Autonomous vascular networks synchronize GABA neuron migration in the embryonic forebrain.
Authors:
Journal: Nature communications
Publication Type: Journal Article
Date: 2013
DOI: NIHMS494181
ID: 23857367
Abstract
Gamma-aminobutyric acid neurons, born in remote germinative zones in the ventral forebrain (telencephalon), migrate tangentially in two spatially distinct streams to adopt their specific positions in the developing cortex. The cell types and molecular cues that regulate this divided migratory route remains to be elucidated. Here we show that embryonic vascular networks are strategically positioned to fulfil the task of providing support as well as critical guidance cues that regulate the divided migratory routes of gamma-aminobutyric acid neurons in the telencephalon. Interestingly, endothelial cells of the telencephalon are not homogeneous in their gene expression profiles. Endothelial cells of the periventricular vascular network have molecular identities distinct from those of the pial network. Our data suggest that periventricular endothelial cells have intrinsic programs that can significantly mould neuronal development and uncovers new insights into concepts and mechanisms of central nervous system angiogenesis from both developmental and disease perspectives.
Chemical List
- Receptors, GABA-A|||Green Fluorescent Proteins|||gamma-Aminobutyric Acid
Reference List
- Treiman DM. GABAergic mechanisms in epilepsy. Epilepsia. 2001;42(Suppl. 3):8–12.|||Marin O. Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci. 2012;13:107–120.|||Levitt P, Eagleson KL, Powell EM. Regulation of neocortical interneuron development and the implications for neurodevelopmental disorders. Trends Neurosci. 2004;27:400–406.|||Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci. 2005;6:312–324.|||Vasudevan A, Long JE, Crandall JE, Rubenstein JL, Bhide PG. Compartment-specific transcription factors orchestrate angiogenesis gradients in the embryonic brain. Nat Neurosci. 2008;11:429–439.|||Vasudevan A, Bhide PG. Angiogenesis in the embryonic CNS: a new twist on an old tale. Cell Adh Migr. 2008;2:167–169.|||Hogan KA, Ambler CA, Chapman DL, Bautch VL. The neural tube patterns vessels developmentally using the VEGF signaling pathway. Development. 2004;131:1503–1513.|||Lopez-Bendito G, et al. Preferential origin and layer destination of GAD65-GFP cortical interneurons. Cereb Cortex. 2004;14:1122–1133.|||Marin O, Rubenstein JL. A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci. 2001;2:780–790.|||Corbin JG, Nery S, Fishell G. Telencephalic cells take a tangent: non-radial migration in the mammalian forebrain. Nat Neurosci. 2001;4(Suppl):1177–1182.|||Parnavelas JG. The origin and migration of cortical neurones: new vistas. Trends Neurosci. 2000;23:126–131.|||Hatten ME. New directions in neuronal migration. Science. 2002;297:1660–1663.|||Rakic P. Specification of cerebral cortical areas. Science. 1988;241:170–176.|||Lois C, Garcia-Verdugo JM, Alvarez-Buylla A. Chain migration of neuronal precursors. Science. 1996;271:978–981.|||Denaxa M, Chan CH, Schachner M, Parnavelas JG, Karagogeos D. The adhesion molecule TAG-1 mediates the migration of cortical interneurons from the ganglionic eminence along the corticofugal fiber system. Development. 2001;128:4635–4644.|||O'Rourke NA, Sullivan DP, Kaznowski CE, Jacobs AA, McConnell SK. Tangential migration of neurons in the developing cerebral cortex. Development. 1995;121:2165–2176.|||Tanaka D, Nakaya Y, Yanagawa Y, Obata K, Murakami F. Multimodal tangential migration of neocortical GABAergic neurons independent of GPI-anchored proteins. Development. 2003;130:5803–5813.|||Marin O, et al. Directional guidance of interneuron migration to the cerebral cortex relies on subcortical Slit1/2-independent repulsion and cortical attraction. Development. 2003;130:1889–1901.|||Marin O, Rubenstein JL. Cell migration in the forebrain. Annu Rev Neurosci. 2003;26:441–483.|||Wichterle H, Alvarez-Dolado M, Erskine L, Alvarez-Buylla A. Permissive corridor and diffusible gradients direct medial ganglionic eminence cell migration to the neocortex. Proc Natl Acad Sci U S A. 2003;100:727–732.|||Yuan W, et al. The mouse SLIT family: secreted ligands for ROBO expressed in patterns that suggest a role in morphogenesis and axon guidance. Dev Biol. 1999;212:290–306.|||Skaliora I, Singer W, Betz H, Puschel AW. Differential patterns of semaphorin expression in the developing rat brain. Eur J Neurosci. 1998;10:1215–1229.|||Marin O, Yaron A, Bagri A, Tessier-Lavigne M, Rubenstein JL. Sorting of striatal and cortical interneurons regulated by semaphorin-neuropilin interactions. Science. 2001;293:872–875.|||Flames N, et al. Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron. 2004;44:251–261.|||Powell EM, Mars WM, Levitt P. Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron. 2001;30:79–89.|||Zhu Y, Li H, Zhou L, Wu JY, Rao Y. Cellular and molecular guidance of GABAergic neuronal migration from an extracortical origin to the neocortex. Neuron. 1999;23:473–485.|||Stumm RK, et al. CXCR4 regulates interneuron migration in the developing neocortex. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2003;23:5123–5130.|||Pozas E, Ibanez CF. GDNF and GFRalpha1 promote differentiation and tangential migration of cortical GABAergic neurons. Neuron. 2005;45:701–713.|||Polleux F, Whitford KL, Dijkhuizen PA, Vitalis T, Ghosh A. Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling. Development. 2002;129:3147–3160.|||Tiveron MC, et al. Molecular interaction between projection neuron precursors and invading interneurons via stromal-derived factor 1 (CXCL12)/CXCR4 signaling in the cortical subventricular zone/intermediate zone. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2006;26:13273–13278.|||Ingber D, et al. Synthetic analogues of fumagillin that inhibit angiogenesis and suppress tumour growth. Nature. 1990;348:555–557.|||Castronovo V, Belotti D. TNP-470 (AGM-1470): mechanisms of action and early clinical development. Eur J Cancer. 1996;32A:2520–2527.|||DeFelipe J. Chandelier cells and epilepsy. Brain. 1999;122(Pt 10):1807–1822.|||Lewis DA, Levitt P. Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci. 2002;25:409–432.|||Benes FM, Berretta S. GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology. 2001;25:1–27.|||Wang DD, Kriegstein AR. Defining the role of GABA in cortical development. J Physiol. 2009;587:1873–1879.|||Behar TN, Schaffner AE, Scott CA, Greene CL, Barker JL. GABA receptor antagonists modulate postmitotic cell migration in slice cultures of embryonic rat cortex. Cereb Cortex. 2000;10:899–909.|||Heck N, et al. GABA-A receptors regulate neocortical neuronal migration in vitro and in vivo. Cereb Cortex. 2007;17:138–148.|||Petryshen TL, et al. Genetic investigation of chromosome 5q GABAA receptor subunit genes in schizophrenia. Mol Psychiatry. 2005;10:1074–1088. 1057.|||Kang JQ, Macdonald RL. Making sense of nonsense GABA(A) receptor mutations associated with genetic epilepsies. Trends Mol Med. 2009;15:430–438.|||Fatemi SH, Reutiman TJ, Folsom TD, Thuras PD. GABA(A) receptor downregulation in brains of subjects with autism. J Autism Dev Disord. 2009;39:223–230.|||Tyagi N, et al. Differential expression of gamma-aminobutyric acid receptor A (GABA(A)) and effects of homocysteine. Clin Chem Lab Med. 2007;45:1777–1784.|||Ong J, Kerr DI. GABA-receptors in peripheral tissues. Life Sci. 1990;46:1489–1501.|||Imai H, Okuno T, Wu JY, Lee TJ. GABAergic innervation in cerebral blood vessels: an immunohistochemical demonstration of L-glutamic acid decarboxylase and GABA transaminase. J Cereb Blood Flow Metab. 1991;11:129–134.|||Katarova Z, Sekerkova G, Prodan S, Mugnaini E, Szabo G. Domain-restricted expression of two glutamic acid decarboxylase genes in midgestation mouse embryos. J Comp Neurol. 2000;424:607–627.|||Bergen SE, Fanous AH, Walsh D, O'Neill FA, Kendler KS. Polymorphisms in SLC6A4, PAH, GABRB3, and MAOB and modification of psychotic disorder features. Schizophr Res. 2009;109:94–97.|||Sun J, Jayathilake K, Zhao Z, Meltzer HY. Investigating association of four gene regions (GABRB3, MAOB, PAH, and SLC6A4) with five symptoms in schizophrenia. Psychiatry Res. 2012|||DeLorey TM, et al. Mice lacking the beta3 subunit of the GABAA receptor have the epilepsy phenotype and many of the behavioral characteristics of Angelman syndrome. J Neurosci. 1998;18:8505–8514.|||DeLorey TM, Olsen RW. GABA and epileptogenesis: comparing gabrb3 gene-deficient mice with Angelman syndrome in man. Epilepsy Res. 1999;36:123–132.|||DeLorey TM. GABRB3 gene deficient mice: a potential model of autism spectrum disorder. Int Rev Neurobiol. 2005;71:359–382.|||DeLorey TM, Sahbaie P, Hashemi E, Homanics GE, Clark JD. Gabrb3 gene deficient mice exhibit impaired social and exploratory behaviors, deficits in non-selective attention and hypoplasia of cerebellar vermal lobules: a potential model of autism spectrum disorder. Behav Brain Res. 2008;187:207–220.|||Behar TN, et al. GABA stimulates chemotaxis and chemokinesis of embryonic cortical neurons via calcium-dependent mechanisms. The Journal of neuroscience : the official journal of the Society for Neuroscience. 1996;16:1808–1818.|||Behar TN, Schaffner AE, Scott CA, O'Connell C, Barker JL. Differential response of cortical plate and ventricular zone cells to GABA as a migration stimulus. The Journal of neuroscience : the official journal of the Society for Neuroscience. 1998;18:6378–6387.|||Varju P, Katarova Z, Madarasz E, Szabo G. GABA signalling during development: new data and old questions. Cell Tissue Res. 2001;305:239–246.|||Graybiel AM, Liu FC, Dunnett SB. Intrastriatal grafts derived from fetal striatal primordia. I. Phenotypy and modular organization. The Journal of neuroscience : the official journal of the Society for Neuroscience. 1989;9:3250–3271.|||Wichterle H, Garcia-Verdugo JM, Herrera DG, Alvarez-Buylla A. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat Neurosci. 1999;2:461–466.|||Ekins S, Nikolsky Y, Bugrim A, Kirillov E, Nikolskaya T. Pathway mapping tools for analysis of high content data. Methods Mol Biol. 2007;356:319–350.|||Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45.