Glucose activates a protein phosphatase-1-mediated signaling pathway to enhance overall translation in pancreatic β-cells

Endocrinology

Volumn 148, Issue 2, 2007, Pages 609-617

  Vander Mierde, Dirk ^a   Scheuner, Donalyn ^b   Quintens, Roel ^a   Patel, Rupali ^b   Song, Benbo ^b   Tsukamoto, Katsura ^a,d   Beullens, Monique ^a   Kaufman, Randal J ^b,c   Bollen, Mathieu ^a   Schuit, Frans C ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d SANWA KAGAKU KENKYUSHO CO LTD   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL EXTRACT; CYCLOHEXIMIDE; GLUCOSE; INITIATION FACTOR 4B; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 1;

ANIMAL CELL; ARTICLE; CELL CLONE; CONTROLLED STUDY; DEPHOSPHORYLATION; DIABETES MELLITUS; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME ACTIVITY; MALE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CYCLOHEXIMIDE; DRUG SYNERGISM; EIF-2 KINASE; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; EUKARYOTIC INITIATION FACTOR-2; GLUCOSE; HOMEOSTASIS; INSULIN-SECRETING CELLS; MALE; MICE; MICE, INBRED C57BL; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; PROTEIN SYNTHESIS INHIBITORS; PROTEINS; SIGNAL TRANSDUCTION;

EID: 33846459471     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2006-1012     Document Type: Article

References (39)

1. Hinke SA, Hellemans K, Schuit FC 2004 Plasticity of the β cell insulin secretory competence: preparing the pancreatic β cell for the next meal. J Physiol 558:369-380
2. Schuit FC, In't Veld PA, Pipeleers DG 1988 Glucose stimulates proinsulin biosynthesis by a dose-dependent recruitment of pancreatic β cells. Proc Natl Acad Sci USA 85:3865-3869
3. Knoch KP, Bergert H, Borgonovo B, Saeger HD, Altkruger A, Verkade P, Solimena M 2004 Polypyrimidine tract-binding protein promotes insulin secretory granule biogenesis. Nat Cell Biol 6:207-214
4. Wicksteed B, Herbert TP, Alarcon C, Lingohr MK, Moss LG, Rhodes CJ 2001 Cooperativity between the preproinsulin mRNA untranslated regions is necessary for glucose-stimulated translation. J Biol Chem 276:22553-22558
5. Gomez E, Powell ML, Greenman IC, Herbert TP 2004 Glucose-stimulated protein synthesis in pancreatic β-cells parallels an increase in the availability of the translational ternary complex (eIF2-GTP.Met-tRNAi) and the dephosphorylation of eIF2 α. J Biol Chem 279:53937-53946
6. Dever TE 1999 Translation initiation: adept at adapting. Trends Biochem Sci 24:398-403
7. Dever TE 2002 Gene-specific regulation by general translation factors. Cell 108:545-556
8. Krishnamoorthy T, Pavitt GD, Zhang F, Dever TE, Hinnebusch AG 2001 Tight binding of the phosphorylated α subunit of initiation factor 2 (eIF2α) to the regulatory subunits of guanine nucleotide exchange factor eIF2B is required for inhibition of translation initiation. Mol Cell Biol 21:5018-5030
9. Kaufman RJ 1999 Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13:1211-1233
10. Kaufman RJ 2004 Regulation of mRNA translation by protein folding in the endoplasmic reticulum. Trends Biochem Sci 29:152-158
11. Harding HP, Zhang Y, Ron D 1999 Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271-274
12. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D 2000 Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 5:897-904
13. Kaufman RJ, Scheuner D, Schroder M, Shen X, Lee K, Liu CY, Arnold SM 2002 The unfolded protein response in nutrient sensing and differentiation. Nat Rev Mol Cell Biol 3:411-421
14. Liu CY, Kaufman RJ 2003 The unfolded protein response. J Cell Sci 116:1861-1862
15. Schroder M, Kaufman RJ 2005 ER stress and the unfolded protein response. Mutat Res 569:29-63
16. Shen X, Zhang K, Kaufman RJ 2004 The unfolded protein response - a stress signaling pathway of the endoplasmic reticulum. J Chem Neuroanat 28:79-92
17. Zhang K, Kaufman RJ 2004 Signaling the unfolded protein response from the endoplasmic reticulum. J Biol Chem 279:25935-25938
18. Scheuner D, Song B, McEwen E, Liu C, Laybutt R, Gillespie P, Saunders T, Bonner-Weir S, Kaufman RJ 2001 Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 7:1165-1176
19. Scheuner D, Mierde DV, Song B, Flamez D, Creemers JW, Tsukamoto K, Ribick M, Schuit FC, Kaufman RJ 2005 Control of mRNA translation preserves endoplasmic reticulum function in β cells and maintains glucose homeostasis. Nat Med 11:757-764
20. Ceulemans H, Bollen M 2004 Functional diversity of protein phosphatase-1, a cellular economizer and reset button. Physiol Rev 84:1-39
21. Bollen M 2001 Combinatorial control of protein phosphatase-1. Trends Biochem Sci 26:426-431
22. Connor JH, Weiser DC, Li S, Hallenbeck JM, Shenolikar S 2001 Growth arrest and DNA damage-inducible protein GADD34 assembles a novel signaling complex containing protein phosphatase 1 and inhibitor 1. Mol Cell Biol 21:6841-6850
23. Novoa I, Zeng H, Harding HP, Ron D 2001 Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J Cell Biol 153:1011-1022
24. Schuit FC, Kiekens R, Pipeleers DG 1991 Measuring the balance between insulin synthesis and insulin release. Biochem Biophys Res Commun 178:1182-1187
25. Beullens M, Stalmans W, Bollen M 1998 The biochemical identification and characterization of new species of protein phosphatase 1. Methods Mol Biol 93:145-155
26. Ivarsson R, Quintens R, Dejonghe S, Tsukamoto K, in't Veld P, Renstrom E, Schuit FC 2005 Redox control of exocytosis: regulatory role of NADPH, thioredoxin, and glutaredoxin. Diabetes 54:2132-2142
27. Miura Y, Gilon P, Henquin JC 1996 Muscarinic stimulation increases Na+ entry in pancreatic B-cells by a mechanism other than the emptying of intracellular Ca2+ pools. Biochem Biophys Res Commun 224:67-73
28. Skelly RH, Schuppin GT, Ishihara H, Oka Y, Rhodes CJ 1996 Glucose-regulated translational control of proinsulin biosynthesis with that of the proinsulin endopeptidases PC2 and PC3 in the insulin-producing MIN6 cell line. Diabetes 45:37-43
29. Ishihara H, Asano T, Tsukuda K, Katagiri H, Inukai K, Anai M, Kikuchi M, Yazaki Y, Miyazaki JI, Oka Y 1993 Pancreatic β cell line MIN6 exhibits characteristics of glucose metabolism and glucose-stimulated insulin secretion similar to those of normal islets. Diabetologia 36:1139-1145
30. Harding HP, Zeng H, Zhang Y, Jungries R, Chung P, Plesken H, Sabatini DD, Ron D 2001 Diabetes mellitus and exocrine pancreatic dysfunction in perk-/- mice reveals a role for translational control in secretory cell survival. Mol Cell 7:1153-1163
31. Haystead TA, Sim AT, Carling D, Honnor RC, Tsukitani Y, Cohen P, Hardie DG 1989 Effects of the tumour promoter okadaic acid on intracellular protein phosphorylation and metabolism. Nature 337:78-81
32. Takai A, Murata M, Torigoe K, Isobe M, Mieskes G, Yasumoto T 1992 Inhibitory effect of okadaic acid derivatives on protein phosphatases. A study on structure-affinity relationship. Biochem J 284(Pt 2):539-544
33. Boyce M, Bryant KF, Jousse C, Long K, Harding HP, Scheuner D, Kaufman RJ, Ma D, Coen DM, Ron D, Yuan J 2005 A selective inhibitor of eIF2α dephosphorylation protects cells from ER stress. Science 307:935-939
34. Beullens M, Vulsteke V, Van Eynde A, Jagiello I, Stalmans W, Bollen M 2000 The C-terminus of NIPP1 (nuclear inhibitor of protein phosphatase-1) contains a novel binding site for protein phosphatase-1 that is controlled by tyrosine phosphorylation and RNA binding. Biochem J 352(Pt 3):651-658
35. Morris JA, Dorner AJ, Edwards CA, Hendershot LM, Kaufman RJ 1997 Immunoglobulin binding protein (BiP) function is required to protect cells from endoplasmic reticulum stress but is not required for the secretion of selective proteins. J Biol Chem 272:4327-4334
36. Harding HP, Novoa I, Bertolotti A, Zeng H, Zhang Y, Urano F, Jousse C, Ron D 2001 Translational regulation in the cellular response to biosynthetic load on the endoplasmic reticulum. Cold Spring Harb Symp Quant Biol 66:499-508
37. Kojima E, Takeuchi A, Haneda M, Yagi A, Hasegawa T, Yamaki K, Takeda K, Akira S, Shimokata K, Isobe K 2003 The function of GADD34 is a recovery from a shutoff of protein synthesis induced by ER stress: elucidation by GADD34-deficient mice. FASEB J 17:1573-1575
38. Latreille M, Larose L 2006 Nck in a complex containing the catalytic subunit of protein phosphatase 1 regulates eukaryotic initiation factor 2α signaling and cell survival to endoplasmic reticulum stress. J Biol Chem 281:26633-26644
39. Bollen M, Keppens S, Stalmans W 1998 Specific features of glycogen metabolism in the liver. Biochem J 336(Pt 1):19-31