{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,29]],"date-time":"2026-10-29T23:28:18Z","timestamp":1793316498713,"version":"4.5.0"},"reference-count":110,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,3,15]],"date-time":"2022-03-15T00:00:00Z","timestamp":1647302400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Mol. Neurosci."],"abstract":"<jats:p>The bone morphogenetic proteins (BMPs) are a group of potent morphogens which are critical for the patterning, development, and function of the central nervous system. The appropriate function of the BMP pathway depends on its interaction with other signaling pathways involved in neural differentiation, leading to synergistic or antagonistic effects and ultimately favorable biological outcomes. These opposite or cooperative effects are observed when BMP interacts with fibroblast growth factor (FGF), cytokines, Notch, Sonic Hedgehog (Shh), and Wnt pathways to regulate the impact of BMP-induced signaling in neural differentiation. Herein, we review the cross-talk between BMP signaling and the prominent signaling pathways involved in neural differentiation, emphasizing the underlying basic molecular mechanisms regarding the process of neural differentiation. Knowing these cross-talks can help us to develop new approaches in regenerative medicine and stem cell based therapy. Recently, cell therapy has received significant attention as a promising treatment for traumatic or neurodegenerative diseases. Therefore, it is important to know the signaling pathways involved in stem cell differentiation toward neural cells. Our better insight into the cross-talk of signaling pathways during neural development would improve neural differentiation within <jats:italic>in vitro<\/jats:italic> tissue engineering approaches and pre-clinical practices and develop futuristic therapeutic strategies for patients with neurological disease.<\/jats:p>","DOI":"10.3389\/fnmol.2022.827275","type":"journal-article","created":{"date-parts":[[2022,3,15]],"date-time":"2022-03-15T07:53:45Z","timestamp":1647330825000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":60,"title":["The Cross-Talks Among Bone Morphogenetic Protein (BMP) Signaling and Other Prominent Pathways Involved in Neural Differentiation"],"prefix":"10.3389","volume":"15","author":[{"given":"Asma","family":"Manzari-Tavakoli","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amirhesam","family":"Babajani","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohammad Hadi","family":"Farjoo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mostafa","family":"Hajinasrollah","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Soheyl","family":"Bahrami","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hassan","family":"Niknejad","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,3,15]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"308","DOI":"10.1016\/j.ydbio.2004.02.015","article-title":"Converse control of oligodendrocyte and astrocyte lineage development by Sonic hedgehog in the chick spinal cord","volume":"270","author":"Agius","year":"2004","journal-title":"Dev. Biol."},{"key":"B2","doi-asserted-by":"publisher","first-page":"37170","DOI":"10.1074\/jbc.M705414200","article-title":"Bone morphogenetic protein 2 opposes Shh-mediated proliferation in cerebellar granule cells through a TIEG-1-based regulation of Nmyc","volume":"282","author":"\u00c1lvarez-Rodr\u00edguez","year":"2007","journal-title":"J. Biol. Chem."},{"key":"B3","doi-asserted-by":"publisher","first-page":"3593","DOI":"10.1242\/dev.063610","article-title":"Notch signaling: simplicity in design, versatility in function","volume":"138","author":"Andersson","year":"2011","journal-title":"Development"},{"key":"B5","doi-asserted-by":"publisher","first-page":"748","DOI":"10.3389\/fbioe.2020.00748","article-title":"Recent advances on drug-loaded mesenchymal stem cells with anti-neoplastic agents for targeted treatment of cancer","volume":"8","author":"Babajani","year":"2020","journal-title":"Front. Bioeng. Biotechnol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"3149","DOI":"10.1101\/gad.13.23.3149","article-title":"Wnt signaling in Xenopus embryos inhibits bmp4 expression and activates neural development","volume":"13","author":"Baker","year":"1999","journal-title":"Genes Dev."},{"key":"B7","doi-asserted-by":"publisher","first-page":"1707","DOI":"10.3906\/sag-2003-127","article-title":"BMP and TGFSS use and release in bone regeneration","volume":"50","author":"Bal","year":"2020","journal-title":"Turk. J. Med. Sci."},{"key":"B8","doi-asserted-by":"publisher","first-page":"857","DOI":"10.1016\/j.bcp.2013.01.004","article-title":"BMP signaling in development and diseases: a pharmacological perspective","volume":"85","author":"Bandyopadhyay","year":"2013","journal-title":"Biochem. Pharmacol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1111\/j.1749-6632.2009.03986.x","article-title":"Cytokine control of adult neural stem cells","volume":"1153","author":"Bauer","year":"2009","journal-title":"Ann. N Y Acad. Sci."},{"key":"B10","doi-asserted-by":"publisher","first-page":"66","DOI":"10.1002\/dneu.22209","article-title":"The double inhibition of endogenously produced BMP and W nt factors synergistically triggers dorsal telencephalic differentiation of mouse ES cells","volume":"75","author":"Bertacchi","year":"2015","journal-title":"Dev. Neurobiol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"615","DOI":"10.1016\/s0092-8674(03)00928-0","article-title":"Neural tissue in ascidian embryos is induced by FGF9\/16\/20, acting via a combination of maternal GATA and Ets transcription factors","volume":"115","author":"Bertrand","year":"2003","journal-title":"Cell"},{"key":"B12","doi-asserted-by":"publisher","first-page":"e2863","DOI":"10.1371\/journal.pone.0002863","article-title":"Induction of Olig2+ precursors by FGF involves BMP signalling blockade at the Smad level","volume":"3","author":"Bilican","year":"2008","journal-title":"PLoS One"},{"key":"B13","doi-asserted-by":"publisher","first-page":"751","DOI":"10.1007\/s00441-020-03280-z","article-title":"The differentiation effect of bone morphogenetic protein (BMP) on human amniotic epithelial stem cells to express ectodermal lineage markers","volume":"383","author":"Biniazan","year":"2021","journal-title":"Cell Tissue Res."},{"key":"B14","doi-asserted-by":"publisher","first-page":"126","DOI":"10.1006\/dbio.1995.0010","article-title":"Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo","volume":"172","author":"Bitgood","year":"1995","journal-title":"Dev. Biol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"723","DOI":"10.1083\/jcb.200305112","article-title":"Cross-talk between the Notch and TGF-\u03b2 signaling pathways mediated by interaction of the Notch intracellular domain with Smad3","volume":"163","author":"Blokzijl","year":"2003","journal-title":"J. Cell Biol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"1068","DOI":"10.1002\/dneu.22022","article-title":"The dynamic role of bone morphogenetic proteins in neural stem cell fate and maturation","volume":"72","author":"Bond","year":"2012","journal-title":"Dev. Neurobiol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"477","DOI":"10.1126\/science.278.5337.477","article-title":"Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway","volume":"278","author":"Bonni","year":"1997","journal-title":"Science"},{"key":"B18","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1016\/j.bbamcr.2015.11.020","article-title":"The Notch intracellular domain integrates signals from Wnt, Hedgehog, TGF\u03b2\/BMP and hypoxia pathways","volume":"1863","author":"Borggrefe","year":"2016","journal-title":"Biochim. Biophys. Acta"},{"key":"B19","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/j.tins.2014.12.006","article-title":"The role of inflammatory cytokines as key modulators of neurogenesis","volume":"38","author":"Borsini","year":"2015","journal-title":"Trends Neurosci."},{"key":"B4","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1210\/er.2003-0040","article-title":"Fibroblast growth factor signaling during early vertebrate development","volume":"26","author":"B\u00f6ttcher","year":"2005","journal-title":"Endocr. Rev."},{"key":"B20","doi-asserted-by":"publisher","first-page":"437","DOI":"10.4252\/wjsc.v7.i2.437","article-title":"Neural differentiation from embryonic stem cells in vitro: an overview of the signaling pathways","volume":"7","author":"Chuang","year":"2015","journal-title":"World J. Stem Cells"},{"key":"B22","doi-asserted-by":"publisher","first-page":"450","DOI":"10.1016\/j.ydbio.2010.01.030","article-title":"The role of FGF-signaling in early neural specification of human embryonic stem cells","volume":"340","author":"Cohen","year":"2010","journal-title":"Dev. Biol."},{"key":"B23","doi-asserted-by":"publisher","first-page":"299","DOI":"10.1242\/dev.01582","article-title":"Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition","volume":"132","author":"Delaune","year":"2005","journal-title":"Development"},{"key":"B24","doi-asserted-by":"publisher","first-page":"58","DOI":"10.3389\/fcell.2017.00058","article-title":"The multiple roles of FGF signaling in the developing spinal cord","volume":"5","author":"Diez del Corral","year":"2017","journal-title":"Front. Cell Dev. Biol."},{"key":"B25","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.bbi.2017.02.019","article-title":"Bone morphogenetic proteins in multiple sclerosis: role in neuroinflammation","volume":"68","author":"Eixarch","year":"2018","journal-title":"Brain Behav. Immun."},{"key":"B26","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1016\/j.cytogfr.2005.01.001","article-title":"Cellular signaling by fibroblast growth factor receptors","volume":"16","author":"Eswarakumar","year":"2005","journal-title":"Cytokine Growth Factor Rev."},{"key":"B27","doi-asserted-by":"publisher","first-page":"2435","DOI":"10.1016\/j.bbagen.2012.09.002","article-title":"Signaling mechanisms regulating adult neural stem cells and neurogenesis","volume":"1830","author":"Faigle","year":"2013","journal-title":"Biochim. Biophys. Acta"},{"key":"B28","doi-asserted-by":"publisher","first-page":"AN20110004","DOI":"10.1042\/AN20110004","article-title":"Canonical Wnt signalling requires the BMP pathway to inhibit oligodendrocyte maturation","volume":"3","author":"Feigenson","year":"2011","journal-title":"ASN Neuro"},{"key":"B29","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1002\/(SICI)1097-4695(19990905)40:3<271::AID-NEU1>3.0.CO;2-C","article-title":"BMP-4 inhibits neural differentiation of murine embryonic stem cells","volume":"40","author":"Finley","year":"1999","journal-title":"J. Neurobiol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"980","DOI":"10.1016\/j.cell.2007.09.027","article-title":"Integrating patterning signals: Wnt\/GSK3 regulates the duration of the BMP\/Smad1 signal","volume":"131","author":"Fuentealba","year":"2007","journal-title":"Cell"},{"key":"B31","doi-asserted-by":"publisher","first-page":"4931","DOI":"10.1128\/MCB.02435-06","article-title":"Potentiation of astrogliogenesis by STAT3-mediated activation of bone morphogenetic protein-Smad signaling in neural stem cells","volume":"27","author":"Fukuda","year":"2007","journal-title":"Mol. Cell. Biol."},{"key":"B32","doi-asserted-by":"publisher","first-page":"87","DOI":"10.3389\/fncel.2013.00087","article-title":"BMP signaling in telencephalic neural cell specification and maturation","volume":"7","author":"G\u00e1mez","year":"2013","journal-title":"Front. Cell. Neurosci."},{"key":"B33","doi-asserted-by":"publisher","first-page":"R60","DOI":"10.1093\/hmg\/ddn119","article-title":"Neur-ons and neur-offs: regulators of neural induction in vertebrate embryos and embryonic stem cells","volume":"17","author":"Gaulden","year":"2008","journal-title":"Hum. Mol. Genet."},{"key":"B34","doi-asserted-by":"publisher","first-page":"164","DOI":"10.1016\/s0012-1606(02)00037-4","article-title":"Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglial lineage commitment","volume":"255","author":"Gomes","year":"2003","journal-title":"Dev. Biol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"e11505","DOI":"10.15252\/emmm.201911505","article-title":"Therapeutic repair for spinal cord injury: combinatory approaches to address a multifaceted problem","volume":"12","author":"Griffin","year":"2020","journal-title":"EMBO Mol. Med."},{"key":"B36","doi-asserted-by":"publisher","first-page":"9862","DOI":"10.1523\/JNEUROSCI.23-30-09862.2003","article-title":"Sonic hedgehog and bone morphogenetic protein regulate interneuron development from dorsal telencephalic progenitors in vitro","volume":"23","author":"Gulacsi","year":"2003","journal-title":"J. Neurosci."},{"key":"B37","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1038\/cr.2008.302","article-title":"Signaling cross-talk between TGF-\u03b2\/BMP and other pathways","volume":"19","author":"Guo","year":"2009","journal-title":"Cell Res."},{"key":"B38","doi-asserted-by":"publisher","first-page":"696","DOI":"10.1016\/s1044-7431(03)00232-x","article-title":"Wnt signalling inhibits neural differentiation of embryonic stem cells by controlling bone morphogenetic protein expression","volume":"24","author":"Haegele","year":"2003","journal-title":"Mol. Cell. Neurosci."},{"key":"B39","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1186\/1471-213X-6-43","article-title":"Eye and neural defects associated with loss of GDF6","volume":"6","author":"Hanel","year":"2006","journal-title":"BMC Dev. Biol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"113455","DOI":"10.1016\/j.expneurol.2020.113455","article-title":"Bone morphogenetic proteins: new insights into their roles and mechanisms in CNS development, pathology and repair","volume":"334","author":"Hart","year":"2020","journal-title":"Exp. Neurol."},{"key":"B41","doi-asserted-by":"publisher","first-page":"616","DOI":"10.1038\/nn1440","article-title":"A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis","volume":"8","author":"He","year":"2005","journal-title":"Nat. Neurosci."},{"key":"B42","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1007\/s12264-013-1318-y","article-title":"Coordinated control of oligodendrocyte development by extrinsic and intrinsic signaling cues","volume":"29","author":"He","year":"2013","journal-title":"Neurosci. Bull."},{"key":"B43","doi-asserted-by":"publisher","first-page":"1213","DOI":"10.1097\/00006123-200005000-00038","article-title":"Bone morphogenetic proteins and bone morphogenetic protein gene therapy in neurological surgery: a review","volume":"46","author":"Helm","year":"2000","journal-title":"Neurosurgery"},{"key":"B44","doi-asserted-by":"publisher","first-page":"2791","DOI":"10.1242\/dev.01165","article-title":"The Wnt\/\u03b2-catenin pathway directs neuronal differentiation of cortical neural precursor cells","volume":"131","author":"Hirabayashi","year":"2004","journal-title":"Development"},{"key":"B45","doi-asserted-by":"publisher","first-page":"394","DOI":"10.1016\/j.ydbio.2006.12.045","article-title":"Wnt\/BMP signal integration regulates the balance between proliferation and differentiation of neuroepithelial cells in the dorsal spinal cord","volume":"304","author":"Ille","year":"2007","journal-title":"Dev. Biol."},{"key":"B46","doi-asserted-by":"publisher","first-page":"64","DOI":"10.1093\/jmcb\/mjt051","article-title":"Wnt signaling in the nervous system and in Alzheimer\u2019s disease","volume":"6","author":"Inestrosa","year":"2014","journal-title":"J. Mol. Cell Biol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"237","DOI":"10.1002\/jcp.10208","article-title":"HES and HERP families: multiple effectors of the Notch signaling pathway","volume":"194","author":"Iso","year":"2003","journal-title":"J. Cell. Physiol."},{"key":"B48","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1002\/dvdy.22009","article-title":"Crosstalk between Wnt and bone morphogenic protein signaling: a turbulent relationship","volume":"239","author":"Itasaki","year":"2010","journal-title":"Dev. Dyn."},{"key":"B49","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1038\/sj.emboj.7600065","article-title":"Synergy and antagonism between Notch and BMP receptor signaling pathways in endothelial cells","volume":"23","author":"Itoh","year":"2004","journal-title":"EMBO J."},{"key":"B50","doi-asserted-by":"publisher","first-page":"11772719211013352","DOI":"10.1177\/11772719211013352","article-title":"Multiple sclerosis biomarker discoveries by proteomics and metabolomics approaches","volume":"16","author":"Jafari","year":"2021","journal-title":"Biomark. Insights"},{"key":"B51","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1186\/gb-2004-5-6-226","article-title":"An overview of the basic helix-loop-helix proteins","volume":"5","author":"Jones","year":"2004","journal-title":"Genome Biol."},{"key":"B53","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1002\/3527608036.ch1","article-title":"Roles of Hes bHLH factors in neural development","volume-title":"Transcription Factors in the Nervous System: Development, Brain Function and Diseases","author":"Kageyama","year":"2006"},{"key":"B54","doi-asserted-by":"publisher","first-page":"777","DOI":"10.1111\/j.1365-2443.2005.00876.x","article-title":"Wnt signaling regulates the sequential onset of neurogenesis and gliogenesis via induction of BMPs","volume":"10","author":"Kasai","year":"2005","journal-title":"Genes Cells"},{"key":"B55","doi-asserted-by":"publisher","first-page":"1816","DOI":"10.1002\/stem.511","article-title":"Differential regulation of proliferation and differentiation in neural precursor cells by the Jak pathway","volume":"28","author":"Kim","year":"2010","journal-title":"Stem cells"},{"key":"B56","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1083\/jcb.200411095","article-title":"Neural crest stem cell maintenance by combinatorial Wnt and BMP signaling","volume":"169","author":"Kl\u00e9ber","year":"2005","journal-title":"J. Cell Biol."},{"key":"B57","doi-asserted-by":"publisher","first-page":"681","DOI":"10.1016\/j.ceb.2004.08.006","article-title":"Wnt signaling and the regulation of stem cell function","volume":"16","author":"Kl\u00e9ber","year":"2004","journal-title":"Curr. Opin. Cell Biol."},{"key":"B58","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1111\/j.1741-4520.2012.00368.x","article-title":"Sonic hedgehog signaling coordinates the proliferation and differentiation of neural stem\/progenitor cells by regulating cell cycle kinetics during development of the neocortex","volume":"52","author":"Komada","year":"2012","journal-title":"Congenit. Anom. (Kyoto)"},{"key":"B59","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1016\/j.devcel.2015.03.005","article-title":"Notch activity modulates the responsiveness of neural progenitors to sonic hedgehog signaling","volume":"33","author":"Kong","year":"2015","journal-title":"Dev. Cell"},{"key":"B60","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1006\/dbio.2002.0581","article-title":"Inhibition of BMP activity by the FGF signal promotes posterior neural development in zebrafish","volume":"244","author":"Koshida","year":"2002","journal-title":"Dev. Biol."},{"key":"B61","doi-asserted-by":"publisher","first-page":"1022","DOI":"10.1101\/gad.1306605","article-title":"Default neural induction: neuralization of dissociated Xenopus cells is mediated by Ras\/MAPK activation","volume":"19","author":"Kuroda","year":"2005","journal-title":"Genes Dev."},{"key":"B62","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1186\/2041-9139-5-30","article-title":"Non-canonical notch signaling represents an ancestral mechanism to regulate neural differentiation","volume":"5","author":"Layden","year":"2014","journal-title":"Evodevo"},{"key":"B63","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1038\/s41467-020-20112-4","article-title":"Transneuronal delivery of hyper-interleukin-6 enables functional recovery after severe spinal cord injury in mice","volume":"12","author":"Leibinger","year":"2021","journal-title":"Nat. Commun."},{"key":"B64","doi-asserted-by":"publisher","first-page":"180","DOI":"10.1002\/cbf.3582","article-title":"The role of Shh signalling pathway in central nervous system development and related diseases","volume":"39","author":"Li","year":"2021","journal-title":"Cell Biochem. Funct."},{"key":"B65","doi-asserted-by":"publisher","first-page":"4855","DOI":"10.1242\/dev.127.22.4855","article-title":"Regulation of the neural patterning activity of sonic hedgehog by secreted BMP inhibitors expressed by notochord and somites","volume":"127","author":"Liem","year":"2000","journal-title":"Development"},{"key":"B52","doi-asserted-by":"publisher","first-page":"969","DOI":"10.1016\/0092-8674(95)90276-7","article-title":"Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm","volume":"82","author":"Liem","year":"1995","journal-title":"Cell"},{"key":"B66","doi-asserted-by":"publisher","first-page":"5671","DOI":"10.1242\/dev.01445","article-title":"Neural induction requires BMP inhibition only as a late step and involves signals other than FGF and Wnt antagonists","volume":"131","author":"Linker","year":"2004","journal-title":"Development"},{"key":"B67","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1038\/3793","article-title":"Carboxy-terminally truncated Gli3 proteins associate with Smads","volume":"20","author":"Liu","year":"1998","journal-title":"Nat. Genet."},{"key":"B68","doi-asserted-by":"publisher","first-page":"22012","DOI":"10.1038\/s41598-020-78650-2","article-title":"Fabrication of nanochitosan incorporated polypyrrole\/alginate conducting scaffold for neural tissue engineering","volume":"10","author":"Manzari-Tavakoli","year":"2020","journal-title":"Sci. Rep."},{"key":"B69","doi-asserted-by":"publisher","first-page":"17437","DOI":"10.1073\/pnas.0906352106","article-title":"BMP inhibition initiates neural induction via FGF signaling and Zic genes","volume":"106","author":"Marchal","year":"2009","journal-title":"Proc. Natl. Acad. Sci. U S A"},{"key":"B70","doi-asserted-by":"publisher","first-page":"30814","DOI":"10.1074\/jbc.M110.142869","article-title":"ZFP423 coordinates Notch and bone morphogenetic protein signaling, selectively up-regulating Hes5 gene expression","volume":"285","author":"Masserdotti","year":"2010","journal-title":"J. Biol. Chem."},{"key":"B71","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1016\/s0166-2236(96)01046-6","article-title":"Bone morphogenetic proteins in the nervous system","volume":"20","author":"Mehler","year":"1997","journal-title":"Trends Neurosci."},{"key":"B72","doi-asserted-by":"publisher","first-page":"a022244","DOI":"10.1101\/cshperspect.a022244","article-title":"TGF-\u03b2 family signaling in neural and neuronal differentiation, development and function","volume":"9","author":"Meyers","year":"2017","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"B74","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1093\/jb\/mvp148","article-title":"Bone morphogenetic protein receptors and signal transduction","volume":"147","author":"Miyazono","year":"2010","journal-title":"J. Biochem."},{"key":"B75","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1016\/j.cytogfr.2005.01.009","article-title":"BMP receptor signaling: transcriptional targets, regulation of signals and signaling cross-talk","volume":"16","author":"Miyazono","year":"2005","journal-title":"Cytokine Growth Factor Rev."},{"key":"B76","doi-asserted-by":"publisher","first-page":"663","DOI":"10.1038\/nrg2417","article-title":"EvoD\/Vo: the origins of BMP signalling in the neuroectoderm","volume":"9","author":"Mizutani","year":"2008","journal-title":"Nat. Rev. Genet."},{"key":"B77","doi-asserted-by":"publisher","first-page":"5868","DOI":"10.1073\/pnas.101109698","article-title":"BMP2-mediated alteration in the developmental pathway of fetal mouse brain cells from neurogenesis to astrocytogenesis","volume":"98","author":"Nakashima","year":"2001","journal-title":"Proc. Natl. Acad. Sci. U S A"},{"key":"B78","doi-asserted-by":"publisher","first-page":"479","DOI":"10.1126\/science.284.5413.479","article-title":"Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300","volume":"284","author":"Nakashima","year":"","journal-title":"Science"},{"key":"B79","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1016\/s0014-5793(99)00997-7","article-title":"Astrocyte differentiation mediated by LIF in cooperation with BMP2","volume":"457","author":"Nakashima","year":"","journal-title":"FEBS Lett."},{"key":"B80","doi-asserted-by":"publisher","first-page":"e22925","DOI":"10.4161\/jkst.22925","article-title":"The role of JAK-STAT signaling within the CNS","volume":"2","author":"Nicolas","year":"2013","journal-title":"JAKSTAT"},{"key":"B81","doi-asserted-by":"publisher","first-page":"2083","DOI":"10.1242\/jcs.145755","article-title":"Notch signaling regulates neural crest differentiation from human pluripotent stem cells","volume":"127","author":"Noisa","year":"2014","journal-title":"J. Cell Sci."},{"key":"B82","doi-asserted-by":"publisher","first-page":"264","DOI":"10.1006\/cyto.2001.0883","article-title":"Astrocyte differentiation of fetal neuroepithelial cells involving cardiotrophin-1-induced activation of STAT3","volume":"14","author":"Ochiai","year":"2001","journal-title":"Cytokine"},{"key":"B83","doi-asserted-by":"publisher","first-page":"1097","DOI":"10.3727\/096368914X679237","article-title":"Mesenchymal stem cells increase hippocampal neurogenesis and neuronal differentiation by enhancing the Wnt signaling pathway in an Alzheimer\u2019s disease model","volume":"24","author":"Oh","year":"2015","journal-title":"Cell Transplant."},{"key":"B84","doi-asserted-by":"publisher","first-page":"76","DOI":"10.1002\/cyto.a.22161","article-title":"Functions of neurotrophins and growth factors in neurogenesis and brain repair","volume":"83","author":"Oliveira","year":"2013","journal-title":"Cytometry A"},{"key":"B85","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1002\/wdev.176","article-title":"The fibroblast growth factor signaling pathway","volume":"4","author":"Ornitz","year":"2015","journal-title":"Wiley Interdiscip. Rev. Dev. Biol."},{"key":"B86","doi-asserted-by":"publisher","first-page":"3545","DOI":"10.1242\/dev.01218","article-title":"\u03b2-Catenin signaling is required for neural differentiation of embryonic stem cells","volume":"131","author":"Otero","year":"2004","journal-title":"Development"},{"key":"B87","doi-asserted-by":"publisher","first-page":"3023","DOI":"10.1101\/gad.1153603","article-title":"Integration of IGF, FGF and anti-BMP signals via Smad1 phosphorylation in neural induction","volume":"17","author":"Pera","year":"2003","journal-title":"Genes Dev."},{"key":"B88","doi-asserted-by":"publisher","first-page":"15005","DOI":"10.1038\/boneres.2015.5","article-title":"TGF-\u03b2\/BMP signaling and other molecular events: regulation of osteoblastogenesis and bone formation","volume":"3","author":"Rahman","year":"2015","journal-title":"Bone Res."},{"key":"B89","doi-asserted-by":"publisher","first-page":"3381","DOI":"10.1242\/dev.01901","article-title":"Depletion of Bmp2, Bmp4, Bmp7 and Spemann organizer signals induces massive brain formation in Xenopus embryos","volume":"132","author":"Reversade","year":"2005","journal-title":"Development"},{"key":"B90","doi-asserted-by":"publisher","first-page":"3159","DOI":"10.1242\/dev.01188","article-title":"Bmp2 antagonizes sonic hedgehog-mediated proliferation of cerebellar granule neurones through Smad5 signalling","volume":"131","author":"Rios","year":"2004","journal-title":"Development"},{"key":"B91","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1038\/nrendo.2016.12","article-title":"BMP signalling in skeletal development, disease and repair","volume":"12","author":"Salazar","year":"2016","journal-title":"Nat. Rev. Endocrinol."},{"key":"B92","doi-asserted-by":"publisher","first-page":"441","DOI":"10.1016\/j.molcel.2007.01.006","article-title":"Balancing BMP signaling through integrated inputs into the Smad1 linker","volume":"25","author":"Sapkota","year":"2007","journal-title":"Mol. Cell"},{"key":"B93","doi-asserted-by":"publisher","first-page":"1265","DOI":"10.1523\/JNEUROSCI.21-04-01265.2001","article-title":"The basic helix-loop-helix gene hesr2 promotes gliogenesis in mouse retina","volume":"21","author":"Satow","year":"2001","journal-title":"J. Neurosci."},{"key":"B94","doi-asserted-by":"publisher","first-page":"136","DOI":"10.1016\/j.bbcan.2013.12.005","article-title":"Targeting the STAT3 signaling pathway in cancer: role of synthetic and natural inhibitors","volume":"1845","author":"Siveen","year":"2014","journal-title":"Biochim. Biophys. Acta"},{"key":"B95","doi-asserted-by":"publisher","first-page":"2889","DOI":"10.1242\/dev.02858","article-title":"A discrete period of FGF-induced Erk1\/2 signalling is required for vertebrate neural specification","volume":"134","author":"Stavridis","year":"2007","journal-title":"Development"},{"key":"B96","doi-asserted-by":"publisher","first-page":"5723","DOI":"10.1093\/nar\/gkg778","article-title":"Enhanced gene activation by Notch and BMP signaling cross-talk","volume":"31","author":"Takizawa","year":"2003","journal-title":"Nucleic Acids Res."},{"key":"B97","doi-asserted-by":"publisher","first-page":"2640","DOI":"10.4161\/cc.6.21.4822","article-title":"Morphogens and the control of cell proliferation and patterning in the spinal cord","volume":"6","author":"Ulloa","year":"2007","journal-title":"Cell Cycle"},{"key":"B98","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1002\/dvdy.22058","article-title":"Wnt won the war: antagonistic role of Wnt over Shh controls dorso-ventral patterning of the vertebrate neural tube","volume":"239","author":"Ulloa","year":"2010","journal-title":"Dev. Dyn."},{"key":"B99","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1016\/j.gendis.2014.07.005","article-title":"Bone morphogenetic protein (BMP) signaling in development and human diseases","volume":"1","author":"Wang","year":"2014","journal-title":"Genes Dis."},{"key":"B100","doi-asserted-by":"publisher","first-page":"141","DOI":"10.3892\/br.2014.401","article-title":"The role of the JAK-STAT pathway in neural stem cells, neural progenitor cells and reactive astrocytes after spinal cord injury","volume":"3","author":"Wang","year":"2015","journal-title":"Biomed. Rep."},{"key":"B101","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1016\/B978-0-12-405943-6.00008-7","article-title":"Hey bHLH transcription factors","volume":"110","author":"Weber","year":"2014","journal-title":"Curr. Top. Dev. Biol."},{"key":"B102","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1006\/dbio.2001.0258","article-title":"Neural induction in the absence of mesoderm: \u03b2-catenin-dependent expression of secreted BMP antagonists at the blastula stage in Xenopus","volume":"234","author":"Wessely","year":"2001","journal-title":"Dev. Biol."},{"key":"B103","doi-asserted-by":"publisher","first-page":"871","DOI":"10.1016\/j.cell.2012.02.066","article-title":"BMP8B increases brown adipose tissue thermogenesis through both central and peripheral actions","volume":"149","author":"Whittle","year":"2012","journal-title":"Cell"},{"key":"B104","doi-asserted-by":"publisher","first-page":"421","DOI":"10.1016\/s0960-9822(00)00431-0","article-title":"An early requirement for FGF signalling in the acquisition of neural cell fate in the chick embryo","volume":"10","author":"Wilson","year":"2000","journal-title":"Curr. Biol."},{"key":"B105","doi-asserted-by":"publisher","first-page":"6651","DOI":"10.1523\/JNEUROSCI.4876-11.2012","article-title":"Differential modulation of the oligodendrocyte transcriptome by sonic hedgehog and bone morphogenetic protein 4 via opposing effects on histone acetylation","volume":"32","author":"Wu","year":"2012","journal-title":"J. Neurosci."},{"key":"B106","doi-asserted-by":"publisher","first-page":"965","DOI":"10.1016\/j.conb.2013.09.002","article-title":"Signaling mechanisms of non-conventional axon guidance cues: the Shh, BMP and Wnt morphogens","volume":"23","author":"Yam","year":"2013","journal-title":"Curr. Opin. Neurobiol."},{"key":"B107","doi-asserted-by":"publisher","first-page":"543","DOI":"10.1007\/s10735-012-9431-1","article-title":"The cell-specific upregulation of bone morphogenetic protein-10 (BMP-10) in a model of rat cortical brain injury","volume":"43","author":"Yan","year":"2012","journal-title":"J. Mol. Histol."},{"key":"B108","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1016\/s0014-5793(01)02095-6","article-title":"Signaling crosstalk underlying synergistic induction of astrocyte differentiation by BMPs and IL-6 family of cytokines","volume":"489","author":"Yanagisawa","year":"2001","journal-title":"FEBS Lett."},{"key":"B109","doi-asserted-by":"publisher","first-page":"406","DOI":"10.1016\/s0012-1606(03)00123-4","article-title":"\u03b2-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system","volume":"258","author":"Zechner","year":"2003","journal-title":"Dev. Biol."},{"key":"B110","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1016\/j.ydbio.2006.10.045","article-title":"Bmp and Wnt\/\u03b2-catenin signals control expression of the transcription factor Olig3 and the specification of spinal cord neurons","volume":"303","author":"Zechner","year":"2007","journal-title":"Dev. Biol."},{"key":"B111","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/j.biomaterials.2014.11.007","article-title":"Canonical Wnt signaling acts synergistically on BMP9-induced osteo\/odontoblastic differentiation of stem cells of dental apical papilla (SCAPs)","volume":"39","author":"Zhang","year":"2015","journal-title":"Biomaterials"},{"key":"B112","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1016\/j.fct.2014.05.031","article-title":"Salidroside induces neuronal differentiation of mouse mesenchymal stem cells through Notch and BMP signaling pathways","volume":"71","author":"Zhao","year":"2014","journal-title":"Food Chem. Toxicol."}],"container-title":["Frontiers in Molecular Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnmol.2022.827275\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,3,15]],"date-time":"2022-03-15T07:53:51Z","timestamp":1647330831000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnmol.2022.827275\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,3,15]]},"references-count":110,"alternative-id":["10.3389\/fnmol.2022.827275"],"URL":"https:\/\/doi.org\/10.3389\/fnmol.2022.827275","relation":{},"ISSN":["1662-5099"],"issn-type":[{"value":"1662-5099","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,3,15]]},"article-number":"827275"}}