Regulatory Mechanisms of Environmental Molecular Signaling in the Tangential Migration of Cortical Interneurons
MO Fei1), TAN Guo-He1),2),3),4)*, LIU Yuan-Yuan1),2),3),4)*
1)Guangxi Medical University, Guangxi-ASEAN Collaborative Innovation Center for Major Disease Prevention and Treatment, Guangxi Collaborative Innovation Center for Biomedicine and Guangxi Key Laboratory of Regenerative Medicine, Nanning 530021, China; 2)School of Basic Medical Sciences, Guangxi Medical University, Nanning 530021, China; 3)Key Laboratory of Longevity and Aging-related Diseases of Chinese Ministry of Education, Nanning 530021, China; 4)China-ASEAN Research Center for Innovation and Development in Brain Science, Nanning 530021, China
Abstract:Brain activity requires the regulation of excitatory and inhibitory neurons. GABAergic interneurons are considered to prevent hyperexcitability in brain. Severe GABAergic deficits have been proved to cause pathological hyperexcitability. Most cortical interneurons originate from the ventral telencephalon and then undergo a long tangential migration to the cortex, followed by radial migration into developing cortical plate. Among them, tangential migration is considered to be the main migration manner of interneurons. The process is rather complex but also precise. With the deepening research on the tangential migration of cortical neurons, many molecules have been proved to play important roles in the process of migration. In this review, we mainly describe the migration path and migration manner of interneurons, and its underlying mechanism in two aspects. On the one hand, neurotrophins such as BDNF, NT-4, GDNF, HGF and neurotransmitters such as GABA, Glu, DA can enhance the motility of interneurons. On the other hand, several protein families as well as proteoglycans, such as Ephrin, Sema and Nrg, can bind to membrane-bound or secreted guidance cues of interneurons, providing direction clues for neuronal migration. In this review, we discussed the tangential migration of interneurons in mice, in order to provide novel insights into the regulatory molecular mechanisms of cerebral cortical development and help to develop new targets against defects in neural developments.
莫非, 谭国鹤, 刘媛媛. 环境分子信号调控大脑皮层中间神经元切向迁移的机制[J]. 中国生物化学与分子生物学报, 2021, 37(9): 1138-1144.
MO Fei, TAN Guo-He, LIU Yuan-Yuan. Regulatory Mechanisms of Environmental Molecular Signaling in the Tangential Migration of Cortical Interneurons. Chinese Journal of Biochemistry and Molecular Biol, 2021, 37(9): 1138-1144.
[1] Owen SF, Berke JD, Kreitzer AC. Fast-Spiking Interneurons Supply Feedforward Control of Bursting, Calcium, and Plasticity for Efficient Learning [J]. Cell,2018,172(4):683-695.e15 [2] Silva CG, Peyre E, Adhikari MH, et al. Cell-Intrinsic Control of Interneuron Migration Drives Cortical Morphogenesis [J]. Cell,2018,172(5):1063-1078.e19 [3] Müller Smith K, Fagel DM, Stevens HE, et al. Deficiency in inhibitory cortical interneurons associates with hyperactivity in fibroblast growth factor receptor 1 mutant mice[J]. Biol Psychiatry,2008,63(10):953-962 [4] Muraki K, Tanigaki K. Neuronal migration abnormalities and its possible implications for schizophrenia [J]. Front Neurosci,2015,9:74 [5] Marín O. Interneuron dysfunction in psychiatric disorders [J]. Nat Rev Neurosci,2012,13(2):107-120 [6] Zhu Q, Naegele JR, Chung S. Cortical GABAergic Interneuron/Progenitor Transplantation as a Novel Therapy for Intractable Epilepsy [J]. Front Cell Neurosci,2018,12:167 [7] Bandler RC, Mayer C, Fishell G. Cortical interneuron specification: the juncture of genes, time and geometry [J]. Curr Opin Neurobiol, 2017,42:17-24 [8] Miyoshi G, Hjerling-Leffler J, Karayannis T, et al. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons[J]. J Neurosci,2010,30 (5):1582-1594 [9] Lim L, Mi D, Llorca A, Marín O. Development and Functional Diversification of Cortical Interneurons [J]. Neuron, 2018,100(2):294-313 [10] Myers AK, Cunningham JG, Smith SE, et al. JNK signaling is required for proper tangential migration and laminar allocation of cortical interneurons[J]. Development,2020,147(2):dev180646 [11] Polleux F, Whitford KL, Dijkhuizen PA, et al. Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling[J]. Development,2002,129(13):3147-3160 [12] Barreda Tomás FJ, Turko P, Heilmann H, et al. BDNF Expression in Cortical GABAergic Interneurons [J]. Int J Mol Sci,2020,21(5):1567 [13] Bagley JA, Belluscio L. Dynamic imaging reveals that brain-derived neurotrophic factor can independently regulate motility and direction of neuroblasts within the rostral migratory stream [J]. Neuroscience,2010,169 (3):1449-1461 [14] Bespalov MM, Sidorova YA, Tumova S, et al. Heparan sulfate proteoglycan syndecan-3 is a novel receptor for GDNF, neurturin, and artemin[J]. J Cell Biol,2011,192(1):153-169 [15] Perrinjaquet M, Sjöstrand D, Moliner A, et al. MET signaling in GABAergic neuronal precursors of the medial ganglionic eminence restricts GDNF activity in cells that express GFRα1 and a new transmembrane receptor partner[J]. J Cell Sci,2011,124(Pt 16):2797-2805 [16] Marguet F, Friocourt G, Brosolo M, et al. Prenatal alcohol exposure is a leading cause of interneuronopathy in humans [J]. Acta Neuropathol Commun,2020,8(1):208 [17] Kim KT, Kwak YJ, Han SC, et al. Impairment of motor coordination and interneuron migration in perinatal exposure to glufosinate-ammonium[J]. Sci Rep,2020,10(1):20647 [18] Luhmann HJ, Fukuda A, Kilb W. Control of cortical neuronal migration by glutamate and GABA [J]. Front Cell Neurosci,2015,9:4 [19] Priya R, Rakela B, Kaneko M, et al. Vesicular GABA Transporter Is Necessary for Transplant-Induced Critical Period Plasticity in Mouse Visual Cortex [J]. J Neurosci,2019,39(14):2635-2648 [20] Su P, Lai TKY, Lee FHF, et al. Disruption of SynGAP-dopamine D1 receptor complexes alters actin and microtubule dynamics and impairs GABAergic interneuron migration [J]. Sci Signal,2019,12(593):eaau9122 [21] Ohira K. Dopamine stimulates differentiation and migration of cortical interneurons [J]. Biochem Biophys Res Commun,2019,512(3):577-583 [22] 陈永庄,刘超,石小东.Eph家族蛋白在阿尔茨海默症等神经精神疾病中的作用[J].中国生物化学与分子生物学报(Chen YZ, Liu C, Shi XD. The Role of Eph/ephrin System in Alzheimer's disease and Other Neurologic and Psychiatric Diseases [J]. Chin J Biochem Mol Biol),2018,34(11):1160-1165 [23] Rudolph J, Zimmer G, Steinecke A, et al. Ephrins guide migrating cortical interneurons in the basal telencephalon[J]. Cell Adh Migr,2010,4(3):400-408 [24] Zimmer G, Garcez P, Rudolph J, et al. Ephrin-A5 acts as a repulsive cue for migrating cortical interneurons[J]. Eur J Neurosci,2008,28(1):62-73 [25] Liu YH, Tsai JW, Chen JL, et al. Ascl1 promotes tangential migration and confines migratory routes by induction of Ephb2 in the telencephalon[J]. Sci Rep,2017,7:42895 [26] Steinecke A, Gampe C, Zimmer G, et al. EphA/ephrin A reverse signaling promotes the migration of cortical interneurons from the medial ganglionic eminence[J]. Development,2014,141(2):460-471 [27] Nakayama H, Bruneau S, Kochupurakkal N, et al. Regulation of mTOR Signaling by Semaphorin 3F- Neuropilin 2 Interactions In Vitro and In Vivo[J]. Sci Rep,2015,5:11789 [28] Andrews WD, Barber M, Nemitz M, et al. Semaphorin3A-neuropilin1 signalling is involved in the generation of cortical interneurons[J]. Brain Struct Funct,2017,222(5):2217-2233 [29] Marín O, Yaron A, Bagri A, et al. Sorting of striatal and cortical interneurons regulated by semaphorin- neuropilin interactions [J]. Science,2001,293(5531):872-875 [30] Tamamaki N, Fujimori K, Nojyo Y, et al. Evidence that Sema3A and Sema3F regulate the migration of GABAergic neurons in the developing neocortex[J]. J Comp Neurol,2003,455(2):238-248 [31] Kanatani S, Honda T, Aramaki M, et al. The COUP-TFII/Neuropilin-2 is a molecular switch steering diencephalon-derived GABAergic neurons in the developing mouse brain [J]. Proc Natl Acad Sci U S A, 2015,112(36):E4985-E4994 [32] Li Z, Jagadapillai R, Gozal E, et al. Deletion of Semaphorin 3F in Interneurons Is Associated with Decreased GABAergic Neurons, Autism-like Behavior, and Increased Oxidative Stress Cascades[J]. Mol Neurobiol,2019, 56(8):5520-5538 [33] Gant JC, Thibault O, Blalock EM, et al. Decreased number of interneurons and increased seizures in neuropilin 2 deficient mice: implications for autism and epilepsy[J]. Epilepsia,2009,50(4):629-645 [34] Tong M, Jun T, Nie Y, et al. The Role of the Slit/Robo Signaling Pathway [J]. J Cancer,2019,10(12): 2694- 2705 [35] Zelina P, Blockus H, Zagar Y, et al. Signaling switch of the axon guidance receptor Robo3 during vertebrate evolution[J]. Neuron,2014,84(6):1258-1272 [36] Blockus H, Chédotal A. Slit-Robo signaling [J]. Development,2016,143(17):3037-3044 [37] Marín O, Plump AS, Flames N, et al. Directional guidance of interneuron migration to the cerebral cortex relies on subcortical Slit1/2-independent repulsion and cortical attraction[J]. Development,2003,130(9): 1889- 1901 [38] Andrews W, Liapi A, Plachez C, et al. Robo1 regulates the development of major axon tracts and interneuron migration in the forebrain [J]. Development,2006,133(11):2243-2252 [39] Hernández-Miranda L R, Cariboni A, Faux C, et al. Robo1 regulates semaphorin signaling to guide the migration of cortical interneurons through the ventral forebrain[J]. J Neurosci,2011,31(16):6174-6187 [40] Marín O. Interneuron dysfunction in psychiatric disorders [J]. Nat Rev Neurosci,2012,13(2):107-120 [41] Marín O. Cellular and molecular mechanisms controlling the migration of neocortical interneurons[J]. Eur J Neurosci. 2013 Jul;38(1):2019-29 [42] Fornasari BE, El Soury M, De Marchis S, et al. Neuregulin1 alpha activates migration of neuronal progenitors expressing ErbB4[J]. Mol Cell Neurosci, 2016,77:87-94 [43] Neddens J, Buonanno A. Selective populations of hippocampal interneurons express ErbB4 and their number and distribution is altered in ErbB4 knockout mice [J]. Hippocampus,2010,20(6):724-744 [44] Li H, Chou SJ, Hamasaki T, et al. Neuregulin repellent signaling via ErbB4 restricts GABAergic interneurons to migratory paths from ganglionic eminence to cortical destinations [J]. Neural Dev,2012,7:10 [45] Chang CC, Kuo HY, Chen SY, et al. Developmental characterization of Zswim5 expression in the progenitor domains and tangential migration pathways of cortical interneurons in the mouse forebrain[J]. J Comp Neurol, 2020,528(14):2404-2419 [46] Elbert A, Vogt D, Watson A, et al. CTCF Governs the Identity and Migration of MGE-Derived Cortical Interneurons [J]. J Neurosci,2019,39(1):177-192 [47] Ma T, Wang C, Wang L, et al. Subcortical origins of human and monkey neocortical interneurons[J]. Nat Neurosci,2013,16(11):1588-1597 [48] Sousa A M M, Zhu Y, Raghanti M A, et al. Molecular and cellular reorganization of neural circuits in the human lineage [J]. Science,2017,358(6366): 1027-1032