Cholesterol-induced hepatic inflammation does not underlie the predisposition to insulin resistance in dyslipidemic female LDL receptor knockout mice

Journal of Diabetes Research

Volumn 2015, Issue , 2015, Pages

  Gruben, Nanda ^a   Funke, Anouk ^a   Kloosterhuis, Niels J ^a   Schreurs, Marijke ^a   Sheedfar, Fareeba ^a   Havinga, Rick ^b   Houten, Sander M ^c   Shiri Sverdlov, Ronit ^d   Van De Sluis, Bart ^a   Kuivenhoven, Jan Albert ^a   Koonen, Debby P Y ^a   Hofker, Marten H ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

^d MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD68 ANTIGEN; CHOLESTEROL; GLUCOSE; INSULIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; TRIACYLGLYCEROL; GLUCOSE BLOOD LEVEL; LIPID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL DIET; DISEASE PREDISPOSITION; DYSLIPIDEMIA; FEMALE; GENE EXPRESSION; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; HEPATITIS; IMMUNOHISTOCHEMISTRY; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN TOLERANCE TEST; KNOCKOUT MOUSE; LIPID LIVER LEVEL; METABOLIC CLEARANCE RATE; MOUSE; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; PRIORITY JOURNAL; TRIACYLGLYCEROL BLOOD LEVEL; WILD TYPE MOUSE; ADIPOSE TISSUE; ANIMAL; BLOOD; C57BL MOUSE; CHEMISTRY; GENETICS; GLUCOSE CLAMP TECHNIQUE; GLUCOSE TOLERANCE TEST; INFLAMMATION; LIVER; MASS FRAGMENTOGRAPHY; METABOLISM; RISK FACTOR;

ADIPOSE TISSUE; ANIMALS; BLOOD GLUCOSE; CHOLESTEROL; DYSLIPIDEMIAS; FEMALE; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GLUCOSE CLAMP TECHNIQUE; GLUCOSE TOLERANCE TEST; INFLAMMATION; INSULIN RESISTANCE; LIPIDS; LIVER; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, LDL; RISK FACTORS; TRIGLYCERIDES;

EID: 84924529835     PISSN: 23146745     EISSN: 23146753     Source Type: Journal    
DOI: 10.1155/2015/956854     Document Type: Article

References (76)

1. M. F. Gregor and G. S. Hotamisligil, "inflammatory mechanisms in obesity," Annual Review of Immunology, Vol. 29, pp. 415-445, 2011.
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.
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.
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.
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.
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.
7. G. Steiner and M. Vranic, "Hyperinsulinemia and hypertriglyc-eridemia, a vicious cycle with atherogenic potential," International Journal of Obesity, Vol. 6, supplement 1, pp. 117-124, 1982.
8. U. Risérus, J. ä rnlöv, 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.
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.
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.
11. S. B. Biddinger, A. Hernandez-Ono, C. Rask-Madsen et al., "Hepatic insulin resistance is suficient to produce dyslipidemia and susceptibility to atherosclerosis," Cell Metabolism, Vol. 7, no. 2, pp. 125-134, 2008.
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.
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.
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.
15. V. Bieghs, P. J. van Gorp, K. Wouters et al., "Ldl receptor knockout 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.
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.
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.
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.
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.
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.
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.
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.
23. T. J. Aitman, I. F. Godsland, B. Farren, D. Crook, H. J. Wong, and J. Scott, "Deffects 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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
39. M. F. Gregor and G. S. Hotamisligil, "inflammatory mechanisms in obesity," Annual Review of Immunology, Vol. 29, pp. 415-445, 2011.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. G. Steiner and M. Vranic, "Hyperinsulinemia and hypertriglyc-eridemia, a vicious cycle with atherogenic potential," International Journal of Obesity, Vol. 6, supplement 1, pp. 117-124, 1982.
46. U. Risérus, J. ä rnlöv, 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.
47. 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.
48. 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.
49. S. B. Biddinger, A. Hernandez-Ono, C. Rask-Madsen et al., "Hepatic insulin resistance is suficient to produce dyslipidemia and susceptibility to atherosclerosis," Cell Metabolism, Vol. 7, no. 2, pp. 125-134, 2008.
50. 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.
51. 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.
52. 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.
53. V. Bieghs, P. J. van Gorp, K. Wouters et al., "Ldl receptor knockout 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.
54. 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.
55. 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.
56. 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.
57. 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.
58. 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.
59. 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.
60. A. M. F. Johnson and J. M. Olefsky, "The origins and drivers of insulin resistance," Cell, Vol. 152, no. 4, pp. 673-684, 2013.
61. T. J. Aitman, I. F. Godsland, B. Farren, D. Crook, H. J. Wong, and J. Scott, "Deffects 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.
62. 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.
63. 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.
64. 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.
65. 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.
66. 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.
67. 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.
68. 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.
69. 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.
70. 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.
71. 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.
72. 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.
73. 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.
74. 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.
75. 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.
76. 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.