Advertisement
JOURNAL ARTICLES
Interactions between rhombomeres modulate Krox-20 and follistatin expression in the chick embryo hindbrain
A. Graham, A. Lumsden
Development 1996 122: 473-480;

Summary

The rhombomeres of the embryonic hindbrain display compartment properties, including cell lineage restriction, genetic definition and modular anatomical phenotype. Consistent with the idea that rhombomeres are autonomous developmental units, previous studies have shown that certain aspects of rhombomere phenotype are determined early, at the time of rhombomere formation. By contrast, the apoptotic depletion of neural crest from rhombomeres 3 and 5 is due to an interaction with their neighbouring rhombomeres, involving the signalling molecule Bmp4. In this paper, we have examined whether inter-rhombomere interactions control further aspects of rhombomere phenotype. We find that the expression of Krox-20 and the repression of follistatin in r3 is dependent upon neighbour interaction, whereas these genes are expressed autonomously in r5. We further demonstrate that modulation of Krox-20 and follistatin expression is not dependent on Bmp4, indicating the existence of multiple pathways of interaction between adjacent rhombomeres. We also show that, although some phenotypic aspects of r3 are controlled by neighbour interactions, the axial identity of the segment is intrinsically determined.

Reference

    1. Albano R. M.,
    2. Arkell R.,
    3. Beddington R. S. P.,
    4. Smith J. C.
    (1994) Expression of inhibin subunits and follistatin during postimplantation mouse development: decidual expression of activin and expression of follistatin in primitive streak, somites and hindbrain. Development 120, 803–813
    OpenUrlAbstract
    1. Birgbauer E.,
    2. Fraser S. E.
    (1994) Violation of cell lineage restriction compartments in the chick hindbrain. Development 120, 1347–1356
    OpenUrlAbstract
    1. Chavrier P.,
    2. Vesque C.,
    3. Galliot B.,
    4. Vigeron M.,
    5. Dolle. P.,
    6. Duboule D.,
    7. Charnay P.
    (1990). The segment-specific gene Krox-20 encodes a transcription factor with binding sites in the promoter of the Hox 1.4 gene. EMBO J 9, 1209–1218
    OpenUrlPubMedWeb of Science
    1. Cordes S. P.,
    2. Barsh G.
    (1994) The mouse segmentation gene kr encodes a novel basic domain-leucine zipper transcription factor. Cell 79, 1025–1034
    OpenUrlCrossRefPubMedWeb of Science
    1. Feijen A.,
    2. Goumans M. J.,
    3. van den Eijnden-van Raaij A. J. M.
    (1994) Expression of activin subunits, activin receptors and follistatin in postimplantation mouse embryos suggest specific developmental functions for different activins. Development 120, 3621–3637
    OpenUrlAbstract
    1. Fraser S. E.,
    2. Keynes R.,
    3. Lumsden A.
    (1990) Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions. Nature 344, 431–435
    OpenUrlCrossRefPubMed
    1. Frohman M. A.,
    2. Martin G. R.,
    3. Cordes S. P.,
    4. Halamek L. P.,
    5. Barsh G. S.
    (1993) Altered rhombomere-specific gene expression and hyoid bone differentiation in the mouse segmentation mutant, kreisler (kr). Development 117, 925–936
    OpenUrlAbstract
    1. Graham A.,
    2. Heyman I.,
    3. Lumsden A.
    (1993) Even-numbered rhombomeres control the apoptotic elimination of neural crest cells from odd-numbered rhombomeres in the chick hindbrain. Development 119, 233–245
    OpenUrlAbstract
    1. Graham A.,
    2. Francis-West P.,
    3. Brickell P.,
    4. Lumsden A.
    (1994) The signalling molecule Bmp4 mediates apoptosis in the rhombencephalic neural crest. Nature 372, 684–686
    OpenUrlCrossRefPubMed
    1. Guthrie S. C.,
    2. Muchamore I.,
    3. Marshall H.,
    4. Kuriowa A.,
    5. Krumlauf R.,
    6. Lumsden A.
    (1992). Neuroectodermal autonomy of Hox 2.9 expression revealed by rhombomere transpositions. Nature 356, 157–159
    OpenUrlCrossRefPubMed
    1. Hamburger V.,
    2. Hamilton H.
    (1951) A series of normal stages in the development of the chick embryo. J. Morph 88, 49–92
    OpenUrlCrossRefPubMedWeb of Science
    1. Hemmati-Brivanlou A.,
    2. Kelly O. G.,
    3. Melton D. A.
    (1994) follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralising activity. Cell 77, 283–295
    OpenUrlCrossRefPubMedWeb of Science
    1. Henrique D.,
    2. Adam J.,
    3. Myat A.,
    4. Chitnis A.,
    5. Lewis J.,
    6. Ish-Horowicz D.
    (1995) Expression of a Delta homologue in the prospective neurons in the chick. Nature 375, 787–790
    OpenUrlCrossRefPubMed
    1. Kuratani S. C.,
    2. Eichele G.
    (1993) Rhombomere transplantation repatterns the segmental organisation of the cranial nerves and reveals cell-autonomous expression of a homeodomain protein. Development, 117, 105–17
    OpenUrlAbstract/FREE Full Text
    1. Lumsden A.,
    2. Keynes R.
    (1989) Segmental patterns of neuronal development in the chick hindbrain. Nature 337, 424–428
    OpenUrlCrossRefPubMedWeb of Science
    1. Lumsden A.
    (1990) The cellular basis of segmentation in the developing hundbrain. Trends Neurosci 13, 329–335
    OpenUrlCrossRefPubMedWeb of Science
    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. McKay I. J.,
    2. Muchamore I.,
    3. Krumlauf R.,
    4. Maden M.,
    5. Lumsden A.,
    6. Lewis J.
    (1994) The kreisler mouse: a hindbrain segmentation mutant that lacks two rhombomeres. Development 120, 2199–2211
    OpenUrlAbstract
    1. Matzuk M. M.,
    2. Rajendra Kumar T.,
    3. Vassalli A.,
    4. Bickenbach J. R.,
    5. Roop D. R.,
    6. Jaenisch R.,
    7. Bradley A.
    (1995) Functional analysis of activins during mammalian development. Nature 374, 354–356
    OpenUrlCrossRefPubMed
    1. Matzuk M. M.,
    2. Lu N.,
    3. Vogel H.,
    4. Sellheyer K.,
    5. Roop D. R.,
    6. Bradley A.
    (1995) Multiple defects and perinatal death in mice deficient in follistatin. Nature 374, 360–363
    OpenUrlCrossRefPubMed
    1. Miyanaga K.,
    2. Shimasaki S.
    (1993) Structural and functional characterisation of the rat follistatin (activin binding protein) gene promoter. Mol. Cell. Endocrinol 92, 99–109
    OpenUrlCrossRefPubMedWeb of Science
    1. Nieto M. A.,
    2. Sechrist J.,
    3. Wilkinson D. G.,
    4. Bronner-Fraser M.
    (1995) Relationship between spatially restricted Krox-20 gene expression in branchial neural crest and segmentation in the chick embryo hindbrain. EMBO J 14, 1697–1710
    OpenUrlPubMedWeb of Science
    1. Patthy L.,
    2. Nikolics K.
    (1993) Functions of agrin and agrin related proteins. Trends Neurosci 13, 329–335
    1. Prince V.,
    2. Lumsden A.
    (1994) Hoxa-2 expression in normal and transposed rhombomeres: independent regulation in the neural tube and neural crest. Development, 120, 911–923
    OpenUrlAbstract
    1. Schneider-Maunoury S.,
    2. Topiko P.,
    3. Seitanidou T.,
    4. Levi G.,
    5. Cohen-Tannoudji M.,
    6. Pournin S.,
    7. Babinet C.,
    8. Charnay P.
    (1993) Disruption of Krox-20 results in the alteration of rhombomeres 3 and 5 in the developing hindbrain. Cell 75, 1199–1214
    OpenUrlCrossRefPubMedWeb of Science
    1. Sechrist J.,
    2. Serbedzija G.,
    3. Scherson T.,
    4. Fraser S.,
    5. Bronner-Fraser M.
    (1993) Segmental migration of the hindbrain neural crest does not arise from its segmental generation. Development 118, 691–703
    OpenUrlAbstract
    1. Shimasaki S.,
    2. Koga M.,
    3. Esch F.,
    4. Cooksey K.,
    5. Mercado M.,
    6. Koba A.,
    7. Ueno N.,
    8. Ying S. Y.,
    9. Ling N.,
    10. Guillemin R.
    (1988) Primary structure of the human follistatin precursor and its genomic organisation. Proc. Natl. Acad. Sci. USA 85, 4218–4222
    OpenUrlAbstract/FREE Full Text
    1. Shukovski L.,
    2. Dyson M.,
    3. Findlay J.
    (1993) The effects of follistatin, activin and inhibin on steroidogenesis by bovine thecal cells. Mol. Cell. Endocrinol 97, 19–27
    OpenUrlCrossRefPubMedWeb of Science
    1. Simon H.,
    2. Lumsden A.
    (1993) Rhombomere-specific origin of the contralateral vestibulo-acoustic efferent neurons and their migration across the embryonic midline. Neuron 11, 209–220
    OpenUrlCrossRefPubMedWeb of Science
    1. Simon H.,
    2. Hornbruch A.,
    3. Lumsden A.
    (1995) Independent assignment of antero-posterior and dorso-ventral positional values in the developing chick hindbrain. Current Biol 5, 205–214
    OpenUrlCrossRefPubMedWeb of Science
    1. Sundin O. H.,
    2. Eichele G.
    (1990) A homeo domain protein reveals the metameric nature of the developing chick hindbrain. Genes Dev 4, 1267–1276
    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 Krox-20. Genes Dev 7, 2071–2084
    OpenUrlAbstract/FREE Full Text
    1. Wilkinson D.G.,
    2. Bhatt S.,
    3. Cook M.,
    4. Boncinelli E.,
    5. Krumlauf R.
    (1989) Segmental expression of Hox-2 homeobox-containing genes in the developing mouse hindbrain. Nature 341, 405–409
    OpenUrlCrossRefPubMed
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Interactions between rhombomeres modulate Krox-20 and follistatin expression in the chick embryo hindbrain
A. Graham, A. Lumsden
Development 1996 122: 473-480;
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