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Discriminating Gene Expression Profiles of Memory B Cell

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Discriminating Gene Expression Profiles of Memory B Cell ARTICLE Discriminating gene expression profi les of memory B cell subpopulations 1,2 5 5 G ö tz R.A. Ehrhardt , Atsushi Hijikata , Hiroshi Kitamura, 5 6 1,2,3,4 Osamu Ohara , Ji-Yang Wang , and Max D. Cooper 1 Department of Pathology and Laboratory Medicine and 2 Emory Vaccine Center, Emory University School of Medicine, Atlanta, GA 30322 3 Georgia Research Alliance, Atlanta, GA 30303 4 Emory Center for AIDS Research, Rollins School of Public Health, Emory University, Atlanta, GA 30322 5 Immunogenomics Group and 6 Laboratory for Immune Diversity, RIKEN Center for Allergy and Immunology, Tsurumi-ku, Yokohama City, Kanagawa 230-0045, Japan Morphologically and functionally distinct subpopulations of human memory B (BMem ) cells are identifi able by either their expression of CD27 or Fc receptor – like 4 (FCRL4), an immuno- globulin domain containing a receptor with strong inhibitory potential. We have conducted ؊ + comparative transcriptome and proteome analyses of FCRL4 and FCRL4 BMem cells and found that these two subsets have very distinctive expression profi les for genes encoding transcription factors, cell-surface proteins, intracellular signaling molecules, and modifi ers of the cell-cycle status. Among the differentially expressed transcription factors, runt- ,related transcription factor 1 (RUNX1) transcript levels were up-regulated in FCRL4 ؊ cells whereas RUNX2 transcripts were preferentially detected in FCRL4+ cells. In vitro evidence for FCRL4 promoter responsiveness and in vivo promoter occupancy suggested that RUNX transcription factors are involved in the generation of these BMem cell subpopulations. A + distinctive signature profi le was defi ned for the FCRL4 BMem cells by their expression of CD11c, receptor activator for nuclear factor ␬ B ligand, and FAS cell-surface proteins, in combination with increased levels of SOX5 , RUNX2 , DLL1 , and AICDA expression. We con- clude that this recently identifi ed subpopulation of BMem cells, which normally resides in epithelial tissue-based niches, may serve a unique role in mucosal defense and, conversely, as a target for neoplastic transformation events. CORRESPONDENCE Protective immunity elicited by T cell – depen- named immunoreceptor superfamily translo- Max D. Cooper: dent antigens may last for decades without fur- cation-associated 1 ( 11 ), and an independent [email protected] ther exposure to the immunizing antigen ( 1, 2 ), identifi cation through its sequence similarity to The Journal of Experimental Medicine Abbreviations used: AICDA, and the memory B (BMem ) cells serve an impor- known Fc receptors led to the name Fc receptor activation-induced cytidine tant role in sustaining humoral immunity. A de- homologue 4 ( 12 ). A unifi ed nomenclature was deaminase; B , memory B; Mem fi ning characteristic of BMem cells is their ability recently adopted in which this gene was renamed CBF ␤ , core-binding factor ␤ ; ChIP, chromatin immunopre- to respond rapidly upon reencounter with their FCRL4 ( 13 ). cipitation; DLL1, delta-like 1; cognate antigens. Most BMem cells in humans are FCRL4 expression is restricted to a subpop- FCRL, Fc receptor like; GC, characterized by their expression of CD27 and ulation of BMem cells with a distinctive phenotype germinal center; HCK, hemo- poietic cell kinase; LCK, lym- switched Ig isotype ( 3 – 5 ). However, recent re- and tissue localization pattern ( 7, 14 ). Its intracel- phocyte-specifi c protein tyrosine ports describe an additional population of tissue- lular domain contains three consensus immuno- kinase; RANKL, receptor acti- based B cells that do not express CD27 ( 6 – 9 ) receptor tyrosine-based inhibition motifs, and ␬ Mem vator for NF- B ligand; but instead express Fc receptor– like 4 (FCRL4) coligation of FCRL4 with the BCR aborts BCR- RUNX, runt-related transcrip- tion factor; SHP, Src homology ( 7 ). FCRL4 is a member of a recently identifi ed mediated signaling via recruitment of the Src 2 domain – containing phospha- family of transmembrane proteins with immuno- homology 2 domain– containing phosphatase 1 tase; SOX5, SRY-box 5; XBP1, regulatory potential, fi ve of which display prefer- (SHP-1) and/or SHP-2 tyrosine phosphatases (15 ). X-box binding protein 1. ential B cell expression (for review see reference 10 ). Originally identifi ed as a translocation fusion © 2008 Ehrhardt et al. This article is distributed under the terms of an Attribu- tion–Noncommercial–Share Alike–No Mirror Sites license for the fi rst six months partner in a myeloma cell line, FCRL4 was after the publication date (see http://www.jem.org/misc/terms.shtml). After six months it is available under a Creative Commons License (Attribution–Noncom- mercial–Share Alike 3.0 Unported license, as described at http://creativecommons. The online version of this article contains supplemental material. org/licenses/by-nc-sa/3.0/). The Rockefeller University Press $30.00 J. Exp. Med. Vol. 205 No. 8 1807-1817 1807 www.jem.org/cgi/doi/10.1084/jem.20072682 + The FCRL4 cells are rarely seen in the bone marrow, blood, these two BMem cell subpopulations. This transcriptome analysis and spleen, but are found instead in the crypt epithelium and revealed a surprisingly large number of diff erentially expressed perifollicular regions of the palatine tonsils, intestinal lymphoid genes. Using this gene expression data as a starting point, we tissues, and mesenteric lymph nodes, wherein their numbers obtained evidence indicating that diff erences in transcription are increased in patients with lymphadenitis caused by Toxo- factors, cell-surface receptors, and cell-cycle status character- plasmosis gondii , HIV-1, and EBV infections ( 7, 14, 16 ). Most ize the diff erentiation profi les that distinguish these two B Mem + of the FCRL4 tissue-resident cells do not express CD27, the cell subpopulations. currently favored marker for human B Mem cells. Although the Ϫ + FCRL4 /CD27 BMem cells respond vigorously to in vitro RESULTS stimulation by T cell – derived cytokines (IL-2 and IL-10) and Transcriptome profi les differ for FCRL4 + ؊ + CD40L or BCR ligation, the FCRL4 cells preferentially re- and FCRL4 BMem cells + spond to T cell cytokines and CD40L alone ( 7 ). The relatively A comparison of transcripts expressed by FCRL4 versus + Ϫ Ϫ large FCRL4 BMem cells and the relatively small FCRL4 FCRL4 BMem cells was conducted by a gene array analysis BMem cells thus represent morphologically, topographically, and of tonsillar tissues from three young donors, none of whom functionally distinguishable subpopulations. showed signs of illness at the time of tonsillectomy. This com- To gain additional insight into their diff erentiation status parison led to the identifi cation of 164 transcripts that were and function, we examined the transcript expression profi les of expressed with a greater than fourfold diff erence by the two + Ϫ + Ϫ Figure 1. Transcriptome analysis of FCRL4 and FCRL4 BMem cells. The transcripts differentially expressed by FCRL4 and FCRL4 BMem from three independent tonsillar cell preparations are displayed. Up- and down-regulated transcripts are indicated in red and green, respectively. The magnitude of expression is depicted by the color bar. Arrowheads indicate transcripts whose expression was validated by quantitative RT-PCR and/or by FACS analysis of other tonsillar samples. 1808 MEMORY B CELL SUBSETS | Ehrhardt et al. ARTICLE BMem cell populations. The large array of diff erentially ex- B cells has also been observed ( 17 – 20 ). As would be antici- pressed genes revealed in this analysis included ones encod- pated, signifi cant diff erences in transcription levels were not ing transcription factors, cell-cycle modulators, cell-surface detected for the prototypical B cell src kinase LYN (Fig. 2 B , molecules, and components of signal transduction cascades. top). Overall, this transcriptome analysis revealed a relatively Fig. 1 shows a heat map of the diff erentially regulated transcripts. large number of transcripts (128) with increased levels of ex- The majority of these up-regulated genes were identified pression in FCRL4 + cells, and a more limited set of transcripts in the FCRL4 + cells. Not surprisingly, FCRL4 was among (36) with increased expression levels in FCRL4 Ϫ cells. the strongly up-regulated transcripts in the FCRL4+ popu- lation, as were CCR1 transcripts, in keeping with a previ- Distinctive surface marker profi le of FCRL4 + cells ous analysis ( 7 ). Surprisingly, one of the strongly up-regulated We performed quantitative RT-PCR and FACS profi le ana- transcripts encoded receptor activator for NF- ␬ B ligand lyses to verify the diff erential expression of transcripts for cell- (RANKL), and this unanticipated fi nding was confi rmed by surface receptors that might be useful in distinguishing the quantitative RT-PCR analysis and measurement of protein two BMem cell populations ( Fig. 3 ). Flow cytometric immuno- expression in other tonsil samples ( Fig. 2 A ). Quantitative fl uorescence analysis confi rmed that the FCRL4 + cells ex- RT-PCR analyses likewise confi rmed the higher expression press relatively high levels of CD95 (FAS) in comparison Ϫ + levels of runt-related transcription factor 2 (RUNX2) and with FCRL4 cells. Interestingly, the FCRL4 BMem cells + SRY-box 5 (SOX5) for the FCRL4 BMem cells and rela- expressed CD11c, and most were negative for cell-surface Ϫ Ϫ tively higher RUNX1 expression by FCRL4 BMem cells CD11b, whereas the opposite was true for the FCRL4 BMem ( Fig. 2 B ). The diff erential expression patterns
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