The role of the Eph/ephrin family during cortical development and cerebral malformations

Main Article Content

Katrin Gerstmann Geraldine Zimmer

Abstract

Neuronal numbers and the associated size of the cerebral cortex, surface folding and laminar organisation are determined by precise developmental mechanisms that are orchestrated by several intrinsic and extrinsic molecules. Abnormalities during development can cause manifold microscopic and macroscopic cortical malformations, mostly accompanied by clinical consequences such as mental disorders, intellectual disabilities, or epileptic seizures. Most cortical malformations and associated neurological disorders result from genetic defects, however the cellular mechanisms remain complex and poorly understood. Eph receptor tyrosine kinases and their ligands, the ephrins, are abundantly expressed in the developing brain where they regulate several developmental processes that are crucial for correct brain formation. Ephrin family members represent membrane-bound proteins that are key players in complex short-range cell-cell communication. In addition, mechanisms for long-range interactions have been described recently. Several ephrins have already been shown to control cell cycle dynamics of cortical stem cells during corticogenesis and the positioning of postmitotic neurons. In addition, mutations in genes encoding for members of the Eph/ephrin family are implicated in mental disorders, although the underlying mechanisms remain to be elucidated. A deeper understanding of Eph/ephrin interactions during cerebral cortex development will be beneficial to shed light on developmental disabilities. Here, we discuss the function of Eph/ephrin system during the different processes of corticogenesis and the impact on cerebral malformations.

Article Details

How to Cite
GERSTMANN, Katrin; ZIMMER, Geraldine. The role of the Eph/ephrin family during cortical development and cerebral malformations. Medical Research Archives, [S.l.], v. 6, n. 3, mar. 2018. ISSN 2375-1924. Available at: <https://journals.ke-i.org/index.php/mra/article/view/1694>. Date accessed: 22 july 2018. doi: https://doi.org/10.18103/mra.v6i3.1694.
Section
Research Articles

References

References:

1. Götz M, Huttner WB, editors. The cell biology of neurogenesis. England2005.
2. McConnell SK. Strategies for the generation of neuronal diversity in the developing central nervous system. J Neurosci. 1995;15(11):6987-98.
3. Rakic P, editor. A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. England1995.
4. Haubensak W, Attardo A, Denk W, Huttner WB, editors. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. United States2004.
5. Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR, editors. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. United States2004.
6. Gerstmann K, Pensold D, Symmank J, Khundadze M, Hubner CA, Bolz J, et al. Thalamic afferents influence cortical progenitors via ephrin A5-EphA4 interactions. Development. 2015;142(1):140-50.
7. Rakic P. Defects of neuronal migration and the pathogenesis of cortical malformations. Progress in brain research. 1988;73:15-37.
8. Franco SJ, Gil-Sanz C, Martinez-Garay I, Espinosa A, Harkins-Perry SR, Ramos C, et al. Fate-restricted neural progenitors in the mammalian cerebral cortex. Science. 2012;337(6095):746-9.
9. Bizzotto S, Francis F. Morphological and functional aspects of progenitors perturbed in cortical malformations. Frontiers in cellular neuroscience. 2015;9:30.
10. Niehage R. Expressionsanalyse des Ephrin-/Eph Systems im frontalen Gehirn der Maus während der embryonalen und postnatalen Entwicklung. Friedrich Schiller Universität, Jena. 2008.
11. Peuckert C, Wacker E, Rapus J, Levitt P, Bolz J, editors. Adaptive changes in gene expression patterns in the somatosensory cortex after deletion of ephrinA5. United States2008.
12. Yun ME, Johnson RR, Antic A, Donoghue MJ. EphA family gene expression in the developing mouse neocortex: regional patterns reveal intrinsic programs and extrinsic influence. J Comp Neurol. 2003;456(3):203-16.
13. Liebl DJ, Morris CJ, Henkemeyer M, Parada LF. mRNA expression of ephrins and Eph receptor tyrosine kinases in the neonatal and adult mouse central nervous system. J Neurosci Res. 2003;71(1):7-22.
14. Gale NW, Holland SJ, Valenzuela DM, Flenniken A, Pan L, Ryan TE, et al., editors. Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. United States1996.
15. Torres R, Firestein BL, Dong H, Staudinger J, Olson EN, Huganir RL, et al. PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands. Neuron. 1998;21(6):1453-63.
16. Song J, Vranken W, Xu P, Gingras R, Noyce RS, Yu Z, et al. Solution structure and backbone dynamics of the functional cytoplasmic subdomain of human ephrin B2, a cell-surface ligand with bidirectional signaling properties. Biochemistry. 2002;41(36):10942-9.
17. Kullander K, Klein R, editors. Mechanisms and functions of Eph and ephrin signalling. England2002.
18. Pasquale EB. Eph-ephrin bidirectional signaling in physiology and disease. Cell. 2008;133(1):38-52.
19. Himanen JP, Chumley MJ, Lackmann M, Li C, Barton WA, Jeffrey PD, et al. Repelling class discrimination: ephrin-A5 binds to and activates EphB2 receptor signaling. Nat Neurosci. 2004;7(5):501-9.
20. Flanagan JG, Vanderhaeghen P. The ephrins and Eph receptors in neural development. Annu Rev Neurosci. 1998;21:309-45.
21. Blits-Huizinga CT, Nelersa CM, Malhotra A, Liebl DJ. Ephrins and their receptors: binding versus biology. IUBMB life. 2004;56(5):257-65.
22. Monschau B, Kremoser C, Ohta K, Tanaka H, Kaneko T, Yamada T, et al. Shared and distinct functions of RAGS and ELF-1 in guiding retinal axons. Embo J. 1997;16(6):1258-67.
23. Knoll B, Drescher U, editors. Ephrin-As as receptors in topographic projections. England2002.
24. Murai KK, Nguyen LN, Irie F, Yamaguchi Y, Pasquale EB, editors. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. United States2003.
25. Wilkinson DG, editor. Topographic mapping: organising by repulsion and competition? England2000.
26. Davy A, Gale NW, Murray EW, Klinghoffer RA, Soriano P, Feuerstein C, et al. Compartmentalized signaling by GPI-anchored ephrin-A5 requires the Fyn tyrosine kinase to regulate cellular adhesion. Genes & development. 1999;13(23):3125-35.
27. Lim BK, Matsuda N, Poo MM. Ephrin-B reverse signaling promotes structural and functional synaptic maturation in vivo. Nat Neurosci. 2008;11(2):160-9.
28. Himanen JP, Yermekbayeva L, Janes PW, Walker JR, Xu K, Atapattu L, et al. Architecture of Eph receptor clusters. Proc Natl Acad Sci U S A. 2010;107(24):10860-5.
29. Janes PW, Nievergall E, Lackmann M. Concepts and consequences of Eph receptor clustering. Seminars in cell & developmental biology. 2012;23(1):43-50.
30. Seiradake E, Schaupp A, del Toro Ruiz D, Kaufmann R, Mitakidis N, Harlos K, et al. Structurally encoded intraclass differences in EphA clusters drive distinct cell responses. Nature structural & molecular biology. 2013;20(8):958-64.
31. Yin Y, Yamashita Y, Noda H, Okafuji T, Go MJ, Tanaka H. EphA receptor tyrosine kinases interact with co-expressed ephrin-A ligands in cis. Neuroscience research. 2004;48(3):285-96.
32. Davis S, Gale NW, Aldrich TH, Maisonpierre PC, Lhotak V, Pawson T, et al. Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science. 1994;266(5186):816-9.
33. Wykosky J, Palma E, Gibo DM, Ringler S, Turner CP, Debinski W. Soluble monomeric EphrinA1 is released from tumor cells and is a functional ligand for the EphA2 receptor. Oncogene. 2008;27(58):7260-73.
34. Lema Tome CM, Palma E, Ferluga S, Lowther WT, Hantgan R, Wykosky J, et al. Structural and functional characterization of monomeric EphrinA1 binding site to EphA2 receptor. The Journal of biological chemistry. 2012;287(17):14012-22.
35. Ieguchi K, Tomita T, Omori T, Komatsu A, Deguchi A, Masuda J, et al. ADAM12-cleaved ephrin-A1 contributes to lung metastasis. Oncogene. 2014;33(17):2179-90.
36. Lehtinen MK, Walsh CA. Neurogenesis at the brain-cerebrospinal fluid interface. The Journal of cell biology. 2011;27:653-79.
37. Arbeille E, Reynaud F, Sanyas I, Bozon M, Kindbeiter K, Causeret F, et al. Cerebrospinal fluid-derived Semaphorin3B orients neuroepithelial cell divisions in the apicobasal axis. Nature communications. 2015;6:6366.
38. Baird GS, Nelson SK, Keeney TR, Stewart A, Williams S, Kraemer S, et al. Age-dependent changes in the cerebrospinal fluid proteome by slow off-rate modified aptamer array. The American journal of pathology. 2012;180(2):446-56.
39. Gong J, Korner R, Gaitanos L, Klein R. Exosomes mediate cell contact-independent ephrin-Eph signaling during axon guidance. 2016;214(1):35-44.
40. Sun T, Hevner RF. Growth and folding of the mammalian cerebral cortex: from molecules to malformations. Nature reviews Neuroscience. 2014;15(4):217-32.
41. North HA, Zhao X, Kolk SM, Clifford MA, Ziskind DM, Donoghue MJ, editors. Promotion of proliferation in the developing cerebral cortex by EphA4 forward signaling. England2009.
42. Qiu R, Wang X, Davy A, Wu C, Murai K, Zhang H, et al., editors. Regulation of neural progenitor cell state by ephrin-B. United States2008.
43. Arvanitis DN, Jungas T, Behar A, Davy A. Ephrin-B1 reverse signaling controls a posttranscriptional feedback mechanism via miR-124. Molecular and cellular biology. 2010;30(10):2508-17.
44. Wu C, Qiu R, Wang J, Zhang H, Murai K, Lu Q. ZHX2 Interacts with Ephrin-B and regulates neural progenitor maintenance in the developing cerebral cortex. J Neurosci. 2009;29(23):7404-12.
45. Aoki M, Yamashita T, Tohyama M. EphA receptors direct the differentiation of mammalian neural precursor cells through a mitogen-activated protein kinase-dependent pathway. The Journal of biological chemistry. 2004;279(31):32643-50.
46. Homman-Ludiye J, Kwan WC, de Souza MJ, Rodger J. Ephrin-A2 regulates excitatory neuron differentiation and interneuron migration in the developing neocortex. 2017;7(1):11813.
47. Huttner WB, Kosodo Y, editors. Symmetric versus asymmetric cell division during neurogenesis in the developing vertebrate central nervous system. United States2005.
48. Betizeau M, Cortay V, Patti D, Pfister S, Gautier E, Bellemin-Menard A, et al. Precursor diversity and complexity of lineage relationships in the outer subventricular zone of the primate. Scientific reports. 2013;80(2):442-57.
49. Smart IH, Dehay C, Giroud P, Berland M, Kennedy H. Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb Cortex. 2002;12(1):37-53.
50. Reillo I, de Juan Romero C, Garcia-Cabezas MA, Borrell V. A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb Cortex. 2011;21(7):1674-94.
51. Borrell V, Gotz M. Role of radial glial cells in cerebral cortex folding. Current opinion in neurobiology. 2014;27:39-46.
52. Pilz GA, Shitamukai A, Reillo I, Pacary E, Schwausch J, Stahl R, et al. Amplification of progenitors in the mammalian telencephalon includes a new radial glial cell type. Nature communications. 2013;4:2125.
53. Alkuraya FS, Cai X, Emery C, Mochida GH, Al-Dosari MS, Felie JM, et al. Human mutations in NDE1 cause extreme microcephaly with lissencephaly [corrected]. American journal of human genetics. 2011;88(5):536-47.
54. Budday S, Raybaud C, Kuhl E. A mechanical model predicts morphological abnormalities in the developing human brain. Scientific reports. 2014;4:5644.
55. Wallace GL, Robustelli B, Dankner N, Kenworthy L, Giedd JN, Martin A. Increased gyrification, but comparable surface area in adolescents with autism spectrum disorders. Brain. 2013;136(Pt 6):1956-67.
56. Stahl R, Walcher T, De Juan Romero C, Pilz GA, Cappello S, Irmler M, et al. Trnp1 regulates expansion and folding of the mammalian cerebral cortex by control of radial glial fate. Cell. 2013;153(3):535-49.
57. Quinn JC, Molinek M, Martynoga BS, Zaki PA, Faedo A, Bulfone A, et al., editors. Pax6 controls cerebral cortical cell number by regulating exit from the cell cycle and specifies cortical cell identity by a cell autonomous mechanism. United States2007.
58. Donoghue MJ, Rakic P. Molecular gradients and compartments in the embryonic primate cerebral cortex. Cereb Cortex. 1999;9(6):586-600.
59. Kuida K, Haydar TF, Kuan CY, Gu Y, Taya C, Karasuyama H, et al., editors. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. United States1998.
60. Pompeiano M, Blaschke AJ, Flavell RA, Srinivasan A, Chun J. Decreased apoptosis in proliferative and postmitotic regions of the Caspase 3-deficient embryonic central nervous system. J Comp Neurol. 2000;423(1):1-12.
61. Furne C, Ricard J, Cabrera JR, Pays L, Bethea JR, Mehlen P, et al. EphrinB3 is an anti-apoptotic ligand that inhibits the dependence receptor functions of EphA4 receptors during adult neurogenesis. Biochimica et biophysica acta. 2009;1793(2):231-8.
62. Holmberg J, Armulik A, Senti KA, Edoff K, Spalding K, Momma S, et al. Ephrin-A2 reverse signaling negatively regulates neural progenitor proliferation and neurogenesis. Genes & development. 2005;19(4):462-71.
63. Theus MH, Ricard J, Bethea JR, Liebl DJ. EphB3 limits the expansion of neural progenitor cells in the subventricular zone by regulating p53 during homeostasis and following traumatic brain injury. Stem cells (Dayton, Ohio). 2010;28(7):1231-42.
64. Park S. Brain-Region Specific Apoptosis Triggered by Eph/ephrin Signaling. Experimental neurobiology. 2013;22(3):143-8.
65. Depaepe V, Suarez-Gonzalez N, Dufour A, Passante L, Gorski JA, Jones KR, et al. Ephrin signalling controls brain size by regulating apoptosis of neural progenitors. Nature. 2005;435(7046):1244-50.
66. Reddy S, Dolzhanskaya N, Krogh J, Velinov M. A novel 1.4 Mb de novo microdeletion of chromosome 1q21.3 in a child with microcephaly, dysmorphic features and mental retardation. European journal of medical genetics. 2009;52(6):443-5.
67. Paridaen JT, Wilsch-Brauninger M, Huttner WB. Asymmetric inheritance of centrosome-associated primary cilium membrane directs ciliogenesis after cell division. Cell. 2013;155(2):333-44.
68. Wang X, Tsai JW, Imai JH, Lian WN, Vallee RB, Shi SH. Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature. 2009;461(7266):947-55.
69. Caviness VS, Jr., Takahashi T, Nowakowski RS, editors. Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. England1995.
70. Nestor-Bergmann A, Goddard G, Woolner S. Force and the spindle: mechanical cues in mitotic spindle orientation. Seminars in cell & developmental biology. 2014;34:133-9.
71. Lancaster OM, Baum B. Shaping up to divide: coordinating actin and microtubule cytoskeletal remodelling during mitosis. Seminars in cell & developmental biology. 2014;34:109-15.
72. Negishi T, Nishida H. Asymmetric and Unequal Cell Divisions in Ascidian Embryos. Results and problems in cell differentiation. 2017;61:261-84.
73. Picco V, Hudson C, Yasuo H. Ephrin-Eph signalling drives the asymmetric division of notochord/neural precursors in Ciona embryos. Development. 2007;134(8):1491-7.
74. Lee HS, Daar IO. EphrinB reverse signaling in cell-cell adhesion: is it just par for the course? Cell adhesion & migration. 2009;3(3):250-5.
75. Lee HS, Nishanian TG, Mood K, Bong YS, Daar IO. EphrinB1 controls cell-cell junctions through the Par polarity complex. Nature cell biology. 2008;10(8):979-86.
76. Nakayama M, Berger P. Coordination of VEGF receptor trafficking and signaling by coreceptors. Experimental cell research. 2013;319(9):1340-7.
77. Costa MR, Gotz M, Berninger B, editors. What determines neurogenic competence in glia? Netherlands2010.
78. Kalani MY, Cheshier SH, Cord BJ, Bababeygy SR, Vogel H, Weissman IL, et al. Wnt-mediated self-renewal of neural stem/progenitor cells. Proc Natl Acad Sci U S A. 2008;105(44):16970-5.
79. Chenn A. Wnt/beta-catenin signaling in cerebral cortical development. Organogenesis. 2008;4(2):76-80.
80. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell. 2006;127(3):469-80.
81. Fang Y, Cho KS, Tchedre K, Lee SW, Guo C, Kinouchi H, et al. Ephrin-A3 suppresses Wnt signaling to control retinal stem cell potency. Stem cells (Dayton, Ohio). 2013;31(2):349-59.
82. Boitard M, Bocchi R, Egervari K, Petrenko V, Viale B, Gremaud S, et al. Wnt signaling regulates multipolar-to-bipolar transition of migrating neurons in the cerebral cortex. Cell reports. 2015;10(8):1349-61.
83. D'Avino PP. Citron kinase - renaissance of a neglected mitotic kinase. Journal of cell science. 2017;130(10):1701-8.
84. Sarkisian MR, Li W, Di Cunto F, D'Mello SR, LoTurco JJ. Citron-kinase, a protein essential to cytokinesis in neuronal progenitors, is deleted in the flathead mutant rat. J Neurosci. 2002;22(8):Rc217.
85. Basit S, Al-Harbi KM, Alhijji SA, Albalawi AM, Alharby E, Eldardear A, et al. CIT, a gene involved in neurogenic cytokinesis, is mutated in human primary microcephaly. Human genetics. 2016;135(10):1199-207.
86. Jungas T, Perchey RT, Fawal M, Callot C, Froment C, Burlet-Schiltz O, et al. Eph-mediated tyrosine phosphorylation of citron kinase controls abscission. The Journal of cell biology. 2016;214(5):555-69.
87. Zhang J, Woodhead GJ, Swaminathan SK, Noles SR, McQuinn ER, Pisarek AJ, et al. Cortical neural precursors inhibit their own differentiation via N-cadherin maintenance of beta-catenin signaling. Developmental cell. 2010;18(3):472-9.
88. Arvanitis DN, Behar A, Tryoen-Toth P, Bush JO, Jungas T, Vitale N, et al. Ephrin B1 maintains apical adhesion of neural progenitors. Development. 2013;140(10):2082-92.
89. Rousso DL, Pearson CA, Gaber ZB, Miquelajauregui A, Li S, Portera-Cailliau C, et al. Foxp-mediated suppression of N-cadherin regulates neuroepithelial character and progenitor maintenance in the CNS. Neuron. 2012;74(2):314-30.
90. Cooper MA, Son AI, Komlos D, Sun Y, Kleiman NJ, Zhou R. Loss of ephrin-A5 function disrupts lens fiber cell packing and leads to cataract. Proc Natl Acad Sci U S A. 2008;105(43):16620-5.
91. Zimmer G, Kastner B, Weth F, Bolz J. Multiple effects of ephrin-A5 on cortical neurons are mediated by SRC family kinases. J Neurosci. 2007;27(21):5643-53.
92. Winning RS, Scales JB, Sargent TD. Disruption of cell adhesion in Xenopus embryos by Pagliaccio, an Eph-class receptor tyrosine kinase. Developmental biology. 1996;179(2):309-19.
93. Zisch AH, Stallcup WB, Chong LD, Dahlin-Huppe K, Voshol J, Schachner M, et al. Tyrosine phosphorylation of L1 family adhesion molecules: implication of the Eph kinase Cek5. J Neurosci Res. 1997;47(6):655-65.
94. Huynh-Do U, Stein E, Lane AA, Liu H, Cerretti DP, Daniel TO. Surface densities of ephrin-B1 determine EphB1-coupled activation of cell attachment through alphavbeta3 and alpha5beta1 integrins. Embo J. 1999;18(8):2165-73.
95. Davy A, Robbins SM. Ephrin-A5 modulates cell adhesion and morphology in an integrin-dependent manner. Embo J. 2000;19(20):5396-405.
96. Fietz SA, Kelava I, Vogt J, Wilsch-Brauninger M, Stenzel D, Fish JL, et al. OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat Neurosci. 2010;13(6):690-9.
97. Radakovits R, Barros CS, Belvindrah R, Patton B, Muller U. Regulation of radial glial survival by signals from the meninges. J Neurosci. 2009;29(24):7694-705.
98. Bennett KM, Afanador MD, Lal CV, Xu H, Persad E, Legan SK, et al. Ephrin-B2 reverse signaling increases alpha5beta1 integrin-mediated fibronectin deposition and reduces distal lung compliance. American journal of respiratory cell and molecular biology. 2013;49(4):680-7.
99. Makarov A, Ylivinkka I, Nyman TA, Hyytiainen M, Keski-Oja J. Ephrin-As, Eph receptors and integrin alpha3 interact and colocalise at membrane protrusions of U251MG glioblastoma cells. Cell biology international. 2013;37(10):1080-8.
100. Radmanesh F, Caglayan AO, Silhavy JL, Yilmaz C, Cantagrel V, Omar T, et al. Mutations in LAMB1 cause cobblestone brain malformation without muscular or ocular abnormalities. American journal of human genetics. 2013;92(3):468-74.
101. Rodriguez S, Rudloff S, Koenig KF, Karthik S, Hoogewijs D, Huynh-Do U. Bidirectional signalling between EphA2 and ephrinA1 increases tubular cell attachment, laminin secretion and modulates erythropoietin expression after renal hypoxic injury. Pflugers Archiv : European journal of physiology. 2016;468(8):1433-48.
102. Savino W, Mendes-da-Cruz DA, Golbert DC, Riederer I, Cotta-de-Almeida V. Laminin-Mediated Interactions in Thymocyte Migration and Development. Frontiers in immunology. 2015;6:579.
103. Holmberg J, Clarke DL, Frisen J. Regulation of repulsion versus adhesion by different splice forms of an Eph receptor. Nature. 2000;408(6809):203-6.
104. Rakic P. Radial versus tangential migration of neuronal clones in the developing cerebral cortex. Proc Natl Acad Sci U S A. 1995;92(25):11323-7.
105. Nishimura YV, Sekine K, Chihama K, Nakajima K, Hoshino M, Nabeshima Y, et al. Dissecting the factors involved in the locomotion mode of neuronal migration in the developing cerebral cortex. The Journal of biological chemistry. 2010;285(8):5878-87.
106. Rudolph J, Gerstmann K, Zimmer G, Steinecke A, Doding A, Bolz J. A dual role of EphB1/ephrin-B3 reverse signaling on migrating striatal and cortical neurons originating in the preoptic area: should I stay or go away? Frontiers in cellular neuroscience. 2014;8:185.
107. Rudolph J, Zimmer G, Steinecke A, Barchmann S, Bolz J. Ephrins guide migrating cortical interneurons in the basal telencephalon. Cell adhesion & migration. 2010;4(3):400-8.
108. Steinecke A, Gampe C, Zimmer G, Rudolph J, Bolz J. EphA/ephrin A reverse signaling promotes the migration of cortical interneurons from the medial ganglionic eminence. Development. 2014;141(2):460-71.
109. Zimmer G, Garcez P, Rudolph J, Niehage R, Weth F, Lent R, et al., editors. Ephrin-A5 acts as a repulsive cue for migrating cortical interneurons. France2008.
110. Zimmer G, Rudolph J, Landmann J, Gerstmann K, Steinecke A, Gampe C, et al. Bidirectional ephrinB3/EphA4 signaling mediates the segregation of medial ganglionic eminence- and preoptic area-derived interneurons in the deep and superficial migratory stream. J Neurosci. 2011;31(50):18364-80.
111. Ohtaka-Maruyama C, Hirai S, Miwa A, Heng JI, Shitara H, Ishii R, et al. RP58 regulates the multipolar-bipolar transition of newborn neurons in the developing cerebral cortex. Cell reports. 2013;3(2):458-71.
112. Nadarajah B. Radial glia and somal translocation of radial neurons in the developing cerebral cortex. Glia. 2003;43(1):33-6.
113. Nadarajah B, Alifragis P, Wong RO, Parnavelas JG. Neuronal migration in the developing cerebral cortex: observations based on real-time imaging. Cereb Cortex. 2003;13(6):607-11.
114. Rakic P. Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol. 1972;145(1):61-83.
115. Super H, Soriano E, Uylings HB, editors. The functions of the preplate in development and evolution of the neocortex and hippocampus. Netherlands1998.
116. Nichols AJ, Carney LH, Olson EC. Comparison of slow and fast neocortical neuron migration using a new in vitro model. BMC neuroscience. 2008;9:50.
117. Xie MJ, Yagi H, Kuroda K, Wang CC, Komada M, Zhao H, et al. WAVE2-Abi2 complex controls growth cone activity and regulates the multipolar-bipolar transition as well as the initiation of glia-guided migration. Cereb Cortex. 2013;23(6):1410-23.
118. Schaar BT, McConnell SK. Cytoskeletal coordination during neuronal migration. Proc Natl Acad Sci U S A. 2005;102(38):13652-7.
119. Hu Y, Li S, Jiang H, Li MT, Zhou JW. Ephrin-B2/EphA4 forward signaling is required for regulation of radial migration of cortical neurons in the mouse. Neuroscience bulletin. 2014;30(3):425-32.
120. Gongidi V, Ring C, Moody M, Brekken R, Sage EH, Rakic P, et al. SPARC-like 1 regulates the terminal phase of radial glia-guided migration in the cerebral cortex. Neuron. 2004;41(1):57-69.
121. Kawauchi T, Sekine K, Shikanai M, Chihama K, Tomita K, Kubo K, et al. Rab GTPases-dependent endocytic pathways regulate neuronal migration and maturation through N-cadherin trafficking. Neuron. 2010;67(4):588-602.
122. Senturk A, Pfennig S, Weiss A, Burk K, Acker-Palmer A. Ephrin Bs are essential components of the Reelin pathway to regulate neuronal migration. Nature. 2011;472(7343):356-60.
123. Pohlkamp T, Xiao L, Sultana R, Bepari A, Bock HH, Henkemeyer M, et al. Ephrin Bs and canonical Reelin signalling. Nature. 2016;539(7630):E4-e6.
124. Mountcastle VB. The columnar organization of the neocortex. Brain. 1997;120 ( Pt 4):701-22.
125. Torii M, Hashimoto-Torii K, Levitt P, Rakic P, editors. Integration of neuronal clones in the radial cortical columns by EphA and ephrin-A signalling. England2009.
126. Dimidschstein J, Passante L, Dufour A, van den Ameele J, Tiberi L, Hrechdakian T, et al. Ephrin-B1 controls the columnar distribution of cortical pyramidal neurons by restricting their tangential migration. Neuron. 2013;79(6):1123-35.
127. Villar-Cerviño V, Kappeler C, Nóbrega-Pereira S, Henkemeyer M, Rago L, Nieto MA, Marín O. Molecular mechanisms controlling the migration of striatal interneurons. J Neurosci. 2015 Jun 10;35(23):8718-29
128. Homman-Ludiye J, Kwan WC, de Souza MJ, Rodger J, Bourne JA. Ephrin-A2 regulates excitatory neuron differentiation and interneuron migration in the developing neocortex. Sci Rep. 2017 Sep 18;7(1):11813.
129. Wurzman R, Forcelli PA, Griffey CJ, Kromer LF. Repetitive grooming and sensorimotor abnormalities in an ephrin-A knockout model for Autism Spectrum Disorders. Behav Brain Res. 2015 Feb 1;278:115-28
130. Traylor RN, Fan Z, Hudson B, Rosenfeld JA, Shaffer LG, Torchia BS, Ballif BC. Microdeletion of 6q16.1 encompassing EPHA7 in a child with mild neurological abnormalities and dysmorphic features: case report. Mol Cytogenet. 2009 Aug 7;2:17.
131. Barquilla A, Pasquale EB. Eph receptors and ephrins: therapeutic opportunities. Annu Rev Pharmacol Toxicol. 2015;55:465-87.
132. Kushima I, Nakamura Y, Aleksic B, Ikeda M, Ito Y, Shiino T, Okochi T, Fukuo Y, Ujike H, Suzuki M, Inada T, Hashimoto R, Takeda M, Kaibuchi K, Iwata N, Ozaki N. Resequencing and association analysis of the KALRN and EPHB1 genes and their contribution to schizophrenia susceptibility. Schizophr Bull. 2012 May;38(3):552-60.
133: Stoner R, Chow ML, Boyle MP, Sunkin SM, Mouton PR, Roy S, Wynshaw-Boris A, Colamarino SA, Lein ES, Courchesne E. Patches of disorganization in the neocortex of children with autism. N Engl J Med. 2014 Mar 27;370(13):1209-1219.
134. Xia Y, Luo C, Dai S, Yao D. Increased EphA/ephrinA expression in hippocampus of pilocarpine treated mouse. Epilepsy Res. 2013 Jul;105(1-2):20-9
135. Sutrala SR, Goossens D, Williams NM, Heyrman L, Adolfsson R, Norton N, Buckland PR, Del-Favero J. Gene copy number variation in schizophrenia. Schizophr Res. 2007 Nov;96(1-3):93-9. Epub 2007 Sep 7

Most read articles by the same author(s)

Obs.: This plugin requires at least one statistics/report plugin to be enabled. If your statistics plugins provide more than one metric then please also select a main metric on the admin's site settings page and/or on the journal manager's settings pages.