Skip to main content
PMC home page
The American Journal of Pathology logoLink to The American Journal of Pathology
. 1983 Apr;111(1):112–124.

Dendritic cell and macrophage staining by monoclonal antibodies in tissue sections and epidermal sheets.

T J Flotte, T A Springer, G J Thorbecke
PMCID: PMC1916197  PMID: 6340516

Abstract

Mouse tissue sections were stained by monoclonal antibodies to macrophage antigens (Mac-1 (M1/70), Mac-2 (M3/38), Mac-3 (M3/84) with the use of immunoperoxidase. Mac-1 was located diffusely in the cytoplasm of round cells in a high percentage of alveolar macrophages, resident peritoneal and bone marrow cells, in splenic red pulp, and in rare perivascular cells in the thymus. Mac-1 was absent in epithelial cells and Langerhans cells. Mac-2 was strongly positive in many dendritic cells in the thymic medulla, more than the cortex, in paracortex and medulla of lymph nodes, sparing the follicles, and in the marginal zone of spleen. There were a few positive cells in germinal centers. Mac-2 was located in a low percentage of bone marrow and a high percentage of resident peritoneal cells. When positive in sections Mac-3 always showed granular cytoplasmic staining. Bone marrow showed a high percentage of cytoplasmic staining (greater than 50%), as compared with low surface staining (less than 1%). It was found in hematopoietic cells, and in all endothelium, including postcapillary venules and lining of sinuses. It was probable that the resulting dendritic staining pattern for Mac-3 in paracortex of lymph node, white and red pulp, thymic cortex, and medulla included dendritic cells other than endothelial cells. Alveolar macrophages and Kupffer cells were positive for Mac-2 and Mac-3. Mac-3 also stained bile canaliculi. Clearly different staining patterns were found in epithelial cells for Mac-2 and Mac-3 in kidney tubules, intestinal mucosal lining, bronchi, choroid plexus, and epidermis.

Full text

PDF
112

Images in this article

116Figure 1
on p.116
117Figure 2
on p.117
118Figure 3
on p.118
119Figure 4
on p.119
121Figure 5
on p.121

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barclay A. N. Different reticular elements in rat lymphoid tissue identified by localization of Ia, Thy-1 and MRC OX 2 antigens. Immunology. 1981 Dec;44(4):727–736. [PMC free article] [PubMed] [Google Scholar]
  2. Barclay A. N., Mayrhofer G. Bone marrow origin of Ia-positive cells in the medulla rat thymus. J Exp Med. 1981 Jun 1;153(6):1666–1671. doi: 10.1084/jem.153.6.1666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berken A., Benacerraf B. Properties of antibodies cytophilic for macrophages. J Exp Med. 1966 Jan 1;123(1):119–144. doi: 10.1084/jem.123.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bhan A. K., Reinherz E. L., Poppema S., McCluskey R. T., Schlossman S. F. Location of T cell and major histocompatibility complex antigens in the human thymus. J Exp Med. 1980 Oct 1;152(4):771–782. doi: 10.1084/jem.152.4.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bhattacharya A., Dorf M. E., Springer T. A. A shared alloantigenic determinant on Ia antigens encoded by the I-A and I-E subregions: evidence for I region gene duplication. J Immunol. 1981 Dec;127(6):2488–2495. [PubMed] [Google Scholar]
  6. Burke K., Gigli I. Receptors for complement of Langerhans cells. J Invest Dermatol. 1980 Jul;75(1):46–51. doi: 10.1111/1523-1747.ep12521115. [DOI] [PubMed] [Google Scholar]
  7. CLARK S. L., Jr The reticulum of lymph nodes in mice studied with the electron microscope. Am J Anat. 1962 May;110:217–257. doi: 10.1002/aja.1001100303. [DOI] [PubMed] [Google Scholar]
  8. Chen L. L., Adams J. C., Steinman R. M. Anatomy of germinal centers in mouse spleen, with special reference to "follicular dendritic cells". J Cell Biol. 1978 Apr;77(1):148–164. doi: 10.1083/jcb.77.1.148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cocchia D., Michetti F., Donato R. Immunochemical and immuno-cytochemical localization of S-100 antigen in normal human skin. Nature. 1981 Nov 5;294(5836):85–87. doi: 10.1038/294085a0. [DOI] [PubMed] [Google Scholar]
  10. Dulbecco R., Unger M., Bologna M., Battifora H., Syka P., Okada S. Cross-reactivity between Thy-1 and a component of intermediate filaments demonstrated using a monoclonal antibody. Nature. 1981 Aug 20;292(5825):772–774. doi: 10.1038/292772a0. [DOI] [PubMed] [Google Scholar]
  11. Eikelenboom P. Dendritic cells in the rat spleen follicles. A combined immuno- and enzyme histochemical study. Cell Tissue Res. 1978 Jun 26;190(1):79–87. doi: 10.1007/BF00210038. [DOI] [PubMed] [Google Scholar]
  12. Fischer H. D., Gonzalez-Noriega A., Sly W. S., Morré D. J. Phosphomannosyl-enzyme receptors in rat liver. Subcellular distribution and role in intracellular transport of lysosomal enzymes. J Biol Chem. 1980 Oct 25;255(20):9608–9615. [PubMed] [Google Scholar]
  13. Fithian E., Kung P., Goldstein G., Rubenfeld M., Fenoglio C., Edelson R. Reactivity of Langerhans cells with hybridoma antibody. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2541–2544. doi: 10.1073/pnas.78.4.2541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ho M. K., Springer T. A. Mac-1 antigen: quantitative expression in macrophage populations and tissues, and immunofluorescent localization in spleen. J Immunol. 1982 May;128(5):2281–2286. [PubMed] [Google Scholar]
  15. Ho M. K., Springer T. A. Mac-2, a novel 32,000 Mr mouse macrophage subpopulation-specific antigen defined by monoclonal antibodies. J Immunol. 1982 Mar;128(3):1221–1228. [PubMed] [Google Scholar]
  16. Holmberg L. A., Springer T. A., Ault K. A. Natural killer activity in the peritoneal exudates of mice infected with Listeria monocytogenes: characterization of the natural killer cells by using a monoclonal rat anti-murine macrophage antibody (M1/70). J Immunol. 1981 Nov;127(5):1792–1799. [PubMed] [Google Scholar]
  17. Humphrey J. H., Grennan D. Isolation and properties of spleen follicular dendritic cells. Adv Exp Med Biol. 1982;149:823–827. doi: 10.1007/978-1-4684-9066-4_113. [DOI] [PubMed] [Google Scholar]
  18. Janossy G., Thomas J. A., Bollum F. J., Granger S., Pizzolo G., Bradstock K. F., Wong L., McMichael A., Ganeshaguru K., Hoffbrand A. V. The human thymic microenvironment: an immunohistologic study. J Immunol. 1980 Jul;125(1):202–212. [PubMed] [Google Scholar]
  19. Kaiserling E., Stein H., Müller-Hermelink H. K. Interdigitating reticulum cells in the human thymus. Cell Tissue Res. 1974;155(1):47–55. doi: 10.1007/BF00220283. [DOI] [PubMed] [Google Scholar]
  20. Katz S. I., Tamaki K., Sachs D. H. Epidermal Langerhans cells are derived from cells originating in bone marrow. Nature. 1979 Nov 15;282(5736):324–326. doi: 10.1038/282324a0. [DOI] [PubMed] [Google Scholar]
  21. Klareskog L., Tjernlund U., Forsum U., Peterson P. A. Epidermal Langerhans cells express Ia antigens. Nature. 1977 Jul 21;268(5617):248–250. doi: 10.1038/268248a0. [DOI] [PubMed] [Google Scholar]
  22. Klaus G. G., Humphrey J. H., Kunkl A., Dongworth D. W. The follicular dendritic cell: its role in antigen presentation in the generation of immunological memory. Immunol Rev. 1980;53:3–28. doi: 10.1111/j.1600-065x.1980.tb01038.x. [DOI] [PubMed] [Google Scholar]
  23. Kürzinger K., Reynolds T., Germain R. N., Davignon D., Martz E., Springer T. A. A novel lymphocyte function-associated antigen (LFA-1): cellular distribution, quantitative expression, and structure. J Immunol. 1981 Aug;127(2):596–602. [PubMed] [Google Scholar]
  24. LADMAN A. J., PADYKULA H. A., STRAUSS E. W. A morphological study of fat transport in the normal human jejunum. Am J Anat. 1963 May;112:389–419. doi: 10.1002/aja.1001120307. [DOI] [PubMed] [Google Scholar]
  25. Lautenschlager I., Häyry P. Expression of the major histocompatibility complex antigens on different liver cellular components in rat and man. Scand J Immunol. 1981 Oct;14(4):421–426. doi: 10.1111/j.1365-3083.1981.tb00582.x. [DOI] [PubMed] [Google Scholar]
  26. Lay W. H., Nussenzweig V. Receptors for complement of leukocytes. J Exp Med. 1968 Nov 1;128(5):991–1009. doi: 10.1084/jem.128.5.991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mandel T. E., Phipps R. P., Abbot A., Tew J. G. The follicular dendritic cell: long term antigen retention during immunity. Immunol Rev. 1980;53:29–59. doi: 10.1111/j.1600-065x.1980.tb01039.x. [DOI] [PubMed] [Google Scholar]
  28. Nossal G. J., Abbot A., Mitchell J., Lummus Z. Antigens in immunity. XV. Ultrastructural features of antigen capture in primary and secondary lymphoid follicles. J Exp Med. 1968 Feb 1;127(2):277–290. doi: 10.1084/jem.127.2.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nussenzweig M. C., Steinman R. M. Contribution of dendritic cells to stimulation of the murine syngeneic mixed leukocyte reaction. J Exp Med. 1980 May 1;151(5):1196–1212. doi: 10.1084/jem.151.5.1196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nussenzweig M. C., Steinman R. M., Unkeless J. C., Witmer M. D., Gutchinov B., Cohn Z. A. Studies of the cell surface of mouse dendritic cells and other leukocytes. J Exp Med. 1981 Jul 1;154(1):168–187. doi: 10.1084/jem.154.1.168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nussenzweig M. C., Steinman R. M., Witmer M. D., Gutchinov B. A monoclonal antibody specific for mouse dendritic cells. Proc Natl Acad Sci U S A. 1982 Jan;79(1):161–165. doi: 10.1073/pnas.79.1.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Oláh I., Dunay C., Röhlich P., Törö I. A special type of cells in the medulla of the rat thymus. Acta Biol Acad Sci Hung. 1968;19(1):97–113. [PubMed] [Google Scholar]
  33. Poppema S., Bhan A. K., Reinherz E. L., McCluskey R. T., Schlossman S. F. Distribution of T cell subsets in human lymph nodes. J Exp Med. 1981 Jan 1;153(1):30–41. doi: 10.1084/jem.153.1.30. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Raff H. V., Picker L. J., Stobo J. D. Macrophage heterogeneity in man. A subpopulation of HLA-DR-bearing macrophages required for antigen-induced T cell activation also contains stimulators for autologous-reactive T cells. J Exp Med. 1980 Sep 1;152(3):581–593. doi: 10.1084/jem.152.3.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Richman L. K., Klingenstein R. J., Richman J. A., Strober W., Berzofsky J. A. The murine Kupffer cell. I. Characterization of the cell serving accessory function in antigen-specific T cell proliferation. J Immunol. 1979 Dec;123(6):2602–2609. [PubMed] [Google Scholar]
  36. Rouse R. V., van Ewijk W., Jones P. P., Weissman I. L. Expression of MHC antigens by mouse thymic dendritic cells. J Immunol. 1979 Jun;122(6):2508–2515. [PubMed] [Google Scholar]
  37. Rowden G., Lewis M. G., Sullivan A. K. Ia antigen expression on human epidermal Langerhans cells. Nature. 1977 Jul 21;268(5617):247–248. doi: 10.1038/268247a0. [DOI] [PubMed] [Google Scholar]
  38. Schwartz R. H., Dickler H. B., Sachs D. H., Schwartz B. D. Studies of Ia antigens on murine peritoneal macrophages. Scand J Immunol. 1976;5(6-7):731–743. doi: 10.1111/j.1365-3083.1976.tb03023.x. [DOI] [PubMed] [Google Scholar]
  39. Silberberg I., Baer R. L., Rosenthal S. A., Thorbecke G. J., Berezowsky V. Dermal and intravascular Langerhans cells at sites of passively induced allergic contact sensitivity. Cell Immunol. 1975 Aug;18(2):435–453. doi: 10.1016/0008-8749(75)90071-4. [DOI] [PubMed] [Google Scholar]
  40. Springer T. A. Monoclonal antibody analysis of complex biological systems. Combination of cell hybridization and immunoadsorbents in a novel cascade procedure and its application to the macrophage cell surface. J Biol Chem. 1981 Apr 25;256(8):3833–3839. [PubMed] [Google Scholar]
  41. Springer T., Galfré G., Secher D. S., Milstein C. Mac-1: a macrophage differentiation antigen identified by monoclonal antibody. Eur J Immunol. 1979 Apr;9(4):301–306. doi: 10.1002/eji.1830090410. [DOI] [PubMed] [Google Scholar]
  42. Steinman R. M., Cohn Z. A. Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med. 1973 May 1;137(5):1142–1162. doi: 10.1084/jem.137.5.1142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Steinman R. M., Cohn Z. A. Identification of a novel cell type in peripheral lymphoid organs of mice. II. Functional properties in vitro. J Exp Med. 1974 Feb 1;139(2):380–397. doi: 10.1084/jem.139.2.380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Steinman R. M., Nussenzweig M. C. Dendritic cells: features and functions. Immunol Rev. 1980;53:127–147. doi: 10.1111/j.1600-065x.1980.tb01042.x. [DOI] [PubMed] [Google Scholar]
  45. Stingl G., Katz S. I., Clement L., Green I., Shevach E. M. Immunologic functions of Ia-bearing epidermal Langerhans cells. J Immunol. 1978 Nov;121(5):2005–2013. [PubMed] [Google Scholar]
  46. Takahashi K., Yamaguchi H., Ishizeki J., Nakajima T., Nakazato Y. Immunohistochemical and immunoelectron microscopic localization of S-100 protein in the interdigitating reticulum cells of the human lymph node. Virchows Arch B Cell Pathol Incl Mol Pathol. 1981;37(2):125–135. doi: 10.1007/BF02892562. [DOI] [PubMed] [Google Scholar]
  47. Tamaki K., Stingl G., Gullino M., Sachs D. H., Katz S. I. Ia antigens in mouse skin are predominantly expressed on Langerhans cells. J Immunol. 1979 Aug;123(2):784–787. [PubMed] [Google Scholar]
  48. Tew J. G., Thorbecke G. J., Steinman R. M. Dendritic cells in the immune response: characteristics and recommended nomenclature (A report from the Reticuloendothelial Society Committee on Nomenclature). J Reticuloendothel Soc. 1982 May;31(5):371–380. [PubMed] [Google Scholar]
  49. Thorbecke G. J., Silberberg-Sinakin I., Flotte T. J. Langerhans cells as macrophages in skin and lymphoid organs. J Invest Dermatol. 1980 Jul;75(1):32–43. doi: 10.1111/1523-1747.ep12521083. [DOI] [PubMed] [Google Scholar]
  50. Unkeless J. C. Characterization of a monoclonal antibody directed against mouse macrophage and lymphocyte Fc receptors. J Exp Med. 1979 Sep 19;150(3):580–596. doi: 10.1084/jem.150.3.580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Van Voorhis W. C., Hair L. S., Steinman R. M., Kaplan G. Human dendritic cells. Enrichment and characterization from peripheral blood. J Exp Med. 1982 Apr 1;155(4):1172–1187. doi: 10.1084/jem.155.4.1172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Veerman A. J., van Ewijk W. White pulp compartments in the spleen of rats and mice. A light and electron microscopic study of lymphoid and non-lymphoid celltypes in T- and B-areas. Cell Tissue Res. 1975;156(4):417–441. doi: 10.1007/BF00225103. [DOI] [PubMed] [Google Scholar]
  53. Wolff K. Die Langerhans-Zelle. Ergebnisse neuerer experimenteller Untersuchungen. I. Arch Klin Exp Dermatol. 1967;229(1):54–75. [PubMed] [Google Scholar]

Articles from The American Journal of Pathology are provided here courtesy of American Society for Investigative Pathology

RESOURCES