Interactions between hepatic iron and lipid metabolism with possible relevance to steatohepatitis

World Journal of Gastroenterology

Volumn 18, Issue 34, 2012, Pages 4651-4658

  Ahmed, Umbreen ^a   Latham, Patricia S ^b   Oates, Phillip S ^c  

^a NATIONAL UNIVERSITY OF SCIENCES AND TECHNOLOGY   (Pakistan)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Hepcidin; Iron; Lipids; Non alcoholic fatty liver disease non alcoholic steatohepatitis; Oxidative stress

Indexed keywords

ADIPOPHILIN; FERROPORTIN; HEPCIDIN; INSULIN; IRON; LIPID; PHOSPHATIDYLCHOLINE STEROL ACYLTRANSFERASE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN;

AEROBIC METABOLISM; ARTICLE; DISEASE COURSE; FATTY ACID METABOLISM; FATTY ACID OXIDATION; FENTON REACTION; GENE EXPRESSION; HUMAN; IRON ABSORPTION; IRON DEFICIENCY; IRON DEPLETION; IRON METABOLISM; IRON OVERLOAD; IRON STORAGE; LIPID METABOLISM; LIPID PEROXIDATION; LIPID STORAGE; LIPID TRANSPORT; LIPOGENESIS; LIPOPROTEIN SECRETION; NONALCOHOLIC FATTY LIVER; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS;

EID: 84867733827     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v18.i34.4651     Document Type: Article

References (101)

1. Bacon BR, Farahvash MJ, Janney CG, Neuschwander-Tetri BA. Nonalcoholic steatohepatitis: an expanded clinical entity. Gastroenterology 1994; 107: 1103-1109
2. George DK, Goldwurm S, MacDonald GA, Cowley LL, Walker NI, Ward PJ, Jazwinska EC, Powell LW. Increased hepatic iron concentration in nonalcoholic steatohepatitis is associated with increased fibrosis. Gastroenterology 1998; 114: 311-318
3. Fargion S, Mattioli M, Fracanzani AL, Sampietro M, Tavazzi D, Fociani P, Taioli E, Valenti L, Fiorelli G. Hyperferritinemia, iron overload, and multiple metabolic alterations identify patients at risk for nonalcoholic steatohepatitis. Am J Gastroenterol 2001; 96: 2448-2455
4. Sherman AR, Guthrie HA, Wolinsky I, Zulak IM. Iron deficiency hyperlipidemia in 18-day-old rat pups: effects of milk lipids, lipoprotein lipase, and triglyceride synthesis. J Nutr 1978; 108: 152-162
5. Sherman AR, Bartholmey SJ, Perkins EG. Fatty acid patterns in iron-deficient maternal and neonatal rats. Lipids 1982; 17: 639-643
6. Brasaemle DL, Barber T, Wolins NE, Serrero G, Blanchette-Mackie EJ, Londos C. Adipose differentiation-related protein is an ubiquitously expressed lipid storage droplet-associated protein. J Lipid Res 1997; 38: 2249-2263
7. Sparks JD, Sparks CE. Insulin regulation of triacylglycerolrich lipoprotein synthesis and secretion. Biochim Biophys Acta 1994; 1215: 9-32
8. Debeer LJ, Beynen AC, Mannaerts GP, Geelen MJ. Lipolysis of hepatic triacylglycerol stores. FEBS Lett 1982; 140: 159-164
9. Patsch W, Franz S, Schonfeld G. Role of insulin in lipoprotein secretion by cultured rat hepatocytes. J Clin Invest 1983; 71: 1161-1174
10. Adeli K, Theriault A. Insulin modulation of human apolipoprotein B mRNA translation: studies in an in vitro cellfree system from HepG2 cells. Biochem Cell Biol 1992; 70: 1301-1312
11. Sparks JD, Sparks CE. Insulin modulation of hepatic synthesis and secretion of apolipoprotein B by rat hepatocytes. J Biol Chem 1990; 265: 8854-8862
12. Phillips SA, Choe CC, Ciaraldi TP, Greenberg AS, Kong AP, Baxi SC, Christiansen L, Mudaliar SR, Henry RR. Adipocyte differentiation-related protein in human skeletal muscle: relationship to insulin sensitivity. Obes Res 2005; 13: 1321-1329
13. Shimomura I, Bashmakov Y, Ikemoto S, Horton JD, Brown MS, Goldstein JL. Insulin selectively increases SREBP-1c mRNA in the livers of rats with streptozotocin-induced diabetes. Proc Natl Acad Sci USA 1999; 96: 13656-13661
14. Lau BW, Klevay LM. Postheparin plasma lipoprotein lipase in copper-deficient rats. J Nutr 1982; 112: 928-933
15. Muratsubaki H, Enomoto K, Ichijoh Y, Yamamoto Y. Hypertriglyceridemia associated with decreased post-heparin plasma hepatic triglyceride lipase activity in hypoxic rats. Arch Physiol Biochem 2003; 111: 449-454
16. Mochizuki S, Murase T, Yamaoka H, Ishiki M, Tada N, Nagano M. Lipoprotein lipase activity in ischaemic and anoxic myocardium. Basic Res Cardiol 1987; 82 Suppl 1: 45-52
17. Lewis M, Iammarino RM. Lipemia in rodent iron-deficiency anemia. J Lab Clin Med 1971; 78: 546-554
18. Vaziri ND, Liang K. Down-regulation of tissue lipoprotein lipase expression in experimental chronic renal failure. Kidney Int 1996; 50: 1928-1935
19. Brown MS, Kovanen PT, Goldstein JL. Regulation of plasma cholesterol by lipoprotein receptors. Science 1981; 212: 628-635
20. Vaziri ND, Liang K. Down-regulation of VLDL receptor expression in chronic experimental renal failure. Kidney Int 1997; 51: 913-919
21. Rao GA, Crane RT, Larkin EC. Reduced plasma lecithin cholesterol acyl transferase activity in rats fed iron-deficient diets. Lipids 1983; 18: 673-676
22. Jain SK, Yip R, Pramanik AK, Dallman PR, Shohet SB. Reduced plasma cholesterol esterifying activity in iron-deficient rats: its possible role in the lipemia of iron deficiency. J Nutr 1982; 112: 1230-1232
23. Sherman AR. Lipogenesis in iron-deficient adult rats. Lipids 1978; 13: 473-478
24. Bartholmey SJ, Sherman AR. Carnitine levels in iron-deficient rat pups. J Nutr 1985; 115: 138-145
25. Hulse JD, Ellis SR, Henderson LM. Carnitine biosynthesis. beta-Hydroxylation of trimethyllysine by an alpha-ketoglutarate-dependent mitochondrial dioxygenase. J Biol Chem 1978; 253: 1654-1659
26. Davis MR, Rendina E, Peterson SK, Lucas EA, Smith BJ, Clarke SL. Enhanced expression of lipogenic genes may contribute to hyperglycemia and alterations in plasma lipids in response to dietary iron deficiency. Genes Nutr 2012; 7:415-425
27. Amine EK, Desilets EJ, Hegsted DM. Effect of dietary fat on lipogenesis in iron deficiency anemic chicks and rats. Journal of Nutrition 1976; 106: 405-411
28. Bailey-Wood R, Blayney LM, Muir JR, Jacobs A. The effects of iron deficiency on rat liver enzymes. Br J Exp Pathol 1975; 56: 193-198
29. Stangl GI, Kirchgessner M. Different degrees of moderate iron deficiency modulate lipid metabolism of rats. Lipids 1998; 33: 889-895
30. Sochor M, Baquer NZ, McLean P. Bio-inorganic regulation of pathways of carbohydrate and lipid metabolism. II. The effect of iron-deficiency on the profile of enzymes in the developing rat adrenal gland. Enzyme 1982; 27: 149-155
31. Dallman PR, Goodman JR. The effects of iron deficiency on the hepatocyte: a biochemical and ultrastructural study. J Cell Biol 1971; 48: 79-90
32. Amine EK, Hegsted DM. Iron deficiency lipemia in the rat and chick. J Nutr 1971; 101: 1575-1582
33. Floch MH, Shearman DJ, Herskovic T, Levine RJ, Spiro HM. Iron deficiency anemia and hepatic lesions in weanling rats. Arch Pathol 1969; 87: 526-532
34. Puig S, Askeland E, Thiele DJ. Coordinated remodeling of cellular metabolism during iron deficiency through targeted mRNA degradation. Cell 2005; 120: 99-110
35. Protchenko O, Philpott CC. Regulation of intracellular heme levels by HMX1, a homologue of heme oxygenase, in Saccharomyces cerevisiae. J Biol Chem 2003; 278: 36582-36587
36. Shakoury-Elizeh M, Protchenko O, Berger A, Cox J, Gable K, Dunn TM, Prinz WA, Bard M, Philpott CC. Metabolic response to iron deficiency in Saccharomyces cerevisiae. J Biol Chem 2010; 285: 14823-14833
37. Au YP, Schilling RF. Relationship between anemia and cholesterol metabolism in 'sex-linked anemic' (gene symbol, sla) mouse. Biochim Biophys Acta 1986; 883: 242-246
38. Johnston SM, Murray KP, Martin SA, Fox-Talbot K, Lipsett PA, Lillemoe KD, Pitt HA. Iron deficiency enhances cholesterol gallstone formation. Surgery 1997; 122: 354-361; discussion 361-362
39. Rao GA, Crane RT, Larkin EC. Reduction of hepatic stearoyl-CoA desaturase activity in rats fed iron-deficient diets. Lipids 1983; 18: 573-575
40. Cunnane SC, McAdoo KR. Iron intake influences essential fatty acid and lipid composition of rat plasma and erythrocytes. J Nutr 1987; 117: 1514-1519
41. Li J, Grigoryev DN, Ye SQ, Thorne L, Schwartz AR, Smith PL, O'Donnell CP, Polotsky VY. Chronic intermittent hypoxia upregulates genes of lipid biosynthesis in obese mice. J Appl Physiol 2005; 99: 1643-1648
42. Barker DJ. Fetal growth and adult disease. Br J Obstet Gynaecol 1992; 99: 275-276
43. Barker DJ, Martyn CN, Osmond C, Hales CN, Fall CH. Growth in utero and serum cholesterol concentrations in adult life. BMJ 1993; 307: 1524-1527
44. Lucas A, Baker BA, Desai M, Hales CN. Nutrition in pregnant or lactating rats programs lipid metabolism in the offspring. Br J Nutr 1996; 76: 605-612
45. Kruidenier L, Verspaget HW. Review article: oxidative stress as a pathogenic factor in inflammatory bowel disease--radicals or ridiculous? Aliment Pharmacol Ther 2002; 16: 1997-2015
46. Moldovan L, Moldovan NI. Oxygen free radicals and redox biology of organelles. Histochem Cell Biol 2004; 122: 395-412
47. Bacon BR, O'Neill R, Park CH. Iron-induced peroxidative injury to isolated rat hepatic mitochondria. J Free Radic Biol Med 1986; 2: 339-347
48. Högberg J, Bergstrand A, Jakobsson SV. Lipid peroxidation of rat-liver microsomes. Its effect on the microsomal membrane and some membrane-bound microsomal enzymes. Eur J Biochem 1973; 37: 51-59
49. Myers BM, Prendergast FG, Holman R, Kuntz SM, LaRusso NF. Alterations in the structure, physicochemical properties, and pH of hepatocyte lysosomes in experimental iron overload. J Clin Invest 1991; 88: 1207-1215
50. Bacon BR, Britton RS. The pathology of hepatic iron overload: a free radical--mediated process? Hepatology 1990; 11: 127-137
51. Bacon BR, O'Neill R, Britton RS. Hepatic mitochondrial energy production in rats with chronic iron overload. Gastroenterology 1993; 105: 1134-1140
52. Ohyashiki T, Ohtsuka T, Mohri T. A change in the lipid fluidity of the porcine intestinal brush-border membranes by lipid peroxidation. Studies using pyrene and fluorescent stearic acid derivatives. Biochim Biophys Acta 1986; 861: 311-318
53. Curtis MT, Gilfor D, Farber JL. Lipid peroxidation increases the molecular order of microsomal membranes. Arch Biochem Biophys 1984; 235: 644-649
54. Schachter D. Fluidity and function of hepatocyte plasma membranes. Hepatology 1984; 4: 140-151
55. Brunet S, Thibault L, Delvin E, Yotov W, Bendayan M, Levy E. Dietary iron overload and induced lipid peroxidation are associated with impaired plasma lipid transport and hepatic sterol metabolism in rats. Hepatology 1999; 29: 1809-1817
56. Whittaker P, Chanderbhan RF. Effect of increasing iron supplementation on blood lipids in rats. Br J Nutr 2001; 86: 587-592
57. Foretz M, Foufelle F, Ferré P. Polyunsaturated fatty acids inhibit fatty acid synthase and spot-14-protein gene expression in cultured rat hepatocytes by a peroxidative mechanism. Biochem J 1999; 341 (Pt 2): 371-376
58. Kirsch R, Sijtsema HP, Tlali M, Marais AD, Hall Pde L. Effects of iron overload in a rat nutritional model of nonalcoholic fatty liver disease. Liver Int 2006; 26: 1258-1267
59. Graham RM, Chua AC, Carter KW, Delima RD, Johnstone D, Herbison CE, Firth MJ, O'Leary R, Milward EA, Olynyk JK, Trinder D. Hepatic iron loading in mice increases cholesterol biosynthesis. Hepatology 2010; 52: 462-471
60. Pigeon C, Legrand P, Leroyer P, Bouriel M, Turlin B, Brissot P, Loréal O. Stearoyl coenzyme A desaturase 1 expression and activity are increased in the liver during iron overload. Biochim Biophys Acta 2001; 1535: 275-284
61. Cabrita M, Pereira CF, Rodrigues P, Cardoso EM, Arosa FA. Altered expression of CD1d molecules and lipid accumulation in the human hepatoma cell line HepG2 after iron loading. FEBS J 2005; 272: 152-165
62. Iguchi K, Hirano K, Hamatake M, Ishida R. Phosphatidylserine induces apoptosis in adherent cells. Apoptosis 2001; 6: 263-268
63. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol 2007; 35: 495-516
64. Imeryuz N, Tahan V, Sonsuz A, Eren F, Uraz S, Yuksel M, Akpulat S, Ozcelik D, Haklar G, Celikel C, Avsar E, Tozun N. Iron preloading aggravates nutritional steatohepatitis in rats by increasing apoptotic cell death. J Hepatol 2007; 47: 851-859
65. Jou J, Choi SS, Diehl AM. Mechanisms of disease progression in nonalcoholic fatty liver disease. Semin Liver Dis 2008; 28: 370-379
66. Dowman JK, Tomlinson JW, Newsome PN. Pathogenesis of non-alcoholic fatty liver disease. QJM 2010; 103: 71-83
67. Bugianesi E, Moscatiello S, Ciaravella MF, Marchesini G. Insulin resistance in nonalcoholic fatty liver disease. Curr Pharm Des 2010; 16: 1941-1951
68. She H, Xiong S, Lin M, Zandi E, Giulivi C, Tsukamoto H. Iron activates NF-kappaB in Kupffer cells. Am J Physiol Gastrointest Liver Physiol 2002; 283: G719-G726
69. Xiong S, She H, Tsukamoto H. Signaling role of iron in NFkappa B activation in hepatic macrophages. Comp Hepatol 2004; 3 Suppl 1: S36
70. Ramm GA, Crawford DH, Powell LW, Walker NI, Fletcher LM, Halliday JW. Hepatic stellate cell activation in genetic haemochromatosis. Lobular distribution, effect of increasing hepatic iron and response to phlebotomy. J Hepatol 1997; 26: 584-592
71. Bonkovsky HL, Jawaid Q, Tortorelli K, LeClair P, Cobb J, Lambrecht RW, Banner BF. Non-alcoholic steatohepatitis and iron: increased prevalence of mutations of the HFE gene in non-alcoholic steatohepatitis. J Hepatol 1999; 31: 421-429
72. Nelson JE, Bhattacharya R, Lindor KD, Chalasani N, Raaka S, Heathcote EJ, Miskovsky E, Shaffer E, Rulyak SJ, Kowdley KV. HFE C282Y mutations are associated with advanced hepatic fibrosis in Caucasians with nonalcoholic steatohepatitis. Hepatology 2007; 46: 723-729
73. Sumida Y, Nakashima T, Yoh T, Furutani M, Hirohama A, Kakisaka Y, Nakajima Y, Ishikawa H, Mitsuyoshi H, Okanoue T, Kashima K, Nakamura H, Yodoi J. Serum thioredoxin levels as a predictor of steatohepatitis in patients with nonalcoholic fatty liver disease. J Hepatol 2003; 38: 32-38
74. Duseja A, Das R, Nanda M, Das A, Garewal G, Chawla Y. Nonalcoholic steatohepatitis in Asian Indians is neither associated with iron overload nor with HFE gene mutations. World J Gastroenterol 2005; 11: 393-395
75. Deguti MM, Sipahi AM, Gayotto LC, Palácios SA, Bittencourt PL, Goldberg AC, Laudanna AA, Carrilho FJ, Cançado EL. Lack of evidence for the pathogenic role of iron and HFE gene mutations in Brazilian patients with nonalcoholic steatohepatitis. Braz J Med Biol Res 2003; 36: 739-745
76. Younossi ZM, Gramlich T, Bacon BR, Matteoni CA, Boparai N, O'Neill R, McCullough AJ. Hepatic iron and nonalcoholic fatty liver disease. Hepatology 1999; 30: 847-850
77. Angulo P, Keach JC, Batts KP, Lindor KD. Independent predictors of liver fibrosis in patients with nonalcoholic steatohepatitis. Hepatology 1999; 30: 1356-1362
78. Chitturi S, Weltman M, Farrell GC, McDonald D, Kench J, Liddle C, Samarasinghe D, Lin R, Abeygunasekera S, George J. HFE mutations, hepatic iron, and fibrosis: ethnic-specific association of NASH with C282Y but not with fibrotic severity. Hepatology 2002; 36: 142-149
79. Valenti L, Fracanzani AL, Bugianesi E, Dongiovanni P, Galmozzi E, Vanni E, Canavesi E, Lattuada E, Roviaro G, Marchesini G, Fargion S. HFE genotype, parenchymal iron accumulation, and liver fibrosis in patients with nonalcoholic fatty liver disease. Gastroenterology 2010; 138: 905-912
80. Duseja A, Das A, Das R, Dhiman RK, Chawla Y, Bhansali A, Kalra N. The clinicopathological profile of Indian patients with nonalcoholic fatty liver disease (NAFLD) is different from that in the West. Dig Dis Sci 2007; 52: 2368-2374
81. Yamauchi N, Itoh Y, Tanaka Y, Mizokami M, Minami M, Morita A, Toyama T, Yamaguchi K, Fujii H, Okanoue T. Clinical characteristics and prevalence of GB virus C, SEN virus, and HFE gene mutation in Japanese patients with nonalcoholic steatohepatitis. J Gastroenterol 2004; 39: 654-660
82. Facchini FS, Hua NW, Stoohs RA. Effect of iron depletion in carbohydrate-intolerant patients with clinical evidence of nonalcoholic fatty liver disease. Gastroenterology 2002; 122: 931-939
83. Fargion S, Dongiovanni P, Guzzo A, Colombo S, Valenti L, Fracanzani AL. Iron and insulin resistance. Aliment Pharmacol Ther 2005; 22 Suppl 2: 61-63
84. Sumida Y, Kanemasa K, Fukumoto K, Yoshida N, Sakai K, Nakashima T, Okanoue T. Effect of iron reduction by phlebotomy in Japanese patients with nonalcoholic steatohepatitis: A pilot study. Hepatol Res 2006; 36: 315-321
85. Riquelme A, Soza A, Nazal L, Martínez G, Kolbach M, Patillo A, Arellano JM, Duarte I, Martínez J, Molgó M, Arrese M. Histological resolution of steatohepatitis after iron depletion. Dig Dis Sci 2004; 49: 1012-1015
86. González-Alonso J, Mortensen SP, Dawson EA, Secher NH, Damsgaard R. Erythrocytes and the regulation of human skeletal muscle blood flow and oxygen delivery: role of erythrocyte count and oxygenation state of haemoglobin. J Physiol 2006; 572: 295-305
87. Duke M, Abelmann WH. The hemodynamic response to chronic anemia. Circulation 1969; 39: 503-515
88. Roy SB, Bhatia ML, Mathur VS, Virmani S. Hemodynamic effects of chronic severe anemia. Circulation 1963; 28: 346-356
89. Mackintosh VS, Elsegood CL, Redgrave TG. Effects of adrenoreceptor antagonists and agonists on clearance of emulsion models of triacylglycerol-rich lipoproteins from plasma in rats. Clin Exp Pharmacol Physiol 1991; 18: 775-788
90. Mackintosh V, Redgrave TG. Effects of adrenaline and noradrenaline on clearance of triacylglycerol-rich lipoproteins from plasma: studies with chylomicron-like lipid emulsions in rats. Clin Exp Pharmacol Physiol 1991; 18: 137-143
91. Diehl AM. Lessons from animal models of NASH. Hepatol Res 2005; 33: 138-144
92. Ludwig J, Hashimoto E, Porayko MK, Moyer TP, Baldus WP. Hemosiderosis in cirrhosis: a study of 447 native livers. Gastroenterology 1997; 112: 882-888
93. Batey RG, Johnston R. Effects of alcohol, carbon tetrachloride, and choline deficiency on iron metabolism in the rat. Alcohol Clin Exp Res 1993; 17: 931-934
94. Lee AW, Oates PS, Trinder D. Effects of cell proliferation on the uptake of transferrin-bound iron by human hepatoma cells. Hepatology 2003; 38: 967-977
95. Sharp PA. New insights into the role of iron in the development of nonalcoholic fatty liver disease. Hepatology 2010; 52: 408-410
96. Fujita N, Takei Y. Iron overload in nonalcoholic steatohepatitis. Adv Clin Chem 2011; 55: 105-132
97. Le Guenno G, Chanséaume E, Ruivard M, Morio B, Mazur A. Study of iron metabolism disturbances in an animal model of insulin resistance. Diabetes Res Clin Pract 2007; 77: 363-370
98. Tsuchiya H, Sakabe T, Akechi Y, Ikeda R, Nishio R, Terabayashi K, Matsumi Y, Hoshikawa Y, Kurimasa A, Shiota G. A close association of abnormal iron metabolism with steatosis in the mice fed a choline-deficient diet. Biol Pharm Bull 2010; 33: 1101-1104
99. Aigner E, Theurl I, Theurl M, Lederer D, Haufe H, Dietze O, Strasser M, Datz C, Weiss G. Pathways underlying iron accumulation in human nonalcoholic fatty liver disease. Am J Clin Nutr 2008; 87: 1374-1383
100. Otogawa K, Kinoshita K, Fujii H, Sakabe M, Shiga R, Nakatani K, Ikeda K, Nakajima Y, Ikura Y, Ueda M, Arakawa T, Hato F, Kawada N. Erythrophagocytosis by liver macrophages (Kupffer cells) promotes oxidative stress, inflammation, and fibrosis in a rabbit model of steatohepatitis: implications for the pathogenesis of human nonalcoholic steatohepatitis. Am J Pathol 2007; 170: 967-980
101. Gentile CL, Pagliassotti MJ. The role of fatty acids in the development and progression of nonalcoholic fatty liver disease. J Nutr Biochem 2008; 19: 567-576