Modulation of type 1 inositol (1,4,5)-trisphosphate receptor function by protein kinase A and protein phosphatase 1α

Journal of Neuroscience

Volumn 23, Issue 2, 2003, Pages 403-415

  Tang, Tie Shan ^a   Tu, Huiping ^a   Wang, Zhengnan ^a   Bezprozvanny, Ilya ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Calcium signaling; Dopamine; Inositol trisphosphate receptor; Planar lipid bilayers; Protein phosphorylation; Yeast two hybrid

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; PHOSPHOPROTEIN PHOSPHATASE 1;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; DNA LIBRARY; ENZYME ACTIVATION; ENZYME MODIFICATION; LIPID BILAYER; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SECOND MESSENGER; SYNAPTOSOME;

EID: 0037439746     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-02-00403.2003     Document Type: Article

References (66)

1. Allen PB, Hvalby O, Jensen V, Errington ML, Ramsay M, Chaudhry FA, Bliss TV, Storm-Mathisen J, Morris RG, Andersen P, Greengard P (2000) Protein phosphatase-1 regulation in the induction of long-term potentiation: heterogeneous molecular mechanisms. J Neurosci 20:3537-3543.
2. Berridge MJ (1993) Inositol trisphosphate and calcium signalling. Nature 361:315-325.
3. Berridge MJ (1998) Neuronal calcium signaling. Neuron 21:13-26.
4. Bezprozvanny I, Ehrlich BE (1993) ATP modulates the function of inositol 1,4,5-trisphosphate-gated channels at two sites. Neuron 10:1175-1184.
5. 3) receptor. J Membr Biol 145:205-216.
6. 3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 351:751-754.
7. Blank T, Nijholt I, Teichert U, Kugler H, Behrsing H, Fienberg A, Greengard P, Spiess J (1997) The phosphoprotein DARPP-32 mediates cAMP-dependent potentiation of striatal N-methyl-D-aspartate responses. Proc Natl Acad Sci USA 94:14859-14864.
8. 3R-3, expressed in pancreatic islets, gastrointestinal tract, and other tissues. J Biol Chem 268:11356-11363.
9. Bultynck G, Rossi D, Callewaert G, Missiaen L, Sorrentino V, Parys JB, De Smedt H (2001a) The conserved sites for the FK506-binding proteins in ryanodine receptors and inositol 1,4,5-trisphosphate receptors are structurally and functionally different. J Biol Chem 276:47715-47724.
10. Bultynck G, De Smet P, Rossi D, Callewaert G, Missiaen L, Sorrentino V, De Smedt H, Parys JB (2001b) Characterization and mapping of the 12 kDa FK506-binding protein (FKBP12)-binding site on different isoforms of the ryanodine receptor and of the inositol 1,4,5-trisphosphate receptor. Biochem J 354:413-422.
11. 2+ flux. Cell 83:463-472.
12. Cameron AM, Nucifora Jr FC, Fung ET, Livingston DJ, Aldape RA, Ross CA, Snyder SH (1997) FKBP12 binds the inositol 1,4,5-trisphosphate receptor at leucine-proline (1400-1401) and anchors calcineurin to this FK506-like domain. J Biol Chem 272:27582-27588.
13. Cepeda C, Colwell CS, Itri JN, Chandler SH, Levine MS (1998) Dopaminergic modulation of NMDA-induced whole cell currents in neostriatal neurons in slices: contribution of calcium conductances. J Neurophysiol 79:82-94.
14. Colquhoun D, Hawkes AG (1983) The principles of stochastic interpretation of ion-channel mechanisms. In: Single-channel recording (Sakmann B, Neher E, eds), pp 135-174. New York: Plenum.
15. da Cruz e Silva EF, Fox CA, Ouimet CC, Gustafson E, Watson SJ, Greengard P (1995) Differential expression of protein phosphatase 1 isoforms in mammalian brain. J Neurosci 15:3375-3389.
16. Danoff SK, Ferris CD, Donath C, Fischer GA, Munemitsu S, Ullrich A, Snyder SH, Ross CA (1991) Inositol 1,4,5-trisphosphate receptors: distinct neuronal and nonneuronal forms derived by alternative splicing differ in phosphorylation. Proc Natl Acad Sci USA 88:2951-2955.
17. DeSouza N, Reiken S, Ondrias K, Yang YM, Matkovich S, Marks AR (2002) Protein kinase A and two phosphatases are components of the inositol 1,4,5-trisphosphate receptor macromolecular signaling complex. J Biol Chem 277:39397-39400.
18. Fabiato A (1988) Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol 157:378-417.
19. Ferris CD, Huganir RL, Snyder SH (1990) Calcium flux mediated by purified inositol 1,4,5-trisphosphate receptor in reconstituted lipid vesicles is allosterically regulated by adenine nucleotides. Proc Natl Acad Sci USA 87:2147-2151.
20. Ferris CD, Cameron AM, Bredt DS, Huganir RL, Snyder SS (1991a) Inositol 1,4,5-trisphosphate receptor is phosphorylated by cyclic AMP-dependent protein kinase at serines 1755 and 1589. Biochem Biophys Res Commun 175:192-198.
21. Ferris CD, Huganir RL, Bredt DS, Cameron AM, Snyder SH (1991b) Inositol trisphosphate receptor-phosphorylation by protein kinase-C and calcium calmodulin-dependent protein kinases in reconstituted lipid vesicles. Proc Natl Acad Sci USA 88:2232-2235.
22. Finch EA, Turner TJ, Goldin SM (1991) Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. Science 252:443-446.
23. Furuichi T, Kohda K, Miyawaki A, Mikoshiba K (1994) Intracellular channels. Curr Opin Neurobiol 4:294-303.
24. Greengard P, Allen PB, Nairn AC (1999) Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron 23:435-447.
25. Hain J, Onoue H, Mayrleitner M, Fleischer S, Schindler H (1995) Phosphorylation modulates the function of the calcium release channel of sarcoplasmic reticulum from cardiac muscle. J Biol Chem 270:2074-2081.
26. Hata Y, Butz S, Sudhof TC (1996) CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J Neurosci 16:2488-2494.
27. Haug LS, Jensen V, Hvalby O, Walaas SI, Ostvold AC (1999) Phosphorylation of the inositol 1,4,5-trisphosphate receptor by cyclic nucleotide-dependent kinases in vitro and in rat cerebellar slices in situ. J Biol Chem 274:7467-7473.
28. 2+ currents and excitability via a novel PLC[β]1-IP3-calcineurin-signaling cascade. J Neurosci 20:8987-8995.
29. Horn R (1991) Estimating the number of channels in patch recordings. Biophys J 60:433-439.
30. 2+ dependence of inositol 1,4,5-trisphosphate-induced Ca release in smooth muscle cells of the guinea pig taenia caeci. J Gen Physiol 95:1103-1122.
31. Iino M (1991) Effects of adenine nucleotides on inositol 1,4,5- trisphosphate-induced calcium release in vascular smooth muscle cells. J Gen Physiol 98:681-698.
32. Jones DH, Matus AI (1974) Isolation of synaptic plasma membrane from brain by combined flotation-sedimentation density gradient centrifugation. Biochim Biophys Acta 356:276-287.
33. Kaznacheyeva E, Lupu VD, Bezprozvanny I (1998) Single-channel properties of inositol (1,4,5)-trisphosphate receptor heterologously expressed in HEK-293 cells. J Gen Physiol 111:847-856.
34. Lindskog M, Svenningsson P, Fredholm BB, Greengard P, Fisone G (1999) Activation of dopamine D2 receptors decreases DARPP-32 phosphorylation in striatonigral and striatopallidal projection neurons via different mechanisms. Neuroscience 88:1005-1008.
35. Lupu VD, Kaznacheyeva E, Krishna UM, Falck JR, Bezprozvanny I (1998) Functional coupling of phosphatidylinositol 4,5-bisphosphate to inositol 1,4,5-trisphosphate receptor. J Biol Chem 273:14067-14070.
36. 3 receptor complex. EMBO J 9:61-67.
37. Marx SO, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, Rosemblit N, Marks AR (2000) PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101:365-376.
38. Marx SO, Reiken S, Hisamatsu Y, Gaburjakova M, Gaburjakova J, Yang YM, Rosemblit N, Marks AR (2001) Phosphorylation-dependent regulation of ryanodine receptors: a novel role for leucine/isoleucine zippers. J Cell Biol 153:699-708.
39. Matsumoto M, Nakagawa T, Inoue T, Nagata E, Tanaka K, Takano H, Minowa O, Kuno J, Sakakibara S, Yamada M, Yoneshima H, Miyawaki A, Fukuuchi Y, Furuichi T, Okano H, Mikoshiba K, Noda T (1996) Ataxia and epileptic seizures in mice lacking type 1 inositol 1,4,5-trisphosphate receptor. Nature 379:168-171.
40. Maximov A, Sudhof TC, Bezprozvanny I (1999) Association of neuronal calcium channels with modular adaptor proteins. J Biol Chem 274:24453-24456.
41. Mignery GA, Newton CL, Archer BT, Sudhof TC (1990) Structure and expression of the rat inositol 1,4,5-trisphosphate receptor. J Biol Chem 265:12679-12685.
42. 2+ flux in reconstituted vesicles. J Biol Chem 269:6735-6742.
43. Nishi A, Snyder GL, Greengard P (1997) Bidirectional regulation of DARPP-32 phosphorylation by dopamine. J Neurosci 17:8147-8155.
44. Nishi A, Snyder GL, Nairn AC, Greengard P (1999) Role of calcineurin and protein phosphatase-2A in the regulation of DARPP-32 dephosphorylation in neostriatal neurons. J Neurochem 72:2015-2021.
45. Nosyreva E, Miyakawa T, Wang Z, Glouchankova L, Mizushima A, Iino M, Bezprozvanny I (2002) The high affinity calcium-calmodulin-binding site does not play a role in modulation of type 1 inositol (1,4,5)-trisphosphate receptor function by calcium and calmodulin. Biochem J 365:659-667.
46. Ouimet CC, da Cruz e Silva EF, Greengard P (1995) The α and γ1 isoforms of protein phosphatase 1 are highly and specifically concentrated in dendritic spines. Proc Natl Acad Sci USA 92:3396-3400.
47. Pieper AA, Brat DJ, O'Hearn E, Krug DK, Kaplin AI, Takahashi K, Greenberg JH, Ginty D, Molliver ME, Snyder SH (2001) Differential neuronal localizations and dynamics of phosphorylated and unphosphorylated type 1 inositol 1,4,5-trisphosphate receptors. Neuroscience 102:433-444.
48. Sharp AH, Dawson TM, Ross CA, Fotuhi M, Mourey RJ, Snyder SH (1993a) Inositol 1,4,5-trisphosphate receptors: immunohistochemical localization to discrete areas of rat central nervous system. Neuroscience 53:927-942.
49. 2+ release channels in rat brain. J Neurosci 13:3051-3063.
50. 2+ and calmodulin. J Biol Chem 274:12157-12162.
51. r 32 kDa)/protein phosphatase-1 pathway regulates dephosphorylation of the NMDA receptor. J Neurosci 18:10297-10303.
52. 3 receptor. EMBO J 10:3199-3206.
53. Supattapone S, Danoff SK, Theibert A, Joseph SK, Steiner J, Snyder SH (1988) Cyclic AMP-dependent phosphorylation of a brain inositol trisphosphate receptor decreases its release of calcium. Proc Natl Acad Sci USA 85:8747-8750.
54. Surmeier DJ, Bargas J, Hemmings Jr HC, Nairn AC, Greengard P (1995) Modulation of calcium currents by a D1 dopaminergic protein kinase/phosphatase cascade in rat neostriatal neurons. Neuron 14:385-397.
55. Surmeier DJ, Song WJ, Yan Z (1996) Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J Neurosci 16:6579-6591.
56. Taylor CW, Genazzani AA, Morris SA (1999) Expression of inositol trisphosphate receptors. Cell Calcium 26:237-251.
57. Thrower EC, Hagar RE, Ehrlich BE (2001) Regulation of Ins(1,4,5)P3 receptor isoforms by endogenous modulators. Trends Pharmacol Sci 22:580-586.
58. Tu H, Miyakawa T, Wang Z, Glouchankova L, Iino M, Bezprozvanny I (2002) Functional characterization of the type 1 inositol 1,4,5-trisphosphate receptor coupling domain SII(+/-) splice variants and the opisthotonos mutant form. Biophys J 82:1995-2004.
59. Tu JC, Xiao B, Yuan JP, Lanahan AA, Leoffert K, Li M, Linden DJ, Worley PF (1998) Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron 21:717-726.
60. 2+ concentration decrease in GH4C1 cells. J Biol Chem 265:10320-10326.
61. 2+ release. II. Effect of cAMP-dependent protein kinase. Am J Physiol 258:C1086-C1091.
62. r 260,000. J Neurosci 6:954-961.
63. Wojcikiewicz RJ, Luo SG (1998) Phosphorylation of inositol 1,4,5-trisphosphate receptors by cAMP-dependent protein kinase. Type I, II, and III receptors are differentially susceptible to phosphorylation and are phosphorylated in intact cells. J Biol Chem 273:5670-5677.
64. Yamada M, Miyawaki A, Saito K, Nakajima T, Yamamoto-Hino M, Ryo Y, Furuichi T, Mikoshiba K (1995) The calmodulin-binding domain in the mouse type 1 inositol 1,4,5-trisphosphate receptor. Biochem J 308:83-88.
65. Yan Z, Hsieh-Wilson L, Feng J, Tomizawa K, Allen PB, Fienberg AA, Nairn AC, Greengard P (1999) Protein phosphatase 1 modulation of neostriatal AMPA channels: regulation by DARPP-32 and spinophilin. Nat Neurosci 2:13-17.
66. 2+ release channels. Proc Natl Acad Sci USA 7:7-12.