Summary
Hofbauer cells are a major cell type of the human placental villous core and they are particularly numerous at the beginning of pregnancy. In the present study we describe a method suitable to obtain HC suspensions in a highly purified form. These suspensions have been analyzed for surface markers using a battery of monoclonal antibodies. Of all the surface markers used, Hofbauer cells were only positive for 4F2, LeuM2 and LeuM3 monoclonals which mainly detect cells of the monocyte-macrophage lineage. Hofbauer cells were consistently negative for HLA-DR antigens, C3bR and T- or B-cell markers. Hofbauer cells appeared capable of phagocytosing latex beads, adhering to and spreading over plastic surface and secreting lysozyme. In contrast, they failed to originate an efficient respiratory burst in response to appropriate stimulation. Hofbauer cells were positive for ANAE with a perinuclear localization of the enzyme activity, but consistently negative for peroxidase. These observations suggest that they share a number of features with cells of the monocyte-macrophage lineage and yet have some distinctive properties.
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References
Abo T, Balch CM (1981) A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1). J Immunol 127:1024–1029
Babior BM (1978) Oxygen-dependent microbial killing by phagocytes. N Engl J Med 298:659–668
Beller DI, Ho K (1982) Regulation of macrophage population. V. Evaluation of the control of macrophage Ia expression in vitro. J Immunol 129:971–976
Boyd JD, Hamilton WJ (1970) Stroma of villi. In: Boyd JD, Hamilton WJ (eds) The human placenta. Heffer and Sons, Cambridge, p 232
Bulmer JN, Johnson PM (1984) Macrophage populations in the human placenta and amniochorion. Clin Exp Immunol 57:393–403
Bulmer JN, Morrison L, Smith JC (1988) Expression of class II MHC gene products by macrophages in human uteroplacental tissue. Immunology 63:707–714
Castellucci M, Zaccheo D, Pescetto G (1980) A three-dimensional study of the normal human placental villous core. I. The Hofbauer cells. Cell Tissue Res 210:235–247
Corte G, Damiani G, Fabbi M, Bargellesi A (1981) Analysis of HLA-DR polymorphism by two dimensional peptide mapping. Proc Natl Acad Sci USA 78:534–538
Daems WT, Koerten HK, Soranzo MR (1976) Differences between monocyte-derived and tissue macrophages. In: Reichard SM, Escobar MR, Friedman M (eds) The Reticuloendothelial system in health and diseases: function and characteristics. Plenum Press, New York, p 27
Dimitriu-Bona A, Burmester GR, Waters SJ, Winchester RJ (1983) Human mononuclear phagocyte differentiation antigens. I. Patterns of antigenic expression of the surface of human monocytes and macrophages defined by monoclonal antibodies. J Immunol 130:145–152
Edwards JA, Jones DB, Evans PR, Smith JL (1985) Differential expression of HLA class II antigens on human fetal and adult lymphocytes and macrophages. Immunol 55:489–500
Enders AC, King BF (1970) The cytology of Hofbauer cell. Anat Rec 167:231–252
Ferrarini M, Bargellesi A, Corte G, Viale G, Pernis B (1975) Comparative study of membrane and intracytoplasmic Ig classes in human lymphoid cells. Am NY Acad Sci 254:243–253
Fox H (1967) The incidence and significance of Hofbauer cells in mature human placenta. J Pathol Bact 93:710–717
Fox H, Kharkongor NF (1969) Enzyme histochemistry of the Hofbauer cells of the human placenta. J Obstet Gynaecol Br Commonw 76:918–921
Frauli M, Ludwig H (1987a) Identification of human chorionic gonadotropin (HCG) secreting cells and other cell types using antibody to HCG and a new monoclonal antibody (mABlu-5) in cultures of human placental villi. Arch Gynecol Obstet 241:97–110
Frauli M, Ludwig H (1987b) Demonstration of the ability of Hofbauer cells to phagocytose exogenous antibodies. Eur J Obstet Gynecol Reprod Biol 26:135–144
Graham RC, Karnovsky ML (1966) The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem 14:291–302
Haynes BF, Hemler ME, Mann DL, Eisenbarth GS, Shelhamer RJ, Mostowsky HS, Thomas CA, Strominger JL, Fauci AS (1981) Characterization of a monoclonal antibody (4F2) that binds to human monocytes and to a subset of activated lymphocytes. J Immunol 126:1409–1414
Johnston RB, Godzik CA, Cohn ZA (1978) Increased superoxide anion production by immunologically activated and chemically elicited macrophages. J Exp Med 148:115–127
Kawata M, Parnes JR, Herzenberg LA (1984) Transcriptional control of HLA-ABC antigen in human placental cytotrophoblast isolated using trophoblast and HLA specific monoclonal antibodies and the fluorescence activated cell sorter. J Exp Med 160:633–651
Kurnick JT, Ostberg L, Stegagno M, Kimura AK, Orn A, Sjoberg O (1979) A rapid method for the separation of functional lymphoid cell population of human and animal origin on PVP-Silica (Percoll) density gradients. Scand J Immunol 10:563–573
Lachman PI, Hobart MJ, Aston PN (1978) Complement technology. In: Weir DM (ed) Handbook of experimental immunology, Chapt. 5.1–5.17. Blackwell, Oxford
Loke YM, Eremin O, Ashby J, Day S (1982) Characteization of the phagocytic cells isolated from the human placenta. J Reticuloendothel Soc 31:317–324
Lu CY, Beller DI, Unanue ER (1980) During ontogeny, Ia-bearing accessory cells are found early in the thymus but late in the spleen. Proc Natl Acad Sci USA 77:1597–1601
Lu CY, Changelian PS, Unanue ER (1984) Alpha-fetoprotein inhibits macrophage expression of Ia antigens. J Immunol 132:1722–1727
Martinoli C, Castellucci M, Zaccheo D, Kaufmann P (1984) Scanning elctron microscopy of stromal cells of human placental villi throughout pregnancy. Cell Tissue Res 235:647–655
Moretta L, Ferrarini M, Cooper MD (1978) Characterization of human T-cell subpopulations as defined by specific receptors for immunoglobulins. Contemp Top Immunobiol 8:19–53
Moretta L, Mingari MC, Romanzi CA (1978) Loss of Fc receptors for IgG from human T lymphocytes exposed to IgG immune complexes. Nature 272:618–620
Moskalewski S, Ptak W, Czarnik Z (1975) Demonstration of cells with IgG receptors in human placenta. Biol Neonate 26:268–273
Mueller J, Brun Del Re G, Buerk H, Keller HV, Hess HW, Cottier H (1975) Nonspecific acid esterase activity: a criterion for differentiation of T and B lymphocytes in mouse lymph nodes. Eur J Immunol 5:270–273
Nocera A, Cadoni A, Zicca A, Di Primio R, Leprini A, Ferrarini M (1982) Receptors for the third complement component on a proportion of large granular lymphocytes from human peripheral blood. Scand J Immunol 15:573–579
Oliveira LHS, Leandro SV, Fonseca MEF, Dias LMS (1986) A new technique for the isolation of placental phagocyte cells and a description of their macrophage properties after in vitro culture. Braz J Med Biol Res 19:249–255
Ossermann EF, Lawlor DP (1966) Serum and urinary lysozyme (muramidase) in monocytic and monomyelocytic leukemia. J Exp Med 124:921–952
Raff HV, Picken LJ, Stobo JD (1980) Macrophage heterogeneity in man. A subpopulation of HLA-DR bearing macrophages required for antigen-induced T-cell activation also contain stimulators for autologous-reactive T-cells. J Exp Med 152:581–593
Reinherz EL, Kung PC, Piesando JH, Ritz J, Goldstein G, Schlossmann SF (1979) Ia determinants on human T-cell subset defined by monoclonal antibody. Activation stimuli required for expression. J Exp Med 150:1472–1482
Reinherz EL, Schlossmann SF (1980) The differentiation and function of human T lymphocytes. Cell 19:821–827
Rocklin RE, Kitzmiller JL, Kaye MD (1979) Immunobiology of the maternal-fetal relationship. Ann Rev Med 30:375–404
Scher MG, Beller DI, Unanue ER (1980) Demonstration of a soluble mediator that induces exudates rich in Ia-positive macrophages. J Exp Med 152:1684–1698
Scher MG, Unanue ER, Beller DU (1982) Regulation of macrophage populations. III. The immunologic induction of exudates rich in Ia-positive macrophages is radiosensitive process. J Immunol 128:447–450
Shaw DR, Griffin FM (1981) Antibody-dependent and antibody-independent phagocytosis. In: Adams DO, Edelson PJ, Koren J (eds) Methods for studying mononuclear phagocytes, Chapt 54. Academic Press, New York, p 511
Snyder DS, Beller DI, Unanue ER (1982) Prostaglandins modulate macrophage Ia expression. Nature 299:163–165
Steeg DS, Moore RN, Johnson HM, Oppenheim JJ (1982) Regulation of immune macrophage Ia antigen expression by a lymphokine with immune interferon activity. J Exp Med 156:1780–1793
Steeg P, Moore R, Oppenheim JJ (1980) Regulation of macrophage Ia expression by products of activated cells. J Immunol 152:1734–1744
Sutton L, Mason DY, Redman CWG (1982) HLA-DR positive cells in the human placenta. Immunol 49:103–112
Sutton L, Gadd M, Mason DY, Redman CWG (1986) Cells bearing class II MHC antigens in the human placenta and amniochorion. Immunology 58:23–29
Unanue ER, Beller DI, Lu CY, Allen PM (1984) Antigen presentation: comments on its regulation and mechanism. J Immunol 132:1–5
Uren S, Boyle W (1985) Isolation of macrophages from human placenta. J Immunol Meth 78:25–34
Wilson CB, Haas JE, Weaver WH (1983) Isolation, purification and characteristics of mononuclear phagocytes from human placentas. J Immunol Meth 56:305–317
Wood G (1980) Mononuclear phagocytes in the human placenta. Placenta 1:113–123
Wood GW, King Jr CR (1982) Trapping antigen-antibody complexes within the human placenta. Cell Immunol 69:347–362
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
Wynn RM (1967) Derivation and ultrastructure of the so-called Hofbauer cells. Am J Obstet Gynaecol 97:235–248
Zarling JM, Clouse KA, Biddinson WE, Kung PC (1981) Phenotype of human natural killer cell populations detected with monoclonal antibodies. J Immunol 127:2575–2580
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Zaccheo, D., Pistoia, V., Castellucci, M. et al. Isolation and characterization of Hofbauer cells from human placental villi. Arch Gynecol Obstet 246, 189–200 (1989). https://doi.org/10.1007/BF00934518
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DOI: https://doi.org/10.1007/BF00934518