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During B Lymphocyte Development Regulation of Mouse CD72 Gene

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During B Lymphocyte Development Regulation of Mouse CD72 Gene Regulation of Mouse CD72 Gene Expression During B Lymphocyte Development Han Ying, James I. Healy, Christopher C. Goodnow and Jane R. Parnes This information is current as of September 26, 2021. J Immunol 1998; 161:4760-4767; ; http://www.jimmunol.org/content/161/9/4760 Downloaded from References This article cites 53 articles, 29 of which you can access for free at: http://www.jimmunol.org/content/161/9/4760.full#ref-list-1 Why The JI? Submit online. http://www.jimmunol.org/ • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *average by guest on September 26, 2021 Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 1998 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Regulation of Mouse CD72 Gene Expression During B Lymphocyte Development1 Han Ying,* James I. Healy,† Christopher C. Goodnow,† and Jane R. Parnes2* CD72 is a 45-kDa transmembrane glycoprotein that is predominantly expressed on cells of the B lineage except plasma cells. Previously, we identified the 255-bp minimal mouse CD72 promoter capable of tissue-specific and developmental stage-specific expression. DNase I footprinting analysis of the 255-bp CD72 promoter revealed three protected elements, footprint (FP) I, FP II, and FP III. FP II, which extends from nucleotide 2189 to 2169 of the mouse CD72 promoter, exhibited both tissue-specific and developmental stage-specific activity that was reflective of the activity of the CD72 gene in vivo. In this report, we show that FP II is specifically recognized by the transcription factor B cell-specific activator protein (BSAP). Mutations eliminating the binding of BSAP in reporter constructs also eliminated the increase of reporter activity in B cells. In addition, cotransfections with reporter constructs plus different amounts of expression plasmids for BSAP showed that CD72 promoter activity was up-regulated by Downloaded from BSAP in plasmacytoma cells and T cells in a dose-dependent manner. Moreover, the expression level of CD72 decreased 10-fold on normal plasma cells. Compared with the presence of BSAP binding in mature B cells, the binding of BSAP was undetectable in those plasma cells. This study strongly suggests that BSAP-FP II interaction plays a critical role in determining the cell-type specificity of the CD72 promoter. The absence of positive factors such as BSAP accounts for at least part of the loss of mouse CD72 expression in plasma cells and thus might be common for the down-regulation of many molecules at the plasma cell stage. The Journal of Immunology, 1998, 161: 4760–4767. http://www.jimmunol.org/ he development of B lymphocytes is a multistage process. Abs specific for human or mouse CD72 can enhance the B cell This process, like any other developmental process, in- proliferation induced by anti-IgM or Ag (17), induce the prolifer- T volves an ordered, sequential induction and extinction of ation of B cells and synergize with IL-4 in the induction of Ag- specific sets of structural and regulatory gene products that are specific B cells (18), partially rescue splenic B cells from the ap- primarily controlled by a combination of tissue-specific and ubiq- optosis induced by hypercross-linking of the B cell receptor (19), uitous transcription factors. Therefore, regulation of cell type-spe- enhance MHC class II expression on activated B cells (20, 21), cific gene expression is a central issue in B lymphopoiesis. Inter- induce the mobilization of small amounts cytoplasmic-free cal- estingly, there are many proteins that are expressed at all stages of cium (21), and induce an increase in the metabolism of phospha- by guest on September 26, 2021 B cell development, except terminally differentiated, Ab-produc- tidylinositol in purified small splenic B cells (22). In addition, ing plasma cells. These proteins include surface proteins such as anti-CD72 mAb inhibits the production of IgG1 but not IgG2b or Ig-a (1), Ig-b (2), CD72 (3), CD40 (4), CD19 (5), CD20 (6), and IgG3 in mouse splenic B cells cultured with LPS and IL-4 (23). CD24 (7); cytoplasmic proteins such as the tyrosine kinases Btk Recently, CD722/2 mice were generated by targeted mutation (C. (8) and Blk (9); and nuclear proteins such as B cell-specific acti- Pan and J.R.P., manuscript in preparation). Preliminary character- vator protein (BSAP)3 (10) and early B cell factor (11). Many ization of the mutant mice demonstrated that there is a significant studies have been performed to elucidate the roles of these proteins decrease in the total number of B cells in the spleen and lymph in B cell development and function, but our understanding of the nodes. These studies suggest that proper expression of the CD72 mechanisms involved in regulating their tissue specificity and de- gene is essential for B cell development and function. velopmental stage specificity is rudimentary. Previously, we have defined the 255-bp minimal CD72 pro- CD72 is among those proteins that are expressed on cells of the moter that is required for tissue-specific and developmental stage- B lineage, except plasma cells (3, 12–16). Studies have shown that specific expression (24). We also reported the identification of sev- eral cis-acting elements contributing to the tissue specificity and developmental stage specificity of the mouse CD72 promoter. One *Division of Immunology and Rheumatology, Department of Medicine, and †Howard 2 2 Hughes Medical Institute, Department of Microbiology and Immunology, Stanford of the cis elements, encompassing 196 to 163 of the mouse University School of Medicine, Stanford, CA 94305 CD72 promoter, yielded enhanced promoter activity only in pre-B Received for publication January 15, 1998. Accepted for publication June 24, 1998. and mature B cells but not in T cells or plasma cells, which is The costs of publication of this article were defrayed in part by the payment of page reflective of the activity of endogenous CD72 gene in vivo (24). charges. This article must therefore be hereby marked advertisement in accordance Analysis of the DNA fragment 2196 to 2163 demonstrated that with 18 U.S.C. Section 1734 solely to indicate this fact. there is a highly conserved, putative BSAP-binding site in the 1 This work is supported by National Institutes of Health Grant CA68675 (to J.R.P.). DNA fragment 2196 to 2163. BSAP is a transcription factor ex- H.Y. was supported in part by U.S. Public Health Service Training Grant CA09302 awarded by the National Cancer Institute, Department of Health and Human Services. pressed in the developing central nervous system, testis, and cells 2 Address correspondence and reprint requests to Dr. Jane R. Parnes, Division of of B lymphocyte lineage except terminally differentiated plasma Immunology and Rheumatology, MSLS P-306, Stanford University School of Med- cells (25, 26). Therefore, the distribution pattern of BSAP in B icine, Stanford, CA 94305-5487. cells correlates with that of CD72. The gene coding for BSAP is 3 Abbreviations used in this paper: BSAP, B cell-specific activator protein; HEL, hen Pax 5, which belongs to the Pax gene family; members of this egg white lysozyme; PDBu, phorbol-12,13-dibutyrate; EMSA, electrophoretic mo- b b family share a common DNA-binding paired domain (26, 27). Pax bility shift assay; wt, wild type; -gal, -galactosidase; nt, nucleotide(s); FP, foot- 2 2 print; BSAPmut, BSAP site mutant; doublemut, BSAP and PU.1 double mutant. 5 / mice fail to produce small pre-B, B, and plasma cells because Copyright © 1998 by The American Association of Immunologists 0022-1767/98/$02.00 The Journal of Immunology 4761 they have a complete arrest of B cell development at an early stage carry two point mutations (indicated as underlined) in each half site, re- (28). BSAP-binding sites have been identified in genes encoding placing the two most critical nucleotides for BSAP binding in each half l5 and VpreB1 (29), which encode the pre-B cell-specific surro- site. Mutant luciferase constructs were generated by PCR according to standard protocols and were confirmed by sequence analysis. gate light chain complex; the promoter region of blk, which is a The two (reverse complementary) oligonucleotides used for site-specific tyrosine kinase involved in B cell signaling (30, 31); the promoter mutagenesis were BSAPmut1, 59-CCCAAGGACCTCTCTAATTCATGA region of mb-1, which encodes Ig a, a component of the B cell AGTCCATCT-39 and BSAPmut2, 59-AGATGGACTTCATGAATTAGAG receptor complex (32); and the promoter of the gene coding for AGGTCCTTGGG-39. CD19, which is a costimulatory molecule associated with Ag re- ceptor signaling (33). These studies suggest that BSAP is a trans- Electrophoretic mobility shift assay (EMSA) activator for these genes. In contrast, BSAP confers a negative effect when binding to the J chain promoter (34) and Ig 39 a en- Nuclear proteins were prepared from cultured cells as described previously hancer (35–37), suggesting that BSAP plays a dual regulatory role (41). The double-stranded oligonucleotides were end-labeled with [g-32P]ATP (Amersham, Arlington Heights, IL). A total of 1 to 3 fmol of during B cell development. the probe was incubated with 15 mg of nuclear protein extract and 1 mgof In this report, we show that BSAP is a positive regulator for the poly(dI-dC) in a final volume of 30 ml of a buffer consisting of 8 mM CD72 gene.
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