Lrig1 regulates cell fate specification of glutamatergic neurons via FGF-driven Jak2/Stat3 signaling in cortical progenitors.

De Vincenti, Ana Paula; Bonafina, Antonela; Ledda, Fernanda; Paratcha, Gustavo

doi:10.1242/dev.202879

Article (Scientific journals)

Lrig1 regulates cell fate specification of glutamatergic neurons via FGF-driven Jak2/Stat3 signaling in cortical progenitors.

De Vincenti, Ana Paula; Bonafina, Antonela; Ledda, Fernanda et al.

2024 • In Development, 151 (17)

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/330704

DOI
10.1242/dev.202879

PubMed
39250533

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

De Vincenti and Bonafina et al 2024 development.pdf

Author postprint (8.88 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Cortical progenitors; Embryonic cortical development; Glutamatergic neurogenesis; IL6/Jak2/Stat3 pathway; Lrig1; STAT3 Transcription Factor; Janus Kinase 2; Membrane Glycoproteins; Lrig1 protein, mouse; Stat3 protein, mouse; Jak2 protein, mouse; Fibroblast Growth Factors; Nerve Tissue Proteins; Animals; Mice; Cell Proliferation; Cerebral Cortex/metabolism; Cerebral Cortex/cytology; Cerebral Cortex/embryology; Cell Differentiation; Fibroblast Growth Factors/metabolism; STAT3 Transcription Factor/metabolism; STAT3 Transcription Factor/genetics; Janus Kinase 2/metabolism; Signal Transduction; Neural Stem Cells/metabolism; Neural Stem Cells/cytology; Neurogenesis/genetics; Neurons/metabolism; Neurons/cytology; Membrane Glycoproteins/metabolism; Membrane Glycoproteins/genetics; Mice, Knockout; Cerebral Cortex; Neural Stem Cells; Neurogenesis; Neurons; Molecular Biology; Developmental Biology

Abstract :

[en] The cell-intrinsic mechanisms underlying the decision of a stem/progenitor cell to either proliferate or differentiate remain incompletely understood. Here, we identify the transmembrane protein Lrig1 as a physiological homeostatic regulator of FGF2-driven proliferation and self-renewal of neural progenitors at early-to-mid embryonic stages of cortical development. We show that Lrig1 is expressed in cortical progenitors (CPs), and its ablation caused expansion and increased proliferation of radial/apical progenitors and of neurogenic transit-amplifying Tbr2+ intermediate progenitors. Notably, our findings identify a previously unreported EGF-independent mechanism through which Lrig1 negatively regulates neural progenitor proliferation by modulating the FGF2-induced IL6/Jak2/Stat3 pathway, a molecular cascade that plays a pivotal role in the generation and maintenance of CPs. Consistently, Lrig1 knockout mice showed a significant increase in the density of pyramidal glutamatergic neurons placed in superficial layers 2 and 3 of the postnatal neocortex. Together, these results support a model in which Lrig1 regulates cortical neurogenesis by influencing the cycling activity of a set of progenitors that are temporally specified to produce upper layer glutamatergic neurons.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

De Vincenti, Ana Paula ; Laboratorio de Neurociencia Molecular y Celular, Instituto de Biología Celular y Neurociencias (IBCN)-CONICET-UBA, Facultad de Medicina. Universidad de Buenos Aires (UBA), Buenos Aires CP1121, Argentina

Bonafina, Antonela ; Université de Liège - ULiège > GIGA > GIGA Neurosciences - Molecular Regulation of Neurogenesis ; Laboratorio de Neurociencia Molecular y Celular, Instituto de Biología Celular y Neurociencias (IBCN)-CONICET-UBA, Facultad de Medicina. Universidad de Buenos Aires (UBA), Buenos Aires CP1121, Argentina ; Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas de Buenos Aires, Buenos Aires C1405 BWE, Argentina

Ledda, Fernanda ; Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas de Buenos Aires, Buenos Aires C1405 BWE, Argentina

Paratcha, Gustavo ; Laboratorio de Neurociencia Molecular y Celular, Instituto de Biología Celular y Neurociencias (IBCN)-CONICET-UBA, Facultad de Medicina. Universidad de Buenos Aires (UBA), Buenos Aires CP1121, Argentina

Language :

English

Title :

Lrig1 regulates cell fate specification of glutamatergic neurons via FGF-driven Jak2/Stat3 signaling in cortical progenitors.

Publication date :

01 September 2024

Journal title :

Development

ISSN :

0950-1991

eISSN :

1477-9129

Publisher :

Company of Biologists Ltd, England

Volume :

151

Issue :

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://journals.biologists.com/dev/article-pdf/doi/10.1242/dev.202879/3563622/dev202879.pdf

Funders :

ANPCyT - Agencia Nacional de Promoción Científica y Tecnológica
CONICET - Consejo Nacional de Investigaciones Científicas y Técnicas

Funding text :

We thank Dr Alejandro Schinder and Ignacio Satorre for technical assistance with the preparation and isolation of retroviral particles; Mar\u0131\u00E1 Mercedes Olivera, Marianela Ceol and Andrea Pecile for animal care; Lic. Nerina Villalba for confocal microscopy assistance; and UBATEC for research grant administration. This work was supported by the Agencia Nacional de Promoci\u00F3n Cient\u0131f\u0301ica y Tecnol\u00F3gica (PICT2019-1472, PICT2019-4597 and PICT2020-1524) and the Consejo Nacional de Investigaciones Cient\u0131f\u0301icas y T\u00E9cnicas (IBCN-P-UE 2018-22920180100009). G.P. and F.L. were supported by an Independent Career Position from the Consejo Nacional de Investigaciones Cient\u0131f\u0301icas y T\u00E9cnicas. A.P.D.V. was supported by fellowships from the Consejo Nacional de Investigaciones Cient\u0131f\u0301icas y T\u00E9cnicas and the Agencia Nacional de Promoci\u00F3n Cient\u0131f\u0301ica y Tecnol\u00F3gica, and A.B. was supported by a fellowship from the Agencia Nacional de Promoci\u00F3n Cient\u0131f\u0301ica y Tecnol\u00F3gica.This work was supported by the Agencia Nacional de Promocio\u0301n Cient\u0131f\u0301 ica y Tecnolo\u0301gica (PICT2019-1472, PICT2019-4597 and PICT2020-1524) and the Consejo Nacional de Investigaciones Cient\u0131f\u0301 icas y Te\u0301cnicas (IBCN-P-UE 2018-22920180100009). G.P. and F.L. were supported by an Independent Career Position from the Consejo Nacional de Investigaciones Cient\u0131f\u0301 icas y Te\u0301cnicas. A.P.D.V. was supported by fellowships from the Consejo Nacional de Investigaciones Cient\u0131f\u0301 icas y Te\u0301cnicas and the Agencia Nacional de Promocio\u0301n Cient\u0131f\u0301 ica y Tecnolo\u0301gica, and A.B. was supported by a fellowship from the Agencia Nacional de Promocio\u0301n Cient\u0131f\u0301 ica y Tecnolo\u0301gica.

Available on ORBi :

since 15 April 2025

Statistics

Number of views

185 (0 by ULiège)

Number of downloads

95 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenAlex citations

Bibliography

Ahmad, S. T., Rogers, A. D., Chen, M. J., Dixit, R., Adnani, L., Frankiw, L. S., Lawn, S. O., Blough, M. D., Alshehri, M., Wu, W. et al. (2019). Capicua regulates neural stem cell proliferation and lineage specification through control of Ets factors. Nat. Commun. 10, 2000. doi:10.1038/s41467-019-09949-6
Alsina, F. C., Hita, F. J., Fontanet, P. A., Irala, D., Hedman, H., Ledda, F. and Paratcha, G. (2016). Lrig1 is a cell-intrinsic modulator of hippocampal dendrite complexity and BDNF signaling. EMBO Rep. 17, 601-616. doi:10.15252/embr. 201541218
Andoh, A., Bamba, S., Fujino, S., Inatomi, O., Zhang, Z., Kim, S., Takayanagi, A., Shimizu, N. and Fujiyama, Y. (2004). Fibroblast growth factor-2 stimulates interleukin-6 secretion in human pancreatic periacinar myofibroblasts. Pancreas 29, 278-283. doi:10.1097/00006676-200411000-00006
Bohrer, L. R., Chuntova, P., Bade, L. K., Beadnell, T. C., Leon, R. P., Brady, N. J., Ryu, Y., Goldberg, J. E., Schmechel, S. C., Koopmeiners, J. S. et al. (2014). Activation of the FGFR-STAT3 pathway in breast cancer cells induces a hyaluronan-rich microenvironment that licenses tumor formation. Cancer Res. 74, 374-386. doi:10.1158/0008-5472.CAN-13-2469
Bonafina, A., Fontanet, P. A., Paratcha, G. and Ledda, F. (2018). GDNF/ GFRalpha1 complex abrogates self-renewing activity of cortical neural precursors inducing their differentiation. Stem Cell Rep. 10, 1000-1015. doi:10.1016/j.stemcr. 2018.01.019
Bonnefont, J. and Vanderhaeghen, P. (2021). Neuronal fate acquisition and specification: time for a change. Curr. Opin. Neurobiol. 66, 195-204. doi:10.1016/j. conb.2020.12.006
Borrell, V. and Reillo, I. (2012). Emerging roles of neural stem cells in cerebral cortex development and evolution. Dev. Neurobiol. 72, 955-971. doi:10.1002/ dneu.22013
Bruining, H., Hardstone, R., Juarez-Martinez, E. L., Sprengers, J., Avramiea, A. E., Simpraga, S., Houtman, S. J., Poil, S. S., Dallares, E., Palva, S. et al. (2020). Measurement of excitation-inhibition ratio in autism spectrum disorder using critical brain dynamics. Sci. Rep. 10, 9195. doi:10.1038/s41598-020-65500-4
Burrows, R. C., Wancio, D., Levitt, P. and Lillien, L. (1997). Response diversity and the timing of progenitor cell maturation are regulated by developmental changes in EGFR expression in the cortex. Neuron 19, 251-267. doi:10.1016/ S0896-6273(00)80937-X
Chen, J.-X., Xu, L.-L., Wang, X.-C., Qin, H.-Y. and Wang, J.-L. (2011). Involvement of c-Src/STAT3 signal in EGF-induced proliferation of rat spermatogonial stem cells. Mol. Cell. Biochem. 358, 67-73. doi:10.1007/s11010-011-0922-2
Chen, L., Guo, Z., Zhou, Y., Ni, J., Zhu, J., Fan, X., Chen, X., Liu, Y., Li, Z. and Zhou, H. (2021). microRNA-1246-containing extracellular vesicles from acute myeloid leukemia cells promote the survival of leukemia stem cells via the LRIG1-meditated STAT3 pathway. Aging (Albany NY) 13, 13644-13662. doi:10.18632/ aging.202893
Courchesne, E., Mouton, P. R., Calhoun, M. E., Semendeferi, K., Ahrens-Barbeau, C., Hallet, M. J., Barnes, C. C. and Pierce, K. (2011). Neuron number and size in prefrontal cortex of children with autism. JAMA 306, 2001-2010. doi:10. 1001/jama.2011.1638
De Vincenti, A. P., Alsina, F. C., Ferrero Restelli, F., Hedman, H., Ledda, F. and Paratcha, G. (2021). Lrig1 and Lrig3 cooperate to control Ret receptor signaling, sensory axonal growth and epidermal innervation. Development 148, dev197020. doi:10.1242/dev.197020
Dehay, C. and Kennedy, H. (2007). Cell-cycle control and cortical development. Nat. Rev. Neurosci. 8, 438-450. doi:10.1038/nrn2097
Di Bella, D. J., Habibi, E., Stickels, R. R., Scalia, G., Brown, J., Yadollahpour, P., Yang, S. M., Abbate, C., Biancalani, T., Macosko, E. Z. et al. (2021). Molecular logic of cellular diversification in the mouse cerebral cortex. Nature 595, 554-559. doi:10.1038/s41586-021-03670-5
Dwyer, N. D., Chen, B., Chou, S. J., Hippenmeyer, S., Nguyen, L. and Ghashghaei, H. T. (2016). Neural stem cells to cerebral cortex: emerging mechanisms regulating progenitor behavior and productivity. J. Neurosci. 36, 11394-11401. doi:10.1523/JNEUROSCI.2359-16.2016
Englund, C., Fink, A., Lau, C., Pham, D., Daza, R. A., Bulfone, A., Kowalczyk, T. and Hevner, R. F. (2005). Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 25, 247-251. doi:10.1523/JNEUROSCI.2899-04.2005
Fame, R. M., Macdonald, J. L. and Macklis, J. D. (2011). Development, specification, and diversity of callosal projection neurons. Trends Neurosci. 34, 41-50. doi:10.1016/j.tins.2010.10.002
Fang, W. Q., Chen, W. W., Jiang, L., Liu, K., Yung, W. H., Fu, A. K. Y. and Ip, N. Y. (2014). Overproduction of upper-layer neurons in the neocortex leads to autism-like features in mice. Cell Rep. 9, 1635-1643. doi:10.1016/j.celrep.2014.11.003
Fox, I. J. and Kornblum, H. I. (2005). Developmental profile of ErbB receptors in murine central nervous system: implications for functional interactions. J. Neurosci. Res. 79, 584-597. doi:10.1002/jnr.20381
Fu, Y., Yang, M., Yu, H., Wang, Y., Wu, X., Yong, J., Mao, Y., Cui, Y., Fan, X., Wen, L. et al. (2021). Heterogeneity of glial progenitor cells during the neurogenesis-to-gliogenesis switch in the developing human cerebral cortex. Cell Rep. 34, 108788. doi:10.1016/j.celrep.2021.108788
Gallagher, D., Norman, A. A., Woodard, C. L., Yang, G., Gauthier-Fisher, A., Fujitani, M., Vessey, J. P., Cancino, G. I., Sachewsky, N., Woltjen, K. et al. (2013). Transient maternal IL-6 mediates long-lasting changes in neural stem cell pools by deregulating an endogenous self-renewal pathway. Cell Stem Cell 13, 564-576. doi:10.1016/j.stem.2013.10.002
Gaspard, N., Bouschet, T., Hourez, R., Dimidschstein, J., Naeije, G., Van Den Ameele, J., Espuny-Camacho, I., Herpoel, A., Passante, L., Schiffmann, S. N. et al. (2008). An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455, 351-357. doi:10.1038/nature07287
Gur, G., Rubin, C., Katz, M., Amit, I., Citri, A., Nilsson, J., Amariglio, N., Henriksson, R., Rechavi, G., Hedman, H. et al. (2004). LRIG1 restricts growth factor signaling by enhancing receptor ubiquitylation and degradation. EMBO J. 23, 3270-3281. doi:10.1038/sj.emboj.7600342
Hedman, H. and Henriksson, R. (2007). LRIG inhibitors of growth factor signalling - double-edged swords in human cancer? Eur. J. Cancer 43, 676-682. doi:10.1016/ j.ejca.2006.10.021
Herdenberg, C. and Hedman, H. (2023). HYPOTHESIS: do LRIG proteins regulate stem cell quiescence by promoting BMP signaling? Stem Cell Rev. Rep. 19, 59-66. doi:10.1007/s12015-022-10442-9
Herdenberg, C., Mutie, P. M., Billing, O., Abdullah, A., Strawbridge, R. J., Dahlman, I., Tuck, S., Holmlund, C., Arner, P., Henriksson, R. et al. (2021). LRIG proteins regulate lipid metabolism via BMP signaling and affect the risk of type 2 diabetes. Commun. Biol. 4, 90. doi:10.1038/s42003-020-01613-w
Hong, S. and Song, M. R. (2015). Signal transducer and activator of transcription-3 maintains the stemness of radial glia at mid-neurogenesis. J. Neurosci. 35, 1011-1023. doi:10.1523/JNEUROSCI.2119-14.2015
Jensen, K. B. and Watt, F. M. (2006). Single-cell expression profiling of human epidermal stem and transit-amplifying cells: Lrig1 is a regulator of stem cell quiescence. Proc. Natl. Acad. Sci. USA 103, 11958-11963. doi:10.1073/pnas. 0601886103
Jensen, K. B., Collins, C. A., Nascimento, E., Tan, D. W., Frye, M., Itami, S. and Watt, F. M. (2009). Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell 4, 427-439. doi:10.1016/j.stem. 2009.04.014
Jeong, D., Lozano Casasbuenas, D., Gengatharan, A., Edwards, K., Saghatelyan, A., Kaplan, D. R., Miller, F. D. and Yuzwa, S. A. (2020). LRIG1-mediated inhibition of EGF receptor signaling regulates neural precursor cell proliferation in the neocortex. Cell Rep. 33, 108257. doi:10.1016/j.celrep.2020. 108257
Ji, Y., Kumar, R., Gokhale, A., Chao, H. P., Rycaj, K., Chen, X., Li, Q. and Tang, D. G. (2022). LRIG1, a regulator of stem cell quiescence and a pleiotropic feedback tumor suppressor. Semin. Cancer Biol. 82, 120-133. doi:10.1016/j. semcancer.2020.12.016
Kam, J. W., Raja, R. and Cloutier, J. F. (2014). Cellular and molecular mechanisms regulating embryonic neurogenesis in the rodent olfactory epithelium. Int. J. Dev. Neurosci. 37, 76-86. doi:10.1016/j.ijdevneu.2014.06.017
Kast, R. J. and Levitt, P. (2019). Precision in the development of neocortical architecture: from progenitors to cortical networks. Prog. Neurobiol. 175, 77-95. doi:10.1016/j.pneurobio.2019.01.003
Kilpatrick, T. J. and Bartlett, P. F. (1995). Cloned multipotential precursors from the mouse cerebrum require FGF-2, whereas glial restricted precursors are stimulated with either FGF-2 or EGF. J. Neurosci. 15, 3653-3661. doi:10.1523/JNEUROSCI. 15-05-03653.1995
Kornblum, H. I., Hussain, R. J., Bronstein, J. M., Gall, C. M., Lee, D. C. and Seroogy, K. B. (1997). Prenatal ontogeny of the epidermal growth factor receptor and its ligand, transforming growth factor alpha, in the rat brain. J. Comp. Neurol. 380, 243-261. doi:10.1002/(SICI)1096-9861(19970407)380:2<243::AID-CNE7>3.0.CO;2-3
Kozawa, O., Suzuki, A. and Uematsu, T. (1997). Basic fibroblast growth factor induces interleukin-6 synthesis in osteoblasts: autoregulation by protein kinase C. Cell. Signal. 9, 463-468. doi:10.1016/S0898-6568(97)00043-0
Laederich, M. B., Funes-Duran, M., Yen, L., Ingalla, E., Wu, X., Carraway, K. L., 3rd and Sweeney, C. (2004). The leucine-rich repeat protein LRIG1 is a negative regulator of ErbB family receptor tyrosine kinases. J. Biol. Chem. 279, 47050-47056. doi:10.1074/jbc.M409703200
Ledda, F. and Paratcha, G. (2016). Assembly of neuronal connectivity by neurotrophic factors and leucine-rich repeat proteins. Front. Cell Neurosci. 10, 199. doi:10.3389/fncel.2016.00199
Ledda, F., Bieraugel, O., Fard, S. S., Vilar, M. and Paratcha, G. (2008). Lrig1 is an endogenous inhibitor of Ret receptor tyrosine kinase activation, downstream signaling, and biological responses to GDNF. J. Neurosci. 28, 39-49. doi:10.1523/ JNEUROSCI.2196-07.2008
Lee, E., Lee, J. and Kim, E. (2017). Excitation/inhibition imbalance in animal models of autism spectrum disorders. Biol. Psychiatry 81, 838-847. doi:10.1016/j. biopsych.2016.05.011
Lillien, L. and Raphael, H. (2000). BMP and FGF regulate the development of EGF-responsive neural progenitor cells. Development 127, 4993-5005. doi:10.1242/ dev.127.22.4993
Lukaszewicz, A., Savatier, P., Cortay, V., Kennedy, H. and Dehay, C. (2002). Contrasting effects of basic fibroblast growth factor and neurotrophin 3 on cell cycle kinetics of mouse cortical stem cells. J. Neurosci. 22, 6610-6622. doi:10. 1523/JNEUROSCI.22-15-06610.2002
Ma, J. H., Qin, L. and Li, X. (2020). Role of STAT3 signaling pathway in breast cancer. Cell Commun. Signal 18, 33. doi:10.1186/s12964-020-0527-z
Mao, F., Holmlund, C., Faraz, M., Wang, W., Bergenheim, T., Kvarnbrink, S., Johansson, M., Henriksson, R. and Hedman, H. (2018). Lrig1 is a haploinsufficient tumor suppressor gene in malignant glioma. Oncogenesis 7, 13. doi:10.1038/s41389-017-0012-8
Marques-Torrejon, M. A., Williams, C. A. C., Southgate, B., Alfazema, N., Clements, M. P., Garcia-Diaz, C., Blin, C., Arranz-Emparan, N., Fraser, J., Gammoh, N. et al. (2021). LRIG1 is a gatekeeper to exit from quiescence in adult neural stem cells. Nat. Commun. 12, 2594. doi:10.1038/s41467-021-22813-w
Mira, H., Andreu, Z., Suh, H., Lie, D. C., Jessberger, S., Consiglio, A., San Emeterio, J., Hortiguela, R., Marques-Torrejon, M. A., Nakashima, K. et al. (2010). Signaling through BMPR-IA regulates quiescence and long-term activity of neural stem cells in the adult hippocampus. Cell Stem Cell 7, 78-89. doi:10. 1016/j.stem.2010.04.016
Molyneaux, B. J., Arlotta, P., Menezes, J. R. and Macklis, J. D. (2007). Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 8, 427-437. doi:10.1038/nrn2151
Mukhtar, T. and Taylor, V. (2018). Untangling cortical complexity during development. J. Exp. Neurosci. 12, 117906951875933. doi:10.1177/1179069518759332
Nakamura, T., Hamuro, J., Takaishi, M., Simmons, S., Maruyama, K., Zaffalon, A., Bentley, A. J., Kawasaki, S., Nagata-Takaoka, M., Fullwood, N. J. et al. (2014). LRIG1 inhibits STAT3-dependent inflammation to maintain corneal homeostasis. J. Clin. Invest. 124, 385-397. doi:10.1172/JCI71488
Nam, H. S. and Capecchi, M. R. (2020). Lrig1 expression prospectively identifies stem cells in the ventricular-subventricular zone that are neurogenic throughout adult life. Neural Dev. 15, 3. doi:10.1186/s13064-020-00139-5
Nam, H. S. and Capecchi, M. R. (2023). Lrig1 expression identifies quiescent stem cells in the ventricular-subventricular zone from postnatal development to adulthood and limits their persistent hyperproliferation. Neural Dev. 18, 1. doi:10.1186/s13064-022-00169-1
Neirinckx, V., Hedman, H. and Niclou, S. P. (2017). Harnessing LRIG1-mediated inhibition of receptor tyrosine kinases for cancer therapy. Biochim. Biophys. Acta Rev. Cancer 1868, 109-116. doi:10.1016/j.bbcan.2017.02.007
Ohtsuka, T. and Kageyama, R. (2019). Regulation of temporal properties of neural stem cells and transition timing of neurogenesis and gliogenesis during mammalian neocortical development. Semin. Cell Dev. Biol. 95, 4-11. doi:10. 1016/j.semcdb.2019.01.007
Page, M. E., Lombard, P., Ng, F., Gottgens, B. and Jensen, K. B. (2013). The epidermis comprises autonomous compartments maintained by distinct stem cell populations. Cell Stem Cell 13, 471-482. doi:10.1016/j.stem.2013.07.010
Powell, A. E., Wang, Y., Li, Y., Poulin, E. J., Means, A. L., Washington, M. K., Higginbotham, J. N., Juchheim, A., Prasad, N., Levy, S. E. et al. (2012). The pan-ErbB negative regulator Lrig1 is an intestinal stem cell marker that functions as a tumor suppressor. Cell 149, 146-158. doi:10.1016/j.cell.2012.02.042
Reynolds, B. A. and Weiss, S. (1996). Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol. 175, 1-13. doi:10.1006/dbio.1996.0090
Salazar-Grueso, E. F., Kim, S. and Kim, H. (1991). Embryonic mouse spinal cord motor neuron hybrid cells. Neuroreport 2, 505-508. doi:10.1097/00001756-199109000-00002
Sano, S., Chan, K. S., Carbajal, S., Clifford, J., Peavey, M., Kiguchi, K., Itami, S., Nickoloff, B. J. and Digiovanni, J. (2005). Stat3 links activated keratinocytes and immunocytes required for development of psoriasis in a novel transgenic mouse model. Nat. Med. 11, 43-49. doi:10.1038/nm1162
Sessa, A., Mao, C. A., Hadjantonakis, A. K., Klein, W. H. and Broccoli, V. (2008). Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesis in the developing neocortex. Neuron 60, 56-69. doi:10.1016/j.neuron.2008.09.028
Shattuck, D. L., Miller, J. K., Laederich, M., Funes, M., Petersen, H., Carraway, K. L., 3rd and Sweeney, C. (2007). LRIG1 is a novel negative regulator of the Met receptor and opposes Met and Her2 synergy. Mol. Cell. Biol. 27, 1934-1946. doi:10.1128/MCB.00757-06
Simion, C., Cedano-Prieto, M. E. and Sweeney, C. (2014). The LRIG family: enigmatic regulators of growth factor receptor signaling. Endocr Relat. Cancer 21, R431-R443. doi:10.1530/ERC-14-0179
Sun, W., Cornwell, A., Li, J., Peng, S., Osorio, M. J., Aalling, N., Wang, S., Benraiss, A., Lou, N., Goldman, S. A. et al. (2017). SOX9 Is an Astrocyte-Specific Nuclear Marker in the Adult Brain Outside the Neurogenic Regions. J. Neurosci. 37, 4493-4507. doi:10.1523/JNEUROSCI.3199-16.2017
Suzuki, Y., Miura, H., Tanemura, A., Kobayashi, K., Kondoh, G., Sano, S., Ozawa, K., Inui, S., Nakata, A., Takagi, T. et al. (2002). Targeted disruption of LIG-1 gene results in psoriasiform epidermal hyperplasia. FEBS Lett. 521, 67-71. doi:10.1016/S0014-5793(02)02824-7
Telley, L., Govindan, S., Prados, J., Stevant, I., Nef, S., Dermitzakis, E., Dayer, A. and Jabaudon, D. (2016). Sequential transcriptional waves direct the differentiation of newborn neurons in the mouse neocortex. Science 351, 1443-1446. doi:10.1126/science.aad8361
Todd, L., Squires, N., Suarez, L. and Fischer, A. J. (2016). Jak/Stat signaling regulates the proliferation and neurogenic potential of Muller glia-derived progenitor cells in the avian retina. Sci. Rep. 6, 35703. doi:10.1038/srep35703
Toma, K. and Hanashima, C. (2015). Switching modes in corticogenesis: mechanisms of neuronal subtype transitions and integration in the cerebral cortex. Front. Neurosci. 9, 274. doi:10.3389/fnins.2015.00274
Vaccarino, F. M., Grigorenko, E. L., Smith, K. M. and Stevens, H. E. (2009). Regulation of cerebral cortical size and neuron number by fibroblast growth factors: implications for autism. J. Autism Dev. Disord. 39, 511-520. doi:10.1007/ s10803-008-0653-8
Van Erp, S., Van Den Heuvel, D. M. A., Fujita, Y., Robinson, R. A., Hellemons, A., Adolfs, Y., Van Battum, E. Y., Blokhuis, A. M., Kuijpers, M., Demmers, J. A. A. et al. (2015). Lrig2 negatively regulates ectodomain shedding of axon guidance receptors by ADAM proteases. Dev. Cell 35, 537-552. doi:10.1016/j.devcel.2015. 11.008
Wang, Y., Poulin, E. J. and Coffey, R. J. (2013). LRIG1 is a triple threat: ERBB negative regulator, intestinal stem cell marker and tumour suppressor. Br. J. Cancer 108, 1765-1770. doi:10.1038/bjc.2013.138
Wegiel, J., Kuchna, I., Nowicki, K., Imaki, H., Wegiel, J., Marchi, E., Ma, S. Y., Chauhan, A., Chauhan, V., Bobrowicz, T. W. et al. (2010). The neuropathology of autism: defects of neurogenesis and neuronal migration, and dysplastic changes. Acta Neuropathol. 119, 755-770. doi:10.1007/s00401-010-0655-4
Wendt, M. K., Balanis, N., Carlin, C. R. and Schiemann, W. P. (2014). STAT3 and epithelial-mesenchymal transitions in carcinomas. JAKSTAT 3, e28975. doi:10. 4161/jkst.28975
Wong, V. W., Stange, D. E., Page, M. E., Buczacki, S., Wabik, A., Itami, S., Van De Wetering, M., Poulsom, R., Wright, N. A., Trotter, M. W. et al. (2012). Lrig1 controls intestinal stem-cell homeostasis by negative regulation of ErbB signalling. Nat. Cell Biol. 14, 401-408. doi:10.1038/ncb2464
Xie, Y., Kuan, A. T., Wang, W., Herbert, Z. T., Mosto, O., Olukoya, O., Adam, M., Vu, S., Kim, M., Tran, D. et al. (2022). Astrocyte-neuron crosstalk through Hedgehog signaling mediates cortical synapse development. Cell Rep. 38, 110416. doi:10.1016/j.celrep.2022.110416
Yoshimatsu, T., Kawaguchi, D., Oishi, K., Takeda, K., Akira, S., Masuyama, N. and Gotoh, Y. (2006). Non-cell-autonomous action of STAT3 in maintenance of neural precursor cells in the mouse neocortex. Development 133, 2553-2563. doi:10.1242/dev.02419
Zhao, H., Tanegashima, K., Ro, H. and Dawid, I. B. (2008). Lrig3 regulates neural crest formation in Xenopus by modulating Fgf and Wnt signaling pathways. Development 135, 1283-1293. doi:10.1242/dev.015073