Partial impairment of insulin receptor expression mimics fasting to prevent diet-induced fatty liver disease.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
29 04 2020
29 04 2020
Historique:
received:
06
06
2018
accepted:
19
03
2020
entrez:
1
5
2020
pubmed:
1
5
2020
medline:
30
7
2020
Statut:
epublish
Résumé
Excessive insulin signaling through the insulin receptor (IR) may play a role in the pathogenesis of diet-induced metabolic disease, including obesity and type 2 diabetes. Here we investigate whether heterozygous impairment of insulin receptor (IR) expression limited to peripheral, i.e. non-CNS, tissues of adult mice impacts the development of high-fat diet-induced metabolic deterioration. While exhibiting some features of insulin resistance, PerIRKO
Identifiants
pubmed: 32350271
doi: 10.1038/s41467-020-15623-z
pii: 10.1038/s41467-020-15623-z
pmc: PMC7190665
doi:
Substances chimiques
Receptor, Insulin
EC 2.7.10.1
Glucose
IY9XDZ35W2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2080Commentaires et corrections
Type : ErratumIn
Références
Despres, J. P. & Lemieux, I. Abdominal obesity and metabolic syndrome. Nature 444, 881–887 (2006).
pubmed: 17167477
Michelotti, G. A., Machado, M. V. & Diehl, A. M. NAFLD, NASH and liver cancer. Nat. Rev. Gastroenterol. Hepatol. 10, 656–665 (2013).
pubmed: 24080776
Saltiel, A. R. & Kahn, C. R. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414, 799–806 (2001).
pubmed: 11742412
Biddinger, S. B. & Kahn, C. R. From mice to men: insights into the insulin resistance syndromes. Annu Rev. Physiol. 68, 123–158 (2006).
pubmed: 16460269
Johnson, A. M. & Olefsky, J. M. The origins and drivers of insulin resistance. Cell 152, 673–684 (2013).
pubmed: 23415219
Michael, M. D. et al. Loss of insulin signaling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction. Mol. Cell 6, 87–97 (2000).
pubmed: 10949030
Merry, T. L. et al. High-fat-fed obese glutathione peroxidase 1-deficient mice exhibit defective insulin secretion but protection from hepatic steatosis and liver damage. Antioxid. Redox Signal. 20, 2114–2129 (2014).
pubmed: 24252128
Mehran, A. E. et al. Hyperinsulinemia drives diet-induced obesity independently of brain insulin production. Cell Metab. 16, 723–737 (2012). [pii].
pubmed: 23217255
Templeman, N. M. et al. Reduced circulating insulin enhances insulin sensitivity in old mice and extends lifespan. Cell Rep. 20, 451–463 (2017).
pubmed: 28700945
Page, M. M. et al. Reducing insulin via conditional partial gene ablation in adults reverses diet-induced weight gain. FASEB J. 32, 1196–1206 (2018).
pubmed: 29122848
Le Stunff, C. & Bougneres, P. Early changes in postprandial insulin secretion, not in insulin sensitivity, characterize juvenile obesity. Diabetes 43, 696–702 (1994).
pubmed: 8168647
Shanik, M. H. et al. Insulin resistance and hyperinsulinemia: is hyperinsulinemia the cart or the horse. Diabetes Care 31, S262–S268 (2008).
pubmed: 18227495
Gray, S. L., Donald, C., Jetha, A., Covey, S. D. & Kieffer, T. J. Hyperinsulinemia precedes insulin resistance in mice lacking pancreatic beta-cell leptin signaling. Endocrinology 151, 4178–4186 (2010).
pubmed: 20631001
Rizza, R. A., Mandarino, L. J., Genest, J., Baker, B. A. & Gerich, J. E. Production of insulin resistance by hyperinsulinaemia in man. Diabetologia 28, 70–75 (1985).
pubmed: 3884419
Koopmans, S. J., Ohman, L., Haywood, J. R., Mandarino, L. J. & DeFronzo, R. A. Seven days of euglycemic hyperinsulinemia induces insulin resistance for glucose metabolism but not hypertension, elevated catecholamine levels, or increased sodium retention in conscious normal rats. Diabetes 46, 1572–1578 (1997).
pubmed: 9313752
Semple, R. K. et al. Postreceptor insulin resistance contributes to human dyslipidemia and hepatic steatosis. J. Clin. Invest 119, 315–322 (2009).
pubmed: 19164855
pmcid: 2631303
Hoehn, K. L. et al. IRS1-independent defects define major nodes of insulin resistance. Cell Metab. 7, 421–433 (2008).
pubmed: 18460333
pmcid: 2443409
Zarse, K. et al. Impaired insulin/IGF1-signaling extends life span by promoting mitochondrial L-proline catabolism to induce a transient ROS signal. Cell Metab. 15, 451–465 (2012).
pubmed: 22482728
pmcid: 4844853
Blüher, M., Kahn, B. B. & Kahn, C. R. Extended longevity in mice lacking the insulin receptor in adipose tissue. Science 299, 572–574 (2003).
pubmed: 12543978
Clancy, D. J. et al. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292, 104–106 (2001).
pubmed: 11292874
Holzenberger, M. et al. IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421, 182–187 (2003).
pubmed: 12483226
Perry, R. J., Samuel, V. T., Petersen, K. F. & Shulman, G. I. The role of hepatic lipids in hepatic insulin resistance and type 2 diabetes. Nature 510, 84–91 (2014).
pubmed: 24899308
pmcid: 4489847
Brown, M. S. & Goldstein, J. L. Selective versus total insulin resistance: a pathogenic paradox. Cell Metab. 7, 95–96 (2008).
pubmed: 18249166
Merry, T. L. et al. Impairment of insulin signalling in peripheral tissue fails to extend murine lifespan. Aging Cell 16, 761–772 (2017).
pubmed: 28544360
pmcid: 5506415
Koch, L. et al. Central insulin action regulates peripheral glucose and fat metabolism in mice. J. Clin. Invest 118, 2132–2147 (2008).
pubmed: 18451994
pmcid: 2350427
Tokarz, V. L., MacDonald, P. E. & Klip, A. The cell biology of systemic insulin function. J. Cell Biol. 217, 2273–2289 (2018).
pubmed: 29622564
pmcid: 6028526
Hardie, D. G., Ross, F. A. & Hawley, S. A. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 13, 251–262 (2012).
pubmed: 22436748
pmcid: 5726489
Blüher, M. et al. Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance. Dev. Cell 3, 25–38 (2002).
pubmed: 12110165
Schwartz, M. W., Woods, S. C., Porte, D. Jr., Seeley, R. J. & Baskin, D. G. Central nervous system control of food intake. Nature 404, 661–671 (2000).
pubmed: 10766253
Pramfalk, C. et al. Fasting plasma insulin concentrations are associated with changes in hepatic fatty acid synthesis and partitioning prior to changes in liver fat content in healthy adults. Diabetes 65, 1858–1867 (2016).
pubmed: 27207513
Li, S., Brown, M. S. & Goldstein, J. L. Bifurcation of insulin signaling pathway in rat liver: mTORC1 required for stimulation of lipogenesis, but not inhibition of gluconeogenesis. Proc. Natl Acad. Sci. USA 107, 3441–3446 (2010).
pubmed: 20133650
Kucejova, B. et al. Hepatic mTORC1 opposes impaired insulin action to control mitochondrial metabolism in obesity. Cell Rep. 16, 508–519 (2016).
pubmed: 27346353
pmcid: 4951107
Berglund, E. D. et al. Glucagon and lipid interactions in the regulation of hepatic AMPK signaling and expression of PPARalpha and FGF21 transcripts in vivo. Am. J. Physiol. Endocrinol. Metab. 299, E607–E614 (2010).
pubmed: 20663988
pmcid: 2957865
Li, Y. et al. AMPK phosphorylates and inhibits SREBP activity to attenuate hepatic steatosis and atherosclerosis in diet-induced insulin-resistant mice. Cell Metab. 13, 376–388 (2011).
pubmed: 21459323
pmcid: 3086578
Seo, Y. S. et al. PPAR agonists treatment is effective in a nonalcoholic fatty liver disease animal model by modulating fatty-acid metabolic enzymes. J. Gastroenterol. Hepatol. 23, 102–109 (2008).
pubmed: 18171348
Harano, Y. et al. Fenofibrate, a peroxisome proliferator-activated receptor alpha agonist, reduces hepatic steatosis and lipid peroxidation in fatty liver Shionogi mice with hereditary fatty liver. Liver Int 26, 613–620 (2006).
pubmed: 16762007
Titchenell, P. M. et al. Direct hepatocyte insulin signaling is required for lipogenesis but is dispensable for the suppression of glucose production. Cell Metab. 23, 1154–1166 (2016).
pubmed: 27238637
pmcid: 4909537
Perry, R. J. et al. Hepatic acetyl CoA links adipose tissue inflammation to hepatic insulin resistance and type 2 diabetes. Cell 160, 745–758 (2015).
pubmed: 25662011
pmcid: 4498261
Titchenell, P. M., Chu, Q., Monks, B. R. & Birnbaum, M. J. Hepatic insulin signalling is dispensable for suppression of glucose output by insulin in vivo. Nat. Commun. 6, 7078 (2015).
pubmed: 25963408
pmcid: 4429930
Softic, S. et al. Lipodystrophy due to adipose tissue-specific insulin receptor knockout results in progressive NAFLD. Diabetes 65, 2187–2200 (2016).
pubmed: 27207510
pmcid: 4955986
Okada, T. et al. From the cover: insulin receptors in beta-cells are critical for islet compensatory growth response to insulin resistance. Proc. Natl Acad. Sci. USA 104, 8977–8982 (2007).
pubmed: 17416680
Brüning, J. C. et al. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol. Cell 2, 559–569 (1998).
pubmed: 9844629
Srere, P. A. Citrate synthase. Methods Enzymol. 13, 3–11 (1969).
Passonneau, J. V. & Lauderdale, V. R. A comparison of three methods of glycogen measurement in tissues. Anal. Biochem. 60, 405–412 (1974).
pubmed: 4844560
Lazzarino, G. et al. Single-sample preparation for simultaneous cellular redox and energy state determination. Anal. Biochem. 322, 51–59 (2003).
pubmed: 14705780
Rytka, J. M., Wueest, S., Schoenle, E. J. & Konrad, D. The portal theory supported by venous drainage-selective fat transplantation. Diabetes 60, 56–63 (2011).
pubmed: 20956499