The regulation of hepcidin expression by serum treatment: Requirements of the BMP response element and STAT- and AP-1-binding sites

Gene

Volumn 551, Issue 2, 2014, Pages 119-126

  Kanamori, Yohei ^a   Murakami, Masaru ^b   Matsui, Tohru ^a   Funaba, Masayuki ^a  

^a KYOTO UNIVERSITY   (Japan)

^b AZABU UNIVERSITY   (Japan)

Author keywords

AP 1; BMP; Hepcidin; Liver; Serum

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; BONE MORPHOGENETIC PROTEIN RESPONSE ELEMENT; HEPCIDIN; MESSENGER RNA; PROTEIN C FOS; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; STAT PROTEIN; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR JUNB; UNCLASSIFIED DRUG; 6 [4 (1 PIPERAZINYL)PHENYL] 3 (4 QUINOLINYL)PYRAZOLO[1,5 A]PYRIMIDINE; CULTURE MEDIUM; PROTEIN C JUN; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; HEPG2 CELL LINE; LIVER CELL; MALE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; ANIMAL; CHEMISTRY; CULTURE MEDIUM; CYTOLOGY; DNA RESPONSIVE ELEMENT; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; PHARMACOLOGY; PHOSPHORYLATION; PRIMARY CELL CULTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SERUM; SPRAGUE DAWLEY RAT; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; BASE SEQUENCE; BINDING SITES; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEINS; CELL LINE, TUMOR; CULTURE MEDIA; GENE EXPRESSION REGULATION; HEP G2 CELLS; HEPATOCYTES; HEPCIDINS; HUMANS; MALE; MUTATION; PHOSPHORYLATION; PRIMARY CELL CULTURE; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-JUN; PYRAZOLES; PYRIMIDINES; RATS, SPRAGUE-DAWLEY; RESPONSE ELEMENTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SERUM; STAT TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR AP-1;

EID: 84908399647     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2014.08.037     Document Type: Article

References (46)

1. Anderson C.P., Shen M., Eisenstein R.S., Leibold E.A. Mammalian iron metabolism and its control by iron regulatory proteins. Biochim. Biophys. Acta 2012, 1823:1468-1483.
2. Andriopoulos B., Corradini E., Xia Y., Faasse S.A., Chen S., Grgurevic L., Knutson M.D., Pietrangelo A., Vukicevic S., Lin H.Y., Babitt J.L. BMP6 is a key endogenous regulator of hepcidin expression and iron metabolism. Nat. Genet. 2009, 41:482-487.
3. Asano H., Yamada T., Hashimoto O., Umemoto T., Sato R., Ohwatari S., Kanamori Y., Terachi T., Funaba M., Matsui T. Diet-induced changes in Ucp1 expression in bovine adipose tissues. Gen. Comp. Endocrinol. 2013, 184:87-92.
4. Botelho F.M., Edwards D.R., Richards C.D. Oncostatin M stimulates c-Fos to bind a transcriptionally responsive AP-1 element within the tissue inhibitor of metalloproteinase-1 promoter. J. Biol. Chem. 1998, 273:5211-5218.
5. Busnadiego O., González-Santamaría J., Lagares D., Guinea-Viniegra J., Pichol-Thievend C., Muller L., Rodríguez-Pascual F. LOXL4 is induced by transforming growth factor β1 through Smad and JunB/Fra2 and contributes to vascular matrix remodeling. Mol. Cell. Biol. 2013, 33:2388-2401.
6. Casanovas G., Mleczko-Sanecka K., Altamura S., Hentze M.W., Muckenthaler M.U. Bone morphogenetic protein (BMP)-responsive elements located in the proximal and distal hepcidin promoter are critical for its response to HJV/BMP/SMAD. J. Mol. Med. (Berl.) 2009, 87:471-480.
7. Chung B., Verdier F., Matak P., Deschemin J.C., Mayeux P., Vaulont S. Oncostatin M is a potent inducer of hepcidin, the iron regulatory hormone. FASEB J. 2010, 24:2093-2103.
8. Duran E.M., Shapshak P., Worley J., Minagar A., Ziegler F., Haliko S., Moleon-Borodowsky I., Haslett P.A. Presenilin-1 detection in brain neurons and FOXP3 in peripheral blood mononuclear cells: normalizer gene selection for real time reverse transcriptase PCR using the deltadeltaCt method. Front. Biosci. 2005, 10:2955-2965.
9. Finberg K.E. Regulation of systemic iron homeostasis. Curr. Opin. Hematol. 2013, 20:208-214.
10. Funaba M., Murakami M. A sensitive detection of phospho-Smad1/5/8 and Smad2 in Western blot analyses. J. Biochem. Biophys. Methods 2008, 70:816-819.
11. Funaba M., Ikeda T., Murakami M., Ogawa K., Nishino Y., Tsuchida K., Sugino H., Abe M. Transcriptional regulation of mouse mast cell protease-7 by TGF-β. Biochim. Biophys. Acta 2006, 1759:166-170.
12. Ginsberg M., Czeko E., Müller P., Ren Z., Chen X., Darnell J.E. Amino acid residues required for physical and cooperative transcriptional interaction of STAT3 and AP-1 proteins c-Jun and c-Fos. Mol. Cell. Biol. 2007, 27:6300-6308.
13. Guo W., Bachman E., Li M., Roy C.N., Blusztajn J., Wong S., Chan S.Y., Serra C., Jasuja R., Travison T.G., Muckenthaler M.U., Nemeth E., Bhasin S. Testosterone administration inhibits hepcidin transcription and is associated with increased iron incorporation into red blood cells. Aging Cell 2013, 12:280-291.
14. Hentze M.W., Muckenthaler M.U., Galy B., Camaschella C. Two to tango: regulation of mammalian iron metabolism. Cell 2010, 142:24-38.
15. Herrera B., Inman G.J. A rapid and sensitive bioassay for the simultaneous measurement of multiple bone morphogenetic proteins. Identification and quantification of BMP4, BMP6 and BMP9 in bovine and human serum. BMC Cell Biol. 2009, 10:20.
16. Hess J., Angel P., Schorpp-Kistner M. AP-1 subunits: quarrel and harmony among siblings. J. Cell Sci. 2004, 117:5965-5973.
17. Ihle J.N. The Stat family in cytokine signaling. Curr. Opin. Cell Biol. 2001, 13:211-217.
18. Kanamori Y., Murakami M., Matsui T., Funaba M. Hepcidin expression in liver cells: evaluation of mRNA levels and transcriptional regulation. Gene 2014, 546:50-55.
19. Kanda J., Uchiyama T., Tomosugi N., Higuchi M., Uchiyama T., Kawabata H. Oncostatin M and leukemia inhibitory factor increase hepcidin expression in hepatoma cell lines. Int. J. Hematol. 2009, 90:545-552.
20. Kim S.J., Angel P., Lafyatis R., Hattori K., Kim K.Y., Sporn M.B., Karin M., Roberts A.B. Autoinduction of transforming growth factor β1 is mediated by the AP-1 complex. Mol. Cell. Biol. 1990, 10:1492-1497.
21. Lee P.L., Beutler E. Regulation of hepcidin and iron-overload disease. Annu. Rev. Pathol. 2009, 4:489-515.
22. Liberati N.T., Datto M.B., Frederick J.P., Shen X., Wong C., Rougier-Chapman E.M., Wang X.F. Smads bind directly to the Jun family of AP-1 transcription factors. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:4844-4849.
23. Maes K., Nemeth E., Roodman G.D., Huston A., Esteve F., Freytes C., Callander N., Katodritou E., Tussing-Humphreys L., Rivera S., Vanderkerken K., Lichtenstein A., Ganz T. In anemia of multiple myeloma, hepcidin is induced by increased bone morphogenetic protein 2. Blood 2010, 116:3635-3644.
24. Massagué J. TGFβ signalling in context. Nat. Rev. Mol. Cell Biol. 2012, 13:616-630.
25. Meynard D., Kautz L., Darnaud V., Canonne-Hergaux F., Coppin H., Roth M.P. Lack of the bone morphogenetic protein BMP6 induces massive iron overload. Nat. Genet. 2009, 41:478-481.
26. Miyazono K., Kamiya Y., Morikawa M. Bone morphogenetic protein receptors and signal transduction. J. Biochem. 2010, 147:35-51.
27. Muckenthaler M.U. Fine tuning of hepcidin expression by positive and negative regulators. Cell Metab. 2008, 8:1-3.
28. Nemeth E., Valore E.V., Territo M., Schiller G., Lichtenstein A., Ganz T. Hepcidin, a putative mediator of anemia of inflammation, is a type II acute-phase protein. Blood 2003, 101:2461-2463.
29. Ohta H., Wakitani S., Tensho K., Horiuchi H., Wakabayashi S., Saito N., Nakamura Y., Nozaki K., Imai Y., Takaoka K. The effects of heat on the biological activity of recombinant human bone morphogenetic protein-2. J. Bone Miner. Metab. 2005, 23:420-425.
30. Ransone L.J., Visvader J., Wamsley P., Verma I.M. Trans-dominant negative mutants of Fos and Jun. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:3806-3810.
31. Sakaki-Yumoto M., Katsuno Y., Derynck R. TGF-β family signaling in stem cells. Biochim. Biophys. Acta 2013, 1830:2280-2296.
32. Shanmugam N.K., Cherayil B.J. Serum-induced up-regulation of hepcidin expression involves the bone morphogenetic protein signaling pathway. Biochem. Biophys. Res. Commun. 2013, 441:383-386.
33. Shaulian E., Karin M. AP-1 as a regulator of cell life and death. Nat. Cell Biol. 2002, 4:E131-E136.
34. Smith C.L., Arvedson T.L., Cooke K.S., Dickmann L.J., Forte C., Li H., Merriam K.L., Perry V.K., Tran L., Rottman J.B., Maxwell J.R. IL-22 regulates iron availability in vivo through the induction of hepcidin. J. Immunol. 2013, 191:1845-1855.
35. Truksa J., Peng H., Lee P., Beutler E. 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, 103:10289-10293.
36. Truksa J., Lee P., Beutler E. The role of STAT, AP-1, E-box and TIEG motifs in the regulation of hepcidin by IL-6 and BMP-9: lessons from human HAMP and murine Hamp1 and Hamp2 gene promoters. Blood Cells Mol. Dis. 2007, 39:255-262.
37. Truksa J., Lee P., Beutler E. Two BMP responsive elements, STAT, and bZIP/HNF4/COUP motifs of the hepcidin promoter are critical for BMP, SMAD1, and HJV responsiveness. Blood 2009, 113:688-695.
38. Verga Falzacappa M.V., Vujic Spasic M., Kessler R., Stolte J., Hentze M.W., Muckenthaler M.U. STAT3 mediates hepatic hepcidin expression and its inflammatory stimulation. Blood 2007, 109:353-358.
39. Wang R.H., Li C., Xu X., Zheng Y., Xiao C., Zerfas P., Cooperman S., Eckhaus M., Rouault T., Mishra L., Deng C.X. A role of SMAD4 in iron metabolism through the positive regulation of hepcidin expression. Cell Metab. 2005, 2:399-409.
40. Wong C., Rougier-Chapman E.M., Frederick J.P., Datto M.B., Liberati N.T., Li J.M., Wang X.F. Smad3-Smad4 and AP-1 complexes synergize in transcriptional activation of the c-Jun promoter by transforming growth factor β. Mol. Cell. Biol. 1999, 19:1821-1830.
41. Wrighting D.M., Andrews N.C. Interleukin-6 induces hepcidin expression through STAT3. Blood 2006, 108:3204-3209.
42. Wu X., Yung L.M., Cheng W.H., Yu P.B., Babitt J.L., Lin H.Y., Xia Y. Hepcidin regulation by BMP signaling in macrophages is lipopolysaccharide dependent. PLoS One 2012, 7:e44622.
43. Yu P.B., Deng D.Y., Lai C.S., Hong C.C., Cuny G.D., Bouxsein M.L., Hong D.W., McManus P.M., Katagiri T., Sachidanandan C., Kamiya N., Fukuda T., Mishina Y., Peterson R.T., Bloch K.D. BMP type I receptor inhibition reduces heterotopic ossification. Nat. Med. 2008, 14:1363-1369.
44. Yu P.B., Hong C.C., Sachidanandan C., Babitt J.L., Deng D.Y., Hoyng S.A., Lin H.Y., Bloch K.D., Peterson R.T. Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat. Chem. Biol. 2008, 4:33-41.
45. Zhang Y., Feng X.H., Derynck R. Smad3 and Smad4 cooperate with c-Jun/c-Fos to mediate TGF-β-induced transcription. Nature 1998, 394:909-913.
46. Zhou G., Myers R., Li Y., Chen Y., Shen X., Fenyk-Melody J., Wu M., Ventre J., Doebber T., Fujii N., Musi N., Hirshman M.F., Goodyear L.J., Moller D.E. Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Invest. 2001, 108:1167-1174.