Mir-23a and mir-125b regulate neural stem/progenitor cell proliferation by targeting Musashi1

RNA Biology

Volumn 11, Issue 9, 2014, Pages 1105-1112

  Gioia, Ubaldo ^a,b   Di Carlo, Valerio ^a,c   Caramanica, Pasquale ^a   Toselli, Camilla ^a,d   Cinquino, Antonella ^a   Marchioni, Marcella ^c   Laneve, Pietro ^d   Biagioni, Stefano ^a,c,d   Bozzoni, Irene ^a,c,d   Cacci, Emanuele ^a,c   Caffarelli, Elisa ^c,d  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

Astrocyte differentiation; Cell proliferation; microRNAs; Musashi1; Neural progenitors; Post transcriptional gene regulation

Indexed keywords

MICRORNA; MICRORNA 125B; MICRORNA 23A; MUSASHI1 PROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; MESSENGER RNA; MIRN125 MICRORNA, MOUSE; MIRN23B MICRORNA, MOUSE; MSI1H PROTEIN, MOUSE; NERVE PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; ASTROCYTE CULTURE; BRAIN CORTEX; CELL GROWTH; CELL POPULATION; CELL PROLIFERATION; FEMALE; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; NORTHERN BLOTTING; PROTEIN EXPRESSION; REGULATORY MECHANISM; UPREGULATION; ANIMAL; ANIMAL EMBRYO; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; ENZYME IMMUNOASSAY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOENZYME TECHNIQUES; MICE; MICRORNAS; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NEUROGENESIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA-BINDING PROTEINS; TRANSCRIPTIONAL ACTIVATION;

EID: 84921906552     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.35508     Document Type: Article

References (31)

1. Okano H, Imai T, Okabe M. Musashi: a translational regulator of cell fate. J Cell Sci 2002; 115:1355-9; PMID:11896183
2. Okano H, Kawahara H, Toriya M, Nakao K, Shibata S, Imai T. Function of RNA-binding protein musashi1 in stem cells. Exp Cell Res 2005; 306:349-56; PMID:15925591; http://dx.doi.org/10.1016/j.yexcr.2005.02.021
3. Kaneko Y, Sakakibara S, Imai T, Suzuki A, Nakamura Y, Sawamoto K, Ogawa Y, Toyama Y, Miyata T, Okano H. Musashi1: an evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev Neurosci 2000; 22:139-53; PMID:10657706; http://dx.doi.org/10.1159/000017435
4. Sakakibara S, Nakamura Y, Yoshida T, Shibata S, Koike M, Takano H, Ueda S, Uchiyama Y, Noda T, Okano H. RNA-binding protein musashi family: roles for CNS stem cells and a subpopulation of ependymal cells revealed by targeted disruption and antisense ablation. Proc Natl Acad Sci U S A 2002; 99:15194-9; PMID:12407178; http://dx.doi.org/10.1073/pnas.232087499
5. Siddall NA, McLaughlin EA, Marriner NL, Hime GR. The RNA-binding protein musashi is required intrinsically to maintain stem cell identity. Proc Natl Acad Sci U S A 2006; 103:8402-7; PMID:16717192; http://dx.doi.org/10.1073/pnas.0600906103
6. Takeda H, Koso H, Tessarollo L, Copeland NG, Jenkins NA. Musashi1-CreER(T2): a new cre line for conditional mutagenesis in neural stem cells. Genesis 2013; 51:128-34; PMID:23132814; http://dx.doi.org/10.1002/dvg.22357
7. Wakamatsu Y, Maynard TM, Jones SU, Weston JA. NUMB localizes in the basal cortex of mitotic avian neuroepithelial cells and modulates neuronal differentiation by binding to NOTCH-1. Neuron 1999; 23:71-81; PMID:10402194; http://dx.doi.org/10.1016/S0896-6273(00)80754-0
8. Imai T, Tokunaga A, Yoshida T, Hashimoto M, Mikoshiba K, Weinmaster G, Nakafuku M, Okano H. The neural RNA-binding protein musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA. Mol Cell Biol 2001; 21:3888-900; PMID:11359897; http://dx.doi.org/10.1128/MCB.21.12.3888-3900.2001
9. Kawahara H, Imai T, Imataka H, Tsujimoto M, Matsumoto K, Okano H. Neural RNA-binding protein Musashi1 inhibits translation initiation by competing with eIF4G for PABP. J Cell Biol 2008; 181:639-53; PMID:18490513; http://dx.doi.org/10.1083/jcb.200708004
10. Sakakibara S, Imai T, Hamaguchi K, Okabe M, Aruga J, Nakajima K, et al. Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev Biol 1996; 176:230-42; PMID:8660864; http://dx.doi.org/10.1006/dbio.1996.0130
11. Kawahara H, Okada Y, Imai T, Iwanami A, Mischel PS, Okano H. Musashi1 cooperates in abnormal cell lineage protein 28 (Lin28)-mediated let-7 family microRNA biogenesis in early neural differentiation. J Biol Chem 2011; 286:16121-30; PMID:21378162; http://dx.doi.org/10.1074/jbc.M110.199166
12. Rybak A, Fuchs H, Smirnova L, Brandt C, Pohl EE, Nitsch R, Wulczyn FG. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat Cell Biol 2008; 10:987-93; PMID:18604195; http://dx.doi.org/10.1038/ncb1759
13. Kanemura Y, Mori K, Sakakibara S, Fujikawa H, Hayashi H, Nakano A, Matsumoto T, Tamura K, Imai T, Ohnishi T, et al. Musashi1, an evolutionarily conserved neural RNA-binding protein, is a versatile marker of human glioma cells in determining their cellular origin, malignancy, and proliferative activity. Differentiation 2001; 68:141-52; PMID:11686236; http://dx.doi.org/10.1046/j.1432-0436.2001.680208.x
14. Toda M, Iizuka Y, Yu W, Imai T, Ikeda E, Yoshida K, Kawase T, Kawakami Y, Okano H, Uyemura K. Expression of the neural RNA-binding protein musashi1 in human gliomas. Glia 2001; 34:1-7; PMID:11284014; http://dx.doi.org/10.1002/glia.1034
15. Kawase S, Imai T, Miyauchi-Hara C, Yaguchi K, Nishimoto Y, Fukami S, Matsuzaki Y, Miyawaki A, Itohara S, Okano H. Identification of a novel intronic enhancer responsible for the transcriptional regulation of musashi1 in neural stem/progenitor cells. Mol Brain 2011; 4:14; PMID:21486496; http://dx.doi.org/10.1186/1756-6606-4-14
16. Cacci E, Ajmone-Cat MA, Anelli T, Biagioni S, Minghetti L. In vitro neuronal and glial differentiation from embryonic or adult neural precursor cells are differently affected by chronic or acute activation of microglia. Glia 2008; 56:412-25; PMID:18186084; http://dx.doi.org/10.1002/glia.20616
17. Ajmone-Cat MA, Cacci E, Ragazzoni Y, Minghetti L, Biagioni S. Pro-gliogenic effect of IL-1alpha in the differentiation of embryonic neural precursor cells in vitro. J Neurochem 2010; 113:1060-72; PMID:20236219; http://dx.doi.org/10.1111/j.1471-4159.2010.06670.x
18. Soldati C, Cacci E, Biagioni S, Carucci N, Lupo G, Perrone-Capano C, Saggio I, Augusti-Tocco G. Restriction of neural precursor ability to respond to nurr1 by early regional specification. PLoS One 2012; 7:e51798; PMID:23240065; http://dx.doi.org/10.1371/journal.pone.0051798
19. Sinno M, Biagioni S, Ajmone-Cat MA, Pafumi I, Caramanica P, Medda V, Tonti G, Minghetti L, Mannello F, Cacci E. The matrix metalloproteinase inhibitor marimastat promotes neural progenitor cell differentiation into neurons by gelatinase-independent TIMP-2-dependent mechanisms. Stem Cells Dev 2013; 22:345-58; PMID:23098139; http://dx.doi.org/10.1089/scd.2012.0299
20. Bonaguidi MA, McGuire T, Hu M, Kan L, Samanta J, Kessler JA. LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development 2005; 132:5503-14; PMID:16314487; http://dx.doi.org/10.1242/dev.02166
21. Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella G, et al. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 2005; 3:e283; PMID:16086633; http://dx.doi.org/10.1371/journal.pbio.0030283
22. Panchision DM, Pickel JM, Studer L, Lee SH, Turner PA, Hazel TG, McKay RD. Sequential actions of BMP receptors control neural precursor cell production and fate. Genes Dev 2001; 15:2094-110; PMID:11511541; http://dx.doi.org/10.1101/gad.894701
23. Ge W, Martinowich K, Wu X, He F, Miyamoto A, Fan G, Weinmaster G, Sun YE. Notch signaling promotes astrogliogenesis via direct CSL-mediated glial gene activation. J Neurosci Res 2002; 69:848-60; PMID:12205678; http://dx.doi.org/10.1002/jnr.10364
24. Borghese L, Dolezalova D, Opitz T, Haupt S, Leinhaas A, Steinfarz B, Koch P, Edenhofer F, Hampl A, Brüstle O. Inhibition of notch signaling in human embryonic stem cell-derived neural stem cells delays G1/S phase transition and accelerates neuronal differentiation in vitro and in vivo. Stem cells 2010; 28:955-64; PMID:20235098; http://dx.doi.org/10.1002/stem.408
25. Jovicic A, Roshan R, Moisoi N, Pradervand S, Moser R, Pillai B, Luthi-Carter R. Comprehensive expression analyses of neural cell-type-specific miRNAs identify new determinants of the specification and maintenance of neuronal phenotypes. J Neurosci 2013; 33:5127-37; PMID:23516279; http://dx.doi.org/10.1523/JNEUROSCI.0600-12.2013
26. Smirnova L, Grafe A, Seiler A, Schumacher S, Nitsch R, Wulczyn FG. Regulation of miRNA expression during neural cell specification. Eur J Neurosci 2005; 21:1469-77; PMID:15845075; http://dx.doi.org/10.1111/j.1460-9568.2005.03978.x
27. Freeman MR. Specification and morphogenesis of astrocytes. Science 2010; 330:774-8; PMID:21051628; http://dx.doi.org/10.1126/science.1190928
28. Zheng K, Li H, Huang H, Qiu M. MicroRNAs and glial cell development. Neuroscientist 2012; 18:114-8; PMID:21555783; http://dx.doi.org/10.1177/1073858411398322
29. Morlando M, Dini Modigliani S, Torrelli G, Rosa A, Di Carlo V, Caffarelli E, Bozzoni I. FUS stimulates microRNA biogenesis by facilitating co-transcriptional drosha recruitment. EMBO J 2012; 31:4502-10; PMID:23232809; http://dx.doi.org/10.1038/emboj.2012.319
30. Laneve P, Gioia U, Andriotto A, Moretti F, Bozzoni I, Caffarelli E. A minicircuitry involving REST and CREB controls miR-9-2 expression during human neuronal differentiation. Nucleic Acids Res 2010; 38:6895-905; PMID:20624818; http://dx.doi.org/10.1093/nar/gkq604
31. Di Carlo V, Grossi E, Laneve P, Morlando M, Dini Modigliani S, Ballarino M, Bozzoni I, Caffarelli E. TDP-43 Regulates the microprocessor complex activity during in vitro neuronal differentiation. Mol Neurobiol 2013; 48:952-63; PMID:24113842; http://dx.doi.org/10.1007/s12035-013-8564-x