Cell migration in the normal and pathological postnatal mammalian brain
Section snippets
Introduction: from development to the adult brain
The development of a structure as complex as the brain from the embryo to the adult organism is a continued source of fascination for neurobiologists. Successive, overlapping phases occur during brain development: first, the proliferation of embryonic neural stem cells in the ventricular neuroepithelium produces growth of the structure, second, a neurogenic phase takes place and gives rise to cortical neurons, third, gliogenesis occurs, and finally myelination, axon pruning, synaptic
Cell migration in the early postnatal period
An extensive amount of cell migration occurs in the first few postnatal weeks of the rodent brain. Much of this is by glial progenitors, since most neuronal migration has been completed by this time, with a few exceptions. Two of the exceptions, olfactory bulb interneuron generation in the forebrain SVZ and migration along the RMS, and dentate gyrus granule cell generation and migration in the hippocampus, continue to occur throughout adult life (see below). Another exception is the cerebellum,
Factors involved in the regulation of progenitor cell migration in the normal adult brain
A fundamental issue concerning adult migration is to understand the intrinsic and extracellular cues that allow the persistence of migratory progenitors. Increasing evidence argues for the involvement of developmental signals that are maintained in restricted adult brain structures. It thus appears that the adult brain uses developmental strategies in order to maintain a higher degree of plasticity permissive for cell remodeling. In the adult as in development, orientated neuronal migration
Psychiatric disorders
In the last few years, a number of studies have examined the impact of neurological pathologies on neurogenesis niches in the adult brain. They lead to the conclusion that cell proliferation and cell migration in the SVZ and DG are almost always disturbed in the diseased brain, including models of psychiatric disorders, neurodegenerative diseases or traumatic injuries. However, it is not clear whether these modifications of neurogenesis are the causes or the consequences of brain pathologies (
Therapeutic strategies and perspectives
Considering the migratory and potential migratory abilities of stem/progenitor cells, one could propose the mobilization of endogenous stem and progenitor cells as an alternative to grafting. Repair by endogenous cells would overcome the problem of transplant rejection. Despite its status of “immuno-privileged organ”, recent findings demonstrate that the brain remains sensitive to immune attacks via some activated lymphocytes and microglial cells with antigen presenting properties (Wekerle, 2007
Conclusion
The recent finding that neural stem cells reside in the adult central nervous system throughout life and present the capacity to migrate through this mature structure raised hope to develop new therapeutic strategies. However, the endogenous progenitor cell mobilization that spontaneously occurs after a lesion or in neurodegenerative pathologies only leads to very low rates of cell replacement. Transplantation strategies can be considered an interesting alternative since (i) white matter tracts
Glossary
- Neural stem cells
- Cells that reside in the neural tissue and are multipotent (can give rise to astrocytes, oligodendrocytes and neurons) and have the capacity to self renew (they divide and maintain a pool of cells identical to themselves all life long).
- Neural progenitors
- Derive from neural stem cells but present a restricted potentiality (often unipotent). Although they are proliferative cells, they present limited self-renewal potential. Here we used the term “neuroblast” to design a neuronal
References (352)
- et al.
ATP regulates oligodendrocyte progenitor migration, proliferation, and differentiation: involvement of metabotropic P2 receptors
Brain Res. Brain Res. Rev.
(2005) - et al.
The origin of remyelinating cells in the central nervous system
J. Neuroimmunol.
(1999) - et al.
Co-expression of glial fibrillary acidic protein and vimentin in reactive astrocytes following brain injury in rats
Brain Res.
(1991) - et al.
Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat
Neuroscience
(1993) - et al.
LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal
Neuron
(2002) - et al.
Migrating and myelinating potential of subventricular zone neural progenitor cells in white matter tracts of the adult rodent brain
Mol. Cell. Neurosci.
(2006) - et al.
Expression of ezrin in glial tubes in the adult subventricular zone and rostral migratory stream
Neuroscience
(2006) - et al.
Quantitative analysis of the generation of different striatal neuronal subtypes in the adult brain following excitotoxic injury
Exp. Neurol.
(2005) - et al.
Integrins: molecular determinants of glioma invasion
J. Clin. Neurosci.
(2007) - et al.
NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS
Mol. Cell. Neurosci.
(2003)
Oligodendrocyte precursor migration and differentiation: combined effects of PSA residues, growth factors, and substrates
Mol. Cell. Neurosci.
Subventricular zone astrocytes are neural stem cells in the adult mammalian brain
Cell
Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain
Cell
alpha6beta1 integrin directs migration of neuronal precursors in adult mouse forebrain
Exp. Neurol.
Granule cell dispersion is not accompanied by enhanced neurogenesis in temporal lobe epilepsy patients
Exp. Neurol.
Reelin glycoprotein in autism and schizophrenia
Int. Rev. Neurobiol.
Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces
Neuron
Down-regulation of polysialic acid is required for efficient myelin formation
J. Biol. Chem.
Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons
Neuron
Stem and progenitor cell-mediated tumor selective gene therapy
Gene Therapy
A functional role for EGFR signaling in myelination and remyelination
Nat. Neurosci.
Overexpression of the epidermal growth factor receptor confers migratory properties to nonmigratory postnatal neural progenitors
J. Neurosci.
The place of neuronal migration abnormalities in child neurology
Can. J. Neurol. Sci.
Proliferation of progenitor cells in the adult rat brain correlates with the presence of vimentin-expressing astrocytes
Glia
Turning astrocytes from the rostral migratory stream into neurons: a role for the olfactory sensory organ
J. Neurosci.
Prolonged sojourn of developing pyramidal cells in the intermediate zone of the hippocampus and their settling in the stratum pyramidale
J. Comp. Neurol.
Development of the Cerebellar System
ApoER2/VLDL receptor and Dab1 in the rostral migratory stream function in postnatal neuronal migration independently of Reelin
Proc. Natl. Acad. Sci. U.S.A.
Chemoattractive activity of sonic hedgehog in the adult subventricular zone modulates the number of neural precursors reaching the olfactory bulb
Stem Cells
Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain
Nat. Neurosci.
Type 1 astrocytes and oligodendrocyte-type 2 astrocyte glial progenitors migrate toward distinct molecules
J. Neurosci. Res.
TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination
Nat. Neurosci.
Neuronal replacement from endogenous precursors in the adult brain after stroke
Nat. Med.
Glial progenitors in adult white matter are driven to form malignant gliomas by platelet-derived growth factor-expressing retroviruses
J. Neurosci.
The duality of epidermal growth factor receptor (EGFR) signaling and neural stem cell phenotype: cell enhancer or cell transformer?
Curr. Stem Cell Res. Ther.
Dopaminergic nigrostriatal projections regulate neural precursor proliferation in the adult mouse subventricular zone
Eur. J. Neurosci.
Hedgehog signaling in the subventricular zone is required for both the maintenance of stem cells and the migration of newborn neurons
J. Neurosci.
A progressive and cell non-autonomous increase in striatal neural stem cells in the Huntington's disease R6/2 mouse
J. Neurosci.
The role of myosin ii in glioma invasion of the brain
Mol. Biol. Cell
Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons
J. Cell. Biol.
Nucleokinesis in tangentially migrating neurons comprises two alternating phases: forward migration of the Golgi/centrosome associated with centrosome splitting and myosin contraction at the rear
J. Neurosci.
Electrophysiological differentiation of new neurons in the olfactory bulb
J. Neurosci.
Chemokines regulate the migration of neural progenitors to sites of neuroinflammation
J. Neurosci.
The regulation of proliferation and differentiation in oligodendrocyte progenitor cells by alphaV integrins
Development
Beta1 integrins control the formation of cell chains in the adult rostral migratory stream
J. Neurosci.
Adenoviral brain-derived neurotrophic factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain
J. Neurosci.
Newly generated neurons in the amygdala and adjoining cortex of adult primates
Proc. Natl. Acad. Sci. U.S.A.
Increase of nestin-immunoreactive neural precursor cells in the dentate gyrus of pediatric patients with early-onset temporal lobe epilepsy
Hippocampus
GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone
J. Neurosci.
Dopamine and adult neurogenesis
J. Neurochem.
Cited by (192)
Endocannabinoids are potential inhibitors of glioblastoma multiforme proliferation
2023, Journal of Integrative MedicineNeuroblasts contribute to oligodendrocytes generation upon demyelination in the adult mouse brain
2022, iScienceCitation Excerpt :This suggests that an increased glycolytic activity, besides being important for cell fate reprogramming, may be a general feature of oligodendroglial cell identity acquisition (Gascon et al., 2016). In addition to altering the transcriptional state of a many SVZ NBs, demyelination signals also modify their migratory path by redirecting them toward the areas of damage and cell loss (Cayre et al., 2009; El Waly et al., 2014). Indeed, after lesion, NBs rapidly leave the RMS (Jin et al., 2003) and perform long-distance migration through the brain parenchyma (Cayre et al., 2009).
BKM120 alters the migration of doublecortin-positive cells in the dentate gyrus of mice
2022, Pharmacological ResearchThe Vestibular Nuclei: A Cerebral Reservoir of Stem Cells Involved in Balance Function in Normal and Pathological Conditions
2024, International Journal of Molecular SciencesMicroglial morphology in the somatosensory cortex across lifespan. A quantitative study
2023, Developmental DynamicsGlioblastoma Microenvironment and Invasiveness: New Insights and Therapeutic Targets
2023, International Journal of Molecular Sciences