Skip to main content
Advertisement

Main menu

  • Home
  • Articles
    • Accepted manuscripts
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Advertising
    • Feedback
    • For library administrators
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

User menu

  • Log in
  • Log out

Search

  • Advanced search
Development
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

supporting biologistsinspiring biology

Development

  • Log in
Advanced search

RSS  Twitter  Facebook  YouTube 

  • Home
  • Articles
    • Accepted manuscripts
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Advertising
    • Feedback
    • For library administrators
JOURNAL ARTICLES
Differential regulation of T-box and homeobox transcription factors suggests roles in controlling chick limb-type identity
M. Logan, H.G. Simon, C. Tabin
Development 1998 125: 2825-2835;
M. Logan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
H.G. Simon
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
C. Tabin
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Info & metrics
  • PDF
Loading

Summary

The wing and the leg of the chick, although homologous structures, have characteristic patterns of skeletal elements, muscles, tendons, featherbuds and scales. Despite recent advances in understanding the common genetic pathways patterning the wing and leg, the molecular nature of the specification of limb-type identity has remained elusive. Embryological experiments have indicated the existence of limb-specific territories in the flank. In the newt, deviation of nerves from the limb into the flank can induce ectopic limbs to form from this tissue. In the chick, Fibroblast growth factor (FGF)-soaked beads applied to the flank can induce ectopic formation of limbs from the surrounding tissue. In both cases, the type of limb that forms, either a wing/forelimb or leg/hindlimb, is dependent upon the location to which the limb-inducing signal is applied. We have isolated and characterised three candidate genes for controlling limb identity in the chick. Two T-box transcription factors, cTbx4 and cTbx5, are expressed in a restricted manner in the leg bud and wing buds, respectively. cPtx1, a member of the Otx-related subclass of paired-type homeodomain proteins, is expressed exclusively in the leg bud. Using FGF to induce ectopic limb buds of wing, leg and intermediate identity, we show that early expression of cTbx5, cTbx4 and cPtx1 in the induced limb buds correlates with later wing- or leg-type identity of ectopic limbs. We observe a general correlation between the location of an ectopic outgrowth induced by FGF and the identity of the resulting limb but, significantly, we report that there is no definitive rostral-caudal level that divides the ectopic wing and leg territories.

REFERENCES

    1. Agulnik S. I.,
    2. Garvey N.,
    3. Hancock S.,
    4. Ruvinsky I.,
    5. Chapman D. L.,
    6. Agulnik I.,
    7. Bollag R.,
    8. Papaioannou V. E.,
    9. Silver L. M.
    (1996) Evolution of mouse T-box genes by tandem duplication and cluster dispersion. Genetics 144, 249–254
    OpenUrlAbstract
    1. Akam M.,
    2. Averof M.,
    3. Castelli-Gair J.,
    4. Dawes R.,
    5. Falciani F.,
    6. Ferrier D.
    (1994) The evolving role of Hox genes in arthropods. Development 1994, 209–215
    1. Balinsky B. I.
    (1957) New experiments in the mode of action of the limb inductor. J. Exp. Zool 134, 239–273
    1. Bamshad M.,
    2. Lin R. C.,
    3. Law D. J.,
    4. Watkins W. S.,
    5. Krakowiak P. A.,
    6. Moore M. E.,
    7. Franceschini P.,
    8. Lala R.,
    9. Holmes L. B.,
    10. Gebuhr T. C.,
    11. Bruneau B. G.,
    12. Schinzel A.,
    13. Seidman J. G.,
    14. Seidman C. E.,
    15. Jorde L.
    (1997) Mutations in Human TBX3 alter limb, apocrine and genital development in ulnar-mammary syndrome. Nature Genetics 16, 311–315
    OpenUrlCrossRefPubMedWeb of Science
    1. Bamshad M.,
    2. Root S.,
    3. Carey J. C.
    (1996) Clinical Analysis of a Large Kindred With the Pallister Ulnar-Mammary Sybndrome. Amer. J. Med. Genet 65, 325–331
    OpenUrlCrossRefPubMed
    1. Bao Z. Z.,
    2. Cepko C. L.
    (1997) The Expression and function of Notch pathway genes in the developing rat retina. J. Neurosci 17, 1425–1434
    OpenUrlAbstract/FREE Full Text
    1. Basson C. T.,
    2. Bachinsky D. R.,
    3. Lin R.C.,
    4. Levi T.,
    5. Elkins J. A.,
    6. Soults J.,
    7. Grayzel D.,
    8. Kroumpouzou E.,
    9. Trail T. A.,
    10. Leblanc-Straceski J.,
    11. Renault B.,
    12. Kucherlapati R.,
    13. Seidman J. G.,
    14. Seidman C. E.
    (1997) Mutations in Human TBX5 cause limb and cardiac malformations in Holt-Oram syndrome. Nature Genetics 15, 30–35
    OpenUrlCrossRefPubMedWeb of Science
    1. Bollag R.,
    2. Siegfried Z.,
    3. Cebra-Thomas J. A.,
    4. Garvey N.,
    5. Davison E. M.,
    6. Silver L. M.
    (1994) An ancient family of embryonically expressed mouse genes sharing a conserved protein motif with the T locus. Nature Genetics 7, 383–389
    OpenUrlCrossRefPubMedWeb of Science
    1. Chapman D. L.,
    2. Garvey N.,
    3. Hancock S.,
    4. Alexiou M.,
    5. Agulnik S. I.,
    6. Gibson-Brown J. J.,
    7. Cebra-Thomas J.,
    8. Bollag R. J.,
    9. Silver L. M.,
    10. Papaioannou V. E.
    (1996) Expression of the T-box Family Genes, TBX1-TBX5, During Early Mouse Development. Dev. Dynam 206, 379–390
    OpenUrlCrossRefPubMedWeb of Science
    1. Chapman D.L.,
    2. Papaioannou V.E.
    (1998) Three neural tubes in mouse embryos with mutations in the T-box gene Tbx6. Nature 391, 695–697
    OpenUrlCrossRefPubMed
    1. Cohn M. J.,
    2. Izpisua-Belmonte J.-C.,
    3. Abud H.,
    4. Heath J. K.,
    5. Tickle C.
    (1995) Fibroblast Growth Factors Induce Additional Limb Development from the Flank of Chick Embryos. Cell 80, 739–746
    OpenUrlCrossRefPubMedWeb of Science
    1. Cohn M. J.,
    2. Patel K.,
    3. Krumlauf R.,
    4. Wilkinson D. G.,
    5. Clarke J. D. W.,
    6. Tickle C.
    (1997) Hox9 genes and vertebrate limb specification. Nature 387, 97–101
    OpenUrlCrossRefPubMed
    1. Conlon F. L.,
    2. Sedgwick K.,
    3. Weston K.,
    4. Smith J. C.
    (1996) Inhibition of Xbra transcription activation causes defects in mesodermal patterning and reveeals autoregulation of Xbra in dorsal mesoderm. Development 122, 2427–2435
    OpenUrlAbstract
    1. Crossley P. H.,
    2. Minowada G.,
    3. MacArthur C. A.,
    4. Martin G. A.
    (1996) Roles for FGF8 in the induction, initiation and maintenance of chick limb development. Cell 84, 127–136
    OpenUrlCrossRefPubMedWeb of Science
    1. Gibson-Brown J. J.,
    2. Agulnik S. I.,
    3. Chapman D. L.,
    4. Alexiou M.,
    5. Garvey N.,
    6. Silver L. M.,
    7. Papaioannou V. E.
    (1996) Evidence of a role for T-box genes in the evolution of limb morphogenesis and the specification of forelimb/hindlimb identity. Mech. Dev 56, 93–101
    OpenUrlCrossRefPubMedWeb of Science
    1. Glick B.
    (1931) The induction of supernumeracy limbs in Amblystoma. Anat. Rec 48, 407–414
    OpenUrlCrossRef
    1. Guyenot E.,
    2. Dinichert-Favarger J.,
    3. Gallard M.
    (1948) L'exploration di territoire de la patte anterieure du Triton. Revue Suisse de Zoologie 55, 1–120
    OpenUrl
    1. Hamburger V.,
    2. Hamilton H. L.
    (1951) A series of normal stages in the development of the chick embryo. J. Exp. Morph 88, 49–92
    OpenUrl
    1. Isaac A.,
    2. Rodriguez-Esteban C.,
    3. Ryan A.,
    4. Altabef M.,
    5. Tsukui T.,
    6. Patel K.,
    7. Tickle C.,
    8. Izpisua Belmonte J. C.
    (1998) Tbx genes and limb identity in chick embryo development. Development 125, 1867–1875
    OpenUrlAbstract
    1. Johnson R. J.,
    2. Tabin C. T.
    (1997) Molecular models for vertebrate limb development. Cell 90, 979–990
    OpenUrlCrossRefPubMedWeb of Science
    1. Kieny M.
    (1964) Etude du mecanisme de la regulation dans le development du bourgeon de membre de l'embryon de poulet II. Regulation des deficiences dans les chimeres ‘aile-patte’ et ‘patte-aile’. J. Embryol. Exp. Morph 12, 357–371
    1. Kispert A.,
    2. Herrman B. G.
    (1993) The Brachyury gene encodes a novel DNA binding protein. EMBO J 12, 3211–3220
    OpenUrlPubMedWeb of Science
    1. Kispert A.,
    2. Koschorz B.,
    3. Herrman B. G.
    (1995) The T-protein encoded by Brachyury is a tissue-specific transcription factor. EMBO J 14, 4763–4772
    OpenUrlPubMedWeb of Science
    1. Lamonerie T.,
    2. Tremblay J. J.,
    3. Lanctot C.,
    4. Therrien M.,
    5. Gauthier Y.,
    6. Drouin J.
    (1996) Ptx1, a bicoid -related homeo box transcription factor involved in transcription of the pro-opiomelanocortin gene. Genes Dev 10, 1284–1295
    OpenUrlAbstract/FREE Full Text
    1. Laufer E.,
    2. Nelson C. E.,
    3. Johnson R. L.,
    4. Morgan B. A.,
    5. Tabin C.
    (1994) Sonic hedgehog and FGF-4 act through a signalling cascade and feedback loop to intergrate growth and patterning of the developing limb bud. Cell 79, 993–1003
    OpenUrlCrossRefPubMedWeb of Science
    1. Li Q. Y.,
    2. Newbury-Ecob R. A.,
    3. Terrett J. A.,
    4. Wilson D. I.,
    5. Curtis A. R. J.,
    6. Yi C. H.,
    7. Gebuhr T.,
    8. Bullen P. J.,
    9. Robson S. C.,
    10. Strachan T.,
    11. Bonnet D.,
    12. Lyonnet S.,
    13. Young I. D.,
    14. Raeburn J.A.,
    15. Buckler A. J.,
    16. Law D. J.,
    17. Brook J. D.
    (1997) Holt-Oram syndrome is caused by mutations in TBX5, a member of the Brachyury(T) gene family. Nature Genetics 15, 21–29
    OpenUrlCrossRefPubMedWeb of Science
    1. Nelson C. E.,
    2. Morgan B. A.,
    3. Burke A. C.,
    4. Laufer E.,
    5. DiMambro E.,
    6. Murtaugh L. C.,
    7. Gonzales E.,
    8. Tessarollo L.,
    9. Parada L. F.,
    10. Tabin C.
    (1996) Analysis of Hox gene expression in the chick limb bud. Development 122, 1449–1466
    OpenUrlAbstract
    1. Niswander L.,
    2. Jeffrey S.,
    3. Martin G. R.,
    4. Tickle C.
    (1994) A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature 371, 609–612
    OpenUrlCrossRefPubMed
    1. Ohuchi H.,
    2. Nakagawa T.,
    3. Yamamoto A.,
    4. Araga A.,
    5. Ohata T.,
    6. Ishimaru Y.,
    7. Yoshioka H.,
    8. Kuwana T.,
    9. Nohno T.,
    10. Yamasaki M.,
    11. Itoh N.,
    12. Noji S.
    (1997) The mesenchymal factor, FGF10, initiates and maintains the outgrowth of the chick limb bud through interaction with FGF8, an apical ectodermal factor. Development 124, 2235–2244
    OpenUrlAbstract
    1. Ohuchi H.,
    2. Nakagawa T.,
    3. Yamamoto A.,
    4. Araga A.,
    5. Ohata T.,
    6. Ishiumura Y.,
    7. Yoshioka H.,
    8. Kuwana T.,
    9. Nohno T.,
    10. Yamasaki M.,
    11. Itoh N.,
    12. Noji S.
    (1995) An additional limb can be induced from the flank of the chick embryo by FGF4. Biochem. Biophys. Res. Commun 209, 809–816
    OpenUrlCrossRefPubMedWeb of Science
    1. Ohuchi H.,
    2. Takeuchi J.,
    3. Yoshioka H.,
    4. Ishimaru Y.,
    5. Ogura K.,
    6. Takahasi N.,
    7. Ogura T.,
    8. Noji S.
    (1998) Correlation of wing-leg identity in ectopic FGF-induced chimeric limbs with the differential expression of chick Tbx5 and Tbx4. Development 125, 51–60
    OpenUrlAbstract
    1. Oliver G.,
    2. Wright C. V.,
    3. Hardwicke J.,
    4. De Robertis E. M.
    (1988) A gradient of homeodomain protein in developing forelimbs of Xenopus and mouse embryos. Cell 55, 1017–1024
    OpenUrlCrossRefPubMedWeb of Science
    1. Papaioannou V. E.,
    2. Silver L. M.
    (1998) The T-box gene family. BioEssays 20, 9–19
    OpenUrlCrossRefPubMedWeb of Science
    1. Papapetrou C.,
    2. Edwards Y. H.,
    3. Sowden J. C.
    (1997) The T transcription factor functions as a dimer and exhibits a common human polymorphism Gly-177-Asp in the conserved DNA-binding domain. FEBS Letters 409, 201–206
    OpenUrlCrossRefPubMedWeb of Science
    1. Riddle R. D.,
    2. Johnson R. L.,
    3. Laufer E.,
    4. Tabin C. J.
    (1993) Sonic hedgehog mediates the polarizing activity in the ZPA. Cell 75, 1401–1416
    OpenUrlCrossRefPubMedWeb of Science
    1. Saunders J., Jr
    (1966) Death in embryonic systems. [Review]. Science 154, 604–12
    OpenUrlAbstract/FREE Full Text
    1. Saunders J. W.,
    2. Cairns J. M.,
    3. Gasseling M. T.
    (1957) The role of the apical ridge of ectoderm in the differentiation of the morphological structure and inductive specificity of limb parts in the chick. J. Morph 101, 57–88
    OpenUrlCrossRef
    1. Schulte-Merker S.,
    2. van Eden F. J. M.,
    3. Halpern M. E.,
    4. Kimmel C. B.,
    5. Nusslein-Volhard C.
    (1994) no tail (ntl) is the zebrafish homologue of the mouse T (Brachyury) gene. Development 120, 1009–1015
    OpenUrlAbstract
    1. Semina E. V.,
    2. Reiter R.,
    3. Leysens N. J.,
    4. Alward W. L.,
    5. Small K. W.,
    6. Datson N. A.,
    7. Siegel-Bartelt J.,
    8. Bierke-Nelson D.,
    9. Bitoun P.,
    10. Zabel B. U.,
    11. Carey J. C.,
    12. Murray J. C.
    (1996) Cloning and characterizationof a novel bicoid-related homeobox transcription factor gene, RIEG, involved in Rieger syndrome. Nature Genetics 14, 392–9
    OpenUrlCrossRefPubMedWeb of Science
    1. Semina E. V.,
    2. Reiter R. S.,
    3. Murray J. C.
    (1997) Isolation of a new homeobox gene belonging to the Pitx/Rieg family: expression during lens development and mapping to the aphakia region on mouse chromosome 19. Hum. Mol. Genet 6, 2109–16
    OpenUrlAbstract/FREE Full Text
    1. Shang J.,
    2. Li X.,
    3. Ring H. Z.,
    4. Clayton D. A.,
    5. Francke U.
    (1997) Backfoot, a Novel Homeobox Gene, Maps to Human Chromosome 5 (BFT) and Mouse Chromosome 13 (Bft). Genomics 40, 108–113
    OpenUrlCrossRefPubMedWeb of Science
    1. Simon H.-G.,
    2. Kittappa R.,
    3. Khan P. A.,
    4. Tsilfidis C.,
    5. Liversage R. A.,
    6. Oppenheimer S.
    (1997) A novel family of T-box genes in urodele amphibian limb development and regeneration: candidate genes involved in vertebrate forelimb/hindlimb patterning. Development 124, 1355–1366
    OpenUrlAbstract
    1. Simon H.-G.,
    2. Tabin C. J.
    (1993). Analysts of Hox 4.5 and Hox 3.6 expression during newt limb regeneration: differential regulation ofparalogous Hox genes suggests different roles for members of different Hox clusters. Development 117, 1397–1407
    OpenUrlAbstract
    1. Stephens T. D.,
    2. Beier R. L.,
    3. Bringhurst D. C.,
    4. Hiatt S. R.,
    5. Prestidge M.,
    6. Pugmire D. E.,
    7. Willis H. J.
    (1989) Limbness in the early chick embryo lateral plate. Dev. Biol 133, 1–7
    OpenUrlCrossRefPubMed
    1. Szeto D. P.,
    2. Ryan A. K.,
    3. O'Connell S. M.,
    4. Rosenfeld M. G.
    (1996) P-OTX: A PIT-1-interacting homeodomain factor expressed during anterior pituitary gland development. Proc. Natl. Acad. Sci. USA 93, 7706–7710
    OpenUrlAbstract/FREE Full Text
    1. Vogel A.,
    2. Rodriguez C.,
    3. Izpisua-Belmonte J.-C.
    (1996) Involvement of FGF8 in initiation, outgrowth and patterning of the vertebrate limb. Development 122, 1737–1750
    OpenUrlAbstract
    1. Zwilling E.
    (1956) Ectoderm-mesoderm relationship in the development of the chick embryo limb bud. J. Exp. Zool 128, 423–441
    OpenUrlCrossRef
    1. Zwilling E.
    (1956) Interaction between limb bud ectoderm and mesoderm in the chick embryo i. axis establishment. J. Exp. Zool 132, 157–171
    OpenUrlCrossRef
Previous ArticleNext Article
Back to top
Previous ArticleNext Article

This Issue

 Download PDF

Email

Thank you for your interest in spreading the word on Development.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Differential regulation of T-box and homeobox transcription factors suggests roles in controlling chick limb-type identity
(Your Name) has sent you a message from Development
(Your Name) thought you would like to see the Development web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
JOURNAL ARTICLES
Differential regulation of T-box and homeobox transcription factors suggests roles in controlling chick limb-type identity
M. Logan, H.G. Simon, C. Tabin
Development 1998 125: 2825-2835;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
JOURNAL ARTICLES
Differential regulation of T-box and homeobox transcription factors suggests roles in controlling chick limb-type identity
M. Logan, H.G. Simon, C. Tabin
Development 1998 125: 2825-2835;

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Alerts

Please log in to add an alert for this article.

Sign in to email alerts with your email address

Article navigation

  • Top
  • Article
  • Info & metrics
  • PDF

Related articles

Cited by...

More in this TOC section

  • Non-imprinted Igf2r expression decreases growth and rescues the Tme mutation in mice
  • REF-1, a protein with two bHLH domains, alters the pattern of cell fusion in C. elegans by regulating Hox protein activity
  • Centrosome migration into the Drosophila oocyte is independent of BicD and egl, and of the organisation of the microtubule cytoskeleton
Show more JOURNAL ARTICLES

Similar articles

Other journals from The Company of Biologists

Journal of Cell Science

Journal of Experimental Biology

Disease Models & Mechanisms

Biology Open

Advertisement

A new society for regenerative biologists

Kenneth Poss and Elly Tanaka announce the launch of the International Society for Regenerative Biology (ISRB), which will promote research and education in the field of regenerative biology.


Upcoming special issue: call for papers

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

The special issue welcomes Review articles as well as Research articles, and will be widely promoted online and at key global conferences.


An interview with Cagney Coomer

Over a virtual chat, we spoke to Cagney Coomer about her experiences in the lab, the classroom and the community centre, and why she thinks outreach and role models are vital to science.


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, Michèle Romanos talks about her new preprint, which mixes experimentation in quail embryos and computational modelling to understand how heterogeneity in a tissue influences cell rate.

Save your spot at our next session:

10 March
Time: 9:00 (GMT)
Chaired by: Thomas Lecuit

Join our mailing list to receive news and updates on the series.

Articles

  • Accepted manuscripts
  • Latest complete issue
  • Issue archive
  • Archive by article type
  • Special issues
  • Subject collections
  • Sign up for alerts

About us

  • About Development
  • About the Node
  • Editors and board
  • Editor biographies
  • Travelling Fellowships
  • Grants and funding
  • Journal Meetings
  • Workshops
  • The Company of Biologists

For authors

  • Submit a manuscript
  • Aims and scope
  • Presubmission enquiries
  • Article types
  • Manuscript preparation
  • Cover suggestions
  • Editorial process
  • Promoting your paper
  • Open Access
  • Biology Open transfer

Journal info

  • Journal policies
  • Rights and permissions
  • Media policies
  • Reviewer guide
  • Sign up for alerts

Contact

  • Contact Development
  • Subscriptions
  • Advertising
  • Feedback
  • Institutional usage stats (logged-in users only)

 Twitter   YouTube   LinkedIn

© 2021   The Company of Biologists Ltd   Registered Charity 277992