Expression, Activity, and Subcellular Localization of the Yin Yang 1 Transcription Factor in Xenopus Oocytes and Embryos

Yin Yang 1 (YY1) is a multifunctional transcription factor that acts as an activator, repressor, or initiator of transcription of numerous cellular and viral genes. Previous studies in tissue culture model systems suggest YY1 plays a role in development and differentiation in multiple cell types, but the biological role of YY1 in vertebrate oocytes and embryos is not well understood. Here we analyzed expression, activity, and subcellular localization profiles of YY1 during Xenopus laevis development. Abundant levels of YY1 mRNA and protein were detected in early stage oocytes and in all subsequent stages of oocyte and embryonic development through to swimming larval stages. The DNA binding activity of YY1 was detected only in early oocytes (stages I and II) and in embryos after the midblastula transition (MBT), which suggested that its potential to modulate gene expression may be specifically repressed in the intervening period of development. Experiments to determine transcriptional activity showed that addition of YY1 recognition sites upstream of the thymidine kinase promoter had no stimulatory or repressive effect on basal transcription in oocytes and post-MBT embryos. Although the apparent transcriptional inactivity of YY1 in oocytes could be explained by the absence of DNA binding activity at this stage of development, the lack of transcriptional activity in post-MBT embryos was not expected given the ability of YY1 to bind its recognition elements. Subsequent Western blot and immunocytochemical analyses showed that YY1 is localized in the cytoplasm in oocytes and in cells of developing embryos well past the MBT. These findings suggest a novel mode of YY1 regulation during early development in which the potential transcriptional function of the maternally expressed factor is repressed by cytoplasmic localization. Yin Yang 1 (YY1) is a multifunctional transcription factor that acts as an activator, repressor, or initiator of transcription of numerous cellular and viral genes. Previous studies in tissue culture model systems suggest YY1 plays a role in development and differentiation in multiple cell types, but the biological role of YY1 in vertebrate oocytes and embryos is not well understood. Here we analyzed expression, activity, and subcellular localization profiles of YY1 during Xenopus laevis development. Abundant levels of YY1 mRNA and protein were detected in early stage oocytes and in all subsequent stages of oocyte and embryonic development through to swimming larval stages. The DNA binding activity of YY1 was detected only in early oocytes (stages I and II) and in embryos after the midblastula transition (MBT), which suggested that its potential to modulate gene expression may be specifically repressed in the intervening period of development. Experiments to determine transcriptional activity showed that addition of YY1 recognition sites upstream of the thymidine kinase promoter had no stimulatory or repressive effect on basal transcription in oocytes and post-MBT embryos. Although the apparent transcriptional inactivity of YY1 in oocytes could be explained by the absence of DNA binding activity at this stage of development, the lack of transcriptional activity in post-MBT embryos was not expected given the ability of YY1 to bind its recognition elements. Subsequent Western blot and immunocytochemical analyses showed that YY1 is localized in the cytoplasm in oocytes and in cells of developing embryos well past the MBT. These findings suggest a novel mode of YY1 regulation during early development in which the potential transcriptional function of the maternally expressed factor is repressed by cytoplasmic localization. Yin Yang 1 amino acid thymidine kinase midblastula transition polymerase chain reaction Chinese hamster ovary chloramphenicol acetyltransferase proliferating cell nuclear antigen CCAAT box transcription factor Yin Yang 1 (YY11; previously referred to as FIII, NF-E1, δ, F-ACT1, CF1, or UCRBP) is a GLI-Kruppel family transcription factor that functions either as a repressor, activator, or initiator of transcription (reviewed in Ref.1Galvin K.M. Shi Y. Mol. Cell. Biol. 1997; 17: 3723-3732Crossref PubMed Scopus (162) Google Scholar). It is expressed in a wide variety of different cell types and shows a high degree of sequence similarity among divergent organisms (2Shi Y. Seto E. Chang L.S. Shenk T. Cell. 1991; 67: 377-388Abstract Full Text PDF PubMed Scopus (873) Google Scholar, 3Flanagan J.R. Becker K.G. Ennist D.L. Gleason S.L. Driggers P.H. Levi B.Z. Appella E. Ozato K. Mol. Cell. Biol. 1992; 12: 38-44Crossref PubMed Scopus (236) Google Scholar, 4Pisaneschi G. Ceccotti S. Falchetti M.L. Fiumicino S. Carnevali F. Beccari E. Biochem. Biophys. Res. Commun. 1994; 205: 1236-1242Crossref PubMed Scopus (37) Google Scholar, 5Eliassen K.A. Baldwin A. Sikorski E.M. Hurt M.M. Mol. Cell. Biol. 1998; 18: 7106-7118Crossref PubMed Scopus (49) Google Scholar). The mammalian YY1 protein (414 aa) contains four C-terminal zinc fingers, an N-terminal bipartite transcriptional activation domain, and a number of domains that function to mediate interactions with other proteins (6Bushmeyer S. Park K. Atchison M.L. J. Biol. Chem. 1995; 270: 30213-30220Abstract Full Text Full Text PDF PubMed Scopus (125) Google Scholar). The Xenopus YY1 cDNA is highly conserved, but the predicted protein is somewhat smaller at 373 aa (4Pisaneschi G. Ceccotti S. Falchetti M.L. Fiumicino S. Carnevali F. Beccari E. Biochem. Biophys. Res. Commun. 1994; 205: 1236-1242Crossref PubMed Scopus (37) Google Scholar). Numerous studies have revealed that YY1 is subject to complex regulatory mechanisms in different cell types. The emerging picture is that the functional diversity of YY1 as an activator, repressor, or initiator of transcription is context-specific and is modulated by interactions with various cellular factors and adaptor proteins. YY1 has been shown to interact physically with a number of proteins including c-Myc (7Shrivastava A. Saleque S. Kalpana G.V. Artandi S. Goff S.P. Calame K. Science. 1993; 262: 1889-1892Crossref PubMed Scopus (237) Google Scholar, 8Shrivastava A., Yu, J. Artandi S. Calame K. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 10638-10641Crossref PubMed Scopus (69) Google Scholar), p300/CBP (9Lee J.S. See R.H. Galvin K.M. Wang J. Shi Y. Nucleic Acids Res. 1995; 23: 925-931Crossref PubMed Scopus (78) Google Scholar), CREB (10O'Connor M.J. Tan S.H. Tan C.H. Bernard H.U. J. Virol. 1996; 70: 6529-6539Crossref PubMed Google Scholar), ATF/CBP (11Zhou Q. Engel D.A. J. Virol. 1995; 69: 7402-7409Crossref PubMed Google Scholar), poly(A)DP-ribosyl transferase (12Oei S.L. Griesenbeck J. Schweiger M. Babich V. Kropotov A. Tomilin N. Biochem. Biophys. Res. Commun. 1997; 240: 108-111Crossref PubMed Scopus (93) Google Scholar), histone deacetylase (13Yang W.M. Inouye C. Zeng Y. Bearss D. Seto E. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 12845-12850Crossref PubMed Scopus (489) Google Scholar), the E1A oncoprotein (2Shi Y. Seto E. Chang L.S. Shenk T. Cell. 1991; 67: 377-388Abstract Full Text PDF PubMed Scopus (873) Google Scholar), and a number of general transcription factors (14Austen M. Cerni C. Henriksson M. Hilfenhaus S. Luscher-Firzlaff J.M. Menkel A. Seelos C. Sommer A. Luscher B. Curr. Top. Microbiol. Immunol. 1997; 224: 123-130PubMed Google Scholar,15Adrian G.S. Seto E. Fischbach K.S. Rivera E.V. Adrian E.K. Herbert D.C. Walter C.A. Weaker F.J. Bowman B.H. J. Gerontol. A Biol. Sci. Med. Sci. 1996; 51: B66-B75Crossref PubMed Scopus (48) Google Scholar). A variety of tissue culture studies have shown that YY1 controls expression of developmentally regulated genes, and so it is thought to play important roles in development and differentiation (reviewed in Ref. 1Galvin K.M. Shi Y. Mol. Cell. Biol. 1997; 17: 3723-3732Crossref PubMed Scopus (162) Google Scholar). Recognition sites for YY1 have been identified in the regulatory regions of transferring (15Adrian G.S. Seto E. Fischbach K.S. Rivera E.V. Adrian E.K. Herbert D.C. Walter C.A. Weaker F.J. Bowman B.H. J. Gerontol. A Biol. Sci. Med. Sci. 1996; 51: B66-B75Crossref PubMed Scopus (48) Google Scholar), dystrophin (16Galvagni F. Cartocci E. Oliviero S. J. Biol. Chem. 1998; 273: 33708-33713Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar), and actin (17Lee T.C. Shi Y. Schwartz R.J. Proc. Natl. Acad. Sci. U. S. A. 1992; 89: 9814-9818Crossref PubMed Scopus (198) Google Scholar, 18Lee T.C. Zhang Y. Schwartz R.J. Oncogene. 1994; 9: 1047-1052PubMed Google Scholar, 19MacLellan W.R. Lee T.C. Schwartz R.J. Schneider M.D. J. Biol. Chem. 1994; 269: 16754-16760Abstract Full Text PDF PubMed Google Scholar, 20Patten M. Hartogensis W.E. Long C.S. J. Biol. Chem. 1996; 271: 21134-21141Abstract Full Text Full Text PDF PubMed Scopus (54) Google Scholar, 21Chen C.Y. Schwartz R.J. Mol. Endocrinol. 1997; 11: 812-822PubMed Google Scholar, 22Martin K.A. Gualberto A. Kolman M.F. Lowry J. Walsh K. DNA Cell Biol. 1997; 16: 653-661Crossref PubMed Scopus (25) Google Scholar, 23Walowitz J.L. Bradley M.E. Chen S. Lee T. J. Biol. Chem. 1998; 273: 6656-6661Abstract Full Text Full Text PDF PubMed Scopus (75) Google Scholar) genes expressed in differentiating and aging muscle, fetal and embryonic globin genes (24Gumucio D.L. Shelton D.A. Bailey W.J. Slightom J.L. Goodman M. Proc. Natl. Acad. Sci. U. S. A. 1993; 90: 6018-6022Crossref PubMed Scopus (86) Google Scholar, 25Peters B. Merezhinskaya N. Diffley J.F. J. Biol. Chem. 1993; Full Text PDF PubMed Google Scholar, N. C.H. J. P.H. G. J. 1995; PubMed Scopus Google Scholar, C. M. T. E. N. Goodman M. D.L. 93: PubMed Google Scholar), the gene expressed in cells K. Atchison M.L. Proc. Natl. Acad. Sci. U. S. A. 1991; PubMed Scopus Google Scholar), and the gene B. J. Med. PubMed Scopus (48) Google Scholar). YY1 to the regulation of the gene in Engel K. Biochem. Biophys. Res. Commun. PubMed Scopus Google Scholar) and to the gene in B. F. B. G.S. J.L. Proc. Natl. Acad. Sci. U. S. A. 1997; PubMed Scopus Google Scholar). the activity of YY1 to be by to the and nuclear B. J. S. J.L. G.S. Proc. Natl. Acad. Sci. U. S. A. 1995; PubMed Scopus Google Scholar, S. B. J.L. S. Seto E. Atchison M.L. S. G.S. J. Cell. Biochem. 1998; PubMed Scopus Google Scholar). developing muscle, of YY1 is thought to be for of genes J.L. Bradley M.E. Chen S. Lee T. J. Biol. Chem. 1998; 273: 6656-6661Abstract Full Text Full Text PDF PubMed Scopus (75) Google Scholar). its apparent with cell and differentiation in cell types, is the expression and regulation of YY1 in vertebrate oocytes and and the biological role of YY1 during early vertebrate development is understood. A of YY1 in development revealed that it is expressed in oocytes and early a of subcellular localization in early development, and is expressed in in development M.E. Zhang J. E. Shi Y. Mol. Cell. Biol. PubMed Scopus Google Scholar). of YY1 in the in and and embryonic it that YY1 functions at multiple stages of development M.E. Zhang J. E. Shi Y. Mol. Cell. Biol. PubMed Scopus Google Scholar). The of the was to and YY1 in the Xenopus model that YY1 mRNA and protein were expressed in early oocytes and were at levels oocyte and embryonic development. The ability of YY1 to interact with its was to early oocytes and to post-MBT stages in that the DNA binding activity of the factor is specifically during development. showed that YY1 had no effect on transcription the thymidine kinase promoter in but we a lack of transcriptional activity in post-MBT embryos at a in development its DNA binding is of the subcellular localization of YY1 showed it is in the cytoplasm of oocytes and in cells the to as as the stage of development. suggest that cytoplasmic is a mode of regulation to the transcriptional activity of YY1 during early stages of Xenopus development and that YY1 functions in cell differentiation that in development. Xenopus were Xenopus I were and cells were by in 1 1 1 for were in 1 J. PubMed Scopus Google Scholar) to or of cell expression of YY1 in of in mRNA was the and oocytes were for to of protein YY1 mRNA (4Pisaneschi G. Ceccotti S. Falchetti M.L. Fiumicino S. Carnevali F. Beccari E. Biochem. Biophys. Res. Commun. 1994; 205: 1236-1242Crossref PubMed Scopus (37) Google Scholar) was a E. were as in A. Hurt M.M. N. Biol. 1997; PubMed Scopus Google Scholar). protein oocytes or embryos were in of and A. Hurt M.M. N. Biol. 1997; PubMed Scopus Google Scholar), cell was for at and the were in and in or stage and oocytes were and in a of protein oocytes at stages and were in stages and in and stages I and in 1 and cytoplasmic of embryos were as by J. S. M. Mol. Cell. Biol. 1995; PubMed Scopus Google Scholar). protein cells were in and by in a and The was at in and were at nuclear were as previously K. M. U. Cell. Full Text PDF PubMed Scopus Google Scholar). were and in a 1 and a were and for at in a were in nuclear 1 1 with for and with a were at in a were in nuclear and to were oocytes or embryos as D.A. Cell. 18: Full Text PDF PubMed Scopus Google Scholar), by in A K. The was at for 1 and with an of and were by after the addition of and of were in of 1 DNA of was and the was at The was at for in and as DNA was by after the addition of of to were as previously N. Biol. PubMed Scopus Google Scholar). were at and at in The was the cDNA of the Xenopus YY1 mRNA (4Pisaneschi G. Ceccotti S. Falchetti M.L. Fiumicino S. Carnevali F. Beccari E. Biochem. Biophys. Res. Commun. 1994; 205: 1236-1242Crossref PubMed Scopus (37) Google Scholar) DNA binding embryonic or stages and oocyte 1 or oocyte for early stage oocyte oocyte of stage an and oocyte of the stage I and The YY1 recognition the was with with the of DNA polymerase The sequence of is binding reaction of of protein of 1 and were on for and 1 were for at and were and to cells were in with fetal as previously S. Biochem. Cell Biol. PubMed Scopus Google Scholar). Chinese hamster ovary cells were in with and were as previously K.A. Baldwin A. Sikorski E.M. Hurt M.M. Mol. Cell. Biol. 1998; 18: 7106-7118Crossref PubMed Scopus (49) Google Scholar). for cells were with the as in the and for expression in oocytes were as previously A. S. N. Mol. Cell. Biol. 1998; 18: PubMed Scopus Google Scholar). cell were to of at were to with and proteins were with a of at and of was to the and were were by with in and to at for and were with and at embryos and at in were by in at were by in and were in and at and were to and were on and at were and by in a of and for in 1 and in at subsequent were at were for in 1 and were to at a of in for 1 were YY1 and proliferating cell nuclear antigen were with were in in and to for of YY1 were and for were in 1 and in 1 in for 1 with and in 1 in for and with were in in and of a we a DNA binding activity in Xenopus embryos to the of histone genes, but the proteins in were not identified A. Hurt M.M. N. Biol. 1997; PubMed Scopus Google Scholar). a of a cell cDNA that the protein with the histone regulatory sequence in mammalian cells was YY1 K.A. Baldwin A. Sikorski E.M. Hurt M.M. Mol. Cell. Biol. 1998; 18: 7106-7118Crossref PubMed Scopus (49) Google Scholar). the of we the which contains the YY1 in with recognition in The addition of YY1 to binding with cell the Xenopus cell or stage embryos the YY1 and were with nuclear The were not by YY1 and of the YY1 complex was not in controls other proteins. it that YY1 to and the of the cell The cell for were analyzed on Western YY1 The amino acid sequence with for is the and A protein at was detected in cells and stage embryos and a at was detected in of in mRNA Xenopus YY1 oocytes in an of the 1 that the mammalian detected the protein in Western The of the and YY1 on the blot predicted the number of amino and has been for the which as a protein its predicted is this is thought to be to protein K.M. Shi Y. Mol. Cell. Biol. 1997; 17: 3723-3732Crossref PubMed Scopus (162) Google Scholar). The protein expressed in embryos and cells of Xenopus was smaller mammalian this is with the predicted protein of 373 aa for Xenopus (4Pisaneschi G. Ceccotti S. Falchetti M.L. Fiumicino S. Carnevali F. Beccari E. Biochem. Biophys. Res. Commun. 1994; 205: 1236-1242Crossref PubMed Scopus (37) Google Scholar) aa for (2Shi Y. Seto E. Chang L.S. Shenk T. Cell. 1991; 67: 377-388Abstract Full Text PDF PubMed Scopus (873) Google Scholar, 5Eliassen K.A. Baldwin A. Sikorski E.M. Hurt M.M. Mol. Cell. Biol. 1998; 18: 7106-7118Crossref PubMed Scopus (49) Google Scholar). analyzed the YY1 factor by of cell on Cell were and in a The of YY1 binding activity at 1 Western blot of the YY1 showed that the in the DNA binding The the of the YY1 and shown in 1 as well as the of 1 the of the YY1 transcription factor in Xenopus YY1 was detected in at but was no It is that for DNA binding were not in the or it could be that the Western blot of YY1 protein is of activity in Previous of YY1 as an important factor in cell and differentiation to the of YY1 mRNA during oocyte and embryonic development. were on oocytes and embryos at various stages of development A mRNA was detected with the YY1 cDNA A of YY1 mRNA was detected in early and stage in and early and in swimming the not midblastula stage J. M. Cell. Full Text PDF PubMed Scopus Google Scholar), it that transcription of the maternally YY1 gene early during and YY1 through and early embryonic development. The YY1 mRNA detected in the the of to we for of the YY1 in and The YY1 mRNA was detected in mRNA but not in the the of YY1 protein expression during development. the Western shown in were to YY1 in cell of oocytes and embryos. A at was detected in and in developing embryos early through to stages. with the of mRNA expression, were no in the of YY1 protein detected of development. expression of YY1 during and through oocyte and the Western blot to YY1 in and early embryos is shown in C. of the YY1 were in stage in and at in early YY1 to be smaller at A at stage of showed that YY1 was a protein in early but by stage the of YY1 at the of YY1 DNA binding activity during development, cell were and embryos and analyzed in the with the YY1 recognition sequence The YY1 complex was detected in stage I and stage oocytes and in embryos after the but it was in the intervening stages. The addition of YY1 to the of YY1 in in The activity of other transcription factors to be through this period of development S. S. A. A. N. Biol. 1997; PubMed Scopus Google Scholar), and the DNA binding activity of transcription factor is in the the in YY1 DNA binding activity through early development were not to in the levels of the were in the Western in which of YY1 were of is that DNA binding activity was in oocytes at stages and so not to be a DNA binding activity and the in to that stages and Previous studies have that the of YY1 its DNA binding activity K.A. Baldwin A. Sikorski E.M. Hurt M.M. Mol. Cell. Biol. 1998; 18: 7106-7118Crossref PubMed Scopus (49) Google Scholar). YY1 during development. of stage in a of DNA binding that YY1 in the and that the DNA binding activity of YY1 be regulated by during oocyte development. the that the in the apparent of YY1 in stage oocytes could be to Western YY1 was detected at in and the in apparent of YY1 at stage is not to the transcriptional activity of YY1 a of the thymidine kinase promoter to YY1 binding either YY1 in or upstream of the of a YY1 binding or a YY1 binding the histone sequence expression was analyzed in embryos that were to to stage at past of YY1 not or activity the promoter in post-MBT embryos. numerous of this were no in activity to we that YY1 was to transcription in of the promoter YY1 a activation the basal that to in Xenopus it that YY1 is in post-MBT embryos. were in expression with stage oocytes not which was expected given the of YY1 DNA binding activity at stages of oocyte development findings in with previously the YY1 binding and protein genes not transcription in E. G. Beccari E. Biochem. 1998; PubMed Scopus Google Scholar). It was shown that YY1 is localized in the cytoplasm of oocytes and a of subcellular localization in M.E. Zhang J. E. Shi Y. Mol. Cell. Biol. PubMed Scopus Google Scholar). determine the subcellular of YY1 during we oocytes and analyzed nuclear and cytoplasmic for the of YY1 by Western stages and YY1 was detected in the cytoplasm but was in nuclear that YY1 is cytoplasmic in stage oocytes and that the in to which stage and stage is not with nuclear for DNA binding activity in cytoplasmic and nuclear Although YY1 not bind DNA in stage activity was by in as in B. of subcellular stage and oocytes revealed that YY1 DNA binding could be in cytoplasmic but not in nuclear controls showed that were specifically by YY1 These the findings of Western that YY1 is in the cytoplasm in stage and The DNA binding activity of YY1 is in stage I and after to a DNA binding and nuclear localization during binding be with nuclear localization. that YY1 be a nuclear protein in early to the cytoplasm in stage cytoplasmic in the during and early and after MBT. this we an immunocytochemical of developing oocytes and embryos the YY1 as for Western and a we an which in nuclear in all controls were in which were to oocyte and embryonic for of not a YY1 was to we had high levels of DNA binding activity in nuclear A was detected in but YY1 to be localized in the cytoplasm in early and stage A cytoplasmic was in cells of developing embryos. YY1 not in the of stage in stage embryos past the in stage embryos at a in development past the of The that YY1 DNA binding activity after the but to cytoplasmic was and this and to the of we for the of YY1 in nuclear and cytoplasmic stage embryos. The Western shown in that YY1 was a blot the the antigen was detected only in nuclear and cell it that YY1 in the cytoplasm during early embryonic development and not to early gene this we have that YY1 is a maternally protein that is early YY1 is expressed in early oocytes as a cytoplasmic protein in oocytes and early and its DNA binding activity is to early oocytes and to post-MBT embryos. the of DNA binding to that YY1 function to modulate expression of genes in stage I oocytes and after expression the in the J. M. Cell. Full Text PDF PubMed Scopus Google Scholar). we that YY1 binding sites had no effect on expression the promoter in oocytes or in post-MBT and so we that YY1 is during early development. The transcriptional inactivity of YY1 is with that YY1 in the cytoplasm of oocytes and in cells the developing well past MBT. we suggest that the potential function of YY1 as a transcriptional is specifically repressed by cytoplasmic during and early embryonic development. YY1 is a maternally expressed protein in oocytes in M.E. Zhang J. E. Shi Y. Mol. Cell. Biol. PubMed Scopus Google Scholar) and the subcellular localization of YY1 in Xenopus is somewhat different that in development. M.E. Zhang J. E. Shi Y. Mol. Cell. Biol. PubMed Scopus Google Scholar) showed that YY1 is cytoplasmic in oocytes and nuclear in embryos with the of and suggested that YY1 functions to gene expression early in mammalian embryonic development. nuclear in Xenopus embryos at the apparent of its DNA binding activity at this embryos in which YY1 nuclear at the stage with the of is no apparent nuclear localization and the it that YY1 not have a transcriptional regulatory function at the stages of gene expression in Xenopus embryos or in early development to the The expression and subcellular localization in this suggest for the potential function of YY1 may function to the transcription of genes important for differentiation and which in development. has been suggested by numerous studies in various tissue culture model systems K.M. Shi Y. Mol. Cell. Biol. 1997; 17: 3723-3732Crossref PubMed Scopus (162) Google Scholar) and is with the expression of YY1 in embryos and the of YY1 M.E. Zhang J. E. Shi Y. Mol. Cell. Biol. PubMed Scopus Google Scholar). YY1 may play an important role in the cytoplasm during and early in the or regulation of a cytoplasmic function be to that for the CCAAT box transcription factor which is in the cytoplasm to through its binding and is with J. C. S. G. T. M. G. M. M. J. PubMed Scopus Google Scholar). of is with of J. C. S. G. T. M. G. M. M. J. PubMed Scopus Google Scholar). YY1 not to the after which suggest that it with analyses be at YY1 has binding activity and with to its cytoplasmic localization. It is that YY1 in the cytoplasm and the ability to bind DNA through development, with activity in early oocytes and in post-MBT embryos. it is that the DNA binding at we suggest that maternally YY1 is subject to that in the It could be that YY1 to transcription but the cellular to nuclear in during in development. is for in the DNA binding activity of YY1 during was no apparent nuclear localization and the ability of YY1 to bind DNA in DNA binding is not regulated by subcellular YY1 was in the cytoplasm the which YY1 and The ability to DNA binding activity in stage oocytes by in that YY1 may be by we no that the of YY1 as oocytes through stages DNA binding activity is or and so the and mode of in DNA binding during early development the suggest that the potential transcriptional activity of YY1 is repressed specifically during oocyte and embryonic development by to the The functional of in the DNA binding activity of YY1 is and the potential role of YY1 the cytoplasm during development to be of YY1 during early development the of expression analyses in which YY1 binding sites had stimulatory repressive on basal transcription the promoter in oocytes and embryos. for and for with of

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