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Expression in Human Keratinocytes in Regulating Cd1d Gene Β C/EBP

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Expression in Human Keratinocytes in Regulating Cd1d Gene Β C/EBP A Central Role for Transcription Factor C/EBP- β in Regulating CD1d Gene Expression in Human Keratinocytes This information is current as Hashmat Sikder, Yuming Zhao, Anna Balato, Andre of October 3, 2021. Chapoval, Rita Fishelevich, Padmaja Gade, Ishwar S. Singh, Dhananjaya V. Kalvakolanu, Peter F. Johnson and Anthony A. Gaspari J Immunol 2009; 183:1657-1666; Prepublished online 10 July 2009; doi: 10.4049/jimmunol.0900057 Downloaded from http://www.jimmunol.org/content/183/3/1657 References This article cites 45 articles, 21 of which you can access for free at: http://www.jimmunol.org/ http://www.jimmunol.org/content/183/3/1657.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists by guest on October 3, 2021 • Fast Publication! 4 weeks from acceptance to publication *average 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 Errata An erratum has been published regarding this article. Please see next page or: /content/183/6/4135.1.full.pdf 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 © 2009 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology A Central Role for Transcription Factor C/EBP-␤ in Regulating CD1d Gene Expression in Human Keratinocytes1 Hashmat Sikder,* Yuming Zhao,* Anna Balato,* Andre Chapoval,† Rita Fishelevich,* Padmaja Gade,‡ Ishwar S. Singh,§ Dhananjaya V. Kalvakolanu,¶ Peter F. Johnson,* and Anthony A. Gaspari2*‡ CD1d is a nonclassical Ag-presenting molecule that presents glycolipid Ags to NKT cells that are involved in immune defense and tumor rejection. It also plays a role in immunoregulatory functions in the epidermis. The mechanisms controlling the expression of CD1d are not well understood. Therefore, we cloned the CD1d gene promoter and characterized its activities in primary human keratinocytes and other cell lines of epithelial origin. We found that a CCAAT box in the CD1d promoter is required for its expression in keratinocytes. We show here that transcription factor C/EBP-␤ binds to the CCAAT box in the CD1d promoter in ␤ vitro and in vivo. Consistent with these observations, deletion of the gene encoding for C/EBP- caused a loss of CD1d expression. Downloaded from The in vivo regulation of CD1d has significant implications for the pathologic mechanisms of certain immunologic skin diseases in which NKT cells play a role, such as allergic contact dermatitis and psoriasis. Together, these data show a central role for C/EBP-␤ in regulating CD1d transcription. The Journal of Immunology, 2009, 183: 1657–1666. uman keratinocytes (KC)3 can influence immune re- Overexpression of CD1d is observed in the epidermal KC of the sponses in the skin through the production of cytokines skin lesions of allergic contact dermatitis (ACD) (17), as well as in http://www.jimmunol.org/ H and by presentation of Ags to T cells (1). Besides MHC psoriatic lesions (4). During allergic reactions to cow’s milk, class I and II that present Ag peptide to CD8 and CD4 T cells, CD1d is overexpressed by cells located in the duodenal lamina respectively (2, 3), KC also express a MHC class I -like, nonpoly- propria (18). Similarly, in primary biliary cirrhosis, epithelial cells morphic Ag-presenting molecule CD1d that presents glycolipids to of the small bile ducts overexpress CD1d (19). Thus, CD1d is NKT cells (4, 5). CD1d is a glycoprotein noncovalently associated overexpressed in allergic, inflammatory, and autoimmune tissue- ␤ with 2-microglobulin and forms a heterodimeric structure similar based pathologies. The presence of infiltrating NKT cells in these to the MHC class I molecules (6–9). This molecule is highly con- tissues raises the possibility that tissue-homing NKT cells play a served across species and is the only member of the group CD1 major role in these varied inflammatory conditions. CD1d expres- molecules functionally present in mice and rats (6). In humans, sion varies significantly among T lymphocytes, monocytes, and by guest on October 3, 2021 there are two subgroups of CD1 genes. Group 1 members include monocyte-derived dendritic cells of different individuals (16). CD1A, CD1B, CD1C, and CD1E, which share homology in their However, the reason for this individual variations in CD1d expres- 5Ј untranslated region (6). Group 2 is constituted by CD1D alone. sion is not clearly understood, but may be related to genetic back- CD1d is expressed centrally in the thymus and by several other ground and/or environmental stimuli. Thus, very little is known peripheral epithelia or stromal cells of the skin, intestine, liver, about the transcriptional control of human CD1d at the tissue level. kidney, pancreas, and uterus (8). CD1d is also expressed by some A previous report (20) demonstrated that the human gene-en- bone marrow-derived cells such as T cells, B cells, monocytes, and coding CD1d molecule (CD1D) has the TATA-less promoter with monocyte-derived dendritic cells (10–13). Human CD1d expres- multiple transcription initiation sites. These sequences were found sion can be up-regulated in the intestinal epithelial cells and KC by to be active in Jurkat and K562 cells (both are immortalized leu- ␥ IFN- (4, 14, 15) and in peripheral blood T cells by mitogens (16). kemia cell lines). The proximal promoter (located within the re- gion of Ϫ106 to ϩ24) was more active in Jurkat cells while the Ϫ Ϫ *Department of Dermatology, †Department of Otolaryngology-Head and Neck Sur- distal promoter (located between 665 to 202) was more active gery, ‡Department of Microbiology and Immunology, and §Department of Internal in K562 cells, indicating a cell type-specific activity of the two Medicine, University of Maryland School of Medicine, Baltimore, MD 21201; and promoters (20). ¶National Cancer Institute, Frederick, MD 21702 In vivo, human epidermal KC have been demonstrated to Received for publication January 9, 2009. Accepted for publication May 20, 2009. express CD1d (5), but there is little understanding of the reg- The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance ulation of this Ag-presenting molecule in the skin. To under- with 18 U.S.C. Section 1734 solely to indicate this fact. stand the mechanism of CD1d gene expression in epidermal 1 This work was supported by Grant R0-1-AR46108-05 (to A.A.G.), CA78282 and KC, we isolated the human CD1d promoter and investigated its CA105005 (to D.V.K.), and the Intramural Research Program of the Center for Can- activity in primary human KC, some KC-derived cell lines, as cer Research, National Cancer Institute (to P.F.J.). well as other cell lines of epithelial origin. We found a signif- 2 Address correspondence and reprint requests to Dr. Peter F. Johnson and Dr. An- thony A. Gaspari, Department of Dermatology, School of Medicine, University of icant stimulatory role for a CCAAT box located in the CD1d Maryland Baltimore, 405 West Redwood Street, 6th floor, Baltimore, MD 21201. proximal promoter, which binds to the C/EBP-␤. In this report, E-mail address: [email protected] we demonstrate that C/EBP-␤ controls CD1d, which in turn 3 Abbreviations used in this paper: KC, keratinocyte; ChIP, chromatin immunopre- plays a role in presenting glycolipids to invariant NKT (iNKT) cipitation; qPCR, quantitative PCR; siRNA, small interfering RNA; ACD, allergic contact dermatitis; RARE, retinoid acid response element; iNKT, invariant NKT; cells. These data have implications for the common inflamma- qRT-PCR, quantitative real-time RT-PCR. tory skin diseases ACD and psoriasis. www.jimmunol.org/cgi/doi/10.4049/jimmunol.0900057 1658 C/EBP-␤ AND CD1d GENE EXPRESSION Materials and Methods bating for 10 min in radioimmunoprecipitation assay buffer containing pro- Cell culture and reagents tease inhibitors (catalog no. 8340; Sigma-Aldrich). Cell lysates were son- icated on ice to shear DNA to lengths between 400 and 600 bp using a Normal human epidermal KC cultures were explanted from neonatal Sonic Dismembrator model 100 (Fisher Scientific). Lysates were sonicated foreskins and were generated as described previously (5) and main- at 50% power for a total of 50 one-second pulses with 20–30 s cooling on tained in EpiLife HKGS medium (Invitrogen). Newly established pri- ice after every 10 pulses. Sonicated cell supernatant was diluted 10-fold in mary KC (two to five passages) cultures were used in all experiments. ChIP Dilution Buffer (ChIP kit, catalog no. 17-295; Upstate Biologicals) Cell lines used in this study were maintained in DMEM supplemented with added protease inhibitors and precleared with protein A-agarose/ with 10% FBS. salmon sperm DNA (Upstate Biologicals) for 30 min at 4°C with agitation. Precleared supernatant fraction was divided equally in three tubes for Promoter constructs cloning and probes C/EBP-␤ Ab (catalog no. sc-150; Santa Cruz Biotechnology), normal rab- bit IgG control, and no Ab control. Five micrograms of the immunopre- A 1762-nt sequence from Ϫ1738 to ϩ24 of the promoter and 5Ј untrans- cipitating Ab or control IgG was added and incubated for4hat4°Cwith lated region of the human CD1D gene was generated by PCR amplification rotation. After 4 h, 30 ␮l of protein G magnetic beads (Active Motif part of human genomic DNA that was isolated from whole blood using a no.
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