Skip to main content
Journal of Anatomy logoLink to Journal of Anatomy
. 2001 Feb;198(Pt 2):229–238. doi: 10.1046/j.1469-7580.2001.19820229.x

Specialised cell types in the chorioallantoic membrane express carbonic anhydrase during chick embryogenesis

M GABRIELLA GABRIELLI 1 ,, GIOVANNI MATERAZZI 1 , JOHN V COX 2 , GIOVANNA MENGHI 1
PMCID: PMC1468206  PMID: 11273047

Abstract

The expression of carbonic anhydrase in the chorioallantoic membrane (CAM) of the chick embryo was investigated by means of the histochemical localisation of the enzyme catalytic sites and the immunohistochemical identification of its isoenzymatic forms. The results show that carbonic anhydrase is developmentally expressed in a subset of cells both in the ectodermal and the endodermal epithelium. The distribution patterns from both methodological approaches indicated that carbonic anhydrase is a marker of the villus cavity cells and the mitochondria-rich cells in the ectodermal and the endodermal epithelium, respectively. Such a cell-specific pattern of the enzyme expression provides a further contribution to characterising the heterogeneous cell population of the chick CAM and supports specific functional involvement for the distinct cell types in CAM-mediated processes, such as calcium transport, maintenance of acid-base balance and water and electrolyte reabsorption, during chick embryogenesis.

Keywords: Avian development, extra-embryonic structures

Full Text

The Full Text of this article is available as a PDF (935.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson R. E., Gay C. V., Schraer H. Ultrastructural localization of carbonic anhydrase in the chorioallantoic membrane by immunocytochemistry. J Histochem Cytochem. 1981 Oct;29(10):1121–1127. doi: 10.1177/29.10.6170666. [DOI] [PubMed] [Google Scholar]
  2. Ausprunk D. H. Distribution of hyaluronic acid and sulfated glycosaminoglycans during blood-vessel development in the chick chorioallantoic membrane. Am J Anat. 1986 Nov;177(3):313–331. doi: 10.1002/aja.1001770304. [DOI] [PubMed] [Google Scholar]
  3. Brown D., Breton S. Mitochondria-rich, proton-secreting epithelial cells. J Exp Biol. 1996 Nov;199(Pt 11):2345–2358. doi: 10.1242/jeb.199.11.2345. [DOI] [PubMed] [Google Scholar]
  4. Carter M. J. Carbonic anhydrase: isoenzymes, properties, distribution, and functional significance. Biol Rev Camb Philos Soc. 1972 Nov;47(4):465–513. doi: 10.1111/j.1469-185x.1972.tb01079.x. [DOI] [PubMed] [Google Scholar]
  5. Dawes C. M., Simkiss K. The effects of respiratory acidosis in the chick embryo. J Exp Biol. 1971 Aug;55(1):77–84. doi: 10.1242/jeb.55.1.77. [DOI] [PubMed] [Google Scholar]
  6. Gabrielli M. G., Materazzi G., Menghi G. The metanephros of the quail embryo. Developmental expression of carbonic anhydrase investigated by multiple approaches. J Anat. 2000 Jan;196(Pt 1):31–40. doi: 10.1046/j.1469-7580.2000.19610031.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gabrielli M. G., Palatroni P., Vincenzetti S. Renal carbonic anhydrase in the quail Coturnix coturnix japonica: I. Activity and distribution in male and female metanephros. Histochem J. 1990 Nov;22(11):579–587. doi: 10.1007/BF01072939. [DOI] [PubMed] [Google Scholar]
  8. Hansson H. P. Histochemical demonstration of carbonic anhydrase activity. Histochemie. 1967;11(2):112–128. doi: 10.1007/BF00571716. [DOI] [PubMed] [Google Scholar]
  9. Jeffery D., Edwards Y. H., Jackson M. J., Jeffery S., Carter N. D. Zinc and carbonic anhydrase III distribution in mammalian muscle. Comp Biochem Physiol B. 1982;73(4):971–975. doi: 10.1016/0305-0491(82)90345-5. [DOI] [PubMed] [Google Scholar]
  10. LEESON T. S., LEESON C. R. THE CHORIO-ALLANTOIS OF THE CHICK. LIGHT AND ELECTRON MICROSCOPIC OBSERVATIONS AT VARIOUS TIMES OF INCUBATION. J Anat. 1963 Oct;97:585–595. [PMC free article] [PubMed] [Google Scholar]
  11. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  12. Linser P., Moscona A. A. Induction of glutamine synthetase in embryonic neural retina: localization in Müller fibers and dependence on cell interactions. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6476–6480. doi: 10.1073/pnas.76.12.6476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Maren T. H. Carbonic anhydrase: chemistry, physiology, and inhibition. Physiol Rev. 1967 Oct;47(4):595–781. doi: 10.1152/physrev.1967.47.4.595. [DOI] [PubMed] [Google Scholar]
  14. Narbaitz R., Bastani B., Galvin N. J., Kapal V. K., Levine D. Z. Ultrastructural and immunocytochemical evidence for the presence of polarised plasma membrane H(+)-ATPase in two specialised cell types in the chick embryo chorioallantoic membrane. J Anat. 1995 Apr;186(Pt 2):245–252. [PMC free article] [PubMed] [Google Scholar]
  15. Narbaitz R. Structure of the intra-chorionic blood sinus in the chick embryo. J Anat. 1977 Nov;124(Pt 2):347–354. [PMC free article] [PubMed] [Google Scholar]
  16. Parkkila S., Parkkila A. K. Carbonic anhydrase in the alimentary tract. Roles of the different isozymes and salivary factors in the maintenance of optimal conditions in the gastrointestinal canal. Scand J Gastroenterol. 1996 Apr;31(4):305–317. doi: 10.3109/00365529609006403. [DOI] [PubMed] [Google Scholar]
  17. Rieder E., Gay C. V., Schraer H. Autoradiographic localization of carbonic anhydrase in the developing chorioallantoic membrane. Anat Embryol (Berl) 1980;159(1):17–31. doi: 10.1007/BF00299252. [DOI] [PubMed] [Google Scholar]
  18. Sanyal G. Comparative carbon dioxide hydration kinetics and inhibition of carbonic anhydrase isozymes in vertebrates. Ann N Y Acad Sci. 1984;429:165–178. doi: 10.1111/j.1749-6632.1984.tb12330.x. [DOI] [PubMed] [Google Scholar]
  19. Sly W. S., Hu P. Y. Human carbonic anhydrases and carbonic anhydrase deficiencies. Annu Rev Biochem. 1995;64:375–401. doi: 10.1146/annurev.bi.64.070195.002111. [DOI] [PubMed] [Google Scholar]
  20. Stewart M. E., Terepka A. R. Transport functions of the chick chorio-allantoic membrane. I. Normal histology and evidence for active electrolyte transport from the allantoic fluid, in vivo. Exp Cell Res. 1969 Nov;58(1):93–106. doi: 10.1016/0014-4827(69)90119-0. [DOI] [PubMed] [Google Scholar]
  21. Terepka A. R., Stewart M. E., Merkel N. Transport functions of the chick chorio-allantoic membrane. II. Active calcium transport, in vitro. Exp Cell Res. 1969 Nov;58(1):107–117. doi: 10.1016/0014-4827(69)90120-7. [DOI] [PubMed] [Google Scholar]
  22. Tuan R. S. Calcium transport and related functions in the chorioallantoic membrane of cultured shell-less chick embryos. Dev Biol. 1980 Jan;74(1):196–204. doi: 10.1016/0012-1606(80)90061-5. [DOI] [PubMed] [Google Scholar]
  23. Tuan R. S. Carbonic anhydrase and calcium transport function of the chick embryonic chorioallantoic membrane. Ann N Y Acad Sci. 1984;429:459–472. doi: 10.1111/j.1749-6632.1984.tb12372.x. [DOI] [PubMed] [Google Scholar]
  24. Tuan R. S., Carson M. J., Jozefiak J. A., Knowles K. A., Shotwell B. A. Calcium-transport function of the chick embryonic chorioallantoic membrane. II. Functional involvement of calcium-binding protein, Ca2+-ATPase and carbonic anhydrase. J Cell Sci. 1986 Jun;82:85–97. doi: 10.1242/jcs.82.1.85. [DOI] [PubMed] [Google Scholar]
  25. Tuan R. S. Mechanism and regulation of calcium transport by the chick embryonic chorioallantoic membrane. J Exp Zool Suppl. 1987;1:1–13. [PubMed] [Google Scholar]
  26. Tuan R. S., Zrike J. Functional involvement of carbonic anhydrase in calcium transport of the chick chorioallantoic membrane. Biochem J. 1978 Oct 15;176(1):67–74. doi: 10.1042/bj1760067. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Anatomy are provided here courtesy of Anatomical Society of Great Britain and Ireland

RESOURCES