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Investigating Evolutionarily Conserved Molecular Mechanisms Controlling Gene Expression in the Notochord

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Transgenic Ascidians

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1029))

Abstract

Ascidian embryos have been employed as model systems for studies of developmental biology for well over a century, owing to their desirable blend of experimental advantages, which include their rapid development, traceable cell lineage, and evolutionarily conserved morphogenetic movements. Two decades ago, the development of a streamlined electroporation method drastically reduced the time and cost of transgenic experiments, and, along with the elucidation of the complete genomic sequences of several ascidian species, propelled these simple chordates to the forefront of the model organisms available for studies of regulation of gene expression. Numerous ascidian sequences with tissue-specific enhancer activity were isolated and rapidly characterized through systematic in vivo experiments that would require several weeks in most other model systems. These cis-regulatory sequences include a large collection of notochord enhancers, which have been used to visualize notochord development in vivo, to generate mutant phenotypes, and to knock down genes of interest. Moreover, their detailed characterization has allowed the reconstruction of different branches of the notochord gene regulatory network. This chapter describes how the use of transgenic techniques has rendered the ascidian Ciona a competitive model organism for studies of notochord development, evolution, and gene regulation.

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Abbreviations

bp:

Base pair(s)

cDNA:

Complementary DNA

ChIP:

Chromatin immunoprecipitation

CRM:

cis-regulatory module

DAPI:

4′,6-diamidino-2-phenylindole

FACS:

fluorescence-activated cell sorting

GFP:

Green fluorescent protein

GRN:

Gene regulatory network

NOCE:

Notochord enhancer

OBS:

Orphan binding site

P3H1:

prolyl 3-hydroxylase1

shRNA:

Short hairpin RNA

References

  • Adams RR, Tavares AA, Salzberg A, Bellen HJ, Glover DM (1998) Pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis. Genes Dev 12(10):1483–1494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alten L, Schuster-Gossler K, Eichenlaub MP, Wittbrodt B, Wittbrodt J, Gossler A (2012) A novel mammal-specific three partite enhancer element regulates node and notochord-specific Noto expression. PLoS One 7(10):e47785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ang SL, Rossant J (1994) HNF-3 beta is essential for node and notochord formation in mouse development. Cell 78:561–574

    Article  CAS  PubMed  Google Scholar 

  • Anno C, Satou A, Fujiwara S (2006) Transcriptional regulation of ZicL in the Ciona intestinalis embryo. Dev Genes Evol 216(10):597–605

    Article  CAS  PubMed  Google Scholar 

  • Bagheri-Fam S, Barrionuevo F, Dohrmann U, Günther T, Schüle R, Kemler R, Mallo M, Kanzler B, Scherer G (2006) Long-range upstream and downstream enhancers control distinct subsets of the complex spatiotemporal Sox9 expression pattern. Dev Biol 291(2):382–397

    Article  CAS  PubMed  Google Scholar 

  • Capellini TD, Dunn MP, Passamaneck YJ, Selleri L, Di Gregorio A (2008) Conservation of notochord gene expression across chordates: insights from the Leprecan gene family. Genesis 46(11):683–696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casey ES, O'Reilly MA, Conlon FL, Smith JC (1998) The T-box transcription factor Brachyury regulates expression of eFGF through binding to a non-palindromic response element. Development 125(19):3887–3894

    CAS  PubMed  Google Scholar 

  • Chiba S, Jiang D, Satoh N, Smith WC (2009) Brachyury null mutant-induced defects in juvenile ascidian endodermal organs. Development 136(1):35–39

    Article  CAS  PubMed  Google Scholar 

  • Christiaen L, Davidson B, Kawashima T, Powell W, Nolla H, Vranizan K, Levine M (2008) The transcription/migration interface in heart precursors of Ciona intestinalis. Science 320(5881):1349–1352

    Article  CAS  PubMed  Google Scholar 

  • Cleaver O, Krieg PA (2001) Notochord patterning of the endoderm. Dev Biol 234(1):1–12

    Article  CAS  PubMed  Google Scholar 

  • Cloney RA (1964) Development of the ascidian notochord. Acta Embryol Morphol Exp 7:111–130

    Google Scholar 

  • Conklin EG (1905) The organization and cell-lineage of the ascidian egg. J Acad Nat Sci 13:1–119

    Google Scholar 

  • Corbo JC, Levine M, Zeller RW (1997) Characterization of a notochord-specific enhancer from the Brachyury promoter region of the ascidian, Ciona intestinalis. Development 124(3):589–602

    CAS  PubMed  Google Scholar 

  • Corbo JC, Fujiwara S, Levine M, Di Gregorio A (1998) Suppressor of hairless activates brachyury expression in the Ciona embryo. Dev Biol 203(2):358–368

    Article  CAS  PubMed  Google Scholar 

  • Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, Davidson B, Di Gregorio A et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298(5601):2157–2167

    Article  CAS  PubMed  Google Scholar 

  • Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439(7079):965–968

    Article  CAS  PubMed  Google Scholar 

  • Denker E, Jiang D (2012) Ciona intestinalis notochord as a new model to investigate the cellular and molecular mechanisms of tubulogenesis. Semin Cell Dev Biol 23(3):308–319

    Article  CAS  PubMed  Google Scholar 

  • Denker E, Bocina I, Jiang D (2013) Tubulogenesis in a simple cell cord requires the formation of bi-apical cells through two discrete par domains. Development 140(14):2985–2996

    Article  CAS  PubMed  Google Scholar 

  • Denker E, Sehring IM, Dong B, Audisso J, Mathiesen B, Jiang D (2015) Regulation by a TGFβ-ROCK-actomyosin axis secures a non-linear lumen expansion that is essential for tubulogenesis. Development 142(9):1639–1650

    Article  CAS  PubMed  Google Scholar 

  • Deschet K, Nakatani Y, Smith WC (2003) Generation of ci-Brachyury-GFP stable transgenic lines in the ascidian Ciona savignyi. Genesis 35(4):248–259

    Article  CAS  PubMed  Google Scholar 

  • Di Gregorio A (2017) T-box genes and developmental gene regulatory networks in ascidians. Curr Top Dev Biol 122:55–91

    Article  PubMed  Google Scholar 

  • Di Gregorio A, Levine M (1999) Regulation of Ci-tropomyosin-like, a Brachyury target gene in the ascidian, Ciona intestinalis. Development 126(24):5599–5609

    PubMed  Google Scholar 

  • Di Gregorio A, Corbo JC, Levine M (2001) The regulation of forkhead/HNF-3beta expression in the Ciona embryo. Dev Biol 229(1):31–43

    Article  PubMed  Google Scholar 

  • Di Gregorio A, Harland RM, Levine M, Casey ES (2002) Tail morphogenesis in the ascidian, Ciona intestinalis, requires cooperation between notochord and muscle. Dev Biol 244(2):385–395

    Article  PubMed  Google Scholar 

  • Dong B, Deng W, Jiang D (2011) Distinct cytoskeleton populations and extensive crosstalk control Ciona notochord tubulogenesis. Development 138(8):1631–1641

    Article  CAS  PubMed  Google Scholar 

  • Dunn MP, Di Gregorio A (2009) The evolutionarily conserved leprecan gene: its regulation by Brachyury and its role in the developing Ciona notochord. Dev Biol 328(2):561–574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans AL, Faial T, Gilchrist MJ, Down T, Vallier L, Pedersen RA, Wardle FC, Smith JC (2012) Genomic targets of Brachyury (T) in differentiating mouse embryonic stem cells. PLoS One 7(3):e33346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farley EK, Olson KM, Zhang W, Rokhsar DS, Levine MS (2016) Syntax compensates for poor binding sites to encode tissue specificity of developmental enhancers. Proc Natl Acad Sci U S A 113(23):6508–6513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friedman JR, Kaestner KH (2006) The Foxa family of transcription factors in development and metabolism. Cell Mol Life Sci 63(19–20):2317–2328

    Article  CAS  PubMed  Google Scholar 

  • Gluecksohn-Schoenheimer S (1940) The effect of an early lethal (t) in the house mouse. Genetics 25(4):391–400

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hikosaka A, Kusakabe T, Satoh N, Makabe KW (1992) Introduction and expression of recombinant genes in ascidian embryos. Develop Growth Differ 34:631–638

    Article  Google Scholar 

  • Hikosaka A, Kusakabe T, Satoh N (1994) Short upstream sequences associated with the muscle-specific expression of an actin gene in ascidian embryos. Dev Biol 166:763–769

    Article  CAS  PubMed  Google Scholar 

  • Holland LZ, Laudet V, Schubert M (2004) The chordate amphioxus: an emerging model organism for developmental biology. Cell Mol Life Sci 61(18):2290–2308

    Article  CAS  PubMed  Google Scholar 

  • Hotta K, Takahashi H, Erives A, Levine M, Satoh N (1999) Temporal expression patterns of 39 Brachyury-downstream genes associated with notochord formation in the Ciona intestinalis embryo. Develop Growth Differ 41(6):657–664

    Article  CAS  Google Scholar 

  • Hotta K, Takahashi H, Asakura T, Saitoh B, Takatori N, Satou Y, Satoh N (2000) Characterization of Brachyury-downstream notochord genes in the Ciona intestinalis embryo. Dev Biol 224(1):69–80

    Article  CAS  PubMed  Google Scholar 

  • Hotta K, Mitsuhara K, Takahashi H, Inaba K, Oka K, Gojobori T, Ikeo K (2007a) A web-based interactive developmental table for the ascidian Ciona intestinalis, including 3D real-image embryo reconstructions: I. From fertilized egg to hatching larva. Dev Dyn 236(7):1790–1805

    Article  PubMed  Google Scholar 

  • Hotta K, Yamada S, Ueno N, Satoh N, Takahashi H (2007b) Brachyury-downstream notochord genes and convergent extension in Ciona intestinalis embryos. Develop Growth Differ 49(5):373–382

    Article  CAS  Google Scholar 

  • Hotta K, Takahashi H, Satoh N, Gojobori T (2008) Brachyury-downstream gene sets in a chordate, Ciona intestinalis: integrating notochord specification, morphogenesis and chordate evolution. Evol Dev 10(1):37–51

    Article  CAS  PubMed  Google Scholar 

  • Imai KS, Hino K, Yagi K, Satoh N, Satou Y (2004) Gene expression profiles of transcription factors and signaling molecules in the ascidian embryo: towards a comprehensive understanding of gene networks. Development 131(16):4047–4058

    Article  CAS  PubMed  Google Scholar 

  • Imai KS, Levine M, Satoh N, Satou Y (2006) Regulatory blueprint for a chordate embryo. Science 312(5777):1183–1187

    Article  CAS  PubMed  Google Scholar 

  • Irvine SQ (2013) Study of cis-regulatory elements in the Ascidian Ciona intestinalis. Curr Genomics 14(1):56–67

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jeffery WR, Ewing N, Machula J, Olsen CL, Swalla BJ (1998) Cytoskeletal actin genes function downstream of HNF-3beta in ascidian notochord development. Int J Dev Biol 42(8):1085–1092

    CAS  PubMed  Google Scholar 

  • Jeong Y, Epstein DJ (2003) Distinct regulators of Shh transcription in the floor plate and notochord indicate separate origins for these tissues in the mouse node. Development 130(16):3891–3902

    Article  CAS  PubMed  Google Scholar 

  • Jiang D, Smith WC (2007) Ascidian notochord morphogenesis. Dev Dyn 236(7):1748–1757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang D, Munro EM, Smith WC (2005) Ascidian prickle regulates both mediolateral and anterior-posterior cell polarity of notochord cells. Curr Biol 15(1):79–85

    Article  CAS  PubMed  Google Scholar 

  • José-Edwards DS, Kerner P, Kugler JE, Deng W, Jiang D, Di Gregorio A (2011) The identification of transcription factors expressed in the notochord of Ciona intestinalis adds new potential players to the brachyury gene regulatory network. Dev Dyn 240(7):1793–1805

    Article  PubMed  PubMed Central  Google Scholar 

  • José-Edwards DS, Oda-Ishii I, Nibu Y, Di Gregorio A (2013) Tbx2/3 is an essential mediator within the Brachyury gene network during Ciona notochord development. Development 140(11):2422–2433

    Article  PubMed  PubMed Central  Google Scholar 

  • José-Edwards DS, Oda-Ishii I, Kugler JE, Passamaneck YJ, Katikala L, Nibu Y, Di Gregorio A (2015) Brachyury, Foxa2 and the cis-Regulatory Origins of the Notochord. PLoS Genet 11(12):e1005730

    Google Scholar 

  • Katikala L, Aihara H, Passamaneck YJ, Gazdoiu S, José-Edwards DS, Kugler JE, Oda-Ishii I, Imai JH, Nibu Y, Di Gregorio A (2013) Functional Brachyury binding sites establish a temporal read-out of gene expression in the Ciona notochord. PLoS Biol 11(10):e1001697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kispert A, Koschorz B, Herrmann BG (1995) The T protein encoded by Brachyury is a tissue-specific transcription factor. EMBO J 14(19):4763–4772

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kubo A, Suzuki N, Yuan X, Nakai K, Satoh N, Imai KS, Satou Y (2010) Genomic cis-regulatory networks in the early Ciona intestinalis embryo. Development 137(10):1613–1623

    Article  CAS  PubMed  Google Scholar 

  • Kumano G, Yamaguchi S, Nishida H (2006) Overlapping expression of FoxA and Zic confers responsiveness to FGF signaling to specify notochord in ascidian embryos. Dev Biol 300(2):770–784

    Article  CAS  PubMed  Google Scholar 

  • Lacalli T (2012) The Middle Cambrian fossil Pikaia and the evolution of chordate swimming. Evodevo 3(1):12

    Google Scholar 

  • Lawson L, Harfe BD (2015) Notochord to nucleus pulposus transition. Curr Osteoporos Rep 13(5):336–341

    Article  PubMed  Google Scholar 

  • Lemaire P (2009) Unfolding a chordate developmental program, one cell at a time: invariant cell lineages, short-range inductions and evolutionary plasticity in ascidians. Dev Biol 332(1):48–60

    Article  CAS  PubMed  Google Scholar 

  • Levine M (2010) Transcriptional enhancers in animal development and evolution. Curr Biol 20(17):R754–R763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu GH, Mao CZ, Wu HY, Zhou DC, Xia JB, Kim SK, Cai DQ, Zhao H, Qi XF (2016) Expression profile of rrbp1 genes during embryonic development and in adult tissues of Xenopus laevis. Gene Expr Patterns 23–24:1–6

    PubMed  Google Scholar 

  • Mallatt J, Holland N (2013) Pikaia gracilens Walcott: stem chordate, or already specialized in the Cambrian? J Exp Zool B Mol Dev Evol 320:247–271

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Miyamoto DM, Crowther RJ (1985) Formation of the notochord in living ascidian embryos. J Embryol Exp Morphol 86:1–17

    CAS  PubMed  Google Scholar 

  • Morris SC, Caron JB (2012) Pikaia gracilens Walcott, a stem-group chordate from the middle Cambrian of British Columbia. Biol Rev Camb Philos Soc 87:480–512

    Article  PubMed  Google Scholar 

  • Müller F, Chang B, Albert S, Fischer N, Tora L, Strähle U (1999) Intronic enhancers control expression of zebrafish sonic hedgehog in floor plate and notochord. Development 126(10):2103–2116

    PubMed  Google Scholar 

  • Myllyharju J, Kivirikko KI (1997) Characterization of the iron- and 2-oxoglutarate-binding sites of human prolyl 4-hydroxylase. EMBO J 16(6):1173–1180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newman-Smith E, Kourakis MJ, Reeves W, Veeman M, Smith WC (2015) Reciprocal and dynamic polarization of planar cell polarity core components and myosin. Elife 13(4):e05361

    Google Scholar 

  • Nibu Y, José-Edwards DS, Di Gregorio A (2013) From notochord formation to hereditary chordoma: the many roles of Brachyury. Biomed Res Int 2013:826435

    Article  PubMed  PubMed Central  Google Scholar 

  • Nishida H, Satoh N (1983) Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. I. Up to the eight-cell stage. Dev Biol 99:382–394

    Article  CAS  PubMed  Google Scholar 

  • Nishida H, Satoh N (1985) Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. II. The 16- and 32-cell stages. Dev Biol 110:440–454

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama A, Fujiwara S (2008) RNA interference by expressing short hairpin RNA in the Ciona intestinalis embryo. Develop Growth Differ 50(6):521–529

    Article  CAS  Google Scholar 

  • Oda-Ishii I, Di Gregorio A (2007) Lineage-independent mosaic expression and regulation of the Ciona multidom gene in the ancestral notochord. Dev Dyn 236(7):1806–1819

    Article  CAS  PubMed  Google Scholar 

  • Olsen CL, Jeffery WR (1997) A forkhead gene related to HNF-3beta is required for gastrulation and axis formation in the ascidian embryo. Development 124(18):3609–3619

    CAS  PubMed  Google Scholar 

  • Ortolani G (1954) Risultati definitive sulla distribuzione dei territory presuntivi degli organi nel germe di Ascidie allo stadio VIII, determinati con le marche al carbone. Pubbl Staz Zool Napoli 25:161–187

    Google Scholar 

  • Passamaneck YJ, Di Gregorio A (2005) Ciona intestinalis: chordate development made simple. Dev Dyn 233(1):1–19

    Article  CAS  PubMed  Google Scholar 

  • Passamaneck YJ, Katikala L, Perrone L, Dunn MP, Oda-Ishii I, Di Gregorio A (2009) Direct activation of a notochord cis-regulatory module by Brachyury and FoxA in the ascidian Ciona intestinalis. Development 136(21):3679–3689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rastegar S, Hess I, Dickmeis T, Nicod JC, Ertzer R, Hadzhiev Y, Thies WG, Scherer G, Strähle U (2008) The words of the regulatory code are arranged in a variable manner in highly conserved enhancers. Dev Biol 318(2):366–377

    Article  CAS  PubMed  Google Scholar 

  • Reese DE, Hall CE, Mikawa T (2004) Negative regulation of midline vascular development by the notochord. Dev Cell 6(5):699–708

    Article  CAS  PubMed  Google Scholar 

  • Reverberi G (1971) Ascidians. In: Reverberi G (ed) Experimental embryology of marine and fresh-water invertebrates. North-Holland, Amsterdam, pp 507–550

    Google Scholar 

  • Rhee JM, Oda-Ishii I, Passamaneck YJ, Hadjantonakis AK, Di Gregorio A (2005) Live imaging and morphometric analysis of embryonic development in the ascidian Ciona intestinalis. Genesis 43(3):136–147

    Article  PubMed  Google Scholar 

  • Sasaki H, Hogan BL (1993) Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118(1):47–59

    CAS  PubMed  Google Scholar 

  • Sasaki H, Yoshida K, Hozumi A, Sasakura Y (2014) CRISPR/Cas9-mediated gene knockout in the ascidian Ciona intestinalis. Develop Growth Differ 56(7):499–510

    Article  CAS  Google Scholar 

  • Sasakura Y, Suzuki MM, Hozumi A, Inaba K, Satoh N (2010) Maternal factor-mediated epigenetic gene silencing in the ascidian Ciona intestinalis. Mol Gen Genomics 283(1):99–110

    Article  CAS  Google Scholar 

  • Satoh N, Tagawa K, Takahashi H (2012) How was the notochord born? Evol Dev 14(1):56–75

    Article  CAS  PubMed  Google Scholar 

  • Sawada A, Nishizaki Y, Sato H, Yada Y, Nakayama R et al (2005) Tead proteins activate the Foxa2 enhancer in the node in cooperation with a second factor. Development 132:4719–4729

    Article  CAS  PubMed  Google Scholar 

  • Segade F, Cota C, Famiglietti A, Cha A, Davidson B (2016) Fibronectin contributes to notochord intercalation in the invertebrate chordate, Ciona intestinalis. EvoDevo 7(1):21

    Article  PubMed  PubMed Central  Google Scholar 

  • Sehring IM, Dong B, Denker E, Bhattachan P, Deng W, Mathiesen BT, Jiang D (2014) An equatorial contractile mechanism drives cell elongation but not cell division. PLoS Biol 12(2):e1001781

    Article  PubMed  PubMed Central  Google Scholar 

  • Sehring IM, Recho P, Denker E, Kourakis M, Mathiesen B, Hannezo E, Dong B, Jiang D (2015) Assembly and positioning of actomyosin rings by contractility and planar cell polarity. Elife 21(4):e09206

    Google Scholar 

  • Smith J (1999) T-box genes: what they do and how they do it. Trends Genet 15(4):154–158

    Article  CAS  PubMed  Google Scholar 

  • Søviknes AM, Glover JC (2008) Continued growth and cell proliferation into adulthood in the notochord of the appendicularian Oikopleura dioica. Biol Bull 214(1):17–28

    Article  PubMed  Google Scholar 

  • Stemple DL (2005) Structure and function of the notochord: an essential organ for chordate development. Development 132:2503–2512

    Article  CAS  PubMed  Google Scholar 

  • Stolfi A, Christiaen L (2012) Genetic and genomic toolbox of the chordate Ciona intestinalis. Genetics 192(1):55–66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stolfi A, Gandhi S, Salek F, Christiaen L (2014) Tissue-specific genome editing in Ciona embryos by CRISPR/Cas9. Development 141(21):4115–4120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tada M, Casey ES, Fairclough L, Smith JC (1998) Bix1, a direct target of Xenopus T-box genes, causes formation of ventral mesoderm and endoderm. Development 125(20):3997–4006

    CAS  PubMed  Google Scholar 

  • Takada N, Satoh N, Swalla BJ (2002) Expression of Tbx6, a muscle lineage T-box gene, in the tailless embryo of the ascidian Molgula tectiformis. Dev Genes Evol 212:354–356

    Article  CAS  PubMed  Google Scholar 

  • Takahashi H, Hotta K, Erives A, Di Gregorio A, Zeller RW, Levine M, Satoh N (1999) Brachyury downstream notochord differentiation in the ascidian embryo. Genes Dev 13(12):1519–1523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi H, Hotta K, Takagi C, Ueno N, Satoh N, Shoguchi E (2010) Regulation of notochord-specific expression of Ci-Bra downstream genes in Ciona intestinalis embryos. Zool Sci 27(2):110–118

    Article  CAS  PubMed  Google Scholar 

  • Tamplin OJ, Cox BJ, Rossant J (2011) Integrated microarray and ChIP analysis identifies multiple Foxa2 dependent target genes in the notochord. Dev Biol 360(2):415–425

    Article  CAS  PubMed  Google Scholar 

  • Thompson JM, Di Gregorio A (2015) Insulin-like genes in ascidians: findings in Ciona and hypotheses on the evolutionary origins of the pancreas. Genesis 53(1):82–104

    Article  CAS  PubMed  Google Scholar 

  • Urry LA, Whittaker CA, Duquette M, Lawler J, DeSimone DW (1998) Thrombospondins in early Xenopus embryos: dynamic patterns of expression suggest diverse roles in nervous system, notochord, and muscle development. Dev Dyn 211:390–407

    Article  CAS  PubMed  Google Scholar 

  • Veeman MT, Nakatani Y, Hendrickson C, Ericson V, Lin C, Smith WC (2008) Chongmague reveals an essential role for laminin-mediated boundary formation in chordate convergence and extension movements. Development 135(1):33–41

    Article  CAS  PubMed  Google Scholar 

  • Wada H, Okuyama M, Satoh N, Zhang S (2006) Molecular evolution of fibrillar collagen in chordates, with implications for the evolution of vertebrate skeletons and chordate phylogeny. Evol Dev 8:370–377

    Article  CAS  PubMed  Google Scholar 

  • Weisblat DA, Sawyer RT, Stent GS (1978) Cell lineage analysis by intracellular injection of a tracer enzyme. Science 202:1295–1298

    Article  CAS  PubMed  Google Scholar 

  • Yagi K, Satou Y, Satoh N (2004) A zinc finger transcription factor, ZicL, is a direct activator of Brachyury in the notochord specification of Ciona intestinalis. Development 131(6):1279–1288

    Article  CAS  PubMed  Google Scholar 

  • Yamada S, Ueno N, Satoh N, Takahashi H (2011) Ciona intestinalis Noto4 contains a phosphotyrosine interaction domain and is involved in the midline intercalation of notochord cells. Int J Dev Biol 55(1):11–18

    Article  CAS  PubMed  Google Scholar 

  • Yasuo H, Satoh N (1993) Function of vertebrate T gene. Nature 364(6438):582–583

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Thanks to all present and past laboratory members and collaborators. We are particularly indebted to Drs. Diana José-Edwards, Lavanya Katikala, Izumi Oda-Ishii, and Yale Passamaneck for their original microphotographs. Research in our laboratory is supported by the National Institute of General Medical Sciences of the National Institutes of Health under award number R01GM100466.

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Maguire, J.E., Pandey, A., Wu, Y., Di Gregorio, A. (2018). Investigating Evolutionarily Conserved Molecular Mechanisms Controlling Gene Expression in the Notochord. In: Sasakura, Y. (eds) Transgenic Ascidians . Advances in Experimental Medicine and Biology, vol 1029. Springer, Singapore. https://doi.org/10.1007/978-981-10-7545-2_8

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