Neural System - Glial Development

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Introduction

Neural Development timeline
Neural Development

The term gliogenesis refers to the development of the many different types of glial cells within the developing and adult nervous system (CNS and PNS) including: radial glia, astrocytes, oligodendrocytes, Schwann cells, and microglia. Within the neural tube stem cells generate the 2 major classes of cells that make the majority of the nervous system: neurons and most CNS glia. Both these classes of cells differentiate into many different types generated with highly specialized functions and shapes.


Glia (Greek, glia = "glue") and neurons have the same general embryonic origin, generated from neural tube ventricular layer stem cells and neural crest. The developmental process of glial cell development is described as gliogenesis. Glial cells have important roles in neural development and in the adult nervous system and have come a long way from their original description as "supportive cells".


Myelination is the process of close wrapping around a neural axon by a glial cell. This second process occurs as a late feature of glial and nervous system development in both the central and peripheral nervous system and has mainly been studied in relation to demyelinating diseases, such as multiple sclerosis.


Glia Types: radial glia | astroglia | oligodendroglia | microglia | Schwann cell radial glia, astroglia, oligodendroglia, microglia and Schwann cells.


Development of the neural crest and sensory systems (hearing/vision/smell) are only briefly introduced in these notes and are covered in detail in another notes sections. (More? neural crest | sensory).


Neural Links: neural | ventricular | ectoderm | Stage 22 | gliogenesis | neural fetal | Medicine Lecture - Neural | Lecture - Ectoderm | Lecture - Neural Crest | Lab - Early Neural | neural crest | Sensory | neural abnormalities | folic acid | iodine deficiency | Fetal Alcohol Syndrome | Postnatal | Postnatal - Neural Examination | Histology | Historic Neural | Category:Neural
Neural Crest Development | Sensory System Development

Some Recent Findings

  • Emx2 and Foxg1 inhibit gliogenesis and promote neuronogenesis[1] " Neural stem cells (NSCs) give rise to all cell types forming the cortex: neurons, astrocytes, and oligodendrocytes. The transition from the former to the latter ones takes place via lineage-restricted progenitors in a highly regulated way."
  • A common progenitor for retinal astrocytes and oligodendrocytes[2] "Here we use retroviruses to label clones of glial cells in the chick retina. We found that almost every clone had both astrocytes and oligodendrocytes. In addition, we discovered a novel glial cell type, with features intermediate between those of astrocytes and oligodendrocytes, which we have named the diacyte. Diacytes also share a progenitor cell with both astrocytes and oligodendrocytes."
  • Neural Stem Cell Differentiation[3] "Upon evaluating distinct growth-permissive substrates in an embryonic stem cell-neurogenesis assay, we found that laminin, fibronectin, and gelatin instruct neural fate and alter the functional specification of neurons when applied at distinct stages of development." (More? Stem Cells )
More recent papers  
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This table shows an automated computer PubMed search using the listed sub-heading term.

  • Therefore the list of references do not reflect any editorial selection of material based on content or relevance.
  • References appear in this list based upon the date of the actual page viewing.

References listed on the rest of the content page and the associated discussion page (listed under the publication year sub-headings) do include some editorial selection based upon both relevance and availability.

Links: References | Discussion Page | Pubmed Most Recent | Journal Searches


Search term: Glial Embryology

Xiaoxiao Wang, Wenxin Zhuang, Wenyu Fu, Xiaocui Wang, E Lv, Fengjie Li, Shuanhu Zhou, Wolf-Dieter Rausch, Xin Wang The lentiviral-mediated Nurr1 genetic engineering mesenchymal stem cells protect dopaminergic neurons in a rat model of Parkinson's disease. Am J Transl Res: 2018, 10(6);1583-1599 PubMed 30018702

Mihály Kálmán, Erzsébet Oszwald, Károly Pócsai, Zsolt Bagyura, István Adorján Disappearance of cerebrovascular laminin immunoreactivity as related to the maturation of astroglia in rat brain. Int. J. Dev. Neurosci.: 2018; PubMed 30009882

M Grobe, G Kretzschmar, A Vuica, N Filipovic Expression of vitamin D receptors in the superior cervical ganglia of rats. Biotech Histochem: 2018;1-8 PubMed 29954226

Mihály Kálmán, Erzsébet Oszwald, István Adorján Appearance of β-dystroglycan precedes the formation of glio-vascular end-feet in developing rat brain. Eur J Histochem: 2018, 62(2);2908 PubMed 29943956

Jinkun Wen, Dandan Tan, Lixia Li, Xianghai Wang, Mengjie Pan, Jiasong Guo RhoA regulates Schwann cell differentiation through JNK pathway. Exp. Neurol.: 2018; PubMed 29940159


Search term: Radial Glia

Yuto Ueda, Yuki Shimizu, Nobuyuki Shimizu, Tohru Ishitani, Toshio Ohshima Involvement of Sonic hedgehog and Notch signaling in regenerative neurogenesis in adult zebrafish optic tectum after stab injury. J. Comp. Neurol.: 2018; PubMed 30014463

Mihály Kálmán, Erzsébet Oszwald, Károly Pócsai, Zsolt Bagyura, István Adorján Disappearance of cerebrovascular laminin immunoreactivity as related to the maturation of astroglia in rat brain. Int. J. Dev. Neurosci.: 2018; PubMed 30009882

José-Manuel Baizabal, Meeta Mistry, Miguel Turrero García, Nicolás Gómez, Olubusola Olukoya, Diana Tran, Matthew B Johnson, Christopher A Walsh, Corey C Harwell The Epigenetic State of PRDM16-Regulated Enhancers in Radial Glia Controls Cortical Neuron Position. Neuron: 2018, 99(1);239-241 PubMed 30001508

Adrián Cárdenas, Ana Villalba, Camino de Juan Romero, Esther Picó, Christina Kyrousi, Athanasia C Tzika, Marc Tessier-Lavigne, Le Ma, Micha Drukker, Silvia Cappello, Víctor Borrell Evolution of Cortical Neurogenesis in Amniotes Controlled by Robo Signaling Levels. Cell: 2018; PubMed 29961574

Yuto Watanabe, Takumi Kawaue, Takaki Miyata Differentiating cells mechanically limit progenitor cells' interkinetic nuclear migration to secure apical cytogenesis. Development: 2018; PubMed 29945866

Radial Glia

Interneuron-radial glial interactions[4]

Radial glia were historically identified by Wilhelm His in 1880's studies of the human fetal brain using classical Golgi silver impregnation histology and were postulated to have a role in the developing central nervous system. It was not until Paso Rakic's much later studies in the 1970's[5][6] (see review[7]) that this roel was confirmed. These cells have an important role in nervous system development, guiding newly formed neurons from their birth zone (ventricular layer) outward to their final adult position. Radial glia generate initially neurons then astrocytes after neurogenesis has been completed.[8][9]

At about 19 weeks (GA 21 weeks) neuronal migration ends and the radial glial cells that aided the migration now become transformed into astrocytes and astrocytic precursors.[10]


Links: PubMed - Pasko Rakic

Astroglia

Astrocytes and neonatal hypoxia ischemia.[11]

Astrocytes are glial cells named by their "star-like" branching appearance, and are the most abundant cells in the brain. They form a key component of the blood-brain barrier and the transfer of circulating nutrients to neurons.

Blood-Brain Barrier

Blood-brain barrier cartoon

Blood-brain barrier cartoon[12]

A layer of brain endothelial cells connected by tight junctions forms the blood-brain barrier (BBB). The intimate contact of these specialized endothelial cells with different cell types constitutes the neurovascular unit (NVU).
  • Basement membrane embeds the brain endothelial cells, the pericytes, and astrocytes.
  • Brain endothelial cells and pericytes connect through peg-socket junctions in areas where the basement membrane is absent.
  • Glial astrocytes extend end-feet and establish a close interaction with endothelial cells through transmembrane proteins, such as aquaporins.
  • Astrocytes also connect with pericytes and neurons and together regulate BBB maintenance and function.


Terms

  • aquaporins - transmembrane proteins that form channels for water and small solutes transfer across the membrane.
  • astrocytes - glial cells named by their "star-like" branching appearance, are the most abundant cells in the brain.
  • basement membrane - specialised extracellular matrix that underlies all epithelia.
  • end-feet - specialised cellular club-shaped endings, often associated with neural synapses, but also found in other cell junctions.
  • endothelial cells - squamous epithelial cells that line all blood vessels.
  • pericytes - (Rouget cells) cells located at the abluminal surface of microvessels close to endothelial cells, mainly found associated with CNS vessels and involved in vessel formation, remodeling and stabilization.

See reviews:

  • Steindler DA, Laywell ED.] Astrocytes as stem cells: nomenclature, phenotype, and translation.[13]
  • Scemes E, Giaume C. Astrocyte calcium waves: what they are and what they do. [14]

Oligodendroglia

In the early spinal cord, a ventral ventricular zone region generates oligodendrocyte precursors initially which then migrate both laterally and dorsally.

In the later spinal cord, the dorsal region provides a secondary source of oligodendrocyte precursors.

Oligodendrocyte wars. Richardson WD, Kessaris N, Pringle N. Nat Rev Neurosci. 2006 Jan;7(1):11-8. Review.

Baron W, Colognato H, ffrench-Constant C. Integrin-growth factor interactions as regulators of oligodendroglial development and function. Glia. 2005 Mar;49(4):467-79. Review.

Microglia

Glial cells that act within the central nervous system in the same role as macrophages in other body tissues and act as an innate immune system. There other role is as the cellular mediators of neuroinflammatory processes[15] and cell death[16]. In the mouse embryo, these cells derive from you sac progenitor cells migrating and then proliferating within the CNS.[17][18]

Schwann cells

Schwann cell myelination and dedifferentiation[19]

These cells are named after Theodor Schwann (1810 - 1882), a German physiologist and histologist, who along with Schleiden were early developers of the "cell theory". Neural crest cells differentiate to form the glial lineage, which in turn generate Schwann cell precursors. (More? Neural Crest Development).

Schwann cells formation is regulated by at least two signals, neuregulin-1 and endothelin. Neuregulins are a family (NRG1, NRG2, NRG3, and NRG4) of EGF-like signaling molecules that bind ErbB receptor tyrosine kinase receptors. Neuregulin-1 type III is expressed on axon surface and has been shown to also regulate Schwann cell membrane growth, adjusting myelin sheath thickness to match axonal calibre.

Mouse-sciatic nerve Schwann cell.jpg

Mouse - sciatic nerve Schwann cell interaction[20]


Links: Neural Crest Development

Development Overview

Human Neuralation - Early Stages

The stages below refer to specific Carneigie stages of development.

  • stage 8 (about 18 postovulatory days) neural groove and folds are first seen
  • stage 9 the three main divisions of the brain, which are not cerebral vesicles, can be distinguished while the neural groove is still completely open.
  • stage 10 (two days later) neural folds begin to fuse near the junction between brain and spinal cord, when neural crest cells are arising mainly from the neural ectoderm
  • stage 11 (about 24 days) the rostral (or cephalic) neuropore closes within a few hours
    • closure is bidirectional
    • it takes place from the dorsal and terminal lips and may occur in several areas simultaneously
    • The two lips, however, behave differently.
  • stage 12 (about 26 days) The caudal neuropore takes a day to close
    • the level of final closure is approximately at future somitic pair 31
    • corresponds to the level of sacral vertebra 2
  • stage 13 (4 weeks) the neural tube is normally completely closed
  • Secondary neurulation begins at stage 12
    • is the differentiation of the caudal part of the neural tube from the caudal eminence (or end-bud) without the intermediate phase of a neural plate.

(Text modified from: Neurulation in the normal human embryo. O'Rahilly R, Muller F Ciba Found Symp 1994;181:70-82)


Spinal Cord Glia

Radial glia, astrocytes, oligodendrocytes and microglia have been reported in the human spinal cord from the end of the embryonic period (GA week 10).

Table data below from an imnuohistological study of the human fetal spinal cord.[21]

week GA week Staining Location
10 12 vimentin-positive radial glia radial glia present at all three levels of the spinal cord
13 15 vimentin-positive processes radially arranged in the white matter astrocytes (GFAP+) obvious in the anterior and anterolateral funiculi
18 20 gradients of glial fibrillary acidic protein and vimentin expression difficult to discern microglia more abundant in white matter than grey matter

Fetal - Third Trimester

Three-dimensional magnetic resonance imaging and image-processing algorithms have been used to quantitate between 29-41 weeks volumes of: total brain, cerebral gray matter, unmyelinated white matter, myelinated, and cerebrospinal fluid (grey matter- mainly neuronal cell bodies; white matter- mainly neural processes and glia). A study of 78 premature and mature newborns showed that total brain tissue volume increased linearly over this period at a rate of 22 ml/week. Total grey matter also showed a linear increase in relative intracranial volume of approximately 1.4% or 15 ml/week. The rapid increase in total grey matter is mainly due to a fourfold increase in cortical grey matter. Quantification of extracerebral and intraventricular CSF was found to change only minimally.[22]

Neural-development.jpg

Myelination

The electron micrograph images below are selected neural tissues of adult mouse axon cross-sections surrounded by glial-derived myelin (black rings).

Links: http://www.ncbi.nlm.nih.gov/bookshelf/br.fcgi?book=bnchm&part=A244

Postnatal Neural

Neural development continues after birth with substantial growth, death and reorganization occuring during the postnatally. (More? Postnatal Development - Neural) The references below give a sample of some recent findings and research methods.

Cortex Matures Faster in Youth with Highest IQ (More? NIH - Cortex Matures Faster in Youth with Highest IQ)

  • Neural induction: old problem, new findings, yet more questions.[23] "During neural induction, the embryonic neural plate is specified and set aside from other parts of the ectoderm. A popular molecular explanation is the 'default model' of neural induction, which proposes that ectodermal cells give rise to neural plate if they receive no signals at all, while BMP activity directs them to become epidermis. However, neural induction now appears to be more complex than once thought, and can no longer be fully explained by the default model alone. This review summarizes neural induction events in different species and highlights some unanswered questions about this important developmental process."
  • Diffusion tensor imaging of neurodevelopment in children and young adults.[24] "Diffusion tensor magnetic resonance imaging (DTI) was used to study regional changes in the brain's development from childhood (8-12 years, mean 11.1 +/- 1.3, N = 32) to young adulthood (21-27 years, mean 24.4 +/- 1.8, N = 28). ..... These findings suggest a continuation of the brain's microstructural development through adolescence."

Abnormalities

Multiple Sclerosis

  • Activation of the subventricular zone in multiple sclerosis: evidence for early glial progenitors.[25]"In multiple sclerosis (MS), oligodendrocyte and myelin destruction lead to demyelination with subsequent axonal loss. Experimental demyelination in rodents has highlighted the activation of the subventricular zone (SVZ) and the involvement of progenitor cells expressing the polysialylated form of neural cell adhesion molecule (PSA-NCAM) in the repair process."

Experimental Autoimmune Encephalomyelitis

(EAE) This is an animal model of autoimmune demyelination, such as in multiple sclerosis (MS).[26]

Nogo (= Reticulon 4, RTN4, Neurite Growth Inhibitor 220) one of several myelin-associated proteins with inhibitory effects for neuronal neurite outgrowth. Nogo exists as 3 splice transcript variants (NOGO-A, NOGO-B and NOGO-C) which are differentially expressed in the developing central nervous system. Also associated with autoimmune demyelination, shown in models of multiple sclerosis (MS) such as experimental autoimmune encephalomyelitis (EAE).

Nogo-A myelin-associated protein which can inhibit neurite outgrowth and prevent regeneration in the adult central nervous system. Secreted by oligodendrocytes in the central nervous system, but not by Schwann cells in the peripheral nervous system. (More? OMIM - Reticulon 4)

Glioma

References

  1. Brancaccio M, Pivetta C, Granzotto M, Filippis C & Mallamaci A. (2010). Emx2 and Foxg1 inhibit gliogenesis and promote neuronogenesis. Stem Cells , 28, 1206-18. PMID: 20506244 DOI.
  2. Rompani SB & Cepko CL. (2010). A common progenitor for retinal astrocytes and oligodendrocytes. J. Neurosci. , 30, 4970-80. PMID: 20371817 DOI.
  3. Goetz AK, Scheffler B, Chen HX, Wang S, Suslov O, Xiang H, Brüstle O, Roper SN & Steindler DA. (2006). Temporally restricted substrate interactions direct fate and specification of neural precursors derived from embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. , 103, 11063-8. PMID: 16832065 DOI.
  4. Yokota Y, Gashghaei HT, Han C, Watson H, Campbell KJ & Anton ES. (2007). Radial glial dependent and independent dynamics of interneuronal migration in the developing cerebral cortex. PLoS ONE , 2, e794. PMID: 17726524 DOI.
  5. Rakic P. (1971). Guidance of neurons migrating to the fetal monkey neocortex. Brain Res. , 33, 471-6. PMID: 5002632
  6. Rakic P. (1972). Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. , 145, 61-83. PMID: 4624784 DOI.
  7. Rakic P. (2003). Elusive radial glial cells: historical and evolutionary perspective. Glia , 43, 19-32. PMID: 12761862 DOI.
  8. Kriegstein AR & Götz M. (2003). Radial glia diversity: a matter of cell fate. Glia , 43, 37-43. PMID: 12761864 DOI.
  9. Nadarajah B. (2003). Radial glia and somal translocation of radial neurons in the developing cerebral cortex. Glia , 43, 33-6. PMID: 12761863 DOI.
  10. Kadhim HJ, Gadisseux JF & Evrard P. (1988). Topographical and cytological evolution of the glial phase during prenatal development of the human brain: histochemical and electron microscopic study. J. Neuropathol. Exp. Neurol. , 47, 166-88. PMID: 3339373
  11. Bain JM, Ziegler A, Yang Z, Levison SW & Sen E. (2010). TGFbeta1 stimulates the over-production of white matter astrocytes from precursors of the "brain marrow" in a rodent model of neonatal encephalopathy. PLoS ONE , 5, e9567. PMID: 20221422 DOI.
  12. Haddad-Tóvolli R, Dragano NRV, Ramalho AFS & Velloso LA. (2017). Development and Function of the Blood-Brain Barrier in the Context of Metabolic Control. Front Neurosci , 11, 224. PMID: 28484368 DOI.
  13. Steindler DA & Laywell ED. (2003). Astrocytes as stem cells: nomenclature, phenotype, and translation. Glia , 43, 62-9. PMID: 12761868 DOI.
  14. Scemes E & Giaume C. (2006). Astrocyte calcium waves: what they are and what they do. Glia , 54, 716-25. PMID: 17006900 DOI.
  15. Streit WJ, Mrak RE & Griffin WS. (2004). Microglia and neuroinflammation: a pathological perspective. J Neuroinflammation , 1, 14. PMID: 15285801 DOI.
  16. Bessis A, Béchade C, Bernard D & Roumier A. (2007). Microglial control of neuronal death and synaptic properties. Glia , 55, 233-8. PMID: 17106878 DOI.
  17. Alliot F, Godin I & Pessac B. (1999). Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain. Brain Res. Dev. Brain Res. , 117, 145-52. PMID: 10567732
  18. Pont-Lezica L, Béchade C, Belarif-Cantaut Y, Pascual O & Bessis A. (2011). Physiological roles of microglia during development. J. Neurochem. , 119, 901-8. PMID: 21951310 DOI.
  19. Salzer JL. (2008). Switching myelination on and off. J. Cell Biol. , 181, 575-7. PMID: 18490509 DOI.
  20. Chan JR. (2007). Myelination: all about Rac 'n' roll. J. Cell Biol. , 177, 953-5. PMID: 17576794 DOI.
  21. Weidenheim KM, Epshteyn I, Rashbaum WK & Lyman WD. (1994). Patterns of glial development in the human foetal spinal cord during the late first and second trimester. J. Neurocytol. , 23, 343-53. PMID: 7522270
  22. Hüppi PS, Warfield S, Kikinis R, Barnes PD, Zientara GP, Jolesz FA, Tsuji MK & Volpe JJ. (1998). Quantitative magnetic resonance imaging of brain development in premature and mature newborns. Ann. Neurol. , 43, 224-35. PMID: 9485064 DOI.
  23. Stern CD. (2005). Neural induction: old problem, new findings, yet more questions. Development , 132, 2007-21. PMID: 15829523 DOI.
  24. Matsuoka T, Ahlberg PE, Kessaris N, Iannarelli P, Dennehy U, Richardson WD, McMahon AP & Koentges G. (2005). Neural crest origins of the neck and shoulder. Nature , 436, 347-55. PMID: 16034409 DOI.
  25. Nait-Oumesmar B, Picard-Riera N, Kerninon C, Decker L, Seilhean D, Höglinger GU, Hirsch EC, Reynolds R & Baron-Van Evercooren A. (2007). Activation of the subventricular zone in multiple sclerosis: evidence for early glial progenitors. Proc. Natl. Acad. Sci. U.S.A. , 104, 4694-9. PMID: 17360586 DOI.
  26. Gold R, Linington C & Lassmann H. (2006). Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain , 129, 1953-71. PMID: 16632554 DOI.

Journals

Online Textbooks

Developmental Biology (6th ed) Gilbert, Scott F. Sunderland (MA): Sinauer Associates, Inc.; c2000. Formation of the Neural Tube | Differentiation of the Neural Tube | Tissue Architecture of the Central Nervous System | Neuronal Types | Snapshot Summary: Central Nervous System and Epidermis

Neuroscience Purves, Dale; Augustine, George J.; Fitzpatrick, David; Katz, Lawrence C.; LaMantia, Anthony-Samuel; McNamara, James O.; Williams, S. Mark. Sunderland (MA): Sinauer Associates, Inc. ; c2001 Early Brain Development | Construction of Neural Circuits | Modification of Brain Circuits as a Result of Experience

Molecular Biology of the Cell (4th Edn) Alberts, Bruce; Johnson, Alexander; Lewis, Julian; Raff, Martin; Roberts, Keith; Walter, Peter. New York: Garland Publishing; 2002. The three phases of neural development |

Search NLM Online Textbooks- "glial development" : Developmental Biology | Neuroscience | The Cell- A molecular Approach | Molecular Biology of the Cell | Endocrinology

Reviews

Götz M & Huttner WB. (2005). The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. , 6, 777-88. PMID: 16314867 DOI.

Greene ND & Copp AJ. (2009). Development of the vertebrate central nervous system: formation of the neural tube. Prenat. Diagn. , 29, 303-11. PMID: 19206138 DOI.

Articles

Saitsu H & Shiota K. (2008). Involvement of the axially condensed tail bud mesenchyme in normal and abnormal human posterior neural tube development. Congenit Anom (Kyoto) , 48, 1-6. PMID: 18230116 DOI.

Ogata T, Yamamoto S, Nakamura K & Tanaka S. (2006). Signaling axis in schwann cell proliferation and differentiation. Mol. Neurobiol. , 33, 51-62. PMID: 16388110

Jessen KR & Mirsky R. (2002). Signals that determine Schwann cell identity. J. Anat. , 200, 367-76. PMID: 12090403

Weidenheim KM, Epshteyn I, Rashbaum WK & Lyman WD. (1994). Patterns of glial development in the human foetal spinal cord during the late first and second trimester. J. Neurocytol. , 23, 343-53. PMID: 7522270

Search PubMed

Search Pubmed: Gliogenesis | Glial Development | Myelination

Historic

Schwann T (1839) Mikroskopische Untersuchungen über die Uebereinstimmung in der Struktur und dem Wachsthum der Thiere und Pflanzen

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Cite this page: Hill, M.A. (2018, July 20) Embryology Neural System - Glial Development. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Neural_System_-_Glial_Development

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