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.
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References
Baranes A, Wendling J (1981) The early stages of development in Carcharhinus plumbeus. J Fish Biol 18:159–175
Brierley J, Hemmings WA (1956) Selective transport of antibodies from the yolk sac to the circulation of the chick. J Embryol Exp Morphol 4:34–41
DiDio LJA (1972) The ubiquity of “myelin figures” as seen with electron microscopy. Ateneo Parmense Acta Bio-Medica 43:341–406
Fuji T (1960) Comparative biochemical studies on the egg — yolk proteins of various animal species. Acta Embryol Morphol Exptl 3:260–285
Haar JL, Ackerman GA (1971) Ultrastructural changes in mouse yolk sac associated with the initiation of vitelline circulation. Anat Rec 170:437–456
Hamlett WC (1983) Maternal-fetal relations in elasmobranch fishes. Ph.D. Dissertation, Clemson University, Clemson, South Carolina, USA
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, Tokyo
Hamlett WC, Wourms JP (1983) Electron microscopy of a shark yolk sac placenta prior to implantation and differentiation. Micron 14:85–86
Hamlett WC, Wourms JP (1984) Ultrastructure of the preimplantation shark yolk sac placenta. Tissue Cell 16:613–625
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 17:31–40
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 91:192–206
Hamlett WC, Wourms JP, Hudson JS (1985b) Ultrastructure of the full term shark yolk sac placenta. II. The smooth, proximal segment. J Ultrastruct Res 91:207–220
Hamlett WC, Wourms JP, Hudson JS (1985c) Ultrastructure of the full term shark yolk sac placenta. III. The maternal attachment site. J Ultrastruct Res 91:221–231
Jollie WP, Jollie LG (1967) Electron microscopic observations on the yolk sac of the spiny dogfish, Squalus acanthias. J Ultrastruct Res 18:102–126
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:59–60
Jurand A, Selman GG (1964) Yolk utilization in the notochord of the newt as studied by electron microscopy. J Embryol Exp Morphol 12:43–50
Karasaki S (1963) Studies on amphibian yolk. 5. Electron microscopic observations on the utilization of yolk platelets during embryogenesis. J Ultrastruct Res 9:225–247
Kerr JG (1979) Textbook of Embryology. Vol 2, The Macmillan Co, New York
King BF, Enders AC (1970) Protein absorption and transport by the guinea pig visceral yolk sac. Am J Anat 129:261–288
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 129:1–20
Lange RH (1981) Highly conserved lipoprotein assembly in teleost and amphibian yolk-platelet crystals. Nature 289:329–330
Lange RH (1985) The vertebrate yolk-platelet crystal: comparative analysis of an in vivo crystalline aggregate. Int Rev Cytol 97:133–181
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 222:159–165
Mobbs IG, McMillan DB (1979) Structure of the endodermal epithelium of the chick yolk sac during early stages of development. Am J Anat 155:287–310
Mobbs IG, McMillan DB (1981) Transport across endodermal cells of the chick yolk sac during early stages of development. Am J Anat 160:285–308
Mollenhauer HH (1964) Plastic embedding mixtures for use in electron microscopy. Stain Technol 39:111–114
Moxon LA, Wild AE, Slade BS (1976) Localization of proteins in coated micropinocytotic vesicles during transport across rabbit yolk sac endoderm. Cell Tissue Res 171:175–193
Needham J (1942) Biochemistry and Morphogenesis. Cambridge University Press, London and New York
Nelsen OE (1953) Comparative Embryology of the Vertebrates. The Blakiston Co, Inc, New York
Ohlendorf DH, Wrenn RF, Banaszak LJ (1978) Three dimensional structure of the lipovitellin-phosvitin complex from amphibian oocytes. Nature 272:28–32
Panijel J (1950) L'organisation du vitellus dans œufs d'amphibiens. Biochim Biophys Acta 5:343–357
Romanoff AL (1960) The Avian Embryo: Structural and Functional Development. The Macmillan Co, New York
Romanoff AL (1967) Biochemistry of the Avian Embryo: A Quantitative Analysis of Prenatal Development. John Wiley and Sons, Inc, New York
Romanoff AL, Romanoff AJ (1949) The Avian Egg. John Wiley and Sons, Inc, New York
Schlernitzauer DA, Gilbert PW (1966) Placentation and associated aspects of gestation in the bonnethead shark, Sphyrna tiburo. J Morphol 120:219–232
Slade BS (1970) An attempt to visualize protein transmission across the rabbit yolk sac. J Anat 107:531–545
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 152:123–137
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 1:209–579
Van der Ghinst M (1935) Mise en evidence de ferments dans le syncytium vitellin de la truite. Bull Hist Phys Pathol Techn Microsc 12:257–258
Venable JH, Coggeshall R (1965) A simplified lead citrate stain for use in electron microscopy. J Cell Biol 25:407–408
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 29:99–112
Wallace RA (1963a) Studies on amphibian yolk. III. A resolution of yolk platelet components. Biochim Biophys Acta 74:495–504
Wallace RA (1963b) Studies on amphibian yolk IV. An analysis of the main-body component of yolk platelets. Biochim Biophys Acta 74:505
Wallace RA, Selman K (1978) Oogenesis in Fundulus heteroclitus I. Preliminary observations on oocyte maturation in vivo and in vitro. Dev Biol 62:345–369
Wallace RA, Selman K (1981) Cellular and dynamic aspects of oocyte growth in teleosts. Am Zool 21:325–343
Wallace RA, Selman K (1985) Major protein changes during vitellogenesis and maturation of Fundulus oocytes. Dev Biol 110:492–498
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 196:59–73
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 196:75–93
Ward RT (1980) The origin of protein and fatty yolk in Rana pipiens. V. Unusual paracrystalline configurations within the yolk precursor complex. J Morphol 165:255–260
Wild AE (1970) Protein transmission across rabbit foetal membranes. J Embryol Exp Morphol 24:313–330
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 123:168–177
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 341–382
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 10:99–108
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 10:325–336
Yamamoto M (1967) Electron microscopy of fish development. V. The fine structure of the periblast in Oryzias latipes. J Fac Sci Univ Tokyo 10:483–490
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Hamlett, W.C., Schwartz, F.J. & DiDio, L.J.A. Subcellular organization of the yolk syncytial-endoderm complex in the preimplantation yolk sac of the shark, Rhizoprionodon terraenovae . Cell Tissue Res. 247, 275–285 (1987). https://doi.org/10.1007/BF00218309
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DOI: https://doi.org/10.1007/BF00218309