Downregulation of the Host Gene jigr1 by miR-92 Is Essential for Neuroblast Self-Renewal in Drosophila

PLoS Genetics

Volumn 11, Issue 5, 2015, Pages

  Yuva Aydemir, Yeliz ^a   Xu, Xia Lian ^b,d   Aydemir, Ozkan ^a   Gascon, Eduardo ^a   Sayin, Serkan ^a,e   Zhou, Wenke ^c   Hong, Yang ^c   Gao, Fen Biao ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d ProMab Technologies   (United States)

^e UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 92; MICRORNA 92B; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; JIGR1 PROTEIN, DROSOPHILA; MESSENGER RNA; MIRN92 MICRORNA, DROSOPHILA;

3' UNTRANSLATED REGION; ADULT; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL RENEWAL; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA; FEEDBACK SYSTEM; GENE; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE TARGETING; IN VIVO STUDY; INTRON; JIGR1 GENE; LARVA; MALE; NEUROBLAST; NONHUMAN; PHENOTYPE; ANIMAL; BRAIN; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; GLIA; METABOLISM; NEURAL STEM CELL; SEQUENCE ALIGNMENT;

ANIMALIA;

3' UNTRANSLATED REGIONS; ANIMALS; BRAIN; DNA-BINDING PROTEINS; DOWN-REGULATION; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LARVA; MALE; MICRORNAS; NEURAL STEM CELLS; NEUROGLIA; RNA, MESSENGER; SEQUENCE ALIGNMENT;

EID: 84930804212     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005264     Document Type: Article

References (39)

1. Ambros V, microRNAs: tiny regulators with great potential. Cell [Internet]. 2001 Dec 28 [cited 2014 Sep 19];107(7):823–6. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11779458 11779458
2. Ebert MS, Sharp PA, Roles for microRNAs in conferring robustness to biological processes. Cell [Internet]. 2012 Apr 27 [cited 2014 Jul 9];149(3):515–24. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3351105&tool=pmcentrez&rendertype=abstract doi: 10.1016/j.cell.2012.04.005 22541426
3. Newman M a, Hammond SM, Emerging paradigms of regulated microRNA processing. Genes Dev [Internet]. 2010 Jun 1 [cited 2014 Jun 5];24(11):1086–92. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2878647&tool=pmcentrez&rendertype=abstract doi: 10.1101/gad.1919710 20516194
4. Kim Y-K, Kim VN, Processing of intronic microRNAs. EMBO J [Internet]. 2007 Feb 7 [cited 2014 Aug 14];26(3):775–83. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1794378&tool=pmcentrez&rendertype=abstract 17255951
5. Rodriguez A, Griffiths-Jones S, Ashurst JL, Bradley A, Identification of mammalian microRNA host genes and transcription units. Genome Res [Internet]. 2004 Oct [cited 2014 Jul 9];14(10A):1902–10. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=524413&tool=pmcentrez&rendertype=abstract 15364901
6. Baskerville S, Bartel DP, Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA [Internet]. 2005 Mar [cited 2014 Aug 27];11(3):241–7. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1370713&tool=pmcentrez&rendertype=abstract 15701730
7. 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 [Internet]. 2012 May [cited 2014 Sep 24];40(9):4002–12. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3351155&tool=pmcentrez&rendertype=abstract doi: 10.1093/nar/gkr1312 22238379
8. Ramalingam P, Palanichamy JK, Singh A, Das P, Bhagat M, Kassab MA, et al. Biogenesis of intronic miRNAs located in clusters by independent transcription and alternative splicing. RNA [Internet]. 2014 Jan [cited 2014 Jun 2];20(1):76–87. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24226766 doi: 10.1261/rna.041814.113 24226766
9. Hartenstein V, Rudloff E, Campos-Ortega JA, The pattern of proliferation of the neuroblasts in the wild-type embryo of Drosophila melanogaster. Roux’s Arch Dev Biol [Internet]. 1987 Dec [cited 2014 Sep 25];196(8):473–85. Available from: http://link.springer.com/10.1007/BF00399871
10. Truman JW, Bate M, Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev Biol [Internet]. 1988 Jan;125(1):145–57. Available from: http://www.ncbi.nlm.nih.gov/pubmed/3119399 3119399
11. Maurange C, Gould AP, Brainy but not too brainy: starting and stopping neuroblast divisions in Drosophila. Trends Neurosci [Internet]. 2005 Jan [cited 2014 Jul 7];28(1):30–6. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15626494 15626494
12. Jiang Y, Reichert H. Drosophila Neural Stem Cells in Brain Development and Tumor Formation. J Neurogenet [Internet]. 2014 May 12 [cited 2014 Sep 25];1–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24766377
13. Sun X, Morozova T, Sonnenfeld M, Glial and neuronal functions of the Drosophila homolog of the human SWI/SNF gene ATR-X (DATR-X) and the jing zinc-finger gene specify the lateral positioning of longitudinal glia and axons. Genetics [Internet]. 2006 Jul [cited 2014 Jun 11];173(3):1397–415. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1526706&tool=pmcentrez&rendertype=abstract 16648585
14. Egger B, Boone JQ, Stevens NR, Brand AH, Doe CQ. Regulation of spindle orientation and neural stem cell fate in the Drosophila optic lobe. Neural Dev [Internet]. 2007 Jan [cited 2012 Aug 30];2(January):1. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1779784&tool=pmcentrez&rendertype=abstract
15. Parks AL, Cook KR, Belvin M, Dompe NA, Fawcett R, Huppert K, et al. Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat Genet [Internet]. 2004 Mar [cited 2014 Jul 14];36(3):288–92. Available from: http://www.ncbi.nlm.nih.gov/pubmed/14981519 14981519
16. Huang J, Zhou W, Dong W, Watson AM, Hong Y, From the Cover: Directed, efficient, and versatile modifications of the Drosophila genome by genomic engineering. Proc Natl Acad Sci U S A [Internet]. 2009 May 19 [cited 2014 Sep 15];106(20):8284–9. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2688891&tool=pmcentrez&rendertype=abstract doi: 10.1073/pnas.0900641106 19429710
17. Chen Z, Liang S, Zhao Y, Han Z, miR-92b regulates Mef2 levels through a negative-feedback circuit during Drosophila muscle development. Development [Internet]. 2012 Oct [cited 2013 Aug 12];139(19):3543–52. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22899845 doi: 10.1242/dev.082719 22899845
18. Fuse N, Hisata K, Katzen AL, Matsuzaki F, Heterotrimeric G Proteins Regulate Daughter Cell Size Asymmetry in Drosophila Neuroblast Divisions. Curr Biol. 2003;13(15):947–54.
19. Song Y, Lu B, Regulation of cell growth by Notch signaling and its differential requirement in normal vs. tumor-forming stem cells in Drosophila. Genes Dev [Internet]. 2011 Dec 15 [cited 2014 Jun 4];25(24):2644–58. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3248685&tool=pmcentrez&rendertype=abstract doi: 10.1101/gad.171959.111 22190460
20. Xiao Q, Komori H, Lee C-Y, Klumpfuss Distinguishes Stem Cells From Progenitor Cells During Asymmetric Neuroblast Division. Development [Internet]. 2012 Aug [cited 2014 Mar 22];139(15):2670–80. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3392700&tool=pmcentrez&rendertype=abstract doi: 10.1242/dev.081687 22745313
21. Maurange C, Cheng L, Gould AP, Temporal transcription factors and their targets schedule the end of neural proliferation in Drosophila. Cell [Internet]. 2008 May 30 [cited 2014 Jun 7];133(5):891–902. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18510932 doi: 10.1016/j.cell.2008.03.034 18510932
22. Lai S-L, Doe CQ, Transient nuclear Prospero induces neural progenitor quiescence. Elife [Internet]. 2014 Jan [cited 2015 Jan 31];3:1–12. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4212206&tool=pmcentrez&rendertype=abstract doi: 10.7554/eLife.03363 25354199
23. Lee T, Luo L, Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron [Internet]. 1999 Mar;22(3):451–61. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10197526 10197526
24. Bartel DP, MicroRNAs: target recognition and regulatory functions. Cell [Internet]. 2009 Jan 23 [cited 2014 Jul 9];136(2):215–33. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3794896&tool=pmcentrez&rendertype=abstract doi: 10.1016/j.cell.2009.01.002 19167326
25. Hinske LCG, Galante P a F, Kuo WP, Ohno-Machado L, A potential role for intragenic miRNAs on their hosts’ interactome. BMC Genomics [Internet]. 2010 Jan;11:533. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3091682&tool=pmcentrez&rendertype=abstract doi: 10.1186/1471-2164-11-533 20920310
26. Liu M, Roth A, Yu M, Morris R, Bersani F, Rivera MN, et al. The IGF2 intronic miR-483 selectively enhances transcription from IGF2 fetal promoters and enhances tumorigenesis. Genes Dev [Internet]. 2013 Dec 1 [cited 2014 Jun 11];27(23):2543–8. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3861668&tool=pmcentrez&rendertype=abstract doi: 10.1101/gad.224170.113 24298054
27. Kos A, Olde Loohuis NFM, Wieczorek ML, Glennon JC, Martens GJM, Kolk SM, et al. A potential regulatory role for intronic microRNA-338-3p for its host gene encoding apoptosis-associated tyrosine kinase. PLoS One [Internet]. 2012 Jan [cited 2014 Jun 30];7(2):e31022. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3281898&tool=pmcentrez&rendertype=abstract doi: 10.1371/journal.pone.0031022 22363537
28. Dill H, Linder B, Fehr A, Fischer U, Intronic miR-26b controls neuronal differentiation by repressing its host transcript, ctdsp2. Genes Dev [Internet]. 2012 Jan 1 [cited 2014 Jun 14];26(1):25–30. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3258962&tool=pmcentrez&rendertype=abstract doi: 10.1101/gad.177774.111 22215807
29. Cao G, Huang B, Liu Z, Zhang J, Xu H, Xia W, et al. Intronic miR-301 feedback regulates its host gene, ska2, in A549 cells by targeting MEOX2 to affect ERK/CREB pathways. Biochem Biophys Res Commun [Internet]. Elsevier Inc.; 2010 Jun 11 [cited 2014 Jun 30];396(4):978–82. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20470754 doi: 10.1016/j.bbrc.2010.05.037 20470754
30. Zhu Y, Lu Y, Zhang Q, Liu J, Li T, Yang J, et al. MicroRNA-26a / b and their host genes cooperate to inhibit the G1 / S transition by activating the pRb protein. Nucleic Acids Res. 2012;40(10):4615–25. doi: 10.1093/nar/gkr1278 22210897
31. Zhou H, Rigoutsos I, MiR-103a-3p targets the 5 ′ UTR of GPRC5A in pancreatic cells. RNA. 2014;20:1–9. doi: 10.1261/rna.038182.113 24255166
32. Barik S, An intronic microRNA silences genes that are functionally antagonistic to its host gene. Nucleic Acids Res. 2008;36(16):5232–41. doi: 10.1093/nar/gkn513 18684991
33. Okamura K, Hagen JW, Duan H, Tyler DM, Lai EC, The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell [Internet]. 2007 Jul 13 [cited 2014 May 24];130(1):89–100. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2729315&tool=pmcentrez&rendertype=abstract 17599402
34. Sundaram GM, Common JEA, Gopal FE, Srikanta S, Lakshman K, Lunny DP, et al. “See-saw” expression of microRNA-198 and FSTL1 from a single transcript in wound healing. Nature [Internet]. 2013 Mar 7 [cited 2014 Jul 12];495(7439):103–6. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23395958 doi: 10.1038/nature11890 23395958
35. Bian S, Hong J, Li Q, Schebelle L, Pollock A, Knauss JL, et al. MicroRNA cluster miR-17-92 regulates neural stem cell expansion and transition to intermediate progenitors in the developing mouse neocortex. Cell Rep [Internet]. The Authors; 2013 May 30 [cited 2014 Jan 22];3(5):1398–406. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23623502 doi: 10.1016/j.celrep.2013.03.037 23623502
36. Nowakowski TJ, Fotaki V, Pollock A, Sun T, Pratt T, Price DJ. MicroRNA-92b regulates the development of intermediate cortical progenitors in embryonic mouse brain. 2013;1–6.
37. Fei J-F, Haffner C, Huttner WB, 3’ UTR-dependent, miR-92-mediated restriction of Tis21 expression maintains asymmetric neural stem cell division to ensure proper neocortex size. Cell Rep [Internet]. The Authors; 2014 Apr 24 [cited 2014 Jun 6];7(2):398–411. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24726360 doi: 10.1016/j.celrep.2014.03.033 24726360
38. Scotto-Lavino E, Du G, Frohman M a. 3’ end cDNA amplification using classic RACE. Nat Protoc [Internet]. 2006 Jan [cited 2015 Feb 26];1(6):2742–5. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17406530 17406530
39. Li Z, Lu Y, Xu X-L, Gao F-B, The FTD/ALS-associated RNA-binding protein TDP-43 regulates the robustness of neuronal specification through microRNA-9a in Drosophila. Hum Mol Genet [Internet]. 2013 Jan 15 [cited 2014 Sep 25];22(2):218–25. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3526156&tool=pmcentrez&rendertype=abstract doi: 10.1093/hmg/dds420 23042786