Advertisement
JOURNAL ARTICLES
BMP-7 influences pattern and growth of the developing hindbrain of mouse embryos
R. Arkell, R.S. Beddington
Development 1997 124: 1-12;

Summary

The expression pattern of bone morphogenetic protein-7 (BMP-7) in the hindbrain region of the headfold and early somite stage developing mouse embryo suggests a role for BMP-7 in the patterning of this part of the cranial CNS. In chick embryos it is thought that BMP-7 is one of the secreted molecules which mediates the dorsalizing influence of surface ectoderm on the neural tube, and mouse surface ectoderm has been shown to have a similar dorsalizing effect. While we confirm that BMP-7 is expressed in the surface ectoderm of mouse embryos at the appropriate time to dorsalize the neural tube, we also show that at early stages of hindbrain development BMP-7 transcripts are present in paraxial and ventral tissues, within and surrounding the hindbrain neurectoderm, and only later does expression become restricted to a dorsal domain. To determine more directly the effect that BMP-7 may have on the developing hindbrain we have grafted COS cells expressing BMP-7 into the ventrolateral mesoderm abutting the neurectoderm in order to prolong BMP-7 expression in the vicinity of ventral hindbrain. Three distinct actvities of BMP-7 are apparent. Firstly, as expected from previous work in chick, BMP-7 can promote dorsal characteristics in the neural tube. Secondly, we show that it can also attenuate the expression of sonic hedgehog (Shh) in the floorplate without affecting Shh expression in the notochord. Finally, we find that ectopic BMP-7 appears to promote growth of the neurectoderm. These findings are discussed with respect to possible timing mechanisms necessary for the coordination of hindbrain dorsoventral patterning.

REFERENCES

    1. Albano R.M.,
    2. Groome N.,
    3. Smith J.C.
    (1993) Activins are expressed in preimplantation mouse embryos and in ES and EC cells and are regulated on their differentiation. Development 117711–723
    OpenUrlAbstract
    1. Andrews P.W.,
    2. Damjanov I.,
    3. Berends J.,
    4. Kumpf S.,
    5. Zappavigna V.,
    6. Mavilio F.,
    7. Sampath K.
    (1994) Inhibition of proliferation and induction of differentiation of pluripotent human embryonal carcinoma cells by osteogenic protein-1 (or bone morphogenetic protein-7). Lab. Invest 71, 243–251
    OpenUrlPubMedWeb of Science
    1. Ang S.-L.,
    2. Rossant J.
    (1994) HNF-3 is essential for node and notochord formation in mouse development. Cell 78, 561–574
    OpenUrlCrossRefPubMedWeb of Science
    1. Artinger K.B.,
    2. Bronner-Fraser M.
    (1992) Notochord grafts do not suppress formation of neural crest cells or commissural neurons. Development 116, 877–886
    OpenUrlAbstract/FREE Full Text
    1. Basler K.,
    2. Edlund T.,
    3. Jessell T.M.,
    4. Yamada T.
    (1993) Control of cell pattern in the neural tube: regulation of cell differentiation by dorsalin-1, a novel TGFβ family member. Cell 73, 687–702
    OpenUrlCrossRefPubMedWeb of Science
    1. Chan W.Y.,
    2. Tam P.P.L.
    (1988) A morphological and experimental study of the mesencephalic neural crest cells in the mouse embryo using wheat germ agglutinin-gold conjugate as the cell marker. Development 102, 427–442
    OpenUrlAbstract
    1. Chen P.,
    2. Vukicevic S.,
    3. Sampath T.K.,
    4. Luyten F.P.
    (1995) Osteogenicprotein-1 promotes growth and maturation of chick sternal chondrocytes in serum-free cultures. J. Cell Sci 108, 105–114
    OpenUrlAbstract/FREE Full Text
    1. Clarke J.D.W.,
    2. Holder N.,
    3. Soffe S.R.,
    4. Storm-Mathisen J.
    (1991) Neuroanatomical and functional analysis of neural tube formation in notochordless Xenopus embryos; laterality of the ventral spinal cord is lost. Development 112, 499–516
    OpenUrlAbstract
    1. Darnell D.K.,
    2. Schoenwolf G.C.,
    3. Ordahl C.P.
    (1992) Changes in dorsoventral but not rostrocaudal regionalization of the chick neural tube in the absence of cranial notochord, as revealed by expression of Engrailed-2. Dev. Dyn 193, 389–396
    OpenUrlPubMed
    1. Dickinson M.E.,
    2. Selleck M.A.J.,
    3. McMahon A.P.,
    4. Bronner-Fraser M.
    (1995) Dorsalization of the neural tube by the non-neural ectoderm. Development 121, 2099–2106
    OpenUrlAbstract
    1. Dodd J.,
    2. Morton S.B.,
    3. Karagogeos D.,
    4. Yamamoto M.,
    5. Jessell T.M.
    (1988) Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron 1, 105–116
    OpenUrlCrossRefPubMedWeb of Science
    1. Downs K.M.,
    2. Davies T.
    (1993) Staging of gastrulating mouse embryos by morphological landmarks in the dissecting microscope. Development 118, 1255–1266
    OpenUrlAbstract/FREE Full Text
    1. Dudley A.T.,
    2. Lyons K.M.,
    3. Robertson E.J.
    (1995) A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev 9, 2795–2807
    OpenUrlAbstract/FREE Full Text
    1. Echelard Y.,
    2. Epstein D.J.,
    3. St-Jacques B.,
    4. Shen L.,
    5. Mohler J.,
    6. McMahon J.A.,
    7. McMahon A.P.
    (1993) Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417–1430
    OpenUrlCrossRefPubMedWeb of Science
    1. Furley A.J.,
    2. Morton S.B.,
    3. Manalo D.,
    4. Karagogeos D.,
    5. Dodd J.,
    6. Jessell T.M.
    (1990) The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. Cell 61, 157–170
    OpenUrlCrossRefPubMedWeb of Science
    1. Goulding M.D.,
    2. Chalepakis G.,
    3. Deutsch U.,
    4. Erselius J.R.,
    5. Gruss P.
    (1991) Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. EMBO J 10, 1135–1147
    OpenUrlPubMedWeb of Science
    1. Goulding M.D.,
    2. Lumsden A.,
    3. Gruss P.
    (1993) Signals from the notochord and floor plate regulate the region-specific expression of two Pax genes in the developing spinal cord. Development 117, 1001–1016
    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.,
    2. Butcher M.,
    3. Lumsden A.
    (1991) Patterns of cell division and interkinetic nuclear migration in the chick embryo hindbrain. J. Neurobiol 22, 742–754
    OpenUrlCrossRefPubMedWeb of Science
    1. Harrison S.M.,
    2. Dunwoodie S.L.,
    3. Arkell R.M.,
    4. Lehrach H.,
    5. Beddington R.S.P.
    (1995) Isolation of novel tissue-specific genes from cDNA libraries representing the individual tissue constituents of the gastrulating mouse embryo. Development 121, 2479–2489
    OpenUrlAbstract
    1. Heimer G.V.,
    2. Taylor C.E.D.
    (1974) Improved mountant for immunofluorescence preparations. J. Clin. Pathol 27, 254–256
    OpenUrlFREE Full Text
    1. Hill R.E.,
    2. Jones P.F.,
    3. Rees A.R.,
    4. Sime C.M.,
    5. Justice M.J.,
    6. Copeland N.G.,
    7. Jenkins N.A.,
    8. Graham E.,
    9. Davidson D.R.
    (1989) A new family of mouse homeo box-containing genes: molecular structure, chromosomal location and developmental expression of Hox-7.1 Genes Dev 3, 26–37
    OpenUrlAbstract/FREE Full Text
    1. Hirano S.,
    2. Fuse S.,
    3. Sohal G.S.
    (1991) The effect of floor plate on pattern and polarity in the developing central nervous system. Science 251, 310–313
    OpenUrlAbstract/FREE Full Text
    1. Hogan B.L.M.
    (1995) Upside-down ideas vindicated. Nature 376, 210–211
    OpenUrlCrossRefPubMed
    1. Ingham P.W.
    (1995) Signalling by hedgehog family proteins in Drosophila and vertebrate development. Curr. Opin. Genet. Dev 5, 492–498
    OpenUrlCrossRefPubMedWeb of Science
    1. Knutsen R.,
    2. Wergedal J.E.,
    3. Sampath T.K.,
    4. Baylink D.J.,
    5. Mohan S.
    (1993) Osteogenic protein-1 stimulates proliferation and differentiation of human bone cells in vitro. Biochem. Biophys. Res. Commun 194, 1352–1358
    OpenUrlCrossRefPubMed
    1. Krauss S.,
    2. Concordet J.P.,
    3. Ingham P.W.
    (1993) A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75, 1431–1444
    OpenUrlCrossRefPubMedWeb of Science
    1. Liem K.F.J.,
    2. Tremml G.,
    3. Roelink H.,
    4. Jessell T.M.
    (1995) Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82, 969–979
    OpenUrlCrossRefPubMedWeb of Science
    1. Luo G.,
    2. Hofmann C.,
    3. Bronckers A.L.J.J.,
    4. Sohocki M.,
    5. Bradley A.,
    6. Karsenty G.
    (1995) BMP-7 is an inducer of nephrogenesis, and is alsorequired for eye development and skeletal patterning. Genes Dev 9, 2808–2820
    OpenUrlAbstract/FREE Full Text
    1. Lyons K.M.,
    2. Hogan B.L.M.,
    3. Robertson E.J.
    (1995) Colocalization of BMP 7 and BMP 2 RNAs suggests that these factors cooperatively mediate tissue interactions during murine development. Mech. Dev 50, 71–83
    OpenUrlCrossRefPubMedWeb of Science
    1. Mishina Y.,
    2. Suzuki A.,
    3. Ueno N.,
    4. Behringer R.R.
    (1995) Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev 9, 3027–3037
    OpenUrlAbstract/FREE Full Text
    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. Moury J.D.,
    2. Jacobson A.G.
    (1989) Neural fold formation at newly created boundaries between neural plate and epidermis in the axolotl. Dev. Biol 133, 44–57
    OpenUrlCrossRefPubMedWeb of Science
    1. Moury J.D.,
    2. Jacobson A.G.
    (1990) The origins of neural crest in the axolotl. Dev. Biol 141, 243–253
    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. exp. Morph 64, 105–120
    OpenUrlPubMedWeb of Science
    1. Placzek M.
    (1995) The role of the notochord and floor plate in inductive interactions. Curr. Opin. Genet. Dev 5, 499–506
    OpenUrlCrossRefPubMedWeb of Science
    1. Placzek M.,
    2. Jessell T.M.,
    3. Dodd J.
    (1993) Induction of floor plate differentiation by contact-dependent, homeogenetic signals. Development 117, 205–218
    OpenUrlAbstract/FREE Full Text
    1. Placzek M.,
    2. Tessier-Lavigne M.,
    3. Yamada T.,
    4. Jessell T.,
    5. Dodd J.
    (1990) Mesodermal control of neural cell identity: floor plate induction by the notochord. Science 250, 985–988
    OpenUrlAbstract/FREE Full Text
    1. Rashbass P.,
    2. Wilson V.,
    3. Rosen B.,
    4. Beddington R.S.P.
    (1994) Alterations in gene expression during mesoderm formation and axial patterning in Brachyury (T) embryos. Int. J. Dev. Biol 38, 35–44
    OpenUrlPubMed
    1. Riddle R.D.,
    2. Johnson R.L.,
    3. Laufer E.,
    4. Tabin C.
    (1993) Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401–1416
    OpenUrlCrossRefPubMedWeb of Science
    1. Roelink H.,
    2. Augsburger A.,
    3. Heemskerk J.,
    4. Korzh V.,
    5. Norlin S.,
    6. Ruiz i Altaba A.,
    7. Tanabe Y.,
    8. Placzek M.,
    9. Edlund T.,
    10. Jessell T.M.,
    11. Dodd J.
    (1994) Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76, 761–775
    OpenUrlCrossRefPubMedWeb of Science
    1. Rosen B.,
    2. Beddington R.S.P.
    (1993) Whole-mount in situ hybridization in the mouse embryo: gene expression in three dimensions. Trends Genet 9, 162–167
    OpenUrlCrossRefPubMedWeb of Science
    1. Ruiz i Altaba A.,
    2. Cox C.,
    3. Jessell T.M.,
    4. Klar A.
    (1993) Ectopic neural expression of a floor plate marker in frog embryos injected with the midline transcription factor Pintallavis. Proc. Natl. Acad. Sci. USA 90, 8268–8272
    OpenUrlAbstract/FREE Full Text
    1. Ruiz i Altaba A.,
    2. Jessell T.M.,
    3. Roelink H.
    (1995) Restrictions to floor plate induction by hedgehog and winged-helix genes in the neural tube of frog embryos. Mol. Cell. Neurosci 6, 106–121
    OpenUrlCrossRefPubMedWeb of Science
    1. Ruiz i Altaba A.,
    2. Placzek M.,
    3. Baldassare M.,
    4. Dodd J.,
    5. Jessell T.M.
    (1995) Early stages of notochord and floor plate development in the chick embryo defined by normal and induced expression of HNF-3. Dev. Biol 170, 299–313
    OpenUrlCrossRefPubMedWeb of Science
    1. Sadaghiani B.,
    2. Thiebaud C.H.
    (1987) Neural crest development in the Xenopus laevis embryo, studied by interspecific transplantation and scanning electron microscopy. Dev. Biol 124, 91–110
    OpenUrlCrossRefPubMedWeb of Science
    1. Sasaki H.,
    2. Hogan B.L.M.
    (1994) HNF-3 as a regulator of floor plate development. Cell 76, 103–115
    OpenUrlCrossRefPubMedWeb of Science
    1. Selleck M.A.J.,
    2. Bronner-Fraser M.
    (1995) Origins of the avian neural crest: the role of neural plate-epidermal interactions. Development 121, 525–538
    OpenUrlAbstract
    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. Fraser S.E.,
    3. Bronner-Fraser M.
    (1990) Pathways of trunk neural crest cell migration in the mouse embryo as revealed by vital dye labelling. Development 108, 605–612
    OpenUrlAbstract/FREE Full Text
    1. Smith J.L.,
    2. Schoenwolf G.C.
    (1989) Notochordal induction of cell wedging in the chick neural plate and its role in neural tube formation. J. exp. Zool 250, 49–62
    OpenUrlCrossRefPubMedWeb of Science
    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. Tosney K.W.
    (1982) The segregation and early migration of cranial neural crest cells in the avian embryo. Dev. Biol 89, 13–24
    OpenUrlCrossRefPubMedWeb of Science
    1. Trainor P.A.,
    2. Tam P.P.L.
    (1995) Cranial paraxial mesoderm and neural crest cells of the mouse embryo: co-distribution in the craniofacial mesenchyme but distinct segregation in branchial arches. Development 121, 2569–2582
    OpenUrlAbstract
    1. van Straaten H.W.M.,
    2. Hekking J.W.M.,
    3. Wiertz-Hoessels E.J.L.M.,
    4. Thors F.,
    5. Drukker J.
    (1988) Effect of the notochord on the differentiation of a floor plate area in the neural tube of the chick embryo. Anat. Embryol 177, 317–324
    OpenUrlCrossRefPubMed
    1. Winnier G.,
    2. Blessing M.,
    3. Labosky P.A.,
    4. Hogan B.L.M.
    (1995) Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 9, 2105–2116
    OpenUrlAbstract/FREE Full Text
    1. Yamada T.,
    2. Pfaff S.L.,
    3. Edlund T.,
    4. Jessell T.M.
    (1993) Control of cell pattern in the neural tube: motor neuron induction by diffusible factors from notochord and floor plate. Cell 73, 673–686
    OpenUrlCrossRefPubMedWeb of Science
    1. Yamada T.,
    2. Placzek M.,
    3. Tanaka H.,
    4. Dodd J.,
    5. Jessell 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
Back to top

 Download PDF

Email
JOURNAL ARTICLES
BMP-7 influences pattern and growth of the developing hindbrain of mouse embryos
R. Arkell, R.S. Beddington
Development 1997 124: 1-12;
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