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Rostro-caudal polarity in the avian somite related to paraxial segmentation

A study on HNK-1, tenascin and neurofilament expression

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Abstract

Segmental organization of the vertebrate body is one of the major patterns arising during embryonic development. Somites that play an important role in this process show intrinsic patterns of gene expression and differentiation. The somites become polarized in all three dimensions, rostrocaudal, mediolateral and dorsoventral, the quadrants giving rise to several tissue components. The timing of polarization was studied by means of antibodies against HNK-1, tenascin and neurofilament. Whole mounts and serial sections of quail and chick embryos show that somites are already polarized at the moment of their segregation from the segmental plate. The rostral hemisomite carries the HNK-1 epitope preferentially, while the caudal hemisomite stains more strongly for tenascin. HNK-1-stained areas in the segmental plate strongly relate to the notochordal sheath, suggesting that axial structures determine the fate of paraxial structures. Neural crest cells were only seen to colonize the rostral part of a somite after they had differentiated into HNK-1 positive cells. Their colonization pattern seems to be guided by the segmental organization of the somite. Moreover, this somite organization probably dictates the organization of both sensory and motor fibres converging towards the segmental dorsal root ganglia, justifying a shift in the connections between neural tube and somites. This segmental shift takes place over one quarter of a somite length in a rostral direction.

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References

  • Abo T, Balch CM (1981) A differentiation antigen of human NK and K cells identified by a monoclonal antibody HNK-1. J Immunol 127:1024–1029

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Bronner-Fraser M (1986) Analysis of early stages of trunk neural crest migration in avian embryos using monoclonal antibody HNK-1. Dev Biol 115:44–55

    CAS  PubMed  Google Scholar 

  • Bronner-Fraser M (1988) Distribution and function of tenascin during cranial neural crest development in the chick. J Neurosci Res 21:135–147

    Google Scholar 

  • Bronner-Fraser M, Stern CD (1991) Effects of mesodermal tissues on avian neural crest cell migration. Dev Biol 143:213–217

    Google Scholar 

  • Chiquet-Ehrismann R (1990) What distinguishes tenascin from fibronectin? FASEB J 4:2598–2604

    Google Scholar 

  • Christ B, Wilting J (1992) From somites to vertebral column. Ann Anat 174:23–32

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Christ B, Jacob HJ, Jacob M (1974) Die Somitogenese beim Hühnerembryo. Zur Determination der Segmentierungsrichtung. Verh Anat Ges 68:573–579

    Google Scholar 

  • Duband JC, Dufour S, Hatta K, Takaichi M, Edelman GM, Thiery J-P (1987) Adhesion molecules during somitogenesis in the avian embryo. J Cell Biol 104:1361–1374

    Article  CAS  PubMed  Google Scholar 

  • Erickson CA, Perris R (1993) The role of cell-cell and cell-matrix interactions in the morphogenesis of the neural crest. Dev Biol 159:60–74

    Google Scholar 

  • Goedbloed JF, Smits-van Prooije AE (1986) A quantitative analysis of the temporal pattern of somite formation in mouse and rat. A simple and accurate method for age determination. Acta Anat 125:76–82

    Google Scholar 

  • Kaehn K, Jacob HJ, Christ B, Hinrichsen H, Poelmann RE (1988) The onset of myotome formation in the chick. Anat Embryol 177:191–201

    CAS  PubMed  Google Scholar 

  • Kalcheim C, Teillet M (1989) Consequences of somite manipulation on the pattern of dorsal root ganglion development. Development 106:85–93

    CAS  PubMed  Google Scholar 

  • Kenny-Mobbs T, Thorogood P (1987) Autonomy of differentiation in avian brachial somites and the influence of adjacent tissues. Development 100:449–462

    Google Scholar 

  • Keynes RJ, Stern CD (1984) Segmentation in the vertebrate nervous system. Nature 310:786–789

    CAS  PubMed  Google Scholar 

  • Kuratani SC, Kirby MC (1991) Initial migration and distribution of the cardiac neural crest in the avian embryo: an introduction to the concept of the circumpharyngeal crest. Am J Anat 191:215–227

    Google Scholar 

  • Lee M-V, Carden MJ, Schlaepfer WW, Trojanowski JQ (1987) Monoclonal antibodies distinguish several differentially phosphorylated states of the two largest rat neurofilament subunits (NF-H and NF-M) and demonstrate their existence in the normal nervous system of adult rats. J Neurosci 7:3474–3488

    Google Scholar 

  • Lim TM, Lunn ER, Keynes RJ, Stern CD (1987) The differing aspects of occipital and trunk somites on neural development in the chick embryo. Development 100:525–533

    Google Scholar 

  • Luider TM, Bravenboer N, Meijers C, Van der Kamp AWM, Tibboel D, Poelmann RE (1993) The distribution and characterization of HNK-1 antigens in the developing avian heart. Anat Embryol 188:307–316

    Google Scholar 

  • Luider TM, Peters-Van der Sanden MJH, Molenaar JC, Tibboel D, Van der Kamp AWM, Meijers C (1992) Characterization of HNK-1 antigens during the formation of the avian enteric nervous system. Development 115:561–572

    Google Scholar 

  • Mackie EJ, Tucker RP, Halfter W, Chiquet-Ehrismann R, Epperlein HH (1988) The distribution of tenascin coincides with pathways of neural crest cell migration. Development 102:237–250

    CAS  PubMed  Google Scholar 

  • Meier S (1979) Development of the chick embryo mesoblast. Formation of the embryonic axis and establishment of the metameric pattern. Dev Biol 73:25–45

    Google Scholar 

  • Newgreen DF, Thiery JP (1980) Fibronectin in early avian embryos: synthesis and distribution along migration pathways of neural crest cells. Cell Tissue Res 211:269–291

    Google Scholar 

  • Newgreen DF, Scheel M, Kastner V (1986) Morphogenesis of sclerotome and neural crest in avian embryos: in vivo and in vitro studies on the role of notochordal extracellular matrix. Cell Tissue Res 244:299–313

    Google Scholar 

  • Newgreen DF, Powell ME, Moser B (1990) Spatiotemporal changes in HNK-1/L2 glycoconjugates on avian embryo somite and neural crest cells. Dev Biol 139:100–120

    Google Scholar 

  • Oakley RA, Tosney KW (1991) Peanut agglutinin and chondroitin-6-sulphate are molecular markers for tissues that act as barriers to axon advance in the avian embryo. Dev Biol 147:187–206

    Google Scholar 

  • Ordahl CP, Le Douarin NM (1992) Two myogenic lineages within the developing somite. Development 114:339–353

    CAS  PubMed  Google Scholar 

  • Ott M, Bober E, Lyons G, Arnold H, Buckingham M (1991) Early expression of the myogenic regulatory gene, myf5, in precursor cells of skeletal muscle in the mouse embryo. Development 111:1097–1107

    CAS  PubMed  Google Scholar 

  • Perris R, Krotoski D, Bronner-Fraser M (1991) Collagens in avian neural crest development: distribution in vivo and migration-promoting ability in vitro. Development 113:969–984

    Google Scholar 

  • Poelmann RE (1981a) The formation of the embryonic mesoderm in the early post-implantation mouse embryo. Anat Embryol 162:29–40

    Google Scholar 

  • Poelmann RE (1981b) The head-process and the formation of the definitive endoderm in the mouse embryo. Anat Embryol 162:41–49

    Google Scholar 

  • Poelmann RE, Gittenberger-De Groot AC, Mentink MMT, Delpech B, Girard N, Christ B (1990) The extracellular matrix during neural crest formation and migration in rat embryos. Anat Embryol 182:29–39

    Google Scholar 

  • Pownall ME, Emerson CP (1992) Sequential activation of three myogenic regulatory genes during somite morphogenesis in quail embryos. Dev Biol 151:67–79

    CAS  PubMed  Google Scholar 

  • Rickmann M, Fawcett J, Keynes RJ (1985) The migration of neural crest cells and the growth of motor axons through the ventral half of the chick somite. J Embryol Exp Morphol 90:437–453

    Google Scholar 

  • Selleck M, Stern BD (1991) Fate mapping and cell lineage analysis of Hensen's node in the chick embryo. Development 112:615–626

    CAS  PubMed  Google Scholar 

  • Smits-Van Prooije AE, Poelmann RE, Dubbeldam JA, Mentink MMT, Vermeij-Keers C (1986) Wheat germ agglutinin-gold as a novel marker for mesectoderm formation in mouse embryos cultured in vitro. Stain Technol 61:97–106

    Google Scholar 

  • Stern CD, Keynes R (1987) Interactions between somite cells: the formation and maintenance of segment boundaries in the chick embry. Development 99:261–272

    Google Scholar 

  • Stern CD, Norris WE, Bronner-Fraser M, Carlson GJ, Faissner A, Keynes RJ, Schachner M (1989) J1/tenascin-related molecules are responsible for the segmented pattern of neural crest cells or motor axons in the chick embryo. Development 107:309–319

    Google Scholar 

  • Stern CD, Jacques KF, Lim TM, Fraser SE, Keynes RJ (1991) Segmental lineage restrictions in the chick embryo spinal cord depend on the adjacent somites. Development 113:239–244

    Google Scholar 

  • Tan SS, Crossin KL, Hoffman S, Edelman GM (1987) Asymmetric expression in somites of cytotactin and its proteoglycan ligand is correlated with neural crest cell distribution. Proc Natl Acad Sci USA 84:7977–7981

    Google Scholar 

  • Teillet M, Kalcheim C, Le Douarin NM (1987) Formation of the dorsal root ganglia in the avian embryo: segmental origin and migratory behavior of neural crest progenitor cells. Dev Biol 120:329–347

    CAS  PubMed  Google Scholar 

  • Verbout AJ (1985) The development of the vertebral column. Adv Anat Embryol Cell Biol 90:1–122

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy and Embryology, University of Leiden, P.O. Box 9602, NL-2300 RC, Leiden, The Netherlands

    Robert E. Poelmann, Monica M. T. Mentink & Adriana C. Gittenberger-de Groot

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  1. Robert E. Poelmann
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  2. Monica M. T. Mentink
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  3. Adriana C. Gittenberger-de Groot
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Poelmann, R.E., Mentink, M.M.T. & Gittenberger-de Groot, A.C. Rostro-caudal polarity in the avian somite related to paraxial segmentation. Anat Embryol 190, 101–111 (1994). https://doi.org/10.1007/BF00193408

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