Abstract
In the bone marrow, an elaborate stroma forms the structural basis of the hemopoietic microenvironment. In this study, two different types of stromal cells were identified with certainty on tissue sections of intact bone marrow of rats and mice using light and electron microscopic histochemistry: (a) a fibroblast-type of reticulum cell which is characterized by having alkaline phosphatase associated with its plasma membrane. We refer to this cell as the alkaline-phosphatase- positive reticulum cell (Al-RC). It is closely associated with granulocytic precursors, particularly myeloblasts and neutrophilic promyelocytes. These reticulum cells may be found throughout the marrow but are concentrated near the endosteum. (b) a macrophage-type of reticulum cell which is characterized by its abundance of lysosomal acid phosphatase and is mainly associated with erythroid precursors (as observed by others). In contrast to the above-mentioned cell type, this latter cell was found to be distributed uniformly throughout the marrow. We speculate that the Al-RC are mesenchymal stromal cells necessary for granulocytic differentiation in bone marrow.
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- Amsel S., Maniatis A., Tavassoli M., Crosby W. H. The significance of intramedullary cancellous bone formation in the repair of bone marrow tissue. Anat Rec. 1969 May;164(1):101–111. doi: 10.1002/ar.1091640107. [DOI] [PubMed] [Google Scholar]
- Ben-Ishay Z., Yoffey J. M. Ultrastructural studies of erythroblastic islands of rat bone marrow. II. The resumption of erythropoiesis in erythropoietically depressed rebound marrow. Lab Invest. 1972 Jun;26(6):637–647. [PubMed] [Google Scholar]
- Borgers M., Thoné F. The inhibition of alkaline phosphatase by L-p-bromotetramisole. Histochemistry. 1975 Aug 28;44(3):277–280. doi: 10.1007/BF00491496. [DOI] [PubMed] [Google Scholar]
- Burkhardt R. Zytologie und Histologie des menschlichen Knochenmarkes. Hamatol Bluttransfus. 1968;4:11–29. [PubMed] [Google Scholar]
- Calvo W., Haas R. J. Die Histogense des Knochenmarks der Ratte. Nervale Versorgung, Knochenmarkstroma und ihre Beziehung zur Blutzellbildung. Z Zellforsch Mikrosk Anat. 1969;95(3):377–395. [PubMed] [Google Scholar]
- Chan S. H., Metcalf D. Local production of colony-stimulating factor within the bone marrow: role of nonhematopoietic cells. Blood. 1972 Nov;40(5):646–653. [PubMed] [Google Scholar]
- Chen L. T., Weiss L. The development of vertebral bone marrow of human fetuses. Blood. 1975 Sep;46(3):389–408. [PubMed] [Google Scholar]
- De Bruyn P. P., Michelson S., Becker R. P. Endocytosis, transfer tubules, and lysosomal activity in myeloid sinusoidal endothelium. J Ultrastruct Res. 1975 Nov;53(2):133–151. doi: 10.1016/s0022-5320(75)80131-6. [DOI] [PubMed] [Google Scholar]
- FRESEN O. THE SUBMICROSCOPICAL STRUCTURE OF THE RETICULAR CELL TISSUE. Acta Haematol. 1964 Oct;32:193–199. doi: 10.1159/000209587. [DOI] [PubMed] [Google Scholar]
- Ferguson R. J., Hayes E. R., Webber R. H. The nature of the reticulum cell of the bone marrow of the rat: an electron microscopic study of the effects of methotrexate. Acta Anat (Basel) 1972;83(4):556–574. doi: 10.1159/000143899. [DOI] [PubMed] [Google Scholar]
- Friedenstein A. J., Gorskaja J. F., Kulagina N. N. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol. 1976 Sep;4(5):267–274. [PubMed] [Google Scholar]
- Heusermann U., Stutte H. J. Enzymhistochemische, histometrische und ultrastrukturelle Untersuchungen von Milzen bei der Vinylchlorid-Krankheit. Virchows Arch A Pathol Anat Histol. 1977 Oct 7;375(4):303–317. doi: 10.1007/BF00427061. [DOI] [PubMed] [Google Scholar]
- Huhn D. Die Feinstruktur des Knochenmarks der Ratte bei Anwendung neuerer Aldehydfixationen. Blut. 1966 Aug;13(5):291–304. doi: 10.1007/BF01631926. [DOI] [PubMed] [Google Scholar]
- Ito U. Electron microscopic study on benzene intoxicated rat bone marrow, with special reference to its reticulo-endothelial structure. Bull Tokyo Med Dent Univ. 1965 Mar;12(1):1–29. [PubMed] [Google Scholar]
- KAPLOW L. S. A histochemical procedure for localizing and evaluating leukocyte alkaline phosphatase activity in smears of blood and marrow. Blood. 1955 Oct;10(10):1023–1029. [PubMed] [Google Scholar]
- Kaplan A., Fischer D., Achord D., Sly W. Phosphohexosyl recognition is a general characteristic of pinocytosis of lysosomal glycosidases by human fibroblasts. J Clin Invest. 1977 Nov;60(5):1088–1093. doi: 10.1172/JCI108860. [DOI] [PMC free article] [PubMed] [Google Scholar]
- La Pushin R. W., Trentin J. J. Identification of distinctive stromal elements in erythroid and neutrophil granuloid spleen colonies: light and electron microscopic study. Exp Hematol. 1977 Nov;5(6):505–522. [PubMed] [Google Scholar]
- Leder L. D. On the terms "reticulosis" and "reticulum cell sarcoma" with regard to the modern concept of the monocyte macrophage system. Klin Wochenschr. 1978 Nov 15;56(22):1091–1096. doi: 10.1007/BF01477130. [DOI] [PubMed] [Google Scholar]
- Lundgren E. Conditions for induction of alkaline phosphatase in cultured human fetal skin fibroblasts. Exp Cell Res. 1977 Nov;110(1):25–30. doi: 10.1016/0014-4827(77)90265-8. [DOI] [PubMed] [Google Scholar]
- Metcalf D. Studies on colony formation in vitro by mouse bone marrow cells. II. Action of colony stimulating factor. J Cell Physiol. 1970 Aug;76(1):89–99. doi: 10.1002/jcp.1040760113. [DOI] [PubMed] [Google Scholar]
- Owen M. The origin of bone cells. Int Rev Cytol. 1970;28:213–238. doi: 10.1016/s0074-7696(08)62544-9. [DOI] [PubMed] [Google Scholar]
- POLICARD A., BESSIS M. Sur un mode d'incorporation des macromolécules par la cellule, visible au microscope électronique: la rhophéocytose. C R Hebd Seances Acad Sci. 1958 Jun 9;246(23):3194–3197. [PubMed] [Google Scholar]
- Patt H. M., Maloney M. A. Bone marrow regeneration after local injury: a review. Exp Hematol. 1975 Apr;3(2):135–148. [PubMed] [Google Scholar]
- Ruddell C. L. Embedding media for 1-2 micron sectioning. 2. Hydroxyethyl methacrylate combined with 2-butoxyethanol. Stain Technol. 1967 Sep;42(5):253–255. doi: 10.3109/10520296709115020. [DOI] [PubMed] [Google Scholar]
- Steinman R. M., Kaplan G., Witmer M. D., Cohn Z. A. Identification of a novel cell type in peripheral lymphoid organs of mice. V. Purification of spleen dendritic cells, new surface markers, and maintenance in vitro. J Exp Med. 1979 Jan 1;149(1):1–16. doi: 10.1084/jem.149.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tavassoli M., Shaklai M. Absence of tight junctions in endothelium of marrow sinuses: possible significance for marrow cell egress. Br J Haematol. 1979 Mar;41(3):303–307. doi: 10.1111/j.1365-2141.1979.tb05863.x. [DOI] [PubMed] [Google Scholar]
- Trubowitz S., Masek B. A histochemical study of the reticuloendothelial system of human marrow--its possible transport role. Blood. 1968 Oct;32(4):610–628. [PubMed] [Google Scholar]
- Virolainen M. Hematopoietic origin of macrophages as studied by chromosome markers in mice. J Exp Med. 1968 May 1;127(5):943–952. doi: 10.1084/jem.127.5.943. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Watanabe Y. An electron microscopic study on the reticuloendothelial system in the bone marrow. Tohoku J Exp Med. 1966 Jun 25;89(2):167–176. doi: 10.1620/tjem.89.167. [DOI] [PubMed] [Google Scholar]
- Weiss L. The hematopoietic microenvironment of the bone marrow: an ultrastructural study of the stroma in rats. Anat Rec. 1976 Oct;186(2):161–184. doi: 10.1002/ar.1091860204. [DOI] [PubMed] [Google Scholar]
- Wetzel B. K., Spicer S. S., Horn R. G. Fine structural localization of acid and alkaline phosphatases in cells of rabbit blood and bone marrow. J Histochem Cytochem. 1967 Jun;15(6):311–334. doi: 10.1177/15.6.311. [DOI] [PubMed] [Google Scholar]
- YOUNG R. W. Cell proliferation and specialization during endochondral osteogenesis in young rats. J Cell Biol. 1962 Sep;14:357–370. doi: 10.1083/jcb.14.3.357. [DOI] [PMC free article] [PubMed] [Google Scholar]