MicroRNA-Mediated Regulation of BMP Signaling in the Developing Neural Tube

Page: [63 - 81] Pages: 19

  • * (Excluding Mailing and Handling)

Abstract

Background: Neural tube (NT) morphogenesis is reliant on the proper temporospatial expression of numerous genes and synchronized crosstalk between diverse signaling cascades and gene regulatory networks governing key cellular processes. MicroRNAs (miRNAs), a group of small non-coding regulatory RNAs, execute defining roles in directing key canonical pathways during embryogenesis.

Objective: In order to comprehend the mechanistic underpinnings of miRNA regulation of NT morphogenesis, we have identified in the current study various miRNAs and their target mRNAs associated with BMP signaling during critical stages of neurulation.

Methods: We previously demonstrated the expression of several miRNAs during the critical stages of neurulation (gestational days (GD) 8.5, 9.0, and 9.5) employing high-sensitivity, high-coverage microarrays. In the present study, bioinformatic analyses were used to identify miRNAs differentially expressed (DE) in the embryonic NT that target messenger RNAs (mRNAs) associated with the bone morphogenetic protein (BMP) signaling pathway. RNAs extracted from the developing NT were hybridized to both miRNA and mRNA arrays to evaluate miRNA-mRNA interactions.

Results: Bioinformatic analysis identified several DE miRNAs that targeted mRNAs encoding members of (and proteins associated with) the BMP signaling pathway – a signaling cascade central to normal NT development.

Conclusion: Identification of the miRNAs and their mRNA targets associated with BMP signaling facilitates a better understanding of the crucial epigenetic mechanisms underlying normal NT development as well as the pathogenesis of NT defects. The current study supports the notion that miRNAs function as key regulators of neural tube morphogenesis via modulation of the BMP signaling cascade. Altered expression of these miRNAs during neurulation may therefore result in NT defects.

Keywords: BMP signaling, Embryonic development, miRNA, Neural tube

Graphical Abstract

[1]
Wilde JJ, Petersen JR, Niswander L. Genetic, epigenetic, and environmental contributions to neural tube closure. Annu Rev Genet 2014; 48(1): 583-611.
[http://dx.doi.org/10.1146/annurev-genet-120213-092208] [PMID: 25292356]
[2]
Nikolopoulou E, Galea GL, Rolo A, Greene NDE, Copp AJ. Neural tube closure: Cellular, molecular and biomechanical mechanisms. Development 2017; 144(4): 552-66.
[http://dx.doi.org/10.1242/dev.145904] [PMID: 28196803]
[3]
Massarwa R, Ray HJ, Niswander L. Morphogenetic movements in the neural plate and neural tube: Mouse. Wiley Interdiscip Rev Dev Biol 2014; 3(1): 59-68.
[http://dx.doi.org/10.1002/wdev.120] [PMID: 24902834]
[4]
Greene NDE, Copp AJ. Neural tube defects. Annu Rev Neurosci 2014; 37(1): 221-42.
[http://dx.doi.org/10.1146/annurev-neuro-062012-170354] [PMID: 25032496]
[5]
Blencowe H, Kancherla V, Moorthie S, Darlison MW, Modell B. Estimates of global and regional prevalence of neural tube defects for 2015: A systematic analysis. Ann N Y Acad Sci 2018; 1414(1): 31-46.
[http://dx.doi.org/10.1111/nyas.13548] [PMID: 29363759]
[6]
Au KS, Findley TO, Northrup H. Finding the genetic mechanisms of folate deficiency and neural tube defects-Leaving no stone unturned. Am J Med Genet A 2017; 173(11): 3042-57.
[http://dx.doi.org/10.1002/ajmg.a.38478] [PMID: 28944587]
[7]
Yang SL, Yang M, Herrlinger S, Liang C, Lai F, Chen JF. MiR-302/367 regulate neural progenitor proliferation, differentiation timing, and survival in neurulation. Dev Biol 2015; 408(1): 140-50.
[http://dx.doi.org/10.1016/j.ydbio.2015.09.020] [PMID: 26441343]
[8]
Wang F, Xu C, Reece EA, et al. Protein kinase C-alpha suppresses autophagy and induces neural tube defects via miR-129-2 in diabetic pregnancy. Nat Commun 2017; 8(1): 15182.
[http://dx.doi.org/10.1038/ncomms15182] [PMID: 28474670]
[9]
Wolujewicz P, Ross ME. The search for genetic determinants of human neural tube defects. Curr Opin Pediatr 2019; 31(6): 739-46.
[http://dx.doi.org/10.1097/MOP.0000000000000817] [PMID: 31693581]
[10]
Nikolopoulou E, Hirst CS, Galea G, et al. Spinal neural tube closure depends on regulation of surface ectoderm identity and biomechanics by Grhl2. Nat Commun 2019; 10(1): 2487.
[http://dx.doi.org/10.1038/s41467-019-10164-6] [PMID: 31171776]
[11]
Seelan RS, Mukhopadhyay P, Philipose J, Greene RM, Pisano MM. Gestational folate deficiency alters embryonic gene expression and cell function. Differentiation 2021; 117: 1-15.
[http://dx.doi.org/10.1016/j.diff.2020.11.001] [PMID: 33302058]
[12]
Zhang Z, Chang H, Li Y, et al. MicroRNAs: Potential regulators involved in human anencephaly. Int J Biochem Cell Biol 2010; 42(2): 367-74.
[http://dx.doi.org/10.1016/j.biocel.2009.11.023] [PMID: 19962448]
[13]
Mukhopadhyay P, Brock G, Appana S, Webb C, Greene RM, Pisano MM. MicroRNA gene expression signatures in the developing neural tube. Birth Defects Res A Clin Mol Teratol 2011; 91(8): 744-62.
[http://dx.doi.org/10.1002/bdra.20819] [PMID: 21770019]
[14]
Krupp DR, Xu PT, Thomas S, et al. Transcriptome profiling of genes involved in neural tube closure during human embryonic development using long serial analysis of gene expression (long-SAGE). Birth Defects Res A Clin Mol Teratol 2012; 94(9): 683-92.
[http://dx.doi.org/10.1002/bdra.23040] [PMID: 22806986]
[15]
Hollins SL, Goldie BJ, Carroll AP, et al. Ontogeny of small RNA in the regulation of mammalian brain development. BMC Genomics 2014; 15(1): 777.
[http://dx.doi.org/10.1186/1471-2164-15-777] [PMID: 25204312]
[16]
Ramya S, Shyamasundar S, Bay BH, Dheen ST. Maternal diabetes alters expression of microRNAs that regulate genes critical for neural tube development. Front Mol Neurosci 2017; 10: 237.
[http://dx.doi.org/10.3389/fnmol.2017.00237] [PMID: 28798665]
[17]
Ward NJ, Green D, Higgins J, et al. microRNAs associated with early neural crest development in Xenopus laevis. BMC Genomics 2018; 19(1): 59.
[http://dx.doi.org/10.1186/s12864-018-4436-0] [PMID: 29347911]
[18]
Keuls RA, Kojima K, Lozzi B, et al. MiR-302 regulates glycolysis to control cell-cycle during neural tube closure. Int J Mol Sci 2020; 21(20): 7534.
[http://dx.doi.org/10.3390/ijms21207534] [PMID: 33066028]
[19]
Mukhopadhyay P, Greene RM, Pisano MM. MicroRNA targeting of the non‐canonical planar cell polarity pathway in the developing neural tube. Cell Biochem Funct 2020; 38(7): 905-20.
[http://dx.doi.org/10.1002/cbf.3512] [PMID: 32129905]
[20]
Xu C, Shen WB, Reece EA, et al. Maternal diabetes induces senescence and neural tube defects sensitive to the senomorphic rapamycin. Sci Adv 2021; 7(27): eabf5089.
[http://dx.doi.org/10.1126/sciadv.abf5089] [PMID: 34193422]
[21]
Theiler K. The house mouse. In: atlas of embryonic development. Springer Verlag New York, Inc. 1989.
[http://dx.doi.org/10.1007/978-3-642-88418-4]
[22]
Karagkouni D, Paraskevopoulou MD, Chatzopoulos S, et al. DIANA-TarBase v8: A decade-long collection of experimentally supported miRNA-Gene interactions. Nucleic Acids Res 2018; 46(D1): D239-45.
[http://dx.doi.org/10.1093/nar/gkx1141] [PMID: 29156006]
[23]
Mukhopadhyay P, Greene RM, Pisano MM. Integrated expression profiling of microRNAs and messenger RNAs in the developing murine neural tube.Gene Expression Omnibus 2019. Available from: [https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE140777
[24]
Wang Y, Stricker HM, Gou D, Liu L. microRNA: Past and present. Front Biosci 2007; 12(1): 2316-29.
[http://dx.doi.org/10.2741/2234] [PMID: 17127242]
[25]
Maller Schulman BR, Liang X, Stahlhut C, DelConte C, Stefani G, Slack FJ. The let-7 microRNA target gene, Mlin41/Trim71 is required for mouse embryonic survival and neural tube closure. Cell Cycle 2008; 7(24): 3935-42.
[http://dx.doi.org/10.4161/cc.7.24.7397] [PMID: 19098426]
[26]
Zhai K, Liu B, Teng J. MicroRNA-212-3p regulates early neurogenesis through the AKT/mTOR pathway by targeting MeCP2. Neurochem Int 2020; 137: 104734.
[http://dx.doi.org/10.1016/j.neuint.2020.104734] [PMID: 32246981]
[27]
Richman JM, Tickle C. Epithelia are interchangeable between facial primordia of chick embryos and morphogenesis is controlled by the mesenchyme. Dev Biol 1989; 136(1): 201-10.
[http://dx.doi.org/10.1016/0012-1606(89)90142-5] [PMID: 2806720]
[28]
Leduc RYM, Singh P, McDermid HE. Genetic backgrounds and modifier genes of NTD mouse models: An opportunity for greater understanding of the multifactorial etiology of neural tube defects. Birth Defects Res 2017; 109(2): 140-52.
[http://dx.doi.org/10.1002/bdra.23554] [PMID: 27768235]
[29]
Mayanil CS. Transcriptional and epigenetic regulation of neural crest induction during neurulation. Dev Neurosci 2013; 35(5): 361-72.
[http://dx.doi.org/10.1159/000354749] [PMID: 24051984]
[30]
Moreno-Moya JM, Vilella F, Simón C. MicroRNA: Key gene expression regulators. Fertil Steril 2014; 101(6): 1516-23.
[http://dx.doi.org/10.1016/j.fertnstert.2013.10.042] [PMID: 24314918]
[31]
Giraldez AJ, Cinalli RM, Glasner ME, et al. MicroRNAs regulate brain morphogenesis in zebrafish. Science 2005; 308(5723): 833-8.
[http://dx.doi.org/10.1126/science.1109020] [PMID: 15774722]
[32]
Takada S, Berezikov E, Yamashita Y, et al. Mouse microRNA profiles determined with a new and sensitive cloning method. Nucleic Acids Res 2006; 34(17): e115.
[http://dx.doi.org/10.1093/nar/gkl653] [PMID: 16973894]
[33]
Darnell DK, Kaur S, Stanislaw S, Konieczka JK, Yatskievych TA, Antin PB. MicroRNA expression during chick embryo development. Dev Dyn 2006; 235(11): 3156-65.
[http://dx.doi.org/10.1002/dvdy.20956] [PMID: 17013880]
[34]
Xu H, Wang X, Du Z, Li N. Identification of microRNAs from different tissues of chicken embryo and adult chicken. FEBS Lett 2006; 580(15): 3610-6.
[http://dx.doi.org/10.1016/j.febslet.2006.05.044] [PMID: 16750530]
[35]
Hoesel B, Bhujabal Z, Przemeck GKH, et al. Combination of in silico and in situ hybridisation approaches to identify potential Dll1 associated miRNAs during mouse embryogenesis. Gene Expr Patterns 2010; 10(6): 265-73.
[http://dx.doi.org/10.1016/j.gep.2010.06.002] [PMID: 20558326]
[36]
Song PP, Hu Y, Liu CM, et al. Embryonic ectoderm development protein is regulated by microRNAs in human neural tube defects. Am J Obstet Gynecol 2011; 204(6): 544.e9-544.e17.
[http://dx.doi.org/10.1016/j.ajog.2011.01.045] [PMID: 21497788]
[37]
Wang R, Hu Y, Song G, et al. MiR-206 regulates neural cells proliferation and apoptosis via Otx2. Cell Physiol Biochem 2012; 29(3-4): 381-90.
[http://dx.doi.org/10.1159/000338493] [PMID: 22508046]
[38]
Gu H, Li H, Zhang L, et al. Diagnostic role of microRNA expression profile in the serum of pregnant women with fetuses with neural tube defects. J Neurochem 2012; 122(3): 641-9.
[http://dx.doi.org/10.1111/j.1471-4159.2012.07812.x] [PMID: 22642222]
[39]
Xi J, Wu Y, Li G, et al. Mir-29b mediates the neural tube versus neural crest fate decision during embryonic stem cell neural differentiation. Stem Cell Reports 2017; 9(2): 571-86.
[http://dx.doi.org/10.1016/j.stemcr.2017.06.017] [PMID: 28757169]
[40]
Zhang J, Yang L, Yu J, Yang Q, Mu J, Xie J. Alteration of the microRNA expression profile and identification of miRNA/mRNA negative regulation pairs in neural tube defects. Acta Biochim Biophys Sin (Shanghai) 2019; 51(7): 761-5.
[http://dx.doi.org/10.1093/abbs/gmz050] [PMID: 31169880]
[41]
Heusinkveld HJ, Staal YCM, Baker NC, Daston G, Knudsen TB, Piersma A. An ontology for developmental processes and toxicities of neural tube closure. Reprod Toxicol 2021; 99: 160-7.
[http://dx.doi.org/10.1016/j.reprotox.2020.09.002] [PMID: 32926990]
[42]
Roth DM, Bayona F, Baddam P, Graf D. Craniofacial development: Neural crest in molecular embryology. Head Neck Pathol 2021; 15(1): 1-15.
[http://dx.doi.org/10.1007/s12105-021-01301-z] [PMID: 33723764]
[43]
Su YH, Chen YC, Ting HC, et al. BMP controls dorsoventral and neural patterning in indirect-developing hemichordates providing insight into a possible origin of chordates. Proc Natl Acad Sci USA 2019; 116(26): 12925-32.
[http://dx.doi.org/10.1073/pnas.1901919116] [PMID: 31189599]
[44]
Li X, Cao X. BMP signaling and skeletogenesis. Ann N Y Acad Sci 2006; 1068(1): 26-40.
[http://dx.doi.org/10.1196/annals.1346.006] [PMID: 16831903]
[45]
Ybot-Gonzalez P, Gaston-Massuet C, Girdler G, et al. Neural plate morphogenesis during mouse neurulation is regulated by antagonism of Bmp signalling. Development 2007; 134(17): 3203-11.
[http://dx.doi.org/10.1242/dev.008177] [PMID: 17693602]
[46]
Rogers CD, Moody SA, Casey ES. Neural induction and factors that stabilize a neural fate. Birth Defects Res C Embryo Today 2009; 87(3): 249-62.
[http://dx.doi.org/10.1002/bdrc.20157] [PMID: 19750523]
[47]
Stottmann RW, Klingensmith J. Bone morphogenetic protein signaling is required in the dorsal neural folds before neurulation for the induction of spinal neural crest cells and dorsal neurons. Dev Dyn 2011; 240(4): 755-65.
[http://dx.doi.org/10.1002/dvdy.22579] [PMID: 21394823]
[48]
Correia AC, Costa M, Moraes F, Bom J, Nóvoa A, Mallo M. Bmp2 is required for migration but not for induction of neural crest cells in the mouse. Dev Dyn 2007; 236(9): 2493-501.
[http://dx.doi.org/10.1002/dvdy.21256] [PMID: 17676634]
[49]
Ko SO, Chung IH, Xu X, et al. Smad4 is required to regulate the fate of cranial neural crest cells. Dev Biol 2007; 312(1): 435-47.
[http://dx.doi.org/10.1016/j.ydbio.2007.09.050] [PMID: 17964566]
[50]
McMahon JA, Takada S, Zimmerman LB, Fan CM, Harland RM, McMahon AP. Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev 1998; 12(10): 1438-52.
[http://dx.doi.org/10.1101/gad.12.10.1438] [PMID: 9585504]
[51]
Chang H, Huylebroeck D, Verschueren K, Guo Q, Matzuk MM, Zwijsen A. Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development 1999; 126(8): 1631-42.
[http://dx.doi.org/10.1242/dev.126.8.1631] [PMID: 10079226]
[52]
Solloway MJ, Robertson EJ. Early embryonic lethality in Bmp5;Bmp7 double mutant mice suggests functional redundancy within the 60A subgroup. Development 1999; 126(8): 1753-68.
[http://dx.doi.org/10.1242/dev.126.8.1753] [PMID: 10079236]
[53]
Stottmann RW, Berrong M, Matta K, Choi M, Klingensmith J. The BMP antagonist Noggin promotes cranial and spinal neurulation by distinct mechanisms. Dev Biol 2006; 295(2): 647-63.
[http://dx.doi.org/10.1016/j.ydbio.2006.03.051] [PMID: 16712836]
[54]
Castranio T, Mishina Y. Bmp2 is required for cephalic neural tube closure in the mouse. Dev Dyn 2009; 238(1): 110-22.
[http://dx.doi.org/10.1002/dvdy.21829] [PMID: 19097048]
[55]
Liu JAJ, Wu MH, Yan CH, et al. Phosphorylation of Sox9 is required for neural crest delamination and is regulated downstream of BMP and canonical Wnt signaling. Proc Natl Acad Sci USA 2013; 110(8): 2882-7.
[http://dx.doi.org/10.1073/pnas.1211747110] [PMID: 23382206]
[56]
Amarnath S, Agarwala S. Cell cycle dependent TGFβ-BMP antagonism regulates neural tube closure by modulating tight junctions. J Cell Sci 2016; 130(1): jcs.179192.
[http://dx.doi.org/10.1242/jcs.179192] [PMID: 27034139]
[57]
Davidson LA, Keller RE. Neural tube closure in Xenopus laevis involves medial migration, directed protrusive activity, cell intercalation and convergent extension. Development 1999; 126(20): 4547-56.
[http://dx.doi.org/10.1242/dev.126.20.4547] [PMID: 10498689]
[58]
Colas JF, Schoenwolf GC. Towards a cellular and molecular understanding of neurulation. Dev Dyn 2001; 221(2): 117-45.
[http://dx.doi.org/10.1002/dvdy.1144] [PMID: 11376482]
[59]
Eom DS, Amarnath S, Fogel JL, Agarwala S. Bone morphogenetic proteins regulate hinge point formation during neural tube closure by dynamic modulation of apicobasal polarity. Birth Defects Res A Clin Mol Teratol 2012; 94(10): 804-16.
[http://dx.doi.org/10.1002/bdra.23052] [PMID: 22865775]
[60]
Eom DS, Amarnath S, Fogel JL, Agarwala S. Bone morphogenetic proteins regulate neural tube closure by interacting with the apicobasal polarity pathway. Development 2011; 138(15): 3179-88.
[http://dx.doi.org/10.1242/dev.058602] [PMID: 21750029]
[61]
Le Dréau G, Garcia-Campmany L, Rabadán MA, et al. Canonical BMP7 activity is required for the generation of discrete neuronal populations in the dorsal spinal cord. Development 2012; 139(2): 259-68.
[http://dx.doi.org/10.1242/dev.074948] [PMID: 22159578]
[62]
Tozer S, Le Dréau G, Marti E, Briscoe J. Temporal control of BMP signalling determines neuronal subtype identity in the dorsal neural tube. Development 2013; 140(7): 1467-74.
[http://dx.doi.org/10.1242/dev.090118] [PMID: 23462473]
[63]
Yanagita M. BMP antagonists: Their roles in development and involvement in pathophysiology. Cytokine Growth Factor Rev 2005; 16(3): 309-17.
[http://dx.doi.org/10.1016/j.cytogfr.2005.02.007] [PMID: 15951218]
[64]
Bier E, De Robertis EM. BMP gradients: A paradigm for morphogen-mediated developmental patterning. Science 2015; 348(6242): aaa5838.
[http://dx.doi.org/10.1126/science.aaa5838] [PMID: 26113727]
[65]
Smith WC, Harland RM. Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 1992; 70(5): 829-40.
[http://dx.doi.org/10.1016/0092-8674(92)90316-5] [PMID: 1339313]
[66]
Bauer H, Meier A, Hild M, et al. Follistatin and noggin are excluded from the zebrafish organizer. Dev Biol 1998; 204(2): 488-507.
[http://dx.doi.org/10.1006/dbio.1998.9003] [PMID: 9882485]
[67]
Itoh N, Ohta H. Secreted bone morphogenetic protein antagonists of the Chordin family. Biomol Concepts 2010; 1(3-4): 297-304.
[http://dx.doi.org/10.1515/bmc.2010.026] [PMID: 25962004]
[68]
Stottmann RW, Anderson RM, Klingensmith J. The BMP antagonists Chordin and Noggin have essential but redundant roles in mouse mandibular outgrowth. Dev Biol 2001; 240(2): 457-73.
[http://dx.doi.org/10.1006/dbio.2001.0479] [PMID: 11784076]
[69]
Dal-Pra S, Fürthauer M, Van-Celst J, Thisse B, Thisse C. Noggin1 and Follistatin-like2 function redundantly to Chordin to antagonize BMP activity. Dev Biol 2006; 298(2): 514-26.
[http://dx.doi.org/10.1016/j.ydbio.2006.07.002] [PMID: 16890217]
[70]
Kozmikova I, Candiani S, Fabian P, Gurska D, Kozmik Z. Essential role of Bmp signaling and its positive feedback loop in the early cell fate evolution of chordates. Dev Biol 2013; 382(2): 538-54.
[http://dx.doi.org/10.1016/j.ydbio.2013.07.021] [PMID: 23933491]
[71]
Liem KF Jr, Tremml G, Roelink H, Jessell TM. Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 1995; 82(6): 969-79.
[http://dx.doi.org/10.1016/0092-8674(95)90276-7] [PMID: 7553857]
[72]
Reichert S, Randall RA, Hill CS. A BMP regulatory network controls ectodermal cell fate decisions at the neural plate border. Development 2013; 140(21): 4435-44.
[http://dx.doi.org/10.1242/dev.098707] [PMID: 24089471]
[73]
Cao S, Reece EA, Shen WB, Yang P. Restoring BMP4 expression in vascular endothelial progenitors ameliorates maternal diabetes-induced apoptosis and neural tube defects. Cell Death Dis 2020; 11(10): 859.
[http://dx.doi.org/10.1038/s41419-020-03078-5] [PMID: 33060561]
[74]
Hester M, Thompson JC, Mills J, Liu Y, El-Hodiri HM, Weinstein M. Smad1 and Smad8 function similarly in mammalian central nervous system development. Mol Cell Biol 2005; 25(11): 4683-92.
[http://dx.doi.org/10.1128/MCB.25.11.4683-4692.2005] [PMID: 15899870]
[75]
Binato R, Alvarez Martinez CE, Pizzatti L, Robert B, Abdelhay E. SMAD 8 binding to mice Msx1 basal promoter is required for transcriptional activation. Biochem J 2006; 393(1): 141-50.
[http://dx.doi.org/10.1042/BJ20050327] [PMID: 16101586]
[76]
Chesnutt C, Burrus LW, Brown AMC, Niswander L. Coordinate regulation of neural tube patterning and proliferation by TGFβ and WNT activity. Dev Biol 2004; 274(2): 334-47.
[http://dx.doi.org/10.1016/j.ydbio.2004.07.019] [PMID: 15385163]
[77]
Kalkan T, Iwasaki Y, Park CY, Thomsen GH. Tumor necrosis factor-receptor-associated factor-4 is a positive regulator of transforming growth factor-beta signaling that affects neural crest formation. Mol Biol Cell 2009; 20(14): 3436-50.
[http://dx.doi.org/10.1091/mbc.e08-03-0325] [PMID: 19458200]
[78]
Tang S, Snider P, Firulli AB, Conway SJ. Trigenic neural crest-restricted Smad7 over-expression results in congenital craniofacial and cardiovascular defects. Dev Biol 2010; 344(1): 233-47.
[http://dx.doi.org/10.1016/j.ydbio.2010.05.004] [PMID: 20457144]
[79]
Xie Z, Chen Y, Li Z, et al. Smad6 promotes neuronal differentiation in the intermediate zone of the dorsal neural tube by inhibition of the Wnt/β-catenin pathway. Proc Natl Acad Sci USA 2011; 108(29): 12119-24.
[http://dx.doi.org/10.1073/pnas.1100160108] [PMID: 21730158]
[80]
Das S, Chang C. Regulation of early xenopus embryogenesis by smad ubiquitination regulatory factor 2. Dev Dyn 2012; 241(8): 1260-73.
[http://dx.doi.org/10.1002/dvdy.23811] [PMID: 22674516]
[81]
Dudas M, Sridurongrit S, Nagy A, Okazaki K, Kaartinen V. Craniofacial defects in mice lacking BMP type I receptor Alk2 in neural crest cells. Mech Dev 2004; 121(2): 173-82.
[http://dx.doi.org/10.1016/j.mod.2003.12.003] [PMID: 15037318]
[82]
Caronia G, Wilcoxon J, Feldman P, Grove EA. Bone morphogenetic protein signaling in the developing telencephalon controls formation of the hippocampal dentate gyrus and modifies fear-related behavior. J Neurosci 2010; 30(18): 6291-301.
[http://dx.doi.org/10.1523/JNEUROSCI.0550-10.2010] [PMID: 20445055]
[83]
Schille C, Heller J, Schambony A. Differential requirement of bone morphogenetic protein receptors Ia (ALK3) and Ib (ALK6) in early embryonic patterning and neural crest development. BMC Dev Biol 2016; 16(1): 1.
[http://dx.doi.org/10.1186/s12861-016-0101-5] [PMID: 26780949]
[84]
Park KS, Gumbiner BM. Cadherin-6B stimulates an epithelial mesenchymal transition and the delamination of cells from the neural ectoderm via LIMK/cofilin mediated non-canonical BMP receptor signaling. Dev Biol 2012; 366(2): 232-43.
[http://dx.doi.org/10.1016/j.ydbio.2012.04.005] [PMID: 22537493]
[85]
Ponferrada VG, Fan J, Vallance JE, et al. CRIM1 complexes with ß-catenin and cadherins, stabilizes cell-cell junctions and is critical for neural morphogenesis. PLoS One 2012; 7(3): e32635.
[http://dx.doi.org/10.1371/journal.pone.0032635] [PMID: 22427856]
[86]
Tsurubuchi T, Allender EV, Siddiqui MR, et al. A critical role of noggin in developing folate-nonresponsive NTD in Fkbp8 −/− embryos. Childs Nerv Syst 2014; 30(8): 1343-53.
[http://dx.doi.org/10.1007/s00381-014-2428-1] [PMID: 24817375]
[87]
Yin C, Cai H, Yang D, et al. Cigarette smoke induced neural tube defects by down‐regulating noggin expression. Birth Defects Res 2021; 113(1): 5-13.
[http://dx.doi.org/10.1002/bdr2.1804] [PMID: 32949110]
[88]
Young JJ, Kjolby RAS, Wu G, Wong D, Hsu S, Harland RM. Noggin is required for first pharyngeal arch differentiation in the frog Xenopus tropicalis. Dev Biol 2017; 426(2): 245-54.
[http://dx.doi.org/10.1016/j.ydbio.2016.06.034] [PMID: 27364468]
[89]
Xu J, Zhang Q, Li X, Zhan S, Wang L, Chen D. The effects of copper oxide nanoparticles on dorsoventral patterning, convergent extension, and neural and cardiac development of zebrafish. Aquat Toxicol 2017; 188: 130-7.
[http://dx.doi.org/10.1016/j.aquatox.2017.05.002] [PMID: 28521150]