Advertisement
JOURNAL ARTICLES
Equivalence in the genetic control of hindbrain segmentation in fish and mouse
C.B. Moens, S.P. Cordes, M.W. Giorgianni, G.S. Barsh, C.B. Kimmel
Development 1998 125: 381-391;

Summary

The vertebrate hindbrain is subdivided into a series of rhombomeres whose segmental organization serves to pattern the architecture and innervation of the developing head. The zebrafish gene valentino is required cell-autonomously in the development of rhombomeres 5 and 6, and valentino mutants lack visible hindbrain segmentation caudal to the r3/4 boundary (Moens, C. B., Yan, Y.-L., Appel, B., Force, A. G., and Kimmel, C. B. (1996) Development 122, 3981–3990). Here we show that valentino is the zebrafish homologue of the mouse segmentation gene kreisler, which encodes a bZip transcription factor. The valentino gene is expressed in a manner consistent with its proposed role in subdividing rhombomeres 5 and 6 from their common precursor ‘proto-segment’ in the presumptive hindbrain, a process that we also demonstrate is reflected in the normal order of appearance of rhombomere boundaries. As well as having similar phenotypes with respect to visible hindbrain segmentation and patterns of marker gene expression, valentino and kreisler mutants have similar pharyngeal arch and inner ear defects, consistent with a conserved role for this gene in hindbrain segmentation and in patterning of the head periphery.

REFERENCES

    1. Chandrasekhar A.,
    2. Moens C. B.,
    3. Warren J. T., Jr,
    4. Kimmel C. B.,
    5. Kuwada J. Y.
    (1997) Development of branchiomotor neurons in zebrafish. Development 124, 2633–2644
    OpenUrlAbstract
    1. Cordes S. P.,
    2. Barsh G. S.
    (1994) The mouse segmentation gene kr encodes a novel basic domain-leucine zipper transcription factor. Cell 79, 1025–1034
    OpenUrlCrossRefPubMedWeb of Science
    1. Cubbage C. C.,
    2. Mabee P. M.
    (1996) Development of the cranium and paired fins in the zebrafish Danio rerio (Ostariophysi, Cyprinidae). J. Morphol 229, 1–40
    OpenUrlCrossRef
    1. Deol M. S.
    (1964) The abnormalities of the inner ear in kreisler mice. J. Embryol. Exp. Morph 12, 475–490
    1. Detrich H. W.,
    2. Kieran M. W.,
    3. Chan F. Y.,
    4. Barone L. M.,
    5. Yee K.,
    6. Rundstadler J. A.,
    7. Pratt S.,
    8. Ranson D.,
    9. Zon L. I.
    (1995) Intraembryonic hematopoietic cell migration during vertebrate development. Proc. Natl. Acad. Sci. USA 92, 10713–10717
    OpenUrlAbstract/FREE Full Text
    1. Eichmann A.,
    2. Grapin-Botton A.,
    3. Kelly L.,
    4. Graf T.,
    5. Le Douarin N. M.,
    6. Sieweke M.
    (1997) The expression pattern of the mafB/kr gene in birds and mice reveals that the kreisler phenotype does not represent a null mutant. Mech. Dev 65, 111–122
    OpenUrlCrossRefPubMedWeb of Science
    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. 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. Gilland E.,
    2. Baker R.
    (1993) Conservation of neuroepithelial and mesodermal segments in the embryonic vertebrate head. Acta Anat 148, 110–123
    OpenUrlPubMedWeb of Science
    1. Goddard J. M.,
    2. Rossel. M.,
    3. Manley N. R.,
    4. Capecchi M. R.
    (1996) Mice with targeted disruption of Hoxb-1 fail to form the motor nucleus of the VIIth nerve. Development 122, 3217–3216
    OpenUrlAbstract
    1. Guthrie S.,
    2. Lumsden A.
    (1991) Formation and regeneration of rhombomere boundaries in the developing chick hindbrain. Development 112, 221–229
    OpenUrlAbstract
    1. Guthrie S.
    (1995) The status of the neural segment. Trends Neurosci 18, 74–79
    OpenUrlPubMedWeb of Science
    1. Hauptmann G.,
    2. Gerster T.
    (1994) Two-color whole-mount in situ hybridization to vertebrate and Drosophila embryos. Trends Genet 10, 266–267
    OpenUrlCrossRefPubMedWeb of Science
    1. Johnson S. L.,
    2. Gates M. A.,
    3. Johnson M.,
    4. Talbot W. S.,
    5. Horne S.,
    6. Baik K.,
    7. Rude S.,
    8. Wong J. R.,
    9. Postlethwait J. H.
    (1996) Centromere-linkage analysis and consolidation of the zebrafish genetic map. Genetics 142, 1277–1288
    OpenUrlAbstract/FREE Full Text
    1. Kataoka K.,
    2. Fujiwara K.-T.,
    3. Noda M.,
    4. Nishizawa M.
    (1994) MafB, a new Maf family transcription activator that can associate with Maf and Fos but not with Jun. Mol. Cell. Biol 14, 7581–7591
    OpenUrlAbstract/FREE Full Text
    1. Kerppola T. K.,
    2. Curran T.
    (1994) A conserved region adjacent to the basic domain is required for recognition of an extended DNA binding site by Maf/Nr1 family proteins. Oncogene 9, 3149–3158
    OpenUrlPubMedWeb of Science
    1. Kimmel C. B.,
    2. Ballard W. W.,
    3. Kimmel S. R.,
    4. Ullmann B.,
    5. Schilling T. F.
    (1995) Stages of embryonic development of the zebrafish. Dev. Dyn 203, 253–310
    OpenUrlPubMedWeb of Science
    1. Krumlauf R.
    (1994) Hox genes in vertebrate development. Cell 78, 191–201
    OpenUrlCrossRefPubMedWeb of Science
    1. Lumsden A.,
    2. Keynes R.
    (1989) Segmental patterns of neuronal development in the chick hindbrain. Nature 337, 424–428
    OpenUrlCrossRefPubMed
    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. Manzanares M.,
    2. Cordes S.,
    3. Kwan C.-T.,
    4. Sham M. H.,
    5. Barsh G. S.,
    6. Krumlauf R.
    (1997) Segmental regulation of Hoxb-3 by kreisler. Nature 387, 191–195
    OpenUrlCrossRefPubMed
    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. McKay I. J.,
    2. Lewis J.,
    3. Lumsden A.
    (1997) Organization and development of facial motor neurons in the Kreisler mutant mouse. Eur. J. Neurosci 9, 1499–1507
    OpenUrlCrossRefPubMedWeb of Science
    1. Moens C. B.,
    2. Yan Y.-L.,
    3. Appel B.,
    4. Force A. G.,
    5. Kimmel C. B.
    (1996) valentino: a zebrafish gene required for normal hindbrain segmentation. Development 122, 3981–3990
    OpenUrlAbstract
    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 hindbrain. EMBO J 14, 1697–1710
    OpenUrlPubMedWeb of Science
    1. Oxtoby E.,
    2. Jowett T.
    (1993) Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. Nucleic Acids Res 21, 1087–1095
    OpenUrlAbstract/FREE Full Text
    1. Postlethwait J. H.,
    2. Johnson S. L.,
    3. Midson C. N.,
    4. Talbot W. S.,
    5. Gates M.,
    6. Ballinger E. W.,
    7. Africa D.,
    8. Andrews R.,
    9. Carl T.,
    10. Eisen J. S.
    (1994) A genetic linkage map for the zebrafish. Science 264, 699–703
    OpenUrlAbstract/FREE Full Text
    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. Schilling T. F.,
    2. Kimmel C. B.
    (1994) Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 120, 483–494
    OpenUrlAbstract
    1. Schilling T. F.,
    2. Kimmel C. B.
    (1997) Musculoskeletal patterning in the pharyngeal segments of the zebrafish embryo. Development 124, 2945–2960
    OpenUrlAbstract
    1. Sieweke M. H.,
    2. Tekotte H.,
    3. Frampton J.,
    4. Graf T.
    (1996) MafB is an interaction partner and repressor of Ets-1 that inhibits erythroid differentiation. Cell 85, 49–60
    OpenUrlCrossRefPubMedWeb of Science
    1. Studer M.,
    2. Lumsden A.,
    3. Ariza-McNaughton L.,
    4. Bradley A.,
    5. Krumlauf R.
    (1996) Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384, 630–634
    OpenUrlCrossRefPubMed
    1. Yoon C.,
    2. Kawakami K.,
    3. Hopkins N.
    (1997) Zebrafish vasa homologue RNA is localized to the cleavage planes of 2-and 4-cell-stage embryos and is expressed in the primordial germ cells. Development 124, 3157–3166
    OpenUrlAbstract
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Equivalence in the genetic control of hindbrain segmentation in fish and mouse
C.B. Moens, S.P. Cordes, M.W. Giorgianni, G.S. Barsh, C.B. Kimmel
Development 1998 125: 381-391;
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