Localisation of glycans in the placenta: A comparative study of epitheliochorial, endotheliochorial, and haemomonochorial placentation

Microscopy Research and Technique

Volumn 38, Issue 1-2, 1997, Pages 100-114

  Jones, Carolyn J P ^a   Dantzer, Vibeke ^b   Leiser, Rudolf ^c   Krebs, Christiane ^c   Stoddart, Robert W ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Capillary; Cow; Horse; Human; Lectins; Mink; Pig; Sheep; Trophoblast; Uterus

Indexed keywords

CAPILLARITY; HISTOLOGY; MAMMALS; POLYSACCHARIDES; PROTEINS;

CAPILLARY; COW; HORSE; HUMAN; LECTIN; MINK; PIG; SHEEP; TROPHOBLAST; UTERUS;

TISSUE;

GLYCAN; LECTIN;

ANIMAL TISSUE; ARTICLE; CAPILLARY; COMPARATIVE STUDY; COW; HORSE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MINK; NONHUMAN; PLACENTA; PRIORITY JOURNAL; SHEEP; SWINE; TISSUE DISTRIBUTION; TROPHOBLAST; UTERUS;

ANIMALIA; EQUUS CABALLUS; MAMMALIA; MUSTELA VISON; OVIS ARIES; SUS SCROFA;

EID: 0030853936     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0029(19970701/15)38:1/2<100::AID-JEMT11>3.0.CO;2-T     Document Type: Article

References (103)

1. Allen, A.K., Neuberger, A., and Sharon, N. (1973) The purification, composition and specificity of wheat germ agglutinin. Biochem. J., 131:155-162.
2. Anderson, T.L., Olson, G.E., and Hoffman, L.H. (1986) Stage-specific alterations in the apical membrane glycoproteins of endometrial epithelial cells related to implantation in rabbits. Biol. Reprod., 34:701-720.
3. Azuma, M., Kanai, Y., Ogura, A., Kurohmaru, M., and Hayashi, Y. (1991) Changes in cell surface and intracellular glycoproteins of trophoblastic giant cells during mouse placentation. Histochemistry, 95:541-548.
4. Bahia, S.S., McMahon, R.F.T., Hobbis, J., Taylor, T.V., and Stoddart, R.W. (1993) Pelvic ileo-anal reservoirs: A lectin histochemical study. Histochem. J., 25:392-400.
5. Baker, D.A., Sugii, S., Kabat, E.A., Murray Ratcliffe, R.M., Hermentin, P., and Lemieux, R.U. (1983) Immunochemical studies on the combining sites of Forssman hapten reactive hemagglutinins from Dolichos biflorus, Helixpomatia and Wisteria floribunda. Biochemistry 22:2741-2750.
6. Ball, R.Y., Stoddart, R.W., Jones, C.J.P., and Mitchinson, M.J. (1989) Saccharide expression on wounded endothelial cell monolayers in vitro. J. Cell Sci., 93:163-172.
7. Bazer, F.W., and Roberts, R.M. (1983) Biochemical aspects of conceptus-endometrial interactions. J. Exp. Zool., 228:373-383.
8. Bhattacharyya, L., Haraldsson, M., and Brewer, C.F. (1988) Precipitation of galactose-specific lectins by complex-type oligosaccharides and glycopeptides: Studies with lectins from Ricinus communis (Agglutinin I), Erythrina indica, Erythrina arborescens, Abrus precatorius (Agglutinin), and Glycine max (Soybean). Biochemistry, 27:1034-1041.
9. Billington, W.D., and Wild A.E. (1979) Maternal immunological factors in embryonic and post-natal development. In: Maternal Effects in Development. D.R. Newth and M. Balls, eds. British Society for Developmental Biology Symposium 4. Cambridge University Press, pp. 321-350.
10. Björkman, N., Dantzer, V., and Leiser, R. (1989) Comparative placentation in laboratory animals. A review. Scand. J. Lab. Sci., 16:129-158.
11. Boeck De, H., Loontiens, F.G., Lis, H., and Sharon, N. (1984) Binding of simple carbohydrates and some N-acetyllactosamine-containing oligosaccharides to Erythrina cristagalli agglutinin as followed with a fluorescent indicator ligand. Arch. Biochem. Biophys., 234:297-304.
12. Bükers, A., Friedrich J., Nalbach, B.P., and Denker, H.-W. (1990) Changes in lectin binding patterns in rabbit endometrium during pseudopregnancy, early pregnancy and implantation. Trophoblast Res., 4:285-305.
13. Byatt, J.C., Welply, J.K., Leimgruber, R.M., and Collier, R.J. (1990) Characterization of glycosylated bovine placental lactogen and the effect of enzymatic deglycosylation on receptor binding and biological activity. Endocrinology, 127:1041-1049.
14. Chávez, D.J. (1990) Possible involvement of D-galactose in the implantation process. Trophoblast Res., 4:259-272.
15. Cook, G.M.W., and Stoddart, R.W. (1973) Surface Carbohydrates of the Eukaryotic Cell. Academic Press, New York.
16. Damjanov, I., and Lee M.-C. (1986) Pregnancy-related changes in murine and human endometrium revealed by differential binding of fluoresceinated lectins. In: Pregnancy Proteins in Animals. J. Hau, ed. Walter de Gruyter, Berlin, pp. 177-183.
17. Dantzer, V. (1985) Electron microscopy of the initial stages of placentation in the pig. Anat. Embryol., 172:281-293.
18. Dantzer, V., and Leiser, R. (1992) Areola-gland subunits in the epitheliochorial types of placentae from the horse and pig. Micron Microsc. Acta, 23:79-80.
19. Dantzer, V., Leiser, R., Kaufmann P., and Luckhardt, M. (1988) Comparative morphological aspects of placental vasculature. Trophoblast Res., 3:235-260.
20. Debray, H., Decout, D., Strecker, G., Spik, G., and Montreuil, J. (1981) Specificity of twelve lectins towards oligosaccharides and glycopeptides related to N-glycosylproteins. Eur. J. Biochem., 117:41-55.
21. Denker, H.-W. (1994) Endometrial receptivity: Cell biological aspects of an unusual epithelium. A review. Ann. Anat., 176:53-60.
22. Donaldson, W.L., Oriol, J.G., Pelkaus, C.L., and Antczak, D.F. (1994) Paternal and maternal major histocompatibility complex class 1 antigens are expressed co-dominantly by equine trophoblast. Placenta, 15:123-135.
23. Dreskin, R.B., Spicer, S.S., and Greene, W.B. (1970) Ultrastructural localization of chorionic gonadotropin in human term placenta. J. Histochem. Cytochem., 18:862-874.
24. Edwards, D., Jones, C.J.P., Sibley, C.P., and Nelson, D.M. (1993) Paracellular permeability pathways in the human placenta: A quantitative and morphological study of maternal-fetal transfer of horseradish peroxidase. Placenta, 14:63-73.
25. Enders, A.C. (1957) Histological observations on the chorio-allantoic placenta of the mink. Anat. Rec., 127:231-245.
26. Etzler, M.E., and Kabat, E.A. (1970) Purification and characterization of a lectin (plant hemagglutinin) with blood group A specificity from Dolichos biflorus. Biochemistry, 9:869-877.
27. Foidart, J.M., Christiane, Y., and Emonard, H. (1990) Interactions between human trophoblast cells and the extracellular matrix of the endometrium. Specific expression of α-galactose residues by invasive human trophoblast cells. Trophoblast Res., 4:159-177.
28. Gallagher, J.T., Morris, A., and Dexter, T.M. (1985) Identification of two binding sites for wheat germ agglutinin on polylactosamine-type oligosaccharides. Biochem. J., 231:115-122.
29. Ghosh, N.K., Goldman, S.S., and Fishman, W.H. (1967) Human placental alkaline phosphatase. A sialoprotein. Enzymologia, 33:113-124.
30. Green, E.D., and Baenziger, J.U. (1987) Oligosaccharide specificities of Phaseolus vulgaris leukoagglutinating and erythroagglutinating phytohemagglutinins. Interactions with N-glycanase-released oligosaccharides. J. Biol. Chem., 262:12018-12029.
31. Guillomot, M., Fléchon, J.-E., and Winterberger-Torres, S. (1982) Cytochemical studies of uterine and trophoblastic surface coats during blastocyst attachment in the ewe. J. Reprod. Fert., 65:1-8.
32. Hammarström, S., Hammarström, M.L., Sunblad, G., Arnarp, J., and Lönngren, J. (1982) Mitogenic leukoagglutinin from Phaseolus vulgaris binds to a pentasaccharide unit in N-acetyllactosamine-type glycoprotein glycans. Proc. Natl Acad. Sci. USA, 79:1611-1615.
33. Hewitt, K., Beer, A.E., and Grinnell, F. (1979) Disappearance of anionic sites from the surface of the rat endometrial epithelium at the time of blastocyst implantation. Biol. Reprod., 21:691-707.
34. Hill, J.A. (1990) Immunological mechanisms of pregnancy maintenance and failure: A critique of theories and therapy. Am. J. Reprod. Immunol., 22:33-42.
35. Hindsgaul, O., Khare, D.P., Bach, M., and Lemieux, R.U. (1985) Molecular recognition III. The binding of the H-type 2 human blood group determinant by the lectin of Ulex europaeus. Canad. J. Chem., 63:2653-2658.
36. Iglesias, J.L., Lis, H., and Sharon, N. (1982) Purification and properties of a D-galactose/N-acetyl-D-galactosamine-specific lectin from Erythrina cristagalli. Eur. J. Biochem., 123:247-252.
37. Ito, S., and Karnovsky, J.M. (1968) Formaldehyde-glutaraldehydetrinitro fixation (yellow fix). J. Cell Biol., 39:168a-169a.
38. Johnson, P.M., and White, C.M. (1979) Distribution of lectin binding on human placental tissue sections. Protides Biol. Fluids, 27th Colloquium 1979. H. Peeters, ed. Pergamon Press, Oxford and New York, pp. 503-506.
39. Johnson, P.M., Brown, P.J., and Page Faulk, W. (1980) Immunobiological aspects of the human placenta. Oxford Rev. Reprod. Biol., 2:1-40.
40. Jones, C.J.P., and Fox, H. (1976) An ultrahistochemical study of the distribution of acid and alkaline phosphatases in placentae from normal and complicated pregnancies. J. Path., 118:143-151.
41. Jones, C.J.P., Mosley, S.M., Jeffrey, I.J.M., and Stoddart, R.W. (1987) Elimination of the non-specific binding of avidin to tissue sections. Histochem. J., 19:264-268.
42. Jones, C.J.P., Benbow, E.W., Knox, W.F., and Stoddart, R.W. (1988) Method for showing human spermatogenesis using Arachis hypogaea (AHA) lectin. J. Clin. Pathol., 41:1017-1018.
43. Jones, C.J.P., Stoddart, R.W., Bierings, M.B., and van Dijk, H.P. (1991) Expression of glycoproteins on and within placental cytotrophoblast cells in culture. Trophoblast Res., 5:311-329.
44. Jones, C.J.P, Morrison, C.A., and Stoddart, R.W. (1992a) Histochemical analysis of rat testicular glycoconjugates. 2) β-galactosyl residues in O- and N-linked glycans in seminiferous tubules. Histochem. J., 24:327-336.
45. Jones, C.J.P., Ward, B.S., and Stoddart, R.W. (1992b) Glycan distribution at the interaction zone of the porcine placenta. J. Pathol., 168:134A.
46. Jones, C.J.P., Morrison, C.A., and Stoddart, R.W. (1993) Histochemical analysis of rat testicular glycoconjugates. 3) Non-reducing terminal residues in seminiferous tubules. Histochem. J., 25:711-718.
47. Jones, C.J.P., Koob, B., Stoddart, R.W., Hoffmann, B., and Leiser, R. (1994) Histochemical analysis of glycans in ovine and bovine near-term placental binucleate cells. Cell Tissue Res., 278:601-610.
48. Jones, C.J.P., Dantzer, V., and Stoddart, R.W. (1995) Changes in glycan distribution within the porcine interhaemal barrier during gestation. Cell Tissue Res., 279:551-564.
49. Jones, C.J.P., Bäcklin, B-M., Stoddart, R.W., and Dantzer, V. (1997) Environmental pollutants as aetiological agents in female reproductive pathology: placental glycan expression in normal and polychlorinated biphenyl (PCB)-exposed mink (Mustela vision). Placenta (in press).
50. Kabawat, S.E., Mostoufi-Zadeh, M., Driscoll, S.G., and Bhan, A.K. (1985) Implantation site in normal pregnancy. A study with monoclonal antibodies. Am. J. Path., 118:76-84.
51. Kessler, M.A., Duello, T.M., and Schuler, L.A. (1991) Expression of prolactin-related hormones in the early bovine conceptus, and potential for paracrine effect on the endometrium. Endocrinology, 129:1885-1895.
52. Kimber, S.J. (1986) Distribution of lectin receptors in postimplantation mouse embryos at 6-8 days gestation. Am. J. Anat., 177:203-219.
53. Knibbs, R.N., Osborne, S.E., Glick, G.D., and Goldstein, I.J. (1993) Binding determinants of the sialic acid-specific lectin from the slug Limax flavus. J. Biol. Chem., 268:18524-18531.
54. Krebs, C., Winther, H., Dantzer, V., and Leiser, R. (1995) Vascular interrelationship of near term mink placenta: Light microscopy combined with scanning electron microscopy of corrosion casts. Microsc. Res. Techn. (this issue).
55. Lala, P.K., Kearns, M., Parhar, R.S., Scodras, J., and Johnson, S. (1986) Immunological role of the cellular constituents of the decidua in the maintenance of semiallogeneic pregnancy. Ann. N.Y. Acad. Sci. USA, 476:183-205.
56. Lalani, E.-N. M.A., Bulmer, J.N., and Wells, M. (1987) Peroxidase-labelled lectin binding of human extravillous trophoblast. Placenta, 8:15-26.
57. Lee, M.-C., and Damjanov, I. (1984) Lectin histochemistry of human placenta. Differentiation, 28:123-128.
58. Lee, M.-C., Wu, T.-C., Wan, Y.-J., and Damjanov, I. (1983) Pregnancyrelated changes in the mouse oviduct and uterus revealed by differential binding of fluoresceinated lectins. Histochemistry, 79: 365-375.
59. Lehmann, M., Rüsse I., and Sinowatz, F. (1992) Nachweis von Lektinbindungsstellen am Trophoblast des Rindes während der Frühgravidität. Anat. Histol. Embryol., 21:263-273.
60. Leiser, R., and Kaufmann, P. (1994) Placental structure: In a comparative aspect. Exp. Clin. Endocrinol., 102:122-134.
61. Loke, Y.W., King, A., and Grabowska, A. (1990) Antigenic expression by migrating trophoblast and its relevance to implantation. Trophoblast Res., 4:191-207.
62. Lotan, R., and Sharon N. (1978) Peanut (Arachis hypogaea) agglutinin Meth. Enzymol., 50:361-367.
63. Maddox, P.H., and Jenkins, D. (1987) 3-Aminopropyltriethoxysilane (APES): A new advance in section adhesion. J. Clin. Pathol., 40:1256-1257.
64. Martin, B.J., Spicer, S.S., and Smythe, N.M. (1974) Cytochemical studies of the maternal surface of the syncytiotrophoblast of human early and term placenta. Anat. Rec., 178:769-785.
65. McMahon, R.F.T., Benbow, E.W., Lofthouse, A.K., and Stoddart, R.W. (1989) Human salivary gland glycoconjugates: A lectin histochemical study. Histochem. J., 21:663-674.
66. Miller, R.L., Collawn, J.F. Jr., and Fish, W.W. (1982) Purification and macromolecular properties of a sialic acid-specific lectin from the slug Limax flavus. J. Biol. Chem., 257:7574-7580.
67. Mossman, H.W. (1987) Vertebrate Fetal Membranes. Rutgers University Press, New Brunswick, New Jersey.
68. Munson, L., Kao, J.J., and Schlafer, D.H. (1989) Characterisation of glycoconjugates in the bovine endometrium and chorion by lectin histochemistry. J. Reprod. Fert., 87:509-517.
69. Muramatsu, T., Condamine, H., Gachelin G., and Jacob, F. (1980) Changes in fucosyl-glycopeptides during early post-implantation embryogenesis in the mouse. J. Embryol. Morphol., 57:25-36.
70. Nalbach, B.P., and Denker, H.-W. (1983) Stage-dependent changes in lectin binding patterns in rabbit uterus during the preimplantation period and implantation. Eur. J. Cell Biol Suppl. 4:13.
71. Nelson, D.M., Smith, C.S., Enders, A.C., and Donohue T.M. (1975) The nonuniform distribution of acidic components on the human placental syncytial trophoblast surface membrane: A cytochemical and analytical study. Anat. Rec., 184:159-182.
72. Nicolson, G.L. (1978) Ultrastructural localization of lectin receptors. In: Advanced Techniques in Biological Electron Microscopy, Vol 2. J.K. Koehler, ed. Springer-Verlag, New York, pp. 1-38.
73. Nilsson, O. (1974) Changes of the luminal surface of the rat uterus at blastocyst implantation. Z. Anat. Entwickl., 144:337-342.
74. Pereira, M.E.A., and Kabat, E.A. (1974) Specificity of purified hemagglutinin (lectin) from Lotus tetragonolobus. Biochemistry, 13:3184-3192.
75. Pereira, M.E.A., Kabat, E.A., and Sharon, N. (1974) Immunochemical studies on the specificity of Soybean agglutinin. Carbohydrate Res., 37:89-102.
76. Pereira, M.E.A., Kisailus, E.C., Gruezo, F., and Kabat, E.A. (1978) Immunochemical studies on the combining site of the blood group H-specific lectin 1 from Ulex europeus seeds. Arch. Biochem. Biophys., 185:108-115.
77. Psychoyos, A., and Martel, D. (1985) Embryo-endometnal interactions at implantation. In: Implantation of the Human Embryo. R.E. Edwards, J.M. Purdy, and P.C. Steptoe, eds. Academic Press, London, pp. 195-210.
78. Redline, R. W., and Lu, C.Y. (1989) Localization of fetal major histocompatibility complex antigens and maternal leukocytes in murine placenta. Implications for maternal-fetal immunological relationship. Lab. Invest., 61:27-36.
79. Roberts. I.S.D., Jones, C.J.P., and Stoddart, R.W. (1990) Lectin histochemistry of the mast cell: Heterogeneity of rodent and human mast cell populations. Histochem. J., 22:73-80.
80. Sarkar, M., Wu, A.M., and Kabat, E.A. (1981) Immunochemical studies on the carbohydrate specificity of Maclura pomifera lectin. Arch. Biochem. Biophys., 209:204-218.
81. Schlafke, S., and Enders, A.C. (1975) Cellular basis of interaction between trophoblast and uterus at implantation. Biol. Reprod., 12:41-65.
82. Sharon, N. (1984) Carbohydrates as recognition determinants in phagocytosis and in lectin-mediated killing of target cells. Biol. Cell, 51:239-246.
83. Shibuya, N., Goldstein, I.J., Broekaert, W.F., Nsimba-Lubaki, M., Peeters, B., and Peumans, W.J. (1987) The elderberry (Sambucus nigra L.) bark lectin recognizes the Neu5Ac(α2,6)Gal/GalNAc sequence. J. Biol. Chem., 262:1596-1601.
84. Shibuya, N., Goldstein, I.J., Van Damme, E.J.M., and Peumans, W.J. (1988) Binding properties of a mannose-specific lectin from the Snowdrop (Galanthus nivalis) bulb. J. Biol. Chem., 263:728-734.
85. Smith, C.H., Nelson, D.M., King, B.F., Donohue, T.M., Ruzycki, S.M., and Kelley, L.K. (1977) Characterization of a microvillous membrane preparation from human placental syncytiotrophoblast: A morphologic, biochemical and physiologic study. Am. J. Obstet. Gynecol., 128:190-197.
86. Sueyoshi, S., Tsuji, T., and Osawa, T. (1988) Carbohydrate-binding specificities of five lectins that bind to O-glycosyl-linked carbohydrate chains. Quantitative analysis by frontal-affinity chromatography. Carbohydrate Res., 178:213-224.
87. Sugii, S., and Kabat, E.A. (1980) Immunochemical specificity of the combining site of Wisteria floribunda hemagglutinin. Biochemistry, 19:1192-1199.
88. Surani, M.A.H., and Fishel, S.B. (1980) Blastocyst-uterine interactions at implantation. Progr. reprod. Biol., 7:14-27.
89. Sutton, P., Stoddart, R.W., and Hutchinson, I.V. (1992) Altered patterns of glycosylation on rat lymphocytes associated with activation. Immunology, 76:472-477.
90. Swaminathan, N., and Bahl, O.P. (1970) Dissociation and recombination of the subunits of human chorionic gonadotropin. Biochem. Biophys. Res. Comm., 40:422-447.
91. Thrower, S., Bulmer, J.N., Griffin, N.R., and Wells, M. (1991) Further studies of lectin binding by villous and extravillous trophoblast in normal and pathological pregnancy. Int. J. Gynecol. Path., 10:238-251.
92. Trowbridge, I.S. (1974) Isolation and characterization of a mitogenic lectin from Pisum sativum. J. Biol. Chem., 249:6004-6012.
93. Wang, W-C., and Cummings, R.D. (1988) The immobilized leukoagglutinin from the seeds of Maackia amurensis binds with high affinity to complex-type Asn-linked oligosacharides containing terminal sialic acid-linked α2,3 to penultimate galactose residues. J. Biol. Chem., 263:4576-4585.
94. Whyte, A. (1980) Lectin binding by microvillous membranes and coated-pit regions of human syncytial trophoblast. Histochem. J., 12:599-607.
95. Whyte, A. (1983) Biochemistry of the human syncytiotropnoblast plasma membrane. In: Biology of Trophoblast. Y.W. Loke and A. Whyte, eds. Elsevier Science Publishers B.V., Amsterdam, pp. 513-533.
96. Whyte, A., and Allen, W.R. (1985) Equine endometrium at preimplantation stages of pregnancy has specific glycosylated regions. Placenta, 6:537-542.
97. Whyte, A., and Robson, T. (1984) Saccharides localized by fluorescent lectins on trophectoderm and endometrium prior to implantation in pigs, sheep and equids. Placenta, 5:533-540.
98. Wimsatt, W.A. (1962) Some aspects of the comparative anatomy of the mammalian placenta. Am. J. Obs. Gyn., 84:1568-1594.
99. Wooding, F.P.B. (1992) Current topic: The synepitheliochorial placenta of ruminants: Binucleate cell fusions and hormone production. Placenta, 13:101-113.
100. Wooding, F.B.P., and Flint, A.P.F. (1994) Placentation. In: Marshall's Physiology of Reproduction, Vol. 3, Pregnancy and Lactation, Ch. 4. G.E. Lamming, ed. Chapman and Hall, London, pp. 233-460.
101. Yanagimachi, R., and Nicolson, G.L. (1976) Lectin binding Properties of hamster egg zona pellucida and plasma membrane during maturation and pre-implantation development. Exp. Cell Res., 100:249-257.
102. Zhou, Z.X., Deng, Z.P., and Chen, J.L. (1994) Characterization of glycoconjugates in the endometrium of the miniature pig during different reproductive periods. J. Reprod. Fert., 100:417-423.
103. Zieler, C.G., Kessler, M.A., and Schuler, L.A. (1990) Characterization of a novel prolactin-related protein from bovine fetal placenta. Endocrinology, 126:2377-2382.