Skip to main content
Log in

Pax-1, a regulator of sclerotome development is induced by notochord and floor plate signals in avian embryos

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

Abstract

Pax-1 encodes for a DNA-binding transcriptional activator that was originally discovered in murine embryos using a probe from the Drosophila paired-box-containing gene, gooseberry-distal. We have cloned the avian Pax-1 gene as a basis for experimental studies of the induction of Pax-1 in the paraxial mesoderm. The amino acid sequence of the paired-domain is exactly the same in the quail and mouse, whereas outside the paired-domain there is 61% homology. Starting at about the eight-somite stage, quail Pax-1 is expressed in the paraxial mesoderm in a craniocaudal sequence. The unsegmented paraxial mesoderm and the two most recently formed somites do not express Pax-1. In the epithelial somite, the somitocoele cells and the cells of the ventral two-thirds of the epithelial wall are positive. As soon as the sclerotome is formed, only a subset of sclerotome cells expresses Pax-1. These are the cells that migrate towards the notochord to form the perinotochordal tube. Expression then becomes restricted to the intervertebral discs, the perichondrium of the vertebral bodies and the connective tissue surrounding the spinal ganglia. Additional expression domains are found in the scapula and the pelvic region, distinct areas of the head, and the epithelium of the second to the fourth visceral pouch. In later stages the thymus is positive. In vitro and in vivo experiments show that the notochord induces Pax-1 in the paraxial mesoderm, but limb bud mesoderm is not competent to respond to notochordal signals. Floor plate is also capable of inducing Pax-1 expression in sclerotome cells. Our studies show that in competent cells of the paraxial mesoderm, Pax-1 is a mediator of signals emanating from the notochord and the floor plate.

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

  • Avery G, Chow M, Holtzer H (1956) An experimental analysis of the development of the spinal column. V. Reactivity of chick somites. J Exp Zool 132:409–426

    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 

  • Balling R, Ebensperger C, Hoffmann I, Imai K, Koseki H, Mizutani Y, Wallin J (1993) The genetics of skeletal development. Ann Genet 36:56–62

    Google Scholar 

  • Baumgartner S, Bopp D, Burri M, Noll M (1987) Structure of two genes at the gooseberry locus related to the paired gene and their spatial expression during embryogenesis. Genes Dev 1:1247–1267

    Google Scholar 

  • Bellairs R (1963) The development of the somites in the chick embryo. J Embryol exp Morphol 11:697–714

    Google Scholar 

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

    Google Scholar 

  • Bopp D, Burri M, Baumgartner S, Frigerio G, Noll M (1986) Conservation of a large protein domain in the segmentation gene paired and in functionally related genes of Drosophila. Cell 47:1033–1040

    Google Scholar 

  • Bopp D, Jamet E, Baumgartner S, Burri M, Noll M (1989) Isolation of two tissue-specific Drosophila paired box genes, pox meso and pox neuro. EMBO J 8:3447–3457

    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 embryos. Anat Embryol 188:239–245

    Google Scholar 

  • Braun T, Rudnicki MA, Arnold HH, Jaenisch R (1992) Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell 71:369–382

    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 

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

    Google Scholar 

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

    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 

  • 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 

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

    Google Scholar 

  • Eichmann A, Marcelle C, Bréant C, Le Douarin N (1993) Two molecules related to the VEGF-receptor are expressed in early endothelial cells during avian embryonic development. Mech Dev 42:33–48

    Google Scholar 

  • Gonda TJ, Sheiness DK, Bishop JM (1982) Transcripts from the cellular homologues of retroviral oncogenes: distribution among chicken tissues. Mol Cell Biol 2:617–624

    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 M, Lumsden A, Paquette AJ (1994) Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 120:957–971

    Google Scholar 

  • Grobstein C, Holtzer H (1955) In vitro studies of cartilage induction in mouse somite mesoderm. J Exp Zool 128:333–357

    Google Scholar 

  • Grobstein C, Parker G (1954) In vitro induction of cartilage in mouse somite mesoderm by embryonic spinal cord. Proc Soc Exp Biol Med 85:477–481

    Google Scholar 

  • Gruss P, Walther C (1992) Pax in development. Cell 69:719–722

    Google Scholar 

  • Halpern ME, Ho RK, Walker C, Kimmel CB (1993) Induction of muscle pioneers and floor plate is distinguished by the zebrafish no tail mutation. Cell 75:99–111

    Google Scholar 

  • Hamburger V, Hamilton H (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92

    Google Scholar 

  • Hopp TP, Woods KR (1981) Prediction of protein antigenic determinants from amino acid sequences. Proc Natl Acad Sci USA 78:3824–3828

    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 

  • 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 

  • 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 

  • 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 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Google Scholar 

  • Le Douarin N (1971) Caractéristiques ultrastructurales du noyau interphasique chez la caille et chez le poulet et utilisation de cellules de caille comme “marqueurs biologiques” en embryologie expérimentale. Ann Embryol Morphol 4:125–135

    Google Scholar 

  • Lipman DJ, Pearson WR (1985) Rapid and sensitive protein similarity searches. Science 227:1435–1441

    Google Scholar 

  • Love JM, Tuan RS (1993) Pair-rule gene expression in the somitic stage chick embryo: association with somite segmentation and border formation. Differentiation 54:73–83

    Google Scholar 

  • Maulbecker CC, Gruss P (1993) The oncogenic potential of Pax genes. EMBO J 12:2361–2367

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Pourquié O, Coltey M, Teillet MA, Ordahl C, Le Douarin N (1993) Control of dorsoventral patterning of somitic derivatives by notochord and floor plate. Proc Natl Acad Sci USA 90:5242–5246

    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 

  • Rong PM, Teillet MA, Ziller C, Le Douarin NM (1992) The neural tube/notochord complex is necessary for verterbal but not limb and body wall striated muscle differentiation. Development 115:657–672

    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 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Strudel GL (1955) L'action morphogène du tube nerveux et de la corde sur la différenciation des vertèbres et des muscles vertébraux chez l'embryon de poulet. Arch Anat Microsc Morphol Exp 44:209–235

    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 

  • Wallin J, Mizutani Y, Imai K, Miyashita N, Moriwaki K, Taniguchi M, Koseki H, Balling R (1993) A new Pax gene, Pax-9, maps to mouse chromosome 12. Mamm Genome 4:354–358

    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 

  • Walther C, Guenet JL, Simon D, Deutsch U, Jostes B, Goulding M, Plachov D, Balling R, Gruss P (1991) Pax: a murine multigene family of paired box containing genes. Genomics 11:424–434

    Google Scholar 

  • Watterson RL, Fowler I, Fowler BJ (1954) The role of the neural tube and notochord in development of the axial skeleton of the chick. Am J Anat 95:337–397

    Google Scholar 

  • Williams B A, Ordahl C (1994) Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification. Development 120:785–796

    Google Scholar 

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

    Google Scholar 

  • Yamada T, Pfaff SL, Edlund T, Jessell TM (1993) Control of cell pattern in the neural tube: motor neuron induction by diffusible factors from the notochord and floor plate. Cell 73:673–686

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ebensperger, C., Wilting, J., Brand-Saberi, B. et al. Pax-1, a regulator of sclerotome development is induced by notochord and floor plate signals in avian embryos. Anat Embryol 191, 297–310 (1995). https://doi.org/10.1007/BF00534682

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00534682

Key words

Navigation