Skip to main content
Log in

Pax-1 in the development of the cervico-occipital transitional zone

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

Abstract

The Pax-1 gene has been found to play an important role in the development of the vertebral column. The cervico-occipital transitional zone is a specialized region of the vertebral column, and malformations of this region have frequently been described in humans. The exact embryonic border between head and trunk is a matter of controversy. In order to determine a possible role of Pax-1 in the development of the cervico-occipital transitional zone we studied the expression of this gene in a series of quail embryos and murine fetuses with in situ hybridization and immunohistochemistry. Pax-1 is expressed in all somites of the embryo, including the first five occipital ones. During embryonic days 3–5 the gene is down-regulated in the caudal direction within the first five somites, whereas more caudally Pax-1 is strongly expressed in the cells of the perinotochordal tube. In 5-day-old quail embryos, the cartilaginous anlage of the basioccipital bone has developed and there is no more expression of Pax-1 in this region. The fusion of the dens axis with the body of the axis also coincides with switching off of the Pax-1 gene. More caudally, the gene is continuously expressed in the intervertebral discs of murine embryos and therefore seems to be important for the process of resegmentation. Quail embryos do not possess permanent intervertebral discs. “Hyper-” or “hyposegmentation” defects may be explained by an over- or under-expression of Pax-1 during development. We also reinvestigated the border between the head and trunk in chick embryos by performing homotopical grafting experiments of the 5th somite between chick and quail embryos. Grafted quail cells formed mainly the caudal end of the basioccipital bone. They were also located in the cranial half of the ventral atlantic arch, and only a few cells were found in the tip of the dens axis.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Albrecht P (1880) Über den Proatlas, einen zwischen dem Occipitale und dem Atlas der amnioten Wirbelthiere gelegenen Wirbel, und den Nervus spinalis I s. proatlanticus. Zool Anz 3:450–454; 472–478

    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 chimera-model. Development 103:69–85

    Google Scholar 

  • Balling R, Deutsch U, Gruss P (1988) Undulated, a mutation affecting the development of the mouse skeleton, has a point mutation in the paired box of Pax-1. Cell 55:531–535

    Google Scholar 

  • Barge JAJ (1918) Probleme im Kranio-Vertebralgebiet. Verh K Akad Wet Amsterdam (Tweede Sectie). Deel. XX, no 2. Müller, Amsterdam

    Google Scholar 

  • Blechschmidt E (1961) The stages of human development before birth. Karger, Basel London New York, pp 1–684

    Google Scholar 

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

    Google Scholar 

  • Bystrow OP (1931) Assimilation des Atlas und Manifestation des Proatlas. Z Anat Entwicklungsgesch 95:210–242

    Google Scholar 

  • Chalepakis G, Fritsch R, Fickenscher H, Deutsch U, Goulding M, Gruss P (1991) The molecular basis of the undulated/Pax-1 mutation. Cell 66:873–884

    Google Scholar 

  • Charité J, Graaff W de, Shen S, Dechamps J (1994) Ectopic expression of Hoxb-8 causes duplication of the ZPA in the forelimb and homeotic transformation of axial structures. Cell 78:589–601

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Condie BG, Capecchi MR (1994) Mice with targeted disruptions in the paralogous genes hoxa-3 and hoxd-3 reveal synergistic interactions. Nature 370:304–307

    Google Scholar 

  • Couly GF, Coltey PM, Le Douarin NM (1993) The triple origin of the skull in higher vertebrates: a study in quail-chick chimeras. Development 117:409–429

    Google Scholar 

  • Deutsch U, Dressler GR, Gruss P (1988) Pax 1, a member of a paired box homologous murine gene family, is expressed in segmented structures during development. Cell 53:617–625

    Google Scholar 

  • Dietrich S, Schubert FR, Gruss P (1993) Altered Pax gene expression in murine notochord mutants: the notochord is required to initiate and maintain ventral identity in the somite. Mech Dev 44:189–207

    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 

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

    Google Scholar 

  • Froriep A (1883) Zur Entwicklungsgeschichte der Wirbelsäule, insbesondere des Atlas und Epistropheus und der Occipitalregion. Arch Anat Physiol Anat Abt 177–234

  • Glaesmer E (1909) Die Atlanto-Occipital-Synostose. Über ihre pathologischen und morphologischen Ursachen auf Grund eines Weichteilpräparates. Anat Anz 36:129–148.

    Google Scholar 

  • Hadley LA (1948) Atlanto-occipital fusion, ossiculum terminale, occipitale vertebra as related to basilar impression with neurological symptoms. Am J Roentgenol 59:511–524

    Google Scholar 

  • Hayek H von (1923) Über den Proatlas und über die Entwicklung der Kopfgelenke beim Menschen und bei einigen Säugetieren. Sitzungsber Akad Wiss Wien, Math Naturwiss Kl Abt 3 130/131:25–60

    Google Scholar 

  • Hayek H von (1924) Über das Schicksal des Proatlas und über die Entwicklung der Kopfgelenke bei Reptilien und Vögeln. Morphol Jahrb 53:137–163

    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 

  • Hunter RH (1923) An abnormal atlas. J Anat 58:140–141

    Google Scholar 

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

    Google Scholar 

  • Jenkins FA (1969) The evolution and development of the dens of the mammalian axis. Anat Rec 164:173–184

    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 a Hox-1.1 transgene in mice. Cell 61:301–308

    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 

  • Kladetzky J (1954) Zur Entwicklung des Dens epistrophei. Morphol Jahrb 94:520–550

    Google Scholar 

  • Koseki H, Wallin J, Wilting J, Mizutani Y, Kispert A, Ebensperger C, Herrmann BG, 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 

  • Le Douarin NM (1969) Particularités du noyau interphasique chez la caille japonaise (Coturnix coturnix japonica). Utilisation de ces particularités comme “marquage biologique” dans les recherches sur les interactions tissulaires et les migrationes cellulaires au cours de l'ontogenèse. Bull Biol Fr Belg 103:435–452

    Google Scholar 

  • Lewis EB (1978) A gene complex controlling segmentation in Drosophila. Nature 276:565–570

    Google Scholar 

  • Müller F, O'Rahilly R (1994) Occipitocervical segmentation in staged human embryos. J Anat 185:251–258

    Google Scholar 

  • Putz R (1975) Zur Manifestation der hypochordalen Spangen im cranio-vertebralen Grenzgebiet beim Menschen. Anat Anz 137:65–74

    Google Scholar 

  • Reiter A (1944) Die Frühentwicklung der menschlichen Wirbelsäule. II. Mitteilung: Die Entwicklung der Occipitalsegmente und der Halswirbelsäule. Z Anat Entwicklungsgesch 113:66–104

    Google Scholar 

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

    Google Scholar 

  • Rentrop M, Knapp B, Winter H, Schweizer J (1986) Differential localization of distinct keratin RNA-species in mouse tongue epithelium by in situ hybridization with specific cDNA probes. J Cell Biol 103:2583–2591

    Google Scholar 

  • Rosen B, Beddington RSP (1993) Whole-mount in situ hybridization in the mouse embryo: gene expression in three dimensions. Trends Genet 9:162–167

    Google Scholar 

  • Sensenig EC (1957) The development of the occipital and cervical segments and their associated structures in human embryos. Contrib Embryol Carnegie Inst 36:141–151

    Google Scholar 

  • Serra JA (1946) Histochemical tests for protein and aminoacids: the characterization of basic proteins. Stain Technol 21:5–18

    Google Scholar 

  • Timmons PM, Wallin J, Rigby PWJ, Balling R (1994) Expression and function of Pax-1 during development of the pectoral girdle. Development 120:2773–2785

    Google Scholar 

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

    Google Scholar 

  • Wallin J, Wilting J, Koseki H, Fritsch R, Christ B, Balling R (1994) The role of Pax-1 in axial skeleton development. Development 120:1109–1121

    Google Scholar 

  • Wilting J, Kurz H, Brand-Saberi B, Steding G, Yang YX, Hasselhorn HM, Epperlein HH, Christ B (1994) Kinetics and differentiation of somitic cells forming the vertebral column: studies on human and chick embryos. Anat Embryol 190:573–581

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wilting, J., Ebensperger, C., Müller, T.S. et al. Pax-1 in the development of the cervico-occipital transitional zone. Anat Embryol 192, 221–227 (1995). https://doi.org/10.1007/BF00184746

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00184746

Key words

Navigation