MicroRNA-9 Coordinates Proliferation and Migration of Human Embryonic Stem Cell-Derived Neural Progenitors

Cell Stem Cell

Volumn 6, Issue 4, 2010, Pages 323-335

  Delaloy, Celine ^a   Liu, Lei ^a   Lee, Jin A ^a   Su, Hua ^b   Shen, Fanxia ^b   Yang, Guo Yuan ^b   Young, William L ^b   Ivey, Kathy N ^c   Gao, Fen Biao ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

STEMCELL

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; MICRORNA; MICROTUBULE ASSOCIATED PROTEIN 2; OCTAMER TRANSCRIPTION FACTOR 4; STATHMIN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR SOX2;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENZYME INHIBITION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOSS; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MICROTUBULE; MOUSE; NEURAL STEM CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STROKE; UPREGULATION;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICE; MICRORNAS; NEURONS; RATS; RNA, MESSENGER; STATHMIN;

RATTUS;

EID: 77949903674     PISSN: 19345909     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stem.2010.02.015     Document Type: Article

References (44)

1. Ambros V. microRNAs: Tiny regulators with great potential. Cell 107 (2001) 823-826
2. Ambros V., and Chen X. The regulation of genes and genomes by small RNAs. Development 134 (2007) 1635-1641
3. Ayala R., Shu T., and Tsai L.H. Trekking across the brain: The journey of neuronal migration. Cell 128 (2007) 29-43
4. Baldassarre G., Belletti B., Nicoloso M.S., Schiappacassi M., Vecchione A., Spessotto P., Morrione A., Canzonieri V., and Colombatti A. p27(Kip1)-stathmin interaction influences sarcoma cell migration and invasion. Cancer Cell 7 (2005) 51-63
5. Bartel D.P. MicroRNAs: Target recognition and regulatory functions. Cell 136 (2009) 215-233
6. Belletti B., Nicoloso M.S., Schiappacassi M., Berton S., Lovat F., Wolf K., Canzonieri V., D'Andrea S., Zucchetto A., Friedl P., et al. Stathmin activity influences sarcoma cell shape, motility, and metastatic potential. Mol. Biol. Cell 19 (2008) 2003-2013
7. Belmont L.D., and Mitchison T.J. Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell 84 (1996) 623-631
8. Biryukova I., Asmar J., Abdesselem H., and Heitzler P. Drosophila mir-9a regulates wing development via fine-tuning expression of the LIM only factor, dLMO. Dev. Biol. 327 (2009) 487-496
9. Bushati N., and Cohen S.M. microRNA functions. Annu. Rev. Cell Dev. Biol. 23 (2007) 175-205
10. Cobos I., Borello U., and Rubenstein J.L. Dlx transcription factors promote migration through repression of axon and dendrite growth. Neuron 54 (2007) 873-888
11. Delaloy C., and Gao F.-B. microRNA-9 multitasking near organizing centers. Nat. Neurosci. 11 (2008) 625-626
12. Deo M., Yu J.Y., Chung K.H., Tippens M., and Turner D.L. Detection of mammalian microRNA expression by in situ hybridization with RNA oligonucleotides. Dev. Dyn. 235 (2006) 2538-2548
13. Duan X., Kang E., Liu C.Y., Ming G.L., and Song H. Development of neural stem cell in the adult brain. Curr. Opin. Neurobiol. 18 (2008) 108-115
14. Elkabetz Y., Panagiotakos G., Al Shamy G., Socci N.D., Tabar V., and Studer L. Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev. 22 (2008) 152-165
15. Filipowicz W., Bhattacharyya S.N., and Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight?. Nat. Rev. Genet. 9 (2008) 102-114
16. Fish J.E., Santoro M.M., Morton S.U., Yu S., Yeh R.F., Wythe J.D., Ivey K.N., Bruneau B.G., Stainier D.Y., and Srivastava D. miR-126 regulates angiogenic signaling and vascular integrity. Dev. Cell 15 (2008) 272-284
17. Gadea G., de Toledo M., Anguille C., and Roux P. Loss of p53 promotes RhoA-ROCK-dependent cell migration and invasion in 3D matrices. J. Cell Biol. 178 (2007) 23-30
18. Gao F.B. Posttranscriptional control of neuronal development by microRNA networks. Trends Neurosci. 31 (2008) 20-26
19. Giampietro C., Luzzati F., Gambarotta G., Giacobini P., Boda E., Fasolo A., and Perroteau I. Stathmin expression modulates migratory properties of GN-11 neurons in vitro. Endocrinology 146 (2005) 1825-1834
20. Hobert O. Gene regulation by transcription factors and microRNAs. Science 319 (2008) 1785-1786
21. Hochedlinger K., and Jaenisch R. Nuclear transplantation, embryonic stem cells, and the potential for cell therapy. N. Engl. J. Med. 349 (2003) 275-286
22. Jin K., Mao X.O., Cottrell B., Schilling B., Xie L., Row R.H., Sun Y., Peel A., Childs J., Gendeh G., et al. Proteomic and immunochemical characterization of a role for stathmin in adult neurogenesis. FASEB J. 18 (2004) 287-299
23. Kosik K.S. The neuronal microRNA system. Nat. Rev. Neurosci. 7 (2006) 911-920
24. Lagos-Quintana M., Rauhut R., Yalcin A., Meyer J., Lendeckel W., and Tuschl T. Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12 (2002) 735-739
25. Leucht C., Stigloher C., Wizenmann A., Klafke R., Folchert A., and Bally-Cuif L. MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nat. Neurosci. 11 (2008) 641-648
26. Li X.-J., and Zhang S.C. In vitro differentiation of neural precursors from human embryonic stem cells. Methods Mol. Biol. 331 (2006) 169-177
27. Li Y., Wang F., Lee J.A., and Gao F.B. MicroRNA-9a ensures the precise specification of sensory organ precursors in Drosophila. Genes Dev. 20 (2006) 2793-2805
28. Mao Y., Ge X., Frank C.L., Madison J.M., Koehler A.N., Doud M.K., Tassa C., Berry E.M., Soda T., Singh K.K., et al. Disrupted in schizophrenia 1 regulates neuronal progenitor proliferation via modulation of GSK3beta/beta-catenin signaling. Cell 136 (2009) 1017-1031
29. Pietrzykowski A.Z., Friesen R.M., Martin G.E., Puig S.I., Nowak C.L., Wynne P.M., Siegelmann H.T., and Treistman S.N. Posttranscriptional regulation of BK channel splice variant stability by miR-9 underlies neuroadaptation to alcohol. Neuron 59 (2008) 274-287
30. Politz J.C., Zhang F., and Pederson T. MicroRNA-206 colocalizes with ribosome-rich regions in both the nucleolus and cytoplasm of rat myogenic cells. Proc. Natl. Acad. Sci. USA 103 (2006) 18957-18962
31. Rosenfeld N., Aharonov R., Meiri E., Rosenwald S., Spector Y., Zepeniuk M., Benjamin H., Shabes N., Tabak S., Levy A., et al. MicroRNAs accurately identify cancer tissue origin. Nat. Biotechnol. 26 (2008) 462-469
32. Rubin C.I., and Atweh G.F. The role of stathmin in the regulation of the cell cycle. J. Cell. Biochem. 93 (2004) 242-250
33. Shibata M., Kurokawa D., Nakao H., Ohmura T., and Aizawa S. MicroRNA-9 modulates Cajal-Retzius cell differentiation by suppressing Foxg1 expression in mouse medial pallium. J. Neurosci. 28 (2008) 10415-10421
34. Suh M.R., Lee Y., Kim J.Y., Kim S.K., Moon S.H., Lee J.Y., Cha K.Y., Chung H.M., Yoon H.S., Moon S.Y., et al. Human embryonic stem cells express a unique set of microRNAs. Dev. Biol. 270 (2004) 488-498
35. Tay Y., Zhang J., Thomson A.M., Lim B., and Rigoutsos I. MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 455 (2008) 1124-1128
36. Vasudevan S., Tong Y., and Steitz J.A. Switching from repression to activation: MicroRNAs can up-regulate translation. Science 318 (2007) 1931-1934
37. Wichterle H., Garcia-Verdugo J.M., Herrera D.G., Alvarez-Buylla A., and Alvarez-Buylla A. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat. Neurosci. 2 (1999) 461-466
38. Yamanaka S. Strategies and new developments in the generation of patient-specific pluripotent stem cells. Cell Stem Cell 1 (2007) 39-49
39. Yu J., and Thomson J.A. Pluripotent stem cell lines. Genes Dev. 22 (2008) 1987-1997
40. Zhang S.C., Wernig M., Duncan I.D., Brüstle O., and Thomson J.A. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 19 (2001) 1129-1133
41. Zhao Y., and Srivastava D. A developmental view of microRNA function. Trends Biochem. Sci. 32 (2007) 189-197
42. Zhao C., Deng W., and Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 132 (2008) 645-660
43. Zhao C., Sun G., Li S., and Shi Y. A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination. Nat. Struct. Mol. Biol. 16 (2009) 365-371
44. Zhu W., Fan Y., Frenzel T., Gasmi M., Bartus R.T., Young W.L., Yang G.Y., and Chen Y. Insulin growth factor-1 gene transfer enhances neurovascular remodeling and improves long-term stroke outcome in mice. Stroke 39 (2008) 1254-1261