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JOURNAL ARTICLES
Early myotome specification regulates PDGFA expression and axial skeleton development
M.D. Tallquist, K.E. Weismann, M. Hellstrom, P. Soriano
Development 2000 127: 5059-5070;
M.D. Tallquist
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K.E. Weismann
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M. Hellstrom
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P. Soriano
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Summary

Reciprocal defects in signaling between the myotome and the sclerotome compartments of the somites in PDGFRalpha and Myf5 mutant embryos lead to alterations in the formation of the vertebrae and the ribs. To investigate the significance of these observations, we have examined the role of PDGF signaling in the developing somite. PDGFA ligand expression was not detected in the myotome of Myf5 null mutant embryos and PDGFA promoter activity was regulated by Myf5 in vitro. PDGFA stimulated chondrogenesis in somite micromass cultures as well as in embryos when PDGFA was knocked into the Myf5 locus, resulting in increased vertebral and rib development. PDGFA expression in the myotome was fully restored in embryos in which MyoD has been introduced at the Myf5 locus but to a lesser extent in similar myogenin knock-in embryos. These results underscore the importance of growth factor signaling within the developing somite and suggest an important role for myogenic determination factors in orchestrating normal development of the axial skeleton.

REFERENCES

    1. Bhandari B.,
    2. Wenzel U. O.,
    3. Marra F.,
    4. Abboud H. E.
    (1995) A nuclear protein in mesangial cells that binds to the promoter region of the platelet-derived growth factor-A chain gene. Induction by phorbol ester. J. Biol. Chem 270, 5541–5548
    OpenUrlAbstract/FREE Full Text
    1. Blackwell T. K.,
    2. Weintraub H.
    (1990) Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection. Science 250, 1104–1110
    OpenUrlAbstract/FREE Full Text
    1. Bonthron D. T.,
    2. Morton C. C.,
    3. Orkin S. H.,
    4. Collins T.
    (1988) Platelet-derived growth factor A chain: gene structure, chromosomal location, and basis for alternative mRNA splicing. Proc. Natl. Acad. Sci. USA 85, 1492–1496
    OpenUrlAbstract/FREE Full Text
    1. Borycki A. G.,
    2. Emerson C. P., Jr
    (2000) Multiple tissue interactions and signal transduction pathways control somite myogenesis. Curr. Top. Dev. Biol 48, 165–224
    OpenUrlPubMed
    1. Boström H.,
    2. Willetts K.,
    3. Pekny M.,
    4. Leveen P.,
    5. Lindahl P.,
    6. Hedstrand H.,
    7. Pekna M.,
    8. Hellstrom M.,
    9. Gebre-Medhin S.,
    10. Schalling M.,
    11. et al.
    (1996) PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 85, 863–873
    OpenUrlCrossRefPubMedWeb of Science
    1. Braun T.,
    2. Arnold H. H.
    (1995) Inactivation of Myf-6 and Myf-5 genesin mice leads to alterations in skeletal muscle development. EMBO J 14, 1176–1186
    OpenUrlPubMedWeb of Science
    1. Braun T.,
    2. Buschhausen-Denker G.,
    3. Bober E.,
    4. Tannich E.,
    5. Arnold H. H.
    (1989) A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblasts. EMBO J 8, 701–709
    OpenUrlPubMedWeb of Science
    1. Braun T.,
    2. Rudnicki M. A.,
    3. Arnold H. H.,
    4. Jaenisch R.
    (1992) Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell 71, 369–382
    OpenUrlCrossRefPubMedWeb of Science
    1. Chen P.,
    2. Carrington J. L.,
    3. Paralkar V. M.,
    4. Pierce G. F.,
    5. Reddi A. H.
    (1992) Chick limb bud mesodermal cell chondrogenesis: inhibition by isoforms of platelet-derived growth factor and reversal by recombinant bone morphogenetic protein. Exp. Cell Res 200, 110–117
    OpenUrlCrossRefPubMed
    1. Chen P.,
    2. Yu Y. M.,
    3. Reddi A. H.
    (1993) Chondrogenesis in chick limb bud mesodermal cells: reciprocal modulation by activin and inhibin. Exp. Cell Res 206, 119–127
    OpenUrlCrossRefPubMed
    1. Cossu G.,
    2. Kelly R.,
    3. Tajbakhsh S.,
    4. Di Donna S.,
    5. Vivarelli E.,
    6. Buckingham M.
    (1996) Activation of different myogenic pathways: myf-5 is induced by the neural tube and MyoD by the dorsal ectoderm in mouse paraxial mesoderm. Development 122, 429–437
    OpenUrlAbstract
    1. Davis R. L.,
    2. Weintraub H.,
    3. Lassar A. B.
    (1987) Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51, 987–1000
    OpenUrlCrossRefPubMedWeb of Science
    1. deLapeyriere O.,
    2. Ollendorff V.,
    3. Planche J.,
    4. Ott M. O.,
    5. Pizette S.,
    6. Coulier F.,
    7. Birnbaum D.
    (1993) Expression of the Fgf6 gene is restricted to developing skeletal muscle in the mouse embryo. Development 118, 601–611
    OpenUrlAbstract
    1. Feldman B.,
    2. Poueymirou W.,
    3. Papaioannou V. E.,
    4. DeChiara T. M.,
    5. Goldfarb M.
    (1995) Requirement of FGF-4 for postimplantation mouse development. Science 267, 246–249
    OpenUrlAbstract/FREE Full Text
    1. Fiering S.,
    2. Epner E.,
    3. Robinson K.,
    4. Zhuang Y.,
    5. Telling A.,
    6. Hu M.,
    7. Martin D. I.,
    8. Enver T.,
    9. Ley T. J.,
    10. Groudine M.
    (1995) Targeted deletion of 5HS2 of the murine beta-globin LCR reveals that it is not essential for proper regulation of the beta-globin locus. Genes Dev 9, 2203–2213
    OpenUrlAbstract/FREE Full Text
    1. Floss T.,
    2. Arnold H. H.,
    3. Braun T.
    (1997) A role for FGF-6 in skeletal muscle regeneration. Genes Dev 11, 2040–2051
    OpenUrlAbstract/FREE Full Text
    1. Fraidenraich D.,
    2. Lang R.,
    3. Basilico C.
    (1998) Distinct regulatory elements govern Fgf4 gene expression in the mouse blastocyst, myotomes, and developing limb. Dev. Biol 204, 197–209
    OpenUrlCrossRefPubMedWeb of Science
    1. Frenz D. A.,
    2. Liu W.,
    3. Williams J. D.,
    4. Hatcher V.,
    5. Galinovic-Schwartz V.,
    6. Flanders K. C.,
    7. Van de Water T. R.
    (1994) Induction of chondrogenesis: requirement for synergistic interaction of basic fibroblast growth factor and transforming growth factor-beta. Development 120, 415–424
    OpenUrlAbstract
    1. Grass S.,
    2. Arnold H. H.,
    3. Braun T.
    (1996) Alterations in somite patterning of Myf-5-deficient mice: a possible role for FGF-4 and FGF-6. Development 122, 141–150
    OpenUrlAbstract
    1. Hasty P.,
    2. Bradley A.,
    3. Morris J. H.,
    4. Edmondson D. G.,
    5. Venuti J. M.,
    6. Olson E. N.,
    7. Klein W. H.
    (1993) Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364, 501–506
    OpenUrlCrossRefPubMedWeb of Science
    1. Hebert J. M.,
    2. Basilico C.,
    3. Goldfarb M.,
    4. Haub O.,
    5. Martin G. R.
    (1990) Isolation of cDNAs encoding four mouse FGF family members and characterization of their expression patterns during embryogenesis. Dev. Biol 138, 454–463
    OpenUrlCrossRefPubMedWeb of Science
    1. Huang R.,
    2. Zhi Q.,
    3. Schmidt C.,
    4. Wilting J.,
    5. Brand-Saberi B.,
    6. Christ B.
    (2000) Sclerotomal origin of the ribs. Development 127, 527–532
    OpenUrlAbstract
    1. Imamoto A.,
    2. Soriano P.
    (1993) Disruption of the csk gene, encoding a negative regulator of Src family tyrosine kinases, leads to neural tube defects and embryonic lethality in mice. Cell 73, 1117–1124
    OpenUrlCrossRefPubMedWeb of Science
    1. Ishizaki Y.,
    2. Burne J. F.,
    3. Raff M. C.
    (1994) Autocrine signals enable chondrocytes to survive in culture. J. Cell Biol 126, 1069–1077
    OpenUrlAbstract/FREE Full Text
    1. Kablar B.,
    2. Krastel K.,
    3. Ying C.,
    4. Asakura A.,
    5. Tapscott S. J.,
    6. Rudnicki M. A.
    (1997) MyoD and Myf-5 differentially regulate the development of limb versus trunk skeletal muscle. Development 124, 4729–4738
    OpenUrlAbstract
    1. Karsenty G.
    (1999) The genetic transformation of bone biology. Genes Dev 13, 3037–3051
    OpenUrlFREE Full Text
    1. Kato N.,
    2. Aoyama H.
    (1998) Dermomyotomal origin of the ribs as revealed by extirpation and transplantation experiments in chick and quail embryos. Development 125, 3437–3443
    OpenUrlAbstract
    1. Kaul A.,
    2. Koster M.,
    3. Neuhaus H.,
    4. Braun T.
    (2000) Myf-5 revisited: Loss of early myotome formation does not lead to a rib phenotype in homozygous Myf-5 mutant mice. Cell 102, 17–19
    OpenUrlCrossRefPubMedWeb of Science
    1. Lev R.,
    2. Spicer S. S.
    (1964) Specific staining of sulfate groups with Alcian blue at low pH. J. Histochem. Cytochem 12, 309–319
    OpenUrlFREE Full Text
    1. Mercola M.,
    2. Wang C. Y.,
    3. Kelly J.,
    4. Brownlee C.,
    5. Jackson-Grusby L.,
    6. Stiles C.,
    7. Bowen-Pope D.
    (1990) Selective expression of PDGF A and its receptor during early mouse embryogenesis. Dev. Biol 138, 114–122
    OpenUrlCrossRefPubMedWeb of Science
    1. Meyers E. N.,
    2. Lewandoski M.,
    3. Martin G. R.
    (1998) An Fgf8 mutant allelic series generated by Cre-and Flp-mediated recombination. Nature Genet 18, 136–141
    OpenUrlCrossRefPubMedWeb of Science
    1. Nabeshima Y.,
    2. Hanaoka K.,
    3. Hayasaka M.,
    4. Esumi E.,
    5. Li S.,
    6. Nonaka I.
    (1993) Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364, 532–535
    OpenUrlCrossRefPubMedWeb of Science
    1. Niswander L.,
    2. Martin G. R.
    (1992) Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 114, 755–768
    OpenUrlAbstract
    1. Olson E. N.,
    2. Arnold H. H.,
    3. Rigby P. W.,
    4. Wold B. J.
    (1996) Know your neighbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4. Cell 85, 1–4
    OpenUrlCrossRefPubMedWeb of Science
    1. Orr-Urtreger A.,
    2. Bedford M. T.,
    3. Do M. S.,
    4. Eisenbach L.,
    5. Lonai P.
    (1992) Developmental expression of the alpha receptor for platelet-derived growth factor, which is deleted in the embryonic lethal Patch mutation. Development 115, 289–303
    OpenUrlAbstract
    1. Orr-Urtreger A.,
    2. Lonai P.
    (1992) Platelet-derived growth factor-A and its receptor are expressed in separate, but adjacent cell layers of the mouse embryo. Development 115, 1045–1058
    OpenUrlAbstract
    1. Ott M. O.,
    2. Bober E.,
    3. Lyons G.,
    4. Arnold H.,
    5. Buckingham M.
    (1991) Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 111, 1097–1107
    OpenUrlAbstract/FREE Full Text
    1. Patapoutian A.,
    2. Yoon J. K.,
    3. Miner J. H.,
    4. Wang S.,
    5. Stark K.,
    6. Wold B.
    (1995) Disruption of the mouse MRF4 gene identifies multiple waves of myogenesis in the myotome. Development 121, 3347–3358
    OpenUrlAbstract
    1. Reinertsen K. K.,
    2. Bronson R. T.,
    3. Stiles C. D.,
    4. Wang C.
    (1997) Temporal and spatial specificity of PDGF alpha receptor promoter in transgenic mice [published erratum appears in Gene Expr 1998;7(2):131]. Gene Expression 6, 301–314
    OpenUrlPubMed
    1. Rudnicki M. A.,
    2. Braun T.,
    3. Hinuma S.,
    4. Jaenisch R.
    (1992) Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71, 383–390
    OpenUrlCrossRefPubMedWeb of Science
    1. Rudnicki M. A.,
    2. Schnegelsberg P. N.,
    3. Stead R. H.,
    4. Braun T.,
    5. Arnold H. H.,
    6. Jaenisch R.
    (1993) MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75, 1351–1359
    OpenUrlCrossRefPubMedWeb of Science
    1. Schatteman G. C.,
    2. Morrison-Graham K.,
    3. van Koppen A.,
    4. Weston J. A.,
    5. Bowen-Pope D. F.
    (1992) Regulation and role of PDGF receptor alpha-subunit expression during embryogenesis. Development 115, 123–131
    OpenUrlAbstract
    1. Schofield J. N.,
    2. Wolpert L.
    (1990) Effect of TGF-beta 1, TGF-beta 2, and bFGF on chick cartilage and muscle cell differentiation. Exp. Cell Res 191, 144–148
    OpenUrlCrossRefPubMed
    1. Soriano P.
    (1997) The PDGF alpha receptor is required for neural crest cell development and for normal patterning of the somites. Development 124, 2691–2700
    OpenUrlAbstract
    1. Soriano P.
    (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nature Genet 21, 70–71
    OpenUrlCrossRefPubMedWeb of Science
    1. Soriano P.,
    2. Montgomery C.,
    3. Geske R.,
    4. Bradley A.
    (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64, 693–702
    OpenUrlCrossRefPubMedWeb of Science
    1. Tajbakhsh S.,
    2. Bober E.,
    3. Babinet C.,
    4. Pournin S.,
    5. Arnold H.,
    6. Buckingham M.
    (1996) Gene targeting the myf-5 locus with nlacZ reveals expression of this myogenic factor in mature skeletal muscle fibres as well as early embryonic muscle. Dev. Dyn 206, 291–300
    OpenUrlCrossRefPubMedWeb of Science
    1. Tajbakhsh S.,
    2. Buckingham M.
    (2000) The birth of muscle progenitor cells in the mouse: spatiotemporal considerations. Curr. Top. Dev. Biol 48, 225–268
    OpenUrlPubMedWeb of Science
    1. Takimoto Y.,
    2. Wang Z. Y.,
    3. Kobler K.,
    4. Deuel T. F.
    (1991) Promoter region of the human platelet-derived growth factor A-chain gene. Proc. Natl. Acad. Sci. USA 88, 1686–1690
    OpenUrlAbstract/FREE Full Text
    1. Wang Y.,
    2. Jaenisch R.
    (1997) Myogenin can substitute for Myf5 inpromoting myogenesis but less efficiently. Development 124, 2507–2513
    OpenUrlAbstract
    1. Wang Y.,
    2. Schnegelsberg P. N.,
    3. Dausman J.,
    4. Jaenisch R.
    (1996) Functional redundancy of the muscle-specific transcription factors Myf5 and myogenin. Nature 379, 823–825
    OpenUrlCrossRefPubMed
    1. Yoon J. K.,
    2. Olson E. N.,
    3. Arnold H. H.,
    4. Wold B. J.
    (1997) Different MRF4 knockout alleles differentially disrupt Myf-5 expression: cis-regulatory interactions at the MRF4/Myf-5 locus. Dev. Biol 188, 349–362
    OpenUrlCrossRefPubMed
    1. Zhang W.,
    2. Behringer R. R.,
    3. Olson E. N.
    (1995) Inactivation of the myogenic bHLH gene MRF4 results in up-regulation of myogenin and rib anomalies. Genes Dev 9, 1388–1399
    OpenUrlAbstract/FREE Full Text
    1. Zhang X. Q.,
    2. Afink G. B.,
    3. Svensson K.,
    4. Jacobs J. J.,
    5. Gunther T.,
    6. Forsberg-Nilsson K.,
    7. van Zoelen E. J.,
    8. Westermark B.,
    9. Nister M.
    (1998) Specific expression in mouse mesoderm-and neural crest-derived tissues of a human PDGFRA promoter/lacZ transgene. Mech. Dev 70, 167–180
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Early myotome specification regulates PDGFA expression and axial skeleton development
M.D. Tallquist, K.E. Weismann, M. Hellstrom, P. Soriano
Development 2000 127: 5059-5070;
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JOURNAL ARTICLES
Early myotome specification regulates PDGFA expression and axial skeleton development
M.D. Tallquist, K.E. Weismann, M. Hellstrom, P. Soriano
Development 2000 127: 5059-5070;

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