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Transcription Inhibition (Homeobox/Paired Box/DNA Binding) GEORGES CHALEPAKIS*, FREDERICK S

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Transcription Inhibition (Homeobox/Paired Box/DNA Binding) GEORGES CHALEPAKIS*, FREDERICK S Proc. Natl. Acad. Sci. USA Vol. 91, pp. 12745-12749, December 1994 Developmental Biology Pax-3 contains domains for transcription activation and transcription inhibition (homeobox/paired box/DNA binding) GEORGES CHALEPAKIS*, FREDERICK S. JONESt, GERALD M. EDELMANt, AND PETER GRUSS*t *Department of Molecular Cell Biology, Max Planck Institute for Biophysical Chemistry, D-37077 Gottingen, Federal Republic of Germany; and tDepartment of Neurobiology, The Scripps Research Institute, La Jolla, CA 92037 Communicated by Mario R. Capecchi, September 19, 1994 (receivedfor review July 11, 1994) ABSTRACT Pax-3 is a member of the Pax family of describe the dissection of the Pax-3 protein functions and transcription factors involved in transcriptional control events ascribe specific functional activities, such as transcription during embryonic development. Here we report a functional inhibition and activation, to discrete domains ofPax-3. When dissection of the Pax-3 protein and describe the protein do- PRSs are inserted in front of a minimal promoter, Pax-3 can mains which are responsible for different activities. A tran- utilize these sequences to modulate the transcription rate of scription inhibition activity is located in the rst 90 N-terminal a linked reporter gene. Lower Pax-3 concentrations activate amino acids and includes part of the paired domain. Further- transcription, whereas higher concentrations inhibit the basal more, the C terminus of Pax-3 is able to confer transcriptional promoter activity in cell culture experiments. These data activation of basal promoters. Pax-3 can utilize both transcrip- suggest that Pax-3 may be a bifunctional transcriptional tion modulating functions and activates transcription over a regulatory protein. narrow range of protein concentration in the presence of promoter elements containing functional binding sites. MATERIALS AND METHODS Pax-3 is expressed early during embryonic development in Recombinant Plasmids. The plasmids RF1-Pax3 and pS1- spatially restricted domains in the nervous system and in Pax3 (15) were the starting plasmids used to generate all some mesodermally derived structures (1). The expression Pax-3 deletion mutants. Numbers in the parentheses refer to pattern ofPax-3 suggests that it plays an important role in the the nucleotide positions on the Pax-3 cDNA (1). The regional specification of certain aspects of the nervous sys- HincII(408)-Xba I, Stu I(442)-Xba I, and Nco I(534)-Xba I tem. Recently, this hypothesis has been confirmed as muta- fragments were blunt-ended and subcloned into the Sac I tions in the Pax-3 gene were found to be responsible for the (blunt-ended with T4 DNA polymerase) site ofpSl-Pax3. The splotch (sp) phenotype in mice (2-5) and the Waardenburg Xba I site of the fragments was always cloned into the Xba syndrome type 1 (WS1) in humans (6-10). Furthermore, a I site of the vector. The BamHI-HindIII fragments of these chromosomal translocation of PAX3 (the human homolog of constructs were then subcloned into the BamHI/HindIII mouse Pax-3; ref. 11) is implicated in the generation of the sites of RF1-Pax3 to create A-Hinc, A-Stu, and A-Nco. pediatric solid tumor alveolar rhabdomyosarcoma (12, 13). BamHI and Cla I(858) restriction digestion of RF1-Pax3, Finally, several Pax gene products, including Pax-3, have treatment with the Klenow fragment of DNA polymerase I, been shown to induce transformation of cells in culture, and and religation led to A-Cla. A-Sma lacks the internal Sma I these Pax-transformed cells can subsequently induce tumors fragment (342-673). The BamHI-Pvu 11(985) and BamHI- in recipient mice (14). Pvu 11(1213) fragments from RF1-Pax3 were subcloned into The Pax-3 protein (479 amino acids long) contains two the BamHI/Sma I sites ofpSl and the resulting BamHI-Xba different DNA-binding domains, a paired domain (PD) and a I fragments were introduced into the BamHI/Xba I sites of paired-type homeodomain (HD). An octapeptide sequence pEVRF1 to generate Pvul-A and Pvu2-A. The BamHI-Pvu motif that is conserved among most PD-containing proteins II(1578) fragment from RF1-Pax3 was subcloned into the is located between the PD and the HD. Pax-3 binds in vitro BamHI/Sma I sites of pSl. The Pax-3 cDNA fragment was to a DNA sequence derived from the Drosophila even then excised by digestion with BamHI and Dra I and sub- skipped promoter (1, 15). This sequence contains an up- cloned into the BamHI/Pvu II(1844) sites of RF1-Pax3 to stream ATTA motifrecognized by the HD and a downstream generate Pvu3-A. A 33-bp DNA fragment from the polylinker paired domain recognition site (PRS), either GTTCC (PRS-1) region of pSl (5'-CTGATCCGTCGACGGTACCCCGGG- or GTTAC (PRS-9), bound by the PD (15). Efficient binding GAATTCGAG-3') was inserted into the HindIII(1065) site in of Pax-3 to the PRS sequences requires the presence of both RF1-Pax3 to introduce 11 amino acids (Leu-Ile-Arg-Arg-Arg- DNA recognition motifs (ATTA and either GTTCC or GT- Tyr-Pro-Gly-Glu-Phe-Glu) between the lysine and leucine in TAC), suggesting a synergistic interaction of the two DNA- the turn of the helix-turn-helix motif of the Pax-3 HD and to binding domains with the PRS sequences. The length of the create Pax3-MHD. Pax3-Moct was constructed by introduc- spacer sequence between the ATTA and GTTCC motifs can ing 9 bp into the Cla I(858) site of RF1-Pax3 (5'- vary considerably without affecting the binding of Pax-3 (16). CGAATTCCC-3'), which then introduces three additional In addition, the space between the PD and the HD (53 amino amino acids (Glu-Phe-Pro) between the isoleucine and aspar- acids) can be shortened without changing the flexibility of tic acid in the Pax-3 octapeptide. The reporter plasmid Pax-3 to interact with the PRS sequences (16). Finally, the 17M2-TK-CAT was kindly provided by P. Chambon (17) and protein region between the PD and the HD was found to the GAL4 expression vector pSG424 was by I. participate in the homodimerization of truncated Pax-3 pro- provided tein products when bound to the DNA (15). In this work, we Abbreviations: PD, paired domain; HD, homeodomain; PRS, paired domain recognition site; sp, splotch; WS, Waardenburg syndrome; The publication costs of this article were defrayed in part by page charge N-CAM, neural cell adhesion molecule; CAT, chloramphenicol payment. This article must therefore be hereby marked "advertisement" acetyltransferase. in accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 12745 Downloaded by guest on September 25, 2021 12746 Developmental Biology: Chalepakis et al. Proc. Natl. Acad. Sci. USA 91 (1994) Sadowski and M. Ptashne (18). The DNA fragments BamHI- A Xba I, BamHI-Cla 1(858), Nco I(489)-Xba I, BamHI-Sma PD HD 1(673), and BamHI-HindIII(1065) were blunt-ended and sub- 33 aaaz c Pax-3 cloned into the T4-polymerase-blunt-ended Sac I site of 3 aap c Pax-6 pSG424 to generate the constructs GAP3-NB, GAP3-NC, 8 aa 13_ 0 Pax-8 GAP3-Nco, GAP3-NS, and GAP3-NH, respectively. GAP3- CP1, GAP3-CP2, and GAP3-CP3 contain Cla I(858)-Pvu 2 aat g0c Pax-l 11(985), Cla I(858)-Pvu 11(1213), and Cla I(858)-Pvu 11(1578) fragments of Pax-3 cDNA blunt-ended by treatment with Klenow fragment in the Sma I site of pSG424, respectively. B The Cla 1(858; Klenow fragment treated)Xba I and the Sma -336 -193 -140 -12 -413 +53 I fragments from RF1-Pax3 were introduced into .......... I(673)-Xba -j -CAT the Sma I/Xba I sites of pSG424 to generate GAP3-CB and GAP3-SB, respectively. The Asp 7181(1499; Klenow treat- ed)-Xba I fragment from RF1-Pax3 subcloned into the Asp 7181/Xba I sites of pSG424 gives rise to GAP3-KB. GAP3-NK was generated by introducing the Bgl II-Kpn C D-t< 1(563) fragment of GAP3-NB into the II/Kpn I sites of Bgl x A co MM0 M P x X L pSG424. GAP3-NK was digested with Stu I(442) and BamHI, C PA t o4 en,g C Mtp X OX AX blunt-ended, and religated to create GAP3-StuK. To generate GAP3-NStu, the plasmid GAP3-NH was digested with Stu 1(442) and Xba I, blunt-ended, and religated. To create the Pax-8.* N-CAM-Sty reporter construct, the Sty I(-414 in the mouse neural cell adhesion molecule (N-CAM) promoter; ref. 19)- Sal I fragment from N-CAM-Pro-CAT (20) was subcloned Pax1-l-p into the Sph I(blunt-ended with T4 polymerase)/Sal I sites of Iod 01 1+3.1 25 the pCAT-Basic vector (Promega) upstream of the chloram- rinductioid 1. 1- 1+3.01ii phenicol acetyltransferase (CAT) gene. Reporter plasmids that contain six direct of the PRSs were constructed repeats '*.Pvu1.A4. : as previously reported (21). Cell Culture and DNA-Binding Experiments. COS-7 and -i -x NIH 3T3 cells were grown in Dulbecco's modified Eagle's medium (DMEM) supplemented with 10% fetal calf serum. NIH 3T3 cells were transfected in 60-mm dishes (approxi- mately 30% confluent) by using the calcium phosphate FIG. 1. Binding of Pax proteins to the N-CAM promoter and method. Calcium phosphate/DNA precipitate was formed in binding-independent transcription inhibition by Pax-3. (A) Schematic linear representation of Pax proteins used in this study. Numbers on a volume of 0.7 ml containing a total of 14 ,g of DNA.
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