3' UTR-Dependent, miR-92-Mediated Restriction of Tis21 Expression Maintains Asymmetric Neural Stem Cell Division to Ensure Proper Neocortex Size

Cell Reports

Volumn 7, Issue 2, 2014, Pages 398-411

  Fei, Ji Feng ^a,b   Haffner, Christiane ^a   Huttner, Wieland B ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 92; TIS21 PROTEIN; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; BTG2 PROTEIN, MOUSE; IMMEDIATE EARLY PROTEIN; MIRN92 MICRORNA, MOUSE; TUMOR SUPPRESSOR PROTEIN;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; APICAL PROGENITOR; ARTICLE; BASAL PROGENITOR; CELL DIVISION; CELL FRACTIONATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENE EXPRESSION; KNOCKOUT MOUSE; MICROCEPHALY; MOUSE; NEOCORTEX; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; ASYMMETRIC CELL DIVISION; C57BL MOUSE; CYTOLOGY; EMBRYOLOGY; GENETICS; METABOLISM; ORGAN SIZE; PATHOLOGY; PHYSIOLOGY;

3' UNTRANSLATED REGIONS; ANIMALS; ASYMMETRIC CELL DIVISION; DOWN-REGULATION; IMMEDIATE-EARLY PROTEINS; MICE; MICE, INBRED C57BL; MICROCEPHALY; MICRORNAS; NEOCORTEX; NEURAL STEM CELLS; NEUROGENESIS; ORGAN SIZE; TUMOR SUPPRESSOR PROTEINS;

EID: 84899657478     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.03.033     Document Type: Article

References (31)

1. Arai Y., Pulvers J.N., Haffner C., Schilling B., Nusslein I., Calegari F., Huttner W.B. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat Commun 2011, 2:154.
2. Attardo A., Calegari F., Haubensak W., Wilsch-Brauninger M., Huttner W.B. Live imaging at the onset of cortical neurogenesis reveals differential appearance of the neuronal phenotype in apical versus basal progenitor progeny. PLoS ONE 2008, 3:e2388.
3. Bian S., Hong J., Li Q., Schebelle L., Pollock A., Knauss J.L., Garg V., Sun T. MicroRNA cluster miR-17-92 regulates neural stem cell expansion and transition to intermediate progenitors in the developing mouse neocortex. Cell Rep 2013, 3:1398-1406.
4. Borrell V., Reillo I. Emerging roles of neural stem cells in cerebral cortex development and evolution. Dev. Neurobiol. 2012, 72:955-971.
5. Bradbury A., Possenti R., Shooter E.M., Tirone F. Molecular cloning of PC3, a putatively secreted protein whose mRNA is induced by nervegrowth factor and depolarization. Proc. Natl. Acad. Sci. USA 1991, 88:3353-3357.
6. Canzoniere D., Farioli-Vecchioli S., Conti F., Ciotti M.T., Tata A.M., Augusti-Tocco G., Mattei E., Lakshmana M.K., Krizhanovsky V., Reeves S.A., et al. Dual control of neurogenesis by PC3 through cell cycle inhibition and induction of Math1. J.Neurosci. 2004, 24:3355-3369.
7. Chen C.Y., Shyu A.B. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 1995, 20:465-470.
8. De Pietri Tonelli D., Pulvers J.N., Haffner C., Murchison E.P., Hannon G.J., Huttner W.B. 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 2008, 135:3911-3921.
9. de Pontual L., Yao E., Callier P., Faivre L., Drouin V., Cariou S., Van Haeringen A., Geneviève D., Goldenberg A., Oufadem M., et al. Germline deletion of the miR-17~92 cluster causes skeletal and growth defects in humans. Nat. Genet. 2011, 43:1026-1030.
10. Englund C., Fink A., Lau C., Pham D., Daza R.A., Bulfone A., Kowalczyk T., Hevner R.F. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J.Neurosci. 2005, 25:247-251.
11. Fietz S.A., Huttner W.B. Cortical progenitor expansion, self-renewal and neurogenesis-a polarized perspective. Curr. Opin. Neurobiol. 2011, 21:23-35.
12. Fletcher B.S., Lim R.W., Varnum B.C., Kujubu D.A., Koski R.A., Herschman H.R. Structure and expression of TIS21, a primary response gene induced by growth factors and tumor promoters. J.Biol. Chem. 1991, 266:14511-14518.
13. Gotz M., Huttner W.B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 2005, 6:777-788.
14. Haubensak W., Attardo A., Denk W., Huttner W.B. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc. Natl. Acad. Sci. USA 2004, 101:3196-3201.
15. Huntzinger E., Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat. Rev. Genet. 2011, 12:99-110.
16. Iacopetti P., Michelini M., Stuckmann I., Oback B., Aaku-Saraste E., Huttner W.B. Expression of the antiproliferative gene TIS21 at the onset of neurogenesis identifies single neuroepithelial cells that switch from proliferative to neuron-generating division. Proc. Natl. Acad. Sci. USA 1999, 96:4639-4644.
17. Jalava S.E., Urbanucci A., Latonen L., Waltering K.K., Sahu B., Janne O.A., Seppala J., Lahdesmaki H., Tammela T.L., Visakorpi T. Androgen-regulated miR-32 targets BTG2 and is overexpressed in castration-resistant prostate cancer. Oncogene 2012, 31:4460-4471.
18. Kowalczyk T., Pontious A., Englund C., Daza R.A., Bedogni F., Hodge R., Attardo A., Bell C., Huttner W.B., Hevner R.F. Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb. Cortex 2009, 19:2439-2450.
19. Kriegstein A., Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 2009, 32:149-184.
20. Lai E.C., Posakony J.W. The Bearded box, a novel 3' UTR sequence motif, mediates negative post-transcriptional regulation of Bearded and Enhancer of split Complex gene expression. Development 1997, 124:4847-4856.
21. Lui J.H., Hansen D.V., Kriegstein A.R. Development and evolution of the human neocortex. Cell 2011, 146:18-36.
22. Malatesta P., Gotz M., Barsacchi G., Price J., Zoncu R., Cremisi F. PC3 overexpression affects the pattern of cell division of rat cortical precursors. Mech. Dev. 2000, 90:17-28.
23. Matsuda S., Rouault J., Magaud J., Berthet C. In search of a function for the TIS21/PC3/BTG1/TOB family. FEBS Lett. 2001, 497:67-72.
24. Miska E.A., Alvarez-Saavedra E., Townsend M., Yoshii A., Sestan N., Rakic P., Constantine-Paton M., Horvitz H.R. Microarray analysis ofmicroRNA expression in the developing mammalian brain. Genome Biol. 2004, 5:R68.
25. Molyneaux B.J., Arlotta P., Menezes J.R., Macklis J.D. Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 2007, 8:427-437.
26. Murchison E.P., Partridge J.F., Tam O.H., Cheloufi S., Hannon G.J. Characterization of Dicer-deficient murine embryonic stem cells. Proc. Natl. Acad. Sci. USA 2005, 102:12135-12140.
27. Rakic P. Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 2009, 10:724-735.
28. Rouault J.P., Falette N., Guéhenneux F., Guillot C., Rimokh R., Wang Q., Berthet C., Moyret-Lalle C., Savatier P., Pain B., et al. Identification of BTG2, an antiproliferative p53-dependent component of the DNA damage cellular response pathway. Nat. Genet. 1996, 14:482-486.
29. Tirone F. The gene PC3(TIS21/BTG2), prototype member of the PC3/BTG/TOB family: regulator in control of cell growth, differentiation, and DNA repair?. J.Cell. Physiol. 2001, 187:155-165.
30. Yang C.H., Yue J., Pfeffer S.R., Handorf C.R., Pfeffer L.M. MicroRNA miR-21 regulates the metastatic behavior of B16 melanoma cells. J.Biol. Chem. 2011, 286:39172-39178.
31. Yao M.J., Chen G., Zhao P.P., Lu M.H., Jian J., Liu M.F., Yuan X.B. Transcriptome analysis of microRNAs in developing cerebral cortex of rat. BMC Genomics 2012, 13:232.