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JOURNAL ARTICLES
Inactivation of the (β)-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development
V. Brault, R. Moore, S. Kutsch, M. Ishibashi, D.H. Rowitch, A.P. McMahon, L. Sommer, O. Boussadia, R. Kemler
Development 2001 128: 1253-1264;

Summary

('bgr;)-Catenin is a central component of both the cadherin-catenin cell adhesion complex and the Wnt signaling pathway. We have investigated the role of (β)-catenin during brain morphogenesis, by specifically inactivating the (β)-catenin gene in the region of Wnt1 expression. To achieve this, mice with a conditional ('floxed') allele of (β)-catenin with required exons flanked by loxP recombination sequences were intercrossed with transgenic mice that expressed Cre recombinase under control of Wnt1 regulatory sequences. (β)-catenin gene deletion resulted in dramatic brain malformation and failure of craniofacial development. Absence of part of the midbrain and all of the cerebellum is reminiscent of the conventional Wnt1 knockout (Wnt1(−)(/)(−)), suggesting that Wnt1 acts through (β)-catenin in controlling midbrain-hindbrain development. The craniofacial phenotype, not observed in embryos that lack Wnt1, indicates a role for (β)-catenin in the fate of neural crest cells. Analysis of neural tube explants shows that (β)-catenin is efficiently deleted in migrating neural crest cell precursors. This, together with an increased apoptosis in cells migrating to the cranial ganglia and in areas of prechondrogenic condensations, suggests that removal of (β)-catenin affects neural crest cell survival and/or differentiation. Our results demonstrate the pivotal role of (β)-catenin in morphogenetic processes during brain and craniofacial development.

Reference

    1. Aberle H.,
    2. Butz S.,
    3. Stappert J.,
    4. Weissig H.,
    5. Kemler R.,
    6. Hoschuetzky H.
    (1994) Assembly of the cadherin-catenin complex in vitro with recombinant proteins. J. Cell Sci 107, 3655–3663
    OpenUrlAbstract/FREE Full Text
    1. Aberle H.,
    2. Schwartz H.,
    3. Hoschuetzky H.,
    4. Kemler R.
    (1996) Single amino acid substitutions in proteins of the armadillo gene family abolish their binding to alpha-catenin. J. Biol. Chem 271, 1520–1526
    OpenUrlAbstract/FREE Full Text
    1. Aberle H.,
    2. Schwartz H.,
    3. Kemler R.
    (1996) Cadherin-catenin complex: protein interactions and their implications for cadherin function. J. Cell Biochem 61, 514–523
    OpenUrlCrossRefPubMedWeb of Science
    1. Achatz G.,
    2. Nitschke L.,
    3. Lamers M. C.
    (1997) Effect of transmembrane and cytoplasmic domains of IgE on the IgE response. Science 276, 409–411
    OpenUrlAbstract/FREE Full Text
    1. Bally-Cuif L.,
    2. Cholley B.,
    3. Wassef M.
    (1995) Involvement of Wnt-1 in the formation of the mes/metencephalic boundary. Mech. Dev 53, 23–34
    OpenUrlCrossRefPubMedWeb of Science
    1. Berx G.,
    2. Nollet F.,
    3. van Roy F.
    (1998) Dysregulation of the E-cadherin/catenin complex by irreversible mutations in human carcinomas. Cell Adhes. Commun 6, 171–184
    OpenUrlCrossRefPubMedWeb of Science
    1. Butz S.,
    2. Stappert J.,
    3. Weissig H.,
    4. Kemler R.
    (1992) Plakoglobin and beta-catenin: distinct but closely related. Science 257, 1142–1144
    OpenUrlFREE Full Text
    1. Cadigan K. M.,
    2. Nusse R.
    (1997) Wnt signaling: a common theme in animal development. Genes Dev 11, 3286–3305
    OpenUrlFREE Full Text
    1. Chai Y.,
    2. Bringas P., Jr.,
    3. Shuler C.,
    4. Devaney E.,
    5. Grosschedl R.,
    6. Slavkin H. C.
    (1998) A mouse mandibular culture model permits the study of neural crest cell migration and tooth development. Int. J. Dev. Biol 42, 87–94
    OpenUrlPubMed
    1. Chai Y.,
    2. Jian X.,
    3. Ito Y.,
    4. Bringas P.,
    5. Han J.,
    6. Rowitch D. H.,
    7. Soriano P.,
    8. McMahon A. P.,
    9. Sucov H. M.
    (2000) Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127, 1671–1679
    OpenUrlAbstract
    1. Crossley P.,
    2. Martin G. R.
    (1995) The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121, 439–451
    OpenUrlAbstract
    1. Danielian P. S.,
    2. White R.,
    3. Lees J. A.,
    4. Parker M. G.
    (1992) Identification of a conserved region required for hormone dependent transcriptional activation by steroid hormone receptors. EMBO J 11, 1025–1033
    OpenUrlPubMedWeb of Science
    1. Danielian P. S.,
    2. McMahon A. P.
    (1996) Engrailed-1 as a target of the Wnt-1 signalling pathway in vertebrate midbrain development. Nature 383, 332–334
    OpenUrlCrossRefPubMedWeb of Science
    1. Danielian P. S.,
    2. Muccino D.,
    3. Rowitch D. H.,
    4. Michael S. K.,
    5. McMahon A. P.
    (1998) Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol 8, 1323–1326
    OpenUrlCrossRefPubMedWeb of Science
    1. Davis C. A.,
    2. Joyner A. L.
    (1988) Expression patterns of the homeo box-containing genes En-1 and En-2 and the proto-oncogene int-1 diverge during mouse development. Genes Dev 2, 1736–1744
    OpenUrlAbstract/FREE Full Text
    1. Davis C. A.,
    2. Holmyard D. P.,
    3. Millen K. J.,
    4. Joyner A. L.
    (1991) Examining pattern formation in mouse, chicken, and frog embryos with an En -specific antiserum. Development 111, 287–298
    OpenUrlAbstract
    1. Dickinson M. E.,
    2. Krumlauf R.,
    3. McMahon A. P.
    (1994) Evidence fora mitogenic effect of Wnt-1 in the developing mammalian central nervous system. Development 120, 1453–1471
    OpenUrlAbstract
    1. Eastman Q.,
    2. Grosschedl R.
    (1999) Regulation of LEF-1/TCF transcription factors by Wnt and other signals. Curr. Opin. Cell Biol 11, 233–240
    OpenUrlCrossRefPubMedWeb of Science
    1. Echelard Y.,
    2. Vassileva G.,
    3. McMahon A. P.
    (1994) Cis-acting regulatory sequences governing Wnt-1 expression in the developing mouse CNS. Development 120, 13–24
    OpenUrlAbstract/FREE Full Text
    1. Etchevers H. C.,
    2. Couly G.,
    3. Vincent C.,
    4. Le Douarin N. M.
    (1999) Anterior cephalic neural crest is required for forebrain viability. Development 126, 3533–3543
    OpenUrlAbstract
    1. Gendron-Maguire M.,
    2. Mallo M.,
    3. Zhang M.,
    4. Gridley T.
    (1993) Hoxa-2 mutant mice exhibit homeotic transformation of skeletal elements derived from cranial neural crest. Cell 75, 1317–1331
    OpenUrlCrossRefPubMedWeb of Science
    1. Gerhardt H.,
    2. Wolburg H.,
    3. Redies C.
    (2000) N-cadherin mediates pericytic-endothelial interaction during brain angiogenesis in the chicken. Dev. Dyn 218, 472–479
    OpenUrlCrossRefPubMedWeb of Science
    1. Gonzalez F.,
    2. Swales I.,
    3. Bejsovec A.,
    4. Skaer H.,
    5. Martinez-Arias A.
    (1991) Secretion and movement of the wingless protein in the epidermis of the Drosophila embryo. Mech. Dev 35, 43–54
    OpenUrlCrossRefPubMedWeb of Science
    1. Grove E. A.,
    2. Tole S.,
    3. Limon J.,
    4. Yip L.-W.,
    5. Ragsdale C.
    (1998) The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3 -deficient mice. Development 125, 2315–2325
    OpenUrlAbstract
    1. Haegel H.,
    2. Larue L.,
    3. Ohsugi M.,
    4. Fedorov L.,
    5. Herrenknecht K.,
    6. Kemler R.
    (1995) Lack of-catenin affects mouse development at gastrulation. Development 121, 3529–3537
    OpenUrlAbstract
    1. Hagedorn L.,
    2. Suter U.,
    3. Sommer L.
    (1999) PO and PM22 mark a multipotent neural crest-derived cell type that displays community effects in response to TGF-family factors. Development 126, 3781–3794
    OpenUrlAbstract
    1. Heikinheimo M.,
    2. Lawshe A.,
    3. Shackleford G. M.,
    4. Wilson D. B.,
    5. McArthur C. A.
    (1994) Fgf-8 expression in the post-gastrulation mouse suggests roles in the development of the face, limbs, and central nervous system. Mech. Dev 48, 129–138
    OpenUrlCrossRefPubMedWeb of Science
    1. Hollyday M.,
    2. McMahon J. A.,
    3. McMahon A. P.
    (1995) Wnt expression patterns in chick embryo nervous system. Mech. Dev 52, 9–25
    OpenUrlCrossRefPubMedWeb of Science
    1. Huelsken J.,
    2. Vogel R.,
    3. Brinkmann V.,
    4. Erdmann B.,
    5. Birchmeier C.,
    6. Birchmeier W.
    (2000) Requirement for-catenin in anterior-posterior axis formation in mice. J. Cell Biol 148, 567–578
    OpenUrlAbstract/FREE Full Text
    1. Hulsken J.,
    2. Birchmeier W.,
    3. Behrens J.
    (1994) E-cadherin and APC compete for the interaction with-catenin and the cytoskeleton. J. Cell Biol 127, 2061–2069
    OpenUrlAbstract/FREE Full Text
    1. Ikeya M.,
    2. Lee S. M. K.,
    3. Johnson J. E.,
    4. McMahon A. P.,
    5. Takada S.
    (1997) Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389, 966–970
    OpenUrlCrossRefPubMedWeb of Science
    1. Inoue T.,
    2. Chisaka O.,
    3. Matsunami H.,
    4. Takeichi M.
    (1997) Cadherin-6 expression transiently delineates specific rhombomeres, other neural tube subdivisions, and neural crest subpopulations in mouse embryos. Dev. Biol 183, 183–194
    OpenUrlCrossRefPubMedWeb of Science
    1. Jiang X.,
    2. Rowitch D. H.,
    3. Soriano P.,
    4. McMahon A. P.,
    5. Sucov H. M.
    (2000) Fate of the mammalian cardiac neural crest. Development 127, 1607–1616
    OpenUrlAbstract
    1. Jou T. S.,
    2. Stewart D. B.,
    3. Stappert J.,
    4. Nelson W. J.,
    5. Marrs J. A.
    (1995) Genetic and biochemical dissection of protein linkages in the cadherin-catenin complex. Proc. Natl. Acad. Sci. USA 92, 5067–5071
    OpenUrlAbstract/FREE Full Text
    1. Jue S. F.,
    2. Bradley R. S.,
    3. Rudnicki J. A.,
    4. Varmus H. E.,
    5. Brown A.M.
    (1992) The mouse Wnt-1 gene can act via a paracrine mechanism in transformation of mammary epithelial cells. Mol. Cell Biol 12, 321–328
    OpenUrlAbstract/FREE Full Text
    1. Kanzler B.,
    2. Foreman R. K.,
    3. Labosky P. A.,
    4. Mallo M.
    (2000) BMP signaling is essential for development of skeletogenic and neurogenic cranial neural crest. Development 127, 1095–1104
    OpenUrlAbstract
    1. Kimura Y.,
    2. Matsunami H.,
    3. Takeichi M.
    (1996) Expression of cadherin-11 delineates boundaries, neuromeres, and nuclei in the developing mouse brain. Dev. Dyn 206, 455–462
    OpenUrlCrossRefPubMedWeb of Science
    1. Knecht A. K.,
    2. Good P. J.,
    3. Dawid I. B.,
    4. Harland R. M.
    (1995) Dorsal-ventral patterning and differentiation of noggin-induced neural tissue in the absence of mesoderm. Development 121, 1927–1936
    OpenUrlAbstract
    1. Le Douarin N. M.
    (1984) Cell migrations in embryos. Cell 38, 353–366
    OpenUrlCrossRefPubMedWeb of Science
    1. Lee S. M. K.,
    2. Tole S.,
    3. Grove E.,
    4. McMahon A. P.
    (2000) A local Wnt-3a signal is required for development of mammalian hippocampus. Development 127, 457–467
    OpenUrlAbstract
    1. Maden M.,
    2. Horton C.,
    3. Graham A.,
    4. Leonard L.,
    5. Pizzey J.,
    6. Siegenthaler G.,
    7. Lumsden A.,
    8. Eriksson U.
    (1992) Domains of cellular retinoic acid-binding protein I (CRABP I) expression in the hindbrain and neural crest of the mouse embryo. Mech. Dev 37, 13–23
    OpenUrlCrossRefPubMedWeb of Science
    1. Mahmood R.,
    2. Bresnick J.,
    3. Hornbruch A.,
    4. Mahony C.,
    5. Morton N.,
    6. Colquhoun K.,
    7. Martin P.,
    8. Lumsden A.,
    9. Dickson C.,
    10. Mason I.
    (1995) A role for FGF-8 in the initiation and maintenance of vertebrate limb bud outgrowth. Curr. Biol 5, 797–806
    OpenUrlCrossRefPubMedWeb of Science
    1. Mallo M.
    (1997) Retinoic acid disturbs mouse middle ear development in a stage-specific fashion. Dev. Biol 184, 175–186
    OpenUrlCrossRefPubMedWeb of Science
    1. Mallo M.,
    2. Brändlin I.
    (1997) Segmental identity can change independently in the hindbrain and rhombencephalic neural crest. Dev. Dyn 210, 146–156
    OpenUrlCrossRefPubMedWeb of Science
    1. Mastick G. S.,
    2. Fan C. M.,
    3. Tessier-Lavigne M.,
    4. Serbedzija G. N.,
    5. McMahon A. P.,
    6. Easter S. E.
    (1996) Early deletion of neuromeres in Wnt/ mutant mice: Evaluation by morphological and molecular markers. J. Comp. Neurol 374, 246–258
    OpenUrlCrossRefPubMedWeb of Science
    1. McCrea P. D.,
    2. Turck C. W.,
    3. Gumbiner B. M.
    (1991) A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin. Science 254, 1359–1361
    OpenUrlAbstract/FREE Full Text
    1. McMahon A. P.,
    2. Bradley A.
    (1990) The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 62, 1073–1085
    OpenUrlCrossRefPubMedWeb of Science
    1. McMahon A. P.,
    2. Joyner A.,
    3. Bradley A.,
    4. McMahon J.
    (1992). The midbrain-hindbrain phenotype of Wnt-1-/Wnt-1- mice results from stepwise deletion of engrailed -expressing cells by 9.5 days postcoitum. Cell 69, 581–595
    OpenUrlCrossRefPubMedWeb of Science
    1. Millet S.,
    2. Bloch-Gallego E.,
    3. Simeone A.,
    4. Alvarado-Mallart R.-M.
    (1996) The caudal limit of Otx2 gene expression as a marker of the midbrain/hindbrain boundary: a study using in situ hybridization and chick/quail homotypic grafts. Development 122, 3785–3797
    OpenUrlAbstract
    1. Miller J. R.,
    2. Hocking A. M.,
    3. Brown J. D.,
    4. Moon R. T.
    (1999) Mechanism and function of signal transduction by the Wnt/-catenin and Wnt/Ca2+pathways. Oncogene 18, 7860–7872
    OpenUrlCrossRefPubMedWeb of Science
    1. Mitchell P. J.,
    2. Timmons P. M.,
    3. Hebert J. M.,
    4. Rigby P. W. J.,
    5. Tjian R.
    (1991) Transcription factor AP-2 is expressed in neural crest cell lineages during mouse embryogenesis. Genes Dev 5, 105–119
    OpenUrlAbstract/FREE Full Text
    1. Nagafuchi A.,
    2. Takeichi M.
    (1989) Transmembrane control of cadherin-mediated cell adhesion: a 94 kDa protein functionally associated with a specific region of the cytoplasmic domain of E-cadherin. Cell. Regul 1, 37–55
    OpenUrlPubMedWeb of Science
    1. Nagy A.,
    2. Rossant J.,
    3. Nagy R.,
    4. Abramow-Newerly W.,
    5. Roder J. C.
    (1993) Derivation of completely cell culture-derived mice from early passage embryonic stem cells. Proc. Natl. Acad. Sci. USA 90, 8424–8428
    OpenUrlAbstract/FREE Full Text
    1. Neidhardt L.,
    2. Gasca S.,
    3. Wertz K.,
    4. Obermayr F.,
    5. Worpenberg S.,
    6. Lehrach H.,
    7. Herrmann B. G.
    (2000) Large-scale screen for genes controlling mammalian embryogenesis, using high-throughput gene expression analysis in mouse embryos. Mech. Dev 98, 77–93
    OpenUrlCrossRefPubMedWeb of Science
    1. Nichols D. H.
    (1981) Neural crest formation in the head of the mouse embryo as observed using a new histological technique. J. Embryol. Morphol 64, 105–120
    OpenUrlPubMedWeb of Science
    1. Noden D. M.
    (1978) The control of avian cephalic neural crest cytodifferentiation. II. Neural tissues. Dev. Biol 67, 313–329
    OpenUrlCrossRefPubMedWeb of Science
    1. Ohuchi H.,
    2. Yoshioka H.,
    3. Tanaka A.,
    4. Kawakami Y.,
    5. Nohno T.,
    6. Noji S.
    (1994) Involvement of androgen-induced growth factor (FGF-8) gene in mouse embryogenesis and morphogenesis. Biochem. Biophys. Res. Comm 204, 882–888
    OpenUrlCrossRefPubMedWeb of Science
    1. Ozawa M.,
    2. Baribault H.,
    3. Kemler R.
    (1989) The cytoplasmic domain of the cell adhesion uvomorulin associates with three independent proteins structurally related in different species. EMBO J 8, 1711–1717
    OpenUrlPubMedWeb of Science
    1. Parr B. A.,
    2. Shea M. J.,
    3. Vassileva G.,
    4. McMahon A. P.
    (1993) Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 119, 247–261
    OpenUrlAbstract
    1. Pfaff S. L.,
    2. Mendelsohn M.,
    3. Stewart C. L.,
    4. Edlund T.,
    5. Jessell T. M.
    (1996) Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84, 309–320
    OpenUrlCrossRefPubMedWeb of Science
    1. Redies C.
    (1995) Cadherin expression in the developing vertebrate CNS: from neuromeres to brain nuclei and neural circuits. Exp. Cell Res 220, 243–256
    OpenUrlCrossRefPubMedWeb of Science
    1. Redies C.,
    2. Takeichi M.
    (1996) Cadherins in the developing centralnervous system: an adhesive code for segmental and functional subdivisions. Dev. Biol 180, 413–423
    OpenUrlCrossRefPubMedWeb of Science
    1. Redies C.
    (2000) Cadherins in the central nervous system. Prog. Neurobiol 61, 611–648
    OpenUrlCrossRefPubMedWeb of Science
    1. Redies C.,
    2. Ast M.,
    3. Nakagawa S.,
    4. Takeichi M.,
    5. Martinez-de-la-Torre M.,
    6. Puelles L.
    (2000) Morphologic fate of the diencephalic prosomeres and their subdivisions revealed by mapping cadherin expression. J. Comp. Neurol 421, 481–514
    OpenUrlCrossRefPubMedWeb of Science
    1. Rijli F. M.,
    2. Mark M.,
    3. Lakkaraju S.,
    4. Dierich A.,
    5. Dolle P.,
    6. Chambon P.
    (1993) A homeotic transformation is generated in the rostral branchial region of the head by disruption of Hoxa-2, which acts as a selector gene. Cell 75, 1333–1349
    OpenUrlCrossRefPubMedWeb of Science
    1. Rimm D. L.,
    2. Koslov E. R.,
    3. Kebriaei P.,
    4. Cianci C. D.,
    5. Morrow J. S.
    (1995) Alpha 1(E)-catenin is an actin-binding andbundling protein mediating the attachment of F-actin to the membrane adhesion complex. Proc. Natl. Acad. Sci. USA 92, 8813–8817
    OpenUrlAbstract/FREE Full Text
    1. Roelink H.,
    2. Nusse R.
    (1991) Expression of two members of the Wnt family during mouse development—restricted temporal and spatial patterns in the developing neural tube. Genes Dev 5, 381–388
    OpenUrlAbstract/FREE Full Text
    1. Salinas P. C.,
    2. Nusse R.
    (1992) Regional expression of the Wnt-3 gene in the developing mouse forebrain in relationship to diencephalic neuromeres. Mech. Dev 39, 151–160
    OpenUrlCrossRefPubMedWeb of Science
    1. Schorle H.,
    2. Meier P.,
    3. Buchert M.,
    4. Jaenisch R.,
    5. Mitchell P. J.
    (1996) Transcription factor AP-2 essential for cranial closure and craniofacial development. Nature 381, 235–238
    OpenUrlCrossRefPubMedWeb of Science
    1. Schwenk F.,
    2. Baron U.,
    3. Rajewsky K.
    (1995) A Cre -transgenic mouse strain for the ubiquitous deletion of loxP -flanked gene segments including deletion in germ cells. Nucleic Acids Res 23, 5080–5081
    OpenUrlFREE Full Text
    1. Serbedzija G. N.,
    2. Fraser S. E.,
    3. Bronner-Fraser M.
    (1990) Pathways of trunk neural crest migration in the mouse embryo as revealed by vital dye labelling. Development 108, 605–612
    OpenUrlAbstract/FREE Full Text
    1. Serbedzija G. N.,
    2. Bronner-Fraser M.,
    3. Fraser S. E.
    (1992) Vital dye analysis of cranial neural crest cell migration in the mouse embryo. Development 116, 297–307
    OpenUrlAbstract/FREE Full Text
    1. Serbedzija G. N.,
    2. Dickinson M.,
    3. McMahon A. P.
    (1996) Cell death in the CNS of the Wnt-1 mutant mouse. J. Neurobiol 31, 275–282
    OpenUrlCrossRefPubMed
    1. Shimamura K.,
    2. Takeichi M.
    (1992) Local and transient expression of E-cadherin involved in mouse embryonic brain morphogenesis. Development 116, 1011–1019
    OpenUrlAbstract/FREE Full Text
    1. Simeone A.,
    2. Acampora D.,
    3. Gulisano M.,
    4. Stornaiuolo A.,
    5. Boncinelli E.
    (1992) Nested expression domains of four homeobox genes in developing rostral brain. Nature 358, 687–690
    OpenUrlCrossRefPubMed
    1. Simeone A.,
    2. Acampora D.,
    3. Mallamaci A.,
    4. Stornaiuolo A.,
    5. D'Apice M.,
    6. Nigro V.,
    7. Boncinelli E.
    (1993) A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J 12, 2735–2747
    OpenUrlPubMedWeb of Science
    1. Sommer L.,
    2. Shah N.,
    3. Rao M.,
    4. Anderson D. J.
    (1995) The cellular function of MASH1 in autonomic neurogenesis. Neuron 15, 1245–1258
    OpenUrlCrossRefPubMedWeb of Science
    1. Stemple D. K.,
    2. Anderson D. J.
    (1992) Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71, 973–985
    OpenUrlCrossRefPubMedWeb of Science
    1. Stoner C. M.,
    2. Gudas L. J.
    (1989) Mouse cellular retinoic acid binding protein: cloning, complementary DNA sequence, and messenger RNA expression during the retinoic acid-induced differentiation of F9 wild-typeand RA-3-10 mutant teratocarcinoma cells. Cancer Res 49, 1497–1504
    OpenUrlAbstract/FREE Full Text
    1. Swiatek P. J.,
    2. Gridley T.
    (1993) Perinatal lethality and defects in hindbrain development in mice homozygous for a targeted mutation of the zinc finger gene Krox20. Genes Dev 7, 2071–2084
    OpenUrlAbstract/FREE Full Text
    1. Takada S.,
    2. Stark K. L.,
    3. Shea M. J.,
    4. Vassileva G.,
    5. McMahon J. A.,
    6. McMahon A. P.
    (1994) Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev 8, 174–189
    OpenUrlAbstract/FREE Full Text
    1. Tan S. S.,
    2. Morriss-Kay G. M.
    (1985) The development and distribution of the cranial neural crest in rat embryo. Cell Tissue Res 240, 403–416
    OpenUrlPubMedWeb of Science
    1. Tan S. S.,
    2. Morriss-Kay G. M.
    (1986) Analysis of cranial neural crest cell migration and early fates in postimplantation rat chimaeras. J. Embryol. Exp. Morphol 98, 21–58
    OpenUrlPubMedWeb of Science
    1. Tanaka A.,
    2. Miyamoto K.,
    3. Minamino N.,
    4. Takeda M.,
    5. Sato B.,
    6. Matsuo H.,
    7. Matsumoto K.
    (1992) Cloning and characterization of an androgen-induced growth factor essential for the androgen-dependent growth of mouse mammary carcinoma cells. Proc. Natl. Acad. Sci. USA 89, 8928–8932
    OpenUrlAbstract/FREE Full Text
    1. Thomas K. R.,
    2. Capecchi M. R.
    (1990) Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature 346, 847–850
    OpenUrlCrossRefPubMedWeb of Science
    1. Thomas K. R.,
    2. Musci T. S.,
    3. Neumann P. E.,
    4. Capecchi M. R.
    (1991) Swaying is a mutant allele of the proto-oncogene Wnt-1. Cell 67, 969–976
    OpenUrlCrossRefPubMedWeb of Science
    1. Vestweber D.,
    2. Kemler R.
    (1984) Some structural and functional aspects of the cell adhesion molecule uvomorulin. Cell Diff 15, 269–273
    OpenUrlCrossRefPubMed
    1. Wilkinson D. G.,
    2. Bailes J. A.,
    3. McMahon A. P.
    (1987) Expression of the proto-oncogene int-1 is restricted to specific neural cells in the developing mouse embryo. Cell 50, 79–88
    OpenUrlCrossRefPubMedWeb of Science
    1. Wurst W.,
    2. Auerbach A. B.,
    3. Joyner A. L.
    (1994) Multiple developmental defects in Engrailed-1 mutant mice: an early mid-hindbrain deletion and patterning defects in forelimbs and sternum. Development 120, 2065–2075
    OpenUrlAbstract
    1. Yamaguchi T. P.,
    2. Bradley A.,
    3. McMahon A. P.,
    4. Jones S.
    (1999) A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126, 1211–1223
    OpenUrlAbstract
    1. Zhang J.,
    2. Hagopian-Donaldson S.,
    3. Serbedzija G.,
    4. Elsemore J.,
    5. Plehn-Dujowich D.,
    6. McMahon A. P.,
    7. Flavell R. A.,
    8. Williams T.
    (1996) Neural tube, skeletal and body wall defects in mice lacking transcription factor AP-2. Nature 381, 238–241
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Inactivation of the (β)-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development
V. Brault, R. Moore, S. Kutsch, M. Ishibashi, D.H. Rowitch, A.P. McMahon, L. Sommer, O. Boussadia, R. Kemler
Development 2001 128: 1253-1264;
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The people behind the papers – George Britton and Aryeh Warmflash

George and Aryeh

First author George Britton and his supervisor Aryeh Warmflash discuss their new Development paper in which they apply advanced in vitro culturing techniques to investigate embryonic ectoderm patterning.

Travelling Fellowship – New imaging approach unveils a bigger picture

Highlights from Travelling Fellowship trips

Find out how Pamela Imperadore’s Travelling Fellowship grant from The Company of Biologists took her to Germany, where she used new imaging techniques to investigate the cellular machinery underlying octopus arm regeneration. Don’t miss the next application deadline for 2020 travel, coming up on 29 November. Where will your research take you?

Protein function can be controlled by light using optogenetic techniques. In their new Primer, Stefano De Renzis and his colleagues in Heidelberg provide an overview of the most commonly used optogenetic tools and their application in developmental biology.

preLights – Self-organised symmetry breaking in zebrafish reveals feedback from morphogenesis to pattern formation

Sundar Naganathan

preLighter Sundar Naganathan explains his selected preprint by Vikas Trivedi, Benjamin Steventon and their co-workers on pescoids, a new in vitro model system to study early zebrafish embryogenesis.

Spotlight – Can laboratory model systems instruct human limb regeneration?

An extract from a schematic demonstrating the possible pipeline for how discovery in lab model systems can influence applications for regenerative therapies.

One of the most challenging objectives of tissue regeneration research is regrowth of a lost or amputated limb. Here, Ben Cox, Maximina Yun and Kenneth Poss outline the research avenues yet to be explored to move closer to this capstone achievement.

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Tox4 modulates cell fate reprogramming

Lotte Vanheer, Juan Song, Natalie De Geest, Adrian Janiszewski, Irene Talon, Caterina Provenzano, Taeho Oh, Joel Chappell, Vincent Pasque
Journal of Cell Science

Drosophila melanogaster: a simple system for understanding complexity

Stephanie E. Mohr, Norbert Perrimon
Disease Models & Mechanisms