Table of Contents Author Guidelines Submit a Manuscript
Journal of Diabetes Research
Volume 2015, Article ID 956854, 12 pages
http://dx.doi.org/10.1155/2015/956854
Research Article

Cholesterol-Induced Hepatic Inflammation Does Not Underlie the Predisposition to Insulin Resistance in Dyslipidemic Female LDL Receptor Knockout Mice

1Molecular Genetics Section, Department of Pediatrics, University Medical Center Groningen, University of Groningen, Antonius Deusinglaan 1, 9713 AV Groningen, Netherlands
2Center for Liver, Digestive and Metabolic Diseases, Department of Pediatrics, University Medical Center Groningen, University of Groningen, Hanzeplein 1, 9713 GZ Groningen, Netherlands
3Academic Medical Center, Laboratory Genetic Metabolic Diseases, Meibergdreef 9, 1105 AZ Amsterdam, Netherlands
4Department of Molecular Genetics, Maastricht University, P.O. Box 616, 6200 MD Maastricht, Netherlands

Received 30 November 2014; Revised 10 February 2015; Accepted 14 February 2015

Academic Editor: Kazuya Yamagata

Copyright © 2015 Nanda Gruben et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. F. Gregor and G. S. Hotamisligil, “Inflammatory mechanisms in obesity,” Annual Review of Immunology, vol. 29, pp. 415–445, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. N. Gruben, R. Shiri-Sverdlov, D. P. Y. Koonen, and M. H. Hofker, “Nonalcoholic fatty liver disease: a main driver of insulin resistance or a dangerous liaison?” Biochimica et Biophysica Acta—Molecular Basis of Disease, vol. 1842, no. 11, pp. 2329–2343, 2014. View at Publisher · View at Google Scholar
  3. M. Aparicio-Vergara, P. P. H. Hommelberg, M. Schreurs et al., “Tumor necrosis factor receptor 1 gain-of-function mutation aggravates nonalcoholic fatty liver disease but does not cause insulin resistance in a murine model,” Hepatology, vol. 57, no. 2, pp. 566–576, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Funke, M. Schreurs, M. Aparicio-Vergara et al., “Cholesterol-induced hepatic inflammation does not contribute to the development of insulin resistance in male LDL receptor knockout mice,” Atherosclerosis, vol. 232, no. 2, pp. 390–396, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. N. Lanthier, O. Molendi-Coste, P. D. Cani, N. van Rooijen, Y. Horsmans, and I. A. Leclercq, “Kupffer cell depletion prevents but has no therapeutic effect on metabolic and inflammatory changes induced by a high-fat diet,” The FASEB Journal, vol. 25, no. 12, pp. 4301–4311, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. Z. Papackova, E. Palenickova, H. Dankova et al., “Kupffer cells ameliorate hepatic insulin resistance induced by high-fat diet rich in monounsaturated fatty acids: the evidence for the involvement of alternatively activated macrophages,” Nutrition and Metabolism, vol. 9, article 22, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. G. Steiner and M. Vranic, “Hyperinsulinemia and hypertriglyceridemia, a vicious cycle with atherogenic potential,” International Journal of Obesity, vol. 6, supplement 1, pp. 117–124, 1982. View at Google Scholar · View at Scopus
  8. U. Risérus, J. Ärnlöv, and L. Berglund, “Long-term predictors of insulin resistance: role of lifestyle and metabolic factors in middle-aged men,” Diabetes Care, vol. 30, no. 11, pp. 2928–2933, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. P. W. F. Wilson, R. B. D'Agostino, C. S. Fox, L. M. Sullivan, and J. B. Meigs, “Type 2 diabetes risk in persons with dysglycemia: the framingham offspring study,” Diabetes Research and Clinical Practice, vol. 92, no. 1, pp. 124–127, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. P. Anagnostis, V. G. Athyros, A. Karagiannis, and D. P. Mikhailidis, “Impact of statins on glucose metabolism—a matter of debate,” The American Journal of Cardiology, vol. 107, no. 12, p. 1866, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. S. B. Biddinger, A. Hernandez-Ono, C. Rask-Madsen et al., “Hepatic insulin resistance is sufficient to produce dyslipidemia and susceptibility to atherosclerosis,” Cell Metabolism, vol. 7, no. 2, pp. 125–134, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. S. A. Schreyer, C. Vick, T. C. Lystig, P. Mystkowski, and R. C. LeBoeuf, “LDL receptor but not apolipoprotein E deficiency increases diet-induced obesity and diabetes in mice,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 282, pp. E207–E214, 2002. View at Google Scholar
  13. S. Ishibashi, M. S. Brown, J. L. Goldstein, R. D. Gerard, R. E. Hammer, and J. Herz, “Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery,” The Journal of Clinical Investigation, vol. 92, no. 2, pp. 883–893, 1993. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Wouters, P. J. van Gorp, V. Bieghs et al., “Dietary cholesterol, rather than liver steatosis, leads to hepatic inflammation in hyperlipidemic mouse models of nonalcoholic steatohepatitis,” Hepatology, vol. 48, no. 2, pp. 474–486, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. V. Bieghs, P. J. van Gorp, K. Wouters et al., “Ldl receptor knock-out mice are a physiological model particularly vulnerable to study the onset of inflammation in non-alcoholic fatty liver disease,” PLoS ONE, vol. 7, no. 1, Article ID e30668, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. N. Pamir, T. S. McMillen, K. J. Kaiyala, M. W. Schwartz, and R. C. LeBoeuf, “Receptors for tumor necrosis factor-α play a protective role against obesity and alter adipose tissue macrophage status,” Endocrinology, vol. 150, no. 9, pp. 4124–4134, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Grefhorst, T. H. van Dijk, A. Hammer et al., “Differential effects of pharmacological liver X receptor activation on hepatic and peripheral insulin sensitivity in lean and ob/ob mice,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 289, no. 5, pp. E829–E838, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. T. H. van Dijk, T. S. Boer, R. Havinga, F. Stellaard, F. Kuipers, and D.-J. Reijngoud, “Quantification of hepatic carbohydrate metabolism in conscious mice using serial blood and urine spots,” Analytical Biochemistry, vol. 322, no. 1, pp. 1–13, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. E. G. Bligh and W. J. Dyer, “A rapid method of total lipid extraction and purification.,” Canadian Journal of Biochemistry and Physiology, vol. 37, no. 8, pp. 911–917, 1959. View at Publisher · View at Google Scholar · View at Scopus
  20. J. I. Odegaard and A. Chawla, “Pleiotropic actions of insulin resistance and inflammation in metabolic homeostasis,” Science, vol. 339, no. 6116, pp. 172–177, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. V. T. Samuel and G. I. Shulman, “Mechanisms for insulin resistance: common threads and missing links,” Cell, vol. 148, no. 5, pp. 852–871, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. A. M. F. Johnson and J. M. Olefsky, “The origins and drivers of insulin resistance,” Cell, vol. 152, no. 4, pp. 673–684, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. T. J. Aitman, I. F. Godsland, B. Farren, D. Crook, H. J. Wong, and J. Scott, “Defects of insulin action on fatty acid and carbohydrate metabolism in familial combined hyperlipidemia,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 17, no. 4, pp. 748–754, 1997. View at Publisher · View at Google Scholar · View at Scopus
  24. S. J. H. Bredie, C. J. J. Tack, P. Smits, and A. F. H. Stalenhoef, “Nonobese patients with familial combined hyperlipidemia are insulin resistant compared with their nonaffected relatives,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 17, no. 7, pp. 1465–1471, 1997. View at Google Scholar · View at Scopus
  25. I. Skoumas, C. Masoura, C. Pitsavos et al., “Evidence that non-lipid cardiovascular risk factors are associated with high prevalence of coronary artery disease in patients with heterozygous familial hypercholesterolemia or familial combined hyperlipidemia,” International Journal of Cardiology, vol. 121, no. 2, pp. 178–183, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Skoumas, L. Papadimitriou, C. Pitsavos et al., “Metabolic syndrome prevalence and characteristics in Greek adults with familial combined hyperlipidemia,” Metabolism: Clinical and Experimental, vol. 56, no. 1, pp. 135–141, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. M. C. G. J. Brouwers, C. J. H. van der Kallen, N. C. Schaper, M. M. J. van Greevenbroek, and C. D. A. Stehouwer, “Five-year incidence of type 2 diabetes mellitus in patients with familial combined hyperlipidaemia,” Netherlands Journal of Medicine, vol. 68, no. 4, pp. 163–167, 2010. View at Google Scholar · View at Scopus
  28. N. Li, M. R. van der Sijde, S. J. L. Bakker et al., “Pleiotropic effects of lipid genes on plasma glucose, HbA1c, and HOMA-IR levels,” Diabetes, vol. 63, no. 9, pp. 3149–3158, 2014. View at Publisher · View at Google Scholar
  29. M. C. Arkan, A. L. Hevener, F. R. Greten et al., “IKK-beta links inflammation to obesity-induced insulin resistance,” Nature Medicine, vol. 11, no. 2, pp. 191–198, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. D. Cai, M. Yuan, D. F. Frantz et al., “Local and systemic insulin resistance resulting from hepatic activation of IKK-β and NF-κB,” Nature Medicine, vol. 11, no. 2, pp. 183–190, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. O. Osborn and J. M. Olefsky, “The cellular and signaling networks linking the immune system and metabolism in disease,” Nature Medicine, vol. 18, no. 3, pp. 363–374, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. W. Huang, A. Metlakunta, N. Dedousis et al., “Depletion of liver kupffer cells prevents the development of diet-induced hepatic steatosis and insulin resistance,” Diabetes, vol. 59, no. 2, pp. 347–357, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. A. M. Neyrinck, P. D. Cani, E. M. Dewulf, F. De Backer, L. B. Bindels, and N. M. Delzenne, “Critical role of Kupffer cells in the management of diet-induced diabetes and obesity,” Biochemical and Biophysical Research Communications, vol. 385, no. 3, pp. 351–356, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. A. H. Clementi, A. M. Gaudy, N. van Rooijen, R. H. Pierce, and R. A. Mooney, “Loss of Kupffer cells in diet-induced obesity is associated with increased hepatic steatosis, STAT3 signaling, and further decreases in insulin signaling,” Biochimica et Biophysica Acta—Molecular Basis of Disease, vol. 1792, no. 11, pp. 1062–1072, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. S. Lee, P. Li, J. Y. Huh et al., “Inflammation is necessary for long-term but not short-term high-fat diet-induced insulin resistance,” Diabetes, vol. 60, no. 10, pp. 2474–2483, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Subramanian, C. Y. Han, T. Chiba et al., “Dietary cholesterol worsens adipose tissue macrophage accumulation and atherosclerosis in obese LDL receptor-deficient mice,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 28, no. 4, pp. 685–691, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. G. Sabio, M. Das, A. Mora et al., “A stress signaling pathway in adipose tissue regulates hepatic insulin resistance,” Science, vol. 322, no. 5907, pp. 1539–1543, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Monetti, N. Nagaraj, K. Sharma, and M. Mann, “Large-scale phosphosite quantification in tissues by a spike-in SILAC method,” Nature Methods, vol. 8, no. 8, pp. 655–658, 2011. View at Publisher · View at Google Scholar · View at Scopus