XB-ART-50287
Dev Biol
December 15, 2015;
408
(2):
269-91.
An in vivo screen to identify candidate neurogenic genes in the developing Xenopus visual system.
Bestman JE
,
Huang LC
,
Lee-Osbourne J
,
Cheung P
,
Cline HT
.
Abstract
Neurogenesis in the brain of Xenopus laevis continues throughout larval stages of development. We developed a 2-tier screen to identify candidate genes controlling neurogenesis in Xenopus optic tectum in vivo. First, microarray and NanoString analyses were used to identify candidate genes that were differentially expressed in Sox2-expressing neural progenitor cells or their neuronal progeny. Then an in vivo, time-lapse imaging-based screen was used to test whether morpholinos against 34 candidate genes altered neural progenitor cell proliferation or neuronal differentiation over 3 days in the optic tectum of intact Xenopus tadpoles. We co-electroporated antisense morpholino oligonucleotides against each of the candidate genes with a plasmid that drives GFP expression in Sox2-expressing neural progenitor cells and quantified the effects of morpholinos on neurogenesis. Of the 34 morpholinos tested, 24 altered neural progenitor cell proliferation or neuronal differentiation. The candidates which were tagged as differentially expressed and validated by the in vivo imaging screen include: actn1, arl9, eif3a, elk4, ephb1, fmr1-a, fxr1-1, fbxw7, fgf2, gstp1, hat1, hspa5, lsm6, mecp2, mmp9, and prkaca. Several of these candidates, including fgf2 and elk4, have known or proposed neurogenic functions, thereby validating our strategy to identify candidates. Genes with no previously demonstrated neurogenic functions, gstp1, hspa5 and lsm6, were identified from the morpholino experiments, suggesting that our screen successfully revealed unknown candidates. Genes that are associated with human disease, such as such as mecp2 and fmr1-a, were identified by our screen, providing the groundwork for using Xenopus as an experimental system to probe conserved disease mechanisms. Together the data identify candidate neurogenic regulatory genes and demonstrate that Xenopus is an effective experimental animal to identify and characterize genes that regulate neural progenitor cell proliferation and differentiation in vivo.
PubMed ID: 25818835
PMC ID: PMC4584193
Article link: Dev Biol
Grant support: [+]
R01 EY011261 NEI NIH HHS , R01 NS076006 NINDS NIH HHS , EY011261 NEI NIH HHS , NS076006 NINDS NIH HHS
Species referenced: Xenopus
Genes referenced: actn1 arl9 armc8 chn2 cpeb1 ctdnep1 dio3 efna3 eif3a elk4 ephb1 epx fbxw7 fgf2 fmr1 fxr1 glis2 gstp1 hat1 hdac6 hspa5 hspd1 lsm6 mecp2 mkrn2 mocs3 prkaca pura r3hdm2 rbfox2 slc12a2 sox2 tecta.2 tle1 vangl1 wnt7b
Morpholinos: actn1 MO1 arl9 MO1 armc8 MO1 chn1 MO1 cpeb1 MO2 ctdnep1 MO3 dio3 MO1 efna3 MO1 eif3a MO1 elk4 MO1 ephb1 MO1 epx MO1 fbxw7 MO1 fgf2 MO1 fmr1 MO2 fxr1 MO1 glis2 MO1 gstp1 MO1 hat1 MO1 hdac6 MO1 hspa5 MO2 lsm6 MO1 mecp2 MO2 mkrn2 MO3 mmp9.1 MO2 mocs3 MO1 prkaca MO2 pura MO1 r3hdm2 MO1 rbfox2 MO1 slc12a2 MO1 tle1 MO1 vangl1 MO1 wnt7b MO1
Phenotypes: Xla Wt + actn1 MO (fig.8) [+]
Xla Wt + actn1 MO
(Fig.8.A)
Xla Wt + arl9 MO (fig.8)
Xla Wt + arl9 MO (Fig.8.A)
Xla Wt + armc8 MO (fig.7.d1-d5)
Xla Wt + armc8 MO (fig.7.d1-d5)
Xla Wt + armc8 MO (fig.8)
Xla Wt + armc8 MO (fig.8)
Xla Wt + armc8 MO (Fig.8.A)
Xla Wt + armc8 MO (Fig.8.B-C)
Xla Wt + chn1 MO (fig.8)
Xla Wt + chn1 MO (fig.8)
Xla Wt + chn1 MO (Fig.8.A)
Xla Wt + chn1 MO (Fig.8.B-C)
Xla Wt + cpeb1 MO (fig.8)
Xla Wt + cpeb1 MO (Fig.8.A)
Xla Wt + ctdnep1 MO (fig.8)
Xla Wt + ctdnep1 MO (Fig.8.A)
Xla Wt + elk4 MO (fig.8)
Xla Wt + elk4 MO (Fig.8.A)
Xla Wt + ephb1 MO (fig.8)
Xla Wt + ephb1 MO (Fig.8.A)
Xla Wt + fgf2 MO (fig.8)
Xla Wt + fgf2 MO (Fig.8.A)
Xla Wt + fmr1 MO (fig.8)
Xla Wt + fmr1 MO (Fig.8.A)
Xla Wt + fxr1 MO (fig.8)
Xla Wt + fxr1 MO (Fig.8.A)
Xla Wt + glis2 MO (fig.8)
Xla Wt + glis2 MO (Fig.8.A)
Xla Wt + gstp1 MO (fig.7.b1-b5)
Xla Wt + gstp1 MO (fig.7.b1-b5)
Xla Wt + gstp1 MO (fig.8)
Xla Wt + gstp1 MO (fig.8)
Xla Wt + gstp1 MO (Fig.8.A)
Xla Wt + gstp1 MO (Fig.8.B-C)
Xla Wt + hat1 MO (fig.8)
Xla Wt + hdac6 MO (fig.8)
Xla Wt + hdac6 MO (Fig.8.A)
Xla Wt + hspa5 MO (fig.7.c1-c5)
Xla Wt + hspa5 MO (fig.7.c1-c5)
Xla Wt + hspa5 MO (fig.7.c1-c5)
Xla Wt + hspa5 MO (fig.8)
Xla Wt + hspa5 MO (fig.8)
Xla Wt + hspa5 MO (Fig.8.A)
Xla Wt + hspa5 MO (Fig.8.B-C)
Xla Wt + lsm6 MO (fig.8)
Xla Wt + lsm6 MO (Fig.8.A)
Xla Wt + mmp9 MO (fig.8)
Xla Wt + mmp9 MO (Fig.8.A)
Xla Wt + mocs3 MO (fig.8)
Xla Wt + mocs3 MO (Fig.8.A)
Xla Wt + prkaca MO (fig.8)
Xla Wt + prkaca MO (Fig.8.A)
Xla Wt + arl9 MO (fig.8)
Xla Wt + arl9 MO (Fig.8.A)
Xla Wt + armc8 MO (fig.7.d1-d5)
Xla Wt + armc8 MO (fig.7.d1-d5)
Xla Wt + armc8 MO (fig.8)
Xla Wt + armc8 MO (fig.8)
Xla Wt + armc8 MO (Fig.8.A)
Xla Wt + armc8 MO (Fig.8.B-C)
Xla Wt + chn1 MO (fig.8)
Xla Wt + chn1 MO (fig.8)
Xla Wt + chn1 MO (Fig.8.A)
Xla Wt + chn1 MO (Fig.8.B-C)
Xla Wt + cpeb1 MO (fig.8)
Xla Wt + cpeb1 MO (Fig.8.A)
Xla Wt + ctdnep1 MO (fig.8)
Xla Wt + ctdnep1 MO (Fig.8.A)
Xla Wt + elk4 MO (fig.8)
Xla Wt + elk4 MO (Fig.8.A)
Xla Wt + ephb1 MO (fig.8)
Xla Wt + ephb1 MO (Fig.8.A)
Xla Wt + fgf2 MO (fig.8)
Xla Wt + fgf2 MO (Fig.8.A)
Xla Wt + fmr1 MO (fig.8)
Xla Wt + fmr1 MO (Fig.8.A)
Xla Wt + fxr1 MO (fig.8)
Xla Wt + fxr1 MO (Fig.8.A)
Xla Wt + glis2 MO (fig.8)
Xla Wt + glis2 MO (Fig.8.A)
Xla Wt + gstp1 MO (fig.7.b1-b5)
Xla Wt + gstp1 MO (fig.7.b1-b5)
Xla Wt + gstp1 MO (fig.8)
Xla Wt + gstp1 MO (fig.8)
Xla Wt + gstp1 MO (Fig.8.A)
Xla Wt + gstp1 MO (Fig.8.B-C)
Xla Wt + hat1 MO (fig.8)
Xla Wt + hdac6 MO (fig.8)
Xla Wt + hdac6 MO (Fig.8.A)
Xla Wt + hspa5 MO (fig.7.c1-c5)
Xla Wt + hspa5 MO (fig.7.c1-c5)
Xla Wt + hspa5 MO (fig.7.c1-c5)
Xla Wt + hspa5 MO (fig.8)
Xla Wt + hspa5 MO (fig.8)
Xla Wt + hspa5 MO (Fig.8.A)
Xla Wt + hspa5 MO (Fig.8.B-C)
Xla Wt + lsm6 MO (fig.8)
Xla Wt + lsm6 MO (Fig.8.A)
Xla Wt + mmp9 MO (fig.8)
Xla Wt + mmp9 MO (Fig.8.A)
Xla Wt + mocs3 MO (fig.8)
Xla Wt + mocs3 MO (Fig.8.A)
Xla Wt + prkaca MO (fig.8)
Xla Wt + prkaca MO (Fig.8.A)
Article Images: [+] show captions
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Giachino, Lineage analysis of quiescent regenerative stem cells in the adult brain by genetic labelling reveals spatially restricted neurogenic niches in the olfactory bulb. 2009, Pubmed
Gu, Hematopoietic cell regulation by Rac1 and Rac2 guanosine triphosphatases. 2003, Pubmed
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Hardwick, Nervous decision-making: to divide or differentiate. 2014, Pubmed
Holmes, The long-term effects of neonatal seizures. 2009, Pubmed
Hosking, The transcriptional repressor Glis2 is a novel binding partner for p120 catenin. 2007, Pubmed
Huang, Extracting biological meaning from large gene lists with DAVID. 2009, Pubmed
Inaguma, SIL1, a causative cochaperone gene of Marinesco-Söjgren syndrome, plays an essential role in establishing the architecture of the developing cerebral cortex. 2014, Pubmed
Janesick, ERF and ETV3L are retinoic acid-inducible repressors required for primary neurogenesis. 2013, Pubmed , Xenbase
Kaikkonen, SUMOylation can regulate the activity of ETS-like transcription factor 4. 2010, Pubmed
Kaplan, Neuronal matrix metalloproteinase-9 is a determinant of selective neurodegeneration. 2014, Pubmed
Karsten, Global analysis of gene expression in neural progenitors reveals specific cell-cycle, signaling, and metabolic networks. 2003, Pubmed
Kim, A centrosomal Cdc20-APC pathway controls dendrite morphogenesis in postmitotic neurons. 2009, Pubmed
Kobayashi, RanBPM, Muskelin, p48EMLP, p44CTLH, and the armadillo-repeat proteins ARMC8alpha and ARMC8beta are components of the CTLH complex. 2007, Pubmed
Kok, Reverse genetic screening reveals poor correlation between morpholino-induced and mutant phenotypes in zebrafish. 2015, Pubmed
Kriegstein, Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. 2006, Pubmed
Lamar, Identification of NKL, a novel Gli-Kruppel zinc-finger protein that promotes neuronal differentiation. 2001, Pubmed , Xenbase
Le Belle, Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. 2011, Pubmed
Lee, Long-term depression-inducing stimuli promote cleavage of the synaptic adhesion molecule NGL-3 through NMDA receptors, matrix metalloproteinases and presenilin/γ-secretase. 2013, Pubmed
Lichti-Kaiser, Gli-similar proteins: their mechanisms of action, physiological functions, and roles in disease. 2012, Pubmed
Lilja, Like a rolling histone: epigenetic regulation of neural stem cells and brain development by factors controlling histone acetylation and methylation. 2013, Pubmed
LoTurco, GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. 1996, Pubmed
Lugert, Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. 2010, Pubmed
Maisel, Transcription profiling of adult and fetal human neuroprogenitors identifies divergent paths to maintain the neuroprogenitor cell state. 2007, Pubmed
Marei, Gene expression profiling of embryonic human neural stem cells and dopaminergic neurons from adult human substantia nigra. 2011, Pubmed
Meighan, Effects of matrix metalloproteinase inhibition on short- and long-term plasticity of schaffer collateral/CA1 synapses. 2007, Pubmed
Michaluk, Beta-dystroglycan as a target for MMP-9, in response to enhanced neuronal activity. 2007, Pubmed
Mochizuki, Thioredoxin regulates cell cycle via the ERK1/2-cyclin D1 pathway. 2009, Pubmed
Molnár, Evolution of cerebral cortical development. 2011, Pubmed
Morest, Precursors of neurons, neuroglia, and ependymal cells in the CNS: what are they? Where are they from? How do they get where they are going? 2003, Pubmed
Nacher, The role of N-methyl-D-asparate receptors in neurogenesis. 2006, Pubmed
Nagy, Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. 2006, Pubmed
Okano, Function of RNA-binding protein Musashi-1 in stem cells. 2005, Pubmed
Okulski, TIMP-1 abolishes MMP-9-dependent long-lasting long-term potentiation in the prefrontal cortex. 2007, Pubmed
Park, The characterization of gene expression during mouse neural stem cell differentiation in vitro. 2011, Pubmed
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