Abstract
Bone marrow stromal cells promote B cell development involving recombinase gene-directed rearrangement of the immunoglobulin genes. We observed that the stromal cell-derived cytokine interleukin 7 (IL-7) enhances the expression of CD19 molecules on progenitor B-lineage cells in human bone marrow samples and downregulates the expression of terminal deoxynucleotidyl transferase (TdT) and the recombinase- activating genes RAG-1 and RAG-2. Initiation of the TdT downregulation on the first day of treatment, CD19 upregulation during the second day, and RAG-1 and RAG-2 downmodulation during the third day implied a cascade of IL-7 effects. While CD19 ligation by divalent antibodies had no direct effect on TdT or RAG gene expression, CD19 cross-linkage complete blocked the IL-7 downregulation of RAG expression without affecting the earlier TdT response. These results suggest that signals generated through CD19 and the IL-7 receptor could modulate immunoglobulin gene rearrangement and repertoire diversification during the early stages of B cell differentiation.
Full Text
The Full Text of this article is available as a PDF (1.3 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Alt F. W., Baltimore D. Joining of immunoglobulin heavy chain gene segments: implications from a chromosome with evidence of three D-JH fusions. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4118–4122. doi: 10.1073/pnas.79.13.4118. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Alt F. W., Oltz E. M., Young F., Gorman J., Taccioli G., Chen J. VDJ recombination. Immunol Today. 1992 Aug;13(8):306–314. doi: 10.1016/0167-5699(92)90043-7. [DOI] [PubMed] [Google Scholar]
- Billips L. G., Petitte D., Dorshkind K., Narayanan R., Chiu C. P., Landreth K. S. Differential roles of stromal cells, interleukin-7, and kit-ligand in the regulation of B lymphopoiesis. Blood. 1992 Mar 1;79(5):1185–1192. [PubMed] [Google Scholar]
- Bollum F. J. Terminal deoxynucleotidyl transferase as a hematopoietic cell marker. Blood. 1979 Dec;54(6):1203–1215. [PubMed] [Google Scholar]
- Callard R. E., Rigley K. P., Smith S. H., Thurstan S., Shields J. G. CD19 regulation of human B cell responses. B cell proliferation and antibody secretion are inhibited or enhanced by ligation of the CD19 surface glycoprotein depending on the stimulating signal used. J Immunol. 1992 May 15;148(10):2983–2987. [PubMed] [Google Scholar]
- Campana D., Farrant J., Inamdar N., Webster A. D., Janossy G. Phenotypic features and proliferative activity of B cell progenitors in X-linked agammaglobulinemia. J Immunol. 1990 Sep 15;145(6):1675–1680. [PubMed] [Google Scholar]
- Campana D., Janossy G., Bofill M., Trejdosiewicz L. K., Ma D., Hoffbrand A. V., Mason D. Y., Lebacq A. M., Forster H. K. Human B cell development. I. Phenotypic differences of B lymphocytes in the bone marrow and peripheral lymphoid tissue. J Immunol. 1985 Mar;134(3):1524–1530. [PubMed] [Google Scholar]
- Campana D., Janossy G., Coustan-Smith E., Amlot P. L., Tian W. T., Ip S., Wong L. The expression of T cell receptor-associated proteins during T cell ontogeny in man. J Immunol. 1989 Jan 1;142(1):57–66. [PubMed] [Google Scholar]
- Carroll W. L., Starnes C. O., Levy R., Levy S. Alternative V kappa gene rearrangements in a murine B cell lymphoma. An explantation for idiotypic heterogeneity. J Exp Med. 1988 Nov 1;168(5):1607–1620. doi: 10.1084/jem.168.5.1607. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carter R. H., Fearon D. T. CD19: lowering the threshold for antigen receptor stimulation of B lymphocytes. Science. 1992 Apr 3;256(5053):105–107. doi: 10.1126/science.1373518. [DOI] [PubMed] [Google Scholar]
- Carter R. H., Tuveson D. A., Park D. J., Rhee S. G., Fearon D. T. The CD19 complex of B lymphocytes. Activation of phospholipase C by a protein tyrosine kinase-dependent pathway that can be enhanced by the membrane IgM complex. J Immunol. 1991 Dec 1;147(11):3663–3671. [PubMed] [Google Scholar]
- Chalupny N. J., Kanner S. B., Schieven G. L., Wee S. F., Gilliland L. K., Aruffo A., Ledbetter J. A. Tyrosine phosphorylation of CD19 in pre-B and mature B cells. EMBO J. 1993 Jul;12(7):2691–2696. doi: 10.1002/j.1460-2075.1993.tb05930.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Cooper M. D., Kearney J. F., Gathings W. E., Lawton A. R. Effects of anti-Ig antibodies on the development and differentiation of B cells. Immunol Rev. 1980;52:29–53. doi: 10.1111/j.1600-065x.1980.tb00329.x. [DOI] [PubMed] [Google Scholar]
- Dadi H. K., Ke S., Roifman C. M. Interleukin 7 receptor mediates the activation of phosphatidylinositol-3 kinase in human B-cell precursors. Biochem Biophys Res Commun. 1993 Apr 30;192(2):459–464. doi: 10.1006/bbrc.1993.1437. [DOI] [PubMed] [Google Scholar]
- DiSanto J. P., Müller W., Guy-Grand D., Fischer A., Rajewsky K. Lymphoid development in mice with a targeted deletion of the interleukin 2 receptor gamma chain. Proc Natl Acad Sci U S A. 1995 Jan 17;92(2):377–381. doi: 10.1073/pnas.92.2.377. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Faust E. A., Saffran D. C., Toksoz D., Williams D. A., Witte O. N. Distinctive growth requirements and gene expression patterns distinguish progenitor B cells from pre-B cells. J Exp Med. 1993 Apr 1;177(4):915–923. doi: 10.1084/jem.177.4.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Feeney A. J. Lack of N regions in fetal and neonatal mouse immunoglobulin V-D-J junctional sequences. J Exp Med. 1990 Nov 1;172(5):1377–1390. doi: 10.1084/jem.172.5.1377. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilfillan S., Dierich A., Lemeur M., Benoist C., Mathis D. Mice lacking TdT: mature animals with an immature lymphocyte repertoire. Science. 1993 Aug 27;261(5125):1175–1178. doi: 10.1126/science.8356452. [DOI] [PubMed] [Google Scholar]
- Gimble J. M., Pietrangeli C., Henley A., Dorheim M. A., Silver J., Namen A., Takeichi M., Goridis C., Kincade P. W. Characterization of murine bone marrow and spleen-derived stromal cells: analysis of leukocyte marker and growth factor mRNA transcript levels. Blood. 1989 Jul;74(1):303–311. [PubMed] [Google Scholar]
- Grabstein K. H., Waldschmidt T. J., Finkelman F. D., Hess B. W., Alpert A. R., Boiani N. E., Namen A. E., Morrissey P. J. Inhibition of murine B and T lymphopoiesis in vivo by an anti-interleukin 7 monoclonal antibody. J Exp Med. 1993 Jul 1;178(1):257–264. doi: 10.1084/jem.178.1.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gu H., Förster I., Rajewsky K. Sequence homologies, N sequence insertion and JH gene utilization in VHDJH joining: implications for the joining mechanism and the ontogenetic timing of Ly1 B cell and B-CLL progenitor generation. EMBO J. 1990 Jul;9(7):2133–2140. doi: 10.1002/j.1460-2075.1990.tb07382.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hayashi S., Kunisada T., Ogawa M., Sudo T., Kodama H., Suda T., Nishikawa S., Nishikawa S. Stepwise progression of B lineage differentiation supported by interleukin 7 and other stromal cell molecules. J Exp Med. 1990 May 1;171(5):1683–1695. doi: 10.1084/jem.171.5.1683. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heller M., Owens J. D., Mushinski J. F., Rudikoff S. Amino acids at the site of V kappa-J kappa recombination not encoded by germline sequences. J Exp Med. 1987 Sep 1;166(3):637–646. doi: 10.1084/jem.166.3.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kincade P. W. Experimental models for understanding B lymphocyte formation. Adv Immunol. 1987;41:181–267. doi: 10.1016/s0065-2776(08)60032-2. [DOI] [PubMed] [Google Scholar]
- Kincade P. W., Lawton A. R., Bockman D. E., Cooper M. D. Suppression of immunoglobulin G synthesis as a result of antibody-mediated suppression of immunoglobulin M synthesis in chickens. Proc Natl Acad Sci U S A. 1970 Dec;67(4):1918–1925. doi: 10.1073/pnas.67.4.1918. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kitamura D., Rajewsky K. Targeted disruption of mu chain membrane exon causes loss of heavy-chain allelic exclusion. Nature. 1992 Mar 12;356(6365):154–156. doi: 10.1038/356154a0. [DOI] [PubMed] [Google Scholar]
- Komori T., Okada A., Stewart V., Alt F. W. Lack of N regions in antigen receptor variable region genes of TdT-deficient lymphocytes. Science. 1993 Aug 27;261(5125):1171–1175. doi: 10.1126/science.8356451. [DOI] [PubMed] [Google Scholar]
- Lassoued K., Nuñez C. A., Billips L., Kubagawa H., Monteiro R. C., LeBlen T. W., Cooper M. D. Expression of surrogate light chain receptors is restricted to a late stage in pre-B cell differentiation. Cell. 1993 Apr 9;73(1):73–86. doi: 10.1016/0092-8674(93)90161-i. [DOI] [PubMed] [Google Scholar]
- Ledbetter J. A., Rabinovitch P. S., June C. H., Song C. W., Clark E. A., Uckun F. M. Antigen-independent regulation of cytoplasmic calcium in B cells with a 12-kDa B-cell growth factor and anti-CD19. Proc Natl Acad Sci U S A. 1988 Mar;85(6):1897–1901. doi: 10.1073/pnas.85.6.1897. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee G., Namen A. E., Gillis S., Ellingsworth L. R., Kincade P. W. Normal B cell precursors responsive to recombinant murine IL-7 and inhibition of IL-7 activity by transforming growth factor-beta. J Immunol. 1989 Jun 1;142(11):3875–3883. [PubMed] [Google Scholar]
- Lin W. C., Desiderio S. Regulation of V(D)J recombination activator protein RAG-2 by phosphorylation. Science. 1993 May 14;260(5110):953–959. doi: 10.1126/science.8493533. [DOI] [PubMed] [Google Scholar]
- Ma A., Fisher P., Dildrop R., Oltz E., Rathbun G., Achacoso P., Stall A., Alt F. W. Surface IgM mediated regulation of RAG gene expression in E mu-N-myc B cell lines. EMBO J. 1992 Jul;11(7):2727–2734. doi: 10.1002/j.1460-2075.1992.tb05338.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Manz J., Denis K., Witte O., Brinster R., Storb U. Feedback inhibition of immunoglobulin gene rearrangement by membrane mu, but not by secreted mu heavy chains. J Exp Med. 1988 Oct 1;168(4):1363–1381. doi: 10.1084/jem.168.4.1363. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maruyama S., Kubagawa H., Cooper M. D. Activation of human B cells and inhibition of their terminal differentiation by monoclonal anti-mu antibodies. J Immunol. 1985 Jul;135(1):192–199. [PubMed] [Google Scholar]
- McNiece I. K., Langley K. E., Zsebo K. M. The role of recombinant stem cell factor in early B cell development. Synergistic interaction with IL-7. J Immunol. 1991 Jun 1;146(11):3785–3790. [PubMed] [Google Scholar]
- Melchers F., Karasuyama H., Haasner D., Bauer S., Kudo A., Sakaguchi N., Jameson B., Rolink A. The surrogate light chain in B-cell development. Immunol Today. 1993 Feb;14(2):60–68. doi: 10.1016/0167-5699(93)90060-X. [DOI] [PubMed] [Google Scholar]
- Mombaerts P., Iacomini J., Johnson R. S., Herrup K., Tonegawa S., Papaioannou V. E. RAG-1-deficient mice have no mature B and T lymphocytes. Cell. 1992 Mar 6;68(5):869–877. doi: 10.1016/0092-8674(92)90030-g. [DOI] [PubMed] [Google Scholar]
- Muegge K., Vila M. P., Durum S. K. Interleukin-7: a cofactor for V(D)J rearrangement of the T cell receptor beta gene. Science. 1993 Jul 2;261(5117):93–95. doi: 10.1126/science.7686307. [DOI] [PubMed] [Google Scholar]
- Nadler L. M., Anderson K. C., Marti G., Bates M., Park E., Daley J. F., Schlossman S. F. B4, a human B lymphocyte-associated antigen expressed on normal, mitogen-activated, and malignant B lymphocytes. J Immunol. 1983 Jul;131(1):244–250. [PubMed] [Google Scholar]
- Nakamura T., Kubagawa H., Cooper M. D. Heterogeneity of immunoglobulin-associated molecules on human B cells identified by monoclonal antibodies. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8522–8526. doi: 10.1073/pnas.89.18.8522. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Namen A. E., Schmierer A. E., March C. J., Overell R. W., Park L. S., Urdal D. L., Mochizuki D. Y. B cell precursor growth-promoting activity. Purification and characterization of a growth factor active on lymphocyte precursors. J Exp Med. 1988 Mar 1;167(3):988–1002. doi: 10.1084/jem.167.3.988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nishikawa S. I., Hayashi S. I., Ogawa M., Kunisada T., Nishikawa S., Sudo T., Nakauchi H., Suda T. Control of cell growth and differentiation during early B-cell development by stromal cell molecules. Cold Spring Harb Symp Quant Biol. 1989;54(Pt 1):171–174. doi: 10.1101/sqb.1989.054.01.021. [DOI] [PubMed] [Google Scholar]
- Nishimoto N., Kubagawa H., Ohno T., Gartland G. L., Stankovic A. K., Cooper M. D. Normal pre-B cells express a receptor complex of mu heavy chains and surrogate light-chain proteins. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6284–6288. doi: 10.1073/pnas.88.14.6284. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Noguchi M., Yi H., Rosenblatt H. M., Filipovich A. H., Adelstein S., Modi W. S., McBride O. W., Leonard W. J. Interleukin-2 receptor gamma chain mutation results in X-linked severe combined immunodeficiency in humans. Cell. 1993 Apr 9;73(1):147–157. doi: 10.1016/0092-8674(93)90167-o. [DOI] [PubMed] [Google Scholar]
- Nussenzweig M. C., Shaw A. C., Sinn E., Danner D. B., Holmes K. L., Morse H. C., 3rd, Leder P. Allelic exclusion in transgenic mice that express the membrane form of immunoglobulin mu. Science. 1987 May 15;236(4803):816–819. doi: 10.1126/science.3107126. [DOI] [PubMed] [Google Scholar]
- Oettinger M. A., Schatz D. G., Gorka C., Baltimore D. RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science. 1990 Jun 22;248(4962):1517–1523. doi: 10.1126/science.2360047. [DOI] [PubMed] [Google Scholar]
- Pandrau-Garcia D., de Saint-Vis B., Saeland S., Renard N., Ho S., Moreau I., Banchereau J., Galizzi J. P. Growth inhibitory and agonistic signals of interleukin-7 (IL-7) can be mediated through the CDw127 IL-7 receptor. Blood. 1994 Jun 15;83(12):3613–3619. [PubMed] [Google Scholar]
- Pezzutto A., Dörken B., Rabinovitch P. S., Ledbetter J. A., Moldenhauer G., Clark E. A. CD19 monoclonal antibody HD37 inhibits anti-immunoglobulin-induced B cell activation and proliferation. J Immunol. 1987 May 1;138(9):2793–2799. [PubMed] [Google Scholar]
- Raff M. C., Megson M., Owen J. J., Cooper M. D. Early production of intracellular IgM by B-lymphocyte precursors in mouse. Nature. 1976 Jan 22;259(5540):224–226. doi: 10.1038/259224a0. [DOI] [PubMed] [Google Scholar]
- Reth M. G., Alt F. W. Novel immunoglobulin heavy chains are produced from DJH gene segment rearrangements in lymphoid cells. 1984 Nov 29-Dec 5Nature. 312(5993):418–423. doi: 10.1038/312418a0. [DOI] [PubMed] [Google Scholar]
- Rigley K. P., Callard R. E. Inhibition of B cell proliferation with anti-CD19 monoclonal antibodies: anti-CD19 antibodies do not interfere with early signaling events triggered by anti-IgM or interleukin 4. Eur J Immunol. 1991 Mar;21(3):535–540. doi: 10.1002/eji.1830210302. [DOI] [PubMed] [Google Scholar]
- Roifman C. M., Wang G. X., Freedman M., Pan Z. Q. IL-7 receptor mediates tyrosine phosphorylation but does not activate the phosphatidylinositol-phospholipase C-gamma 1 pathway. J Immunol. 1992 Feb 15;148(4):1136–1142. [PubMed] [Google Scholar]
- Rolink A., Grawunder U., Haasner D., Strasser A., Melchers F. Immature surface Ig+ B cells can continue to rearrange kappa and lambda L chain gene loci. J Exp Med. 1993 Oct 1;178(4):1263–1270. doi: 10.1084/jem.178.4.1263. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Russell S. M., Keegan A. D., Harada N., Nakamura Y., Noguchi M., Leland P., Friedmann M. C., Miyajima A., Puri R. K., Paul W. E. Interleukin-2 receptor gamma chain: a functional component of the interleukin-4 receptor. Science. 1993 Dec 17;262(5141):1880–1883. doi: 10.1126/science.8266078. [DOI] [PubMed] [Google Scholar]
- Saeland S., Duvert V., Pandrau D., Caux C., Durand I., Wrighton N., Wideman J., Lee F., Banchereau J. Interleukin-7 induces the proliferation of normal human B-cell precursors. Blood. 1991 Nov 1;78(9):2229–2238. [PubMed] [Google Scholar]
- Schatz D. G., Oettinger M. A., Schlissel M. S. V(D)J recombination: molecular biology and regulation. Annu Rev Immunol. 1992;10:359–383. doi: 10.1146/annurev.iy.10.040192.002043. [DOI] [PubMed] [Google Scholar]
- Seckinger P., Fougereau M. Activation of src family kinases in human pre-B cells by IL-7. J Immunol. 1994 Jul 1;153(1):97–109. [PubMed] [Google Scholar]
- Shinkai Y., Rathbun G., Lam K. P., Oltz E. M., Stewart V., Mendelsohn M., Charron J., Datta M., Young F., Stall A. M. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell. 1992 Mar 6;68(5):855–867. doi: 10.1016/0092-8674(92)90029-c. [DOI] [PubMed] [Google Scholar]
- Storb U. Transgenic mice with immunoglobulin genes. Annu Rev Immunol. 1987;5:151–174. doi: 10.1146/annurev.iy.05.040187.001055. [DOI] [PubMed] [Google Scholar]
- Sudo T., Ito M., Ogawa Y., Iizuka M., Kodama H., Kunisada T., Hayashi S., Ogawa M., Sakai K., Nishikawa S. Interleukin 7 production and function in stromal cell-dependent B cell development. J Exp Med. 1989 Jul 1;170(1):333–338. doi: 10.1084/jem.170.1.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sudo T., Nishikawa S., Ohno N., Akiyama N., Tamakoshi M., Yoshida H., Nishikawa S. Expression and function of the interleukin 7 receptor in murine lymphocytes. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9125–9129. doi: 10.1073/pnas.90.19.9125. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tedder T. F., Zhou L. J., Engel P. The CD19/CD21 signal transduction complex of B lymphocytes. Immunol Today. 1994 Sep;15(9):437–442. doi: 10.1016/0167-5699(94)90274-7. [DOI] [PubMed] [Google Scholar]
- Tuveson D. A., Carter R. H., Soltoff S. P., Fearon D. T. CD19 of B cells as a surrogate kinase insert region to bind phosphatidylinositol 3-kinase. Science. 1993 May 14;260(5110):986–989. doi: 10.1126/science.7684160. [DOI] [PubMed] [Google Scholar]
- Uckun F. M., Burkhardt A. L., Jarvis L., Jun X., Stealey B., Dibirdik I., Myers D. E., Tuel-Ahlgren L., Bolen J. B. Signal transduction through the CD19 receptor during discrete developmental stages of human B-cell ontogeny. J Biol Chem. 1993 Oct 5;268(28):21172–21184. [PubMed] [Google Scholar]
- Uckun F. M., Dibirdik I., Smith R., Tuel-Ahlgren L., Chandan-Langlie M., Schieven G. L., Waddick K. G., Hanson M., Ledbetter J. A. Interleukin 7 receptor ligation stimulates tyrosine phosphorylation, inositol phospholipid turnover, and clonal proliferation of human B-cell precursors. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3589–3593. doi: 10.1073/pnas.88.9.3589. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Uckun F. M., Jaszcz W., Ambrus J. L., Fauci A. S., Gajl-Peczalska K., Song C. W., Wick M. R., Myers D. E., Waddick K., Ledbetter J. A. Detailed studies on expression and function of CD19 surface determinant by using B43 monoclonal antibody and the clinical potential of anti-CD19 immunotoxins. Blood. 1988 Jan;71(1):13–29. [PubMed] [Google Scholar]
- Uckun F. M., Ledbetter J. A. Immunobiologic differences between normal and leukemic human B-cell precursors. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8603–8607. doi: 10.1073/pnas.85.22.8603. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Uckun F. M. Regulation of human B-cell ontogeny. Blood. 1990 Nov 15;76(10):1908–1923. [PubMed] [Google Scholar]
- Venkitaraman A. R., Cowling R. J. Interleukin 7 receptor functions by recruiting the tyrosine kinase p59fyn through a segment of its cytoplasmic tail. Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):12083–12087. doi: 10.1073/pnas.89.24.12083. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vetrie D., Vorechovský I., Sideras P., Holland J., Davies A., Flinter F., Hammarström L., Kinnon C., Levinsky R., Bobrow M. The gene involved in X-linked agammaglobulinaemia is a member of the src family of protein-tyrosine kinases. Nature. 1993 Jan 21;361(6409):226–233. doi: 10.1038/361226a0. [DOI] [PubMed] [Google Scholar]
- Whitlock C. A., Witte O. N. Long-term culture of B lymphocytes and their precursors from murine bone marrow. Proc Natl Acad Sci U S A. 1982 Jun;79(11):3608–3612. doi: 10.1073/pnas.79.11.3608. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wolf M. L., Weng W. K., Stieglbauer K. T., Shah N., LeBien T. W. Functional effect of IL-7-enhanced CD19 expression on human B cell precursors. J Immunol. 1993 Jul 1;151(1):138–148. [PubMed] [Google Scholar]
- Zhou L. J., Smith H. M., Waldschmidt T. J., Schwarting R., Daley J., Tedder T. F. Tissue-specific expression of the human CD19 gene in transgenic mice inhibits antigen-independent B-lymphocyte development. Mol Cell Biol. 1994 Jun;14(6):3884–3894. doi: 10.1128/mcb.14.6.3884. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Rie M. A., Schumacher T. N., van Schijndel G. M., van Lier R. A., Miedema F. Regulatory role of CD19 molecules in B-cell activation and differentiation. Cell Immunol. 1989 Feb;118(2):368–381. doi: 10.1016/0008-8749(89)90385-7. [DOI] [PubMed] [Google Scholar]