A unilateral negative feedback loop between miR-200 microRNAs and Sox2/E2F3 controls neural progenitor cell-cycle exit and differentiation

Journal of Neuroscience

Volumn 32, Issue 38, 2012, Pages 13292-13308

  Peng, Changgeng ^a   Li, Na ^b   Ng, Yen Kar ^a   Zhang, Jingzhong ^a   Meier, Florian ^a   Theis, Fabian J ^c   Merkenschlager, Matthias ^d   Chen, Wei ^b   Wurst, Wolfgang ^a,e,f   Prakash, Nilima ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^f MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA 200; TRANSCRIPTION FACTOR E2F3; TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL CYCLE REGULATION; CONTROLLED STUDY; EMBRYO; FEMALE; GENE SILENCING; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MESENCEPHALON; MOUSE; NEGATIVE FEEDBACK; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHOMBENCEPHALON; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

AGE FACTORS; ANIMALS; CELL COUNT; CELL CYCLE; CELL DEATH; CELL DIFFERENTIATION; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; DEAD-BOX RNA HELICASES; DEOXYURIDINE; E2F3 TRANSCRIPTION FACTOR; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; HUMANS; MALE; MESENCEPHALON; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICRORNAS; MODELS, BIOLOGICAL; MUTATION; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; RHOMBENCEPHALON; RIBONUCLEASE III; SEROTONIN; SIGNAL TRANSDUCTION; SOXB1 TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR BRN-3A; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 84866414208     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2124-12.2012     Document Type: Article

References (65)

1. Adams MR, Sears R, Nuckolls F, Leone G, Nevins JR (2000) Complex transcriptional regulatory mechanisms control expression of the E2F3 locus. Mol Cell Biol 20:3633-3639. CrossRef Medline
2. Ameres SL, Horwich MD, Hung JH, Xu J, Ghildiyal M, Weng Z, Zamore PD (2010) Target RNA-directed trimming and tailing of small silencing RNAs. Science 328:1534-1539. CrossRef Medline
3. Andersson T, Rahman S, Sansom SN, Alsiö JM, Kaneda M, Smith J, O'Carroll D, Tarakhovsky A, Livesey FJ (2010) Reversible block of mouse neural stem cell differentiation in the absence of dicer and microRNAs. PLoS One 5:e13453. CrossRef Medline
4. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R (2003) Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17:126-140. CrossRef Medline
5. Bibel M, Richter J, Lacroix E, Barde YA (2007) Generation of a defined and uniform population of CNS progenitors and neurons from mouse embryonic stem cells. Nat Protoc 2:1034-1043. CrossRef Medline
6. Brabletz S, Brabletz T (2010) The ZEB/miR-200 feedback loop-a motor of cellular plasticity in development and cancer? EMBO Rep 11:670-677. CrossRef Medline
7. Chi CL, Martinez S, Wurst W, Martin GR (2003) The isthmic organizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum. Development 130:2633-2644. CrossRef Medline
8. Choi PS, Zakhary L, Choi WY, Caron S, Alvarez-Saavedra E, Miska EA, McManus M, Harfe B, Giraldez AJ, Horvitz HR, Schier AF, Dulac C (2008) Members of the miRNA-200 family regulate olfactory neurogenesis. Neuron 57:41-55. CrossRef Medline
9. Chong JL, Wenzel PL, Sáenz-Robles MT, Nair V, Ferrey A, Hagan JP, Gomez YM, Sharma N, Chen HZ, Ouseph M, Wang SH, Trikha P, Culp B, Mezache L, Winton DJ, Sansom OJ, Chen D, Bremner R, Cantalupo PG, Robinson ML, Pipas JM, Leone G (2009) E2f1-3 switch from activators in progenitor cells to repressors in differentiating cells. Nature 462:930-934. CrossRef Medline
10. Cobb BS, Nesterova TB, Thompson E, Hertweck A, O'Connor E, Godwin J, Wilson CB, Brockdorff N, Fisher AG, Smale ST, Merkenschlager M (2005) T cell lineage choice and differentiation in the absence of the RNase III enzyme Dicer. J Exp Med 201:1367-1373. CrossRef Medline
11. Coolen M, Bally-Cuif L (2009) MicroRNAs in brain development and physiology. Curr Opin Neurobiol 19:461-470. CrossRef Medline
12. de Pietri Tonelli D, Pulvers JN, Haffner C, Murchison EP, Hannon GJ, Huttner WB (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. CrossRef Medline
13. DeGregori J (2002) The genetics of the E2F family of transcription factors: shared functions and unique roles. Biochim Biophys Acta 1602:131-150. Medline
14. Ebert MS, Neilson JR, Sharp PA (2007) MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 4:721-726. CrossRef Medline
15. Fischer T, Guimera J, Wurst W, Prakash N (2007) Distinct but redundant expression of the Frizzled Wnt receptor genes at signaling centers of the developing mouse brain. Neuroscience 147:693-711. CrossRef Medline
16. Fischer T, Faus-Kessler T, Welzl G, Simeone A, Wurst W, Prakash N (2011) Fgf15-mediated control of neurogenic and proneural gene expression regulates dorsal midbrain neurogenesis. Dev Biol 350:496-510. CrossRef Medline
17. Gill JG, Langer EM, Lindsley RC, Cai M, Murphy TL, Kyba M, Murphy KM (2011) Snail and the microRNA-200 family act in opposition to regulate epithelial-to-mesenchymal transition and germ layer fate restriction in differentiating ESCs. Stem Cells 29:764-776. CrossRef Medline
18. Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39:749-765. CrossRef Medline
19. Guillemot F, Zimmer C (2011) From cradle to grave: the multiple roles of fibroblast growth factors in neural development. Neuron 71:574-588. CrossRef Medline
20. Guo C, Qiu HY, Huang Y, Chen H, Yang RQ, Chen SD, Johnson RL, Chen ZF, Ding YQ (2007) Lmx1b is essential for Fgf8 and Wnt1 expression in the isthmic organizer during tectum and cerebellum development in mice. Development 134:317-325. CrossRef Medline
21. Harfe BD, McManus MT, Mansfield JH, Hornstein E, Tabin CJ (2005) The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc Natl Acad Sci U S A 102:10898-10903. CrossRef Medline
22. Heo I, Joo C, Kim YK, Ha M, Yoon MJ, Cho J, Yeom KH, Han J, Kim VN (2009) TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 138:696-708. CrossRef Medline
23. Hirata H, Tomita K, Bessho Y, Kageyama R (2001) Hes1 and Hes3 regulate maintenance of the isthmic organizer and development of the mid/hindbrain. EMBO J 20:4454-4466. CrossRef Medline
24. Huang T, Liu Y, Huang M, Zhao X, Cheng L (2010) Wnt1-cre-mediated conditional loss of Dicer results in malformation of the midbrain and cerebellum and failure of neural crest and dopaminergic differentiation in mice. J Mol Cell Biol 2:152-163. CrossRef Medline
25. Humbert PO, Verona R, Trimarchi JM, Rogers C, Dandapani S, Lees JA (2000) E2f3 is critical for normal cellular proliferation. Genes Dev 14:690-703. Medline
26. Huntzinger E, Izaurralde E (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12:99-110. CrossRef Medline
27. Ivey KN, Srivastava D (2010) MicroRNAs as regulators of differentiation and cell fate decisions. Cell Stem Cell 7:36-41. CrossRef Medline
28. Kawase-Koga Y, Low R, Otaegi G, Pollock A, Deng H, Eisenhaber F, Maurer-Stroh S, Sun T (2010) RNAase-III enzyme Dicer maintains signaling pathways for differentiation and survival in mouse cortical neural stem cells. J Cell Sci 123:586-594. CrossRef Medline
29. Kimmel RA, Turnbull DH, Blanquet V, Wurst W, Loomis CA, Joyner AL (2000) Two lineage boundaries coordinate vertebrate apical ectodermal ridge formation. Genes Dev 14:1377-1389. Medline
30. Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39:D152-D157. CrossRef Medline
31. Krichevsky AM, Sonntag KC, Isacson O, Kosik KS (2006) Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 24:857-864. CrossRef Medline
32. Krol J, Loedige I, Filipowicz W (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11:597-610. CrossRef Medline
33. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T (2002) Identification of tissue-specific microRNAs from mouse. Curr Biol 12:735-739. CrossRef Medline
34. Lau P, Verrier JD, Nielsen JA, Johnson KR, Notterpek L, Hudson LD (2008) Identification of dynamically regulated microRNA and mRNA networks in developing oligodendrocytes. J Neurosci 28:11720-11730. CrossRef Medline
35. Leone G, DeGregori J, Yan Z, Jakoi L, Ishida S, Williams RS, Nevins JR (1998) E2F3 activity is regulated during the cell cycle and is required for the induction of S phase. Genes Dev 12:2120-2130. CrossRef Medline
36. Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24:713-714. CrossRef Medline
37. Lin CH, Jackson AL, Guo J, Linsley PS, Eisenman RN (2009) Myc-regulated microRNAs attenuate embryonic stem cell differentiation. EMBO J 28:3157-3170. CrossRef Medline
38. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408. CrossRef Medline
39. Mallanna SK, Rizzino A (2010) Emerging roles of microRNAs in the control of embryonic stem cells and the generation of induced pluripotent stem cells. Dev Biol 344:16-25. CrossRef Medline
40. Martinez NJ, Gregory RI (2010) MicroRNA gene regulatory pathways in the establishment and maintenance of ESC identity. Cell Stem Cell 7:31-35. CrossRef Medline
41. Matsuda T, Cepko CL (2004) Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc Natl Acad Sci U S A 101:16-22. CrossRef Medline
42. McMahon AP, Bradley A (1990) The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 62:1073-1085. CrossRef Medline
43. Mukherji S, Ebert MS, Zheng GX, Tsang JS, Sharp PA, van Oudenaarden A (2011) MicroRNAs can generate thresholds in target gene expression. Nat Genet 43:854-859. CrossRef Medline
44. Muller H, Bracken AP, Vernell R, Moroni MC, Christians F, Grassilli E, Prosperini E, Vigo E, Oliner JD, Helin K (2001) E2Fs regulate the expression of genes involved in differentiation, development, proliferation, and apoptosis. Genes Dev 15:267-285. CrossRef Medline
45. Nakamura T, Colbert MC, Robbins J (2006) Neural crest cells retain multipotential characteristics in the developing valves and label the cardiac conduction system. Circ Res 98:1547-1554. CrossRef Medline
46. Pauli A, Rinn JL, Schier AF (2011) Non-coding RNAs as regulators of embryogenesis. Nat Rev Genet 12:136-149. CrossRef Medline
47. Peng C, Fan S, Li X, Fan X, Ming M, Sun Z, Le W (2007) Overexpression of Pitx3 upregulates expression of BDNF and GDNF in SH-SY5Y cells and primary ventral mesencephalic cultures. FEBS Lett 581:1357-1361. CrossRef Medline
48. Peng C, Aron L, Klein R, Li M, Wurst W, Prakash N, Le W (2011) Pitx3 is a critical mediator of GDNF-induced BDNF expression in nigrostriatal dopaminergic neurons. J Neurosci 31:12802-12815. CrossRef Medline
49. Peter ME (2009) Let-7 and miR-200 microRNAs: guardians against pluripotency and cancer progression. Cell Cycle 8:843-852. CrossRef Medline
50. Pettitt SJ, Liang Q, Rairdan XY, Moran JL, Prosser HM, Beier DR, Lloyd KC, Bradley A, Skarnes WC (2009) Agouti C57BL/6N embryonic stem cells for mouse genetic resources. Nat Methods 6:493-495. CrossRef Medline
51. Pevny LH, Nicolis SK (2010) Sox2 roles in neural stem cells. Int J Biochem Cell Biol 42:421-424. CrossRef Medline
52. Prakash N, Puelles E, Freude K, Trumbach D, Omodei D, Di Salvio M, Sussel L, Ericson J, Sander M, Simeone A, Wurst W (2009) Nkx6-1 controls the identity and fate of red nucleus and oculomotor neurons in the mouse midbrain. Development 136:2545-2555. CrossRef Medline
53. Puelles E, Annino A, Tuorto F, Usiello A, Acampora D, Czerny T, Brodski C, Ang SL, Wurst W, Simeone A (2004) Otx2 regulates the extent, identity and fate of neuronal progenitor domains in the ventral midbrain. Development 131:2037-2048. CrossRef Medline
54. Rubinson DA, Dillon CP, Kwiatkowski AV, Sievers C, Yang L, Kopinja J, Rooney DL, Zhang M, Ihrig MM, McManus MT, Gertler FB, Scott ML, Van Parijs L (2003) A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat Genet 33:401-406. CrossRef Medline
55. Schwarz M, Alvarez-Bolado G, Urbánek P, Busslinger M, Gruss P (1997) Conserved biological function between Pax-2 and Pax-5 in midbrain and cerebellum development: evidence from targeted mutations. Proc Natl Acad Sci U S A 94:14518-14523. CrossRef Medline
56. Silahtaroglu AN, Nolting D, Dyrskjøt L, Berezikov E, Møller M, Tommerup N, Kauppinen S (2007) Detection of microRNAs in frozen tissue sections by fluorescence in situ hybridization using locked nucleic acid probes and tyramide signal amplification. Nat Protoc 2:2520-2528. CrossRef Medline
57. Simon HH, Saueressig H, Wurst W, Goulding MD, O'Leary DD (2001) Fate of midbrain dopaminergic neurons controlled by the engrailed genes. J Neurosci 21:3126-3134. Medline
58. Tomioka M, Nishimoto M, Miyagi S, Katayanagi T, Fukui N, Niwa H, Muramatsu M, Okuda A (2002) Identification of Sox-2 regulatory region which is under the control of Oct-3/4-Sox-2 complex. Nucleic Acids Res 30:3202-3213. CrossRef Medline
59. Uhlmann S, Zhang JD, Schwäger A, Mannsperger H, Riazalhosseini Y, Burmester S, Ward A, Korf U, Wiemann S, Sahin O (2010) miR-200bc/429 cluster targets PLCgamma1 and differentially regulates proliferation and EGF-driven invasion than miR-200a/141 in breast cancer. Oncogene 29:4297-4306. CrossRef Medline
60. Wang Y, Blelloch R (2009) Cell cycle regulation by MicroRNAs in embryonic stem cells. Cancer Res 69:4093-4096. CrossRef Medline
61. Wang Y, Baskerville S, Shenoy A, Babiarz JE, Baehner L, Blelloch R (2008) Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation. Nat Genet 40:1478-1483. CrossRef Medline
62. Wittmann DM, Blöchl F, Trumbach D, Wurst W, Prakash N, Theis FJ (2009) Spatial analysis of expression patterns predicts genetic interactions at the mid-hindbrain boundary. PLoS Comput Biol 5:e1000569. CrossRef Medline
63. Wurst W, Bally-Cuif L (2001) Neural plate patterning: upstream and downstream of the isthmic organizer. Nat Rev Neurosci 2:99-108. CrossRef Medline
64. Wurst W, Auerbach AB, Joyner AL (1994) Multiple developmental defects in Engrailed-1 mutant mice: an early mid-hindbrain deletion and patterning defects in forelimbs and sternum. Development 120:2065-2075. Medline
65. Zervas M, Blaess S, Joyner AL (2005) Classical embryological studies and modern genetic analysis of midbrain and cerebellum development. Curr Top Dev Biol 69:101-138. CrossRef Medline