Non-cell autonomous promotion of astrogenesis at late embryonic stages by constitutive YAP activation.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
27 04 2020
27 04 2020
Historique:
received:
16
07
2018
accepted:
08
03
2020
entrez:
29
4
2020
pubmed:
29
4
2020
medline:
15
12
2020
Statut:
epublish
Résumé
Although astrocytes have gained increased recognition as an important regulator in normal brain function and pathology, the mechanisms underlying their genesis are not well understood. In this study, we show that constitutive YAP activation by in utero introduction of a non-degradable form of the YAP gene (YAP 5SA) causes productive GFAP
Identifiants
pubmed: 32341445
doi: 10.1038/s41598-020-63890-z
pii: 10.1038/s41598-020-63890-z
pmc: PMC7184574
doi:
Substances chimiques
Bone Morphogenetic Protein 4
0
Ciliary Neurotrophic Factor
0
Glial Fibrillary Acidic Protein
0
Oncogene Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
7041Subventions
Organisme : NIMH NIH HHS
ID : R01 MH077694
Pays : United States
Références
Piet, R., Vargová, L., Syková, E., Poulain, D. A. & Oliet, S. H. Physiological contribution of the astrocytic environment of neurons to intersynaptic crosstalk. Proc. Natl. Acad. Sci. USA 101, 2151–2155 (2004).
pubmed: 14766975
doi: 10.1073/pnas.0308408100
pmcid: 14766975
Parri, R. & Crunelli, V. An astrocyte bridge from synapse to blood flow. Nat. Neurosci. 6, 5–6 (2003).
pubmed: 12494240
doi: 10.1038/nn0103-5
pmcid: 12494240
Alvarez, J. I., Katayama, T. & Prat, A. Glial influence on the blood brain barrier. Glia 61, 1939–1958 (2013).
pubmed: 24123158
pmcid: 4068281
doi: 10.1002/glia.22575
Han, X. et al. Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. Cell Stem Cell 12, 342–353 (2013).
pubmed: 23472873
pmcid: 3700554
doi: 10.1016/j.stem.2012.12.015
Anderson, M. A. et al. Astrocyte scar formation aids central nervous system axon regeneration. Nature 532, 195–200 (2016).
pubmed: 27027288
pmcid: 5243141
doi: 10.1038/nature17623
Barker, A. J. & Ullian, E. M. New roles for astrocytes in developing synaptic circuits. Commun. Integr. Biol. 1, 207–211 (2008).
pubmed: 19513261
pmcid: 2686024
doi: 10.4161/cib.1.2.7284
Sloan, S. A. & Barres, B. A. Mechanisms of astrocyte development and their contributions to neurodevelopmental disorders. Curr Opin. Neurobiol. 27, 75–81 (2014).
pubmed: 24694749
pmcid: 4433289
doi: 10.1016/j.conb.2014.03.005
Ge, W.-P., Miyawaki, A., Gage, F. H., Jan, Y. N. & Jan, L. Y. Local generation of glia is a major astrocyte source in postnatal cortex. Nature 484, 376–380 (2012).
pubmed: 22456708
pmcid: 3777276
doi: 10.1038/nature10959
Ochiai, W., Yanagisawa, M., Takizawa, T., Nakashima, K. & Taga, T. Astrocyte differentiation of fetal neuroepithelial cells involving cardiotrophin-1-induced activation of STAT3. Cytokine 14, 264–271 (2001).
pubmed: 11444906
doi: 10.1006/cyto.2001.0883
pmcid: 11444906
Nakashima, K., Yanagisawa, M., Arakawa, H. & Taga, T. Astrocyte differentiation mediated by LIF in cooperation with BMP2. FEBS. Lett. 457, 43–46 (1999).
pubmed: 10486560
doi: 10.1016/S0014-5793(99)00997-7
pmcid: 10486560
Rajan, P. & McKay, R. D. Multiple routes to astrocytic differentiation in the CNS. J. Neurosci. 18, 3620–3629 (1998).
pubmed: 9570793
pmcid: 6793143
doi: 10.1523/JNEUROSCI.18-10-03620.1998
Derouet, D. et al. Neuropoietin, a new IL-6-related cytokine signaling through the ciliary neurotrophic factor receptor. Proc. Natl. Acad. Sci. USA. 101, 4827–4832 (2004).
pubmed: 15051883
doi: 10.1073/pnas.0306178101
pmcid: 15051883
Uemura, A. et al. Cardiotrophin-like cytokine induces astrocyte differentiation of fetal neuroepithelial cells via activation of STAT3. Cytokine 18, 1–7 (2002).
pubmed: 12090754
doi: 10.1006/cyto.2002.1006
Miyazono, K., Kusanagi, K. & Inoue, H. Divergence and convergence of TGF‐β/BMP signaling. J Cell Physiol 187, 265–276 (2001).
pubmed: 11319750
doi: 10.1002/jcp.1080
pmcid: 11319750
Lee, J., Borboa, A. K., Baird, A. & Eliceiri, B. P. Non-invasive quantification of brain tumor-induced astrogliosis. BMC. Neurosci. 12, 9, https://doi.org/10.1186/1471-2202-12-9 (2011).
doi: 10.1186/1471-2202-12-9
pubmed: 21247490
pmcid: 3033849
O’Callaghan, J. P., Kelly, K. A., VanGilder, R. L., Sofroniew, M. V. & Miller, D. B. Early activation of STAT3 regulates reactive astrogliosis induced by diverse forms of neurotoxicity. PLoS One 9, e102003 (2014).
pubmed: 25025494
pmcid: 4098997
doi: 10.1371/journal.pone.0102003
Yu, Z., Yu, P., Chen, H. & Geller, H. M. Targeted inhibition of KCa3. 1 attenuates TGF‐β‐induced reactive astrogliosis through the Smad2/3 signaling pathway. J. Neurochem. 130, 41–49 (2014).
pubmed: 24606313
pmcid: 4065629
doi: 10.1111/jnc.12710
Saucedo, L. J. & Edgar, B. A. Filling out the Hippo pathway. Nat. Rev. Mol. Cell. Biol. 8, 613–621 (2007).
pubmed: 17622252
doi: 10.1038/nrm2221
pmcid: 17622252
Hilman, D. & Gat, U. The evolutionary history of YAP and the hippo/YAP pathway. Mol Biol Evol 28, 2403–2417 (2011).
pubmed: 21415026
doi: 10.1093/molbev/msr065
Kanai, F. et al. TAZ: a novel transcriptional co-activator regulated by interactions with 14‐3‐3 and PDZ domain proteins. EMBO J 19, 6778–6791 (2000).
pubmed: 11118213
pmcid: 305881
doi: 10.1093/emboj/19.24.6778
Cao, X., Pfaff, S. L. & Gage, F. H. YAP regulates neural progenitor cell number via the TEA domain transcription factor. Genes. Dev. 22, 3320–3334 (2008).
pubmed: 19015275
pmcid: 2600760
doi: 10.1101/gad.1726608
Gee, S. T., Milgram, S. L., Kramer, K. L., Conlon, F. L. & Moody, S. A. Yes-associated protein 65 (YAP) expands neural progenitors and regulates Pax3 expression in the neural plate border zone. PloS One 6, e20309 (2011).
pubmed: 21687713
pmcid: 3110623
doi: 10.1371/journal.pone.0020309
Lavado, A. et al. Tumor suppressor Nf2 limits expansion of the neural progenitor pool by inhibiting Yap/Taz transcriptional coactivators. Development 140, 3323–3334 (2013).
pubmed: 23863479
pmcid: 3737715
doi: 10.1242/dev.096537
Huang, Z. et al. YAP stabilizes SMAD1 and promotes BMP2-induced neocortical astrocytic differentiation. Development 143, 2398–2409 (2016).
pubmed: 27381227
pmcid: 4958318
doi: 10.1242/dev.130658
Huang, Z. et al. Neogenin promotes BMP2 activation of YAP and Smad1 and enhances astrocytic differentiation in developing mouse neocortex. J. Neurosci. 36, 5833–5849 (2016).
pubmed: 27225772
pmcid: 4879200
doi: 10.1523/JNEUROSCI.4487-15.2016
Zhao, B. et al. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes. Dev. 21, 2747–2761 (2007).
pubmed: 17974916
pmcid: 2045129
doi: 10.1101/gad.1602907
Byun, S.-H. et al. TRBP maintains mammalian embryonic neural stem cell properties by acting as a novel transcriptional coactivator of the Notch signaling pathway. Development 144, 778–783 (2017).
pubmed: 28174252
pmcid: 6514399
doi: 10.1242/dev.139493
Oka, T. et al. Functional complexes between YAP2 and ZO-2 are PDZ domain-dependent, and regulate YAP2 nuclear localization and signalling. Biochem. J 432, 461–478 (2010).
pubmed: 20868367
doi: 10.1042/BJ20100870
pmcid: 20868367
Zhao, B. et al. TEAD mediates YAP-dependent gene induction and growth control. Genes. Dev. 22, 1962–1971 (2008).
pubmed: 18579750
pmcid: 2492741
doi: 10.1101/gad.1664408
Oka, T., Mazack, V. & Sudol, M. Mst2 and Lats kinases regulate apoptotic function of Yes kinase-associated protein (YAP). J Biol Chem 283, 27534–27546 (2008).
pubmed: 18640976
doi: 10.1074/jbc.M804380200
pmcid: 18640976
Lai, D. & Yang, X. BMP4 is a novel transcriptional target and mediator of mammary cell migration downstream of the Hippo pathway component TAZ. Cell Signal 25, 1720–1728 (2013).
pubmed: 23673366
doi: 10.1016/j.cellsig.2013.05.002
pmcid: 23673366
Bhat, K. P. et al. The transcriptional coactivator TAZ regulates mesenchymal differentiation in malignant glioma. Genes. Dev. 25, 2594–2609 (2011).
pubmed: 22190458
pmcid: 3248681
doi: 10.1101/gad.176800.111
Skoff, R. P. & Knapp, P. E. Division of astroblasts and oligodendroblasts in postnatal rodent brain: evidence for separate astrocyte and oligodendrocyte lineages. Glia 4, 165–174 (1991).
pubmed: 1827776
doi: 10.1002/glia.440040208
pmcid: 1827776
Mallamaci, A. Developmental control of cortico-cerebral astrogenesis. Int. J. Dev. Biol. 57, 689–706 (2013).
pubmed: 24307293
doi: 10.1387/ijdb.130148am
pmcid: 24307293
Mendes, F. et al. Connective-tissue growth factor (CTGF/CCN2) induces astrogenesis and fibronectin expression of embryonic neural cells in vitro. PLoS One 10, e0133689, https://doi.org/10.1371/journal.pone.0133689 (2015).
doi: 10.1371/journal.pone.0133689
pubmed: 26241738
pmcid: 4524627
Cole, A. E., Murray, S. S. & Xiao, J. Bone morphogenetic protein 4 signalling in neural stem and progenitor cells during development and after Injury. Stem Cells Int 2016, https://doi.org/10.1155/2016/9260592 (2016).
Nakashima, K. et al. Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 284, 479–482 (1999).
pubmed: 10205054
doi: 10.1126/science.284.5413.479
pmcid: 10205054
Fukuda, S. et al. Potentiation of astrogliogenesis by STAT3-mediated activation of bone morphogenetic protein-Smad signaling in neural stem cells. Mol. Cell. Biol. 27, 4931–4937 (2007).
pubmed: 17452461
pmcid: 1951480
doi: 10.1128/MCB.02435-06
Ignatova, T. N. et al. Human cortical glial tumors contain neural stem‐like cells expressing astroglial and neuronal markers in vitro. Glia 39, 193–206 (2002).
pubmed: 12203386
doi: 10.1002/glia.10094
Hemmati, H. D. et al. Cancerous stem cells can arise from pediatric brain tumors. Proc. Natl. Acad. Sci. USA. 100, 15178–15183 (2003).
pubmed: 14645703
doi: 10.1073/pnas.2036535100
pmcid: 14645703
Orr, B. A. et al. Yes-associated protein 1 is widely expressed in human brain tumors and promotes glioblastoma growth. J. Neuropathol. Exp. Neurol. 70, 568–577 (2011).
pubmed: 21666501
pmcid: 3130608
doi: 10.1097/NEN.0b013e31821ff8d8
Le, D. M. et al. Exploitation of astrocytes by glioma cells to facilitate invasiveness: a mechanism involving matrix metalloproteinase-2 and the urokinase-type plasminogen activator–plasmin cascade. J. Neurosci. 23, 4034–4043 (2003).
pubmed: 12764090
pmcid: 6741112
doi: 10.1523/JNEUROSCI.23-10-04034.2003
Becher, O. J. et al. Gli activity correlates with tumor grade in platelet-derived growth factor–induced gliomas. Cancer Res. 68, 2241–2249 (2008).
pubmed: 18381430
doi: 10.1158/0008-5472.CAN-07-6350
pmcid: 18381430
Liu, L. et al. Astrocyte elevated gene-1 upregulates matrix metalloproteinase-9 and induces human glioma invasion. Cancer Res. 70, 3750–3759 (2010).
pubmed: 20388776
doi: 10.1158/0008-5472.CAN-09-3838
pmcid: 20388776
Hoelzinger, D. B., Demuth, T. & Berens, M. E. Autocrine factors that sustain glioma invasion and paracrine biology in the brain microenvironment. J. Natl. Cancer Inst. 99, 1583–1593 (2007).
pubmed: 17971532
doi: 10.1093/jnci/djm187
pmcid: 17971532
Bajetto, A. et al. Glial and neuronal cells express functional chemokine receptor CXCR4 and its natural ligand stromal cell-derived factor 1. J. Neurochem 73, 2348–2357 (1999).
pubmed: 10582593
doi: 10.1046/j.1471-4159.1999.0732348.x
pmcid: 10582593
Barbero, S. et al. Expression of the chemokine receptor CXCR4 and its ligand stromal cell‐derived factor 1 in human brain tumors and their involvement in glial proliferation in vitro. Ann. N. Y. Acad. Sci. 973, 60–69 (2002).
pubmed: 12485835
doi: 10.1111/j.1749-6632.2002.tb04607.x
pmcid: 12485835
Kahn, M., Ellison, J., Speight, G. & De Vellis, J. CNTF regulation of astrogliosis and the activation of microglia in the developing rat central nervous system. Brain Res. 685, 55–67 (1995).
pubmed: 7583254
doi: 10.1016/0006-8993(95)00411-I
pmcid: 7583254
Winter, C. G., Saotome, Y., Levison, S. W. & Hirsh, D. A role for ciliary neurotrophic factor as an inducer of reactive gliosis, the glial response to central nervous system injury. Proc. Natl. Acad. Sci. USA. 92, 5865–5869 (1995).
pubmed: 7597043
doi: 10.1073/pnas.92.13.5865
pmcid: 7597043
Bhat, K. P. et al. Mesenchymal differentiation mediated by NF-κB promotes radiation resistance in glioblastoma. Cancer Cell. 24, 331–346 (2013).
pubmed: 23993863
doi: 10.1016/j.ccr.2013.08.001
pmcid: 23993863
Carro, M. S. et al. The transcriptional network for mesenchymal transformation of brain tumours. Nature 463, 318–325 (2010).
pubmed: 20032975
doi: 10.1038/nature08712
pmcid: 20032975
Mizuno, T. et al. YAP induces malignant mesothelioma cell proliferation by upregulating transcription of cell cycle-promoting genes. Oncogene 31, 5117–5122 (2012).
pubmed: 22286761
doi: 10.1038/onc.2012.5
pmcid: 22286761
Han, D. et al. Human cytomegalovirus IE2 protein disturbs brain development by the dysregulation of neural stem cell maintenance and the polarization of migrating neurons. J. Virol 91, e00799–00717, https://doi.org/10.1128/JVI.00799-17 (2017).
doi: 10.1128/JVI.00799-17
pubmed: 28615204
pmcid: 5553173