Identification of the structural determinant responsible for the phosphorylation of G-protein activated potassium channel 1 by cAMP-dependent protein kinase

FEBS Journal

Volumn 276, Issue 21, 2009, Pages 6218-6226

  Müllner, Carmen ^a   Steinecker, Bibiane ^a   Gorischek, Astrid ^a   Schreibmayer, Wolfgang ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

GIRK; IK+Ach; PKA

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; OLIGOMER; PHOSPHORUS 32; SERINE; THREONINE;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENETIC ENGINEERING; IMMUNOPRECIPITATION; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; REGULATORY MECHANISM; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FEMALE; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; XENOPUS LAEVIS;

EID: 70349967808     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07325.x     Document Type: Article

References (38)

1. Dascal N (2001) Ion-channel regulation by G proteins. Trends Endocrinol Metab 12, 391 398.
2. Dascal N (1997) Signalling via the G protein-activated K+ channels. Cell Signal 9, 551 573.
3. Smith PA, Sellers LA Humphrey PPA (2001) Somatostatin activates two types of inwardly rectifying K+ channels in MIN-6 cells. J Physiol (Lond) 532, 127 142.
4. Shankar H, Kahner BN, Prabhakar J, Lakhani P, Kim S Kunapuli SP (2006) G-protein-gated inwardly rectifying potassium channels regulate ADP-induced cPLA(2) activity in platelets through Src family kinases. Blood 108, 3027 3034.
5. Perry CA, Pravetoni M, Teske JA, Aguado C, Erickson DJ, Medrano JF, Lujan R, Kotz CM Wickman K (2008) Predisposition to late-onset obesity in GIRK4 knockout mice. Proc Natl Acad Sci USA 105, 8148 8153.
6. Iwanir S Reuveny E (2008) Adrenaline-induced hyperpolarization of mouse pancreatic islet cells is mediated by G protein-gated inwardly rectifying potassium (GIRK) channels. Pflugers Arch 456, 1097 1108.
7. Stringer BK, Cooper AG Shepard SB (2001) Overexpression of the G-protein inwardly rectifying potassium channel 1 (GIRK1) in primary breast carcinomas correlates with axillary lymph node metastasis. Cancer Res 61, 582 588.
8. Schreibmayer W, Dessauer CW, Vorobiov D, Gilman AG, Lester HA, Davidson N Dascal N (1996) Inhibition of an inwardly rectifying K+ channel by G-protein alpha-subunits. Nature 380, 624 627.
9. Rubinstein M, Peleg S, Berlin S, Brass D Dascal N (2007) G alpha(i3) primes the G protein-activated K+ channels for activation by coexpressed G beta gamma in intact Xenopus oocytes. J Physiol (Lond) 581, 17 32.
10. Ruppersberg JP (2000) Intracellular regulation of inward rectifier K+ channels. Pflugers Arch 441, 1 11.
11. Mao JZ, Wang XR, Chen FX, Wang RP, Rojas A, Shi Y, Piao H Jiang C (2004) Molecular basis for the inhibition of G protein-coupled inward rectifier K+ channels by protein kinase C. Proc Natl Acad Sci USA 101, 1087 1092.
12. Mora SI Escobar LI (2005) Phosphorylation of a tyrosine at the N-terminus regulates the surface expression of GIRK5 homomultimers. FEBS Lett 579, 3019 3023.
13. Ippolito DL, Xu M, Bruchas MR, Wickman K Chavkin C (2005) Tyrosine phosphorylation of K(ir)3.1 in spinal cord is induced by acute inflammation, chronic neuropathic pain, and behavioral stress. J Biol Chem 280, 41683 41693.
14. Chung HJ, Qian X, Ehlers M, Jan YN Jan LY (2009) Neuronal activity regulates phosphorylation-dependent surface delivery of G protein-activated inwardly rectifying potassium channels. Proc Natl Acad Sci USA 106, 629 634.
15. Huang CL, Feng SY Hilgemann DW (1998) Direct activation of inward rectifier potassium channels by PIP2 and its stabilization by G beta gamma. Nature 391, 803 806.
16. Zhang HL, He C, Yan XX, Mirshahi T Logothetis DE (1999) Activation of inwardly rectifying K+ channels by distinct PtdIns(4,5)P-2 interactions. Nat Cell Biol 1, 183 188.
17. Medina I, Krapivinsky G, Arnold S, Kovoor P, Krapivinsky L Clapham DE (2000) A switch mechanism for G ss gamma activation of I-KACh. J Biol Chem 275, 29709 29716.
18. Mullner C, Vorobiov D, Bera AK, Uezono Y, Yakubovich D, Frohnwieser-Steinecker B, Dascal N Schreibmayer W (2000) Heterologous facilitation of G protein-activated K+ channels by beta-adrenergic stimulation via cAMP-dependent protein kinase. J Gen Physiol 115, 547 557.
19. Kim D (1990) Beta-adrenergic regulation of the muscarinic-gated K+ channel via cyclic Amp-dependent protein-kinase in atrial cells. Circ Res 67, 1292 1298.
20. Mullner C, Yakubovich D, Dessauer CW, Platzer D Schreibmayer W (2003) Single channel analysis of the regulation of GIRK1/GIRK4 channels by protein phosphorylation. Biophys J 84, 1399 1409.
21. Nikolov EN Ivanova-Nikolova TT (2004) Coordination of membrane excitability through a GIRK1 signaling complex in the atria. J Biol Chem 279, 23630 23636.
22. Muellner C, Steinecker-Frohnwieser B Schreibmayer WF (2002) Structural determinant responsible for the cAMP dependent phosphorylation of the GIRK1 subunit. Biophysical Society Meeting Abstracts Biophys J Supplement, 82, 2890 Pos.
23. Lopes CMB, Remon JI, Matavel A, Sui JL, Keselman I, Medei E, Shen YM, Rosenhouse-Dantsker A, Rohacs T Logothetis DE (2007) Protein kinase A modulates PLC-dependent regulation and PIP2-sensitivity of K+ channels. Channels 1, 124 134.
24. Krapivinsky G, Gordon EA, Wickman K, Velimirovic B, Krapivinsky L Clapham DE (1995) The G-protein-gated atrial K+ channel I-Kach is a Heteromultimer of 2 inwardly rectifying K+-channel proteins. Nature 374, 135 141.
25. Ivanina T, Rishal I, Varon D, Mullner C, Frohnwieser-Steinecke B, Schreibmayer W, Dessauer CW Dascal N (2003) Mapping the G beta gamma-binding sites in GIRK1 and GIRK2 subunits of the G protein-activated K+ channel. J Biol Chem 278, 29174 29183.
26. Kennelly PJ Krebs EG (1991) Consensus sequences as substrate-specificity determinants for protein-kinases and protein phosphatases. J Biol Chem 266, 15555 15558.
27. Chan KW, Sui JL, Vivaudou M Logothetis DE (1996) Control of channel activity through a unique amino acid residue of a G protein-gated inwardly rectifying K+ channel subunit. Proc Natl Acad Sci USA 93, 14193 14198.
28. Vivaudou M, Chan KW, Sui JL, Jan LY, Reuveny E Logothetis DE (1997) Probing the G-protein regulation of GIRK1 and GIRK4, the two subunits of the K-ACh channel, using functional homomeric mutants. J Biol Chem 272, 31553 31560.
29. McConnachie G, Langeberg LK Scott JD (2006) AKAP signaling complexes: getting to the heart of the matter. Trends Mol Med 12, 317 323.
30. Rusinova R, Shen Y-MA, Dolios G, Padovan J, Yang H, Kirchberger M, Wang R Logothetis DE (2009) Mass spectrometric analysis reveals a functionally important PKA phosphorylation site in a Kir3 channel subunit. Pflugers Arch-Eur J Physiol 458, 303 314.
31. Pinna LA Ruzzene M (1996) How do protein kinases recognize their substrates? Biochim Biophys Acta 1314, 191 225.
32. Bender K, Nasrollahzadeh P, Timpert M, Liu B, Pott L Kienitz MC (2008) A role for RGS10 in beta-adrenergic modulation of G-protein-activated K+ (GIRK) channel current in rat atrial myocytes. J Physiol (Lond) 586, 2049 2060.
33. Hedin KE, Lim NF Clapham DE (1996) Cloning of a Xenopus laevis inwardly rectifying K+ channel subunit that permits GIRK1 expression of I-KACh currents in oocytes. Neuron 16, 423 429.
34. Laemmli UK (1970) Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature 227, 680 685.
35. Sambrook J Russel DW (2001) Molecular Cloning, 3 edn. CSH, Cold Spring Harbour.
36. Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72, 248 254.
37. Dascal N Lotan I (1992) Expression of exogenous ion channels and neurotransmitter receptors in RNA-injected Xenopus oocytes. In Methods in Neurobiology (Longstaff ARP, ed), pp. 205 225. Humana Press, Totowa, NJ.
38. Schreibmayer W, Lester HA Dascal N (1994) Voltage clamping of Xenopus laevis oocytes utilizing agarose-cushion electrodes. Pflugers Arch 426, 453 458.