Comparative Development of the Mammalian Yolk Sac

  • B. F. King
  • A. C. Enders

Abstract

The yolk sac is the first fetal membrane to be formed in all mammals, even though, among modern mammals, only the monotremes have retained a macrolecithal egg. Although no longer utilized for yolk storage and digestion, the yolk sac of eutherian mammals continues to subserve a wide variety of functions related to embryonic development. In many instances it is the primary, if not the sole, organ involved in maternal-fetal transfer of nutrients in early gestation during the critical period of organogenesis. In other species a yolk sac placenta remains functional throughout pregnancy, complementing the role of the chorioallantoic placenta. The yolk sac is also the first hemopoietic organ and has been shown, in most species, to synthesize and secrete a number of polypeptides important to normal embryonic development.

Keywords

Permeability Albumin Polypeptide Luminal Fibril 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aldred AR, Grimes A, Schreiber G, Mercer JF (1987) Rat ceruloplasmin. Molecular cloning and gene expression in liver, choroid plexus, yolk sac, placenta and testis. J Biol Chem 262:2875–2878.PubMedGoogle Scholar
  2. Batten BE, Haar JL (1979) Fine structural differentiation of germ layers in the mouse at the time of mesoderm formation. Anat Rec 194:125–142.PubMedGoogle Scholar
  3. Baumbach GA, Climer AH, Bartley NG, Kattesh HG, Godkin JD (1988) Purification, characterization and immunocytochemical localization of the major basic protein of pig blastocysts. Biol Reprod 39:1171–1182.PubMedGoogle Scholar
  4. Beckman DA, Koszalka TR, Jensen M, Brent RL (1990a) Experimental manipulation of the rodent visceral yolk sac. Teratology 41:395–404.PubMedGoogle Scholar
  5. Beckman DA, Pugarelli JE, Jensen M, Koszalka TR, Brent RL, Lloyd JB (1990b) Sources of amino acids for protein synthesis during early organogenesis in the rat. I. Relative contributions of free amino acids and proteins. Placenta 11:109–121.PubMedGoogle Scholar
  6. Brambell FWR (1970) The transmission of passive immunity from mother to young. North Holland, Amsterdam.Google Scholar
  7. Bremer D, Merker H-J, Gossrau R (1985) Ultrastructure and hydrolase cytochemistry of the developing marmoset yolk sac. Anat Embryol (Berl) 172:101–113.Google Scholar
  8. Brent RL, Beckman DA, Jensen M, Koszalka TR (1990) Experimental yolk sac dysfunction as a model for studying nutritional disturbances in the embryo during early organogenesis. Teratology 41:405–413.PubMedGoogle Scholar
  9. Bruns MEH, Kleeman E, Mills SE, Bruns DE, Herr JC (1985) Immunocytochemical localization of vitamin D-dependent calcium-binding protein in mouse placenta and yolk sac. Anat Rec 213:514–517.PubMedGoogle Scholar
  10. Butt JH, Wilson TH (1968) Development of sugar and amino acid transport by intestine and yolk sac of the guinea pig. Am J Physiol 215:1468–1477.PubMedGoogle Scholar
  11. Chan STH, Wong PYD (1978) Evidence of active sodium transport in the visceral yolk sac of the rat in vitro. J Physiol (Lond) 279:385–394.Google Scholar
  12. Clark CC, Minor RR, Koszalka TR, Brent RL, Kefalides NA (1975) The embryonic rat parietal yolk sac. Changes in morphology and composition of its basement membrane during development. Dev Biol 46:243–261.PubMedGoogle Scholar
  13. Cross JC, Roberts RM (1989) Porcine conceptuses secrete an interferon during the preattachment period of early pregnancy. Biol Reprod 40:1109–1118.PubMedGoogle Scholar
  14. Danan JL, Delmore AC, Ripoche MA, Bouillon R, Van Baelen H, Mathieu H (1985) Presence of immunoreactive vitamin D-binding protein in rat yolk sac endodermal cells. Endocrinology 117:243–247.PubMedGoogle Scholar
  15. Delorme AC, Cassier P, Geny B, Mathieu H (1983) Immunocytochemical localization of vitamin D-dependent calcium-binding protein in the yolk sac of the rat. Placenta 4:263–270.PubMedGoogle Scholar
  16. Deren JJ, Padykula HA, Wilson TH (1966a) Development of structure and function in the mammalian yolk sac. II. Vitamin B12 uptake by rabbit yolk sac. Dev Biol 13:349–369.PubMedGoogle Scholar
  17. Deren JJ, Padykula HA, Wilson TH (1966b) Development of structure and function in the mammalian yolk sac. III. The development of amino acid transport by rabbit yolk sac. Dev Biol 13:370–384.PubMedGoogle Scholar
  18. Duval M (1892) La placenta des rongeurs. Alcan, Paris (Ancienne Libraire Germer Bailier et Cie).Google Scholar
  19. Ekblom P, Thesleff I (1985) Control of kidney differentiation by soluble factors secreted by the embryonic liver and the yolk sac. Dev Biol 110:29–38.PubMedGoogle Scholar
  20. Enders AC (1989) Morphological manifestations of maturation of the blastocyst. In: Yoshinaga K, Mori T (eds) Development of preimplantation embryos and their environment. Liss, New York, pp 211–223.Google Scholar
  21. Enders AC, King BF (1988) Formation and differentiation of extraembryonic mesoderm in the rhesus monkey. Am J Anat 181:327–340.PubMedGoogle Scholar
  22. Enders AC, Liu IKM (1991) Lodgement of the equine blastocyst in the uterus from fixation through endometrial cup formation. J Reprod Fertil [Suppl] 44:427–438.Google Scholar
  23. Enders AC, Schlafke S (1967) A morphological analysis of the early implantation stages in the rat. Am J Anat 120:185–226.Google Scholar
  24. Enders AC, Wimsatt WA, King BF (1976) Cytological development of the yolk sac endoderm and protein-absorptive mesothelium in the little brown bat, Myotis lucifugus. Am J Anat 146:1–30.PubMedGoogle Scholar
  25. Enders AC, Given RL, Schlafke S (1978) Differentiation and migration of endoderm in the rat and mouse at implantation. Anat Rec 190:65–78.PubMedGoogle Scholar
  26. Enders AC, Schlafke S, Hendrickx AG (1986) Differentiation of the embryonic disc, amnion, and yolk sac in the rhesus monkey. Am J Anat 177:161–185.PubMedGoogle Scholar
  27. Enders AC, Lantz KC, Schlafke S (1989) Differentiation of trophoblast of the baboon blastocyst. Anat Rec 225:329–340.PubMedGoogle Scholar
  28. Enders AC, Lantz KC, Schlafke S (1990) Differentiation of the inner cell mass of the baboon blastocyst. Anat Rec 226:237–248.PubMedGoogle Scholar
  29. Fleming TP, Warren PD, Chisholm JC, Johnson MH (1984) Trophectodermal processes regulate the expression of totipotency within the inner cell mass of the mouse expanding blastocyst. J Embryol Exp Morphol 84:63–90.PubMedGoogle Scholar
  30. Freeman SJ, Lloyd JB (1983) Evidence the protein ingested by the rat visceral yolk sac yields amino acids for synthesis of embryonic protein. J Embryol Exp Morphol 73:307–315.PubMedGoogle Scholar
  31. Gardner RL (1989) Cell allocation and lineage in the early mouse embryo. Ciba Found Symp 144:172–186.PubMedGoogle Scholar
  32. Gerard P (1932) Etudes sur l’ovogenése et l’ontogénése chez les lemuriens du genre Galago. Arch Biol 43:93–151.Google Scholar
  33. Geisert RD, Brookbank JW, Roberts RM, Bazer FW (1982) Establishment of pregnancy in the pig. IL Cellular remodeling of the porcine blastocyst during elongation on day 12 of pregnancy. Biol Reprod 27:941–955.PubMedGoogle Scholar
  34. Ginther OJ (1992) Reproductive biology of the mare: basic and applied aspects. Equine, Cross Plains.Google Scholar
  35. Gitlin D, Kitzes J, Boesman M (1967) Cellular distribution of serum α-fetoprotem m organs of the foetal rat. Nature 215:534.PubMedGoogle Scholar
  36. Godkin JD, Bazer FW, Lewis GS, Geisert RD, Roberts RM (1982) Synthesis and release of polypeptides by pig conceptuses during the period of blastocyst elongation and attachment. Biol Reprod 27:977–987.PubMedGoogle Scholar
  37. Godkin JD, Bazer FW, Roberts RM (1985) Protein production by cultures established from day 14–16 sheep and pig conceptuses. J Reprod Fertil 74:377–382.PubMedGoogle Scholar
  38. Gonzalez-Crussi F, Roth LM (1976) The human yolk sac and yolk sac carcinoma. An ultrastructural study. Hum Pathol 7:675–691.PubMedGoogle Scholar
  39. Gossrau R, Merker H-J (1984) Ultrastructure and enzyme histochemistry of the marmoset yolk sac and embryonic intestinal epithelium. Histochem J 16:360–363.PubMedGoogle Scholar
  40. Haar JL (1977) An in vitro morphological study of the mouse visceral yolk sac and possible yolk sac immunocyte precursors. Cell Tissue Res 184:113–119.PubMedGoogle Scholar
  41. Haar JL, Ackerman GA (1971) A phase and electron microscopic study of vasculogenesis and erythropoiesis in the yolk sac of the mouse. Anat Rec 170:199–224.PubMedGoogle Scholar
  42. Hamilton WJ, Mossman HW (1972) Human embryology. Williams and Wilkins, Baltimore.Google Scholar
  43. Harney JP, Bazer FW (1989) Effects of conceptus and conceptus secretory products on uterine development in the pig. Reprod Fertil Dev 2:179–188.Google Scholar
  44. Harney JP, Mirando MA, Smith LC, Bazer FW (1989) Retinol-binding protein: a major secretory product of the pig conceptus. Biol Reprod 42:523–532.Google Scholar
  45. Hartfield PJ, Williams KE, Geddes R, Lloyd JB (1989) Glycogen metabolism in the rat visceral yolk sac. I. Glycogen content and gestational age. Placenta 10:45–54.PubMedGoogle Scholar
  46. Heap RB, Hamon M, Allen WR (1982) Studies on oestrogen synthesis by the preimplantation equine conceptus. J Reprod Fert [Suppl] 32:343–352.Google Scholar
  47. Hendrickx AG, Sawyer RH (1975) Embryology of the rhesus monkey. In: The rhesus monkey, vol II: management, reproduction and pathology. Academic, New York, pp 141–169.Google Scholar
  48. Hertig AT (1935) Angiogenesis in the early human chorion and in the primary placenta of the macaque monkey. Contrib Embryol Carnegie Inst 25:37–82.Google Scholar
  49. Hertig AT (1968) Human trophoblast. Thomas, Springfield.Google Scholar
  50. Hesseldahl H, Falck-Larsen JF (1969) Ultrastructure of human yolk sac: endoderm, mesenchyme, tubules and mesothelium. Am J Anat 126:315–336.PubMedGoogle Scholar
  51. Heuser CH (1927) A study of the implantation of the ovum of the pig from the stage of the bilaminar blastocyst to the completion of the fetal membranes. Contrib Embryol Carnegie Inst 19:231–243.Google Scholar
  52. Heuser CH, Streeter GL (1929) Early stages in the development of pig embryos, trom the period of initial cleavage to the time of the appearance of limb-buds. Contrib Embryol Carnegie Inst 394:1–29.Google Scholar
  53. Heuser CH, Streeter GL (1941) Development of the macaque embryo. Contrib Embryol Carnegie Inst 29:15–55.Google Scholar
  54. Hill JP (1932) The developmental history of the primates. Philos Trans R Soc [Biol] 221:45–178.Google Scholar
  55. Hogan B, Newman R (1984) A scanning electron microscope study of the extra-embryonic endoderm of the 8th-day mouse embryo. Differentiation 26:138–143.PubMedGoogle Scholar
  56. Hoyes AD (1969) The human foetal yolk sac. An ultrastructural study of four specimens. Z Zellforsch 99:469–490.PubMedGoogle Scholar
  57. Janzen RG, Andrews GK, Tamaoki T (1982) Synthesis of secretory proteins in developing mouse yolk sac. Dev Biol 90:18–23.PubMedGoogle Scholar
  58. Jollie WP (1986) Review article: ultrastructural studies of protein transfer across rodent yolk sac. Placenta 7:263–281.PubMedGoogle Scholar
  59. Jollie WP (1990) Development, morphology, and function of the yolk-sac placenta of laboratory rodents. Teratology 41:361–381.PubMedGoogle Scholar
  60. Jordan HE (1907) The histology of the yolk sac of a 9.2 mm human embryo. Anat Anz 31:291–303.Google Scholar
  61. Jordan HE (1910a) A further study of the human umbilical vesicle. Anat Rec 4:341–353.Google Scholar
  62. Jordan HE (1910b) A microscopic study of the umbilical vesicle of a 13 mm human embryo, with special reference to the entodermal tubules and the blood islands. Anat Anz 37:12–66.Google Scholar
  63. Jordan HE (1916) The microscopic structure of the yolk-sac of the pig embryo, with special reference to the origin of the erythrocytes. Am J Anat 19:277–303.Google Scholar
  64. Karim KB, Wimsatt WA, Enders AC, Gopalakrishna A (1979) Electron microscopic observations on the yolk sac of the Indian fruit bat, Rousettus leschenaulti (Demarest) (Pteropodidae). Anat Rec 190:493–509.Google Scholar
  65. Kernis MM, Johnson EM (1969) Effects of trypan blue and Niagara blue 2B on the in vitro absorption of ions by the rat visceral yolk sac. J Embryol Exp Morphol 22:115–125.PubMedGoogle Scholar
  66. King BF (1971) Differentiation of parietal endoderm cells of the guinea pig yolk sac, with particular reference to the development of endoplasmic reticulum. Dev Biol 26:547–559.PubMedGoogle Scholar
  67. King BF (1972) The permeability of the guinea pig parietal yolk sac placenta to peroxidase and ferritin. Am J Anat 134:365–376.PubMedGoogle Scholar
  68. King BF (1987) Ultrastructural differentiation of stromal and vascular components in early macaque placental villi. Am J Anat 178:30–44.PubMedGoogle Scholar
  69. King BF, Mossman HW (1974) The fetal membranes and unusual giant cell placenta of the jerboa (Jaculus) and jumping mouse (Zapus). Am J Anat 140:405–432.PubMedGoogle Scholar
  70. King BF, Wilson JM (1983) A fine structural and cytochemical study of the rhesus monkey yolk sac: endoderm and mesothelium. Anat Rec 205:143–158.PubMedGoogle Scholar
  71. King BF, Enders AC, Wimsatt WA (1978) The annular hematoma of the shrew yolk-sac placenta. Am J Anat 152:45–58.PubMedGoogle Scholar
  72. Koszalka TR, Andrew CL, Lloyd JB, Brent RL (1988) Carrier-mediated uptake of hexoses by the rat visceral yolk sac. Placenta 9:547–558.PubMedGoogle Scholar
  73. Lee HU, Campbell DJ, Habener JF (1987) Developmental expression of the angiotensinogen gene in rat embryos. Endocrinology 121:1335–1342.PubMedGoogle Scholar
  74. Lee SY, Anderson JW, Scott GL, Mossman HW (1983) Ultrastructure of the placenta and fetal membranes of the dog: II. The yolk sac. Am J Anat 166:313–327.PubMedGoogle Scholar
  75. Lerman S, Koszalka TR, Jensen M, Andrew CL, Beckman DA, Brent RL (1986) In vitro studies on the effect of yolk sac antisera on functions of the visceral yolk sac. I. Pinocytosis and transport of small molecules. Teratol 34:335–341.Google Scholar
  76. Letcher R, Simmen RCM, Bazer FW, Simmen FA (1989) Insulin-like growth factor-1 expression during early conceptus development in the pig. Biol Reprod 41:1143–1151.PubMedGoogle Scholar
  77. Lloyd JB (1990) Cell physiology of the rat visceral yolk sac: a study of pinocytosis and lysosome function. Teratology 41:383–393.PubMedGoogle Scholar
  78. Luckett WP (1974) Comparative development and evolution of the placenta in primates. Contrib Primatol 3:142–234.PubMedGoogle Scholar
  79. Luckett WP (1978) Origin and differentiation of the yolk sac and extraembryonic mesoderm in presomite human and rhesus monkey embryos. Am J Anat 152:59–98.PubMedGoogle Scholar
  80. Masters RA, Roberts RM, Lewis GS, Thatcher WW, Bazer FW, Godkin JD (1982) High molecular weight glycoproteins released by expanding, pre-attachment sheep, pig and cow blastocysts in culture. J Reprod Fertil 66:571–583.PubMedGoogle Scholar
  81. Matsumura G, Sasaki K (1988) The ultrastructure of megakaryopoietic cells of the yolk sac and liver in mouse embryo. Anat Rec 222:164–169.PubMedGoogle Scholar
  82. McArdle HJ, Priscott PK (1984) Uptake and metabolism of transferrin and albumin by rat yolk sac placenta. Am J Physiol 247:C409–C414.PubMedGoogle Scholar
  83. McDowell KJ, Sharp DC, Fazleabas AT, Roberts RM (1990) Two-dimensional polyacrylamide gel electrophoresis of proteins synthesized and released by conceptuses and endometria from pony mares. J Reprod Fertil 89:107–115.PubMedGoogle Scholar
  84. Meehan RR, Barlow RE, Hill RE, Hogan BL, Hastie ND (1984) Pattern of serum protein gene expression in mouse visceral yolk sac and foetal liver. EMBO J 3:1881–1885.PubMedGoogle Scholar
  85. Minor RR, Hoch PS, Koszalka TR, Brent TL, Kefalides NA (1976a) Organ cultures of the embryonic rat parietal yolk sac. I. Morphologic and autoradiographic studies of the deposition of the collagen and noncollagen glycoprotein components of basement membrane. Dev Biol 48:344–364.PubMedGoogle Scholar
  86. Minor RR, Strause EL, Koszalka TR, Brent RL, Kefalides NA (1976b) Organ cultures of the embryonic rat parietal yolk sac. II. Synthesis, accumulation and turnover of collagen and non-collagen basement membrane glycoproteins. Dev Biol 48:365–376.PubMedGoogle Scholar
  87. Minuth WW, Tiedemann K (1980) The pig yolk sac II. Analysis of synthesized proteins. Histochemistry 68:147–158.PubMedGoogle Scholar
  88. Moore MAS, Johnson GR (1976) Hemopoietic stem cells during embryonic development and growth. In: Carnie AB, Lala PK, Osmond DG (eds) Stem cells of renewing cell populations. Academic, New York, pp 323–330.Google Scholar
  89. Moore MAS, Metcalf D (1970) Ontogeny of the haemopoietic system. Yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Br J Haematol 18:279–296.PubMedGoogle Scholar
  90. Mossman HW (1987) Vertebrate fetal membranes. Rutgers University Press, New Brunswick.Google Scholar
  91. Murray MK, Segerson EC, Hansen PJ, Bazer FW, Roberts RM (1987) Suppression of lymphocyte activation by a high-molecular-weight glycoprotein released from preimplantation ovine and porcine conceptuses. Am J Reprod Immunol 14:38–44.Google Scholar
  92. Nahon J-L, Venetianer A, Sala-Trepat JM (1987) Specific sets of DNase I-hyper-sensitive sites are associated with the potential and overt expression of the rat albumin and α-fetoprotein genes. Proc Natl Acad Sci USA 84:2135–2139.PubMedGoogle Scholar
  93. Padykula HA, Deren JJ, Wilson TH (1966) Development of structure and function in the mammalian yolk sac. I. Developmental morphology and vitamin B12 uptake of the rat yolk sac. Dev Biol 13:311–348.PubMedGoogle Scholar
  94. Parr MB, Parr EL (1986) Permeability of the primary decidual zone in the rat uterus; studies using fluorescein-labeled proteins and dextrans. Biol Reprod 34:393–403.PubMedGoogle Scholar
  95. Poelman RE (1981) The head-process and the formation of definitive endoderm in the mouse embryo. Anat Embryol (Berl) 162:41–49.Google Scholar
  96. Ramsey EM (1982) The placenta, human and animal. Praeger, New York.Google Scholar
  97. Rasweiler JJ, IV (1974) Reproduction in the long-tongued bat, Glossophaga soriçina. II. Implantation and early embryonic development. Am J Anat 139:1–36.PubMedGoogle Scholar
  98. Rasweiler JJ, IV (1990) Implantation, development of the fetal membranes, and placentation in the captive black mastiff bat, Molossus ater. Am J Anat 187:109–136.PubMedGoogle Scholar
  99. Rossant J (1987) Cell lineage analysis in mammalian embryogenesis. Curr Top Dev Biol 23:115–146.PubMedGoogle Scholar
  100. Sasaki K, Kendall MD (1985) The morphology of the haematopoietic cells of the yolk sac in mice with particular reference to nucleolar changes. J Anat 140:279–295.PubMedGoogle Scholar
  101. Schlafke S, Welsh AO, Enders AC (1985) Penetration of the basal lamina of the uterine luminal epithelium during implantation in the rat. Anat Rec 212:47–56.PubMedGoogle Scholar
  102. Sheth K, Koszalka TR, Brent RL (1982) Steroid metabolism in the rat visceral yolk sac during pregnancy. Biol Reprod 26:209–217.PubMedGoogle Scholar
  103. Shi W-K, Heath JK (1984) Apolipoprotein expression by murine visceral yolk sac endoderm. J Embryol Exp Morphol 81:143–152.PubMedGoogle Scholar
  104. Sinha AA, Mossman HW (1966) Placentation of the sea otter. Am J Anat 119:521–554.PubMedGoogle Scholar
  105. Sklan D, Ross AC (1987) Synthesis of retinol-binding protein and transthyretin in yolk sac and fetus in the rat. J Nutr 117:436–442.PubMedGoogle Scholar
  106. Soprano DR, Soprano KJ, Goodman DS (1986) Retinol-binding protein and trans-thyretin mRNA levels in visceral yolk sac and liver during fetal development in the rat. Proc Natl Acad Sci USA 83:7330–7334.PubMedGoogle Scholar
  107. Steven DH (1975) Anatomy of the placental barrier. In: Steven DH (ed) Comparative placentation. Academic, New York, pp 25–57.Google Scholar
  108. Steven DH (1981) Placentation in the mare. J Reprod Fertil [Suppl] 31:41–55.Google Scholar
  109. Stephens RJ, Easterbrook N (1968) Development of the cytoplasmic membranous organelle in the endodermal cells of the yolk sac of the bat Tadarida brasiliensis cynocephala. J Ultrastruct Res 24:239–248.PubMedGoogle Scholar
  110. Stephens RJ, Easterbrook N (1969) A new cytoplasmic organelle, related to both lipid and glycogen storage materials in the yolk sac of the bat, Tadarida brasiliensis cynocephala. Am J Anat 124:47–56.PubMedGoogle Scholar
  111. Stephens RJ, Easterbrook N (1971) Ultrastructural differentiation of the endodermal cells of the yolk sac of the bat, Tadarida brasiliensis cynocephala. Anat Rec 169:207–242.PubMedGoogle Scholar
  112. Stroband HWJ, Taverne N, Bogaard M (1984) The pig blastocyst: its ultrastructure and the uptake of protein macromolecules. Cell Tissue Res 235:347–356.PubMedGoogle Scholar
  113. Takahashi K, Yamamura F, Naito M (1989) Differentiation, maturation, and proliferation of macrophages in the mouse yolk sac: a light-microscopic, enzymecytochemical, immunohistochemical, and ultrastructural study. J Leukocyte Biol 45:87–96.PubMedGoogle Scholar
  114. Thiriot-Hebert M (1987) Uptake of transferrin by the yolk-sac and its materno fetal transfer in vivo. Cell Mol Biol 33:183–189.PubMedGoogle Scholar
  115. Thoene JG, Forster S, Lloyd JB (1985) The role of pinocytosis in the cellular uptake of an amino acid. Biochem Biophys Res Commun 127:733–738.PubMedGoogle Scholar
  116. Tiedemann K (1976) On the yolk sac of the cat. Endoderm and mesothelium. Cell Tissue Res 173:109–127.PubMedGoogle Scholar
  117. Tiedemann K (1977) On the yolk sac of the cat. II. Erythropoietic phases, ultrastructure of aging primitive erythroblasts, and blood vessels. Cell Tissue Res 183:71–89.PubMedGoogle Scholar
  118. Tiedemann K (1979) The amniotic, allantoic and yolk sac epithelia of the cat: SEM and TEM studies. Anat Embryol (Berl) 158:75–94.Google Scholar
  119. Tiedemann K, Minuth WW (1980a) The pig yolk sac. I. Fine structure of the post-haematopoietic organ. Histochemistry 68:133–146.PubMedGoogle Scholar
  120. Tiedemann K, Minuth WW (1980b) Synthesis of serum proteins by the posthaemato-poietic feline yolk sac. Histochemistry 67:155–167.PubMedGoogle Scholar
  121. Van den Heuvel RL, Versele RM, Schoeters GER, Vanderborght LJ (1987) Stromal stem cells (CFU-f) in yolk sac, liver, spleen and bone marrow of pre-and postnatal mice. Br J Haematol 66:15–20.PubMedGoogle Scholar
  122. van Niekerk CH, Allen WH (1975) Early embryonic development in the horse. J Reprod Fertil [Suppl] 23:495–498.Google Scholar
  123. Welsh AO, Enders AC (1983) Occlusion and reformation of the rat uterine lumen during pregnancy. Am J Anat 167:463–477.PubMedGoogle Scholar
  124. Welsh AO, Enders AC (1987) Trophoblast-decidual cell interaction and establishment of maternal blood circulation in the parietal yolk sac placenta of the rat. Anat Rec 217:203–219.PubMedGoogle Scholar
  125. Williams CL, Priscott PK, Oliver IT, Yeoh GCT (1986) Albumin and transferrin synthesis in whole rat embryo cultures. J Embryol Exp Morphol 92:33–41.PubMedGoogle Scholar
  126. Wilson JM, King BF (1985) Transport of horseradish peroxidase across monkey trophoblastic epithelium in coated and uncoated vesicles. Anat Rec 211:174–183.PubMedGoogle Scholar
  127. Wimsatt WA (1962) Some aspects of the comparative anatomy of the mammalian placenta. Am J Obstet Gynecol 84:1568–1594.PubMedGoogle Scholar
  128. Wimsatt WA (1974) Morphogenesis of the fetal membranes and placenta of the black bear, Ursus americanus (Pallas). Am J Anat 140:471–496.PubMedGoogle Scholar
  129. Wimsatt WA, Enders AC (1980) Structure and morphogenesis of the uterus, placenta, and paraplacental organs of the neotropical disc-winged bat Thyroptera tricolor spix (Microchiroptera: Thyropteridae). Am J Anat 159:209–243.PubMedGoogle Scholar
  130. Wimsatt WA, Wislocki GB (1947) The placentation of the American shrews, Blarina brevicauda and Sorex fumeus. Am J Anat 80:361–436.PubMedGoogle Scholar
  131. Zavy MT, Mayer R, Vernon MW, Bazer FW, Sharp DC (1979) An investigation of the uterine luminal environment of non-pregnant and pregnant pony mares. J Reprod Fert [Suppl] 27:403–411.Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1993

Authors and Affiliations

  • B. F. King
  • A. C. Enders

There are no affiliations available

Personalised recommendations