Significance of Birth in the Maintenance of Quiescent Neural Stem Cells

Overview

Journal Sci Adv

Date 2025 Jan 22

PMID 39841848

Authors

Koya Kawase

Yasuhisa Nakamura

Laura Wolbeck

Shoko Takemura

Kei Zaitsu

Takehiro Ando

Hideo Jinnou

Masato Sawada

Chikako Nakajima

Rasmus Rydbirk

Sakura Gokenya

Akira Ito

Hitomi Fujiyama

Akari Saito

Akira Iguchi

Panagiotis Kratimenos

Nobuyuki Ishibashi

Vittorio Gallo

Osuke Iwata

Shinji Saitoh

Konstantin Khodosevich

Kazunobu Sawamoto

Affiliations

Soon will be listed here.

Abstract

Birth is one of the most important life events for animals. However, its significance in the developmental process is not fully understood. Here, we found that birth-induced alteration of glutamine metabolism in radial glia (RG), the embryonic neural stem cells (NSCs), is required for the acquisition of quiescence and long-term maintenance of postnatal NSCs. Preterm birth impairs this cellular process, leading to transient hyperactivation of RG. Consequently, in the postnatal brain, the NSC pool is depleted and neurogenesis is decreased. We also found that the maintenance of quiescent RG after preterm birth improves postnatal neurogenesis. This study demonstrates the significance of birth in the maintenance of quiescent NSCs.

References

Lois C, Alvarez-Buylla A . Long-distance neuronal migration in the adult mammalian brain. Science. 1994; 264(5162):1145-8. DOI: 10.1126/science.8178174. View

Barkas N, Petukhov V, Nikolaeva D, Lozinsky Y, Demharter S, Khodosevich K . Joint analysis of heterogeneous single-cell RNA-seq dataset collections. Nat Methods. 2019; 16(8):695-698. PMC: 6684315. DOI: 10.1038/s41592-019-0466-z. View

Nakamura-Ishizu A, Ito K, Suda T . Hematopoietic Stem Cell Metabolism during Development and Aging. Dev Cell. 2020; 54(2):239-255. PMC: 7418032. DOI: 10.1016/j.devcel.2020.06.029. View

Ito K, Suda T . Metabolic requirements for the maintenance of self-renewing stem cells. Nat Rev Mol Cell Biol. 2014; 15(4):243-56. PMC: 4095859. DOI: 10.1038/nrm3772. View

Garcia-Verdugo J, Ferron S, Flames N, Collado L, Desfilis E, Font E . The proliferative ventricular zone in adult vertebrates: a comparative study using reptiles, birds, and mammals. Brain Res Bull. 2002; 57(6):765-75. DOI: 10.1016/s0361-9230(01)00769-9. View

Llorens-Bobadilla E, Zhao S, Baser A, Saiz-Castro G, Zwadlo K, Martin-Villalba A . Single-Cell Transcriptomics Reveals a Population of Dormant Neural Stem Cells that Become Activated upon Brain Injury. Cell Stem Cell. 2015; 17(3):329-40. DOI: 10.1016/j.stem.2015.07.002. View

Jinnou H, Sawada M, Kawase K, Kaneko N, Herranz-Perez V, Miyamoto T . Radial Glial Fibers Promote Neuronal Migration and Functional Recovery after Neonatal Brain Injury. Cell Stem Cell. 2017; 22(1):128-137.e9. DOI: 10.1016/j.stem.2017.11.005. View

Mirzadeh Z, Doetsch F, Sawamoto K, Wichterle H, Alvarez-Buylla A . The subventricular zone en-face: wholemount staining and ependymal flow. J Vis Exp. 2010; (39). PMC: 3144601. DOI: 10.3791/1938. View

Matsumoto M, Sawada M, Garcia-Gonzalez D, Herranz-Perez V, Ogino T, Bang Nguyen H . Dynamic Changes in Ultrastructure of the Primary Cilium in Migrating Neuroblasts in the Postnatal Brain. J Neurosci. 2019; 39(50):9967-9988. PMC: 6978947. DOI: 10.1523/JNEUROSCI.1503-19.2019. View

10.

Dong X, Zhang Q, Yu X, Wang D, Ma J, Ma J . Metabolic lactate production coordinates vasculature development and progenitor behavior in the developing mouse neocortex. Nat Neurosci. 2022; 25(7):865-875. DOI: 10.1038/s41593-022-01093-7. View

11.

Zaitsu K, Hayashi Y, Murata T, Ohara T, Nakagiri K, Kusano M . Intact Endogenous Metabolite Analysis of Mice Liver by Probe Electrospray Ionization/Triple Quadrupole Tandem Mass Spectrometry and Its Preliminary Application to in Vivo Real-Time Analysis. Anal Chem. 2016; 88(7):3556-61. DOI: 10.1021/acs.analchem.5b04046. View

12.

Hibino Y, Iguchi A, Zaitsu K . Preliminary study to classify mechanisms of mitochondrial toxicity by in vitro metabolomics and bioinformatics. Toxicol Appl Pharmacol. 2022; :116316. DOI: 10.1016/j.taap.2022.116316. View

13.

Kaslin J, Ganz J, Brand M . Proliferation, neurogenesis and regeneration in the non-mammalian vertebrate brain. Philos Trans R Soc Lond B Biol Sci. 2007; 363(1489):101-22. PMC: 2605489. DOI: 10.1098/rstb.2006.2015. View

14.

Danciu D, Hooli J, Martin-Villalba A, Marciniak-Czochra A . Mathematics of neural stem cells: Linking data and processes. Cells Dev. 2023; 174:203849. DOI: 10.1016/j.cdev.2023.203849. View

15.

Ota H, Hikita T, Sawada M, Nishioka T, Matsumoto M, Komura M . Speed control for neuronal migration in the postnatal brain by Gmip-mediated local inactivation of RhoA. Nat Commun. 2014; 5:4532. DOI: 10.1038/ncomms5532. View

16.

Carvajal Ibanez D, Skabkin M, Hooli J, Cerrizuela S, Gopferich M, Jolly A . Interferon regulates neural stem cell function at all ages by orchestrating mTOR and cell cycle. EMBO Mol Med. 2023; 15(4):e16434. PMC: 10086582. DOI: 10.15252/emmm.202216434. View

17.

Yu G, Wang L, Han Y, He Q . clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS. 2012; 16(5):284-7. PMC: 3339379. DOI: 10.1089/omi.2011.0118. View

18.

Takubo K, Goda N, Yamada W, Iriuchishima H, Ikeda E, Kubota Y . Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell. 2010; 7(3):391-402. DOI: 10.1016/j.stem.2010.06.020. View

19.

Pellegrini E, Mouriec K, Anglade I, Menuet A, Le Page Y, Gueguen M . Identification of aromatase-positive radial glial cells as progenitor cells in the ventricular layer of the forebrain in zebrafish. J Comp Neurol. 2007; 501(1):150-67. DOI: 10.1002/cne.21222. View

20.

Hartman N, Lin T, Zhang L, Paquelet G, Feliciano D, Bordey A . mTORC1 targets the translational repressor 4E-BP2, but not S6 kinase 1/2, to regulate neural stem cell self-renewal in vivo. Cell Rep. 2013; 5(2):433-44. DOI: 10.1016/j.celrep.2013.09.017. View