Involvement of long non-coding RNAs in beta cell failure at the onset of type 1 diabetes in NOD mice

Diabetologia

Volumn 58, Issue 8, 2015, Pages 1827-1835

  Motterle, Anna ^a   Gattesco, Sonia ^a   Caille, Dorothée ^b   Meda, Paolo ^b   Regazzi, Romano ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Apoptosis; Beta cell; Cytokines; Diabetes; Islet; lncRNAs; Long non coding RNAs

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; GAMMA INTERFERON; GLUCAGON LIKE PEPTIDE 1; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 15; INTERLEUKIN 1BETA; JANUS KINASE 3; LONG UNTRANSLATED RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; RNA 18S; STAT1 PROTEIN; STAT2 PROTEIN; STAT3 PROTEIN; STAT4 PROTEIN; INSULIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DAMAGE; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; MICROARRAY ANALYSIS; MIN6 CELL LINE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; CELL LINE; DISEASE COURSE; IMPAIRED GLUCOSE TOLERANCE; METABOLISM; NONOBESE DIABETIC MOUSE; PANCREAS ISLET; PATHOLOGY;

ANIMALS; CELL LINE; DIABETES MELLITUS, TYPE 1; DISEASE PROGRESSION; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE; MICE, INBRED NOD; PREDIABETIC STATE; RNA, LONG NONCODING;

EID: 84937512955     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-015-3641-5     Document Type: Article

References (49)

1. Eizirik DL, Colli ML, Ortis F (2009) The role of inflammation in insulitis and beta-cell loss in type 1 diabetes. Nat Rev Endocrinol 5:219–226
2. Donath MY, Storling J, Berchtold LA, Billestrup N, Mandrup-Poulsen T (2008) Cytokines and beta-cell biology: from concept to clinical translation. Endocr Rev 29:334–350
3. Pipeleers D, Hoorens A, Marichal-Pipeleers M, van de Casteele M, Bouwens L, Ling Z (2001) Role of pancreatic beta-cells in the process of beta-cell death. Diabetes 50(Suppl 1):S52–S57
4. Kaminitz A, Stein J, Yaniv I, Askenasy N (2007) The vicious cycle of apoptotic beta-cell death in type 1 diabetes. Immunol Cell Biol 85:582–589
5. Kutlu B, Cardozo AK, Darville MI et al (2003) Discovery of gene networks regulating cytokine-induced dysfunction and apoptosis in insulin-producing INS-1 cells. Diabetes 52:2701–2719
6. Ortis F, Naamane N, Flamez D et al (2010) Cytokines interleukin-1beta and tumor necrosis factor-alpha regulate different transcriptional and alternative splicing networks in primary beta-cells. Diabetes 59:358–374
7. Eizirik DL, Sammeth M, Bouckenooghe T et al (2012) The human pancreatic islet transcriptome: expression of candidate genes for type 1 diabetes and the impact of pro-inflammatory cytokines. PLoS Genet 8:e1002552
8. Guay C, Jacovetti C, Nesca V, Motterle A, Tugay K, Regazzi R (2012) Emerging roles of non-coding RNAs in pancreatic beta-cell function and dysfunction. Diabetes Obes Metab 14(Suppl 3):12–21
9. Roggli E, Britan A, Gattesco S et al (2010) Involvement of microRNAs in the cytotoxic effects exerted by proinflammatory cytokines on pancreatic beta-cells. Diabetes 59:978–986
10. Roggli E, Gattesco S, Caille D et al (2012) Changes in microRNA expression contribute to pancreatic beta-cell dysfunction in prediabetic NOD mice. Diabetes 61:1742–1751
11. Carninci P, Kasukawa T, Katayama S et al (2005) The transcriptional landscape of the mammalian genome. Science 309:1559–1563
12. Mattick JS (2009) The genetic signatures of noncoding RNAs. PLoS Genet 5:e1000459
13. Consortium EP (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489:57–74
14. Wang KC, Chang HY (2011) Molecular mechanisms of long noncoding RNAs. Mol Cell 43:904–914
15. Guttman M, Donaghey J, Carey BW et al (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477:295–300
16. Khaitan D, Dinger ME, Mazar J et al (2011) The melanoma-upregulated long noncoding RNA SPRY4-IT1 modulates apoptosis and invasion. Cancer Res 71:3852–3862
17. Ginger MR, Shore AN, Contreras A et al (2006) A noncoding RNA is a potential marker of cell fate during mammary gland development. Proc Natl Acad Sci U S A 103:5781–5786
18. Paralkar VR, Weiss MJ (2011) A new 'Linc' between noncoding RNAs and blood development. Genes Dev 25:2555–2558
19. Tripathi V, Ellis JD, Shen Z et al (2010) The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell 39:925–938
20. Wapinski O, Chang HY (2011) Long noncoding RNAs and human disease. Trends Cell Biol 21:354–361
21. Batista PJ, Chang HY (2013) Long noncoding RNAs: cellular address codes in development and disease. Cell 152:1298–1307
22. Debussche X, Lormeau B, Boitard C, Toublanc M, Assan R (1994) Course of pancreatic beta cell destruction in prediabetic NOD mice: a histomorphometric evaluation. Diabetes Metab 20:282–290
23. Gotoh M, Maki T, Satomi S et al (1987) Reproducible high yield of rat islets by stationary in vitro digestion following pancreatic ductal or portal venous collagenase injection. Transplantation 43:725–730
24. Lilla V, Webb G, Rickenbach K et al (2003) Differential gene expression in well-regulated and dysregulated pancreatic beta-cell (MIN6) sublines. Endocrinology 144:1368–1379
25. Marr RA, Rockenstein E, Mukherjee A et al (2003) Neprilysin gene transfer reduces human amyloid pathology in transgenic mice. J Neurosci 23:1992–1996
26. Moore F, Naamane N, Colli ML et al (2011) STAT1 is a master regulator of pancreatic β-cell apoptosis and islet inflammation. J Biol Chem 286:929–941
27. Wolden-Kirk H, Rondas D, Bugliani M et al (2014) Discovery of molecular pathways mediating 1,25-dihydroxyvitamin D3 protection against cytokine-induced inflammation and damage of human and male mouse islets of Langerhans. Endocrinology 155:736–747
28. Carrero JA, Calderon B, Towfic F, Artyomov MN, Unanue ER (2013) Defining the transcriptional and cellular landscape of type 1 diabetes in the NOD mouse. PLoS One 8:e59701
29. Norlin S, Ahlgren U, Edlund H (2005) Nuclear factor-{kappa}B activity in β-cells is required for glucose-stimulated insulin secretion. Diabetes 54:125–132
30. Cardozo AK, Heimberg H, Heremans Y et al (2001) A comprehensive analysis of cytokine-induced and nuclear factor-kappa B-dependent genes in primary rat pancreatic beta cells. J Biol Chem 276:48879–48886
31. Ortis F, Pirot P, Naamane N et al (2008) 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 51:1213–1225
32. Ortis F, Cardozo AK, Crispim D, Storling J, Mandrup-Poulsen T, Eizirik DL (2006) Cytokine-induced proapoptotic gene expression in insulin-producing cells is related to rapid, sustained, and nonoscillatory nuclear factor-kappaB activation. Mol Endocrinol 20:1867–1879
33. Kurrer MO, Pakala SV, Hanson HL, Katz JD (1997) Beta cell apoptosis in T cell-mediated autoimmune diabetes. Proc Natl Acad Sci U S A 94:213–218
34. O'Brien BA, Harmon BV, Cameron DP, Allan DJ (1997) Apoptosis is the mode of beta-cell death responsible for the development of IDDM in the nonobese diabetic (NOD) mouse. Diabetes 46:750–757
35. Derrien T, Johnson R, Bussotti G et al (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22:1775–1789
36. Ravasi T, Suzuki H, Pang KC et al (2006) Experimental validation of the regulated expression of large numbers of non-coding RNAs from the mouse genome. Genome Res 16:11–19
37. Ize-Ludlow D, Lightfoot YL, Parker M et al (2011) Progressive erosion of beta-cell function precedes the onset of hyperglycemia in the NOD mouse model of type 1 diabetes. Diabetes 60:2086–2091
38. Eizirik DL, Mandrup-Poulsen T (2001) A choice of death—the signal-transduction of immune-mediated beta-cell apoptosis. Diabetologia 44:2115–2133
39. Gurzov EN, Eizirik DL (2011) Bcl-2 proteins in diabetes: mitochondrial pathways of beta-cell death and dysfunction. Trends Cell Biol 21:424–431
40. Eizirik DL, Cardozo AK, Cnop M (2008) The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev 29:42–61
41. Hayden MS, Ghosh S (2004) Signaling to NF-kappaB. Genes Dev 18:2195–2224
42. Giannoukakis N, Rudert WA, Trucco M, Robbins PD (2000) Protection of human islets from the effects of interleukin-1beta by adenoviral gene transfer of an Ikappa B repressor. J Biol Chem 275:36509–36513
43. Heimberg H, Heremans Y, Jobin C et al (2001) Inhibition of cytokine-induced NF-kappaB activation by adenovirus-mediated expression of a NF-kappaB super-repressor prevents beta-cell apoptosis. Diabetes 50:2219–2224
44. Eldor R, Yeffet A, Baum K et al (2006) Conditional and specific NF-kappaB blockade protects pancreatic beta cells from diabetogenic agents. Proc Natl Acad Sci U S A 103:5072–5077
45. Gough DJ, Levy DE, Johnstone RW, Clarke CJ (2008) IFNgamma signaling-does it mean JAK-STAT? Cytokine Growth Factor Rev 19:383–394
46. Lin Y, Jamison S, Lin W (2012) Interferon-gamma activates nuclear factor-kappa B in oligodendrocytes through a process mediated by the unfolded protein response. PLoS One 7:e36408
47. Rimbach G, Valacchi G, Canali R, Virgili F (2000) Macrophages stimulated with IFN-gamma activate NF-kappa B and induce MCP-1 gene expression in primary human endothelial cells. Mol Cell Biol Res Commun 3:238–242
48. Ku GM, Kim H, Vaughn IW et al (2012) Research resource: RNA-Seq reveals unique features of the pancreatic beta-cell transcriptome. Mol Endocrinol 26:1783–1792
49. Cabili MN, Trapnell C, Goff L et al (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25:1915–1927