nach oben

Brain Structure and Function

Erschienen in:

28.10.2019 | Original Article

Non-radial tortuous migration with cell polarity alterations of newly generated granule neurons in the neonatal rat dentate gyrus

verfasst von: Takashi Namba, Hiroshi Shinohara, Tatsunori Seki

Erschienen in: Brain Structure and Function | Ausgabe 9/2019

Einloggen, um Zugang zu erhalten

Abstract

To establish functional neuronal circuits, newborn neurons generally migrate from the ventricular germinal zones to their final positions during embryonic periods. However, most excitatory neurons of the hippocampal dentate gyrus are born postnatally in the hilus, far from the lateral ventricle. Newly generated granule neurons must then migrate to the surrounding granule cell layer (GCL), which suggests that newborn granule cells may migrate by unique cellular mechanisms. In the present study, we describe the migratory behaviors of postnatally generated granule neurons using combined retroviral labeling and time-lapse imaging analysis. Our results show that whereas half of the newly generated neurons undergo radial migration, the remainder engages in more complex migratory patterns with veering and turning movements accompanied by process formation and cell polarity alterations. These data reveal a previously unappreciated diversity of mechanisms by which granule neurons distribute throughout the GCL to contribute to hippocampal circuitry.

Nur mit Berechtigung zugänglich

Abrous DN, Wojtowicz JM (2015) Interaction between neurogenesis and hippocampal memory system: new vistas. Cold Spring Harb Perspect Biol. https://doi.org/10.1101/cshperspect.a018952 CrossRefPubMedPubMedCentral

Altman J, Bayer SA (1990a) Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301:365–381CrossRef

Altman J, Bayer SA (1990b) Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J Comp Neurol 301:325–342CrossRef

Altman J, Das GD (1965) Post-natal origin of microneurones in the rat brain. Nature 207:953–956CrossRef

Amaral DG, Dent JA (1981) Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 195:51–86. https://doi.org/10.1002/cne.901950106 CrossRefPubMed

Barnes AP, Polleux F (2009) Establishment of axon–dendrite polarity in developing neurons. Annu Rev Neurosci 32:347–381. https://doi.org/10.1146/annurev.neuro.31.060407.125536 CrossRefPubMedPubMedCentral

Bayer SA (1980) Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography. J Comp Neurol 190:87–114CrossRef

Bayer SA, Altman J (1975) Radiation-induced interference with postnatal hippocampal cytogenesis in rats and its long-term effects on the acquisition of neurons and glia. J Comp Neurol 163:1–19. https://doi.org/10.1002/cne.901630102 CrossRef

Blaabjerg M, Zimmer J (2007) The dentate mossy fibers: structural organization, development and plasticity. Prog Brain Res 163:85–107. https://doi.org/10.1016/S0079-6123(07)63005-2 CrossRefPubMed

Cooper JA (2014) Molecules and mechanisms that regulate multipolar migration in the intermediate zone. Front Cell Neurosci 8:386. https://doi.org/10.3389/fncel.2014.00386 CrossRefPubMedPubMedCentral

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. https://doi.org/10.1038/3305 CrossRefPubMed

Funahashi Y, Namba T, Nakamuta S, Kaibuchi K (2014) Neuronal polarization in vivo: growing in a complex environment. Curr Opin Neurobiol 27:215–223. https://doi.org/10.1016/j.conb.2014.04.009 CrossRefPubMed

Gertz CC, Kriegstein AR (2015) Neuronal migration dynamics in the developing ferret cortex. J Neurosci 35:14307–14315. https://doi.org/10.1523/JNEUROSCI.2198-15.2015 CrossRefPubMedPubMedCentral

Hatanaka Y, Yamauchi K (2013) Excitatory cortical neurons with multipolar shape establish neuronal polarity by forming a tangentially oriented axon in the intermediate zone. Cereb Cortex 23:105–113. https://doi.org/10.1093/cercor/bhr383 CrossRefPubMed

Hevner RF (2016) Evolution of the mammalian dentate gyrus. J Comp Neurol 524:578–594. https://doi.org/10.1002/cne.23851 CrossRefPubMed

Josselyn SA, Kohler S, Frankland PW (2015) Finding the engram. Nat Rev Neurosci 16:521–534. https://doi.org/10.1038/nrn4000 CrossRefPubMed

Jossin Y, Cooper JA (2011) Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex. Nat Neurosci 14:697–703. https://doi.org/10.1038/nn.2816 CrossRefPubMedPubMedCentral

Kawauchi T (2015) Cellullar insights into cerebral cortical development: focusing on the locomotion mode of neuronal migration. Front Cell Neurosci 9:394. https://doi.org/10.3389/fncel.2015.00394 CrossRefPubMedPubMedCentral

Kempermann G (2019) Environmental enrichment, new neurons and the neurobiology of individuality. Nat Rev Neurosci 20:235–245. https://doi.org/10.1038/s41583-019-0120-x CrossRefPubMed

Kerjan G, Gleeson JG (2007) Genetic mechanisms underlying abnormal neuronal migration in classical lissencephaly. Trends Genet TIG 23:623–630. https://doi.org/10.1016/j.tig.2007.09.003 CrossRefPubMed

Kornack DR, Rakic P (1995) Radial and horizontal deployment of clonally related cells in the primate neocortex: relationship to distinct mitotic lineages. Neuron 15:311–321CrossRef

Koyama R et al (2012) GABAergic excitation after febrile seizures induces ectopic granule cells and adult epilepsy. Nat Med 18:1271–1278. https://doi.org/10.1038/nm.2850 CrossRefPubMed

Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027–2033CrossRef

LaMonica BE, Lui JH, Wang X, Kriegstein AR (2012) OSVZ progenitors in the human cortex: an updated perspective on neurodevelopmental disease. Curr Opin Neurobiol 22:747–753. https://doi.org/10.1016/j.conb.2012.03.006 CrossRefPubMedPubMedCentral

Li G, Pleasure SJ (2014) The development of hippocampal cellular assemblies Wiley interdisciplinary reviews. Dev Biol 3:165–177. https://doi.org/10.1002/wdev.127 CrossRef

Martinez-Martinez MA, Ciceri G, Espinos A, Fernandez V, Marin O, Borrell V (2018) Extensive branching of radially-migrating neurons in the mammalian cerebral cortex. J Comp Neurol. https://doi.org/10.1002/cne.24597 CrossRef

Matsue K, Minakawa S, Kashiwagi T, Toda K, Sato T, Shioda S, Seki T (2018) Dentate granule progenitor cell properties are rapidly altered soon after birth. Brain Struct Funct 223:357–369. https://doi.org/10.1007/s00429-017-1499-7 CrossRefPubMed

Moser EI, Moser MB, McNaughton BL (2017) Spatial representation in the hippocampal formation: a history. Nat Neurosci 20:1448–1464. https://doi.org/10.1038/nn.4653 CrossRefPubMed

Murakawa R, Kosaka T (1999) Diversity of the calretinin immunoreactivity in the dentate gyrus of gerbils, hamsters, guinea pigs, and laboratory shrews. J Comp Neurol 411:413–430CrossRef

Nadarajah B, Alifragis P, Wong RO, Parnavelas JG (2002) Ventricle-directed migration in the developing cerebral cortex. Nat Neurosci 5:218–224CrossRef

Nadarajah B, Alifragis P, Wong RO, Parnavelas JG (2003) Neuronal migration in the developing cerebral cortex: observations based on real-time imaging. Cereb Cortex 13:607–611CrossRef

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 483:329–340CrossRef

Nakazawa K, McHugh TJ, Wilson MA, Tonegawa S (2004) NMDA receptors, place cells and hippocampal spatial memory. Nat Rev Neurosci 5:361–372. https://doi.org/10.1038/nrn1385 CrossRefPubMed

Namba T, Huttner WB (2017) Neural progenitor cells and their role in the development and evolutionary expansion of the neocortex. WIREs Dev Biol 6:e256. https://doi.org/10.1002/wdev.256 CrossRef

Namba T, Mochizuki H, Onodera M, Mizuno Y, Namiki H, Seki T (2005) The fate of neural progenitor cells expressing astrocytic and radial glial markers in the postnatal rat dentate gyrus. Eur J Neurosci 22:1928–1941. https://doi.org/10.1111/j.1460-9568.2005.04396.x CrossRefPubMed

Namba T, Mochizuki H, Onodera M, Namiki H, Seki T (2007) Postnatal neurogenesis in hippocampal slice cultures: early in vitro labeling of neural precursor cells leads to efficient neuronal production. J Neurosci Res 85:1704–1712CrossRef

Namba T et al (2011a) NMDA receptor regulates migration of newly generated neurons in the adult hippocampus via disrupted-in-schizophrenia 1 (DISC1). J Neurochem 118:34–44. https://doi.org/10.1111/j.1471-4159.2011.07282.x CrossRefPubMedPubMedCentral

Namba T et al (2011b) Time-lapse imaging reveals symmetric neurogenic cell division of GFAP-expressing progenitors for expansion of postnatal dentate granule neurons. PLoS One 6:e25303. https://doi.org/10.1371/journal.pone.0025303 CrossRefPubMedPubMedCentral

Namba T et al (2014) Pioneering axons regulate neuronal polarization in the developing cerebral cortex. Neuron 81:814–829. https://doi.org/10.1016/j.neuron.2013.12.015 CrossRefPubMed

Namba T, Funahashi Y, Nakamuta S, Xu C, Takano T, Kaibuchi K (2015) Extracellular and intracellular signaling for neuronal polarity. Physiol Rev 95:995–1024. https://doi.org/10.1152/physrev.00025.2014 CrossRefPubMed

Nicola Z, Fabel K, Kempermann G (2015) Development of the adult neurogenic niche in the hippocampus of mice. Front Neuroanat 9:53. https://doi.org/10.3389/fnana.2015.00053 CrossRefPubMedPubMedCentral

Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409:714–720CrossRef

Nowakowski RS, Rakic P (1981) The site of origin and route and rate of migration of neurons to the hippocampal region of the rhesus monkey. J Comp Neurol 196:129–154. https://doi.org/10.1002/cne.901960110 CrossRefPubMed

Nowakowski RS, Lewin SB, Miller MW (1989) Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 18:311–318CrossRef

Rakic P, Nowakowski RS (1981) The time of origin of neurons in the hippocampal region of the rhesus monkey. J Comp Neurol 196:99–128. https://doi.org/10.1002/cne.901960109 CrossRefPubMed

Reid CB, Tavazoie SF, Walsh CA (1997) Clonal dispersion and evidence for asymmetric cell division in ferret cortex. Development 124:2441–2450PubMed

Reiner O, Sapir T (2013) LIS1 functions in normal development and disease. Curr Opin Neurobiol 23:951–956. https://doi.org/10.1016/j.conb.2013.08.001 CrossRefPubMed

Rickmann M, Amaral DG, Cowan WM (1987) Organization of radial glial cells during the development of the rat dentate gyrus. J Comp Neurol 264:449–479CrossRef

Sakakibara A, Sato T, Ando R, Noguchi N, Masaoka M, Miyata T (2014) Dynamics of centrosome translocation and microtubule organization in neocortical neurons during distinct modes of polarization. Cereb Cortex 24:1301–1310. https://doi.org/10.1093/cercor/bhs411 CrossRefPubMed

Schlessinger AR, Cowan WM, Gottlieb DI (1975) An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J Comp Neurol 159:149–175CrossRef

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 13:2351–2358CrossRef

Seki T, Arai Y (1995) Age-related production of new granule cells in the adult dentate gyrus. NeuroReport 6:2479–2482CrossRef

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. https://doi.org/10.1002/cne.21301 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. https://doi.org/10.1002/cne.23460 CrossRefPubMed

Sievers J, Hartmann D, Pehlemann FW, Berry M (1992) Development of astroglial cells in the proliferative matrices, the granule cell layer, and the hippocampal fissure of the hamster dentate gyrus. J Comp Neurol 320:1–32CrossRef

Stouffer MA, Golden JA, Francis F (2016) Neuronal migration disorders: focus on the cytoskeleton and epilepsy. Neurobiol Dis 92:18–45. https://doi.org/10.1016/j.nbd.2015.08.003 CrossRefPubMed

Suzuki A et al (2002) Feasibility of ex vivo gene therapy for neurological disorders using the new retroviral vector GCDNsap packaged in the vesicular stomatitis virus G protein. J Neurochem 82:953–960CrossRef

Tabata H, Nakajima K (2003) Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J Neurosci 23:9996–10001CrossRef

Tahirovic S, Bradke F (2009) Neuronal polarity. Cold Spring Harb Perspect Biol 1:a001644. https://doi.org/10.1101/cshperspect.a001644 CrossRefPubMedPubMedCentral

Tanaka DH et al (2009) Random walk behavior of migrating cortical interneurons in the marginal zone: time-lapse analysis in flat-mount cortex. J Neurosci 29:1300–1311. https://doi.org/10.1523/JNEUROSCI.5446-08.2009 CrossRefPubMedPubMedCentral

Toda T, Gage FH (2018) Review: adult neurogenesis contributes to hippocampal plasticity. Cell Tissue Res 373:693–709. https://doi.org/10.1007/s00441-017-2735-4 CrossRefPubMed

Valiente M, Martini FJ (2009) Migration of cortical interneurons relies on branched leading process dynamics. Cell Adhes Migr 3:278–280CrossRef

Varodayan FP, Zhu XJ, Cui XN, Porter BE (2009) Seizures increase cell proliferation in the dentate gyrus by shortening progenitor cell-cycle length. Epilepsia 50:2638–2647. https://doi.org/10.1111/j.1528-1167.2009.02244.x CrossRefPubMedPubMedCentral

Wang S et al (2018) Trajectory analysis unveils Reelin’s role in the directed migration of granule cells in the dentate gyrus. J Neurosci 38:137–148. https://doi.org/10.1523/JNEUROSCI.0988-17.2017 CrossRefPubMedPubMedCentral

Ware ML, Tavazoie SF, Reid CB, Walsh CA (1999) Coexistence of widespread clones and large radial clones in early embryonic ferret cortex. Cereb Cortex 9:636–645CrossRef

Titel: Non-radial tortuous migration with cell polarity alterations of newly generated granule neurons in the neonatal rat dentate gyrus
verfasst von: Takashi Namba
Hiroshi Shinohara
Tatsunori Seki
Publikationsdatum: 28.10.2019
Verlag: Springer Berlin Heidelberg
Erschienen in: Brain Structure and Function / Ausgabe 9/2019
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-019-01971-0

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

25.04.2024 | Hypotonie | Nachrichten

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Non-radial tortuous migration with cell polarity alterations of newly generated granule neurons in the neonatal rat dentate gyrus

Abstract

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

Demenzkranke durch Antipsychotika vielfach gefährdet

Parkinson-Therapie im Wandel – aktuelle Leitlinie im Fokus

Auf diese Krankheiten bei Geflüchteten sollten Sie vorbereitet sein

Update Neurologie

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 9/2019

Correction to: Central serotonin modulates neural responses to virtual violent actions in emotion regulation networks

White-matter microstructural properties of the corpus callosum: test–retest and repositioning effects in two parcellation schemes

The functional microscopic neuroanatomy of the human subthalamic nucleus

Cerebellar neural markers of susceptibility to social isolation and positive affective processing

Individual differences in neonatal white matter are associated with executive function at 3 years of age

A dimensional approach to jealousy reveals enhanced fronto-striatal, insula and limbic responses to angry faces

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

Demenzkranke durch Antipsychotika vielfach gefährdet

Parkinson-Therapie im Wandel – aktuelle Leitlinie im Fokus

Auf diese Krankheiten bei Geflüchteten sollten Sie vorbereitet sein

Update Neurologie