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Dura mater secretes soluble heparin-binding factors required for cranial suture morphogenesis

  • Lynne A. Opperman
  • Ralph W. Passarelli
  • Amber A. Nolen
  • Thomas J. Gampper
  • Kant Y. K. Lin
  • Roy C. Ogle
Cellular Models

Summary

Cranial sutures play a critical role in calvarial morphogenesis, serving as bone growth centers during skull enlargement. Defective suture morphogenesis, resulting in premature osseous obliteration of sutures and their failure to function appropriately, causes severe craniofacial anomalies. Previously published data demonstrated osseous obliteration of coronal suturesin vitro in the absence of dura mater and the rescue of sutures from osseous obliteration in rudiments cocultured with dura mater on the opposite sides of 0.45-μm polycarbonate filters. With thisin vitro culture system, experiments were designed to examine the nature of the soluble signal secreted by dura mater, required for maintaining intact sutures. The signal remained active in conditioned medium produced from dura mater, which was capable of rescuing coronal sutures from osseous obliteration in calvaria cultured without dura mater. When conditioned medium was segregated into heparin-binding and non-heparin-binding fractions, the signal capable of maintaining intact coronal sutures cosegregated with the heparin-binding component and remained functional in the absence of the non-heparin-binding component of conditioned medium. Evidence indicates that soluble, heparin-binding factors secreted by the dura mater act as osteoinhibitory signals at the suture site.

Key words

development in vitro calvaria rat growth factors 

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References

  1. Alberius, P.; Jonell, O. Immunohistochemical assessment of cranial suture development in rats. J. Anat. 173:61–68; 1990.PubMedGoogle Scholar
  2. Baer, M. J. Patterns of growth of the skull as revealed by vital staining. Hum. Biol. 26:80–126; 1954.PubMedGoogle Scholar
  3. Burgess, W. H.; Maciag, T. The heparin-binding (fibroblast) growth factor family of proteins. Ann. Rev. Biochem. 58:575–606; 1989.PubMedCrossRefGoogle Scholar
  4. Centrella, M.; Massague, J.; Canalis, E. Human platelet-derived transforming growth factor-β stimulates parameters of bone growth in fetal rat calvaria. Endocrinology 119:2306–2312; 1986.PubMedCrossRefGoogle Scholar
  5. Cohen, M. M., Jr. Sutural biology and the correlates of craniosynostosis. Am. J. Med. Genet. 47:581–616; 1993.PubMedCrossRefGoogle Scholar
  6. Couly, G. F.; Coltey, P. M.; Le Douarin, N. M. The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 114:1–15; 1992.PubMedGoogle Scholar
  7. Couly, G. F.; Coltey, P. M.; Le Douarin, N. M. The triple origin of skull in higher vertebrates. Development 117:40–429; 1993.Google Scholar
  8. DrsAmore, P. Modes of FGF release in vivo and in vitro. Cancer Met. Rev. 9:227–238; 1990.CrossRefGoogle Scholar
  9. Dionne, C. A.; Crumley, A.; Bellot, F., et al. Cloning and expression of two distinct high affinity receptors cross-reacting with acidic and basic fibroblast growth factors. EMBO J. 9:2685–2692; 1990.PubMedGoogle Scholar
  10. Drake, D. B.; Persing, J. A.; Berman, D. E., et al. Calvarial deformity regeneration following subtotal calvariectomy for craniosynostosis: a case report and theoretical implications. J. Craniofac. Surg. 4:85–89; 1993.PubMedCrossRefGoogle Scholar
  11. Enlow, D. H. Normal and abnormal patterns of craniofacial growth. In: Persing, J. A.; Edgerton, M. T.; Jane, J. A. (Eds.). Scientific Foundations and Surgical Treatment of Craniosynostosis. Williams and Wilkins, Baltimore: 83–86; 1989.Google Scholar
  12. Frenkel, S. R.; Grande, D. A.; Collins, M., et al. Fibroblast growth factor in chick osteogenesis. Biomaterials 11:38–40; 1990.PubMedGoogle Scholar
  13. Frenkel, S. R.; Herskovits, M. S.; Singh, I. J. Fibroblast growth factor: effect on osteogenesis and chondrogenesis in the chick embryo. Acta Anat. 145:265–268; 1992.PubMedCrossRefGoogle Scholar
  14. Jabs, E. W.; Muller, U.; Li, X., et al. A mutation in the homeodomain of the human msx2 gene in a family affected with autosomal dominant craniosynostosis. Cell 75:443–450; 1993.PubMedCrossRefGoogle Scholar
  15. Jabs, E. W.; Li, X.; Scott, A. F., et al. Jackson-Weiss and Crouzon syndromes are allelic with mutations in fibroblast receptor 2. Nature Genet. 8:275–279; 1994.PubMedCrossRefGoogle Scholar
  16. Kasperk, C. H.; Wergedal, J. E.; Mohan, S., et al. Interactions of growth factors present in bone matrix with bone cells: effects on DNA synthesis and alkaline phosphatase. Growth Fact. 3:147–158; 1990.Google Scholar
  17. Liu, Y. H.; Kundu, R.; Wu, L., et al. Premature suture closure and ectopic cranial bone in mice expressing Msx2 transgenes in the developing skull. Proc. Natl. Acad. Sci. USA 92:6137–6141; 1995.PubMedCrossRefGoogle Scholar
  18. Mabbutt, L. W.; Kokich, V. G. Calvarial and sutural redevelopment following craniectomy in the neonatal rabbit. J. Anat. 2:413–422; 1979.Google Scholar
  19. McCaffrey, T. A.; Falcone, D. J.; Du, B. Transforming growth factor-β1 is a heparin-binding protein: identification of putative heparin-binding regions and isolation of heparins with varying affinity for TGF-β1. J. Cell. Physiol. 152:430–440; 1992.PubMedCrossRefGoogle Scholar
  20. Melcher, A. H. Cells from soft connective tissue depress osteogenesisin vitro. In: Davidovich, Z., ed. The biological mechanisms of tooth eruption and root resorption. Birmingham, AL: EBSCO Media; 1988:87–91.Google Scholar
  21. Miki, T.; Bottaro, D. P.; Fleming, T. P., et al. Determination of ligand-binding specificity by alternative splicing: two distinct growth factor receptors encoded by a single gene. Proc. Natl. Acad. Sci. USA 89:246–250; 1992.PubMedCrossRefGoogle Scholar
  22. Moss, M. L. Inhibition and stimulation of sutural fusion in the rat calvaria. Anat. Rec. 136:457–467; 1960.PubMedCrossRefGoogle Scholar
  23. Muenke, M.; Schell, U.; Hehr, A., et al. A common mutation in the fibroblast growth factor receptor 1 gene in Pfeiffer syndrome. Nature Genet. 8:269–274; 1994.PubMedCrossRefGoogle Scholar
  24. Ogiso, B.; Hughes, F. J.; Melcher, A. H., et al. Fibroblasts inhibit mineralized bone nodule formation by rat bone marrow stromal cells in vitro. J. Cell. Physiol. 146:442–450; 1991.PubMedCrossRefGoogle Scholar
  25. Opperman, L. A.; Passarelli, R. W.; Morgan, E. P., et al. Cranial sutures require tissue interactions with dura mater to resist osseous obliteration in vitro. J. Bone Min. Res. 12:1978–1987; 1995.CrossRefGoogle Scholar
  26. Opperman, L. A.; Persing, J. A.; Sheen, R., et al. In the absence of periosteum, fetal and neonatal coronal sutures resist osseous obliteration in a rat transplant model. J. Craniofac. Surg. 5:327–332; 1994.PubMedCrossRefGoogle Scholar
  27. Opperman, L. A.; Saunders, T. J.; Bruns, D. E., et al. Estrogen inhibits calbindin-D28k expression in mouse uterus. Endocrinology 130:1728–1735; 1992.PubMedCrossRefGoogle Scholar
  28. Opperman, L. A.; Sweeney, T. M.; Redmon, J., et al. Tissue interactions with underlying dura mater inhibit osseous obliteration of developing cranial sutures. Dev. Dynam. 198:312–322; 1993.Google Scholar
  29. Orr-Uretreger, A.; Bedford, M. T.; Burakova, T., et al. Developmental localization of the splicing alternatives of fibroblast growth factor receptor-2 (FGFR2). Dev. Biol. 158:475–486; 1993.CrossRefGoogle Scholar
  30. Orr-Uretreger, A.; Givol, D.; Yahon, A., et al. Developmental expression of two murine fibroblast growth factor receptors, flg and bek. Development 113:1419–1434; 1991.Google Scholar
  31. Reardon, W.; Winter, R. M.; Rutland, P., et al. Mutations in the fibroblast growth factor receptor 2 gene cause Crouzon syndrome. Nature Genet. 8:98–103; 1994.PubMedCrossRefGoogle Scholar
  32. Roth, D. A.; Longaker, M. T.; Breitbart, A. S., et al. The role of transforming growth factor beta-1 in rat cranial suture fusion. 63rd Annual Scientific Meeting ASPRS-PSEF-ASMS, San Diego, California, September, 1994: 39–40.Google Scholar
  33. Smith, D. W.; Tondury, G. Origin of the calvaria and its sutures. Am. J. Dis. Child. 132:662–666; 1978.PubMedGoogle Scholar
  34. ten Dijke, P.; Iwata, K. K.; Goddard, C., et al. Recombinant transforming growth factor type β3: biological activities and receptor-binding properties in isolated bone cells. Mol. Cell. Biol. 10:4473–4479; 1990.PubMedGoogle Scholar
  35. Wilkie, A. O. M.; Slaney, S. F.; Oldridge, M., et al. Apert syndrome results from localized mutations ofFGFR2 and is allelic with Crouzon syndrome. Nature Genet. 9:165–172; 1995.PubMedCrossRefGoogle Scholar
  36. Yahon, A.; Zimmer, Y.; Guo-Hong, S., et al. A confined variable region confers ligand binding specificity on fibroblast growth factor receptors: implications for the origin of the immunoglobulin fold. EMBO J. 11:1885–1890; 1992.Google Scholar

Copyright information

© Society for In Vitro Biology 1996

Authors and Affiliations

  • Lynne A. Opperman
    • 1
    • 2
  • Ralph W. Passarelli
    • 2
  • Amber A. Nolen
    • 1
  • Thomas J. Gampper
    • 2
  • Kant Y. K. Lin
    • 2
  • Roy C. Ogle
    • 1
  1. 1.Department of Neurological SurgeryHealth Sciences Center, University of VirginiaCharlottesville
  2. 2.Department of Plastic SurgeryHealth Sciences Center, University of VirginiaCharlottesville

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