The SMAD pathway is required for Hepcidin response during endoplasmic reticulum stress

Endocrinology

Volumn 157, Issue 10, 2016, Pages 3935-3945

  Canali, Susanna ^a,b   Vecchi, Chiara ^a   Garuti, Cinzia ^a   Montosi, Giuliana ^a   Babitt, Jodie L ^b   Pietrangelo, Antonello ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 [4 (1 PIPERAZINYL)PHENYL] 3 (4 QUINOLINYL)PYRAZOLO[1,5 A]PYRIMIDINE; HEPCIDIN; MESSENGER RNA; SMAD PROTEIN; RECEPTOR REGULATED SMAD PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; GENE SILENCING; HEPG2 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; C57BL MOUSE; HEP-G2 CELL LINE; METABOLISM;

ANIMALS; ENDOPLASMIC RETICULUM STRESS; HEP G2 CELLS; HEPCIDINS; HUMANS; MALE; MICE, INBRED C57BL; SIGNAL TRANSDUCTION; SMAD PROTEINS, RECEPTOR-REGULATED;

EID: 84990942595     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2016-1258     Document Type: Article

References (45)

1. KrauseA, NeitzS, Magert HJ, etal. LEAP-1, anovel highly disulfidebonded human peptide, exhibits antimicrobial activity. FEBS Lett. 2000;480(2-3):147-150.
2. Park CH, Valore EV, Waring AJ, Ganz T. Hepcidin, a urinary antimicrobial peptide synthesized in the liver. J Biol Chem. 2001;276(11):7806-7810.
3. Pigeon C, Ilyin G, Courselaud B, et al. A new mouse liver-specific gene, encoding a protein homologous to human antimicrobial peptide hepcidin, is overexpressed during iron overload. J Biol Chem. 2001;276(11):7811-7819.
4. Ganz T. Hepcidin in iron metabolism. Curr Opin Hematol. 2004;11(4):251-254.
5. Nemeth E, Tuttle MS, Powelson J, et al. Hepcidin regulates cellular iron effluxbybinding toferroportin and inducing its internalization. Science. 2004;306(5704):2090-2093.
6. Abboud S, Haile DJ. A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J Biol Chem. 2000;275(26):19906-19912.
7. Donovan A, Brownlie A, Zhou Y, et al. Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter. Nature. 2000;403(6771):776-781.
8. McKie AT, Marciani P, Rolfs A, et al. A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol Cell. 2000;5(2):299-309.
9. Qiao B, Sugianto P, Fung E, et al. Hepcidin-induced endocytosis of ferroportin is dependent on ferroportin ubiquitination. Cell Metab. 2012;15(6):918-924.
10. Ross SL, Tran L, Winters A, et al. Molecular mechanism of hepcidinmediated ferroportin internalization requires ferroportin lysines, not tyrosines or JAK-STAT. Cell Metab. 2012;15(6):905-917.
11. Corradini E, Meynard D, Wu Q, et al. Serum and liver iron differently regulate the bone morphogenetic protein 6 (BMP6)-SMAD signaling pathway in mice. Hepatology. 2011;54(1):273-284.
12. Ramos E, Kautz L, Rodriguez R, et al. Evidence for distinct pathways of hepcidin regulation by acute and chronic iron loading in mice. Hepatology. 2011;53(4):1333-1341.
13. Nemeth E, Rivera S, Gabayan V, et al. IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J Clin Invest. 2004;113(9):1271-1276.
14. Wrighting DM, Andrews NC. Interleukin-6 induces hepcidin expression through STAT3. Blood. 2006;108(9):3204-3209.
15. Pietrangelo A, Dierssen U, Valli L, et al. STAT3 is required for IL-6-gp130-dependent activation of hepcidin in vivo. Gastroenterology. 2007;132(1):294-300.
16. Verga Falzacappa MV, Vujic Spasic M, Kessler R, Stolte J, Hentze MW, Muckenthaler MU. STAT3 mediates hepatic hepcidin expression and its inflammatory stimulation. Blood. 2007;109(1):353-358.
17. Verga Falzacappa MV, Casanovas G, Hentze MW, Muckenthaler MU. A bone morphogenetic protein (BMP)-responsive element in the hepcidin promoter controls HFE2-mediated hepatic hepcidin expression and its response to IL-6 in cultured cells. J Mol Med. 2008;86(5):531-540.
18. Lee P, Peng H, Gelbart T, Wang L, Beutler E. Regulation of hepcidin transcription by interleukin-1 and interleukin-6. Proc Natl Acad Sci USA. 2005;102(6):1906-1910.
19. Armitage AE, Eddowes LA, Gileadi U, et al. Hepcidin regulation by innate immune and infectious stimuli. Blood. 2011;118(15):4129-4139.
20. Smith CL, Arvedson TL, Cooke KS, et al. IL-22 regulates iron availability in vivo through the induction of hepcidin. J Immunol. 2013;191(4):1845-1855.
21. Besson-Fournier C, Latour C, Kautz L, et al. Induction of activin B by inflammatory stimuli up-regulates expression of the iron-regulatory peptide hepcidin through Smad1/5/8 signaling. Blood. 2012;120(2):431-439.
22. Canali S, Core AB, Zumbrennen-Bullough KB, et al. Activin B induces noncanonical SMAD1/5/8 signaling via BMP type I receptors in hepatocytes: evidence for a role in hepcidin induction by inflammation in male mice. Endocrinology. 2016;157(3):1146-1162.
23. Corradini E, Babitt JL, Lin HY. The RGM/DRAGON family of BMP co-receptors. Cytokine Growth Factor Rev. 2009;20(5-6):389-398.
24. Casanovas G, Mleczko-Sanecka K, Altamura S, Hentze MW, Muckenthaler MU. 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. 2009;87(5):471-480.
25. Truksa J, Lee P, Peng H, Flanagan J, Beutler E. The distal location of the iron responsive region of the hepcidin promoter. Blood. 2007;110(9):3436-3437.
26. Core AB, Canali S, Babitt JL. Hemojuvelin and bone morphogenetic protein (BMP) signaling in iron homeostasis. Front Pharmacol. 2014;5:104.
27. Vecchi C, Montosi G, Zhang K, et al. ER stress controls iron metabolism through induction of hepcidin. Science. 2009;325(5942):877-880.
28. MisraJ, ChandaD, Kim DK, etal. Curcumin differentially regulates endoplasmic reticulum stress through transcriptional corepressor SMILE (small heterodimer partner-interacting leucine zipper protein)-mediated inhibition of CREBH (cAMP responsive elementbinding protein H). J Biol Chem. 2011;286(49):41972-41984.
29. Shin DY, Chung J, Joe Y, et al. Pretreatment with CO-releasing molecules suppresses hepcidin expression during inflammation and endoplasmic reticulum stress through inhibition of the STAT3 and CREBH pathways. Blood. 2012;119(11):2523-2532.
30. Zhang C, Wang G, Zheng Z, et al. Endoplasmic reticulum-tethered transcription factor cAMP responsive element-binding protein, hepatocyte specific, regulates hepatic lipogenesis, fatty acid oxidation, and lipolysis upon metabolic stress in mice. Hepatology. 2012;55(4):1070-1082.
31. VecchiC, MontosiG, GarutiC, etal. Gluconeogenic signals regulate iron homeostasis via hepcidin in mice. Gastroenterology. 2014;146(4):1060-1069.
32. SonnweberT, NachbaurD, SchrollA, etal. Hypoxiainduceddownregulation of hepcidin is mediated by platelet derived growth factor BB. Gut. 2014;63(12):1951-1959.
33. UmansL, Vermeire L, Francis A, Chang H, Huylebroeck D, Zwijsen A. Generation of a floxed allele of Smad5 for cre-mediated conditional knockout in the mouse. Genesis. 2003;37(1):5-11.
34. Tremblay KD, Dunn NR, Robertson EJ. Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development. 2001;128(18):3609-3621.
35. Theurl I, Schroll A, Sonnweber T, et al. Pharmacologic inhibition of hepcidin expression reverses anemia of chronic inflammation in rats. Blood. 2011;118(18):4977-4984.
36. Steinbicker AU, Sachidanandan C, Vonner AJ, et al. Inhibition of bone morphogenetic protein signaling attenuates anemia associated with inflammation. Blood. 2011;117(18):4915-4923.
37. Mayeur C, Kolodziej SA, Wang A, et al. Oral administration of a bone morphogenetic protein type I receptor inhibitor prevents the development of anemia of inflammation. Haematologica. 2015;100(2):e68-e71.
38. Yu PB, Deng DY, Lai CS, et al. BMP type I receptor inhibition reduces heterotopic [corrected] ossification. Nat Med. 2008;14(12):1363-1369.
39. Kolb PS, Ayaub EA, Zhou W, Yum V, Dickhout JG, Ask K. The therapeutic effects of 4-phenylbutyric acid in maintaining proteostasis. Int J Biochem Cell Biol. 2015;61:45-52.
40. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem. 2005;74:739-789.
41. WuJ, Kaufman RJ. From acuteERstresstophysiological rolesofthe Unfolded Protein Response. Cell Death Differ. 2006;13(3):374-384.
42. ZhangK, ShenX, WuJ, etal. Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell. 2006;124(3):587-599.
43. Lee MW, Chanda D, Yang J, et al. Regulation of hepatic gluconeogenesis by an ER-bound transcription factor, CREBH. Cell Metab. 2010;11(4):331-339.
44. Zhang N, Subbaramaiah K, Yantiss RK, et al. Id1 expression in endothelial cells of the colon is required for normal response to injury. Am J Pathol. 2015;185(11):2983-2993.
45. Ohta Y, Nakagawa K, Imai Y, Katagiri T, Koike T, Takaoka K. Cyclic AMP enhances Smad-mediated BMP signaling through PKA-CREB pathway. J Bone Miner Metab. 2008;26(5):478-484.