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Differential regulation of avian pelvic girdle development by the limb field ectoderm

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Abstract

Although limb development has been a subject of intense research over the last decades, development of the girdles has been poorly investigated. Particularly, a detailed analysis of pelvic girdle development including functional data is not available to date. Here, we describe the early steps of the formation of mesenchymal and cartilaginous anlagen of the pelvic elements using alcian blue staining in whole mount embryos and serial histological sections, and the expression pattern of several marker genes to provide an operative basis for further research in pelvis development. Moreover, we describe pelvis development after unilateral hindlimb bud amputation and somatopleural ectoderm extirpation. We show for the first time, that ectodermal signals at pre-limb bud stages are required for pelvis formation. We present evidence suggesting that the regulation of ilium development is different from the development of ischium and pubis.

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References

  • Akiyama H, Chaboissier MC, Martin JF, Schedl A, de Crombrugghe B (2002) The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev 16:2813–2828

    Article  PubMed  CAS  Google Scholar 

  • Bardeen CR, Lewis WH (1901) Development of the limbs, body-wall and back in man. Amer J Anat 11:3

    Google Scholar 

  • Baumel JJ, King AS, Lucas AM, Breazile JE, Evans HE (1979) fNomina Anatomica Avium (An annotated anatomical dictionary of birds). Academic, London

    Google Scholar 

  • Bell E, Ensini M, Gulisano M, Lumsden A (2001) Dynamic domains of gene expression in the early avian forebrain. Dev Biol 236:76–88

    Article  PubMed  CAS  Google Scholar 

  • Boas JEV (1933) Kreuzbein, Becken, und Plexus lumbosacralis der Vogel. Mem l‘Acad Roy Sci Lettr Danemark 5:1–74

    Google Scholar 

  • Borkhvardt VG (1995) On the formation of sacroiliac skeletal complex in the onthogenesis (sic) of Tetrapoda (in Russian). Zool Zhurn 74:84–94

    Google Scholar 

  • Borkhvardt VG, Malashichev YB (2000) Correlative changes during early morphogenesis of the sacroiliac complex in squamate reptiles. Ann Anat (Anat Anz) 182:439–444

    Article  CAS  Google Scholar 

  • Capdevila J, Izpisua Belmonte JC (2001) Patterning mechanisms controlling vertebrate limb development. Annu Rev Cell Dev Biol 17:87–132

    Article  PubMed  CAS  Google Scholar 

  • Carrington JL, Fallon JF (1988) Initial limb budding is independent of apical ectodermal ridge activity; evidence from a limbless mutant. Development 104:361–367

    PubMed  CAS  Google Scholar 

  • Chevallier A (1977) Origine des ceintures scapulaires et pelviennes chez l’embryon d’oiseau. J Embryol exp Morphol 42:275–292

    Google Scholar 

  • Dudley AT, Ros MA, Tabin C (2002) A re-examination of proximodistal patterning during vertebrate limb development. Nature 418:539–544

    Article  PubMed  CAS  Google Scholar 

  • Elliot AM, Roeder ER, Witt DR, Rimon DL, Lachman RS (2000) Scapuloiliac dysostosis (Kosenow syndrome, pelvis–shoulder dysplasia) spectrum: three additional cases. Am J Med Genet 95:496–506

    Article  PubMed  Google Scholar 

  • Fallon JF, Frederick JM, Carrington JL, Lanser ME, Simandl BK (1983) Studies on a limbless mutant in the chick embryo. Prog Clin Biol Res 110 Pt A, 33–43

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Hauser SE, Chemke JM, Bankier A (1998) Pelvis–shoulder dysplasia. Pediatr Radiol 28:681–682

    Article  PubMed  CAS  Google Scholar 

  • Hosokawa H (1951) On the pelvic cartilages of the Balaenoptera foetuses, with remarks on the specifical and sexual difference. Sci Rep Whales Res Inst Tokyo 5:5–15

    Google Scholar 

  • Huang R, Zhi Q, Patel K, Wilting J, Christ B (2000) Dual origin and segmental organization of the avian scapula. Development 127:3789–3794

    PubMed  CAS  Google Scholar 

  • Johnson A (1893) On the development of the pelvic girdle and skeleton of the hind-limb in the chick. Quart J Micr Sci 23(pls 26, 27):399–411

    Google Scholar 

  • Kant R, Goldstein RS (1999) Plasticity of axial identity among somites: cranial somites can generate vertebrae without expressing HOX genes appropriate to the trunk. Dev Biol 216:507–520

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Kuijper S, Beverdam A, Kroon C, Brouwer A, Candille S, Barsh G, Meijlink F (2005) Genetics of shoulder girdle formation: roles of Tbx15 and aristaless-like genes. Development 132:1601–1610

    Article  PubMed  CAS  Google Scholar 

  • Laing NG (1982) Abnormal development of vertebrae in paralyzed chick embryos. J Morphol 173:179–184

    Article  PubMed  CAS  Google Scholar 

  • Lebedinsky NG (1913) Beitrage zur Morphologie und Entwicklungsgeschichte des Vogelbeckens. Jen Zeitschr Naturwissenschaft 50:647–714

    Google Scholar 

  • Malashichev Y,M (2001) Sacrum and pelvic girdle development in Lacertidae. Russ J Herpetol 8:1–16

    Google Scholar 

  • McGowan C, Motani R (2003) Ichthyopterygia. Handbook of paleontology. Verlag Dr Friedrich Pfeil, Munchen,

    Google Scholar 

  • Mehnert E (1887) Untersuchungen über die Entwicklung des Os pelvis der Vögel. Morph Jahrb 13:259–295

    Google Scholar 

  • Nickel R, Schummer A, Seiferle E (1992) Lehrbuch der Anatomie der Haustiere. In: Band V Anatomie der Vögel Parey, Berlin

  • Nieto MA, Patel K, Wilkinson DG (1996) In situ hybridization analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol 51:219–235

    Article  PubMed  CAS  Google Scholar 

  • Niswander L (2002) Interplay between the molecular signals that control vertebrate limb development. Int J Dev Biol 46:877–881

    PubMed  CAS  Google Scholar 

  • Ordahl CP, Christ B (1998) Avian somite transplantation: a review of basic methods. Meth Cell Biol 52:3–27

    Google Scholar 

  • Pellegrini M, Pantano S, Fumi MP, Lucchini F, Forabosco A (2001) Agenesis of the scapula in Emx2 homozygous mutants. Dev Biol 232:149–156

    Article  PubMed  CAS  Google Scholar 

  • Prahlad KV, Skala G, Jones DG, Briles WE (1979) Limbless: a new genetic mutant in the chick. J Exp Zool 209:427–434

    Article  PubMed  CAS  Google Scholar 

  • Pröls F, Ehehalt F, Rodriguez-Niedenfuhr M, He L, Huang R, Christ B (2004) The role of Emx2 during scapula development. Dev Biol 275:315–324

    Article  PubMed  CAS  Google Scholar 

  • Raynaud A (1962) Les ebauches des membres de l’emryon d’Orvet (Anguis fragilis L). Cr Seanc Acad Sci, Paris 254:4349–4351

    Google Scholar 

  • Raynaud A (1985) Development of limbs and embryonic limb reduction. In: Gans C, Billett F (eds) "Biology of the Reptilia" Vol 15, Development B. Wiley, New York, pp 59–148

    Google Scholar 

  • Raynaud A, Gasc J-P, Renous S, Pieau C (1975) Etude comparative, embryologique et anatomique, de la region pelvi-cloacale et de sa musculature chez le lezard vert (Lacerta viridis Laur) et l’Orvet (Anguis fragilis L). Mem Mus nation Hist nat, Paris Nouv Ser, Ser A, Zool 95:1–62

    Google Scholar 

  • Rogulska T (1965) The development of the pelvic girdle of the chick embryo (Gallus domesticus L) after the extirpation of the posterior limb bud. Zool Pol 15:65–76

    Google Scholar 

  • Romanoff AL (1960) The avian embryo: structural and functional development. The Macmillan Company, New York

    Google Scholar 

  • Rowe DA, Fallon JF (1982) The proximodistal determination of skeletal parts in the developing chick leg. J Embryol Exp Morphol 68:1–7

    PubMed  CAS  Google Scholar 

  • Saunders JW Jr (1948) The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectoderm. J Exp Zool 108:363–403

    Article  Google Scholar 

  • Scaal M, Christ B (2004) Formation and differentiation of the avian dermomyotome. Anat Embryol (Berl) 208:411–424

    Google Scholar 

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

    Google Scholar 

  • Sewertzoff AN (1931) Studien uber die Reduktion der Organe der Wirbeltiere. Zool Jahrb (Anat) 53:611–699

    Google Scholar 

  • Spurling RG (1923) The effect of extirpation of the posterior limb bud on the development of the limb and pelvic girdle in chick embryos. Anat Rec 26:41–56

    Article  Google Scholar 

  • Starck D (1979) Vergleichende Anatomie der Wirbeltiere auf evolutionsbiologischer Grundlage Band 2: Das Skeletsystem. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Summerbell D (1974) A quantitative analysis of the effect of excision of the AER from the chick limb-bud. J Embryol exp Morphol 32:651–660

    PubMed  CAS  Google Scholar 

  • Summerbell D, Lewis JH, Wolpert L (1973) Positional information in chick limb morphogenesis. Nature 244:492–496

    Article  PubMed  CAS  Google Scholar 

  • Sun X, Mariani FV, Martin GR (2002) Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature 418:501–508

    Article  PubMed  CAS  Google Scholar 

  • Tickle C (2004) The contribution of chicken embryology to the understanding of vertebrate limb development. Mech Dev 121:1019–1029

    Article  PubMed  CAS  Google Scholar 

  • Timmons PM, Wallin J, Rigby PWJ, Balling R (1994) Expression and function of Pax1 during development of the pectoral girdle. Development 120:2773–2785

    PubMed  CAS  Google Scholar 

  • Todt WL, Fallon JF (1986) Development of the apical ectodermal ridge in the chick leg bud and a comparison with the wing bud. Anat Rec 215:288–304

    Article  PubMed  CAS  Google Scholar 

  • Vitale MG, Skaggs DL (2001) Developmental dysplasia of the hip from six months to four years of age. J Am Acad Orthop Surg 9:401–411

    PubMed  CAS  Google Scholar 

  • Wassif K, Amer FI, Mohammed FA (1980) The synsacrum, pygostyle and pelvic girdle in some common Egyptian birds. Bull Zool Soc Egypt 30:37–51

    Google Scholar 

  • Weinstein SL, Mubarak SJ, Wenger DR (2004) Developmental hip dysplasia and dislocation: (Parts I and II). Instr Course Lect 53:523–530; 531–542

  • Williams MS (2003) Developmental anomalies of the scapula-the "omo"st forgotten bone. Am J Med Genet 120:583–587

    Article  Google Scholar 

Download references

Acknowledgements

We thank Ulrike Pein, Ellen Gimbel, Lydia Koschny, Susanna Konradi for excellent technical assistance, and Florian Ehehalt and Ruijin Huang for discussion of experiments. This work was supported by EMBO and Alexander von Humboldt Foundation (Y.M.), and by the Medical Faculty of University of Freiburg and DFG (SFB592, A1) to B.C. and M.S.

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Authors and Affiliations

  1. Department of Vertebrate Zoology, St. Petersburg State University, Universitetskaya nab. 7/9, 199034, St. Petersburg, Russia

    Yegor Malashichev & Valentin Borkhvardt

  2. Anatomisches Institut der Universität Freiburg, Albertstrasse 17, 79104, Freiburg, Germany

    Yegor Malashichev, Bodo Christ & Martin Scaal

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  1. Yegor Malashichev
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  2. Valentin Borkhvardt
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  3. Bodo Christ
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  4. Martin Scaal
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Correspondence to Bodo Christ.

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Malashichev, Y., Borkhvardt, V., Christ, B. et al. Differential regulation of avian pelvic girdle development by the limb field ectoderm. Anat Embryol 210, 187–197 (2005). https://doi.org/10.1007/s00429-005-0014-8

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