Uncovering microRNA and transcription factor mediated regulatory networks in Glioblastoma

PLoS Computational Biology

Volumn 8, Issue 7, 2012, Pages

  Sun, Jingchun ^a   Gong, Xue ^a   Purow, Benjamin ^b   Zhao, Zhongming ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; RNA; TISSUE; TRANSCRIPTION;

BRAIN TUMORS; FEEDFORWARD LOOPS; GLIOBLASTOMA MULTIFORME; GLIOBLASTOMAS; MICRORNA EXPRESSION; NOTCH SIGNALING PATHWAYS; REGULATORY MECHANISM; REGULATORY NETWORK; SUBNETWORKS; TISSUE SAMPLES;

TRANSCRIPTION FACTORS;

MICRORNA; MICRORNA 124; MICRORNA 137; MICRORNA 219 5P; MICRORNA 34A; MICRORNA 9; MICRORNA 92B; NOTCH RECEPTOR; RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; DISEASE ASSOCIATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE REGULATORY NETWORK; GENE REPRESSION; GENE STRUCTURE; GENETIC ASSOCIATION; GLIOBLASTOMA; RNA ANALYSIS; SIGNAL TRANSDUCTION;

EID: 84864592682     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002488     Document Type: Article

References (90)

1. Holland EC, (2000) Glioblastoma multiforme: the terminator. Proc Natl Acad Sci U S A 97: 6242-6244.
2. Purow B, Schiff D, (2009) Advances in the genetics of glioblastoma: are we reaching critical mass? Nat Rev Neurol 5: 419-426.
3. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, et al. (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321: 1807-1812.
4. Shete S, Hosking FJ, Robertson LB, Dobbins SE, Sanson M, et al. (2009) Genome-wide association study identifies five susceptibility loci for glioma. Nat Genet 41: 899-904.
5. Wrensch M, Jenkins RB, Chang JS, Yeh RF, Xiao Y, et al. (2009) Variants in the CDKN2B and RTEL1 regions are associated with high-grade glioma susceptibility. Nat Genet 41: 905-908.
6. TCGA (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455: 1061-1068.
7. Jornsten R, Abenius T, Kling T, Schmidt L, Johansson E, et al. (2011) Network modeling of the transcriptional effects of copy number aberrations in glioblastoma. Mol Syst Biol 7: 486.
8. Ladha J, Donakonda S, Agrawal S, Thota B, Srividya MR, et al. (2010) Glioblastoma-specific protein interaction network identifies PP1A and CSK21 as connecting molecules between cell cycle-associated genes. Cancer Res 70: 6437-6447.
9. Cerami E, Demir E, Schultz N, Taylor BS, Sander C, (2010) Automated network analysis identifies core pathways in glioblastoma. PLoS One 5: e8918.
10. Wuchty S, Arjona D, Li A, Kotliarov Y, Walling J, et al. (2011) Prediction of Associations between microRNAs and gene expression in glioma biology. PLoS One 6: e14681.
11. Shalgi R, Brosh R, Oren M, Pilpel Y, Rotter V, (2009) Coupling transcriptional and post-transcriptional miRNA regulation in the control of cell fate. Aging (Albany NY) 1: 762-770.
12. Cohen EE, Zhu H, Lingen MW, Martin LE, Kuo WL, et al. (2009) A feed-forward loop involving protein kinase Calpha and microRNAs regulates tumor cell cycle. Cancer Res 69: 65-74.
13. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, et al. (2006) A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 103: 2257-2261.
14. Esquela-Kerscher A, Slack FJ, (2006) Oncomirs- microRNAs with a role in cancer. Nat Rev Cancer 6: 259-269.
15. Bartel DP, (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
16. Cho WC, (2007) OncomiRs: the discovery and progress of microRNAs in cancers. Mol Cancer 6: 60.
17. Srinivasan S, Patric IR, Somasundaram K, (2011) A ten-microRNA expression signature predicts survival in glioblastoma. PLoS One 6: e17438.
18. Novakova J, Slaby O, Vyzula R, Michalek J, (2009) MicroRNA involvement in glioblastoma pathogenesis. Biochem Biophys Res Commun 386: 1-5.
19. Purow B, (2011) The elephant in the room: do microRNA-based therapies have a realistic chance of succeeding for brain tumors such as glioblastoma? J Neurooncol 103: 429-436.
20. Chan JA, Krichevsky AM, Kosik KS, (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65: 6029-6033.
21. Conti A, Aguennouz M, La Torre D, Tomasello C, Cardali S, et al. (2009) miR-21 and 221 upregulation and miR-181b downregulation in human grade II-IV astrocytic tumors. J Neurooncol 93: 325-332.
22. Gabriely G, Wurdinger T, Kesari S, Esau CC, Burchard J, et al. (2008) MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol 28: 5369-5380.
23. Papagiannakopoulos T, Shapiro A, Kosik KS, (2008) MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res 68: 8164-8172.
24. Silber J, Lim DA, Petritsch C, Persson AI, Maunakea AK, et al. (2008) miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med 6: 14.
25. Kim TM, Huang W, Park R, Park PJ, Johnson MD, (2011) A developmental taxonomy of glioblastoma defined and maintained by microRNAs. Cancer Res 71: 3387-3399.
26. Dong H, Luo L, Hong S, Siu H, Xiao Y, et al. (2010) Integrated analysis of mutations, miRNA and mRNA expression in glioblastoma. BMC Syst Biol 4: 163.
27. Krex D, Klink B, Hartmann C, von Deimling A, Pietsch T, et al. (2007) Long-term survival with glioblastoma multiforme. Brain 130: 2596-2606.
28. Davidson EH, (2006) The regulatory genome: gene regulatory networks in development and evolution New York Academic Press pp. 31-34.
29. Hobert O, (2008) Gene regulation by transcription factors and microRNAs. Science 319: 1785-1786.
30. Shalgi R, Lieber D, Oren M, Pilpel Y, (2007) Global and local architecture of the mammalian microRNA-transcription factor regulatory network. PLoS Comput Biol 3: e131.
31. Tsang J, Zhu J, van Oudenaarden A, (2007) MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol Cell 26: 753-767.
32. Barski A, Jothi R, Cuddapah S, Cui K, Roh TY, et al. (2009) Chromatin poises miRNA- and protein-coding genes for expression. Genome Res 19: 1742-1751.
33. Coppe A, Ferrari F, Bisognin A, Danieli GA, Ferrari S, et al. (2009) Motif discovery in promoters of genes co-localized and co-expressed during myeloid cells differentiation. Nucleic Acids Res 37: 533-549.
34. Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S, et al. (2006) TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 34: D108-110.
35. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB, (2003) Prediction of mammalian microRNA targets. Cell 115: 787-798.
36. Kel AE, Gossling E, Reuter I, Cheremushkin E, Kel-Margoulis OV, et al. (2003) MATCH: A tool for searching transcription factor binding sites in DNA sequences. Nucleic Acids Res 31: 3576-3579.
37. Sosa-Pineda B, (2004) The gene Pax4 is an essential regulator of pancreatic beta-cell development. Mol Cells 18: 289-294.
38. Martinez NJ, Ow MC, Barrasa MI, Hammell M, Sequerra R, et al. (2008) A C. elegans genome-scale microRNA network contains composite feedback motifs with high flux capacity. Genes Dev 22: 2535-2549.
39. Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, et al. (2010) Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17: 98-110.
40. Margolin AA, Nemenman I, Basso K, Wiggins C, Stolovitzky G, et al. (2006) ARACNE: an algorithm for the reconstruction of gene regulatory networks in a mammalian cellular context. BMC Bioinformatics 7 (Suppl 1): S7.
41. Li S, Liang ZG, Wang GY, Yavetz B, Kim ED, et al. (2000) Molecular cloning and characterization of functional domains of a human testis-specific isoform of calpastatin. Biol Reprod 63: 172-178.
42. Shen-Orr SS, Milo R, Mangan S, Alon U, (2002) Network motifs in the transcriptional regulation network of Escherichia coli. Nat Genet 31: 64-68.
43. Goldberg DS, Roth FP, (2003) Assessing experimentally derived interactions in a small world. Proc Natl Acad Sci U S A 100: 4372-4376.
44. Yu G, Li F, Qin Y, Bo X, Wu Y, et al. (2010) GOSemSim: an R package for measuring semantic similarity among GO terms and gene products. Bioinformatics 26: 976-978.
45. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, et al. (2008) The Pfam protein families database. Nucleic Acids Res 36: D281-288.
46. Zhang B, Kirov S, Snoddy J, (2005) WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res 33: W741-748.
47. Barabasi AL, Oltvai ZN, (2004) Network biology: understanding the cell's functional organization. Nat Rev Genet 5: 101-113.
48. Zotenko E, Mestre J, O'Leary DP, Przytycka TM, (2008) Why do hubs in the yeast protein interaction network tend to be essential: reexamining the connection between the network topology and essentiality. PLoS Comput Biol 4: e1000140.
49. Sun J, Zhao Z, (2010) A comparative study of cancer proteins in the human protein-protein interaction network. BMC Genomics 11 (Suppl 3): S5.
50. Yu H, Greenbaum D, Xin Lu H, Zhu X, Gerstein M, (2004) Genomic analysis of essentiality within protein networks. Trends Genet 20: 227-231.
51. Zhang LV, King OD, Wong SL, Goldberg DS, Tong AH, et al. (2005) Motifs, themes and thematic maps of an integrated Saccharomyces cerevisiae interaction network. J Biol 4: 6.
52. Pereira-Leal JB, Enright AJ, Ouzounis CA, (2004) Detection of functional modules from protein interaction networks. Proteins 54: 49-57.
53. Takebe N, Harris PJ, Warren RQ, Ivy SP, (2011) Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways. Nat Rev Clin Oncol 8: 97-106.
54. Purow BW, Haque RM, Noel MW, Su Q, Burdick MJ, et al. (2005) Expression of Notch-1 and its ligands, Delta-like-1 and Jagged-1, is critical for glioma cell survival and proliferation. Cancer Res 65: 2353-2363.
55. Kanamori M, Kawaguchi T, Nigro JM, Feuerstein BG, Berger MS, et al. (2007) Contribution of Notch signaling activation to human glioblastoma multiforme. J Neurosurg 106: 417-427.
56. Kanehisa M, Goto S, (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27-30.
57. Adamcsek B, Palla G, Farkas IJ, Derenyi I, Vicsek T, (2006) CFinder: locating cliques and overlapping modules in biological networks. Bioinformatics 22: 1021-1023.
58. Wang L, Jia P, Wolfinger RD, Chen X, Grayson BL, et al. (2011) An efficient hierarchical generalized linear mixed model for pathway analysis of genome-wide association studies. Bioinformatics 27: 686-692.
59. Guessous F, Zhang Y, Kofman A, Catania A, Li Y, et al. (2010) microRNA-34a is tumor suppressive in brain tumors and glioma stem cells. Cell Cycle 9: 1031-1036.
60. Li Y, Guessous F, Zhang Y, Dipierro C, Kefas B, et al. (2009) MicroRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res 69: 7569-7576.
61. de Antonellis P, Medaglia C, Cusanelli E, Andolfo I, Liguori L, et al. (2011) MiR-34a targeting of Notch ligand delta-like 1 impairs CD15+/CD133+ tumor-propagating cells and supports neural differentiation in medulloblastoma. PLoS One 6: e24584.
62. Nalls D, Tang SN, Rodova M, Srivastava RK, Shankar S, (2011) Targeting epigenetic regulation of miR-34a for treatment of pancreatic cancer by inhibition of pancreatic cancer stem cells. PLoS One 6: e24099.
63. Pang RT, Leung CO, Ye TM, Liu W, Chiu PC, et al. (2010) MicroRNA-34a suppresses invasion through downregulation of Notch1 and Jagged1 in cervical carcinoma and choriocarcinoma cells. Carcinogenesis 31: 1037-1044.
64. Chen JS, Pedro MS, Zeller RW, (2011) miR-124 function during Ciona intestinalis neuronal development includes extensive interaction with the Notch signaling pathway. Development 138: 4943-4953.
65. Chen F, Hu SJ, (2011) Effect of microRNA-34a in cell cycle, differentiation, and apoptosis: A review. J Biochem Mol Toxicol DOI:10.1002/jbt.20412.
66. Li J, Zimmerman LJ, Park BH, Tabb DL, Liebler DC, et al. (2009) Network-assisted protein identification and data interpretation in shotgun proteomics. Mol Syst Biol 5: 303.
67. Hashimi ST, Fulcher JA, Chang MH, Gov L, Wang S, et al. (2009) MicroRNA profiling identifies miR-34a and miR-21 and their target genes JAG1 and WNT1 in the coordinate regulation of dendritic cell differentiation. Blood 114: 404-414.
68. Wei JS, Song YK, Durinck S, Chen QR, Cheuk AT, et al. (2008) The MYCN oncogene is a direct target of miR-34a. Oncogene 27: 5204-5213.
69. Cole KA, Attiyeh EF, Mosse YP, Laquaglia MJ, Diskin SJ, et al. (2008) A functional screen identifies miR-34a as a candidate neuroblastoma tumor suppressor gene. Mol Cancer Res 6: 735-742.
70. Choi YJ, Lin CP, Ho JJ, He X, Okada N, et al. (2011) miR-34 miRNAs provide a barrier for somatic cell reprogramming. Nat Cell Biol 13: 1353-1360.
71. Chen QR, Yu LR, Tsang P, Wei JS, Song YK, et al. (2011) Systematic proteome analysis identifies transcription factor YY1 as a direct target of miR-34a. J Proteome Res 10: 479-487.
72. Re A, Cora D, Taverna D, Caselle M, (2009) Genome-wide survey of microRNA-transcription factor feed-forward regulatory circuits in human. Mol Biosyst 5: 854-867.
73. Guo AY, Sun J, Jia P, Zhao Z, (2010) A novel microRNA and transcription factor mediated regulatory network in schizophrenia. BMC Syst Biol 4: 10.
74. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, et al. (2011) COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res 39: D945-950.
75. Amberger J, Bocchini CA, Scott AF, Hamosh A, (2009) McKusick's Online Mendelian Inheritance in Man (OMIM). Nucleic Acids Res 37: D793-796.
76. Becker KG, Barnes KC, Bright TJ, Wang SA, (2004) The genetic association database. Nat Genet 36: 431-432.
77. Jiang Q, Wang Y, Hao Y, Juan L, Teng M, et al. (2009) miR2Disease: a manually curated database for microRNA deregulation in human disease. Nucleic Acids Res 37: D98-104.
78. Ruepp A, Kowarsch A, Schmidl D, Buggenthin F, Brauner B, et al. (2010) PhenomiR: a knowledgebase for microRNA expression in diseases and biological processes. Genome Biol 11: R6.
79. Lu M, Zhang Q, Deng M, Miao J, Guo Y, et al. (2008) An analysis of human microRNA and disease associations. PLoS One 3: e3420.
80. Kozomara A, Griffiths-Jones S, (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39: D152-157.
81. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, et al. (2005) Combinatorial microRNA target predictions. Nat Genet 37: 495-500.
82. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, et al. (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27: 91-105.
83. Betel D, Wilson M, Gabow A, Marks DS, Sander C, (2008) The microRNA.org resource: targets and expression. Nucleic Acids Res 36: D149-153.
84. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, et al. (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455: 58-63.
85. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, et al. (2008) The impact of microRNAs on protein output. Nature 455: 64-71.
86. Xu J, Li CX, Li YS, Lv JY, Ma Y, et al. (2011) MiRNA-miRNA synergistic network: construction via co-regulating functional modules and disease miRNA topological features. Nucleic Acids Res 39: 825-836.
87. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, et al. (2002) The human genome browser at UCSC. Genome Res 12: 996-1006.
88. Margolin AA, Wang K, Lim WK, Kustagi M, Nemenman I, et al. (2006) Reverse engineering cellular networks. Nat Protocols 1: 662-671.
89. Benjamini Y, Hochberg Y, (1995) Controlling the False Discovery Rate: a Practical and Powerful Approach to Multiple Testing. J R Statist Soc B 57: 289-300.
90. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T, (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27: 431-432.