Angiotensin II alters the expression of duodenal iron transporters, hepatic hepcidin, and body iron distribution in mice

European Journal of Nutrition

Volumn 54, Issue 5, 2015, Pages 709-719

  Tajima, Soichiro ^a,b   Ikeda, Yasumasa ^a   Enomoto, Hideaki ^a,c   Imao, Mizuki ^a   Horinouchi, Yuya ^a   Izawa Ishizawa, Yuki ^a   Kihira, Yoshitaka ^a   Miyamoto, Licht ^a   Ishizawa, Keisuke ^a   Tsuchiya, Koichiro ^a   Tamaki, Toshiaki ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b KYUSHU UNIVERSITY HOSPITAL   (Japan)

^c UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

Angiotensin II; Ferritin; Hepcidin; Iron metabolism

Indexed keywords

ANGIOTENSIN 2 RECEPTOR ANTAGONIST; ANGIOTENSIN II; BONE MORPHOGENETIC PROTEIN 6; CCAAT ENHANCER BINDING PROTEIN ALPHA; CD71 ANTIGEN; FERRITIN; FERROPORTIN; HEPCIDIN; IRON; MESSENGER RNA; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; BIOLOGICAL MARKER; BMP6 PROTEIN, MOUSE; CATION TRANSPORT PROTEIN; CCAAT ENHANCER BINDING PROTEIN; CEBPA PROTEIN, MOUSE; DMRT1 PROTEIN; METAL TRANSPORTING PROTEIN 1; SOLUTE CARRIER FAMILY 11- (PROTON-COUPLED DIVALENT METAL ION TRANSPORTERS), MEMBER 2; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FERRITIN BLOOD LEVEL; HYPERTENSION; IRON ABSORPTION; IRON METABOLISM; IRON STORAGE; MACROPHAGE; MALE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; RNA BINDING; ANIMAL; BLOOD; C57BL MOUSE; DOWN REGULATION; DRUG EFFECTS; DUODENUM; GENETICS; KIDNEY; LIVER; METABOLISM; SPLEEN;

MUS;

ANGIOTENSIN II; ANIMALS; BIOMARKERS; BONE MORPHOGENETIC PROTEIN 6; CATION TRANSPORT PROTEINS; CCAAT-ENHANCER-BINDING PROTEINS; DOWN-REGULATION; DUODENUM; FERRITINS; HEPCIDINS; IRON; KIDNEY; LIVER; MALE; MICE; MICE, INBRED C57BL; RNA, MESSENGER; SPLEEN; TRANSCRIPTION FACTORS;

EID: 84937513465     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-014-0749-1     Document Type: Article

References (45)

1. Kruszewski M (2003) Labile iron pool: the main determinant of cellular response to oxidative stress. Mutat Res 531(1–2):81–92
2. Cairo G, Recalcati S, Pietrangelo A, Minotti G (2002) The iron regulatory proteins: targets and modulators of free radical reactions and oxidative damage. Free Radic Biol Med 32(12):1237–1243
3. Khan ZA, Farhangkhoee H, Barbin YP, Adams PC, Chakrabarti S (2005) Glucose-induced regulation of novel iron transporters in vascular endothelial cell dysfunction. Free Radic Res 39(11):1203–1210. doi:10.1080/10715760500143254
4. Nanami M, Ookawara T, Otaki Y, Ito K, Moriguchi R, Miyagawa K, Hasuike Y, Izumi M, Eguchi H, Suzuki K, Nakanishi T (2005) Tumor necrosis factor-alpha-induced iron sequestration and oxidative stress in human endothelial cells. Arterioscler Thromb Vasc Biol 25(12):2495–2501. doi:10.1161/01.ATV.0000190610.63878.20
5. Mehta PK, Griendling KK (2007) Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol 292(1):C82–C97. doi:10.1152/ajpcell.00287.2006
6. Ogihara T, Asano T, Ando K, Chiba Y, Sakoda H, Anai M, Shojima N, Ono H, Onishi Y, Fujishiro M, Katagiri H, Fukushima Y, Kikuchi M, Noguchi N, Aburatani H, Komuro I, Fujita T (2002) Angiotensin II-induced insulin resistance is associated with enhanced insulin signaling. Hypertension 40(6):872–879
7. Henriksen EJ, Jacob S, Kinnick TR, Teachey MK, Krekler M (2001) Selective angiotensin II receptor antagonism reduces insulin resistance in obese Zucker rats. Hypertension 38(4):884–890
8. Abuissa H, Jones PG, Marso SP, O’Keefe JH Jr (2005) Angiotensin-converting enzyme inhibitors or angiotensin receptor blockers for prevention of type 2 diabetes: a meta-analysis of randomized clinical trials. J Am Coll Cardiol 46(5):821–826. doi:10.1016/j.jacc.2005.05.051
9. Ishizaka N, Saito K, Noiri E, Sata M, Ikeda H, Ohno A, Ando J, Mori I, Ohno M, Nagai R (2005) Administration of ANG II induces iron deposition and upregulation of TGF-beta1 mRNA in the rat liver. Am J Physiol Regul Integr Comp Physiol 288(4):R1063–R1070. doi:10.1152/ajpregu.00281.2004
10. Ishizaka N, Aizawa T, Yamazaki I, Usui S, Mori I, Kurokawa K, Tang SS, Ingelfinger JR, Ohno M, Nagai R (2002) Abnormal iron deposition in renal cells in the rat with chronic angiotensin II administration. Lab Invest 82(1):87–96
11. Ishizaka N, Saito K, Mitani H, Yamazaki I, Sata M, Usui S, Mori I, Ohno M, Nagai R (2002) Iron overload augments angiotensin II-induced cardiac fibrosis and promotes neointima formation. Circulation 106(14):1840–1846
12. Ishizaka N, Saito K, Mori I, Matsuzaki G, Ohno M, Nagai R (2005) Iron chelation suppresses ferritin upregulation and attenuates vascular dysfunction in the aorta of angiotensin II-infused rats. Arterioscler Thromb Vasc Biol 25(11):2282–2288. doi:10.1161/01.ATV.0000181763.57495.2b
13. Ishizaka N, Saito K, Furuta K, Matsuzaki G, Koike K, Noiri E, Nagai R (2007) Angiotensin II-induced regulation of the expression and localization of iron metabolism-related genes in the rat kidney. Hypertens Res 30(2):195–202. doi:10.1291/hypres.30.195
14. Tajima S, Tsuchiya K, Horinouchi Y, Ishizawa K, Ikeda Y, Kihira Y, Shono M, Kawazoe K, Tomita S, Tamaki T (2010) Effect of angiotensin II on iron-transporting protein expression and subsequent intracellular labile iron concentration in human glomerular endothelial cells. Hypertens Res 33(7):713–721. doi:10.1038/hr.2010.63
15. Piperno A, Trombini P, Gelosa M, Mauri V, Pecci V, Vergani A, Salvioni A, Mariani R, Mancia G (2002) Increased serum ferritin is common in men with essential hypertension. J Hypertens 20(8):1513–1518
16. Wrede CE, Buettner R, Bollheimer LC, Scholmerich J, Palitzsch KD, Hellerbrand C (2006) Association between serum ferritin and the insulin resistance syndrome in a representative population. Eur J Endocrinol 154(2):333–340. doi:10.1530/eje.1.02083
17. Ikeda Y, Tajima S, Izawa-Ishizawa Y, Kihira Y, Ishizawa K, Tomita S, Tsuchiya K, Tamaki T (2012) Estrogen regulates hepcidin expression via GPR30-BMP6-dependent signaling in hepatocytes. PLoS One 7(7):e40465. doi:10.1371/journal.pone.0040465
18. Ikeda Y, Enomoto H, Tajima S, Izawa-Ishizawa Y, Kihira Y, Ishizawa K, Tomita S, Tsuchiya K, Tamaki T (2013) Dietary iron restriction inhibits progression of diabetic nephropathy in db/db mice. Am J Physiol Renal Physiol 304(7):F1028–F1036. doi:10.1152/ajprenal.00473.2012
19. Tajima S, Ikeda Y, Sawada K, Yamano N, Horinouchi Y, Kihira Y, Ishizawa K, Izawa-Ishizawa Y, Kawazoe K, Tomita S, Minakuchi K, Tsuchiya K, Tamaki T (2012) Iron reduction by deferoxamine leads to amelioration of adiposity via the regulation of oxidative stress and inflammation in obese and type 2 diabetes KKAy mice. Am J Physiol Endocrinol Metab 302(1):E77–E86. doi:10.1152/ajpendo.00033.2011
20. Mastrogiannaki M, Matak P, Keith B, Simon MC, Vaulont S, Peyssonnaux C (2009) HIF-2alpha, but not HIF-1alpha, promotes iron absorption in mice. J Clin Invest 119(5):1159–1166. doi:10.1172/JCI38499
21. Nemeth E, Tuttle MS, Powelson J, Vaughn MB, Donovan A, Ward DM, Ganz T, Kaplan J (2004) Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 306(5704):2090–2093. doi:10.1126/science.1104742
22. Andriopoulos B Jr, Corradini E, Xia Y, Faasse SA, Chen S, Grgurevic L, Knutson MD, Pietrangelo A, Vukicevic S, Lin HY, Babitt JL (2009) BMP6 is a key endogenous regulator of hepcidin expression and iron metabolism. Nat Genet 41(4):482–487. doi:10.1038/ng.335
23. Meynard D, Kautz L, Darnaud V, Canonne-Hergaux F, Coppin H, Roth MP (2009) Lack of the bone morphogenetic protein BMP6 induces massive iron overload. Nat Genet 41(4):478–481. doi:10.1038/ng.320
24. Courselaud B, Pigeon C, Inoue Y, Inoue J, Gonzalez FJ, Leroyer P, Gilot D, Boudjema K, Guguen-Guillouzo C, Brissot P, Loreal O, Ilyin G (2002) 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 277(43):41163–41170. doi:10.1074/jbc.M202653200
25. Cohen LA, Gutierrez L, Weiss A, Leichtmann-Bardoogo Y, Zhang DL, Crooks DR, Sougrat R, Morgenstern A, Galy B, Hentze MW, Lazaro FJ, Rouault TA, Meyron-Holtz EG (2010) Serum ferritin is derived primarily from macrophages through a nonclassical secretory pathway. Blood 116(9):1574–1584. doi:10.1182/blood-2009-11-253815
26. Atlas SA (2007) The renin-angiotensin aldosterone system: pathophysiological role and pharmacologic inhibition. J Manag Care Pharm 13(8 Suppl B):9–20
27. Catt KJ, Cain MD, Zimmet PZ, Cran E (1969) Blood angiotensin II levels of normal and hypertensive subjects. Br Med J 1(5647):819–821
28. Jacobs A, Worwood M (1975) Ferritin in serum. Clinical and biochemical implications. N Engl J Med 292(18):951–956. doi:10.1056/NEJM197505012921805
29. Yeh KY, Yeh M, Watkins JA, Rodriguez-Paris J, Glass J (2000) Dietary iron induces rapid changes in rat intestinal divalent metal transporter expression. Am J Physiol Gastrointest Liver physiol 279(5):G1070–G1079
30. Donovan A, Lima CA, Pinkus JL, Pinkus GS, Zon LI, Robine S, Andrews NC (2005) The iron exporter ferroportin/Slc40a1 is essential for iron homeostasis. Cell Metab 1(3):191–200. doi:10.1016/j.cmet.2005.01.003
31. Park CH, Valore EV, Waring AJ, Ganz T (2001) Hepcidin, a urinary antimicrobial peptide synthesized in the liver. J Biol Chem 276(11):7806–7810. doi:10.1074/jbc.M008922200
32. Brasse-Lagnel C, Karim Z, Letteron P, Bekri S, Bado A, Beaumont C (2011) Intestinal DMT1 cotransporter is down-regulated by hepcidin via proteasome internalization and degradation. Gastroenterology 140(4):1261–1271 e1261. doi:10.1053/j.gastro.2010.12.037
33. Frazer DM, Wilkins SJ, Becker EM, Vulpe CD, McKie AT, Trinder D, Anderson GJ (2002) Hepcidin expression inversely correlates with the expression of duodenal iron transporters and iron absorption in rats. Gastroenterology 123(3):835–844
34. Pigeon C, Ilyin G, Courselaud B, Leroyer P, Turlin B, Brissot P, Loreal O (2001) A new mouse liver-specific gene, encoding a protein homologous to human antimicrobial peptide hepcidin, is overexpressed during iron overload. J Biol Chem 276(11):7811–7819. doi:10.1074/jbc.M008923200
35. Hentze MW, Muckenthaler MU, Andrews NC (2004) Balancing acts: molecular control of mammalian iron metabolism. Cell 117(3):285–297
36. Xia Y, Babitt JL, Sidis Y, Chung RT, Lin HY (2008) Hemojuvelin regulates hepcidin expression via a selective subset of BMP ligands and receptors independently of neogenin. Blood 111(10):5195–5204. doi:10.1182/blood-2007-09-111567
37. Gkouvatsos K, Wagner J, Papanikolaou G, Sebastiani G, Pantopoulos K (2011) Conditional disruption of mouse HFE2 gene: maintenance of systemic iron homeostasis requires hepatic but not skeletal muscle hemojuvelin. Hepatology 54(5):1800–1807. doi:10.1002/hep.24547
38. Zhang AS, Gao J, Koeberl DD, Enns CA (2010) The role of hepatocyte hemojuvelin in the regulation of bone morphogenic protein-6 and hepcidin expression in vivo. J Biol Chem 285(22):16416–16423. doi:10.1074/jbc.M110.109488
39. Corna G, Campana L, Pignatti E, Castiglioni A, Tagliafico E, Bosurgi L, Campanella A, Brunelli S, Manfredi AA, Apostoli P, Silvestri L, Camaschella C, Rovere-Querini P (2010) Polarization dictates iron handling by inflammatory and alternatively activated macrophages. Haematologica 95(11):1814–1822. doi:10.3324/haematol.2010.023879
40. Recalcati S, Locati M, Marini A, Santambrogio P, Zaninotto F, De Pizzol M, Zammataro L, Girelli D, Cairo G (2010) Differential regulation of iron homeostasis during human macrophage polarized activation. Eur J Immunol 40(3):824–835. doi:10.1002/eji.200939889
41. Ma LJ, Corsa BA, Zhou J, Yang H, Li H, Tang YW, Babaev VR, Major AS, Linton MF, Fazio S, Hunley TE, Kon V, Fogo AB (2011) Angiotensin type 1 receptor modulates macrophage polarization and renal injury in obesity. Am J Physiol Renal Physiol 300(5):F1203–F1213. doi:10.1152/ajprenal.00468.2010
42. Yamamoto S, Yancey PG, Zuo Y, Ma LJ, Kaseda R, Fogo AB, Ichikawa I, Linton MF, Fazio S, Kon V (2011) Macrophage polarization by angiotensin II-type 1 receptor aggravates renal injury-acceleration of atherosclerosis. Arterioscler Thromb Vasc Biol 31(12):2856–2864. doi:10.1161/ATVBAHA.111.237198
43. Rouault TA (2006) The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat Chem Biol 2(8):406–414. doi:10.1038/nchembio807
44. Galy B, Ferring-Appel D, Becker C, Gretz N, Grone HJ, Schumann K, Hentze MW (2013) Iron regulatory proteins control a mucosal block to intestinal iron absorption. Cell Rep 3(3):844–857. doi:10.1016/j.celrep.2013.02.026
45. Vanoaica L, Darshan D, Richman L, Schumann K, Kuhn LC (2010) Intestinal ferritin H is required for an accurate control of iron absorption. Cell Metab 12(3):273–282. doi:10.1016/j.cmet.2010.08.003