Astrocytes of the Anterior Commissure Regulate the Axon Guidance Pathways of Newly Generated Neocortical Neurons in the Opossum Monodelphis domestica
<p>The distribution of BrdU+ and Satb2+ cells in the developing opossum brains. (<b>A</b>–<b>C</b>) coronal sections from the brain rostral part of P12 (<b>A</b>), P14 (<b>B</b>), and P17 (<b>C</b>), showing BrdU-labeled cells in the cingulate cortex, motor cortex, somatosensory cortex, granular insular cortex, piriform cortex, and anterior commissure. (<b>E</b>,<b>G</b>,<b>I</b>) coronal section from the brain caudal part of P12 (<b>E</b>), P14 (<b>G</b>), and P17 (<b>I</b>), demonstrating BrdU-labeled cells in the retrosplenial cortex and visual cortex. (<b>A</b>–<b>C</b>,<b>E</b>,<b>G</b>,<b>I</b>) BrdU-labeled cells were located in the neocortical upper layers of opossums that were injected at P12, P14, and P17, and sacrificed at P90. A few BrdU-immunopositive cells were observed in the anterior commissure at P12 (<b>A</b>,<b>D</b>), and their numbers gradually increased at P14 (<b>B</b>,<b>F</b>), and P17 (<b>C</b>,<b>H</b>); (<b>D</b>,<b>F</b>,<b>H</b>) Zoomed areas shown in (<b>A</b>), (<b>B</b>) and (<b>C</b>), respectively. (<b>J</b>–<b>L</b>) Immunostaining of developing cortical plate with Satb2 (red) at P12, P14, and P17 in opossum brains. The scale bar in (<b>C</b>), (<b>H</b>), and (<b>I</b>) refers to (<b>A</b>,<b>B</b>), (<b>D</b>,<b>F</b>), and (<b>E</b>,<b>G</b>), respectively. The scale bar in (<b>L</b>) refers to both images (<b>J</b>) and (<b>K</b>). AC, anterior commissure; Cg, cingulate cortex; ec, external capsule; GI, granular insular cortex; M, motor cortex; P, postnatal day; Pir, piriform cortex; RS, retrosplenial cortex; S, somatosensory cortex; V, visual cortex.</p> "> Figure 2
<p>Nrp1 protein in the developing cerebral cortex of opossums. (<b>A</b>–<b>C</b>) The distribution of Nrp1-immunolabeled cells in the cerebral cortex of P14, P17, and P19 opossums. (<b>D</b>) Representative Western blot of Nrp1 and loading control GAPDH protein expression in the cerebral cortex of opossums at P14, P17, P24, and P35. (<b>E</b>) The quantification of Nrp1 protein in the developing cerebral cortex. The scale bar in (<b>C</b>) refers to both (<b>A</b>,<b>B</b>).</p> "> Figure 3
<p>Development and cellular organization of the anterior commissure. (<b>A</b>–<b>C</b>) Double GFAP (red) and DAPI (blue)-immunolabeled brain sections from the anterior commissure at P12 (<b>A</b>), P14 (<b>B</b>) and P17 (<b>C</b>), and the cerebral cortex (<b>F</b>,<b>I</b>) at P17 (<b>F</b>) and P31 (<b>I</b>) in the opossums. (<b>D</b>,<b>E</b>,<b>G</b>,<b>H</b>) High magnification confocal images showing GFAP-labeled cells in the anterior commissure of P17 (<b>D</b>) and cerebral cortex of opossums at P17 (<b>E</b>) and P31 (<b>G</b>,<b>H</b>). (<b>L</b>) Double labeled with DAPI (<b>K</b>) and vimentin (<b>J</b>)-stained brain coronal sections at the level of the anterior commissure. The scale bar in (<b>C</b>), and (<b>L</b>) refers to (<b>A</b>,<b>B</b>), and (<b>J</b>,<b>K</b>), respectively.</p> "> Figure 4
<p>Development of oligodendrocytes in opossums. (<b>A</b>–<b>C</b>) Olig2 (red) and DAPI (blue) immunostaining in the anterior commissure of opossums at P17 (<b>A</b>), P21 (<b>B</b>) and P30 (<b>C</b>). (<b>D</b>–<b>F</b>) BrdU (green) and CC1 (red) immunolabeled cells in brain sections presenting the anterior commissure in opossums at P19 (<b>D</b>), P21 (<b>E</b>) and P30 (<b>F</b>). (<b>G</b>,<b>H</b>) Percentage of cells colocalizing Olig2 and DAPI (<b>G</b>) or BrdU and CC1 (<b>H</b>) expressed as mean ± SEM. * <span class="html-italic">p</span> = 0.02, ** <span class="html-italic">p</span> < 0.0001. The scale bar in (<b>C</b>), and (<b>F</b>) refers to (<b>A</b>,<b>B</b>), and (<b>D</b>,<b>E</b>), respectively.</p> "> Figure 5
<p>Myelination of the anterior commissure in the developing opossum. (<b>A</b>–<b>C</b>) Myelin basic protein (MBP) immunostaining in the anterior commissure of opossums at P30 (<b>A</b>), P40 (<b>B</b>) and P50 (<b>C</b>). (<b>D</b>–<b>L</b>) Fiber staining of the anterior commissure using the Gallyas silver impregnation method. Individual myelinated axons were visualized in the anterior commissure in the 30-day-old opossum brain (<b>D</b>), and the intense staining of fiber tracts was seen in 50-day-old (<b>F</b>–<b>I</b>) and 90-day-old opossums (<b>J</b>–<b>L</b>). The scale bar in (<b>C</b>) refers to both (<b>A</b>) and (<b>B</b>). The scale bar in (<b>F</b>) and (<b>J)</b> refers to (<b>D</b>,<b>E</b>,<b>H</b>,<b>I</b>,<b>K</b>,<b>L</b>), and (<b>G</b>), respectively.</p> "> Figure 6
<p>The pattern of axon projection neocortical neurons in the developing opossum brain is defined by DiI labeling (<b>A</b>–<b>F</b>) or virus infection (<b>G</b>–<b>J</b>). The pattern of the DiI-labeled axons of neocortical neurons in 12-day-old (<b>A</b>–<b>C</b>), 14-day-old (<b>D</b>–<b>F</b>), and 30-day-old (<b>G</b>–<b>J</b>) opossum brains. (<b>B</b>,<b>E</b>) and (<b>C</b>,<b>F</b>) The zoomed area showing the external capsule (<b>B</b>,<b>E</b>) and the anterior commissure (<b>C</b>,<b>F</b>) in 12-day-old (<b>B</b>,<b>C</b>) and 14-day-old (<b>E</b>,<b>F</b>) opossums. (<b>H</b>) the zoomed area from the coronal brain section (<b>G</b>), showing just below the injection site; (<b>I</b>) the zoomed area from the anterior cortex, showing mCherry-expressing axons; and (<b>J</b>) the zoomed area from the contralateral neocortex. (<b>K</b>) Schematic representation of the coronal section presented in G, showing the injection site and fiber tract containing neocortical neuronal axons that cross the anterior commissure and reach the contralateral neocortex. The scale bar in (<b>A</b>), and (<b>F</b>) refers to (<b>D</b>), and (<b>B</b>,<b>C</b>,<b>E</b>), respectively. The scale bar in (<b>J</b>) refers to both images (<b>H</b>,<b>I</b>). 3V, third ventricle; AC, anterior commissure; CTX, cerebral cortex; HIP, hippocampus; PIR, piriform cortex; STR, striatum.</p> ">
Abstract
:1. Introduction
2. Results
2.1. BrdU-Labeled Cells in the Cerebral Cortex and Anterior Commissure
2.2. Cellular Organization of the Anterior Commissure
2.3. The Pattern of Neocortical Axons Forming the Anterior Commissure
3. Discussion
4. Materials and Methods
4.1. Animals
4.2. Injections of BrdU, DiI and Viruses
4.3. Brain Tissue Preparation
4.4. Myelin Staining by Gallyas Silver Impregnation
4.5. Immunofluorescent Labeling
4.6. Immunolabeling for BrdU
Double Immunolabeling
4.7. Western Blot
4.8. Data Analysis and Statistics
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Luo, Z.X.; Yuan, C.X.; Meng, Q.J.; Ji, Q. A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 2011, 476, 442–445. [Google Scholar] [CrossRef]
- Rose, R.W. Embryonic growth rates of marsupials with a note on monotremes. J. Zool. Lond. 1989, 218, 11–16. [Google Scholar] [CrossRef]
- Bartkowska, K.; Tepper, B.; Turlejski, K.; Djavadian, R. Postnatal and Adult Neurogenesis in Mammals, Including Marsupials. Cells 2022, 11, 2735–2741. [Google Scholar] [CrossRef]
- Saunders, N.R.; Adam, E.; Reader, M.; Møllgrd, K. Monodelphis domestica (grey short-tailed opossum): An accessible model for studies of early neocortical development. Anat. Embryol. 1989, 180, 227–236. [Google Scholar] [CrossRef]
- Ashwell, K.W.S. The Neurobiology of Australian Marsupials. In Brain Evolution in the Other Mammalian Radiation; Cambridge University Press: Cambridge, UK; New York, NY, USA, 2010; pp. 18–119. [Google Scholar]
- Bartkowska, K.; Gajerska, M.; Turlejski, K.; Djavadian, R.L. Expression of TrkC receptors in the developing brain of the Monodelphis opossum and its effect on the development of cortical cells. PLoS ONE 2013, 8, e74346. [Google Scholar] [CrossRef] [PubMed]
- Reynolds, M.L.; Cavanagh, M.E.; Dziegielewska, K.M.; Hinds, L.A.; Saunders, N.R. Tyndale-Biscoe CH. Postnatal development of the telencephalon of the tammar wallaby (Macropus eugenii). An accessible model of neocortical differentiation. Anat. Embryol. 1985, 173, 81–94. [Google Scholar] [CrossRef]
- Fenlon, L.R.; Suarez, R.; Lynton, Z.; Richards, L.J. The evolution, formation and connectivity of the anterior commissure. Semin. Cell Dev. Biol. 2021, 118, 50–59. [Google Scholar] [CrossRef] [PubMed]
- Donahoo, A.L.; Richards, L.J. Understanding the mechanisms of callosal development through the use of transgenic mouse models. Semin. Pediatr. Neurol. 2009, 16, 127–142. [Google Scholar] [CrossRef] [PubMed]
- Henkemeyer, M.; Orioli, D.; Henderson, J.T.; Saxton, T.M.; Roder, J.; Pawson, T.; Klein, R. Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 1996, 86, 35–46. [Google Scholar] [CrossRef]
- Hu, Z.; Yue, X.; Shi, G.; Yue, Y.; Crockett, D.P.; Blair-Flynn, J.; Reuhl, K.; Tessarollo, L.; Zhou, R. Corpus callosum deficiency in transgenic mice expressing a truncated ephrin-A receptor. J. Neurosci. 2003, 23, 10963–10970. [Google Scholar] [CrossRef]
- Srivatsa, S.; Parthasarathy, S.; Britanova, O.; Bormuth, I.; Donahoo, A.L.; Ackerman, S.L.; Richards, L.J.; Tarabykin, V. Unc5C and DCC act downstream of Ctip2 and Satb2 and contribute to corpus callosum formation. Nat. Commun. 2014, 5, 3708. [Google Scholar] [CrossRef]
- Bagri, A.; Marín, O.; Plump, A.S.; Mak, J.; Pleasure, S.J.; Rubenstein, J.L.; Tessier-Lavigne, M. Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 2002, 33, 233–248. [Google Scholar] [CrossRef] [PubMed]
- Piper, M.; Plachez, C.; Zalucki, O.; Fothergill, T.; Goudreau, G.; Erzurumlu, R.; Gu, C.; Richards, L.J. Neuropilin 1-Sema signaling regulates crossing of cingulate pioneering axons during development of the corpus callosum. Cereb. Cortex 2009, 19 (Suppl. S1), i11–i21. [Google Scholar] [CrossRef] [PubMed]
- Cheung, A.F.; Kondo, S.; Abdel-Mannan, O.; Chodroff, R.A.; Sirey, T.M.; Bluy, L.E.; Webber, N.; DeProto, J.; Karlen, S.J.; Krubitzer, L.; et al. The subventricular zone is the developmental milestone of a 6-layered neocortex: Comparisons in metatherian and eutherian mammals. Cereb. Cortex 2010, 20, 1071–1081. [Google Scholar] [CrossRef] [PubMed]
- Puzzolo, E.; Mallamaci, A. Cortico-cerebral histogenesis in the opossum Monodelphis domestica: Generation of a hexalaminar neocortex in the absence of a basal proliferative compartment. Neural. Dev. 2010, 5, 8. [Google Scholar] [CrossRef] [PubMed]
- Bartkowska, K.; Tepper, B.; Gawda, A.; Jarosik, M.; Sobolewska, P.; Turlejski, K.; Djavadian, R.L. Inhibition of TrkB- and TrkC-Signaling Pathways Affects Neurogenesis in the Opossum Developing Neocortex. Cereb. Cortex 2019, 29, 3666–3675. [Google Scholar] [CrossRef]
- Kushwaha, R.S.; VandeBerg, J.F.; VandeBerg, J.L. Effect of dietary cholesterol with or without saturated fat on plasma lipoprotein cholesterol levels in the laboratory opossum (Monodelphis domestica) model for diet-induced hyperlipidaemia. Br. J. Nutr. 2004, 92, 63–70. [Google Scholar] [CrossRef]
- Kolb, B.; Pedersen, B.; Ballermann, M.; Gibb, R.; Whishaw, I.Q. Embryonic and postnatal injections of bromodeoxyuridine produce age-dependent morphological and behavioral abnormalities. J. Neurosci. 1999, 19, 2337–2346. [Google Scholar] [CrossRef]
- Kuwagata, M.; Ogawa, T.; Nagata, T.; Shioda, S. The evaluation of early embryonic neurogenesis after exposure to the genotoxic agent 5-bromo-2′-deoxyuridine in mice. Neurotoxicology 2007, 28, 780–789. [Google Scholar] [CrossRef]
- Turovsky, E.A.; Turovskaya, M.V.; Fedotova, E.I.; Babaev, A.A.; Tarabykin, V.S.; Varlamova, E.G. Role of Satb1 and Satb2 Transcription Factors in the Glutamate Receptors Expression and Ca2+ Signaling in the Cortical Neurons In Vitro. Int. J. Mol. Sci. 2021, 22, 5968. [Google Scholar] [CrossRef]
- Nomura, T.; Yamashita, W.; Gotoh, H.; Ono, K. Species-Specific Mechanisms of Neuron Subtype Specification Reveal Evolutionary Plasticity of Amniote Brain Development. Cell Rep. 2018, 22, 3142–3151. [Google Scholar] [CrossRef] [PubMed]
- Britanova, O.; Akopov, S.; Lukyanov, S.; Gruss, P.; Tarabykin, V. Novel transcription factor Satb2 interacts with matrix attachment region DNA elements in a tissue-specific manner and demonstrates cell-type-dependent expression in the developing mouse CNS. Eur. J. Neurosci. 2005, 21, 658–668. [Google Scholar] [CrossRef] [PubMed]
- Szemes, M.; Gyorgy, A.; Paweletz, C.; Dobi, A.; Agoston, D.V. Isolation and characterization of SATB2, a novel AT-rich DNA binding protein expressed in development- and cell-specific manner in the rat brain. Neurochem. Res. 2006, 31, 237–246. [Google Scholar] [CrossRef] [PubMed]
- Kohno, T.; Ishii, K.; Hirota, Y. Reelin-Nrp1 Interaction Regulates Neocortical Dendrite Development in a Context-Specific Manner. J. Neurosci. 2020, 40, 8248–8261. [Google Scholar] [CrossRef] [PubMed]
- Zhou, J.; Wen, Y.; She, L.; Sui, Y.N.; Liu, L.; Richards, L.J.; Poo, M.M. Axon position within the corpus callosum determines contralateral cortical projection. Proc. Natl. Acad. Sci. USA 2013, 110, E2714–E2723. [Google Scholar] [CrossRef]
- Noctor, S.C.; Flint, A.C.; Weissman, T.A.; Dammerman, R.S.; Kriegstein, A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001, 409, 714–720. [Google Scholar] [CrossRef] [PubMed]
- Rakic, P. Evolution of the neocortex: A perspective from developmental biology. Nat. Rev. Neurosci. 2009, 10, 724–735. [Google Scholar] [CrossRef]
- Clavreul, S.; Abdeladim, L.; Hernández-Garzón, E. Cortical astrocytes develop in a plastic manner at both clonal and cellular levels. Nat. Commun. 2019, 10, 4884. [Google Scholar] [CrossRef]
- Tabata, H. Diverse subtypes of astrocytes and their development during corticogenesis. Front. Neurosci. 2015, 9, 114. [Google Scholar] [CrossRef]
- Polleux, F.; Dehay, C.; Kennedy, H. The timetable of laminar neurogenesis contributes to the specification of cortical areas in mouse isocortex. J. Comp. Neurol. 1997, 385, 95–116. [Google Scholar] [CrossRef]
- Heath, C.J.; Jones, E.G. Interhemispheric pathways in the absence of a corpus callosum. An experimental study of commissural connections in the marsupial phalanger. J. Anat. 1971, 109, 253–270. [Google Scholar]
- Cummings, D.M.; Malun, D.; Brunjes, P.C. Development of the anterior commissure in the opossum: Midline extracellular space and glia coincide with early axon decussation. J. Neurobiol. 1997, 32, 403–414. [Google Scholar] [CrossRef]
- Sansom, S.N.; Livesey, F.J. Gradients in the brain: The control of the development of form and function in the cerebral cortex. Cold Spring Harb. Perspect. Biol. 2009, 1, a002519. [Google Scholar] [CrossRef] [PubMed]
- Cabana, T.; Martin, G.F. The development of commissural connections of somatic motor-sensory areas of neocortex in the North American opossum. Anat. Embryol. 1985, 171, 121–128. [Google Scholar] [CrossRef] [PubMed]
- Granger, E.M.; Masterton, R.B.; Glendenning, K.K. Origin of interhemispheric fibers in acallosal opossum (with a comparison to callosal origins in rat). J. Comp. Neurol. 1985, 241, 82–98. [Google Scholar] [CrossRef] [PubMed]
- Aboitiz, F.; Montiel, J. One hundred million years of interhemispheric communication: The history of the corpus callosum. Braz. J. Med. Biol. Res. 2003, 36, 409–420. [Google Scholar] [CrossRef] [PubMed]
- Land, P.W.; Monaghan, A.P. Expression of the transcription factor, tailless, is required for formation of superficial cortical layers. Cereb. Cortex 2003, 13, 921–931. [Google Scholar] [CrossRef] [PubMed]
- Gyorgy, A.B.; Szemes, M.; de Juan Romero, C.; Tarabykin, V.; Agoston, D.V. SATB2 interacts with chromatin-remodeling molecules in differentiating cortical neurons. Eur. J. Neurosci. 2008, 27, 865–873. [Google Scholar] [CrossRef] [PubMed]
- Baranek, C.; Dittrich, M.; Parthasarathy, S.; Bonnon, C.G.; Britanova, O.; Lanshakov, D.; Boukhtouche, F.; Sommer, J.E.; Colmenares, C.; Tarabykin, V.; et al. Protooncogene Ski cooperates with the chromatin-remodeling factor Satb2 in specifying callosal neurons. Proc. Natl. Acad. Sci. USA 2012, 109, 3546–3551. [Google Scholar] [CrossRef]
- Silver, J.; Lorenz, S.E.; Wahlsten, D.; Coughlin, J. Axonal guidance during development of the great cerebral commissures: Descriptive and experimental studies, in vivo, on the role of preformed glial pathways. J. Comp. Neurol. 1982, 210, 10–29. [Google Scholar] [CrossRef]
- Rash, B.G.; Richards, L.J. A role for cingulate pioneering axons in the development of the corpus callosum. J. Comp. Neurol. 2001, 434, 147–157. [Google Scholar] [CrossRef]
- Alcamo, E.A.; Chirivella, L.; Dautzenberg, M.; Dobreva, G.; Fariñas, I.; Grosschedl, R.; McConnell, S.K. Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron 2008, 57, 364–377. [Google Scholar] [CrossRef]
- Valentino, K.L.; Jones, E.G. The early formation of the corpus callosum: A light and electron microscopic study in foetal and neonatal rats. J. Neurocytol. 1982, 11, 583–609. [Google Scholar] [CrossRef] [PubMed]
- Santacana, M.; Heredia, M.; Valverde, F. Development of the main efferent cells of the olfactory bulb and of the bulbar component of the anterior commissure. Brain Res. Dev. Brain Res. 1992, 65, 75–83. [Google Scholar] [CrossRef]
- Berbel, P.; Innocenti, G.M. The development of the corpus callosum in cats: A light- and electron-microscopic study. J. Comp. Neurol. 1988, 276, 132–156. [Google Scholar] [CrossRef]
- Pires-Neto, M.A.; Lent, R. The prenatal development of the anterior commissure in hamsters: Pioneer fibers lead the way. Brain Res. Dev. Brain Res. 1993, 72, 59–66. [Google Scholar] [CrossRef]
- Shang, F.; Ashwell, K.W.; Marotte, L.R.; Waite, P.M. Development of commissural neurons in the wallaby (Macropus eugenii). J. Comp. Neurol. 1997, 387, 507–523. [Google Scholar] [CrossRef]
- Ashwell, K.W.; Waite, P.M.; Marotte, L. Ontogeny of the projection tracts and commissural fibres in the forebrain of the tammar wallaby (Macropus eugenii): Timing in comparison with other mammals. Brain Behav. Evol. 1996, 47, 8–22. [Google Scholar] [CrossRef]
- Miller, F.D.; Gauthier, A.S. Timing is everything: Making neurons versus glia in the developing cortex. Neuron 2007, 54, 357–369. [Google Scholar] [CrossRef]
- Ge, W.P.; Miyawaki, A.; Gage, F.H.; Jan, Y.N. Local generation of glia is a major astrocyte source in postnatal cortex. Nature 2012, 484, 376–380. [Google Scholar] [CrossRef]
- Falcone, C. Evolution of astrocytes: From invertebrates to vertebrates. Front. Cell Dev. Biol. 2022, 10, 931311. [Google Scholar] [CrossRef]
- Lu, Q.R.; Sun, T.; Zhu, Z.; Ma, N.; Garcia, M.; Stiles, C.D.; Rowitch, D.H. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 2002, 109, 75–86. [Google Scholar] [CrossRef]
- Cai, J.; Chen, Y.; Cai, W.H.; Hurlock, E.C.; Wu, H.; Kernie, S.G.; Parada, L.F.; Lu, Q.R. A crucial role for Olig2 in white matter astrocyte development. Development 2007, 134, 1887–1899. [Google Scholar] [CrossRef]
- Cao, G.; Sun, C.; Shen, H.; Qu, D.; Shen, C.; Lu, H. Conditional Deletion of Foxg1 Delayed Myelination during Early Postnatal Brain Development. Int. J. Mol. Sci. 2023, 24, 13921. [Google Scholar] [CrossRef] [PubMed]
- Ono, K.; Takebayashi, H.; Ikeda, K.; Furusho, M.; Nishizawa, T.; Watanabe, K.; Ikenaka, K. Regional- and temporal-dependent changes in the differentiation of Olig2 progenitors in the forebrain, and the impact on astrocyte development in the dorsal pallium. Dev. Biol. 2008, 320, 456–468. [Google Scholar] [CrossRef] [PubMed]
- Silver, J.; Edwards, M.A.; Levitt, P. Immunocytochemical demonstration of early appearing astroglial structures that form boundaries and pathways along axon tracts in the fetal brain. J. Comp. Neurol. 1993, 328, 415–436. [Google Scholar] [CrossRef] [PubMed]
- Fletcher, J.L.; Makowiecki, K.; Cullen, C.L.; Young, K.M. Oligodendrogenesis and myelination regulate cortical development, plasticity and circuit function. Semin. Cell Dev. Biol. 2021, 118, 14–23. [Google Scholar] [CrossRef] [PubMed]
- Smith, K.M.; Ohkubo, Y.; Maragnoli, M.E.; Rašin, M.R.; Schwartz, M.L.; Šestan, N.; Vaccarino, F.M. Midline radial glia translocation and corpus callosum formation require FGF signaling. Nat. Neurosci. 2006, 9, 787–797. [Google Scholar] [CrossRef] [PubMed]
- Bignami, A.; Eng, L.F.; Dahl, D.; Uyeda, C.T. Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res. 1972, 43, 429–435. [Google Scholar] [CrossRef] [PubMed]
- Shu, T.; Richards, L.J. Cortical axon guidance by the glial wedge during the development of the corpus callosum. J. Neurosci. 2001, 21, 2749–2758. [Google Scholar] [CrossRef]
- Chinn, G.A.; Hirokawa, K.E.; Chuang, T.M.; Urbina, C.; Patel, F.; Fong, J.; Funatsu, N.; Monuki, E.S. Agenesis of the Corpus Callosum Due to Defective Glial Wedge Formation in Lhx2 Mutant Mice. Cereb. Cortex 2015, 25, 2707–2718. [Google Scholar] [CrossRef] [PubMed]
- Nishikimi, M.; Oishi, K.; Nakajima, K. Axon guidance mechanisms for establishment of callosal connections. Neural. Plast. 2013, 2013, 149060. [Google Scholar] [CrossRef] [PubMed]
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Bartkowska, K.; Koguc-Sobolewska, P.; Djavadian, R.; Turlejski, K. Astrocytes of the Anterior Commissure Regulate the Axon Guidance Pathways of Newly Generated Neocortical Neurons in the Opossum Monodelphis domestica. Int. J. Mol. Sci. 2024, 25, 1476. https://doi.org/10.3390/ijms25031476
Bartkowska K, Koguc-Sobolewska P, Djavadian R, Turlejski K. Astrocytes of the Anterior Commissure Regulate the Axon Guidance Pathways of Newly Generated Neocortical Neurons in the Opossum Monodelphis domestica. International Journal of Molecular Sciences. 2024; 25(3):1476. https://doi.org/10.3390/ijms25031476
Chicago/Turabian StyleBartkowska, Katarzyna, Paulina Koguc-Sobolewska, Ruzanna Djavadian, and Krzysztof Turlejski. 2024. "Astrocytes of the Anterior Commissure Regulate the Axon Guidance Pathways of Newly Generated Neocortical Neurons in the Opossum Monodelphis domestica" International Journal of Molecular Sciences 25, no. 3: 1476. https://doi.org/10.3390/ijms25031476