MicroRNAs in neural stem cells and neurogenesis

Frontiers in Neuroscience

Volumn , Issue MAR, 2012, Pages 1-13

  Kawahara, Hironori ^a,b   Imai, Takao ^a   Okano, Hideyuki ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Let 7; Lin28; Microrna biogenesis; Musashi1; Neural progenitor cells; Neural stem cells; Neurogenesis

Indexed keywords

EXPORTIN 5; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN L; LIN28 PROTEIN; MICRORNA; MICRORNA 124; MICRORNA 132; MICRORNA 138; MICRORNA 142; MICRORNA 151; MICRORNA 212; MICRORNA 451; MICRORNA 9; MUSASHI 1; RETINOIC ACID INDUCIBLE PROTEIN I; RNA; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; BIOGENESIS; CELL DIFFERENTIATION; CHROMOSOME 19; EXON; GENE MUTATION; HUMAN; IMMUNOPRECIPITATION; INTERSPERSED REPEAT; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INTERACTION; REVIEW; RNA PROCESSING; RNA STRUCTURE; RNA TRANSCRIPTION; RNA TRANSLATION; TRANSLATION REGULATION;

EID: 84862206162     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2012.00030     Document Type: Review

References (129)

1. Andersson, T., Rahman, S., Sansom, S. N., Alsio, J. M., Kaneda, M., Smith, J., O'Carroll, D., Tarakhovsky, A., and Livesey, F. J. (2010). Reversible block of mouse neural stem cell differentiation in the absence of dicer and microRNAs. PLoS ONE 5, e13453. doi:10.1371/journal.pone.0013453
2. Balzer, E., and Moss, E. G. (2007). Localization of the developmental timing regulator Lin28 to mRNP complexes, P-bodies and stress granules. RNA Biol. 4, 16-25.
3. Bartel, D. P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233.
4. Bernstein, E., Caudy, A. A., Hammond, S. M., and Hannon, G. J. (2001). Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363-366.
5. Bhattacharyya, S. N., Habermacher, R., Martine, U., Closs, E. I., and Filipowicz, W. (2006). Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125, 1111-1124.
6. Blackshaw, S., Harpavat, S., Trimarchi, J., Cai, L., Huang, H., Kuo, W. P., Weber, G., Lee, K., Fraioli, R. E., Cho, S. H., Yung, R., Asch, E., Ohno-Machado, L., Wong, W. H., and Cepko, C. L. (2004). Genomic analysis of mouse retinal development. PLoS Biol. 2, e247. doi:10.1371/journal.pbio.0020247
7. Blow, M. J., Grocock, R. J., van Dongen, S., Enright, A. J., Dicks, E., Futreal, P. A., Wooster, R., and Stratton, M. R. (2006). RNA editing of human microRNAs. Genome Biol. 7, R27.
8. Bohnsack, M. T. (2004). Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of premiRNAs. RNA 10, 185-191.
9. Bonev, B., Pisco, A., and Papalopulu, N. (2011). MicroRNA-9 reveals regional diversity of neural progenitors along the anterior-posterior axis. Dev. Cell 20, 19-32.
10. Borchert, G. M., Lanier, W., and Davidson, B. L. (2006). RNA polymerase III transcribes human microRNAs. Nat. Struct. Mol. Biol. 13, 1097-1101.
11. Bortolin-Cavaille, M. L., Dance, M., Weber, M., and Cavaille, J. (2009). C19MC microRNAs are processed from introns of large Pol-II, non-proteincoding transcripts. Nucleic Acids Res. 37, 3464-3473.
12. Buratti, E., De Conti, L., Stuani, C., Romano, M., Baralle, M., and Baralle, F. (2010). Nuclear factor TDP-43 can affect selected microRNA levels. FEBS J. 277, 2268-2281.
13. Bussing, I., Slack, F. J., and Grosshans, H. (2008). let-7 microRNAs in development, stem cells and cancer. Trends Mol. Med. 14, 400-409.
14. Camargos, S., Scholz, S., Simon-Sanchez, J., Paisan-Ruiz, C., Lewis, P., Hernandez, D., Ding, J., Gibbs, J. R., Cookson, M. R., Bras, J., Guerreiro, R., Oliveira, C. R., Lees, A., Hardy, J., Cardoso, F., and Singleton, A. B. (2008). DYT16, a novel young-onset dystonia-parkinsonism disorder: identification of a segregating mutation in the stress-response protein PRKRA. Lancet Neurol. 7, 207-215.
15. Cao, X., Pfaff, S. L., and Gage, F. H. (2007). A functional study of miR-124 in the developing neural tube. Genes Dev. 21, 531-536.
16. Caudy, A. A., Ketting, R. F., Hammond, S. M., Denli, A. M., Bathoorn, A. M., Tops, B. B., Silva, J. M., Myers, M. M., Hannon, G. J., and Plasterk, R. H. (2003). A micrococcal nuclease homologue in RNAi effector complexes. Nature 425, 411-414.
17. Cheloufi, S., Dos Santos, C. O., Chong, M. M., and Hannon, G. J. (2010). A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 465, 584-589.
18. Chen, C. Y., Zheng, D., Xia, Z., and Shyu, A.B. (2009).Ago-TNRC6 triggers microRNA-mediated decay by promoting two deadenylation steps. Nat. Struct. Mol. Biol. 16, 1160-1166.
19. Chendrimada, T. P., Gregory, R. I., Kumaraswamy, E., Norman, J., Cooch, N., Nishikura, K., and Shiekhattar, R. (2005). TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436, 740-744.
20. Cheng, L. C., Pastrana, E., Tavazoie, M., and Doetsch, F. (2009). miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat. Neurosci. 12, 399-408.
21. Chiang, A. P., Beck, J. S., Yen, H. J., Tayeh, M. K., Scheetz, T. E., Swiderski, R. E., Nishimura, D. Y., Braun, T. A., Kim, K. Y., Huang, J., Elbedour, K., Carmi, R., Slusarski, D. C., Casavant, T. L., Stone, E. M., and Sheffield, V. C. (2006). Homozygosity mapping with SNP arrays identifies TRIM32, an E3 ubiquitin ligase, as a Bardet-Biedl syndrome gene (BBS11). Proc. Natl. Acad. Sci. U.S.A. 103, 6287-6292.
22. Chou, M. Y., Underwood, J. G., Nikolic, J., Luu, M. H., and Black, D. L. (2000). Multisite RNA binding and release of polypyrimidine tract binding protein during the regulation of c-src neural-specific splicing. Mol. Cell 5, 949-957.
23. Cifuentes, D., Xue, H., Taylor, D. W., Patnode, H., Mishima, Y., Cheloufi, S., Ma, E., Mane, S., Hannon, G. J., Lawson, N. D., Wolfe, S. A., and Giraldez, A. J. (2010). A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science 328, 1694-1698.
24. Czech, B., and Hannon, G. J. (2011). Small RNA sorting: matchmaking for Argonautes. Nat. Rev. Genet. 12, 19-31.
25. Davis, B. N., and Hata, A. (2010). MicroRNA in cancer - the involvement of aberrant microRNA biogenesis regulatory pathways. Genes Cancer 1, 1100-1114.
26. De Pietri Tonelli, D., Pulvers, J. N., Haffner, C., Murchison, E. P., Hannon, G. J., and Huttner, W. B. (2008). miRNAs are essential for survival and differentiation of newborn neurons but not for expansion of neural progenitors during early neurogenesis in the mouse embryonic neocortex. Development 135, 3911-3921.
27. Delaloy, C., Liu, L., Lee, J. A., Su, H., Shen, F., Yang, G. Y., Young, W. L., Ivey, K. N., and Gao, F. B. (2010). MicroRNA-9 coordinates proliferation and migration of human embryonic stem cell-derived neural progenitors. Cell Stem Cell 6, 323-335.
28. Dreyfuss, G., Kim, V. N., and Kataoka, N. (2002). Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell Biol. 3, 195-205.
29. Edbauer, D., Neilson, J. R., Foster, K. A., Wang, C. F., Seeburg, D.P., Batterton, M. N., Tada, T., Dolan, B. M., Sharp, P. A., and Sheng, M. (2010). Regulation of synaptic structure and function by FMRP-associated microR-NAs miR-125b and miR-132. Neuron 65, 373-384.
30. Enciu, A. M., Popescu, B. O., and Gheorghisan-Galateanu, A. (2011). MicroRNAs in brain development and degeneration. Mol. Biol. Rep. 39, 2243-2252.
31. Frosk, P., Weiler, T., Nylen, E., Sudha, T., Greenberg, C. R., Morgan, K., Fujiwara, T. M., and Wrogemann, K. (2002). Limb-girdle muscular dystrophy type 2H associated with mutation in TRIM32, a putative E3-ubiquitin-ligase gene. Am. J. Hum. Genet. 70, 663-672.
32. Fukuda, T., Yamagata, K., Fujiyama, S., Matsumoto, T., Koshida, I., Yoshimura, K., Mihara, M., Naitou, M., Endoh, H., Nakamura, T., Akimoto, C., Yamamoto, Y., Katagiri, T., Foulds, C., Takezawa, S., Kitagawa, H., Takeyama, K., O'Malley, B. W., and Kato, S. (2007). DEAD-boxRNA helicase subunits of the Drosha complex are required for processing of rRNA and a subset of microRNAs. Nat. Cell Biol. 9, 604-611.
33. Giraldez, A. J., Mishima, Y., Rihel, J., Grocock, R. J., Van Dongen, S., Inoue, K., Enright, A. J., and Schier, A. F. (2006). Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312, 75-79.
34. Greenway, M. J., Andersen, P. M., Russ, C., Ennis, S., Cashman, S., Donaghy, C., Patterson, V., Swingler, R., Kieran, D., Prehn, J., Morrison, K. E., Green, A., Acharya, K. R., Brown, R. H. Jr., and Hardiman, O. (2006). ANG mutations segregate with familial and "sporadic" amyotrophic lateral sclerosis. Nat. Genet. 38, 411-413.
35. Gregory, R. I., Yan, K. P., Amuthan, G., Chendrimada, T., Doratotaj, B., Cooch, N., and Shiekhattar, R. (2004). The microprocessor complex mediates the genesis of microRNAs. Nature 432, 235-240.
36. Haase, A. D., Jaskiewicz, L., Zhang, H., Laine, S., Sack, R., Gatignol, A., and Filipowicz, W. (2005). TRBP, a regulator of cellular PKR and HIV-1 virus expression, interacts with Dicer and functions in RNA silencing. EMBO Rep. 6, 961-967.
37. Hagan, J. P., Piskounova, E., and Gregory, R. I. (2009). Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat. Struct. Mol. Biol. 16, 1021-1025.
38. Han, J., Lee, Y., Yeom, K. H., Kim, Y. K., Jin, H., and Kim, V. N. (2004). The Drosha-DGCR8 complexin primary microRNA processing. Genes Dev. 18, 3016-3027.
39. Han, J., Lee, Y., Yeom, K. H., Nam, J. W., Heo, I., Rhee, J. K., Sohn, S. Y., Cho, Y., Zhang, B. T., and Kim, V. N. (2006). Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 125, 887-901.
40. Heo, I., Joo, C., Cho, J., Ha, M., Han, J., and Kim, V. N. (2008). Lin28 mediates the terminal uridylation of let-7 precursor microRNA. Mol. Cell 32, 276-284.
41. Ho, L., and Crabtree, G. R. (2010). Chromatin remodelling during development. Nature 463, 474-484.
42. Imai, T., Tokunaga, A., Yoshida, T., Hashimoto, M., Mikoshiba, K., Weinmaster, G., Nakafuku, M., and Okano, H. (2001). The neural RNA-binding protein Musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA. Mol. Cell. Biol. 21, 3888-3900.
43. Jin, P., Zarnescu, D. C., Ceman, S., Nakamoto, M., Mowrey, J., Jongens, T. A., Nelson, D. L., Moses, K., and Warren, S. T. (2004). Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nat. Neurosci. 7, 113-117.
44. Kawahara, H., Imai, T., Imataka, H., Tsujimoto, M., Matsumoto, K., and Okano, H. (2008). Neural RNA-binding protein Musashi1 inhibits translation initiation by competing with eIF4G for PABP. J. Cell Biol. 181, 639-653.
45. Kawahara, H., Okada, Y., Imai, T., Iwanami, A., Mischel, P. S., and Okano, H. (2011). Musashi1 cooperates in abnormal cell lineage protein 28 (Lin28)-mediated Let-7 family microRNA biogenesis in early neural differentiation. J. Biol. Chem. 286, 16121-16130.
46. Kawahara, Y., Zinshteyn, B., Chendrimada, T. P., Shiekhattar, R., and Nishikura, K. (2007a). RNA editing of the microRNA-151 precursor blocks cleavage by the Dicer-TRBP complex. EMBO Rep. 8, 763-769.
47. Kawahara, Y., Zinshteyn, B., Sethupathy, P., Iizasa, H., Hatzigeorgiou, A. G., and Nishikura, K. (2007b). Redirection of silencing targets by adenosine-to-inosine editing of miRNAs. Science 315, 1137-1140.
48. Kawamata, T., and Tomari, Y. (2010). Making RISC. Trends Biochem. Sci. 35, 368-376.
49. Kawase-Koga, Y., Otaegi, G., and Sun, T. (2009). Different timings of Dicer deletion affect neurogenesis and gliogenesis in the developing mouse central nervous system. Dev. Dyn. 238, 2800-2812.
50. Kedde, M., Strasser, M. J., Boldajipour, B., Oude Vrielink, J. A., Slanchev, K., Le Sage, C., Nagel, R., Voorhoeve, P. M., van Duijse, J., Orom, U. A., Lund, A. H., Perrakis, A., Raz, E., and Agami, R. (2007). RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131, 1273-1286.
51. Ketting, R. F., Fischer, S. E., Bernstein, E., Sijen, T., Hannon, G. J., and Plasterk, R. H. (2001). Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev. 15, 2654-2659.
52. Khvorova, A., Reynolds, A., and Jayasena, S. D. (2003). Functional siRNAs and miRNAs exhibit strand bias. Cell 115, 209-216.
53. Kim, H. H., Kuwano, Y., Srikantan, S., Lee, E. K., Martindale, J. L., and Gorospe, M. (2009a). HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev. 23, 1743-1748.
54. Kim, V. N., Han, J., and Siomi, M. C. (2009b). Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10, 126-139.
55. Kim, H. J., Sohn, K. M., Shy, M. E., Krajewski, K. M., Hwang, M., Park, J. H., Jang, S. Y., Won, H. H., Choi, B. O., Hong, S. H., Kim, B. J., Suh, Y. L., Ki, C. S., Lee, S. Y., Kim, S. H., and Kim, J. W. (2007). Mutations in PRPS1, which encodes the phosphoribosyl pyrophosphate synthetase enzyme critical for nucleotide biosynthesis, cause hereditary peripheral neuropathy with hearing loss and optic neuropathy (cmtx5). Am. J. Hum. Genet. 81, 552-558.
56. Ko, M. H., Kim, S., Hwang do, W., Ko, H. Y., Kim, Y. H., and Lee, D. S. (2008). Bioimaging of the unbalanced expression of microRNA9 and microRNA9* during the neuronal differentiation of P19 cells. FEBS J. 275, 2605-2616.
57. Kumar, M. S., Lu, J., Mercer, K. L., Golub, T. R., and Jacks, T. (2007). Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat. Genet. 39, 673-677.
58. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Radmark, O., Kim, S., Yim, J., Lee, J., Provost, P., Rådmark, O., Kim, S., and Kim, V. N. (2003). The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415-419.
59. Lee, Y., Hur, I., Park, S.Y., Kim, Y. K., Suh, M. R., and Kim, V. N. (2006). The role of PACT in the RNA silencing pathway. EMBO J. 25, 522-532.
60. Lee, Y., Kim, M., Han, J., Yeom, K. H., Lee, S., Baek, S. H., and Kim, V. N. (2004). MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23, 4051-4060.
61. Leucht, C., Stigloher, C., Wizenmann, A., Klafke, R., Folchert, A., and Bally-Cuif, L. (2008). MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nat. Neurosci. 11, 641-648.
62. Li, M., Lee, K. F., Lu, Y., Clarke, I., Shih, D., Eberhart, C., Collins, V. P., Van Meter, T., Picard, D., Zhou, L., Boutros, P. C., Modena, P., Liang, M. L., Scherer, S. W., Bouffet, E., Rutka, J. T., Pomeroy, S. L., Lau, C. C., Taylor, M. D., Gajjar, A., Dirks, P. B., Hawkins, C. E., and Huang, A. (2009). Frequent amplification of a chr19q13.41 microRNA polycistron in aggressive primitive neuroecto-dermal brain tumors. Cancer Cell 16, 533-546.
63. Li, Y., Wang, F., Lee, J. A., and Gao, F. B. (2006). MicroRNA-9a ensures the precise specification of sensory organ precursors in Drosophila. Genes Dev. 20, 2793-2805.
64. Liu, H. K., Wang, Y., Belz, T., Bock, D., Takacs, A., Radlwimmer, B., Barbus, S., Reifenberger, G., Lichter, P., and Schutz, G. (2010). The nuclear receptor tailless induces long-term neural stem cell expansion and brain tumor initiation. Genes Dev. 24, 683-695.
65. Liu, J., Rivas, F.V., Wohlschlegel, J., Yates, J. R. III, Parker, R., and Hannon, G. J. (2005).Aroleforthe P-body component GW182 in microRNA function. Nat. Cell Biol. 7, 1261-1266.
66. Luikart, B. W., Bensen, A. L., Washburn, E. K., Perederiy, J. V., Su, K. G., Li, Y., Kernie, S. G., Parada, L. F., and Westbrook, G. L. (2011). miR-132 mediates the integrationof newborn neurons into the adult dentate gyrus. PLoS ONE 6, e19077. doi:10.1371/journal.pone.0019077
67. Lund, E., Guttinger, S., Calado, A., Dahlberg, J. E., and Kutay, U. (2004). Nuclear export of microRNA precursors. Science 303, 95-98.
68. Magill, S. T., Cambronne, X. A., Luikart, B. W., Lioy, D. T., Leighton, B. H., Westbrook, G. L., Mandel, G., and Goodman, R.H. (2010).MicroRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus. Proc. Natl. Acad. Sci. U.S.A. 107, 20382-20387.
69. Makeyev, E. V., Zhang, J., Carrasco, M. A., and Maniatis, T. (2007). The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell 27, 435-448.
70. Marson, A., Levine, S. S., Cole, M. F., Frampton, G. M., Brambrink, T., Johnstone, S., Guenther, M. G., Johnston, W. K., Wernig, M., Newman, J., Calabrese, J. M., Dennis, L. M., Volkert, T. L., Gupta, S., Love, J., Hannett, N., Sharp, P. A., Bartel, D. P., Jaenisch, R., and Young, R. A. (2008). Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134, 521-533.
71. McLaughlin, R. L., Phukan, J., McCormack, W., Lynch, D. S., Greenway, M., Cronin, S., Saunders, J., Slowik, A., Tomik, B., Andersen, P. M., Bradley, D. G., Jakeman, P., and Hardiman, O. (2010). Angiogenin levels and ANG genotypes: dysregulation in amyotrophic lateral sclerosis. PLoS ONE 5, e15402. doi:10.1371/journal.pone.0015402
72. Melton, C., Judson, R. L., and Blelloch, R. (2010). Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature 463, 621-626.
73. Michlewski, G., and Caceres, J. F. (2010). Antagonistic role of hnRNP A1 and KSRP in the regulation of let-7a biogenesis. Nat. Struct. Mol. Biol. 17, 1011-1018.
74. Mishima, Y., Giraldez, A. J., Takeda, Y., Fujiwara, T., Sakamoto, H., Schier, A. F., and Inoue, K. (2006). Differential regulation of germline mRNAs in soma and germ cells by zebrafish miR-430. Curr. Biol. 16, 2135-2142.
75. Moss, E. G., Lee, R. C., and Ambros, V. (1997). The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA. Cell 88, 637-646.
76. Neumuller, R. A., Betschinger, J., Fischer, A., Bushati, N., Poernbacher, I., Mechtler, K., Cohen, S. M., and Knoblich, J. A. (2008). Mei-P26 regulates microRNAs and cell growth in the Drosophila ovarian stem cell lineage. Nature 454, 241-245.
77. Newman, M. A., and Hammond, S. M. (2010). Emerging paradigms of regulated microRNA processing. Genes Dev. 24, 1086-1092.
78. Newman, M. A., Thomson, J. M., and Hammond, S. M. (2008). Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA 14, 1539-1549.
79. Nishikura, K. (2010). Functions and regulation of RNA editing by ADAR deaminases. Annu. Rev. Biochem. 79, 321-349.
80. Nishino, J., Kim, I., Chada, K., and Morrison, S. J. (2008). Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4aand p19Arf expression. Cell 135, 227-239.
81. Obernosterer, G., Leuschner, P. J., Alenius, M., and Martinez, J. (2006). Post-transcriptional regulation of microRNA expression. RNA 12, 1161-1167.
82. Okamura, K., Hagen, J. W., Duan, H., Tyler, D. M., and Lai, E. C. (2007). The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 130, 89-100.
83. Okano, H., Imai, T., and Okabe, M. (2002). Musashi: a translational regulator of cell fate. J. Cell. Sci. 115, 1355-1359.
84. Okano, H., Kawahara, H., Toriya, M., Nakao, K., Shibata, S., and Imai, T. (2005). Function of RNA-binding protein Musashi-1 in stem cells. Exp. Cell Res. 306, 349-356.
85. Okano, H. J., and Darnell, R. B. (1997). A hierarchy of Hu RNA binding proteins in developing and adult neurons. J. Neurosci. 17, 3024-3037.
86. Ozsolak, F., Poling, L. L., Wang, Z., Liu, H., Liu, X. S., Roeder, R. G., Zhang, X., Song, J. S., and Fisher, D. E. (2008). Chromatin structure analyses identify miRNA promoters. Genes Dev. 22, 3172-3183.
87. Park, H. J., Kim, J. K., Jeon, H. M., Oh, S. Y., Kim, S. H., Nam, D. H., and Kim, H. (2010). The neural stem cell fate determinant TLX promotes tumorigenesis and genesis of cells resembling glioma stem cells. Mol. Cells 30, 403-408.
88. Peters, L., and Meister, G. (2007). Argonaute proteins: mediators of RNA silencing. Mol. Cell 26, 611-623.
89. Pillai, R. S. (2005). MicroRNA function: multiple mechanisms for a tiny RNA? RNA 11, 1753-1761.
90. Piskounova, E., Viswanathan, S. R., Janas, M., LaPierre, R. J., Daley, G. Q., Sliz, P., and Gregory, R. I. (2008). Determinants of microRNA processing inhibition by the developmentally regulated RNA-binding protein Lin28. J. Biol. Chem. 283, 21310-21314.
91. Polesskaya, A., Cuvellier, S., Naguibneva, I., Duquet, A., Moss, E. G., and Harel-Bellan, A. (2007). Lin-28 binds IGF-2 mRNA and participates in skeletal myogenesis by increasing translation efficiency. Genes Dev. 21, 1125-1138.
92. Ponomarev, E. D., Veremeyko, T., Barteneva, N., Krichevsky, A. M., and Weiner, H. L. (2011). MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-alpha-PU.1 pathway. Nat. Med. 17, 64-70.
93. Qu, Q., and Shi, Y. (2009). Neural stem cells in the developing and adult brains. J. Cell. Physiol. 221, 5-9.
94. Qu, Q., Sun, G., Li, W., Yang, S., Ye, P., Zhao, C., Yu, R. T., Gage, F. H., Evans, R. M., and Shi, Y. (2010). Orphan nuclear receptor TLX activates Wnt/beta-catenin signalling to stimulate neural stem cell proliferation and self-renewal. Nat. Cell Biol. 12, 31-40; sup 31-39.
95. Romanelli, M. G., Lorenzi, P., and Morandi, C. (2000). Organization of the human gene encoding heterogeneous nuclear ribonucleoprotein type I (hnRNP I) and characterization of hnRNP I related pseudogene. Gene 255, 267-272.
96. Ruby, J. G., Jan, C. H., and Bartel, D. P. (2007). Intronic microRNA precursors that bypass Drosha processing. Nature 448, 83-86.
97. Rybak, A., Fuchs, H., Smirnova, L., Brandt, C., Pohl, E. E., Nitsch, R., and Wulczyn, F. G. (2008). A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat. Cell Biol. 10, 987-993.
98. Saini, H. K., Enright, A. J., and Griffiths-Jones, S. (2008). Annotation of mammalian primary microRNAs. BMC Genomics 9, 564. doi:10.1186/1471-2164-9-564
99. Sakakibara, S., Imai, T., Hamaguchi, K., Okabe, M., Aruga, J., Nakajima, K., Yasutomi, D., Nagata, T., Kurihara, Y., Uesugi, S., Miyata, T., Ogawa, M., Mikoshiba, K., and Okano, H. (1996). Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev. Biol. 176, 230-242.
100. Sakakibara, S., Nakamura, Y., Yoshida, T., Shibata, S., Koike, M., Takano, H., Ueda, S., Uchiyama, Y., Noda, T., andOkano, H. (2002).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. 99, 15194-15199.
101. Sanuki, R., Onishi, A., Koike, C., Muramatsu, R., Watanabe, S., Muranishi, Y., Irie, S., Uneo, S., Koyasu, T., Matsui, R., Chérasse, Y., Urade, Y., Watanabe, D., Kondo, M., Yamashita, T., and Furukawa, T. (2011). miR-124a is required for hippocampal axogenesis and retinal cone survival through Lhx2 suppression. Nat. Neurosci. 14, 1125-1134.
102. Schwamborn, J. C., Berezikov, E., and Knoblich, J. A. (2009). The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 136, 913-925.
103. Schwarz, D. S., Hutvagner, G., Du, T., Xu, Z., Aronin, N., and Zamore, P. D. (2003). Asymmetry in the assembly of the RNAi enzyme complex. Cell 115, 199-208.
104. Seoane, J., Le, H. V., Shen, L., Anderson, S. A., and Massague, J. (2004). Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 117, 211-223.
105. Shibata, M., Kurokawa, D., Nakao, H., Ohmura, T., and Aizawa, S. (2008). MicroRNA-9 modulates Cajal-Retzius cell differentiation by suppressing Foxg1 expression in mouse medial pallium. J. Neurosci. 28, 10415-10421.
106. Shibata, M., Nakao, H., Kiyonari, H., Abe, T., and Aizawa, S. (2011). MicroRNA-9 regulates neurogenesis in mouse telencephalon by targeting multiple transcription factors. J. Neurosci. 31, 3407-3422.
107. Siomi, H., and Siomi, M. C. (2010). Posttranscriptional regulation of microRNA biogenesis in animals. Mol. Cell 38, 323-332.
108. Song, J. J., Liu, J., Tolia, N. H., Schneiderman, J., Smith, S. K., Martienssen, R. A., Hannon, G. J., and Joshua-Tor, L. (2003). The crystal structure of the Argonaute2 PAZ domain reveals an RNA binding motif in RNAi effector complexes. Nat. Struct. Biol. 10, 1026-1032.
109. Thomson, J. M., Newman, M., Parker, J. S., Morin-Kensicki, E. M., Wright, T., and Hammond, S. M. (2006). Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev. 20, 2202-2207.
110. Tomari, Y., and Zamore, P. D. (2005). Perspective: machines for RNAi. Genes Dev. 19, 517-529.
111. Vierbuchen, T., Ostermeier, A., Pang, Z. P., Kokubu, Y., Sudhof, T. C., and Wernig, M. (2010). Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463, 1035-1041.
112. Viswanathan, S. R., Daley, G. Q., and Gregory, R. I. (2008). Selective blockade of microRNA processing by Lin28. Science 320, 97-100.
113. Viswanathan, S. R., Powers, J. T., Einhorn, W., Hoshida, Y., Ng, T. L., Toffanin, S., O'Sullivan, M., Lu, J., Phillips, L. A., Lockhart, V. L., Shah, S. P., Tanwar, P. S., Mermel, C. H., Beroukhim, R., Azam, M., Teixeira, J., Meyerson, M., Hughes, T. P., Llovet, J. M., Radich, J., Mullighan, C. G., Golub, T. R., Sorensen, P. H., and Daley, G. Q. (2009). Lin28 promotes transformation and is associated with advanced human malignancies.Nat. Genet.41, 843-848.
114. Vo, N., Klein, M. E., Varlamova, O., Keller, D. M., Yamamoto, T., Goodman, R. H., and Impey, S. (2005). A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc. Natl. Acad. Sci. U.S.A. 102, 16426-16431.
115. Wang, Y., Juranek, S., Li, H., Sheng, G., Tuschl, T., and Patel, D. J. (2008a). Structure of an argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature 456, 921-926.
116. Wang, Y., Sheng, G., Juranek, S., Tuschl, T., and Patel, D. J. (2008b). Structure of the guide-strand-containing argonaute silencing complex. Nature 456, 209-213.
117. Wang, Y., Medvid, R., Melton, C., Jaenisch, R., and Blelloch, R. (2007). DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat. Genet. 39, 380-385.
118. Wu, L., Fan, J., and Belasco, J. G. (2006). MicroRNAs direct rapid deadenylation of mRNA. Proc. Natl. Acad. Sci. U.S.A. 103, 4034-4039.
119. Wulczyn, F. G., Smirnova, L., Rybak, A., Brandt, C., Kwidzinski, E., Ninnemann, O., Strehle, M., Seiler, A., Schumacher, S., and Nitsch, R. (2007). Post-transcriptional regulation of the let-7 microRNA during neural cell specification. FASEB J. 21, 415-426.
120. Xu, X. L., Li, Y., Wang, F., and Gao, F. B. (2008). The steady-state level of the nervous-system-specific microRNA-124a is regulated by dFMR1 in Drosophila. J. Neurosci. 28, 11883-11889.
121. Yamagata, K., Fujiyama, S., Ito, S., Ueda, T., Murata, T., Naitou, M., Takeyama, K., Minami, Y., O'Malley, B. W., and Kato, S. (2009). Maturation of microRNA is hormonally regulated by a nuclear receptor. Mol. Cell 36, 340-347.
122. Yamasaki, S., Ivanov, P., Hu, G. F., and Anderson, P. (2009). Angiogenin cleaves tRNA and promotes stress-induced translational repression. J. Cell Biol. 185, 35-42.
123. Yang, W., Chendrimada, T. P., Wang, Q., Higuchi, M., Seeburg, P. H., Shiekhattar, R., and Nishikura, K. (2006). Modulation of microRNA processing and expression through RNA editing by ADAR deaminases. Nat. Struct. Mol. Biol. 13, 13-21.
124. Yano, M., Okano, H. J., and Okano, H. (2005). Involvement of Hu and heterogeneous nuclear ribonucleoprotein K in neuronal differentiation through p21 mRNA post-transcriptional regulation. J. Biol. Chem. 280, 12690-12699.
125. Yi, R., Qin, Y., Macara, I. G., and Cullen, B. R. (2003). Exportin-5 mediates the nuclear export of pre-microRNAsand short hairpin RNAs. Genes Dev. 17, 3011-3016.
126. Yoo, A. S., Staahl, B. T., Chen, L., and Crabtree, G. R. (2009). MicroRNA-mediated switching of chromatin-remodelling complexes in neural development. Nature 460, 642-646.
127. Yoo, A. S., Sun, A. X., Li, L., Shcheglovitov, A., Portmann, T., Li, Y., Lee-Messer, C., Dolmetsch, R. E., Tsien, R. W., and Crabtree, G. R. (2011). MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 476, 228-231.
128. Yu, J., Vodyanik, M. A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J. L., Tian, S., Nie, J., Jonsdottir, G. A., Ruotti, V., Stewart, R., Slukvin, I. I., and Thomson, J. A. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920.
129. Zhao, C., Sun, G., Li, S., Lang, M. F., Yang, S., Li, W., and Shi, Y. (2010). MicroRNA let-7b regulates neural stem cell proliferation and differentiation by targeting nuclear receptor TLX signaling. Proc. Natl. Acad. Sci. U.S.A. 107, 1876-1881.