Expression of microRNA-93 and interleukin-8 during Pseudomonas aeruginosa-mediated induction of proinflammatory responses

American Journal of Respiratory Cell and Molecular Biology

Volumn 50, Issue 6, 2014, Pages 1144-1155

  Fabbri, Enrica ^a   Borgatti, Monica ^a   Montagner, Giulia ^a   Bianchi, Nicoletta ^a   Finotti, Alessia ^b   Lampronti, Ilaria ^a   Bezzerri, Valentino ^c   Dechecchi, Maria Cristina ^c   Cabrini, Giulio ^c   Gambari, Roberto ^a,b  

^a Department of Life Sciences and Biotechnology Section of Biochemistry and Molecular Biology   (Italy)

^b UNIVERSITY OF FERRARA   (Italy)

^c UNIVERSITY HOSPITAL OF VERONA   (Italy)

Author keywords

Cystic fibrosis; In flammation; lung; MicroRNA

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MICRORNA; MICRORNA 93; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; CONSENSUS SEQUENCE; CONTROLLED STUDY; CYSTIC FIBROSIS; DOWN REGULATION; EPITHELIUM CELL; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; UPREGULATION;

3' UNTRANSLATED REGIONS; BRONCHI; CELL LINE; CYSTIC FIBROSIS; DOWN-REGULATION; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INTERLEUKIN-8; MICRORNAS; MINICHROMOSOME MAINTENANCE COMPLEX COMPONENT 7; NF-KAPPA B; PROTEIN PROCESSING, POST-TRANSLATIONAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RNA, MESSENGER; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84901810692     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0160OC     Document Type: Article

References (49)

1. Alvarez-Garcia I, Miska EA. MicroRNA functions in animal development and human disease. Development 2005;132:4653-4662. (Pubitemid 41685276)
2. Sun K, Lai EC. Adult-speci fic functions of animal microRNAs. Nat Rev Genet 2013;14:535-548.
3. Stark A, Brennecke J, Bushati N, Russell RB, Cohen SM. Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3'UTR evolution. Cell 2005;123:1133-1146. (Pubitemid 41785426)
4. Chekulaeva M, Filipowicz W. Mechanisms of miRNA-mediated posttranscriptional regulation in animal cells. Curr Opin Cell Biol 2009;21:452-460.
5. Lin PY, Yu SL, Yang PC. MicroRNA in lung cancer. Br J Cancer 2010;103:1144-1148.
6. Kuhn AR, Schlauch K, Lao R, Halayko AJ, Gerthoffer WT, Singer CA. MicroRNA expression in human airway smooth muscle cells: role of miR-25 in regulation of airway smooth muscle phenotype. Am J Respir Cell Mol Biol 2010;42:506-513.
7. Moschos SA, Williams AE, Perry MM, Birrell MA, Belvisi MG, Lindsay MA. Expression profiling in vivo demonstrates rapid changes in lung microRNA levels following lipopolysaccharide-induced inflammation but not in the anti-inflammatory action of glucocorticoids. BMC Genomics 2007;8:240.
8. Koehler DR, Downey GP, Sweezey NB, Tanswell AK, Hu J. Lung inflammation as a therapeutic target in cystic fibrosis. Am J Respir Cell Mol Biol 2004;31:377-381. (Pubitemid 39330947)
9. Fang Y, Shi C, Manduchi E, Civelek M, Davies PF. MicroRNA-10a regulation of proinflammatory phenotype in athero-susceptible endothelium in vivo and in vitro. Proc Natl Acad Sci USA 2010;107:13450-13455.
10. O'Connell RM, Rao DS, Baltimore D. microRNA regulation of inflammatory responses. Annu Rev Immunol 2012;30:295-312.
11. Li N, Xu X, Xiao B, Zhu ED, Li BS, Liu Z, Tang B, Zou QM, Liang HP, Mao XHH. H. pylori related proinflammatory cytokines contribute to the induction of miR-146a in human gastric epithelial cells. Mol Biol Rep 2012;39:4655-4661.
12. Liu Z, Xiao B, Tang B, Li B, Li N, Zhu E, Guo G, Gu J, Zhuang Y, Liu X, et al. Up-regulated microRNA-146a negatively modulate Helicobacter pylori-induced inflammatory response in human gastric epithelial cells. Microbes Infect 2010;12:854-863.
13. Tang B, Xiao B, Liu Z, Li N, Zhu ED, Li BS, Xie QH, Zhuang Y, Zou QM, Mao XH. Identi fication of MyD88 as a novel target of miR-155, involved in negative regulation of Helicobacter pylori-induced inflammation. FEBS Lett 2010;584:1481-1486.
14. Oglesby IK, McElvaney NG, Greene CM. MicroRNAs in inflammatory lung disease: master regulators or target practice? Respir Res 2010;11:148-160.
15. Gillen AE, Gosalia N, Leir SH, Harris A. MicroRNA regulation of expression of the cystic fibrosis transmembrane conductance regulator gene. Biochem J 2011;438:25-32.
16. Ramachandran S, Karp PH, Jiang P, Ostedgaard LS, Walz AE, Fisher JT, Keshavjee S, Lennox KA, Jacobi AM, Rose SD, et al. A microRNA network regulates expression and biosynthesis of wild-type and DeltaF508 mutant cystic fibrosis transmembrane conductance regulator. Proc Natl Acad Sci USA 2012;109:13362- 13367.
17. Jentsch TJ, Stein V, Weinreich F, Zdebik AA. Molecular structure and physiological function of chloride channels. Physiol Rev 2002;82:503-568. (Pubitemid 34654460)
18. Anderson MP, Gregory RJ, Thompson S, Souza DW, Paul S, Mulligan RC, Smith AE, Welsh MJ. Demonstration that CFTR is a chloride channel by alteration of its anion selectivity. Science 1991;253:202-205. (Pubitemid 21917143)
19. Bonfield TL, Panuska JR, Konstan MW, Hilliard KA, Hilliard JB, Ghnaim H, Berger M. Inflammatory cytokines in cystic fibrosis lungs. Am J Respir Crit Care Med 1995;152:2111-2118.
20. Lyczak JB, Cannon CL, Pier GB. Lung infections associated with cystic fibrosis. Clin Microbiol Rev 2002;15:194-222. (Pubitemid 34303763)
21. McAuley DF, Elborn JS. Cystic fibrosis: basic science. Paediatr Respir Rev 2000;1:93-100.
22. De Rose V. Mechanisms and markers of airway inflammation in cystic fibrosis. Eur Respir J 2002;19:333-340. (Pubitemid 34162837)
23. Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A, Meyer KC, Birrer P, Bellon G, Berger J, Weiss T, et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 2002;109:317-325. (Pubitemid 34141805)
24. Zeitlin PL, Lu L, Rhim J, Cutting G, Stetten G, Kieffer KA, Craig R, Guggino WB. A cystic fibrosis bronchial epithelial cell line: immortalization by adeno-12-SV40 infection. Am J Respir Cell Mol Biol 1991;4:313-319.
25. Zabner J, Karp P, Seiler M, Phillips SL, Mitchell CJ, Saavedra M, Welsh M, Klingelhutz AJ. Development of cystic fibrosis and non cystic fibrosis airway cell lines. Am J Physiol Lung Cell Mol Physiol 2003;284:L844-L854. (Pubitemid 36459031)
26. Dechecchi MC, Nicolis E, Bezzerri V, Vella A, Colombatti M, Assael BM, Mettey Y, Borgatti M, Mancini I, Gambari R, et al. MPB-07 reduces the inflammatory response to Pseudomonas aeruginosa in cystic fibrosis bronchial cells. Am J Respir Cell Mol Biol 2007;36:615-624. (Pubitemid 46676721)
27. Bezzerri V, Borgatti M, Nicolis E, Lampronti I, Dechecchi MC, Mancini I, Rizzotti P, Gambari R, Cabrini G. Transcription factor oligodeoxynucleotides to NF-kappaB inhibit transcription of IL-8 in bronchial cells. Am J Respir Cell Mol Biol 2008;39:86-96. (Pubitemid 351883962)
28. Bianchi N, Zuccato C, Lampronti I, Borgatti M, Gambari R. Expression of miR-210 during erythroid differentiation and induction of gamma-globin gene expression. BMB Rep 2009;42:493-499.
29. Borgatti M, Mancini I, Bianchi N, Guerrini A, Lampronti I, Rossi D, Sacchetti G, Gambari R. Bergamot (Citrus bergamia Risso) fruit extracts and identified components alter expression of interleukin 8 gene in cystic fibrosis bronchial epithelial cell lines. BMC Biochem 2011;12:15.
30. Penolazzi L, Lambertini E, Tavanti E, Torreggiani E, Vesce F, Gambari R, Piva R. Evaluation of chemokine and cytokine profiles in osteoblast progenitors from umbilical cord blood stem cells by BIOPLEX technology. Cell Biol Int 2008;32:320-325. (Pubitemid 351282502)
31. Cabrini G, Bezzerri V, Mancini I, Nicolis E, Dechecchi MC, Tamanini A, Lampronti I, Piccagli L, Bianchi N, Borgatti M, et al. Targeting transcription factor activity as a strategy to inhibit pro-inflammatory genes involved in cystic fibrosis: decoy oligonucleotides and low-molecular weight compounds. Curr Med Chem 2010;17:4392-4404.
32. Gambari R, Borgatti M, Bezzerri V, Nicolis E, Lampronti I, Dechecchi MC, Mancini I, Tamanini A, Cabrini G. Decoy oligodeoxyribonucleotides and peptide nucleic acids-DNA chimeras targeting nuclear factor kappa-B: inhibition of IL-8 gene expression in cystic fibrosis cells infected with Pseudomonas aeruginosa. Biochem Pharmacol 2010;80:1887-1894.
33. Bezzerri V, Borgatti M, Finotti A, Tamanini A, Gambari R, Cabrini G. Mapping the transcriptional machinery of the IL-8 gene in human bronchial epithelial cells. J Immunol 2011;187:6069-6081.
34. Chuang TD, Luo X, Panda H, Chegini N. miR-93/106b and their host gene, MCM7, are differentially expressed in leiomyomas and functionally target F3 and IL-8. Mol Endocrinol 2012;26:1028-1042.
35. Du L, Schageman JJ, Subauste MC, Saber B, Hammond SM, Prudkin L, Wistuba II, Ji L, Roth JA, Minna JD, et al. miR-93, miR-98, and miR-197 regulate expression of tumor suppressor gene FUS1. Mol Cancer Res 2009;7:1234-1243.
36. Poliseno L, Salmena L, Riccardi L, Fornari A, Song MS, Hobbs RM, Sportoletti P, Varmeh S, Egia A, Fedele G, et al. Identification of the miR-106bz25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation. Sci Signal 2010;3:ra29.
37. Fang L, Deng Z, Shatseva T, Yang J, Peng C, Du WW, Yee AJ, Ang LC, He C, Shan SW, et al. MicroRNA miR-93 promotes tumor growth and angiogenesis by targeting integrin-b8. Oncogene 2011;30:806-821.
38. Borchert GM, Holton NW, Larson ED. Repression of human activation induced cytidine deaminase by miR-93 and miR-155. BMC Cancer 2011;11:347.
39. Fu X, Tian J, Zhang L, Chen Y, Hao Q. Involvement of microRNA-93, a new regulator of PTEN/Akt signaling pathway, in regulation of chemotherapeutic drug cisplatin chemosensitivity in ovarian cancer cells. FEBS Lett 2012;586:1279-1286.
40. Petrocca F, Visone R, Onelli MR, Shah MH, Nicoloso MS, de Martino I, Iliopoulos D, Pilozzi E, Liu CG, Negrini M, et al. E2F1-regulated microRNAs impair TGFbeta-dependent cell-cycle arrest and apoptosis in gastric cancer. Cancer Cell 2008;13:272-286. (Pubitemid 351318375)
41. Zhao ZN, Bai JX, Zhou Q, Yan B, Qin WW, Jia LT, Meng YL, Jin BQ, Yao LB, Wang T, et al. TSA suppresses miR-106b-93-25 cluster expression through downregulation of MYC and inhibits proliferation and induces apoptosis in human EMC. PLoS ONE 2012;7:e45133.
42. Fabbri E, Manicardi A, Tedeschi T, Sforza S, Bianchi N, Brognara E, Finotti A, Breveglieri G, Borgatti M, Corradini R, et al. Modulation of the biological activity of microRNA-210 with peptide nucleic acids (PNAs). ChemMedChem 2011;6:2192-2202.
43. Ma L, Reinhardt F, Pan E, Soutschek J, Bhat B, Marcusson EG, Teruya-Feldstein J, Bell GW, Weinberg RA. Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nat Biotechnol 2010;28:341-347.
44. Brock M, Samillan VJ, Trenkmann M, Schwarzwald C, Ulrich S, Gay RE, Gassmann M, Ostergaard L, Gay S, Speich R, Huber LC. AntagomiR directed against miR-20a restores functional BMPR2 signalling and prevents vascular remodeling in hypoxia-induced pulmonary hypertension. Eur Heart J (In press)
45. Cohen TS, Prince A. Cystic fibrosis: a mucosal immunodeficiency syndrome. Nat Med 2012;18:509-519.
46. Long J, Wang Y, Wang W, Chang BH, Danesh FR. Identification of microRNA-93 as a novel regulator of vascular endothelial growth factor in hyperglycemic conditions. J Biol Chem 2010;285:23457-23465.
47. Yeung ML, Yasunaga J, Bennasser Y, Dusetti N, Harris D, Ahmad N, Matsuoka M, Jeang KT. Roles for microRNAs, miR-93 and miR-130b, and tumor protein 53-induced nuclear protein 1 tumor suppressor in cell growth dysregulation by human T-cell lymphotrophic virus 1. Cancer Res 2008;68:8976-8985.
48. Liu S, Patel SH, Ginestier C, Ibarra I, Martin-Trevino R, Bai S, McDermott SP, Shang L, Ke J, Ou SJ, et al . MicroRNA93 regulates proliferation and differentiation of normal and malignant breast stem cells. PLoS Genet 2012;8:e1002751.
49. Bhattacharyya S, Balakathiresan NS, Dalgard C, Gutti U, Armistead D, Jozwik C, Srivastava M, Pollard HB, Biswas R. Elevated miR-155 promotes inflammation in cystic fibrosis by driving hyperexpression of interleukin-8. J Biol Chem 2011;286:11604-11615.