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. 1995 Oct 1;131(1):243–249. doi: 10.1083/jcb.131.1.243

E-cadherin is functionally involved in the maturation of the erythroid lineage

PMCID: PMC2120602  PMID: 7559781

Abstract

Differentiation and proliferation of hematopoietic progenitors take place in the bone marrow and is a tightly controlled process. Cell adhesion molecules of the integrin and immunoglobulin families have been shown to be involved in these processes, but almost nothing was known about the involvement of the cadherin family in the hematopoietic system. A PCR screening of RNA of human bone marrow mononuclear cells with specific primers for classical cadherins revealed that E-cadherin, which is mainly expressed by cells of epithelial origin, is also expressed by bone marrow cells. Western blot analysis and immunofluorescence staining of bone marrow sections confirmed this unexpected finding. A more detailed analysis using immunoaffinity columns and dual color flow cytometry showed that the expression of E- cadherin is restricted to defined maturation stages of the erythropoietic lineage. Erythroblasts and normoblasts express E- cadherin, mature erythrocytes do not. A functional role of E-cadherin in the differentiation process of the erythroid lineage was indicated by antibody-inhibition studies. The addition of anti-E-cadherin antibody to bone marrow mononuclear cultures containing exogeneous erythropoietin drastically diminished the formation of erythropoietic cells. These data suggest a non-anticipated expression and function of E-cadherin in one defined hematopoietic cell lineage.

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Selected References

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  1. Barnstable C. J., Bodmer W. F., Brown G., Galfre G., Milstein C., Williams A. F., Ziegler A. Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens-new tools for genetic analysis. Cell. 1978 May;14(1):9–20. doi: 10.1016/0092-8674(78)90296-9. [DOI] [PubMed] [Google Scholar]
  2. Bennett J. M., Catovsky D., Daniel M. T., Flandrin G., Galton D. A., Gralnick H. R., Sultan C. Proposed revised criteria for the classification of acute myeloid leukemia. A report of the French-American-British Cooperative Group. Ann Intern Med. 1985 Oct;103(4):620–625. doi: 10.7326/0003-4819-103-4-620. [DOI] [PubMed] [Google Scholar]
  3. Bussemakers M. J., van Bokhoven A., Mees S. G., Kemler R., Schalken J. A. Molecular cloning and characterization of the human E-cadherin cDNA. Mol Biol Rep. 1993 Feb;17(2):123–128. doi: 10.1007/BF00996219. [DOI] [PubMed] [Google Scholar]
  4. Campbell A. D., Wicha M. S. Extracellular matrix and the hematopoietic microenvironment. J Lab Clin Med. 1988 Aug;112(2):140–146. [PubMed] [Google Scholar]
  5. Cepek K. L., Shaw S. K., Parker C. M., Russell G. J., Morrow J. S., Rimm D. L., Brenner M. B. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature. 1994 Nov 10;372(6502):190–193. doi: 10.1038/372190a0. [DOI] [PubMed] [Google Scholar]
  6. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  7. Dexter T. M., Coutinho L. H., Spooncer E., Heyworth C. M., Daniel C. P., Schiro R., Chang J., Allen T. D. Stromal cells in haemopoiesis. Ciba Found Symp. 1990;148:76–95. doi: 10.1002/9780470513880.ch6. [DOI] [PubMed] [Google Scholar]
  8. Dorshkind K. Regulation of hemopoiesis by bone marrow stromal cells and their products. Annu Rev Immunol. 1990;8:111–137. doi: 10.1146/annurev.iy.08.040190.000551. [DOI] [PubMed] [Google Scholar]
  9. Erle D. J. Intraepithelial lymphocytes. Scratching the surface. Curr Biol. 1995 Mar 1;5(3):252–254. doi: 10.1016/s0960-9822(95)00052-2. [DOI] [PubMed] [Google Scholar]
  10. Geiger B., Ayalon O. Cadherins. Annu Rev Cell Biol. 1992;8:307–332. doi: 10.1146/annurev.cb.08.110192.001515. [DOI] [PubMed] [Google Scholar]
  11. Gordon M. Y. Adhesive properties of haemopoietic stem cells. Br J Haematol. 1988 Feb;68(2):149–151. doi: 10.1111/j.1365-2141.1988.tb06181.x. [DOI] [PubMed] [Google Scholar]
  12. Grunwald G. B. The structural and functional analysis of cadherin calcium-dependent cell adhesion molecules. Curr Opin Cell Biol. 1993 Oct;5(5):797–805. doi: 10.1016/0955-0674(93)90028-o. [DOI] [PubMed] [Google Scholar]
  13. Hanspal M., Hanspal J. S. The association of erythroblasts with macrophages promotes erythroid proliferation and maturation: a 30-kD heparin-binding protein is involved in this contact. Blood. 1994 Nov 15;84(10):3494–3504. [PubMed] [Google Scholar]
  14. Kemler R. From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet. 1993 Sep;9(9):317–321. doi: 10.1016/0168-9525(93)90250-l. [DOI] [PubMed] [Google Scholar]
  15. Klein G., Beck S., Müller C. A. Tenascin is a cytoadhesive extracellular matrix component of the human hematopoietic microenvironment. J Cell Biol. 1993 Nov;123(4):1027–1035. doi: 10.1083/jcb.123.4.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Klein G., Conzelmann S., Beck S., Timpl R., Müller C. A. Perlecan in human bone marrow: a growth-factor-presenting, but anti-adhesive, extracellular matrix component for hematopoietic cells. Matrix Biol. 1995 Feb;14(6):457–465. doi: 10.1016/0945-053x(95)90003-9. [DOI] [PubMed] [Google Scholar]
  17. Klein G., Langegger M., Goridis C., Ekblom P. Neural cell adhesion molecules during embryonic induction and development of the kidney. Development. 1988 Apr;102(4):749–761. doi: 10.1242/dev.102.4.749. [DOI] [PubMed] [Google Scholar]
  18. Lichtman M. A. The ultrastructure of the hemopoietic environment of the marrow: a review. Exp Hematol. 1981 Apr;9(4):391–410. [PubMed] [Google Scholar]
  19. Liesveld J. L., Winslow J. M., Frediani K. E., Ryan D. H., Abboud C. N. Expression of integrins and examination of their adhesive function in normal and leukemic hematopoietic cells. Blood. 1993 Jan 1;81(1):112–121. [PubMed] [Google Scholar]
  20. Loken M. R., Shah V. O., Dattilio K. L., Civin C. I. Flow cytometric analysis of human bone marrow: I. Normal erythroid development. Blood. 1987 Jan;69(1):255–263. [PubMed] [Google Scholar]
  21. Long M. W. Blood cell cytoadhesion molecules. Exp Hematol. 1992 Mar;20(3):288–301. [PubMed] [Google Scholar]
  22. Petrides P. E., Dittmann K. H. How do normal and leukemic white blood cells egress from the bone marrow? Morphological facts and biochemical riddles. Blut. 1990 Jul;61(1):3–13. doi: 10.1007/BF01739426. [DOI] [PubMed] [Google Scholar]
  23. Ranscht B. Cadherins and catenins: interactions and functions in embryonic development. Curr Opin Cell Biol. 1994 Oct;6(5):740–746. doi: 10.1016/0955-0674(94)90102-3. [DOI] [PubMed] [Google Scholar]
  24. Shimoyama Y., Hirohashi S., Hirano S., Noguchi M., Shimosato Y., Takeichi M., Abe O. Cadherin cell-adhesion molecules in human epithelial tissues and carcinomas. Cancer Res. 1989 Apr 15;49(8):2128–2133. [PubMed] [Google Scholar]
  25. Springer T. A. Adhesion receptors of the immune system. Nature. 1990 Aug 2;346(6283):425–434. doi: 10.1038/346425a0. [DOI] [PubMed] [Google Scholar]
  26. Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science. 1991 Mar 22;251(5000):1451–1455. doi: 10.1126/science.2006419. [DOI] [PubMed] [Google Scholar]
  27. Takeichi M. Cadherins in cancer: implications for invasion and metastasis. Curr Opin Cell Biol. 1993 Oct;5(5):806–811. doi: 10.1016/0955-0674(93)90029-p. [DOI] [PubMed] [Google Scholar]
  28. Tang A., Amagai M., Granger L. G., Stanley J. R., Udey M. C. Adhesion of epidermal Langerhans cells to keratinocytes mediated by E-cadherin. Nature. 1993 Jan 7;361(6407):82–85. doi: 10.1038/361082a0. [DOI] [PubMed] [Google Scholar]
  29. Tanihara H., Kido M., Obata S., Heimark R. L., Davidson M., St John T., Suzuki S. Characterization of cadherin-4 and cadherin-5 reveals new aspects of cadherins. J Cell Sci. 1994 Jun;107(Pt 6):1697–1704. doi: 10.1242/jcs.107.6.1697. [DOI] [PubMed] [Google Scholar]
  30. Tanihara H., Sano K., Heimark R. L., St John T., Suzuki S. Cloning of five human cadherins clarifies characteristic features of cadherin extracellular domain and provides further evidence for two structurally different types of cadherin. Cell Adhes Commun. 1994 Apr;2(1):15–26. doi: 10.3109/15419069409014199. [DOI] [PubMed] [Google Scholar]
  31. Teixidó J., Hemler M. E., Greenberger J. S., Anklesaria P. Role of beta 1 and beta 2 integrins in the adhesion of human CD34hi stem cells to bone marrow stroma. J Clin Invest. 1992 Aug;90(2):358–367. doi: 10.1172/JCI115870. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Vestweber D., Kemler R. Identification of a putative cell adhesion domain of uvomorulin. EMBO J. 1985 Dec 16;4(13A):3393–3398. doi: 10.1002/j.1460-2075.1985.tb04095.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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