MicroRNA-130a is up-regulated in mouse liver by iron deficiency and targets the bone morphogenetic protein (BMP) receptor ALK2 to attenuate BMP signaling and hepcidin transcription

Journal of Biological Chemistry

Volumn 289, Issue 34, 2014, Pages 23796-23808

  Zumbrennen Bullough, Kimberly B ^a   Wu, Qifang ^a   Core, Amanda B ^a   Canali, Susanna ^a   Chen, Wenjie ^a   Theurl, Igor ^a   Meynard, Delphine ^a   Babitt, Jodie L ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALS; RNA; TRANSCRIPTION;

BIOLOGIC SYSTEMS; BONE MORPHOGENETIC PROTEINS; DOWN-REGULATION; IRON AVAILABILITY; IRON DEFICIENCY; IRON HOMEOSTASIS; PEPTIDE HORMONES; UNTRANSLATED REGIONS;

IRON;

BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; BONE MORPHOGENETIC PROTEIN RECEPTOR TYPE 1 ALK2; HEPCIDIN; IRON; MICRORNA; MICRORNA 130A; SMAD PROTEIN; SMAD4 PROTEIN; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; MIRN130 MICRORNA, HUMAN; PRIMER DNA;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BMP6 GENE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION REGULATION; GENETIC STABILITY; HEMATOLOGICAL PARAMETERS; HORMONAL REGULATION; HORMONE INHIBITION; HUMAN; HUMAN CELL; IN VIVO STUDY; IRON BALANCE; IRON BLOOD LEVEL; IRON DEFICIENCY; IRON RESTRICTION; MALE; MOUSE; NONHUMAN; NUCLEOTIDE BINDING SITE; NUTRIENT AVAILABILITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN RNA BINDING; PROTEIN TARGETING; RECEPTOR DOWN REGULATION; RNA DEGRADATION; SIGNAL TRANSDUCTION; TISSUE LEVEL; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; C57BL MOUSE; CELL LINE; DEFICIENCY; GENETIC TRANSCRIPTION; GENETICS; LIVER; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; CELL LINE; DNA PRIMERS; FEMALE; HEPCIDINS; HUMANS; IRON; LIVER; MALE; MICE; MICE, INBRED C57BL; MICRORNAS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84906545323     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.577387     Document Type: Article

References (35)

1. Ganz, T., and Nemeth, E. (2012) Hepcidin and iron homeostasis. Biochim. Biophys. Acta 1823, 1434-1443
2. Babitt, J. L., Huang, F. W., Wrighting, D. M., Xia, Y., Sidis, Y., Samad, T. A., Campagna, J. A., Chung, R. T., Schneyer, A. L., Woolf, C. J., Andrews, N. C., and Lin, H. Y. (2006) Bone morphogenetic protein signaling by hemojuvelin regulates hepcidin expression. Nat. Genet. 38, 531-539
3. Andriopoulos, B., Jr., Corradini, E., Xia, Y., Faasse, S. A., Chen, S., Grgurevic, L., Knutson, M. D., Pietrangelo, A., Vukicevic, S., Lin, H. Y., and Babitt, J. L. (2009) BMP6 is a key endogenous regulator of hepcidin expression and iron metabolism. Nat. Genet. 41, 482-487
4. Meynard, D., Kautz, L., Darnaud, V., Canonne-Hergaux, F., Coppin, H., and Roth, M. P. (2009) Lack of the bone morphogenetic protein BMP6 induces massive iron overload. Nat. Genet. 41, 478-481
5. Yu, P. B., Hong, C. C., Sachidanandan, C., Babitt, J. L., Deng, D. Y., Hoyng, S. A., Lin, H. Y., Bloch, K. D., and Peterson, R. T. (2008) Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat. Chem. Biol. 4, 33-41
6. Corradini, E., Meynard, D., Wu, Q., Chen, S., Ventura, P., Pietrangelo, A., and Babitt, J. L. (2011) Serum and liver iron differently regulate the bone morphogenetic protein 6 (BMP6)-SMAD signaling pathway in mice. Hepatology 54, 273-284
7. Kautz, L., Meynard, D., Monnier, A., Darnaud, V., Bouvet, R., Wang, R. H., Deng, C., Vaulont, S., Mosser, J., Coppin, H., and Roth, M. P. (2008) Iron regulates phosphorylation of Smad1/5/8 and gene expression of Bmp6, Smad7, Id1, and Atoh8 in the mouse liver. Blood 112, 1503-1509
8. Corradini, E., Garuti, C., Montosi, G., Ventura, P., Andriopoulos, B., Jr., Lin, H. Y., Pietrangelo, A., and Babitt, J. L. (2009) Bone morphogenetic protein signaling is impaired in an HFE knockout mouse model of hemochromatosis. Gastroenterology 137, 1489-1497
9. Steinbicker, A. U., Bartnikas, T. B., Lohmeyer, L. K., Leyton, P., Mayeur, C., Kao, S. M., Pappas, A. E., Peterson, R. T., Bloch, D. B., Yu, P. B., Fleming, M. D., and Bloch, K. D. (2011) Perturbation of hepcidin expression by BMP type I receptor deletion induces iron overload in mice. Blood 118, 4224-4230
10. Xia, Y., Babitt, J. L., Sidis, Y., Chung, R. T., Lin, H. Y. (2008) Hemojuvelin regulates hepcidin expression via a selective subset of BMP ligands and receptors independently of neogenin. Blood 111, 5195-5204
11. Sayed, D., and Abdellatif, M. (2011) MicroRNAs in development and disease. Physiol. Rev. 91, 827-887
12. Castoldi, M., and Muckenthaler, M. U. (2012) Regulation of iron homeostasis by microRNAs. Cell. Mol. Life Sci. 10.1007/s00018-012-1031-4
13. Castoldi, M., Vujic Spasic, M., Altamura, S., Elmén, J., Lindow, M., Kiss, J., Stolte, J., Sparla, R., D'Alessandro, L. A., Klingmüller, U., Fleming, R. E., Longerich, T., Gröne, H. J., Benes, V., Kauppinen, S., Hentze, M. W., and Muckenthaler, M. U. (2011) The liver-specific microRNA miR-122 controls systemic iron homeostasis in mice. J. Clin. Invest. 121, 1386-1396
14. Faller, M., Matsunaga, M., Yin, S., Loo, J. A., and Guo, F. (2007) Heme is involved in microRNA processing. Nat. Struct. Mol. Biol. 14, 23-29
15. Li, Y., Lin, L., Li, Z., Ye, X., Xiong, K., Aryal, B., Xu, Z., Paroo, Z., Liu, Q., He, C., and Jin, P. (2012) Iron homeostasis regulates the activity of the microRNA pathway through poly(C)-binding protein 2. Cell Metab. 15, 895-904
16. Babitt, J. L., Huang, F. W., Xia, Y., Sidis, Y., Andrews, N. C., and Lin, H. Y. (2007) Modulation of bone morphogenetic protein signaling in vivo regulates systemic iron balance. J. Clin. Invest. 117, 1933-1939
17. Meynard, D., Vaja, V., Sun, C. C., Corradini, E., Chen, S., López-Otín, C., Grgurevic, L., Hong, C. C., Stirnberg, M., Gütschow, M., Vukicevic, S., Babitt, J. L., and Lin, H. Y. (2011) Regulation of TMPRSS6 by BMP6 and iron in human cells and mice. Blood 118, 747-756
18. Zhang, A. S., Xiong, S., Tsukamoto, H., and Enns, C. A. (2004) Localization of iron metabolism-related mRNAs in rat liver indicate that HFE is expressed predominantly in hepatocytes. Blood 103, 1509-1514
19. Häger, M., Pedersen, C. C., Larsen, M. T., Andersen, M. K., Hother, C., Grønbæk, K., Jarmer, H., Borregaard, N., and Cowland, J. B. (2011) MicroRNA-130a-mediated down-regulation of Smad4 contributes to reduced sensitivity to TGF-β1 stimulation in granulocytic precursors. Blood 118, 6649-6659
20. Korchynskyi, O., and ten Dijke, P. (2002) Identification and functional characterization of distinct critically important bone morphogenetic protein- specific response elements in the Id1 promoter. J. Biol. Chem. 277, 4883-4891
21. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675
22. Corradini, E., Schmidt, P. J., Meynard, D., Garuti, C., Montosi, G., Chen, S., Vukicevic, S., Pietrangelo, A., Lin, H. Y., and Babitt, J. L. (2010) BMP6 treatment compensates for the molecular defect and ameliorates hemochromatosis in Hfe knockout mice. Gastroenterology 139, 1721-1729
23. Zhang, A. S., Anderson, S. A., Wang, J., Yang, F., DeMaster, K., Ahmed, R., Nizzi, C. P., Eisenstein, R. S., Tsukamoto, H., and Enns, C. A. (2011) Suppression of hepatic hepcidin expression in response to acute iron depriva tion is associated with an increase of matriptase-2 protein. Blood 117, 1687-1699
24. Theurl, I., Schroll, A., Nairz, M., Seifert, M., Theurl, M., Sonnweber, T., Kulaksiz, H., and Weiss, G. (2011) Pathways for the regulation of hepcidin expression in anemia of chronic disease and iron deficiency anemia in vivo. Haematologica 96, 1761-1769
25. Mole, D. R. (2010) Iron homeostasis and its interaction with prolyl hydroxylases. Antioxid. Redox Signal. 12, 445-458
26. Saito, K., Kondo, E., and Matsushita, M. (2011) MicroRNA 130 family regulates the hypoxia response signal through the P-body protein DDX6. Nucleic Acids Res. 39, 6086-6099
27. Sakamoto, N., Yoshimura, M., Kimura, T., Toyama, K., Sekine-Osajima, Y., Watanabe, M., and Muramatsu, M. (2007) Bone morphogenetic protein- 7 and interferon-α synergistically suppress hepatitis C virus replicon. Biochem. Biophys. Res. Commun. 357, 467-473
28. Silvestri, L., Pagani, A., Nai, A., De Domenico, I., Kaplan, J., and Camaschella, C. (2008) The serine protease matriptase-2 (TMPRSS6) inhibits hepcidin activation by cleaving membrane hemojuvelin. Cell Metab. 8, 502-511
29. Theurl, I., Schroll, A., Sonnweber, T., Nairz, M., Theurl, M., Willenbacher, W., Eller, K., Wolf, D., Seifert, M., Sun, C. C., Babitt, J. L., Hong, C. C., Menhall, T., Gearing, P., Lin, H. Y., and Weiss, G. (2011) Pharmacologic inhibition of hepcidin expression reverses anemia of chronic inflammation in rats. Blood 118, 4977-4984
30. Janssen, H. L., Reesink, H. W., Lawitz, E. J., Zeuzem, S., Rodriguez-Torres, M., Patel, K., van der Meer, A. J., Patick, A. K., Chen, A., Zhou, Y., Persson, R., King, B. D., Kauppinen, S., Levin, A. A., and Hodges, M. R. (2013) Treatment ofHCVinfection by targeting MicroRNA. N. Engl. J. Med. 368, 1685-1694
31. Liang, Y., Ridzon, D., Wong, L., and Chen, C. (2007) Characterization of microRNA expression profiles in normal human tissues. BMC Genomics 8, 166
32. Bhanja Chowdhury, J., Shrivastava, S., Steele, R., Di Bisceglie, A. M., Ray, R., and Ray, R. B. (2012) Hepatitis C virus infection modulates expression of interferon stimulatory gene IFITM1 by upregulating miR-130A. J. Virol. 86, 10221-10225
33. Xu, N., Shen, C., Luo, Y., Xia, L., Xue, F., Xia, Q., and Zhang, J. (2012) Upregulated miR-130a increases drug resistance by regulating RUNX3 and Wnt signaling in cisplatin-treated HCC cell. Biochem. Biophys. Res. Commun. 425, 468-472
34. Boll, K., Reiche, K., Kasack, K., Mörbt, N., Kretzschmar, A. K., Tomm, J. M., Verhaegh, G., Schalken, J., von Bergen, M., Horn, F., and Hackermüller J. (2013) miR-130a, miR-203, and miR-205 jointly repress key oncogenic pathways and are downregulated in prostate carcinoma. Oncogene 32, 277-285
35. Zhang, X., Daucher, M., Armistead, D., Russell, R., and Kottilil, S. (2013) MicroRNA expression profiling in HCV-infected human hepatoma cells identifies potential anti-viral targets induced by interferon-α. PLoS One 8, e55733