An Intronic microRNA Links Rb/E2F and EGFR Signaling

PLoS Genetics

Volumn 10, Issue 7, 2014, Pages

  Truscott, Mary ^a   Islam, Abul B M M K ^b,c   Lightfoot, James ^a   López Bigas, Núria ^c,d   Frolov, Maxim V ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF DHAKA   (Bangladesh)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CBL PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; MICRORNA; MICRORNA 998; MITOGEN ACTIVATED PROTEIN KINASE; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F1; UNCLASSIFIED DRUG; CBL PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; E2F PROTEIN, DROSOPHILA; EGFR PROTEIN, DROSOPHILA; MIRN11 MICRORNA, DROSOPHILA; MIRN998 MICRORNA, DROSOPHILA; RECEPTOR; TRANSCRIPTION FACTOR E2F;

ADULT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; DE2F1 GENE; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; IN VIVO STUDY; INTRON; MUTANT; NONHUMAN; PROTEIN FUNCTION; WOUND HEALING; ANIMAL; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; E2F TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTRONS; MICRORNAS; PROTO-ONCOGENE PROTEINS C-CBL; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, INVERTEBRATE PEPTIDE; SIGNAL TRANSDUCTION;

EID: 84905483292     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004493     Document Type: Article

References (64)

1. Miska EA, Alvarez-Saavedra E, Abbott AL, Lau NC, Hellman AB, et al. (2007) Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genet 3: e215 doi:10.1371/journal.pgen.0030215.
2. Alvarez-Saavedra E, Horvitz HR, (2010) Many families of C. elegans microRNAs are not essential for development or viability. Curr Biol 20: 367-373 doi:10.1016/j.cub.2009.12.051.
3. Brenner JL, Jasiewicz KL, Fahley AF, Kemp BJ, Abbott AL, (2010) Loss of individual microRNAs causes mutant phenotypes in sensitized genetic backgrounds in C. elegans. Curr Biol 20: 1321-1325 doi:10.1016/j.cub.2010.05.062.
4. Izumiya M, Okamoto K, Tsuchiya N, Nakagama H, (2010) Functional screening using a microRNA virus library and microarrays: a new high-throughput assay to identify tumor-suppressive microRNAs. Carcinogenesis 31: 1354-1359 doi:10.1093/carcin/bgq112.
5. Herranz H, Hong X, Hung NT, Voorhoeve PM, Cohen SM, (2012) Oncogenic cooperation between SOCS family proteins and EGFR identified using a Drosophila epithelial transformation model. Genes & Development 26: 1602-1611 doi:10.1101/gad.192021.112.
6. Kim VN, Han J, Siomi MC, (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10: 126-139 doi:10.1038/nrm2632.
7. Baskerville S, Bartel DP, (2005) Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 11: 241-247 doi:10.1261/rna.7240905.
8. Truscott M, Islam ABMMK, López-Bigas N, Frolov MV, (2011) mir-11 limits the proapoptotic function of its host gene, dE2f1. Genes & Development 25: 1820-1834 doi:10.1101/gad.16947411.
9. Najafi-Shoushtari SH, Kristo F, Li Y, Shioda T, Cohen DE, et al. (2010) MicroRNA-33 and the SREBP Host Genes Cooperate to Control Cholesterol Homeostasis. Science 328: 1566-1569 doi:10.1126/science.1189123.
10. Dill H, Linder B, Fehr A, Fischer U, (2012) Intronic miR-26b controls neuronal differentiation by repressing its host transcript, ctdsp2. Genes & Development 26: 25-30 doi:10.1101/gad.177774.111.
11. Hinske LCG, Galante PAF, Kuo WP, Ohno-Machado L, (2010) A potential role for intragenic miRNAs on their hosts' interactome. BMC Genomics 11: 533 doi:10.1186/1471-2164-11-533.
12. van Rooij E, Sutherland LB, Qi X, Richardson JA, Hill J, et al. (2007) Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 316: 575-579 doi:10.1126/science.1139089.
13. Moon N-S, Di Stefano L, Dyson N, (2006) A gradient of epidermal growth factor receptor signaling determines the sensitivity of rbf1 mutant cells to E2F-dependent apoptosis. Molecular and Cellular Biology 26: 7601-7615 doi:10.1128/MCB.00836-06.
14. Morris EJ, Michaud WA, Ji J-Y, Moon N-S, Rocco JW, et al. (2006) Functional identification of Api5 as a suppressor of E2F-dependent apoptosis in vivo. PLoS Genet 2: e196 doi:10.1371/journal.pgen.0020196.
15. Du W, Xie JE, Dyson N, (1996) Ectopic expression of dE2F and dDP induces cell proliferation and death in the Drosophila eye. EMBO J 15: 3684-3692.
16. Gabay L, Seger R, Shilo BZ, (1997) In situ activation pattern of Drosophila EGF receptor pathway during development. Science 277: 1103-1106.
17. Kumar JP, Moses K, (2001) EGF receptor and Notch signaling act upstream of Eyeless/Pax6 to control eye specification. Cell 104: 687-697 doi:10.1016/S0092-8674(01)00265-3.
18. Lesokhin AM, Yu SY, Katz J, Baker NE, (1999) Several levels of EGF receptor signaling during photoreceptor specification in wild-type, Ellipse, and null mutant Drosophila. Dev Biol 205: 129-144 doi:10.1006/dbio.1998.9121.
19. Freeman M, (1996) Reiterative Use of the EGF Receptor Triggers Differentiation of All Cell Types in the Drosophila Eye. Cell 87: 651-660.
20. Zak NB, Shilo BZ, (1992) Localization of DER and the pattern of cell divisions in wild-type and Ellipse eye imaginal discs. Dev Biol 149: 448-456.
21. Kanehisa M, Goto S, (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27-30.
22. Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B, et al. (2009) AmiGO: online access to ontology and annotation data. Bioinformatics 25: 288-289 doi:10.1093/bioinformatics/btn615.
23. Moses K. (2002) Drosophila eye development. Berlin; New York: Springer.
24. Abella JV, Park M, (2009) Breakdown of endocytosis in the oncogenic activation of receptor tyrosine kinases. Am J Physiol Endocrinol Metab 296: E973-E984 doi:10.1152/ajpendo.90857.2008.
25. Pai LM, Barcelo G, Schüpbach T, (2000) D-cbl, a negative regulator of the Egfr pathway, is required for dorsoventral patterning in Drosophila oogenesis. Cell 103: 51-61 doi:10.1016/S0092-8674(00)00104-5.
26. Jékely G, Sung H-H, Luque CM, Rørth P, (2005) Regulators of endocytosis maintain localized receptor tyrosine kinase signaling in guided migration. Developmental Cell 9: 197-207 doi:10.1016/j.devcel.2005.06.004.
27. Chang W-L, Liou W, Pen H-C, Chou H-Y, Chang Y-W, et al. (2008) The gradient of Gurken, a long-range morphogen, is directly regulated by Cbl-mediated endocytosis. Development 135: 1923-1933 doi:10.1242/dev.017103.
28. Pai L-M, Wang P-Y, Chen S-R, Barcelo G, Chang W-L, et al. (2006) Differential effects of Cbl isoforms on Egfr signaling in Drosophila. Mech Dev 123: 450-462 doi:10.1016/j.mod.2006.04.001.
29. Wang P-Y, Pai L-M, (2011) D-Cbl Binding to Drk Leads to Dose-Dependent Down-Regulation of EGFR Signaling and Increases Receptor-Ligand Endocytosis. PLoS ONE 6: e17097 Available: http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0017097.
30. Ibáñez-Ventoso C, Vora M, Driscoll M, (2008) Sequence relationships among C. elegans, D. melanogaster and human microRNAs highlight the extensive conservation of microRNAs in biology. PLoS ONE 3: e2818 doi:10.1371/journal.pone.0002818.
31. Miranda KC, Huynh T, Tay Y, Ang Y-S, Tam W-L, et al. (2006) A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell 126: 1203-1217 doi:10.1016/j.cell.2006.07.031.
32. Hyun S, Lee JH, Jin H, Nam J, Namkoong B, et al. (2009) Conserved MicroRNA miR-8/miR-200 and its target USH/FOG2 control growth by regulating PI3K. Cell 139: 1096-1108.
33. Bellare P, Ganem D, (2009) Regulation of KSHV lytic switch protein expression by a virus-encoded microRNA: an evolutionary adaptation that fine-tunes lytic reactivation. Cell Host Microbe 6: 570-575 doi:10.1016/j.chom.2009.11.008.
34. Muniyappa MK, Dowling P, Henry M, Meleady P, Doolan P, et al. (2009) MiRNA-29a regulates the expression of numerous proteins and reduces the invasiveness and proliferation of human carcinoma cell lines. Eur J Cancer 45: 3104-3118 doi:10.1016/j.ejca.2009.09.014.
35. Baek D, Villén J, Shin C, Camargo FD, Gygi SP, et al. (2008) The impact of microRNAs on protein output. Nature 455: 64-71 doi:10.1038/nature07242.
36. Mukherji S, Ebert MS, Zheng GXY, Tsang JS, Sharp PA, et al. (2011) MicroRNAs can generate thresholds in target gene expression. Nat Genet 43: 854-859 doi:10.1038/ng.905.
37. Hirsch DS, Shen Y, Wu WJ, (2006) Growth and motility inhibition of breast cancer cells by epidermal growth factor receptor degradation is correlated with inactivation of Cdc42. Cancer Research 66: 3523-3530 doi:10.1158/0008-5472.CAN-05-1547.
38. Tan Y-HC, Krishnaswamy S, Nandi S, Kanteti R, Vora S, et al. (2010) CBL is frequently altered in lung cancers: its relationship to mutations in MET and EGFR tyrosine kinases. PLoS ONE 5: e8972 doi:10.1371/journal.pone.0008972.
39. Vial E, Sahai E, Marshall CJ, (2003) ERK-MAPK signaling coordinately regulates activity of Rac1 and RhoA for tumor cell motility. Cancer Cell 4: 67-79 doi:10.1016/S1535-6108(03)00162-4.
40. Ambros V, (2010) MicroRNAs: genetically sensitized worms reveal new secrets. Curr Biol 20: R598-R600 doi:10.1016/j.cub.2010.05.054.
41. Klein DE, Nappi VM, Reeves GT, Shvartsman SY, Lemmon MA, (2004) Argos inhibits epidermal growth factor receptor signalling by ligand sequestration. Nature 430: 1040-1044 doi:10.1038/nature02840.
42. Freeman M, (1997) Cell determination strategies in the Drosophila eye. Development 124: 261-270.
43. Bejarano F, Bortolamiol-Becet D, Dai Q, Sun K, Saj A, et al. (2012) A genome-wide transgenic resource for conditional expression of Drosophila microRNAs. Development 139: 2821-2831 doi:10.1242/dev.079939.
44. Gebeshuber CA, Zatloukal K, Martinez J, (2009) miR-29a suppresses tristetraprolin, which is a regulator of epithelial polarity and metastasis. EMBO Rep 10: 400-405 doi:10.1038/embor.2009.9.
45. Tumaneng K, Schlegelmilch K, Russell RC, Yimlamai D, Basnet H, et al. (2012) YAP mediates crosstalk between the Hippo and PI(3)K-TOR pathways by suppressing PTEN via miR-29. Nat Cell Biol 14: 1322-1329 doi:10.1038/ncb2615.
46. Kincaid RP, Burke JM, Sullivan CS, (2012) RNA virus microRNA that mimics a B-cell oncomiR. Proc Natl Acad Sci USA 109: 3077-3082 doi:10.1073/pnas.1116107109.
47. Mott JL, Kobayashi S, Bronk SF, Gores GJ, (2007) mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 26: 6133-6140 doi:10.1038/sj.onc.1210436.
48. Anastasiadou E, Boccellato F, Vincenti S, Rosato P, Bozzoni I, et al. (2010) Epstein-Barr virus encoded LMP1 downregulates TCL1 oncogene through miR-29b. Oncogene 29: 1316-1328 doi:10.1038/onc.2009.439.
49. Park S-Y, Lee JH, Ha M, Nam J-W, Kim VN, (2009) miR-29 miRNAs activate p53 by targeting p85 alpha and CDC42. Nat Struct Mol Biol 16: 23-29 doi:10.1038/nsmb.1533.
50. Bae HJ, Noh JH, Kim JK, Eun JW, Jung KH, et al. (2013) MicroRNA-29c functions as a tumor suppressor by direct targeting oncogenic SIRT1 in hepatocellular carcinoma. Oncogene 33: 2557-67 doi:10.1038/onc.2013.216.
51. Bueno MJ, Gómez de Cedrón M, Laresgoiti U, Fernández-Piqueras J, Zubiaga AM, et al. (2010) Multiple E2F-induced microRNAs prevent replicative stress in response to mitogenic signaling. Molecular and Cellular Biology 30: 2983-2995 doi:10.1128/MCB.01372-09.
52. Marzi MJ, Puggioni EMR, Dall'Olio V, Bucci G, Bernard L, et al. (2012) Differentiation-associated microRNAs antagonize the Rb-E2F pathway to restrict proliferation. J Cell Biol 199: 77-95 doi:10.1083/jcb.201206033.
53. Daneshvar K, Nath S, Khan A, Shover W, Richardson C, et al. (2013) MicroRNA miR-308 regulates dMyc through a negative feedback loop in Drosophila. Biol Open 2: 1-9 doi:10.1242/bio.20122725.
54. Parks AL, Cook KR, Belvin M, Dompe NA, Fawcett R, et al. (2004) Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat Genet 36: 288-292 doi:10.1038/ng1312.
55. Haley B, Hendrix D, Trang V, Levine M, (2008) A simplified miRNA-based gene silencing method for Drosophila melanogaster. Dev Biol 321: 482-490 doi:10.1016/j.ydbio.2008.06.015.
56. Ruby JG, Stark A, Johnston WK, Kellis M, Bartel DP, et al. (2007) Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Research 17: 1850-1864 doi:10.1101/gr.6597907.
57. Schnall-Levin M, Zhao Y, Perrimon N, Berger B, (2010) Conserved microRNA targeting in Drosophila is as widespread in coding regions as in 3′UTRs. Proc Natl Acad Sci USA 107: 15751-15756 doi:10.1073/pnas.1006172107.
58. Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E, (2007) The role of site accessibility in microRNA target recognition. Nat Genet 39: 1278-1284 doi:10.1038/ng2135.
59. Enright AJ, John B, Gaul U, Tuschl T, Sander C, et al. (2003) MicroRNA targets in Drosophila. Genome Biol 5: R1 doi:10.1186/gb-2003-5-1-r1.
60. Rehmsmeier M, Steffen P, Höchsmann M, Giegerich R, (2004) Fast and effective prediction of microRNA/target duplexes. RNA 10: 1507-1517 doi:10.1261/rna.5248604.
61. Lewis BP, Burge CB, Bartel DP, (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20 doi:10.1016/j.cell.2004.12.035.
62. Gautier L, Cope L, Bolstad BM, Irizarry RA, (2004) affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315 doi:10.1093/bioinformatics/btg405.
63. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3 doi:10.2202/1544-6115.1027.
64. Perez-Llamas C, López-Bigas N, (2011) Gitools: analysis and visualisation of genomic data using interactive heat-maps. PLoS ONE 6: e19541 doi:10.1371/journal.pone.0019541.