Cited by 39

miR-200 family controls late steps of postnatal forebrain neurogenesis via Zeb2 inhibition

Beclin, Christophe, Follert, Philipp, Stappers, Elke, Barral, Serena, Coré, Nathalie, de Chevigny, Antoine, Magnone, Virginie, Lebrigand, Kévin +6 more·2016·Scientific Reports

Abstract

During neurogenesis, generation, migration and integration of the correct numbers of each neuron sub-type depends on complex molecular interactions in space and time. MicroRNAs represent a key control level allowing the flexibility and stability needed for this process. Insight into the role of this regulatory pathway in the brain is still limited. We performed a sequential experimental approach using postnatal olfactory bulb neurogenesis in mice, starting from global expression analyses to the investigation of functional interactions between defined microRNAs and their targets. Deep sequencing of small RNAs extracted from defined compartments of the postnatal neurogenic system demonstrated that the miR-200 family is specifically induced during late neuronal differentiation stages. Using in vivo strategies we interfered with the entire miR-200 family in loss- and gain-of-function settings, showing a role of miR-200 in neuronal maturation. This function is mediated by targeting the transcription factor Zeb2. Interestingly, so far functional interaction between miR-200 and Zeb2 has been exclusively reported in cancer or cultured stem cells. Our data demonstrate that this regulatory interaction is also active during normal neurogenesis.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/srep35729

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 56

  1. Lim D. A. & Alvarez-Buylla A. Adult neural stem cells stake their ground. Trends Neurosci 37, 563– 571 (2014). 25223700 PMC4203324
  2. Follert P., Cremer H. & Beclin C. MicroRNAs in brain development and function: a matter of flexibility and stability. Front Mol Neurosci 7, 5 (2014). 24570654 PMC3916726
  3. Kawase-Koga Y., Otaegi G. & Sun T. Different timings of Dicer deletion affect neurogenesis and gliogenesis in the developing mouse central nervous system. Dev Dyn 238, 2800– 2812 (2009). 19806666 PMC2831750
  4. Davis T. H.. Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J Neurosci 28, 4322– 4330 (2008). 18434510 PMC3844796
  5. Cuellar T. L.. Dicer loss in striatal neurons produces behavioral and neuroanatomical phenotypes in the absence of neurodegeneration. Proc Natl Acad Sci USA 105, 5614– 5619 (2008). 18385371 PMC2291142
  6. De Pietri Tonelli D.. 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 (2008). 18997113 PMC2798592
  7. Schaefer A.. Cerebellar neurodegeneration in the absence of microRNAs. J Exp Med 204, 1553– 1558 (2007). 17606634 PMC2118654
  8. Zhao C., Sun G., Li S. & Shi Y. A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination. Nat Struct Mol Biol 16, 365– 371 (2009). 19330006 PMC2667220
  9. Conaco C., Otto S., Han J. J. & Mandel G. Reciprocal actions of REST and a microRNA promote neuronal identity. Proc Natl Acad Sci USA 103, 2422– 2427 (2006). 16461918 PMC1413753
  10. Yoo A. S., Staahl B. T., Chen L. & Crabtree G. R. MicroRNA-mediated switching of chromatin-remodelling complexes in neural development. Nature 460, 642– 646 (2009). 19561591 PMC2921580
  11. Cheng L. C., Pastrana E., Tavazoie M. & Doetsch F. miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat Neurosci 12, 399– 408 (2009). 19287386 PMC2766245
  12. de Chevigny A.. miR-7a regulation of Pax6 controls spatial origin of forebrain dopaminergic neurons. Nat Neurosci 15, 1120– 1126 (2012). 22729175
  13. Chen J. A.. Mir-17-3p controls spinal neural progenitor patterning by regulating Olig2/Irx3 cross-repressive loop. Neuron 69, 721– 735 (2011). 21338882 PMC3062262
  14. Schratt G. M.. A brain-specific microRNA regulates dendritic spine development. Nature 439, 283– 289 (2006). 16421561
  15. Fiore R.. Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. EMBO J 28, 697– 710 (2009). 19197241 PMC2647767
  16. Alvarez-Buylla A. & Garcia-Verdugo J. M. Neurogenesis in adult subventricular zone. J Neurosci 22, 629– 634 (2002). 11826091 PMC6758521
  17. Lledo P. M., Merkle F. T. & Alvarez-Buylla A. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 31, 392– 400 (2008). 18603310 PMC4059175
  18. Boutin C., Diestel S., Desoeuvre A., Tiveron M. C. & Cremer H. Efficient in vivo electroporation of the postnatal rodent forebrain. PLoS One 3, e1883 (2008). 18382666 PMC2270900
  19. Sun A. X., Crabtree G. R. & Yoo A. S. MicroRNAs: regulators of neuronal fate. Curr Opin Cell Biol 25, 215– 221 (2013). 23374323 PMC3836262
  20. Song R.. miR-34/449 miRNAs are required for motile ciliogenesis by repressing cp110. Nature 510, 115– 120 (2014). 24899310 PMC4119886
  21. Wu J.. Two miRNA clusters, miR-34b/c and miR-449, are essential for normal brain development, motile ciliogenesis, and spermatogenesis. Proc Natl Acad Sci USA 111, E2851– E2857 (2014). 24982181 PMC4104921
  22. Marcet B.. Control of vertebrate multiciliogenesis by miR-449 through direct repression of the Delta/Notch pathway. Nat Cell Biol 13, 693– 699 (2011). 21602795
  23. Spassky N.. Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci 25, 10– 18 (2005). 15634762 PMC6725217
  24. Pandey A.. Critical role of the miR-200 family in regulating differentiation and proliferation of neurons. J Neurochem 133, 640– 652 (2015). 25753155
  25. Choi P. S.. Members of the miRNA-200 family regulate olfactory neurogenesis. Neuron 57, 41– 55 (2008). 18184563 PMC2204047
  26. Acuna-Goycolea C., Tamamaki N., Yanagawa Y., Obata K. & van den Pol A. N. Mechanisms of neuropeptide Y, peptide YY, and pancreatic polypeptide inhibition of identified green fluorescent protein-expressing GABA neurons in the hypothalamic neuroendocrine arcuate nucleus. J Neurosci 25, 7406– 7419 (2005). 16093392 PMC6725307
  27. Shepherd G. M. The synaptic organization of the brain (Oxford University Press, Oxford, 2004).
  28. Bracken C. P.. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res 68, 7846– 7854 (2008). 18829540
  29. Brabletz S. & Brabletz T. The ZEB/miR-200 feedback loop–a motor of cellular plasticity in development and cancer? EMBO Rep 11, 670– 677 (2010). 20706219 PMC2933868
  30. Price J. L. & Powell T. P. The mitral and short axon cells of the olfactory bulb. J Cell Sci 7, 631– 651 (1970). 5492279
  31. Kosaka K.. Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb. Neurosci Res 23, 73– 88 (1995). 7501303
  32. Merkle F. T., Mirzadeh Z. & Alvarez-Buylla A. Mosaic organization of neural stem cells in the adult brain. Science 317, 381– 384 (2007). 17615304
  33. Merkle F. T.. Adult neural stem cells in distinct microdomains generate previously unknown interneuron types. Nat Neurosci 17, 207– 214 (2014). 24362763 PMC4100623
  34. Lopez-Juarez A.. Gsx2 controls region-specific activation of neural stem cells and injury-induced neurogenesis in the adult subventricular zone. Genes Dev 27, 1272– 1287 (2013). 23723414 PMC3690400
  35. van den Berghe V.. Directed migration of cortical interneurons depends on the cell-autonomous action of Sip1. Neuron 77, 70– 82 (2013). 23312517
  36. Shao N. Y.. Comprehensive survey of human brain microRNA by deep sequencing. BMC Genomics 11, 409 (2010). 20591156 PMC2996937
  37. Yao M. J.. Transcriptome analysis of microRNAs in developing cerebral cortex of rat. BMC Genomics 13, 232 (2012). 22691069 PMC3441217
  38. Shibata M., Nakao H., Kiyonari H., Abe T. & Aizawa S. MicroRNA-9 regulates neurogenesis in mouse telencephalon by targeting multiple transcription factors. J Neurosci 31, 3407– 3422 (2011). 21368052 PMC6623912
  39. Barca-Mayo O. & Tonelli De Pietri, D. Convergent microRNA actions coordinate neocortical development. Cell Mol Life Sci 71, 2975– 2995 (2014). 24519472 PMC4111863
  40. de Chevigny A., Cremer H. & Core N. [Micro-RNA miR-7a controls the production of dopaminergic neurons in the mouse forebrain]. Med Sci (Paris) 29, 153– 155 (2013). 23452602
  41. Korpal M., Lee E. S., Hu G. & Kang Y. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 283, 14910– 14914 (2008). 18411277 PMC3258899
  42. Park S. M., Gaur A. B., Lengyel E. & Peter M. E. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 22, 894– 907 (2008). 18381893 PMC2279201
  43. Gregory P. A.. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10, 593– 601 (2008). 18376396
  44. Burk U.. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 9, 582– 589 (2008). 18483486 PMC2396950
  45. Seuntjens E.. Sip1 regulates sequential fate decisions by feedback signaling from postmitotic neurons to progenitors. Nat Neurosci 12, 1373– 1380 (2009). 19838179
  46. Belvindrah R., Nissant A. & Lledo P. M. Abnormal neuronal migration changes the fate of developing neurons in the postnatal olfactory bulb. J Neurosci 31, 7551– 7562 (2011). 21593340 PMC6622602
  47. Comijn J.. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell 7, 1267– 1278 (2001). 11430829
  48. Busskamp V.. miRNAs 182 and 183 are necessary to maintain adult cone photoreceptor outer segments and visual function. Neuron 83, 586– 600 (2014). 25002228
  49. Lumayag S.. Inactivation of the microRNA-183/96/182 cluster results in syndromic retinal degeneration. Proc Natl Acad Sci USA 110, E507– E516 (2013). 23341629 PMC3568372
  50. Kundu S. T.. The miR-200 family and the miR-183~96~182 cluster target Foxf2 to inhibit invasion and metastasis in lung cancers. Oncogene 35, 173– 186 (2016). 25798833 PMC4580489
  51. Higashi Y.. Generation of the floxed allele of the SIP1 (Smad-interacting protein 1) gene for Cre-mediated conditional knockout in the mouse. Genesis 32, 82– 84 (2002). 11857784
  52. Sousa V. H., Miyoshi G., Hjerling-Leffler J., Karayannis T. & Fishell G. Characterization of Nkx6-2-derived neocortical interneuron lineages. Cereb Cortex 19 Suppl 1, i1– 10 (2009). 19363146 PMC2693535
  53. Morin X., Jaouen F. & Durbec P. Control of planar divisions by the G-protein regulator LGN maintains progenitors in the chick neuroepithelium. Nat Neurosci 10, 1440– 1448 (2007). 17934458
  54. Ebert M. S., Neilson J. R. & Sharp P. A. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 4, 721– 726 (2007). 17694064 PMC3857099
  55. Tamamaki N.. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467, 60– 79 (2003). 14574680
  56. Saeed A. I.. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374– 378 (2003). 12613259

Cited by

Sorted by citations

Authors
Beclin, C., Follert, P., Stappers, E., Barral, S., Coré, N., de Chevigny, A., Magnone, V., Lebrigand, K., Bissels, U., Huylebroeck, D., Bosio, A., Barbry, P., Seuntjens, E., & Cremer, H.
Venue
Scientific Reports
Published
2016-10-21
Volume
6
Issue
1
ISSN
2045-2322
Cited by
39
References
4
Language
en

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review