Mechanisms of glial development

Current Opinion in Neurobiology

Volumn 14, Issue 1, 2004, Pages 37-44

  Colognato, Holly ^a   Ffrench Constant, Charles ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

2 ,3 cyclic nucleotide 3 phosphosdiesterase; Basic helix loop helix; BHLH; BMP; Bone morphogen protein; CNP; ERM; Family of proteins composed of Ezrin, Radixin and Moesin; GDNF; Glial derived neurotrophic factor; HA; Histone deacetylase; NCAM

Indexed keywords

CELL ADHESION MOLECULE; EZRIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; INTEGRIN; LAMININ; MOESIN; NERVE CELL ADHESION MOLECULE; NEU DIFFERENTIATION FACTOR; PLATELET DERIVED GROWTH FACTOR; RADIXIN;

ASTROCYTE; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CYTOSKELETON; GENE CONTROL; GENETIC ANALYSIS; GENETIC ASSOCIATION; GLIA CELL; HUMAN; MOTONEURON; MYELINATION; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLIGODENDROGLIA; PERIPHERAL NERVOUS SYSTEM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FAMILY; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SPINAL CORD; STEM CELL;

EID: 1342285545     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2004.01.009     Document Type: Review

References (70)

1. Kessaris N., Pringle N., Richardson W.D. Ventral neurogenesis and the neuron-glial switch. Neuron. 31:2001;677-680.
2. Lu Q.R., Sun T., Zhu Z., Ma N., Garcia M., Stiles C.D., Rowitch D.H. Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron. 25:2000;317-329.
3. Zhou Q., Wang S., Anderson D.J. Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron. 25:2000;331-343.
4. Richardson W.D., Smith H.K., Sun T., Pringle N.P., Hall A., Woodruff R. Oligodendrocyte lineage and the motor neuron connection. Glia. 29:2000;136-142.
5. Rowitch D.H., Lu Q.R., Kessaris N., Richardson W.D. An 'oligarchy' rules neural development. Trends Neurosci. 25:2002;417-422.
6. ••].
7. ••].
8. ••] use knockout technology to examine the functions of the Olig1/2 bHLH transcription factors in cell specification during CNS development. They show that Olig2 is required for oligodendrocyte and motor neuron specification in the spinal cord, with Olig1 contributing to oligodendrocyte formation in the brain but not spinal cord. In the absence of Olig2, cells that would normally form oligodendrocytes and motor neurons become respecified to produce astrocytes and V2 interneurons. Together, these papers show that the Olig genes make a necessary contribution to the combinatorial code that specifies cell fate in the CNS. They also show that distinct cells normally produce both a glial cell (the oligodendrocyte) and a neuron (motor neurons), while other cells produce astrocytes. As such, the work provides clear evidence against the concept derived from cell culture studies of a glial restricted precursor cell that forms both oligodendrocytes and astrocytes.
9. Soula C., Danesin C., Kan P., Grob M., Poncet C., Cochard P. Distinct sites of origin of oligodendrocytes and somatic motoneurons in the chick spinal cord: oligodendrocytes arise from Nkx2.2-expressing progenitors by a Shh-dependent mechanism. Development. 128:2001;1369-1379.
10. Fu H., Qi Y., Tan M., Cai J., Takebayashi H., Nakafuku M., Richardson W., Qiu M. Dual origin of spinal oligodendrocyte progenitors and evidence for the cooperative role of Olig2 and Nkx2.2 in the control of oligodendrocyte differentiation. Development. 129:2002;681-693.
11. Morrison S.J. Neuronal differentiation: proneural genes inhibit gliogenesis. Curr Biol. 11:2001;R349-R351.
12. Stolt C.C., Lommes P., Sock E., Chaboissier M.C., Schedl A., Wegner M. The Sox9 transcription factor determines glial fate choice in the developing spinal cord. Genes Dev. 17:2003;1677-1689.
13. Stolt C.C., Rehberg S., Ader M., Lommes P., Riethmacher D., Schachner M., Bartsch U., Wegner M. Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10. Genes Dev. 16:2002;165-170.
14. Kagawa T., Wada T., Ikenaka K. Regulation of oligodendrocyte development. Microsc Res Tech. 52:2001;740-745.
15. Gaiano N., Fishell G. The role of notch in promoting glial and neural stem cell fates. Annu Rev Neurosci. 25:2002;471-490.
16. Grandbarbe L., Bouissac J., Rand M., Hrabe de Angelis M., Artavanis-Tsakonas S., Mohier E. Delta-Notch signaling controls the generation of neurons/glia from neural stem cells in a stepwise process. Development. 130:2003;1391-1402.
17. Park H.C., Appel B. Delta-Notch signaling regulates oligodendrocyte specification. Development. 130:2003;3747-3755.
18. Wang S., Sdrulla A.D., diSibio G., Bush G., Nofziger D., Hicks C., Winmaster G., Barres B.A. Notch receptor activation inhibits oligodendrocyte differentiation. Neuron. 21:1998;63-75.
19. Genoud S., Lappe-Siefke C., Goebbels S., Radtke F., Aguet M., Scherer S.S., Suter U., Nave K.A., Mantei N. Notch1 control of oligodendrocyte differentiation in the spinal cord. J Cell Biol. 158:2002;709-718.
20. Hu Q.D., Ang B.T., Karsak M., Hu W.P., Cui X.Y., Duka T., Takeda Y., Chia W., Sankar N., Ng Y.K., et al. F3/Contactin acts as a functional ligand for Notch during oligodendrocyte maturation. Cell. 115:2003;163-175.
21. Grinspan J.B., Edell E., Carpio D.F., Beesley J.S., Lavy L., Pleasure D., Golden J.A. Stage-specific effects of bone morphogenetic proteins on the oligodendrocyte lineage. J Neurobiol. 43:2000;1-17.
22. Mabie P.C., Mehler M.F., Kessler J.A. Multiple roles of bone morphogenetic protein signaling in the regulation of cortical cell number and phenotype. J Neurosci. 19:1999;7077-7088.
23. Mekki-Dauriac S., Agius E., Kan P., Cochard P. Bone morphogenetic proteins negatively control oligodendrocyte precursor specification in the chick spinal cord. Development. 129:2002;5117-5130.
24. Yung S.Y., Gokhan S., Jurcsak J., Molero A.E., Abrajano J.J., Mehler M.F. Differential modulation of BMP signaling promotes the elaboration of cerebral cortical GABAergic neurons or oligodendrocytes from a common sonic hedgehog-responsive ventral forebrain progenitor species. Proc Natl Acad Sci USA. 99:2002;16273-16278.
25. Corbin J.G., Rutlin M., Gaiano N., Fishell G. Combinatorial function of the homeodomain proteins Nkx2.1 and Gsh2 in ventral telencephalic patterning. Development. 130:2003;4895-4906.
26. Pringle N.P., Yu W.P., Howell M., Colvin J.S., Ornitz D.M., Richardson W.D. Fgfr3 expression by astrocytes and their precursors: evidence that astrocytes and oligodendrocytes originate in distinct neuroepithelial domains. Development. 130:2003;93-102.
27. Oh L.Y., Denninger A., Colvin J.S., Vyas A., Tole S., Ornitz D.M., Bansal R. Fibroblast growth factor receptor 3 signaling regulates the onset of oligodendrocyte terminal differentiation. J Neurosci. 23:2003;883-894.
28. Heins N., Malatatesta P., Cecconi F., Nakafuku M., Tucker K.L., Hack M.A., Chapouton P., Barde Y.A., Gotz M. Glial cells generate neurons: the role of the transcription factor Pax6. Nat Neurosci. 5:2002;308-315.
29. Schmid R.S., McGrath B., Berechid B.E., Boyles B., Marchionni M., Sestan N., Anton E.S. Neuregulin 1-erbB2 signaling is required for the establishment of radial glia and their transformation into astrocytes in cerebral cortex. Proc Natl Acad Sci USA. 100:2003;4251-4256.
30. Patten B.A., Peyrin J.M., Weinmaster G., Corfas G. Sequential signaling through Notch1 and erbB receptors mediates radial glia differentiation. J Neurosci. 23:2003;6132-6140.
31. Malatesta P., Hack M.A., Hartfuss E., Kettenmann H., Klinkert W., Kirchhoff F., Gotz M. Neuronal or glial progeny: regional differences in radial glia fate. Neuron. 37:2003;751-764 This paper addresses the identity of the neuronal precursor cell during CNS development. Previous work has established that radial glia can divide and produce neurons, but the extent to which this occurs in normal development is unclear. To address this, the authors use a GFAP promotor to express Cre recombinase in radial glia, and cross these mice with a reporter line expressing LacZ following recombination. This technique labels all the progeny of the radial glia, and shows that most cortical projection neurons derive from these glia. By contrast, few neurons from the basal ganglia derive from radial glia, and these differences are cell-autonomous (i.e. they are also seen in cell culture). These results show, convincingly, that radial glia, once thought of as having a primary function as guidepost cells for migration neurons, are, themselves, the precursor cells for many neurons during development and form an important part of the neural stem cell pool in the CNS.
32. Belachew S., Chittajallu R., Aguirre A.A., Yuan X., Kirby M., Anderson S., Gallo V. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J Cell Biol. 161:2003;169-186 This paper examines the fate of the NG2+ proliferative precursor cell population that is present in many regions of the postnatal CNS. Previous work has suggested that this population represents restricted oligodendrocyte precursor cells. Using a transgenic mouse expressing GFP (green fluorescent protein), driven by the oligodendroglial CNP promotor (in which the majority of GFP+ cells express the NG2 marker), the authors show that these cells can generate functional neurons in vitro and that GFP+ cells that express markers of early neuronal differentiation can be seen in the hippocampus in vivo. These data add to the evidence against the concept of NG2+ cells being restricted oligodendrocyte precursor cells, and suggests that this population might also be part of the neurogenic precursor cells that are present throughout life in the CNS.
33. Mallon B.S., Shick H.E., Kidd G.J., Macklin W.B. Proteolipid promoter activity distinguishes two populations of NG2-positive cells throughout neonatal cortical development. J Neurosci. 22:2002;876-885.
34. Suzuki S.O., Goldman J.E. Multiple cell populations in the early postnatal subventricular zone take distinct migratory pathways: a dynamic study of glial and neuronal progenitor migration. J Neurosci. 23:2003;4240-4250.
35. Tsai H.H., Frost E., To V., Robinson S., ffrench-Constant C., Geertman R., Ransohoff R.M., Miller R.H. The chemokine receptor CXCR2 controls positioning of oligodendrocyte precursors in developing spinal cord by arresting their migration. Cell. 110:2002;373-383.
36. Tsai H.H., Miller R.H. Glial cell migration directed by axon guidance cues. Trends Neurosci. 25:2002;173-175.
37. Tsai H.H., Tessier-Lavigne M., Miller R.H. Netrin 1 mediates spinal cord oligodendrocyte precursor dispersal. Development. 130:2003;2095-2105.
38. Jarjour A.A., Manitt C., Moore S.W., Thompson K.M., Yuh S.J., Kennedy T.E. Netrin-1 is a chemorepellent for oligodendrocyte precursor cells in the embryonic spinal cord. J Neurosci. 23:2003;3735-3744.
39. Spassky N., de Castro F., Le Bras B., Heydon K., Queraud-LeSaux F., Bloch-Gallego E., Chedotal A., Zalc B., Thomas J.L. Directional guidance of oligodendroglial migration by class 3 semaphorins and netrin-1. J Neurosci. 22:2002;5992-6004.
40. Ye P., Li L., Richards R.G., DiAugustine R.P., D'Ercole A.J. Myelination is altered in insulin-like growth factor-I null mutant mice. J Neurosci. 22:2002;6041-6051.
41. Stevens B., Porta S., Haak L.L., Gallo V., Fields R.D. Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron. 36:2002;855-868 Electrical activity is known to promote myelination in the CNS, but the mechanisms of this axo-glial interaction have been unclear. In the PNS, ATP has been shown to play such a role. This paper shows that oligodendrocyte precursor cells respond to electrical activity in axons in vitro, by displaying a reduction in cell proliferation and enhanced differentiation. These effects were inhibited by blocking purinergic adenosine receptors, as was myelination in co-cultures with dorsal root ganglia neurons. Added adenosine also inhibits proliferation and promotes differentiation and migration. These results identify adenosine and the purinergic receptors expressed on oligodendrocyte precursor cells as an important part of activity-dependent axo-glial interactions in the CNS, and point to an interesting difference in axo-glial signaling between the CNS and PNS.
42. Nakahara J., Tan-Takeuchi K., Seiwa C., Gotoh M., Kaifu T., Ujike A., Inui M., Yagi T., Ogawa M., Aiso S., Takai T., Asou H. Signaling via immunoglobulin Fc receptors induces oligodendrocyte precursor cell differentiation. Dev Cell. 4:2003;841-852.
43. Kim J.Y., Sun Q., Oglesbee M., Yoon S.O. The role of ErbB2 signaling in the onset of terminal differentiation of oligodendrocytes in vivo. J Neurosci. 23:2003;5561-5571.
44. Marin-Husstege M., Muggironi M., Liu A., Casaccia-Bonnefil P. Histone deacetylase activity is necessary for oligodendrocyte lineage progression. J Neurosci. 22:2002;10333-10345 Modifications to chromatin structure and consequent changes in gene repression are an important part of the mechanisms by which cells adopt neuronal or non-neuronal fates in CNS development. This paper shows that the later stages of oligodendrocyte differentiation also involve chromatin remodeling, as histone deacetylase (HA) activity is associated with differentiation, and inhibitors of HA prevent differentiation. Because HA causes chromatin compaction (turning genes off or rendering binding sites inaccessible), the consequences of HA activity during normal differentiation may be inhibition of the binding of a repressor of differentiation. As such, the paper adds an important new mechanism to the regulation of oligodendrocyte development.
45. Cosgaya J.M., Chan J.R., Shooter E.M. The neurotrophin receptor p75NTR as a positive modulator of myelination. Science. 298:2002;1245-1248.
46. McTigue D.M., Horner P.J., Stokes B.T., Gage F.H. Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J Neurosci. 18:1998;5354-5365.
47. Chan J.R., Cosgaya J.M., Wu Y.J., Shooter E.M. Neurotrophins are key mediators of the myelination program in the peripheral nervous system. Proc Natl Acad Sci USA. 98:2001;14661-14668.
48. Nickols J.C., Valentine W., Kanwal S., Carter B.D. Activation of the transcription factor NF-kappaB in Schwann cells is required for peripheral myelin formation. Nat Neurosci. 6:2003;161-167.
49. Jaegle M., Ghazvini M., Mandemakers W., Piirsoo M., Driegen S., Levavasseur F., Raghoenath S., Grosveld F., Meijer D. The POU proteins Brn-2 and Oct-6 share important functions in Schwann cell development. Genes Dev. 17:2003;1380-1391.
50. Patton B.L. Laminins of the neuromuscular system. Microsc Res Tech. 51:2000;247-261.
51. Previtali S.C., Nodari A., Taveggia C., Pardini C., Dina G., Villa A., Wrabetz L., Quattrini A., Feltri M.L. Expression of laminin receptors in Schwann cell differentiation: evidence for distinct roles. J Neurosci. 23:2003;5520-5530.
52. Feltri M.L., Graus Porta D., Previtali S.C., Nodari A., Migliavacca B., Cassetti A., Littlewood-Evans A., Reichardt L.F., Messing A., Quattrini A., et al. Conditional disruption of beta 1 integrin in Schwann cells impedes interactions with axons. J Cell Biol. 156:2002;199-209 Extracellular matrix molecules of the laminin family are required for normal myelination, as demonstrated by dysmyelination in mice and humans lacking the laminin-α2 subunit found in laminin-2 (merosin), -4 and -12. To identify the receptors involved, this paper uses a conditional knockout strategy to remove β1 integrin from differentiating Schwann cells (so overcoming the early embryonic lethality of the β1 knockout mouse) and shows a necessary role for β1 integrins in Schwann cell process formation and axon sorting, during myelination. Surprisingly, some cells do myelinate normally and no effects are seen on cell proliferation and survival, although this might reflect the late stage at which the β1 gene was excised when using the P0 promotor to drive cre recombinase expression. The results, therefore, clearly demonstrate a necessary role for β1 integrins (which contain several laminin receptors) in PNS myelination.
53. •]), as well as between the glial cell and the overlying basal lamina.
54. Gatto C.L., Walker B.J., Lambert S. Local ERM activation and dynamic growth cones at Schwann cell tips implicated in efficient formation of nodes of Ranvier. J Cell Biol. 162:2003;489-498.
55. Fernandez-Valle C., Tang Y., Ricard J., Rodenas-Ruano A., Taylor A., Hackler E., Biggerstaff J., Iacovelli J. Paxillin binds schwannomin and regulates its density-dependent localization and effect on cell morphology. Nat Genet. 31:2002;354-362.
56. Colognato H., Baron W., Avellana-Adalid V., Relvas J.B., Baron-Van Evercooren A., Georges-Labouesse E., ffrench-Constant C. CNS integrins switch growth factor signalling to promote target-dependent survival. Nat Cell Biol. 4:2002;833-841 This paper examines the role of α6β1 integrin laminin receptors in CNS myelination. The authors confirm previous reports of axon-associated laminin alpha2 expression and then use α6 integrin knockout mice to show increased oligodendrocyte cell death and reduced differentiation when oligodendrocyte interaction with this laminin is perturbed by the loss of the integrin receptor. Potential mechanisms, dependent on integrin-growth factor interactions, are revealed by the amplification of PDGF survival signaling and the switching of neuregulin survival signaling from a PI3K pathway that inhibits differentiation to a MAPK pathway that promotes differentiation. In this way, the integrin mediates a classic target-dependent survival mechanism for the regulation of oligodendrocyte numbers and also provides a mechanism for the spatial regulation of growth factor signaling that ensures that differentiation only occurs in the appropriate context of axonal contact.
57. Gudz T.I., Schneider T.E., Haas T.A., Macklin W.B. Myelin proteolipid protein forms a complex with integrins and may participate in integrin receptor signaling in oligodendrocytes. J Neurosci. 22:2002;7398-7407.
58. Chun S.J., Rasband M.N., Sidman R.L., Habib A.A., Vartanian T. Integrin-linked kinase is required for laminin-2-induced oligodendrocyte cell spreading and CNS myelination. J Cell Biol. 163:2003;397-408.
59. Baron W., Shattil S.J., ffrench-Constant C. The oligodendrocyte precursor mitogen PDGF stimulates proliferation by activation of alpha(v)beta3 integrins. EMBO J. 21:2002;1957-1966.
60. Baron W., Decker L., Colognato H., ffrench-Constant C. Regulation of integrin growth factor interactions in oligodendrocytes by lipid raft microdomains. Curr Biol. 13:2003;151-155.
61. Paratcha G., Ledda F., Ibanez C.F. The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell. 113:2003;867-879 A traditional view of the cell-surface molecule NCAM is that it is an adhesion molecule that is involved in close-range cell-cell interactions via a homophilic binding mechanism. Here, the authors show that one NCAM isoform, NCAM140, binds the neurotrophic factor GDNF and initiates downstream signaling in association with the GDNF family receptor GFR1α. This results in decreased homophilic NCAM-mediated adhesion, increased cell migration and enhanced axon outgrowth in cell culture. Mice lacking the GFR1α show a similar migration-defective phenotype to the NCAM knockout in the rostral migratory stream, consistent with a role for a GDNF/GFR1α/NCAM interaction in this migration. This paper, therefore, provides an illustration of how cell-surface adhesion receptors can have a wider role in the integration of both short- and long-range cues in the regulation of cell behavior.
62. Campbell K., Gotz M. Radial glia: multi-purpose cells for vertebrate brain development. Trends Neurosci. 25:2002;235-238.
63. D'Arcangelo G., Miao G.G., Chen S.C., Soares H.D., Morgan J.I., Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature. 374:1995;719-723.
64. Georges-Labouesse E., Mark M., Messaddeq N., Gansmuller A. Essential role of alpha 6 integrins in cortical and retinal lamination. Curr Biol. 8:1998;983-986.
65. Graus-Porta D., Blaess S., Senften M., Littlewood-Evans A., Damsky C., Huang Z., Orban P., Klein R., Schittny J.C., Muller U. Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron. 31:2001;367-379.
66. Hartfuss E., Forster E., Bock H.H., Hack M.A., Leprince P., Luque J.M., Herz J., Frotscher M., Gotz M. Reelin signaling directly affects radial glia morphology and biochemical maturation. Development. 130:2003;4597-4609.
67. Forster E., Tielsch A., Saum B., Weiss K.H., Johanssen C., Graus-Porta D., Muller U., Frotscher M. Reelin, Disabled 1, and beta 1 integrins are required for the formation of the radial glial scaffold in the hippocampus. Proc Natl Acad Sci USA. 99:2002;13178-13183.
68. Lappe-Siefke C., Goebbels S., Gravel M., Nicksch E., Lee J., Braun P.E., Griffiths I.R., Nave K.A. Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet. 33:2003;366-374 Mice that lack CNP, an enzyme that is highly expressed in oligodendrocytes, show marked axonal degeneration but no abnormalities of myelin sheath development and structure. This gives a clear example of how the glial cell provides essential trophic support for the axon, independently of the integrity of the myelin sheath. It is of particular relevance to multiple sclerosis, where the chronic progressive nature of the disease is thought to result from axonal degeneration that is secondary to long-term demyelination and the failure of remyelination.
69. Chen S., Rio C., Ji R.R., Dikkes P., Coggeshall R.E., Woolf C.J., Corfas G. Disruption of ErbB receptor signaling in adult non-myelinating Schwann cells causes progressive sensory loss. Nat Neurosci. 6:2003;1186-1193.
70. Mathis C., Collin L., Borrelli E. Oligodendrocyte ablation impairs cerebellum development. Development. 130:2003;4709-4718.