The NF-κB family member RelB regulates microRNA miR-146a to suppress cigarette smoke-induced COX-2 protein expression in lung fibroblasts

Toxicology Letters

Volumn 226, Issue 2, 2014, Pages 107-116

  Zago, Michela ^a   Rico de Souza, Angela ^b   Hecht, Emelia ^a   Rousseau, Simon ^a,b   Hamid, Qutayba ^a,b   Eidelman, David H ^a,b   Baglole, Carolyn J ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

Chronic obstructive pulmonary disease; Cigarette smoke; Cyclooxygenase 2; Fibroblast; MicroRNA; NF B

Indexed keywords

CIGARETTE SMOKE; CYCLOOXYGENASE 2; INTERLEUKIN 1BETA; MICRORNA 146A; PROSTAGLANDIN E2; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RELB; TUMOR NECROSIS FACTOR ALPHA;

ADENOVIRUS INFECTION; ANIMAL CELL; ARTICLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; LUNG CANCER; LUNG FIBROBLAST; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA STABILITY; SIGNAL TRANSDUCTION; WILD TYPE;

CHRONIC OBSTRUCTIVE PULMONARY DISEASE; CIGARETTE SMOKE; CYCLOOXYGENASE-2; FIBROBLAST; MICRORNA; NF-ΚB;

ANIMALS; CELLS, CULTURED; CYCLOOXYGENASE 2; DOSE-RESPONSE RELATIONSHIP, DRUG; FIBROBLASTS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; LUNG; MICE; MICE, KNOCKOUT; MICRORNAS; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RNA INTERFERENCE; RNA STABILITY; RNA, MESSENGER; SIGNAL TRANSDUCTION; SMOKE; SMOKING; TIME FACTORS; TRANSCRIPTION FACTOR RELB; TRANSFECTION;

EID: 84896031376     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2014.01.020     Document Type: Article

References (52)

1. Agra Andrieu N., Motino O., Mayoral R., Llorente Izquierdo C., Fernandez-Alvarez A., Bosca L., Casado M., Martin-Sanz P. Cyclooxygenase-2 is a target of microRNA-16 in human hepatoma cells. PLoS One 2012, 7:e50935.
2. Arnson Y., Shoenfeld Y., Amital H. Effects of tobacco smoke on immunity, inflammation and autoimmunity. J. Autoimmun. 2010, 34:J258-J265.
3. Baglole C.J., Bushinsky S.M., Garcia T.M., Kode A., Rahman I., Sime P.J., Phipps R.P. Differential induction of apoptosis by cigarette smoke extract in primary human lung fibroblast strains: implications for emphysema. Am. J. Physiol. Lung Cell. Mol. Physiol. 2006, 291:L19-L29.
4. Baglole C.J., Maggirwar S.B., Gasiewicz T.A., Thatcher T.H., Phipps R.P., Sime P.J. The aryl hydrocarbon receptor attenuates tobacco smoke-induced cyclooxygenase-2 and prostaglandin production in lung fibroblasts through regulation of the NF-κB family member RelB. J. Biol. Chem. 2008, 283:28944-28957.
5. Baglole C.J., Reddy S.Y., Pollock S.J., Feldon S.E., Sime P.J., Smith T.J., Phipps R.P. Isolation and phenotypic characterization of lung fibroblasts. Methods Mol. Med. 2005, 117:115-127.
6. Baglole C.J., Sime P.J., Phipps R.P. Cigarette smoke-induced expression of heme oxygenase-1 in human lung fibroblasts is regulated by intracellular glutathione. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 295:L624-L636.
7. Barnes P.J. Mediators of chronic obstructive pulmonary disease. Pharmacol. Rev. 2004, 56:515-548.
8. Beinke S., Ley S.C. Functions of NF-κB1 and NF-κB2 in immune cell biology. Biochem. J. 2004, 382:393-409.
9. Bren G.D., Solan N.J., Miyoshi H., Pennington K.N., Pobst L.J., Paya C.V. Transcription of the RelB gene is regulated by NF-κB. Oncogene 2001, 20:7722-7733.
10. Carp H., Janoff A. Possible mechanisms of emphysema in smokers. In vitro suppression of serum elastase-inhibitory capacity by fresh cigarette smoke and its prevention by antioxidants. Am. Rev. Respir. Dis. 1978, 118:617-621.
11. Chen Y., Chen P., Hanaoka M., Droma Y., Kubo K. Enhanced levels of prostaglandin E2 and matrix metalloproteinase-2 correlate with the severity of airflow limitation in stable COPD. Respirology 2008, 13:1014-1021.
12. Dejardin E. The alternative NF-κB pathway from biochemistry to biology: pitfalls and promises for future drug development. Biochem. Pharmacol. 2006, 72:1161-1179.
13. Dong B., Nishimura N., Vogel C.F., Tohyama C., Matsumura F. TCDD-induced cyclooxygenase-2 expression is mediated by the nongenomic pathway in mouse MMDD1 macula densa cells and kidneys. Biochem. Pharmacol. 2010, 79:487-497.
14. du Rieu M.C., Torrisani J., Selves J., Al Saati T., Souque A., Dufresne M., Tsongalis G.J., Suriawinata A.A., Carrere N., Buscail L., Cordelier P. MicroRNA-21 is induced early in pancreatic ductal adenocarcinoma precursor lesions. Clin. Chem. 2010, 56:603-612.
15. Edwards M.R., Bartlett N.W., Clarke D., Birrell M., Belvisi M., Johnston S.L. Targeting the NF-κB pathway in asthma and chronic obstructive pulmonary disease. Pharmacol. Ther. 2009, 121:1-13.
16. El Gazzar M., Church A., Liu T., McCall C.E. MicroRNA-146a regulates both transcription silencing and translation disruption of TNF-{α} during TLR4-induced gene reprograming. J. Leukoc. Biol. 2011.
17. Etzrodt M., Cortez-Retamozo V., Newton A., Zhao J., Ng A., Wildgruber M., Romero P., Wurdinger T., Xavier R., Geissmann F., Meylan E., Nahrendorf M., Swirski F.K., Baltimore D., Weissleder R., Pittet M.J. Regulation of monocyte functional heterogeneity by miR-146a and RelB. Cell Rep. 2012, 1:317-324.
18. Fields W.R., Leonard R.M., Odom P.S., Nordskog B.K., Ogden M.W., Doolittle D.J. Gene expression in normal human bronchial epithelial (NHBE) cells following in vitro exposure to cigarette smoke condensate. Toxicol. Sci. 2005, 86:84-91.
19. Grossmann M., Nakamura Y., Grumont R., Gerondakis S. New insights into the roles of ReL/NF-κB transcription factors in immune function, hemopoiesis and human disease. Int. J. Biochem. Cell Biol. 1999, 31:1209-1219.
20. Harper K.A., Tyson-Capper A.J. Complexity of COX-2 gene regulation. Biochem. Soc. Trans. 2008, 36:543-545.
21. Huang R.Y., Chen G.G. Cigarette smoking, cyclooxygenase-2 pathway and cancer. Biochim. Biophys. Acta 2011, 1815:158-169.
22. Hyman R.W., Davidson N. Kinetics of the in vitro inhibition of transcription by actinomycin. J. Mol. Biol. 1970, 50:421-438.
23. Jacque E., Tchenio T., Piton G., Romeo P.H., Baud V. RelA repression of RelB activity induces selective gene activation downstream of TNF receptors. Proc. Natl. Acad. Sci. U S A 2005, 102:14635-14640.
24. Jiang J., Lee E.J., Gusev Y., Schmittgen T.D. Real-time expression profiling of microRNA precursors in human cancer cell lines. Nucleic Acids Res. 2005, 33:5394-5403.
25. Kang Y.J., Mbonye U.R., DeLong C.J., Wada M., Smith W.L. Regulation of intracellular cyclooxygenase levels by gene transcription and protein degradation. Prog. Lipid Res. 2007, 46:108-125.
26. Keene J.D. RNA regulons: coordination of post-transcriptional events. Nat. Rev. Genet. 2007, 8:533-543.
27. Liu E.S., Shin V.Y., Ye Y.N., Luo J.C., Wu W.K., Cho C.H. Cyclooxygenase-2 in cancer cells and macrophages induces colon cancer cell growth by cigarette smoke extract. Eur. J. Pharmacol. 2005, 518:47-55.
28. Liu Z., Lu C.L., Cui L.P., Hu Y.L., Yu Q., Jiang Y., Ma T., Jiao D.K., Wang D., Jia C.Y. MicroRNA-146a modulates TGF-β1-induced phenotypic differentiation in human dermal fibroblasts by targeting SMAD4. Arch. Dermatol. Res. 2012, 304:195-202.
29. Liu Z., Wang D., Hu Y., Zhou G., Zhu C., Yu Q., Chi Y., Cao Y., Jia C., Zou Q. MicroRNA-146a negatively regulates PTGS2 expression induced by Helicobacter pylori in human gastric epithelial cells. J. Gastroenterol. 2013, 48:86-92.
30. Lo D., Quill H., Burkly L., Scott B., Palmiter R.D., Brinster R.L. A recessive defect in lymphocyte or granulocyte function caused by an integrated transgene. Am. J. Pathol. 1992, 141:1237-1246.
31. Madge L.A., May M.J. The NF-κB paradox: RelB induces and inhibits gene expression. Cell Cycle 2011, 10:6-7.
32. Martey C.A., Pollock S.J., Turner C.K., O'Reilly K.M., Baglole C.J., Phipps R.P., Sime P.J. Cigarette smoke induces cyclooxygenase-2 and microsomal prostaglandin E2 synthase in human lung fibroblasts: implications for lung inflammation and cancer. Am. J. Physiol. Lung Cell. Mol. Physiol. 2004, 287:L981-L991.
33. McMillan D.H., Baglole C.J., Thatcher T.H., Maggirwar S., Sime P.J., Phipps R.P. Lung-targeted over expression of the NF-κB member RelB inhibits cigarette smoke-induced inflammation. Am. J. Pathol. 2011, 179:125-133.
34. McMillan D.H., Woeller C.F., Thatcher T.H., Spinelli S.L., Maggirwar S.B., Sime P.J., Phipps R.P. Attenuation of inflammatory mediator production by the NF-κB member RelB is mediated by microRNA-146a in lung fibroblasts. Am. J. Physiol. Lung Cell. Mol. Physiol. 2013, 304:L774-L781.
35. Montuschi P., Kharitonov S.A., Ciabattoni G., Barnes P.J. Exhaled leukotrienes and prostaglandins in COPD. Thorax 2003, 58:585-588.
36. Perkins N.D., Schmid R.M., Duckett C.S., Leung K., Rice N.R., Nabel G.J. Distinct combinations of NF-κB subunits determine the specificity of transcriptional activation. Proc. Natl. Acad. Sci. U S A 1992, 89:1529-1533.
37. Perry M.M., Moschos S.A., Williams A.E., Shepherd N.J., Larner-Svensson H.M., Lindsay M.A. Rapid changes in microRNA-146a expression negatively regulate the IL-1β-induced inflammatory response in human lung alveolar epithelial cells. J. Immunol. 2008, 180:5689-5698.
38. Petkova D.K., Pang L., Range S.P., Holland E., Knox A.J. Immunocytochemical localization of cyclo-oxygenase isoforms in cultured human airway structural cells. Clin. Exp. Allergy 1999, 29:965-972.
39. Profita M., Sala A., Bonanno A., Riccobono L., Ferraro M., La Grutta S., Albano G.D., Montalbano A.M., Gjomarkaj M. Chronic obstructive pulmonary disease and neutrophil infiltration: role of cigarette smoke and cyclooxygenase products. Am. J. Physiol. Lung Cell. Mol. Physiol. 2010, 298:L261-L269.
40. Puga A., Hoffer A., Zhou S., Bohm J.M., Leikauf G.D., Shertzer H.G. Sustained increase in intracellular free calcium and activation of cyclooxygenase-2 expression in mouse hepatoma cells treated with dioxin. Biochem. Pharmacol. 1997, 54:1287-1296.
41. Rico de Souza A., Zago M., Pollock S.J., Sime P.J., Phipps R.P., Baglole C.J. Genetic ablation of the aryl hydrocarbon receptor causes cigarette smoke-induced mitochondrial dysfunction and apoptosis. J. Biol. Chem. 2011, 286:43214-43228.
42. Roth M. Pathogenesis of COPD. Part III. Inflammation in COPD. Int. J. Tuberc. Lung Dis. 2008, 12:375-380.
43. Ryseck R.P., Bull P., Takamiya M., Bours V., Siebenlist U., Dobrzanski P., Bravo R. RelB, a new Rel family transcription activator that can interact with p50-NF-κB. Mol. Cell. Biol. 1992, 12:674-684.
44. Sasaki C.Y., Ghosh P., Longo D.L. Recruitment of RelB to the Csf2 promoter enhances RelA-mediated transcription of granulocyte-macrophage colony-stimulating factor. J. Biol. Chem. 2011, 286:1093-1102.
45. Sato T., Liu X., Nelson A., Nakanishi M., Kanaji N., Wang X., Kim M., Li Y., Sun J., Michalski J., Patil A., Basma H., Holz O., Magnussen H., Rennard S.I. Reduced MiR-146a increases prostaglandin E2 in chronic obstructive pulmonary disease fibroblasts. Am. J. Respir. Crit. Care Med. 2010.
46. Shin V.Y., Jin H., Ng E.K., Cheng A.S., Chong W.W., Wong C.Y., Leung W.K., Sung J.J., Chu K.M. NF-κB targets miR-16 and miR-21 in gastric cancer: involvement of prostaglandin E receptors. Carcinogenesis 2011, 32:240-245.
47. Vogel C.F., Sciullo E., Li W., Wong P., Lazennec G., Matsumura F. RelB, a new partner of aryl hydrocarbon receptor-mediated transcription. Mol. Endocrinol. 2007, 21:2941-2955.
48. Weih F., Carrasco D., Durham S.K., Barton D.S., Rizzo C.A., Ryseck R.P., Lira S.A., Bravo R. Multiorgan inflammation and hematopoietic abnormalities in mice with a targeted disruption of RelB, a member of the NF-κB/Rel family. Cell 1995, 80:331-340.
49. Xia Y., Pauza M.E., Feng L., Lo D. RelB regulation of chemokine expression modulates local inflammation. Am. J. Pathol. 1997, 151:375-387.
50. Yang C.M., Lee I.T., Lin C.C., Yang Y.L., Luo S.F., Kou Y.R., Hsiao L.D. Cigarette smoke extract induces COX-2 expression via a PKCα/c-Src/EGFR, PDGFR/PI3 K/Akt/NF-κB pathway and p300 in tracheal smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 297:L892-L902.
51. Zago M., Sheridan J.A., Nair P., Rico de Souza A., Gallouzi I.E., Rousseau S., Di Marco S., Hamid Q., Eidelman D.H., Baglole C.J. Aryl hydrocarbon receptor-dependent retention of nuclear HuR suppresses cigarette smoke-induced cyclooxygenase-2 expression independent of DNA-binding. PLoS One 2013, 8:e74953.
52. Zhang Y., Cao H.J., Graf B., Meekins H., Smith T.J., Phipps R.P. CD40 engagement up-regulates cyclooxygenase-2 expression and prostaglandin E2 production in human lung fibroblasts. J. Immunol. 1998, 160:1053-1057.