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Kinetics and differentiation of somite cells forming the vertebral column: studies on human and chick embryos

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Abstract

We have studied the kinetics of somite cells with an antibody against proliferating cell nuclear antigen (PCNA/cyclin) in human and chick embryos, and with the BrdU anti-BrdU method in chick embryos, to investigate whether the metameric pattern of the developing vertebral column can be explained by different proliferation rates. Furthermore we applied antibodies against differentiation markers of chondrogenic and myogenic cells of the somites in order to study the correlation between proliferation and differentiation. There are no principal differences in the proliferation pattern of the vertebral column between human and chick embryos. In all stages examined, the cell density is higher in the caudal sclerotome halves than in the cranial halves. Laterally, the caudal sclerotome halves, which give rise to the neural arches, are characterized by a higher proliferative activity than the cranial halves. Although there is a high variability, the labelling indices show significant differences between the two halves with both proliferation markers. With the onset of chondrogenic differentiation, only the perichondrial cells retain a high proliferation rate. During fetal development, the neural arches and their processes grow appositionally. Even at the earliest stages, there is practically no immunostaining for PCNA or BrdU in the desmin-positive myotome cells of human and chick embryos. Axially, a higher proliferation rate is found in the condensed mesenchyme of the anlagen of the intervertebral discs than in the anlagen of the vertebral bodies. During fetal development, cells at the borders between vertebral bodies and intervertebral discs proliferate, indicating appositional growth. Our results show that local differences in the proliferation rates of the paraxial mesoderm exist, and may be an important mechanism for the establishment of the metameric pattern of the vertebral column in human and chick embryos.

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References

  • Bagnall KM, Sanders EJ (1989) The binding pattern of peanut lectin associated with sclerotome migration and the formation of the vertebral axis in the chick embryo. Anat Embryol 180:505–513

    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

    CAS  PubMed  Google Scholar 

  • Baur R (1969) Zum Problem der Neugliederung der Wirbelsäule. Acta Anat 72:321–356

    Google Scholar 

  • Blechschmidt E (1957) Die Entwicklungsbewegungen der Somiten und ihre Bedeutung für die Gliederung der Wirbelsäule. Z Anat Entwicklungsgesch 120:150–172

    Google Scholar 

  • Blechschmidt E (1960) The stages of human development before birth. An introduction to human embryology. Karger, Basel

    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 (1978) On the formation of the myotomes in avian embryos. An experimental and scanning electron microscopic study. Experientia 34:514–516

    Google Scholar 

  • Christ B, Jacob HJ, Jacob M (1979) Über die Gestaltungsfunktionen der Somiten bei der Entwicklung der Körperwand von Hühnerembryonen. Verh Anat Ges 73:509–518

    Google Scholar 

  • Dalgleish AE (1985) A study of the development of thoracic vertebrae in the mouse assisted by autoradiography. Acta Anat 122:91–98

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ebner von E (1888) Urwirbel und Neugliederung der Wirbelsäule. Sitzungsber Akad Wiss Wien III/97:194–206

    Google Scholar 

  • Elias H, Hyde DM (1980) Elementary stereology. Am J Anat 159:411–446

    Google Scholar 

  • Götz W, Fischer G, Herken R (1991) Lectin binding pattern in the embryonal and early fetal human vertebral column. Anat Embryol 184:345–353

    Google Scholar 

  • Gratzner HG (1982) Monoclonal antibody to 5-bromo 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218:474–475

    Google Scholar 

  • Hall PA, Levison DA, Woods AL, Yu CC-W, Kellock DB, Watkins JA (1990) Proliferating cell nuclear antigen (PCNA) immunolocalization in paraffin sections: an index of cell proliferation with evidence of deregulated expression in some neoplasms. J Pathol 162:285–294

    Google Scholar 

  • Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Exp Zool 80:347–389

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Jacob M, Christ B, Jacob HJ (1975a) Über die regionale Determination des paraxialen Mesoderms junger Hühnerembryonen. Verh Anat Ges 69:263–269

    CAS  PubMed  Google Scholar 

  • Jacob M, Jacob HJ, Christ B (1975b) Die frühe Differenzierung des chordanahen Bindegewebes. Raster- und transmissionselektronenmikroskopische Untersuchungen an Hühnerembryonen. Experientia 31:1083–1086

    CAS  PubMed  Google Scholar 

  • Jacob M, Christ B, Jacob HJ, Poelmann R (1991) The role of fibronectin and laminin in development and migration of the avian Wolffian duct with refence to somitogenesis. Anat Embryol 183:385–395

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kessel M, Gruss P (1991) Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67:1–20

    Google Scholar 

  • Kessel M, Balling R, Gruss P (1990) Variations of cervical vertebrae after expression of Hox-1.1 transgene in mice. Cell 61:301–308

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Langman J, Nelson GR (1968) A radioautographic study of the development of the somite in the chick embryo. J Embryol Exp Morphol 19/2:217–226

    Google Scholar 

  • Lee SH, Hurwitz J (1990) Mechanism of elongation of primed DNA by DNA polymerase delta, proliferating cell nuclear antigen, and activator 1. Proc Natl Acad Sci USA 87:5672–5676

    Google Scholar 

  • Levine M, Rudin GM, Tjian R (1984) Human DNA sequences homologous to a protein coding region conserved between homoetic genes of Drosophila. Cell 38:667–673

    Google Scholar 

  • Mathews MB, Bernstein RM, Franza BR Jr, Garrels JI (1984) Identity of the proliferating cell nuclear antigen and cyclin. Nature 309:374–376

    Google Scholar 

  • Miyachi K, Fritzler MJ, Tan EM (1978) Autoantibody to a nuclear antigen in proliferating cells. J Immunol 121:2228–2234

    Google Scholar 

  • Murakami G, Nakamura H (1991) Somites and the pattern formation of trunk muscles: a study in quail-chick chimera. Arch Histol Cytol 54:249–258

    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 

  • Ranscht B, Bronner-Fraser M (1991) T-cadherin expression alternates with migrating neural crest cells in the trunk of the avian embryo. Development 111:15–22

    Google Scholar 

  • Remak R (1855) Untersuchungen über die Entwicklung der Wirbeltiere. Reimer, Berlin

    Google Scholar 

  • Shrestha P, Yamada K, Wada T, Maeda S, Watatani M, Yasutomi M, Takagi H, Mori M (1992) Proliferating cell nuclear antigen in breast lesions: correlation of c-erbB- 2 oncoprotein and EGF receptor and its clinicopathological significance in breast cancer. Virchows Archiv A Pathol Anat Histopathol 421:193–202

    Google Scholar 

  • Siegel S (1956) Nonparametric statistics. McGraw-Hill, New York

    Google Scholar 

  • Sterio DC (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134:127–136.

    PubMed  Google Scholar 

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

    Google Scholar 

  • Stern CD, Sisodiya SM, Keynes RJ (1986) Interactions between neurites and somite cells: inhibition and stimulation of nerve growth in the chick embryo. J Embryol Exp Morphol 91:209–226

    Google Scholar 

  • Sternberger LA (1979) Immunocytochemistry, 2nd edn. Wiley, New York

    Google Scholar 

  • Takasaki Y, Fishwild D, Tan EM (1984) Characterization of proliferating cell nuclear antigen recognized by autoantibodies in lupus sera. J Exp Med 159:981–992

    Google Scholar 

  • Trelstad RL (1977) Mesenchymal cell polarity and morphogenesis of chick cartilage. Dev Biol 59:153–163

    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 

  • Waseem NH, Lane DP (1990) Monoclonal antibody analysis of the proliferating cell nuclear antigen (PCNA). Structural conversation and the detection of a nucleolar form. J Cell Sci 96:121–129

    Google Scholar 

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Wilting, J., Kurz, H., Brand-Saberi, B. et al. Kinetics and differentiation of somite cells forming the vertebral column: studies on human and chick embryos. Anat Embryol 190, 573–581 (1994). https://doi.org/10.1007/BF00190107

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