Protein kinase Cδ regulates nuclear export of FOXO1 through phosphorylation of the chaperone 14-3-3ζ

Diabetologia

Volumn 58, Issue 12, 2015, Pages 2819-2831

  Gerst, Felicia ^a,b   Kaiser, Gabriele ^a,b   Panse, Madhura ^a   Sartorius, Tina ^a,b   Pujol, Anna ^c,d   Hennige, Anita M ^a   Machicao, Fausto ^a,b   Lammers, Reiner ^a   Bosch, Fatima ^c,d   Häring, Hans Ulrich ^a,b   Ullrich, Susanne ^a,b  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

^c UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^d INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

14 3 3 ; Apoptosis; FOXO1; Insulin secreting beta cells; JNK; Palmitate; PKC

Indexed keywords

GLUCOSE; INSULIN; PALMITIC ACID; PROTEIN KINASE C DELTA; SOMATOMEDIN; STRATIFIN; TRANSCRIPTION FACTOR FKHR; 14-3-3ZETA PROTEIN, MOUSE; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, MOUSE; PRKCD PROTEIN, MOUSE; PROTEIN 14 3 3;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CROSS LINKING; DIMERIZATION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; GLUCOSE HOMEOSTASIS; HUMAN; HUMAN CELL; INSULIN RELEASE; MALE; MOUSE; NONHUMAN; NUCLEAR EXPORT SIGNAL; PANCREAS ISLET CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUNEL ASSAY; WESTERN BLOTTING; ACTIVE TRANSPORT; ANIMAL; C57BL MOUSE; CELL NUCLEUS; GENETICS; METABOLISM; PANCREAS ISLET BETA CELL; PHOSPHORYLATION; PRIMARY CELL CULTURE; TRANSGENIC MOUSE;

14-3-3 PROTEINS; ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INSULIN-SECRETING CELLS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHOSPHORYLATION; PRIMARY CELL CULTURE; PROTEIN KINASE C-DELTA; SIGNAL TRANSDUCTION;

EID: 84946497205     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-015-3744-z     Document Type: Article

References (49)

1. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC (2003) β-cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes 52:102–110
2. Donath MY, Boni-Schnetzler M, Ellingsgaard H, Ehses JA (2009) Islet inflammation impairs the pancreatic β-cell in type 2 diabetes. Physiology 24:325–331
3. Maechler P, Li N, Casimir M, Vetterli L, Frigerio F, Brun T (2010) Role of mitochondria in β-cell function and dysfunction. Adv Exp Med Biol 654:193–216
4. Cunha DA, Hekerman P, Ladriere L et al (2008) Initiation and execution of lipotoxic ER stress in pancreatic β-cells. J Cell Sci 121:2308–2318
5. Buteau J, Accili D (2007) Regulation of pancreatic β-cell function by the forkhead protein FoxO1. Diabetes Obes Metab 9:140–146
6. Ren D, Sun J, Mao L, Ye H, Polonsky KS (2014) BH3-only molecule Bim mediates β-cell death in IRS2 deficiency. Diabetes 63:3378–3387
7. Martinez SC, Tanabe K, Cras-Méneur C, Abumrad NA, Bernal-Mizrachi E, Permutt MA (2008) Inhibition of Foxo1 protects pancreatic islet β-cells against fatty acid and endoplasmic reticulum stress-induced apoptosis. Diabetes 57:846–859
8. Talchai C, Xuan S, Lin HV, Sussel L, Accili D (2012) Pancreatic β cell dedifferentiation as a mechanism of diabetic β cell failure. Cell 150:1223–1234
9. Talchai SC, Accili D (2015) Legacy effect of FoxO1 in pancreatic endocrine progenitors on adult β-cell mass and function. Diabetes 64:1–12
10. Kobayashi M, Kikuchi O, Sasaki T et al (2012) FoxO1 as a double-edged sword in the pancreas: analysis of pancreas- and β-cell-specific FoxO1 knockout mice. Am J Physiol Endocrinol Metab 302:E603–E613
11. Kim-Muller JY, Zhao S, Srivastava S et al (2014) Metabolic inflexibility impairs insulin secretion and results in MODY-like diabetes in triple FoxO-deficient mice. Cell Metab 20:593–602
12. Mussig K, Staiger H, Machicao F et al (2009) Association of common genetic variation in the FOXO1 gene with β-cell dysfunction, impaired glucose tolerance, and type 2 diabetes. J Clin Endocrinol Metab 94:1353–1360
13. Eijkelenboom A, Burgering BM (2013) FOXOs: signalling integrators for homeostasis maintenance. Nat Rev Mol Cell Biol 14:83–97
14. Martinez SC, Cras-Meneur C, Bernal-Mizrachi E, Permutt MA (2006) Glucose regulates Foxo1 through insulin receptor signaling in the pancreatic islet β-cell. Diabetes 55:1581–1591
15. Yan L, Lavin VA, Moser LR, Cui Q, Kanies C, Yang E (2008) PP2A regulates the pro-apoptotic activity of FOXO1. J Biol Chem 283:7411–7420
16. Kaiser G, Gerst F, Michael D et al (2013) Regulation of forkhead box O1 (FOXO1) by protein kinase B and glucocorticoids: different mechanisms of induction of beta cell death in vitro. Diabetologia 56:1587–1595
17. Brunet A, Kanai F, Stehn J et al (2002) 14-3-3 transits to the nucleus and participates in dynamic nucleocytoplasmic transport. J Cell Biol 156:817–828
18. Rena G, Prescott AR, Guo S, Cohen P, Unterman TG (2001) Roles of the forkhead in rhabdomyosarcoma (FKHR) phosphorylation sites in regulating 14-3-3 binding, transactivation and nuclear targetting. Biochem J 354:605–612
19. Brunet A, Bonni A, Zigmond MJ et al (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857–868
20. Zhao X, Gan L, Pan H et al (2004) Multiple elements regulate nuclear/cytoplasmic shuttling of FOXO1: characterization of phosphorylation- and 14-3-3-dependent and -independent mechanisms. Biochem J 378:839–849
21. Park JK, Kang MY, Kim YH et al (2008) PKCδ in preeclamptic placentas promotes Bax dissociation from 14-3-3 ζ through 14-3-3ζ phosphorylation. Placenta 29:584–592
22. Lim GE, Piske M, Johnson JD (2013) 14-3-3 proteins are essential signalling hubs for beta cell survival. Diabetologia 56:825–837
23. Eitel K, Staiger H, Rieger J et al (2003) Protein kinase C delta activation and translocation to the nucleus are required for fatty acid-induced apoptosis of insulin-secreting cells. Diabetes 52:991–997
24. Carpenter L, Cordery D, Biden TJ (2002) Inhibition of protein kinase C δ protects rat INS-1 cells against interleukin-1beta and streptozotocin-induced apoptosis. Diabetes 51:317–324
25. Cantley J, Boslem E, Laybutt DR et al (2011) Deletion of protein kinase Cδ in mice modulates stability of inflammatory genes and protects against cytokine-stimulated beta cell death in vitro and in vivo. Diabetologia 54:380–389
26. Hennige AM, Ranta F, Heinzelmann I et al (2010) Overexpression of kinase-negative protein kinase Cδ in pancreatic β-cells protects mice from diet-induced glucose intolerance and β-cell dysfunction. Diabetes 59:119–127
27. Bezy O, Tran TT, Pihlajamaki J et al (2011) PKCδ regulates hepatic insulin sensitivity and hepatosteatosis in mice and humans. J Clin Invest 121:2504–2517
28. Greene MW, Burrington CM, Lynch DT et al (2014) Lipid metabolism, oxidative stress and cell death are regulated by PKCδ in a dietary model of nonalcoholic steatohepatitis. PLoS One 9, e85848
29. Greene MW, Burrington CM, Luo Y, Ruhoff MS, Lynch DT, Chaithongdi N (2014) PKCδ is activated in the liver of obese Zucker rats and mediates diet-induced whole body insulin resistance and hepatocyte cellular insulin resistance. J Nutr Biochem 25:281–288
30. George M, Ayuso E, Casellas A, Costa C, Devedjian JC, Bosch F (2002) β cell expression of IGF-I leads to recovery from type 1 diabetes. J Clin Invest 109:1153–1163
31. Li W, Yu JC, Shin DY, Pierce JH (1995) Characterization of a protein kinase C-δ (PKC-δ) ATP binding mutant. An inactive enzyme that competitively inhibits wild type PKC-δ enzymatic activity. J Biol Chem 270:8311–8318
32. Ullrich S, Berchtold S, Ranta F et al (2005) Serum- and glucocorticoid-inducible kinase 1 (SGK1) mediates glucocorticoid-induced inhibition of insulin secretion. Diabetes 54:1090–1099
33. Smith AL, Friedman DB, Yu H, Carnahan RH, Reynolds AB (2011) ReCLIP (reversible cross-link immuno-precipitation): an efficient method for interrogation of labile protein complexes. PLoS One 6, e16206
34. Kawamori D, Kaneto H, Nakatani Y et al (2006) The forkhead transcription factor Foxo1 bridges the JNK pathway and the transcription factor PDX-1 through its intracellular translocation. J Biol Chem 281:1091–1098
35. Woodcock JM, Murphy J, Stomski FC, Berndt MC, Lopez AF (2003) The dimeric versus monomeric status of 14-3-3ζ is controlled by phosphorylation of Ser58 at the dimer interface. J Biol Chem 278:36323–36327
36. Kim YS, Choi MY, Kim YHJ et al (2010) Protein kinase Cdelta is associated with 14-3-3 phosphorylation in seizure-induced neuronal death. Epilepsy Res 92:30–40
37. Zhang X, Gan L, Pan H et al (2002) Phosphorylation of serine 256 suppresses transactivation by FKHR (FOXO1) by multiple mechanisms. Direct and indirect effects on nuclear/cytoplasmic shuttling and DNA binding. J Biol Chem 277:45276–45284
38. Basu A, Pal D (2010) Two faces of protein kinase Cδ: the contrasting roles of PKCδ in cell survival and cell death. Sci World J 10:2272–2284
39. Jackson DN, Foster DA (2004) The enigmatic protein kinase Cδ: complex roles in cell proliferation and survival. FASEB J 18:627–636
40. McLoughlin TJ, Smith SM, DeLong AD, Wang H, Unterman TG, Esser KA (2009) FoxO1 induces apoptosis in skeletal myotubes in a DNA-binding-dependent manner. Am J Physiol Cell Physiol 297:C548–C555
41. Shalev A (2014) Minireview: thioredoxin-interacting protein: regulation and function in the pancreatic β-cell. Mol Endocrinol 28:1211–1220
42. Chen J, Saxena G, Mungrue IN, Lusis AJ, Shalev A (2008) Thioredoxin-interacting protein: a critical link between glucose toxicity and β-cell apoptosis. Diabetes 57:938–944
43. Guo S, Dunn SL, White MF (2006) The reciprocal stability of FOXO1 and IRS2 creates a regulatory circuit that controls insulin signaling. Mol Endocrinol 20:3389–3399
44. Weigert C, Hennige AM, Lehmann R et al (2006) Direct cross-talk of interleukin-6 and insulin signal transduction via insulin receptor substrate-1 in skeletal muscle cells. J Biol Chem 281:7060–7067
45. Di Pietro N, Panel V, Hayes S et al (2010) Serum- and glucocorticoid-inducible kinase 1 (SGK1) regulates adipocyte differentiation via forkhead box O1. Mol Endocrinol 24:370–380
46. Yun H, Park S, Kim MJ et al (2014) AMP-activated protein kinase mediates the antioxidant effects of resveratrol through regulation of the transcription factor FoxO1. FEBS J 281:4421–4438
47. Alejandro EU, Lim GE, Mehran AE et al (2011) Pancreatic β-cell Raf-1 is required for glucose tolerance, insulin secretion, and insulin 2 transcription. FASEB J 25:3884–3895
48. Qiang L, Banks AS, Accili D (2010) Uncoupling of acetylation from phosphorylation regulates FoxO1 function independent of its subcellular localization. J Biol Chem 285:27396–27401
49. Sunayama J, Tsuruta F, Masuyama N, Gotoh Y (2005) JNK antagonizes Akt-mediated survival signals by phosphorylating 14-3-3. J Cell Biol 170:295–304