Skip to main content
Log in

Isolation and characterization of Hofbauer cells from human placental villi

  • Originals
  • Published:
Archives of Gynecology and Obstetrics Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. 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

    PubMed  Google Scholar 

  2. Babior BM (1978) Oxygen-dependent microbial killing by phagocytes. N Engl J Med 298:659–668

    PubMed  Google Scholar 

  3. 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

    PubMed  Google Scholar 

  4. Boyd JD, Hamilton WJ (1970) Stroma of villi. In: Boyd JD, Hamilton WJ (eds) The human placenta. Heffer and Sons, Cambridge, p 232

    Google Scholar 

  5. Bulmer JN, Johnson PM (1984) Macrophage populations in the human placenta and amniochorion. Clin Exp Immunol 57:393–403

    PubMed  Google Scholar 

  6. Bulmer JN, Morrison L, Smith JC (1988) Expression of class II MHC gene products by macrophages in human uteroplacental tissue. Immunology 63:707–714

    PubMed  Google Scholar 

  7. 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

    PubMed  Google Scholar 

  8. 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

    PubMed  Google Scholar 

  9. 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

    Google Scholar 

  10. 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

    PubMed  Google Scholar 

  11. 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

    Google Scholar 

  12. Enders AC, King BF (1970) The cytology of Hofbauer cell. Anat Rec 167:231–252

    PubMed  Google Scholar 

  13. 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

    Google Scholar 

  14. Fox H (1967) The incidence and significance of Hofbauer cells in mature human placenta. J Pathol Bact 93:710–717

    Google Scholar 

  15. Fox H, Kharkongor NF (1969) Enzyme histochemistry of the Hofbauer cells of the human placenta. J Obstet Gynaecol Br Commonw 76:918–921

    PubMed  Google Scholar 

  16. 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

    PubMed  Google Scholar 

  17. 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

    PubMed  Google Scholar 

  18. 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

    PubMed  Google Scholar 

  19. 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

    PubMed  Google Scholar 

  20. Johnston RB, Godzik CA, Cohn ZA (1978) Increased superoxide anion production by immunologically activated and chemically elicited macrophages. J Exp Med 148:115–127

    PubMed  Google Scholar 

  21. 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

    PubMed  Google Scholar 

  22. 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

    PubMed  Google Scholar 

  23. Lachman PI, Hobart MJ, Aston PN (1978) Complement technology. In: Weir DM (ed) Handbook of experimental immunology, Chapt. 5.1–5.17. Blackwell, Oxford

    Google Scholar 

  24. 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

    PubMed  Google Scholar 

  25. 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

    PubMed  Google Scholar 

  26. Lu CY, Changelian PS, Unanue ER (1984) Alpha-fetoprotein inhibits macrophage expression of Ia antigens. J Immunol 132:1722–1727

    PubMed  Google Scholar 

  27. 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

    PubMed  Google Scholar 

  28. 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

    PubMed  Google Scholar 

  29. 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

    PubMed  Google Scholar 

  30. Moskalewski S, Ptak W, Czarnik Z (1975) Demonstration of cells with IgG receptors in human placenta. Biol Neonate 26:268–273

    PubMed  Google Scholar 

  31. 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

    PubMed  Google Scholar 

  32. 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

    PubMed  Google Scholar 

  33. 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

    PubMed  Google Scholar 

  34. Ossermann EF, Lawlor DP (1966) Serum and urinary lysozyme (muramidase) in monocytic and monomyelocytic leukemia. J Exp Med 124:921–952

    PubMed  Google Scholar 

  35. 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

    PubMed  Google Scholar 

  36. 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

    PubMed  Google Scholar 

  37. Reinherz EL, Schlossmann SF (1980) The differentiation and function of human T lymphocytes. Cell 19:821–827

    PubMed  Google Scholar 

  38. Rocklin RE, Kitzmiller JL, Kaye MD (1979) Immunobiology of the maternal-fetal relationship. Ann Rev Med 30:375–404

    PubMed  Google Scholar 

  39. 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

    PubMed  Google Scholar 

  40. 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

    PubMed  Google Scholar 

  41. 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

    Google Scholar 

  42. Snyder DS, Beller DI, Unanue ER (1982) Prostaglandins modulate macrophage Ia expression. Nature 299:163–165

    PubMed  Google Scholar 

  43. 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

    PubMed  Google Scholar 

  44. Steeg P, Moore R, Oppenheim JJ (1980) Regulation of macrophage Ia expression by products of activated cells. J Immunol 152:1734–1744

    Google Scholar 

  45. Sutton L, Mason DY, Redman CWG (1982) HLA-DR positive cells in the human placenta. Immunol 49:103–112

    Google Scholar 

  46. 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

    PubMed  Google Scholar 

  47. Unanue ER, Beller DI, Lu CY, Allen PM (1984) Antigen presentation: comments on its regulation and mechanism. J Immunol 132:1–5

    PubMed  Google Scholar 

  48. Uren S, Boyle W (1985) Isolation of macrophages from human placenta. J Immunol Meth 78:25–34

    Google Scholar 

  49. Wilson CB, Haas JE, Weaver WH (1983) Isolation, purification and characteristics of mononuclear phagocytes from human placentas. J Immunol Meth 56:305–317

    Google Scholar 

  50. Wood G (1980) Mononuclear phagocytes in the human placenta. Placenta 1:113–123

    PubMed  Google Scholar 

  51. Wood GW, King Jr CR (1982) Trapping antigen-antibody complexes within the human placenta. Cell Immunol 69:347–362

    PubMed  Google Scholar 

  52. 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

    PubMed  Google Scholar 

  53. Wynn RM (1967) Derivation and ultrastructure of the so-called Hofbauer cells. Am J Obstet Gynaecol 97:235–248

    Google Scholar 

  54. 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

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00934518

Key words

Navigation