Role of Intermediate Progenitor Cells in Cerebral Cortex Development
Abstract
Intermediate progenitor cells (IPCs) are a type of neurogenic transient amplifying cells in the developing cerebral cortex. IPCs divide symmetrically at basal (abventricular) positions in the neuroepithelium to produce pairs of new neurons or, in amplifying divisions, pairs of new IPCs. In contrast, radial unit progenitors (neuroepithelial cells and radial glia) divide at the apical (ventricular) surface and produce only single neurons or single IPCs by asymmetric division, or self-amplify by symmetric division. Histologically, IPCs are most prominent during the middle and late stages of neurogenesis, when they accumulate in the subventricular zone, a progenitor compartment linked to the genesis of upper neocortical layers (II–IV). Nevertheless, IPCs are present throughout cortical neurogenesis and produce neurons for all layers. In mice, changes in the abundance of IPCs caused by mutations of Pax6, Ngn2, Id4 and other genes are associated with parallel changes in cortical thickness but not surface area. In gyrencephalic brains, IPCs may play broader roles in determining not only laminar thickness, but also cortical surface area and gyral patterns. We propose that regulation of IPC genesis and amplification across developmental stages and regional subdivisions modulates laminar neurogenesis and contributes to the cytoarchitectonic differentiation of cortical areas.
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Cortical surface area and thickness are controlled by mechanisms involved in RGC and IPC proliferation and differentiation decisions.
“Cortical surface area and thickness are controlled by the mechanisms involved in RGC and IPC proliferation and differentiation decisions [99, 100].”
From The ASD Living Biology: from cell proliferation to clinical phenotype (2019) · cites this paper as [99]
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Self-citationSamuels, I. S., Karlo, J. C., Faruzzi, A. N., Pickering, K., Herrup, K., Sweatt, J. D., Saitta, S. C., & Landreth, G. E. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0679-08.2008 · Cited by 278 · see citing works
“The nascent IPC continues to undergo asymmetric renewal or, more frequently, divides symmetrically, yielding two neurons (Noctor et al., 2004; Pontious et al., 2008).”
BackgroundVijayakumar, N., Allen, N. B., Youssef, G. J., Dennison, M., Yücel, M., Simmons, J. G., & Whittle, S. (2016) · Human Brain Mapping · doi:10.1002/hbm.23154 · Cited by 273 · see citing works
“Experimental manipulation of progenitor cells, which are thought to play a role in neurogenesis, has also been found to affect cortical thickness, but not cortical surface area [Pontious et al., 2008].”
BackgroundMaking bigger brains–the evolution of neural-progenitor-cell division
Fish, J. L., Dehay, C., Kennedy, H., & Huttner, W. B. (2008) · Journal of Cell Science · doi:10.1242/jcs.023465 · Cited by 274 · see citing works
“Nonetheless, this single round of division doubles the number of neurons that are present in each radial unit, which suggests an important role for BPs in generating radial thickness (Abdel-Mannan et al., 2008; Farkas et al., 2008; Pontious et al., 2008).”
BackgroundCdk5rap2 regulates centrosome function and chromosome segregation in neuronal progenitors
Lizarraga, S. B., Margossian, S. P., Harris, M. H., Campagna, D. R., Han, A., Blevins, S., Mudbhary, R., Barker, J. E., Walsh, C. A., & Fleming, M. D. (2010) · Development · doi:10.1242/dev.040410 · Cited by 270 · see citing works
“Apical progenitors give rise to deep layer neurons and basal progenitors, whereas basal progenitors primarily produce superficial layer neurons (Pontious et al., 2008).”
BackgroundCell cycle control of mammalian neural stem cells: putting a speed limit on G1
Salomoni, P., & Calegari, F. (2010) · Trends in Cell Biology · doi:10.1016/j.tcb.2010.01.006 · Cited by 272 · see citing works
Cortical progenitor expansion, self-renewal and neurogenesis—a polarized perspective
Fietz, S. A., & Huttner, W. Β. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.10.002 · Cited by 270 · see citing works
Farkas, L. M., & Huttner, W. Β. (2008) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2008.09.008 · Cited by 247 · see citing works
Genetic causes of microcephaly and lessons for neuronal development
Gilmore, E. C., & Walsh, C. A. (2012) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.89 · Cited by 244 · see citing works
Albert‐Gascó, H., Ros‐Bernal, F., Castillo-Gómez, E., & Olucha-Bordonau, F. E. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21124471 · Cited by 241 · see citing works
Brain Surface Anatomy in Adults With Autism
Ecker, C., Ginestet, C. E., Feng, Y., Johnston, P., Lombardo, M. V., Lai, M., John Suckling, A., Palaniyappan, L. K., Daly, E., Murphy, C. M., et al. (2012) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.265 · Cited by 226 · see citing works
Neurogenesis at the Brain–Cerebrospinal Fluid Interface
Lehtinen, M. K., & Walsh, C. A. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-092910-154026 · Cited by 212 · see citing works
“Basal progenitors are derived from apical progenitors, but they localize their nuclei in the SVZ and divide almost exclusively in a symmetric fashion to generate pairs of postmitotic daughter neurons (Kriegstein et al. 2006, Martinez-Cerdeno et al. 2006, Noctor et al. 2008, Pontious et al. 2008).”
BackgroundERK/MAPK signalling in the developing brain: Perturbations and consequences
Iroegbu, J. D., Ijomone, O. K., Femi-Akinlosotu, O. M., & Ijomone, O. M. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.10.009 · Cited by 206 · see citing works
MAP'ing CNS Development and Cognition: An ERKsome Process
Samuels, I. S., Saitta, S. C., & Landreth, G. E. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.001 · Cited by 200 · see citing works
Sanabria-Díaz, G., Melie‐García, L., Iturria‐Medina, Y., Alemán‐Gómez, Y., Hernández-González, G., Valdés-Urrutia, L., Galán, L., & Valdes-Sosa, P. A. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.01.028 · Cited by 191 · see citing works
“A recent extension of the radial unit hypothesis, referred to as the radial amplification hypothesis, highlights the contribution of intermediate progenitor cells to neurogenesis and how their manipulation within animal models results in changes to cortical thickness but not surface area (Pontious et al., 2008).”
BackgroundVieira, M. S., Santos, A. K., Vasconcellos, R., Goulart, V. A. M., Parreira, R. C., Kihara, A. H., Ulrich, H., & Resende, R. R. (2018) · Biotechnology Advances · doi:10.1016/j.biotechadv.2018.08.002 · Cited by 191 · see citing works
Silver, D. L., Watkins‐Chow, D. E., Schreck, K. C., Pierfelice, T. J., Larson, D. M., Burnetti, A., Liaw, H., Myung, K., Walsh, C. A., Gaiano, N., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2527 · Cited by 177 · see citing works
“5) 50% (14) 50% (14) NA NA MagohGT0150/+ 89% (321) 11% (40)** NA NA MagohGT027/+ 93% (192) 7% (15)** NA NA Tg-BAC1; MagohMos2/+ 37% (65) 0% 33% (58) 30% (51)** Tg-BAC2; MagohMos2/+ 31% (84) 1% (3) 33% (88) 35% (96)**”
Chromatin Regulation by BAF170 Controls Cerebral Cortical Size and Thickness
Tuoc, T. C., Boretius, S., Sansom, S. N., Pitulescu, M.-E., Frahm, J., Livesey, F. J., & Stoykova, A. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.04.005 · Cited by 177 · see citing works
“5 they contributemore significantly to generation of neurons with upper layer identities (UL, L4–L2) during late neurogenesis (Pontious et al., 2008).”
BackgroundThe clinical impact of deficiency in DNA non-homologous end-joining
Woodbine, L. J., Gennery, A. R., & Jeggo, P. A. (2014) · DNA repair · doi:10.1016/j.dnarep.2014.02.011 · Cited by 176 · see citing works
Meechan, D. W., Tucker, E. S., Maynard, T. M., & LaMantia, A.-S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905696106 · Cited by 173 · see citing works
BMP-Smad 1/5/8 signalling in the development of the nervous system
Hegarty, S. V., O’Keeffe, G. W., & Sullivan, A. M. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.07.002 · Cited by 175 · see citing works
Differential Tangential Expansion as a Mechanism for Cortical Gyrification
Ronan, L., Voets, N., Rua, C., Alexander‐Bloch, A. F., Hough, M., Mackay, C. E., Crow, T. J., James, A. C., Giedd, J. N., & Fletcher, P. C. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht082 · Cited by 174 · see citing works
“Observations of the developmental cortex suggest that early differences in the cytoarchitecture are predictive of the emergence of individual folds (Smart et al. 2002; Bayer and Altman 2006; Kriegstein et al. 2006; Pontious et al. 2008; Lui et al. 2011; Reillo et al. 2011).”
BackgroundResearch Review: Pediatric Anxiety Disorders—What Have We Learnt in the Last 10 Years?
Strawn, J. R., Lu, L., Peris, T. S., Levine, A., & Walkup, J. T. (2021) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13262 · Cited by 168 · see citing works
Role of mTOR Complexes in Neurogenesis
Licausi, F., & Hartman, N. W. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19051544 · Cited by 165 · see citing works
“Proliferation of RGCs eventually produce intermediate progenitor cells that migrate into the SVZ and typically undergo at least one round of cell division to produce immature neurons [95,96].”
BackgroundFarkas, L. M., Haffner, C., Giger, T., Khaitovich, P., Nowick, K., Birchmeier, C., Pääbo, S., & Huttner, W. Β. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.020 · Cited by 159 · see citing works
“Insm1, a Constituent of the Molecular Machinery Underlying the Evolutionary Expansion of the Mammalian Cerebral Cortex Given that the expansion of the mammalian cerebral cortex is associated with an increase in BPs relative to APs (Bystron et al., 2008; Kriegstein et al., 2006; Pontious et al., 2008; Rakic, 2003; Smar…”
BackgroundInfluentialWeng, M., Golden, K. L., & Lee, C. (2010) · Developmental Cell · doi:10.1016/j.devcel.2009.12.007 · Cited by 158 · see citing works
“Yet the developmental potential of transit amplifying cells must be tightly restricted to ensure generation of differentiated progeny and to prevent unrestrained proliferation that might lead to tumorigenesis (Morrison and Kimble, 2006; Pontious et al., 2008; Vescovi et al., 2006).”
BackgroundNotaras, M., Lodhi, A., Dündar, F., Collier, P., Sayles, N. M., Tilgner, H., Greening, D., & Colak, D. (2022) · Molecular Psychiatry · doi:10.1038/s41380-021-01316-6 · Cited by 150 · see citing works
Slit/Robo Signaling Modulates the Proliferation of Central Nervous System Progenitors
Borrell, V., Cárdenas, A., Ciceri, G., Galcerán, J., Flames, N., Pla, R., Pereira, S. N., Garcı́a-Frigola, C., Peregrín, S., Zhao, Z., et al. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.003 · Cited by 151 · see citing works
“We focusedmost of our analysis in the developing cerebral cortex, for which the cellular mechanisms of neurogenesis are beginning to be elucidated (Fietz and Huttner, 2011; Noctor et al., 2007; Pontious et al., 2008).”
BackgroundResultInfluentialA Stem Cell Niche for Intermediate Progenitor Cells of the Embryonic Cortex
Javaherian, A., & Kriegstein, A. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp029 · Cited by 155 · see citing works
“inside-out assembly of the 6-layered cortex (Smart 1973; McConnell 1995; Kriegstein et al. 2006; Rakic 2006; Cheung et al. 2007; Dehay and Kennedy 2007; Pontious et al. 2008).”
BackgroundGarcía‐Moreno, F., Vasistha, N. A., Trévia, N., Bourne, J. A., & Molnár, Z. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr312 · Cited by 154 · see citing works
“types (Pontious et al. 2008; Kowalczyk et al. 2009; Molnár 2011).”
BackgroundLi, R., Sun, L., Fang, A., Li, P., Wu, Q., & Wang, X. (2017) · Protein & Cell · doi:10.1007/s13238-017-0479-2 · Cited by 154 · see citing works
“…et al., 2010; LaMonica et al., 2012; Ostrem et al., 2014; Taverna and Huttner, 2010; Gertz et al., 2014) instead of neurons, as in mice (Wang et al., 2011), and serve as transit amplifying machinery for proliferative pool expansion (Lui et al., 2011; Fietz and Huttner, 2011; Pontious et al., 2008).”
BackgroundThe role of BAF (mSWI/SNF) complexes in mammalian neural development
Son, E., & Crabtree, G. R. (2014) · American Journal of Medical Genetics Part C Seminars in Medical Genetics · doi:10.1002/ajmg.c.31416 · Cited by 151 · see citing works
“While direct neurogenesis from RGs produces deep‐layer neurons during early corticogenesis, indirect neurogenesis via production of IPs contributes most to the neurons in the upper layer [Pontious et al., 2007].”
BackgroundFoxP2 Regulates Neurogenesis during Embryonic Cortical Development
Tsui, D. C. C., Vessey, J. P., Tomita, H., Kaplan, D. R., & Miller, F. D. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1665-12.2013 · Cited by 151 · see citing works
“Since recent work suggests that an increase in intermediate progenitors was important for evolution of a larger human cortex (Noctor et al., 2007; Pontious et al., 2008), then this raises the possibility that a more active FoxP2 was perhaps somehow involved in facilitating this evolution.”
BackgroundCell-type-specific 3D epigenomes in the developing human cortex
Song, M., Pebworth, M.-P., Yang, X., Abnousi, A., Fan, C., Wen, J., Rosen, J. D., Choudhary, M. N. K., Cui, X., Jones, I. R., et al. (2020) · Nature · doi:10.1038/s41586-020-2825-4 · Cited by 143 · see citing works
Regulation of neural progenitor cell development in the nervous system
Corbin, J. G., Gaiano, N., Juliano, S. L., Poluch, S., Stancik, E. K., & Haydar, T. F. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05522.x · Cited by 145 · see citing works
“Instead the neocortical germinal zone is comprised of numerous distinct proliferative cell types (Grove et al. 1993; Hartfuss et al. 2001b; Haubensak et al. 2004; Gal et al. 2006; Mizutani et al. 2007; Pontious et al. 2008).”
BackgroundMirzaa, G., Parry, D. A., Fry, A. E., Giamanco, K. A., Schwartzentruber, J., Vanstone, M. R., Logan, C. V., Roberts, N. Y., Johnson, C. A., Singh, S., et al. (2014) · Nature Genetics · doi:10.1038/ng.2948 · Cited by 148 · see citing works
Self-citationLiu, J., Liu, W., Yang, L., Wu, Q., Zhang, H., Fang, A., Li, L., Xu, X., Sun, L., Zhang, J., et al. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.08.013 · Cited by 138 · see citing works
14-3-3 Proteins in Brain Development: Neurogenesis, Neuronal Migration and Neuromorphogenesis
Cornell, B., & Toyo‐oka, K. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00318 · Cited by 142 · see citing works
“During neurogenesis, RGCs will divide symmetrically to produce two RGCs, or asymmetrically to generate an RGC and a neuron either directly or indirectly through the production of an intermediate progenitor cell (IPC; Pontious et al., 2008).”
BackgroundENIGMA Clinical High Risk for Psychosis Working Group, Jalbrzikowski, M., Hayes, R. A., Wood, S. J., Nordholm, D., Zhou, J. H., Fusar-Poli, P., Uhlhaas, P. J., Takahashi, T., Sugranyes, G., et al. (2021) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2021.0638 · Cited by 137 · see citing works
Id proteins synchronize stemness and anchorage to the niche of neural stem cells
Niola, F., Zhao, X., Singh, D., Castano, A. M., Sullivan, R. J., Lauria, M., Nam, H.-S., Zhuang, Y., Benezra, R., di Bernardo, D., et al. (2012) · Nature Cell Biology · doi:10.1038/ncb2490 · Cited by 138 · see citing works
Liu, Q., Nguyen, D. H. A., Dong, Q., Shitaku, P., Chung, K., Liu, O. Y., Tso, J. L., Liu, J. Y., Konkankit, V., Cloughesy, T. F., et al. (2009) · Journal of Neuro-Oncology · doi:10.1007/s11060-009-9919-z · Cited by 130 · see citing works
“Therefore, loss of CD133 (or with other genes) may restrict CD133- GBM daughter cells to the symmetric mode of cell division and act like proliferative intermediate progenitor cells [60, 61].”
BackgroundCyclin D2 Is Critical for Intermediate Progenitor Cell Proliferation in the Embryonic Cortex
Glickstein, S. B., Monaghan, J. A., Koeller, H. B., Jones, T. K., & Ross, M. E. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2284-09.2009 · Cited by 124 · see citing works
Cerebral cortical development in rodents and primates
Molnár, Z., & Clowry, G. J. (2012) · Progress in brain research · doi:10.1016/b978-0-444-53860-4.00003-9 · Cited by 130 · see citing works
“Hevner and colleagues demonstrated that some intermediate progenitors contribute to all layers throughout all stages (early, middle, and late) of cortical neurogenesis in mice (Kowalczyk et al., 2009; Pontious et al., 2008).”
BackgroundYang, D. Y. ‐., Beam, D. E., Pelphrey, K. A., Abdullahi, S. M., & Jou, R. J. (2016) · Molecular Autism · doi:10.1186/s13229-016-0076-x · Cited by 128 · see citing works
“According to the intermediate progenitor hypothesis [43], intermediate progenitor cells (IPC) produce only neurons through symmetric division at subventricular and intermediate zones; the newborn neurons migrate along radial glial fibers to their final cortical destinations and form ontogenetic columns arranged as rad…”
BackgroundMapping the molecular and cellular complexity of cortical malformations
Klingler, E., Francis, F., Jabaudon, D., & Cappello, S. (2021) · Science · doi:10.1126/science.aba4517 · Cited by 122 · see citing works
“Intermediate progenitors are more neurogenic than aRG and act to boost neuronal production (19).”
BackgroundFate and freedom in developing neocortical circuits
Jabaudon, D. (2017) · Nature Communications · doi:10.1038/ncomms16042 · Cited by 125 · see citing works
Toyo‐oka, K., Wachi, T., Hunt, R. F., Baraban, S. C., Taya, S., Ramshaw, H. S., Kaibuchi, K., Schwarz, Q., Lopez, A. F., & Wynshaw-Boris, A. J. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2513-13.2014 · Cited by 115 · see citing works
Integrin αvβ3 and thyroid hormones promote expansion of progenitors in embryonic neocortex
Stenzel, D., Wilsch‐Bräuninger, M., Wong, F. K., Heuer, H., & Huttner, W. Β. (2014) · Development · doi:10.1242/dev.101907 · Cited by 114 · see citing works
Sex-dependent association of common variants of microcephaly genes with brain structure
Rimol, L. M., Agartz, I., Djurovic, S., Brown, A. A., Roddey, J. C., Kähler, A. K., Mattingsdal, M., Athanasiu, L., Joyner, A. H., Schork, N. J., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908454107 · Cited by 111 · see citing works
“Moreover, cortical area and thickness may have independent cellular determinants (i.e., radial progenitor cells and intermediate progenitor cells, respectively) (23).”
Joyner, A. H., Cooper Roddey, J., Bloss, C. S., Bakken, T. E., Rimol, L. M., Melle, I. S., Agartz, I., Djurovic, S., Topol, E. J., Schork, N. J., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901866106 · Cited by 111 · see citing works
Dual requirement for Pax6 in retinal progenitor cells
Oron‐Karni, V., Farhy, C., Elgart, M., Marquardt, T., Remizova, L., Yaron, O., Xie, Q. M., Cvekl, A., & Ashery‐Padan, R. (2008) · Development · doi:10.1242/dev.028308 · Cited by 111 · see citing works
“Considering that all retinal cell types eventually populate both central and peripheral retina in the adult, it seems likely that the differences documented here between central and peripheral OC RPCs primarily reflect distinct differentiation stages of the multipotent progenitor pools, similar to the transient states…”
Fibroblast growth factor signaling in development of the cerebral cortex
Iwata, T., & Hevner, R. F. (2009) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2009.01104.x · Cited by 108 · see citing works
“Neurogenesis at this phase, mainly from IPCs but also from radial glia, evidently contributes to the thickness of the cortex (Pontious et al. 2008; Kowalczyk et al. 2009).”
BackgroundSelf-citationPromotion of embryonic cortico-cerebral neuronogenesis by miR-124
Maiorano, N. A., & Mallamaci, A. (2009) · Neural Development · doi:10.1186/1749-8104-4-40 · Cited by 110 · see citing works
“Remarkably, a few intensely labeled cells could be seen at the VZ-SVZ border (Figure 1C).”
BackgroundInfluentialCheung, A. F. P., Kondo, S., Abdel‐Mannan, O., Chodroff, R. A., Sirey, T., Bluy, L. E., Webber, N., DeProto, J., Karlen, S. J., Krubitzer, L. A., et al. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp168 · Cited by 104 · see citing works
“The 2-step pattern of neurogenesis could facilitate the formation of a 6-layered cortex with a larger surface area (Martı´nez-Cerdenõ et al. 2006; Pontious et al. 2007).”
BackgroundMethodPucilowska, J., Puzerey, P. A., Karlo, J. C., Galan, R. F., & Landreth, G. E. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1107-12.2012 · Cited by 99 · see citing works
“Conversely, neurogenic divisions generate neurons determining cortical thickness (Pontious et al., 2008).”
BackgroundEmx2 and Foxg1 Inhibit Gliogenesis and Promote Neuronogenesis
Brancaccio, M., Pivetta, C., Granzotto, M., Filippis, C., & Mallamaci, A. (2010) · Stem Cells · doi:10.1002/stem.443 · Cited by 102 · see citing works
Dave, R. K., Ellis, T., Toumpas, M. C., Robson, J. P., Julian, E., Adolphe, C., Bartlett, P. F., Cooper, H. M., Reynolds, B. A., & Wainwright, B. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0014680 · Cited by 103 · see citing works
“). Nestin is expressed in both neuroepithelial and radial glial cells but not basal progenitors”
BackgroundNeural Progenitor Cell Polarity and Cortical Development
Arai, Y., & Taverna, E. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00384 · Cited by 104 · see citing works
“…cortical development (Yokota et al., 2010; Figure 2). aRGCs have been extensively studied in the last decades and it is now clear that they contribute to neurogenesis mainly via the generation of a second type of neural progenitor cells: the BPs (Pontious et al., 2008; Kowalczyk et al., 2009).”
BackgroundThe autism puzzle: Diffuse but not pervasive neuroanatomical abnormalities in children with ASD
Sussman, D., Leung, R. C., Vogan, V. M., Lee, W., Trelle, S., Lin, S., Cassel, D. B., Chakravarty, M. M., Lerch, J. P., Anagnostou, E. A., et al. (2015) · NeuroImage Clinical · doi:10.1016/j.nicl.2015.04.008 · Cited by 102 · see citing works
“, 2008); whereas SA is shaped by radial-unit progenitor cells, which divide in the periventricular area and dictate the number of radial units (Chenn and Walsh, 2002; Pontious et al., 2008).”
InfluentialZhu, S., Barshow, S., Wildonger, J., Jan, L. Y., & Jan, Y. N. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1118595109 · Cited by 96 · see citing works
Nelson, B. R., Hodge, R. D., Bedogni, F., & Hevner, R. F. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0791-13.2013 · Cited by 102 · see citing works
“…progenitors (INPs) in the VZ (INPvz, also known as short neural precursors, SNPs) and SVZ (INPsvz) (Gal et al., 2006; Corbin et al., 2008; Pontious et al., 2008; Kriegstein and Alvarez-Buylla, 2009; Fietz et al., 2010; Hansen et al., 2010; Stancik et al., 2010; Taverna and Huttner, 2010;…”
BackgroundSelf-citationNeuroimaging in autism—from basic science to translational research
Ecker, C., & Murphy, D. (2014) · Nature Reviews Neurology · doi:10.1038/nrneurol.2013.276 · Cited by 98 · see citing works
Regulated Reprogramming in the Regeneration of Sensory Receptor Cells
Bermingham‐McDonogh, O., & Reh, T. A. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.015 · Cited by 98 · see citing works
Differences in Cortical Structure and Functional MRI Connectivity in High Functioning Autism
Pereira, A. M., de Campos, B. M., Coan, A. C., Pegoraro, L. F., de Rezende, T. J. R., Obeso, I., Dalgalarrondo, P., da Costa, J. C., Dreher, J., & Cendes, F. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00539 · Cited by 97 · see citing works
“However, cortical thickness and surface area measurements represent distinct aspects of the cortical architecture and may represent different early neurodevelopmental pathologies (37, 127, 128).”
BackgroundEvolution and development of the mammalian cerebral cortex
Molnár, Z., Kaas, J. H., de Carlos, J. A., Hevner, R. F., Lein, E., & Němec, P. (2014) · Brain Behavior and Evolution · doi:10.1159/000357753 · Cited by 93 · see citing works
“However, other observations suggested that IPs produce the majority of glutamatergic neurons in all cortical layers [Haubensak et al., 2004; Pontious et al., 2008; Kowalczyk et al., 2009].”
BackgroundDistinguishing bipolar and major depressive disorders by brain structural morphometry: a pilot study
Fung, G., Deng, Y., Zhao, Q., Li, Z., Qu, M., Li, K., Zeng, Y., Jin, Z. H., Ma, Y., Yu, X., et al. (2015) · BMC Psychiatry · doi:10.1186/s12888-015-0685-5 · Cited by 93 · see citing works
“Surface area, on the other hand, has been associated with the proliferation of radial unit progenitors, which consist of neuroepithelial cells and radial glial cells [13], and functionally involve in the mechanisms of arborization, pruning within grey matter [14], and varying myelination at the grey/white matter inter…”
BackgroundMicroRNA-92b regulates the development of intermediate cortical progenitors in embryonic mouse brain
Nowakowski, T. J., Fotaki, V., Pollock, A., Sun, T., Pratt, T., & Price, D. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219385110 · Cited by 95 · see citing works
Prediction of brain maturity based on cortical thickness at different spatial resolutions
Khundrakpam, B. S., Tohka, J., & Evans, A. C. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.02.046 · Cited by 90 · see citing works
“…(of age) is plausible given emerging evidence from recent findings that suggest that CT and SA may result from different phylogenetic processes (Pontious et al., 2008; Rakic, 1995), and their etiologymay involve different genetic mechanisms (Chen et al., 2011; Chouinard-Decorte et al., 2014;…”
BackgroundStevens, H. E. (2010) · Frontiers in Neuroscience · doi:10.3389/fnins.2010.00059 · Cited by 90 · see citing works
“The committed neuronal progenitors of the SVZ, referred to as intermediate progenitor cells (IPCs) express the transcription factor TBR2 and lack the self-renewal properties of true stem cells (Pontious et al., 2008).”
BackgroundSurface Vulnerability of Cerebral Cortex to Major Depressive Disorder
Peng, D., Shi, F., Li, G., Fralick, D., Shen, T., Qiu, M., Liu, J., Jiang, K., Shen, D. G., & Fang, Y. (2015) · PLoS ONE · doi:10.1371/journal.pone.0120704 · Cited by 89 · see citing works
“First, cortical thickness might be a sensitive measurement of neuronal density [12, 13], which has been used to assess mental disorders and related pathological changes [14, 15].”
BackgroundElsen, G. E., Hodge, R. D., Bedogni, F., Daza, R. A. M., Nelson, B. R., Shiba, N., Reiner, S. L., & Hevner, R. F. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209076110 · Cited by 87 · see citing works
Self-citationCerebral cortex assembly: generating and reprogramming projection neuron diversity
Lodato, S., Shetty, A. S., & Arlotta, P. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.11.003 · Cited by 86 · see citing works
Loss of Cdk2 and Cdk4 Induces a Switch from Proliferation to Differentiation in Neural Stem Cells
Lim, S., & Kaldis, P. (2012) · Stem Cells · doi:10.1002/stem.1114 · Cited by 86 · see citing works
Jalbrzikowski, M., Jonas, R. K., Şentürk, D., Patel, A. B., Chow, C. C., Green, M. F., & Bearden, C. E. (2013) · NeuroImage Clinical · doi:10.1016/j.nicl.2013.09.013 · Cited by 84 · see citing works
“…are also believed to arise from different progenitor cells, which create glial cells and neurons at distinct points in corticogenesis, resulting in SA ultimately reflecting the number of cortical columns and CT representing numbers of neurons within the columns (Pontious et al., 2008; Rakic, 1988).”
BackgroundInfluentialEFHC1 interacts with microtubules to regulate cell division and cortical development
de Nijs, L., Léon, C., Nguyen, L., LoTurco, J. J., Delgado‐Escueta, A. V., Grisar, T. M., & Lakaye, B. (2009) · Nature Neuroscience · doi:10.1038/nn.2390 · Cited by 82 · see citing works
“On the other hand, it is now well established that the developing neocortex contains both types of progenitors: radial progenitors dividing at the apical surface (ventricular zone) and basal progenitors dividing at a basal position (SVZ”
Dwyer, N. D., Chen, B., Chou, S., Hippenmeyer, S., Nguyen, L., & Ghashghaei, H. T. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2359-16.2016 · Cited by 79 · see citing works
“The model was revised when cleavage angle failed to always predict daughter fate (Noctor et al., 2008), and mutations that cause irregular cleavage angles affect cortical thickness in some mutants (Postiglione et al., 2011), but not others (Konno et al., 2008).”
BackgroundLate Origin of Glia-Restricted Progenitors in the Developing Mouse Cerebral Cortex
Costa, M. R., Bucholz, O., Schroeder, T., & Götz, M. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp046 · Cited by 81 · see citing works
“…developmental period from progenitors located in the ventricular zone (VZ) and subventricular zone (SVZ) in both ventral and dorsal telencephalon (Götz and Huttner 2005; Miller and Gauthier 2007; Pontious et al. 2008), as well as from progenitors in the dorsal marginal zone (Costa et al. 2007).”
BackgroundXiang, C., Baubet, V., Pal, S., Holderbaum, L., Tatard-Leitman, V. M., Jiang, P., Davuluri, R. V., & Dahmane, N. (2011) · Cell Death and Differentiation · doi:10.1038/cdd.2011.144 · Cited by 79 · see citing works
Zhang, W., Kim, P. J., Chen, Z., Lokman, H., Qiu, L., Zhang, K., Rozen, S., Tan, E., Je, H. S., & Zeng, L. (2016) · eLife · doi:10.7554/elife.11324 · Cited by 77 · see citing works
“Nuclei were counterstained with DAPI, and mitotic cells were immunostained with PH3.”
MethodInfluentialTyler, W. A., & Haydar, T. F. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.5380-12.2013 · Cited by 81 · see citing works
- Authors
- Pontious, A., Kowalczyk, T., Englund, C., & Hevner, R. F.
- Affiliations
- University of Washington (US)
- ORCID
- Hevner, Robert F.
- Venue
- Developmental Neuroscience
- Publisher
- S. Karger AG
- Published
- 2007-12-13
- Volume
- 30
- Issue
- 1-3
- Pages
- 24-32
- ISSN
- 0378-5866 (ISSN-L)
- 1421-9859
- OpenAlex
- W2012470399
- Cited by
- 378
- References
- 73
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 18 · 2023: 13 · 2022: 15 · 2021: 18 · 2020: 22 · 2019: 22 · 2018: 18 · 2017: 19 · 2016: 20 · 2015: 22 · 2014: 30 · 2013: 31 · 2012: 28
- FWCI
- 2.07
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Developmental Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- 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 › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
- Keywords
- intermediate progenitor cells, cortical development, cortical neurogenesis, subventricular zone, radial glia, neuroepithelial cells, cortical lamination, cortical thickness, cortical surface area, Pax6, Ngn2, Id4, cytoarchitecture, gyrencephaly
- MeSH terms
- Animals, Cell Differentiation, Cerebral Cortex, Humans, Nerve Growth Factors, Nervous System Malformations, Neural Pathways, Neurons, Stem Cells, Signal Transduction, Gene Expression Regulation, Developmental, Mice
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