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Upstream Regulatory Region of Zebrafish lunatic fringe: Isolation and Promoter Analysis

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Abstract

Lunatic fringe (Lfng), one modulator of Notch signaling, plays an essential part in demarcation of tissues boundaries during animal early development, especially somitogenesis. To characterize the promoter of zebrafish lfng and generate somite-specific transgenic zebrafish, we isolated the upstream regulatory region of zebrafish lfng by blast search at the Ensembl genome database (http://www.ensembl.org) and analyzed the promoter activity using green fluorescent protein (GFP) as a reporter. Promoter activity assay in zebrafish shows that the 0.2-kb fragment containing GC-box, CAAT-box, and TATA-box can direct tissue-specific GFP expression, while the 0.4-kb and 1.2-kb fragments with further upstream sequence included drive GFP expression more efficiently. We produced lfngEGFP-transgenic founders showing somite-specific expression of GFP and consequently generated a hemizygous lfngEGFP-transgenic line. The eggs from lfngEGFP-transgenic female zebrafish show strong GFP expression, which is consistent to the reverse-transcription polymerase chain reaction PCR (RT-PCR) detection of lfng transcripts in the fertilized eggs. This reveals that zebrafish lfng is a maternal factor existing in matured eggs, suggesting that fish somitogenesis may be influenced by maternal factors.

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References

  • A Amsterdam S Lin N Hopkins (1995) ArticleTitleThe Aequorea victoria green fluorescent protein can be used as a reporter in live zebrafish embryos Dev Biol 171 123–129 Occurrence Handle10.1006/dbio.1995.1265

    Article  Google Scholar 

  • B Appel P Marasco LE McClung AJ Latimer (2003) ArticleTitleLunatic fringe regulates Delta-Notch induction of hypochord in zebrafish Dev Dyn 228 281–286 Occurrence Handle10.1002/dvdy.10375

    Article  Google Scholar 

  • A Astola JA Calduch-Giner M Ortiz J Perez-Sanchez MM Valdivia (2004) ArticleTitleGenomic structure and functional analysis of promoter region of somatolactin gene of sea bream (Sparus aurata) Mar Biotechnol 6 411–418 Occurrence Handle10.1007/s10126-004-3210-2

    Article  Google Scholar 

  • A Aulehla RL Johnson (1999) ArticleTitleDynamic expression of lunatic fringe suggests a link between notch signaling and an autonomous cellar oscillator driving somite segmentation Dev Biol 207 49–61 Occurrence Handle10.1006/dbio.1998.9164

    Article  Google Scholar 

  • K Bruckner L Perez H Clausen S Cohen (2000) ArticleTitleGlycosyltransferase activity of Fringe modulates Notch-Delta interactions Nature 406 411–415 Occurrence Handle10.1038/35019075

    Article  Google Scholar 

  • CW Chen CM Chuong (2000) ArticleTitleDynamic expression of lunatic fringe during feather morphogenesis: a switch from medial-lateral to anterior-posterior asymmetry Mech Dev 91 351–354 Occurrence Handle10.1016/S0925-4773(99)00285-3

    Article  Google Scholar 

  • B Cohen A Bashirullah L Dagnino C Campbell WW Fisher CC Leon E Whiting D Ryan D Zinyk G Boulianne CC Hui B Gallie RA Phillips HD Lipshitz SE Egan (1997) ArticleTitleFringe boundaries coincide with notch-dependent patterning centres in mammals and alter Notch-dependent development in Drosophila Nat Genet 16 283–288 Occurrence Handle10.1038/ng0797-283

    Article  Google Scholar 

  • LK Cole I Roux ParticleLe F Nunes E Laufer J Lewis DK Wu (2000) ArticleTitleSensory organ generation in the chicken inner ear: contributions of bone morphogenetic protein 4, Serrate1, and Lunatic fringe J Comp Neurol 424 509–520 Occurrence Handle10.1002/1096-9861(20000828)424:3<509::AID-CNE8>3.0.CO;2-Q

    Article  Google Scholar 

  • SE Cole JM Levorse SM Tilghman TF Vogt (2002) ArticleTitleClock regulatory elements control cyclic expression of Lunatic fringe during somitogenesis Dev Cell 3 75–84 Occurrence Handle10.1016/S1534-5807(02)00212-5

    Article  Google Scholar 

  • O Couronne A Poliakov N Bray T Ishkhanov D Ryaboy E Rubin L Pachter I Dubchak (2003) ArticleTitleStrategies and tools for whole-genome alignments Genome Res 13 73–80 Occurrence Handle10.1101/gr.762503

    Article  Google Scholar 

  • JK Dale M Maroto ML Dequeant P Malapert M McGrew O Pourquie (2003) ArticleTitlePeriodic notch inhibition by lunatic fringe underlies the chick segmentation clock Nature 421 275–278 Occurrence Handle10.1038/nature01244

    Article  Google Scholar 

  • YA Evrard Y Lun A Aulehla L Gan RL John (1998) ArticleTitleLunatic fringe is an essential mediator of somite segmentation and patterning Nature 394 377–381 Occurrence Handle10.1038/28034

    Article  Google Scholar 

  • B Favier I Fliniaux J Thelu JP Viallet M Demarchez CA Jahoda D Dhouailly (2000) ArticleTitleLocalization of members of the notch system and the differentiation of vibrissa hair follicles: receptors, ligands, and fringe modulators Dev Dyn 218 426–437 Occurrence Handle10.1002/1097-0177(200007)218:3<426::AID-DVDY1004>3.0.CO;2-4

    Article  Google Scholar 

  • RJ Fleming Y Gu NA Hukriede (1997) ArticleTitleSerrate-mediated activation of Notch is specifically blocked by the product of the gene fringe in the dorsal compartment of the Drosophila wing imaginal disc Development 124 2973–2981

    Google Scholar 

  • H Forsberg F Crozet NA Brown (1998) ArticleTitleWaves of mouse Lunatic fringe expression, in four-hour cycles at two-hour internals, precede somite boundary formation Curr Biol 8 1027–1030 Occurrence Handle10.1016/S0960-9822(07)00424-1

    Article  Google Scholar 

  • PD Gibbs MC Schmale (2000) ArticleTitleGFP as a genetic marker scorable throughout the life cycle of transgenic zebrafish Mar Biotechnol 2 107–125

    Google Scholar 

  • F Giudicelli J Lewis (2004) ArticleTitleThe vertebrate segmentation clock Curr Opin Genet Dev 14 407–414 Occurrence Handle10.1016/j.gde.2004.06.014

    Article  Google Scholar 

  • K Hamada K Tamaki T Sasado Y Watai S Kani Y Wakamatsu K Ozato M Kinoshita R Kohno S Takagi M Kimura (1998) ArticleTitleUsefulness of the medaka beta-actin promoter investigated using a mutant GFP reporter gene in transgenic medaka (Oryzias latipes) Mol Mar Biol Biotechnol 7 173–180

    Google Scholar 

  • S Higashijima H Okamoto N Ueno Y Hotta G Eguchi (1997) ArticleTitleHigh-frequency generation of transgenic zebrafish which reliably express GFP in whole muscles or the whole body by using promoters of zebrafish origin Dev Biol 192 289–299 Occurrence Handle10.1006/dbio.1997.8779

    Article  Google Scholar 

  • SA Holly R Geisler C Nusslein-Volhard (2000) ArticleTitleControl of her1 expression during zebrafish somatogenesis by a delta-dependent oscillator and an independent wave-front activity Genes Dev 14 1678–1690

    Google Scholar 

  • KD Irvine E Wieschaus N Osumi (1994) ArticleTitleFringe, a boundary-specific signaling molecule, mediates interactions between dorsal and ventral cells during Drosophila wing development. Cell 79 595–606 Occurrence Handle10.1016/0092-8674(94)90545-2

    Article  Google Scholar 

  • Y Ishii S Nakamura N Osumi (2000) ArticleTitleDemarcation of early mammalian cortical development by differential expression of fringe genes Brain Res Dev Brain Res 119 307–320 Occurrence Handle10.1016/S0165-3806(99)00186-8

    Article  Google Scholar 

  • A Ishikawa S Kitajima Y Takahashi H Kokubo J Kanno T Inoue Y Saga (2004) ArticleTitleMouse Nkd1, a Wnt antagonist, exhibits oscillatory gene expression in the PSM under the control of Notch signaling Mech Dev 121 1443–1453 Occurrence Handle10.1016/j.mod.2004.08.003

    Article  Google Scholar 

  • SH Johnson C Rauskolb R Wilson B Prabhakaran KD Irvine TF Vogt (1997) ArticleTitleA family of mammalian Fringe genes implicated in boundary determination and the Notch pathway Development 124 2245–2254

    Google Scholar 

  • M Kinoshita S Kani K Ozato Y Wakamatsu (2000) ArticleTitleActivity of the medaka translation elongation factor 1alpha-A promoter examined using the GFP gene as a reporter Dev Growth Differ 42 469–478 Occurrence Handle10.1046/j.1440-169x.2000.00530.x

    Article  Google Scholar 

  • E Laufer R Dahn OE Orozco CY Yeo J Pisenti D Henrique UK Abbott JF Fallon C Tabin (1997) ArticleTitleExpression of Radical fringe in limb-bud ectoderm regulates apical ectodermal ridge formation Nature 386 366–373 Occurrence Handle10.1038/386366a0

    Article  Google Scholar 

  • C Leve M Gajewski KB Rohr D Tautz (2001) ArticleTitleHomologues of c-hairy1 (her9) and lunatic fringe in zebrafish are expressed in the developing central nervous system, but not in the presomitic mesoderm Dev Genes Evol 211 493–500 Occurrence Handle10.1007/s00427-001-0181-4

    Article  Google Scholar 

  • MJ McGrew JK Dale S Fraboulet O Pourquie (1998) ArticleTitleThe lunatic fringe gene is a target of the molecular clock linked to somite segmentation in avian embryos Curr Biol 8 979–982 Occurrence Handle10.1016/S0960-9822(98)70401-4

    Article  Google Scholar 

  • AE Melby RM Warga CB Kimmel (1996) ArticleTitleSpecification of cell fates at the dorsal margin of the zebrafish gastrula Development 122 2225–2237

    Google Scholar 

  • A Meng S Lin (2000) ArticleTitleGeneration of germ-line transgenic zebrafish expressing GFP in a tissue-specific manner by using GATA-2 regulatory sequences Chin Sci Bull 45 31–34 Occurrence Handle10.1007/BF02884898

    Article  Google Scholar 

  • A Meng H Tang BA Ong MJ Farrell S Lin (1997) ArticleTitlePromoter analysis in living zebrafish embryos identifies a cis-acting motif required for neuronal expression of GATA-2 Proc Natl Acad Sci USA 94 6267–6272 Occurrence Handle10.1073/pnas.94.12.6267

    Article  Google Scholar 

  • DJ Moloney VM Panin SH Johnston J Chen L Shao R Wilson Y Wang P Stanley KD Irvine RS Haltiwanger TF Vogt (2000) ArticleTitleFringe is a glycosyltransferase that modifies Notch Nature 406 369–375 Occurrence Handle10.1038/35019000

    Article  Google Scholar 

  • L Pouyet TA Mitsiadis (2000) ArticleTitleDynamic Lunatic fringe expression is correlated with boundaries formation in developing mouse teeth Mech Dev 91 399–402 Occurrence Handle10.1016/S0925-4773(99)00299-3

    Article  Google Scholar 

  • VE Prince SA Holley L Bally-Cuif B Prabhakaran AC Oates RK Ho TF Vogt (2001) ArticleTitleZebrafish lunatic fringe demarcates segmental boundaries Mech Dev 105 175–180 Occurrence Handle10.1016/S0925-4773(01)00398-7

    Article  Google Scholar 

  • X Qiu H Xu C Haddon J Lewis YJ Jiang (2004) ArticleTitleSequence and embryonic expression of three zebrafish fringe genes: lunatic fringe, radical fringe, and manic fringe Dev Dyn 231 621–630 Occurrence Handle10.1002/dvdy.20155

    Article  Google Scholar 

  • K Sakamoto L Yan H Imai M Takagi Y Nabeshima S Takeda K Katsube (1997) ArticleTitleIdentification of a chick homologue of Fringe and C-Fringe 1: involvement in the neurogenesis and the somitogenesis Biochem Biophys Res Commun 234 754–759 Occurrence Handle10.1006/bbrc.1997.6652

    Article  Google Scholar 

  • K Serth K Schuster-Gossler R Cordes A Gossler (2003) ArticleTitleTranscriptional oscillation of lunatic fringe is essential for somitogenesis Genes Dev 17 912–925 Occurrence Handle10.1101/gad.250603

    Article  Google Scholar 

  • SE Stachel DJ Grunwald PZ Myers (1993) ArticleTitleLithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish Development 117 1261–1274

    Google Scholar 

  • YH Sun SP Chen YP Wang W Hu ZY Zhu (2005) ArticleTitleCytoplasmic impact on cross-genus cloned fish derived from transgenic common carp (Cyprinus carpio) nuclei and goldfish (Carassius auratus) enucleated eggs Biol Reprod 72 510–515 Occurrence Handle10.1095/biolreprod.104.031302

    Article  Google Scholar 

  • M Syed O Vestrheim B Mikkelsen M Lundin (2003) ArticleTitleIsolation of the promoters of Atlantic salmon MHCII genes Mar Biotechnol 5 253–260 Occurrence Handle10.1007/s10126-002-0063-4

    Article  Google Scholar 

  • P Teng Y Cao WX Wang SX Zhu AM Meng JP Zhang (2004) ArticleTitleThe shh promoter of zebrafish directs the expression of GFP in notochord Yi Chuan Xue Bao 31 39–42

    Google Scholar 

  • J Thelu P Rossio B Favier (2002) ArticleTitleNotch signalling is linked to epidermal cell differentiation level in basal cell carcinoma, psoriasis and wound healing BMC Dermatol 2 7 Occurrence Handle10.1186/1471-5945-2-7

    Article  Google Scholar 

  • FJ Eeden Particlevan M Granato U Schach M Brand M Furutani-Seiki P Haffter M Hammerschmidt CP Heisenberg YJ Jiang DA Kane RN Kelsh MC Mullins J Odenthal RM Warga ML Allende ES Weinberg C Nusslein-Volhard (1996) ArticleTitleMutations affecting somite formation and patterning in zebrafish Danio rerio Development 123 153–164

    Google Scholar 

  • K Woo SE Fraser (1995) ArticleTitleOrder and coherence in the fate map of the zebrafish nervous system Development 121 2595–2609

    Google Scholar 

  • JY Wu L Wen WJ Zhang Y Rao (1996) ArticleTitleThe secreted product of Xenopus gene lunatic Fringe, a vertebrate signaling molecule Science 273 355–358

    Google Scholar 

  • Yazawa R, Hirono I, Aoki T (2005a) Characterization of promoter activities of four different Japanese flounder promoters in transgenic zebrafish. Mar Biotechnol 21 7, 625–633

    Google Scholar 

  • R Yazawa I Hirono T Ohria T Aoki (2005a) ArticleTitleInduction of Japanese flounder tnf promoter activity by lipopolysaccharide in zebrafish embryo Mar Biotechnol 7 231–235 Occurrence Handle10.1007/s10126-004-0403-7

    Article  Google Scholar 

  • LM Zeltser CW Larsen A Lumsden (2001) ArticleTitleA new developmental compartment in the forebrain regulated by Lunatic fringe Nat Neurosci 4 683–684 Occurrence Handle10.1038/89455

    Article  Google Scholar 

  • N Zhang T Gridley (1998) ArticleTitleDefects in somite formation in lunatic fringe-deficient mice Nature 394 374–377 Occurrence Handle10.1038/28625

    Article  Google Scholar 

  • N Zhang GV Martin MW Kelley T Gridley (2000) ArticleTitleA mutation in the Lunatic fringe gene suppresses the effects of a Jagged2 mutation on inner hair cell development in the cochlea Curr Biol 10 659–662 Occurrence Handle10.1016/S0960-9822(00)00522-4

    Article  Google Scholar 

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Acknowledgments

We are grateful to Ming Li for taking care of the experimental fish. This work was supported by the State Key Fundamental Research of China (grant no. 2004CB117406 and G2000016109) and the National Natural Science Foundation of China (grant nos. 90208024 and 30123004).

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Authors and Affiliations

  1. State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China

    Jing Liu, Yong-Hua Sun, Na Wang, Ya-Ping Wang & Zuo-Yan Zhu

  2. Graduate School of the Chinese Academy of Sciences, Beijing, 100039, China

    Jing Liu & Na Wang

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  1. Jing Liu
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  2. Yong-Hua Sun
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  3. Na Wang
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  4. Ya-Ping Wang
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Correspondence to Zuo-Yan Zhu.

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★These authors contributed equally to this work.

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Liu, J., Sun, YH., Wang, N. et al. Upstream Regulatory Region of Zebrafish lunatic fringe: Isolation and Promoter Analysis. Mar Biotechnol 8, 357–365 (2006). https://doi.org/10.1007/s10126-005-5125-y

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