A Sprouty4 reporter to monitor FGF/ERK signaling activity in ESCs and mice
Open accessAbstract
The FGF/ERK signaling pathway is highly conserved throughout evolution and plays fundamental roles during embryonic development and in adult organisms. While a plethora of expression data exists for ligands, receptors and pathway regulators, we know little about the spatial organization or dynamics of signaling in individual cells within populations. To this end we developed a transcriptional readout of FGF/ERK activity by targeting a histone H2B-linked Venus fluorophore to the endogenous locus of Spry4, an early pathway target, and generated Spry4 H2B-Venus embryonic stem cells (ESCs) and a derivative mouse line. The Spry4 H2B-Venus reporter was heterogeneously expressed within ESC cultures and responded to FGF/ERK signaling manipulation. In vivo, the Spry4 H2B-Venus reporter recapitulated the expression pattern of Spry4 and localized to sites of known FGF/ERK activity including the inner cell mass of the pre-implantation embryo and the limb buds, somites and isthmus of the post-implantation embryo. Additionally, we observed highly localized reporter expression within adult organs. Genetic and chemical disruption of FGF/ERK signaling, in vivo in pre- and post-implantation embryos, abrogated Venus expression establishing the reporter as an accurate signaling readout. This tool will provide new insights into the dynamics of the FGF/ERK signaling pathway during mammalian development.
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FGF4 signaling is active across the ICM population and is critical for PrE specification.
“While active across the ICM population25–27, FGF4 signaling is critical for PrE specification28,29.”
From The emergent landscape of the mouse gut endoderm at single-cell resolution (2019) · cites this paper as [25]
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- [1]Brewer JR, Mazot P, and Soriano P, Genetic insights into the mechanisms of Fgf signaling. Genes Dev, 2016 30(7): p. 751– 71. 27036966 PMC4826393
- [2]Ornitz DM and Itoh N, The Fibroblast Growth Factor signaling pathway. Wiley Interdiscip Rev Dev Biol, 2015 4(3): p. 215– 66. 25772309 PMC4393358
- [3]Itoh N and Ornitz DM, Fibroblast growth factors: from molecular evolution to roles in development, metabolism and disease. J Biochem, 2011 149(2): p. 121– 30. 20940169 PMC3106964
- [4]Oulion S, Bertrand S, and Escriva H, Evolution of the FGF Gene Family. Int J Evol Biol, 2012 2012: p. 298147. 22919541 PMC3420111
- [5]Dorey K and Amaya E, FGF signalling: diverse roles during early vertebrate embryogenesis. Development, 2010 137(22): p. 3731– 42. 20978071 PMC3747497
- [6]Nies VJ,, Fibroblast Growth Factor Signaling in Metabolic Regulation. Front Endocrinol (Lausanne), 2015 6: p. 193. 26834701 PMC4718082
- [7]Kelleher FC,, Fibroblast growth factor receptors, developmental corruption and malignant disease. Carcinogenesis, 2013 34(10): p. 2198– 205. 23880303
- [8]Turner N and Grose R, Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer, 2010 10(2): p. 116– 29. 20094046
- [9]Su N, Jin M, and Chen L, Role of FGF/FGFR signaling in skeletal development and homeostasis: learning from mouse models. Bone Res, 2014 2: p. 14003. 26273516 PMC4472122
- [10]Tsai SM, Liu DW, and Wang WP, Fibroblast growth factor (Fgf) signaling pathway regulates liver homeostasis in zebrafish. Transgenic Res, 2013 22(2): p. 301– 14. 22820869
- [11]Turner CA,, Dysregulated fibroblast growth factor (FGF) signaling in neurological and psychiatric disorders. Seminars in Cell & Developmental Biology, 2016 53: p. 136– 143. 26454097 PMC4833700
- [12]Chazaud C,, Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev Cell, 2006 10(5): p. 615– 24. 16678776
- [13]Frankenberg S,, Primitive endoderm differentiates via a three-step mechanism involving Nanog and RTK signaling. Dev Cell, 2011 21(6): p. 1005– 13. 22172669
- [14]Kang M,, FGF4 is required for lineage restriction and salt-and-pepper distribution of primitive endoderm factors but not their initial expression in the mouse. Development, 2013 140(2): p. 267– 79. 23193166 PMC3597205
- [15]Nichols J,, Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo. Development, 2009 136(19): p. 3215– 22. 19710168 PMC2739140
- [16]Yamanaka Y, Lanner F, and Rossant J, FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development, 2010 137(5): p. 715– 24. 20147376
- [17]Krawchuk D,, FGF4 is a limiting factor controlling the proportions of primitive endoderm and epiblast in the ICM of the mouse blastocyst. Dev Biol, 2013 384(1): p. 65– 71. 24063807
- [18]Kang MJ, Garg V, and Hadjantonakis AK, Lineage Establishment and Progression within the Inner Cell Mass of the Mouse Blastocyst Requires FGFR1 and FGFR2. Developmental Cell, 2017 41(5): p. 496– +. 28552559 PMC5530874
- [20]Lu CW,, Ras-MAPK signaling promotes trophectoderm formation from embryonic stem cells and mouse embryos. Nat Genet, 2008 40(7): p. 921– 6. 18536715 PMC2690707
- [21]Orr-Urtreger A,, Developmental localization of the splicing alternatives of fibroblast growth factor receptor-2 (FGFR2). Dev Biol, 1993 158(2): p. 475– 86. 8393815
- [22]Rossant J and Cross JC, Placental development: lessons from mouse mutants. Nat Rev Genet, 2001 2(7): p. 538– 48. 11433360
- [23]Nichols J,, Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell, 1998 95(3): p. 379– 91. 9814708
- [24]Brons IG,, Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature, 2007 448(7150): p. 191– 5. 17597762
- [25]Tesar PJ,, New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature, 2007 448(7150): p. 196– 9. 17597760
- [26]Tanaka S,, Promotion of trophoblast stem cell proliferation by FGF4. Science, 1998 282(5396): p. 2072– 5. 9851926
- [27]Bertrand V,, Neural tissue in ascidian embryos is induced by FGF9/16/20, acting via a combination of maternal GATA and Ets transcription factors. Cell, 2003 115(5): p. 615– 27. 14651852
- [28]Ciruna B and Rossant J, FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Dev Cell, 2001 1(1): p. 37– 49. 11703922
- [29]Deng CX,, Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev, 1994 8(24): p. 3045– 57. 8001823
- [30]Isaacs HV, Pownall ME, and Slack JM, eFGF regulates Xbra expression during Xenopus gastrulation. EMBO J, 1994 13(19): p. 4469– 81. 7925289 PMC395379
- [31]Popovici C,, An evolutionary history of the FGF superfamily. Bioessays, 2005 27(8): p. 849– 57. 16015590
- [32]Stathopoulos A,, pyramus and thisbe: FGF genes that pattern the mesoderm of Drosophila embryos. Genes Dev, 2004 18(6): p. 687– 99. 15075295 PMC387243
- [33]Sun X,, Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev, 1999 13(14): p. 1834– 46. 10421635 PMC316887
- [34]Yamaguchi TP,, fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev, 1994 8(24): p. 3032– 44. 8001822
- [35]Matus DQ, Thomsen GH, and Martindale MQ, FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian. Dev Genes Evol, 2007 217(2): p. 137– 48. 17237944 PMC4580332
- [36]Ciruna BG,, Chimeric analysis of fibroblast growth factor receptor-1 (Fgfr1) function: a role for FGFR1 in morphogenetic movement through the primitive streak. Development, 1997 124(14): p. 2829– 41. 9226454
- [38]Nowotschin S,, A bright single-cell resolution live imaging reporter of Notch signaling in the mouse. BMC Dev Biol, 2013 13: p. 15. 23617465 PMC3663770
- [39]Minowada G,, Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development, 1999 126(20): p. 4465– 75. 10498682
- [40]Gross I,, Mammalian Sprouty proteins inhibit cell growth and differentiation by preventing Ras activation. Journal of Biological Chemistry, 2001 276(49): p. 46460– 46468. 11585837
- [41]Katoh Y and Katoh M, FGF signaling inhibitor, SPRY4, is evolutionarily conserved target of WNT signaling pathway in progenitor cells. Int J Mol Med, 2006 17(3): p. 529– 32. 16465403
- [42]Reich A, Sapir A, and Shilo BZ, Sprouty is a general inhibitor of receptor tyrosine kinase signaling. Development, 1999 126(18): p. 4139– 4147. 10457022
- [43]Taniguchi K,, Sprouty2 and Sprouty4 are essential for embryonic morphogenesis and regulation of FGF signaling. Biochem Biophys Res Commun, 2007 352(4): p. 896– 902. 17156747
- [44]Turner DA,, An interplay between extracellular signalling and the dynamics of the exit from pluripotency drives cell fate decisions in mouse ES cells. Biol Open, 2014 3(7): p. 614– 26. 24950969 PMC4154298
- [45]Skarnes WC,, A conditional knockout resource for the genome-wide study of mouse gene function. Nature, 2011 474(7351): p. 337– 42. 21677750 PMC3572410
- [46]Freyer L,, A loss-of-function and H2B-Venus transcriptional reporter allele for Gata6 in mice. BMC Dev Biol, 2015 15: p. 38. 26498761 PMC4619391
- [47]Schroter C,, FGF/MAPK signaling sets the switching threshold of a bistable circuit controlling cell fate decisions in embryonic stem cells. Development, 2015 142(24): p. 4205– 16. 26511924 PMC4689219
- [48]Beard C,, Efficient method to generate single-copy transgenic mice by site-specific integration in embryonic stem cells. Genesis, 2006 44(1): p. 23– 8. 16400644
- [50]Anastassiadis K,, Dre recombinase, like Cre, is a highly efficient site-specific recombinase in E-coli, mammalian cells and mice. Disease Models & Mechanisms, 2009 2(9–10): p. 508– 515. 19692579
- [51]Behringer R, Gertsenstein M, Nagy K, Nagy A, Manipulating the Mouse Embryo: A Laboratory Manual. Vol. 4 2014, Cold Spring Harbor, New York, USA: Cold Spring Harbor Laboratory Press.
- [52]Saiz N,, Quantitative Analysis of Protein Expression to Study Lineage Specification in Mouse Preimplantation Embryos. J Vis Exp, 2016(108): p. 53654. 26967230 PMC4828170
- [53]Conlon RA and Rossant J, Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development, 1992 116(2): p. 357– 68. 1363087
- [54]Artus J,, Impaired mitotic progression and preimplantation lethality in mice lacking OMCG1, a new evolutionarily conserved nuclear protein. Mol Cell Biol, 2005 25(14): p. 6289– 302. 15988037 PMC1168835
- [55]Lou X,, A rapid and efficient 2D/3D nuclear segmentation method for analysis of early mouse embryo and stem cell image data. Stem Cell Reports, 2014 2(3): p. 382– 97. 24672759 PMC3964288
- [56]Saiz N,, Asynchronous fate decisions by single cells collectively ensure consistent lineage composition in the mouse blastocyst. Nat Commun, 2016 7: p. 13463. 27857135 PMC5120222
- [57]Morgani S.M.S., Nestor; Garg Vidur; Hadjantonakis Anna-Katerina, A Sprouty4 reporter to monitor FGF/ERK signaling activity in ESCs and mice. Figshare, 2018. PMC6455974 29964027
- [58]Yang SH,, A genome-wide RNAi screen reveals MAP kinase phosphatases as key ERK pathway regulators during embryonic stem cell differentiation. PLoS Genet, 2012 8(12): p. e1003112. 23271975 PMC3521700
- [59]Collins PJ, Hale CM, and Xu H, Edited course of biomedical research: leaping forward with CRISPR. Pharmacol Res, 2017 125(Pt B): p. 258– 265. 28918173
- [60]Chambers I,, Nanog safeguards pluripotency and mediates germline development. Nature, 2007 450(7173): p. 1230– U8. 18097409
- [61]Singh AM,, A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem Cells, 2007 25(10): p. 2534– 42. 17615266
- [62]Santostefano KE,, Fibroblast Growth Factor Receptor 2 Homodimerization Rapidly Reduces Transcription of the Pluripotency Gene Nanog without Dissociation of Activating Transcription Factors. Journal of Biological Chemistry, 2012 287(36): p. 30507– 30517. 22787153 PMC3436299
- [63]Kim SH,, ERK1 phosphorylates Nanog to regulate protein stability and stem cell self-renewal. Stem Cell Research, 2014 13(1): p. 1– 11. 24793005
- [64]Ohnishi Y,, Cell-to-cell expression variability followed by signal reinforcement progressively segregates early mouse lineages. Nat Cell Biol, 2014 16(1): p. 27– 37. 24292013 PMC4062977
- [65]Guo G,, Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev Cell, 2010 18(4): p. 675– 85. 20412781
- [66]Arman E,, Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proceedings of the National Academy of Sciences of the United States of America, 1998 95(9): p. 5082– 5087. 9560232 PMC20217
- [67]Lake D, Correa SA, and Muller J, Negative feedback regulation of the ERK1/2 MAPK pathway. Cell Mol Life Sci, 2016 73(23): p. 4397– 4413. 27342992 PMC5075022
- [69]Goto H,, FGF and canonical Wnt signaling cooperate to induce paraxial mesoderm from tailbud neuromesodermal progenitors through regulation of a two-step epithelial to mesenchymal transition. Development, 2017 144(8): p. 1412– 1424. 28242612 PMC5399664
- [71]de Maximy AA,, Cloning and expression pattern of a mouse homologue of drosophila sprouty in the mouse embryo. Mech Dev, 1999 81(1–2): p. 213– 6. 10330503
- [72]Hayashi S,, Sprouty4, an FGF inhibitor, displays cyclic gene expression under the control of the notch segmentation clock in the mouse PSM. PLoS One, 2009 4(5): p. e5603. 19440349 PMC2680047
- [73]Crossley PH, Martinez S, and Martin GR, Midbrain development induced by FGF8 in the chick embryo. Nature, 1996 380(6569): p. 66– 8. 8598907
- [74]Chi CL,, The isthmic organizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum. Development, 2003 130(12): p. 2633– 44. 12736208
- [75]Basson MA,, Specific regions within the embryonic midbrain and cerebellum require different levels of FGF signaling during development. Development, 2008 135(5): p. 889– 98. 18216176 PMC2555978
- [76]Kawakami Y,, MKP3 mediates the cellular response to FGF8 signalling in the vertebrate limb. Nat Cell Biol, 2003 5(6): p. 513– 9. 12766772
- [77]Martin GR, The roles of FGFs in the early development of vertebrate limbs. Genes Dev, 1998 12(11): p. 1571– 86. 9620845
- [78]Probst S,, SHH propagates distal limb bud development by enhancing CYP26B1-mediated retinoic acid clearance via AER-FGF signalling. Development, 2011 138(10): p. 1913– 1923. 21471156 PMC3082298
- [79]Zhang S,, Expression of Sprouty genes 1, 2 and 4 during mouse organogenesis. Mech Dev, 2001 109(2): p. 367– 70. 11731251
- [80]Gros J,, WNT5A/JNK and FGF/MAPK Pathways Regulate the Cellular Events Shaping the Vertebrate Limb Bud. Current Biology, 2010 20(22): p. 1993– 2002. 21055947 PMC2998074
- [81]Mao JH,, Fgf-Dependent Etv4/5 Activity Is Required for Posterior Restriction of Sonic hedgehog and Promoting Outgrowth of the Vertebrate Limb. Developmental Cell, 2009 16(4): p. 600– 606. 19386268 PMC3164484
- [82]Li CY,, Dusp6 (Mkp3) is a negative feedback regulator of FGF-stimulated ERK signaling during mouse development. Development, 2007 134(1): p. 167– 176. 17164422 PMC2424197
- [83]Fernandez-Teran MA, Hinchliffe JR, and Ros MA, Birth and death of cells in limb development: A mapping study. Developmental Dynamics, 2006 235(9): p. 2521– 2537. 16881063
- [84]Kanard RC,, Fibroblast growth factor-10 serves a regulatory role in duodenal development. Journal of Pediatric Surgery, 2005 40(2): p. 313– 316. 15750921
- [85]Thys A,, Hyperplasia of Interstitial Cells of Cajal in Sprouty Homolog 4 Deficient Mice. Plos One, 2015 10(4). PMC4414615 25923139
- [86]Itoh N, Nakayama Y, and Konishi M, Roles of FGFs As Paracrine or Endocrine Signals in Liver Development, Health, and Disease. Front Cell Dev Biol, 2016 4: p. 30. 27148532 PMC4829580
- [87]Alsina FC,, Sprouty4 Is an Endogenous Negative Modulator of TrkA Signaling and Neuronal Differentiation Induced by NGF. Plos One, 2012 7(2). PMC3285629 22384148
- [88]Boros J,, Sef and Sprouty expression in the developing ocular lens: implications for regulating lens cell proliferation and differentiation. Semin Cell Dev Biol, 2006 17(6): p. 741– 52. 17141539 PMC1847394
- [89]Ching ST,, Coordinated activity of Spry1 and Spry2 is required for normal development of the external genitalia. Developmental Biology, 2014 386(1): p. 1– 11. 24361260 PMC3921686
- [90]Walker KA, Sims-Lucas S, and Bates CM, Fibroblast growth factor receptor signaling in kidney and lower urinary tract development. Pediatr Nephrol, 2016 31(6): p. 885– 95. 26293980 PMC4761523
- [91]Cancilla B, Ford-Perriss MD, and Bertram JF, Expression and localization of fibroblast growth factors and fibroblast growth factor receptors in the developing rat kidney. Kidney Int, 1999 56(6): p. 2025– 39. 10594778
- [92]Ford MD,, Expression of fibroblast growth factors and their receptors in rat glomeruli. Kidney Int, 1997 51(6): p. 1729– 38. 9186860
- [93]Tajima K,, Luteinizing hormone-induced extracellular-signal regulated kinase activation differently modulates progesterone and androstenedione production in bovine theca cells. Endocrinology, 2005 146(7): p. 2903– 10. 15817663
- [94]Li QX,, The Antiproliferative Action of Progesterone in Uterine Epithelium Is Mediated by Hand2. Science, 2011 331(6019): p. 912– 916. 21330545 PMC3320855
- [95]Chung D,, Estrogen mediated epithelial proliferation in the uterus is directed by stromal Fgf10 and Bmp8a. Molecular and Cellular Endocrinology, 2015 400(C): p. 48– 60. 25451979 PMC4751583
- [96]Hantak AM, Bagchi IC, and Bagchi MK, Role of uterine stromal-epithelial crosstalk in embryo implantation. International Journal of Developmental Biology, 2014 58(2–4): p. 139– 146. 25023679 PMC4768910
- [97]Iwata T and Hevner RF, Fibroblast growth factor signaling in development of the cerebral cortex. Dev Growth Differ, 2009 51(3): p. 299– 323. 19379279
- [98]Kang WF and Hebert JM, FGF Signaling Is Necessary for Neurogenesis in Young Mice and Sufficient to Reverse Its Decline in Old Mice. Journal of Neuroscience, 2015 35(28): p. 10217– 10223. 26180198 PMC4502262
- [99]Yu T,, Sprouty genes prevent excessive FGF signalling in multiple cell types throughout development of the cerebellum. Development, 2011 138(14): p. 2957– 68. 21693512 PMC3119305
- [100]Tuduce IL, Schuh K, and Bundschu K, Spred2 expression during mouse development. Dev Dyn, 2010 239(11): p. 3072– 85. 20882678
- [101]Faedo A, Borello U, and Rubenstein JL, Repression of Fgf signaling by sprouty1–2 regulates cortical patterning in two distinct regions and times. J Neurosci, 2010 30(11): p. 4015– 23. 20237272 PMC2852648
- [102]Felfly H and Klein OD, Sprouty genes regulate proliferation and survival of human embryonic stem cells. Sci Rep, 2013 3: p. 2277. 23880645 PMC3721083
- [103]Lee JY,, Novel Function of Sprouty4 as a Regulator of Stemness and Differentiation of Embryonic Stem Cells. Dev Reprod, 2016 20(2): p. 171– 7. 27660833 PMC5027223
- [104]Masoumi-Moghaddam S, Amini A, and Morris DL, The developing story of Sprouty and cancer. Cancer Metastasis Rev, 2014 33(2–3): p. 695– 720. 24744103 PMC4113681
- [105]Nagai T,, A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol, 2002 20(1): p. 87– 90. 11753368
- [106]Li X,, Generation of destabilized green fluorescent protein as a transcription reporter. J Biol Chem, 1998 273(52): p. 34970– 5. 9857028
- [107]Vilas-Boas F,, A novel reporter of notch signalling indicates regulated and random Notch activation during vertebrate neurogenesis. BMC Biol, 2011 9: p. 58. 21880129 PMC3201213
- [108]Komatsu N,, Development of an optimized backbone of FRET biosensors for kinases and GTPases. Mol Biol Cell, 2011 22(23): p. 4647– 56. 21976697 PMC3226481
- [109]Kunath T,, FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development, 2007 134(16): p. 2895– 902. 17660198
- [110]Tanaka S, Derivation and culture of mouse trophoblast stem cells in vitro. Methods Mol Biol, 2006 329: p. 35– 44. 16845982
- [111]Sasaki H, Mechanisms of trophectoderm fate specification in preimplantation mouse development. Development Growth & Differentiation, 2010 52(3): p. 263– 273. 20100249
- [112]Feldman B,, Requirement of FGF-4 for postimplantation mouse development. Science, 1995 267(5195): p. 246– 9. 7809630
- [113]Niswander L and Martin GR, Fgf-4 Expression during Gastrulation, Myogenesis, Limb and Tooth Development in the Mouse. Development, 1992 114(3): p. 755– 768. 1618140
- [115]Wright TJ,, Expression of mouse fibroblast growth factor and fibroblast growth factor receptor genes during early inner ear development. Dev Dyn, 2003 228(2): p. 267– 72. 14517998
- [116]Haub O and Goldfarb M, Expression of the Fibroblast Growth Factor-5 Gene in the Mouse Embryo. Development, 1991 112(2): p. 397– &. 1794310
- [117]Hebert JM, Boyle M, and Martin GR, Messenger-Rna Localization Studies Suggest That Murine Fgf-5 Plays a Role in Gastrulation. Development, 1991 112(2): p. 407– 415. 1794311
- [118]Crossley PH and Martin GR, The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development, 1995 121(2): p. 439– 51. 7768185
- [119]Donnison M, Broadhurst R, and Pfeffer PL, Elf5 and Ets2 maintain the mouse extraembryonic ectoderm in a dosage dependent synergistic manner. Developmental Biology, 2015 397(1): p. 77– 88. 25446535
- [120]Zhao ZA,, The roles of ERAS during cell lineage specification of mouse early embryonic development. Open Biol, 2015 5(8). PMC4554925 26269429
- [121]Chotteau-Lelievre A,, Expression patterns of the Ets transcription factors from the PEA3 group during early stages of mouse development. Mech Dev, 2001 108(1–2): p. 191– 5. 11578874
- [122]Esner M,, Targeted disruption of fibroblast growth factor receptor-1 blocks maturation of visceral endoderm and cavitation in mouse embryoid bodies. Int J Dev Biol, 2002 46(6): p. 817– 25. 12382948
- [123]Winn RA,, Restoration of Wnt-7a expression reverses non-small cell lung cancer cellular transformation through frizzled-9-mediated growth inhibition and promotion of cell differentiation. J Biol Chem, 2005 280(20): p. 19625– 34. 15705594
- [124]Pan YC,, Insertion of a knockout-first cassette in Ampd1 gene leads to neonatal death by disruption of neighboring genes expression. Scientific Reports, 2016 6. PMC5075929 27775065
- [125]Scarff KL,, A retained selection cassette increases reporter gene expression without affecting tissue distribution in SPI3 knockout/GFP knock-in mice. Genesis, 2003 36(3): p. 149– 157. 12872246
- [126]Huh SH, Warchol ME, and Ornitz DM, Cochlear progenitor number is controlled through mesenchymal FGF receptor signaling. Elife, 2015 4. PMC4434254 25915623
- [127]Klein OD,, Sprouty genes control diastema tooth development via bidirectional antagonism of epithelial-mesenchymal FGF signaling. Developmental Cell, 2006 11(2): p. 181– 190. 16890158 PMC2847684
- [128]Rice R,, Disruption of Fgf10/Fgfr2b-coordinated epithelial-mesenchymal interactions causes cleft palate. Journal of Clinical Investigation, 2004 113(12): p. 1692– 1700. 15199404 PMC420504
- [129]Zhang XQ,, Reciprocal epithelial-mesenchymal FGF signaling is required for cecal development. Development, 2006 133(1): p. 173– 180. 16308329 PMC2065859
- [130]El Ramy R,, Fibroblast growth factor (FGF) 2 and FGF9 mediate mesenchymal-epithelial interactions of peritubular and Sertoli cells in the rat testis. Journal of Endocrinology, 2005 187(1): p. 135– 147. 16214949
- [131]Volckaert T and De Langhe SP, Wnt and FGF Mediated Epithelial-Mesenchymal Crosstalk During Lung Development. Developmental Dynamics, 2015 244(3): p. 342– 366. 25470458 PMC4344844
- Authors
- Morgani, S. M., Saiz, N., Garg, V., Raina, D., Simon, C. S., Kang, M., Arias, A. M., Nichols, J., Schröter, C., & Hadjantonakis, A.-K.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- Max Planck Institute of Molecular Physiology (DE)
- Wellcome/MRC Cambridge Stem Cell Institute (GB)
- Corresponding author
- Hadjantonakis, Anna-Katerina
- ORCID
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2018-09
- Volume
- 441
- Issue
- 1
- Pages
- 104-126
- ISSN
- 0012-1606 (ISSN-L)
- PMC
- PMC6455974
- OpenAlex
- W2810807384
- Cited by
- 55
- References
- 134
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 9 · 2023: 8 · 2022: 7 · 2021: 8 · 2020: 4 · 2019: 7 · 2018: 2
- FWCI
- 1.87
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Max Planck Digital Library (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Repositori digital de la UPF (Universitat Pompeu Fabra) (submittedVersion)
- Funders
- NIH (R01HD094868, R01DK084391, P30CA00874)
- BBSRC Project (BB/M023370/1)
- Wellcome Trust Sir Henry Wellcome Postdoctoral Fellowship (110151/Z/15/Z)
- Starr Foundation Tri-Institutional Stem Cell Initiative
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fibroblast Growth Factor Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Keywords
- SPRY4, embryonic stem cells, preimplantation embryo, postimplantation embryo, limb bud, somites, isthmus
- MeSH terms
- Mouse Embryonic Stem Cells, Animals, Embryo, Mammalian, Fibroblast Growth Factors, Nerve Tissue Proteins, MAP Kinase Signaling System, Organogenesis, Embryonic Development, Extracellular Signal-Regulated MAP Kinases, Mice, Cell Tracking
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Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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