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JOURNAL ARTICLES
Differential induction of four msx homeobox genes during fin development and regeneration in zebrafish
M.A. Akimenko, S.L. Johnson, M. Westerfield, M. Ekker
Development 1995 121: 347-357;
M.A. Akimenko
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S.L. Johnson
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M. Westerfield
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M. Ekker
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Summary

To study the genetic regulation of growth control and pattern formation during fin development and regeneration, we have analysed the expression of four homeobox genes, msxA, msxB, msxC and msxD in zebrafish fins. The median fin fold, which gives rise to the unpaired fins, expresses these four msx genes during development. Transcripts of the genes are also present in cells of the presumptive pectoral fin buds. The most distal cells, the apical ectodermal ridge of the paired fins and the cleft and flanking cells of the median fin fold express all these msx genes with the exception of msxC. Mesenchymal cells underlying the most distal cells express all four genes. Expression of the msx genes in the fin fold and fin buds is transient and, by 3 days after fertilization, msx expression in the median fin fold falls below levels detectable by in situ hybridization. Although the fins of adult zebrafish normally have levels of msx transcripts undetectable by in situ hybridization, expression of all four genes is strongly reinduced during regeneration of both paired and unpaired fins. Induction of msx gene expression in regenerating caudal fins occurs as early as 30 hours postamputation. As the blastema forms, the levels of expression increase and reach a maximum between the third and fifth days. Then, msx expression progressively declines and disappears by day 12 when the caudal fin has grown back to its normal size. In the regenerating fin, the blastema cells that develop at the tip of each fin ray express msxB and msxC. Cells of the overlying epithelium express msxA and msxD, but do not express msxB or msxC. Amputations at various levels along the proximodistal axis of the fin suggest that msxB expression depends upon the position of the blastema, with cells of the rapidly proliferating proximal blastema expressing higher levels than the cells of the less rapidly proliferating distal blastema. Expression of msxC and msxD is independent of the position of the blastema cell along this axis. Our results suggest distinct roles for each of the four msx genes during fin development and regeneration and differential regulation of their expression.

Reference

    1. Akimenko M.-A.,
    2. Ekker M.,
    3. Wegner J.,
    4. Lin W.,
    5. Westerfield M.
    (1994) Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J. Neurosci 14, 3475–3486
    OpenUrlAbstract
    1. Beauchemin M.,
    2. Savard P.
    (1992) Two distal-less related homeobox-containing genes expressed in regeneration blastemas of the newt. Dev. Biol 154, 55–65
    OpenUrlCrossRefPubMedWeb of Science
    1. Brown R.,
    2. Brockes J. P.
    (1991) Identification and expression of a regeneration-specific homeobox gene in the limb blastema. Development 111, 489–496
    OpenUrlAbstract
    1. Coelho C. N. D.,
    2. Sumoy L.,
    3. Rodgers B. J.,
    4. Davidson D. R.,
    5. Hill R. E.,
    6. Upholt W. B.,
    7. Kosher R. A.
    (1991) Expression of the chicken homeobox-containing gene GHox-8 during embryonic chick development. Mech. Devel 34, 143–154
    OpenUrlCrossRefPubMed
    1. Coelho C. N. D.,
    2. Krabbenhoft K. M.,
    3. Upholt W. B.,
    4. Fallon J. F.,
    5. Kosher R. A.
    (1991) Altered expression of the chicken homeobox-containing genes Ghox-7 and Ghox-8 in the limb buds of limbless mutant chick embryos. Development 113, 1487–1493
    OpenUrlAbstract
    1. Dane P. J.,
    2. Tucker J. B.
    (1985) Modulation of epidermal cell shaping and extracellular matrix during caudal fin morphogenesis in the zebra fish Brachydanio rerio. J. Embryo. Exp. Morph 87, 145–161
    OpenUrlPubMed
    1. Davidson D. R.,
    2. Crawley A.,
    3. Hill R. E.,
    4. Tickle C.
    (1991) Position-dependent expression of two related homeobox genes in developing vertebrate limbs. Nature 352, 429–431
    OpenUrlCrossRefPubMedWeb of Science
    1. Dolle P.,
    2. Izpisua-Belmonte J.-C.,
    3. Falkenstein H.,
    4. Renucci A.,
    5. Duboule D.
    (1989) Coordinate expression of the murine Hox-5 complex homeobox-containing genes during limb pattern formation. Nature 342, 767–772
    OpenUrlCrossRefPubMed
    1. Dolle P.,
    2. Dierich A.,
    3. LeMeur M.,
    4. Schimmang T.,
    5. Schuhbaur B.,
    6. Chambon P.,
    7. Duboule D.
    (1993) Disruption of the Hoxd-13 gene induces localized heterochrony leading to mice with neotenic limbs. Cell 75, 431–441
    OpenUrlCrossRefPubMedWeb of Science
    1. Duboule D.,
    2. Dolle P.
    (1989) The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. EMBO J 8, 1497–1505
    OpenUrlPubMedWeb of Science
    1. Ekker M.,
    2. Akimenko M.-A.,
    3. Bremiller R.,
    4. Westerfield M.
    (1992) Regional expression of three homeobox transcripts in the inner ear of zebrafish embryos. Neuron 9, 27–35
    OpenUrlCrossRefPubMedWeb of Science
    1. Ekker M.,
    2. Wegner J.,
    3. Akimenko M.-A.,
    4. Westerfield M.
    (1992) Coordinate expression of three zebrafish engrailed genes. Development 116, 1001–1012
    OpenUrlAbstract/FREE Full Text
    1. Graham A.,
    2. Papalopulu N.,
    3. Krumlauf R.
    (1989) The murine and Drosophila homeobox clusters have common features of organization and expression. Cell 57, 367–378
    OpenUrlCrossRefPubMedWeb of Science
    1. Hill R. E.,
    2. Jones P. F.,
    3. Rees A. R.,
    4. Sime C. M.,
    5. Justice M. J.,
    6. Copeland N. G.,
    7. Jenkins N. A.,
    8. Graham E.,
    9. Davidson D. R.
    (1989). A new family of mouse homeobox-containing genes: molecular structure, chromosomal location, and developmental expression of Hox-7.1. Genes Dev 3, 26–37
    OpenUrlAbstract/FREE Full Text
    1. Holland P. W. H.
    (1991) Cloning and evolutionary analysis of msh -like homeobox genes from mouse, zebrafish and ascidian. Gene 98, 253–257
    OpenUrlCrossRefPubMedWeb of Science
    1. Hyatt G. A.,
    2. Schmitt E. A.,
    3. Marsh-Armstrong N. R.,
    4. Dowling J. E.
    (1992) Retinoic acid-induced duplication of the zebrafish retina. Proc. Natl. Acad. Sci. USA 89, 8293–8297
    OpenUrlAbstract/FREE Full Text
    1. Izpisua-Belmonte J. C.,
    2. Tickle C.,
    3. Dolle P.,
    4. Wolpert L.,
    5. Duboule D.
    (1991) Expression of the homeobox Hox-4 genes and the specification of position in chick wing development. Nature 350, 585–589
    OpenUrlCrossRefPubMed
    1. Kappen C.,
    2. Scughart K.,
    3. Ruddle F. H.
    (1989) Two steps in the evolution of antennapedia-class vertebrate homeobox genes. Proc. Natl. Acad. Sci. USA 86, 5459–5463
    OpenUrlAbstract/FREE Full Text
    1. Kessel M.,
    2. Gruss P.
    (1990) Murine developmental control genes. Science 249, 374–379
    OpenUrlAbstract/FREE Full Text
    1. Kozak M.
    (1987) An analysis of 5-noncoding sequences from 699 vertebrate messenger RNAs. Nucl. Acids Res 15, 8125–8148
    OpenUrlAbstract/FREE Full Text
    1. Lyons G. E.,
    2. Houzelstein D.,
    3. Sassoon D.,
    4. Robert B.,
    5. Buckingham M. E.
    (1992) Multiple sites of Hox-7 expression during mouse embryogenesis—Comparison with retinoic acid receptor messenger RNA localization. Molecular Reproduction and Development 32, 303–314
    OpenUrlCrossRefPubMedWeb of Science
    1. MacKenzie A.,
    2. Ferguson M. W.,
    3. Sharpe P. T.
    (1992) Expression patterns of the homeobox gene Hox-8, in the mouse embryo suggest a role in specifying tooth initiation and shape. Development 115, 403–420
    OpenUrlAbstract
    1. Monaghan A. P.,
    2. Davidson D. R.,
    3. Sime C.,
    4. Graham E.,
    5. Baldock R.,
    6. Bhattacharya S. S.,
    7. Hill R. E.
    (1991) The msh -like homeobox genes define domains in the vertebrate eye. Development 112, 1053–1061
    OpenUrlAbstract
    1. Morgan B. A.,
    2. Izpisúa-Belmonte J.-C.,
    3. Duboule D.,
    4. Tabin C. J.
    (1992). Targetted misexpression of Hox-4.6 in the avian limb bud causes apparent homeotic transformations. Nature 358, 236–239
    OpenUrlCrossRefPubMed
    1. Muneoka K.,
    2. Sassoon D.
    (1992) Molecular aspects of regeneration in developing vertebrate limbs. Dev. Biol 152, 37–49
    OpenUrlCrossRefPubMed
    1. Nohno T.,
    2. Noji T.,
    3. Koyama E.,
    4. Ohyama K.,
    5. Myokai F.,
    6. Kuroiwa A.,
    7. Saito T.,
    8. Taniguchi S.
    (1991) Involvement of the Chox-4 homeobox genes in determination of antero-posterior axial polarity during limb development. Cell 64, 1197–1205
    OpenUrlCrossRefPubMedWeb of Science
    1. Oliver G.,
    2. Sidell N.,
    3. Fiske W.,
    4. Heinzman C.,
    5. Mohandas T.,
    6. Sparkes R. S.,
    7. De Robertis E. M.
    (1989) Complementary homeoprotein gradients in developing limb buds. Genes Dev 3, 641–650
    OpenUrlAbstract/FREE Full Text
    1. Puschel A. W.,
    2. Gruss P.,
    3. Westerfield M.
    (1992) Sequence and expression pattern of pax-6 are highly conserved between zebrafish and mice. Development 114, 643–651
    OpenUrlAbstract
    1. Robert B.,
    2. Sassoon D.,
    3. Jacq B.,
    4. Gehring W.,
    5. Buckingham M.
    (1989) Hox-7, a mouse homeobox gene with a novel pattern of expression during embryogenesis. EMBO J 8, 91–100
    OpenUrlPubMedWeb of Science
    1. Robert B.,
    2. Lyons G.,
    3. Simandl B. K.,
    4. Kuroiwa A.,
    5. Buckingham M.
    (1991) The apical ectodermal ridge regulates Hox-7 and Hox-8 gene expression in developing limb buds. Genes Dev 5, 2363–2374
    OpenUrlAbstract/FREE Full Text
    1. Ros M. A.,
    2. Lyons G.,
    3. Kosher R. A.,
    4. Upholt W. B.,
    5. Coelho C. N. D.,
    6. Fallon J. F.
    (1992) Apical ridge dependent and independent mesodermal domains of Ghox-7 and Ghox-8 expression in chick limb buds. Development 116, 811–818
    OpenUrlAbstract
    1. Sanger F.,
    2. Nicklen S.,
    3. Coulson A. R.
    (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463–5467
    OpenUrlAbstract/FREE Full Text
    1. Satokata I.,
    2. Maas R.
    (1994) Msx1 deficient mice exhibit cleft palate and abnormalities of caniofacial and tooth development. Nature Genetics 6, 348–355
    OpenUrlCrossRefPubMedWeb of Science
    1. Savard P.,
    2. Gates P. B.,
    3. Brockes J. P.
    (1988) Position dependentexpression of a homeobox gene transcript in relation to amphibian limb regeneration. EMBO J 7, 4275–4282
    OpenUrlPubMedWeb of Science
    1. Simon H.-G.,
    2. Tabin C. J.
    (1993). Analysis of Hox-4.5 and Hox-3.6 expression during newt limb regeneration: differential regulation of paralogous Hox genes suggest different roles for members of different Hox clusters. Development 117, 1397–1405
    OpenUrlAbstract
    1. Smith M.,
    2. Hickman A.,
    3. Amanze D.,
    4. Lumsden A.,
    5. Thorogood P.
    (1994) Trunk neural crest origin of caudal fin mesenchyme in the zebrafish Brachydanio rerio. Proc. R. Soc. Lond. B 256, 137–145
    OpenUrlAbstract/FREE Full Text
    1. Song K.,
    2. Wang Y.,
    3. Sassoon D.
    (1992). Expression of Hox-7.1 in myoblasts inhibits terminal differentiation and induces cell transformation. Nature 360, 477–481
    OpenUrlCrossRefPubMed
    1. Stocum D. L.,
    2. Dearlove G. E.
    (1972) Epidermal-mesodermal interaction during morphogenesis of the limb regeneration blastema in larval salamanders. J. Exp. Zool 181, 49–61
    OpenUrlCrossRef
    1. Suzuki H. R.,
    2. Padanilam B. J.,
    3. Vitale E.,
    4. Ramirez F.,
    5. Solursh M.
    (1991) Repeating developmental expression of G-Hox-7, a novel homeobox-containing gene in the chicken. Dev. Biol 148, 375–388
    OpenUrlCrossRefPubMedWeb of Science
    1. Tabin C. J.
    (1991) Retinoids, homeoboxes, and growth factors: Towards molecular models for limb development. Cell 66, 199–217
    OpenUrlCrossRefPubMedWeb of Science
    1. Takahashi Y.,
    2. Bontoux M.,
    3. Le Douarin N. M.
    (1991) Epithelio-mensenchymal interactions are critical for Quox 7 expression and membrane bone differentiation in the neural crest derived mandibular mesenchyme. EMBO J 9, 2387–2393
    OpenUrl
    1. Tassava R. A.,
    2. Goss R. J.
    (1966) Regeneration rate and amputation level in fish and lizard tails. Growth 30, 9–21
    OpenUrlPubMedWeb of Science
    1. Tickle C.
    (1991) Retinoic acid and the chick limb bud development. Development 1991, 113–121
    1. White J. A.,
    2. Boffa M. B.,
    3. Jones B.,
    4. Petkovich M.
    (1994) A zebrafish retinoic receptor expressed in the regenerating caudal fin. Development 120, 1861–1872
    OpenUrlAbstract
    1. Wood A.
    (1982) Early pectoral fin development and morphogenesis of the apical ectodermal ridge in the killifish, Aphysosemion scheeli. Anat. Rec 204, 349–356
    OpenUrlCrossRefPubMed
    1. Yokouchi Y.,
    2. Oshugi K.,
    3. Sasaki H.,
    4. Kuroiwa A.
    (1991) Chicken homeobox gene Msx-1: structure, expression in limb buds and effect of retinoic acid. Development 113, 431–444
    OpenUrlAbstract
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JOURNAL ARTICLES
Differential induction of four msx homeobox genes during fin development and regeneration in zebrafish
M.A. Akimenko, S.L. Johnson, M. Westerfield, M. Ekker
Development 1995 121: 347-357;
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JOURNAL ARTICLES
Differential induction of four msx homeobox genes during fin development and regeneration in zebrafish
M.A. Akimenko, S.L. Johnson, M. Westerfield, M. Ekker
Development 1995 121: 347-357;

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