Onecut factors and Pou2f2 regulate the distribution of V2 interneurons in the mouse developing spinal cord
Open accessPreprint — published as 10.3389/fncel.2019.00184
Abstract
Acquisition of proper neuronal identity and position is critical for the formation of neural circuits. In the embryonic spinal cord, cardinal populations of interneurons diversify into specialized subsets and migrate to defined locations within the spinal parenchyma. However, the factors that control interneuron diversification and migration remain poorly characterized. Here, we show that the Onecut transcription factors are necessary for proper diversification and distribution of the V2 interneurons in the developing spinal cord. Furthermore, we uncover that these proteins restrict and moderate the expression of spinal isoforms of Pou2f2 , a transcription factor known to regulate B-cell differentiation. By gain- or loss-of-function experiments, we show that Pou2f2 contribute to regulate the position of V2 populations in the developing spinal cord. Thus, we uncovered a genetic pathway that regulates the diversification and the distribution of V2 interneurons during embryonic development. Significance statement: In this study, we identify the Onecut and Pou2f2 transcription factors as regulators of spinal interneuron diversification and migration, two events that are critical for proper CNS development.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The lateral V2a subgroup diversifies further into subgroups labelled by Shox2 and Maf/onecut family TFs.
“Furthermore, the lateral subgroup appears to diversify further into subgroups that are labelled by Shox2 and Maf/onecut family TFs (Francius et al., 2013; Harris et al., 2018 preprint).”
From Single cell transcriptomics reveals spatial and temporal dynamics of gene expression in the developing mouse spinal cord (2019) · cites this paper as Harris et al., 2018 preprint
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Thaler, J. P., Lee, S., Jurata, L. W., Gill, G. N., & Pfaff, S. L. (2002) · Cell · doi:10.1016/s0092-8674(02)00823-1 · Cited by 363 · see citing works
Clotman, F., Jacquemin, P., Plumb–Rudewiez, N., Pierreux, C. E., Smissen, P. V. D., Dietz, H. C., Courtoy, P. J., Rousseau, G. G., & Lemaigre, F. P. (2005) · Genes & Development · doi:10.1101/gad.340305 · Cited by 363 · see citing works
Self-citationCrone, S. A., Quinlan, K. A., Zagoraiou, L., Droho, S., Restrepo, C. E., Lundfald, L., Endo, T., Setlak, J., Jessell, T. M., Kiehn, O., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.08.009 · Cited by 358 · see citing works
Skilled reaching relies on a V2a propriospinal internal copy circuit
Azim, E., Jiang, J., Alstermark, B., & Jessell, T. M. (2014) · Nature · doi:10.1038/nature13021 · Cited by 355 · see citing works
Dual-mode operation of neuronal networks involved in left–right alternation
Talpalar, A. E., Bouvier, J., Borgius, L., Fortin, G., Pierani, A., & Kiehn, O. (2013) · Nature · doi:10.1038/nature12286 · Cited by 345 · see citing works
Jacquemin, P., Durviaux, S. M., Jensen, J. N., Godfraind, C., Gradwohl, G., Guillemot, F., Madsen, O. D., Carmeliet, P., Dewerchin, M. A., Collen, D., et al. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.12.4445-4454.2000 · Cited by 326 · see citing works
Corcoran, L. M., Karvelas, M., Nossal, G. J. V., Ye, Z. S., Jacks, T., & Baltimore, D. (1993) · Genes & Development · doi:10.1101/gad.7.4.570 · Cited by 266 · see citing works
Self-citationSpinal inhibitory interneuron diversity delineates variant motor microcircuits
Bikoff, J. B., Gabitto, M. I., Rivard, A. F., Drobac, E., Machado, T. A., Miri, A., Brenner-Morton, S., Famojure, E., Diaz, C., Alvarez, F. J., et al. (2016) · Cell · doi:10.1016/j.cell.2016.01.027 · Cited by 262 · see citing works
Locomotor rhythm generation linked to the output of spinal Shox2 excitatory interneurons
Dougherty, K. J., Zagoraiou, L., Satoh, D., Rozani, I., Doobar, S., Arber, S., Jessell, T. M., & Kiehn, O. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.015 · Cited by 229 · see citing works
Motor antagonism exposed by spatial segregation and timing of neurogenesis
Tripodi, M., Stepien, A. E., & Arber, S. (2011) · Nature · doi:10.1038/nature10538 · Cited by 203 · see citing works
Molecular and cellular development of spinal cord locomotor circuitry
Lu, D. C.-T., Niu, T., & Alaynick, W. A. (2015) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2015.00025 · Cited by 193 · see citing works
Making sense out of spinal cord somatosensory development
Lai, H. C., Seal, R. P., & Johnson, J. E. (2016) · Development · doi:10.1242/dev.139592 · Cited by 188 · see citing works
Hayashi, M., Hinckley, C. A., Driscoll, S. P., Moore, N. J., Levine, A. J., Hilde, K. L., Sharma, K., & Pfaff, S. L. (2018) · Neuron · doi:10.1016/j.neuron.2018.01.023 · Cited by 188 · see citing works
Jacquemin, P., Lemaigre, F., & Rousseau, G. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00115-5 · Cited by 187 · see citing works
Ampatzis, K., Song, J., Ausborn, J., & El Manira, A. (2014) · Neuron · doi:10.1016/j.neuron.2014.07.018 · Cited by 186 · see citing works
Patterns of Spinal Sensory-Motor Connectivity Prescribed by a Dorsoventral Positional Template
Sürmeli, G., Akay, T., Ippolito, G. C., Tucker, P. W., & Jessell, T. M. (2011) · Cell · doi:10.1016/j.cell.2011.10.012 · Cited by 179 · see citing works
Notch and MAML Signaling Drives Scl-Dependent Interneuron Diversity in the Spinal Cord
Peng, C., Yajima, H., Burns, C. E., Zon, L. I., Sisodia, S. S., Pfaff, S. L., & Sharma, K. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.019 · Cited by 178 · see citing works
Landry, C., Clotman, F., Hioki, T., Oda, H., Picard, J. J., Lemaigre, F. P., & Rousseau, G. G. (1997) · Developmental Biology · doi:10.1006/dbio.1997.8757 · Cited by 148 · see citing works
Self-citationLemaigre, F. P., Durviaux, S. M., Truong, O., et al. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.18.9460 · Cited by 146 · see citing works
Multiple Oct2 isoforms are generated by alternative splicing
Wirth, T. C., Priess, A., Annweiler, A., et al. (1991) · Nucleic Acids Research · doi:10.1093/nar/19.1.43 · Cited by 139 · see citing works
Britz, O., Zhang, J., Grossmann, K. S., Dyck, J. R. B., Kim, J. C., Dymecki, S. M., Gosgnach, S., & Goulding, M. (2015) · eLife · doi:10.7554/elife.04718 · Cited by 139 · see citing works
Firing and Cellular Properties of V2a Interneurons in the Rodent Spinal Cord
Dougherty, K. J., & Kiehn, O. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4821-09.2010 · Cited by 138 · see citing works
Barrio, M. G. D., Taveira‐Marques, R., Muroyama, Y., Yuk, D., Li, S., Wines-Samuelson, M., Shen, J., Smith, H. K., Xiang, M., Rowitch, D. H., et al. (2007) · Development · doi:10.1242/dev.005868 · Cited by 123 · see citing works
Hatzopoulos, A. K., Stoykova, A., Erselius, J. R., et al. (1990) · Development · doi:10.1242/dev.109.2.349 · Cited by 122 · see citing works
A regulatory network to segregate the identity of neuronal subtypes.
Lee, S., Lee, B., Joshi, K., Pfaff, S. L., Lee, J. W., & Lee, S.-K. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.03.021 · Cited by 122 · see citing works
Origin and segmental diversity of spinal inhibitory interneurons
Sweeney, L. B., Bikoff, J. B., Gabitto, M. I., Brenner-Morton, S., Baek, M., Yang, J. H., Tabak, E. G., Dasen, J. S., Kintner, C. R., & Jessell, T. M. (2018) · Neuron · doi:10.1016/j.neuron.2017.12.029 · Cited by 116 · see citing works
Stam, F. J., Hendricks, T. J., Zhang, J., Geiman, E. J., Francius, C., Labosky, P. A., Clotman, F., & Goulding, M. (2012) · Development · doi:10.1242/dev.071134 · Cited by 115 · see citing works
Functional subpopulations of V3 interneurons in the mature mouse spinal cord
Borowska, J., Jones, C. T., Zhang, H., Blacklaws, J., Goulding, M., & Zhang, Y. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2005-13.2013 · Cited by 111 · see citing works
Jacquemin, P., Lannoy, V. J., Rousseau, G. G., et al. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.5.2665 · Cited by 108 · see citing works
Regulation of normal B-cell differentiation and malignant B-cell survival by OCT2
Hodson, D. J., Shaffer, A. L., Xiao, W., Wright, G. W., Schmitz, R., Phelan, J. D., Yang, Y., Webster, D. E., Rui, L., Kohlhammer, H., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1600557113 · Cited by 106 · see citing works
Decision making during interneuron migration in the developing cerebral cortex
Guo, J., & Anton, E. S. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2013.12.001 · Cited by 104 · see citing works
Delineating the Diversity of Spinal Interneurons in Locomotor Circuits
Gosgnach, S., Bikoff, J. B., Dougherty, K. J., Manira, A. E., Lanuza, G. M., & Zhang, Y. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1829-17.2017 · Cited by 100 · see citing works
Francius, C., Harris, A., Rucchin, V., Hendricks, T. J., Stam, F. J., Barber, M., Kurek, D., Grosveld, F. G., Pierani, A., Goulding, M., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070325 · Cited by 97 · see citing works
LMO4 Controls the Balance between Excitatory and Inhibitory Spinal V2 Interneurons
Joshi, K., Lee, S., Lee, J. W., Lee, S., & Lee, S. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.011 · Cited by 80 · see citing works
Lillycrop, K. A., & Latchman, D. S. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)73991-x · Cited by 78 · see citing works
Assembly and function of spinal circuits for motor control
Catela, C., Shin, M. M., & Dasen, J. S. (2015) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100814-125155 · Cited by 77 · see citing works
Panayi, H., Panayiotou, E., Orford, M., Genethliou, N., Mean, R. J., Lapathitis, G., Li, S., Xiang, M., Kessaris, N., Richardson, W. D., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2402-10.2010 · Cited by 76 · see citing works
Stoykova, A., Sterrer, S., Erselius, J. R., et al. (1992) · Neuron · doi:10.1016/0896-6273(92)90282-i · Cited by 76 · see citing works
Identification of CD36 as the first gene dependent on the B-cell differentiation factor Oct-2.Preprint
König, H., Pfisterer, P. H., Corcoran, L. M., et al. (1995) · Genes & Development · doi:10.1101/gad.9.13.1598 · Cited by 75 · see citing works
Self-citationRoy, A., Francius, C., Rousso, D. L., Seuntjens, E., Debruyn, J., Luxenhofer, G., Huber, A. B., Huylebroeck, D., Novitch, B. G., & Clotman, F. (2012) · Development · doi:10.1242/dev.078501 · Cited by 75 · see citing works
Self-citationBarber, M., & Pierani, A. (2015) · Developmental Neurobiology · doi:10.1002/dneu.22363 · Cited by 70 · see citing works
Distinct Limb and Trunk Premotor Circuits Establish Laterality in the Spinal Cord
Goetz, C., Pivetta, C., & Arber, S. (2014) · Neuron · doi:10.1016/j.neuron.2014.11.024 · Cited by 69 · see citing works
Francius, C., & Clotman, F. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.09.076 · Cited by 64 · see citing works
Self-citationThe Oct-2 transcription factor
Latchman, D. S. (1996) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/1357-2725(96)00050-7 · Cited by 60 · see citing works
Theodorou, E., Dalembert, G., Heffelfinger, C., White, E., Weissman, S. M., Corcoran, L. M., & Snyder, M. P. (2009) · Genes & Development · doi:10.1101/gad.1772509 · Cited by 60 · see citing works
Self-citationBeaudry, J.-B., Pierreux, C. E., Hayhurst, G. P., Plumb-Rudewiez, N., Weiss, M. C., Rousseau, G. G., & Lemaigre, F. P. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.02445-05 · Cited by 56 · see citing works
Genetic dissection of rhythmic motor networks in mice
Grossmann, K. S., Giraudin, A., Britz, O., Zhang, J., & Goulding, M. (2010) · Progress in brain research · doi:10.1016/b978-0-444-53613-6.00002-2 · Cited by 54 · see citing works
Ziskind‐Conhaim, L., & Hochman, S. (2017) · Journal of Neurophysiology · doi:10.1152/jn.00322.2017 · Cited by 54 · see citing works
Beguin, S., Crépel, V., Aniksztejn, L., Becq, H., Pelosi, B., Pallesi‐Pocachard, E., Bouamrane, L., Pasqualetti, M., Kitamura, K., Cardoso, C., et al. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs138 · Cited by 53 · see citing works
OC-3, a Novel Mammalian Member of the ONECUT Class of Transcription Factors
Vanhorenbeeck, V., Jacquemin, P., Lemaigre, F. P., et al. (2002) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2002.6760 · Cited by 49 · see citing works
Transcriptional Stimulation by Hepatocyte Nuclear Factor-6
Lannoy, V. J., Rodolosse, A., Pierreux, C. E., Rousseau, G. G., & Lemaigre, F. P. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m000855200 · Cited by 48 · see citing works
Cloning and embryonic expression pattern of the mouse Onecut transcription factor OC-2
Jacquemin, P., Pierreux, C. E., Fierens, S., van Eyll, J. M., Lemaigre, F. P., & Rousseau, G. G. (2003) · Gene Expression Patterns · doi:10.1016/s1567-133x(03)00110-8 · Cited by 48 · see citing works
Pelosi, B., Migliarini, S., Pacini, G., Pratelli, M., & Pasqualetti, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0104318 · Cited by 47 · see citing works
Blacklaws, J., Deska‐Gauthier, D., Jones, C. T., Petracca, Y. L., Liu, M., Zhang, H., Fawcett, J. P., Glover, J. C., Lanuza, G. M., & Zhang, Y. (2015) · Developmental Neurobiology · doi:10.1002/dneu.22266 · Cited by 44 · see citing works
Pierreux, C. E., Vanhorenbeeck, V., Jacquemin, P., Lemaigre, F. P., & Rousseau, G. G. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m409038200 · Cited by 43 · see citing works
Chx10 Consolidates V2a Interneuron Identity through Two Distinct Gene Repression Modes
Clovis, Y. M., Seo, S. Y., Kwon, J.-S., Rhee, J. C., Yeo, S., Lee, J. W., Lee, S., & Lee, S. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.06.100 · Cited by 43 · see citing works
Hilde, K. L., Levine, A. J., Hinckley, C. A., Hayashi, M., Montgomery, J. M., Gullo, M., Driscoll, S. P., Grosschedl, R., Kohwi, Y., Kohwi-Shigematsu, T., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.07.014 · Cited by 43 · see citing works
Espana, A., & Clotman, F. (2012) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2012.04.002 · Cited by 42 · see citing works
Self-citationEspana, A., & Clotman, F. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22803 · Cited by 37 · see citing works
Self-citationGenerating spinal motor neuron diversity: a long quest for neuronal identity
Francius, C., & Clotman, F. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1398-x · Cited by 35 · see citing works
Self-citationKabayiza, K. U., Masgutova, G., Harris, A., Rucchin, V., Jacob, B., & Clotman, F. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00157 · Cited by 35 · see citing works
Self-citationMisra, K., Luo, H., Li, S., Matise, M. P., & Xiang, M. (2013) · Development · doi:10.1242/dev.092536 · Cited by 34 · see citing works
Borowska, J., Jones, C. T., Deska‐Gauthier, D., & Zhang, Y. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.03.024 · Cited by 34 · see citing works
Audouard, E., Schakman, O., René, F., Huettl, R.-E., Huber, A. B., Loeffler, J., Gailly, P. L., & Clotman, F. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050509 · Cited by 31 · see citing works
Self-citationAll Known In Vivo Functions of the Oct-2 Transcription Factor Require the C-Terminal Protein Domain
Corcoran, L. M., Köentgen, F., Dietrich, W., Veale, M. F., & Humbert, P. O. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.5.2962 · Cited by 21 · see citing works
Self-citationAudouard, E., Schakman, O., Ginion, A., Bertrand, L., Gailly, P. L., & Clotman, F. (2013) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2013.05.001 · Cited by 19 · see citing works
Self-citationFrancius, C., Hidalgo‐Figueroa, M., Debrulle, S., Pelosi, B., Rucchin, V., Ronellenfitch, K., Panayiotou, E., Makrides, N., Misra, K., Harris, A., et al. (2016) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2016.00145 · Cited by 18 · see citing works
Self-citationRegulated splicing of the Oct-2 transcription factor RNA in neuronal cells
Liu, Y., Lillycrop, K. A., & Latchman, D. S. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(94)11102-o · Cited by 9 · see citing works
Origin and circuitry of spinal locomotor interneurons generating different speeds
Boije, H., & Kullander, K. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.04.024 · Cited by 9 · see citing works
Camós, S., Gubern, C., Sobrado, M., et al. (2013) · NeuroMolecular Medicine · doi:10.1007/s12017-013-8279-1 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Delile, J., Rayon, T., Melchionda, M., Edwards, A., Briscoe, J., & Sagner, A. (2019) · Development · doi:10.1242/dev.173807 · Cited by 356 · see citing works
- Authors
- Harris, A., Masgutova, G., Collin, A., Toch, M., Hidalgo-Figueroa, M., Jacob, B., Corcoran, L. M., Francius, C., & Clotman, F.
- Affiliations
- UCLouvain (BE)
- Walter and Eliza Hall Institute of Medical Research (AU)
- Venue
- bioRxiv (Cold Spring Harbor Laboratory)
- Publisher
- openRxiv
- Published
- 2018-09-10
- OpenAlex
- W2891995326
- Cited by
- 2
- References
- 70
- Citations by year
- 2019: 2
- Type
- posted content
- Language
- en
- Open access
- green
- doi.org
- Locations
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- Funders
- Association Belge contre les Maladies Neuro-Musculaires
- Australian Government
- Fonds De La Recherche Scientifique - FNRS (T.0117.13, U.N027.14)
- Fédération Wallonie-Bruxelles (10/15-026)
- Fonds Spéciaux de Recherche
- National Health and Medical Research Council (575500, 637306)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Health Sciences › Medicine › Surgery › Congenital gastrointestinal and neural anomalies
- Keywords
- POU2F2, spinal cord development, interneuron migration, neuronal identity, transcriptional regulation, mouse embryo
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review