The let-7 microRNA enhances heme oxygenase-1 by suppressing Bach1 and attenuates oxidant injury in human hepatocytes

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1819, Issue 11-12, 2012, Pages 1113-1122

  Hou, Weihong ^a   Tian, Qing ^a   Steuerwald, Nury M ^a,b   Schrum, Laura W ^a,b   Bonkovsky, Herbert L ^a,b,c,d  

^a CAROLINAS MEDICAL CENTER   (United States)

^b UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Bach1; Heme oxygenase1; Huh 7 cell; Let 7; MicroRNA; Oxidative stress

Indexed keywords

BACH1 PROTEIN; HEME OXYGENASE 1; LET 7 MICRORNA; LET 7A MICRORNA; LET 7B MICRORNA; LET 7C MICRORNA; LET 7E MICRORNA; LUCIFERASE; MICRORNA; MICRORNA 98; PROTEIN; TERT BUTYL HYDROPEROXIDE; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; CELL DAMAGE; CELL PROTECTION; CELL STRAIN HEPG2; ENZYME ASSAY; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LIVER CELL; LIVER PROTECTION; MOLECULAR MIMICRY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

3' UNTRANSLATED REGIONS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEME OXYGENASE-1; HEP G2 CELLS; HEPATOCYTES; HUMANS; MICRORNAS; MUTATION; OXIDATIVE STRESS; REAL-TIME POLYMERASE CHAIN REACTION; TERT-BUTYLHYDROPEROXIDE; UP-REGULATION;

EID: 84867050326     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2012.06.001     Document Type: Article

References (43)

1. Elbirt K.K., Bonkovsky H.L. Heme oxygenase: recent advances in understanding its regulation and role. Proc. Assoc. Am. Physicians 1999, 111:438-447.
2. Bonkovsky H.L., Elbirt K.K. Heme oxygenase: its regulation and role. Oxidative Stress and Aging 2002, 699-706. World Scientific, River Edge, NJ. R.G. Cutler, H. Rodriguez (Eds.).
3. Brugger J., Schick M.A., Brock R.W., Baumann A., Muellenbach R.M., Roewer N., Wunder C. Carbon monoxide has antioxidative properties in the liver involving p38 MAP kinase pathway in a murine model of systemic inflammation. Microcirculation 2010, 17:504-513.
4. Wu T.W., Carey D., Wu J., Sugiyama H. The cytoprotective effects of bilirubin and biliverdin on rat hepatocytes and human erythrocytes and the impact of albumin. Biochem. Cell Biol. 1991, 69:828-834.
5. Zhu Z., Wilson A.T., Mathahs M.M., Wen F., Brown K.E., Luxon B.A., Schmidt W.N. Heme oxygenase-1 suppresses hepatitis C virus replication and increases resistance of hepatocytes to oxidant injury. Hepatology 2008, 48:1430-1439.
6. Oyake T., Itoh K., Motohashi H., Hayashi N., Hoshino H., Nishizawa M., Yamamoto M., Igarashi K. Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site. Mol. Cell. Biol. 1996, 16:6083-6095.
7. Ogawa K., Sun J., Taketani S., Nakajima O., Nishitani C., Sassa S., Hayashi N., Yamamoto M., Shibahara S., Fujita H., Igarashi K. Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1. EMBO J. 2001, 20:2835-2843.
8. Kitamuro T., Takahashi K., Ogawa K., Udono-Fujimori R., Takeda K., Furuyama K., Nakayama M., Sun J., Fujita H., Hida W., Hattori T., Shirato K., Igarashi K., Shibahara S. Bach1 functions as a hypoxia-inducible repressor for the heme oxygenase-1 gene in human cells. J. Biol. Chem. 2003, 278:9125-9133.
9. Shan Y., Lambrecht R.W., Ghaziani T., Donohue S.E., Bonkovsky H.L. Role of Bach-1 in regulation of heme oxygenase-1 in human liver cells: insights from studies with small interfering RNAS. J. Biol. Chem. 2004, 279:51769-51774.
10. Shan Y., Lambrecht R.W., Donohue S.E., Bonkovsky H.L. Role of Bach1 and Nrf2 in up-regulation of the heme oxygenase-1 gene by cobalt protoporphyrin. FASEB J. 2006, 20:2651-2653.
11. Hou W., Shan Y., Zheng J., Lambrecht R.W., Donohue S.E., Bonkovsky H.L. Zinc mesoporphyrin induces rapid and marked degradation of the transcription factor Bach1 and up-regulates HO-1. Biochim. Biophys. Acta 2008, 1779:195-203.
12. Hou W., Tian Q., Zheng J., Bonkovsky H.L. MicroRNA-196 represses Bach1 protein and hepatitis C virus gene expression in human hepatoma cells expressing hepatitis C viral proteins. Hepatology 2010, 51:1494-1504.
13. Dhakshinamoorthy S., Jain A.K., Bloom D.A., Jaiswal A.K. Bach1 competes with Nrf2 leading to negative regulation of the antioxidant response element (ARE)-mediated NAD(P)H:quinone oxidoreductase 1 gene expression and induction in response to antioxidants. J. Biol. Chem. 2005, 280:16891-16900.
14. Shan Y., Zheng J., Lambrecht R.W., Bonkovsky H.L. Reciprocal effects of micro-RNA-122 on expression of heme oxygenase-1 and hepatitis C virus genes in human hepatocytes. Gastroenterology 2007, 133:1166-1174.
15. Reinhart B.J., Slack F.J., Basson M., Pasquinelli A.E., Bettinger J.C., Rougvie A.E., Horvitz H.R., Ruvkun G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403:901-906.
16. Pasquinelli A.E., Reinhart B.J., Slack F., Martindale M.Q., Kuroda M.I., Maller B., Hayward D.C., Ball E.E., Degnan B., Muller P., Spring J., Srinivasan A., Fishman M., Finnerty J., Corbo J., Levine M., Leahy P., Davidson E., Ruvkun G. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 2000, 408:86-89.
17. Johnson S.M., Grosshans H., Shingara J., Byrom M., Jarvis R., Cheng A., Labourier E., Reinert K.L., Brown D., Slack F.J. RAS is regulated by the let-7 microRNA family. Cell 2005, 120:635-647.
18. Yu F., Yao H., Zhu P., Zhang X., Pan Q., Gong C., Huang Y., Hu X., Su F., Lieberman J., Song E. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 2007, 131:1109-1123.
19. Wulczyn F.G., Smirnova L., Rybak A., Brandt C., Kwidzinski E., Ninnemann O., Strehle M., Seiler A., Schumacher S., Nitsch R. Post-transcriptional regulation of the let-7 microRNA during neural cell specification. FASEB J. 2007, 21:415-426.
20. Zhao C., Sun G., Li S., Lang M.F., Yang S., Li W., Shi Y. MicroRNA let-7b regulates neural stem cell proliferation and differentiation by targeting nuclear receptor TLX signaling. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:1876-1881.
21. Tzur G., Israel A., Levy A., Benjamin H., Meiri E., Shufaro Y., Meir K., Khvalevsky E., Spector Y., Rojansky N., Bentwich Z., Reubinoff B.E., Galun E. Comprehensive gene and microRNA expression profiling reveals a role for microRNAs in human liver development. PLoS One 2009, 4:e7511.
22. Shimizu S., Takehara T., Hikita H., Kodama T., Miyagi T., Hosui A., Tatsumi T., Ishida H., Noda T., Nagano H., Doki Y., Mori M., Hayashi N. The let-7 family of microRNAs inhibits Bcl-xL expression and potentiates sorafenib-induced apoptosis in human hepatocellular carcinoma. J. Hepatol. 2010, 52:698-704.
23. Lan F.F., Wang H., Chen Y.C., Chan C.Y., Ng S.S., Li K., Xie D., He M.L., Lin M.C., Kung H.F. Hsa-let-7g inhibits proliferation of hepatocellular carcinoma cells by downregulation of c-Myc and upregulation of p16 (INK4A). Int. J. Cancer 2011, 128:319-331.
24. Venugopal S.K., Jiang J., Kim T.H., Li Y., Wang S.S., Torok N.J., Wu J., Zern M.A. Liver fibrosis causes downregulation of miRNA-150 and miRNA-194 in hepatic stellate cells, and their overexpression causes decreased stellate cell activation. Am. J. Physiol. 2010, 298:G101-G106.
25. Wang Y., Lu Y., Toh S.T., Sung W.K., Tan P., Chow P., Chung A.Y., Jooi L.L., Lee C.G. Lethal-7 is down-regulated by the hepatitis B virus x protein and targets signal transducer and activator of transcription 3. J. Hepatol. 2010, 53:57-66.
26. Hou W., Tian Q., Zheng J., Bonkovsky H.L. Zinc mesoporphyrin induces rapid proteasomal degradation of hepatitis C nonstructural 5A protein in human hepatoma cells. Gastroenterology 2010, 138:1909-1919.
27. Gottwein E., Mukherjee N., Sachse C., Frenzel C., Majoros W.H., Chi J.T., Braich R., Manoharan M., Soutschek J., Ohler U., Cullen B.R. A viral microRNA functions as an orthologue of cellular miR-155. Nature 2007, 450:1096-1099.
28. Bolstad B.M., Irizarry R.A., Astrand M., Speed T.P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics (Oxford, England) 2003, 19:185-193.
29. Eisen M.B., Spellman P.T., Brown P.O., Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:14863-14868.
30. Hintze K.J., Katoh Y., Igarashi K., Theil E.C. Bach1 repression of ferritin and thioredoxin reductase1 is heme-sensitive in cells and in vitro and coordinates expression with heme oxygenase1, beta-globin, and NADP(H) quinone (oxido) reductase1. J. Biol. Chem. 2007, 282:34365-34371.
31. Hou W.H., Rossi L., Shan Y., Zheng J.Y., Lambrecht R.W., Bonkovsky H.L. Iron increases HMOX1 and decreases hepatitis C viral expression in HCV-expressing cells. World J. Gastroenterol. 2009, 15:4499-4510.
32. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
33. Bushati N., Cohen S.M. MicroRNA functions. Annu. Rev. Cell Dev. Biol. 2007, 23:175-205.
34. Ghildiyal M., Zamore P.D. Small silencing RNAs: an expanding universe. Nat. Rev. 2009, 10:94-108.
35. Jopling C.L., Yi M., Lancaster A.M., Lemon S.M., Sarnow P. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 2005, 309:1577-1581.
36. Vasudevan S., Tong Y., Steitz J.A. Switching from repression to activation: microRNAs can up-regulate translation. Science (New York, N.Y) 2007, 318:1931-1934.
37. Friedman R.C., Farh K.K., Burge C.B., Bartel D.P. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009, 19:92-105.
38. Beckman J.D., Chen C., Nguyen J., Thayanithy V., Subramanian S., Steer C.J., Vercellotti G.M. Regulation of heme oxygenase-1 protein expression by miR-377 in combination with miR-217. J. Biol. Chem. 2011, 286:3194-3202.
39. Yun J., Frankenberger C.A., Kuo W.L., Boelens M.C., Eves E.M., Cheng N., Liang H., Li W.H., Ishwaran H., Minn A.J., Rosner M.R. Signalling pathway for RKIP and Let-7 regulates and predicts metastatic breast cancer. EMBO J. 2011, 30:4500-4514.
40. Choi J., Ou J.H. Mechanisms of liver injury. III. Oxidative stress in the pathogenesis of hepatitis C virus. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 290:G847-G851.
41. Okuda M., Li K., Beard M.R., Showalter L.A., Scholle F., Lemon S.M., Weinman S.A. Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein. Gastroenterology 2002, 122:366-375.
42. Medina J., Moreno-Otero R. Pathophysiological basis for antioxidant therapy in chronic liver disease. Drugs 2005, 65:2445-2461.
43. Webb C., Twedt D. Oxidative stress and liver disease. Vet. Clin. North Am. 2008, 38:125-135.