Hepcidin is directly regulated by insulin and plays an important role in iron overload in streptozotocin-induced diabetic rats

Diabetes

Volumn 63, Issue 5, 2014, Pages 1506-1518

  Wang, Heyang ^a   Li, Hongxia ^a   Jiang, Xin ^a   Shi, Wencai ^a   Shen, Zhilei ^a   Li, Min ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BUTADIENES; DIABETES MELLITUS, EXPERIMENTAL; ENZYME INHIBITORS; HEPCIDINS; INSULIN; INSULIN RESISTANCE; IRON; IRON OVERLOAD; LIVER; MALE; NITRILES; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84899065291     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-1195     Document Type: Article

References (48)

1. Rajpathak SN, Crandall JP, Wylie-Rosett J, Kabat GC, Rohan TE, Hu FB. The role of iron in type 2 diabetes in humans. Biochim Biophys Acta 2009;1790:671-681
2. Zheng X, Jiang T, Wu H, et al. Hepatic iron stores are increased as assessed by magnetic resonance imaging in a Chinese population with altered glucose homeostasis. Am J Clin Nutr 2011;94:1012-1019
3. Ren Y, Tian H, Li X, Liang J, Zhao G. Elevated serum ferritin concentrations in a glucose-impaired population and in normal glucose tolerant first-degree relatives in familial type 2 diabetic pedigrees. Diabetes Care 2004;27:622-623 (Pubitemid 38174100)
4. Sharifi F, Nasab NM, Zadeh HJ. Elevated serum ferritin concentrations in prediabetic subjects. Diab Vasc Dis Res 2008;5:15-18 (Pubitemid 351507340)
5. Silva M, Bonomo LdeF, Oliveira RdeP, Geraldo de Lima W, Silva ME, Pedrosa ML. Effects of the interaction of diabetes and iron supplementation on hepatic and pancreatic tissues, oxidative stress markers, and liver peroxisome proliferator-activated receptor-α expression. J Clin Biochem Nutr 2011;49:102-108
6. Simcox JA, McClain DA. Iron and diabetes risk. Cell Metab 2013;17:329-341
7. Forouhi NG, Harding AH, Allison M, et al. Elevated serum ferritin levels predict new-onset type 2 diabetes: results from the EPIC-Norfolk prospective study. Diabetologia 2007;50:949-956 (Pubitemid 46559245)
8. Montonen J, Boeing H, Steffen A, et al. Body iron stores and risk of type 2 diabetes: results from the European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam study. Diabetologia 2012;55:2613-2621
9. Valenti L, Fracanzani AL, Dongiovanni P, et al. 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 2007;102:1251-1258 (Pubitemid 46802029)
10. Cooksey RC, Jones D, Gabrielsen S, et al. Dietary iron restriction or iron chelation protects from diabetes and loss of β-cell function in the obese (ob/ob lep-/-) mouse. Am J Physiol Endocrinol Metab 2010;298:E1236-E1243
11. Luque-Ramírez M, Alvarez-Blasco F, Botella-Carretero JI, Sanchón R, San Millán JL, Escobar-Morreale HF. Increased body iron stores of obese women with polycystic ovary syndrome are a consequence of insulin resistance and hyperinsulinism and are not a result of reduced menstrual losses. Diabetes Care 2007;30:2309-2313 (Pubitemid 47359039)
12. Lee DH, Liu DY, Jacobs DR Jr, et al. Common presence of non-transferrin-bound iron among patients with type 2 diabetes. Diabetes Care 2006;29:1090-1095
13. Canturk Z, Cetinarslan B, Tarkun I, Canturk NZ. Serum ferritin levels in poorly- and well-controlled diabetes mellitus. Endocr Res 2003;29:299-306 (Pubitemid 37176589)
14. Shetty JK, Prakash M, Ibrahim MS. Relationship between free iron and glycated hemoglobin in uncontrolled type 2 diabetes patients associated with complications. Indian J Clin Biochem 2008;23:67-70 (Pubitemid 351866254)
15. Ganz T. Hepcidin and iron regulation, 10 years later. Blood 2011;117:4425-4433
16. Aso Y, Takebayashi K, Wakabayashi S, et al. Relation between serum high molecular weight adiponectin and serum ferritin or prohepcidin in patients with type 2 diabetes. Diabetes Res Clin Pract 2010;90:250-255
17. Fernández-Real JM, Equitani F, Moreno JM, Manco M, Ortega F, Ricart W. Study of circulating prohepcidin in association with insulin sensitivity and changing iron stores. J Clin Endocrinol Metab 2009;94:982-988
18. Reed MJ, Meszaros K, Entes LJ, et al. A new rat model of type 2 diabetes: the fat-fed, streptozotocin-treated rat. Metabolism 2000;49:1390-1394
19. Wang RH, Yu H, Deng CX. A requirement for breast-cancer-associated gene 1 (BRCA1) in the spindle checkpoint. Proc Natl Acad Sci U S A 2004;101:17108-17113 (Pubitemid 39627782)
20. Courselaud B, Pigeon C, Inoue Y, et al. C/EBPalpha regulates hepatic transcription of hepcidin, an antimicrobial peptide and regulator of iron metabolism. Cross-talk between C/EBP pathway and iron metabolism. J Biol Chem 2002;277:41163-41170 (Pubitemid 35215708)
21. Matak P, Chaston TB, Chung B, Srai SK, McKie AT, Sharp PA. Activated macrophages induce hepcidin expression in HuH7 hepatoma cells. Haematologica 2009;94:773-780
22. Mirza S, Hossain M, Mathews C, et al. Type 2-diabetes is associated with elevated levels of TNF-alpha, IL-6 and adiponectin and low levels of leptin in a population of Mexican Americans: a cross-sectional study. Cytokine 2012;57:136-142
23. 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 (Pubitemid 47211345)
24. Fleming MD. The regulation of hepcidin and its effects on systemic and cellular iron metabolism. Hematology Am Soc Hematol Educ Program 2008;151-158
25. Wrighting DM, Andrews NC. Interleukin-6 induces hepcidin expression through STAT3. Blood 2006;108:3204-3209
26. Swaminathan S, Fonseca VA, Alam MG, Shah SV. The role of iron in diabetes and its complications. Diabetes Care 2007;30:1926-1933 (Pubitemid 47036384)
27. Nankivell BJ, Tay YC, Boadle RA, Harris DC. Lysosomal iron accumulation in diabetic nephropathy. Ren Fail 1994;16:367-381 (Pubitemid 24338515)
28. Zhao N, Sun Z, Mao Y, et al. Myocardial iron metabolism in the regulation of cardiovascular diseases in rats. Cell Physiol Biochem 2010;25:587-594
29. Rowe PA, Kavanagh K, Zhang L, Harwood HJ Jr, Wagner JD. Short-term hyperglycemia increases arterial superoxide production and iron dysregulation in atherosclerotic monkeys. Metabolism 2011;60:1070-1080
30. Silva M, de Brito Magalhães CL, de Paula Oliveira R, Silva ME, Pedrosa ML. Differential expression of iron metabolism proteins in diabetic and diabetic iron-supplemented rat liver. J Biochem Mol Toxicol 2012;26:123-129
31. Saravanan G, Ponmurugan P, Begum MS. Effect of S-allylcysteine, a sulphur containing amino acid on iron metabolism in streptozotocin induced diabetic rats. J Trace Elem Med Biol 2013;27:143-147
32. Dogukan A, Sahin N, Tuzcu M, et al. The effects of chromium histidinate on mineral status of serum and tissue in fat-fed and streptozotocin-treated type II diabetic rats. Biol Trace Elem Res 2009;131:124-132
33. Kishino Y, Tanaka Y, Ikeda T, et al. Ezetimibe increases hepatic iron levels in mice fed a high-fat diet. J Pharmacol Exp Ther 2013;345:483-491
34. Sam AH, Busbridge M, Amin A, et al. Hepcidin levels in diabetes mellitus and polycystic ovary syndrome. Diabet Med 2013;30:1495-1499
35. De Block CE, Van Campenhout CM, De Leeuw IH, et al. Soluble transferrin receptor level: a new marker of iron deficiency anemia, a common manifestation of gastric autoimmunity in type 1 diabetes. Diabetes Care 2000;23:1384-1388
36. De Block CE, De Leeuw IH, Van Gaal LF. Autoimmune gastritis in type 1 diabetes: a clinically oriented review. J Clin Endocrinol Metab 2008;93:363-371 (Pubitemid 351240803)
37. Hermo JA, González L, Loureiro C. Autoimmune chronic gastritis and iron deficiency anemia. Am J Med 1999;107:401-403 (Pubitemid 29465824)
38. Sonnweber T, Ress C, Nairz M, et al. High-fat diet causes iron deficiency via hepcidin-independent reduction of duodenal iron absorption. J Nutr Biochem 2012;23:1600-1608
39. Tsuchiya H, Ebata Y, Sakabe T, Hama S, Kogure K, Shiota G. High-fat, high-fructose diet induces hepatic iron overload via a hepcidin-independent mechanism prior to the onset of liver steatosis and insulin resistance in mice. Metabolism 2013;62:62-69
40. Jiang F, Sun ZZ, Tang YT, Xu C, Jiao XY. Hepcidin expression and iron parameters change in Type 2 diabetic patients. Diabetes Res Clin Pract 2011;93:43-48
41. Mitsuyoshi H, Yasui K, Harano Y, et al. Analysis of hepatic genes involved in the metabolism of fatty acids and iron in nonalcoholic fatty liver disease. Hepatol Res 2009;39:366-373
42. Aigner E, Felder TK, Oberkofler H, et al. Glucose acts as a regulator of serum iron by increasing serum hepcidin concentrations. J Nutr Biochem 2013;24:112-117
43. Gartsbein M, Alt A, Hashimoto K, Nakajima K, Kuroki T, Tennenbaum T. The role of protein kinase C δ activation and STAT3 Ser727 phosphorylation in insulin-induced keratinocyte proliferation. J Cell Sci 2006;119:470-481
44. Coffer PJ, van Puijenbroek A, Burgering BM, et al. Insulin activates Stat3 independently of p21ras-ERK and PI-3K signal transduction. Oncogene 1997;15:2529-2539 (Pubitemid 27507245)
45. Campos SP, Wang Y, Baumann H. Insulin modulates STAT3 protein activation and gene transcription in hepatic cells. J Biol Chem 1996;271:24418-24424 (Pubitemid 26333175)
46. Ihle JN. STATs and MAPKs: obligate or opportunistic partners in signaling. Bioessays 1996b;18:95-98
47. Carvalheira JB, Siloto RM, Ignacchitti I, et al. Insulin modulates leptin-induced STAT3 activation in rat hypothalamus. FEBS Lett 2001;500:119-124 (Pubitemid 32607544)
48. Hemati N, Ross SE, Erickson RL, Groblewski GE, MacDougald OA. Signaling pathways through which insulin regulates CCAAT/enhancer binding protein alpha (C/EBPalpha) phosphorylation and gene expression in 3T3-L1 adipocytes. Correlation with GLUT4 gene expression. J Biol Chem 1997;272:25913-25919 (Pubitemid 27438917)