p53 Mutation suppresses adult neurogenesis in medaka fish (Oryzias latipes)

Isoe, Yasuko; Okuyama, Toru; Taniguchi, Yoshihito; Kubo, Takeo; Takeuchi, Hideaki

doi:10.1016/j.bbrc.2012.05.125

Cited by 18 publications

(14 citation statements)

References 24 publications

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“…Second, among the various roles of P53, it is also thought to be an important factor in regulating normal brain development through regulation of NPCs self renewal and differentiation (Mendrysa et al, 2011;Quadrato and Di Giovanni, 2012). Several studies have now shown that even low levels of P53 may lead to aberrant closure of the neural tube causing several neural malformations (Armstrong et al, 1995;Isoe et al, 2012;Kawamata and Ochiya, 2012;Mendrysa et al, 2011;Quadrato and Di Giovanni, 2012;Regeling et al, 2011;Rinon et al, 2011;Sah et al, 1995). The low levels of P53 observed in NBS-NPCs might be the cause for neural abnormalities, a prominent feature of NBS.…”

Section: Discussionmentioning

confidence: 99%

Chromosomal Instability and Molecular Defects in Induced Pluripotent Stem Cells from Nijmegen Breakage Syndrome Patients

et al. 2016

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Nijmegen breakage syndrome (NBS) results from the absence of the NBS1 protein, responsible for detection of DNA double-strand breaks (DSBs). NBS is characterized by microcephaly, growth retardation, immunodeficiency, and cancer predisposition. Here, we show successful reprogramming of NBS fibroblasts into induced pluripotent stem cells (NBS-iPSCs). Our data suggest a strong selection for karyotypically normal fibroblasts to go through the reprogramming process. NBS-iPSCs then acquire numerous chromosomal aberrations and show a delayed response to DSB induction. Furthermore, NBS-iPSCs display slower growth, mitotic inhibition, a reduced apoptotic response to stress, and abnormal cell-cycle-related gene expression. Importantly, NBS neural progenitor cells (NBS-NPCs) show downregulation of neural developmental genes, which seems to be mediated by P53. Our results demonstrate the importance of NBS1 in early human development, shed light on the molecular mechanisms underlying this severe syndrome, and further expand our knowledge of the genomic stress cells experience during the reprogramming process.

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Section: Discussionmentioning

confidence: 99%

Chromosomal Instability and Molecular Defects in Induced Pluripotent Stem Cells from Nijmegen Breakage Syndrome Patients

et al. 2016

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“…Thus, heat-inducible Cre/loxP site-specific recombination is also applicable for investigating adult neurogenesis in medaka fish. In contrast to mammals with limited neurogenesis in the adult brains, teleost fish such as medaka fish and zebrafish constitutively generate newborn neurons in numerous proliferating zones across the whole brain throughout life [21], [26], [39]–[41]. As the distribution of proliferation zones in the adult brain is mostly conserved among teleost fish, adult neurogenesis is believed to be important for the maintenance and development of the fundamental structure of the fish brain throughout life [21], [41].…”

Section: Discussionmentioning

confidence: 99%

Controlled Cre/loxP Site-Specific Recombination in the Developing Brain in Medaka Fish, Oryzias latipes

et al. 2013

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BackgroundGenetic mosaic techniques have been used to visualize and/or genetically modify a neuronal subpopulation within complex neural circuits in various animals. Neural populations available for mosaic analysis, however, are limited in the vertebrate brain.Methodology/Principal FindingsTo establish methodology to genetically manipulate neural circuits in medaka, we first created two transgenic (Tg) medaka lines, Tg (HSP:Cre) and Tg (HuC:loxP-DsRed-loxP-GFP). We confirmed medaka HuC promoter-derived expression of the reporter gene in juvenile medaka whole brain, and in neuronal precursor cells in the adult brain. We then demonstrated that stochastic recombination can be induced by micro-injection of Cre mRNA into Tg (HuC:loxP-DsRed-loxP-GFP) embryos at the 1-cell stage, which allowed us to visualize some subpopulations of GFP-positive cells in compartmentalized regions of the telencephalon in the adult medaka brain. This finding suggested that the distribution of clonally-related cells derived from single or a few progenitor cells was restricted to a compartmentalized region. Heat treatment of Tg(HSP:Cre x HuC:loxP-DsRed-loxP-GFP) embryos (0–1 day post fertilization [dpf]) in a thermalcycler (39°C) led to Cre/loxP recombination in the whole brain. The recombination efficiency was notably low when using 2–3 dpf embyos compared with 0–1 dpf embryos, indicating the possibility of stage-dependent sensitivity of heat-inducible recombination. Finally, using an infrared laser-evoked gene operator (IR-LEGO) system, heat shock induced in a micro area in the developing brains led to visualization of clonally-related cells in both juvenile and adult medaka fish.Conclusions/SignificanceWe established a noninvasive method to control Cre/loxP site-specific recombination in the developing nervous system in medaka fish. This method will broaden the neural population available for mosaic analyses and allow for lineage tracing of the vertebrate nervous system in both juvenile and adult stages.

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“…Among teleosts, adult cell proliferation and neurogenesis have been thoroughly characterized in wave type weakly electric gymnotids, particularly in Apteronotus leptorhynchus [ A. leptorhynchus : (Zupanc and Horschke, 1995; Zupanc et al, 1996; Zupanc, 2001; Hinsch and Zupanc, 2006); Eigenmannia sp: (Zupanc and Zupanc, 1992); and Brachyhypopomus gauderio : (Dunlap et al, 2011)]. The spatial distribution of brain proliferation zones in adult wave type weakly electric gymnotids roughly resembles that of other teleosts [ Astatotilapia burtoni (Maruska et al, 2012); Austrolebias (Fernández et al, 2011); Carassius auratus (Raymond and Easter, 1983; Delgado and Schmachtenberg, 2011); Danio rerio (Maeyama and Nakayasu, 2000; Zupanc et al, 2005; Adolf et al, 2006; Grandel et al, 2006; Ampatzis and Dermon, 2007; Kaslin et al, 2009; Ito et al, 2010; März et al, 2010; Zupanc, 2011); Gasterosteus aculeatus (Ekström et al, 2001); Nothobranchius furzeri (Terzibasi et al, 2012); Odontesthes bonariensis (Strobl-Mazzulla et al, 2010); Oreochromis mossambicus (Teles et al, 2012); Oryzias latipes (Nguyen et al, 1999; Candal et al, 2005a; Alunni et al, 2010; Kuroyanagi et al, 2010; Isoe et al, 2012) and Salmo trutta fario (Candal et al, 2005b)], despite the phylogenetic distance to most of those species. However, differences have been observed that were attributed to the functional specialization of weakly electric fish (Zupanc and Horschke, 1995; Grandel et al, 2006; Grandel and Brand, 2013).…”

Section: Introductionmentioning

confidence: 99%

Spatial distribution and cellular composition of adult brain proliferative zones in the teleost, Gymnotus omarorum

Olivera-Pasilio

Peterson

Castelló³

2014

Front. Neuroanat.

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Proliferation of stem/progenitor cells during development provides for the generation of mature cell types in the CNS. While adult brain proliferation is highly restricted in the mammals, it is widespread in teleosts. The extent of adult neural proliferation in the weakly electric fish, Gymnotus omarorum has not yet been described. To address this, we used double thymidine analog pulse-chase labeling of proliferating cells to identify brain proliferation zones, characterize their cellular composition, and analyze the fate of newborn cells in adult G. omarorum. Short thymidine analog chase periods revealed the ubiquitous distribution of adult brain proliferation, similar to other teleosts, particularly Apteronotus leptorhynchus. Proliferating cells were abundant at the ventricular-subventricular lining of the ventricular-cisternal system, adjacent to the telencephalic subpallium, the diencephalic preoptic region and hypothalamus, and the mesencephalic tectum opticum and torus semicircularis. Extraventricular proliferation zones, located distant from the ventricular-cisternal system surface, were found in all divisions of the rombencephalic cerebellum. We also report a new adult proliferation zone at the caudal-lateral border of the electrosensory lateral line lobe. All proliferation zones showed a heterogeneous cellular composition. The use of short (24 h) and long (30 day) chase periods revealed abundant fast cycling cells (potentially intermediate amplifiers), sparse slow cycling (potentially stem) cells, cells that appear to have entered a quiescent state, and cells that might correspond to migrating newborn neural cells. Their abundance and migration distance differed among proliferation zones: greater numbers and longer range and/or pace of migrating cells were associated with subpallial and cerebellar proliferation zones.

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p53 Mutation suppresses adult neurogenesis in medaka fish (Oryzias latipes)

Cited by 18 publications

References 24 publications

Chromosomal Instability and Molecular Defects in Induced Pluripotent Stem Cells from Nijmegen Breakage Syndrome Patients

Chromosomal Instability and Molecular Defects in Induced Pluripotent Stem Cells from Nijmegen Breakage Syndrome Patients

Controlled Cre/loxP Site-Specific Recombination in the Developing Brain in Medaka Fish, Oryzias latipes

Spatial distribution and cellular composition of adult brain proliferative zones in the teleost, Gymnotus omarorum

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