Home LiteratureArticle Details
PMID: 17607365 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Modulation of bone morphogenetic protein signaling in vivo regulates systemic iron balance.

The Journal of clinical investigation ·Vol. 117 ·No. 7 ·2007-07-00 ·Pages 1933-9

Babitt JL, Huang FW, Xia Y, Sidis Y, Andrews NC, Lin HY

Abstract

Systemic iron balance is regulated by hepcidin, a peptide hormone secreted by the liver. By decreasing cell surface expression of the iron exporter ferroportin, hepcidin decreases iron absorption from the intestine and iron release from reticuloendothelial stores. Hepcidin excess has been implicated in the pathogenesis of anemia of chronic disease, while hepcidin deficiency has a key role in the pathogenesis of the iron overload disorder hemochromatosis. We have recently shown that hemojuvelin is a coreceptor for bone morphogenetic protein (BMP) signaling and that BMP signaling positively regulates hepcidin expression in liver cells in vitro. Here we show that BMP-2 administration increases hepcidin expression and decreases serum iron levels in vivo. We also show that soluble hemojuvelin (HJV.Fc) selectively inhibits BMP induction of hepcidin expression in vitro and that administration of HJV.Fc decreases hepcidin expression, increases ferroportin expression, mobilizes splenic iron stores, and increases serum iron levels in vivo. These data support a role for modulators of the BMP signaling pathway in treating diseases of iron overload and anemia of chronic disease.

MeSH Terms
Animals Antimicrobial Cationic Peptides/genetics Bone Morphogenetic Proteins/classification,genetics,metabolism,pharmacology Cation Transport Proteins/genetics,metabolism Cell Line Gene Expression Regulation Hepcidins Humans Interleukin-6/pharmacology Iron/metabolism Ligands Membrane Proteins/genetics,metabolism Mice Mononuclear Phagocyte System/metabolism Signal Transduction/drug effects Solubility Transforming Growth Factor beta/classification,pharmacology
Chemicals
Antimicrobial Cationic Peptides Bone Morphogenetic Proteins Cation Transport Proteins HAMP protein, human Hamp protein, mouse Hepcidins Interleukin-6 Ligands Membrane Proteins Transforming Growth Factor beta metal transporting protein 1 Iron
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Babitt Jodie L
Program in Membrane Biology and Nephrology Division, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA. [email protected]
Huang Franklin W
Xia Yin
Sidis Yisrael
Andrews Nancy C
Lin Herbert Y
References (50)
50 references, click to expand
  1. Bone morphogenetic protein-9. An autocrine/paracrine cytokine in the liver.
    J Biol Chem. 2000 Jun 16;275(24):17937-45 PMID: 10849432
  2. STAT3 is required for IL-6-gp130-dependent activation of hepcidin in vivo.
    Gastroenterology. 2007 Jan;132(1):294-300 PMID: 17241879
  3. Osteogenic protein-1 prevents renal fibrogenesis associated with ureteral obstruction.
    Am J Physiol Renal Physiol. 2000 Jul;279(1):F130-43 PMID: 10894795
  4. LEAP-1, a novel highly disulfide-bonded human peptide, exhibits antimicrobial activity.
    FEBS Lett. 2000 Sep 1;480(2-3):147-50 PMID: 11034317
  5. Characterization of receptors for osteogenic protein-1/bone morphogenetic protein-7 (OP-1/BMP-7) in rat kidneys.
    Kidney Int. 2000 Nov;58(5):1902-11 PMID: 11044210
  6. Hepcidin, a urinary antimicrobial peptide synthesized in the liver.
    J Biol Chem. 2001 Mar 16;276(11):7806-10 PMID: 11113131
  7. A new mouse liver-specific gene, encoding a protein homologous to human antimicrobial peptide hepcidin, is overexpressed during iron overload.
    J Biol Chem. 2001 Mar 16;276(11):7811-9 PMID: 11113132
  8. Bone morphogenetic protein-7 improves renal fibrosis and accelerates the return of renal function.
    J Am Soc Nephrol. 2002 Jan;13 Suppl 1:S14-21 PMID: 11792757
  9. Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter.
    J Biol Chem. 2002 Feb 15;277(7):4883-91 PMID: 11729207
  10. Large-scale analysis of the human and mouse transcriptomes.
    Proc Natl Acad Sci U S A. 2002 Apr 2;99(7):4465-70 PMID: 11904358
  11. RGM is a repulsive guidance molecule for retinal axons.
    Nature. 2002 Sep 26;419(6905):392-5 PMID: 12353034
  12. The gene encoding the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation.
    J Clin Invest. 2002 Oct;110(7):1037-44 PMID: 12370282
  13. Mutant antimicrobial peptide hepcidin is associated with severe juvenile hemochromatosis.
    Nat Genet. 2003 Jan;33(1):21-2 PMID: 12469120
  14. Decreased liver hepcidin expression in the Hfe knockout mouse.
    Blood Cells Mol Dis. 2002 Nov-Dec;29(3):361-6 PMID: 12547226
  15. Disrupted hepcidin regulation in HFE-associated haemochromatosis and the liver as a regulator of body iron homoeostasis.
    Lancet. 2003 Feb 22;361(9358):669-73 PMID: 12606179
  16. Hepcidin, a putative mediator of anemia of inflammation, is a type II acute-phase protein.
    Blood. 2003 Apr 1;101(7):2461-3 PMID: 12433676
  17. Constitutive hepcidin expression prevents iron overload in a mouse model of hemochromatosis.
    Nat Genet. 2003 May;34(1):97-101 PMID: 12704388
  18. Regulatory defects in liver and intestine implicate abnormal hepcidin and Cybrd1 expression in mouse hemochromatosis.
    Nat Genet. 2003 May;34(1):102-7 PMID: 12704390
  19. Mechanisms of TGF-beta signaling from cell membrane to the nucleus.
    Cell. 2003 Jun 13;113(6):685-700 PMID: 12809600
  20. Bone morphogenic protein-7 inhibits progression of chronic renal fibrosis associated with two genetic mouse models.
    Am J Physiol Renal Physiol. 2003 Dec;285(6):F1060-7 PMID: 12915382
  21. Mutations in HFE2 cause iron overload in chromosome 1q-linked juvenile hemochromatosis.
    Nat Genet. 2004 Jan;36(1):77-82 PMID: 14647275
  22. DRAGON: a member of the repulsive guidance molecule-related family of neuronal- and muscle-expressed membrane proteins is regulated by DRG11 and has neuronal adhesive properties.
    J Neurosci. 2004 Feb 25;24(8):2027-36 PMID: 14985445
  23. Balancing acts: molecular control of mammalian iron metabolism.
    Cell. 2004 Apr 30;117(3):285-97 PMID: 15109490
  24. An Hfe-dependent pathway mediates hyposideremia in response to lipopolysaccharide-induced inflammation in mice.
    Nat Genet. 2004 May;36(5):481-5 PMID: 15098034
  25. IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin.
    J Clin Invest. 2004 May;113(9):1271-6 PMID: 15124018
  26. What do BMPs do in mammals? Clues from the mouse short-ear mutation.
    Trends Genet. 1994 Jan;10(1):16-21 PMID: 8146910
  27. Transforming growth factor-beta gene expression in normal and fibrotic rat liver.
    J Hepatol. 1997 Apr;26(4):886-93 PMID: 9126804
  28. Bone morphogenetic protein-6 is expressed in nonparenchymal liver cells and upregulated by transforming growth factor-beta 1.
    Exp Cell Res. 1997 May 1;232(2):263-9 PMID: 9168801
  29. Treatment of rheumatoid arthritis with a recombinant human tumor necrosis factor receptor (p75)-Fc fusion protein.
    N Engl J Med. 1997 Jul 17;337(3):141-7 PMID: 9219699
  30. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene.
    EMBO J. 1998 Jun 1;17(11):3091-100 PMID: 9606191
  31. Osteogenic protein-1 (bone morphogenetic protein-7) reduces severity of injury after ischemic acute renal failure in rat.
    J Clin Invest. 1998 Jul 1;102(1):202-14 PMID: 9649574
  32. Cellular and subcellular localization of the Nramp2 iron transporter in the intestinal brush border and regulation by dietary iron.
    Blood. 1999 Jun 15;93(12):4406-17 PMID: 10361139
  33. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization.
    Science. 2004 Dec 17;306(5704):2090-3 PMID: 15514116
  34. Expression of hepcidin is down-regulated in TfR2 mutant mice manifesting a phenotype of hereditary hemochromatosis.
    Blood. 2005 Jan 1;105(1):376-81 PMID: 15345587
  35. Hepcidin is decreased in TFR2 hemochromatosis.
    Blood. 2005 Feb 15;105(4):1803-6 PMID: 15486069
  36. Regulation of hepcidin transcription by interleukin-1 and interleukin-6.
    Proc Natl Acad Sci U S A. 2005 Feb 8;102(6):1906-10 PMID: 15684062
  37. Anemia of chronic disease.
    N Engl J Med. 2005 Mar 10;352(10):1011-23 PMID: 15758012
  38. DRAGON, a bone morphogenetic protein co-receptor.
    J Biol Chem. 2005 Apr 8;280(14):14122-9 PMID: 15671031
  39. Hemojuvelin is essential for dietary iron sensing, and its mutation leads to severe iron overload.
    J Clin Invest. 2005 Aug;115(8):2180-6 PMID: 16075058
  40. A mouse model of juvenile hemochromatosis.
    J Clin Invest. 2005 Aug;115(8):2187-91 PMID: 16075059
  41. Repulsive guidance molecule (RGMa), a DRAGON homologue, is a bone morphogenetic protein co-receptor.
    J Biol Chem. 2005 Aug 19;280(33):29820-7 PMID: 15975920
  42. Interaction of hemojuvelin with neogenin results in iron accumulation in human embryonic kidney 293 cells.
    J Biol Chem. 2005 Oct 7;280(40):33885-94 PMID: 16103117
  43. Competitive regulation of hepcidin mRNA by soluble and cell-associated hemojuvelin.
    Blood. 2005 Oct 15;106(8):2884-9 PMID: 15998830
  44. A role of SMAD4 in iron metabolism through the positive regulation of hepcidin expression.
    Cell Metab. 2005 Dec;2(6):399-409 PMID: 16330325
  45. Comparative studies of duodenal and macrophage ferroportin proteins.
    Am J Physiol Gastrointest Liver Physiol. 2006 Jan;290(1):G156-63 PMID: 16081760
  46. Bone morphogenetic protein signaling by hemojuvelin regulates hepcidin expression.
    Nat Genet. 2006 May;38(5):531-9 PMID: 16604073
  47. Bone morphogenetic proteins 2, 4, and 9 stimulate murine hepcidin 1 expression independently of Hfe, transferrin receptor 2 (Tfr2), and IL-6.
    Proc Natl Acad Sci U S A. 2006 Jul 5;103(27):10289-93 PMID: 16801541
  48. Hereditary hemochromatosis.
    Biochim Biophys Acta. 2006 Jul;1763(7):700-10 PMID: 16891003
  49. Interleukin-6 induces hepcidin expression through STAT3.
    Blood. 2006 Nov 1;108(9):3204-9 PMID: 16835372
  50. STAT3 mediates hepatic hepcidin expression and its inflammatory stimulation.
    Blood. 2007 Jan 1;109(1):353-8 PMID: 16946298
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2007-07-00
Pages
1933-9
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC1904317
Subset
IM
Grants
NIDDK NIH HHS · K08 DK075846 · United States
NIDDK NIH HHS · R01 DK069533 · United States
NIDDK NIH HHS · R01 DK053813 · United States
NHLBI NIH HHS · T32 HL07623 · United States
NIDDK NIH HHS · R01 DK69533 · United States
NIDDK NIH HHS · K08 DK075846-02 · United States
NIDDK NIH HHS · R01 DK71837 · United States
NHLBI NIH HHS · T32 HL007623 · United States
NIDDK NIH HHS · K08 DK075846-01 · United States
NIDDK NIH HHS · R01 DK053813-10 · United States
NIDDK NIH HHS · R01 DK071837 · United States
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]