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JOURNAL ARTICLES
The development of the posterior body in zebrafish
J.P. Kanki, R.K. Ho
Development 1997 124: 881-893;

Summary

In order to understand the developmental mechanisms of posterior body formation in the zebrafish, a fate map of the zebrafish tailbud was generated along with a detailed analysis of tailbud cell movements. The fate map of the zebrafish tailbud shows that it contains tissue-restricted domains and is not a homogeneous blastema. Furthermore, time-lapse analysis shows that some cell movements and behaviors in the tailbud are similar to those seen during gastrulation, while others are unique to the posterior body. The extension of axial mesoderm and the continuation of ingression throughout zebrafish tail development suggests the continuation of processes initiated during gastrulation. Unique properties of zebrafish posterior body development include the bilateral distribution of tailbud cell progeny and the exhibition of different forms of ingression within specific tailbud domains. The ingression of cells in the anterior tailbud only gives rise to paraxial mesoderm, at the exclusion of axial mesoderm. Cells of the posterior tailbud undergo subduction, a novel form of ingression resulting in the restriction of this tailbud domain to paraxial mesodermal fates. The intermixing of spinal cord and muscle precursor cells, as well as evidence for pluripotent cells within the tailbud, suggest that complex inductive mechanisms accompany these cell movements throughout tail elongation. Rates of cell proliferation in the tailbud were examined and found to be relatively low at the tip of the tail indicating that tail elongation is not due to growth at its posterior end. However, higher rates of cell proliferation in the dorsomedial region of the tail may contribute to the preferential posterior movement of cells in this tailbud region and to the general extension of the tail. Understanding the cellular movements, cell fates and gene expression patterns in the tailbud will help to determine the nature of this important aspect of vertebrate development.

REFERENCES

    1. Barro O.,
    2. Vriz S.,
    3. Joly J. S.,
    4. Joly C.,
    5. Condamine H.,
    6. Boulekbache H.
    (1995) Widespread expression of the eve1 gene in zebrafish embryos affects the anterior-posterior axis pattern. Dev. Genet 17, 117–128
    OpenUrlCrossRefPubMedWeb of Science
    1. Catala M.,
    2. Teillet M. A.,
    3. Le Douarin N. M.
    (1995) Organization and development of the tail bud analyzed with the quail-chick chimaera system. Mech. Dev 51, 51–65
    OpenUrlCrossRefPubMedWeb of Science
    1. Chesley P.
    (1935) Development of the short-tailed mutant in the house mouse. J. Exp. Zool 70, 429–435
    OpenUrlCrossRef
    1. Criley B. B.
    (1969) Analysis of the embryonic sources and mechanisms of development of posterior levels of chick neural tubes. J. Morph 128, 465–501
    OpenUrlCrossRefPubMed
    1. Elsdale T.,
    2. Davidson D.
    (1983) Somitogenesis in amphibia IV. The dynamics of tail development. J. Embryol. Exp. Morph 76, 157–176
    OpenUrlPubMed
    1. Gaertner R. A.
    (1949) Development of the posterior trunk and tail of the chick embryo. J. Exp. Zool 111, 157–174
    OpenUrlCrossRefPubMed
    1. Gont L. K.,
    2. Steinbeisser H.,
    3. Blumberg B.,
    4. De Robertis 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
    1. Griffith C. M.,
    2. Wiley M. J.,
    3. Sanders E. J.
    (1992) The vertebrate tailbud: three germ layers from one tissue. Anat. Embryol 185, 101–113
    OpenUrlPubMed
    1. Halpern M. E.,
    2. Ho R. K.,
    3. Walker C.,
    4. Kimmel C. B.
    (1993) Induction of muscle pioneers and floor plate is distinguished by the zebrafish no tail mutation. Cell 75, 99–111
    OpenUrlCrossRefPubMedWeb of Science
    1. Halpern M. E.,
    2. Thisse C.,
    3. Ho R. K.,
    4. Thisse B.,
    5. Riggleman B.,
    6. Trevarrow B.,
    7. Weinberg E. S.,
    8. Postlethwait J. H.,
    9. Kimmel C. B.
    (1995) Cell-autonomous shift from axial to paraxial mesodermal development in zebrafish floating head mutants. Development 121, 4257–4264
    OpenUrlAbstract
    1. Hamburger V.,
    2. Hamilton H. L.
    (1951) A series of normal stages in the development of the chick embryo. J. Morph 88, 49–92
    OpenUrlCrossRefWeb of Science
    1. Hammerschmidt M.,
    2. Nusslein-Volhard C.
    (1993) The expression of a zebrafish gene homologous to Drosophila snail suggests a conserved function in invertebrate and vertebrate gastrulation. Development 119, 1107–1118
    OpenUrlAbstract
    1. Herrmann B. G.,
    2. Labeit S.,
    3. Poustka A.,
    4. King T. R.,
    5. Lehrach H.
    (1990) Cloning of the T gene required in mesoderm formation in the mouse. Nature 343, 617–622
    OpenUrlCrossRefPubMed
    1. Holmdahl D. E.
    (1925) Experimentelle Untersuchungen uber die Lage der Grenze primarer und sekundarer Korperentwicklung beim Huhn. Anat. Anz 59, 393–396
    OpenUrl
    1. Joly J. S.,
    2. Joly C.,
    3. Schulte-Merker S.,
    4. Boulekbache H.,
    5. Condamine H.
    (1993) The ventral and posterior expression of the zebrafish homeobox gene eve1 is perturbed in dorsalized and mutant embryos. Development 119, 1261–1275
    OpenUrlAbstract
    1. Joly J. S.,
    2. Maury M.,
    3. Joly C.,
    4. Duprey P.,
    5. Boulekbache H.,
    6. Condamine H.
    (1992) Expression of a zebrafish caudal homeobox gene correlates with the establishment of posterior cell lineages at gastrulation. Differentiation 50, 75–87
    OpenUrlCrossRefPubMed
    1. Keller R. E.,
    2. Tibbetts P.
    (1989) Mediolateral cell intercalation is a property of the dorsal, axial mesoderm of Xenopus laevis. Dev. Biol 131, 539–549
    OpenUrlPubMedWeb of Science
    1. Kimmel C. B.
    (1989) Genetics and early development of zebrafish. Trends Genet 5, 283–288
    OpenUrlCrossRefPubMedWeb 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. Kimmel C. B.,
    2. Warga R. M.
    (1987) Cell lineages generating axial muscle in the zebrafish embryo. Nature 327, 234–237
    OpenUrlCrossRefPubMed
    1. Kimmel C. B.,
    2. Warga R. M.
    (1988) Cell lineage and developmental potential of cells in the zebrafish embryo. Trends Genet 4, 68–74
    OpenUrlCrossRefPubMedWeb of Science
    1. Kimmel C. B.,
    2. Warga R. M.,
    3. Schilling T. F.
    (1990) Origin and organization of the zebrafish fate map. Development 108, 581–94
    OpenUrlAbstract/FREE Full Text
    1. Laale H. W.
    (1985) Kupffer's vesicle in Brachydanio rerio: multivesicular origin and proposed function in vitro. Can. J. Zool 63, 2408–2415
    OpenUrl
    1. Mills C. L.,
    2. Bellairs R.
    (1989) Mitosis and cell death in the tail of the chick embryo. Anat. Embryol 180, 301–308
    OpenUrlCrossRefPubMed
    1. Nakao T.,
    2. Ishizawa A.
    (1984) Light-and electron-microscopic observations of the tail bud of the larval lamprey (Lampetra japonica), with special reference to neural tube formation. Am. J. Anat 170, 55–71
    OpenUrlCrossRefPubMed
    1. Neumann P. E.,
    2. Frankel W. N.,
    3. Letts V. A.,
    4. Coffin J. M.,
    5. Copp A. J.,
    6. Bernfield M.
    (1994) Multifactorial inheritance of neural tube defects: localization of the major gene and recognition of modifiers in ct mutant mice. Nat. Genet 6, 357–362
    OpenUrlCrossRefPubMedWeb of Science
    1. Pasteels J.
    (1943) Proliferations et croissance dans la gastrulation et la formation de la queue des Vertebres. Arch. Biol 54, 1–51
    OpenUrl
    1. Sausedo R. A.,
    2. Schoenwolf G. C.
    (1993) Cell behaviors underlying notochord formation and extension in avian embryos: Quantitative and immunocytochemical studies. Anat. Rec 237, 58–70
    OpenUrlCrossRefPubMed
    1. Sausedo R. A.,
    2. Schoenwolf G. C.
    (1994) Quantitative analysis of cell behaviors underlying notochord formation and extension in mouse embryos. Anat. Rec 239, 103–112
    OpenUrlCrossRefPubMed
    1. Schoenwolf G. C.
    (1977) Tail (end) bud contributions to the posterior region of the chick embryo. J. Exp. Zool 201, 227–246
    OpenUrlCrossRef
    1. Schoenwolf G. C.
    (1978) Effects of complete tail extirpation on early development of the posterior region of the chick embryo. Anat. Rec 192, 289–296
    OpenUrlCrossRefPubMed
    1. Schoenwolf G. C.
    (1984) Histological and ultrastructural studies of secondary neurulation in the mouse embryo. Am. J. Anat 169, 361–376
    OpenUrlCrossRefPubMedWeb of Science
    1. Schoenwolf G. C.,
    2. Alvarez I. S.
    (1989) Roles of neuroepithelial cell rearrangement and division in shaping of the avian neural plate. Development 106, 427–439
    OpenUrlAbstract
    1. Schoenwolf G. C.,
    2. Delongo J.
    (1980) Ultrastructure of secondary neurulation in the chick embryo. Am. J. Anat 158, 43–63
    OpenUrlCrossRefPubMed
    1. Schoenwolf G. C.,
    2. Sheard P.
    (1990) Fate Mapping the Avian Epiblast with Focal Injections of a Fluorescent-Histochemical Marker: Ectodermal Derivatives. J. Exp. Zool 255, 323–339
    OpenUrlCrossRefPubMed
    1. Schulte-Merker S.,
    2. Ho R. K.,
    3. Herrmann B. G.,
    4. Nusslein-Volhard C.
    (1992) The protein product of the zebrafish homologue of the mouse T gene is expressed in nuclei of the germ ring and the notochord of the early embryo. Development 116, 1021–1032
    OpenUrlAbstract/FREE Full Text
    1. Schulte-Merker S.,
    2. van Eeden 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. Seevers C. H.
    (1932) Potencies of the end bud and other caudal levels of the early chick embryo with special reference to the origin of the metanephros. Anat. Rec 54, 217–246
    OpenUrlCrossRef
    1. Shih J.,
    2. Fraser S. E.
    (1995) Distribution of tissue progenitors within the shield region of the zebrafish gastrula. Development 121, 2755–2765
    OpenUrlAbstract
    1. Smithberg M.
    (1954) The origin and development of the tail in the frog, Rana pipiens. J. Exp. Zool 127, 397–425
    OpenUrlCrossRef
    1. Spofford W. R.
    (1945) Observations of the posterior part of the neural plate in Amblystoma. J. Exp. Zool 99, 35–52
    OpenUrlCrossRef
    1. Spratt N. T.
    (1947) Regression and shortening of the primitive streak in the explanted chick blastoderm. J. Exp. Zool 104, 69–100
    OpenUrlPubMed
    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. 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
    OpenUrlCrossRefPubMed
    1. Tam P. P. L.
    (1984) The histogenetic capacity of tissues in the caudal end of the embryonic axis of the mouse. J. Embryol. Exp. Morph 82, 253–266
    OpenUrlPubMedWeb of Science
    1. Thisse C.,
    2. Thisse B.,
    3. Schilling T. F.,
    4. Postlethwait J. H.
    (1993) Structure of the zebrafish snail gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119, 1203–1215
    OpenUrlAbstract
    1. Tucker A. S.,
    2. Slack J. M. W.
    (1995) The Xenopus laevis tail-forming region. Development 121, 249–262
    OpenUrlAbstract
    1. Warga R. M.,
    2. Kimmel C. B.
    (1990) Cell movements during epiboly and gastrulation in zebrafish. Development 108, 569–580
    OpenUrlAbstract/FREE Full Text
    1. Wilson V.,
    2. Manson L.,
    3. Skarnes W. C.,
    4. Beddington R. S. P.
    (1995) The T gene is necessary for normal mesodermal morphogenetic cell movements during gastrulation. Development 121, 877–886
    OpenUrlAbstract
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JOURNAL ARTICLES
The development of the posterior body in zebrafish
J.P. Kanki, R.K. Ho
Development 1997 124: 881-893;
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