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IRS-2 mediates the antiapoptotic effect of insulin in neonatal hepatocytes
Angela M Valverde1, Isabel Fabregat, Deborah J Burks
1Instituto de Bioquímica/Departamento de Bioquímica y Biología Molecular II, Centro Mixto CSIC/UCM, Facultad de Farmacia, Universidad Complutense, Madrid, Spain. valverde@farm.ucm.es
Abstract:
To assess the role of insulin action and inaction in the liver, immortalized hepatocyte cell lines have been generated from insulin receptor substrate (IRS)-2(-/-) and wild-type mice. Using this model, we have recently demonstrated that the lack of IRS-2 in neonatal hepatocytes resulted in insulin resistance. In the current study, we show that immortalized neonatal hepatocytes undergo apoptosis on serum withdrawal, with caspase-3 activation and DNA laddering occurring earlier in the absence of IRS-2. Insulin rescued wild-type hepatocytes from serum withdrawal-induced caspase-3 activation and DNA fragmentation in a dose-dependent manner, but it failed to rescue hepatocytes lacking IRS-2. In IRS-2(-/-) cells, insulin failed to phosphorylate Bad. Furthermore, in these cells, insulin was unable to translocate Foxo1 from the nucleus to the cytosol. Adenoviral infection of wild-type cells with constitutively active Foxo1 (ADA) induced caspase-8 and caspase-3 activities, proapoptotic gene expression, DNA laddering and apoptosis. Dominant negative Foxo1 regulated the whole pathway in an opposite manner. Prolonged insulin treatment (24 hours) increased expression of antiapoptotic genes (Bcl-xL), downregulated proapoptotic genes (Bim and nuclear Foxo1), and decreased caspase-3 activity in wild-type hepatocytes but not in IRS-2(-/-) cells. Infection of IRS-2(-/-) hepatocytes with adenovirus encoding IRS-2 reconstituted phosphatidylinositol 3-kinase (PI 3-kinase)/Akt/Foxo1 signaling, restored pro- and antiapoptotic gene expression, and decreased caspase-3 activity in response to insulin, thereby blocking apoptosis. In conclusion, IRS-2 signaling is specifically required through PIP3 generation to mediate the survival effects of insulin. Epidermal growth factor, via PIP3/Akt/Foxo1 phosphorylation, was able to rescue IRS-2(-/-) hepatocytes from serum withdrawal-induced apoptosis, modulating pro- and anti-apoptotic gene expression and downregulating caspase-3 activity.
Insights
Insulin receptor substrate-2 (IRS-2) is crucial for insulin's liver cell survival signals. Its absence triggers apoptosis, which insulin cannot prevent, highlighting IRS-2's essential role in insulin's protective effects.
Area of Science:
- Cell Biology
- Molecular Biology
- Endocrinology
Background:
- Insulin resistance is linked to impaired insulin signaling in hepatocytes.
- Insulin receptor substrate-2 (IRS-2) plays a key role in insulin signal transduction.
- The role of IRS-2 in hepatocyte survival signaling requires further elucidation.
Purpose of the Study:
- To investigate the role of IRS-2 in mediating insulin's anti-apoptotic effects in hepatocytes.
- To determine the downstream signaling pathways involved in IRS-2-dependent hepatocyte survival.
Main Methods:
- Generated immortalized hepatocyte cell lines from IRS-2(-/-) and wild-type mice.
- Induced apoptosis via serum withdrawal and assessed caspase activation and DNA fragmentation.
- Utilized adenoviral vectors to express constitutively active or dominant-negative Foxo1, and to reintroduce IRS-2.
- Measured protein phosphorylation (e.g., Bad), protein localization (e.g., Foxo1), and gene expression (e.g., Bcl-xL, Bim).
Main Results:
- Hepatocytes lacking IRS-2 exhibited accelerated apoptosis upon serum withdrawal, characterized by earlier caspase-3 activation and DNA laddering.
- Insulin protected wild-type hepatocytes from apoptosis but failed to rescue IRS-2(-/-) hepatocytes.
- In IRS-2(-/-) cells, insulin did not phosphorylate Bad or promote Foxo1 nuclear export.
- Reconstitution of IRS-2 in IRS-2(-/-) hepatocytes restored insulin's ability to promote survival signaling and inhibit apoptosis.
- Epidermal growth factor (EGF) could rescue IRS-2(-/-) hepatocytes, indicating a parallel survival pathway.
Conclusions:
- IRS-2 signaling is essential for mediating insulin's survival effects in hepatocytes, specifically through phosphatidylinositol 3-kinase (PI 3-kinase)/Akt/Foxo1 pathway activation.
- The absence of IRS-2 renders hepatocytes susceptible to apoptosis, a process insulin cannot counteract.
- IRS-2 is critical for regulating the expression of pro- and anti-apoptotic genes, thereby controlling cell fate.
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