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Erschienen in: Brain Structure and Function 1/2018

01.01.2018 | Original Article

Dentate granule progenitor cell properties are rapidly altered soon after birth

verfasst von: Kenta Matsue, Shiori Minakawa, Taichi Kashiwagi, Keiko Toda, Toru Sato, Seiji Shioda, Tatsunori Seki

Erschienen in: Brain Structure and Function | Ausgabe 1/2018

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Abstract

Neurogenesis occurs during the embryonic period and ceases soon after birth in the neocortex, but continues to occur in the hippocampus even in the adult. The embryonic neocortex has radial glia or progenitor cells expressing brain lipid-binding protein (BLBP), whereas the adult hippocampus has radial granule progenitor cells expressing BLBP and glial fibrillary acidic protein (GFAP) in the subgranular zone. We previously found that embryonic hippocampal granule progenitor cells express GFAP, but not BLBP, indicating that these cells are different from both embryonic neocortical and adult granule progenitor cells. In the present study, as the first step towards understanding the mechanism of persistent hippocampal neurogenesis, we aimed to determine the stage at which embryonic-type granule progenitors become adult-type progenitors using mouse Gfap-GFP transgenic mice. During the embryonic stages, Gfap-GFP-positive (Gfap-GFP+) cells were distributed in the entire developing dentate gyrus (DG), whereas BLBP-positive (BLBP+) cells were mainly present in the fimbria and subpial region, and to some extent in the DG. Up to postnatal day 0 (P0), double-positive cells were scarcely detected. However, at P1, one-third of the Gfap-GFP+ cells in the DG suddenly began to weakly express BLBP. Thereafter, Gfap-GFP+/BLBP+ cells rapidly increased in number, and extended their radial processes in the inner granular cell layer. At P14 and in the adult, two-thirds of the Gfap-GFP+ cells in the subgranular zone showed BLBP immunoreactivity. These results suggest that the properties of hippocampal granule progenitor cells are rapidly altered from an embryonic to adult type soon after birth.
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Literatur
Zurück zum Zitat Altman J, Bayer SA (1990c) Prolonged sojourn of developing pyramidal cells in the intermediate zone of the hippocampus and their settling in the stratum pyramidale. J Comp Neurol 301:343–364. doi:10.1002/cne.903010303 CrossRefPubMed Altman J, Bayer SA (1990c) Prolonged sojourn of developing pyramidal cells in the intermediate zone of the hippocampus and their settling in the stratum pyramidale. J Comp Neurol 301:343–364. doi:10.​1002/​cne.​903010303 CrossRefPubMed
Zurück zum Zitat Anthony TE, Mason HA, Gridley T, Fishell G, Heintz N (2005) Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells service Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells. Genes Dev 19:1028–1033. doi:10.1101/gad.1302105 CrossRefPubMedPubMedCentral Anthony TE, Mason HA, Gridley T, Fishell G, Heintz N (2005) Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells service Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells. Genes Dev 19:1028–1033. doi:10.​1101/​gad.​1302105 CrossRefPubMedPubMedCentral
Zurück zum Zitat Arai Y, Funatsu N, Numayama-Tsuruta K, Nomura T, Nakamura S, Osumi N (2005) Role of Fabp7, a downstream gene of Pax6, in the maintenance of neuroepithelial cells during early embryonic development of the rat cortex. J Neurosci 25:9752–9761. doi:10.1523/JNEUROSCI.2512-05.2005 CrossRefPubMed Arai Y, Funatsu N, Numayama-Tsuruta K, Nomura T, Nakamura S, Osumi N (2005) Role of Fabp7, a downstream gene of Pax6, in the maintenance of neuroepithelial cells during early embryonic development of the rat cortex. J Neurosci 25:9752–9761. doi:10.​1523/​JNEUROSCI.​2512-05.​2005 CrossRefPubMed
Zurück zum Zitat Belmadani A, Ren D, Bhattacharyya BJ, Rothwangl KB, Hope TJ, Perlman H, Miller RJ (2015) Identification of a sustained neurogenic zone at the dorsal surface of the adult mouse hippocampus and its regulation by the chemokine SDF-1. Hippocampus 25:1224–1241. doi:10.1002/hipo.22428 CrossRefPubMedPubMedCentral Belmadani A, Ren D, Bhattacharyya BJ, Rothwangl KB, Hope TJ, Perlman H, Miller RJ (2015) Identification of a sustained neurogenic zone at the dorsal surface of the adult mouse hippocampus and its regulation by the chemokine SDF-1. Hippocampus 25:1224–1241. doi:10.​1002/​hipo.​22428 CrossRefPubMedPubMedCentral
Zurück zum Zitat Brunne B, Zhao S, Derouiche A, Herz J, May P, Frotscher M, Bock HH (2010) Origin, maturation, and astroglial transformation of secondary radial glial cells in the developing dentate gyrus. Gila 58:1553–1569. doi:10.1002/glia.21029 Brunne B, Zhao S, Derouiche A, Herz J, May P, Frotscher M, Bock HH (2010) Origin, maturation, and astroglial transformation of secondary radial glial cells in the developing dentate gyrus. Gila 58:1553–1569. doi:10.​1002/​glia.​21029
Zurück zum Zitat Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317. doi:10.1038/3305 CrossRefPubMed Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317. doi:10.​1038/​3305 CrossRefPubMed
Zurück zum Zitat Fukuda S, Kato F, Tozuka Y, Yamaguchi M, Miyamoto Y, Hisatsune T (2003) Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J Neurosci 23:9357–9366PubMed Fukuda S, Kato F, Tozuka Y, Yamaguchi M, Miyamoto Y, Hisatsune T (2003) Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J Neurosci 23:9357–9366PubMed
Zurück zum Zitat Garcia ADR, Doan NB, Imura T, Bush TG, Sofroniew MV (2004) GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7:1233–1241. doi:10.1038/nn1340 CrossRefPubMed Garcia ADR, Doan NB, Imura T, Bush TG, Sofroniew MV (2004) GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7:1233–1241. doi:10.​1038/​nn1340 CrossRefPubMed
Zurück zum Zitat Hartfuss E, Förster E, Bock HH, Hack MA, Leprince P, Luque JM, Herz J, Frotscher M, Götz M (2003) Reelin signaling directly affects radial glia morphology and biochemical maturation. Development 130:4597–4609. doi:10.1242/dev.00654 CrossRefPubMed Hartfuss E, Förster E, Bock HH, Hack MA, Leprince P, Luque JM, Herz J, Frotscher M, Götz M (2003) Reelin signaling directly affects radial glia morphology and biochemical maturation. Development 130:4597–4609. doi:10.​1242/​dev.​00654 CrossRefPubMed
Zurück zum Zitat Ito H, Morishita R, Iwamoto I, Nagata KI (2014) Establishment of an in vivo electroporation method into postnatal newborn neurons in the dentate gyrus. Hippocampus 24:1449–1457. doi:10.1002/hipo.22325 CrossRefPubMed Ito H, Morishita R, Iwamoto I, Nagata KI (2014) Establishment of an in vivo electroporation method into postnatal newborn neurons in the dentate gyrus. Hippocampus 24:1449–1457. doi:10.​1002/​hipo.​22325 CrossRefPubMed
Zurück zum Zitat Kempermann G (2011) Adult neurogenesis 2. Oxford University Press, Oxford Kempermann G (2011) Adult neurogenesis 2. Oxford University Press, Oxford
Zurück zum Zitat Li G, Pleasure SJ (2005) Morphogenesis of the dentate gyrus: what we are learning from mouse mutants. Dev Neurosci 27:93–99CrossRefPubMed Li G, Pleasure SJ (2005) Morphogenesis of the dentate gyrus: what we are learning from mouse mutants. Dev Neurosci 27:93–99CrossRefPubMed
Zurück zum Zitat Li G, Pleasure SJ (2014) The development of hippocampal cellular assemblies. Wiley Interdiscip Rev Dev Biol 3:165–177CrossRefPubMed Li G, Pleasure SJ (2014) The development of hippocampal cellular assemblies. Wiley Interdiscip Rev Dev Biol 3:165–177CrossRefPubMed
Zurück zum Zitat Li G, Kataoka H, Coughlin SR, Pleasure SJ (2009) Identification of a transient subpial neurogenic zone in the developing dentate gyrus and its regulation by Cxcl12 and reelin signaling. Development 136:327–335. doi:10.1242/dev.025742 CrossRefPubMed Li G, Kataoka H, Coughlin SR, Pleasure SJ (2009) Identification of a transient subpial neurogenic zone in the developing dentate gyrus and its regulation by Cxcl12 and reelin signaling. Development 136:327–335. doi:10.​1242/​dev.​025742 CrossRefPubMed
Zurück zum Zitat Liu Y, Namba T, Liu J, Suzuki R, Shioda S, Seki T (2010) Glial fibrillary acidic protein-expressing neural progenitors give rise to immature neurons via early intermediate progenitors expressing both glial fibrillary acidic protein and neuronal markers in the adult hippocampus. Neuroscience 166:241–251. doi:10.1016/j.neuroscience.2009.12.026 CrossRefPubMed Liu Y, Namba T, Liu J, Suzuki R, Shioda S, Seki T (2010) Glial fibrillary acidic protein-expressing neural progenitors give rise to immature neurons via early intermediate progenitors expressing both glial fibrillary acidic protein and neuronal markers in the adult hippocampus. Neuroscience 166:241–251. doi:10.​1016/​j.​neuroscience.​2009.​12.​026 CrossRefPubMed
Zurück zum Zitat Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104–9110PubMed Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104–9110PubMed
Zurück zum Zitat Matsumata M, Sakayori N, Maekawa M, Owada Y, Yoshikawa T, Osumi N (2012) The effects of Fabp7 and Fabp5 on postnatal hippocampal neurogenesis in the mouse. Stem Cells 30:1532–1543. doi:10.1002/stem.1124 CrossRefPubMed Matsumata M, Sakayori N, Maekawa M, Owada Y, Yoshikawa T, Osumi N (2012) The effects of Fabp7 and Fabp5 on postnatal hippocampal neurogenesis in the mouse. Stem Cells 30:1532–1543. doi:10.​1002/​stem.​1124 CrossRefPubMed
Zurück zum Zitat Nakahira E, Yuasa S (2005) Neuronal generation, migration, and differentiation in the mouse hippocampal primoridium as revealed by enhanced green fluorescent protein gene transfer by means of in utero electroporation. J Comp Neurol 483:329–340. doi:10.1002/cne.20441 CrossRefPubMed Nakahira E, Yuasa S (2005) Neuronal generation, migration, and differentiation in the mouse hippocampal primoridium as revealed by enhanced green fluorescent protein gene transfer by means of in utero electroporation. J Comp Neurol 483:329–340. doi:10.​1002/​cne.​20441 CrossRefPubMed
Zurück zum Zitat Namba T, Mochizuki H, Suzuki R, Onodera M, Yamaguchi M, Namiki H, Shioda S, Seki T (2011) Time-lapse imaging reveals symmetric neurogenic cell division of GFAP-expressing progenitors for expansion of postnatal dentate granule neurons. PLoS One. doi:10.1371/journal.pone.0025303 Namba T, Mochizuki H, Suzuki R, Onodera M, Yamaguchi M, Namiki H, Shioda S, Seki T (2011) Time-lapse imaging reveals symmetric neurogenic cell division of GFAP-expressing progenitors for expansion of postnatal dentate granule neurons. PLoS One. doi:10.​1371/​journal.​pone.​0025303
Zurück zum Zitat Navaero-Quiroga I, Fernandez-Valdes M, Lin SL, Naegele JR (2006) Postnatal cellular contributions of the hippocampus subventricular zone to the dentate gyrus, corpus callosum, fimbria, and cerebral cortex. J Comp Neurol 497:833–845. doi:10.1002/cne.21037 CrossRef Navaero-Quiroga I, Fernandez-Valdes M, Lin SL, Naegele JR (2006) Postnatal cellular contributions of the hippocampus subventricular zone to the dentate gyrus, corpus callosum, fimbria, and cerebral cortex. J Comp Neurol 497:833–845. doi:10.​1002/​cne.​21037 CrossRef
Zurück zum Zitat Raponi E, Agenes F, Delphin C, Assard N, Baudier J, Legraverend C, Deloulme JC (2007) S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 55:165–177. doi:10.1002/glia.20445 CrossRefPubMedPubMedCentral Raponi E, Agenes F, Delphin C, Assard N, Baudier J, Legraverend C, Deloulme JC (2007) S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 55:165–177. doi:10.​1002/​glia.​20445 CrossRefPubMedPubMedCentral
Zurück zum Zitat Schmid RS, Yokota Y, Anton ES (2006) Generation and characterization of brain lipid-binding protein promoter-based transgenic mouse models for the study of radial glia. Glia 53:345–351. doi:10.1002/glia.20274 CrossRefPubMed Schmid RS, Yokota Y, Anton ES (2006) Generation and characterization of brain lipid-binding protein promoter-based transgenic mouse models for the study of radial glia. Glia 53:345–351. doi:10.​1002/​glia.​20274 CrossRefPubMed
Zurück zum Zitat Seki T, Arai Y (1993) Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J Neurosci 13:2351–2358PubMed Seki T, Arai Y (1993) Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J Neurosci 13:2351–2358PubMed
Zurück zum Zitat Seki T, Namba T, Mochizuki H, Onodera M (2007) Clustering, migration, and neurite formation of neural precursor cells in the adult rat hippocampus. J Comp Neurol 502:275–290. doi:10.1002/cne CrossRefPubMed Seki T, Namba T, Mochizuki H, Onodera M (2007) Clustering, migration, and neurite formation of neural precursor cells in the adult rat hippocampus. J Comp Neurol 502:275–290. doi:10.​1002/​cne CrossRefPubMed
Zurück zum Zitat Seki T, Sato T, Toda K, Osumi N, Imura T, Shioda S (2014) Distinctive population of Gfap-expressing neural progenitors arising around the dentate notch migrate and form the granule cell layer in the developing hippocampus. J Comp Neurol 522:261–283. doi:10.1002/cne.23460 CrossRefPubMed Seki T, Sato T, Toda K, Osumi N, Imura T, Shioda S (2014) Distinctive population of Gfap-expressing neural progenitors arising around the dentate notch migrate and form the granule cell layer in the developing hippocampus. J Comp Neurol 522:261–283. doi:10.​1002/​cne.​23460 CrossRefPubMed
Zurück zum Zitat Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153–7160PubMed Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153–7160PubMed
Zurück zum Zitat Seri B, García-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A (2004) Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 478:359–378. doi:10.1002/cne.20288 CrossRefPubMed Seri B, García-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A (2004) Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 478:359–378. doi:10.​1002/​cne.​20288 CrossRefPubMed
Zurück zum Zitat Shapiro LA, Wang L, Upadhyaya P, Ribak CE (2011) Seizure-induced increased neurogenesis occurs in the dentate gyrus of aged sprague-dawley rats. Aging Dis 2:286–293PubMedPubMedCentral Shapiro LA, Wang L, Upadhyaya P, Ribak CE (2011) Seizure-induced increased neurogenesis occurs in the dentate gyrus of aged sprague-dawley rats. Aging Dis 2:286–293PubMedPubMedCentral
Zurück zum Zitat Sharifi K, Morihiro Y, Maekawa M, Yasumoto Y, Hoshi H, Adachi Y, Sawada T, Tokuda N, Kondo H, Yoshikawa T, Suzuki M, Owada Y (2011) FABP7 expression in normal and stab-injured brain cortex and its role in astrocyte proliferation. Histochem Cell Biol 136:501–513. doi:10.1007/s00418-011-0865-4 CrossRefPubMedPubMedCentral Sharifi K, Morihiro Y, Maekawa M, Yasumoto Y, Hoshi H, Adachi Y, Sawada T, Tokuda N, Kondo H, Yoshikawa T, Suzuki M, Owada Y (2011) FABP7 expression in normal and stab-injured brain cortex and its role in astrocyte proliferation. Histochem Cell Biol 136:501–513. doi:10.​1007/​s00418-011-0865-4 CrossRefPubMedPubMedCentral
Zurück zum Zitat Steiner B, Kronenberg G, Jessberger S, Brandt MD, Reuter K, Kempermann G (2004) Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia 46:41–52. doi:10.1002/glia.10337 CrossRefPubMed Steiner B, Kronenberg G, Jessberger S, Brandt MD, Reuter K, Kempermann G (2004) Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia 46:41–52. doi:10.​1002/​glia.​10337 CrossRefPubMed
Zurück zum Zitat Tabata H, Yoshinaga S, Nakajima K (2012) Cytoarchitecture of mouse and human subventricular zone in developing cerebral neocortex. Exp Brain Res 216:161–168CrossRefPubMed Tabata H, Yoshinaga S, Nakajima K (2012) Cytoarchitecture of mouse and human subventricular zone in developing cerebral neocortex. Exp Brain Res 216:161–168CrossRefPubMed
Zurück zum Zitat Watanabe A, Toyota T, Owada Y, Hayashi T, Iwayama Y, Matsumata M, Ishitsuka Y, Nakaya A, Maekawa M, Ohnishi T, Arai R, Sakurai K, Yamada K, Kondo H, Hashimoto K et al (2007) Fabp7 maps to a quantitative trait locus for a schizophrenia endophenotype. PLoS Biol 5:2469–2483. doi:10.1371/journal.pbio.0050297 CrossRef Watanabe A, Toyota T, Owada Y, Hayashi T, Iwayama Y, Matsumata M, Ishitsuka Y, Nakaya A, Maekawa M, Ohnishi T, Arai R, Sakurai K, Yamada K, Kondo H, Hashimoto K et al (2007) Fabp7 maps to a quantitative trait locus for a schizophrenia endophenotype. PLoS Biol 5:2469–2483. doi:10.​1371/​journal.​pbio.​0050297 CrossRef
Zurück zum Zitat Yamaguchi M, Saito H, Suzuki M, Mori K (2000) Visualization of neurogenesis in the central nervous system using nestin promoterGFP transgenic mice. NeuroReport 11:1991–1996CrossRefPubMed Yamaguchi M, Saito H, Suzuki M, Mori K (2000) Visualization of neurogenesis in the central nervous system using nestin promoterGFP transgenic mice. NeuroReport 11:1991–1996CrossRefPubMed
Zurück zum Zitat Yamamoto T, Yamamoto A, Watanabe M, Matsuo T, Yamazaki N, Kataoka M, Terada H, Shinohara Y (2009) Classification of FABP isoforms and tissues based on quantitative evaluation of transcript levels of these isoforms in various rat tissues. Biotechnol Lett 31:1695–1701. doi:10.1007/s10529-009-0065-7 CrossRefPubMed Yamamoto T, Yamamoto A, Watanabe M, Matsuo T, Yamazaki N, Kataoka M, Terada H, Shinohara Y (2009) Classification of FABP isoforms and tissues based on quantitative evaluation of transcript levels of these isoforms in various rat tissues. Biotechnol Lett 31:1695–1701. doi:10.​1007/​s10529-009-0065-7 CrossRefPubMed
Zurück zum Zitat Yuasa S (2001) Development of astrocytes in the mouse hippocampus as tracked by tenascin-C gene expression. Arch Histol Cytol 64:149–158CrossRefPubMed Yuasa S (2001) Development of astrocytes in the mouse hippocampus as tracked by tenascin-C gene expression. Arch Histol Cytol 64:149–158CrossRefPubMed
Metadaten
Titel
Dentate granule progenitor cell properties are rapidly altered soon after birth
verfasst von
Kenta Matsue
Shiori Minakawa
Taichi Kashiwagi
Keiko Toda
Toru Sato
Seiji Shioda
Tatsunori Seki
Publikationsdatum
01.01.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 1/2018
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1499-7

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