Epinephrine-induced hyperpolarization of pancreatic islet cells is sensitive to PI3K-PDK1 signaling

FEBS Letters

Volumn 583, Issue 18, 2009, Pages 3101-3106

  Zhang, Ying ^a   Shumilina, Ekaterina ^a   Häring, Hans Ulrich ^b   Lang, Florian ^a   Ullrich, Susanne ^a,b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

Cell membrane potential; K+ channel; LY294002; PI3K

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ADRENALIN; GLUCOSE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; WORTMANNIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CELL MEMBRANE POTENTIAL; CONTROLLED STUDY; ENZYME INHIBITION; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PATCH CLAMP; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; EPINEPHRINE; GLUCOSE; ISLETS OF LANGERHANS; MEMBRANE POTENTIALS; MICE; MICE, MUTANT STRAINS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

MUS;

EID: 69949175134     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2009.08.027     Document Type: Article

References (42)

1. Pace C.S., Murphy M., Conant S., and Lacy P.E. Somatostatin inhibition of glucose-induced electrical activity in cultured rat islet cells. Am. J. Physiol. 233 (1977) C165-C171
2. Peterhoff M., Sieg A., Brede M., Chao C.M., Hein L., and Ullrich S. Inhibition of insulin secretion via distinct signaling pathways in alpha2-adrenoceptor knockout mice. Eur. J. Endocrinol. 149 (2003) 343-350
3. Drews G., Detimary P., and Henquin J.C. Non-additivity of adrenaline and galanin effects on 86Rb efflux and membrane potential in mouse B-cells suggests sharing of common targets. Biochim. Biophys. Acta 1175 (1993) 214-218
4. Sieg A., Su J., Munoz A., Buchenau M., Nakazaki M., Aguilar-Bryan L., Bryan J., and Ullrich S. Epinephrine-induced hyperpolarization of islet cells without KATP channels. Am. J. Physiol. Endocrinol. Metab. 286 (2004) E463-E471
5. Kim M.O., Na S.I., Lee M.Y., Heo J.S., and Han H.J. Epinephrine increases DNA synthesis via ERK1/2s through cAMP, Ca(2+)/PKC, and PI3K/Akt signaling pathways in mouse embryonic stem cells. J Cell Biochem. 104 (2008) 1407-1420
6. Yamboliev I.A., and Mutafova-Yambolieva V.N. PI3K and PKC contribute to membrane depolarization mediated by alpha2-adrenoceptors in the canine isolated mesenteric vein. BMC Physiol. 5 (2005) 9
7. Alessi D.R., Andjelkovic M., Caudwell B., Cron P., Morrice N., Cohen P., and Hemmings B.A. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15 (1996) 6541-6551
8. Alessi D.R., and Cohen P. Mechanism of activation and function of protein kinase B. Curr. Opin. Genet. Dev. 8 (1998) 55-62
9. Divecha N., Banfic H., and Irvine R.F. The polyphosphoinositide cycle exists in the nuclei of Swiss 3T3 cells under the control of a receptor (for IGF-I) in the plasma membrane, and stimulation of the cycle increases nuclear diacylglycerol and apparently induces translocation of protein kinase C to the nucleus. EMBO J. 10 (1991) 3207-3214
10. + channels via PI3-kinase, PDK1 and SGK1. Pflugers Arch. 443 (2002) 625-634
11. Kobayashi T., and Cohen P. Activation of serum- and glucocorticoid-regulated protein kinase by agonists that activate phosphatidylinositide 3-kinase is mediated by 3-phosphoinositide-dependent protein kinase-1 (PDK1) and PDK2. Biochem. J. 339 (1999) 319-328
12. Kotani K., Yonezawa K., Hara K., Ueda H., Kitamura Y., Sakaue H., Ando A., Chavanieu A., Calas B., and Grigorescu F. Involvement of phosphoinositide 3-kinase in insulin- or IGF-1-induced membrane ruffling. EMBO J. 13 (1994) 2313-2321
13. Park J., Leong M.L., Buse P., Maiyar A.C., Firestone G.L., and Hemmings B.A. Serum and glucocorticoid-inducible kinase (SGK) is a target of the PI 3-kinase-stimulated signaling pathway. EMBO J. 18 (1999) 3024-3033
14. Flamigni F., Marmiroli S., Capanni C., Stefanelli C., Guarnieri C., and Caldarera C.M. Phosphatidylinositol 3-kinase is required for the induction of ornithine decarboxylase in leukemia cells stimulated to growth. Biochem. Biophys. Res. Commun. 239 (1997) 729-733
15. Yousif M.H. Phosphoinositide 3-kinase contributes to diabetes-induced abnormal vascular reactivity in rat perfused mesenteric bed. Cell Biochem. Funct. 26 (2008) 451-458
16. Carnero A., and Lacal J.C. Wortmannin, an inhibitor of phosphatidylinositol 3-kinase, induces oocyte maturation through a MPF-MAPK-dependent pathway. FEBS Lett. 422 (1998) 155-159
17. Lawlor M.A., Mora A., Ashby P.R., Williams M.R., Murray-Tait V., Malone L., Prescott A.R., Lucocq J.M., and Alessi D.R. Essential role of PDK1 in regulating cell size and development in mice. EMBO J. 21 (2002) 3728-3738
18. Ullrich S., Berchtold S., Ranta F., Seebohm G., Henke G., Lupescu A., Mack A.F., Chao C.M., Su J., Nitschke R., Alexander D., Friedrich B., Wulff P., Kuhl D., and Lang F. Serum- and glucocorticoid-inducible kinase 1 (SGK1) mediates glucocorticoid-induced inhibition of insulin secretion. Diabetes 54 (2005) 1090-1099
19. Barg S., Galvanovskis J., Gopel S.O., Rorsman P., and Eliasson L. Tight coupling between electrical activity and exocytosis in mouse glucagon-secreting alpha-cells. Diabetes 49 (2000) 1500-1510
20. El Kholy W., Macdonald P.E., Lin J.H., Wang J., Fox J.M., Light P.E., Wang Q., Tsushima R.G., and Wheeler M.B. The phosphatidylinositol 3-kinase inhibitor LY294002 potently blocks K(V) currents via a direct mechanism. FASEB J. 17 (2003) 720-722
21. 2+ currents in an insulin-secreting cell line (RINm5F). J. Biol. Chem. 266 (1991) 18025-18033
22. + channel in mouse pancreatic B cells. Nature 349 (1991) 77-79
23. Iwanir S., and Reuveny E. Adrenaline-induced hyperpolarization of mouse pancreatic islet cells is mediated by G protein-gated inwardly rectifying potassium (GIRK) channels. Pflugers Arch. 456 (2008) 1097-1108
24. i in oscillating and non-oscillating HIT-T15 cells. Cell Calcium 27 (2000) 163-173
25. o heterotrimeric G proteins are required to exert the full effect of norepinephrine on the beta-cell K ATP channel. J. Biol. Chem. 283 (2008) 5306-5316
26. + (KATP) channels in rat CRI-G1 insulinoma cells involves disruption of the actin cytoskeleton. J. Physiol. 527 Pt 1 (2000) 95-107
27. + channels. J. Biol. Chem. 284 (2009) 9331-9340
28. Abel K.B., Lehr S., and Ullrich S. Adrenaline-, not somatostatin-induced hyperpolarization is accompanied by a sustained inhibition of insulin secretion in INS-1 cells. Activation of sulphonylurea K+ATP channels is not involved. Pflugers Arch. 432 (1996) 89-96
29. Scheltdorf M., and Mest H.J. Pertussis toxin converts hyperpolarizations caused by alpha(2)-adrenoceptor agonists containing an imidazoline moiety into depolarizations in MIN 6 cells. Naunyn Schmiedebergs Arch. Pharmacol. 366 (2002) 204-208
30. Karkoulias G., Mastrogianni O., Lymperopoulos A., Paris H., and Flordellis C. Alpha(2)-adrenergic receptors activate MAPK and Akt through a pathway involving arachidonic acid metabolism by cytochrome P450-dependent epoxygenase, matrix metalloproteinase activation and subtype-specific transactivation of EGFR. Cell Signal. 18 (2006) 729-739
31. Scarparo A.C., Visconti M.A., and Castrucci A.M. Signalling pathways evoked by alpha1-adrenoceptors in human melanoma cells. Cell Biochem. Funct. 24 (2006) 119-129
32. Nakanishi S., Catt K.J., and Balla T. A wortmannin-sensitive phosphatidylinositol 4-kinase that regulates hormone-sensitive pools of inositolphospholipids. Proc. Natl. Acad. Sci. USA 92 (1995) 5317-5321
33. Cho H., Kim Y.A., Yoon J.Y., Lee D., Kim J.H., Lee S.H., and Ho W.K. Low mobility of phosphatidylinositol 4,5-bisphosphate underlies receptor specificity of Gq-mediated ion channel regulation in atrial myocytes. Proc. Natl. Acad. Sci. USA 102 (2005) 15241-15246
34. Matavel A., and Lopes C.M. PKC activation and PIP(2) depletion underlie biphasic regulation of IKs by Gq-coupled receptors. J. Mol. Cell Cardiol. 46 (2009) 704-712
35. Zhang H.J., Redmon J.B., Andresen J.M., and Robertson R.P. Somatostatin and epinephrine decrease insulin messenger ribonucleic acid in HIT cells through a pertussis toxin-sensitive mechanism. Endocrinology 129 (1991) 2409-2414
36. Gibson T.B., Lawrence M.C., Gibson C.J., Vanderbilt C.A., McGlynn K., Arnette D., Chen W., Collins J., Naziruddin B., Levy M.F., Ehrlich B.E., and Cobb M.H. Inhibition of glucose-stimulated activation of extracellular signal-regulated protein kinases 1 and 2 by epinephrine in pancreatic beta-cells. Diabetes 55 (2006) 1066-1073
37. Biondi R.M., Kieloch A., Currie R.A., Deak M., and Alessi D.R. The PIF-binding pocket in PDK1 is essential for activation of S6K and SGK, but not PKB. EMBO J. 20 (2001) 4380-4390
38. Lang F., Bohmer C., Palmada M., Seebohm G., Strutz-Seebohm N., and Vallon V. (Patho)physiological significance of the serum- and glucocorticoid-inducible kinase isoforms. Physiol. Rev. 86 (2006) 1151-1178
39. Mora A., Komander D., van Aalten D.M., and Alessi D.R. PDK1, the master regulator of AGC kinase signal transduction. Semin. Cell Dev. Biol. 15 (2004) 161-170
40. Embark H.M., Bohmer C., Vallon V., Luft F., and Lang F. Regulation of KCNE1-dependent K(+) current by the serum and glucocorticoid-inducible kinase (SGK) isoforms. Pflugers Arch. 445 (2003) 601-606
41. 2+ dependent and independent secretion. Biosci. Rep. 7 (1987) 443-454
42. Artunc F., Rexhepaj R., Volkl H., Grahammer F., Remy C., Sandulache D., Nasir O., Wagner C.A., Alessi D.R., and Lang F. Impaired intestinal and renal glucose transport in PDK-1 hypomorphic mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291 (2006) R1533-R1538