PERK activation at low glucose concentration is mediated by SERCA pump inhibition and confers preemptive cytoprotection to pancreatic β-cells

Molecular Endocrinology

Volumn 25, Issue 2, 2011, Pages 315-326

  Moore, Claire E ^a   Omikorede, Omotola ^a   Gomez, Edith ^a   Willars, Gary B ^a   Herbert, Terence P ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); CALCIUM; GLUCOSE; INITIATION FACTOR 2ALPHA; NEURONAL CALCIUM SENSOR; PROINSULIN; PROTEIN KINASE R; PROTEIN KINASE R LIKE ER KINASE; PROTEIN TYROSINE KINASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL ENERGY; CELL FUNCTION; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; EVIDENCE BASED PRACTICE; FLUORESCENCE RESONANCE ENERGY TRANSFER; INSULINOMA; MALE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; SARCOPLASM;

ANIMALS; CALCIUM; CELL LINE, TUMOR; CELL SURVIVAL; CELLS, CULTURED; EIF-2 KINASE; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; EUKARYOTIC INITIATION FACTOR-2; FLOW CYTOMETRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GLUCOSE; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MALE; MICE; PHOSPHORYLATION; PROINSULIN; PROTEIN BIOSYNTHESIS; RATS; RATS, WISTAR; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

EUKARYOTA; RATTUS;

EID: 79951705219     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2010-0309     Document Type: Article

References (48)

1. 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 eIF2α. J Biol Chem 279:53937-53946 (Pubitemid 40053124)
2. Guest PC, Rhodes CJ, Hutton JC 1989 Regulation of the biosynthesis of insulin-secretory-granule proteins. Co-ordinate translational control is exerted on some, but not all, granule matrix constituents. Biochem J 257:431-437
3. Itoh N, Okamoto H 1980 Translational control of proinsulin synthesis by glucose. Nature 283:100-102 (Pubitemid 10170895)
4. Itoh N, Sei T, Nose K, Okamoto H 1978 Glucose stimulation of the proinsulin synthesis in isolated pancreatic islets without increasing amount of proinsulin mRNA. FEBS Lett 93:343-347 (Pubitemid 9053257)
5. Permutt MA 1974 Effect of glucose on initiation and elongation rates in isolated rat pancreatic islets. J Biol Chem 249:2738-2742
6. Permutt MA, Kipnis DM 1972 Insulin biosynthesis: studies of islet polyribosomes (nascent peptides-sucrose gradient analysis-gel filtration). Proc Natl Acad Sci USA 69:505-509
7. Harding HP, Zhang Y, Ron D 1999 Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271-274 (Pubitemid 29051178)
8. Harding HP, Ron D 2002 Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes 51(Suppl 3):S455-S461 (Pubitemid 35403430)
9. Herbert TP 2007 PERK in the life and death of the pancreatic β-cell. Biochem Soc Trans 35:1205-1207 (Pubitemid 350206462)
10. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D 2000 Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6:1099-1108
11. 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 (Pubitemid 32607351)
12. Cullinan SB, Zhang D, Hannink M, Arvisais E, Kaufman RJ, Diehl JA 2003 Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol Cell Biol 23:7198-7209 (Pubitemid 37211002)
13. Cullinan SB, Diehl JA 2004 PERK-dependent activation of Nrf2 contributes to redox homeostasis and cell survival following endoplasmic reticulum stress. J Biol Chem 279:20108-20117 (Pubitemid 38623455)
14. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG, Ron D 2002 IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415:92-96 (Pubitemid 34062456)
15. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K 2001 XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:881-891 (Pubitemid 34084979)
16. 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
17. Senée V, Vattem KM, Delépine M, Rainbow LA, Haton C, Lecoq A, Shaw NJ, Robert JJ, Rooman R, Diatloff-Zito C, Michaud JL, Bin-Abbas B, Taha D, Zabel B, Franceschini P, Topaloglu AK, Lathrop GM, Barrett TG, Nicolino M, Wek RC, Julier C 2004 Wolcott-Rallison Syndrome: clinical, genetic, and functional study of EIF2AK3 mutations and suggestion of genetic heterogeneity. Diabetes 53:1876-1883 (Pubitemid 38857047)
18. Back SH, Scheuner D, Han J, Song B, Ribick M, Wang J, Gildersleeve RD, Pennathur S, Kaufman RJ 2009 Translation attenuation through eIF2α phosphorylation prevents oxidative stress and maintains the differentiated state in β cells. Cell Metab 10:13-26
19. Gomez E, Powell ML, Bevington A, Herbert TP 2008 A decrease in cellular energy status stimulates PERK-dependent eIF2α phosphorylation and regulates protein synthesis in pancreatic β-cells. Biochem J 410:485-493 (Pubitemid 351429019)
20. Michalak M, Robert Parker JM, Opas M 2002 Ca2+ signaling and calcium binding chaperones of the endoplasmic reticulum. Cell Calcium 32:269-278 (Pubitemid 36175750)
21. Lodish HF, Kong N 1990 Perturbation of cellular calcium blocks exit of secretory proteins from the rough endoplasmic reticulum. J Biol Chem 265:10893-10899
22. Sambrook JF 1990 The involvement of calcium in transport of secretory proteins from the endoplasmic reticulum. Cell 61:197-199
23. Nakamura K, Bossy-Wetzel E, Burns K, Fadel MP, Lozyk M, Goping IS, Opas M, Bleackley RC, Green DR, Michalak M 2000 Changes in endoplasmic reticulum luminal environment affect cell sensitivity to apoptosis. J Cell Biol 150:731-740 (Pubitemid 30663411)
24. 2+ channels in endoplasmic reticulum stress and β-cell death. Diabetes 58:422-432
25. 2+ analyzed with an improved genetically encoded fluorescent sensor. Proc Natl Acad Sci USA 101:17404-17409
26. MacLennan DH, Rice WJ, Green NM 1997 The mechanism of Ca2+ transport by sarco(endo)plasmic reticulum Ca2+-ATPases. J Biol Chem 272:28815-28818 (Pubitemid 27498155)
27. Hardie DG 2003 The AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology 144:5179-5183 (Pubitemid 37476044)
28. 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
29. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, Sadri N, Yun C, Popko B, Paules R, Stojdl DF, Bell JC, Hettmann T, Leiden JM, Ron D 2003 An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11:619-633 (Pubitemid 36385118)
30. Lu PD, Harding HP, Ron D 2004 Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J Cell Biol 167:27-33 (Pubitemid 39363411)
31. Vattem KM, Wek RC 2004 Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc Natl Acad Sci USA 101:11269-11274 (Pubitemid 39038336)
32. Lu PD, Jousse C, Marciniak SJ, Zhang Y, Novoa I, Scheuner D, Kaufman RJ, Ron D, Harding HP 2004 Cytoprotection by preemptive conditional phosphorylation of translation initiation factor 2. EMBO J 23:169-179 (Pubitemid 38165757)
33. Jonas JC, Bensellam M, Duprez J, Elouil H, Guiot Y, Pascal SM 2009 Glucose regulation of islet stress responses and β-cell failure in type 2 diabetes. Diabetes Obes Metab 11(Suppl 4):65-81
34. Eizirik DL, Cardozo AK, Cnop M 2008 The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev 29:42-61 (Pubitemid 351252746)
35. Maechler P, Kennedy ED, Sebö E, Valeva A, Pozzan T, Wollheim CB 1999 Secretagogues modulate the calcium concentration in the endoplasmic reticulum of insulin-secreting cells. Studies in aequorin-expressing intact and permeabilized ins-1 cells. J Biol Chem 274:12583-12592
36. 2+ in the endoplasmic reticulum of mouse pancreatic β cells. J Biol Chem 274:36883-36890
37. 2+ in mouse pancreatic β-cells. J Physiol 530:533-540
38. 2+-ATPase (SERCA)-2 and ryanodine receptors. Diabetes 51(Suppl 1):S190-S201
39. + channel: a pas de deux. Diabetes 53(Suppl 3):S113-S122
40. Macdonald WA, Stephenson DG 2006 Effect of ADP on slow-twitch muscle fibres of the rat: implications for muscle fatigue. J Physiol 573:187-198 (Pubitemid 43670867)
41. Macdonald WA, Stephenson DG 2004 Effects of ADP on action potential-induced force responses in mechanically skinned rat fast-twitch fibres. J Physiol 559:433-447 (Pubitemid 39263810)
42. Macdonald WA, Stephenson DG 2001 Effects of ADP on sarcoplasmic reticulum function in mechanically skinned skeletal muscle fibres of the rat. J Physiol 532:499-508 (Pubitemid 32390405)
43. Brostrom MA, Brostrom CO 2003 Calcium dynamics and endoplasmic reticular function in the regulation of protein synthesis: implications for cell growth and adaptability. Cell Calcium 34:345-363
44. Elouil H, Bensellam M, Guiot Y, Vander Mierde D, Pascal SM, Schuit FC, Jonas JC 2007 Acute nutrient regulation of the unfolded protein response and integrated stress response in cultured rat pancreatic islets. Diabetologia 50:1442-1452 (Pubitemid 46879004)
45. Greenman IC, Gomez E, Moore CE, Herbert TP 2007 Distinct glucose-dependent stress responses revealed by translational profiling in pancreatic β-cells. J Endocrinol 192:179-187 (Pubitemid 46444408)
46. Robertson R, Zhou H, Zhang T, Harmon JS 2007 Chronic oxidative stress as a mechanism for glucose toxicity of the β cell in type 2 diabetes. Cell Biochem Biophys 48:139-146 (Pubitemid 47340880)
47. Asfari M, Janjic D, Meda P, Li G, Halban PA, Wollheim CB 1992 Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology 130:167-178
48. Purkiss JR, Willars GB 1996 Ionomycin induced changes in intracellular free calcium in SH-SY5Y human neuroblastoma cells: sources of calcium and effects on [3H]noradrenaline release. Cell Calcium 20:21-29 (Pubitemid 26278932)