Pancreatic Β-cell prosurvival effects of the incretin hormones involve post-translational modification of Kv2.1 delayed rectifier channels

Cell Death and Differentiation

Volumn 19, Issue 2, 2012, Pages 333-344

  Kim, S J ^a   Widenmaier, S B ^a   Choi, W S ^a,b   Nian, C ^a   Ao, Z ^a   Warnock, G ^a   McIntosh, C H S ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b Institute Pasteur Korea   (South Korea)

Author keywords

b cell apoptosis; diabetes; GIP; GLP 1; incretins; Kv channel

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; DELAYED RECTIFIER POTASSIUM CHANNEL; DELAYED RECTIFIER POTASSIUM CHANNEL KV2.1; GASTRIC INHIBITORY POLYPEPTIDE; GLUCAGON LIKE PEPTIDE 1; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; INCRETIN; THAPSIGARGIN; UNCLASSIFIED DRUG;

ACETYLATION; APOPTOSIS; ARTICLE; CELL NUCLEUS; CELL SURVIVAL; CONTROLLED STUDY; CYTOPLASM; ENDOPLASMIC RETICULUM STRESS; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INTERNALIZATION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REGULATORY MECHANISM; WESTERN BLOTTING;

ACETYLATION; ADULT; APOPTOSIS; CELL LINE; CELL NUCLEUS; CELL SURVIVAL; CREB-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENDOCYTOSIS; GASTRIC INHIBITORY POLYPEPTIDE; GLUCAGON-LIKE PEPTIDE 1; HISTONE ACETYLTRANSFERASES; HISTONE DEACETYLASES; HUMANS; INCRETINS; INSULIN-SECRETING CELLS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; SHAB POTASSIUM CHANNELS; STAUROSPORINE; THAPSIGARGIN;

EID: 84855685549     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2011.102     Document Type: Article

References (40)

1. Drucker DJ. The role of gut hormones in glucose homeostasis. J Clin Invest 2007; 117: 24-32. (Pubitemid 46048446)
2. McIntosh CHS, Widenmaier S, Kim SJ. Pleiotropic actions of the incretin hormones. Vitam Horm 2010; 84: 21-79.
3. McIntosh CHS, Widenmaier S, Kim SJ. Glucose-dependent insulinotropic polypeptide (gastric inhibitory polypeptide; GIP). Vitam Horm 2009; 80: 409-471.
4. Kim SJ, Winter K, Nian C, Tsuneoka M, Koda Y, McIntosh CHS. Glucose-dependent insulinotropic polypeptide (GIP) stimulation of pancreatic beta-cell survival is dependent upon phosphatidylinositol 3-kinase (PI3 K)/protein kinase B (PKB) signaling, inactivation of the forkhead transcription factor Foxo1, and down-regulation of bax expression. J Biol Chem 2005; 280: 22297-22307. (Pubitemid 40827886)
5. Kim SJ, Nian C, Widenmaier S, McIntosh CHS. Glucose-dependent insulinotropic polypeptide (GIP) mediated up-regulation of b-cell anti-apoptotic Bcl-2 gene expression is coordinated by cAMP-response element binding protein (CREB) and cAMP-responsive CREB coactivator 2 (TORC2). Mol Cell Biol 2008; 28: 1644-1656.
6. Widenmaier SB, Ao Z, Kim SJ, Warnock G, McIntosh CHS. Suppression of p38 MAPK and JNK via Akt-mediated inhibition of apoptosis signal regulating kinase 1 constitutes a core component of the beta-cell pro-survival effects of glucose-dependent insulinotropic polypeptide. J Biol Chem 2009; 284: 30372-30382.
7. Jitrapakdee S, Wutthisathapornchai A, Wallace JC, MacDonald MJ. Regulation of insulin secretion: role of mitochondrial signaling. Diabetologia 2010; 53: 1019-1032.
8. Aras MA, Aizenman E. Obligatory role of ASK1 in the apoptotic surge of K+ currents. Neurosci Lett 2005; 387: 136-140. (Pubitemid 41160544)
9. McLaughlin B, Pal S, Tran MP, Parsons AA, Barone FC, Erhardt JA et al. p38 activation is required upstream of potassium current enhancement and caspase cleavage in thiol oxidant-induced neuronal apoptosis. J Neurosci 2001; 21: 3303-3311. (Pubitemid 32422795)
10. MacDonald PE, Wheeler MB. Voltage-dependent K+ channels in pancreatic beta cells: role, regulation and potential as therapeutic targets. Diabetologia 2003; 46: 1046-1062. (Pubitemid 37041235)
11. Kim SJ, Choi WS, Han JS, Warnock G, Fedida D, McIntosh CHS. A novel mechanism for the suppression of a voltage-gated potassium channel by glucose-dependent insulinotropic polypeptide: protein kinase A-dependent endocytosis. J Biol Chem 2005; 280: 28692-28700. (Pubitemid 41105770)
12. MacDonald PE, Ha XF, Wang J, Smukler SR, Sun AM, Gaisano HY et al. Members of the Kv1 and Kv2 voltage-dependent K+ channel families regulate insulin secretion. Mol Endocrinol 2001; 15: 1423-1435. (Pubitemid 32703488)
13. Jacobson DA, Kuznetsov A, Lopez JP, Kash S, Ammä lä CE, Philipson LH. Kv2.1 ablation alters glucose-induced islet electrical activity, enhancing insulin secretion. Cell Metab 2007; 6: 229-235. (Pubitemid 47324137)
14. Burg ED, Remillard CV, Yuan JXJ. K+ channels in apoptosis. J Memb Biol 2006; 209: 3-20.
15. Storey NM, Gómez-Angelats M, Bortner CD, Armstrong DL, Cidlowski JA. Stimulation of Kv1.3 potassium channels by death receptors during apoptosis in Jurkat T-lymphocytes. J Biol Chem 2003; 278: 33319-33326. (Pubitemid 37055783)
16. Pal SK, Takimoto K, Aizenman E, Levitan ES. Apoptotic surface delivery of K+ channels. Cell Death Differ 2006; 13: 661-667.
17. Close P, Creppe C, Gillard M, Ladang A, Chapelle JP, Nguyen L et al. The emerging role of lysine acetylation of non-nuclear proteins. Cell Mol Life Sci 2010; 67: 1255-1264.
18. Kim SJ, Nian C, McIntosh CHS. Glucose-dependent insulinotropic polypeptide and glucagon-like peptide-1 modulate beta-cell chromatin structure. J Biol Chem 2009; 284: 12896-12904.
19. Ma L, Gao JS, Guan Y, Shi X, Zhang H, Ayrapetov MK et al. Acetylation modulates prolactin receptor dimerization. Proc Natl Acad Sci USA 2010; 107: 19314-19319.
20. Kalkhoven E. CBP and p300: HATs for different occasions. Biochem Pharmacol 2004; 68: 1145-1155. (Pubitemid 39094280)
21. Bortner CD, Cidlowski JA. Cell shrinkage and monovalent cation fluxes: Role in apoptosis. Arch Biochem Biophys 2007; 462: 176-188. (Pubitemid 46863418)
22. Yu SP, Choi DW. Ions, cell volume and apoptosis. Proc Natl Acad Sci USA 2000; 97: 9360-9362.
23. MacDonald PE, Sewing S, Wang J, Joseph JW, Smukler SR, Sakellaropoulos G et al. Inhibition of Kv2.1 voltage-dependent K+ channels in pancreatic beta-cells enhances glucose-dependent insulin secretion. J Biol Chem 2002; 277: 44938-44945. (Pubitemid 36159091)
24. MacDonald PE, Salapatek AM, Wheeler MB. Glucagon-like peptide-1 receptor activation antagonizes voltage-dependent repolarizing K+ currents in beta-cells: a possible glucosedependent insulinotropic mechanism. Diabetes 2002; 51: S443-S447. (Pubitemid 35403428)
25. MacDonald PE, Wang X, Xia F, El-kholy W, Targonsky ED, Tsushima RG et al. Antagonism of rat beta-cell voltage-dependent K+ currents by exendin 4 requires dual activation of the cAMP/protein kinase A and phosphatidylinositol 3-kinase signaling pathways. J Biol Chem 2003; 278: 52446-52453. (Pubitemid 38035837)
26. Benítez-Rangel E, García L, Namorado MC, Reyes JL, Guerrero-Hernández A. Ion channel inhibitors block caspase activation by mechanisms other than restoring intracellular potassium concentration. Cell Death Dis 2011; 2: e113.
27. Leung YM, Kang Y, Gao X, Xia F, Xie H, Sheu L et al. Syntaxin 1A binds to the cytoplasmic C terminus of Kv2.1 to regulate channel gating and trafficking. J Biol Chem 2003; 278: 17532-17538. (Pubitemid 36799641)
28. Xia F, Gao X, Kwan E, Lam PP, Chan L, Sy K et al. Disruption of pancreatic beta-cell lipid rafts modifies Kv2.1 channel gating and insulin exocytosis. J Biol Chem 2004; 279: 24685-246891.
29. Feinshreiber L, Singer-Lahat D, Friedrich R, Matti U, Sheinin A, Yizhar O et al. Nonconducting function of the Kv2.1 channel enables it to recruit vesicles for release in neuroendocrine and nerve cells. J Cell Sci 2010; 123: 1940-1947.
30. O0Connell KM, Loftus R, Tamkun MM. Localization-dependent activity of the Kv2.1 delayed-rectifier K+ channel. Proc Natl Acad Sci USA 2010; 107: 12351-12356.
31. Park KS, Mohapatra DP, Misonou H, Trimmer JS. Graded regulation of the Kv2.1 potassium channel by variable phosphorylation. Science 2006; 313: 976-979. (Pubitemid 44267390)
32. Dai XQ, Kolic J, Marchi P, Sipione S, Macdonald PE. SUMOylation regulates Kv2.1 and modulates pancreatic beta-cell excitability. J Cell Sci 2009; 122: 775-779.
33. Redman PT, He K, Hartnett KA, Jefferson BS, Hu L, Rosenberg PA et al. Apoptotic surge of potassium currents is mediated by p38 phosphorylation of Kv2.1. Proc Natl Acad Sci USA 2007; 104: 3568-3573. (Pubitemid 46364199)
34. Sobko A, Peretz A, Attali B. Constitutive activation of delayed-rectifier potassium channels by a src family tyrosine kinase in Schwann cells. EMBO J 1998; 17: 4723-4734. (Pubitemid 28377172)
35. Redman PT, Hartnett KA, Aras MA, Levitan ES, Aizenman E. Regulation of apoptotic potassium currents by coordinated zinc-dependent signalling. J Physiol 2009; 587: 4393-4404.
36. Jiao S, Liu Z, Ren WH, Ding Y, Zhang YQ, Zhang ZH et al. cAMP/protein kinase A signaling pathway protects against neuronal apoptosis and is associated with modulation of Kv2.1 in cerebellar granule cells. J Neurochem 2007; 100: 979-991. (Pubitemid 46213923)
37. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009; 325: 834-840.
38. Yang XJ, Seto E. Lysine acetylation: codified crosstalk with other posttranslational modficiations. Mol Cell 2008; 31: 449-461.
39. Larsen L, Tonnesen M, Ronn SG, Størling J, Jørgensen S, Mascagni P et al. Inhibition of histone deacetylases prevents cytokine-induced toxicity in beta cells. Diabetologia 2007; 50: 779-789. (Pubitemid 46355819)
40. Lundh M, Christensen DP, Rasmussen DN, Mascagni P, Dinarello CA, Billestrup N et al. Lysine deacetylases are produced in pancreatic beta cells and are differentially regulated by proinflammatory cytokines. Diabetologia 2010; 53: 2569-2578.