C/EBP homologous protein contributes to cytokine-induced pro-inflammatory responses and apoptosis in β-cells

Cell Death and Differentiation

Volumn 19, Issue 11, 2012, Pages 1836-1846

  Allagnat, F ^a,b   Fukaya, M ^a   Nogueira, T C ^a   Delaroche, D ^a   Welsh, N ^c   Marselli, L ^d   Marchetti, P ^d   Haefliger, J A ^b   Eizirik, D L ^a   Cardozo, A K ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c UPPSALA UNIVERSITY   (Sweden)

^d UNIVERSITY OF PISA   (Italy)

Author keywords

apoptosis; Bcl 2 proteins; CHOP; ER stress; inflammation; pancreatic b cell

Indexed keywords

CASPASE 3; CASPASE 9; CHEMOKINE; CYTOKINE; FAS ANTIGEN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 15; PROTEIN BCL 2; PROTEIN MCL 1; RANTES;

ADULT; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; DEGRADATION; HUMAN; HUMAN CELL; INFLAMMATION; INSULITIS; MALE; MONONUCLEAR CELL; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RAT;

ANIMALS; APOPTOSIS; CASPASE 3; CASPASE 9; CELL LINE; CELL NUCLEUS; CYTOKINES; DIABETES MELLITUS, TYPE 1; ENDOPLASMIC RETICULUM STRESS; I-KAPPA B KINASE; INSULIN-SECRETING CELLS; INTERFERON-GAMMA; INTERLEUKIN-1BETA; MITOCHONDRIA; NF-KAPPA B; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84870988528     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2012.67     Document Type: Article

References (50)

1. Patterson CC, Dahlquist GG, Gyurus E, Green A, Soltesz G. Incidence trends for childhood type 1 diabetes in Europe during 1989-2003 and predicted new cases 2005-20: a multicentre prospective registration study. Lancet 2009; 373: 2027-2033.
2. Todd JA. Etiology of type 1 diabetes. Immunity 2010; 32: 457-467.
3. Eizirik DL, Colli ML, Ortis F. The role of inflammation in insulitis and beta-cell loss in type 1 diabetes. Nat Rev Endocrinol 2009; 5: 219-226.
4. Eizirik DL, Cardozo AK, Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev 2008; 29: 42-61.
5. Gurzov EN, Eizirik DL. Bcl-2 proteins in diabetes: mitochondrial pathways of beta-cell death and dysfunction. Trends Cell Biol 2011; 21: 424-431.
6. Thomas HE, McKenzie MD, Angstetra E, Campbell PD, Kay TW. Beta cell apoptosis in diabetes. Apoptosis 2009; 14:1389-1404.
7. Abdelli S, Abderrahmani A, Hering BJ, Beckmann JS, Bonny C. The c-Jun N-terminal kinase JNK participates in cytokine-and isolation stress-induced rat pancreatic islet apoptosis. Diabetologia 2007; 50:1660-1669.
8. Oeckinghaus A, Hayden MS, Ghosh S. Crosstalk in NF-kappaB signaling pathways. Nat Immunol 2011; 12: 695-708.
9. Cardozo AK, Ortis F, Storling J, Feng YM, Rasschaert J, Tonnesen M, 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: 452-461.
10. Tabas I, Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 2011; 13:184-190.
11. Endo M, Mori M, Akira S, Gotoh T. C/EBP homologous protein (CHOP) is crucial for the induction of caspase-11 and the pathogenesis of lipopolysaccharide-induced inflammation. JImmunol 2006; 176: 6245-6253.
12. Miyazaki Y, Kaikita K, Endo M, Horio E, Miura M, Tsujita K, et al. C/EBP homologous protein deficiency attenuates myocardial reperfusion injury by inhibiting myocardial apoptosis and inflammation. Arterioscler Thromb Vasc Biol 2011; 31:1124-1132.
13. Suyama K, Ohmuraya M, Hirota M, Ozaki N, Ida S, Endo M, et al. C/EBP homologous protein is crucial for the acceleration of experimental pancreatitis. Biochem Biophys Res Commun 2008; 367:176-182.
14. Allagnat F, Cunha D, Moore F, Vanderwinden JM, Eizirik DL, Cardozo AK. Mcl-1 downregulation by pro-inflammatory cytokines and palmitate is an early event contributing to beta-cell apoptosis. Cell Death Differ 2011; 18: 328-337.
15. Akerfeldt MC, Howes J, Chan JY, Stevens VA, Boubenna N, McGuire HM, et al. Cytokine-induced beta-cell death is independent of endoplasmic reticulum stress signaling. Diabetes 2008; 57: 3034-3044.
16. Huang CJ, Lin CY, Haataja L, Gurlo T, Butler AE, Rizza RA, et al. High expression rates of human islet amyloid polypeptide induce endoplasmic reticulum stress mediated beta-cell apoptosis, a characteristic of humans with type 2 but not type 1 diabetes. Diabetes 2007; 56: 2016-2027.
17. Oyadomari S, Takeda K, Takiguchi M, Gotoh T, Matsumoto M, Wada I, et al. Nitric oxide-induced apoptosis in pancreatic beta cells is mediated by the endoplasmic reticulum stress pathway. Proc Natl Acad Sci USA 2001; 98:10845-10850.
18. Pirot P, Ortis F, Cnop M, Ma Y, Hendershot LM, Eizirik DL et al. Transcriptional regulation of the endoplasmic reticulum stress gene chop in pancreatic insulin-producing cells. Diabetes 2007; 56:1069-1077.
19. Carrington EM, McKenzie MD, Jansen E, Myers M, Fynch S, Kos C, et al. Islet beta-cells deficient in Bcl-xL develop but are abnormally sensitive to apoptotic stimuli. Diabetes 2009; 58: 2316-2323.
20. Rabinovitch A, Suarez-Pinzon W, Strynadka K, Ju Q, Edelstein D, Brownlee M, et al. Transfection of human pancreatic islets with an anti-apoptotic gene (bcl-2) protects beta-cells from cytokine-induced destruction. Diabetes 1999; 48:1223-1229.
21. Zhou YP, Pena JC, Roe MW, Mittal A, Levisetti M, Baldwin AC, et al. Overexpression of Bcl-x(L) in beta-cells prevents cell death but impairs mitochondrial signal for insulin secretion. Am J Physiol Endocrinol Metab 2000; 278: E340-E351.
22. Gurzov EN, Germano CM, Cunha DA, Ortis F, Vanderwinden JM, Marchetti P, et al. p53 up-regulated modulator of apoptosis (PUMA) activation contributes to pancreatic beta-cell apoptosis induced by proinflammatory cytokines and endoplasmic reticulum stress. J Biol Chem 2010; 285:19910-19920.
23. Gurzov EN, Ortis F, Cunha DA, Gosset G, Li M, Cardozo AK, et al. Signaling by L-1beta + IFN-gamma and ER stress converge on DP5/Hrk activation: a novel mechanism for pancreatic beta-cell apoptosis. Cell Death Differ 2009; 16:1539-1550.
24. McKenzie MD, Carrington EM, Kaufmann T, Strasser A, Huang DC, Kay TW, et al. Proapoptotic BH3-only protein Bid is essential for death receptor-induced apoptosis of pancreatic beta-cells. Diabetes 2008; 57:1284-1292.
25. Barthson J, Germano CM, Moore F, Maida A, Drucker DJ, Marchetti P, et al. Cytokines tumor necrosis factor-alpha and interferon-gamma induce pancreatic beta-cell apoptosis through STAT1-mediated Bim protein activation. J Biol Chem 2011; 286: 39632-39643.
26. Breitschopf K, Haendeler J, Malchow P, Zeiher AM, Dimmeler S. Posttranslational modification of Bcl-2 facilitates its proteasome-dependent degradation: molecular characterization of the involved signaling pathway. Mol Cell Biol 2000; 20:1886-1896.
27. Yang-Yen HF. Mcl-1: a highly regulated cell death and survival controller. J Biomed Sci 2006; 13: 201-204.
28. Vucic D, Dixit VM, Wertz IE. Ubiquitylation in apoptosis: a post-translational modification at the edge of life and death. Nat Rev Mol Cell Biol 2011;12: 439-452.
29. Stewart DP, Koss B, Bathina M, Perciavalle RM, Bisanz K, Opferman JT. Ubiquitin-independent degradation of antiapoptotic MCL-1. Mol Cell Biol 2010; 30: 3099-3110.
30. Ortis F, Cardozo AK, Crispim D, Storling J, Mandrup-Poulsen T, Eizirik DL. Cytokine-induced proapoptotic gene expression in insulin-producing cells is related to rapid, sustained, and nonoscillatory nuclear factor-kappaB activation. Mol Endocrinol 2006; 20: 1867-1879.
31. Darville MI, Eizirik DL. Cytokine induction of Fas gene expression in insulin-producing cells requires the transcription factors NF-kappaB and C/EBP. Diabetes 2001; 50: 1741-1748.
32. Darville MI, Eizirik DL. Regulation by cytokines of the inducible nitric oxide synthase promoter in insulin-producing cells. Diabetologia 1998; 41:1101-1108.
33. Ortis F, Pirot P, Naamane N, Kreins AY, Rasschaert J, Moore F, et al. Induction of nuclear factor-kappaB and its downstream genes by TNF-alpha and IL-1beta has a pro-apoptotic role in pancreatic beta cells. Diabetologia 2008; 51:1213-1225.
34. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR. The BCL-2 family reunion. Mol Cell 2010;37: 299-310.
35. Bassik MC, Scorrano L, Oakes SA, Pozzan T, Korsmeyer SJ. Phosphorylation of BCL-2 regulates ER Ca2+ homeostasis and apoptosis. EMBO J2004; 23:1207-1216.
36. Wei Y, Pattingre S, Sinha S, Bassik M, Levine B. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell 2008; 30: 678-688.
37. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 2001; 21:1249-1259.
38. Back SH, Scheuner D, Han J, Song B, Ribick M, Wang J, et al. Translation attenuation through eIF2alpha phosphorylation prevents oxidative stress and maintains the differentiated state in beta cells. Cell Metab 2009; 10:13-26.
39. Marciniak SJ, Yun CY, Oyadomari S, Novoa I, Zhang Y, Jungreis R, et al. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev 2004; 18:3066-3077.
40. Stein B, Cogswell PC, Baldwin AS Jr. Functional and physical associations between NF-kappa B and C/EBP family members: a Rel domain-bZIP interaction. Mol Cell Biol 1993; 13: 3964-3974.
41. Cappello C, Zwergal A, Kanclerski S, Haas SC, Kandemir JD, Huber R, et al. C/EBPbeta enhances NF-kappaB-associated signalling by reducing the level of IkappaB-alpha. Cellular Signalling 2009; 21:1918-1924.
42. Verstrepen L, Verhelst K, van Loo G, Carpentier I, Ley SC, Beyaert R. Expression, biological activities and mechanisms of action of A20 (TNFAIP3). Biochem Pharmacol 2010; 80: 2009-2020.
43. Bodur C, Kutuk O, Tezil T, Basaga H. Inactivation of Bcl-2 through IkappaB kinase (IKK)-dependent phosphorylation mediates apoptosis upon exposure to 4-hydroxynonenal (HNE). J Cell Physiol 2012;e-pubaheadof print21 January 2012;doi:10.1002/jcp.24057.
44. Ortis F, Naamane N, Flamez D, Ladriere L, Moore F, Cunha DA, et al. Cytokines interleukin-1beta and tumor necrosis factor-alpha regulate different transcriptional and alternative splicing networks in primary beta-cells. Diabetes 2010; 59: 358-374.
45. Ariyama Y, Tanaka Y, Shimizu H, Shimomura K, Okada S, Saito T, et al. The role of CHOP messenger RNA expression in the link between oxidative stress and apoptosis. Metabolism 2008; 57:1625-1635.
46. Satoh T, Abiru N, Kobayashi M, Zhou H, Nakamura K, Kuriya G, et al. CHOP deletion does not impact the development of diabetes but suppresses the early production of insulin autoantibody in the NOD mouse. Apoptosis 2011; 16: 438-448.
47. Eldor R, Yeffet A, Baum K, Doviner V, Amar D, Ben-Neriah Y, et al. Conditional and specific NF-κ B blockade protects pancreatic beta cells from diabetogenic agents. Proc Natl Acad Sci USA 2006;103: 5072-5077.
48. Rasschaert J, Ladriere L, Urbain M, Dogusan Z, Katabua B, Sato S, et al. Toll-like receptor 3 and STAT-1 contribute to double-stranded RNA + interferon-gamma-induced apoptosis in primary pancreatic beta-cells. J Biol Chem 2005; 280: 33984-33991.
49. Allagnat F, Alonso F, Martin D, Abderrahmani A, Waeber G, Haefliger JA. ICER-1gamma overexpression drives palmitate-mediated connexin36 down-regulation in insulin-secreting cells. J Biol Chem 2008; 283: 5226-5234.
50. Moore F, Colli ML, Cnop M, Esteve MI, Cardozo AK, Cunha DA et al. PTPN2, acandidate gene for type 1 diabetes, modulates interferon-gamma-induced pancreatic beta-cell apoptosis. Diabetes 2009; 58:1283-1291.