A novel lipid-anchored A-kinase anchoring protein facilitates cAMP-responsive membrane events

EMBO Journal

Volumn 17, Issue 8, 1998, Pages 2261-2272

  Fraser, Lain D C ^a   Tavalin, Steven J ^a   Lester, Linda B ^a   Langeberg, Lorene K ^a   Westphal, Ann M ^a   Dean, Rebecca A ^a   Marrion, Neil V ^a   Scott, John D ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

AKAP18; Insulin secretion; Kinase anchoring; L type Ca2+ channel; Lipid modification

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DERIVATIVE; INSULIN; MEMBRANE PROTEIN; MUTANT PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CALCIUM CURRENT; CONTROLLED STUDY; DNA TRANSFECTION; HUMAN; HUMAN CELL; INSULIN RELEASE; MEMBRANE; MEMBRANE BINDING; MOLECULAR CLONING; MYRISTYLATION; NUCLEOTIDE SEQUENCE; PALMITOYLATION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; PROTEIN TARGETING; STRUCTURE ACTIVITY RELATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BINDING SITES; CALCIUM CHANNELS; CARRIER PROTEINS; CELL LINE; CELL MEMBRANE; CLONING, MOLECULAR; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA, COMPLEMENTARY; ELECTRIC CONDUCTIVITY; GLUCAGON; GLUCAGON-LIKE PEPTIDE 1; HUMANS; INSULIN; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PEPTIDE MAPPING; PROTEIN KINASES; PROTEIN PRECURSORS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 2642705036     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.8.2261     Document Type: Article

References (64)

1. Aderem,A. (1992) The MARCKS brothers: a family of protein kinase C substrates. Cell, 71, 713-716.
2. Ammala,C., Ashcroft,F.M. and Rorsman,P. (1993) Calcium-independent potentiation of insulin release by cyclic AMP in single B-cells. Nature, 363, 356-358.
3. Ammala,C., Eliasson,L., Bokvist,K., Berggren,P.-O., Honkanen,R.E., Sjoholm,A. and Rorsman,P. (1994) Activation of protein kinases and inhibition of protein phosphatases play a central role in the regulation of exocytosis in mouse pancreatic β cells. Proc. Natl Acad. Sci. USA, 91, 4343-4347.
4. Blackshear,P.J. (1993) The MARCKS family of cellular protein kinase C substrates. J. Biol Chem., 268, 1501-1504.
5. 2+ channels and insulin-containing secretory granules and its significance for the initiation of exocytosis in mouse pancreatic β-cells. EMBO J., 14, 50-57.
6. Bregman,D.B., Bhattacharya,N. and Rubin,C.S. (1989) High affinity binding protein for the regulatory subunit of cAMP-dependent protein kinase II-β. J. Biol. Chem., 264, 4648-4656.
7. 2+ channel activity by cAMP-dependent protein kinase. Proc. Natl Acad. Sci. USA, 94, 11067-11072.
8. Carr,D.W. and Scott,J.D. (1992) Blotting and band-shifting: techniques for studying protein-protein interactions. Trends Biochem. Sci., 17, 246-249.
9. Carr,D.W., Stofko-Hahn,R.E., Fraser,I.D.C., Bishop,S.M., Acott,T.S., Brennan,R.G. and Scott,J.D. (1991) Interaction of the regulatory subunit (RII) of cAMP-dependent protein kinase with RII-anchoring proteins occurs through an amphipathic helix binding motif. J. Biol. Chem., 266, 14188-14192.
10. Carr,D.W., Hausken,Z.E., Fraser,I.D.C., Stofko-Hahn,R.E. and Scott,J.D. (1992a) Association of the type II cAMP-dependent protein kinase with a human thyroid RII-anchoring protein, cloning and characterization of the RII-binding domain. J. Biol. Chem., 267, 13376-13382.
11. Carr,D.W., Stofko-Hahn,R.E., Fraser,I.D.C., Cone,R.D. and Scott,J.D. (1992b) Localization of the cAMP-dependent protein kinase to the postsynaptic densities by A-kinase anchoring proteins: characterization of AKAP79. J. Biol. Chem., 267, 16816-16823.
12. Coghlan,V.M., Langeberg,L.K., Fernandez,A., Lamb,N.J.C. and Scott,J.D. (1994) Cloning and characterization of AKAP95, a nuclear protein that associates with the regulatory subunit of type II cAMP-dependent protein kinase. J. Biol Chem., 269, 7658-7665.
13. Coghlan,V.M., Perrino,B.A., Howard,M., Langeberg,L.K., Hicks,J.B., Gallatin,W.M. and Scott,J.D. (1995) Association of protein kinase A and protein phosphatase 2B with a common anchoring protein. Science, 267, 108-112.
14. Corbin,J.D. and Reimann,E.M. (1974) A filter assay for determining protein kinase activity. Methods Enzymol., 38, 287-294.
15. De Camilli,P., Moretti,M., Donini,S.D., Walter,U. and Lohmann,S.M. (1986) Heterogeneous distribution of the cAMP receptor protein RII in the nervous system: evidence for its intracellular accumulation on microtubules, microtubule-organizing centers, and in the area of the Golgi complex. J. Cell Biol., 103, 189-203.
16. Dell'Acqua,M.L. and Scott,J.D. (1997) Protein kinase A anchoring. J. Biol. Chem., 272, 12881-12884.
17. Dell'Acqua,M.L., Faux,MC., Thorburn,J., Thorburn,A. and Scott,J.D. (1998) Membrane-targeting sequences on AKAP79 bind phosphatidylinositol-4,5-bisphosphate. EMBO J., 17, 2246-2260.
18. Dransfield,D.T., Bradford,A.J., Smith,J., Martin,M., Roy,C., Mangeat, P.H. and Goldenring,J.R. (1997) Ezrin is a cyclic AMP-dependent protein kinase anchoring protein. EMBO J., 16, 101-109.
19. Drucker,D.J., Philippe J., Mojsov,S., Chick,W.L. and Habener,J.F. (1987) Glucagon-like peptide I stimulates insulin gene expression and increases cyclic AMP levels in a rat islet cell line. Proc. Natl Acad. Sci. USA, 84, 3434-3438.
20. Faux,M.C. and Scott,J.D. (1996a) Molecular glue: kinase anchoring and scaffold proteins. Cell, 70, 8-12.
21. Faux,M.C. and Scott,J.D. (1996b) More on target with protein phosphorylation: conferring specificity by location. Trends Biochem. Sci., 21, 312-315.
22. 2+ channels requires membrane targeting of PKA and phosphorylation of channel subunits. Neuron, 19, 185-196.
23. Glantz,S.B., Amat,J.A. and Rubin,C.S. (1992) cAMP signaling in neurons: patterns of neuronal expression and intracellular localization for a novel protein, AKAP 150, that anchors the regulatory subunit of cAMP-dependent protein kinase IIβ. Mol. Biol Chem., 3, 1215-1228.
24. Gray,PC., Tibbs,V.C., Catterall,W.A. and Murphy,B.J. (1997) Identification of a 15-kDa cAMP-dependent protein kinase-anchoring protein associated with skeletal muscle L-type calcium channels. J. Biol. Chem., 272, 6297-6302.
25. Gromada,J., Dissing,S., Bokvist,K., Renstrom,E., Frokjaer-Jensen,J., Wulff,B.S. and Rorsman,P. (1995) Glucagon-like peptide 1 increases cytoplasmic calcium in insulin secreting betaTC3-cells by enhancement of intracellular calcium mobilization. Diabetes, 44, 767-774.
26. Gromada,J., Ding,W.-G., Barg,S., Renstrom,E. and Rorsman,P. (1997) Multisite regulation of insulin secretion by cAMP-increasing agonists: evidence that glucagon-like peptide 1 and glucagon act via distinct receptors. Pflugers Arch., 434, 515-524.
27. Gromada,J., Bokvist,K., Ding,W.-G., Holst,J.J., Nielson,J.H. and Rorsman,P. (1998) Glucagon-like peptide 1(7-36) amide stimulates exocytosis in human pancreatic β-cells by both proximal and distal regulatory steps in stimulus-secretion coupling. Diabetes, 47, 57-65.
28. Hamill,O.P., Marty,E., Neher,E., Sakmann,B. and Sigworth,F.J. (1981) Improved patch-clamp techniques for high resolution current recording from cells and cell-free membrane patches. Pflugers Arch., 391, 85-100.
29. Hausken,Z.E., Coghlan,V.M., Hasting,C.A.S., Reimann,E.M. and Scott,J.D. (1994) Type II regulatory subunit (RII) of the cAMP dependent protein kinase interaction with A-kinase anchor proteins requires isoleucines 3 and 5. J. Biol. Chem., 269, 24245-24251.
30. Hausken,Z.E., Coghlan,V.M, and Scott,J.D. (1996a) In R.M.Clegg (ed.), Overlay, Ligand Blotting and Band-shift Techniques to Study Kinase Anchoring. Humana Press, Inc., pp. 47-64.
31. Hausken,Z.E., Dell'Acqua,M.L., Coghlan,V.M. and Scott,J.D. (1996b) Mutational analysis of the A-kinase anchoring protein (AKAP)-binding site on RII. J. Biol Chem., 271, 29016-29022.
32. Hirsch,A.H., Glantz,S.B., Li,Y., You,Y. and Rubin,C.S. (1992) Cloning and expression of an intronless gene for AKAP75, an anchor protein for the regulatory subunit of cAMP-dependent protein kinase IIβ. J. Biol Chem., 267, 2131-2134.
33. Houslay,M.D. (1991) 'Crosstalk': a pivotal role for protein kinase C in modulating relationships between signal transduction pathways. Eur. J. Biochem., 195, 9-27.
34. Hubbard,M. and Cohen,P. (1993) On target with a mechanism for the regulation of protein phosphorylation. Trends Biochem. Sci., 18, 172-177.
35. Joachim,S. and Schwoch,G. (1990) Localization of cAMP-dependent protein kinase subunits along the secretory pathway in pancreatic and parotid acinar cells and accumulation of the catalytic subunit in parotid secretory granules following β-adrenergic stimulation. Eur. J. Cell Biol., 51, 76-84.
36. 2+ channels in skeletal muscle cells requires anchored cAMP-dependent protein kinase. Proc. Natl Acad. Sci. USA, 91, 11492-11496.
37. 2+ channel by anchored cAMP-dependent protein kinase. J. Neurosci., 17, 1243-1255.
38. Kabouridis,P.S., Magee,A.I. and Ley,S.C. (1997) S-acylation of LCK protein tyrosine kinase is essential for its signalling function in T lymphocytes. EMBO J., 16, 4983-4998.
39. Klauck,T.M., Faux,M.C, Labudda,K., Langeberg,L.K., Jaken,S. and Scott,J.D. (1996) Coordination of three signaling enzymes by AKAP79, a mammalian scaffold protein. Science, 271, 1589-1592.
40. Kouhara,H., Hadari,Y.R., Spivak-Kroizman,T., Schilling,J., Bar-Sagi,D., Lax,I. and Schlessinger,J. (1997) A lipid-anchored Grb2-binding protein that links FGF-receptor activation to the Ras/MAPK signaling pathway. Cell, 89, 693-702.
41. Krebs,E.G. (1985) The phosphorylation of proteins: a major mechanism for biological regulation. Biochem. Soc. Trans., 13, 813-820.
42. Lester,L.B., Langeberg,L.K. and Scott,J.D. (1997) Anchoring of protein kinase A facilitates hormone-mediated insulin secretion. Proc. Natl Acad. Sci. USA, 94, 14942-14947.
43. McCartney,S., Little,B.M., Langeberg,L.K. and Scott,J.D. (1995) Cloning and characterization of A-kinase anchor protein 100 (AKAP100): a protein that targets A-kinase to the sarcoplasmic reticulum. J. Biol. Chem., 270, 9327-9333.
44. Milligan,G., Parenti,M. and Magee,A.I. (1995) The dynamic role of palmitoylation in signal transduction. Trends Biochem. Sci., 20, 181-186.
45. Mochly-Rosen,D. (1995) Localization of protein kinases by anchoring proteins: a theme in signal transduction. Science, 268, 247-251.
46. Nauert,J.B., Klauck,T.M., Langeberg,L.K. and Scott,J.D. (1997) Gravin, an autoantigen recognized by serum from myasthenia gravis patients, is a kinase scaffold protein. Curr. Biol., 7, 52-62.
47. Newlon,M.G., Roy,M., Hausken,Z.E., Scott,J.D. and Jennings,P.A. (1997) The A-kinase anchoring domain of Type IIa cAMP-dependent protein kinase is highly helical. J. Biol. Chem., 272, 23637-23644.
48. Pawson,T. and Scott,J.D. (1997) Signaling through scaffold, anchoring, and adaptor proteins. Science, 278, 2075-2080.
49. Resh,M.D. (1994) Myristoylation and palmitoylation of Src family members: the fats of the matter. Cell, 76, 411-413.
50. Rios,R.M., Celati,C., Lohmann,S.M., Bornens,M. and Keryer,G. (1992) Identification of a high affinity binding protein for the regulatory subunit RIIβ of cAMP-dependent protein kinase in Golgi enriched membranes of human lymphoblasts. EMBO J., 11, 1723-1731.
51. Rosenmund,C., Carr,D.W., Bergeson,S.E., Nilaver,G., Scott,J.D. and Westbrook,G.L. (1994) Anchoring of protein kinase A is required for modulation of AMPA/kainate receptors on hippocampal neurons. Nature, 368, 853-856.
52. Rubin,C.S. (1994) A kinase anchor proteins and the intracellular targeting of signals carried by cAMP. Biochim. Biophys. Acta, 1224, 467-479.
53. Safayhi,H. et al. (1997) L-type calcium channels in insulin-secreting cells: biochemical characterization and phosphorylation in RINm5F cells. Mol. Endocrinol., 11, 619-629.
54. Salvatori,S., Damiani,E., Barhanin,J., Furlan,S., Giovanni,S. and Margreth,A. (1990) Co-localization of the dihydropyridine receptor and cyclic AMP-binding subunit of an intrinsic protein kinase to the junctional membrane of the transverse tubules of skeletal muscle. Biochem. J., 267, 679-687.
55. Schlesinger,M.J. (1993) Lipid Modifications of Proteins. CRC Press, Boca Raton, FL.
56. Sjoholm,A., Honkanen,R.E., Berggren,P.-O. (1995) Inhibition of serine/ threonine protein phosphatases by secretagogues in insulin-secreting cells. Endocrinology, 136, 3391-3397.
57. 2+ channel of rat pancreatic β-cell in a cAMP-dependent manner. Diabetes, 46, 1755-1760.
58. Sutherland,E.W. (1972) Studies on the mechanism of hormone action. Science, 171, 401-408.
59. Theurkauf,W.E. and Vallee,R.B. (1982) Molecular characterization of the cAMP-dependent protein kinase bound to microtubule-associated protein 2. J. Biol. Chem., 257, 3284-3290.
60. Thorens,B., Deriaz,N., Bosco,D., DeVos,A., Pipeleers,D., Schuit,F., Meda,P. and Porret,A. (1996) Protein kinase A-dependent phosphorylation of GLUT2 in pancreatic βcells. J. Biol. Chem., 271, 8075-8081.
61. Ca channels in airway smooth muscle cells by endogenous protein kinase A. Am. J. Physiol., 15, L100-L105.
62. Widmann,C., Dolci,W. and Thorens,B. (1995) Agonist-induced internalization and recycling of the glucagon-like peptide-1 receptor in transfected fibroblasts and in insulinomas. Biochem. J., 310, 203-214.
63. Widmann,C., Dolci,W. and Thorens,B. (1996) Desensitization and phosphorylation of the glucagon like peptide-1 (GLP-1) receptor by GLP-1 and 4-phorbol 12-myristate 13-acetate. Mol. Endocrinol., 10, 62-75.
64. 2+ in rat pancreatic β-cells. Diabetes, 45, 295-301.