A large-scale functional screen identifies Nova1 and Ncoa3 as regulators of neuronal miRNA function

EMBO Journal

Volumn 34, Issue 17, 2015, Pages 2237-2254

  Störchel, Peter H ^a   Thümmler, Juliane ^a   Siegel, Gabriele ^a,b   Aksoy Aksel, Ayla ^a   Zampa, Federico ^a   Sumer, Simon ^a   Schratt, Gerhard ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Ago2; dendrite; miRNA; Ncoa3; Nova1

Indexed keywords

ARGONAUTE PROTEIN; MICRORNA; NCOA3 PROTEIN; NOVA1 PROTEIN; PROTEIN; RNA INDUCED SILENCING COMPLEX; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; AGO2 PROTEIN, RAT; NOVA1 PROTEIN, RAT; RNA BINDING PROTEIN; STEROID RECEPTOR COACTIVATOR 3;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN NUCLEUS; CELL MATURATION; CONTROLLED STUDY; CYTOPLASM; DENDRITE; DENDRITIC SPINE; EMBRYO; FEMALE; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC REGULATION; GENETIC SCREENING; HEK293 CELL LINE; HIPPOCAMPAL NEURONAL CULTURE; HIPPOCAMPUS; HUMAN; HUMAN CELL; LARGE SCALE PRODUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; RAT; ANIMAL; BIOSYNTHESIS; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ARGONAUTE PROTEINS; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; MICRORNAS; NEURONS; NUCLEAR RECEPTOR COACTIVATOR 3; RATS; RATS, SPRAGUE-DAWLEY; RNA-BINDING PROTEINS;

EID: 84940717973     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201490643     Document Type: Article

References (59)

1. Abdelmohsen K, Hutchison ER, Lee EK, Kuwano Y, Kim MM, Masuda K, Srikantan S, Subaran SS, Marasa BS, Mattson MP, Gorospe M, (2010) miR-375 inhibits differentiation of neurites by lowering HuD levels. Mol Cell Biol 30: 4197-4210
2. Agostini M, Tucci P, Steinert JR, Shalom-Feuerstein R, Rouleau M, Aberdam D, Forsythe ID, Young KW, Ventura A, Concepcion CP, Han YC, Candi E, Knight RA, Mak TW, Melino G, (2011) microRNA-34a regulates neurite outgrowth, spinal morphology, and function. Proc Natl Acad Sci USA 108: 21099-21104
3. Ashraf SI, McLoon AL, Sclarsic SM, Kunes S, (2006) Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 124: 191-205
4. Banerjee S, Neveu P, Kosik KS, (2009) A coordinated local translational control point at the synapse involving relief from silencing and MOV10 degradation. Neuron 64: 871-884
5. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W, (2006) Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125: 1111-1124
6. Borner K, Niopek D, Cotugno G, Kaldenbach M, Pankert T, Willemsen J, Zhang X, Schurmann N, Mockenhaupt S, Serva A, Hiet MS, Wiedtke E, Castoldi M, Starkuviene V, Erfle H, Gilbert DF, Bartenschlager R, Boutros M, Binder M, Streetz K, et al, (2013) Robust RNAi enhancement via human Argonaute-2 overexpression from plasmids, viral vectors and cell lines. Nucleic Acids Res 41: e199
7. Buckanovich RJ, Posner JB, Darnell RB, (1993) Nova, the paraneoplastic Ri antigen, is homologous to an RNA-binding protein and is specifically expressed in the developing motor system. Neuron 11: 657-672
8. Burroughs AM, Ando Y, de Hoon MJ, Tomaru Y, Suzuki H, Hayashizaki Y, Daub CO, (2011) Deep-sequencing of human Argonaute-associated small RNAs provides insight into miRNA sorting and reveals Argonaute association with RNA fragments of diverse origin. RNA Biol 8: 158-177
9. Christensen M, Larsen LA, Kauppinen S, Schratt G, (2010) Recombinant adeno-associated virus-mediated microRNA delivery into the postnatal mouse brain reveals a role for miR-134 in dendritogenesis in vivo. Front Neural Circuits 3: 16
10. Chu CY, Rana TM, (2006) Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. PLoS Biol 4: e210
11. Dasgupta S, Lonard DM, O'Malley BW, (2014) Nuclear receptor coactivators: master regulators of human health and disease. Annu Rev Med 65: 279-292
12. Dueck A, Ziegler C, Eichner A, Berezikov E, Meister G, (2012) microRNAs associated with the different human Argonaute proteins. Nucleic Acids Res 40: 9850-9862
13. Eulalio A, Rehwinkel J, Stricker M, Huntzinger E, Yang SF, Doerks T, Dorner S, Bork P, Boutros M, Izaurralde E, (2007) Target-specific requirements for enhancers of decapping in miRNA-mediated gene silencing. Genes Dev 21: 2558-2570
14. Eulalio A, Huntzinger E, Izaurralde E, (2008) Getting to the root of miRNA-mediated gene silencing. Cell 132: 9-14
15. Fabian MR, Sonenberg N, (2012) The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat Struct Mol Biol 19: 586-593
16. Fiore R, Khudayberdiev S, Christensen M, Siegel G, Flavell SW, Kim TK, Greenberg ME, Schratt G, (2009) Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. EMBO J 28: 697-710
17. Fiore R, Khudayberdiev S, Saba R, Schratt G, (2011) MicroRNA function in the nervous system. Prog Mol Biol Transl Sci 102: 47-100
18. Fiore R, Rajman M, Schwale C, Bicker S, Antoniou A, Bruehl C, Draguhn A, Schratt G, (2014) MiR-134-dependent regulation of Pumilio-2 is necessary for homeostatic synaptic depression. EMBO J 33: 2231-2246
19. Gao J, Wang WY, Mao YW, Graff J, Guan JS, Pan L, Mak G, Kim D, Su SC, Tsai LH, (2010) A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 466: 1105-1109
20. Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, Shiekhattar R, (2004) The Microprocessor complex mediates the genesis of microRNAs. Nature 432: 235-240
21. Grimm D, Streetz KL, Jopling CL, Storm TA, Pandey K, Davis CR, Marion P, Salazar F, Kay MA, (2006) Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441: 537-541
22. Huang YW, Ruiz CR, Eyler EC, Lin K, Meffert MK, (2012) Dual regulation of miRNA biogenesis generates target specificity in neurotrophin-induced protein synthesis. Cell 148: 933-946
23. Im HI, Kenny PJ, (2012) MicroRNAs in neuronal function and dysfunction. Trends Neurosci 35: 325-334
24. Jensen KB, Dredge BK, Stefani G, Zhong R, Buckanovich RJ, Okano HJ, Yang YY, Darnell RB, (2000) Nova-1 regulates neuron-specific alternative splicing and is essential for neuronal viability. Neuron 25: 359-371
25. Kedde M, Strasser MJ, Boldajipour B, Oude Vrielink JA, Slanchev K, le Sage C, Nagel R, Voorhoeve PM, van Duijse J, Orom UA, Lund AH, Perrakis A, Raz E, Agami R, (2007) RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131: 1273-1286
26. Kedde M, van Kouwenhove M, Zwart W, Oude Vrielink JA, Elkon R, Agami R, (2010) A Pumilio-induced RNA structure switch in p27-3′UTR controls miR-221 and miR-222 accessibility. Nat Cell Biol 12: 1014-1020
27. Krol J, Loedige I, Filipowicz W, (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11: 597-610
28. Landthaler M, Gaidatzis D, Rothballer A, Chen PY, Soll SJ, Dinic L, Ojo T, Hafner M, Zavolan M, Tuschl T, (2008) Molecular characterization of human Argonaute-containing ribonucleoprotein complexes and their bound target mRNAs. RNA 14: 2580-2596
29. Law WJ, Cann KL, Hicks GG, (2006) TLS, EWS and TAF15: a model for transcriptional integration of gene expression. Brief Funct Genomic Proteomic 5: 8-14
30. Leo C, Chen JD, (2000) The SRC family of nuclear receptor coactivators. Gene 245: 1-11
31. Licatalosi DD, Mele A, Fak JJ, Ule J, Kayikci M, Chi SW, Clark TA, Schweitzer AC, Blume JE, Wang X, Darnell JC, Darnell RB, (2008) HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 456: 464-469
32. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM, (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433: 769-773
33. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song JJ, Hammond SM, Joshua-Tor L, Hannon GJ, (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science 305: 1437-1441
34. Liu Y, Zhao Z, Yang F, Gao Y, Song J, Wan Y, (2013) microRNA-181a is involved in insulin-like growth factor-1-mediated regulation of the transcription factor CREB1. J Neurochem 126: 771-780
35. Long W, Yi P, Amazit L, LaMarca HL, Ashcroft F, Kumar R, Mancini MA, Tsai SY, Tsai MJ, O'Malley BW, (2010) SRC-3Delta4 mediates the interaction of EGFR with FAK to promote cell migration. Mol Cell 37: 321-332
36. Magill ST, Cambronne XA, Luikart BW, Lioy DT, Leighton BH, Westbrook GL, Mandel G, Goodman RH, (2010) microRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus. Proc Natl Acad Sci USA 107: 20382-20387
37. McKee AE, Minet E, Stern C, Riahi S, Stiles CD, Silver PA, (2005) A genome-wide in situ hybridization map of RNA-binding proteins reveals anatomically restricted expression in the developing mouse brain. BMC Dev Biol 5: 14
38. Meister G, (2013) Argonaute proteins: functional insights and emerging roles. Nat Rev Genet 14: 447-459
39. Meskauskas A, Dinman JD, (2001) Ribosomal protein L5 helps anchor peptidyl-tRNA to the P-site in Saccharomyces cerevisiae. RNA 7: 1084-1096
40. Mollet I, Barbosa-Morais NL, Andrade J, Carmo-Fonseca M, (2006) Diversity of human U2AF splicing factors. FEBS J 273: 4807-4816
41. Muddashetty RS, Nalavadi VC, Gross C, Yao X, Xing L, Laur O, Warren ST, Bassell GJ, (2011) Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling. Mol Cell 42: 673-688
42. Nishino J, Kim I, Chada K, Morrison SJ, (2008) Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf Expression. Cell 135: 227-239
43. Pillai RS, Bhattacharyya SN, Artus CG, Zoller T, Cougot N, Basyuk E, Bertrand E, Filipowicz W, (2005) Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 309: 1573-1576
44. Racca C, Gardiol A, Eom T, Ule J, Triller A, Darnell RB, (2010) The Neuronal Splicing Factor Nova Co-Localizes with Target RNAs in the Dendrite. Front Neural Circuits 4: 5
45. Schratt GM, Nigh EA, Chen WG, Hu L, Greenberg ME, (2004) BDNF regulates the translation of a select group of mRNAs by a mammalian target of rapamycin-phosphatidylinositol 3-kinase-dependent pathway during neuronal development. J Neurosci 24: 9366-9377
46. Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, Greenberg ME, (2006) A brain-specific microRNA regulates dendritic spine development. Nature 439: 283-289
47. Siegel G, Obernosterer G, Fiore R, Oehmen M, Bicker S, Christensen M, Khudayberdiev S, Leuschner PF, Busch CJ, Kane C, Hubel K, Dekker F, Hedberg C, Rengarajan B, Drepper C, Waldmann H, Kauppinen S, Greenberg ME, Draguhn A, Rehmsmeier M, et al, (2009) A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nat Cell Biol 11: 705-716
48. Siegel G, Saba R, Schratt G, (2011) microRNAs in neurons: manifold regulatory roles at the synapse. Curr Opin Genet Dev 21: 491-497
49. Smrt RD, Szulwach KE, Pfeiffer RL, Li X, Guo W, Pathania M, Teng ZQ, Luo Y, Peng J, Bordey A, Jin P, Zhao X, (2010) MicroRNA miR-137 regulates neuronal maturation by targeting ubiquitin ligase mind bomb-1. Stem Cells 28: 1060-1070
50. Stutz F, Izaurralde E, (2003) The interplay of nuclear mRNP assembly, mRNA surveillance and export. Trends Cell Biol 13: 319-327
51. Tang G, (2005) siRNA and miRNA: an insight into RISCs. Trends Biochem Sci 30: 106-114
52. Tharun S, He W, Mayes AE, Lennertz P, Beggs JD, Parker R, (2000) Yeast Sm-like proteins function in mRNA decapping and decay. Nature 404: 515-518
53. Valluy J, Bicker S, Aksoy-Aksel A, Lackinger M, Sumer S, Fiore R, Wust T, Seffer D, Metge F, Dieterich C, Wohr M, Schwarting R, Schratt G, (2015) A coding-independent function of an alternative Ube3a transcript during neuronal development. Nat Neurosci 18: 666-673
54. Wang D, Zhang Z, O'Loughlin E, Lee T, Houel S, O'Carroll D, Tarakhovsky A, Ahn NG, Yi R, (2012) Quantitative functions of Argonaute proteins in mammalian development. Genes Dev 26: 693-704
55. Xu J, Wu RC, O'Malley BW, (2009) Normal and cancer-related functions of the p160 steroid receptor co-activator (SRC) family. Nat Rev Cancer 9: 615-630
56. Yu C, York B, Wang S, Feng Q, Xu J, O'Malley BW, (2007) An essential function of the SRC-3 coactivator in suppression of cytokine mRNA translation and inflammatory response. Mol Cell 25: 765-778
57. Zhang J, Chen QM, (2013) Far upstream element binding protein 1: a commander of transcription, translation and beyond. Oncogene 32: 2907-2916
58. Zhou A, Ou AC, Cho A, Benz EJ Jr, Huang SC, (2008) Novel splicing factor RBM25 modulates Bcl-x pre-mRNA 5′ splice site selection. Mol Cell Biol 28: 5924-5936
59. Zou Y, Chiu H, Zinovyeva A, Ambros V, Chuang CF, Chang C, (2013) Developmental decline in neuronal regeneration by the progressive change of two intrinsic timers. Science 340: 372-376