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JOURNAL ARTICLES
Expression of the LIM class homeobox gene Xlim-1 in pronephros and CNS cell lineages of Xenopus embryos is affected by retinoic acid and exogastrulation
M. Taira, H. Otani, M. Jamrich, I.B. Dawid
Development 1994 120: 1525-1536;

Summary

The LIM class homeobox gene Xlim-1 is expressed in Xenopus embryos in the lineages leading to (i) the notochord, (ii) the pronephros, and (iii) certain cells of the central nervous system (CNS). In its first expression phase, Xlim-1 mRNA arises in the Spemann organizer region, accumulates in prechordal mesoderm and notochord during gastrulation, and decays in these tissues during neurula stages except that it persists in the posterior tip of the notochord. In the second phase, expression in lateral mesoderm begins at late gastrula, and converges to the pronephros at tailbud stages. Expression in a central location of the neural plate also initiates at late gastrula, expands anteriorly and posteriorly, and becomes established in the lateral regions of the spinal cord and hindbrain at tailbud stages. Thus Xlim-1 expression precedes morphogenesis, suggesting that it may be involved in cell specification in these lineages. Enhancement of Xlim-1 expression by retinoic acid (RA) was first detectable in the dorsal mesoderm at initial gastrula. During gastrulation and early neurulation, RA strongly enhanced Xlim-1 expression in all three lineages and also expanded its expressing domains; this overexpression correlated well with RA phenotypes such as enlarged pronephros and hindbrain-like structure. Exogastrulation reduced Xlim-1 expression in the lateral mesoderm and ectoderm but not in the notochord, suggesting that the second phase of Xlim-1 expression requires mesoderm/ectoderm interactions. RA treatment of exogastrulae did not revert this reduction.

REFERENCES

    1. Bolce M. E.,
    2. Hemmati-Brivanlou A.,
    3. Kushner P. D.,
    4. Harland R. M.
    (1992) Ventral ectoderm of Xenopus forms neural tissue, including hindbrain, in response to activin. Development 115, 681–688
    OpenUrlAbstract
    1. Boncinelli E.,
    2. Simeone A.,
    3. Acampora D.,
    4. Mavilio F.
    (1991) HOX gene activation by retinoic acid. Trends Genet 7, 329–334
    OpenUrlCrossRefPubMedWeb of Science
    1. Bourgouin C.,
    2. Lundgren S. E.,
    3. Thomas J. B.
    (1992) apterous is a Drosophila LIM domain gene required for the development of a subset of embryonic muscles. Neuron 9, 549–561
    OpenUrlCrossRefPubMedWeb of Science
    1. Bradley L. C.,
    2. Snape A.,
    3. Bhatt S.,
    4. Wilkinson D. G.
    (1992) The structure and expression of the XenopusKrox-20 gene: conserved and divergent patterns of expression in rhombomeres and neural crest. Mech. Dev 40, 73–84
    OpenUrl
    1. Chalfie M.,
    2. Au M.
    (1989) Genetic control of differentiation of the Caenorhabditiselegans touch receptor neurons. Science 243, 1027–1033
    OpenUrlAbstract/FREE Full Text
    1. Chalfie M.,
    2. Sulston J.
    (1981) Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev. Biol 82, 358–370
    OpenUrlCrossRefPubMedWeb of Science
    1. Cho K. W. Y.,
    2. Blumberg B.,
    3. Steinbeisser H.,
    4. De Robertis E. M.
    (1991) Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. Cell 67, 1111–1120
    OpenUrlCrossRefPubMedWeb of Science
    1. Christ B.,
    2. Brand-Saberi B.,
    3. Grim M.,
    4. Wilting J.
    (1992) Local signalling in dermomyotomal cell type specification. Anat. Embryol 186, 505–510
    OpenUrlPubMed
    1. Cohen B.,
    2. McGuffin M. E.,
    3. Pfeifle C.,
    4. Segal D.,
    5. Cohen S. M.
    (1992) apterous, a gene required for imaginal disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins. Genes Dev 6, 715–729
    OpenUrlAbstract/FREE Full Text
    1. Dekker E.-J.,
    2. Pannese M.,
    3. Houtzager E.,
    4. Boncinelli E.,
    5. Durston A.
    (1992) Colinearity in the XenopuslaevisHox-2 complex. Mech. Dev 40, 3–12
    1. Dirksen M. L.,
    2. Jamrich M.
    (1992) A novel, activin-inducible, blastopore lip-specific gene of Xenopuslaevis contains a fork head DNA-binding domain. Genes Dev 6, 599–608
    OpenUrlAbstract/FREE Full Text
    1. Dirksen M.-L.,
    2. Mathers P.,
    3. Jamrich M.
    (1993) Expression of a Xenopus Distal-less homeobox gene involved in forebrain and cranio-facial development. Mech. Dev 41, 121–128
    OpenUrlCrossRefPubMedWeb of Science
    1. Dixon J. E.,
    2. Kintner C. R.
    (1989) Cellular contacts required for neural induction in Xenopus embryos: evidence for two signals. Development 106, 749–757
    OpenUrlAbstract/FREE Full Text
    1. Doniach T.,
    2. Phillips C. R.,
    3. Gerhart J. C.
    (1992) Planar induction of anteroposterior pattern in the developing central nervous system of Xenopus laevis. Science 257, 542–545
    OpenUrlAbstract/FREE Full Text
    1. Dressler G. R.,
    2. Deutsch U.,
    3. Chowdhury K.,
    4. Nornes H. O.,
    5. Gruss P.
    (1990) Pax2, a new murine paired-box containing gene and its expression in the developing excretory system. Development 109, 787–795
    OpenUrlAbstract/FREE Full Text
    1. Dressler G. R.,
    2. Douglass E. C.
    (1992) Pax-2 is a DNA-binding proteinexpressed in embryonic kidney and Wilms tumor. Proc. Nat. Acad. Sci. USA 89, 1179–1183
    OpenUrlAbstract/FREE Full Text
    1. Durston A. J.,
    2. Timmermans J. P. M.,
    3. Hage W. J.,
    4. Hendriks H. F. J.,
    5. de Vries N. J.,
    6. Heideveld M.,
    7. Nieuwkoop P. D.
    (1989) Retinoic acid causes an anteroposterior transformation in the developing central nervous system. Nature 340, 140–144
    OpenUrlCrossRefPubMed
    1. Ferguson E. L.,
    2. Sternberg P. W.,
    3. Horvitz H. R.
    (1987) A genetic pathway for the specification of the vulval cell lineages of Caenorhabditis elegans. Nature 326, 259–267
    OpenUrlCrossRefPubMedWeb of Science
    1. Freyd G.,
    2. Kim S. K.,
    3. Horvitz H. R.
    (1990) Novel cystein-rich motif and homeodomain in the product of the Caenorhabditis elegans cell lineage gene lin-11. Nature 344, 876–879
    OpenUrlCrossRefPubMedWeb of Science
    1. Gerhart J.,
    2. Danilchik M.,
    3. Doniach T.,
    4. Roberts S.,
    5. Rowning B.,
    6. Stewart R.
    (1989) Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development. Development 1989, 37–51
    1. German M. S.,
    2. Wang J.,
    3. Chadwick R. B.,
    4. Rutter W. J.
    (1992) Synergistic activation of the insulin gene by a LIM-homeo domain protein and a basic helix-loop-helix protein: building a functional insulin minienhancer complex. Genes Dev 6, 2165–2176
    OpenUrlAbstract/FREE Full Text
    1. Gilbert S. F.,
    2. Saxen L.
    (1993) Spemann's organizer: models and molecules. Mech. Dev 41, 73–89
    OpenUrlCrossRefPubMedWeb of Science
    1. Gruss P.,
    2. Walther C.
    (1992) Pax in development. Cell 69, 719–722
    OpenUrlCrossRefPubMedWeb of Science
    1. Hartenstein V.
    (1989) Early neurogenesis in Xenopus: the spatio-temporal pattern of proliferation and cell lineages in the embryonic spinal cord. Neuron 3, 399–411
    OpenUrlCrossRefPubMedWeb of Science
    1. Kao K. R.,
    2. Elinson R. P.
    (1988) The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos. Dev. Biol 127, 64–77
    OpenUrlCrossRefPubMedWeb of Science
    1. Karlsson O.,
    2. Thor S.,
    3. Norberg T.,
    4. Ohlsson H.,
    5. Edlund T.
    (1990) Insulin gene enhancer binding protein Isl-1 is a member of a novel class of proteins containing both a homeo-and a Cys-His domain. Nature 344, 879–882
    OpenUrlCrossRefPubMedWeb of Science
    1. Kintner C. R.,
    2. Melton D. A.
    (1987) Expression of Xenopus N-CAM RNA in ectoderm is an early response to neural induction. Development 99, 311–325
    OpenUrlAbstract
    1. Knöchel S.,
    2. Lef J.,
    3. Clement J.,
    4. Klocke B.,
    5. Hille S.,
    6. Köster M.,
    7. Knöchel W.
    (1992) Activin A induced expression of a forkhead related gene in posterior chordamesoderm (notochord) of Xenopuslaevis embryos. Mech. Dev 38, 157–165
    OpenUrlCrossRefPubMedWeb of Science
    1. Korzh V.,
    2. Edlund T.,
    3. Thor S.
    (1993) Zebrafish primary meurons initiate expression of the LIM homeodomain protein ISL-1 at the end of gastrulation. Development 118, 417–425
    OpenUrlAbstract
    1. Langston A. W.,
    2. Gudas L. J.
    (1992). Identification of a retinoic acid responsive enhancer 3of the murine homeobox gene Hox-1.6. Mech. Dev 38, 217–228
    OpenUrlCrossRefPubMedWeb of Science
    1. Leroy P.,
    2. De Robertis E. M.
    (1992) Effects of lithium chloride and retinoic acid on the expression of genes from the XenopuslaevisHox 2 complex. Dev. Dyn 194, 21–32
    OpenUrlCrossRefPubMedWeb of Science
    1. Lopez S. L.,
    2. Carrasco A. E.
    (1992) Retinoic acid induces changes in the localization of homeobox proteins in the antero-posterior axis of Xenopus laevis embryos. Mech. Dev 36, 153–164
    OpenUrlCrossRefPubMed
    1. McGinnis W.,
    2. Krumlauf R.
    (1992) Homeobox genes and axial patterning. Cell 68, 283–302
    OpenUrlCrossRefPubMedWeb of Science
    1. Moriya N.,
    2. Uchiyama H.,
    3. Asashima M.
    (1993) Induction of pronephric tubules by activin and retinoic acid in presumptive ectoderm of Xenopus laevis. Dev. Growth. Diff 35, 123–128
    OpenUrlCrossRef
    1. Oliver G.,
    2. Wright C. V. E.,
    3. Hardwicke J.,
    4. De Robertis E. M.
    (1988) Defferential antero-posterior expression of two proteins encoded by a homeobox gene in Xenopus and mouse embryos. EMBO J 7, 3199–3209
    OpenUrlPubMedWeb of Science
    1. Papalopulu N.,
    2. Clarke J. D. W.,
    3. Bradley L.,
    4. Wilkinson D.,
    5. Krumlauf R.,
    6. Holder N.
    (1991) Retinoic acid causes abnormal development and segmental patterning of the anterior hindbrain in Xenopus embryos. Development 113, 1145–1158
    OpenUrlAbstract
    1. Papalopulu N.,
    2. Lovell-Badge R.,
    3. Krumlauf R.
    (1991) The expression of murine Hox-2 genes is dependent on the differentiation pathway anddisplays a collinear sensitivity to retinoic acid in F9 cells and Xenopus embyros. Nucl. Acids Res 19, 5497–5506
    OpenUrlAbstract/FREE Full Text
    1. Papalopulu N.,
    2. Kintner C.
    (1993) XenopusDistal-less related homeobox genes are expressed in the developing forebrain and are induced by planar signals. Development 117, 961–975
    OpenUrlAbstract
    1. Pöpperl H.,
    2. Featherstone M. S.
    (1993). Identification of a retinoic acid response element upstream of the murine Hox-4.2 gene. Mol. Cell. Biol 13, 257–265
    OpenUrlAbstract/FREE Full Text
    1. Price M.,
    2. Lemaistre M.,
    3. Pischetola M.,
    4. Di Lauro R.,
    5. Duboule D.
    (1991) A mouse gene related to Distal-less shows a restricted expression in the developing forebrain. Nature 351, 748–751
    OpenUrlCrossRefPubMed
    1. Puschel A. W.,
    2. Westerfield M.,
    3. Dressler G. R.
    (1992) Comparative analysis of Pax-2 protein distributions during neurulation in mice and zebrafish. Mech. Dev 38, 197–208
    OpenUrlCrossRefPubMedWeb of Science
    1. Rong P. M.,
    2. Teillet M.-A.,
    3. Ziller C.,
    4. Le Douarin N. M.
    (1992) The neural tube/notochord complex is necessary for vertebral but not limb and body wall striated muscle differentiation. Development 115, 657–672
    OpenUrlAbstract/FREE Full Text
    1. Rothenpieler U. W.,
    2. Dressler G. R.
    (1993) Pax-2 is required for mesenchyme to epithelium conversion during kidney development. Development 119, 711–720
    OpenUrlAbstract/FREE Full Text
    1. Ruiz i Altaba A.
    (1992) Planar and vertical signals in the induction and patterning of the Xenopus nervous system. Development 116, 67–80
    OpenUrlAbstract
    1. Ruiz i Altaba A.,
    2. Jessell T. M.
    (1991) Retinoic acid modifies mesodermal patterning in early Xenopus embryos. Genes Dev 5, 175–187
    OpenUrlAbstract/FREE Full Text
    1. Ruiz i Altaba A.,
    2. Jessell T. M.
    (1991) Retinoic acid modifies the pattern of cell differentiation in the central nervous system of neurula stage Xenopus embryos. Development 112, 945–958
    OpenUrlAbstract
    1. Ruiz i Altaba A.,
    2. Jessell T. M.
    (1992) Pintallavis, a gene expressed in the organizer and midline cells of frog embryos: involvement in the development of the neural axis. Development 116, 81–93
    OpenUrlAbstract
    1. Scott M. P.
    (1993) Vertebrate homeobox gene nomenclature. Cell 71, 551–553
    OpenUrl
    1. Sharpe C. R.
    (1991) Retinoic acid can mimic endogenous signals involved in transformation fo the Xenopus nervous system. Neuron 7, 239–247
    OpenUrlCrossRefPubMedWeb of Science
    1. Simeone A.,
    2. Acampora D.,
    3. Gulisano M.,
    4. Stornaiuolo A.,
    5. Boncinelli E.
    (1992) Nested expression domains of four homeobox genes in developing rostral brain. Nature 358, 687–690
    OpenUrlCrossRefPubMed
    1. Simeone A.,
    2. Acampora D.,
    3. Mallamaci A.,
    4. Stornaiuolo A.,
    5. D'Apice M. R.,
    6. Nigro V.,
    7. Boncinelli E.
    (1993) A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J 12, 2735–2747
    OpenUrlPubMedWeb of Science
    1. Sive H. L.,
    2. Cheng P. F.
    (1991). Retinoic acid perturbs the expression of Xhox.lab genes and alters mesodermal determination in Xenopusleavis. Genes Dev 5, 1321–1332
    OpenUrlAbstract/FREE Full Text
    1. Sive H.,
    2. Draper B. W.,
    3. Harland R. M.,
    4. Weintraub H.
    (1990) Identification of a retinoic acid-sensitive period during primary axis formation in Xenopuslaevis. Genes Dev 4, 932–942
    OpenUrlAbstract/FREE Full Text
    1. Smith J. C.,
    2. Price B. M. J.,
    3. Green J. B. A.,
    4. Weigel D.,
    5. Herrmann B. G.
    (1991) Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell 67, 79–87
    OpenUrlCrossRefPubMedWeb of Science
    1. Tadano T.,
    2. Otani H.,
    3. Taira M.,
    4. Dawid I. B.
    (1993) Differntial induction of regulatory genes during mesoderm formation in Xenopuslaevis embryos. Dev. Genet 14, 204–211
    OpenUrlCrossRefPubMedWeb of Science
    1. Taira M.,
    2. Hayes W. P.,
    3. Otani H.,
    4. Dawid I. B.
    (1993) Expression of LIM class homeobox gene Xlim-3 in Xenopus development is limited to neural and neuroendocrine tissues. Dev. Biol 159, 245–256
    OpenUrlCrossRefPubMedWeb of Science
    1. Taira M.,
    2. Jamrich M.,
    3. Good P. J.,
    4. Dawid I. B.
    (1992) The LIM domain-containing homeo box gene Xlim-1 is expressed specifically in the organizer region of Xenopus gastrula embryos. Genes Dev 6, 356–366
    OpenUrlAbstract/FREE Full Text
    1. Thor S.,
    2. Ericson J.,
    3. Brannstrom T.,
    4. Edlund T.
    (1991) The homeodomain LIM protein Isl-1 is expressed in subsets of neurons and endocrine cells in the adult rat. Neuron 7, 881–889
    OpenUrlCrossRefPubMedWeb of Science
    1. Wagner M.,
    2. Han B.,
    3. Jessell T. M.
    (1992) Regional differences in retinoid release from embryonic neural tissue detected by an in vitro reporter assay. Development 116, 55–66
    OpenUrlAbstract
    1. Way J. C.,
    2. Chalfie M.
    (1988) mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans. Cell 54, 5–16
    OpenUrlCrossRefPubMedWeb of Science
    1. Whittaker C. A.,
    2. DeSimone D. W.
    (1993) Integrinsubunit mRNAs are differentially expressed in early Xenopus embyros. Development 117, 1239–1249
    OpenUrlAbstract
    1. Xu Y.,
    2. Baldassare M.,
    3. Fisher P.,
    4. Rathbun G.,
    5. Oltz E. M.,
    6. Yancopoulos G. D.,
    7. Jessell T. M.,
    8. Alt F. W.
    (1993) LH-2: a LIM/homeodomain gene expressed in developing lymphocytes and neural cells. Proc. Natl. Acad. Sci. USA 90, 227–231
    OpenUrlAbstract/FREE Full Text
    1. Yamada T.,
    2. Pfaff S. L.,
    3. Edlund T.,
    4. Jessell T. M.
    (1993) Control of cell pattern in the neural tube: motor neuron induction by diffusible factors from notochord and floor plate. Cell 73, 673–686
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Expression of the LIM class homeobox gene Xlim-1 in pronephros and CNS cell lineages of Xenopus embryos is affected by retinoic acid and exogastrulation
M. Taira, H. Otani, M. Jamrich, I.B. Dawid
Development 1994 120: 1525-1536;
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