Seminars in Orthodontics
Volume 11, Issue 4 , Pages 199-208 , December 2005

Genetic Factors Influencing Morphogenesis and Growth of Sutures and Synchondroses in the Craniofacial Complex

  • Lynne A. Opperman

      Affiliations

    • Department of Biomedical Sciences, Baylor College of Dentistry, Texas A&M University System Health Science Center, Dallas, TX.
    • Corresponding Author InformationAddress correspondence to Lynne A. Opperman, PhD, Texas A&M University System Health Science Center, Baylor College of Dentistry, Department of Biomedical Sciences, 3302 Gaston Ave, Dallas, TX 75246; Phone: (214) 828-8134; Fax: (214) 828-8951.
  • ,
  • Peter T. Gakunga

      Affiliations

    • University of Texas at San Antonio Health Science Center, San Antonio, TX.
  • ,
  • David S. Carlson

      Affiliations

    • Department of Biomedical Sciences, Baylor College of Dentistry, Texas A&M University System Health Science Center, Dallas, TX.

References 

  1. Enlow DH . Normal craniofacial growth . In:  Cohen MMJ ,  MacLean RE editor. Craniosynostosis, Diagnosis, Evaluation and Management . New York: Oxford University Press; 2000;p. 35–50
  2. Bjork A , Skieller V , et al.   Postnatal growth and development of the maxillary complex. Factors affecting the growth of the midface . In: Craniofacial Growth Series . Vol 6: Ann Arbor: University of Michigan; 1996;p. 61–100
  3. Enlow DH , Bang S . Growth and remodeling of the human maxilla . Am J Orthod . 1965;51:446–464
  4. Enlow DH . Normal and abnormal patterns of craniofacial growth . In:  Persing JA ,  Edgerton MT ,  Jane JA editor. Scientific Foundations and Surgical Treatment of Craniosynostosis . Baltimore: Williams and Wilkins; 1989;p. 83–86
  5. Kember NF , Kirkwood JK . Cell kinetics and the study of longitudinal bone growth (a perspective) . In:  Dixon AD ,  Sarnat BG ,  Hoyt DAN editor. Fundamentals of Bone Growth (Methodology and Applications) . Boca Raton: CRC Press; 1991;p. 153–162
  6. Dixon AD , Gakunga PT . Morphometric changes in growth of the rat pelvis after papain administration . Anat Rec . 1993;235:312–315
  7. Petrovic A , Charlier J-P . La synchondrose spheno-occipital de jeune rat en culture d’organes (mise en evidence d’un potentiel de croissance independent) . C R Acad Sci (Paris) D . 1967;265–268
  8. Copray JC , Jansen HW , Duterloo HS . Growth and growth pressure of mandibular condylar and some primary cartilages of the rat in vitro . Am J Orthodont Dentofac Orthop . 1986;90:19–23
  9. Gakunga PT , Kuboka Y , Opperman LA . Hyaluronan is essential for lacunae expansion during longitudinal growth of the cranial base synchondrosis . J Craniofac Genet Dev Biol . 2000;20:53–63
  10. Shum L , Wang X , Kane AA , et al.   BMP4 promotes chondrocyte proliferation and hypertrophy in the endochondral cranial base . Int J Dev Biol . 2003;47:423–431
  11. Kantomaa T , Pirttiniemi P , Tuominen M . Cranial base and the growth of the cranial vault (an experimental study on the rabbit) . Proc Finn Dent Soc . 1991;87:93–98
  12. Donrebos J . Morphogenesis of the spheno-occipital and the presphenoidal synchondroses in the cranial base of the fetal Wistar rat . Acta Morph Netherlands Scand . 1973;11:63–65
  13. Roberts GJ . Growth of the cartilages of the cranial base (preliminary studies on Rattus norvegicus) . Proc R Soc Med . 1975;68:130–133
  14. Roberts GJ , Blackwood HJ . Growth of the cartilages of the mid-line cranial base (a radiographic and histological study) . J Anat . 1983;136:307–320
  15. Ma W , Lozanoff S . Morphological deficiency in the prenatal anterior cranial base of midfacially retrognathic mice . J Anat . 1996;188(Pt 3):547–555
  16. Chen L , Adar R , Yang X , et al.   Gly368Cys mutation in mouse FGFR3 causes achondroplaysia by affecting both chondrogenesis and osteogenesis . J Clin Invest . 1999;104:1517–1525
  17. Cohen MMJ . Craniosynostosis, diagnosis, evaluation and management . In: 2nd ed.. New York: Oxford University Press; 2000;p. 454
  18. Horowitz SL . The cranial base in craniofacial dysostosis (Crouzon disease). A case report . J Proc Finn Dent Soc . 1981;77:57–62
  19. Peterson-Falzone SJ , Figueroa AA . Longitudinal changes in cranial base angulation in mandibulofacial dysostosis . Cleft Palate Craniofac J . 1989;26:31–35
  20. Jensen BL , Kreiborg S . Development of the skull in infants with cleidocranial dysplasia . J Craniofac Genet Dev Biol . 1993;13:89–97
  21. Kjaer I , Hansen N , Becktor KB . Craniofacial morphology, dentition, and skeletal maturity in four siblings with Seckel syndrome . Cleft Palate Craniofac J . 2001;38:645–651
  22. Baer MJ . Patterns of growth of the skull as revealed by vital staining . Hum Biol . 1954;26:80–126
  23. Moss ML . Growth of the calvaria in the rat. The determination of osseous morphology . Am J Anat . 1954;94:333–362
  24. Kokich VG . The biology of sutures . In:  Cohen MMJ editors. Craniosynostosis, Diagnosis, Evaluation and Management . New York: Raven Press; 1986;p. 81–103
  25. Cohen MM . Craniofacial disorders caused by mutations in homeobox genes MSX1 and MSX2 . J Craniofac Genet Dev Biol . 2000;20:19–25
  26. Mooney MP , Losken HW , Tschakaloff A . Congenital bilateral coronal suture synostosis in a rabbit and craniofacial growth comparisons with experimental models . Cleft Palate Craniofac J . 1993;30:121–128
  27. Stelnicki EJ , Vanderwall K , Harrison MR . The in utero correction of unilateral coronal craniosynostosis . Plast Reconstr Surg . 1998;101:287–296
  28. Perlyn CA , Marsh JL , Pilgram TK . Plasticity of the endocranial base in nonsyndromic craniosynostosis . Plast Reconstr Surg . 2001;108:294–301
  29. Lee KS , Kim YS , Kim DH . Parathyroid hormone-related peptide delays terminal differentiation of chondrocytes during endochondral bone development . Endocrinology . 1996;137:5109–5118
  30. Suda N , Shibata S , Yamazaki K . Parathyroid hormone related protein regulates proliferation of condylar hypertrophic chondrocytes . J Bone Min Res . 1999;14:1838–1847
  31. Ishii-Suzuki M , Suda N , Yamazaki K . Differential responses to parathyroid hormone-related protein (PTHrP) deficiency in the various craniofacial cartilages . Anat Rec . 1999;255:452–457
  32. Chen P , Vukicevic S , Sampath TK . Osteogenic protein-1 promotes growth and maturation of chick sternal chondrocytes in serum-free cultures . J Cell Sci . 1995;108:105–114
  33. Serra R , Johnson M , Filvaroff EH . Expression of a truncated, kinase-defective Tgf-beta type II receptor in mouse skeletal tissue promotes terminal chondrocyte differentiation and osteoarthritis . J Cell Biol . 1997;139:41–52
  34. Kramer J , Hegert C , Guan K , et al.   Embryonic stem cell-derived chondrogenic differentiation in vitro (activation by BMP-2 and BMP-4) . Mech Dev . 2000;92:193–205
  35. Shiang R , Thompson LM , Zhu YZ . Mutations in the transmembrane domain of FGFR3 cause the most common genetic form of dwarfism, achondroplasia . Cell . 1994;78:335–342
  36. Deng C , Wynshaw-Boris A , Zhou F . Fibroblast growth factor receptor 3 is a negative regulator of bone growth . Cell . 1996;84:911–921
  37. Visnapuu V , Peltomaki T , Ronning O . Growth hormone and insulin-like growth factor I receptors in the temporomandibular joint of the rat . J Dent Res . 2001;80:1903–1907
  38. Ito Y , Bringas P , Mogharei A . Receptor-regulated and inhibitory Smads are critical in regulating transforming growth factor beta-mediated Meckel’s cartilage development . Dev Dyn . 2002;224:69–78
  39. Rosado E , Schwartz Z , Sylvia VL . Transforming growth factor beta1 regulation of growth zone chondrocytes is mediated by multiple interacting pathways . Biochim Biophys Acta . 2002;1590:1–15
  40. Gakunga PT , Opperman LA . Tgf-β modulates the differentiation and growth of the cranial base . J Dent Res . 1999;79:1298; (abs)
  41. Wang X , Mao JJ . Accelerated chondrogenesis of the rabbit cranial base growth plate by oscillatory mechanical stimuli . J Bone Miner Res . 2002;17:1843–1850
  42. Wang X , Mao JJ . Chondrocyte proliferation of the cranial base cartilage upon in vivo mechanical stresses . J Dent Res . 2002;81:701–705
  43. Pritchard JJ , Scott JH , Girgis FG . The structure and development of cranial and facial sutures . J Anat . 1956;90:73–86
  44. Johansen VA , Hall SH . Morphogenesis of the mouse coronal suture . Acta Anat . 1982;114:58–67
  45. Kjaer I . Prenatal skeletal maturation of the human maxilla . J Craniofac Genet Dev Biol . 1989;9:257–264
  46. Kim HJ , Rice DP , Kettunen PJ . FGF-, BMP- and Shh-mediated signalling pathways in the regulation of cranial suture morphogenesis and calvarial bone development . Development . 1998;125:1241–1251
  47. Opperman LA , Sweeney TM , Redmon J . Tissue interactions with underlying dura mater inhibit osseous obliteration of developing cranial sutures . Dev Dyn . 1993;198:312–322
  48. Opperman LA , Passarelli RW , Morgan EP . Cranial sutures require tissue interactions with dura mater to resist osseous obliteration in vitro . J Bone Miner Res . 1995;10:1978–1987
  49. Opperman LA , Passarelli RW , Nolen AA . Dura mater secretes soluble heparin-binding factors required for cranial suture morphogenesis . In Vitro Cell Dev Biol Anim . 1996;32:627–632
  50. Cohen MM . Sutural biology and the correlates of craniosynostosis . Am J Med Genet . 1993;47:581–616
  51. Opperman LA , Nolen AA , Ogle RC . TGF-beta 1, TGF-beta 2, and TGF-beta 3 exhibit distinct patterns of expression during cranial suture formation and obliteration in vivo and in vitro [see comments] . J Bone Miner Res . 1997;12:301–310
  52. Roth DA , Bradley JP , Levine JP . Studies in cranial suture biology: part I. Increased immunoreactivity for TGF-beta isoforms (beta 1, beta 2, and beta 3) during rat cranial suture fusion . J Bone Miner Res . 1997;12:311–321 [see comments]
  53. Rice DP , Kim HJ , Thesleff I . Apoptosis in murine calvarial bone and suture development . Eur J Oral Sci . 1999;107:265–275
  54. Roth DA , Gold LI , Han VK . Immunolocalization of transforming growth factor beta 1, beta 2, and beta 3 and insulin-like growth factor I in premature cranial suture fusion . Plast Reconstr Surg . 1997;99:300–309 [see comments]; discussion 310-316
  55. Opperman LA , Adab K , Gakunga PT . TGF-B2 and TGF-B3 regulate fetal rat cranial suture morphogenesis by regulating rates of cell proliferation and apoptosis . Dev Dyn . 2000;219:237–247
  56. Opperman LA , Chhabra A , Cho RW . Cranial suture obliteration is induced by removal of transforming growth factor (TGF)-beta 3 activity and prevented by removal of TGF-beta 2 activity from fetal rat calvaria in vitro . J Craniofac Genet Dev Biol . 1999;19:164–173
  57. Opperman LA , Chhabra A , Nolen AA . Dura mater maintains rat cranial sutures in vitro by regulating suture cell proliferation and collagen production . J Craniofac Genet Dev Biol . 1998;18:150–158
  58. Zhou G , Chen Y , Zhou L . CBFA1 mutation analysis and functional correlation with phenotypic variability in cleidocranial dysplasia . Hum Mol Genet . 1999;8:2311–2316
  59. Liu YH , Kundu R , Wu L . Premature suture closure and ectopic cranial bone in mice expressing Msx2 transgenes in the developing skull . Proc Natl Acad Sci USA . 1995;92:6137–6141
  60. Carver EA , Oram KF , Gridley T . Craniosynostosis in Twist heterozygous mice (a model for Saethre-Chotzen syndrome) . Anat Rec . 2002;268:90–92
  61. Warren SM , Brunet LJ , Harland RM . The BMP antagonist noggin regulates cranial suture fusion . Nature . 2003;422:625–629
  62. Bellus GA , Gaudenz K , Zackai EH . Identical mutations in three different fibroblast growth factor receptor genes in autosomal dominant craniosynostosis syndromes . Nat Genet . 1996;14:174–176
  63. Jabs EW , Muller U , Li X . A mutation in the homeodomain of the human MSX2 gene in a family affected with autosomal dominant craniosynostosis . Cell . 1993;75:443–450
  64. Jabs EW , Li X , Scott AF . Jackson-Weiss and Crouzon syndromes are allelic with mutations in fibroblast growth factor receptor 2 . [published erratum appears in Nat Genet 9:451, 1995] Nat Genet . 1994;8:275–279
  65. Meyers GA , Day D , Goldberg R . FGFR2 exon IIIa and IIIc mutations in Crouzon, Jackson-Weiss, and Pfeiffer syndromes (evidence for missense changes, insertions, and a deletion due to alternative RNA splicing) . Am J Hum Genet . 1996;58:491–498
  66. Muenke M , Schell U , Hehr A . A common mutation in the fibroblast growth factor receptor 1 gene in Pfeiffer syndrome . Nat Genet . 1994;8:269–274
  67. Muenke M , Moloney DM , Twigg SR . A unique point mutation in the fibroblast growth factor receptor 3 gene (FGFR3) defines a new craniosynostosis syndrome . Am J Hum Genet . 1997;60:555–564
  68. Reardon W , Winter RM , Rutland P . Mutations in the fibroblast growth factor receptor 2 gene cause Crouzon syndrome . Nat Genet . 1994;8:98–103
  69. Wilkie AO , Slaney SF , Oldridge M . Apert syndrome results from localized mutations of FGFR2 and is allelic with Crouzon syndrome [see comments] . Nat Genet . 1995;9:165–172
  70. Galvin BD , Hart KC , Meyer AN . Constitutive receptor activation by Crouzon syndrome mutations in fibroblast growth factor receptor (FGFR)2 and FGFR2/Neu chimeras . Proc Natl Acad Sci USA . 1996;93:7894–7899
  71. Naski MC , Colvin JS , Coffin JD . Repression of hedgehog signaling and BMP4 expression in growth plate cartilage by fibroblast growth factor receptor 3 . Development . 1998;125:4977–4988
  72. Anderson J , Burns HD , Enriquez-Harris P . Apert syndrome mutations in fibroblast growth factor receptor 2 exhibit increased affinity for FGF ligand . Hum Mol Genet . 1998;7:1475–1483
  73. Ma L , Golden S , Wu L , et al.   The molecular basis of Boston-type craniosynostosis (the Pro148–>His mutation in the N-terminal arm of the MSX2 homeodomain stabilizes DNA binding without altering nucleotide sequence preferences) . Hum Mol Genet . 1996;5:1915–1920
  74. el Ghouzzi V , Le Merrer M , Perrin-Schmitt F . Mutations of the TWIST gene in the Saethre-Chotzen syndrome . [see comments] Nat Genet . 1997;15:42–46
  75. Howard TD , Paznekas WA , Green ED . Mutations in TWIST, a basic helix-loop-helix transcription factor, in Saethre-Chotzen syndrome . [see comments] Nat Genet . 1997;15:36–41
  76. Rice DP , Kim HJ , Thesleff I . Detection of gelatinase B expression reveals osteoclastic bone resorption as a feature of early calvarial bone development . Bone . 1997;21:479–486
  77. Iseki S , Wilkie AO , Heath JK . Fgfr2 and osteopontin domains in the developing skull vault are mutually exclusive and can be altered by locally applied FGF2 . Development . 1997;124:3375–3384
  78. Kreiborg S . Postnatal growth and development of the craniofacial complex in premature craniosynostosis . In:  Cohen MMJ editors. Craniosynostosis, Diagnosis, Evaluation and Management . New York: Oxford University Press; 2000;p. 158–174
  79. Scott JH . Growth at the facial sutures . Am J Orthod . 1956;42:381–387
  80. Babler W . Relationship of altered cranial suture growth to cranial base and midface . In:  Persing JA ,  Edgerton MT ,  Jane JA editor. Scientific Foundations and Surgical Treatment of Craniosynostosis . Baltimore: Williams and Wilkins; 1989;p. 87–95
  81. Moss ML . The functional matrix . In:  Kraus BS ,  Riedel RA editor. Vistas in Orthodontics . Philadelphia: Lea and Febiger; 1960;p. 279
  82. Scott JH . Growth of the human face . Proc R Soc Med . 1953;47:91–100
  83. Scott JH . The cartilage of the nasal septum . Br Dent J . 1953;95:37–40
  84. Sarnat BG . Postnatal growth of the upper face . Angle Orthod . 1963;33:139; (abs)
  85. Adab K , Sayne JR , Carlson DS . Tgf-β1, Tgf-β2, Tgf-β3 and Msx2 expression is elevated during frontonasal suture morphogenesis and during active postnatal facial growth . Orthod Craniofac Res . 2002;5:227–237
  86. Adab K , Sayne JR , Carlson DS . Tgf-B1, Tgf-B2, Tgf-B3 and Msx2 expression during rat frontonasal suture morphogenesis and postnatal facial growth . Orthod Craniofac Res . 2002;5:227–237
  87. Massler M , Schour I . The growth pattern of the cranial vault in the albino rat as measured by vital staining with alizarin red “S.” . Anat Rec . 1951;110:83–101
  88. Mooney MP , Burrows AM , Smith TD . Correction of coronal suture synostosis using suture and dura mater allografts in rabbits with familial craniosynostosis . Cleft Palate Craniofac J . 2001;38:206–225
  89. Moursi AM , Winnard PL , Fryer D . Delivery of transforming growth factor-beta2-perturbing antibody in a collagen vehicle inhibits cranial suture fusion in calvarial organ culture . Cleft Palate Craniofac J . 2003;40:225–232
  90. Opperman LA , Moursi A , Sayne JR . Transforming growth factor-beta 3 (Tgf-β3) in a collagen gel delays fusion of the rat posterior interfrontal suture in vivo . Anat Rec . 2002;267:120–130
  91. Chong SL , Mitchell R , Moursi AM . Rescue of coronal suture fusion using transforming growth factor-beta 3 (Tgf-β3) in rabbits with delayed-onset craniosynostosis . Anat Rec . 2003;274:962–971

PII: S1073-8746(05)00041-1

doi: 10.1053/j.sodo.2005.07.004

Seminars in Orthodontics
Volume 11, Issue 4 , Pages 199-208 , December 2005