Involvement of strawberry notch homologue 1 in neurite outgrowth of cortical neurons.


Journal

Development, growth & differentiation
ISSN: 1440-169X
Titre abrégé: Dev Growth Differ
Pays: Japan
ID NLM: 0356504

Informations de publication

Date de publication:
Sep 2022
Historique:
revised: 15 06 2022
received: 04 06 2022
accepted: 15 06 2022
pubmed: 4 9 2022
medline: 1 10 2022
entrez: 3 9 2022
Statut: ppublish

Résumé

When the regulation of axonal and dendritic growth is altered, the neuronal network becomes disordered, which may contribute to the development of psychiatric disorders. Some genome analyses have suggested relationships between mutations in strawberry notch homologue 1 (SBNO1) and neurodevelopmental disorders. However, the function of SBNO1 has not yet been reported. Here, SBNO1 expression pattern during the development of the cerebral cortex in mice was examined. SBNO1 was strongly expressed in the cortical plate and its expression was maintained at a low level during the postnatal stage. CRISPR/Cas9-based knockout of Sbno1 in Neuro2A cultured cells showed delayed growth of neurites. A cortical neuron-specific conditional knockout mouse was constructed, which resulted in hypotrophy of axon bundles and dendrites in cortical neurons. Thus, when mutated, SBNO1 is a candidate gene for psychiatric diseases, such as schizophrenia, as suggested by human genome studies.

Identifiants

pubmed: 36057539
doi: 10.1111/dgd.12802
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

379-394

Informations de copyright

© 2022 Japanese Society of Developmental Biologists.

Références

Baba, K., Dekimoto, H., Muraoka, D., Agata, K., Terashima, T., & Katsuyama, Y. (2006). A mouse homologue of strawberry notch is transcriptionally regulated by Reelin signal. Biochemical and Biophysical Research Communications, 350(4), 842-849. https://doi.org/10.1016/j.bbrc.2006.09.135
Beaudoin, G. M., Lee, S. H., Singh, D., Yuan, Y., Ng, Y. G., Reichardt, L. F., & Arikkath, J. (2012). Culturing pyramidal neurons from the early postnatal mouse hippocampus and cortex. Nature Protocols, 7(9), 1741-1754. https://doi.org/10.1038/nprot.2012.099
Britanova, O., de Juan Romero, C., Cheung, A., Kwan, K. Y., Schwark, M., Gyorgy, A., Vogel, T., Akopov, S., Mitkovski, M., Agoston, D., Šestan, N., Molnár, Z., & Tarabykin, V. (2008). Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron, 57(3), 378-392. https://doi.org/10.1016/j.neuron.2007.12.028
Bulayeva, K., Lesch, K. P., Bulayev, O., Walsh, C., Glatt, S., Gurgenova, F., Omarova, J., Berdichevets, I., & Thompson, P. M. (2015). Genomic structural variants are linked with intellectual disability. Journal of Neural Transmission (Vienna), 122(9), 1289-1301. https://doi.org/10.1007/s00702-015-1366-8
Bulfone, A., Kim, H. J., Puelles, L., Porteus, M. H., Grippo, J. F., & Rubenstein, J. L. (1993). The mouse dlx-2 (Tes-1) gene is expressed in spatially restricted domains of the forebrain, face and limbs in midgestation mouse embryos. Mechanisms of Development, 40(3), 129-140. https://doi.org/10.1016/0925-4773(93)90071-5
Bulfone, A., Puelles, L., Porteus, M. H., Frohman, M. A., Martin, G. R., & Rubenstein, J. L. (1993). Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. The Journal of Neuroscience, 13(7), 3155-3172.
Celio, M. R., Schärer, L., Morrison, J. H., Norman, A. W., & Bloom, F. E. (1986). Calbindin immunoreactivity alternates with cytochrome c-oxidase-rich zones in some layers of the primate visual cortex. Nature, 323(6090), 715-717. https://doi.org/10.1038/323715a0
Chen, B., Schaevitz, L. R., & McConnell, S. K. (2005). Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proceedings of the National Academy of Sciences of the United States of America, 102(47), 17184-17189. https://doi.org/10.1073/pnas.0508732102
Chen, L., Chatterjee, M., & Li, J. Y. (2010). The mouse homeobox gene Gbx2 is required for the development of cholinergic interneurons in the striatum. The Journal of Neuroscience, 30(44), 14824-14834. https://doi.org/10.1523/JNEUROSCI.3742-10.2010
Corbin, J. G., Gaiano, N., Juliano, S. L., Poluch, S., Stancik, E., & Haydar, T. F. (2008). Regulation of neural progenitor cell development in the nervous system. Journal of Neurochemistry, 106(6), 2272-2287. https://doi.org/10.1111/j.1471-4159.2008.05522.x
Couso, J. P., Knust, E., & Martinez Arias, A. (1995). Serrate and wingless cooperate to induce vestigial gene expression and wing formation in drosophila. Current Biology, 5(12), 1437-1448. https://doi.org/10.1016/s0960-9822(95)00281-8
Coyle-Thompson, C. A., & Banerjee, U. (1993). The strawberry notch gene functions with notch in common developmental pathways. Development, 119(2), 377-395. https://doi.org/10.1242/dev.119.2.377
Diaz-Benjumea, F. J., & Cohen, S. M. (1995). Serrate signals through notch to establish a wingless-dependent organizer at the dorsal/ventral compartment boundary of the drosophila wing. Development, 121(12), 4215-4225. https://doi.org/10.1242/dev.121.12.4215
Doherty, D., Feger, G., Younger-Shepherd, S., Jan, L. Y., & Jan, Y. N. (1996). Delta is a ventral to dorsal signal complementary to serrate, another notch ligand, in drosophila wing formation. Genes & Development, 10(4), 421-434. https://doi.org/10.1101/gad.10.4.421
Eisen, J. A., Sweder, K. S., & Hanawalt, P. C. (1995). Evolution of the SNF2 family of proteins: Subfamilies with distinct sequences and functions. Nucleic Acids Research, 23(14), 2715-2723. https://doi.org/10.1093/nar/23.14.2715
Eisen, J. S., & Smith, J. C. (2008). Controlling morpholino experiments: don't stop making antisense. Development, 135(10), 1735-1743. https://doi.org/10.1242/dev.001115
El Bejjani, R., & Hammarlund, M. (2012). Notch signaling inhibits axon regeneration. Neuron, 73(2), 268-278. https://doi.org/10.1016/j.neuron.2011.11.017
Eng, L. F., Vanderhaeghen, J. J., Bignami, A., & Gerstl, B. (1971). An acidic protein isolated from fibrous astrocytes. Brain Research, 28(2), 351-354. https://doi.org/10.1016/0006-8993(71)90668-8
Englund, C., Fink, A., Lau, C., Pham, D., Daza, R. A., Bulfone, A., Kowalczyk, T., & Hevner, R. F. (2005). Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. The Journal of Neuroscience, 25(1), 247-251. https://doi.org/10.1523/JNEUROSCI.2899-04.2005
Furusho, M., Ono, K., Takebayashi, H., Masahira, N., Kagawa, T., Ikeda, K., & Ikenaka, K. (2006). Involvement of the Olig2 transcription factor in cholinergic neuron development of the basal forebrain. Developmental Biology, 293(2), 348-357. https://doi.org/10.1016/j.ydbio.2006.01.031
Gilmore, E. C., & Herrup, K. (1997). Cortical development: layers of complexity. Current Biology, 7(4), R231-R234. https://doi.org/10.1016/s0960-9822(06)00108-4
Giniger, E. (1998). A role for Abl in notch signaling. Neuron, 20(4), 667-681. https://doi.org/10.1016/s0896-6273(00)81007-7
Giniger, E. (2012). Notch signaling and neural connectivity. Current Opinion in Genetics & Development, 22(4), 339-346. https://doi.org/10.1016/j.gde.2012.04.003
Girard, S. L., Gauthier, J., Noreau, A., Xiong, L., Zhou, S., Jouan, L., Dionne-Laporte, A., Spiegelman, D., Henrion, E., Diallo, O., Thibodeau, P., Bachand, I., Bao, J. Y. J., Tong, A. H. Y., Lin, C. H., Millet, B., Jaafari, N., Joober, R., Dion, P. A., … Rouleau, G. A. (2011). Increased exonic de novo mutation rate in individuals with schizophrenia. Nature Genetics, 43(9), 860-863. https://doi.org/10.1038/ng.886
Goebbels, S., Bormuth, I., Bode, U., Hermanson, O., Schwab, M. H., & Nave, K. A. (2006). Genetic targeting of principal neurons in neocortex and hippocampus of NEX-Cre mice. Genesis, 44(12), 611-621. https://doi.org/10.1002/dvg.20256
Guo, T., Lu, Y., Li, P., Yin, M. X., Lv, D., Zhang, W., Wang, H., Zhou, Z., Ji, H., Zhao, Y., & Zhang, L. (2013). A novel partner of scalloped regulates hippo signaling via antagonizing scalloped-Yorkie activity. Cell Research, 23(10), 1201-1214. https://doi.org/10.1038/cr.2013.120
Gupta, A., Tsai, L. H., & Wynshaw-Boris, A. (2002). Life is a journey: A genetic look at neocortical development. Nature Reviews. Genetics, 3(5), 342-355. https://doi.org/10.1038/nrg799
Hart, I. K., Richardson, W. D., Heldin, C. H., Westermark, B., & Raff, M. C. (1989). PDGF receptors on cells of the oligodendrocyte-type-2 astrocyte (O-2A) cell lineage. Development, 105(3), 595-603. https://doi.org/10.1242/dev.105.3.595
Hevner, R. F., Shi, L., Justice, N., Hsueh, Y., Sheng, M., Smiga, S., Bulfone, A., Goffinet, A. M., Campagnoni, A. T., & Rubenstein, J. L. R. (2001). Tbr1 regulates differentiation of the preplate and layer 6. Neuron, 29(2), 353-366. https://doi.org/10.1016/s0896-6273(01)00211-2
Hilker, R., Helenius, D., Fagerlund, B., Skytthe, A., Christensen, K., Werge, T. M., Nordentoft, M., & Glenthøj, B. (2018). Heritability of schizophrenia and schizophrenia Spectrum based on the Nationwide Danish twin register. Biological Psychiatry, 83(6), 492-498. https://doi.org/10.1016/j.biopsych.2017.08.017
Joris, M., Schloesser, M., Baurain, D., Hanikenne, M., Muller, M., & Motte, P. (2017). Number of inadvertent RNA targets for morpholino knockdown in Danio rerio is largely underestimated: Evidence from the study of Ser/Arg-rich splicing factors. Nucleic Acids Research, 45(16), 9547-9557. https://doi.org/10.1093/nar/gkx638
Jung, S. H., Evans, C. J., Uemura, C., & Banerjee, U. (2005). The drosophila lymph gland as a developmental model of hematopoiesis. Development, 132(11), 2521-2533. https://doi.org/10.1242/dev.01837
Kageyama, R., & Ohtsuka, T. (1999). The notch-Hes pathway in mammalian neural development. Cell Research, 9(3), 179-188. https://doi.org/10.1038/sj.cr.7290016
Kageyama, R., Ohtsuka, T., Shimojo, H., & Imayoshi, I. (2009). Dynamic regulation of notch signaling in neural progenitor cells. Current Opinion in Cell Biology, 21(6), 733-740. https://doi.org/10.1016/j.ceb.2009.08.009
Kawaguchi, Y., & Kondo, S. (2002). Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. Journal of Neurocytology, 31(3-5), 277-287. https://doi.org/10.1023/a:1024126110356
Kimura, N., Nakashima, K., Ueno, M., Kiyama, H., & Taga, T. (1999). A novel mammalian T-box-containing gene, Tbr2, expressed in mouse developing brain. Brain Research. Developmental Brain Research, 115(2), 183-193. https://doi.org/10.1016/s0165-3806(99)00064-4
Kohtz, J. D., Baker, D. P., Corte, G., & Fishell, G. (1998). Regionalization within the mammalian telencephalon is mediated by changes in responsiveness to sonic hedgehog. Development, 125(24), 5079-5089. https://doi.org/10.1242/dev.125.24.5079
Kok, F. O., Shin, M., Ni, C. W., Gupta, A., Grosse, A. S., van Impel, A., Kirchmaier, B. C., Peterson-Maduro, J., Kourkoulis, G., Male, I., DeSantis, D. F., Sheppard-Tindell, S., Ebarasi, L., Betsholtz, C., Schulte-Merker, S., Wolfe, S. A., & Lawson, N. D. (2015). Reverse genetic screening reveals poor correlation between morpholino-induced and mutant phenotypes in zebrafish. Developmental Cell, 32(1), 97-108. https://doi.org/10.1016/j.devcel.2014.11.018
Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E., & Tanaka, K. (2006). Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature, 441(7095), 880-884. https://doi.org/10.1038/nature04723
Kopan, R. (2012). Notch signaling. Cold Spring Harbor Perspectives in Biology, 4(10), a011213. https://doi.org/10.1101/cshperspect.a011213
Kovall, R. A. (2008). More complicated than it looks: Assembly of notch pathway transcription complexes. Oncogene, 27(38), 5099-5109. https://doi.org/10.1038/onc.2008.223
Lai, E. C. (2002). Keeping a good pathway down: Transcriptional repression of notch pathway target genes by CSL proteins. EMBO Reports, 3(9), 840-845. https://doi.org/10.1093/embo-reports/kvf170
Louvi, A., & Artavanis-Tsakonas, S. (2006). Notch signalling in vertebrate neural development. Nature Reviews. Neuroscience, 7(2), 93-102. https://doi.org/10.1038/nrn1847
Mackintosh, S. G., & Raney, K. D. (2006). DNA unwinding and protein displacement by superfamily 1 and superfamily 2 helicases. Nucleic Acids Research, 34(15), 4154-4159. https://doi.org/10.1093/nar/gkl501
Majumdar, A., Nagaraj, R., & Banerjee, U. (1997). Strawberry notch encodes a conserved nuclear protein that functions downstream of notch and regulates gene expression along the developing wing margin of drosophila. Genes & Development, 11(10), 1341-1353. https://doi.org/10.1101/gad.11.10.1341
Marin, O., Anderson, S. A., & Rubenstein, J. L. (2000). Origin and molecular specification of striatal interneurons. The Journal of Neuroscience, 20(16), 6063-6076.
Menezes, J. R., & Luskin, M. B. (1994). Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. The Journal of Neuroscience, 14(9), 5399-5416.
Mullen, R. J., Buck, C. R., & Smith, A. M. (1992). NeuN, a neuronal specific nuclear protein in vertebrates. Development, 116(1), 201-211. https://doi.org/10.1242/dev.116.1.201
Olmsted, J. B., Carlson, K., Klebe, R., Ruddle, F., & Rosenbaum, J. (1970). Isolation of microtubule protein from cultured mouse neuroblastoma cells. Proceedings of the National Academy of Sciences of the United States of America, 65(1), 129-136. https://doi.org/10.1073/pnas.65.1.129
Reay, W. R., & Cairns, M. J. (2020). Pairwise common variant meta-analyses of schizophrenia with other psychiatric disorders reveals shared and distinct gene and gene-set associations. Translational Psychiatry, 10(1), 134. https://doi.org/10.1038/s41398-020-0817-7
Redmond, L., Oh, S. R., Hicks, C., Weinmaster, G., & Ghosh, A. (2000). Nuclear Notch1 signaling and the regulation of dendritic development. Nature Neuroscience, 3(1), 30-40. https://doi.org/10.1038/71104
Résibois, A., & Rogers, J. H. (1992). Calretinin in rat brain: An immunohistochemical study. Neuroscience, 46(1), 101-134. https://doi.org/10.1016/0306-4522(92)90012-q
Rosner, A., & Rinkevich, B. (2007). The DDX3 subfamily of the DEAD box helicases: Divergent roles as unveiled by studying different organisms and in vitro assays. Current Medicinal Chemistry, 14(23), 2517-2525. https://doi.org/10.2174/092986707782023677
Schmitt, A., Malchow, B., Hasan, A., & Falkai, P. (2014). The impact of environmental factors in severe psychiatric disorders. Frontiers in Neuroscience, 8, 19. https://doi.org/10.3389/fnins.2014.00019
Sestan, N., Artavanis-Tsakonas, S., & Rakic, P. (1999). Contact-dependent inhibition of cortical neurite growth mediated by notch signaling. Science, 286(5440), 741-746. https://doi.org/10.1126/science.286.5440.741
Sharma, D., & Jankowsky, E. (2014). The Ded1/DDX3 subfamily of DEAD-box RNA helicases. Critical Reviews in Biochemistry and Molecular Biology, 49(4), 343-360. https://doi.org/10.3109/10409238.2014.931339
Shi, M., Liu, Z., Lv, Y., Zheng, M., du, F., Zhao, G., Huang, Y., Chen, J., Han, H., & Ding, Y. (2011). Forced notch signaling inhibits commissural axon outgrowth in the developing chick central nerve system. PLoS One, 6(1), e14570. https://doi.org/10.1371/journal.pone.0014570
Sholl, D. A. (1953). Dendritic organization in the neurons of the visual and motor cortices of the cat. Journal of Anatomy, 87(4), 387-406.
Simms, C. L., & Baillie, D. L. (2010). A strawberry notch homolog, let-765/nsh-1, positively regulates lin-3/egf expression to promote RAS-dependent vulval induction in C. elegans. Developmental Biology, 341(2), 472-485. https://doi.org/10.1016/j.ydbio.2010.03.004
Sugiyama, T., Osumi, N., & Katsuyama, Y. (2013). The germinal matrices in the developing dentate gyrus are composed of neuronal progenitors at distinct differentiation stages. Developmental Dynamics, 242(12), 1442-1453. https://doi.org/10.1002/dvdy.24035
Sussel, L., Marin, O., Kimura, S., & Rubenstein, J. L. (1999). Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: Evidence for a transformation of the pallidum into the striatum. Development, 126(15), 3359-3370. https://doi.org/10.1242/dev.126.15.3359
Taal, H. R., St Pourcain, B., Thiering, E., das, S., Mook-Kanamori, D. O., Warrington, N. M., Kaakinen, M., Kreiner-Møller, E., Bradfield, J. P., Freathy, R. M., Geller, F., Guxens, M., Cousminer, D. L., Kerkhof, M., Timpson, N. J., Ikram, M. A., Beilin, L. J., Bønnelykke, K., Buxton, J. L., … Jaddoe, V. W. V. (2012). Common variants at 12q15 and 12q24 are associated with infant head circumference. Nature Genetics, 44(5), 532-538. https://doi.org/10.1038/ng.2238
Takano, A., Zochi, R., Hibi, M., Terashima, T., & Katsuyama, Y. (2010). Expression of strawberry notch family genes during zebrafish embryogenesis. Developmental Dynamics, 239(6), 1789-1796. https://doi.org/10.1002/dvdy.22287
Takano, A., Zochi, R., Hibi, M., Terashima, T., & Katsuyama, Y. (2011). Function of strawberry notch family genes in the zebrafish brain development. The Kobe Journal of Medical Sciences, 56(5), E220-E230.
Takizawa, T., Meaburn, K. J., & Misteli, T. (2008). The meaning of gene positioning. Cell, 135(1), 9-13. https://doi.org/10.1016/j.cell.2008.09.026
Tarnowski, B. I., Spinale, F. G., & Nicholson, J. H. (1991). DAPI as a useful stain for nuclear quantitation. Biotechnic & Histochemistry, 66(6), 297-302.
Thyme, S. B., Pieper, L. M., Li, E. H., Pandey, S., Wang, Y., Morris, N. S., Sha, C., Choi, J. W., Herrera, K. J., Soucy, E. R., Zimmerman, S., Randlett, O., Greenwood, J., McCarroll, S. A., & Schier, A. F. (2019). Phenotypic landscape of schizophrenia-associated genes defines candidates and their shared functions. Cell, 177(2), 478-491.e420. https://doi.org/10.1016/j.cell.2019.01.048
Tsuda, L., Nagaraj, R., Zipursky, S. L., & Banerjee, U. (2002). An EGFR/Ebi/Sno pathway promotes delta expression by inactivating Su(H)/SMRTER repression during inductive notch signaling. Cell, 110(5), 625-637. https://doi.org/10.1016/s0092-8674(02)00875-9
Voss, A. K., Britto, J. M., Dixon, M. P., Sheikh, B. N., Collin, C., Tan, S. S., & Thomas, T. (2008). C3G regulates cortical neuron migration, preplate splitting and radial glial cell attachment. Development, 135(12), 2139-2149. https://doi.org/10.1242/dev.016725
Watanabe, T., Biggins, J. S., Tannan, N. B., & Srinivas, S. (2014). Limited predictive value of blastomere angle of division in trophectoderm and inner cell mass specification. Development, 141(11), 2279-2288. https://doi.org/10.1242/dev.103267
Watanabe, Y., Miyasaka, K. Y., Kubo, A., Kida, Y. S., Nakagawa, O., Hirate, Y., Sasaki, H., & Ogura, T. (2017). Notch and hippo signaling converge on strawberry notch 1 (Sbno1) to synergistically activate Cdx2 during specification of the trophectoderm. Scientific Reports, 7, 46135. https://doi.org/10.1038/srep46135
Xu, Y. F., Cai, Y. Q., Cai, G. Q., Jiang, J., Sheng, Z. J., Wang, Z. G., & Fei, J. (2008). Hypoalgesia in mice lacking GABA transporter subtype 1. Journal of Neuroscience Research, 86(2), 465-470. https://doi.org/10.1002/jnr.21499
Yagi, T., Tokunaga, T., Furuta, T., Nada, S., Yoshida, M., Tsukada, T., Saga, Y., Takeda, N., Ikawa, Y., & Aizawa, S. (1993). A novel ES cell line, TT2, with high germline-differentiating potency. Analytical Biochemistry, 214(1), 70-76. https://doi.org/10.1006/abio.1993.1458
Yoshihara, M., Adolfsen, B., Galle, K. T., & Littleton, J. T. (2005). Retrograde signaling by Syt 4 induces presynaptic release and synapse-specific growth. Science, 310(5749), 858-863. https://doi.org/10.1126/science.1117541
Zappone, M. V., Galli, R., Catena, R., Meani, N., de Biasi, S., Mattei, E., Tiveron, C., Vescovi, A. L., Lovell-Badge, R., Ottolenghi, S., & Nicolis, S. K. (2000). Sox2 regulatory sequences direct expression of a (beta)-geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells. Development, 127(11), 2367-2382. https://doi.org/10.1242/dev.127.11.2367
Zhao, H., Feng, J., Seidel, K., Shi, S., Klein, O., Sharpe, P., & Chai, Y. (2014). Secretion of shh by a neurovascular bundle niche supports mesenchymal stem cell homeostasis in the adult mouse incisor. Cell Stem Cell, 14(2), 160-173. https://doi.org/10.1016/j.stem.2013.12.013
Zhao, Y., Flandin, P., Long, J. E., Cuesta, M. D., Westphal, H., & Rubenstein, J. L. (2008). Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of Lhx6 mutants. The Journal of Comparative Neurology, 510(1), 79-99. https://doi.org/10.1002/cne.21772
Zhao, Y., Marín, O., Hermesz, E., Powell, A., Flames, N., Palkovits, M., Rubenstein, J. L. R., & Westphal, H. (2003). The LIM-homeobox gene Lhx8 is required for the development of many cholinergic neurons in the mouse forebrain. Proceedings of the National Academy of Sciences of the United States of America, 100(15), 9005-9010. https://doi.org/10.1073/pnas.1537759100
Zheng, Z., Lauritzen, J. S., Perlman, E., Robinson, C. G., Nichols, M., Milkie, D., Torrens, O., Price, J., Fisher, C. B., Sharifi, N., Calle-Schuler, S. A., Kmecova, L., Ali, I. J., Karsh, B., Trautman, E. T., Bogovic, J. A., Hanslovsky, P., Jefferis, G. S. X. E., Kazhdan, M., … Bock, D. D. (2018). A complete electron microscopy volume of the brain of adult Drosophila melanogaster. Cell, 174(3), 730-743.e722. https://doi.org/10.1016/j.cell.2018.06.019
Zhou, Z. D., Kumari, U., Xiao, Z. C., & Tan, E. K. (2010). Notch as a molecular switch in neural stem cells. IUBMB Life, 62(8), spcone. https://doi.org/10.1002/iub.372
Zilles, K. (2018). Brodmann: A pioneer of human brain mapping-his impact on concepts of cortical organization. Brain, 141(11), 3262-3278. https://doi.org/10.1093/brain/awy273

Auteurs

Munkhsoyol Erkhembaatar (M)

Division of Neuroanatomy, Department of Anatomy, Shiga University of Medical Science, Otsu, Japan.

Iroha Yamamoto (I)

Division of Neuroanatomy, Department of Anatomy, Shiga University of Medical Science, Otsu, Japan.

Fuduki Inoguchi (F)

Division of Neuroanatomy, Department of Anatomy, Shiga University of Medical Science, Otsu, Japan.

Kosuke Taki (K)

Division of Neuroanatomy, Department of Anatomy, Shiga University of Medical Science, Otsu, Japan.

Satoru Yamagishi (S)

Department of Anatomy & Neuroscience, Hamamatsu University School of Medicine, Hamamatsu, Japan.
Preeminent Medical Photonics Education & Research Center, Hamamatsu University School of Medicine, Hamamatsu, Japan.

Leanne Delaney (L)

Division of Neuroanatomy, Department of Anatomy, Shiga University of Medical Science, Otsu, Japan.
Department of Microbiology and Immunology, Dalhousie University, Halifax, Nova Scotia, Canada.

Nishibe Mariko (N)

Division of Neuroanatomy, Department of Anatomy, Shiga University of Medical Science, Otsu, Japan.

Takaya Abe (T)

Animal Resource Development Unit, Biosystem Dynamics Group, Division of Bio-Function Dynamics Imaging, Center for Life Science Technologies CDB RIKEN, Kobe, Japan.

Hiroshi Kiyonari (H)

Animal Resource Development Unit, Biosystem Dynamics Group, Division of Bio-Function Dynamics Imaging, Center for Life Science Technologies CDB RIKEN, Kobe, Japan.

Carina Hanashima (C)

Department of Biology, Faculty of Education and Integrated Arts and Sciences, Waseda University, Tokyo, Japan.

Hayato Naka-Kaneda (H)

Division of Neuroanatomy, Department of Anatomy, Shiga University of Medical Science, Otsu, Japan.

Dai Ihara (D)

Division of Neuroanatomy, Department of Anatomy, Shiga University of Medical Science, Otsu, Japan.

Yu Katsuyama (Y)

Division of Neuroanatomy, Department of Anatomy, Shiga University of Medical Science, Otsu, Japan.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH