Human placental Fc receptors and the transmission of antibodies from mother to fetus

Journal of Reproductive Immunology

Volumn 37, Issue 1, 1997, Pages 1-23

  Simister, Neil E ^a   Story, Craig M ^b  

^a BRANDEIS UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Annexin II; Fc RI; Fc RII; Fc RIII; FcRn; IgG; Placental; Placental alkaline phosphatase

Indexed keywords

FC RECEPTOR; FETAL ANTIGEN; IMMUNOGLOBULIN G; MATERNAL ANTIBODY;

ANTIGEN ANTIBODY COMPLEX; FEMALE; FETOPLACENTAL UNIT; FETUS; HUMAN; PLACENTAL TRANSFER; PREGNANCY; PRIORITY JOURNAL; REVIEW; SYNCYTIOTROPHOBLAST; VASCULAR ENDOTHELIUM;

ANIMALS; HUMANS; IMMUNITY, MATERNALLY-ACQUIRED; IMMUNOGLOBULIN G; PLACENTA; RATS; RECEPTORS, FC;

EID: 0031574054     PISSN: 01650378     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-0378(97)00068-5     Document Type: Review

References (143)

1. Aarli, Å., Skeie Jensen, T., Ulvestad, E., Matre, R., 1993. Suppression of mitogen-induced lymphoproliferation by soluble IgG Fc receptors in retroplacental serum in normal human pregnancy. Scand. J. Immunol. 37, 237-243.
2. Abrahamson, D.R., Powers, A., Rodewald, R., 1979. Intestinal absorption of immune complexes by neonatal rats: a route of antigen transfer from mother to young. Science 206, 567-569.
3. Ahouse, J.J., Hagerman, C.L., Mittal, P., Gilbert, D.J., Copeland, N.G., Jenkins, N.A., Simister, N.B., 1993. A mouse MHC class-I-like Fc receptor encoded outside the MHC. J. Immunol. 151, 6076-6088.
4. Anderson, C.L., Abraham, G.N., 1980. Characterization of the Fc receptor for IgG on a human macrophage cell line, U937. J. Immunol. 125, 2735-2741.
5. Armato, M., Huppi, P., Imbach, P., Llanto, A., Burgi, W., 1993. Serial IgG and IgM serum levels after infusion of different Ig-preparations (IgG or IgM-enriched) in preterm infants. Pediatr. Allergy Immunol. 4, 217-220.
6. Balfour, A.H., Jones, E.A., 1977. The binding of plasma proteins to human placental cell membranes. Clin. Sci. Mol. Med. 52, 383-394.
7. Balfour, A.H., Jones, E.A., 1978. Properties of receptors for IgG on human placental cell membranes. Int. Archs. Allergy Appl. Immunol. 56, 435-442.
8. Barrett, B., Volwiler, W., 1957. Agammaglobulinemia and hypogammaglobulinemia-the first five years. J. Am. Med. Assoc. 164, 866-870.
9. Beal, R.W., 1979. Non-rhesus (D) blood group isoimmunization in obstetrics. Clin. Obstet. Gynecol. 6, 493-508.
10. Beckman, G., Beckman, L., Holm, S., Sikstrom, C., Wennberg, C., 1995. Placental alkaline phosphatase types and transplacental IgG transport. Hum. Hered. 45, 1-5.
11. Benlounes, N., Chedid, R., Thuillier, F., Desjeux, J.F., Rousselet, F., Heyman, M., 1995. Intestinal transport and processing of immunoglobulin G in the neonatal and adult rat. Biol. Neonate 67, 254-263.
12. Berken, A., Benacerraf, J., 1966. Properties of antibodies cytophilic for macrophages. J. Exp. Med. 123, 119-144.
13. Berryman, M., Rodewald, R., 1995. β2-microglobulin co-distributes with the heavy chain of the intestinal IgG-Fc receptor throughout the transepithelial transport pathway of the neonatal rat. J. Cell Sci. 108, 2347-2360.
14. Blumberg, R.S., Koss, T., Story, C.M., Barisani, D., Polischuk, J., Lipin, A., Pablo, L., Green, R., Simister, N.E., 1995. An MHC class I-related receptor for IgG on rat hepatocytes. J. Clin. Invest. 95, 6246-6251.
15. Börner, P., Deicher, H., Heide, K., Reinecke, J., 1974. Evidence for the participation of the Fc portion of immunoglobulin G in maternofoetal immunoglobulin transfer in the human. In: Centaro, A., Carretti, N. (Eds.), Immunology in Obstetrics and Gynecology. Excerpta Medica, Amsterdam, pp. 272-274.
16. Brambell, F.W.R., Halliday, R., Morris, I.G., 1958. Interference by human and bovine serum and serum protein fractions with the absorption of antibodies by suckling rats and mice. Proc. R. Soc. Lond. B 149, 1-11.
17. Brambell, F.W.R., Hemmings, W.A., Oakley, C.L., Porter, R.R., 1960. The relative transmission of the fractions of papain hydrolysed homologous gamma-globulin from the uterine cavity to the foetal circulation in the rabbit. Proc. R. Soc. Lond. B 151, 478-482.
18. Bright, N.A., Ockleford, C.D., 1994. Heterogeneity of Fc gamma receptor-bearing cells in human term amniochorion. Placenta 15, 247-255.
19. Bright, N.A., Ockleford, C.D., 1995a. Cytotrophoblast cells: a barrier to maternofetal transmission of passive immunity. J. Histochem. Cytochem. 43, 933-944.
20. Bright, N.A., Ockleford, C.D., 1995b. Ultrastructural distribution of endogenous immunoglobulin-G in human term amniochorion. Cell Tissue Res. 281, 367-374.
21. Bright, N.A., Ockleford, C.D., Anwar, M., 1994. Ontogeny and distribution of Fc gamma receptors in the human placenta. Transport or immune surveillance?. J. Anat. 184, 297-308.
22. Brown, P.J., Johnson, P.M., 1981. Fcγ receptor activity on isolated syncytiotrophoblast microvillous membrane. Immunology 42, 313-319.
23. Bryan, E.M., 1977. IgG deficiency in association with placental oedema. Early Hum. Dev. 1, 133-143.
24. Buhl, W.J., Garcia, M.T., Zipfel, M., Schiebler, W., Gehring, U., 1991. A series of annexins from human placenta and their characterization by use of an endogenous phospholipase A2. Eur. J. Cell Biol. 56, 381-390.
25. Burmeister, W.P., Gastinel, L.N., Simister, N.E., Blum, M.L., Bjorkman, P.J., 1994a. Crystal structure at 2.2 Å resolution of the MHC-related neonatal Fc receptor. Nature 372, 336-343.
26. Burmeister, W.P., Huber, A.H., Bjorkman, P.J., 1994b. Crystal structure of the complex between the rat neonatal Fc receptor and Fc. Nature 372, 379-383.
27. Chandra, R.K., 1976. Levels of IgG subclasses, IgA, IgM, and tetanus antitoxin in paired maternal and foetal sera: findings in healthy pregnancy and placental insufficiency. In: Hemmings, W.A. (Ed.), Maternofoetal Transmission of Immunoglobulins, Cambridge University Press, Cambridge, pp. 77-87.
28. Clarkson, S.B., Kimberly, R.P., Valinsky, J.E., Witmer, M.D., Bussel, J.B., Nachman, R.L., Unkeless, J.C., 1986. Blockade of clearance of immune complexes by an anti-Fcγ receptor monoclonal antibody. J. Exp. Med. 164, 474-489.
29. Dancis, J., Lind, J., Oratz, M., Smolens, J., Vara, P., 1961. Placental transfer of proteins in human gestation. Am. J. Obstet. Gynecol. 82, 167-171.
30. Doughty, R.W., Gelsthorpe, K., 1976. Some parameters of lymphocyte antibody activity through pregnancy and further eluates of placental material. Tissue Antigens 8, 43-48.
31. Down, J.A., Kawakami, M., Klein, M.H., Dorrington, K.J., 1989. Proteins associated with activity of Fc receptors on isolated human placental syncytiotrophoblast microvillous plasma membranes. Placenta 10, 227-246.
32. Einhorn, M.S., Granoff, D.M., Nahm, M.H., Quinn, A., Shackelford, P.O., 1987. Concentrations of antibodies in paired maternal and infant sera: relationship to IgG subclass. J. Pediatr. 111, 783-788.
33. Engelhardt, W., Gorczytza, H., Butterweck, A., Monkemann, H., Frey, J., 1991. Structural requirements of the cytoplasmic domains of the human macrophage Fc gamma receptor IIa and B cell Fc gamma receptor IIb2 for the endocytosis of immune complexes. Eur. J. Immunol. 21, 2227-2238.
34. Esterman, A.L., Dancis, J., Lee, J.D., Rindler, M.J., 1995. Two mechanisms for IgG uptake in cultured human trophoblast: evidence for a novel high affinity Fc receptor. Pediatr. Res. 38, 1-6.
35. Faulk, W.P., Temple, A., 1976. Distribution of β2 microglobulin and HLA in chorionic villi of human placentae. Nature 262, 799-802.
36. Faulk, W.P., Johnson, P.M., 1977. Immunological studies of human placentae: identification and distribution of proteins in mature chorionic villi. Clin. Exp. Immunol. 27, 365-375.
37. Firth, J.A., Leach, L., 1996. Not trophoblast alone: a review of the contribution of the fetal microvasculature to transplacental exchange. Placenta 17, 89-96.
38. Fishman, W.H., 1974. Perspectives on alkaline phosphatase isoenzymes. Am. J. Med. 56, 617-650.
39. Friden, B.E., Makiya, R., Nilsson, B.M., Holm, S., Stigbrand, T.I., 1994. The human placental immunoglobulin G receptor and immunoglobulin G transport. Am. J. Obstet. Gynecol. 171, 258-263.
40. Fries, L.F., Hall, R.P., Lawley, T.J., Crabtree, G.R., Frank, M.M., 1982. Monocyte receptors for the Fc portion of IgG studies with monomeric human IgG1 : normal in vitro expression of Fc gamma receptors in HLA-B8/Drw3 subjects with defective Fc gamma-mediated in vivo clearance. J. Immunol. 129, 1041-1049.
41. Ghetie, V., Hubbard, J.G., Kim, J.K., Tsen, M.F., Lee, Y., Ward, E.S., 1996. Abnormally short serum half-lives of IgG in β2-microglobulin-deficient mice. Eur. J. Immunol. 26, 690-696.
42. Gitlin, D., Biasucci, A., 1969. Development of γG, γA, γM, βIC/βIA, C'1 esterase inhibitor, ceruloplasmin, transferrin, hemopexin, haptoglobin, fibrinogen, plasminogen, α1-antitrypsin, orosomucoid, β-lipoprotein, α2-macroglobulin, and prealbumin in the human conceptus. J. Clin. Invest. 48, 1433-1446.
43. Gitlin, D., Kumate, J., Urrusti, J., Morales, C., 1964. The selectivity of the human placenta in the transfer of plasma proteins from mother to fetus. J. Clin. Invest. 43, 1938-1951.
44. 2+-dependent manner. Proc. Natl. Acad. Sci. USA 83, 4258-4262.
45. Gusdon, J.P., 1969. Fetal and maternal immunoglobulin levels during pregnancy. Am. J. Obstet. Gynecol. 103, 895-900.
46. Guyer, R.L., Koshland, M.E., Knopf, P., 1976. Immunoglobulin binding by mouse intestinal epithelial cell Fc receptors. J. Immunol. 117, 587-593.
47. Hajjar, K.A., Jacovina, A.T., Chacko, J., 1994. An endothelial cell receptor for plasminogen/ tissue plasminogen activator. I. Identity with annexin II. J. Biol. Chem. 269, 21191-21197.
48. Harrison, P.T., Davis, W., Norman, J.C., Hockaday, A.R., Allen, J.M., 1994. Binding of monomeric immunoglobulin G triggers Fc gamma RI-mediated endocytosis. J. Biol. Chem. 269, 24396-24402.
49. Hay, F.C., Hull, M.G., Torrigiani, G., 1971. The transfer of human IgG subclasses from mother to foetus. Clin. Exp. Immunol. 9, 355-358.
50. Hillier, L., Clark, N., Dubuque, T., Elliston, K., Hawkins, M., Holman, M., Hultman, M., Kucaba, T., Le, M., Lennon, G., Marra, M., Parsons, J., Rifkin, L., Rohlfing, T., Tan, F., Trevaskis, E., Waterston, R., Williamson, A., Wohldmann, P., Wilson, R., 1995. Accession number AA082737. GenBank.
51. Huizinga, T.W., Kerst, M., Nuyens, J.H., Vlug, A., von dem Borne, A.E., Roos, D., Tetteroo, P.A., 1989. Binding characteristics of dimeric IgG subclass complexes to human neutrophils. J. Immunol. 142, 2359-2364.
52. Israel, E.J., Patel, V.K., Taylor, S.F., Marshak-Rothstein, A., Simister, N.E., 1995. Requirement for a β2-microglobulin-associated Fc receptor for acquisition of maternal IgG by fetal and neonatal mice. J. Immunol. 154, 6246-6251.
53. Israel, E.J., Wilsker, D.F., Hayes, K.C., Schoenfeld, D., Simister, N.E., 1996. Increased clearance of IgG in mice that lack β2-microglobulin: possible protective role of FcRn. Immunology 89, 573-578.
54. Jeannet, M., Werner, C., Ramirez, E., Vassalli, P., Faulk, W.P., 1977. Anti-HLA, anti-human 'Ia-like' and MLC blocking activity of human placental IgG. Transplant. Proc. 9, 1417-1422.
55. Jindal, H.K., Chaney, W.G., Anderson, C.W., Davis, R.G., Vishwanatha, J.K., 1991. The protein-tyrosine kinase substrate, calpactin I heavy chain (p36), is part of the primer recognition protein complex that interacts with DNA polymerase alpha. J. Biol. Chem. 266, 5169-5176.
56. Johnson, P.M., Trenchev, P., Faulk, W.P., 1973. Immunological studies of human placentae. Binding of complexed immunoglobulin by stromal endothelial cells. Clin. Exp. Immunol. 22, 133-138.
57. Johnson, P.M., Molloy, C.M., 1983. Localization in human term placental bed and amniochorion of cells bearing trophoblast antigens identified by monoclonal antibodies. Am. J. Reprod. Immunol. 4, 33-37.
58. Junghans, R.P., Anderson, C.L., 1996. The protection receptor for IgG catabolism is the β2-microglobulin-containing neonatal intestinal transport receptor. Proc. Natl. Acad. Sci. USA 93, 5512-5516.
59. Kameda, T., Koyama, M., Matsuzaki, N., Taniguchi, T., Saji, F., Tanizawa, O., 1991. Localization of three subtypes of Fcγ receptors in human placenta by immunohistochemical analysis. Placenta 12, 15-26.
60. Karas, S.P., Rosse, W.F., Kurlander, R.J., 1982. Characterization of the IgG-Fc receptor on human platelets. Blood 60, 1277-1282.
61. Kaufmann, P., Burton, G., 1994. Anatomy and genesis of the placenta. In: Knobil, E., Neill, J.D. (Eds.), The Physiology of Reproduction. Raven, New York, pp. 441-484.
62. King, B.F., 1982. Absorption of peroxidase-conjugated immunoglobulin G by human placenta: an in vitro study. Placenta 3, 395-406.
63. Koyama, M., Saji, F., Kameda, T., Kimura, T., Nishikiori, N., Kikuchi, T., Tanizawa, O., 1991. Differential mRNA expression of three distinct classes of Fc gamma receptor at the feto-maternal interface. J. Reprod. Immunol. 20, 103-113.
64. Kristoffersen, E.K., Ulvestad, E., Vedeler, C.A., Matre, R., 1990. Fcγ receptor heterogeneity in the human placenta. Scand. J. Immunol. 32, 561-564.
65. Kristoffersen, E.K., Ulvestad, E., Bjørge, L., Aarli, Å., Matre, R., 1994. Fc gamma receptor activity of human placental annexin II. Scand. J. Immunol. 40, 237-242.
66. Kristoffersen, E.K., Matre, R., 1996a. Co-localization of β2-microglobulin and IgG in human placental syncytiotrophoblasts. Eur. J. Immunol. 26, 505-507.
67. Kristoffersen, E.K., Matre, R., 1996b. Co-localization of the neonatal Fc gamma receptor and IgG in human placental term syncytiotrophoblasts. Eur. J. Immunol. 26, 1668-1671.
68. Kristoffersen, E.K., Matre, R., 1996c. Surface annexin II on placental membranes of the fetomaternal interface. Am. J. Reprod. Immunol. 36. 141-149.
69. Kurlander, R.J., Batker, J., 1982. The binding of human immunoglobulin G1 monomer and small, covalently cross-linked polymers of immunoglobulin G1 to human peripheral blood monocytes and polymorphonuclear leukocytes. J. Clin. Invest. 69, 1-8.
70. Lang, I., Hartmann, M., Blaschitz, A., Dohr, G., Skofitsch, G., Desoye, G., 1993. Immunohistochemical evidence for the heterogeneity of maternal and fetal vascular endothelial cells in human full-term placenta. Cell Tissue Res. 274, 211-218.
71. Leach, L., Eaton, B.M., Firth, J.A., Contractor, S.F., 1989. Immunogold localisation of endogenous immunoglobulin-G in ultrathin frozen sections of the human placenta. Cell Tissue Res. 257, 603-607.
72. Leach, L., Eaton, B.M., Firth, J.A., Contractor, S.F., 1990. Uptake and intracellular routing of peroxidase-conjugated immunoglobulin-G by the perfused human placenta. Cell Tissue Res. 261, 383-388.
73. Leach, L., Eaton, B.M., Firth, J.A., Contractor, S.F., 1991. Immunocytochemical and labelled tracer approaches to uptake and intracellular routing of immunoglobulin-G (IgG) in the human placenta. Histochem. J. 23, 444-449.
74. Leach, J.L., Sedmak, D.D., Osborne, J.M., Rahill, B., Lairmore, M.D., Andersen, C.L., 1996. Isolation from human placenta of the IgG transporter. FcRn, and localization to the syncytiotrophoblast: implications for maternal-fetal antibody transport. J. Immunol. 157, 3317-3322.
75. Lee, S.I., Heiner, D.C., Wara, D., 1986. Development of serum IgG subclass levels in children. In: Dukor, P., Kallós, Z., Trnka, Z., Waksman, B.H. (Eds.), Basic and Clinical Aspects of IgG Subclasses. Karger, Basel, pp. 108-121.
76. Lin, C.-T., 1980. Immunoelectron microscopic localization of immunoglobulin G in human placenta. J. Histochem. Cytochem. 28, 339-346.
77. Lubega, J., 1990. A kinetic study of human IgG binding to placental Fc gamma-receptor. Mol. Immunol. 27, 45-55.
78. Mackenzie, N.M., Morris, B., Morris, R., 1983. Protein binding to brush borders of enterocytes from the jejunum of the neonatal rat. Biochim. Biophys. Acta 755, 204-209.
79. Makiya, R., Stigbrand, T., 1992a. Placental alkaline phosphatase as the placental IgG receptor. Clin. Chem. 38, 2543-2545.
80. Makiya, R., Stigbrand, T., 1992b. Placental alkaline phosphatase has a binding site for the human immunoglobulin-G Fc portion. Eur. J. Biochem. 205, 341-345.
81. Makiya, R., Stigbrand, T., 1992c. Placental alkaline phosphatase is related to human IgG internalization in HEp2 cells. Biochem. Biophys. Res. Comm. 182, 624-630.
82. Malek, A., Sager, R., Schneider, H., 1994. Maternal-fetal transport of immunoglobulin G and its subclasses during the third trimester of human pregnancy. Am. J. Reprod. Immunol. 32, 8-14.
83. Matre, R., Tender, O., Endresen, C., 1975. Fc receptors in human placenta. Scand. J. Immunol. 4, 471-475.
84. Matre, R., Johnson, P.M., 1977. Multiple Fc receptors in the human placenta. Acta Pathol. Microbiol. Scand. Sect. C 85, 314-316.
85. Matre, R., Kleppe, G., Tender, O., 1981. Isolation and characterization of Fcγ receptors from human placenta. Acta Pathol. Microbiol. Scand. Sect. C 89, 209-231.
86. Matre, R., Haaheim, L.R., Tonder, O., 1984. A monoclonal antibody inhibiting human placental Fc gamma-receptor activity. Int. Arch. Allergy. Appl. Immunol. 75, 227-229.
87. Matre, R., Kristoffersen, E.K., Ulvestad, E., Vedeler, C.A., 1989. Purification of a functional 40 kDa human placental Fc gamma-receptor using a monoclonal antibody. APMIS 97, 733-737.
88. McCormick, J.N., Faulk, W.P., Fox, H., Fudenberg, H.H., 1971. Immunohistological and elution studies of the human placenta. J. Exp. Med. 133, 1-18.
89. McNabb, T., Koh, T.Y., Dorrington, K.J., Painter, R.H., 1976. Structure and function of imunoglobulin domains. V. Binding of immunoglobulin G and fragments to placental membrane preparations. J. Immunol. 117, 882-888.
90. Mellbye, O.J., Natvig, J.B., 1973. Presence and origin of human IgG subclass proteins in newborns. Vox Sang. 24, 206-215.
91. Mikulska, J., Lisowski, J., 1987. Polyclonal antibodies directed against human placental Fc gamma receptor. Characterization of the antibodies and their interaction with the receptor. Arch. Immunol. Ther. Exp. (Warsz.) 35, 819-830.
92. Mongan, L.C., Ockleford, C.D., 1996. Behavior of two of IgG subclasses in transport across the human placenta. J. Anat. 188, 43-51.
93. Morell, A., Skvaril, F., Hitzig, W.H., Barandum, S., 1972. IgG subclasses: Development of the serum concentrations in 'normal' infants and children. J. Pediatr. 80, 960-964.
94. Morell, A., Skvaril, F., van Loghem, E., Kleemola, M., 1971. Human IgG subclasses in maternal and fetal serum. Vox Sang. 21, 481-492.
95. Morris, I.G., 1963. Interference with uptake of guinea pig agglutinins in mice due to fractions of papain hydrolysed rabbit γ-globulin. Proc. R. Soc. Lond. B 157, 160-169.
96. Moskalewski, S., Ptak, W., Czarnik, K., 1975. Demonstration of cells with IgG receptor in human placenta. Biol. Neonate 26, 268-273.
97. Niezgodka, M., Mikulska, J., Ugorski, M., Boratynski, J., Lisowski, J., 1981. Human placental membrane receptor for IgG-I. Studies on properties and solubilization of the receptor. Mol, Immunol. 18, 163-172.
98. Nishikiori, N., Koyama, M., Kikuchi, T., Kimura, T., Ozaki, M., Harada, S., Saji, F., Tanizawa, O., 1993. Membrane-spanning Fc gamma receptor III isoform expressed on human placental trophoblasts. Am. J. Reprod. Immunol. 29, 17-25.
99. Paraskevas, F., Lee, S.-T., Orr, K.B., Israels, L.G., 1972. A receptor for Fc on mouse B lymphocytes. J. Immunol. 108, 1319-1327.
100. Parren, P.W., Warmerdam, P.A., Boeije, L.C., Arts, J., Westerdaal, N.A., Vlug, A., Capel, P.J.A., Aarden, L.A., van de Winkel, J.G.J., 1992. On the interaction of IgG subclasses with the low affinity Fc gamma RIIa (CD32) on human monocytes, neutrophils, and platelets. Analysis of a functional polymorphism to human IgG2. J. Clin. Invest. 90, 1537-1546.
101. Peppard, J.V., Jackson, L.E., Hall, J.G., Robertson, D., 1984. The transfer of immune complexes from the lumen of the small intestine to the bloodstream in suckling rats. Immunology 53, 385-393.
102. Peppard, J.V., Jackson, L.E., MacKenzie, N.M., 1985. Comparison of in vitro binding to enterocyte brush borders of rat IgG subclasses and their transmission in vivo in the rat. Immunology 56, 51-55.
103. Perussia, B., Ravetch, J.V., 1991. FcγRIII (CD16) on human macrophages is a functional product of the FcγRIII-2 gene. Eur. J. Immunol. 21, 425-429.
104. Pitcher-Wilmott, R.W., Hindocha, P., Wood, B.S., 1980. The placental transfer of IgG subclasses in human pregnancy. Clin. Exp. Immunol. 41, 303-308.
105. Raynal, P., Pollard, H.B., 1994. Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium-and phospholipid-binding proteins. Biochim. Biophys. Acta 1197, 63-93.
106. Roberts, D.M., Guenthert, M., Rodewald, R., 1990. Isolation and Characterization of the Fc receptor from the fetal yolk sac of the rat. J. Cell Biol. 111, 1867-1876.
107. Rodewald, R., 1976. pH-dependent binding of immunoglobulins to intestinal cells of the neonatal rat. J. Cell Biol. 71, 666-670.
108. Rodewald, R., Kraehenbuhl, J.-P., 1984. Receptor-mediated transport of IgG. J. Cell Biol. 99, 159s-164s.
109. Rodewald, R., Lewis, D.M., Kraehenbuhl, J.-P., 1983. Immunoglobulin G receptors of intestinal brush borders from neonatal rats. Ciba Found. Symp. 95, 287-299.
110. Rote, N.S., 1982. Pathophysiology of Rh isoimmunization. Clin. Obstet. Gynecol. 25, 243-253.
111. Sakiyama, T., Robinson, J.C., Chou, J.Y., 1979. Characterization of alkaline phosphatases from human first trimester placentas. J. Biol. Chem. 254, 935-938.
112. Schur, P.H., Alpert, E., Alper, C., 1973. Gamma G subgroups in human fetal, cord, and maternal sera. Clin. Immunol. Immunopathol. 2, 62-66.
113. Sedmak, D.D., Davis, D.H., Singh, U., van de Winkel, J.G.J., Anderson, C.L., 1991. Expression of IgG Fc receptor antigens in placenta and on endothelial cells in humans. An immunohistochemical study. Am. J. Pathol. 138, 175-181.
114. Silver, R.M., Branch, D.W., 1992. Autoimmune disease in pregnancy. Bailliere's Clin. Obstet. Gynaecol. 6, 565-600.
115. Simister, N.E., 1990. Transport of monomeric antibodies across epithelia. In: Metzger, H. (Ed.), Fc Receptors and the Action of Antibodies. American Society for Microbiology, Washington, DC, pp. 57-73.
116. Simister, N.E., 1997. Multiple roles of FcRn. In: van de Winkel, J.G.J., Hogarth, P.M. (Eds.), Immunoglobulin Receptors and their Physiological and Pathological Roles in Immunity. Kluwer, Dordrecht (in press).
117. Simister, N.E., Rees, A.R., 1985. Isolation and characterization of an Fc receptor from neonatal rat small intestine. Eur. J. Immunol. 15, 733-738.
118. Simister, N.E., Mostov, K.E., 1989. An Fc receptor structurally related to MHC class I antigens. Nature 337, 184-187.
119. Simister, N.E., Story, C.M., Chen, H.-L., Hunt, J.S., 1996. An IgG transporting Fc receptor expressed in the syncytiotrophoblast of human placenta. Eur. J. Immunol. 26, 1527-1531.
120. Simpson, R.A., Mayhew, T.M., Barnes, P.R., 1992. From 13 weeks to term, the trophoblast of human placenta grows by the continuous recruitment of new proliferative units: a study of nuclear number using the disector. Placenta 13, 501-512.
121. Sipe, D.M., Murphy, R.F., 1987. High-resolution kinetics of transferrin acidification in BALB/c 3T3 cells: exposure to pH 6 followed by temperature-sensitive alkalinization during recycling. Proc. Natl. Acad. Sci. USA 84, 7119-7123.
122. Sorensen, R.U., Tomford, J.W., Gyves, M.T., Judge, N.E., Polmar, S.H., 1984. Use of intravenous immune globulin in pregnant women with common variable hypogammaglobulinemia. Am. J. Med. 76, 73-77.
123. Story, C.M., Mikulska, J.E., Simister, N.E., 1994. A major histocompatibility complex class I-like Fc receptor cloned from human placenta: possible role in transfer of immunoglobulin G from mother to fetus. J. Exp. Med. 180, 2377-2381.
124. Stuart, S.G., Simister, N.E., Clarkson, S.B., Kacinski, B.M., Shapiro, M., Mellman, I., 1989. Human IgG Fc receptor (hFcRII; CD32) exists as multiple isoforms in macrophages, lymphocytes and IgG-transporting placental epithelium. EMBO. J. 8, 3657-3666.
125. Swarup, G., Cohen, S., Garbers, D.L., 1981, Selective dephosphorylation of proteins containing phosphotyrosine by alkaline phosphatases. J. Biol. Chem. 256, 8197-8201.
126. Tamm, A., Kister, A., Nolte, K.U., Gessner, J.E., Schmidt, R.E., 1996. The IgG binding site of human FcγRIIIB receptor involves CC' and FG loops of the membrane-proximal domain. J. Biol. Chem. 271, 3659-3666.
127. van de Winkel, J.G.J., Capel, P.J.A., 1993. Human IgG Fc receptor heterogeneity: molecular aspects and clinical implications. Immunol. Today 14, 215-221.
128. van den Herik-Oudijk, I.E., Westerdaal, N.A.C., Henriquez, N.V., Capel, P.J.A., van de Winkel, J.G.J., 1994. Functional analysis of human Fc gamma RII (CD32) isoforms expressed in B lymphocytes. J. Immunol. 152, 574-585.
129. van den Herik-Oudijk, I.E., Verbeek, S.J., Capel, P.J.A., van de Winkel, J.G.J., 1996. FcγR on mononuclear cells. In: van de Winkel, J.G.J., Capel, P.J.A. (Eds.), Human IgG Fc receptors. CRC Press, Austin, pp. 57-78.
130. van der Meulen, J.A., McNabb, T.C., Haeffner-Cavaillon, N., Klein, M., Dorrington, K.J., 1980. The Fc gamma receptor on human placental plasma membrane: Studies on the binding of homologous and heterologous immunoglobulin G. J. Immunol. 124, 500-507.
131. van Overmeire, B., Bleyaert, S., van Reempts, P.J., van Acker, K.J., 1993. The use of intravenously administered immunoglobulins in the prevention of severe infection in very low birthweight neonates. Biol. Neonate 64, 110-115.
132. Vance, B.A., Huizinga, T.W.J., Wardwell, K., Guyre, P.M., 1993. Binding of monomeric human IgG defines an expression polymorphism of Fc gamma RIII on large granular lymphocyte/natural killer cells. J. Immunol. 151, 6429-6439.
133. Virella, G., Amélia Silveira Nunes, M., Tamagnini, G., 1972. Placental transfer of human IgG subclasses. Clin. Exp. Immunol. 10, 475-478.
134. Wainwright, S.D., Holmes, C.H., 1993. Distribution of Fcγ receptors on trophoblast during human placental development: an immunohistochemical and immunoblotting study. Immunology 80, 343-351.
135. Wallace, K.H., Rees, A.R., 1980. Studies on the immunoglobulin-G Fc-fragment receptor from neonatal rat small intestine. Biochem. J. 188, 9-16.
136. Wang, A.C., Faulk, W.P., Stuckey, M.A., Fudenberg, H.H., 1970. Chemical differences of adult, fetal and hypogammaglobulinemic IgG immunoglobulins. Immunochemistry 7, 703-708.
137. Warmerdam, P.A.M., van de Winkel, J.G.J., Gosselin, E.J., Capel, P.J.A., 1990. Molecular basis for a polymorphism of human Fc gamma receptor II (CD32). J. Exp. Med. 172, 19-25.
138. Warmerdam, P.A.M., van den Herik-Oudijk, I.E., Parren, P.W.H.I., Westerdaal, N.A.C., van de Winkel, J.G.J., Capel, P.J.A., 1993. Interaction of a human Fc gamma RIIb1 (CD32) isoform with murine and human IgG subclasses. Int. Immunol. 5, 239-247.
139. Watabe, H., Gitlin, J.I., Gitlin, D., 1980. Further characterization of IgG receptors from human placenta. J. Biochem. (Tokyo) 87, 393-397.
140. Wood, G., Reynard, J., Krishnan, E., Racela, L., 1978. Immunobiology of the human placenta. II. Localization of macrophages, in vivo bound IgG and C3. Cell. Immunol. 35, 205-216.
141. Wood, G.W., King, C.R., 1982. Trapping antigen-antibody complexes within the human placenta. Cell. Immunol. 69, 347-362.
142. Wright, J.F., Kurosky, A., Wasi, S., 1994. An endothelial cell-surface form of annexin II binds human cytomegalovirus. Biochem. Biophys. Res. Commun. 198, 983-989.
143. Zokas, L., Glenney, J.R.J., 1987. The calpactin light chain is tightly linked to the cytoskeletal form of calpactin I: studies using monoclonal antibodies to calpactin subunits. J. Cell Biol. 105, 2111-2121.