit of the sodium channel by cAMP-dependent protein kinase. J. Biol. Chem. 257:7918-21
31. K.Ca by phorbol ester-mediated activation of PKC in pleural sensory neurons of Aplysia. J. Neurophysiol. 68:1079-86
32. Curtis BM, Catterall WA. 1985. Phosphorylation of the calcium antagonist receptor of the voltage-sensitive calcium channel by cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. USA 82:2528-32
33. + conductance in internally perfused snail neurons is enhanced by protein phosphorylation. Proc. Natl. Acad. Sci. USA 79:4207-11
34. + currents in human lymphocytes by pH. J. Physiol. 413:399-413
35. Doerner D, Pitler TA, Alger B. 1988. Protein kinase C activators block specific calcium and potassium current components in isolated hippocampal neurons. J. Neurosci. 8:4069-78
36. Downing JEG, Role LW. 1987. Activators of protein kinase C enhance acetylcholine receptor desensitization in sympathetic ganglion neurons. Proc. Nail. Acad. Sci. USA 84:7739-43
37. - channels by protein kinase A corrected by insertion of CFTR. Nature 358: 581-84
38. Egan TM, Dagan D, Levitan IB. 1993. Properties and modulation of a calcium-activated potassium channel in rat olfactory bulb neurons. J. Neurophysiol. 69:1433-42
39. Emerick MC, Agnew WS. 1989. Identification of phosphorylation sites for adenosine 3',5'-cyclic phosphate dependent protein kinase on the voltage-sensitive sodium channel from Electrophorus electricus. Biochemistry 28:8367-80
40. Eusebi F, Molinaro M, Zani BM. 1985. Agents that activate protein kinase C reduce acetylcholine sensitivity in cultured myotubes. J. Cell Biol. 100: 1339-42
41. + channel activity by protein phosphorylation. Nature 315:503-6
42. Flockerzi V, Oeken HJ, Hofmann F, Pelzer D, Cavalie A, Trautwein W. 1986. Purified dihydropyridine-binding site from skeletal muscle t-tubules is a functional calcium channel. Nature 323:66-68
43. + channels. Neuron 9:229-36
44. Gabriel SE, Clarke LL, Boucher RC, Stutts MJ. 1993. CFTR and outward rectifying chloride channels are distinct proteins with a regulatory relationship. Nature 363:263-66
45. Green WN, Ross AF, Claudio T, 1991. cAMP stimulation of acetylcholine receptor expression is mediated through posttranslational mechanisms. Proc. Natl. Acad. Sci. USA 88:854-58
46. Greengard P, Jen J, Nairn AC, Stevens CF. 1991. Enhancement of the glutamate response by cAMP-dependent protein kinase in hippocampal neurons. Science 253:1135-38
47. Halvorsen SW, Berg DK. 1990. Subunit composition of nicotinic acetylcholine receptors from chick ciliary ganglia. J Neurosci. 10:1711-18
48. Hemmings HC, Nairn AC, McGuinness TL, Huganir RL, Greengard P. 1991. Role of protein phosphorylation in neuronal signal transduction. FASEB J. 3:1582-92
49. Hoger JH, Walter AE, Vance D, Yu L, Lester HA, Davidson N. 1991. Modulation of a cloned mouse brain potassium channel. Neuron 6:227-36
50. Hollmann M, O'Shea-Greenfield A, Rogers S, Heinemann S. 1989. Cloning by functional expression of a member of the glutamate receptor family. Nature 342:643-48
51. Hopfield JF, Tank DW, Greengard P, Huganir RL. 1988. Functional modulation of the nicotinic acetylcholine receptor by tyrosine phosphorylation. Nature 336:677-80
52. 2+ -dependent processes. Proc. Natl. Acad. Sci. USA 83:3733-37
53. Hoshi T, Zagotta WN, Aldrich RW. 1990. Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science 250:533-38
54. Houamed KM, Kuijper JL, Gilbert TL, Haldeman BA, O'Hara PJ, et al. 1991. Cloning, expression and gene structure of a G protein-coupled glutamate receptor from rat brain. Science 252: 1318-21
55. Huganir RL, Delcour AH, Greengard P, Hess GP. 1986. Phosphorylation of the nicotinic acetylcholine receptor regulates its rate of desensitization. Nature 321:774-76
56. Huganir RL, Greengard P. 1983. cAMP-dependent protein kinase phosphorylates the nicotinic acetylcholine receptor. Proc. Natl. Acad. Sci. USA 80:1130-34
57. Huganir RL, Miles K, Greengard P. 1984. Phosphorylation of the nicotinic acetylcholine receptor by an endogenous tyrosine-specific protein kinase. Proc. Natl. Acad. Sci. USA 81:6968-72
58. Hyde SC, Emsley P, Hartshorn MJ, Mimmack MM, Gileadi U, et al. 1990. Structural model of ATP-binding proteins associated with cystic fibrosis. multidrug resistance and bacterial transport. Nature 346:362-65
59. Ichinose M, Byrne JH. 1991. Role of protein phosphatases in the modulation of neuronal membrane currents. Brain Res. 549:146-50
60. Ichinose M, Endo S, Critz SD, Shenolikar S, Byrne JH. 1990. Microcystin-LR, a potent phosphatase inhibitor, prolongs the serotonin- and cAMP-induced currents in sensory neurons of Aplysia californica. Brain Res. 533: 137-40
61. Jahr CE, Stevens CF. 1987. Glutamate activates multiple single channel conductances in hippocampal neurons. Nature 325:522-25
62. Jan LY, Jan YN. 1989. Voltage-sensitive ion channels. Cell 56:13-25
63. Kaczmarek LK, Levitan IB. 1987. Neuromodulation: the Biochemical Control of Neuronal Excitability, pp. 3-280. New York: Oxford Univ. Press
64. Kirkness EF, Bovenkerk CF, Ueda T, Turner A. 1989. Phosphorylation of γ-aminobutyrate (GABA)/benzodiazepine receptors by cyclic AMP-dependent protein kinase. Biochem. J. 259:613-16
65. Krafte DS, Snutch TP, Leonard JP, Davidson N, Lester HA. 1988. Evidence for the involvement of more than one mRNA species in controlling the inactivation process of rat and rabbit brain Na channels expressed in Xenopus oocytes. J. Neurosci. 8:2859-68
66. +-channels in tracheal myocytes by phosphorylation. Nature 341:152-54
67. Lancaster B, Nicoll RA, Perkel DJ. 1991. Calcium activates two types of potassium channels in rat hippocampal neurons in culture. J. Neurosci. 11:23-30
68. Latorre R, Oberhauser A, Labarca P, Alvarez O. 1989. Varieties of calcium-activated potassium channels. Annu. Rev. Physiol. 51:385-99
69. + channels through a cAMP pathway in mouse lacrimal cells. Neuron 1:227-35
70. A receptor phosphorylation: multiple sites, actions and artifacts. Trends Pharmacol. Sci. 12: 84-87
71. Levitan IB. 1985. Phosphorylation of ion channels. J. Membr. Biol. 87:177-90
72. Levitan IB. 1988. Modulation of ion channels in neurons and other cells. Annu. Rev. Neurosci. 11:119-36
73. Li M, West JW, Lai Y, Scheuer T, Catterall WA. 1992. Functional modulation of brain sodium channels by cAMP-dependent phosphorylation. Neuron 8:1151-59
74. Liman ER, Knapp AG, Dowling JE. 1989. Enhancement of kainate-gated currents in retinal horizontal cells by cyclic AMP-dependent protein kinase. Brain Res. 481:399-402
75. Lindstrom J, Schoepfer R, Whiting P. 1987. Molecular studies of the neuronal nicotinic acetylcholine receptor family. Mol. Neurobiol. 1:281-337
76. A receptor. J. Neurochem. 61:375-77
77. Madison DV, Malenka RC, Nicoll RA. 1991. Mechanisms underlying long-term potentiation of synaptic transmission. Annu. Rev. Neurosci. 14:379-97
78. Margiotta JF, Berg DK, Dionne VE. 1987. Cyclic AMP regulates the proportion of functional acetylcholine receptors on chicken ciliary ganglion neurons. Proc. Natl. Acad. Sci. USA 84:8155-59
79. Masu M, Tanabe Y, Tsuchida K, Shigemoto R, Nakanishi S. 1991. Sequence and expression of a metabotropic glutamate receptor. Nature 349:760-65
80. 2+ of NMDA responses in spinal cord neurones. Nature 309:261-63
81. McGlade-McCulloh E, Yamamoto H, Tan SE, Brickey DA, Soderling TR. 1993. Phosphorylation and regulation of glutamate receptors by calcium calmodulin-dependent protein kinase II. Nature 362:640-42
82. McMahan UJ, Wallace BG. 1989. Molecules in basal lamina that direct for mation of synaptic specializations at neuromuscular junctions. Dev. Neurosci. 11:227-47
83. Middleton P, Rubin LL, Scheutze SM. 1988. Desensitization of acetylcholine receptors in rat myotubes is enhanced by agents that elevate intracellular cAMP. J. Neurosci. 8:3405-12
84. Miller C. 1983. Integral membrane channels: studies in model membranes. Physiol. Rev. 63:1209-42
85. Miller C. 1986. Ion Channel Reconstitution, New York: Plenum
86. Miller C. 1988. Shaker shakes out potassium channels. Trends Neuro. Sci. 11:185-86
87. 2+ binding reactions. J. Gen. Physiol. 82:511-42
88. Moriyoshi K, Masu M, Ishii T, Shigemoto R, Mizuno N, Nakanishi S. 1991. Molecular cloning and characterization of the rat NMDA receptor. Nature 354:31-37
89. Moss SJ, Doherty CA, Huganir RL. 1992. Identification of the cAMP-dependent protein kinase and protein kinase C phosphorylation sites within the major intracellular domains of the β1, γ2S and γ21. subunits of the GABA A receptor. J. Biol. Chem. 267: 14470-76
90. A receptors by cAMP-dependent protein phosphorylation. Science 257:661-65
91. Mulle C, Benoit P, Pinset C, Roa M, Changeux JP. 1988. Calcitonin generelated peptide enhances the rate of desensitization of the nicotinic acetylcholine receptor in cultured mouse muscle cells. Proc. Natl. Acad. Sci. USA 85:5728-32
92. + channel reconstituted into phospholipid vesicles by protein kinase C. J. Biol. Chem. 267:16129-34
93. Nakanishi N, Shneider NA, Axel R. 1990. A family of glutamate receptor genes: Evidence for the formation of heteromultimeric receptors with distinct properties. Neuron 5:569-81
94. Nakanishi S. 1992. Molecular diversity of glutamate receptors and implications for brain function. Science 258:597-603
95. Noda M, Shimizu S, Tanabe T, et al. 1984. Primary structure of Electroph orus electricus sodium channel deduced from cDNA sequence. Nature 312:121-27
96. Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A. 1984. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307:462-65
97. Numann R, Catterall WA, Scheuer T. 1991. Functional modulation of brain sodium channels by protein kinase C phosphorylation. Science 254:115-18
98. Nunoki K, Florio V, Catterall WA. 1989. Activation of purified calcium channels by stoichiometric protein phosphorylation. Proc. Natl. Acad. Sci. USA 86:6816-20
99. Olsen RW, Towbin AJ. 1990. Molecular biology of GABAA receptors. FASEB J. 4:1469-80
100. + channel in jurkat T lymphocytes by protein kinases A and C. J. Biol. Chem. 267:18270-73
101. Pennefather P, Lancaster B, Adams PR, Nicoll RA. 1985. Two distinct Ca-dependent K currents in bullfrog sympathetic ganglion cells. Proc. Natl. Acad. Sci. USA 82:3040-44
102. Perozo E, Bezanilla F. 1990. Phosphorylation affects voltage gating of the delayed rectifier K channel by electrostatic interactions. Neuron 5: 685-90
103. Perozo E, Jong DS, Bezanilla F. 1991. Single channel studies of the phosphorylation of K channels in the squid giant axon. J. Gen. Physiol. 98:19-34
104. + channels in the squid giant axon. J. Gen. Physiol. 98:1-17
105. A receptor current in mouse spinal neurons. Neuron 5:789-96
106. Qu Z, Moritz E, Huganir RL. 1990. Regulation of tyrosine phosphorylation of the nicotinic acetylcholine receptor at the rat neuromuscular junction. Neuron 2:367-78
107. Raymond LA, Blackstone CD, Huganir RL. 1993. Phosphorylation of amino acid neurotransmitter receptors in synaptic plasticity. Trends Neurosci. 16: 147-53
108. Raymond LA, Blackstone CD, Huganir RL. 1993. Phosphorylation and modulation of recombinant GluR6 glutamate receptors by cAMP-dependent protein kinase. Nature 361:637-41
109. + channel activity that is stimulated by both cAMP-dependent and endogenous phosphorylations. Biochemistry 28:6455-60
110. Reinhart PH, Chung S, Levitan IB. 1989. A family of calcium-dependent potassium channels from rat brain. Neuron 2:1031-41
111. Reinhart PH, Chung SK, Levitan IB. 1993. Phosphoprotein phosphatase activity intimately associated with a reconstituted calcium-dependent potassium channel. Submitted
112. einhart PH, Chung SK, Martin BL, Brautigan DL, Levitan IB. 1991. Modulation of calcium-activated potassium channels from rat brain by protein kinase A and phosphatase 2A. J. Neurosci. 11:1627-35
113. +- channels with different pharmacological properties and different physiological functions. Biochem. Biophys. Res. Commun. 118:669-74
114. Ross AF, Green WN, Hartman DS, Claudio T. 1991. Efficiency of acetylcholine receptor subunit assembly and its regulation by cAMP. J. Cell Biol. 113:623-26
115. Ross AF, Rapuano M, Schmidt JH, Prives JM. 1987. Phosphorylation and assembly of nicotinic acetylcholine receptor subunits in cultured chick muscle cells. J. Biol. Chem. 262:14640-47
116. Rossie S, Catterall WA. 1987. Cyclic AMP-dependent phosphorylation of voltage-sensitive sodium channels in primary cultures of rat brain neurons. J. Biol. Chem. 262:12735-44
117. 687 J. Biol. Chem. 264:14220-24
118. Rossie S, Gordon D, Catterall WA. 1987. Identification of an intracellular domain of the sodium channel having multiple cAMP-dependent phosphorylation sites. J. Biol. Chem. 262:17530-35
119. K(A) channels by cysteine oxidation. Nature 352:711-14
120. Sadoshima J, Akaike N, Kanaide H, Nakamura M. 1988. Cyclic AMP modulates Ca-activated K channel in cultured smooth muscle cells of rat aortas. Am. J. Physiol. 255:H754-59
121. Safran A, Sagi-Eisenberg R, Neumann D, Fuchs S. 1987. Phosphorylation of the acetylcholine receptor by protein kinase C and identification of the phosphorylation site within the receptor δ subunit. J. Biol. Chem. 262:10506-10
122. Shearman MS, Sekiguchi K, Nishizuka Y. 1989. Modulation of ion channel activity: A key function of the protein kinase C enzyme family. Pharmacol. Rev. 41:211-37
123. 2+ and cyclic AMP. Brain Res. 496:113-23
124. Solaro CR, Lingle CJ. 1992. Trypsin-sensitive, rapid inactivation of a calcium-activated potassium channel. Science 257:1694-98
125. A-receptor function in hippocampal cells is maintained by phosphorylation factors. Science 241:339-41
126. Stühmer W, Conti F, Suzuki H. et al. 1989. Structural parts involved in activation and inactivation of the sodium channel. Nature 339:597-603
127. Stühmer W, Methfessel C, Sakmann B, Noda M, Numa S. 1987. Patch clamp characterisation of sodium channels expressed from rat brain cDNA. Eur. Biophys. J. 14:131-38
128. Swain JE, Robitaille R, Dass GR, Charlton MP. 1991. Phosphatases modulate transmission and serotonin facilitation at synapses: Studies with the inhibitor okadaic acid. J. Neurobiol. 22:855-64
129. A benzodiazepine receptor α subunit by a receptor-associated protein kinase. J. Neurochem. 51:1274-84
130. Swope SL, Moss SJ, Blackstone CD, Huganir RL. 1992. Phosphorylation of ligand-gated ion channels: a possible mode of synaptic plasticity. FASEB J. 6:2514-23
131. - channel in CHO cells stably expressing the cystic fibrosis gene. Nature 352:628-31
132. Takumi T, Ohkubo H, Nakanishi S. 1988. Cloning of a membrane protein that induces a slow voltage-gated potassium current. Science 242:1042-45
133. Tingley WG, Roche KW, Thompson AK, Huganir RL. 1993. Regulation of NMDA receptor phosphorylation by alternative splicing of the C-terminal domain. Nature 364:70-73
134. + channel by Shaker B inactivating "ball" peptide. Neuron 9:237-45
135. Traynelis SF, Cull-Candy SG, 1990. Proton inhibition of N-methyl-D-aspartate receptors in cerebellar neurons. Nature 345:347-30
136. Vassilev PM, Scheuer T, Catterall WA. 1988. Identification of an intracellular peptide segment involved in sodium channel inactivation. Science 241: 1658-61
137. Vijayarachavan S, Schmid HA, Halvorsen SW, Berg DK. 1990. Cyclic AMP-dependcnt phosphorylation of a neuronal acetylcholine receptor α-type subunit. J. Neurosci. 10:3255-62
138. A receptor expressed in Xenopus oocytes requires 8 amino acids contained in the γ2 subunit. Neuron 7:27-33
139. A receptors requires phosphorylation of the alternatively spliced variant of the γ2 subunit. FEBS Lett. 313:113-17
140. Wallace BG, Qu Z, Huganir RL. 1991. Agrin induces phosphorylation of the nicotinic acetylcholine receptor. Neuron 6:869-78
141. Wang LY, Salter MW, MacDonald JF. 1991. Regulation of kainate receptors by cAMP-dependent protein kinase and phosphatases. Science 253:1132-35
142. Wane LY, Taverna FA, Huang XP, MacDonald JF, Hampson DR. 1993. Phosphorylation and modulation of a kainate receptor (GluR6) by cAMP-dependent protein kinase. Science 259: 1173-75
143. Welsh MJ, Anderson MP, Rich DP, Berger HA, Denning GM, et al. 1992. Cystic fibrosis transmembrane conductance regulator: A chloride channel with novel regulation. Neuron 8:821-29
144. + channel required for modulation by protein kinase C. Science 254:866-68
145. White RE, Lee AB, Shcherbatko AD, Lincoln TM, Schonbrunn A, Armstrong DL. 1993. Potassium channel stimulation by natriuretic peptides through cGMP-dependent dephosphorylation. Nature 361:263-66
146. + channels through protein dephosphorylation. Nature 351: 570-73
147. Whiting P, McKelran RM, Iversen LL. 1990. Another mechanism for creating diversity in γ-aminobutyrate type A receptors: RNA splicing directs expression of two forms of γ2 subunit, one of which contains a protein kinase C phosphorylation site. Proc. Natl. Acad. Sci. USA 87:9966-70
148. Zagotta WN, Hoshi T, Aldrich RW. 1990. Restoration of inactivation in mutants of Shaker potassium channels by a peptide derived from ShB. Science 250:568-71