MiR-137 and MiR-122, Two Outer Subventricular Zone Non-coding RNAs, Regulate Basal Progenitor Expansion and Neuronal Differentiation

Overview

Journal Cell Rep

Publisher Cell Press

Specialties Biology
Cell Biology
Molecular Biology

Date 2022 Feb 16

PMID 35172154

Authors

Ugo Tomasello

Esther Klingler

Mathieu Niquille

Nandkishor Mule

Antonio J Santinha

Laura de Vevey

Julien Prados

Randall J Platt

Victor Borrell

Denis Jabaudon

Alexandre Dayer

Affiliations

Soon will be listed here.

Abstract

Cortical expansion in primate brains relies on enlargement of germinal zones during a prolonged developmental period. Although most mammals have two cortical germinal zones, the ventricular zone (VZ) and subventricular zone (SVZ), gyrencephalic species display an additional germinal zone, the outer subventricular zone (oSVZ), which increases the number and diversity of neurons generated during corticogenesis. How the oSVZ emerged during evolution is poorly understood, but recent studies suggest a role for non-coding RNAs, which allow tight genetic program regulation during development. Here, using in vivo functional genetics, single-cell RNA sequencing, live imaging, and electrophysiology to assess progenitor and neuronal properties in mice, we identify two oSVZ-expressed microRNAs (miRNAs), miR-137 and miR-122, which regulate key cellular features of cortical expansion. miR-137 promotes basal progenitor self-replication and superficial layer neuron fate, whereas miR-122 decreases the pace of neuronal differentiation. These findings support a cell-type-specific role of miRNA-mediated gene expression in cortical expansion.

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References

Haubensak W, Attardo A, Denk W, Huttner W . Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci U S A. 2004; 101(9):3196-201. PMC: 365766. DOI: 10.1073/pnas.0308600100. View

Diaz J, Siththanandan V, Lu V, Gonzalez-Nava N, Pasquina L, MacDonald J . An evolutionarily acquired microRNA shapes development of mammalian cortical projections. Proc Natl Acad Sci U S A. 2020; 117(46):29113-29122. PMC: 7682328. DOI: 10.1073/pnas.2006700117. View

Martinez-Martinez M, de Juan Romero C, Fernandez V, Cardenas A, Gotz M, Borrell V . A restricted period for formation of outer subventricular zone defined by Cdh1 and Trnp1 levels. Nat Commun. 2016; 7:11812. PMC: 4897765. DOI: 10.1038/ncomms11812. View

Moreau M, Bruse S, Jornsten R, Liu Y, Brzustowicz L . Chronological changes in microRNA expression in the developing human brain. PLoS One. 2013; 8(4):e60480. PMC: 3628885. DOI: 10.1371/journal.pone.0060480. View

Picken Bahrey H, Moody W . Early development of voltage-gated ion currents and firing properties in neurons of the mouse cerebral cortex. J Neurophysiol. 2003; 89(4):1761-73. DOI: 10.1152/jn.00972.2002. View

Fietz S, Kelava I, Vogt J, Wilsch-Brauninger M, Stenzel D, Fish J . OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat Neurosci. 2010; 13(6):690-9. DOI: 10.1038/nn.2553. View

Kowalczyk T, Pontious A, Englund C, Daza R, Bedogni F, Hodge R . Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb Cortex. 2009; 19(10):2439-50. PMC: 2742596. DOI: 10.1093/cercor/bhn260. View

Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, Ogawa M . Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development. 2004; 131(13):3133-45. DOI: 10.1242/dev.01173. View

Noctor S, Martinez-Cerdeno V, Ivic L, Kriegstein A . Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci. 2004; 7(2):136-44. DOI: 10.1038/nn1172. View

10.

Fietz S, Lachmann R, Brandl H, Kircher M, Samusik N, Schroder R . Transcriptomes of germinal zones of human and mouse fetal neocortex suggest a role of extracellular matrix in progenitor self-renewal. Proc Natl Acad Sci U S A. 2012; 109(29):11836-41. PMC: 3406833. DOI: 10.1073/pnas.1209647109. View

11.

Gould S . Ontogeny and phylogeny--revisited and reunited. Bioessays. 1992; 14(4):275-9. DOI: 10.1002/bies.950140413. View

12.

Rakic P . Evolution of the neocortex: a perspective from developmental biology. Nat Rev Neurosci. 2009; 10(10):724-35. PMC: 2913577. DOI: 10.1038/nrn2719. View

13.

Oellig C, Seliger B . Gene transfer into brain tumor cell lines: reporter gene expression using various cellular and viral promoters. J Neurosci Res. 1990; 26(3):390-6. DOI: 10.1002/jnr.490260317. View

14.

De Pietri Tonelli D, Pulvers J, Haffner C, Murchison E, Hannon G, Huttner W . 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(23):3911-21. PMC: 2798592. DOI: 10.1242/dev.025080. View

15.

Davis T, Cuellar T, Koch S, Barker A, Harfe B, McManus M . Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J Neurosci. 2008; 28(17):4322-30. PMC: 3844796. DOI: 10.1523/JNEUROSCI.4815-07.2008. View

16.

Noctor S, Flint A, Weissman T, Dammerman R, Kriegstein A . Neurons derived from radial glial cells establish radial units in neocortex. Nature. 2001; 409(6821):714-20. DOI: 10.1038/35055553. View

17.

Caviness Jr V, Takahashi T, Nowakowski R . Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. Trends Neurosci. 1995; 18(9):379-83. DOI: 10.1016/0166-2236(95)93933-o. View

18.

Stark K, Xu B, Bagchi A, Lai W, Liu H, Hsu R . Altered brain microRNA biogenesis contributes to phenotypic deficits in a 22q11-deletion mouse model. Nat Genet. 2008; 40(6):751-60. DOI: 10.1038/ng.138. View

19.

Nowakowski T, Rani N, Golkaram M, Zhou H, Alvarado B, Huch K . Regulation of cell-type-specific transcriptomes by microRNA networks during human brain development. Nat Neurosci. 2018; 21(12):1784-1792. PMC: 6312854. DOI: 10.1038/s41593-018-0265-3. View

20.

Petanjek Z, Judas M, Simic G, Rasin M, Uylings H, Rakic P . Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci U S A. 2011; 108(32):13281-6. PMC: 3156171. DOI: 10.1073/pnas.1105108108. View