Skip to main content
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1983 Jan 1;157(1):114–129. doi: 10.1084/jem.157.1.114

Purification and characterization of fetal hematopoietic cells that express the common acute lymphoblastic leukemia antigen (CALLA)

PMCID: PMC2186888  PMID: 6571733

Abstract

Fetal hematopoietic cells that express the common acute lymphoblastic leukemia antigen (CALLA) were purified from both fetal liver and fetal bone marrow by immune rosetting with sheep erythrocytes coated with rabbit anti-mouse immunoglobulin and by fluorescence-activated cell sorting. Dual fluorescence techniques disclosed that these cells were heterogenous with respect to the expression of a series of differentiation and activation antigens defined by monoclonal antibodies. Thus, whereas all CALLA+ cells were Ia+ and expressed two activation antigens, J2 and T10, only 30-50% expressed B1 antigen. Furthermore, using methanol-fixed cells, it could be shown that approximately 20% contained intracytoplasmic mu chains (cyto-mu) and that approximately 15% were positive for the terminal transferase enzyme (TdT) marker. The CALLA+ fetal cells thus closely resemble the childhood acute lymphoblastic leukemia cell with respect to surface marker phenotype. A population of CALLA- cells devoid of mature erythroid and myeloid surface markers was found to contain higher numbers of TdT+ cells but lower numbers of cyto-mu, B1, and Ia+ cells than the CALLA+ subset. In vitro analysis of normal, purified CALLA+ cells demonstrated that incubation at 37 degrees C with J5 monoclonal antibody specific for CALLA resulted in the specific modulation of surface antigen. Similar results have previously been obtained with CALLA+ tumor cells. Although phenotypic analysis of CALLA+ cells suggests that these cells are relatively immature lymphoid cells, CALLA+ cells do not appear to contain either myeloid precursor cells (CFU-G/M) or the earliest lymphoid stem cells.

Full Text

The Full Text of this article is available as a PDF (2.4 MB).

Selected References

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

  1. Baldwin D., Jr, Prince M., Marshall S., Davies P., Olefsky J. M. Regulation of insulin receptors: evidence for involvement of an endocytotic internalization pathway. Proc Natl Acad Sci U S A. 1980 Oct;77(10):5975–5978. doi: 10.1073/pnas.77.10.5975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bollum F. J. Terminal deoxynucleotidyl transferase as a hematopoietic cell marker. Blood. 1979 Dec;54(6):1203–1215. [PubMed] [Google Scholar]
  3. Clavell L. A., Lipton J. M., Bast R. C., Jr, Kudisch M., Pesando J., Scholssman S. F., Ritz J. Absence of common ALL antigen on normal bipotent myeloid, erythroid, and granulocyte progenitors. Blood. 1981 Aug;58(2):333–336. [PubMed] [Google Scholar]
  4. Fearon D. T., Kaneko I., Thomson G. G. Membrane distribution and adsorptive endocytosis by C3b receptors on human polymorphonuclear leukocytes. J Exp Med. 1981 Jun 1;153(6):1615–1628. doi: 10.1084/jem.153.6.1615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Greaves M., Delia D., Janossy G., Rapson N., Chessells J., Woods M., Prentice G. Acute lymphoblastic leukaemia associated antigen. IV. Expression on non-leukaemic 'lymphoid' cells. Leuk Res. 1980;4(1):15–32. doi: 10.1016/0145-2126(80)90044-2. [DOI] [PubMed] [Google Scholar]
  6. Griffin J. D., Beveridge R. P., Schlossman S. F. Isolation of myeloid progenitor cells from peripheral blood of chronic myelogenous leukemia patients. Blood. 1982 Jul;60(1):30–37. [PubMed] [Google Scholar]
  7. Griffin J. D., Ritz J., Nadler L. M., Schlossman S. F. Expression of myeloid differentiation antigens on normal and malignant myeloid cells. J Clin Invest. 1981 Oct;68(4):932–941. doi: 10.1172/JCI110348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hercend T., Nadler L. M., Pesando J. M., Reinherz E. L., Schlossman S. F., Ritz J. Expression of a 26,000-dalton glycoprotein on activated human T cells. Cell Immunol. 1981 Oct;64(1):192–199. doi: 10.1016/0008-8749(81)90470-6. [DOI] [PubMed] [Google Scholar]
  9. Hercend T., Ritz J., Schlossman S. F., Reinherz E. L. Comparative expression of T9, T10, and Ia antigens on activated human T cell subsets. Hum Immunol. 1981 Nov;3(3):247–259. doi: 10.1016/0198-8859(81)90021-5. [DOI] [PubMed] [Google Scholar]
  10. Janossy G., Bollum F. J., Bradstock K. F., McMichael A., Rapson N., Greaves M. F. Terminal transferase-positive human bone marrow cells exhibit the antigenic phenotype of common acute lymphoblastic leukemia. J Immunol. 1979 Oct;123(4):1525–1529. [PubMed] [Google Scholar]
  11. Metzgar R. S., Borowitz M. J., Jones N. H., Dowell B. L. Distribution of common acute lymphoblastic leukemia antigen in nonhematopoietic tissues. J Exp Med. 1981 Oct 1;154(4):1249–1254. doi: 10.1084/jem.154.4.1249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Meuer S. C., Schlossman S. F., Reinherz E. L. Clonal analysis of human cytotoxic T lymphocytes: T4+ and T8+ effector T cells recognize products of different major histocompatibility complex regions. Proc Natl Acad Sci U S A. 1982 Jul;79(14):4395–4399. doi: 10.1073/pnas.79.14.4395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Nadler L. M., Ritz J., Bates M. P., Park E. K., Anderson K. C., Sallan S. E., Schlossman S. F. Induction of human B cell antigens in non-T cell acute lymphoblastic leukemia. J Clin Invest. 1982 Aug;70(2):433–442. doi: 10.1172/JCI110633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Nadler L. M., Ritz J., Hardy R., Pesando J. M., Schlossman S. F., Stashenko P. A unique cell surface antigen identifying lymphoid malignancies of B cell origin. J Clin Invest. 1981 Jan;67(1):134–140. doi: 10.1172/JCI110005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Nadler L. M., Stashenko P., Hardy R., Pesando J. M., Yunis E. J., Schlossman S. F. Monoclonal antibodies defining serologically distinct HLA-D/DR related Ia-like antigens in man. Hum Immunol. 1981 Feb;2(1):77–90. doi: 10.1016/0198-8859(81)90009-4. [DOI] [PubMed] [Google Scholar]
  16. Pastan I. H., Willingham M. C. Journey to the center of the cell: role of the receptosome. Science. 1981 Oct 30;214(4520):504–509. doi: 10.1126/science.6170111. [DOI] [PubMed] [Google Scholar]
  17. Pearl E. R., Vogler L. B., Okos A. J., Crist W. M., Lawton A. R., 3rd, Cooper M. D. B lymphocyte precursors in human bone marrow: an analysis of normal individuals and patients with antibody-deficiency states. J Immunol. 1978 Apr;120(4):1169–1175. [PubMed] [Google Scholar]
  18. Pesando J. M., Ritz J., Lazarus H., Tomaselli K. J., Schlossman S. F. Fate of a common acute lymphoblastic leukemia antigen during modulation by monoclonal antibody. J Immunol. 1981 Feb;126(2):540–544. [PubMed] [Google Scholar]
  19. Pesando J. M., Ritz J., Levine H., Terhorst C., Lazarus H., Schlossman S. F. Human leukemia-associated antigen: relation to a family of surface glycoproteins. J Immunol. 1980 Jun;124(6):2794–2799. [PubMed] [Google Scholar]
  20. Reinherz E. L., Hussey R. E., Schlossman S. F. A monoclonal antibody blocking human T cell function. Eur J Immunol. 1980 Oct;10(10):758–762. doi: 10.1002/eji.1830101006. [DOI] [PubMed] [Google Scholar]
  21. Reinherz E. L., Meuer S., Fitzgerald K. A., Hussey R. E., Levine H., Schlossman S. F. Antigen recognition by human T lymphocytes is linked to surface expression of the T3 molecular complex. Cell. 1982 Oct;30(3):735–743. doi: 10.1016/0092-8674(82)90278-1. [DOI] [PubMed] [Google Scholar]
  22. Ritz J., Nadler L. M., Bhan A. K., Notis-McConarty J., Pesando J. M., Schlossman S. F. Expression of common acute lymphoblastic leukemia antigen (CALLA) by lymphomas of B-cell and T-cell lineage. Blood. 1981 Sep;58(3):648–652. [PubMed] [Google Scholar]
  23. Ritz J., Pesando J. M., Notis-McConarty J., Lazarus H., Schlossman S. F. A monoclonal antibody to human acute lymphoblastic leukaemia antigen. Nature. 1980 Feb 7;283(5747):583–585. doi: 10.1038/283583a0. [DOI] [PubMed] [Google Scholar]
  24. Ritz J., Pesando J. M., Notis-McConarty J., Schlossman S. F. Modulation of human acute lymphoblastic leukemia antigen induced by monoclonal antibody in vitro. J Immunol. 1980 Oct;125(4):1506–1514. [PubMed] [Google Scholar]
  25. Ritz J., Pesando J. M., Sallan S. E., Clavell L. A., Notis-McConarty J., Rosenthal P., Schlossman S. F. Serotherapy of acute lymphoblastic leukemia with monoclonal antibody. Blood. 1981 Jul;58(1):141–152. [PubMed] [Google Scholar]
  26. Ritz J., Sallan S. E., Bast R. C., Jr, Lipton J. M., Clavell L. A., Feeney M., Hercend T., Nathan D. G., Schlossman S. F. Autologous bone-marrow transplantation in CALLA-positive acute lymphoblastic leukemia after in-vitro treatment with J5 monoclonal antibody and complement. Lancet. 1982 Jul 10;2(8289):60–63. doi: 10.1016/s0140-6736(82)91686-5. [DOI] [PubMed] [Google Scholar]
  27. Stashenko P., Nadler L. M., Hardy R., Schlossman S. F. Characterization of a human B lymphocyte-specific antigen. J Immunol. 1980 Oct;125(4):1678–1685. [PubMed] [Google Scholar]
  28. Sutherland R., Delia D., Schneider C., Newman R., Kemshead J., Greaves M. Ubiquitous cell-surface glycoprotein on tumor cells is proliferation-associated receptor for transferrin. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4515–4519. doi: 10.1073/pnas.78.7.4515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Todd R. F., 3rd, Nadler L. M., Schlossman S. F. Antigens on human monocytes identified by monoclonal antibodies. J Immunol. 1981 Apr;126(4):1435–1442. [PubMed] [Google Scholar]
  30. Todd R. F., 3rd, Van Agthoven A., Schlossman S. F., Terhorst C. Structural analysis of differentiation antigens Mo1 and Mo2 on human monocytes. Hybridoma. 1982;1(3):329–337. doi: 10.1089/hyb.1.1982.1.329. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES