Dynamic regulation of microRNA expression following interferonγ- induced gene transcription

RNA Biology

Volumn 9, Issue 7, 2012, Pages 978-989

  Reinsbach, Susanne E ^a   Nazarov, Petr V ^b   Philippidou, Demetra ^a   Schmitt, Martina ^a   Wienecke Baldacchino, Anke ^a   Muller, Arnaud ^b   Vallar, Laurent ^b   Behrmann, Iris ^a   Kreis, Stephanie ^a  

^a UNIVERSITY OF LUXEMBOURG   (Luxembourg)

^b LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

Author keywords

Dynamic expression; MicroRNA; Time series microarrays; Transcriptional regulation

Indexed keywords

GAMMA INTERFERON; MICRORNA; MICRORNA 27A; MICRORNA 30A; MICRORNA 34A; STAT1 PROTEIN; UNCLASSIFIED DRUG; INTERFERON REGULATORY FACTOR 1; IRF1 PROTEIN, HUMAN; STAT1 PROTEIN, HUMAN; TRANSCRIPTOME;

ARTICLE; COMPUTER PROGRAM; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MELANOMA CELL; MICROARRAY ANALYSIS; CLUSTER ANALYSIS; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; TRANSCRIPTION INITIATION; TUMOR CELL LINE;

CELL LINE, TUMOR; CLUSTER ANALYSIS; GENE EXPRESSION REGULATION; HUMANS; INTERFERON REGULATORY FACTOR-1; INTERFERON-GAMMA; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; STAT1 TRANSCRIPTION FACTOR; TRANSCRIPTIONAL ACTIVATION; TRANSCRIPTOME;

EID: 84865278613     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.20494     Document Type: Article

References (59)

1. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004; 23:4051-60; PMID:15372072; http://dx.doi.org/10.1038/sj.emboj.7600385.
2. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010; 11:597-610; PMID:20661255.
3. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 2009; 11:228-34; PMID:19255566; http://dx.doi.org/10.1038/ncb0309-228.
4. Altuvia Y, Landgraf P, Lithwick G, Elefant N, Pfeffer S, Aravin A, et al. Clustering and conservation patterns of human microRNAs. Nucleic Acids Res 2005; 33:2697-706; PMID:15891114; http://dx.doi.org/10.1093/nar/gki567.
5. He C, Li Z, Chen P, Huang H, Hurst LD, Chen J. Young intragenic miRNAs are less coexpressed with host genes than old ones: implications of miRNA-host gene coevolution. Nucleic Acids Res 2012; PMID:22238379; http://dx.doi.org/10. 1093/nar/gkr1312.
6. Guo L, Lu Z. Global expression analysis of miRNA gene cluster and family based on isomiRs from deep sequencing data. Comput Biol Chem 2010; 34:165-71; PMID:20619743; http://dx.doi.org/10.1016/j.comp-biolchem.2010.06.001.
7. Kim VN, Han J, Siomi MC. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 2009; 10:126-39; PMID:19165215; http://dx.doi.org/10.1038/nrm2632.
8. Ozsolak F, Poling LL, Wang Z, Liu H, Liu XS, Roeder RG, et al. Chromatin structure analyses identify miRNA promoters. Genes Dev 2008; 22:3172-83; PMID:19056895; http://dx.doi.org/10.1101/gad.1706508.
9. Baskerville S, Bartel DP. Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 2005; 11:241-7; PMID:15701730; http://dx.doi.org/10.1261/rna.7240905.
10. Baek D, Villén J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature 2008; 455:64-71; PMID:18668037; http://dx.doi.org/10.1038/nature07242.
11. Bartel DP, Chen CZ. Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat Rev Genet 2004; 5:396-400; PMID:15143321; http://dx.doi.org/10.1038/nrg1328.
12. Wang J, Lu M, Qiu C, Cui Q. TransmiR: a transcription factor-microRNA regulation database. Nucleic Acids Res 2010; 38:119-22; PMID:19786497; http://dx.doi.org/10.1093/nar/gkp803.
13. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, et al. Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 2006; 38:1060-5; PMID:16878133; http://dx.doi.org/10.1038/ng1855.
14. Kulshreshtha R, Ferracin M, Wojcik SE, Garzon R, Alder H, Agosto-Perez FJ, et al. A microRNA signature of hypoxia. Mol Cell Biol 2007; 27:1859-67; PMID:17194750; http://dx.doi.org/10.1128/MCB.01395-06.
15. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 2005; 435:839-43; PMID:15944709; http://dx.doi.org/10.1038/nature03677.
16. Löffler D, Brocke-Heidrich K, Pfeifer G, Stocsits C, Hackermüller J, Kretzschmar AK, et al. Interleukin-6 dependent survival of multiple myeloma cells involves the Stat3-mediated induction of microRNA-21 through a highly conserved enhancer. Blood 2007; 110:1330-3; PMID:17496199; http://dx.doi.org/10.1182/blood-2007-03-081133.
17. Meng F, Henson R, Wehbe-Janek H, Smith H, Ueno Y, Patel T. The MicroRNA let-7a modulates interleukin-6-dependent STAT-3 survival signaling in malignant human cholangiocytes. J Biol Chem 2007; 282:8256-64; PMID:17220301; http://dx.doi.org/10.1074/jbc.M607712200.
18. Kohanbash G, Okada H. MicroRNAs and STAT interplay. Semin Cancer Biol 2012; 22:70-5; PMID:22210182; http://dx.doi.org/10.1016/j.sem-cancer.2011.12. 010.
19. Kutty RK, Nagineni CN, Samuel W, Vijayasarathy C, Hooks JJ, Redmond TM. Inflammatory cytokines regulate microRNA-155 expression in human retinal pigment epithelial cells by activating JAK/STAT pathway. Biochem Biophys Res Commun 2010; 402:390-5; PMID:20950585; http://dx.doi.org/10.1016/j.bbrc.2010.10.042.
20. Brock M, Trenkmann M, Gay RE, Michel BA, Gay S, Fischler M, et al. Interleukin-6 modulates the expression of the bone morphogenic protein receptor type II through a novel STAT3-microRNA cluster 17/92 pathway. Circ Res 2009; 104:1184-91; PMID:19390056; http://dx.doi.org/10.1161/CIRCRESAHA.109.197491.
21. Iliopoulos D, Jaeger SA, Hirsch HA, Bulyk ML, Struhl K. STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer. Mol Cell 2010; 39:493-506; PMID:20797623; http://dx.doi.org/10.1016/j.molcel.2010.07.023.
22. Haghikia A, Missol-Kolka E, Tsikas D, Venturini L, Brundiers S, Castoldi M, et al. Signal transducer and activator of transcription 3-mediated regulation of miR-199a-5p links cardiomyocyte and endothelial cell function in the heart: a key role for ubiquitin-conjugating enzymes. Eur Heart J 2011; 32:1287-97; PMID:20965886; http://dx.doi.org/10.1093/eurheartj/ehq369.
23. Brivanlou AH, Darnell JE Jr. Signal transduction and the control of gene expression. Science 2002; 295:813-8; PMID:11823631; http://dx.doi.org/10.1126/ science.1066355.
24. Levy DE, Darnell JE Jr. Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 2002; 3:651-62; PMID:12209125; http://dx.doi.org/10.1038/nrm909.
25. Platanias LC. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 2005; 5:375-86; PMID:15864272; http://dx.doi.org/10. 1038/nri1604.
26. Lesinski GB, Anghelina M, Zimmerer J, Bakalakos T, Badgwell B, Parihar R, et al. The antitumor effects of IFNalpha are abrogated in a STAT1-deficient mouse. J Clin Invest 2003; 112:170-80; PMID:12865406.
27. Yang CH, Yue J, Fan M, Pfeffer LM. IFN induces miR-21 through a signal transducer and activator of transcription 3-dependent pathway as a suppressive negative feedback on IFN-induced apoptosis. Cancer Res 2010; 70:8108-16; PMID:20813833; http://dx.doi.org/10.1158/0008-5472.CAN-10-2579.
28. Wang X, Wu M, Li Z, Chan C. Short time-series microarray analysis: methods and challenges. BMC Syst Biol 2008; 2:58; PMID:18605994; http://dx.doi.org/10.1186/1752-0509-2-58.
29. Turner M. Is transcription the dominant force during dynamic changes in gene expression? Adv Exp Med Biol 2011; 780:1-13; PMID:21842360; http://dx.doi.org/10.1007/978-1-4419-5632-3-1.
30. Lowrey PL, Takahashi JS. Genetics of circadian rhythms in Mammalian model organisms. Adv Genet 2011; 74:175-230; PMID:21924978; http://dx.doi.org/10. 1016/B978-0-12-387690-4.00006-4.
31. Dougherty ER, Shmulevich I, Bittner ML. Genomic signal processing: the salient issues. EURASIP J Appl Signal Process 2004; 2004:146-53.
32. Philippidou D, Schmitt M, Moser D, Margue C, Nazarov PV, Muller A, et al. Signatures of microRNAs and selected microRNA target genes in human melanoma. Cancer Res 2010; 70:4163-73; PMID:20442294; http://dx.doi.org/10.1158/0008-5472. CAN-09-4512.
33. Haan C, Kreis S, Margue C, Behrmann I. Jaks and cytokine receptors - an intimate relationship. Biochem Pharmacol 2006; 72:1538-46; PMID:16750817; http://dx.doi.org/10.1016/j.bcp.2006.04.013.
34. Kreis S, Munz GA, Haan S, Heinrich PC, Behrmann I. Cell density dependent increase of constitutive signal transducers and activators of transcription 3 activity in melanoma cells is mediated by Janus kinases. Mol Cancer Res 2007; 5:1331-41; PMID:18171991; http://dx.doi.org/10.1158/1541-7786.MCR-07-0317.
35. Mueller DW, Bosserhoff AK. The evolving concept of 'melano-miRs'- microRNAs in melanomagenesis. Pigment Cell Melanoma Res 2010; 23:620-6; PMID:20557479; http://dx.doi.org/10.1111/j.1755-148X.2010.00734.x.
36. Morris AC, Beresford GW, Mooney MR, Boss JM. Kinetics of a gamma interferon response: expression and assembly of CIITA promoter IV and inhibition by methylation. Mol Cell Biol 2002; 22:4781-91; PMID:12052885; http://dx.doi.org/10.1128/MCB.22.13.4781-91.2002.
37. Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM, Chisari FV, et al. Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature 2007; 449:919-22; PMID:17943132; http://dx.doi.org/10.1038/nature06205.
38. Griffiths-Jones S. The microRNA Registry. Nucleic Acids Res 2004; 32:109-11; PMID:14681370; http://dx.doi.org/10.1093/nar/gkh023.
39. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Müller-Newen G, Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 2003; 374:1-20; PMID:12773095; http://dx.doi.org/10.1042/ BJ20030407.
40. O'Shea JJ, Murray PJ. Cytokine signaling modules in inflammatory responses. Immunity 2008; 28:477-87; PMID:18400190; http://dx.doi.org/10.1016/j. immuni.2008.03.002.
41. Schroder K, Hertzog PJ, Ravasi T, Hume DA. Interferongamma: an overview of signals, mechanisms and functions. J Leukoc Biol 2004; 75:163-89; PMID:14525967; http://dx.doi.org/10.1189/jlb.0603252.
42. Kortylewski M, Komyod W, Kauffmann ME, Bosserhoff A, Heinrich PC, Behrmann I. Interferongamma-mediated growth regulation of melanoma cells: involvement of STAT1-dependent and STAT1-independent signals. J Invest Dermatol 2004; 122:414-22; PMID:15009724; http://dx.doi.org/10.1046/j.0022-202X.2004. 22237.x.
43. Wang G, Wang Y, Teng M, Zhang D, Li L, Liu Y. Signal transducers and activators of transcription-1 (STAT1) regulates microRNA transcription in interferon gamma-stimulated HeLa cells. PLoS One 2010; 5:11794; PMID:20668688; http://dx.doi.org/10.1371/journal.pone.0011794.
44. Thompson JE, Cubbon RM, Cummings RT, Wicker LS, Frankshun R, Cunningham BR, et al. Photochemical preparation of a pyridone containing tetracycle: a Jak protein kinase inhibitor. Bioorg Med Chem Lett 2002; 12:1219-23; PMID:11934592; http://dx.doi.org/10.1016/S0960-894X(02)00106-3.
45. Robertson G, Hirst M, Bainbridge M, Bilenky M, Zhao Y, Zeng T, et al. Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat Methods 2007; 4:651-7; PMID:17558387; http://dx.doi.org/10.1038/nmeth1068.
46. Wang J, Haubrock M, Cao KM, Hua X, Zhang CY, Wingender E, et al. Regulatory coordination of clustered microRNAs based on microRNA-transcription factor regulatory network. BMC Syst Biol 2011; 5:199; PMID:22176772; http://dx.doi.org/10.1186/1752-0509-5-199.
47. Griffiths-Jones S. miRBase: the microRNA sequence database. Methods Mol Biol 2006; 342:129-38; PMID:16957372.
48. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell 2003; 115:787-98; PMID:14697198; http://dx.doi.org/10.1016/S0092-8674(03)01018-3.
49. Huang S, He X, Ding J, Liang L, Zhao Y, Zhang Z, et al. Upregulation of miR-23a approximately 27a approximately 24 decreases transforming growth factorbeta-induced tumor-suppressive activities in human hepatocellular carcinoma cells. Int J Cancer 2008; 123:972-8; PMID:18508316; http://dx.doi.org/10.1002/ijc.23580.
50. Tsang WP, Kwok TT. The miR-18a* microRNA functions as a potential tumor suppressor by targeting on K-Ras. Carcinogenesis 2009; 30:953-9; PMID:19372139; http://dx.doi.org/10.1093/carcin/bgp094.
51. Yang JS, Phillips MD, Betel D, Mu P, Ventura A, Siepel AC, et al. Widespread regulatory activity of vertebrate microRNA* species. RNA 2011; 17:312-26; PMID:21177881; http://dx.doi.org/10.1261/rna.2537911.
52. Perry MM, Williams AE, Tsitsiou E, Larner-Svensson HM, Lindsay MA. Divergent intracellular pathways regulate interleukin-1beta-induced miR-146a and miR-146b expression and chemokine release in human alveolar epithelial cells. FEBS Lett 2009; 583:3349-55; PMID:19786024; http://dx.doi.org/10.1016/j.febslet. 2009.09.038.
53. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002; 3:34; PMID:12184808; http://dx.doi.org/10.1186/gb-2002-3-7-research0034.
54. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization and summaries of high density oligonucleotide array probe level data. Biostatistics 2003; 4:249-64; PMID:12925520; http://dx.doi.org/10.1093/biostatistics/4.2.249.
55. Eichler GS, Huang S, Ingber DE. Gene Expression Dynamics Inspector (GEDI): for integrative analysis of expression profiles. Bioinformatics 2003; 19:2321-2; PMID:14630665; http://dx.doi.org/10.1093/bioinformatics/btg307.
56. Futschik ME, Carlisle B. Noise-robust soft clustering of gene expression time-course data. J Bioinform Comput Biol 2005; 3:965-88; PMID:16078370; http://dx.doi.org/10.1142/S0219720005001375.
57. StoreyJD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci USA 2003; 100:9440-5; PMID:12883005; http://dx.doi.org/10. 1073/pnas.1530509100.
58. Aryee MJ, Gutiérrez-Pabello JA, Kramnik I, Maiti T, Quackenbush J. An improved empirical bayes approach to estimating differential gene expression in microarray time-course data: BETR (Bayesian Estimation of Temporal Regulation). BMC Bioinformatics 2009; 10:409; PMID:20003283; http://dx.doi.org/10.1186/1471-2105-10-409.
59. Tai YC, Speed TP. A multivariate empirical Bayes statistic for replicated microarray time course data. Ann Stat 2006; 34; http://dx.doi.org/10.1214/ 009053606000000759.