The canonical Wnt/ß-catenin signaling pathway regulates Fgf signaling for early facial development

Developmental Biology

Volumn 349, Issue 2, 2011, Pages 250-260

  Wang, Yongping ^a,b   Song, Lanying ^a,b   Zhou, Chengji J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SHRINERS HOSPITALS FOR CHILDREN NORTHERN CALIFORNIA   (United States)

Author keywords

Anterior neural ridge (ANR); Facial ectoderm; Fgf8; Foxg1 Cre; Mice; Wnt catenin signaling

Indexed keywords

BETA CATENIN; CELL PROTEIN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR 17; FIBROBLAST GROWTH FACTOR 3; FIBROBLAST GROWTH FACTOR 4; FIBROBLAST GROWTH FACTOR 8; MESSENGER RNA; PROTEIN TCFAP2A; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; FOXG1 PROTEIN, MOUSE; LUCIFERASE; NERVE PROTEIN; PRIMER DNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIRTH; BRAIN DEVELOPMENT; CELL SURVIVAL; CONTROLLED STUDY; CRANIOFACIAL DEVELOPMENT; ECTODERM; EMBRYO; FACE DEVELOPMENT; FEMALE; FOREBRAIN; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE TARGETING; JAW; MANDIBLE; MOLECULAR BIOLOGY; MOUSE; MOUSE MUTANT; NEUROEPITHELIUM; NONHUMAN; PRIMORDIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TELENCEPHALON; TONGUE; TRANSCRIPTION REGULATION; ABLATION THERAPY; ANIMAL; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; FACIAL BONE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; NICK END LABELING; PHYSIOLOGY; PRENATAL DEVELOPMENT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

MAMMALIA; MUS;

ABLATION TECHNIQUES; ANIMALS; APOPTOSIS; BETA CATENIN; CHROMATIN IMMUNOPRECIPITATION; DNA PRIMERS; ECTODERM; FACIAL BONES; FIBROBLAST GROWTH FACTORS; FLUORESCENT ANTIBODY TECHNIQUE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; LUCIFERASES; MICE; MICE, MUTANT STRAINS; NERVE TISSUE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TELENCEPHALON; WNT PROTEINS;

EID: 78650849731     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.11.004     Document Type: Article

References (71)

1. Abu-Issa R., Smyth G., Smoak I., Yamamura K., Meyers E.N. Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development 2002, 129:4613-4625.
2. Acampora D., Boyl P.P., Signore M., Martinez-Barbera J.P., Ilengo C., Puelles E., Annino A., Reichert H., Corte G., Simeone A. OTD/OTX2 functional equivalence depends on 5' and 3' UTR-mediated control of Otx2 mRNA for nucleo-cytoplasmic export and epiblast-restricted translation. Development 2001, 128:4801-4813.
3. Bachler M., Neubuser A. Expression of members of the Fgf family and their receptors during midfacial development. Mech Dev 2001, 100:313-316.
4. Belloni E., Muenke M., Roessler E., Traverso G., Siegel-Bartelt J., Frumkin A., Mitchell H.F., Donis-Keller H., Helms C., Hing A.V., Heng H.H., Koop B., Martindale D., Rommens J.M., Tsui L.C., Scherer S.W. Identification of Sonic hedgehog as a candidate gene responsible for holoprosencephaly. Nat Genet 1996, 14:353-356.
5. Bendavid C., Dupe V., Rochard L., Gicquel I., Dubourg C., David V. Holoprosencephaly: an update on cytogenetic abnormalities. Am J Med Genet C Semin Med Genet 2010, 154C:86-92.
6. Brault V., Moore R., Kutsch S., Ishibashi M., Rowitch D.H., McMahon A.P., Sommer L., Boussadia O., Kemler R. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 2001, 128:1253-1264.
7. Brugmann S.A., Goodnough L.H., Gregorieff A., Leucht P., ten Berge D., Fuerer C., Clevers H., Nusse R., Helms J.A. Wnt signaling mediates regional specification in the vertebrate face. Development 2007, 134:3283-3295.
8. Carroll T.J., Park J.S., Hayashi S., Majumdar A., McMahon A.P. Wnt9b plays a central role in the regulation of mesenchymal to epithelial transitions underlying organogenesis of the mammalian urogenital system. Dev Cell 2005, 9:283-292.
9. Chai Y., Maxson R.E. Recent advances in craniofacial morphogenesis. Dev Dyn 2006, 235:2353-2375.
10. Chamorro M.N., Schwartz D.R., Vonica A., Brivanlou A.H., Cho K.R., Varmus H.E. FGF-20 and DKK1 are transcriptional targets of beta-catenin and FGF-20 is implicated in cancer and development. Embo J 2005, 24:73-84.
11. Chi C.L., Martinez S., Wurst W., Martin G.R. The isthmic organizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum. Development 2003, 130:2633-2644.
12. Christiansen J.H., Coles E.G., Wilkinson D.G. Molecular control of neural crest formation, migration and differentiation. Curr Opin Cell Biol 2000, 12:719-724.
13. Clouthier D.E., Schilling T.F. Understanding endothelin-1 function during craniofacial development in the mouse and zebrafish. Birth Defects Res C Embryo Today 2004, 72:190-199.
14. Cohen E.D., Wang Z., Lepore J.J., Lu M.M., Taketo M.M., Epstein D.J., Morrisey E.E. Wnt/beta-catenin signaling promotes expansion of Isl-1-positive cardiac progenitor cells through regulation of FGF signaling. J Clin Invest 2007, 117:1794-1804.
15. Creuzet S., Couly G., Le Douarin N.M. Patterning the neural crest derivatives during development of the vertebrate head: insights from avian studies. J Anat 2005, 207:447-459.
16. Depew M.J., Simpson C.A., Morasso M., Rubenstein J.L. Reassessing the Dlx code: the genetic regulation of branchial arch skeletal pattern and development. J Anat 2005, 207:501-561.
17. Dubourg C., Lazaro L., Pasquier L., Bendavid C., Blayau M., Le Duff F., Durou M.R., Odent S., David V. Molecular screening of SHH, ZIC2, SIX3, and TGIF genes in patients with features of holoprosencephaly spectrum: mutation review and genotype-phenotype correlations. Hum Mutat 2004, 24:43-51.
18. Filosa S., Rivera-Perez J.A., Gomez A.P., Gansmuller A., Sasaki H., Behringer R.R., Ang S.L. Goosecoid and HNF-3beta genetically interact to regulate neural tube patterning during mouse embryogenesis. Development 1997, 124:2843-2854.
19. Garcia-Castro M.I., Marcelle C., Bronner-Fraser M. Ectodermal Wnt function as a neural crest inducer. Science 2002, 297:848-851.
20. Goldfarb M. Functions of fibroblast growth factors in vertebrate development. Cytokine Growth Factor Rev 1996, 7:311-325.
21. Goydos J.S., Gorski D.H. Vascular endothelial growth factor C mRNA expression correlates with stage of progression in patients with melanoma. Clin Cancer Res 2003, 9:5962-5967.
22. Grieshammer U., Cebrian C., Ilagan R., Meyers E., Herzlinger D., Martin G.R. FGF8 is required for cell survival at distinct stages of nephrogenesis and for regulation of gene expression in nascent nephrons. Development 2005, 132:3847-3857.
23. Grigoryan T., Wend P., Klaus A., Birchmeier W. Deciphering the function of canonical Wnt signals in development and disease: conditional loss- and gain-of-function mutations of beta-catenin in mice. Genes Dev 2008, 22:2308-2341.
24. Harada N., Tamai Y., Ishikawa T., Sauer B., Takaku K., Oshima M., Taketo M.M. Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. Embo J 1999, 18:5931-5942.
25. Hebert J.M., McConnell S.K. Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures. Dev Biol 2000, 222:296-306.
26. Hu D., Marcucio R.S. A SHH-responsive signaling center in the forebrain regulates craniofacial morphogenesis via the facial ectoderm. Development 2009, 136:107-116.
27. Hu D., Marcucio R.S., Helms J.A. A zone of frontonasal ectoderm regulates patterning and growth in the face. Development 2003, 130:1749-1758.
28. Huang X., Saint-Jeannet J.P. Induction of the neural crest and the opportunities of life on the edge. Dev Biol 2004, 275:1-11.
29. Itoh N., Ornitz D.M. Functional evolutionary history of the mouse Fgf gene family. Dev Dyn 2008, 237:18-27.
30. Jiang R., Bush J.O., Lidral A.C. Development of the upper lip: morphogenetic and molecular mechanisms. Dev Dyn 2006, 235:1152-1166.
31. Junghans D., Hack I., Frotscher M., Taylor V., Kemler R. Beta-catenin-mediated cell-adhesion is vital for embryonic forebrain development. Dev Dyn 2005, 233:528-539.
32. Kato M., Patel M.S., Levasseur R., Lobov I., Chang B.H., Glass D.A., Hartmann C., Li L., Hwang T.H., Brayton C.F., Lang R.A., Karsenty G., Chan L. Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J Cell Biol 2002, 157:303-314.
33. Kawauchi S., Shou J., Santos R., Hebert J.M., McConnell S.K., Mason I., Calof A.L. Fgf8 expression defines a morphogenetic center required for olfactory neurogenesis and nasal cavity development in the mouse. Development 2005, 132:5211-5223.
34. Kelly O.G., Pinson K.I., Skarnes W.C. The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice. Development 2004, 131:2803-2815.
35. Kratochwil K., Galceran J., Tontsch S., Roth W., Grosschedl R. FGF4, a direct target of LEF1 and Wnt signaling, can rescue the arrest of tooth organogenesis in Lef1(-/-) mice. Genes Dev 2002, 16:3173-3185.
36. Lan Y., Ryan R.C., Zhang Z., Bullard S.A., Bush J.O., Maltby K.M., Lidral A.C., Jiang R. Expression of Wnt9b and activation of canonical Wnt signaling during midfacial morphogenesis in mice. Dev Dyn 2006, 235:1448-1454.
37. Lin L., Cui L., Zhou W., Dufort D., Zhang X., Cai C.L., Bu L., Yang L., Martin J., Kemler R., Rosenfeld M.G., Chen J., Evans S.M. Beta-catenin directly regulates Islet1 expression in cardiovascular progenitors and is required for multiple aspects of cardiogenesis. Proc Natl Acad Sci U S A 2007, 104:9313-9318.
38. Liu A., Joyner A.L. EN and GBX2 play essential roles downstream of FGF8 in patterning the mouse mid/hindbrain region. Development 2001, 128:181-191.
39. Logan C.Y., Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 2004, 20:781-810.
40. Macatee T.L., Hammond B.P., Arenkiel B.R., Francis L., Frank D.U., Moon A.M. Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 2003, 130:6361-6374.
41. MacDonald B.T., Tamai K., He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 2009, 17:9-26.
42. Marcucio R.S., Cordero D.R., Hu D., Helms J.A. Molecular interactions coordinating the development of the forebrain and face. Dev Biol 2005, 284:48-61.
43. McLeod M.J. Differential staining of cartilage and bone in whole mouse fetuses by Alcian blue and alizarin red S. Teratology 1980, 22:299-301.
44. Minoux M., Rijli F.M. Molecular mechanisms of cranial neural crest cell migration and patterning in craniofacial development. Development 2010, 137:2605-2621.
45. Mosimann C., Hausmann G., Basler K. Beta-catenin hits chromatin: regulation of Wnt target gene activation. Nat Rev Mol Cell Biol 2009, 10:276-286.
46. Nie X., Luukko K., Kettunen P. BMP signalling in craniofacial development. Int J Dev Biol 2006, 50:511-521.
47. Nie X., Luukko K., Kettunen P. FGF signalling in craniofacial development and developmental disorders. Oral Dis 2006, 12:102-111.
48. Niemann S., Zhao C., Pascu F., Stahl U., Aulepp U., Niswander L., Weber J.L., Muller U. Homozygous WNT3 mutation causes tetra-amelia in a large consanguineous family. Am J Hum Genet 2004, 74:558-563.
49. Noden D.M., Francis-West P. The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 2006, 235:1194-1218.
50. Paek H., Gutin G., Hebert J.M. FGF signaling is strictly required to maintain early telencephalic precursor cell survival. Development 2009, 136:2457-2465.
51. Parr B.A., Shea M.J., Vassileva G., McMahon A.P. Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 1993, 119:247-261.
52. Riley B.M., Mansilla M.A., Ma J., Daack-Hirsch S., Maher B.S., Raffensperger L.M., Russo E.T., Vieira A.R., Dode C., Mohammadi M., Marazita M.L., Murray J.C. Impaired FGF signaling contributes to cleft lip and palate. Proc Natl Acad Sci U S A 2007, 104:4512-4517.
53. Roessler E., Belloni E., Gaudenz K., Jay P., Berta P., Scherer S.W., Tsui L.C., Muenke M. Mutations in the human Sonic Hedgehog gene cause holoprosencephaly. Nat Genet 1996, 14:357-360.
54. Roessler E., El-Jaick K.B., Dubourg C., Velez J.I., Solomon B.D., Pineda-Alvarez D.E., Lacbawan F., Zhou N., Ouspenskaia M., Paulussen A., Smeets H.J., Hehr U., Bendavid C., Bale S., Odent S., David V., Muenke M. The mutational spectrum of holoprosencephaly-associated changes within the SHH gene in humans predicts loss-of-function through either key structural alterations of the ligand or its altered synthesis. Hum Mutat 2009, 30:E921-E935.
55. Schneider R.A., Hu D., Rubenstein J.L., Maden M., Helms J.A. Local retinoid signaling coordinates forebrain and facial morphogenesis by maintaining FGF8 and SHH. Development 2001, 128:2755-2767.
56. Shimamura K., Rubenstein J.L. Inductive interactions direct early regionalization of the mouse forebrain. Development 1997, 124:2709-2718.
57. Song L., Li Y., Wang K., Wang Y.Z., Molotkov A., Gao L., Zhao T., Yamagami T., Wang Y., Gan Q., Pleasure D.E., Zhou C.J. Lrp6-mediated canonical Wnt signaling is required for lip formation and fusion. Development 2009, 136:3161-3371.
58. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 1999, 21:70-71.
59. Suzuki-Hirano A., Shimogori T. The role of Fgf8 in telencephalic and diencephalic patterning. Semin Cell Dev Biol 2009, 20:719-725.
60. Szabo-Rogers H.L., Smithers L.E., Yakob W., Liu K.J. New directions in craniofacial morphogenesis. Dev Biol 2010, 341:84-94.
61. Thisse B., Thisse C. Functions and regulations of fibroblast growth factor signaling during embryonic development. Dev Biol 2005, 287:390-402.
62. Trumpp A., Depew M.J., Rubenstein J.L., Bishop J.M., Martin G.R. Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. Genes Dev 1999, 13:3136-3148.
63. Vendrell V., Summerhurst K., Sharpe J., Davidson D., Murphy P. Gene expression analysis of canonical Wnt pathway transcriptional regulators during early morphogenesis of the facial region in the mouse embryo. Gene Expr Patterns 2009, 9:296-305.
64. Wang Y.Z., Molotkov A., Song L., Li Y., Pleasure D.E., Zhou C.J. Activation of the Wnt/beta-catenin signaling reporter in developing mouse olfactory nerve layer marks a specialized subgroup of olfactory ensheathing cells. Dev Dyn 2008, 237:3157-3168.
65. Wang X.P., O'Connell D.J., Lund J.J., Saadi I., Kuraguchi M., Turbe-Doan A., Cavallesco R., Kim H., Park P.J., Harada H., Kucherlapati R., Maas R.L. Apc inhibition of Wnt signaling regulates supernumerary tooth formation during embryogenesis and throughout adulthood. Development 2009, 136:1939-1949.
66. Wilkie A.O., Morriss-Kay G.M. Genetics of craniofacial development and malformation. Nat Rev Genet 2001, 2:458-468.
67. Willert K., Nusse R. Beta-catenin: a key mediator of Wnt signaling. Curr Opin Genet Dev 1998, 8:95-102.
68. Wu J., Saint-Jeannet J.P., Klein P.S. Wnt-frizzled signaling in neural crest formation. Trends Neurosci 2003, 26:40-45.
69. Zhou C.J., Pinson K.I., Pleasure S.J. Severe defects in dorsal thalamic development in low-density lipoprotein receptor-related protein-6 mutants. J Neurosci 2004, 24:7632-7639.
70. Zhou C.J., Molotkov A., Song L., Li Y., Pleasure D.E., Pleasure S.J., Wang Y.Z. Ocular coloboma and dorsoventral neuroretinal patterning defects in Lrp6 mutant eyes. Dev Dyn 2008, 237:3681-3689.
71. Zhou C.J., Wang Y.Z., Yamagami T., Zhao T., Song L., Wang K. Generation of Lrp6 conditional gene-targeting mouse line for modeling and dissecting multiple birth defects/congenital anomalies. Dev Dyn 2010, 239:318-326.