ER stress and the decline and fall of pancreatic beta cells in type 1 diabetes

Upsala Journal of Medical Sciences

Volumn 121, Issue 2, 2016, Pages 133-139

  Brozzi, Flora ^a   Eizirik, Décio L ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Apoptosis; c Jun N terminal kinase; cytokines; ER stress; IRE1 ; type 1 diabetes

Indexed keywords

ERN1 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; PROTEIN SERINE THREONINE KINASE; RIBONUCLEASE;

ANIMAL; APOPTOSIS; CYTOSOL; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HOMEOSTASIS; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; METABOLISM; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET BETA CELL; PROTEIN DOMAIN; RAT; UNFOLDED PROTEIN RESPONSE;

ANIMALS; APOPTOSIS; CYTOSOL; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENDORIBONUCLEASES; HOMEOSTASIS; HUMANS; INSULIN-SECRETING CELLS; MAP KINASE KINASE 4; MICE; PROTEIN DOMAINS; PROTEIN-SERINE-THREONINE KINASES; RATS; UNFOLDED PROTEIN RESPONSE;

EID: 84959066070     PISSN: 03009734     EISSN: None     Source Type: Journal    
DOI: 10.3109/03009734.2015.1135217     Document Type: Review

References (72)

1. F.C.Schuit, P.A.In’t Veld, D.G.Pipeleers Glucose stimulates proinsulin biosynthesis by a dose-dependent recruitment of pancreatic beta cells. Proc Natl Acad Sci U S A. 1988;85:3865–9.
2. R.K.Plemper, S.Bohmler, J.Bordallo, T.Sommer, D.H.Wolf Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation. Nature. 1997;388:891–5.
3. J.L.Brodsky, E.D.Werner, M.E.Dubas, J.L.Goeckeler, K.B.Kruse, A.A.McCracken The requirement for molecular chaperones during endoplasmic reticulum-associated protein degradation demonstrates that protein export and import are mechanistically distinct. J Biol Chem. 1999;274:3453–60.
4. B.R.Pearse, D.N.Hebert Lectin chaperones help direct the maturation of glycoproteins in the endoplasmic reticulum. Biochim Biophys Acta. 2010;1803:684–93.
5. J.R.Hassler, D.L.Scheuner, S.Wang, J.Han, V.K.Kodali, P.Li, et al. The IRE1α/XBP1s pathway is essential for the glucose response and protection of beta cells. PLoS Biol. 2015;13:e1002277.
6. D.L.Eizirik, A.K.Cardozo, M.Cnop The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev. 2008;29:42–61.
7. P.Walter, D.Ron The unfolded protein response: from stress pathway to homeostatic regulation. Science. 2011;334:1081–6.
8. A.Bertolotti, Y.Zhang, L.M.Hendershot, H.P.Harding, D.Ron Dynamic interaction of BiP and ER stress transducers in the unfolded protein response. Nat Cell Biol. 2000;2:326–32.
9. J.Shen, X.Chen, L.Hendershot, R.Prywes ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell. 2002;3:99–111.
10. H.P.Harding, Y.Zhang, A.Bertolotti, H.Zeng, D.Ron Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell. 2000;5:897–904.
11. H.P.Harding, I.Novoa, Y.Zhang, H.Zeng, R.Wek, M.Schapira, et al. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell. 2000;6:1099–108.
12. J.Somers, T.Poyry, A.E.Willis A perspective on mammalian upstream open reading frame function. Int J Biochem Cell Biol. 2013;45:1690–700.
13. J.Ye, C.Koumenis ATF4, an ER stress and hypoxia-inducible transcription factor and its potential role in hypoxia tolerance and tumorigenesis. Curr Mol Med. 2009;9:411–16.
14. H.Yoshida, T.Matsui, A.Yamamoto, T.Okada, K.Mori XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell. 2001;107:881–91.
15. M.Calfon, H.Zeng, F.Urano, J.H.Till, S.R.Hubbard, H.P.Harding, et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP1 mRNA. Nature. 2002;415:92–6.
16. C.Hetz, F.Martinon, D.Rodriguez, L.H.Glimcher The unfolded protein response: integrating stress signals through the stress sensor IRE1α. Physiol Rev. 2011;91:1219–43.
17. M.D.Shoulders, L.M.Ryno, J.C.Genereux, J.J.Moresco, P.G.Tu, C.Wu, et al. Stress-independent activation of XBP1s and/or ATF6 reveals three functionally diverse ER proteostasis environments. Cell Rep. 2013;3:1279–92.
18. M.Maurel, E.Chevet, J.Tavernier, S.Gerlo Getting RIDD of RNA: IRE1 in cell fate regulation. Trends Biochem Sci. 2014;39:245–54.
19. P.Pirot, N.Naamane, F.Libert, N.E.Magnusson, T.F.Orntoft, A.K.Cardozo, et al. Global profiling of genes modified by endoplasmic reticulum stress in pancreatic beta cells reveals the early degradation of insulin mRNAs. Diabetologia. 2007;50:1006–14.
20. T.Iwawaki, A.Hosoda, T.Okuda, Y.Kamigori, C.Nomura-Furuwatari, Y.Kimata, et al. Translational control by the ER transmembrane kinase/ribonuclease IRE1 under ER stress. Nat Cell Biol. 2001;3:158–64.
21. J.Hollien, J.S.Weissman Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science. 2006;313:104–7.
22. A.G.Lerner, J.P.Upton, P.V.Praveen, R.Ghosh, Y.Nakagawa, A.Igbaria, et al. IRE1α induces thioredoxin-interacting protein to activate the NLRP3 inflammasome and promote programmed cell death under irremediable ER stress. Cell Metab. 2012;16:250–64.
23. D.L.Eizirik, M.Cnop ER stress in pancreatic beta cells: the thin red line between adaptation and failure. Sci Signal. 2010;3:e7.
24. M.Cnop, F.Foufelle, L.A.Velloso Endoplasmic reticulum stress, obesity and diabetes. Trends Mol Med. 2012;18:59–68.
25. F.Engin ER stress and development of type 1 diabetes. J Investig Med. 2015 Jul 30. [Epub ahead of print].
26. S.G.Fonseca, J.Gromada, F.Urano Endoplasmic reticulum stress and pancreatic beta cell death. Trends Endocrinol Metab. 2011;22:266–74.
27. D.L.Eizirik, M.Miani, A.K.Cardozo Signalling danger: endoplasmic reticulum stress and the unfolded protein response in pancreatic islet inflammation. Diabetologia. 2013;56:234–41.
28. M.Cnop, N.Welsh, J.C.Jonas, A.Jorns, S.Lenzen, D.L.Eizirik Mechanisms of pancreatic beta cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes. 2005;54(Suppl 2):S97–107.
29. T.J.Biden, E.Boslem, K.Y.Chu, N.Sue Lipotoxic endoplasmic reticulum stress, beta cell failure, and type 2 diabetes mellitus. Trends Endocrinol Metab. 2014;25:389–98.
30. E.N.Gurzov, D.L.Eizirik Bcl-2 proteins in diabetes: mitochondrial pathways of beta cell death and dysfunction. Trends Cell Biol. 2011;21:424–31.
31. S.A.Tersey, Y.Nishiki, A.T.Templin, S.M.Cabrera, N.D.Stull, S.C.Colvin, et al. Islet beta cell endoplasmic reticulum stress precedes the onset of type 1 diabetes in the nonobese diabetic mouse model. Diabetes. 2012;61:818–27.
32. F.Engin, A.Yermalovich, T.Nguyen, S.Hummasti, W.Fu, D.L.Eizirik, et al. Restoration of the unfolded protein response in pancreatic beta cells protects mice against type 1 diabetes. Sci Transl Med. 2013;5:211ra156.
33. K.D.McCullough, J.L.Martindale, L.O.Klotz, T.Y.Aw, N.J.Holbrook Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol. 2001;21:1249–59.
34. F.Urano, X.Wang, A.Bertolotti, Y.Zhang, P.Chung, H.P.Harding, et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science. 2000;287:664–6.
35. A.Ammendrup, A.Maillard, K.Nielsen, A.N.Aabenhus, P.Serup, M.O.Dragsbaek, et al. The c-Jun amino-terminal kinase pathway is preferentially activated by interleukin-1 and controls apoptosis in differentiating pancreatic beta cells. Diabetes. 2000;49:1468–76.
36. C.Bonny, A.Oberson, M.Steinmann, D.F.Schorderet, P.Nicod, G.Waeber IB1 reduces cytokine-induced apoptosis of insulin-secreting cells. J Biol Chem. 2000;275:16466–72.
37. C.Bonny, A.Oberson, S.Negri, C.Sauser, D.F.Schorderet Cell-permeable peptide inhibitors of JNK: novel blockers of beta cell death. Diabetes. 2001;50:77–82.
38. E.N.Gurzov, F.Ortis, D.A.Cunha, G.Gosset, M.Li, A.K.Cardozo, et al. Signaling by IL-1β + IFN-γ and ER stress converge on DP5/Hrk activation: a novel mechanism for pancreatic beta cell apoptosis. Cell Death Differ. 2009;16:1539–50.
39. L.Marroqui, I.Santin, R.S.Dos Santos, L.Marselli, P.Marchetti, D.L.Eizirik BACH2, a candidate risk gene for type 1 diabetes, regulates apoptosis in pancreatic beta cells via JNK1 modulation and crosstalk with the candidate gene PTPN2. Diabetes. 2014;63:2516–27.
40. F.Brozzi, S.Gerlo, F.A.Grieco, T.R.Nardelli, S.Lievens, C.Gysemans, et al. A combined “omics” approach identifies N-myc interactor as a novel cytokine-induced regulator of IRE1α protein and c-Jun N-terminal kinase in pancreatic beta cells. J Biol Chem. 2014;289:20677–93.
41. F.Brozzi, T.R.Nardelli, M.Lopes, I.Millard, J.Barthson, M.Igoillo-Esteve, et al. Cytokines induce endoplasmic reticulum stress in human, rat and mouse beta cells via different mechanisms. Diabetologia. 2015;58:2307–16.
42. J.H.Lin, H.Li, D.Yasumura, H.R.Cohen, C.Zhang, B.Panning, et al. IRE1 signaling affects cell fate during the unfolded protein response. Science. 2007;318:944–9.
43. F.Walter, J.Schmid, H.Dussmann, C.G.Concannon, J.H.Prehn Imaging of single cell responses to ER stress indicates that the relative dynamics of IRE1/XBP1 and PERK/ATF4 signalling rather than a switch between signalling branches determine cell survival. Cell Death Differ. 2015;22:1502–16.
44. U.Woehlbier, C.Hetz Modulating stress responses by the UPRosome: a matter of life and death. Trends Biochem Sci. 2011;36:329–37.
45. B.M.Gardner, P.Walter Unfolded proteins are IRE1-activating ligands that directly induce the unfolded protein response. Science. 2011;333:1891–4.
46. J.Groenendyk, Z.Peng, E.Dudek, X.Fan, M.J.Mizianty, E.Dufey, et al. Interplay between the oxidoreductase PDIA6 and microRNA-322 controls the response to disrupted endoplasmic reticulum calcium homeostasis. Sci Signal. 2014;7:ra54.
47. D.Eletto, D.Eletto, D.Dersh, T.Gidalevitz, Y.Argon Protein disulfide isomerase A6 controls the decay of IRE1α signaling via disulfide-dependent association. Mol Cell. 2014;53:562–76.
48. C.Hetz, L.H.Glimcher Fine-tuning of the unfolded protein response: assembling the IRE1α interactome. Mol Cell. 2009;35:551–61.
49. C.Hetz, E.Chevet, S.A.Oakes Proteostasis control by the unfolded protein response. Nat Cell Biol. 2015;17:829–38.
50. C.Hetz, P.Bernasconi, J.Fisher, A.H.Lee, M.C.Bassik, B.Antonsson, et al. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1α. Science. 2006;312:572–6.
51. D.A.Rodriguez, S.Zamorano, F.Lisbona, D.Rojas-Rivera, H.Urra, J.R.Cubillos-Ruiz, et al. BH3-only proteins are part of a regulatory network that control the sustained signalling of the unfolded protein response sensor IRE1α. EMBO J. 2012;31:2322–35.
52. Y.Qiu, T.Mao, Y.Zhang, M.Shao, J.You, Q.Ding, et al. A crucial role for RACK1 in the regulation of glucose-stimulated IRE1α activation in pancreatic beta cells. Sci Signal. 2010;3:ra7.
53. D.L.Eizirik, S.Sandler, J.P.Palmer Repair of pancreatic beta-cells. A relevant phenomenon in early IDDM? Diabetes. 1993;42:1383–91.
54. D.L.Eizirik, D.G.Pipeleers, Z.Ling, N.Welsh, C.Hellerstrom, A.Andersson Major species differences between humans and rodents in the susceptibility to pancreatic beta cell injury. Proc Natl Acad Sci U S A. 1994;91:9253–6.
55. N.Welsh, B.Margulis, L.A.Borg, H.J.Wiklund, J.Saldeen, M.Flodstrom,. Differences in the expression of heat-shock proteins and antioxidant enzymes between human and rodent pancreatic islets: implications for the pathogenesis of insulin-dependent diabetes mellitus. Mol Med. 1995;1:806–20.
56. D.L.Eizirik, C.A.Delaney, M.H.Green, J.M.Cunningham, J.R.Thorpe, D.G.Pipeleers, et al. Nitric oxide donors decrease the function and survival of human pancreatic islets. Mol Cell Endocrinol. 1996;118:71–83.
57. B.J.Oleson, J.A.McGraw, K.A.Broniowska, M.Annamalai, J.Chen, J.R.Bushkofsky, et al. Distinct differences in the responses of the human pancreatic beta cell line EndoC-βH1 and human islets to proinflammatory cytokines. Am J Physiol Regul Integr Comp Physiol. 2015;309:R525–34.
58. D.L.Eizirik, G.S.Korbutt, Hellerstrom C. Prolonged exposure of human pancreatic islets to high glucose concentrations in vitro impairs the beta cell function. J Clin Invest. 1992;90:1263–8.
59. L.Jansson, D.L.Eizirik, D.G.Pipeleers, L.A.Borg, C.Hellerstrom, A.Andersson Impairment of glucose-induced insulin secretion in human pancreatic islets transplanted to diabetic nude mice. J Clin Invest. 1995;96:721–6.
60. D.L.Eizirik, L.Jansson, M.Flodstrom, C.Hellerstrom, A.Andersson Mechanisms of defective glucose-induced insulin release in human pancreatic islets transplanted to diabetic nude mice. J Clin Endocrinol Metab. 1997;82:2660–3.
61. M.Igoillo-Esteve, A.Genin, N.Lambert, J.Desir, I.Pirson, B.Abdulkarim, et al. tRNA methyltransferase homolog gene TRMT10A mutation in young onset diabetes and primary microcephaly in humans. PLoS Genet. 2013;9:e1003888.
62. B.D.Price, L.A.Mannheim-Rodman, S.K.Calderwood Brefeldin A, thapsigargin, and AIF4 stimulate the accumulation of GRP78 mRNA in a cycloheximide dependent manner, whilst induction by hypoxia is independent of protein synthesis. J Cell Physiol. 1992;152:545–52.
63. M.Cnop, M.Igoillo-Esteve, M.Rai, A.Begu, Y.Serroukh, C.Depondt, et al. Central role and mechanisms of beta cell dysfunction and death in friedreich ataxia-associated diabetes. Ann Neurol. 2012;72:971–82.
64. A.K.Cardozo, F.Ortis, J.Storling, Y.M.Feng, J.Rasschaert, M.Tonnesen, et al. Cytokines downregulate the sarcoendoplasmic reticulum pump Ca2 + ATPase 2b and deplete endoplasmic reticulum Ca2+, leading to induction of endoplasmic reticulum stress in pancreatic beta cells. Diabetes. 2005;54:452–61.
65. J.Y.Chan, G.J.Cooney, T.J.Biden, D.R.Laybutt Differential regulation of adaptive and apoptotic unfolded protein response signalling by cytokine-induced nitric oxide production in mouse pancreatic beta cells. Diabetologia. 2011;54:1766–76.
66. D.Liu, D.Pavlovic, M.C.Chen, M.Flodstrom, S.Sandler, D.L.Eizirik Cytokines induce apoptosis in beta cells isolated from mice lacking the inducible isoform of nitric oxide synthase (iNOS-/-). Diabetes. 2000;49:1116–22.
67. F.Allagnat, M.Fukaya, T.C.Nogueira, D.Delaroche, N.Welsh, L.Marselli, et al. C/EBP homologous protein contributes to cytokine-induced pro-inflammatory responses and apoptosis in beta cells. Cell Death Differ. 2012;19:1836–46.
68. D.L.Eizirik, S.Sandler, N.Welsh, M.Cetkovic-Cvrlje, A.Nieman, D.A.Geller, et al. Cytokines suppress human islet function irrespective of their effects on nitric oxide generation. J Clin Invest. 1994;93:1968–74.
69. K.Hostens, D.Pavlovic, Y.Zambre, Z.Ling, C.Van Schravendijk, D.L.Eizirik, et al. Exposure of human islets to cytokines can result in disproportionately elevated proinsulin release. J Clin Invest. 1999;104:67–72.
70. P.Ravassard, Y.Hazhouz, S.Pechberty, E.Bricout-Neveu, M.Armanet, P.Czernichow, et al. A genetically engineered human pancreatic beta cell line exhibiting glucose-inducible insulin secretion. J Clin Invest. 2011;121:3589–97.
71. D.Pavlovic, M.C.Chen, L.Bouwens, D.L.Eizirik, D.Pipeleers Contribution of ductal cells to cytokine responses by human pancreatic islets. Diabetes. 1999;48:29–33.
72. D.Pipeleers, A.Hoorens, M.Marichal-Pipeleers, M.Van de Casteele, L.Bouwens, Z.Ling Role of pancreatic beta cells in the process of beta cell death. Diabetes. 2001;50(Suppl 1):S52–7.