Global profiling of double stranded RNA and IFN-γ-induced genes in rat pancreatic beta cells (original) (raw)

Global profiling of double stranded RNA- and IFN-?-induced genes in rat pancreatic beta cells

Diabetologia, 2003

Aims/hypothesis. Viral infections and local production of IFN-γ might contribute to beta-cell dysfunction/ death in Type 1 Diabetes. Double stranded RNA (dsRNA) accumulates in the cytosol of viral-infected cells, and exposure of purified rat beta cells to dsRNA (tested in the form of polyinosinic-polycytidylic acid, PIC) in combination with IFN-γ results in beta-cell dysfunction and apoptosis. To elucidate the molecular mechanisms involved in PIC + IFN-γ-effects, we determined the global profile of genes modified by these agents in primary rat beta cells. Methods. FACS-purified rat beta cells were cultured for 6 or 24 h in control condition or with IFN-γ, PIC or a combination of both agents. The gene expression profile was analysed in duplicate by high-density oligonucleotide arrays representing 5000 full-length genes and 3000 EST's. Changes of greater than or equal to 2.5-fold were considered as relevant. Results. Following a 6-or 24-h treatment with IFN-γ, PIC or IFN-γ and PIC, we observed changes in the expression of 51 to 189 genes. IFN-γ modified the expression of MHC-related genes, and also of genes in-volved in beta-cell metabolism, protein processing, cytokines and signal transduction. PIC affected preferentially the expression of genes related to cell adhesion, cytokines and dsRNA signal transduction, transcription factors and MHC. PIC and/or IFN-γ up-regulated the expression of several chemokines and cytokines that could contribute to mononuclear cell homing and activation during viral infection, while IFN-γ induced a positive feedback on its own signal transduction. PIC + IFN-γ inhibited insulin and GLUT-2 expression without modifying pdx-1 mRNA expression. Conclusion/interpretation. This study provides the first comprehensive characterization of the molecular responses of primary beta cells to dsRNA + IFN-γ, two agents that are probably present in the beta cell milieu during the course of virally-induced insulitis and Type 1 Diabetes. Based on these findings, we propose an integrated model for the molecular mechanisms involved in dsRNA + IFN-γ induced beta-cell dysfunction and death. [Diabetologia (2003[Diabetologia ( ) 46:1641[Diabetologia ( -1657

Mechanisms of β-Cell Death in Response to Double-Stranded (ds) RNA and Interferon-γ

The American Journal of Pathology, 2001

Viral infection is one environmental factor that has been implicated as a precipitating event that may initiate ␤-cell damage during the development of diabetes. This study examines the mechanisms by which the viral replicative intermediate, double-stranded (ds) RNA impairs ␤-cell function and induces ␤-cell death. The synthetic dsRNA molecule polyinosinicpolycytidylic acid (poly IC) stimulates ␤-cell DNA damage and apoptosis without impairing islet secretory function. In contrast, the combination of poly IC and interferon (IFN)-␥ stimulates DNA damage, apoptosis, and necrosis of islet cells, and this damage is associated with the inhibition of glucose-stimulated insulin secretion. Nitric oxide mediates the inhibitory and destructive actions of poly IC ؉ IFN-␥ on insulin secretion and islet cell necrosis. Inhibitors of nitric oxide synthase, aminoguanidine, and N G-monomethyl-L-arginine, attenuate poly IC ؉ IFN-␥-induced DNA damage to levels observed in response to poly IC alone, prevent islet cell necrosis, and prevent the inhibitory actions on glucose-stimulated insulin secretion. N G-monomethyl-L-arginine fails to prevent poly IC-and poly IC ؉ IFN-␥-induced islet cell apoptosis. PKR, the dsRNA-dependent protein kinase that mediates the antiviral response in infected cells, is required for poly IC-and poly IC ؉ IFN-␥-induced islet cell apoptosis, but not nitric oxide-mediated islet cell necrosis. Alone, poly IC fails to stimulate DNA damage in islets isolated from PKR-deficient mice; how-Supported by National Institutes of Health grants AI44458 (to J. A. C.) and AI42394 (R. J. K.).

Double-Stranded RNA Induces Pancreatic β-Cell Apoptosis by Activation of the Toll-Like Receptor 3 and Interferon Regulatory Factor 3 Pathways

Diabetes, 2008

OBJECTIVE— Viral infections contribute to the pathogenesis of type 1 diabetes. Viruses, or viral products such as double-stranded RNA (dsRNA), affect pancreatic β-cell survival and trigger autoimmunity by unknown mechanisms. We presently investigated the mediators and downstream effectors of dsRNA-induced β-cell death. RESEARCH DESIGN AND METHODS— Primary rat β-cells and islet cells from wild-type, toll-like receptor (TLR) 3, type I interferon receptor (IFNAR1), or interferon regulatory factor (IRF)-3 knockout mice were exposed to external dsRNA (external polyinosinic-polycytidylic acid [PICex]) or were transfected with dsRNA ([PICin]). RESULTS— TLR3 signaling mediated PICex-induced nuclear factor-κB (NF-κB) and IRF-3 activation and β-cell apoptosis. PICin activated NF-κB and IRF-3 in a TLR3-independent manner, induced eukaryotic initiation factor 2α phosphorylation, and triggered a massive production of interferon (IFN)-β. This contributed to β-cell death, as islet cells from IFNAR...

Double-stranded RNA Inhibits beta -Cell Function and Induces Islet Damage by Stimulating beta -Cell Production of Nitric Oxide

Journal of Biological Chemistry, 1999

Viral infection has been implicated as a triggering event that may initiate ␤-cell damage during the development of autoimmune diabetes. In this study, the effects of the viral replicative intermediate, doublestranded RNA (dsRNA) (in the form of synthetic polyinosinic-polycytidylic acid (poly IC)) on islet expression of inducible nitric oxide synthase (iNOS), production of nitric oxide, and islet function and viability were investigated. Treatment of rat islets with poly(IC) ؉ interferon-␥ (IFN-␥) stimulates the time-and concentrationdependent expression of iNOS and production of nitrite by rat islets. iNOS expression and nitrite production by rat islets in response to poly(IC) ؉ IFN-␥ correlate with an inhibition of insulin secretion and islet degeneration, effects that are prevented by the iNOS inhibitor aminoguanidine (AG). We have previously shown that poly(IC) ؉ IFN-␥ activates resident macrophages, stimulating iNOS expression, nitric oxide production and interleukin-1 (IL-1) release. In addition, in response to tumor necrosis factor-␣ (TNF-␣) ؉ lipopolysaccharide, activated resident macrophages mediate ␤-cell damage via intraislet IL-1 release followed by IL-1-induced iNOS expression by ␤-cells. The inhibitory and destructive effects of poly(IC) ؉ IFN-␥, however, do not appear to require resident macrophages. Treatment of macrophage-depleted rat islets for 40 h with poly(IC) ؉ IFN-␥ results in the expression of iNOS, production of nitrite, and inhibition of insulin secretion. The destructive effects of dsRNA ؉ IFN-␥ on islets appear to be mediated by a direct interaction with ␤-cells. Poly IC ؉ IFN-␥ stimulates iNOS expression and inhibits insulin secretion by primary ␤-cells purified by fluorescence-activated cell sorting. In addition, AG prevents the inhibitory effects of poly(IC) ؉ IFN-␥ on glucose-stimulated insulin secretion by ␤-cells. These results indicate that dsRNA ؉ IFN-␥ interacts directly with ␤-cells stimulating iNOS expression and inhibiting insulin secretion in a nitric oxide-dependent manner. These findings provide biochemical evidence for a novel mechanism by which viral infection may directly mediate the initial destruction of ␤-cells during the development of autoimmune diabetes.

Double-Stranded RNA Cooperates with Interferon-γ and IL-1β to Induce Both Chemokine Expression and Nuclear Factor-κB-Dependent Apoptosis in Pancreatic β-Cells: Potential Mechanisms for Viral-Induced Insulitis and β-Cell Death in Type 1 Diabetes Mellitus

Endocrinology, 2002

Viral infections may trigger the autoimmune assault leading to type 1 diabetes mellitus. Double-stranded RNA (dsRNA) is produced by many viruses during their replicative cycle. The dsRNA, tested as synthetic poly(IC) (PIC), in synergism with the proinflammatory cytokines interferon-␥ (IFN-␥) and/or IL-1␤, results in nitric oxide production, Fas expression, ␤-cell dysfunction, and death. Activation of the transcription nuclear factor-B (NF-B) is required for PIC-induced inducible nitric oxide synthase expression in ␤-cells, and we hypothesized that this transcription factor may also participate in PIC-induced Fas expression and ␤-cell apoptosis. This hypothesis, and the possibility that PIC induces expression of additional chemokines and cytokines (previously reported as NF-B dependent) in pancreatic ␤-cells, was investigated in the present study. We observed that the PIC-responsive region in the Fas promoter is located between nucleotides ؊223 and ؊54. Site-directed mutations at the NF-B and CCAAT/ enhancer binding protein-binding sites prevented PICinduced Fas promoter activity. Increased Fas promoter ac-tivity was paralleled by enhanced susceptibility of PIC ؉ cytokine-treated ␤-cells to apoptosis induced by Fas ligand.

MDA5 and PTPN2, two candidate genes for type 1 diabetes, modify pancreatic β-cell responses to the viral by-product double-stranded RNA

Human Molecular Genetics, 2009

b-Cell destruction in type 1 diabetes (T1D) is at least in part consequence of a 'dialog' between b-cells and immune system. This dialog may be affected by the individual's genetic background. We presently evaluated whether modulation of MDA5 and PTPN2, two candidate genes for T1D, affects b-cell responses to doublestranded RNA (dsRNA), a by-product of viral replication. These genes were selected following comparison between known candidate genes for T1D and genes expressed in pancreatic b-cells, as identified in previous array analysis. INS-1E cells and primary fluorescence-activated cell sorting-purified rat b-cells were transfected with small interference RNAs (siRNAs) targeting MDA5 or PTPN2 and subsequently exposed to intracellular synthetic dsRNA (polyinosinic-polycitidilic acid-PIC). Real-time RT-PCR, western blot and viability assays were performed to characterize gene/protein expression and viability. PIC increased MDA5 and PTPN2 mRNA expression, which was inhibited by the specific siRNAs. PIC triggered apoptosis in INS-1E and primary b-cells and this was augmented by PTPN2 knockdown (KD), although inhibition of MDA5 did not modify PICinduced apoptosis. In contrast, MDA5 silencing decreased PIC-induced cytokine and chemokine expression, although inhibition of PTPN2 induced minor or no changes in these inflammatory mediators. These findings indicate that changes in MDA5 and PTPN2 expression modify b-cell responses to dsRNA. MDA5 regulates inflammatory signals, whereas PTPN2 may function as a defence mechanism against pro-apoptotic signals generated by dsRNA. These two candidate genes for T1D may thus modulate b-cell apoptosis and/or local release of inflammatory mediators in the course of a viral infection by acting, at least in part, at the pancreatic b-cell level.

Identification of IL-1β-induced messenger RNAs in rat pancreatic beta cells by differential display of messenger RNA

Diabetologia, 1999

Type I (insulin-dependent) diabetes mellitus is an autoimmune disease, where T-cells and macrophages invade the islets of Langerhans and lead to specific destruction of pancreatic beta cells . Cytokines such as interleukin-1b (IL-1b) and interferon-g are released by these infiltrating mononuclear cells and can contribute to beta-cell death . Recent observations indicate that genes and proteins activated by the beta cells are crucial to determine whether these cells will survive or undergo apoptosis when faced with immune-mediated cell damage [4±6]. We and others have previously adopted the ªcandidate geneº approach to characterize beta-cell responses to immune-mediated assaults and observed that cytokines induce the expression of different genes in rodent and human pancreatic islets, encoding both proteins involved in beta-cell damage and Diabetologia (1999) 42: 1199±1203