Abstract
Proper functions of Zic proteins are essential for animals in health and disease. Here, we summarize our current understanding of the molecular properties and functions of the Zic family across animal species and paralog subtypes. Zics are basic proteins with some posttranslational modifications and can move to the cell nucleus via importin- and CRM1-based nucleocytoplasmic shuttling mechanisms. Degradation is mediated by the ubiquitin proteasome system. Many Zic proteins are capable of binding to two types of target DNA sequences (CTGCTG-core-type and GC-stretch-type). Recent chromatin immunoprecipitation assays showed that CTGCTG-core-type target sequences are enriched in enhancers. Nonetheless, the DNA binding is not always required for transcriptional regulation by Zic proteins. On the other hand, Zic proteins bind many proteins including transcription factors (Gli1–3, Tcf1 or Tcf4, Smad2 or Smad3, Oct4, Pax3, Cdx, and SRF), chromatin-remodeling factors (NuRD and NURF), and other nuclear enzymes (DNA-PK, PARP1, and RNA helicase A). Zic family–mediated gene expression control involves both their actions near the transcription start site and those affecting the global gene expression via binding to enhancers. Although Zic proteins perform essential functions in transcriptional regulation of Oct4 and Nanog expression via their promoters, recent genome-wide analyses of the Zic-binding sites and their downstream targets indicate that Zic proteins are associated with distant regulatory elements and are the critical enhancer-priming nuclear regulators in organismal development. Chromatin-remodeling complexes such as NuRD and NURF that interact with Zic proteins have been shown to participate in Zic-mediated enhancer regulation.
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References
Aruga J, Yokota N, Hashimoto M, Furuichi T, Fukuda M, Mikoshiba K (1994) A novel zinc finger protein, zic, is involved in neurogenesis, especially in the cell lineage of cerebellar granule cells. J Neurochem 63(5):1880–1890
Aruga J, Mizugishi K, Koseki H, Imai K, Balling R, Noda T, Mikoshiba K (1999) Zic1 regulates the patterning of vertebral arches in cooperation with Gli3. Mech Dev 89(1–2):141–150
Badis G, Berger MF, Philippakis AA, Talukder S, Gehrke AR, Jaeger SA, Chan ET, Metzler G, Vedenko A, Chen X, Kuznetsov H, Wang CF, Coburn D, Newburger DE, Morris Q, Hughes TR, Bulyk ML (2009) Diversity and complexity in DNA recognition by transcription factors. Science 324(5935):1720–1723. https://doi.org/10.1126/science.1162327
Bae CJ, Park BY, Lee YH, Tobias JW, Hong CS, Saint-Jeannet JP (2014) Identification of Pax3 and Zic1 targets in the developing neural crest. Dev Biol 386(2):473–483. https://doi.org/10.1016/j.ydbio.2013.12.011
Bagutti C, Forro G, Ferralli J, Rubin B, Chiquet-Ehrismann R (2003) The intracellular domain of teneurin-2 has a nuclear function and represses zic-1-mediated transcription. J Cell Sci 116(Pt 14):2957–2966. https://doi.org/10.1242/jcs.00603
Baumgartner S, Martin D, Hagios C, Chiquet-Ehrismann R (1994) Tenm, a Drosophila gene related to tenascin, is a new pair-rule gene. EMBO J 13(16):3728–3740
Bedard JE, Purnell JD, Ware SM (2007) Nuclear import and export signals are essential for proper cellular trafficking and function of ZIC3. Hum Mol Genet 16(2):187–198. https://doi.org/10.1093/hmg/ddl461
Bedard JE, Haaning AM, Ware SM (2011) Identification of a novel ZIC3 isoform and mutation screening in patients with heterotaxy and congenital heart disease. PLoS One 6(8):e23755. https://doi.org/10.1371/journal.pone.0023755
Brayer KJ, Kulshreshtha S, Segal DJ (2008) The protein-binding potential of C2H2 zinc finger domains. Cell Biochem Biophys 51(1):9–19. https://doi.org/10.1007/s12013-008-9007-6
Brewster R, Lee J, Ruiz i Altaba A (1998) Gli/Zic factors pattern the neural plate by defining domains of cell differentiation. Nature 393(6685):579–583. https://doi.org/10.1038/31242
Brown L, Brown S (2009) Zic2 is expressed in pluripotent cells in the blastocyst and adult brain expression overlaps with makers of neurogenesis. Gene Expr Patterns 9(1):43–49. https://doi.org/10.1016/j.gep.2008.08.002
Brown L, Paraso M, Arkell R, Brown S (2005) In vitro analysis of partial loss-of-function ZIC2 mutations in holoprosencephaly: alanine tract expansion modulates DNA binding and transactivation. Hum Mol Genet 14(3):411–420. https://doi.org/10.1093/hmg/ddi037
Buecker C, Srinivasan R, Wu Z, Calo E, Acampora D, Faial T, Simeone A, Tan M, Swigut T, Wysocka J (2014) Reorganization of enhancer patterns in transition from naive to primed pluripotency. Cell Stem Cell 14(6):838–853. https://doi.org/10.1016/j.stem.2014.04.003
Cedar H, Bergman Y (2011) Epigenetics of haematopoietic cell development. Nat Rev Immunol 11(7):478–488. https://doi.org/10.1038/nri2991
Chan DW, Liu VW, Leung LY, Yao KM, Chan KK, Cheung AN, Ngan HY (2011) Zic2 synergistically enhances Hedgehog signalling through nuclear retention of Gli1 in cervical cancer cells. J Pathol 225(4):525–534. https://doi.org/10.1002/path.2901
Chen Z, Wang L, Wang Q, Li W (2010) Histone modifications and chromatin organization in prostate cancer. Epigenomics 2(4):551–560. https://doi.org/10.2217/epi.10.31
Chen L, Ma Y, Qian L, Wang J (2013) Sumoylation regulates nuclear localization and function of zinc finger transcription factor ZIC3. Biochim Biophys Acta 1833(12):2725–2733. https://doi.org/10.1016/j.bbamcr.2013.07.009
Chhin B, Hatayama M, Bozon D, Ogawa M, Schon P, Tohmonda T, Sassolas F, Aruga J, Valard AG, Chen SC, Bouvagnet P (2007) Elucidation of penetrance variability of a ZIC3 mutation in a family with complex heart defects and functional analysis of ZIC3 mutations in the first zinc finger domain. Hum Mutat 28(6):563–570. https://doi.org/10.1002/humu.20480
Christensen GL, Kelstrup CD, Lyngso C, Sarwar U, Bogebo R, Sheikh SP, Gammeltoft S, Olsen JV, Hansen JL (2010) Quantitative phosphoproteomics dissection of seven-transmembrane receptor signaling using full and biased agonists. Mol Cell Proteomics 9(7):1540–1553. https://doi.org/10.1074/mcp.M900550-MCP200
Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14(6):1188–1190. https://doi.org/10.1101/gr.849004
Dephoure N, Zhou C, Villen J, Beausoleil SA, Bakalarski CE, Elledge SJ, Gygi SP (2008) A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci U S A 105(31):10762–10767. https://doi.org/10.1073/pnas.0805139105
Dovat S, Ronni T, Russell D, Ferrini R, Cobb BS, Smale ST (2002) A common mechanism for mitotic inactivation of C2H2 zinc finger DNA-binding domains. Genes Dev 16(23):2985–2990. https://doi.org/10.1101/gad.1040502
Ebert PJ, Timmer JR, Nakada Y, Helms AW, Parab PB, Liu Y, Hunsaker TL, Johnson JE (2003) Zic1 represses Math1 expression via interactions with the Math1 enhancer and modulation of Math1 autoregulation. Development 130(9):1949–1959
Frank CL, Liu F, Wijayatunge R, Song L, Biegler MT, Yang MG, Vockley CM, Safi A, Gersbach CA, Crawford GE, West AE (2015) Regulation of chromatin accessibility and Zic binding at enhancers in the developing cerebellum. Nat Neurosci 18(5):647–656. https://doi.org/10.1038/nn.3995
Fujimi TJ, Hatayama M, Aruga J (2012) Xenopus Zic3 controls notochord and organizer development through suppression of the Wnt/beta-catenin signaling pathway. Dev Biol 361(2):220–231. https://doi.org/10.1016/j.ydbio.2011.10.026
Garcia-Frigola C, Herrera E (2010) Zic2 regulates the expression of Sert to modulate eye-specific refinement at the visual targets. EMBO J 29(18):3170–3183. https://doi.org/10.1038/emboj.2010.172
Grimsrud PA, Carson JJ, Hebert AS, Hubler SL, Niemi NM, Bailey DJ, Jochem A, Stapleton DS, Keller MP, Westphall MS, Yandell BS, Attie AD, Coon JJ, Pagliarini DJ (2012) A quantitative map of the liver mitochondrial phosphoproteome reveals posttranslational control of ketogenesis. Cell Metab 16(5):672–683. https://doi.org/10.1016/j.cmet.2012.10.004
Hatayama M, Aruga J (2010) Characterization of the tandem CWCH2 sequence motif: a hallmark of inter-zinc finger interactions. BMC Evol Biol 10:53. https://doi.org/10.1186/1471-2148-10-53
Hatayama M, Aruga J (2012) Gli protein nuclear localization signal. Vitam Horm 88:73–89. https://doi.org/10.1016/B978-0-12-394622-5.00004-3
Hatayama M, Tomizawa T, Sakai-Kato K, Bouvagnet P, Kose S, Imamoto N, Yokoyama S, Utsunomiya-Tate N, Mikoshiba K, Kigawa T, Aruga J (2008) Functional and structural basis of the nuclear localization signal in the ZIC3 zinc finger domain. Hum Mol Genet 17(22):3459–3473. https://doi.org/10.1093/hmg/ddn239
Hendriks IA, D'Souza RC, Yang B, Verlaan-de Vries M, Mann M, Vertegaal AC (2014) Uncovering global SUMOylation signaling networks in a site-specific manner. Nat Struct Mol Biol 21(10):927–936. https://doi.org/10.1038/nsmb.2890
Himeda CL, Barro MV, Emerson CP Jr (2013) Pax3 synergizes with Gli2 and Zic1 in transactivating the Myf5 epaxial somite enhancer. Dev Biol 383(1):7–14. https://doi.org/10.1016/j.ydbio.2013.09.006
Houtmeyers R, Tchouate Gainkam O, Glanville-Jones HA, Van den Bosch B, Chappell A, Barratt KS, Souopgui J, Tejpar S, Arkell RM (2016) Zic2 mutation causes holoprosencephaly via disruption of NODAL signalling. Hum Mol Genet 25(18):3946–3959. https://doi.org/10.1093/hmg/ddw235
Huttlin EL, Jedrychowski MP, Elias JE, Goswami T, Rad R, Beausoleil SA, Villen J, Haas W, Sowa ME, Gygi SP (2010) A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143(7):1174–1189. https://doi.org/10.1016/j.cell.2010.12.001
Ishiguro A, Aruga J (2008) Functional role of Zic2 phosphorylation in transcriptional regulation. FEBS Lett 582(2):154–158. https://doi.org/10.1016/j.febslet.2007.11.080
Ishiguro A, Inoue T, Mikoshiba K, Aruga J (2004) Molecular properties of Zic4 and Zic5 proteins: functional diversity within Zic family. Biochem Biophys Res Commun 324(1):302–307. https://doi.org/10.1016/j.bbrc.2004.09.052
Ishiguro A, Ideta M, Mikoshiba K, Chen DJ, Aruga J (2007) ZIC2-dependent transcriptional regulation is mediated by DNA-dependent protein kinase, poly(ADP-ribose) polymerase, and RNA helicase A. J Biol Chem 282(13):9983–9995. https://doi.org/10.1074/jbc.M610821200
Jantz D, Berg JM (2004) Reduction in DNA-binding affinity of Cys2His2 zinc finger proteins by linker phosphorylation. Proc Natl Acad Sci U S A 101(20):7589–7593. https://doi.org/10.1073/pnas.0402191101
Jolma A, Yan J, Whitington T, Toivonen J, Nitta KR, Rastas P, Morgunova E, Enge M, Taipale M, Wei G, Palin K, Vaquerizas JM, Vincentelli R, Luscombe NM, Hughes TR, Lemaire P, Ukkonen E, Kivioja T, Taipale J (2013) DNA-binding specificities of human transcription factors. Cell 152(1–2):327–339. https://doi.org/10.1016/j.cell.2012.12.009
Kettenbach AN, Schweppe DK, Faherty BK, Pechenick D, Pletnev AA, Gerber SA (2011) Quantitative phosphoproteomics identifies substrates and functional modules of Aurora and Polo-like kinase activities in mitotic cells. Sci Signal 4(179):rs5. https://doi.org/10.1126/scisignal.2001497
Koyabu Y, Nakata K, Mizugishi K, Aruga J, Mikoshiba K (2001) Physical and functional interactions between Zic and Gli proteins. J Biol Chem 276(10):6889–6892. https://doi.org/10.1074/jbc.C000773200
Kraut N, Snider L, Chen CM, Tapscott SJ, Groudine M (1998) Requirement of the mouse I-mfa gene for placental development and skeletal patterning. EMBO J 17(21):6276–6288. https://doi.org/10.1093/emboj/17.21.6276
Kumano G, Kawai N, Nishida H (2010) Macho-1 regulates unequal cell divisions independently of its function as a muscle determinant. Dev Biol 344(1):284–292. https://doi.org/10.1016/j.ydbio.2010.05.013
Kuo JS, Patel M, Gamse J, Merzdorf C, Liu X, Apekin V, Sive H (1998) Opl: a zinc finger protein that regulates neural determination and patterning in Xenopus. Development 125(15):2867–2882
Lim LS, Loh YH, Zhang W, Li Y, Chen X, Wang Y, Bakre M, Ng HH, Stanton LW (2007) Zic3 is required for maintenance of pluripotency in embryonic stem cells. Mol Biol Cell 18(4):1348–1358. https://doi.org/10.1091/mbc.E06-07-0624
Lim LS, Hong FH, Kunarso G, Stanton LW (2010) The pluripotency regulator Zic3 is a direct activator of the Nanog promoter in ESCs. Stem Cells 28(11):1961–1969. https://doi.org/10.1002/stem.527
Luo Z, Gao X, Lin C, Smith ER, Marshall SA, Swanson SK, Florens L, Washburn MP, Shilatifard A (2015) Zic2 is an enhancer-binding factor required for embryonic stem cell specification. Mol Cell 57(4):685–694. https://doi.org/10.1016/j.molcel.2015.01.007
Matsuda K, Mikami T, Oki S, Iida H, Andrabi M, Boss JM, Yamaguchi K, Shigenobu S, Kondoh H (2017) ChIP-seq analysis of genomic binding regions of five major transcription factors highlights a central role for ZIC2 in the mouse epiblast stem cell gene regulatory network. Development 144(11):1948–1958. https://doi.org/10.1242/dev.143479
Matsumoto J, Kumano G, Nishida H (2007) Direct activation by Ets and Zic is required for initial expression of the Brachyury gene in the ascidian notochord. Dev Biol 306(2):870–882. https://doi.org/10.1016/j.ydbio.2007.03.034
Milet C, Maczkowiak F, Roche DD, Monsoro-Burq AH (2013) Pax3 and Zic1 drive induction and differentiation of multipotent, migratory, and functional neural crest in Xenopus embryos. Proc Natl Acad Sci U S A 110(14):5528–5533. https://doi.org/10.1073/pnas.1219124110
Mizugishi K, Aruga J, Nakata K, Mikoshiba K (2001) Molecular properties of Zic proteins as transcriptional regulators and their relationship to GLI proteins. J Biol Chem 276(3):2180–2188. https://doi.org/10.1074/jbc.M004430200
Mizugishi K, Hatayama M, Tohmonda T, Ogawa M, Inoue T, Mikoshiba K, Aruga J (2004) Myogenic repressor I-mfa interferes with the function of Zic family proteins. Biochem Biophys Res Commun 320(1):233–240. https://doi.org/10.1016/j.bbrc.2004.05.158
Nakajima T, Uchida C, Anderson SF, Lee CG, Hurwitz J, Parvin JD, Montminy M (1997) RNA helicase A mediates association of CBP with RNA polymerase II. Cell 90(6):1107–1112
Nishida H, Sawada K (2001) macho-1 encodes a localized mRNA in ascidian eggs that specifies muscle fate during embryogenesis. Nature 409(6821):724–729. https://doi.org/10.1038/35055568
Ogawa M, Mizugishi K, Ishiguro A, Koyabu Y, Imai Y, Takahashi R, Mikoshiba K, Aruga J (2008) Rines/RNF180, a novel RING finger gene-encoded product, is a membrane-bound ubiquitin ligase. Genes Cells 13(4):397–409. https://doi.org/10.1111/j.1365-2443.2008.01169.x
Okumura K, Hosoe Y, Nakajima N (2004) Zic1 is a transcriptional repressor trough the lamin A/C promoter and has an intrinsic repressor domain. J Health Sci 4:423–427
Olsen JV, Vermeulen M, Santamaria A, Kumar C, Miller ML, Jensen LJ, Gnad F, Cox J, Jensen TS, Nigg EA, Brunak S, Mann M (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal 3(104):ra3. https://doi.org/10.1126/scisignal.2000475
Pardo M, Lang B, Yu L, Prosser H, Bradley A, Babu MM, Choudhary J (2010) An expanded Oct4 interaction network: implications for stem cell biology, development, and disease. Cell Stem Cell 6(4):382–395. https://doi.org/10.1016/j.stem.2010.03.004
Pavletich NP, Pabo CO (1993) Crystal structure of a five-finger GLI-DNA complex: new perspectives on zinc fingers. Science 261(5129):1701–1707
Peterson KA, Nishi Y, Ma W, Vedenko A, Shokri L, Zhang X, McFarlane M, Baizabal JM, Junker JP, van Oudenaarden A, Mikkelsen T, Bernstein BE, Bailey TL, Bulyk ML, Wong WH, McMahon AP (2012) Neural-specific Sox2 input and differential Gli-binding affinity provide context and positional information in Shh-directed neural patterning. Genes Dev 26(24):2802–2816. https://doi.org/10.1101/gad.207142.112
Plouhinec JL, Roche DD, Pegoraro C, Figueiredo AL, Maczkowiak F, Brunet LJ, Milet C, Vert JP, Pollet N, Harland RM, Monsoro-Burq AH (2014) Pax3 and Zic1 trigger the early neural crest gene regulatory network by the direct activation of multiple key neural crest specifiers. Dev Biol 386(2):461–472. https://doi.org/10.1016/j.ydbio.2013.12.010
Pourebrahim R, Houtmeyers R, Ghogomu S, Janssens S, Thelie A, Tran HT, Langenberg T, Vleminckx K, Bellefroid E, Cassiman JJ, Tejpar S (2011) Transcription factor Zic2 inhibits Wnt/beta-catenin protein signaling. J Biol Chem 286(43):37732–37740. https://doi.org/10.1074/jbc.M111.242826
Quinn ME, Haaning A, Ware SM (2012) Preaxial polydactyly caused by Gli3 haploinsufficiency is rescued by Zic3 loss of function in mice. Hum Mol Genet 21(8):1888–1896. https://doi.org/10.1093/hmg/dds002
Rigbolt KT, Prokhorova TA, Akimov V, Henningsen J, Johansen PT, Kratchmarova I, Kassem M, Mann M, Olsen JV, Blagoev B (2011) System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation. Sci Signal 4(164):rs3. https://doi.org/10.1126/scisignal.2001570
Rizkallah R, Alexander KE, Hurt MM (2011) Global mitotic phosphorylation of C2H2 zinc finger protein linker peptides. Cell Cycle 10(19):3327–3336. https://doi.org/10.4161/cc.10.19.17619
Rizkallah R, Batsomboon P, Dudley GB, Hurt MM (2015) Identification of the oncogenic kinase TOPK/PBK as a master mitotic regulator of C2H2 zinc finger proteins. Oncotarget 6(3):1446–1461. 10.18632/oncotarget.2735
Sadoul K, Wang J, Diagouraga B, Khochbin S (2011) The tale of protein lysine acetylation in the cytoplasm. J Biomed Biotechnol 2011:970382. https://doi.org/10.1155/2011/970382
Sakai-Kato K, Ishiguro A, Mikoshiba K, Aruga J, Utsunomiya-Tate N (2008) CD spectra show the relational style between Zic-, Gli-, Glis-zinc finger protein and DNA. Biochim Biophys Acta 1784(7–8):1011–1019. https://doi.org/10.1016/j.bbapap.2008.01.013
Sakai-Kato K, Umezawa Y, Mikoshiba K, Aruga J, Utsunomiya-Tate N (2009) Stability of folding structure of Zic zinc finger proteins. Biochem Biophys Res Commun 384(3):362–365. https://doi.org/10.1016/j.bbrc.2009.04.151
Sakurada T, Mima K, Kurisaki A, Sugino H, Yamauchi T (2005) Neuronal cell type-specific promoter of the alpha CaM kinase II gene is activated by Zic2, a Zic family zinc finger protein. Neurosci Res 53(3):323–330. https://doi.org/10.1016/j.neures.2005.08.001
Salero E, Perez-Sen R, Aruga J, Gimenez C, Zafra F (2001) Transcription factors Zic1 and Zic2 bind and transactivate the apolipoprotein E gene promoter. J Biol Chem 276(3):1881–1888. https://doi.org/10.1074/jbc.M007008200
Sanchez-Ferras O, Bernas G, Laberge-Perrault E, Pilon N (2014) Induction and dorsal restriction of Paired-box 3 (Pax3) gene expression in the caudal neuroectoderm is mediated by integration of multiple pathways on a short neural crest enhancer. Biochim Biophys Acta 1839(7):546–558. https://doi.org/10.1016/j.bbagrm.2014.04.023
Sankar S, Yellajoshyula D, Zhang B, Teets B, Rockweiler N, Kroll KL (2016) Gene regulatory networks in neural cell fate acquisition from genome-wide chromatin association of Geminin and Zic1. Sci Rep 6:37412. https://doi.org/10.1038/srep37412
Sato T, Sasai N, Sasai Y (2005) Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm. Development 132(10):2355–2363. https://doi.org/10.1242/dev.01823
Satow R, Nakamura T, Kato C, Endo M, Tamura M, Batori R, Tomura S, Murayama Y, Fukami K (2017) ZIC5 drives melanoma aggressiveness by PDGFD-mediated activation of FAK and STAT3. Cancer Res 77(2):366–377. https://doi.org/10.1158/0008-5472.CAN-16-0991
Sawada K, Fukushima Y, Nishida H (2005) Macho-1 functions as transcriptional activator for muscle formation in embryos of the ascidian Halocynthia roretzi. Gene Expr Patterns 5(3):429–437. https://doi.org/10.1016/j.modgep.2004.09.003
Sen A, Stultz BG, Lee H, Hursh DA (2010) Odd paired transcriptional activation of decapentaplegic in the Drosophila eye/antennal disc is cell autonomous but indirect. Dev Biol 343(1–2):167–177. https://doi.org/10.1016/j.ydbio.2010.04.003
Siegenthaler JA, Choe Y, Patterson KP, Hsieh I, Li D, Jaminet SC, Daneman R, Kume T, Huang EJ, Pleasure SJ (2013) Foxc1 is required by pericytes during fetal brain angiogenesis. Biol Open 2(7):647–659. https://doi.org/10.1242/bio.20135009
Simoes-Costa MS, McKeown SJ, Tan-Cabugao J, Sauka-Spengler T, Bronner ME (2012) Dynamic and differential regulation of stem cell factor FoxD3 in the neural crest is Encrypted in the genome. PLoS Genet 8(12):e1003142. https://doi.org/10.1371/journal.pgen.1003142
Sone M, Morone N, Nakamura T, Tanaka A, Okita K, Woltjen K, Nakagawa M, Heuser JE, Yamada Y, Yamanaka S, Yamamoto T (2017) Hybrid cellular metabolism coordinated by Zic3 and Esrrb synergistically enhances induction of naive pluripotency. Cell Metab 25(5):1103–1117 e1106. https://doi.org/10.1016/j.cmet.2017.04.017
Song CZ, Keller K, Chen Y, Stamatoyannopoulos G (2003) Functional interplay between CBP and PCAF in acetylation and regulation of transcription factor KLF13 activity. J Mol Biol 329(2):207–215
Suzuki K, Sako K, Akiyama K, Isoda M, Senoo C, Nakajo N, Sagata N (2015) Identification of non-Ser/Thr-Pro consensus motifs for Cdk1 and their roles in mitotic regulation of C2H2 zinc finger proteins and Ect2. Sci Rep 5:7929. https://doi.org/10.1038/srep07929
Tucker RP, Chiquet-Ehrismann R, Chevron MP, Martin D, Hall RJ, Rubin BP (2001) Teneurin-2 is expressed in tissues that regulate limb and somite pattern formation and is induced in vitro and in situ by FGF8. Dev Dyn 220(1):27–39. https://doi.org/10.1002/1097-0177(2000)9999:9999<::AID-DVDY1084>3.0.CO;2-B
Winata CL, Kondrychyn I, Kumar V, Srinivasan KG, Orlov Y, Ravishankar A, Prabhakar S, Stanton LW, Korzh V, Mathavan S (2013) Genome wide analysis reveals Zic3 interaction with distal regulatory elements of stage specific developmental genes in zebrafish. PLoS Genet 9(10):e1003852. https://doi.org/10.1371/journal.pgen.1003852
Winata CL, Kondrychyn I, Korzh V (2015) Changing faces of transcriptional regulation reflected by Zic3. Curr Genomics 16(2):117–127. https://doi.org/10.2174/1389202916666150205124519
Wolfe SA, Nekludova L, Pabo CO (2000) DNA recognition by Cys2His2 zinc finger proteins. Annu Rev Biophys Biomol Struct 29:183–212. https://doi.org/10.1146/annurev.biophys.29.1.183
Wysocka J, Swigut T, Xiao H, Milne TA, Kwon SY, Landry J, Kauer M, Tackett AJ, Chait BT, Badenhorst P, Wu C, Allis CD (2006) A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442(7098):86–90. https://doi.org/10.1038/nature04815
Yagi K, Satoh N, Satou Y (2004a) Identification of downstream genes of the ascidian muscle determinant gene Ci-macho1. Dev Biol 274(2):478–489. https://doi.org/10.1016/j.ydbio.2004.07.013
Yagi K, Satou Y, Satoh N (2004b) A zinc finger transcription factor, ZicL, is a direct activator of Brachyury in the notochord specification of Ciona intestinalis. Development 131(6):1279–1288. https://doi.org/10.1242/dev.01011
Yang Y, Hwang CK, Junn E, Lee G, Mouradian MM (2000) ZIC2 and Sp3 repress Sp1-induced activation of the human D1A dopamine receptor gene. J Biol Chem 275(49):38863–38869. https://doi.org/10.1074/jbc.M007906200
Yokota N, Aruga J, Takai S, Yamada K, Hamazaki M, Iwase T, Sugimura H, Mikoshiba K (1996) Predominant expression of human zic in cerebellar granule cell lineage and medulloblastoma. Cancer Res 56(2):377–383
Yu W, Briones V, Lister R, McIntosh C, Han Y, Lee EY, Ren J, Terashima M, Leighty RM, Ecker JR, Muegge K (2014) CG hypomethylation in Lsh-/- mouse embryonic fibroblasts is associated with de novo H3K4me1 formation and altered cellular plasticity. Proc Natl Acad Sci U S A 111 (16):5890–5895. https://doi.org/10.1073/pnas.1320945111
Zhao S, Xu W, Jiang W, Yu W, Lin Y, Zhang T, Yao J, Zhou L, Zeng Y, Li H, Li Y, Shi J, An W, Hancock SM, He F, Qin L, Chin J, Yang P, Chen X, Lei Q, Xiong Y, Guan KL (2010) Regulation of cellular metabolism by protein lysine acetylation. Science 327(5968):1000–1004. https://doi.org/10.1126/science.1179689
Zhu L, Harutyunyan KG, Peng JL, Wang J, Schwartz RJ, Belmont JW (2007) Identification of a novel role of ZIC3 in regulating cardiac development. Hum Mol Genet 16(14):1649–1660. https://doi.org/10.1093/hmg/ddm106
Zhu L, Zhou G, Poole S, Belmont JW (2008) Characterization of the interactions of human ZIC3 mutants with GLI3. Hum Mutat 29(1):99–105. https://doi.org/10.1002/humu.20606
Zhu P, Wang Y, He L, Huang G, Du Y, Zhang G, Yan X, Xia P, Ye B, Wang S, Hao L, Wu J, Fan Z (2015) ZIC2-dependent OCT4 activation drives self-renewal of human liver cancer stem cells. J Clin Invest 125(10):3795–3808. https://doi.org/10.1172/JCI81979
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Hatayama, M., Aruga, J. (2018). Role of Zic Family Proteins in Transcriptional Regulation and Chromatin Remodeling. In: Aruga, J. (eds) Zic family. Advances in Experimental Medicine and Biology, vol 1046. Springer, Singapore. https://doi.org/10.1007/978-981-10-7311-3_18
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