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PLAG1, the Main Translocation Target in Pleomorphic Adenoma of the Salivary Glands, Is a Positive Regulator of IGF-II1

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PLAG1, the Main Translocation Target in Pleomorphic Adenoma of the Salivary Glands, Is a Positive Regulator of IGF-II1 [CANCER RESEARCH 60, 106–113, January 1, 2000] PLAG1, the Main Translocation Target in Pleomorphic Adenoma of the Salivary Glands, Is a Positive Regulator of IGF-II1 Marianne L. Voz,2 Nancy S. Agten, Wim J. M. Van de Ven, and Koen Kas Laboratory for Molecular Oncology, Center for Human Genetics, University of Leuven and Flanders Interuniversity Institute for Biotechnology, Herestraat 49, B-3000 Leuven, Belgium ABSTRACT The PLAG1 protein contains seven canonical C2H2 zinc finger domains and a serine-rich COOH terminus that exhibits transactiva- PLAG1, a novel developmentally regulated C H zinc finger gene, is 2 2 tion capacities when fused to the Gal4 DNA binding domain (4), consistently rearranged and overexpressed in pleomorphic adenomas of suggesting that it may act as a transcriptional regulator. the salivary glands with 8q12 translocations. In this report, we show that PLAG1 is a nuclear protein that binds DNA in a specific manner. The To extend our knowledge on the function of the PLAG1 gene and consensus PLAG1 binding site is a bipartite element containing a core the mechanisms by which it causes salivary gland adenomas, we sequence, GRGGC, and a G-cluster, RGGK, separated by seven random decided to further investigate functional characteristics of PLAG1 and nucleotides. DNA binding is mediated mainly via three of the seven zinc in particular its potential transcriptional role. We determined in which fingers, with fingers 6 and 7 interacting with the core and finger 3 with the subcellular compartment PLAG1 exerts its function by immunofluo- G-cluster. In transient transactivation assays, PLAG1 specifically acti- rescence studies; determined whether PLAG1 could bind DNA in a vates transcription from its consensus DNA binding site, indicating that sequence-specific manner and identified its consensus DNA binding PLAG1 is a genuine transcription factor. Potential PLAG1 binding sites site by performing CASTing experiments. The zinc fingers required were found in the promoter 3 of the human insulin-like growth factor II for sequence-specific DNA binding were determined by deletion/ (IGF-II) gene. We show that PLAG1 binds IGF-II promoter 3 and stim- mutation analysis; and we used the PLAG1 consensus was used to ulates its activity. Moreover, IGF-II transcripts derived from the P3 promoter are highly expressed in salivary gland adenomas overexpressing screen the eukaryotic promoter databank. Possible target genes were PLAG1. In contrast, they are not detectable in adenomas without abnor- studied regarding the capacity of PLAG1 to bind and activate their mal PLAG1 expression nor in normal salivary gland tissue. This indicates promoter. Finally, we analyzed the expression of such target genes in a perfect correlation between PLAG1 and IGF-II expression. All of these normal salivary gland tissue and in pleomorphic adenomas with or results strongly suggest that IGF-II is one of the PLAG1 target genes, without PLAG1 overexpression to determine whether these genes providing us with the first clue for understanding the role of PLAG1 in could be PLAG1 targets in salivary gland adenomas. salivary gland tumor development. MATERIALS AND METHODS INTRODUCTION Construction and Production of GST-PLAG1 Fusion Proteins. The 3 Activation of the PLAG1 gene on chromosome 8q12 is the most PLAG1 NH2-terminal region (N2-C244) as well as parts of it (N84-C244; frequent gain-of-function mutation found in pleomorphic adenomas of N101-C244; N159-C244) were fused in-frame to GST by inserting in pGEX- the salivary glands (1, 2). This mainly results from recurrent chromo- 5X-2 (Pharmacia) the DNA fragments obtained by the PCR with full-length somal translocations that lead to promoter substitution between PLAG1 cDNA as template. The NH2-terminal oligonucleotides used to gen- Ј PLAG1, a gene mainly expressed in fetal tissue, and more broadly erate the various constructs were: G8N2, 5 -CCCGAATTCTGGCCACTGT- CATTCCTGGT-3Ј; G8N84, 5Ј-CCCGAATTCTGGCTACTCATTCTCCT- expressed genes. The three translocation partners characterized thus Ј Ј Ј ␤ GAGA-3 ; G8N101, 5 -CCCGAATTCTGTTTCACCGGAAAGATCATC-3 ; far are the -catenin gene on 3p21 found in the most common G8N159, 5Ј-CCCGAATTCCTTTTGAAAGCACGGGAGTG-3Ј; and as translocation, the t(3;8)(p21;q12), the leukemia inhibitory factor re- COOH-terminal oligonucleotide G8C244, 5Ј-GGGCTCGAGCTATTTGAC- ceptor gene on 5p13 found in a recurrent (5;8)(p13;q12) translocation CTTCAGAAGCTCTTGA-3Ј. Pfu-amplified fragments were gel purified, di- (2), and the elongation factor SII gene (3). Breakpoints invariably gested with EcoRI and XhoI, and ligated in the EcoRI-XhoI-digested pGEX- occur in the 5Ј noncoding part of the PLAG1 gene, leading to an 5X-2 vector. The construct GST-PLAG1 (N2-C203) was obtained by digesting exchange of the regulatory control elements while preserving PLAG1 GST-PLAG1 (N2-C244) by DraIII and XhoI, blunt ending, and recirculariza- coding sequence. The replacement of the PLAG1 promoter, inactive in tion. All of the fusion proteins were expressed in Escherichia coli BL-21 cells adult salivary glands, by a strong promoter derived from the translo- and purified on Glutathione Sepharose 4B (Pharmacia) according to the cation partner, leads to ectopic expression of PLAG1 in the tumoral manufacturer’s protocol. The protein sizes were estimated by SDS-PAGE, followed by Coomassie blue staining; concentrations were determined by cells. This abnormal PLAG1 expression presumably results in a comparison to a well-defined concentration marker. deregulation of PLAG1 target genes, causing salivary gland tumori- CASTing. To prepare a pool of random double-strand oligomers for the genesis. first round of CASTing, 400 pmol of CAST25 (5Ј-CTGTCGGAATTCGCT- GACGT-(N)25-CGTCTTATCGGATCCTACGT-3Ј) were incubated in 100 ␮l Received 7/20/99; accepted 10/28/99. of polymerase reaction buffer containing 1200 pmol of CAST-LOW (5Ј- The costs of publication of this article were defrayed in part by the payment of page ACGTAGGATCCGATAAGACG-3Ј), 200 ␮M of each deoxynucleoside charges. This article must therefore be hereby marked advertisement in accordance with triphosphate, 2.5 ␮l[␣-32P]dCTP (DuPont NEN), and 10 units of Amplitaq 18 U.S.C. Section 1734 solely to indicate this fact. 1 This work was supported by the “Geconcerteerde Onderzoekacties 1997–2001” and (Perkin-Elmer-Cetus) and treated as follows: 5 min at 94°C, 20 min at 65°C, the “Fonds voor Wetenschappelijk Onderzoek Vlaanderen” (FWO). M. V. is a post-doc of and 20 min at 72°C. Fifty ␮l were incubated with 500 ng of GST-PLAG1 the Flanders Interuniversity Institute for Biotechnology. K. K. is a post-doc of the FWO. (N2-C244) bound to Glutathione Sepharose beads, 50 ␮g of poly polydeoscyi- 2 To whom requests for reprints should be addressed, at Laboratory for Molecular nosinic-deoscycytidylic acid (Sigma), and 50 ␮g of BSA in 500 ␮l of binding Oncology, Center for Human Genetics, University of Leuven and Flanders Interuniversity ␮ Institute for Biotechnology, Herestraat 49, B-3000 Leuven, Belgium. Phone: 32-16- buffer [10 mM Tris (pH 7.5), 200 mM NaCl, 50 M ZnCl2, 10% glycerol, 1 mM 346041; Fax: 32-16-346073; E-mail: [email protected]. MgCl2,and1mM DTT]. After a 30-min incubation on a rotator at room 3 The abbreviations used are: PLAG1, pleomorphic adenoma gene 1; CASTing, cyclic temperature the beads were washed four times with cold binding buffer, and amplification and selection of target sequences; GST, glutathione S-transferase; EMSA, the radioactivity still present on the beads was counted to monitor the level of electrophoretic mobility shift assay; ATCC, American Type Culture Collection; PDGF, platelet-derived growth factor; EPD, Eukaryotic Promoter Databank; IGF, insulin-like enrichment in each step. The oligonucleotides were eluted from the beads by growth factor. resuspending in 100 ␮l of water, followed by phenol extraction and ethanol 106 Downloaded from cancerres.aacrjournals.org on September 27, 2021. © 2000 American Association for Cancer Research. TRANSCRIPTIONAL REGULATION OF IGF-II BY PLAG1 precipitation. An aliquot was used for the subsequent amplification reaction in have been obtained by inserting into pTK81luc (12) six copies of 100 ␮l of polymerase reaction buffer containing 200 pmol of each amplimer the corresponding ds oligonucleotides: WT, 5Ј-CTAGAAGGGGCTCTA- CAST-UP (5Ј-CTGTCGGAATTCGCTGACG-3Ј) and CAST-LOW, 200 ␮M GAAAGGGTAA-3Ј; mCO, 5Ј-CTAGAATGCACTCTAGAAAGGGTAA-3Ј; deoxynucleotide triphosphates, and 2.5 units of Amplitaq (Perkin-Elmer Ce- mCLU, 5Ј-CTAGAAGGGGCTCTAGAAA-TACTAA-3Ј; and mCOmCLU, tus) with 1 ␮lof[␣-32P]-dCTP (DuPont NEN) with 25 cycles of 1 min at 94°C, 5Ј-CTAGAATGCACTCTAGAAATACTAA-3Ј. 1 min at 65°C, and 1 min at 72°C. The amplified products were subsequently Transfections and Luciferase Assay. The human fetal kidney epithelial used for a second round of selection performed as described above. After four cell line 293 (ATCC; CRL 1573) was cultured according to the suppliers’ rounds of selection, the subsequent three steps of selection were performed by protocols. Cells (6-well plates) were transiently cotransfected in triplicate with EMSA with 100 ng of eluted GST-PLAG1 (N2-C244). After X-ray exposure 200 ng of the expression vector DNA, 200 ng of reporter plasmid, and 200 ng of the dried gel, the shifted bands were cut out of the gel, and the double- of internal control Rous sarcoma virus ␤-galactosidase DNA using 3 ␮lof stranded DNA was eluted3hat50°C in 200 ␮l of polymerase reaction buffer. FuGENE 6 Transfection Reagent (Boehringer Mannheim) according to the An aliquot of the eluate was used for amplification. After a total of seven manufacturer’s protocol. Cells were harvested 40 h after the transfection, and amplification cycles, the oligonucleotides were cloned into the pGEM-T Easy luciferase reporter enzyme activity was measured using a Monolight 2010 vector according to the manufacturer’s protocol (Promega), and 23 indepen- luminometer (Analytical Luminiscence Laboratory) and performing end point dent clones were sequenced. assays. EMSA. The different probes were synthesized as complementary oligonu- Preparation of RNA and Northern Blot Analysis.
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