Advertisement
JOURNAL ARTICLES
Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo
H. Sasaki, B.L. Hogan
Development 1993 118: 47-59;

Summary

Four genes encoding fork-head-domain-containing proteins (FD genes) have been isolated from a mouse 8.5 days post coitum (p.c.) embryo cDNA library. Two are mouse homologues of rat HNF-3 beta and HNF-3 alpha. The other two are novel and have been named MF-1 and MF-2 (for mesoderm/mesenchyme fork head). Wholemount in situ hybridization of embryos between 6.5 and 9.5 days p. c. shows that each gene has a unique expression pattern. HNF-3 beta is expressed in the node, notochord, floor plate and gut, while HNF-3 alpha is mainly in the definitive endoderm and gut, but also in the floor plate of the midbrain. These results suggest that HNF-3 beta and HNF-3 alpha, in addition to their known functions as transcriptional activators in adult liver, play a role in body axis formation, neural tube patterning and definitive endoderm formation during gastrulation. MF-1 RNA is present in non-notochordal mesoderm, and in neural-crest-derived head mesenchyme, while MF-2 transcripts are found in the sclerotomes of the somites and in head mesenchyme, including that from neural crest. Studies on gastrulation stage embryos suggest that the early temporal and spatial patterns of HNF-3 beta, MF-1 and HNF-3 alpha correlate with populations of cells undergoing commitment to different developmental fates. A model is proposed linking FD gene expression with gastrulation events in the mouse.

Reference

    1. Blum M.,
    2. Gaunt S. J.,
    3. Cho K. Y.,
    4. Steinbeisser H.,
    5. Blumberg B.,
    6. Bittner D.,
    7. De Robertis E. M.
    (1992) Gastrulation in the mouse: the role of the homeobox gene goosecoid. Cell 69, 1097–1106
    OpenUrlCrossRefPubMedWeb of Science
    1. Blumberg B.,
    2. Wright C. V. E.,
    3. De Robertis E. M.,
    4. Cho K. W. Y.
    (1991) Organizer-specific homeobox genes in Xenopus laevis embryos. Science 253, 194–196
    OpenUrlAbstract/FREE Full Text
    1. Candia A. F.,
    2. Hu. J. C.,
    3. Crosby J.,
    4. Lalley P. A.,
    5. Noden D.,
    6. Nadeau J. H.,
    7. Wright C. V. E.
    (1992) Mox-1 and Mox-2 define a novel homeobox gene subfamily and are differentially expressed during early mesodermal patterning in mouse embryos. Development 116, 1123–1136
    OpenUrlAbstract/FREE Full Text
    1. Cunliffe V.,
    2. Smith J. C.
    (1992) Ectopic mesoderm formation in Xenopus embryos caused by widespread expression of a Brachyury homologue. Nature 358, 427–430
    OpenUrlCrossRefPubMed
    1. De Simone V.,
    2. de Magistris L.,
    3. Lazzaro D.,
    4. Gerstner J.,
    5. Monaci P.,
    6. Nicosia A.,
    7. Cortese R.
    (1991) LFB3. a heterodimer-forming homeoprotein of the LFB1 family, is expressed in specialized epithelia. EMBO J 10, 1435–1443
    OpenUrlPubMedWeb of Science
    1. Dirksen M. L.,
    2. Jamrich M.
    (1992) A novel, activin-inducible, blastopore lip-specific gene of Xenopus laevis contains a fork head DNA-binding domain. Genes Dev 6, 599–608
    OpenUrlAbstract/FREE Full Text
    1. Duprey P.,
    2. Chowdhurry K.,
    3. Dressler G. R.,
    4. Balling R.,
    5. Simon D.,
    6. Guenet J.-L.,
    7. Gruss P.
    (1998) A mouse gene homologous to the Drosophila gene caudal is expressed in epithelial cells from the embryonic intestine. Genes Dev 2, 1647–1654
    OpenUrl
    1. Fahrner K.,
    2. Hogan B. L. M.,
    3. Flavell R. A.
    (1987) Transcription of H-2 and Qa genes in embryonic and adult mice. EMBO J 6, 1265–1271
    OpenUrlPubMed
    1. Frumkin A.,
    2. Rangini Z.,
    3. Ben-Yehuda A.,
    4. Gruenbaum Y.,
    5. Fainsod A.
    (1991) A chicken caudal homologue, CHox-cad, is expressed in the epiblast with posterior localization and in the early endodermal lineage. Development 112, 207–219
    OpenUrlAbstract
    1. Garcia-Martinez V.,
    2. Schoenwolf G. C.
    (1992) Positional control of mesoderm and fate during avian gastrulation and neurulation. Dev. Dynamics 193, 249–256
    OpenUrlPubMedWeb of Science
    1. Grossinklaus U.,
    2. Pearson R. K.,
    3. Gehring W. J.
    (1992) The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes Dev 6, 1030–1051
    OpenUrlAbstract/FREE Full Text
    1. Häcker U.,
    2. Grossinklaus U.,
    3. Gehring W. J.,
    4. Jäckle H.
    (1992) Developmentally regulated Drosophila gene family encoding the fork head domain. Proc. Natl. Acad. Sci.USA 89, 8754–8758
    OpenUrlAbstract/FREE Full Text
    1. Hatta K.
    (1992) Role of the floor plate in axonal patterning in the Zebrafish CNS. Neuron 9, 629–642
    OpenUrlCrossRefPubMedWeb of Science
    1. Hatta K.,
    2. Kimmel C. B.,
    3. Ho R. K.,
    4. Walker C.
    (1991) The cyclops mutation blocks specification of the floor plate of the zebrafish central nervous system. Nature 350, 339–341
    OpenUrlCrossRefPubMed
    1. Herrmann B. G.
    (1991) Expression pattern of the Brachyury gene in whole-mount Twis/Twis mutant embryos. Development 113, 913–917
    OpenUrlAbstract
    1. Kimelman D.,
    2. Christian J. L.,
    3. Moon R. T.
    (1992) Synergistic principles of development: overlapping patterning systems in Xenopus mesoderm induction. Development 116, 1–9
    OpenUrlAbstract
    1. Knöchel S.,
    2. Lef J.,
    3. Clement J.,
    4. Klocke B.,
    5. Hille S.,
    6. Köster M.,
    7. Knöchel W.
    (1992) Activin A induced expression of a fork head related gene in posterior chordamesoderm (notochord) of Xenopus embryos. Mech. Dev 38, 157–165
    OpenUrlCrossRefPubMedWeb of Science
    1. Lai E.,
    2. Prezioso V. R.,
    3. Smith E.,
    4. Livitin H.,
    5. Costa R. H.,
    6. Darnel J. E.
    (1990) HNF-, A hepatocyte-enriched transcription factor of novel structure is regulated transcriptionally. Genes Dev 4, 1427–1436
    OpenUrlAbstract/FREE Full Text
    1. Lai E.,
    2. Prezioso V. R.,
    3. Tao W.,
    4. Chen W. S.,
    5. Darnel J. E.
    (1991) Hepatocyte nuclear factor 3belongs to a gene family in mammals that is homologous to the Drosophila homeotic gene fork head. Genes Dev 5, 416–427
    OpenUrlAbstract/FREE Full Text
    1. Landshulz W. H.,
    2. Johnson P. E.,
    3. McKnight S. L.
    (1988) The Leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science 240, 1759–1764
    OpenUrlAbstract/FREE Full Text
    1. Lawson K. A.,
    2. Meneses J. J.,
    3. Pederson R. A.
    (1991) Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 113, 891–991
    OpenUrlAbstract
    1. Li C.,
    2. Lai C.,
    3. Sigman D. S.,
    4. Gaynor R. B.
    (1991) Cloning of a cellular factor, interleukin binding factor, that binds to NFAT like motifs in the human immunodeficiency virus long terminal repeat. Proc. Natl. Acad. Sci. USA 88, 7739–7743
    OpenUrlAbstract/FREE Full Text
    1. Lumsden A.,
    2. Sprawson N.,
    3. Graham A.
    (1991) Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development 113, 1281–1291
    OpenUrlAbstract
    1. McGinnis W.,
    2. Krumlauf R.
    (1992) Homeobox genes and axial patterning. Cell 68, 283–302
    OpenUrlCrossRefPubMedWeb of Science
    1. Murre C.,
    2. McCaw P. S.,
    3. Baltimore D.
    (1989) A new DNA binding and dimerization motif in immunoglobin enhancer binding, daughterless, MyoD and myc proteins. Cell 56, 777–783
    OpenUrlCrossRefPubMedWeb of Science
    1. Nieto M. A.,
    2. Bennett M. F.,
    3. Sargent M. G.,
    4. Wilkinson D. G.
    (1992) Cloning and developmental expression of Sna, a murine homologue of the Drosophila snail gene. Development 116, 227–237
    OpenUrlAbstract
    1. Niswander L.,
    2. Martin G. R.
    (1992) Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 114, 755–768
    OpenUrlAbstract
    1. Ott M.-O.,
    2. Bober E.,
    3. Lyons G.,
    4. Arnold H.,
    5. Buckingham M.
    (1991) Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 111, 1097–1107
    OpenUrlAbstract/FREE Full Text
    1. Placzek M.,
    2. Tessier-Lavigne M.,
    3. Yamada T.,
    4. Jessel T.,
    5. Dodd J.
    (1990) Mesodermal control of neural cell identity: floor plate induction by notochord. Science 250, 985–988
    OpenUrlAbstract/FREE Full Text
    1. Ruiz i Altaba A.,
    2. Jessel T. M.
    (1992) Pintallavis, a gene expressed in the organizer and midline cells of frog embryos: involvement in the development of the neural axis. Development 116, 81–93
    OpenUrlAbstract
    1. Sassoon D.,
    2. Lyons G.,
    3. Wright W. E.,
    4. Lin V.,
    5. Lasser A.,
    6. Weintraub H.,
    7. Buckingham M.
    (1989) Expression of two myogenic regulatory factors myogenin and MyoD1 during mouse embryogenesis. Nature 341, 303–307
    OpenUrlCrossRefPubMed
    1. Schoenwolf G. C.,
    2. Garcia-Martinetz V.,
    3. Dias M. S.
    (1992) Mesoderm movement and fate during avian gastrulation and neurulation. Dev. Dynamics 193, 235–248
    OpenUrlPubMedWeb of Science
    1. Selleck M. A. J.,
    2. Stern C. D.
    (1991) Fate mapping and cell lineage analysis of Hensen's node in the chick embryo. Development 112, 615–626
    OpenUrlAbstract
    1. Selleck M. A. J.,
    2. Stern C. D.
    (1991) Commitment of mesoderm cells in Hensen's node of the chick embryo to notochord and somite. Development 114, 403–415
    OpenUrl
    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. Sive H. L.,
    2. Hattori K.,
    3. Weintraub H.
    (1989) Progressive determination during formation of the anteroposterior axis in Xenopus laevis. Cell 58, 171–180
    OpenUrlCrossRefPubMedWeb of Science
    1. Slack J. M. W.,
    2. Tannahill D.
    (1992) Mechanism of antero posterior axis specification in vertebrates. Lessons from the amphibians. Development 114, 285–302
    OpenUrlAbstract
    1. Smith W. C.,
    2. Harland R. M.
    (1992) Expression cloning of noggin, a new dorsalizing factor localized to the Spemann Organizer in Xenopus embryos. Cell 70, 829–840
    OpenUrlCrossRefPubMedWeb of Science
    1. Taira M.,
    2. Jamrich M.,
    3. Good P. J.,
    4. David I.
    (1992) The LIM domain-containing homeobox gene Xlim-1 is expressed specifically in the organizer region of Xenopus gastrula embryos. Genes Dev 6, 356–366
    OpenUrlAbstract/FREE Full Text
    1. Tao W.,
    2. Lai E.
    (1992) Telencephalon-restricted expression of BF-1, a new member of the HNF-3/ fork head gene family, in the developing rat brain. Neuron 8, 957–966
    OpenUrlCrossRefPubMedWeb of Science
    1. Weigel D.,
    2. Jäckle H.
    (1990) The fork head domain: a novel DNA binding motif of eukaryotic transcription factors?. Cell 63, 455–456
    OpenUrlCrossRefPubMedWeb of Science
    1. Weigel D.,
    2. Jurgens G.,
    3. Kutter F.,
    4. Seifert E.,
    5. Jäckle H.
    (1989) The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell 57, 645–658
    OpenUrlCrossRefPubMedWeb of Science
    1. Wilkinson D. G.,
    2. Bhatt S.,
    3. Herrmann B. G.
    (1990) Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 343, 657–659
    OpenUrlCrossRefPubMedWeb of Science
    1. Wolf C.,
    2. Thisse C.,
    3. Stoetzel C.,
    4. Thisse B.,
    5. Gerlinger P.,
    6. Perrin-Schmitt F.
    (1991) The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and the Drosophila twist genes. Dev. Biol 143, 363–373
    OpenUrlCrossRefPubMedWeb of Science
    1. Wright C. V. E.,
    2. Schnegelsberg P.,
    3. De Robertis E. M.
    (1988) XlHbox 8: a novel Xenopus homeo protein restricted to a narrow band of endoderm. Development 104, 787–794
    OpenUrl
    1. Xi H.,
    2. Rosenfeld M. G.
    (1991) Mechanism of complex transcriptional regulation: implications for brain development. Neuron 7, 183–196
    OpenUrlCrossRefPubMedWeb of Science
    1. Yamada T.,
    2. Placzek M.,
    3. Tanaka H.,
    4. Dodd J.,
    5. Jessel T. M.
    (1991) Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord. Cell 64, 635–647
    OpenUrlCrossRefPubMedWeb of Science
    1. Yokouchi Y.,
    2. Ohsugi K.,
    3. Sasaki H.,
    4. Kuroiwa A.
    (1991) Chicken homeobox gene Msx-1: structure, expression in limb buds and effect of retinoic acid. Development 113, 431–444
    OpenUrlAbstract
    1. Zhou X.,
    2. Sasaki H.,
    3. Lowe L.,
    4. Hogan B. L. M.,
    5. Kuehn M. R.
    (1993) Nodal, a novel TGF--like gene expressed in the mouse node during gastrulation. Nature 361, 543–547
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo
H. Sasaki, B.L. Hogan
Development 1993 118: 47-59;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

Kathryn Virginia Anderson (1952-2020)

Developmental geneticist Kathryn Anderson passed away at home on 30 November 2020. Tamara Caspary, a former postdoc and friend, remembers Kathryn and her remarkable contribution to developmental biology.

Zooming into 2021

In a new Editorial, Editor-in-Chief James Briscoe and Executive Editor Katherine Brown reflect on the triumphs and tribulations of the last 12 months, and look towards a hopefully calmer and more predictable year.

Read & Publish participation extends worldwide

Over 60 institutions in 12 countries are now participating in our Read & Publish initiative. Here, James Briscoe explains what this means for his institution, The Francis Crick Institute. Find out more and view our full list of participating institutions.

Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Sign up to join our next session:

10 February
Time: 13:00 (GMT)
Chaired by: preLights