Advertisement

Zic family pp 157-177 | Cite as

Zebrafish Zic Genes Mediate Developmental Signaling

Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1046)

Abstract

The introduction of genomics into the field of developmental biology led to a vast expansion of knowledge about developmental genes and signaling mechanisms they are involved in. Unlike mammals, the zebrafish features seven Zic genes. This provides an interesting insight into Zic gene evolution. In addition, an unprecedented bioimaging capability of semitransparent zebrafish embryos turns to be a crucial factor in medium- to large-scale analysis of the activity of potential regulatory elements. The Zic family of zinc finger proteins plays an important, relatively well-established, role in the regulation of stem cells and neural development and, in particular, during neural fate commitment and determination. At the same time, some Zic genes are expressed in mesodermal lineages, and their deficiency causes a number of developmental defects in axis formation, establishing body symmetry and cardiac morphogenesis. In stem cells, Zic genes are required to maintain pluripotency by binding to the proximal promoters of pluripotency genes (Oct4, Nanog, Sox2, etc.). During embryogenesis, the dynamic nature of Zic transcriptional regulation is manifested by the interaction of these factors with distal enhancers and other regulatory elements associated with the control of gene transcription and, in particular, with the Nodal and Wnt signaling pathways that play a role in establishing basic organization of the vertebrate body. Zic transcription factors may regulate development through acting alone as well as in combination with other transcription factors. This is achieved due to Zic binding to sites adjacent to the binding sites of other transcription factors, including Gli. This probably leads to the formation of multi-transcription factor complexes associated with enhancers.

Keywords

Zebrafish Enhancer Promoter Transcription Stem cells Gastrulation Left-right asymmetry Neurogenesis Developmental signaling 

References

  1. Abu-Abed S, Dolle P, Metzger D, Beckett B, Chambon P, Petkovich M (2001) The retinoic acid-metabolizing enzyme, CYP26A1, is essential for normal hindbrain patterning, vertebral identity, and development of posterior structures. Genes Dev 15:226–240PubMedPubMedCentralCrossRefGoogle Scholar
  2. Agalliu D, Takada S, Agalliu I, McMahon AP, Jessell TM (2009) Motor neurons with axial muscle projections specified by Wnt4/5 signaling. Neuron 61:708–720PubMedPubMedCentralCrossRefGoogle Scholar
  3. Aruga J (2004) The role of Zic genes in neural development. Mol Cell Neurosci 26:205–221PubMedCrossRefGoogle Scholar
  4. 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 63:1880–1890PubMedCrossRefGoogle Scholar
  5. Aruga J, Nozaki Y, Hatayama M, Odaka YS, Yokota N (2010) Expression of ZIC family genes in meningiomas and other brain tumors. BMC Cancer 10:79PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bang AG, Papalopulu N, Goulding MD, Kintner C (1999) Expression of Pax-3 in the lateral neural plate is dependent on a Wnt-mediated signal from posterior nonaxial mesoderm. Dev Biol 212:366–380PubMedCrossRefGoogle Scholar
  7. Benedyk MJ, Mullen JR, DiNardo S (1994) Odd-paired: a zinc finger pair-rule protein required for the timely activation of engrailed and wingless in Drosophila embryos. Genes Dev 8:105–117PubMedCrossRefGoogle Scholar
  8. Bilder D, Schober M, Perrimon N (2003) Integrated activity of PDZ protein complexes regulates epithelial polarity. Nat Cell Biol 5:53–58PubMedCrossRefGoogle Scholar
  9. Bisgrove BW, Essner JJ, Yost HJ (2000) Multiple pathways in the midline regulate concordant brain, heart and gut left-right asymmetry. Development 127:3567–3579PubMedGoogle Scholar
  10. Brown SA, Warburton D, Brown LY, Yu CY, Roeder ER, Stengel-Rutkowski S, Hennekam RC, Muenke M (1998) Holoprosencephaly due to mutations in ZIC2, a homologue of Drosophila odd-paired. Nat Genet 20:180–183PubMedCrossRefGoogle Scholar
  11. Carroll SB (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134:25–36PubMedCrossRefGoogle Scholar
  12. Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, Szary AJ, Eeckhoute J, Shao W, Hestermann EV, Geistlinger TR et al (2005) Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122:33–43PubMedCrossRefGoogle Scholar
  13. Cast AE, Gao C, Amack JD, Ware SM (2012) An essential and highly conserved role for Zic3 in left-right patterning, gastrulation and convergent extension morphogenesis. Dev Biol 364:22–31PubMedPubMedCentralCrossRefGoogle Scholar
  14. Chen X, Vega VB, Ng HH (2008) Transcriptional regulatory networks in embryonic stem cells. Cold Spring Harb Symp Quant Biol 73:203–209PubMedCrossRefGoogle Scholar
  15. Chizhikov VV, Millen KJ (2004a) Control of roof plate development and signaling by Lmx1b in the caudal vertebrate CNS. J Neurosci 24:5694–5703PubMedCrossRefGoogle Scholar
  16. Chizhikov VV, Millen KJ (2004b) Mechanisms of roof plate formation in the vertebrate CNS. Nat Rev Neurosci 5:808–812PubMedCrossRefGoogle Scholar
  17. Coolen M, Thieffry D, Drivenes O, Becker TS, Bally-Cuif L (2012) miR-9 controls the timing of neurogenesis through the direct inhibition of antagonistic factors. Dev Cell 22:1052–1064PubMedCrossRefGoogle Scholar
  18. Danos MC, Yost HJ (1996) Role of notochord in specification of cardiac left-right orientation in zebrafish and Xenopus. Dev Biol 177:96–103PubMedCrossRefGoogle Scholar
  19. Drummond DL, Cheng CS, Selland LG, Hocking JC, Prichard LB, Waskiewicz AJ (2013) The role of Zic transcription factors in regulating hindbrain retinoic acid signaling. BMC Dev Biol 13:31PubMedPubMedCentralCrossRefGoogle Scholar
  20. Eisen JS, Weston JA (1993) Development of the neural crest in the zebrafish. Dev Biol 159:50–59PubMedCrossRefGoogle Scholar
  21. Ekker M, Akimenko MA, Allende ML, Smith R, Drouin G, Langille RM, Weinberg ES, Westerfield M (1997) Relationships among msx gene structure and function in zebrafish and other vertebrates. Mol Biol Evol 14:1008–1022PubMedCrossRefGoogle Scholar
  22. Elsen GE, Choi LY, Millen KJ, Grinblat Y, Prince VE (2008) Zic1 and Zic4 regulate zebrafish roof plate specification and hindbrain ventricle morphogenesis. Dev Biol 314:376–392PubMedCrossRefGoogle Scholar
  23. Fernandes M, Hebert JM (2008) The ups and downs of holoprosencephaly: dorsal versus ventral patterning forces. Clin Genet 73:413–423PubMedCrossRefGoogle Scholar
  24. Fogel JL, Chiang C, Huang X, Agarwala S (2008) Ventral specification and perturbed boundary formation in the mouse midbrain in the absence of hedgehog signaling. Dev Dyn 237:1359–1372PubMedPubMedCentralCrossRefGoogle Scholar
  25. Fujimi TJ, Mikoshiba K, Aruga J (2006) Xenopus Zic4: conservation and diversification of expression profiles and protein function among the Xenopus Zic family. Dev Dyn 235:3379–3386PubMedCrossRefGoogle Scholar
  26. 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 361:220–231PubMedCrossRefGoogle Scholar
  27. Gallet A, Staccini-Lavenant L, Therond PP (2008) Cellular trafficking of the glypican Dally-like is required for full-strength Hedgehog signaling and wingless transcytosis. Dev Cell 14:712–725PubMedCrossRefGoogle Scholar
  28. Gamse JT, Sive H (2001) Early anteroposterior division of the presumptive neurectoderm in Xenopus. Mech Dev 104:21–36PubMedCrossRefGoogle Scholar
  29. Garcia-Castro MI, Marcelle C, Bronner-Fraser M (2002) Ectodermal Wnt function as a neural crest inducer. Science 297:848–851PubMedGoogle Scholar
  30. Garnett AT, Square TA, Medeiros DM (2012) BMP, Wnt and FGF signals are integrated through evolutionarily conserved enhancers to achieve robust expression of Pax3 and Zic genes at the zebrafish neural plate border. Development 139:4220–4231PubMedPubMedCentralCrossRefGoogle Scholar
  31. Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van Dongen S, Inoue K, Enright AJ, Schier AF (2006) Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312:75–79PubMedCrossRefGoogle Scholar
  32. Grinblat Y, Sive H (2001) Zic gene expression marks anteroposterior pattern in the presumptive neurectoderm of the zebrafish gastrula. Dev Dyn 222:688–693PubMedCrossRefGoogle Scholar
  33. Hadorn E (1956) Patterns of biochemical and developmental pleiotropy. Cold Spring Harb Symp Quant Biol 21:363–373PubMedCrossRefGoogle Scholar
  34. Harris TJ, Peifer M (2004) Adherens junction-dependent and -independent steps in the establishment of epithelial cell polarity in Drosophila. J Cell Biol 167:135–147PubMedPubMedCentralCrossRefGoogle Scholar
  35. Hashimoto M, Shinohara K, Wang J, Ikeuchi S, Yoshiba S, Meno C, Nonaka S, Takada S, Hatta K, Wynshaw-Boris A et al (2010) Planar polarization of node cells determines the rotational axis of node cilia. Nat Cell Biol 12:170–176PubMedCrossRefGoogle Scholar
  36. Inoue T, Hatayama M, Tohmonda T, Itohara S, Aruga J, Mikoshiba K (2004) Mouse Zic5 deficiency results in neural tube defects and hypoplasia of cephalic neural crest derivatives. Dev Biol 270:146–162PubMedCrossRefGoogle Scholar
  37. 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 324:302–307PubMedCrossRefGoogle Scholar
  38. Keller MJ, Chitnis AB (2007) Insights into the evolutionary history of the vertebrate zic3 locus from a teleost-specific zic6 gene in the zebrafish, Danio rerio. Dev Genes Evol 217:541–547PubMedCrossRefGoogle Scholar
  39. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310PubMedCrossRefGoogle Scholar
  40. Kitaguchi T, Nagai T, Nakata K, Aruga J, Mikoshiba K (2000) Zic3 is involved in the left-right specification of the Xenopus embryo. Development 127:4787–4795PubMedGoogle Scholar
  41. Kondrychyn I, Teh C, Sin M, Korzh V (2013) Stretching morphogenesis of the roof plate and formation of the central canal. PLoS One 8:e56219PubMedPubMedCentralCrossRefGoogle Scholar
  42. Korzh V (2014) Stretching cell morphogenesis during late neurulation and mild neural tube defects. Dev Growth Differ 56:425–433PubMedCrossRefGoogle Scholar
  43. Krispin S, Nitzan E, Kalcheim C (2010a) The dorsal neural tube: a dynamic setting for cell fate decisions. Dev Neurobiol 70:796–812PubMedCrossRefGoogle Scholar
  44. Krispin S, Nitzan E, Kassem Y, Kalcheim C (2010b) Evidence for a dynamic spatiotemporal fate map and early fate restriction of premigratory avian neural crest. Development 137:585–595PubMedCrossRefGoogle Scholar
  45. 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 125:2867–2882PubMedGoogle Scholar
  46. Layden MJ, Meyer NP, Pang K, Seaver EC, Martindale MQ (2010) Expression and phylogenetic analysis of the zic gene family in the evolution and development of metazoans. EvoDevo 1:12PubMedPubMedCentralCrossRefGoogle Scholar
  47. Lecaudey V, Anselme I, Rosa F, Schneider-Maunoury S (2004) The zebrafish Iroquois gene iro7 positions the r4/r5 boundary and controls neurogenesis in the rostral hindbrain. Development 131:3121–3131PubMedCrossRefGoogle Scholar
  48. Lecaudey V, Anselme I, Dildrop R, Ruther U, Schneider-Maunoury S (2005) Expression of the zebrafish Iroquois genes during early nervous system formation and patterning. J Comp Neurol 492:289–302PubMedCrossRefGoogle Scholar
  49. 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 28:1961–1969PubMedCrossRefGoogle Scholar
  50. Lindeman LC, Winata CL, Aanes H, Mathavan S, Alestrom P, Collas P (2010) Chromatin states of developmentally-regulated genes revealed by DNA and histone methylation patterns in zebrafish embryos. Int J Dev Biol 54:803–813PubMedCrossRefGoogle Scholar
  51. Lindeman LC, Andersen IS, Reiner AH, Li N, Aanes H, Ostrup O, Winata C, Mathavan S, Muller F, Alestrom P et al (2011) Prepatterning of developmental gene expression by modified histones before zygotic genome activation. Dev Cell 21:993–1004PubMedCrossRefGoogle Scholar
  52. Lindgens D, Holstein TW, Technau U (2004) Hyzic, the Hydra homolog of the zic/odd-paired gene, is involved in the early specification of the sensory nematocytes. Development 131:191–201PubMedCrossRefGoogle Scholar
  53. Liu A, Majumdar A, Schauerte HE, Haffter P, Drummond IA (2000) Zebrafish wnt4b expression in the floor plate is altered in sonic hedgehog and gli-2 mutants. Mech Dev 91:409–413PubMedCrossRefGoogle Scholar
  54. Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781–810PubMedCrossRefGoogle Scholar
  55. Marchal L, Luxardi G, Thome V, Kodjabachian L (2009) BMP inhibition initiates neural induction via FGF signaling and Zic genes. Proc Natl Acad Sci U S A 106:17437–17442PubMedPubMedCentralCrossRefGoogle Scholar
  56. Marois E, Mahmoud A, Eaton S (2006) The endocytic pathway and formation of the wingless morphogen gradient. Development 133:307–317PubMedCrossRefGoogle Scholar
  57. Merzdorf CS (2007) Emerging roles for zic genes in early development. Dev Dyn 236:922–940PubMedCrossRefGoogle Scholar
  58. Mii Y, Taira M (2009) Secreted frizzled-related proteins enhance the diffusion of Wnt ligands and expand their signalling range. Development 136:4083–4088PubMedCrossRefGoogle Scholar
  59. 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 276:2180–2188PubMedCrossRefGoogle Scholar
  60. Morgan D, Turnpenny L, Goodship J, Dai W, Majumder K, Matthews L, Gardner A, Schuster G, Vien L, Harrison W et al (1998) Inversin, a novel gene in the vertebrate left-right axis pathway, is partially deleted in the inv mouse. Nat Genet 20:149–156PubMedCrossRefGoogle Scholar
  61. Nagai T, Aruga J, Takada S, Gunther T, Sporle R, Schughart K, Mikoshiba K (1997) The expression of the mouse Zic1, Zic2, and Zic3 gene suggests an essential role for Zic genes in body pattern formation. Dev Biol 182:299–313PubMedCrossRefGoogle Scholar
  62. Nakata K, Nagai T, Aruga J, Mikoshiba K (1997) Xenopus Zic3, a primary regulator both in neural and neural crest development. Proc Natl Acad Sci U S A 94:11980–11985PubMedPubMedCentralCrossRefGoogle Scholar
  63. Nakata K, Nagai T, Aruga J, Mikoshiba K (1998) Xenopus Zic family and its role in neural and neural crest development. Mech Dev 75:43–51PubMedCrossRefGoogle Scholar
  64. Nakata K, Koyabu Y, Aruga J, Mikoshiba K (2000) A novel member of the Xenopus Zic family, Zic5, mediates neural crest development. Mech Dev 99:83–91PubMedCrossRefGoogle Scholar
  65. Niederreither K, Vermot J, Schuhbaur B, Chambon P, Dolle P (2000) Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Development 127:75–85PubMedGoogle Scholar
  66. Nyholm MK, Wu SF, Dorsky RI, Grinblat Y (2007) The zebrafish zic2a-zic5 gene pair acts downstream of canonical Wnt signaling to control cell proliferation in the developing tectum. Development 134:735–746PubMedCrossRefGoogle Scholar
  67. Ohtsuka M, Kikuchi N, Yokoi H, Kinoshita M, Wakamatsu Y, Ozato K, Takeda H, Inoko H, Kimura M (2004) Possible roles of zic1 and zic4, identified within the medaka Double anal fin (Da) locus, in dorsoventral patterning of the trunk-tail region (related to phenotypes of the Da mutant). Mech Dev 121:873–882PubMedCrossRefGoogle Scholar
  68. Okada Y, Takeda S, Tanaka Y, Izpisua Belmonte JC, Hirokawa N (2005) Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination. Cell 121:633–644PubMedCrossRefGoogle Scholar
  69. Parinov S, Kondrichin I, Korzh V, Emelyanov A (2004) Tol2 transposon-mediated enhancer trap to identify developmentally regulated zebrafish genes in vivo. Dev Dyn 231:449–459PubMedCrossRefGoogle Scholar
  70. Raible DW, Wood A, Hodsdon W, Henion PD, Weston JA, Eisen JS (1992) Segregation and early dispersal of neural crest cells in the embryonic zebrafish. Dev Dyn 195:29–42PubMedCrossRefGoogle Scholar
  71. Rohr KB, Schulte-Merker S, Tautz D (1999) Zebrafish zic1 expression in brain and somites is affected by BMP and hedgehog signalling. Mech Dev 85:147–159PubMedCrossRefGoogle Scholar
  72. Roy S, Hsiung F, Kornberg TB (2011) Specificity of Drosophila cytonemes for distinct signaling pathways. Science 332:354–358PubMedPubMedCentralCrossRefGoogle Scholar
  73. Sabherwal N, Tsutsui A, Hodge S, Wei J, Chalmers AD, Papalopulu N (2009) The apicobasal polarity kinase aPKC functions as a nuclear determinant and regulates cell proliferation and fate during Xenopus primary neurogenesis. Development 136:2767–2777PubMedPubMedCentralCrossRefGoogle Scholar
  74. 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 53:323–330PubMedCrossRefGoogle Scholar
  75. 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 276:1881–1888PubMedCrossRefGoogle Scholar
  76. Sanek NA, Grinblat Y (2008) A novel role for zebrafish zic2a during forebrain development. Dev Biol 317:325–335PubMedPubMedCentralCrossRefGoogle Scholar
  77. Sanyal A, Lajoie BR, Jain G, Dekker J (2012) The long-range interaction landscape of gene promoters. Nature 489:109–113PubMedPubMedCentralCrossRefGoogle Scholar
  78. Sato T, Sasai N, Sasai Y (2005) Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm. Development 132:2355–2363PubMedCrossRefGoogle Scholar
  79. Sawyer JM, Harrell JR, Shemer G, Sullivan-Brown J, Roh-Johnson M, Goldstein B (2010) Apical constriction: a cell shape change that can drive morphogenesis. Dev Biol 341:5–19PubMedCrossRefGoogle Scholar
  80. Sonawane M, Carpio Y, Geisler R, Schwarz H, Maischein HM, Nuesslein-Volhard C (2005) Zebrafish penner/lethal giant larvae 2 functions in hemidesmosome formation, maintenance of cellular morphology and growth regulation in the developing basal epidermis. Development 132:3255–3265PubMedCrossRefGoogle Scholar
  81. Sonawane M, Martin-Maischein H, Schwarz H, Nusslein-Volhard C (2009) Lgl2 and E-cadherin act antagonistically to regulate hemidesmosome formation during epidermal development in zebrafish. Development 136:1231–1240PubMedCrossRefGoogle Scholar
  82. Stewart RA, Arduini BL, Berghmans S, George RE, Kanki JP, Henion PD, Look AT (2006) Zebrafish foxd3 is selectively required for neural crest specification, migration and survival. Dev Biol 292:174–188PubMedCrossRefGoogle Scholar
  83. Strigini M, Cohen SM (2000) Wingless gradient formation in the Drosophila wing. Curr Biol 10:293–300PubMedCrossRefGoogle Scholar
  84. Teslaa JJ, Keller AN, Nyholm MK, Grinblat Y (2013) Zebrafish Zic2a and Zic2b regulate neural crest and craniofacial development. Dev Biol 380:73–86PubMedCrossRefGoogle Scholar
  85. Thisse B, Pflumio S, Fürthauer M, Loppin B, Heyer V, Degrave A, Woehl R, Lux A, Steffan T, Charbonnier XQ, Thisse C (2001) Expression of the zebrafish genome during embryogenesis. ZFIN direct data submissionGoogle Scholar
  86. Thisse B, Heyer V, Lux A, Alunni V, Degrave A, Seiliez I, Kirchner J, Parkhill JP, Thisse C (2004) Spatial and temporal expression of the zebrafish genome by large-scale in situ hybridization screening. Methods Cell Biol 77:505–519PubMedCrossRefGoogle Scholar
  87. Toyama R, Gomez DM, Mana MD, Dawid IB (2004) Sequence relationships and expression patterns of zebrafish zic2 and zic5 genes. Gene Expr Patterns 4:345–350PubMedCrossRefGoogle Scholar
  88. Ulloa F, Marti E (2010) Wnt won the war: antagonistic role of Wnt over Shh controls dorso-ventral patterning of the vertebrate neural tube. Dev Dyn 239:69–76PubMedGoogle Scholar
  89. Ungar AR, Kelly GM, Moon RT (1995) Wnt4 affects morphogenesis when misexpressed in the zebrafish embryo. Mech Dev 52:153–164PubMedCrossRefGoogle Scholar
  90. van Straaten HW, Sieben I, Hekking JW (2002) Multistep role for actin in initial closure of the mesencephalic neural groove in the chick embryo. Dev Dyn 224:103–108PubMedCrossRefGoogle Scholar
  91. Vastenhouw NL, Zhang Y, Woods IG, Imam F, Regev A, Liu XS, Rinn J, Schier AF (2010) Chromatin signature of embryonic pluripotency is established during genome activation. Nature 464:922–926PubMedPubMedCentralCrossRefGoogle Scholar
  92. Wada S, Saiga H (2002) HrzicN, a new Zic family gene of ascidians, plays essential roles in the neural tube and notochord development. Development 129:5597–5608PubMedCrossRefGoogle Scholar
  93. Wang G, Cadwallader AB, Jang DS, Tsang M, Yost HJ, Amack JD (2011) The Rho kinase Rock2b establishes anteroposterior asymmetry of the ciliated Kupffer’s vesicle in zebrafish. Development 138:45–54PubMedPubMedCentralCrossRefGoogle Scholar
  94. Ware SM, Harutyunyan KG, Belmont JW (2006) Zic3 is critical for early embryonic patterning during gastrulation. Dev Dyn 235:776–785PubMedCrossRefGoogle Scholar
  95. Warr N, Powles-Glover N, Chappell A, Robson J, Norris D, Arkell RM (2008) Zic2-associated holoprosencephaly is caused by a transient defect in the organizer region during gastrulation. Hum Mol Genet 17:2986–2996PubMedCrossRefGoogle Scholar
  96. Wederell ED, Bilenky M, Cullum R, Thiessen N, Dagpinar M, Delaney A, Varhol R, Zhao Y, Zeng T, Bernier B et al (2008) Global analysis of in vivo Foxa2-binding sites in mouse adult liver using massively parallel sequencing. Nucleic Acids Res 36:4549–4564PubMedPubMedCentralCrossRefGoogle Scholar
  97. Whyte WA, Orlando DA, Hnisz D, Abraham BJ, Lin CY, Kagey MH, Rahl PB, Lee TI, Young RA (2013) Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153:307–319PubMedPubMedCentralCrossRefGoogle Scholar
  98. Wilkins AS (2007) Between “design” and “bricolage”: genetic networks, levels of selection, and adaptive evolution. Proc Natl Acad Sci U S A 104(Suppl 1):8590–8596PubMedPubMedCentralCrossRefGoogle Scholar
  99. 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:e1003852PubMedPubMedCentralCrossRefGoogle Scholar
  100. Wittkopp PJ, Kalay G (2012) Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet 13:59–69CrossRefGoogle Scholar
  101. Woda JM, Pastagia J, Mercola M, Artinger KB (2003) Dlx proteins position the neural plate border and determine adjacent cell fates. Development 130:331–342PubMedPubMedCentralCrossRefGoogle Scholar
  102. Yang B, Jia L, Guo Q, Ren H, Hu D, Zhou X, Ren Q, Hu Y, Xie T (2015) MiR-564 functions as a tumor suppressor in human lung cancer by targeting ZIC3. Biochem Biophys Res Commun 467:690–696PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.International Institute of Molecular and Cell BiologyWarsawPoland
  2. 2.Max-Planck Institute for Heart and Lung ResearchBad NauheimGermany

Personalised recommendations