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. 1988 Mar 1;106(3):649–656. doi: 10.1083/jcb.106.3.649

Murine fetal liver macrophages bind developing erythroblasts by a divalent cation-dependent hemagglutinin

PMCID: PMC2115096  PMID: 2831233

Abstract

During mammalian development the fetal liver plays an important role in hematopoiesis. Studies with the macrophage (M phi)-specific mAb F4/80 have revealed an extensive network of M phi plasma membranes interspersed between developing erythroid cells in fetal liver. To investigate the interactions between erythroid cells and stromal M phi, we isolated hematopoietic cell clusters from embryonic day-14 murine fetal liver by collagenase digestion and adherence. Clusters of erythroid cells adhered to glass mainly via M phi, 94% of which bound 19 +/- 11 erythroblasts (Eb) per cell. Bound Eb proliferated vigorously on the surface of fetal liver M phi, with little evidence of ingestion. The M phi could be stripped of their associated Eb and the clusters then reconstituted by incubation with Eb in the presence of divalent cations. The interaction required less Ca++ than Mg++, 100 vs. 250 microM for half-maximal binding, and was mediated by a trypsin- sensitive hemagglutinin on the M phi surface. After trypsin treatment fetal liver M phi recovered the ability to bind Eb and this process could be selectively inhibited by cycloheximide. Inhibition tests showed that the Eb receptor differs from known M phi plasma membrane receptors and fetal liver M phi did not bind sheep erythrocytes, a ligand for a distinct M phi hemagglutinin. We propose that fetal liver M phi interact with developing erythroid cells by a novel nonphagocytic surface hemagglutinin which is specific for a ligand found on Eb and not on mature red cells.

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Selected References

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  1. Allen T. D., Dexter T. M. Ultrastructural aspects of erythropoietic differentiation in long-term bone marrow culture. Differentiation. 1982;21(2):86–94. doi: 10.1111/j.1432-0436.1982.tb01201.x. [DOI] [PubMed] [Google Scholar]
  2. Austyn J. M., Gordon S. F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur J Immunol. 1981 Oct;11(10):805–815. doi: 10.1002/eji.1830111013. [DOI] [PubMed] [Google Scholar]
  3. BESSIS M. C., BRETON-GORIUS J. Iron metabolism in the bone marrow as seen by electron microscopy: a critical review. Blood. 1962 Jun;19:635–663. [PubMed] [Google Scholar]
  4. Bessis M., Mize C., Prenant M. Erythropoiesis: comparison of in vivo and in vitro amplification. Blood Cells. 1978;4(1-2):155–174. [PubMed] [Google Scholar]
  5. Brown P. J., Juliano R. L. Expression and function of a putative cell surface receptor for fibronectin in hamster and human cell lines. J Cell Biol. 1986 Oct;103(4):1595–1603. doi: 10.1083/jcb.103.4.1595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Crocker P. R., Gordon S. Isolation and characterization of resident stromal macrophages and hematopoietic cell clusters from mouse bone marrow. J Exp Med. 1985 Sep 1;162(3):993–1014. doi: 10.1084/jem.162.3.993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Crocker P. R., Gordon S. Properties and distribution of a lectin-like hemagglutinin differentially expressed by murine stromal tissue macrophages. J Exp Med. 1986 Dec 1;164(6):1862–1875. doi: 10.1084/jem.164.6.1862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Damsky C. H., Richa J., Solter D., Knudsen K., Buck C. A. Identification and purification of a cell surface glycoprotein mediating intercellular adhesion in embryonic and adult tissue. Cell. 1983 Sep;34(2):455–466. doi: 10.1016/0092-8674(83)90379-3. [DOI] [PubMed] [Google Scholar]
  9. Giancotti F. G., Comoglio P. M., Tarone G. Fibronectin-plasma membrane interaction in the adhesion of hemopoietic cells. J Cell Biol. 1986 Aug;103(2):429–437. doi: 10.1083/jcb.103.2.429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gordon S., Crocker P. R., Morris L., Lee S. H., Perry V. H., Hume D. A. Localization and function of tissue macrophages. Ciba Found Symp. 1986;118:54–67. doi: 10.1002/9780470720998.ch5. [DOI] [PubMed] [Google Scholar]
  11. Griffin F. M., Jr, Silverstein S. C. Segmental response of the macrophage plasma membrane to a phagocytic stimulus. J Exp Med. 1974 Feb 1;139(2):323–336. doi: 10.1084/jem.139.2.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gruber D. F., Zucali J. R., Mirand E. A. Identification of erythropoietin producing cells in fetal mouse liver cultures. Exp Hematol. 1977 Sep;5(5):392–398. [PubMed] [Google Scholar]
  13. Hatta K., Takeichi M. Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development. Nature. 1986 Apr 3;320(6061):447–449. doi: 10.1038/320447a0. [DOI] [PubMed] [Google Scholar]
  14. Hosein B., Bianco C. Monocyte receptors for fibronectin characterized by a monoclonal antibody that interferes with receptor activity. J Exp Med. 1985 Jul 1;162(1):157–170. doi: 10.1084/jem.162.1.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hsu S. M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem. 1981 Apr;29(4):577–580. doi: 10.1177/29.4.6166661. [DOI] [PubMed] [Google Scholar]
  16. Hyafil F., Babinet C., Jacob F. Cell-cell interactions in early embryogenesis: a molecular approach to the role of calcium. Cell. 1981 Nov;26(3 Pt 1):447–454. doi: 10.1016/0092-8674(81)90214-2. [DOI] [PubMed] [Google Scholar]
  17. Labastie M. C., Thiery J. P., Le Douarin N. M. Mouse yolk sac and intraembryonic tissues produce factors able to elicit differentiation of erythroid burst-forming units and colony-forming units, respectively. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1453–1456. doi: 10.1073/pnas.81.5.1453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mautner V., Hynes R. O. Surface distribution of LETS protein in relation to the cytoskeleton of normal and transformed cells. J Cell Biol. 1977 Dec;75(3):743–768. doi: 10.1083/jcb.75.3.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nathan C. F. Secretory products of macrophages. J Clin Invest. 1987 Feb;79(2):319–326. doi: 10.1172/JCI112815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Patel V. P., Lodish H. F. The fibronectin receptor on mammalian erythroid precursor cells: characterization and developmental regulation. J Cell Biol. 1986 Feb;102(2):449–456. doi: 10.1083/jcb.102.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pierschbacher M., Hayman E. G., Ruoslahti E. Synthetic peptide with cell attachment activity of fibronectin. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1224–1227. doi: 10.1073/pnas.80.5.1224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pommier C. G., O'Shea J., Chused T., Yancey K., Frank M. M., Takahashi T., Brown E. J. Studies on the fibronectin receptors of human peripheral blood leukocytes. Morphologic and functional characterization. J Exp Med. 1984 Jan 1;159(1):137–151. doi: 10.1084/jem.159.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rich I. N., Heit W., Kubanek B. Extrarenal erythropoietin production by macrophages. Blood. 1982 Oct;60(4):1007–1018. [PubMed] [Google Scholar]
  24. Roos P. H., Hartman H. J., Schlepper-Schäfer J., Kolb H., Kolb-Bachofen V. Galactose-specific receptors on liver cells. II. Characterization of the purified receptor from macrophages reveals no structural relationship to the hepatocyte receptor. Biochim Biophys Acta. 1985 Oct 30;847(1):115–121. doi: 10.1016/0167-4889(85)90161-2. [DOI] [PubMed] [Google Scholar]
  25. Shirayoshi Y., Hatta K., Hosoda M., Tsunasawa S., Sakiyama F., Takeichi M. Cadherin cell adhesion molecules with distinct binding specificities share a common structure. EMBO J. 1986 Oct;5(10):2485–2488. doi: 10.1002/j.1460-2075.1986.tb04525.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Stahl P., Gordon S. Expression of a mannosyl-fucosyl receptor for endocytosis on cultured primary macrophages and their hybrids. J Cell Biol. 1982 Apr;93(1):49–56. doi: 10.1083/jcb.93.1.49. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]

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