Cellular Migration and Formation of Axons and Dendrites: Comprehensive Developmental Neuroscience

Cellular Migration and Formation of Axons and Dendrites
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Contributors
1. Development of neuronal polarity in vivo
	1.1 Introduction
	1.2 Axon initiation in vitro versus in vivo
		1.2.1 Axon initiation in vitro
		1.2.2 Axon initiation in vivo
	1.3 Distinction between cues regulating axon specification versus axon growth
	1.4 Extracellular cues regulating neuronal polarization and axon initiation
		1.4.1 Netrin-1 and Wnt control axon initiation in Caenorhabditis elegans
		1.4.2 Polarized emergence of the axon in retinal ganglion cells of Xenopus
		1.4.3 Extracellular cues underlying the emergence of axon and dendrites in mammalian neurons
	1.5 Intracellular pathways underlying neuronal polarization
		1.5.1 Role of protein degradation and local translation in axon specification and axon growth
		1.5.2 Role of cytoskeletal dynamics in axon initiation and growth
		1.5.3 Major signaling pathways involved in axon initiation and growth
			1.5.3.1 LKB1 and its downstream kinases SAD-A/B and MARK1-4
			1.5.3.2 PAR3-PAR6-APKC
			1.5.3.3 Ras- and Rho-family of small GTPases
			1.5.3.4 PI3K and PTEN signaling during axon specification
			1.5.3.5 AKT/protein kinase B
			1.5.3.6 GSK3 and axon specification
	1.6 Conclusion and future directions
	References
2. Role of the cytoskeleton and membrane trafficking in axon-dendrite morphogenesis
	2.1 Introduction
	2.2 Developmental stages
	2.3 Role of cytoskeleton in establishment of neuronal polarity
		2.3.1 Actin
		2.3.2 Actin dynamics during axon formation
		2.3.3 Microtubules
		2.3.4 Microtubules dynamics during axon formation
		2.3.5 Cytoskeletal dynamics during dendritic growth and arborization
		2.3.6 Subcellular cytoskeletal specializations
	2.4 The role of (membrane) trafficking during neuronal polarization
		2.4.1 Trafficking during early neuronal development
		2.4.2 Motor protein-based transport in axons and dendrites
		2.4.3 The secretory and endosomal pathway
		2.4.4 RNA transport and local translation
		2.4.5 Barriers for the segregation of functional domains
		2.4.6 Protein stabilization and degradation
	2.5 Maintaining neuronal polarity
	2.6 Future work on neuronal morphogenesis
	References
3. Axon growth and branching
	3.1 Introduction
	3.2 Cell biological mechanisms
		3.2.1 Growth cones: structure and function
		3.2.2 Regulation of cytoskeleton assembly
			3.2.2.1 Actin
			3.2.2.2 Microtubules
		3.2.3 Interaction between F-actin and microtubules
		3.2.4 Membrane trafficking and axonal transport
		3.2.5 Protein translation and stability
	3.3 Extracellular regulation of axon growth and branching during neural development
		3.3.1 Nerve growth factor and neurotrophic factors
		3.3.2 Guidance molecules: netrin, slit, semaphorin, ephrin, and wnt
		3.3.3 Cell adhesion molecules: permissive or instructive
		3.3.4 Glial cells and myelination
		3.3.5 Neural activity
		3.3.6 Additional axon branching molecules
	3.4 Intracellular signaling mechanisms that mediate axon growth and branching
		3.4.1 Rho family small GTPases: linking receptors to the cytoskeleton
		3.4.2 Calcium
		3.4.3 Cyclic nucleotides as second messengers and modulators
	3.5 Concluding remarks
	References
4. Axon guidance: Netrins
	4.1 Introduction
	4.2 Netrins and their receptors
		4.2.1 Netrin discovery and structure
		4.2.2 Netrin receptors
		4.2.3 Interactions with other signaling systems
		4.2.4 Netrin functional domains and interactions with receptors
	4.3 Netrin function in axon guidance and cell migration
		4.3.1 Mammalian spinal cord
			4.3.1.1 Guidance by midline-derived Netrin-1 in the spinal cord
			4.3.1.2 Guidance by ventricular zone-derived Netrin-1 in the spinal cord
			4.3.1.3 Synergy between Netrin-1 from floor plate and from ventricular zone in the spinal cord
			4.3.1.4 Interpreting the guidance defects caused by loss of Netrin-1 in the spinal cord
		4.3.2 Mammalian hindbrain
			4.3.2.1 In hindbrain, Netrin-1 from ventricular zone is more important than from floor plate
			4.3.2.2 Control of neuronal cell migration by Netrin-1 in the hindbrain
		4.3.3 Guidance of other classes of mammalian axons and cells: attraction, repulsion, and modulation
		4.3.4 Invertebrate systems
			4.3.4.1 Attraction and repulsion by UNC-6 in Caenorhabditis Elegans
			4.3.4.2 Attraction and repulsion by Netrins in Drosophila
	4.4 Beyond axon and cell guidance: additional roles for Netrins in the nervous system
	4.5 Involvement of Netrin signaling in disorders of the nervous system
	4.6 Netrins: players outside the nervous system
	4.7 Conclusion
	References
5. Axon guidance: semaphorin/neuropilin/plexin signaling
	5.1 Introduction
	5.2 Structural features
	5.3 Mechanisms of intracellular signaling
	5.4 Function in neural circuit development
	5.5 Semaphorins, plexins, and neuropilins in neurological disorders
		5.5.1 Autism spectrum disorder
		5.5.2 Kallmann\'s syndrome
		5.5.3 Amyotrophic lateral sclerosis
		5.5.4 Late-onset neurodegenerative diseases
	5.6 Conclusions and perspectives
	References
6. Ephrin/Eph signaling in axon guidance
	6.1 The setting of the play
		6.1.1 Ephs and ephrins
		6.1.2 Rules of interaction
		6.1.3 Fundamental action modes
		6.1.4 Phylogeny
	6.2 Mechanisms of ephrin/Eph signaling in axon guidance
		6.2.1 Biophysical aspects
			6.2.1.1 Membrane distribution
			6.2.1.2 Cis interactions
			6.2.1.3 Trafficking
		6.2.2 Biochemical aspects
			6.2.2.1 Signal transduction of forward signaling
			6.2.2.2 Signal transduction of reverse signaling
	6.3 Ephrins and Ephs in invertebrate axon guidance
		6.3.1 Caenorhabditis elegans
		6.3.2 Insects
	6.4 Binary ephrin/Eph signaling-pathfinding
		6.4.1 Peripheral pathfinding-limb bud innervation
		6.4.2 Pathfinding in the spinal cord
		6.4.3 Pathfinding in the brain stem-auditory system
		6.4.4 Central pathfinding
			6.4.4.1 Optic chiasm
			6.4.4.2 Corpus callosum and anterior commissure
	6.5 Proportional ephrin/Eph signaling-mapping
		6.5.1 Olfactory wiring
		6.5.2 Retinotectal/retinocollicular projection
			6.5.2.1 Mechanisms of mapping along the anterior-posterior axis
			6.5.2.2 Mechanisms of mapping along the dorsoventral axis
			6.5.2.3 Computational modeling
		6.5.3 Retinogeniculate projections
		6.5.4 Thalamocortical projections
		6.5.5 Corticocollicular projections
	6.6 Ephrins and Ephs in regeneration
	6.7 Perspectives and open questions-``curtain down and nothing settled\'\'
	Acknowledgments
	References
7. Axon guidance: Slit-Robo signaling
	7.1 Introduction
	7.2 Slits and their receptors
		7.2.1 Slit discovery and structure
		7.2.2 Identification of the slit receptor robo
		7.2.3 Slit and Robo interactions
			7.2.3.1 Regulation of Slit-Robo interactions
	7.3 Slit-Robo function in midline crossing
		7.3.1 Spatial expression patterns of Slit and Robo
		7.3.2 Posttranscriptional Robo regulation
		7.3.3 Regulation of Robo protein expression at the midline
			7.3.3.1 Drosophila and vertebrate midlines
			7.3.3.2 Caenorhabditis elegans midline
		7.3.4 Regulation of Robo signaling at the midline in vertebrates
		7.3.5 Slit-Robo signaling for exiting the midline
	7.4 Modulation of Slit-Robo signaling
		7.4.1 Transcriptional control
		7.4.2 Regulation of Slit-Robo signaling by metalloprotease cleavage
		7.4.3 Regulation of Slit-Robo signaling by ubiquitination
	7.5 Signaling downstream of Robo
		7.5.1 Rho family of small GTPases
		7.5.2 Abelson tyrosine kinase
		7.5.3 Actin-interacting proteins
	7.6 Beyond the midline: additional roles for Slit-Robo in the nervous system
		7.6.1 Lateral positioning
		7.6.2 Cell migration and cell polarity
		7.6.3 Dendritic and axonal outgrowth and branching
	7.7 Slit-Robo contribution to axon targeting in a complex target field
	7.8 Involvement of Slit-Robo in disorders of the nervous system
	7.9 Conclusion
	References
8. Nonconventional axon guidance cues: Hedgehog, TGF-β/BMP, and Wnts in axon guidance
	8.1 Introduction
		8.1.1 Morphogens as axon guidance cues
	8.2 Sonic hedgehog in axon guidance
		8.2.1 Canonical Shh signaling
		8.2.2 Shh is a chemoattractant for spinal cord commissural axons
		8.2.3 Shh binding to Boc attracts commissural axons through a noncanonical signaling pathway to modulate the growth cone cytoskeleton
		8.2.4 Shh guides axons along the longitudinal axis of the spinal cord
		8.2.5 14-3-3 proteins regulate a cell-intrinsic switch from Shh-mediated attraction to repulsion of commissural axons after midli ...
		8.2.6 Shh guides contralateral and ipsilateral retinal ganglion cell axons
		8.2.7 Shh is a chemoattractant for midbrain dopaminergic axons
		8.2.8 Shh binding to Gas1 repels enteric axons
	8.3 TGF-β superfamily members in axon guidance
		8.3.1 Canonical bone morphogenetic protein signaling
		8.3.2 BMP7:GDF7 repels spinal cord commissural axons
	8.4 Wnts in axon guidance
		8.4.1 Canonical and noncanonical Wnt signaling
		8.4.2 Wnt5 repels commissural axons from the Drosophila posterior commissure via derailed, a Ryk tyrosine kinase family member
		8.4.3 Wnt5, complexed with derailed, repels Drosophila mushroom body axons
		8.4.4 Wnt binding to Ryk repels axons of the corticospinal tract and corpus callosum through a Ca2+-dependent mechanism
		8.4.5 Wnt binding to Fz attracts postcrossing commissural axons via protein kinase C ζ and planar cell polarity signaling
		8.4.6 Wnt binding to Fz regulates dopaminergic axon guidance through planar cell polarity signaling
		8.4.7 Wnt3 mediates mediolateral retinotectal topographic mapping
		8.4.8 Wnts guide axons of Caenorhabditis elegans mechanosensory neurons and D-type motoneurons via Fz-type receptors
		8.4.9 The Wnt ligand CWN2 regulates Caenorhabditis elegans motor neuron axon guidance through a Ror-type receptor CAM-1
	8.5 Cross-talk between axon guidance cues
		8.5.1 Shh induces the response of commissural axons to semaphorin repulsion during midline crossing
		8.5.2 Shh regulates Wnt signaling in postcrossing commissural axons
		8.5.3 The TGF-β family member unc-129 regulates Unc6/Netrin signaling in Caenorhabditis elegans
	8.6 Conclusions and perspectives
	List of Acronyms and Abbreviations
	Glossary
	Acknowledgments
	References
9. Axon regeneration
	9.1 Introduction
	9.2 Anatomy of the spinal cord
	9.3 Spinal cord injury repair: a complex problem
	9.4 Axon regeneration in the injured central nervous system versus peripheral nervous system
		9.4.1 Intrinsic mechanisms of dorsal root ganglion neuron axon regeneration
	9.5 Extrinsic mechanisms: inhibitors of central nervous system axon regeneration
	9.6 Extrinsic mechanisms: growth factors
		9.6.1 The anatomical substrate of neurorepair
	9.7 Axon regeneration in the retinofugal system
	9.8 Lessons learned from an evolutionary perspective
		9.8.1 Immune-mediated neurorepair mechanisms
	9.9 Conclusions
	Acknowledgments
	References
10. Axon maintenance and degeneration
	10.1 Introduction
	10.2 Essentials of axonal transport in axon maintenance
		10.2.1 Cellular components that are transported along the axons
		10.2.2 Regulations of microtubule stability and organization during axon maintenance
		10.2.3 Defects in motor proteins cause axon degeneration
		10.2.4 Role of mitochondria transport in axon maintenance
		10.2.5 Membrane transport and insertion are essential for axon maintenance
	10.3 Proteasome and autophagy pathways in axonal homeostasis
		10.3.1 Ubiquitin-proteasome system in axon maintenance
		10.3.2 Role of autophagy/lysosome pathway in maintaining axonal homeostasis
	10.4 Role of glial cells in axon maintenance
	10.5 Maintaining axon track positions and other structural features
	10.6 Axon pruning and axon degeneration
		10.6.1 Developmental axon pruning
		10.6.2 Pathological axon degeneration
		10.6.3 Molecular mechanisms of pathological axon degeneration
	References
11. Dendrite development: invertebrates
	11.1 Structure and anatomy of invertebrate dendrites
	11.2 Methods for studying dendrite morphology in Drosophila
	11.3 Anatomical background for key model systems in which dendritic morphogenesis is studied in invertebrates
		11.3.1 Drosophila dendritic arborization sensory neurons
		11.3.2 Drosophila motoneurons
		11.3.3 Drosophila olfactory projection neurons
		11.3.4 Caenorhabditis elegans PVD neurons
	11.4 Cell biology of dendritic growth
		11.4.1 Microtubule polarity differs between dendrites and axons
		11.4.2 Dynein-dependent trafficking controls dendritic branching
		11.4.3 Role of the secretory pathway and Golgi outposts in dendritic elaboration
	11.5 Transcriptional control of dendritic morphology
		11.5.1 Control of dendrite morphological identity of Drosophila PNS neurons
		11.5.2 Transcriptional control of dendritic targeting of olfactory PNs
		11.5.3 Chromatin remodeling factors and dendritic development
	11.6 Posttranscriptional control of dendritic development
		11.6.1 Control of mRNA translation in dendritic development
		11.6.2 miRNAs in dendritic development
	11.7 Control of dendritic field formation I: guidance and targeting
		11.7.1 Slit and netrin signaling during midline dendritic guidance
		11.7.2 A combinatorial ligand-receptor complex guides dendritic branches
		11.7.3 Coarse and specific control of PN dendritic targeting
		11.7.4 Glial control of dendritic targeting
	11.8 Control of dendritic field formation II: dendritic self-avoidance and tiling
		11.8.1 Interactions between dendrites generate evenly covered territories
			11.8.1.1 Dendritic self-avoidance
			11.8.1.2 Dendritic tiling
		11.8.2 Scaling growth of arbors and maintenance of evenly covered territories
	11.9 Dendritic remodeling
		11.9.1 Transforming growth factor-β signaling and ecdysone receptor expression during dendritic remodeling
		11.9.2 Sox14 and mical function downstream of ecdysone receptor
		11.9.3 Signaling mechanisms for dendritic pruning
			11.9.3.1 Ubiquitin-proteasome system
			11.9.3.2 Caspases
		11.9.4 The cell biology of dendritic pruning
			11.9.4.1 Microtubule disassembly
			11.9.4.2 Local endocytosis and compartmentalized calcium transients
		11.9.5 Similarities between dendrite pruning and injury-induced axon degeneration
		11.9.6 Similarities and differences in dendrite development, dendrite regrowth after pruning, and dendrite regeneration after injury
	11.10 Concluding remarks
	See also
	References
12. Dendrite development: vertebrates
	12.1 The structure and function of vertebrate dendrites
		12.1.1 Methods for manipulating and studying dendrite morphology in vertebrates
	12.2 The cell biology of dendritic growth
		12.2.1 Regulators of the microtubule network in dendrite formation
		12.2.2 Regulators of the actin cytoskeleton
		12.2.3 Dendrite elaboration requires a satellite secretory pathway
		12.2.4 RNA translation in dendrites
		12.2.5 Powering dendrite growth
		12.2.6 Intracellular cascades that translate extrinsic signals into changes in dendrite structure
	12.3 Control of dendritic field formation I: size
		12.3.1 Afferent-derived neurotrophins limit size
		12.3.2 Control of arbor size by neurotransmission
		12.3.3 Activity-dependent mechanisms that influence dendrite growth and stabilization
	12.4 Control of dendritic field formation II: shape
		12.4.1 Apical dendrite initiation and outgrowth of cortical pyramidal neurons
		12.4.2 Activity-dependent orientation of dendrite growth in the somatosensory cortex
		12.4.3 Positional cues shape asymmetric dendritic arbors in the mouse retina
	12.5 Control of dendritic field formation III: targeting and synapse selectivity
		12.5.1 Formation of a Proto-IPL by retinal amacrine cells
		12.5.2 Laminar targeting of retinal dendrites is coordinated by adhesive and repellent cues
		12.5.3 Transcriptional control of laminar-specific targeting of dendrites in retina
		12.5.4 Local recognition mechanisms to control synapse selectivity
		12.5.5 An integrated, multistep model for synaptic wiring in the retina IPL
	12.6 Space-filling mechanisms to optimize dendritic field distribution
		12.6.1 Tiling and mosaics
		12.6.2 Dendrite self-avoidance
	12.7 Emergence of dendrite compartmentalization
		12.7.1 Subcellular patterning of synaptic inputs along dendritic domains
		12.7.2 Patterning the membrane excitability of dendritic compartments
	12.8 Neurodevelopmental disorders: the price of poor dendritic development?
	12.9 Conclusion
	Abbreviations
	Acknowledgments
	References
13. Cell polarity and initiation of migration
	13.1 Introduction
	13.2 Migratory behaviors during radial migration in the developing cerebral cortex
		13.2.1 Bipolar migrating neurons along the radial glial fibers: locomotion
		13.2.2 Radial glial fiber-independent mode of migration: somal translocation and terminal translocation
		13.2.3 Multipolar migration
		13.2.4 Transformation from multipolar migrating neurons to bipolar locomoting neurons
		13.2.5 Departure from the ventricular zone: differences in migratory behavior between direct progeny of the apical progenitors in  ...
		13.2.6 Behaviors of the progenitor cells in the subventricular zone
	13.3 Molecular mechanisms that regulate the initiation of migration and cell polarity during migration
		13.3.1 Coupling between neuronal differentiation and migration
		13.3.2 Controlling the initiation of radial migration
		13.3.3 Regulation of multipolar migration
		13.3.4 Extracellular molecules that affect migrating cells
	13.4 Conclusion
	See also
	List of abbreviations
	Glossary
	Supplementary data
	References
14. Nucleokinesis
	14.1 Nucleokinesis: introduction
	14.2 The nucleus
		14.2.1 The nuclear membrane and nuclear pores
	14.3 Chromatin
	14.4 Membraneless organelles in the nucleus
	14.5 Higher order structure of the nucleus
	14.6 Diseases
		14.6.1 Cohesinopathies
		14.6.2 Affecting the nuclear envelope
	14.7 Interactions between the nucleus and the cytoskeleton
		14.7.1 The LINC complex, structure
	14.8 The LINC complex, function
	14.9 The LINC complex in nuclear positioning
	14.10 The link between the nucleus and the centrosome
	14.11 The LINC complex in nucleokinesis
	14.12 Nucleokinesis during interkinetic nuclear movement
	14.13 Microtubule binding motors
		14.13.1 Dynein
		14.13.2 Kinesin Kif1a
	14.14 Cytoskeleton dynamics as nuclear drivers
	14.15 Collective mechanisms for nuclear migration
		14.15.1 Intercellular signaling
		14.15.2 Mechanical interactions
	14.16 The role of INM during neurodevelopment
	14.17 INM summary
	14.18 Conclusions and future directions
	Acknowledgments
	References
15. Radial migration in the developing cerebral cortex
	15.1 Introduction
	15.2 Production of cortical projection neurons
	15.3 Organization of the neocortex
	15.4 Trajectory of migrating neurons in the developing brain
	15.5 Modes of migration
	15.6 Radial migration in the developing human neocortex
	15.7 Factors that regulate the radial migration of cortical neurons
		15.7.1 Secreted molecules
			15.7.1.1 Reelin
			15.7.1.2 Semaphorins
		15.7.2 Neurotransmitters
			15.7.2.1 GABA
			15.7.2.2 Glutamate
			15.7.2.3 ATP
		15.7.3 Adhesion molecules
			15.7.3.1 Integrins
			15.7.3.2 Gap junctions
		15.7.4 Cytoskeletal regulators
			15.7.4.1 Lis1
			15.7.4.2 Doublecortin
			15.7.4.3 Filamin A (FLNA/FLN1)
			15.7.4.4 Cdk5
		15.7.5 Transcription factors
			15.7.5.1 Pax6
			15.7.5.2 Tbr2
			15.7.5.3 Neurogenins
	15.8 Summary
	References
16. Mechanisms of tangential migration of interneurons in the developing forebrain
	16.1 Birth of distinct interneuron subtypes and onset of their migration from the subpallium
	16.2 Molecular cues drawing the path of cortical interneuron migration
	16.3 Molecular cues controlling the integration of interneurons into the cortical migratory streams
	16.4 Molecular cues controlling the intracortical dispersion of interneurons
	16.5 Signals dictating the arrest of interneuron migration within the cortical wall
	16.6 Role of subpallial transcription factors in the tangential migration of interneurons into the cortex
	16.7 Cell-intrinsic regulation of cortical interneuron migration
	16.8 Dynamic remodeling of the cytoskeleton during interneuron migration
	16.9 Regulation of the tangential migration of interneurons in the rostral migratory stream to the olfactory bulb
	16.10 Molecular regulation of the migration of striatal interneurons
	16.11 Evolutionary perspective of the tangential migration
	16.12 Conclusions and perspectives
	List of acronyms and abbreviations
	References
17. Migration in the hippocampus
	17.1 Overview of hippocampal structure and lamination
		17.1.1 Terminology important for studying hippocampal structure
	17.2 Developmental specification of hippocampal fields
		17.2.1 The basic developmental scheme of the hippocampus
		17.2.2 The cortical hem
		17.2.3 The cortical hem organizes the hippocampal fields
		17.2.4 The role of canonical Wnt signaling in hippocampal development
	17.3 Migration of Cajal-Retzius cells in the hippocampus
		17.3.1 What are Cajal-Retzius cells?
		17.3.2 What are the functions of Cajal-Retzius cells?
		17.3.3 What are the origins of Cajal-Retzius cells?
		17.3.4 The cortical hem is the major source of Cajal-Retzius cells for the dorsal telencephalon
		17.3.5 The extent of the cortex covered by hem-derived Cajal-Retzius cells
		17.3.6 Recruitment of hem-derived Cajal-Retzius cells to the meninges
		17.3.7 Tangential dispersion of Cajal-Retzius cells in the marginal zone
	17.4 Migration of hippocampal pyramidal neurons
	17.5 Migration of hippocampal interneurons
		17.5.1 Cellular and distributional diversity of interneurons in the hippocampus
		17.5.2 Origins and migration of hippocampal interneurons
	17.6 Migration of neural progenitors and granule cells in the dentate gyrus during development
		17.6.1 The basic developmental scheme of the dentate gyrus
		17.6.2 Migration of granule neurons to form the granule cell layer
		17.6.3 Emergence and migration of long-lived neural stem cells and establishment of subgranular zone
	17.7 Conclusions
	References
18. Hindbrain tangential migration
	18.1 Introduction
	18.2 Tangential migration: a historical overview
	18.3 Molecular mechanisms controlling the tangential migration of precerebellar neurons
		18.3.1 Influence of the midline on tangentially migrating precerebellar neurons
		18.3.2 Why do PCN neurons migrate near the pial surface?
	18.4 Molecular mechanisms controlling the tangential migration of facial motor neurons
		18.4.1 Origin and migration of facial motor neurons
		18.4.2 The caudal migration of FBM neurons
			18.4.2.1 The planar cell polarity pathway
			18.4.2.2 Other molecules controlling FBM caudal migration
		18.4.3 Role of chemoattraction and chemorepulsion
		18.4.4 Role of the meninges in the tangential migration of FBM neurons
	18.5 Ending tangential migration
	18.6 Conclusion
	Acknowledgments
	References
19. Neuronal migration in the developing cerebellar system
	19.1 Introduction
		19.1.1 Part I. Diverse migration pathways and guidance cues during cerebellar system development
			19.1.1.1 Distinct cerebellar germinal zones: the ventricular zone and rhombic lip
				19.1.1.1.1 Early patterning
				19.1.1.1.2 The rhombic lip and Atoh1 domain define the glutamatergic lineage
				19.1.1.1.3 The ventricular zone and Ptf1a domain define the GABAergic lineage
				19.1.1.1.4 Other Rh1 derivatives
			19.1.1.2 Migration of purkinje cells
			19.1.1.3 Migration of minor ventricular zone derivatives: Pax2-positive interneurons, basket cells, golgi cells, and stellate cells
			19.1.1.4 Migration of precerebellar nuclei
			19.1.1.5 Migration of upper rhombic lip derivatives
				19.1.1.5.1 Deep cerebellar nuclei
				19.1.1.5.2 Granule neuron progenitors and cerebellar granule neurons
				19.1.1.5.3 Unipolar brush cells
		19.1.2 Part II. The cytoskeletal organization of cerebellar granule neurons
			19.1.2.1 Cerebellar granule neuron migration diversity after the establishment of the secondary germinal zone
			19.1.2.2 The road to the two-stroke motility paradigm
			19.1.2.3 The roles of the microtubule cytoskeleton and associated motors
			19.1.2.4 The role of the actin cytoskeleton
			19.1.2.5 The role of microtubule-actin cross talk
		19.1.3 Part III. The facets of cerebellar granule neuron polarity: timing cell recognition, differentiation, germinal zone exit, a ...
			19.1.3.1 Cerebellar granule neuron recognition/adhesion: the contribution of astrotactins and the siah2-Pard3-JamC pathway
			19.1.3.2 The Zeb1-Pard6/3A transcriptional pathway
			19.1.3.3 The foxo polarization pathway
		19.1.4 Part IV. Migration deficits in cerebellar medulloblastomas: the effects of perturbed migration pathways are no longer limit ...
	Acknowledgments
	References
20. Neuronal migration of guidepost cells
	Chapters cited
	20.1 An introduction to guidepost cells
		20.1.1 Neuronal migration in the context of axonal tracts formation
		20.1.2 Defining the notion of guidepost cells
	20.2 Role of neuronal migration in the formation of the lateral olfactory tract
		20.2.1 Anatomy and development of the lateral olfactory tract
		20.2.2 Diffusible guidance cues in the pathfinding of lateral olfactory tract axons
		20.2.3 Roles of guidepost ``lot cells\'\'
		20.2.4 Tangential migration of lot cells: specification, routes, and molecular mechanisms
		20.2.5 Fate of lot cells
	20.3 Hippocampal Cajal-retzius cells in the formation of axonal connections
		20.3.1 Anatomy and development of the hippocampus and entorhinohippocampal projections
		20.3.2 Cajal-Retzius cells as putative guidepost neurons for the formation of entorhinal projections
		20.3.3 Toward a more generic role of Cajal-Retzius cells as guideposts?
	20.4 Migration of neuronal guidepost cells in the formation of thalamocortical connections
		20.4.1 Anatomy and development of thalamocortical and corticofugal axons
		20.4.2 Pioneer cortical subplate axons in the pathfinding of thalamocortical projections
		20.4.3 Origin and migration of subplate neurons
		20.4.4 The subpallium is a major intermediate target for thalamocortical axons
		20.4.5 Guidepost cells in the diencephalic and subpallial pathfinding of thalamocortical projections
		20.4.6 Migration of guidepost corridor cells: routes and guidance cues
		20.4.7 Fate of guidepost cells for thalamocortical projections
	20.5 Neuronal migration of guidepost cells in the formation of the corpus callosum
		20.5.1 Anatomy and development of the corpus callosum
		20.5.2 Roles of glial cells in the development of the corpus callosum
		20.5.3 Tangentially migrating neurons in the development of the corpus callosum
	20.6 Neuronal migration of guidepost cells and evolution of brain wiring
		20.6.1 Tangential migration of guidepost neurons: a hallmark of the telencephalon?
		20.6.2 Neuronal migration of guidepost cells in the evolution of the internal capsule
	20.7 Towards an integration of migrating guidepost neurons in normal and pathological brain development
		20.7.1 Guidepost neurons in the shaping of axonal tract organization and topography
		20.7.2 Integrating tangential neuronal migration of guideposts in normal and pathological brain development
	20.8 Conclusions
	References
21. Neuronal migration in the postnatal brain
	21.1 Introduction
	21.2 Regulation of neuronal migration in the normal brain
		21.2.1 Migratory scaffolds
			21.2.1.1 Neighboring cells in the neuronal chain
			21.2.1.2 Astrocytes
			21.2.1.3 Blood vessels
		21.2.2 Directional control from the V-SVZ toward the OB
		21.2.3 Migration termination in the OB
	21.3 Regulation of neuronal migration in the injured brain
		21.3.1 Migratory scaffolds in the injured brain
			21.3.1.1 Neighboring cells in the neuronal chain
			21.3.1.2 Astrocytes
			21.3.1.3 Blood vessels
			21.3.1.4 Radial glial cells
		21.3.2 Directional control toward a lesion
		21.3.3 Enhancement of neuronal migration as a strategy for endogenous neuronal regeneration
	21.4 Postnatal neuronal migration in primates
	21.5 Summary
	References
22. Transcriptional and posttranscriptional mechanisms of neuronal migration
	22.1 Introduction to neuronal migration
		22.1.1 Different ways to migrate: ``I did it my way\'\'
	22.2 Transcriptional and posttranscriptional control of neuronal migration
		22.2.1 Radial migration
			22.2.1.1 Radial migration: locomotion
			22.2.1.2 Radial migration: translocation
			22.2.1.3 Subtypes of neocortical radial glia; outer radial glia and the somal translocation mode of migration
				22.2.1.3.1 Interplay of transcription factors and radial migration guidance cues
				22.2.1.3.2 Posttranscriptional events in radial migration: the role of RNA-binding proteins, microRNA, and long noncoding RNA
			22.2.1.4 RNA-binding proteins
			22.2.1.5 lncRNAs
			22.2.1.6 MicroRNAs
		22.2.2 Tangential migration: transcriptional and posttranscriptional control
			22.2.2.1 Interplay of transcription factors and tangential migration guidance cues
				22.2.2.1.1 Posttranscriptional events in tangential migration: the role of RNA-binding proteins and microRNA
	22.3 Conclusion and future directions
	List of acronyms and abbreviations
	References
23. Migration of myelin-forming cells in the CNS
	23.1 Introduction
		23.1.1 Genesis of myelin-producing cells during development
		23.1.2 Oligodendrocyte precursor cells: born to migrate
	23.2 Migratory paths followed by oligodendrocyte progenitor and precursor cells
	23.3 Chemokinetic factors: the motility of oligodendrocyte precursors
	23.4 Adhesion and chemotactic mechanisms: how the movement of oligodendrocyte precursors is guided?
		23.4.1 Adhesion and surface molecules
		23.4.2 Secreted factors
	23.5 Concluding remarks
	Acknowledgments
	References
24. Coordination of different modes of neuronal migration and functional organization of the cerebral cortex
	24.1 Introduction
		24.1.1 Arealization of the cortex
		24.1.2 Cortical columns constitute cortical areas
		24.1.3 Minicolumns constitute columns
	24.2 Migration of related projection neurons into the same minicolumn
		24.2.1 Early lack of evidence that sister projection neurons migrate into the same minicolumn
		24.2.2 Sister projection neurons migrate into the same minicolumn and intersynapse
	24.3 Integration of projection neurons into cortical minicolumns
		24.3.1 Migratory scaffolds restrict tangential movement of projection neurons
		24.3.2 Molecular signaling limits tangential movement of projection neurons during multipolar stage
	24.4 Integration of interneurons into cortical columns
		24.4.1 Interneuron subtypes areally distribute via tangential migration
		24.4.2 Do sister interneurons migrate into the same minicolumn?
		24.4.3 Sister interneurons preferentially intersynapse
		24.4.4 Regulating the timing of the shift from tangential to radial migration
		24.4.5 Projection neurons attract migrating interneurons into cortical plate
		24.4.6 Radial glial cells trigger a shift in migration mode
	24.5 Genetic and cellular mechanisms controlling shifts in migratory modes
	24.6 Conclusion
	List of abbreviations
	References
25. The impact of different modes of neuronal migration on brain evolution
	25.1 Types of neuronal migration in vertebrate brain development-radial and tangential migration shaping vertebrate brains
	25.2 The impact of radial migration on brain evolution
		25.2.1 Evolution of radial migration
		25.2.2 Radial migration on laminar brains
		25.2.3 Radial migration on elaborated brains
		25.2.4 The influence of radial migration on pallial internal circuitry
			25.2.4.1 Somal translocation
			25.2.4.2 Glial-guided locomotion
			25.2.4.3 Evolutionary origin of glial-aided locomotion
	25.3 The impact of tangential migration on brain evolution
		25.3.1 Pallial interneurons and the modulation of brain circuits
			25.3.1.1 Conserved features of tangential migration of pallial interneurons in vertebrates
			25.3.1.2 Divergence in tangential migratory routes of pallial interneurons
			25.3.1.3 Diversifying complexity of GABAergic subtypes
		25.3.2 Glutamatergic tangential contributions as developmental scaffolds
		25.3.3 Tangential migration shaping brain connections-guidepost neurons in evolution
		25.3.4 Tangential migrations along the central nervous system
	25.4 Conclusions
	Glossary
	References
26. Neuronal migration disorders
	26.1 Introduction
	26.2 Types of malformations
		26.2.1 Pachygyria
		26.2.2 Lissencephaly
		26.2.3 Cobblestone lissencephaly
		26.2.4 Subcortical band heterotopia
		26.2.5 Periventricular heterotopia
		26.2.6 Polymicrogyria
		26.2.7 Mammalian target of rapamycin complex pathway-related malformations
		26.2.8 Microcephaly
	26.3 Identified mutations and mechanisms in neuronal migration disorder
		26.3.1 Mutations in microtubule-associated proteins (LIS1, DCX, KIF5C, KIF2A, DYNC1H1, and EML1)
		26.3.2 Tubulin mutations (TUBA1A, TUBB2B, TUBB3, TUBG1, TUBA8, and TUBB5)
		26.3.3 Periventricular heterotopia and mutations in FLNA, ARFGEF2, C6orf70, FAT4, DCHS1, and MOB2
		26.3.4 Variant lissencephalies and mutations in ARX and RELN
		26.3.5 Cobblestone malformations and mutations in dystroglycan genes
		26.3.6 Focal cortical dysplasias and dysplastic megalencephaly and mutations in mTOR, PIK3CA, DEPDC5, AKT3, NPRL3, and PIK3R2
	26.4 Summary and concluding remarks
	References
Index
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