Advertisement
JOURNAL ARTICLES
Regulation of dorsal-ventral patterning: the ventralizing effects of the novel Xenopus homeobox gene Vox
J.E. Schmidt, G. von Dassow, D. Kimelman
Development 1996 122: 1711-1721;

Summary

The formation of the dorsal-ventral axis in Xenopus laevis is elicited by a signaling cascade on the dorsal side of the embryo initiated by cortical rotation. These early developmental events impart an initial axial polarity to the embryo. By the time gastrulation occurs, the embryo has established opposing dorsal and ventral regulatory regions. Through a dynamic process, the embryo acquires a definitive pattern that reflects the distribution of future cell fates. Here we present a novel homeobox gene, Vox, whose expression reflects this dynamic process. Vox is first expressed throughout the embryo and subsequently eliminated from the notochord and neural plate. Ectopic expression of Vox demonstrates that the normal function of this gene may be to suppress dorsal genes such as Xnot and chordin, and induce ventral and paraxial genes such as Bmp-4 and MyoD. Ectopic expression of BMP-4 ventralizes embryos and positively regulates the expression of Vox, suggesting that these genes are components of a reciprocal regulatory network.

Reference

    1. Blitz I. L.,
    2. Cho K. W. Y.
    (1995) Anterior neurectoderm is progressively induced during gastrulation: the role of the Xenopus homeobox gene orthodenticle. Development 121, 993–1004
    OpenUrlAbstract
    1. Bober E.,
    2. Baum C.,
    3. Braun T.,
    4. Arnold H. H.
    (1994) A novel NK-related mouse homeobox gene: expression in central and peripheral nervous structures during embryonic development. Dev. Biol 162, 288–303
    OpenUrlCrossRefPubMedWeb of Science
    1. Cho K. W. Y.,
    2. Blumberg B.,
    3. Steinbeisser H.,
    4. De Robertis E. M.
    (1991) Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. Cell 67, 1111–1120
    OpenUrlCrossRefPubMedWeb of Science
    1. Christian J. L.,
    2. McMahon J. A.,
    3. McMahon A. P.,
    4. Moon R. T.
    (1991) Xwnt - 8, a XenopusWnt −1/ int −1-related gene responsive to mesoderm inducing factors, may play a role in ventral mesodermal patterning during embryogenesis. Development 111, 1045–56
    OpenUrlAbstract/FREE Full Text
    1. Cornell R. A.,
    2. Kimelman D.
    (1994) Activin-mediated mesoderm induction requires FGF. Development 120, 453–462
    OpenUrlAbstract
    1. Dale L.,
    2. Howes G.,
    3. Price B. M. J.,
    4. Smith J. C.
    (1992) Bonemorphogenetic protein 4: a ventralizing factor in early Xenopus development. Development 115, 573–585
    OpenUrlAbstract
    1. Fainsod A.,
    2. Steinbeisser H.,
    3. De Robertis E. M.
    (1994) On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo. EMBOJ 13, 5015–5025
    OpenUrlPubMedWeb of Science
    1. Frank D.,
    2. Harland R. M.
    (1991) Transient expression of XMyoD in non-somite mesoderm of Xenopus gastrulae. Development 113, 1387–1393
    OpenUrlAbstract
    1. Frasch M.,
    2. Hoey T.,
    3. Rushlow C.,
    4. Doyle H.,
    5. Levine M.
    (1987) Characterization and localization of the even-skipped protein of Drosophila. EMBO J 6, 749–759
    OpenUrlPubMedWeb of Science
    1. Gawantka V.,
    2. Delius H.,
    3. Hirschfeld K.,
    4. Blumenstock C.,
    5. Niehrs C.
    (1995) Antagonizing the Spemann organizer: role of the homeobox gene Xvent-1. EMBOJ 14, 6268–6279
    OpenUrlPubMedWeb of Science
    1. Gont L. K.,
    2. Steinbesser H.,
    3. Blumberg B.,
    4. DeRobertis E. M.
    (1993) Tail formation as a continuation of gastrulation: the multiple cell populations of the Xenopus tailbud derive from the late blastopore lip. Development 119, 991–1004
    OpenUrlAbstract/FREE Full Text
    1. Graff J. M.,
    2. Thies R. S.,
    3. Song J. J.,
    4. Celeste A. J.,
    5. Melton D. A.
    (1994) Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo. Cell 79, 169–179
    OpenUrlCrossRefPubMedWeb of Science
    1. Harvey R. P.
    (1990) The Xenopus MyoD gene: an unlocalised maternal mRNA predates lineage-restricted expression in the early embryo. Development 108, 669–680
    OpenUrlAbstract/FREE Full Text
    1. Jones C. M.,
    2. Kuehn M. R.,
    3. Hogan B. L. M.,
    4. Smith J. C.,
    5. Wright C. V. E.
    (1995) Nodal-related signals induce axial mesoderm and dorsalize mesoderm during gastrulation. Development 121, 3651–3662
    OpenUrlAbstract
    1. Jones C. M.,
    2. Lyons K. M.,
    3. Lapan P. M.,
    4. Wright C. V. E.,
    5. Hogan B. L. M.
    (1992) DVR-4 (bone morphogenetic protein-4) as a posterior ventralizing factor in Xenopus mesoderm induction. Development 115, 639–647
    OpenUrlAbstract
    1. Kao K. R.,
    2. Elinson R. P.
    (1988) The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos. Dev. Biol 127, 64–77
    OpenUrlCrossRefPubMedWeb of Science
    1. Kessler D. S.,
    2. Melton D. A.
    (1994) Vertebrate embryonic induction: mesodermal and neural patterning. Science 266, 596–604
    OpenUrlAbstract/FREE Full Text
    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. Kintner C. R.,
    2. Melton D. A.
    (1987) Expression of Xenopus N-CAM RNA in ectoderm is an early response to neural induction. Development 99, 311–.
    OpenUrlAbstract
    1. Kissinger C. R.,
    2. Liu B.,
    3. Martin-Blanco E.,
    4. Kornebrg T. B.,
    5. Pabo C. O.
    (1990). Crystal structure of an engrailed homeodomain-DNA complex at 2.8 A resolution: a framework for understanding homeodomain-DNA interactions. Cell 63, 579–590
    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. Kobel H. R.,
    2. DuPasquier L.
    (1986) Genetics of polyploid Xenopus. Trends Genet 2, 310–315
    OpenUrlCrossRefWeb of Science
    1. Lemaire P.,
    2. Garrett N.,
    3. Gurdon J. B.
    (1995) Expression cloning of Siamois, a Xenopus homeobox gene expressed in dorsal-vegetal cells of blastulae and able to induce a complete secondary axis. Cell 81, 85–94
    OpenUrlCrossRefPubMedWeb of Science
    1. MacDonald P. M.,
    2. Ingham P.,
    3. Struhl G.
    (1986) Isolation, structure and expression of even-skipped: a second pair-rule gene of Drosophila containing a homeobox. Cell 47, 721–734
    OpenUrlCrossRefPubMedWeb of Science
    1. Melton D. A.,
    2. Krieg P. A.,
    3. Rebagliati M. R.,
    4. Maniatis T.,
    5. Zinn K.,
    6. Green M. R.
    (1984) Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucl. Acids Res 12, 7035–7056
    OpenUrlAbstract/FREE Full Text
    1. Newport J.,
    2. Kirschner M. W.
    (1982) A major developmental transition in early Xenopus embryos. I. Characterization and timing of cellular changes at the midblastula stage. Cell 30, 675–686
    OpenUrlCrossRefPubMedWeb of Science
    1. Northrop J.,
    2. Kimelman D.
    (1994) Dorsal-ventral differences in response to FGF mediated induction in Xenopus. Dev. Biol 161, 490–503
    OpenUrlCrossRefPubMedWeb of Science
    1. Pannese M.,
    2. Polo C.,
    3. Andreazzoli M.,
    4. Vignali R.,
    5. Kablar B.,
    6. Barsacchi G.,
    7. Boncinelli E.
    (1995) The Xenopus homologue of Otx2 is a maternal homeobox gene that demarcates and specifies anterior body regions. Development 121, 707–720
    OpenUrlAbstract
    1. Ruiz i Altaba A.,
    2. Melton D. A.
    (1989) Bimodal and graded expression of the Xenopus homeobox gene Xhox3 during embryonic development. Development 106, 173–83
    OpenUrlAbstract
    1. Ruiz i Altaba A.,
    2. Melton D. A.
    (1989) Involvement of the Xenopus homeobox gene Xhox3 in patterning the anterior-posterior axis. Cell 57, 317–26
    OpenUrlCrossRefPubMedWeb of Science
    1. Rupp R. A.,
    2. Weintraub H.
    (1991) Ubiquitous MyoD transcription at the midblastula transition precedes induction-dependent MyoD expression in presumptive mesoderm of X. laevis. Cell 65, 927–37
    OpenUrlCrossRefPubMedWeb of Science
    1. Sasai Y.,
    2. Lu B.,
    3. Steinbesser H.,
    4. DeRobertis E. M.
    (1995) Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus. Nature 376, 333–336
    OpenUrlCrossRefPubMed
    1. Sasai Y.,
    2. Lu B.,
    3. Steinbesser H.,
    4. Geissert D.,
    5. Gont L. K.,
    6. DeRobertis E. M.
    (1994) Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 79, 779–790
    OpenUrlCrossRefPubMedWeb of Science
    1. Schmidt J. E.,
    2. Suzuki A.,
    3. Ueno N.,
    4. Kimelman D.
    (1995) Localized BMP-4 mediates dorsal-ventral patterning in the early Xenopus embryo. Dev. Biol 169, 37–50
    OpenUrlCrossRefPubMedWeb of Science
    1. Sive H. L.
    (1993) The frog prince-cess: A molecular formula for dorsoventral patterning in Xenopus. Genes Dev 7, 1–12
    OpenUrlFREE Full Text
    1. Slack J. M. W.
    (1994) Inducing factors in Xenopus early embryos. Current Biology 4, 116–126
    OpenUrlCrossRefPubMedWeb of Science
    1. Smith J. C.,
    2. Price B. M. J.,
    3. Green J. B. A.,
    4. Weigel D.,
    5. Herrmann B. G.
    (1991) Expression of a Xenopus homolog of brachyury (T) is an immediate-early response to mesoderm induction. Cell 67, 79–87
    OpenUrlCrossRefPubMedWeb of Science
    1. Smith W. C.,
    2. Harland R. M.
    (1992) Expression cloning of noggin, a new dorsalizing factor localized in the Spemann organizer in Xenopus embryos. Cell 70, 829–840
    OpenUrlCrossRefPubMedWeb of Science
    1. Smith W. C.,
    2. McKendry R.,
    3. Sibisi S. Jr..,
    4. Harland R. M.
    (1995) A nodal -related gene defines a physical and functional domain with the Spemann organizer. Cell 82, 37–46
    OpenUrlCrossRefPubMedWeb of Science
    1. Steinbeisser H.,
    2. Fainsod A.,
    3. Niehrs C.,
    4. Sasai Y.,
    5. De Robertis e. M.
    (1995) The role of gsc and BMP-4 in dorsal-ventral patterning of the marginal zone in Xenopus: a loss-of-function study using antisense RNA. EMBO J 14, 5230–5243
    OpenUrlPubMedWeb of Science
    1. Suzuki A.,
    2. Thies R. S.,
    3. Yamaji N.,
    4. Song J. J.,
    5. Wozney J. M.,
    6. Murakami K.,
    7. Ueno N.
    (1994) A truncated bone morphogenetic protein receptor affects dorsal-ventral patterning in the early Xenopus embryo. Proc. Natl. Acad. Sci. USA 91, 10255–10259
    OpenUrlAbstract/FREE Full Text
    1. Talbot W. S.,
    2. Trevarrow B.,
    3. Halpern M. E.,
    4. Melby A. E.,
    5. Farr G.,
    6. Postlethwait J. H.,
    7. Jowett T.,
    8. Kimmel C. B.,
    9. Kimelman D.
    (1995) A homeobox gene essential for zebrafish notochord development. Nature 378, 150–157
    OpenUrlCrossRefPubMedWeb of Science
    1. Tan D. P.,
    2. Ferrante J.,
    3. Nazarali A.,
    4. Shao X.,
    5. Kozak C. A.,
    6. Guo V.,
    7. Nirenberg M.
    (1992). Murine Hox-1.11 homeobox gene structure and expression. Proc. Natl. Acad. Sci.USA 89, 6280–6284
    OpenUrlAbstract/FREE Full Text
    1. Turner D. L.,
    2. Weintraub H.
    (1994) Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev 8, 1434–1447
    OpenUrlAbstract/FREE Full Text
    1. von Bubnoff A.,
    2. Schmidt J. E.,
    3. Kimelman D.
    (1996) The Xenopus laevis homeobox gene Xgbx-2 is an early marker of anteroposterior patterning in the ectoderm. Mech. Dev 54, 149–160
    OpenUrlCrossRefPubMedWeb of Science
    1. von Dassow G.,
    2. Schmidt J. E.,
    3. Kimelman D.
    (1993) Induction of the Xenopus organizer: expression and regulation of Xnot, a novel FGF and activin-regulated homeobox gene. Genes Dev 7, 355–366
    OpenUrlAbstract/FREE Full Text
    1. Papalopulu N.,
    2. Kintner C.
    (1996) A Xenopus gene, Xbr-1, defines a novel class of homeobox genes and is expressed in the dorsal ciliary margin of the eye. Dev. Biol 174, 104–114
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Regulation of dorsal-ventral patterning: the ventralizing effects of the novel Xenopus homeobox gene Vox
J.E. Schmidt, G. von Dassow, D. Kimelman
Development 1996 122: 1711-1721;
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

An interview with Swathi Arur

Swathi Arur joined the team at Development as an Academic Editor in 2020. Her lab uses multidisciplinary approaches to understand female germline development and fertility. We met with her over Zoom to hear more about her life, her career and her love for C. elegans.

Jim Wells and Hanna Mikkola join our team of Editors

We are pleased to welcome James (Jim) Wells and Hanna Mikkola to our team of Editors. Jim joins us a new Academic Editor, taking over from Gordan Keller, and Hanna joins our team of Associate Editors. Find out more about their research interests and areas of expertise.

New funding scheme supports sustainable events

As part of our Sustainable Conferencing Initiative, we are pleased to announce funding for organisers that seek to reduce the environmental footprint of their event. The next deadline to apply for a Scientific Meeting grant is 26 March 2021.

Read & Publish participation continues to grow

“I’d heard of Read & Publish deals and knew that many universities, including mine, had signed up to them but I had not previously understood the benefits that these deals bring to authors who work at those universities.”

Professor Sally Lowell (University of Edinburgh) shares her experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 150 institutions in 15 countries and four library consortia taking part – 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. Here, Brandon Carpenter talks about how inherited histone methylation defines the germline versus soma decision in C. elegans. 

Sign up to join our next session:

10 March
Time: TBC
Chaired by: Thomas Lecuit