Dietary iron overload induces visceral adipose tissue insulin resistance

American Journal of Pathology

Volumn 182, Issue 6, 2013, Pages 2254-2263

  Dongiovanni, Paola ^a   Ruscica, Massimiliano ^b   Rametta, Raffaela ^a   Recalcati, Stefania ^b   Steffani, Liliana ^b   Gatti, Stefano ^a   Girelli, Domenico ^c   Cairo, Gaetano ^b   Magni, Paolo ^b   Fargion, Silvia ^a   Valenti, Luca ^a,c  

^a FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF VERONA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTOKINE; HEPCIDIN; IRON; LIPOPROTEIN LIPASE; PROTEIN KINASE B; SUPPRESSOR OF CYTOKINE SIGNALING 3; TRIACYLGLYCEROL;

ADIPOCYTE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EPIDIDYMIS FAT; GENE EXPRESSION; GLUCOSE METABOLISM; HYPERTRIGLYCERIDEMIA; INSULIN RESISTANCE; INSULIN TOLERANCE TEST; INTRAABDOMINAL FAT; IRON INTAKE; IRON METABOLISM; IRON OVERLOAD; IRON THERAPY; LIPID METABOLISM; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; UPREGULATION;

ADIPOCYTES; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BLOOD GLUCOSE; GENE EXPRESSION REGULATION; HYPERTRIGLYCERIDEMIA; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; IRON; IRON OVERLOAD; IRON, DIETARY; LIPID METABOLISM; LIVER; MALE; MICE; MICE, INBRED C57BL; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84878248460     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.02.019     Document Type: Article

References (37)

1. P. Dongiovanni, A.L. Fracanzani, S. Fargion, and L. Valenti Iron in fatty liver and in the metabolic syndrome: a promising therapeutic target J Hepatol 55 2011 920 932
2. L. Valenti, A.L. Fracanzani, E. Bugianesi, P. Dongiovanni, E. Galmozzi, E. Vanni, E. Canavesi, E. Lattuada, G. Roviaro, G. Marchesini, and S. Fargion HFE genotype, parenchymal iron accumulation, and liver fibrosis in patients with nonalcoholic fatty liver disease Gastroenterology 138 2010 905 912
3. S.V. Shah, and V.A. Fonseca Iron and diabetes revisited Diabetes Care 34 2011 1676 1677
4. L. Valenti, A.L. Fracanzani, P. Dongiovanni, E. Bugianesi, G. Marchesini, P. Manzini, E. Vanni, and S. Fargion Iron depletion by phlebotomy improves insulin resistance in patients with nonalcoholic fatty liver disease and hyperferritinemia: evidence from a case-control study Am J Gastroenterol 102 2007 1251 1258
5. A. Pietrangelo Hemochromatosis: an endocrine liver disease Hepatology 46 2007 1291 1301
6. E. Nemeth, M.S. Tuttle, J. Powelson, M.B. Vaughn, A. Donovan, D.M. Ward, T. Ganz, and J. Kaplan Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization Science 306 2004 2090 2093
7. E. Aigner, I. Theurl, M. Theurl, D. Lederer, H. Haufe, O. Dietze, M. Strasser, C. Datz, and G. Weiss Pathways underlying iron accumulation in human nonalcoholic fatty liver disease Am J Clin Nutr 87 2008 1374 1383
8. J.M. Fernandez-Real, J.M. Moreno, B. Chico, A. Lopez-Bermejo, and W. Ricart Circulating visfatin is associated with parameters of iron metabolism in subjects with altered glucose tolerance Diabetes Care 30 2007 616 621
9. A. Green, R. Basile, and J.M. Rumberger Transferrin and iron induce insulin resistance of glucose transport in adipocytes Metabolism 55 2006 1042 1045
10. N. Wlazlo, M.M.J. van Greevenbroek, I. Ferreira, E.H.J.M. Jansen, E.J. Feskens, C.J.H. van der Kallen, C.G. Schalkwijk, B. Bravenboer, and C.D. Stehouwer Iron metabolism is associated with adipocyte insulin resistance and plasma adiponectin Diabetes Care 2012 [ePub ahead of print]
11. J. Huang, J.S. Gabrielsen, R.C. Cooksey, B. Luo, L.G. Boros, D.L. Jones, H.A. Jouihan, Y. Soesanto, L. Knecht, M.W. Hazel, J.P. Kushner, and D.A. McClain Increased glucose disposal and AMP-dependent kinase signaling in a mouse model of hemochromatosis J Biol Chem 282 2007 37501 37507
12. J. Huang, D. Jones, B. Luo, M. Sanderson, J. Soto, E.D. Abel, R.C. Cooksey, and D.A. McClain Iron overload and diabetes risk: a shift from glucose to fatty acid oxidation and increased hepatic glucose production in a mouse model of hereditary hemochromatosis Diabetes 60 2010 80 87
13. Y. Minamiyama, S. Takemura, S. Kodai, H. Shinkawa, T. Tsukioka, H. Ichikawa, Y. Naito, T. Yoshikawa, and S. Okada Iron restriction improves type 2 diabetes mellitus in Otsuka Long-Evans Tokushima fatty rats Am J Physiol Endocrinol Metab 298 2010 E1140 E1149
14. R.C. Cooksey, D. Jones, S. Gabrielsen, J. Huang, J.A. Simcox, B. Luo, Y. Soesanto, H. Rienhoff, E.D. Abel, and D.A. McClain Dietary iron restriction or iron chelation protects from diabetes and loss of beta-cell function in the obese (ob/ob lep-/-) mouse Am J Physiol Endocrinol Metab 298 2010 E1236 1243
15. P. Dongiovanni, L. Valenti, A. Ludovica Fracanzani, S. Gatti, G. Cairo, and S. Fargion Iron depletion by deferoxamine up-regulates glucose uptake and insulin signaling in hepatoma cells and in rat liver Am J Pathol 172 2008 738 747
16. N. Martinelli, M. Traglia, N. Campostrini, G. Biino, M. Corbella, C. Sala, F. Busti, C. Masciullo, D. Manna, S. Previtali, A. Castagna, G. Pistis, O. Olivieri, D. Toniolo, C. Camaschella, and D. Girelli Serum hepcidin levels in subjects with the metabolic syndrome: a population study PLoS One 2012 (in press)
17. M.B. Troadec, B. Courselaud, L. Detivaud, C. Haziza-Pigeon, P. Leroyer, P. Brissot, and O. Loreal Iron overload promotes Cyclin D1 expression and alters cell cycle in mouse hepatocytes J Hepatol 44 2006 391 399
18. G. Svegliati-Baroni, C. Candelaresi, S. Saccomanno, G. Ferretti, T. Bachetti, M. Marzioni, S. De Minicis, L. Nobili, R. Salzano, A. Omenetti, D. Pacetti, S. Sigmund, A. Benedetti, and A. Casini A model of insulin resistance and nonalcoholic steatohepatitis in rats: role of peroxisome proliferator-activated receptor-alpha and n-3 polyunsaturated fatty acid treatment on liver injury Am J Pathol 169 2006 846 860
19. Wada T, Kenmochi H, Miyashita Y, Sasaki M, Ojima M, Sasahara M, Koya D, Tsuneki H, Sasaoka T: Spironolactone improves glucose and lipid metabolism by ameliorating hepatic steatosis and inflammation and suppressing enhanced gluconeogenesis induced by high-fat and high-fructose diet. Endocrinology 151:2040-2049
20. M.E. Rinella, and R.M. Green The methionine-choline deficient dietary model of steatohepatitis does not exhibit insulin resistance J Hepatol 40 2004 47 51
21. D.L. Zhang, T. Senecal, M.C. Ghosh, H. Ollivierre-Wilson, T. Tu, and T.A. Rouault Hepcidin regulates ferroportin expression and intracellular iron homeostasis of erythroblasts Blood 118 2011 2868 2877
22. S. Recalcati, L. Tacchini, A. Alberghini, D. Conte, and G. Cairo Oxidative stress-mediated down-regulation of rat hydroxyacid oxidase 1, a liver-specific peroxisomal enzyme Hepatology 38 2003 1159 1166
23. G. Cairo, L. Tacchini, G. Pogliaghi, E. Anzon, A. Tomasi, and A. Bernelli-Zazzera Induction of ferritin synthesis by oxidative stress: transcriptional and post-transcriptional regulation by expansion of the "free" iron pool J Biol Chem 270 1995 700 703
24. Girelli D, Trombini P, Busti F, Campostrini N, Sandri M, Pelucchi S, Westerman M, Ganz T, Nemeth E, Piperno A, Camaschella C: A time course of hepcidin response to iron challenge in patients with HFE and TFR2 hemochromatosis. Haematologica 96:500-506
25. C.M. Steppan, J. Wang, E.L. Whiteman, M.J. Birnbaum, and M.A. Lazar Activation of SOCS-3 by resistin Mol Cell Biol 25 2005 1569 1575
26. I. De Domenico, T.Y. Zhang, C.L. Koening, R.W. Branch, N. London, E. Lo, R.A. Daynes, J.P. Kushner, D. Li, D.M. Ward, and J. Kaplan Hepcidin mediates transcriptional changes that modulate acute cytokine-induced inflammatory responses in mice J Clin Invest 120 2010 2395 2405
27. K. Ueki, T. Kondo, Y.H. Tseng, and C.R. Kahn Central role of suppressors of cytokine signaling proteins in hepatic steatosis, insulin resistance, and the metabolic syndrome in the mouse Proc Natl Acad Sci U S A 101 2004 10422 10427
28. C.M. Kusminski, W.L. Holland, K. Sun, J. Park, S.B. Spurgin, Y. Lin, G.R. Askew, J.A. Simcox, D.A. McClain, C. Li, and P.E. Scherer MitoNEET-driven alterations in adipocyte mitochondrial activity reveal a crucial adaptive process that preserves insulin sensitivity in obesity Nat Med 18 2012 1539 1549
29. T.C. Tan, D.H. Crawford, L.A. Jaskowski, T.M. Murphy, M.L. Heritage, V.N. Subramaniam, A.D. Clouston, G.J. Anderson, and L.M. Fletcher Altered lipid metabolism in Hfe-knockout mice promotes severe NAFLD and early fibrosis Am J Physiol Gastrointest Liver Physiol 301 2011 G865 G876
30. J.E. Nelson, L. Wilson, E.M. Brunt, M.M. Yeh, D.E. Kleiner, A. Unalp-Arida, and K.V. Kowdley Relationship between the pattern of hepatic iron deposition and histological severity in nonalcoholic fatty liver disease Hepatology 53 2011 448 457
31. X. Li, B. Monks, Q. Ge, and M.J. Birnbaum Akt/PKB regulates hepatic metabolism by directly inhibiting PGC-1alpha transcription coactivator Nature 447 2007 1012 1016
32. A. Nandi, Y. Kitamura, C.R. Kahn, and D. Accili Mouse models of insulin resistance Physiol Rev 84 2004 623 647
33. J. Jo, O. Gavrilova, S. Pack, W. Jou, S. Mullen, A.E. Sumner, S.W. Cushman, and V. Periwal Hypertrophy and/or hyperplasia: dynamics of adipose tissue growth PLoS Comput Biol 5 2009 e1000324
34. T. McLaughlin, A. Sherman, P. Tsao, O. Gonzalez, G. Yee, C. Lamendola, G.M. Reaven, and S.W. Cushman Enhanced proportion of small adipose cells in insulin-resistant vs insulin-sensitive obese individuals implicates impaired adipogenesis Diabetologia 50 2007 1707 1715
35. M. Filkova, M. Haluzik, S. Gay, and L. Senolt The role of resistin as a regulator of inflammation: implications for various human pathologies Clin Immunol 133 2009 157 170
36. G. Sabio, M. Das, A. Mora, Z. Zhang, J.Y. Jun, H.J. Ko, T. Barrett, J.K. Kim, and R.J. Davis A stress signaling pathway in adipose tissue regulates hepatic insulin resistance Science 322 2008 1539 1543
37. J.S. Gabrielsen, Y. Gao, J.A. Simcox, J. Huang, D. Thorup, D. Jones, R.C. Cooksey, D. Gabrielsen, T.D. Adams, S.C. Hunt, P.N. Hopkins, W.T. Cefalu, and D.A. McClain Adipocyte iron regulates adiponectin and insulin sensitivity J Clin Invest 122 2012 3529 3540