The molecular orchestra of the migration of oligodendrocyte precursors during development

doi:10.1016/j.brainresrev.2004.12.034

Brain Research Reviews

Volume 49, Issue 2, September 2005, Pages 227-241

Dedicated to Cuca Alvarado-Mallart, a warm friend, a key support, a constant scientific and personal example to everyone who worked close her, and to whom Fernando de Castro wishes to express special thanks

https://doi.org/10.1016/j.brainresrev.2004.12.034 Get rights and content

Abstract

During development of the central nervous system (CNS), postmitotic cells (including neurons and myelin-generating cells, the oligodendrocytes) migrate from the germinal areas of the neural tube where they originate to their final destination sites. The migration of neurons during development has been extensively studied and has been the topic of detailed reviews. The migration of oligodendrocyte precursor cells (OPCs) is also an extremely complex and precise event, with a widespread migration of OPCs across many regions to colonize the entire CNS. Different mechanisms have been shown to direct the migration of OPCs, among them contact-mediated mechanisms (adhesion molecules) and long-range cues (chemotropic molecules). This review provides a detailed overview and discussion of the cellular and molecular basis of OPCs migration during development. Because it has been shown that neuronal and oligodendroglial lineages share some of these mechanisms, we briefly summarize similarities and differences between these two types of neural cells. We also summarize the changes in the normal migration of OPCs during development that would be relevant for different neurological diseases (including demyelinating diseases, such as multiple sclerosis, and glial cancers). We also examine the relevance of these migratory properties of the oligondendrocytic cell lineage for the repair of neural damage.

Introduction

The complete repertoire of the functions of the adult brain results from the production of specific cell types and the migration and interconnection of both neurons and glia. These crucial events mainly occur during development. In the mammalian central nervous system (CNS), a large diversity of postmitotic cells arises from the initially totipotential–multipotential stem cells. The different cell lineages, including neurons, astrocytes, and oligodendrocytes, interact to generate what is perhaps the most complex structure in the body. To produce a structure as highly organized as the brain, there must be an elaborated sequence of migratory movements in tight combination with the establishment of an extremely precise connectivity among neuron elements [10]. It has been suggested that defects in cell migration during development may result in important pathologies, such as mental retardation, epilepsy, or schizophrenia. The cellular and molecular mechanisms underlying the migration of neurons have been the subject of extensive research over the years and many reviews have been published (recent examples of such reviews: Refs. [48], [74], [89], [90]). In contrast, even though there have been many important findings concerning the mechanisms involved in the migration of oligodendroglia, the reviews that have been published to date have focused on very specific subareas of the field (for example, see: Refs. [17], [145]). The aim of this work is to offer a broad and comprehensive review of the molecular basis of the migration of cells derived from the oligodendroglial lineage and, briefly, compare them with the developmental mechanisms involved in neuron migration. We also review the implications of these cellular and molecular mechanisms in the pathogenesis of different neurological diseases, including demyelinating pathologies such as multiple sclerosis (MS) and glial cancers. All these migratory mechanisms may well be relevant for the design of future therapies to treat these and perhaps other neurological diseases.

Section snippets

Oligodendrocytes: generalities and some clues on their early development

Oligodendrocytes are glial cells that interact in complex ways with the soma and the axon of neurons in the CNS. The most singular characteristic of these cells is their ability to form myelin sheaths (for a review, see Ref. [7]). The myelin sheath is essential for the insulation of the axon and for the saltatory conduction of electric impulses. However, there is evidence that neuron-oligodendroglia interactions may be much more complex than previously thought, as evidenced by recent studies

The migration of oligodendrocytes

In the adult, oligodendrocytes are distributed nearly homogeneously throughout the CNS, including both the white and grey matter [71], [77]. During development, these cells arise from oligodendrocyte progenitors, and subsequently precursors (OPCs), in a sequence such as that depicted in Fig. 1. OPCs originate in multiple but discrete foci along the neural tube (for specific reviews on this subject, see: Refs. [78], [112], [132], [163]). In many cases, the germinal foci for OPCs overlap

Contact-mediated mechanisms involved in the migration of oligodendrocytes

During myelination, the surface of axons plays a pivotal role in determining when and where myelination is to occur [27], [105]. For years, it was assumed that the migratory process of oligodendrocyte precursor cells was guided by preformed axonal tracts, in which case, the final destinations of oligodendrocytes would be defined by axonal topography. Given that the establishment of synapses is very precise, this hypothesis seems consistent with the precise patterns of migration followed by OPCs

Secreted molecules involved in oligodendrocyte migration

The results of a number of experiments support the idea that the migration of OPCs does not depend only on contact-mediated mechanisms, but that this migratory process could be modulated by secreted factors, in particular by secreted cues involved in the navigation of axonal growth cones and the migration of neuronal precursors. One example is the fact that OPCs migrate equally well along normal, intact rat optic nerves and also along nerves that have been transected [147]. Moreover, sectioning

Therapeutic implications of the molecular basis of oligodendroglial migration

All the scientific literature reviewed in the present work is not only relevant in the field of developmental neurobiology, but might also lead to interesting ways to design cell and substitution therapies: endogenous OPCs are present physiologically in normal adult brains (for a review, see Ref. [64]) and they can be transplanted, too. It has been observed that endogenous oligodendroglia (in general) and OPCs (in particular) proliferate strongly in response to experimental demyelination [16],

Migration of oligodendrocytes and neurons: a brief comparison

Along the present work, we have reviewed the mechanisms underlying the migration of the oligodendroglial lineage during development. Most of these mechanisms also emerge upon exploring the molecular basis of the migration of neuroblasts. A comparative summary of the mechanisms involved in the migration of neurons and oligodendrocytes is shown in Table 1. From these data, it is evident that the mechanisms are to a large degree shared. This is not surprising, since some oligodendrocytes are

Acknowledgments

Financial support (to FdeC): Fondo de Investigaciones Sanitarias-FIS (PI020768), Junta de Castilla y León (SA11/03 and SA053/04), Fundación La Caixa and Fundación Mutua Madrileña Automovilista. FdeC is a researcher contracted under the “Ramón y Cajal” Program. AB has a fellowship from the FIS (PI020768).

We are in debt to Dr. Ellen Covey for her improvement of our written English, Paloma Merchán for the general preparation of this paper, and Héctor Méndez for his help with figures.

References (167)

N.C. Bambakidis et al.
Transplantation of oligodendrocyte precursors and sonic hedgehog results in improved function and white matter sparing in the spinal cords of adult rats after contusion
Spine J.
(2004)
R. Bansal et al.
Regulation of FGF receptors in the oligodendrocyte lineage
Mol. Cell. Neurosci.
(1996)
B.A. Barres et al.
Neuronal and glial cell biology
Curr. Opin. Neurobiol.
(2000)
M.C. Birling et al.
A study of the potential of the embryonic rat telencephalon to generate oligodendrocytes
Dev. Biol.
(1998)
A.R. Calver et al.
Oligodendrocyte population dynamics and the role of PDGF in vivo
Neuron
(1998)
P.D. Canoll et al.
GGF/Neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits differentiation of oligodendrocyte progenitors
Neuron
(1996)
L. Decker et al.
Oligodendrocyte precursor migration and differentiation: combined effects of PSA residues, growth factors, and substrates
Mol. Cell. Neurosci.
(2000)
M.S. Deiner et al.
Netrin-1 and DCC mediate axon guidance locally at the optic disc: loss of function leads to optic nerve hypoplasia
Neuron
(1997)
J.P. Doyle et al.
Glial–neuron interactions and the regulation of myelin formation
Curr. Opin. Cell Biol.
(1993)
J. Ericson et al.
Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling
Cell
(1997)

N. Flames et al.

Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1

Neuron

(2004)

R.A. Fricker-Gates et al.

EGF infusion stimulates the proliferation and migration of embryonic progenitor cells transplanted in the adult rat striatum

Exp. Neurol.

(2000)

J. Gensert et al.

Endogenous progenitors remyelinate demyelinated axons in the adult CNS

Neuron

(1997)

C. Hildebrand et al.

Myelinated nerve fibres in the CNS

Prog. Neurobiol.

(1993)

H. Hu et al.

A septum-derived chemorepulsive factor for migrating olfactory interneuron precursors

Neuron

(1996)

A. Kakita et al.

Patterns and dynamics of SVZ cell migration in the postnatal forebrain: monitoring living progenitors in slice preparations

Neuron

(1999)

B.W. Kiernan et al.

Tenascin-C inhibits oligodendrocyte precursor cell migration by both adhesion-dependent and adhesion-independent mechanisms

Mol. Cell. Neurosci.

(1996)

F. Lachapelle et al.

Fibroblast growth factor-2 (FGF-2) and platelet-derived growth factor AB (PDGFAB) promote adult SVZ-derived oligodendrogenesis in vivo

Mol. Cell. Neurosci.

(2002)

J.M. Levine et al.

Activation and proliferation of endogenous oligodendrocyte precursor cells during ethidium bromide-induced demyelination

Exp. Neurol.

(1999)

J.M. Levine et al.

The oligodendrocyte precursor cell in health and disease

Trends Neurosci.

(2001)

S.W. Levison et al.

Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain

Neuron

(1993)

Q.R. Lu et al.

Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system

Neuron

(2000)

Q. Lu et al.

Ephrin-B reverse signaling is mediated by a novel PDZ-RGS protein and selectively inhibits G protein-coupled chemoattraction

Cell

(2001)

R.H. Miller

Oligodendrocyte origins

Trends Neurosci.

(1996)

R.H. Miller

Regulation of oligodendrocyte development in the vertebrate CNS

Prog. Neurobiol.

(2002)

M. Miller et al.

Myosin II distribution in neurons is consistent with a role in growth cone motility but not synaptic vesicle mobilization

Neuron

(1992)

K. Ono et al.

Focal ventricular origin and migration of oligodendrocyte precursors into the chick optic nerve

Neuron

(1997)

D.M. Orentas et al.

The origin of spinal cord oligodendrocytes is dependent on local influences from the notochord

Dev. Biol.

(1996)

V.R. Amberger et al.

Spreading and migration of human glioma and rat C6 cells on central nervous system myelin in vitro is correlated with tumor malignancy and involves a metalloproteolytic activity

Cancer Res.

(1998)

S.A. Anderson et al.

Distinct cortical migrations from the medial and lateral ganglionic eminences

Development

(2001)

R.C. Armstrong et al.

Type 1 astrocytes and oligodendrocyte-type 2 astrocyte glial progenitors migrate toward distinct molecules

J. Neurosci. Res.

(1990)

M. Baggiolini

Chemokines and leukocyte traffic

Nature

(1998)

P.V. Belichenko et al.

Relationships between oligodendrocytes and axons

NeuroReport

(1997)

A.M. Butt et al.

Three-dimensional morphology of astrocytes and oligodendrocytes in the intact mouse optic nerve

J. Neurocytol.

(1994)

A.M. Butt et al.

Biochemical subtypes of oligodendrocyte in the anterior medullary velum of the rat as revealed by the monoclonal antibody Rip

Glia

(1995)

A.M. Butt et al.

The relationship between developing oligodendrocyte units and maturing axons during myelinogenesis in the anterior medullary velum of neonatal rats

J. Neurocytol.

(1997)

W.M. Carroll et al.

Early recruitment of oligodendrocyte precursors in CNS demyelination

Brain

(1994)

R.I. Cohen et al.

A role for semaphorins and neuropilins in oligodendrocyte guidance

J. Neurochem.

(2003)

F. de Castro

Chemotropic molecules: guides for axonal pathfinding and cell migration during CNS development

News Physiol. Sci.

(2003)

MS. Deiner et al.

Altered midline axon pathways and ectopic neurons in the developing hypothalamus of netrin-1- and DCC-deficient mice

J. Neurosci.

(1999)

P. del Río Hortega

La neuroglía normal. Conceptos de neuroglioma y angioglioma

Arch. Histol. Norm. Patol.

(1942)

I.C. di Bello et al.

Generation of oligodendroglial progenitors in acute inflammatory demyelinating lesion of the rat brain stem is associated with demyelination rather than inflammation

J. Neurocytol.

(1999)

T.J. Diefenbach et al.

Stimulus history alters behavioral responses of neuronal growth cones

J. Neurosci.

(2000)

H. Ding et al.

Expression and regulation of neuropilin-1 in human astrocytoma

Int. J. Cancer

(2000)

P.B. Dirks

Glioma migration: clues from the biology of neural progenitor cells and embryonic CNS cell migration

J. Neuro-Oncol.

(2001)

M. Dubois-Dalcq et al.

Why are growth factors important in oligodendrocyte physiology?

Pathol. Biol. (Paris)

(2000)

I.F. Dunn et al.

Growth factors in glioma angiogenesis: FGFs, PDGF, EGF, a TGFs

J. Neuro-Oncol.

(2000)

M.L. Fanarraga et al.

Characterization of a putative novel type of oligodendrocyte in cultures from rat spinal cord

Eur. J. Neurosci.

(1997)

M.L. Fanarraga et al.

Oligodendrocytes are not inherently programmed to myelinate a specific size of axon

J. Comp. Neurol.

(1998)

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The impaired myelination may lead to a variety of neurological deficits and delayed nerve conductance (Nickel and Gu, 2018; Chambers and Perrone-Bizzozero, 2004). Oligodendrocyte progenitor cells (OPCs) are the source of new oligodendrocytes in the brain, which undergo extremely complex and tightly controlled sequential events of proliferation, migration and differentiation into myelin-producing cells (de Castro and Bribian, 2005). Defects in oligodendrocyte proliferation and maturation during development may result in demyelinating pathologies, such as multiple sclerosis and schizophrenia (Chambers and Perrone-Bizzozero, 2004; Dutta et al., 2011).
During the mammalian brain development, oligodendrocyte progenitor cells (OPCs) are generated from neuroepithelium and migrate throughout the brain. Myelination is a tightly regulated process which involves time framed sequential events of OPCs proliferation, migration, differentiation and interaction with axons for functional insulated sheath formation. Myelin is essential for efficient and rapid conduction of electric impulses and its loss in the hippocampus of the brain may result in impaired memory and long-term neurological deficits. Carbofuran, a carbamate pesticide is known to cause inhibition of hippocampal neurogenesis and memory dysfunctions in rats. Nonetheless, the effects of carbofuran on OPCs proliferation, fate determination, maturation/differentiation and myelination potential in the hippocampus of the rat brain are still completely elusive. Herein, we investigated the effects of sub-chronic exposure of carbofuran during two different time periods including prenatal and adult brain development in rats. We observed carbofuran hampers OPCs proliferation (BrdU incorporation) and oligodendroglial differentiation in vitro. Similar effects of carbofuran were also observed in the hippocampus region of the brain at both the time points. Carbofuran exposure resulted in reduced expression of key genes and proteins involved in the regulation of oligodendrocyte development and functional myelination. It also affects the survival of oligodendrocytes by inducing apoptotic cell death. The ultrastructural analysis of myelin architecture clearly depicted carbofuran-mediated negative effects on myelin compaction and g-ratio alteration. Conclusively, our study demonstrated that carbofuran alters myelination potential in the hippocampus, which leads to cognitive deficits in rats.

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ReviewThe molecular orchestra of the migration of oligodendrocyte precursors during development

Abstract

Introduction

Section snippets

Oligodendrocytes: generalities and some clues on their early development

The migration of oligodendrocytes

Contact-mediated mechanisms involved in the migration of oligodendrocytes

Secreted molecules involved in oligodendrocyte migration

Therapeutic implications of the molecular basis of oligodendroglial migration

Migration of oligodendrocytes and neurons: a brief comparison

Acknowledgments

Spine J.

Mol. Cell. Neurosci.

Curr. Opin. Neurobiol.

Dev. Biol.

Neuron

Neuron

Mol. Cell. Neurosci.

Neuron

Curr. Opin. Cell Biol.

Cell

Neuron

Exp. Neurol.

Neuron

Prog. Neurobiol.

Neuron

Neuron

Mol. Cell. Neurosci.

Mol. Cell. Neurosci.

Exp. Neurol.

Trends Neurosci.

Neuron

Neuron

Cell

Trends Neurosci.

Prog. Neurobiol.

Neuron

Neuron

Dev. Biol.

Spreading and migration of human glioma and rat C6 cells on central nervous system myelin in vitro is correlated with tumor malignancy and involves a metalloproteolytic activity

Cancer Res.

Distinct cortical migrations from the medial and lateral ganglionic eminences

Development

Type 1 astrocytes and oligodendrocyte-type 2 astrocyte glial progenitors migrate toward distinct molecules

J. Neurosci. Res.

Chemokines and leukocyte traffic

Nature

Relationships between oligodendrocytes and axons

NeuroReport

Three-dimensional morphology of astrocytes and oligodendrocytes in the intact mouse optic nerve

J. Neurocytol.

Biochemical subtypes of oligodendrocyte in the anterior medullary velum of the rat as revealed by the monoclonal antibody Rip

Glia

The relationship between developing oligodendrocyte units and maturing axons during myelinogenesis in the anterior medullary velum of neonatal rats

J. Neurocytol.

Early recruitment of oligodendrocyte precursors in CNS demyelination

Brain

A role for semaphorins and neuropilins in oligodendrocyte guidance

J. Neurochem.

Chemotropic molecules: guides for axonal pathfinding and cell migration during CNS development

News Physiol. Sci.

Altered midline axon pathways and ectopic neurons in the developing hypothalamus of netrin-1- and DCC-deficient mice

J. Neurosci.

La neuroglía normal. Conceptos de neuroglioma y angioglioma

Arch. Histol. Norm. Patol.

Generation of oligodendroglial progenitors in acute inflammatory demyelinating lesion of the rat brain stem is associated with demyelination rather than inflammation

J. Neurocytol.

Stimulus history alters behavioral responses of neuronal growth cones

J. Neurosci.

Expression and regulation of neuropilin-1 in human astrocytoma

Int. J. Cancer

Glioma migration: clues from the biology of neural progenitor cells and embryonic CNS cell migration

J. Neuro-Oncol.

Why are growth factors important in oligodendrocyte physiology?

Pathol. Biol. (Paris)

Growth factors in glioma angiogenesis: FGFs, PDGF, EGF, a TGFs

J. Neuro-Oncol.

Characterization of a putative novel type of oligodendrocyte in cultures from rat spinal cord

Eur. J. Neurosci.

Oligodendrocytes are not inherently programmed to myelinate a specific size of axon

Review
The molecular orchestra of the migration of oligodendrocyte precursors during development