Skip to main content
Springer Nature Link
Log in

Axial structures control laterality in the distribution pattern of endothelial cells

  • Original Article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

In the midline of the embryo an invisible barrier exists that keeps endothelial cells from migrating to the contralateral side. Interspecific grafting experiments between chick and quail were carried out in order to investigate the role of the axial structures in maintaining this barrier. The quail endothelial cells of the graft were therefore stained with QH1 antibody. In all experimental series quail paraxial mesoderm was used as a source of endothelial cells. First, a quail somite was transplanted either ipsilaterally or contralaterally. The results not only show the existence of laterality in the distribution pattern, but also demonstrate that the laterality does not depend on the origin of the graft but on the environment of the host embryo. Laterality in the distribution pattern of endothelial cells means that the endothelial cells of the two body halves migrate independently and do not change from one side to the other. Single cells do not know whether they are cells from the right or from the left half of the body. In the next series of experiments axial structures were removed in order to modify the barrier. In addition, paraxial mesoderm was exchanged with the corresponding quail tissue in order to determine the migration behaviour of the grafted endothelial cells. The removal of the neural tube does not influence the barrier. After notochordectomy, however, the endothelial cells exhibited a balanced distribution pattern over both halves of the embryo. We concluded that the notochord forms a barrier for endothelial cells that presumably operates on the basis of chemical substances. It is conceivable that our results can explain the lateralization of illnesses of the vascular system, as the Klippel-Trénaunay syndrome or the Sturge-Weber syndrome.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
€32.70 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Finland)

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aoyama H, Asamoto K (1988) Determination of somite cells: independence of cell differentiation and morphogenesis. Development 104: 15–28

    Google Scholar 

  • Artinger KB, Bronner-Fraser M (1992) Notochord grafts do not suppress formation of neural crest cells or commissural neurons. Development 116: 877–886

    Google Scholar 

  • Artinger KB, Bronner-Fraser M (1993) Delayed formation of the floor plate after ablation of the avian notochord. Neuron 11: 1147–1161

    Google Scholar 

  • Baer KE von (1828) Über Entwickelungsgeschichte der Thiere. Beobachtung und Reflexion. Erster Theil. Gebrüder Bonträger, Königsberg

    Google Scholar 

  • Bagnall KM, Higgins SJ, Sanders EJ (1988) The contribution made by a single somite to the vertebral column: experimental evidence in support of resegmentation using the chick-quail chimaera model. Development 103: 69–85

    Google Scholar 

  • Bagnall KM, Higgins SJ, Sanders EJ (1989) The contribution made by cells from a single somite to tissues within a body segment and assessment of their integration with similar cells from adjacent segments. Development 107: 931–943

    Google Scholar 

  • Beer GR de (1926) An introduction to experimental embryology. Clarendon Press, Oxford

    Google Scholar 

  • Bircher AJ, Koo JY, Frieden IJ, Berger TG (1994) Angiodysplastic syndrome with capillary and venous malformation associated with soft tissue hypotrophy. Dermatology 189: 292–296

    Google Scholar 

  • Bober E, Brand-Saberi B, Ebensperger C, Wilting J, Balling R, Paterson BM, Arnold H-H, Christ B (1994) Initial steps of myogenesis in somites are independent of influence from axial structures. Development 120: 3073–3082

    Google Scholar 

  • Bovolenta P, Dodd J (1991) Perturbation of neuronal differentiation and axon guidance in the spinal cord of mouse embryos lacking a floor plate: analysis of Danforth's short tail mutation. Development 113: 625–639

    Google Scholar 

  • Brand-Saberi B, Krenn V, Grim M, Christ B (1993a) Differences in the fibronectin-dependence of migration cell populations. Anat Embryol 187: 17–26

    Google Scholar 

  • Brand-Saberi B, Ebensperger C, Wilting J, Balling R, Christ B (1993b) The ventralizing effect of the notochord on somite differentiation in the chick embryo. Anat Embryol 188: 239–245

    Google Scholar 

  • Brand-Saberi B, Köntges G, Wilting J, Christ B (1994) Die angiogene Potenz von Somiten und Somatopleura bei Vogelembryonen. Verh Anat Ges 89: 128–129

    Google Scholar 

  • Brown NA, Wolpert L (1990) The development of handedness in left/right asymmetry. Development 109: 1–9

    Google Scholar 

  • Brueckner M, McGrath J, D'Eustachio P, Horwich AL (1991) Establishment of left-right asymmetry in vertebrates: genetically distinct steps are involved. In: Biological asymmetry and handedness. Wiley, New York (Ciba Foundation Symposium 162), pp 202–218

    Google Scholar 

  • Child CM (1941) Patterns and problems of development. University of Chicago Press, Chicago

    Google Scholar 

  • Christ B (1970) Experimente zur Lageentwicklung der Somiten. Verh Anat Ges 64: 555–564

    Google Scholar 

  • Christ B, Ordahl CP (1995) Early stages of chick somite development. Anat Embryol 191: 381–396

    Google Scholar 

  • Christ B, Jacob HJ, Jacob M (1972) Experimentelle Untersuchungen zur Somitenentstehung beim Hühnerembryo. Z Anat Entwicklungsgesch 138: 82–97

    Google Scholar 

  • Christ B, Poelmann RE, Mentink MMT, Gittenberger-de Groot AC (1990) Vascular endothelian cells migrate centripetally within embryonic arteries. Anat Embryol 181: 333–339

    Google Scholar 

  • Christ B, Grim M, Wilting J, Kirschhofer K, Wachtler F (1991) Differentiation of endothelial cells in avian embryos does not depend on gastrulation. Acta Histochem 91: 193–199

    Google Scholar 

  • Christ B, Brand-Saberi B, Grim M, Wilting J (1992) Local signalling in dermomyotomal cell type specification. Anat Embryol 186: 505–510

    Google Scholar 

  • Danos MC, Yost HJ (1995) Linkage of cardiac left-right asymmetry and dorsal-anterior development in Xenopus. Development 121:1467–1474

    Google Scholar 

  • Dieterlen-Lièvre F (1984) Emergence of intraembryonic blood stem cells in avian chimeras by means of monoclonal antibodies. Dev Comp Immunol [Suppl] 3: 75–80

    Google Scholar 

  • Ebensperger C, Wilting J, Brand-Saberi B, Mizutani Y, Christ B, Balling R, Koseki H (1995) Pax-1, a regulator of sclerotome development is induced by notochord and floor plate signals in avian embryos. Anat Embryol 191: 297–310

    Google Scholar 

  • Echelard Y, Epstein DP, St.Jacques B, Shen L, Mohler J, McMahon JA, McMahon AP (1993) Sonic hedgehog, a member of a family of putative signalling molecules, is implicated in the regulation of CNS polarity. Cell 75: 1417–1430

    Google Scholar 

  • Feulgen R, Rossenbeck H (1924) Mikroskopisch-chemischer Nachweis einer Nucleinsäure vom Typus der Thymonucleinsäure und die darauf beruhende elektive Färbung von Zellkernen in mikroskopischen Präparaten. Hoppe-Seyler's Z Physiol Chem 135: 203–252

    Google Scholar 

  • Fujinaga M, Baden JM (1991) Evidence for an adrenergic mechanism in the control of body asymmetry. Dev Biol 143: 203–205

    Google Scholar 

  • Goulding MD, Lumsden A, 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

    Google Scholar 

  • Goulding MD, Lumsden A, Paquette AJ (1994) Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 117: 1001–1016

    Google Scholar 

  • Hahn H (1908) Experimentelle Studien über die Entstehung des Blutes und der ersten Gefäße beim Hühnchen. Anat Rec 33: 153–170

    Google Scholar 

  • Hamburger V, Hamburger HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88: 49–82

    Google Scholar 

  • Hanzlik AJ, Binder M, Layton WM, Rowe L, Layton M, Taylor BA, Osemlak MM, Richards JE, Kurnit DM, Stewart GD (1990) The murine situs inversus viscerum (iv) gene responsible for visceral asymmetry is linked tightly to the Igh-C cluster on chromosome 12. Genomics 7: 389–393

    Google Scholar 

  • Hatada Y, Stern CD (1994) A fate map of the epiblast of the early chick embryo. Development 120: 2879–2889

    Google Scholar 

  • Huang WJ, Creath CJ (1994) Klippel-Trénaunay-Weber syndrome: literature review and case report. Pediatr Dent 16: 231–235

    Google Scholar 

  • Huang R, Zhi Q, Wilting J, Christ B (1994) The fate of somitocoele cells in avian embryos. Anat Embryol 190: 243–250

    Google Scholar 

  • Huxley JS, Beer GR de (1934) The elements of experimental embryology. Cambridge, University Press, Cambridge

    Google Scholar 

  • Jacob HJ, Christ B, Jacob M (1974) Die Somitogenese beim Hühnerembryo. Experimente zur Lageentwicklung des Myotom. Verh Anat Ges 68: 581–589

    Google Scholar 

  • Jacob HJ, Christ B, Jacob M (1976) Differenzierung des Neuralrohres. Experimentelle Untersuchungen an Hühner- und Wachtelembryonen. Acta Anat 94: 204–220

    Google Scholar 

  • Jurand A (1962) The development of the notochord in chick embryos. J Embryol Exp Morphol 10: 602–621

    Google Scholar 

  • Kessel M (1991) Molecular coding of axial positions by Hox genes. Semin Dev Biol 2: 367–373

    Google Scholar 

  • Kessel M, Gruss P (1991) Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67: 89–104

    Google Scholar 

  • Khaner O (1993) Axis determination in the avian embryo. Curr Top Dev Biol 28: 155–180

    Google Scholar 

  • Kieny M, Mauger A, Sengel P (1972) Early regionalization of the somitic mesoderm as studied by the development of the axial skeleton of the chick embryo. Dev Biol 28: 142–161

    Google Scholar 

  • Kinutani M, Le Douarin NM (1985) Avian spinal cord chimeras. I. Hatching ability and posthatching survival in homoand heterospecific chimeras. Dev Biol 111: 243–255

    Google Scholar 

  • Kinutani M, Coley M, Le Douarin NM (1986) Postnatal development of a demyelinating disease in avian spinal cord chimeras. Cell 45: 307–314

    Google Scholar 

  • Kochav S, Eyal-Giladi H (1971) Bilateral symmetry in chick embryo determination by gravity. Science 171: 1027–1029

    Google Scholar 

  • Koseki H, Wallin J, Wilting J, Mitzutani Y, Kispert A, Ebensperger C, Herrmann BO, Christ B, Balling R (1993) A role for Pax-1 as a mediator of notochordal signals during the dorsoventral specification of vertebrae. Development 119: 649–660

    Google Scholar 

  • Kosher RA, Lash JW (1975) Notochordal stimulation of in vitro somite chondrogenesis before and after enzymatic removal of perinotochordal materials. Dev Biol 42: 362–378

    Google Scholar 

  • Lawson KA, Meneses JJ, Pedersen RA (1991) Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 113: 891–911

    Google Scholar 

  • Levin M, Johnson RL, Stern CD, Kuehn M, Tabin C (1995) A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 82: 803–814

    Google Scholar 

  • Lipton BH, Jacobson AG (1974a) Analysis of normal somite development. Dev Biol 38: 73–90

    Google Scholar 

  • Lipton BH, Jacobson AG (1974b) Experimental analysis of the mechanisms of somite morphogenesis. Dev Biol 38: 91–103

    Google Scholar 

  • Locke FS, Rosenheim O (1907) Contributions to the physiology of the isolated heart. The consumption of dextrose by mammalian cardiac muscle. J Physiol (Lond) 36: 205–220

    Google Scholar 

  • Martí E, Takada R, Bumcrot DA, Sasaki H, McMahen AP (1995) Distribution of sonic hedgehog peptides in the developing chick and mouse embryo. Development 121: 2537–2547

    Google Scholar 

  • McGrath J, Horwich AL, Brueckner M (1992) Duplication/deficiency mapping of situs inversus viscerum (iv), a gene that determines left-right asymmetry in the mouse. Genomics 14: 643–648

    Google Scholar 

  • Noden DM (1988) Interactions and fates of avian cranofacial mesenchyme. Development [Suppl] 103: 121–140

    Google Scholar 

  • Nicolet G (1971) The young notochord can induce somite genesis by means of diffusible substances in the chick. Experientia 27: 938–939

    Google Scholar 

  • Nuccitelli R, Erickson CA (1983) Embryonic cell motility can be guided by physiological electric fields. Exp Cell Res 147: 195–201

    Google Scholar 

  • Packard DS Jr, Jacobson AG (1976) The influence of axial structures on chick somite formation. Dev Biol 53: 36–48

    Google Scholar 

  • Pardanaud L, Dieterlen-Lièvre F (1993) Emergence of endothelial hemopoietic cells in the avian embryo. Anat Embryol 187: 107–114

    Google Scholar 

  • Pardanaud L, Yassine F, Dieterlen-Lièvre F (1987) Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells Development 100: 339–349

    Google Scholar 

  • Patten BM (1971) Early embryology of the chick, 5th edn. McGraw-Hill, New York London

    Google Scholar 

  • Pettway Z, Guillory G, Bronner-Fraser M (1990) Absence of neural crest cells from the region surrounding implanted notochords in situ. Dev Biol 142: 335–345

    Google Scholar 

  • Placzek M, Tessier-Lavigne M, Jessell TM, Dodd J (1990a) Orientation of commissural axons in vitro in response to a floor plate-derived chemoattractant. Development 110: 19–30

    Google Scholar 

  • Placzek M, Tessier-Lavigne M, Yamada T, Jessell T, Dodd J (1990b) Mesodermal control of neural cell identity: floor plate induction by the notochord. Science 250: 985–988

    Google Scholar 

  • Placzek M, Yamada T, Tessier-Lavigne M, Jessell T, Dodd J (1991) Control of dorsoventral pattern in vertebrate neural development: induction and polarizing properties of the floor plate. Development [Suppl] 2: 105–122

    Google Scholar 

  • Placzek M, Jessell TM, Dodd J (1993) Induction of floor plate differentiation by contact-dependent, homeogenetic signals. Development 117: 205–218

    Google Scholar 

  • Reagan FP (1915) Vascularisation phenomena in fragments of embryonic bodies completely isolated from yolk-sac blastoderm. Anat Rec 9: 329–341

    Google Scholar 

  • Riddle R, Johnson RL, Laufer E, Tabin C (1993) Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75: 1401–1416

    Google Scholar 

  • Ruggeri A (1972) Ultrastructural histochemical and autoradiographic studies on the developing chick notochord. Z Anat Entwicklungsges 138: 20–33

    Google Scholar 

  • Rugh R (1962) Experimental embryology: a manual of techniques and procedures, 3rd edn. Burgess, Minneapolis

    Google Scholar 

  • Serra JA (1946) Histochemical tests for proteins and amino acids; the characterisation of basic proteins. Stain Technol 21: 5–18

    Google Scholar 

  • Smith JL, Schoenwolf GC (1987) Cell cycle and neuroepithelial cell shape during bending of the chick neural plate. Anat Rec 218: 196–206

    Google Scholar 

  • Smith JL, Schoenwolf GC (1989) Notochordal induction of cell wedging in the chick neural plate and its role in neural tube formation. J Exp Zool 250: 49–62

    Google Scholar 

  • Steding G (1962) Experimente zur Morphogenese des Rückenmarkes. Untersuchung an Hühnerembryonen (Gallus gallus). Acta Anat 49: 199–231

    Google Scholar 

  • Straaten HWM van, Hekking JWM (1991) Development of floor plate, neurons and axonal outgrowth pattern in the early spinal cord of the notochord-deficient chick embryo. Anat Embryol 184: 55–63

    Google Scholar 

  • Straaten HWM van, Hekking JWM, Thors F, Wiertz-Hoessels ELMJ, Drukker J (1985) Induction of an additional floor plate in the neural tube. Acta Morphol Neerl-Scand 23: 91–97

    Google Scholar 

  • Straaten HWM van, Hekking JWM, Wiertz-Hoessels EJLM, Thors F, Druker 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

    Google Scholar 

  • Straaten HWM van, Hekking JWM, Beursgens JPWM, Terwindt-Rouwenhorst E, Drukker J (1989) Effect of the notochord on proliferation and differentiation in the neural tube of the chick embryo. Development 107: 793–803

    Google Scholar 

  • Strudel G (1970) Etude des conséquences d'excisions de somites sur l'organogenèse du tube nerveux et de ses annexes chez l'embryon de poulet. C R Acad Sci Ser D 270: 128–130

    Google Scholar 

  • Stump RF, Robinson KR (1983) Xenopus neural crest cell migration in an applied electrical field. Cell Biol 97: 1226–1233

    Google Scholar 

  • Tessier-Lavigne M, Placzek M, Lumsden AGS, Dodd J, Jessell TM (1988) Chemotropic guidance of developing axons in the mammalian central nervous system. Nature 336: 775–778

    Google Scholar 

  • Veini M, Bellairs R (1991) Early mesoderm differentiation in the chick embryo. Anat Embryol 183: 143–149

    Google Scholar 

  • Vintemberger P, Clavert J (1960) Sur le détermination de la symétrie bilatérale chez les Oiseaux. XIII. Les facteurs de l'orientation de l'embryon par rapport à l'axe de l'œuf et la règle de von Baer, à la lumière de nos expériences d'orientation dirigée sur l'œuf de poule extrait de l'utérus. C R Seances Soc Biol Fil 154: 1072–1076

    Google Scholar 

  • Wachtler F, Christ B, Jacob HJ (1982) Grafting experiments on determination and migratory behaviour of presomitic, somitic and somatopleural cells in avian embryos. Anat Embryol 164: 369–378

    Google Scholar 

  • Watterson RL, Goodheart CR, Lindberg G (1955) The influence of adjacent structures upon the shape of the neural tube and neural plate of chick embryos. Anat Rec 122: 539–559

    Google Scholar 

  • Wilms P, Christ B, Wilting J, Wachtler F (1991) Distribution and migration of angiogenic cells from grafted avascular intraembryonic mesoderm. Anat Embryol 183: 371–377

    Google Scholar 

  • Wilting J, Christ B (1995) Naturwissenschaften (in press)

  • Wilting J, Christ B, Grim M, Wilms P (1992) Angiogenic capacity of early avian mesoderm. In: Bellairs R, Sanders EJ, Lash JW (eds) Formation and differentiation of early embryonic mesoderm. Plenum Press, New York

    Google Scholar 

  • Wilting J, Brand-Saberi B, Huang R, Zhi Q, Köntges G, Ordahl CP, Christ B (1995) Angiogenic potential of the avian somite. Dev Dyn 202: 165–171

    Google Scholar 

  • Yamada T, Placzek M, Tanaka H, Dodd J, Jessell TM (1991) Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord. Cell 64: 635–647

    Google Scholar 

  • Yokoyama T, Copeland NG, Jenkins NA, Montgomery CA, Elder FFB, Overbeek PA (1993) Reversal of left-right asymmetry: a situs inversus mutation. Science 260: 679–682

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Anatomy, University of Freiburg, P.O. Box 111, D-79001, Freiburg, Germany

    Stephan Klessinger & Bodo Christ

Authors
  1. Stephan Klessinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bodo Christ
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Klessinger, S., Christ, B. Axial structures control laterality in the distribution pattern of endothelial cells. Anat Embryol 193, 319–330 (1996). https://doi.org/10.1007/BF00186689

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00186689

Key words

Search

Navigation