Cell and Tissue Research

, Volume 247, Issue 2, pp 275–285 | Cite as

Subcellular organization of the yolk syncytial-endoderm complex in the preimplantation yolk sac of the shark, Rhizoprionodon terraenovae

  • William C. Hamlett
  • Frank J. Schwartz
  • Liberato J. A. DiDio
Article

Summary

The structure of the yolk syncytial-endoderm complex of the preimplantation yolk sac of the shark is examined by light- and transmission electron microscopy. The yolk syncytium is bounded by a membrane that is anchored to the plasmalemma of adjacent endoderm cells by desmosomes. Enlarged nuclei, rough endoplasmic reticulum, Golgi complexes, mitochondria, and other cellular organelles populate the syncytium. Microtubules and filamentous elements are also observed free in the syncytium. Yolk is present as pleomorphic droplets, the profiles of which are generally spherical but may be vesicular, especially at the periphery of large yolk droplets. Occasionally, large yolk droplets have a paracrystalline configuration. Small yolk droplets are modulated through the Golgi complex of the yolk syncytium, and it is suggested that acid hydrolases are added there. Small yolk droplets released from the maturing face of the Golgi complex are sequestered in membrane-limited packets. The membrane of the packets fuses with the membrane enveloping the yolk syncytium and the yolk droplets are released into the yolk syncytialendoderm interspace. Subsequently, the yolk droplets are endocytosed by the endoderm. Yolk droplets disperse and fuse to form the large irregular yolk inclusions of the endoderm. Yolk metabolites are transported out of the endoderm through the yolk sac endothelium. The yolk sac endoderm thus mediates the transfer of metabolites from the yolk mass to the extraembryonic circulation.

Key words

Yolk sac Endoderm Fetal membranes Endocytosis Shark, Rhizoprionodon terraenovae 

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References

  1. Baranes A, Wendling J (1981) The early stages of development in Carcharhinus plumbeus. J Fish Biol 18:159–175Google Scholar
  2. Brierley J, Hemmings WA (1956) Selective transport of antibodies from the yolk sac to the circulation of the chick. J Embryol Exp Morphol 4:34–41Google Scholar
  3. DiDio LJA (1972) The ubiquity of “myelin figures” as seen with electron microscopy. Ateneo Parmense Acta Bio-Medica 43:341–406Google Scholar
  4. Fuji T (1960) Comparative biochemical studies on the egg — yolk proteins of various animal species. Acta Embryol Morphol Exptl 3:260–285Google Scholar
  5. Haar JL, Ackerman GA (1971) Ultrastructural changes in mouse yolk sac associated with the initiation of vitelline circulation. Anat Rec 170:437–456Google Scholar
  6. Hamlett WC (1983) Maternal-fetal relations in elasmobranch fishes. Ph.D. Dissertation, Clemson University, Clemson, South Carolina, USAGoogle Scholar
  7. Hamlett WC (1986) Prenatal nutrient absorptive structures in selachians. In: Uycno T, Arai R, Taniuchi T, Matsuura K (eds) Indo-Pacific Fish Biology, pp 333–344, Icthyol Soc Jpn, TokyoGoogle Scholar
  8. Hamlett WC, Wourms JP (1983) Electron microscopy of a shark yolk sac placenta prior to implantation and differentiation. Micron 14:85–86Google Scholar
  9. Hamlett WC, Wourms JP (1984) Ultrastructure of the preimplantation shark yolk sac placenta. Tissue Cell 16:613–625Google Scholar
  10. Hamlett WC, Allen DJ, Stribling MD, Schwartz FJ, DiDio LJA (1985) Permeability of embryonic shark external gill filaments. Electron microscopic observations using horseradish peroxidase as a macromolecular tracer. J Submicrosc Cytol 17:31–40Google Scholar
  11. Hamlett WC, Wourms JP, Hudson JS (1985a) Ultrastructure of the full term shark yolk sac placenta. I. Morphology and cellular transport at the fetal attachment site. J Ultrastruct Res 91:192–206Google Scholar
  12. Hamlett WC, Wourms JP, Hudson JS (1985b) Ultrastructure of the full term shark yolk sac placenta. II. The smooth, proximal segment. J Ultrastruct Res 91:207–220Google Scholar
  13. Hamlett WC, Wourms JP, Hudson JS (1985c) Ultrastructure of the full term shark yolk sac placenta. III. The maternal attachment site. J Ultrastruct Res 91:221–231Google Scholar
  14. Jollie WP, Jollie LG (1967) Electron microscopic observations on the yolk sac of the spiny dogfish, Squalus acanthias. J Ultrastruct Res 18:102–126Google Scholar
  15. Jollie WP, Seibel W (1970) Fine structural observations on transport mechanisms in the visceral yolk sac placenta of the rat. 7th Int Congr Elect Microsc, Grenoble, France, Res Comm III:59–60Google Scholar
  16. Jurand A, Selman GG (1964) Yolk utilization in the notochord of the newt as studied by electron microscopy. J Embryol Exp Morphol 12:43–50Google Scholar
  17. Karasaki S (1963) Studies on amphibian yolk. 5. Electron microscopic observations on the utilization of yolk platelets during embryogenesis. J Ultrastruct Res 9:225–247Google Scholar
  18. Kerr JG (1979) Textbook of Embryology. Vol 2, The Macmillan Co, New YorkGoogle Scholar
  19. King BF, Enders AC (1970) Protein absorption and transport by the guinea pig visceral yolk sac. Am J Anat 129:261–288Google Scholar
  20. Lambson RO (1970) An electron microscopic study of entodermal cells of the yolk sac of the chick during incubation and after hatching. Am J Anat 129:1–20Google Scholar
  21. Lange RH (1981) Highly conserved lipoprotein assembly in teleost and amphibian yolk-platelet crystals. Nature 289:329–330Google Scholar
  22. Lange RH (1985) The vertebrate yolk-platelet crystal: comparative analysis of an in vivo crystalline aggregate. Int Rev Cytol 97:133–181Google Scholar
  23. Lange RH, Grodzinski Z, Kilarski W (1982) Yolk-platelet crystals in three ancient bony fishes: Polypterus bichir (Polypteri), Amia calva L., and Lepisosteus osseus L. (Holostei). Cell Tissue Res 222:159–165Google Scholar
  24. Mobbs IG, McMillan DB (1979) Structure of the endodermal epithelium of the chick yolk sac during early stages of development. Am J Anat 155:287–310Google Scholar
  25. Mobbs IG, McMillan DB (1981) Transport across endodermal cells of the chick yolk sac during early stages of development. Am J Anat 160:285–308Google Scholar
  26. Mollenhauer HH (1964) Plastic embedding mixtures for use in electron microscopy. Stain Technol 39:111–114Google Scholar
  27. Moxon LA, Wild AE, Slade BS (1976) Localization of proteins in coated micropinocytotic vesicles during transport across rabbit yolk sac endoderm. Cell Tissue Res 171:175–193Google Scholar
  28. Needham J (1942) Biochemistry and Morphogenesis. Cambridge University Press, London and New YorkGoogle Scholar
  29. Nelsen OE (1953) Comparative Embryology of the Vertebrates. The Blakiston Co, Inc, New YorkGoogle Scholar
  30. Ohlendorf DH, Wrenn RF, Banaszak LJ (1978) Three dimensional structure of the lipovitellin-phosvitin complex from amphibian oocytes. Nature 272:28–32Google Scholar
  31. Panijel J (1950) L'organisation du vitellus dans œufs d'amphibiens. Biochim Biophys Acta 5:343–357Google Scholar
  32. Romanoff AL (1960) The Avian Embryo: Structural and Functional Development. The Macmillan Co, New YorkGoogle Scholar
  33. Romanoff AL (1967) Biochemistry of the Avian Embryo: A Quantitative Analysis of Prenatal Development. John Wiley and Sons, Inc, New YorkGoogle Scholar
  34. Romanoff AL, Romanoff AJ (1949) The Avian Egg. John Wiley and Sons, Inc, New YorkGoogle Scholar
  35. Schlernitzauer DA, Gilbert PW (1966) Placentation and associated aspects of gestation in the bonnethead shark, Sphyrna tiburo. J Morphol 120:219–232Google Scholar
  36. Slade BS (1970) An attempt to visualize protein transmission across the rabbit yolk sac. J Anat 107:531–545Google Scholar
  37. Te Winkel LE (1963) Notes on the smooth dogfish, Mustelus canis, during the first three months of gestation. I. Structural modifications of yolk-sacs and yolk-stalks correlated with increasing absorptive function. J Exp Zool 152:123–137Google Scholar
  38. Thomas JA (1938) Recherches sur les transformations, la multiplication et la spécificité des cellules hors. de l'organisme. La cellule vitelline. Les cellules du type histiocyte. Ann Sci Natl Zool 1:209–579Google Scholar
  39. Van der Ghinst M (1935) Mise en evidence de ferments dans le syncytium vitellin de la truite. Bull Hist Phys Pathol Techn Microsc 12:257–258Google Scholar
  40. Venable JH, Coggeshall R (1965) A simplified lead citrate stain for use in electron microscopy. J Cell Biol 25:407–408CrossRefPubMedGoogle Scholar
  41. Vernier JM, Sire MF (1977) Plaquettes vitellines et activite hydrolasique acide au cours du developpement embryonnaire de la truite arc-en-ciel. Etude ultrastructurale et biochimique. Biol Cell 29:99–112Google Scholar
  42. Wallace RA (1963a) Studies on amphibian yolk. III. A resolution of yolk platelet components. Biochim Biophys Acta 74:495–504Google Scholar
  43. Wallace RA (1963b) Studies on amphibian yolk IV. An analysis of the main-body component of yolk platelets. Biochim Biophys Acta 74:505Google Scholar
  44. Wallace RA, Selman K (1978) Oogenesis in Fundulus heteroclitus I. Preliminary observations on oocyte maturation in vivo and in vitro. Dev Biol 62:345–369Google Scholar
  45. Wallace RA, Selman K (1981) Cellular and dynamic aspects of oocyte growth in teleosts. Am Zool 21:325–343Google Scholar
  46. Wallace RA, Selman K (1985) Major protein changes during vitellogenesis and maturation of Fundulus oocytes. Dev Biol 110:492–498Google Scholar
  47. Walzer C, Schonenberger N (1979a) Ultrastructure and cytochemistry of the yolk syncytial layer in the alevin of the trout (Salmo fario trutta L.) after hatching. I. The vitellolysis zone. Cell Tissue Res 196:59–73Google Scholar
  48. Walzer C, Schonenberger N (1979b) Ultrastructure and cytochemistry of the yolk syncytial layer in the alevin of trout (Salmo fario trutta L. and Salmo gairdneri R.) after hatching. II. The cytoplasmic zone. Cell Tissue Res 196:75–93Google Scholar
  49. Ward RT (1980) The origin of protein and fatty yolk in Rana pipiens. V. Unusual paracrystalline configurations within the yolk precursor complex. J Morphol 165:255–260Google Scholar
  50. Wild AE (1970) Protein transmission across rabbit foetal membranes. J Embryol Exp Morphol 24:313–330Google Scholar
  51. Wild AE, Stauber VV, Slade BS (1972) Simultaneous localization of human-globulin I l25 and ferritin during transport across the rabbit yolk sac splanchnopleure. Z Zellforsch 123:168–177Google Scholar
  52. Williams J (1967) Yolk utilization. In: Weber R (ed) The Biochemistry of Animal Development. Vol II. Biochemical Control Mechanisms and Adaptations in Development, Academic Press Inc New York, pp 341–382Google Scholar
  53. Yamagami K (1960a) Phosphorus metabolism in fish egg. I. Changes in the contents of some phosphorus compounds during early development of Oryzias latipes. Sci Pap Col Gen Educ Univ Tokyo 10:99–108Google Scholar
  54. Yamagami K (1960b) Item II. Transfer of some phosphorus compounds from egg yolk into embryonic tissues in Salmo irideus during development. Sci Pap Col Gen Educ Univ Tokyo 10:325–336Google Scholar
  55. Yamamoto M (1967) Electron microscopy of fish development. V. The fine structure of the periblast in Oryzias latipes. J Fac Sci Univ Tokyo 10:483–490Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • William C. Hamlett
    • 1
  • Frank J. Schwartz
    • 2
  • Liberato J. A. DiDio
    • 1
  1. 1.Department of AnatomyMedical College of OhioToledoUSA
  2. 2.Institute of Marine SciencesUniversity of North CarolinaMorehead CityUSA
  3. 3.Department of AnatomyMedical College of Ohio, C.S. 10008ToledoUSA

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