Research Article

You have full text access to this OnlineOpen article

Twist1 dimer selection regulates cranial suture patterning and fusion

  1. Jeannette Connerney‡,
  2. Viktoria Andreeva‡,
  3. Yael Leshem†,‡,
  4. Christian Muentener,
  5. Miguel A. Mercado,
  6. Douglas B. Spicer*

Article first published online: 24 FEB 2006

DOI: 10.1002/dvdy.20717

Issue

Developmental Dynamics

Developmental Dynamics

Special Issue: Craniofacial Development Special Issue

Volume 235, Issue 5, pages 1334–1346, May 2006

Additional Information

How to Cite

Connerney, J., Andreeva, V., Leshem, Y., Muentener, C., Mercado, M. A. and Spicer, D. B. (2006), Twist1 dimer selection regulates cranial suture patterning and fusion. Dev. Dyn., 235: 1334–1346. doi: 10.1002/dvdy.20717

Author Information

  1. Center for Molecular Medicine, Maine Medical Center Research Institute, Scarborough, Maine

  1. †

    Department of Biological Chemistry, Institute of Life Sciences, The Hebrew University of Jerusalem, 91904, Israel

  1. ‡

    Drs. Connerney, Andreeva, and Leshem contributed equally to this work.

*Center for Molecular Medicine, Maine Medical Center Research Institute, 81 Research Drive, Scarborough, ME 04074

Publication History

  1. Issue published online: 19 APR 2006
  2. Article first published online: 24 FEB 2006
  3. Manuscript Accepted: 16 JAN 2006

Funded by

  • NIH/NIDCR/NCRR. Grant Numbers: P20 RR15555, R01 DE015329
  • American Heart Association. Grant Number: 0130393
Corrected by:

Erratum: Erratum: Twist1 dimer selection regulates cranial suture patterning and fusion

Vol. 241, Issue 2, 433, Article first published online: 16 DEC 2011

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (548K)

REFERENCES

  • Annes JP, Munger JS, Rifkin DB. 2003. Making sense of latent TGFbeta activation. J Cell Sci 116: 217–224.
  • Araki K, Araki M, Miyazaki J, Vassalli P. 1995. Site-specific recombination of a transgene in fertilized eggs by transient expression of Cre recombinase. Proc Natl Acad Sci U S A 92: 160–164.
  • Bakiri L, Matsuo K, Wisniewska M, Wagner EF, Yaniv M. 2002. Promoter specificity and biological activity of tethered AP-1 dimers. Mol Cell Biol 22: 4952–4964.
  • Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. 1990. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61: 49–59.
  • Bialek P, Kern B, Yang X, Schrock M, Sosic D, Hong N, Wu H, Yu K, Ornitz DM, Olson EN, Justice MJ, Karsenty G. 2004. A twist code determines the onset of osteoblast differentiation. Dev Cell 6: 423–435.
  • Bourgeois P, Bolcato-Bellemin AL, Danse JM, Bloch-Zupan A, Yoshiba K, Stoetzel C, Perrin-Schmitt F. 1998. The variable expressivity and incomplete penetrance of the twist-null heterozygous mouse phenotype resemble those of human Saethre-Chotzen syndrome. Hum Mol Genet 7: 945–957.
  • Canfield AE, Sutton AB, Hoyland JA, Schor AM. 1996. Association of thrombospondin-1 with osteogenic differentiation of retinal pericytes in vitro. J Cell Sci 109(Pt 2): 343–353.
  • Carver EA, Oram KF, Gridley T. 2002. Craniosynostosis in Twist heterozygous mice: a model for Saethre-Chotzen syndrome. Anat Rec 268: 90–92.
    Direct Link:
  • Castanon I, Baylies MK. 2002. A Twist in fate: evolutionary comparison of Twist structure and function. Gene 287: 11–22.
  • Castanon I, Von Stetina S, Kass J, Baylies MK. 2001. Dimerization partners determine the activity of the Twist bHLH protein during Drosophila mesoderm development. Development 128: 3145–3159.
  • el Ghouzzi V, Le Merrer M, Perrin-Schmitt F, Lajeunie E, Benit P, Renier D, Bourgeois P, Bolcato-Bellemin AL, Munnich A, Bonaventure J. 1997. Mutations of the TWIST gene in the Saethre-Chotzen syndrome. Nat Genet 15: 42–46.
  • Firulli BA, Krawchuk D, Centonze VE, Vargesson N, Virshup DM, Conway SJ, Cserjesi P, Laufer E, Firulli AB. 2005. Altered Twist1 and Hand2 dimerization is associated with Saethre-Chotzen syndrome and limb abnormalities. Nat Genet 37: 373–381.
  • Funato N, Ohtani K, Ohyama K, Kuroda T, Nakamura M. 2001. Common regulation of growth arrest and differentiation of osteoblasts by helix-loop-helix factors. Mol Cell Biol 21: 7416–7428.
  • Gripp KW, Zackai EH, Stolle CA. 2000. Mutations in the human TWIST gene. Hum Mutat 15: 479.
    Direct Link:
  • Guenou H, Kaabeche K, Mee SL, Marie PJ. 2005. A role for fibroblast growth factor receptor-2 in the altered osteoblast phenotype induced by Twist haploinsufficiency in the Saethre-Chotzen syndrome. Hum Mol Genet 14: 1429–1439.
  • Hardy S, Kitamura M, Harris-Stansil T, Dai Y, Phipps ML. 1997. Construction of adenovirus vectors through Cre-lox recombination. J Virol 71: 1842–1849.
  • Horiuchi K, Amizuka N, Takeshita S, Takamatsu H, Katsuura M, Ozawa H, Toyama Y, Bonewald LF, Kudo A. 1999. Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J Bone Miner Res 14: 1239–1249.
    Direct Link:
  • Howard TD, Paznekas WA, Green ED, Chiang LC, Ma N, Ortiz de Luna RI, Garcia Delgado C, Gonzalez-Ramos M, Kline AD, Jabs EW. 1997. Mutations in TWIST, a basic helix-loop-helix transcription factor, in Saethre-Chotzen syndrome. Nat Genet 15: 36–41.
  • Isaac A, Cohn MJ, Ashby P, Ataliotis P, Spicer DB, Cooke J, Tickle C. 2000. FGF and genes encoding transcription factors in early limb specification. Mech Dev 93: 41–48.
  • Ishii M, Merrill AE, Chan YS, Gitelman I, Rice DP, Sucov HM, Maxson RE Jr. 2003. Msx2 and Twist cooperatively control the development of the neural crest-derived skeletogenic mesenchyme of the murine skull vault. Development 130: 6131–6142.
  • Jiang X, Iseki S, Maxson RE, Sucov HM, Morriss-Kay GM. 2002. Tissue origins and interactions in the mammalian skull vault. Dev Biol 241: 106–116.
  • Johnson D, Iseki S, Wilkie AO, Morriss-Kay GM. 2000. Expression patterns of Twist and Fgfr1, -2 and -3 in the developing mouse coronal suture suggest a key role for twist in suture initiation and biogenesis. Mech Dev 91: 341–345.
  • Lassar AB, Davis RD, Wright WE, Kadesh T, Murre C, Voronova A, Baltimore D, Weintraub H. 1991. Functional Activity of Myogenic HLH Proteins Requires Hetero-oligomerization with E12/E47-like Proteins in Vivo. Cell 66: 305–315.
  • Lee MS, Lowe GN, Strong DD, Wergedal JE, Glackin CA. 1999. TWIST, a basic helix-loop-helix transcription factor, can regulate the human osteogenic lineage. J Cell Biochem 75: 566–577.
    Direct Link:
  • Leshem Y, Spicer DB, Gal-Levi R, Halevy O. 2000. Hepatocyte growth factor (HGF) inhibits skeletal muscle cell differentiation: a role for the bHLH protein twist and the cdk inhibitor p27. J Cell Physiol 184: 101–109.
    Direct Link:
  • Litvin J, Selim AH, Montgomery MO, Lehmann K, Rico MC, Devlin H, Bednarik DP, Safadi FF. 2004. Expression and function of periostin-isoforms in bone. J Cell Biochem 92: 1044–1061.
    Direct Link:
  • Lyden D, Young A, Zagzag D, Yan W, Gerald W, O'Reilly R, Bader B, Hynes R, Zhuang Y, Manova K, Benezra R. 1999. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401: 670–677.
  • Massari ME, Murre C. 2000. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 20: 429–440.
  • Nah H. 2000. Suture biology: lessons from molecular genetics of craniosynostosis syndromes. Clin Orthod Res 3: 37–45.
    Direct Link:
  • Neuhold LA, Wold B. 1993. HLH forced dimers: tethering MyoD to E47 generates a dominant positive myogenic factor insulated from negative regulation by Id. Cell 74: 1033–1042.
  • Novitch BG, Spicer DB, Kim PS, Cheung WL, Lassar AB. 1999. pRb is required for MEF2-dependent gene expression as well as cell-cycle arrest during skeletal muscle differentiation. Curr Biol 9: 449–459.
  • Ogata T, Wozney JM, Benezra R, Noda M. 1993. Bone morphogenetic protein 2 transiently enhances expression of a gene, Id (inhibitor of differentiation), encoding a helix-loop-helix molecule in osteoblast-like cells. Proc Natl Acad Sci U S A 90: 9219–9222.
  • Ogle RC. 2000. Craniofacial skeletal morphogenesis in vitro. Methods Mol Biol 136: 55–59.
  • Opperman LA. 2000. Cranial sutures as intramembranous bone growth sites. Dev Dyn 219: 472–485.
    Direct Link:
  • Oram KF, Gridley T. 2005. Mutations in snail family genes enhance craniosynostosis of Twist1 haplo-insufficient mice: implications for Saethre-Chotzen Syndrome. Genetics 170: 971–974.
  • O'Rourke MP, Tam PP. 2002. Twist functions in mouse development. Int J Dev Biol 46: 401–413.
  • Oshima A, Tanabe H, Yan T, Lowe GN, Glackin CA, Kudo A. 2002. A novel mechanism for the regulation of osteoblast differentiation: transcription of periostin, a member of the fasciclin I family, is regulated by the bHLH transcription factor, twist. J Cell Biochem 86: 792–804.
    Direct Link:
  • Rice DP, Aberg T, Chan Y, Tang Z, Kettunen PJ, Pakarinen L, Maxson RE, Thesleff I. 2000. Integration of FGF and TWIST in calvarial bone and suture development. Development 127: 1845–1855.
  • Rice R, Rice DP, Thesleff I. 2005. Foxc1 integrates Fgf and Bmp signalling independently of twist or noggin during calvarial bone development. Dev Dyn 233: 847–852.
    Direct Link:
  • Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. 1997. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88: 593–602.
  • Shishido E, Higashijima S, Emori Y, Saigo K. 1993. Two FGF-receptor homologues of Drosophila: one is expressed in mesodermal primordium in early embryos. Development 117: 751–761.
  • Sigvardsson M, O'Riordan M, Grosschedl R. 1997. EBF and E47 collaborate to induce expression of the endogenous immunoglobulin surrogate light chain genes. Immunity 7: 25–36.
  • Spicer DB, Rhee J, Cheung WL, Lassar AB. 1996. Inhibition of myogenic bHLH and MEF2 transcription factors by the bHLH protein Twist. Science 272: 1476–1480.
  • Stankiewicz P, Thiele H, Baldermann C, Kruger A, Giannakudis I, Dorr S, Werner N, Kunz J, Rappold GA, Hansmann I. 2001. Phenotypic findings due to trisomy 7p15.3-pter including the TWIST locus. Am J Med Genet 103: 56–62.
    Direct Link:
  • Vinals F, Ventura F. 2004. Myogenin protein stability is decreased by BMP-2 through a mechanism implicating Id1. J Biol Chem 279: 45766–45772.
  • Vinals F, Reiriz J, Ambrosio S, Bartrons R, Rosa JL, Ventura F. 2004. BMP-2 decreases Mash1 stability by increasing Id1 expression. EMBO J 23: 3527–3537.
  • Volpert OV, Pili R, Sikder HA, Nelius T, Zaichuk T, Morris C, Shiflett CB, Devlin MK, Conant K, Alani RM. 2002. Id1 regulates angiogenesis through transcriptional repression of thrombospondin-1. Cancer Cell 2: 473–483.
  • Wilkie AO, Oldridge M, Tang Z, Maxson RE Jr. 2001. Craniosynostosis and related limb anomalies. Novartis Found Symp 232: 122–133; discussion 133–143.
  • Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. 2004. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117: 927–939.
  • Yoshida T, Phylactou LA, Uney JB, Ishikawa I, Eto K, Iseki S. 2005. Twist is required for establishment of the mouse coronal suture. J Anat 206: 437–444.
    Direct Link:
  • Yousfi M, Lasmoles F, Lomri A, Delannoy P, Marie PJ. 2001. Increased bone formation and decreased osteocalcin expression induced by reduced Twist dosage in Saethre-Chotzen syndrome. J Clin Invest 107: 1153–1161.
View Full Article (HTML) Get PDF (548K)