Interplay of mechanical loading and growth factors in the mandibular condyle

Archives of Oral Biology

Volumn 53, Issue 8, 2008, Pages 709-715

  Von den Hoff, J W ^a   Delatte, M ^b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

Author keywords

Cartilage; Craniofacial growth deformities; Functional appliances; Growth factor; Mandibular condyle; Mechanical loading

Indexed keywords

GROWTH PROMOTOR; SIGNAL PEPTIDE;

ANIMAL; HUMAN; MANDIBLE CONDYLE; MECHANICAL STRESS; PHYSIOLOGY; RAT; REVIEW; WEIGHT BEARING;

ANIMALS; GROWTH SUBSTANCES; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MANDIBULAR CONDYLE; RATS; STRESS, MECHANICAL; WEIGHT-BEARING;

EID: 45049083602     PISSN: 00039969     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.archoralbio.2008.03.002     Document Type: Review

References (96)

1. Enlow D.H. Bone and cartilage. In: Enlow D.H. (Ed). Facial growth. 3rd ed. (1990), W B Saunders Co., Philadelphia
2. Vinkka H. Secondary cartilages in the facial skeleton of the rat. Proc Finn Dent Soc 78 Suppl. VII (1982) 1S-137S
3. Beresford W.A. Chondroid bone, secondary cartilage and metaplasia (1981), Urban & Schwarzenberg, Baltimore-Munich
4. Ghafari J, Heeley, Shapiro IM. Morphologic study of cartilages of the rat craniofacial skeleton: classification as osteogenic and/or supportive. In: Davidovitch Z, editor. Biological mechanisms of tooth movement and craniofacial adaptation. Columbus, Ohio: The Ohio state university college of dentistry; 1992.
5. Mizoguchi I., Nakamura M., Takahashi I., Kagayama M., and Mitani H. A comparison of the immunohistochemical localisation of type I and type II collagens in craniofacial cartilages of the rat. Acta Anat 144 (1992) 59-64
6. Delatte M., Von den Hoff J.W., van Rheden R.E., and Kuijpers-Jagtman A.M. Primary and secondary cartilages of the neonatal rat: the femoral head and the mandibular condyle. Eur J Oral Sci 112 (2004) 156-162
7. Delatte M., Von den Hoff J.W., Maltha J.C., and Kuijpers-Jagtman A.M. Growth stimulation of mandibular condyles and femoral heads of newborn rats by IGF-I. Arch Oral Biol 49 (2004) 165-175
8. Delatte M., Von den Hoff J.W., Nottet S.J., De Clerck H.J., and Kuijpers-Jagtman A.M. Growth regulation of the rat mandibular condyle and femoral head by transforming growth factor-{beta}1, fibroblast growth factor-2 and insulin-like growth factor-I. Eur J Orthod 27 (2005) 17-26
9. Delatte M., Von den Hoff J.W., and Kuijpers-Jagtman A.M. Regulatory effects of FGF-2 on the growth of mandibular condyles and femoral heads from newborn rats. Arch Oral Biol 50 (2005) 959-969
10. Ramirez-yanez G.O., Young W.G., Daley T.J., and Waters M.J. Influence of growth hormone on the mandibular condyle of rats. Arch Oral Biol 49 (2004) 585-590
11. Talwar R.M., Wong B.S., Svoboda K., and Harper R.P. Effects of estrogen on chondrocyte proliferation and collagen synthesis in skeletally mature articular cartilage. J Oral Maxillofac Surg 64 (2006) 600-609
12. Shum L., and Nuckolls G. The life cycle of chondrocytes in the developing skeleton. Arthritis Res 4 (2002) 94-106
13. Copray J.C., Jansen H.W., and Duterloo H.S. Effects of compressive forces on proliferation and matrix synthesis in mandibular condylar cartilage of the rat in vitro. Arch Oral Biol 30 (1985) 299-304
14. Salo L., and Kantomaa T. Type II collagen expression in the mandibular condyle during growth adaptation: an experimental study in the rabbit. Calcif Tissue Int 52 (1993) 465-469
15. Kantomaa T., Tuominen M., Pirttiniemi P., and Rönning O. Weaning and the histology of the mandibular condyle in the rat. Acta Anat 144 (1992) 311-315
16. Kantomaa T., Pirttiniemi P., Tuominen M., and Poikela A. Glycosaminoglycan synthesis in the mandibular condyle during growth adaptation. Acta Anat 151 (1994) 88-96
17. Pirttiniemi P., Kantomaa T., Salo L., and Tuominen M. Effect of reduced articular function on deposition of type I and type II collagens in the mandibular condylar cartilage of the rat. Arch Oral Biol 41 (1996) 127-131
18. Nakai H., Niimi A., and Ueda M. The influence of compressive loading on growth of cartilage of the mandibular condyle in vitro. Arch Oral Biol 43 (1998) 505-515
19. Ichikawa J., Hara T., Tamatsu Y., and Ide Y. Morphological changes in the internal structure of the articular eminence of the temporal bone during growth from deciduous to early mixed dentition. J Biomech 40 (2007) 3541-3547
20. Huja S.S., Rummel A.M., and Beck F.M. Changes in mechanical properties of bone within the mandibular condyle with age. J Morphol 269 (2008) 138-143
21. Tuominen M., Kantomaa T., and Pirttiniemi P. Effect of altered loading on condylar growth in the rat. Acta Odontol Scand 52 (1994) 129-134
22. Kantomaa T., and Pirttiniemi P. Differences in the biological response of the mandibular condyle to forward traction or opening of the mandible. An experimental study in the rat. Acta Odontol Scand 54 (1996) 138-144
23. Rabie A.B., She T.T., and Hägg U. Functional appliance therapy accelerates and enhances condylar growth. Am J Dentofacial Orthop 123 (2003) 40-48
24. Asano T. The effects of mandibular retractive force on the growing rat mandible. Am J Dentofacial Orthop 90 (1986) 464-474
25. Cholasueksa P., Warita H., and Soma K. Alterations of the rat temporomandibular joint in functional posterior displacement of the mandible. Angle Orthod 74 (2004) 6777-6783
26. Fuentes M.A., Opperman L.A., Buschang P., Bellinger L.L., Carlson D.S., and Hinton R.J. Lateral functional shift of the mandible. Part II. Effects on gene expression in condylar cartilage. Am J Dentofacial Orthop 123 (2003) 160-166
27. Liu C., Kaneko S., and Soma K. Effects of a mandibular lateral shift on the condyle and mandibular bone in growing rats. Angle Orthod 77 (2007) 787-793
28. Meikle M.C. Remodeling of the dentofacial skeleton: the biological basis of orthodontics and dentofacial orthopedics. J Dent Res 1 (2007) 12-24
29. Cozza P., Baccetti T., Franchi L., De Toffol L., and McNamara J.A. Mandibular changes produced by functional appliances in Class II malocclusion: a systematic review. Am J Orthod Dentofacial Orthop 129 (2006) 599.e1-599.e12
30. Carlevaro M.F., Cermelli S., Cancedda R., and Descalzi Cancedda F. Vascular endothelial growth factor (VEGF) in cartilage neovascularization and chondrocyte differentiation: auto-paracrine role during endochondral bone formation. J Cell Sci 113 (2000) 59-69
31. Rabie A.B., and Hägg U. Factors regulating mandibular condylar growth. Am J Orthod Dentofacial Orthop 122 (2002) 401-409
32. Aoyama J., Tanaka E., Miyauchi, Takata T., Hanaoka K., Hattori Y., et al. Immunolocalization of vascular endothelial growth factor in rat condylar cartilage during postnatal development. Histochem Cell Biol 122 (2004) 35-40
33. Yee G., Yu Y., Walsh W.R., Lindeman R., and Poole M.D. The immunolocalisation of VEGF in the articular cartilage of sheep mandibular condyles. J Craniomaxillofac Surg 31 (2003) 244-251
34. Xiong H., Rabie A.B., and Hägg U. Neovascularization and mandibular condylar bone remodeling in adult rats under mechanical strain. Front Biosci 10 (2005) 74-82
35. Papadopoulou A.K., Papachristou D.J., Chatzopoulos S.A., Pirttiniemie P., Papavassiliou A.G., and Basdra E.K. Load application induces changes in the expression levels of Sox-9. FGFR-3 and VEGF in condylar chondrocytes. FEBS Lett 581 (2007) 2041-2046
36. Mohan S., and Baylink D.J. Bone growth factors. Clin Orthop Relat Res 263 (1991) 30-48
37. Shimaski S., and Ling N. Identification and molecular characterization of insulin-like growth factor binding proteins (IGFBP-1, -2, -3, -4, -5 and -6). Prog Growth Factor Res 3 (1992) 243-266
38. Minuto F., Palermo C., Arvigo M., and Barreca A.M. The IGF system and bone. J Endocrinol Invest 28 (2005) 8-10
39. Werner H., and Katz J. The emerging role of the insulin-like growth factors in oral biology. J Dent Res 83 (2004) 832-836
40. Visnapuu V., Peltomäki T., Rönning O., and Syrjanen S. Distribution of insulin-like growth factor-I mRNA in the mandibular condyle and rib cartilage of the rat during growth. Arch Oral Biol 47 (2002) 791-798
41. Visnapuu V., Peltomäki T., Rönning O., Vahlberg T., and Helenius H. Growth hormone and insulin-like growth factor I receptors in the temporomandibular joint of the rat. J Dent Res 80 (2001) 1903-1907
42. Maor G., Hochberg Z., and Silbermann M. Insulin-like growth factor I accelerates proliferation and differentiation of cartilage progenitor cells in cultures of neonatal mandibular condyles. Acta Endocrinologica 128 (1993) 56-64
43. Fuentes M.A., Opperman L.A., Bellinger L.L., Carlson D.S., and Hinton R.J. Regulation of cell proliferation in rat mandibular condylar cartilage in explant culture by insulin-like growth factor-I and fibroblast growth factor-2. Arch Oral Biol 47 (2002) 643-654
44. Itoh K., Suzuki S., and Kuroda T. Effects of local administration of insulin-like growth factor-I on mandibular condylar growth in rats. J Med Dent Sci 50 (2003) 79-85
45. Haijar D., Santos M.F., and Kimura E.T. Propulsive appliance stimulates the synthesis of insulin-like growth factors I and II in the mandibular condylar cartilage of young rats. Arch Oral Biol 48 (2003) 635-642
46. Filla M.S., Dam P., and Rapraeger A.C. The cell surface proteoglycan syndecan-1 mediates fibroblast growth factor-2 binding and activity. J Cell Physiol 147 (1998) 310-321
47. Gospodarowicz D., Ferrara N., Schweigerer L., and Neufeld G. Structural characterization and biological functions of fibroblast growth factor. Endocr Rev 8 (1987) 95-114
48. Alini M., Marriott A., Chen T., Abe S., and Poole A.R. A novel angiogenic molecule produced at the time of chondrocyte hypertrophy during endochondral bone formation. Dev Biol 176 (1996) 124-132
49. Tajima Y., Kawasaki M., Kurihara K., Ueha T., and Yokose S. Immunohistochemical profile of basic fibroblast growth factor and heparan sulphate in adult rat mandibular condylar cartilage. Arch Oral Biol 43 (1998) 873-877
50. Molteni A., Modrowski D., Hott M., and Marie P.J. Differential expression of fibroblast growth factor receptor-1, -2, and -3 and syndecan-1, -2 and -4 in neonatal rat mandibular condyle and calvaria during osteogenic differenciation in vitro. Bone 24 (1999) 337-347
51. Ogawa T., Shimokawa H., and Fukada K. Localization and inhibitory effect of basic fibroblast growth factor on chondrogenesis in cultured mouse mandibular condyle. J Bone Miner Metab 21 (2003) 145-153
52. Roberts A.B., and Sporn M.B. Physiological actions and clinical applications of transforming growth factor-β (TGF-β). Growth Factors 8 (1993) 1-9
53. Grimaud E., Heymann D., and Redini F. Recent advances in TGF-β effects on chondrocyte metabolism. Potential therapeutic roles of TGF-β in cartilage disorders. Cytokine Growth Factor Rev 13 (2002) 241-257
54. Massague J. Receptors for the TGF-β family. Cell 69 (1992) 1067-1070
55. Horner A., Kemp P., Summers C., Bord S., Bishop N.J., Kelsall A.W., et al. Expression and distribution of transforming growth factor-β isoforms and their signaling receptors in growing human bone. Bone 23 (1998) 95-102
56. Fukumura K., Matsunaga S., Yamamoto T., Nagamine T., Ishidou Y., and Sakou T. Immunolocalization of transforming growth factor-betas and type I and type II receptors in rat articular cartilage. Anticancer Res 18 (1998) 4189-4193
57. Crabb I.D., O'Keefe R.J., Puzas J.E., and Rosier R.N. Synergistic effect of transforming growth factor β and fibroblast growth factor on DNA synthesis in chick growth plate chondrocytes. J Bone Miner Res 11 (1990) 1105-1112
58. O'Keefe R.J., Crabb I.D., Puzas J.E., and Rosier R.N. Effects of transforming growth factor-β1 and fibroblast growth factor on DNA synthesis in growth plate chondrocytes are enhanced by insulin-like growth factor-1. J Orthop Res 12 (1994) 299-310
59. Ballock R.T., Heydemann A., Wakefield L.M., Flanders K.C., Roberts A.B., and Sporn M.B. TGF-beta-1 prevents hypertrophy of epiphyseal chondrocytes: regulation of gene expression for cartilage matrix proteins and metalloproteases. Dev Biol 158 (1993) 414-429
60. Böhme K., Winterhalter K.H., and Bruckner P. Terminal differentiation of chondrocytes in culture is a spontaneous process and is arrested by transforming growth factor-β2 and basic fibroblast growth factor in synergy. Exp Cell Res 216 (1995) 191-198
61. Ferguson C.M., Schwarz E.M., Reynolds P.R., Puzas J.E., Rosier R.N., and O'Keefe R.J. Smad2 and 3 mediate transforming growth factor-β1-induced inhibition of chondrocyte maturation. Endocrinology 141 (2000) 4728-4735
62. 1 in the condylar cartilages of rapidly growing rats. Chin J Dent Res 2 (1998) 52-56
63. Malaviya P., and Nerem R.M. Fluid-induced shear stress stimulates chondrocyte proliferation partially mediated via TGF-beta1. Tissue Eng 8 (2002) 581-590
64. Ohno S., Tanaka N., Ueki M., Honda K., Tanimoto K., Yoneno K., et al. Mechanical regulation of terminal chondrocyte differentiation via RGD-CAP/beta ig-h3 induced by TGF-beta. Connect Tissue Res 46 (2005) 227-234
65. Aspenberg P., Basic N., Tägil M., and Vukicevic S. Reduced expression of BMP-3 due to mechanical loading: a link between mechanical stimuli and tissue differentiation. Acta Orthop Scand 71 (2000) 558-562
66. Vortkamp A., Lee K., Lanske B., Segre G.V., Kronenberg H.M., and Tabin C.J. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273 (1996) 613-622
67. Lee K., Lanske B., Karaplis A.C., Deeds J.D., Kohno H., Nissenson R.A., et al. Parathyroid hormone-related peptide delays terminal differentiation of chondrocytes during endochondral bone development. Endocrinology 137 (1996) 5109-5118
68. Stevens D.A., and Williams G.R. Hormone regulation of chondrocyte differentiation and endochondral bone formation. Mol Cell Endocrinol 151 (1999) 195-204
69. de Crombrugghe B., Lefebvre Véronique, and Nakashima K. Regulatory mechanisms in the pathways of cartilage and bone formation. Curr Opin Cell Biol 13 (2001) 721-727
70. St-Jacques B., Hammerschmidt M., and McMahon A.P. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 13 (1999) 2072-2086
71. Vortkamp A., Pathi S., Peretti G.M., Caruso E.M., Zaleske D.J., and Tabin C.J. Recapitulation of signals regulating embryonic bone formation during postnatal growth and in fracture repair. Mech Dev 71 (1998) 65-76
72. Shibukawa Y., Young B., Wu C., Yamada S., Long F., Pacifi M., et al. Temporomandibular joint formation and condyle growth require Indian hedgehog signaling. Dev Dyn 236 (2007) 426-434
73. Wu Q., Zhang Y., and Chen Q. Indian hedgehog is an essential component of mechanotransduction complex to stimulate chondrocyte proliferation. J Biol Chem 276 (2001) 35290-35296
74. Tang G.H., Rabie A.B.M., and Hägg U. Indian Hedgehog: a mechanotransduction mediator in condylar cartilage. J Dent Res 83 (2004) 434-438
75. Provot S., and Schipani E. Molecular mechanisms of endochondral bone development. Biochem Biophys Res Commun 328 (2005) 658-665
76. Shimizu T. Participation of Runx2 in mandibular condylar cartilage development. Eur J Med Res 11 (2006) 455-461
77. Tang G.H., and Rabie A.B. Runx2 regulates endochondral ossification in condyle during mandibular advancement. J Dent Res 84 (2005) 166-171
78. Xiong H., Rabie A.B., and Hägg U. Mechanical strain leads to condylar growth in adult rats. Front Biosci 10 (2005) 67-73
79. Van Lam S., and Rabie A.B. Mechanical strain induces Cbfa1 and type X collagen expression in mandibular condyle. Front Biosci 10 (2005) 2966-2971
80. Manopinivate A., Kaneko S., and Soma K. An impact of masticatory muscle function on IL-1beta and SOX9 expression in condyle. J Med Dent Sci 53 (2006) 67-74
81. Papachristou D., Pirttiniemi P., Kantomaa T., Papavassiliou A.G., and Basdra E.K. JNK/ERK-AP-1/Runx2 induction "paves the way" to cartilage load-ignited chondroblastic differentiation. Histochem Cell Biol 124 (2005) 215-223
82. Westermark B., and Heldin C.H. Platelet-derived growth factor. Structure, function and implications in normal and malignant cell growth. Acta Oncol 32 (1993) 101-105
83. Wroblewski J., and Edwall C. PDGF BB stimulates proliferation and differentiation in cultured chondrocytes from rat rib growth plate. Cell Biol Int Rep 16 (1992) 133-144
84. Copray J.C., Brouwer N., Prins A.P., and Jansen H.W. Effects of polypeptide growth factors on mandibular condylar cartilage of the rat in vitro. J Biol Buccale 16 (1988) 109-117
85. Visnapuu V., Peltomaki T., Ronning O., Vahlberg T., and Helenius H. Distribution of fibroblast growth factors (FGFR-1 and -3) and platelet-derived growth factor receptors (PDGFR) in the rat mandibular condyle during growth. Orthod Craniofac Res 5 (2002) 147-153
86. Takigawa M., Nakanishi T., Kubota S., and Nishida T. Role of CTGF/HCS24/ecogenin in skeletal growth control. J Cell Physiol 194 (2003) 256-266
87. Fukunaga T., Yamashiro T., Oya S., Takeshita N., Takigawa M., and Takano-Yamamoto T. Connective tissue growth factor mRNA expression pattern in cartilages is associated with their type I collagen expression. Bone 33 (2003) 911-918
88. Wong M., Siegrist M., and Goodwin K. Cyclic tensile strain and cyclic hydrostatic pressure differentially regulate expression of hypertrophic markers in primary chondrocytes. Bone 33 (2003) 685-693
89. Chaqour B., and Goppelt-Struebe M. Mechanical regulation of the Cyr61/CCN1 and CTGF/CCN2 proteins. FEBS Lett 273 (2006) 3639-3649
90. van den Berg W.B. The role of cytokines and growth factors in cartilage destruction in osteoarthritis and rheumatoid arthritis. J Rheumatol 58 (1999) 136-141
91. Goldring S.R., and Goldring M.B. The role of cytokines in cartilage matrix degeneration in osteoarthritis. Clin Orthop Relat Res 427S (2004) S27-S36
92. Cawston T.E., Milner J.M., Catterall J.B., and Rowan A.D. Cytokine synergy, collagenases and cartilage collagen breakdown. Biochem Soc Symp 70 (2003) 125-133
93. Moos V., Fickert S., Müller B., Weber U., and Sieper J. Immunohistological analysis of cytokine expression in human osteoarthritic and healthy cartilage. J Rheumatol 26 (1999) 870-879
94. Millward-Sadler S.J., and Salter D.M. Integrin-dependent signal cascades in chondrocyte mechanotransduction. Ann Biomed Eng 32 (2004) 435-446
95. Li Q.F., and Rabie A.B. A new approach to control condylar growth by regulating angiogenesis. Arch Oral Biol 52 (2007) 1009-1017
96. Rabie A.B., Dai J., and Xu R. Recombinant AAV-mediated VEGF gene therapy induces mandibular condylar growth. Gene Ther 14 (2007) 972-980