Muscle-bone interactions and the development of skeletal phenotype: Jaw muscles and the skull

Epigenetics: Linking Genotype and Phenotype in Development and Evolution

Volumn , Issue , 2011, Pages 221-237

  Herring, Susan W ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84857792305     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (121)

1. Allori, A. C., A. M. Sailon, J. H. Pan, and S. M. Warren. 2008. Biological basis of bone formation, remodeling, and repair. Part III: Biomechanical forces. Tissue Eng 14:285-93.
2. Aubret, F., R. Shine, and X. Bonnet. 2004. Adaptive developmental plasticity in snakes. Nature 431:261-2.
3. Baume, L. J. 1962. Ontogenesis of the human temporomandibular joint: 1. Development of the condyles. J Dent Res 41:1327-39.
4. Bikle, D. D. 2008. Integrins, insulin like growth factors, and the skeletal response to load. Osteoporos Int 19:1237-46.
5. Bouvier, M., and W. L. Hylander. 1996. The mechanical or metabolic function of secondary osteonal bone in the monkey Macaca fascicularis. Arch Oral Biol 41:941-50.
6. Boyd, T. G., W. A. Castelli, and D. F. Huelke. 1967. Removal of the temporalis muscle from its origin: Effects on the size and shape of the coronoid process. J Dent Res 46:997-1001.
7. Burn, A. K. 2007. Dietary consistency and the midline sutures: A study in growing pigs. MSD thesis, University of Washington, Seattle.
8. Carter, D. R., and G. S. Beaupré. 2001. Skeletal Function and Form. Cambridge: Cambridge University Press.
9. Cheema, U., R. Brown, V. Mudera, S. Y. Yang, G. McGrouther, and G. Goldspink. 2005. Mechanical signals and IGF-1 gene splicing in vitro in relation to development of skeletal muscle. J Cell Physiol 202:67-75.
10. Chierici, G., and A. J. Miller. 1984. Experimental study of muscle reattachment following surgical detachment. J Oral Maxillofac Surg 42:485-90.
11. Crisan, M., S. Yap, L. Casteilla, C.-W. Chen, M. Corselli, T. S. Park, G. Andriolo, et al. 2008. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301-13.
12. Cubo, J., P. Legendre, A. de Ricqles, L. Montes, E. de Margerie, J. Castanet, and Y. Desdevises. 2008. Phylogenetic, functional, and structural components of variation in bone growth rate of amniotes. Evol Dev 10:217-27.
13. de Buffrénil, V., A. Houssaye, and W. Bohme. 2008. Bone vascular supply in monitor lizards (Squamata: Varanidae): Influence of size, growth, and phylogeny. J Morphol 269:533-43.
14. Dörfl, J. 1980. Migration of tendinous insertions. I. Cause and mechanism. J Anat 131:179-95.
15. Engler, A. J., S. Sen, H. L. Sweeney, and D. E. Discher. 2006. Matrix elasticity directs stem cell lineage specification. Cell 126:677-89.
16. Engström, C., S. Kiliaridis, and B. Thilander. 1986. The relationship between masticatory function and craniofacial morphology. II. A histological study in the growing rat fed a soft diet. Eur J Orthod 8:271-9.
17. Forwood, M. R., L. Li, W. L. Kelly, and M. B. Bennett. 2001. Growth hormone is permissive for skeletal adaptation to mechanical loading. J Bone Miner Res 16:2284-90.
18. Franz-Odendaal, T. A., K. Ryan, and B. K. Hall. 2007. Developmental and morphological variation in the teleost craniofacial skeleton reveals an unusual mode of ossification. J Exp Zoolog B Mol Dev Evol 308:709-21.
19. Fricke, O., Z. Sumnik, B. Tutlewski, A. Stabrey, T. Remer, and E. Schoenau. 2008. Local body composition is associated with gender differences of bone development at the forearm in puberty. Horm Res 70:105-11.
20. German, R. Z., A. W. Crompton, and A. J. Thexton. 2008. Variation in EMG activity: A hierarchical approach. Integr Comp Biol 48:283-93.
21. Gouchie, G. M., L. F. Roberts, and R. J. Wassersug. 2008. The effect of mirrors on African clawed frog (Xenopus laevis) larval growth, development, and behavior. Behav Ecol Sociobiol 62:1821-9.
22. Graham, M. R., B. Davies, F. M. Grace, A. Kicman, and J. S. Baker. 2008. Anabolic steroid use: Patterns of use and detection of doping. Sports Med 38:505-25.
23. Hall, B. K. 2005. Bones and Cartilage: Developmental and Evolutionary Skeletal Biology. London: Elsevier Academic.
24. Hall, B. K., and S. W. Herring. 1990. Paralysis and growth of the musculoskeletal system in the embryonic chick. J Morphol 206:45-56.
25. Hallgrímsson, B., and D. E. Lieberman. 2008. Mouse models and the evolutionary developmental biology of the skull. Integr Comp Biol 48:373-84.
26. Hamrick, M. W., and S. L. Ferrari. 2008. Leptin and the sympathetic connection of fat to bone. Osteoporos Int 19:905-12.
27. Hamrick, M. W., A. C. McPherron, C. O. Lovejoy, and J. Hudson. 2000. Femoral morphology and crosssectional geometry of adult myostatin-deficient mice. Bone 27:343-9.
28. Hamrick, M. W., K. H. Ding, C. Pennington, Y. J. Chao, Y. D. Wu, B. Howard, D. Immel, et al. 2006. Age-related loss of muscle mass and bone strength in mice is associated with a decline in physical activity and serum leptin. Bone 39:845-53.
29. Hamrick, M. W., K.-H. Ding, S. Ponnala, S. L. Ferrari, and C. M. Isales. 2008. Caloric restriction decreases cortical bone mass but spares trabecular bone in the mouse skeleton: Implications for the regulation of bone mass by body weight. J Bone Miner Res 23:870-8.
30. Heaney, R. P. 2003. Is the paradigm shifting? Bone 33:457-65.
31. Herring, S. W. 1985a. The ontogeny of mammalian mastication. Am Zool 25:339-49.
32. Herring, S. W. 1985b. Morphological correlates of masticatory patterns in peccaries and pigs. J Mammal 66:603-17.
33. Herring, S. W. 1994. Development of functional interactions between skeletal and muscular systems. In: Bone, vol 9, ed. B. K. Hall, 165-91. Boca Raton, FL: CRC Press.
34. Herring, S. W. 2003a. Ontogenetic integration of form and function. In: Keywords and Concepts in Evolutionary Developmental Biology, ed. B. K. Hall and W. M. Olson, 275-9. Cambridge, MA: Harvard University Press.
35. Herring, S. W. 2003b. TMJ anatomy and animal models. J Musculoskelet Neuronal Interact 3:391-4.
36. Herring, S. W. 2007. Masticatory muscles and the skull: A comparative perspective. Arch Oral Biol 52:296-9.
37. Herring, S. W., and T. C. Lakars. 1981. Craniofacial development in the absence of muscle contraction. J Craniofac Genet Dev Biol 1:341-57.
38. Herring, S. W., J. D. Decker, Z. J. Liu, and T. Ma. 2002. The temporomandibular joint in miniature pigs: Anatomy, cell replication, and relation to loading. Anat Rec 266:152-66.
39. Hirukawa, K., K. Miyazawa, H. Maeda, Y. Kameyama, S. Goto, and A. Togari. 2005. Effect of tensile force on the expression of IGF-1 and IGF-1 receptor in the organ-cultured rat cranial suture. Arch Oral Biol 50:367-72.
40. Hoyte, D. A. N. 1971. Mechanisms of growth in the cranial vault and base. J Dent Res 50:1447-59.
41. Hoyte, D. A. N., and D. H. Enlow. 1966. Wolff's law and the problem of muscle attachment on resorptive surfaces of bone. Am J Phys Anthropol 24:205-14.
42. Humphrey, T. 1971. Development of oral and facial motor mechanisms in human fetuses and their relation to craniofacial growth. J Dent Res 50:1428-41.
43. Hylander, W. L. 1975. The human mandible: Lever or link? Am J Phys Anthropol 43:227-42.
44. Hylander, W. L. 1979. An experimental analysis of temporomandibular joint reaction force in macaques. Am J Phys Anthropol 51:433-56.
45. Hylander, W. L., and R. Bays. 1979. An in vivo straingauge analysis of the squamosal-dentary joint reaction force during mastication and incisal biting in Macaca mulatta and Macaca fascicularis. Arch Oral Biol 24:689-97.
46. Karaharju-Suvanto, T., J. Peltonen, R. Ranta, O. Laitinen, and A. Kahri. 1996. The effect of gradual distraction of the mandible on the sheep temporomandibular joint. Int J Oral Maxillofac Surg 25:152-6.
47. Karasik, D., and D. P. Kiel. 2008. Genetics of the musculoskeletal system: A pleiotropic approach. J Bone Miner Res 23:788-802.
48. Kasra, M., and M. D. Grynpas. 1995. The effects of androgens on the mechanical properties of primate bone. Bone 17:265-70.
49. Katsaros, C., A. Zissis, A. Bresin, and S. Kiliaridis. 2006. Functional influence on sutural bone apposition in the growing rat. Am J Orthod Dentofacial Orthop 129:352-7.
50. Kiel, D. P., S. L. Ferrari, L. A. Cupples, D. Karasik, D. Manen, A. Imamovic, A. G. Herbert, and J. Dupuis. 2007. Genetic variation at the low-density lipoprotein receptor-related protein 5 (LRP5) locus modulates Wnt signaling and the relationship of physical activity with bone mineral density in men. Bone 40:587-96.
51. Kiliaridis, S., B. Thilander, H. Kjellberg, N. Topouzelis, and A. Zafiriadis. 1999. Effect of low masticatory function on condylar growth: A morphometric study in the rat. Am J Orthod Dentofacial Orthop 116:121-5.
52. Kim, J.-Y., S.-T. Kim, S.-W. Cho, H.-S. Jung, K.-T. Park, and H.-K. Son. 2008. Growth effects of botulinum toxin type A injected into masseter muscle on a developing rat mandible. Oral Dis 14:626-32.
53. Kim, S. G., J. W. Ha, and J. C. Park. 2004. Histological changes in the temporomandibular joint in rabbits depending on the extent of mandibular lengthening by osteodistraction. Br J Oral Maxillofac Surg 42:559-65.
54. Koh, C. J., D. M. Delo, J. W. Lee, M. M. Siddiqui, R. P. Lanza, S. Soker, J. J. Yoo, and A. Atala. 2009. Parthenogenesis-derived multipotent stem cells adapted for tissue engineering applications. Methods 47:90-7.
55. Lakars, T. C., and S. W. Herring. 1980. Ontogeny of oral function in hamsters (Mesocricetus auratus). J Morphol 165:237-54.
56. Langenbach, G. E. J., B. van der Zwan, L. Mulder, and T. van Eijden. 2008. Influence of muscle activity on the degree of bone mineralisation. Special Issue B, J Dent Res 87:Abstract 3571, www.dentalresearch.org.
57. Lanyon, L. E. 1980. The influence of function on the development of bone curvature. An experimental study on the rat tibia. J Zool 192:457-66.
58. Laron, Z. 2001. Insulin-like growth factor 1 (IGF-1): A growth hormone. Mol Pathol 54:311-6.
59. Lee, A. H. 2004. Histological organization and its relationship to function in the femur of Alligator mississippiensis. J Anat 204:197-207.
60. Lee, K., H. Jessop, R. Suswillo, G. Zaman, and L. Lanyon. 2003. Bone adaptation requires oestrogen receptor-a. Nature 424:389.
61. Lee, T. C., A. Staines, and D. Taylor. 2002. Bone adaptation to load: Microdamage as a stimulus for bone remodelling. J Anat 201:437-46.
62. Lieberman, D. E., G. E. Krovitz, F. W. Yates, M. Devlin, and M. St. Claire. 2004. Effects of food processing on masticatory strain and craniofacial growth in a retrognathic face. J Hum Evol 46:655-77.
63. Lindsten, R., T. Magnusson, B. Ogaard, and E. Larsson. 2004. Effect of food consistency on temporomandibular joint morphology: An experimental study in pigs. J Orofac Pain 18:56-61.
64. Liu, Z. J., and S. W. Herring. 2000. Masticatory strains on osseous and ligamentous components of the jaw joint in miniature pigs. J Orofac Pain 14:265-78.
65. Liu, Z. J., V. Shcherbatyy, G. Gu, and J. A. Perkins. 2008. Effects of tongue volume reduction on craniofacial growth: A longitudinal study on orofacial skeletons and dental arches. Arch Oral Biol 53:991-1001.
66. Luder, H.-U. 1996. Postnatal Development, Aging, and Degeneration of the Temporomandibular Joint in Humans, Monkeys, and Rats. Ann Arbor: Center for Human Growth and Development, University of Michigan.
67. Marks, L., S. Teng, J. Årtun, and S. Herring. 1997. Reaction strains on the condylar neck during mastication and maximum muscle stimulation in different condylar positions: An experimental study in the miniature pig. J Dent Res 76:1412-20.
68. Matic, D. B., A. Yazdani, R. G. Wells, T. Y. Lee, and B. S. Gan. 2007. The effects of masseter muscle paralysis on facial bone growth. J Surg Res 139:243-52.
69. Matsuoka, T., P. E. Ahlberg, N. Kessaris, P. Iannarelli, U. Dennehy, W. D. Richardson, A. P. McMahon, and G. Koentges. 2005. Neural crest origins of the neck and shoulder. Nature 436:347-55.
70. Matsuyuki, T., T. Kitahara, and A. Nakashima. 2006. Developmental changes in craniofacial morphology in subjects with Duchenne muscular dystrophy. Eur J Orthod 28:42-50.
71. Mavropoulos, A., S. Kiliaridis, A. Bresin, and P. Ammann. 2004. Effect of different masticatory functional and mechanical demands on the structural adaptation of the mandibular alveolar bone in young growing rats. Bone 35:191-7.
72. Melton, L. J., III, B. L. Riggs, S. J. Achenbach, S. Amin, J. J. Camp, P. A. Rouleau, R. A. Robb, A. L. Oberg, and S. Khosla. 2006. Does reduced skeletal loading account for age-related bone loss? J Bone Miner Res 21:1847-55.
73. Middleton, K. M., C. E. Shubin, D. C. Moore, P. A. Carter, T. Garland, Jr., and S. M. Swartz. 2008. The relative importance of genetics and phenotypic plasticity in dictating bone morphology and mechanics in aged mice: Evidence from an artificial selection experiment. Zoology (Jena) 111:135-47.
74. Morgan, T. J., T. J. Garland, and P. Carter. 2003. Ontogenies in mice selected for high voluntary wheel-running activity. I. Mean ontogenies. Evolution 57:646-57.
75. Moss, M. L., and M. A. Meehan. 1970. Functional cranial analysis of the coronoid process in the rat. Acta Anat 77:11-24.
76. Nara-Ashizawa, N., L. J. Liu, T. Higuchi, K. Tokuyama, K. Hayashi, Y. Shirasaki, H. Amagai, and S. Saitoh. 2002. Paradoxical adaptation of mature radius to unilateral use in tennis playing. Bone 30:619-23.
77. Noden, D. M., and P. A. Trainor. 2005. Relations and interactions between cranial mesoderm and neural crest populations. J Anat 207:575-601.
78. Notelovitz, M. 2002. Androgen effects on bone and muscle. Fertil Steril 77 (Suppl 4): S34-41.
79. Novacek, M. J. 1992. Mammalian phylogeny: Shaking the tree. Nature 356:121-5.
80. Ochareon, P. 2004. Craniofacial periosteal cell capacities. PhD diss., University of Washington, Seattle.
81. Ödman, A., A. Mavropoulos, and S. Kiliaridis. 2008. Do masticatory functional changes influence the mandibular morphology in adult rats. Arch Oral Biol 53:1149-54.
82. Orwoll, E. S. 2003. Men, bone and estrogen: Unresolved issues. Osteoporos Int 14:93-8.
83. Parfitt, A. M. 2002. Targeted and nontargeted bone remodeling: Relationship to basic multicellular unit origination and progression. Bone 30:5-7.
84. Pearson, H. 2008. Disputed definitions. Nature 455:1023-24.
85. Pearson, O. M., and D. E. Lieberman. 2004. The aging of Wolff's "law": Ontogeny and responses to mechanical loading in cortical bone. Ybk Phys Anthropol 47:63-99.
86. Plochocki, J. H., J. P. Rivera, C. Zhang, and S. A. Ebba. 2008. Bone modeling response to voluntary exercise in the hindlimb of mice. J Morphol 269:313-8.
87. Powell, J. A., L. Petherbridge, and B. E. Flucher. 1996. Formation of triads without the dihydropyridine receptor a subunits in cell lines from dysgenic skeletal muscle. J Cell Biol 134:375-87.
88. Proffit, W. R. 1986. Contemporary Orthodontics. St. Louis: Mosby.
89. Rafferty, K. L., Z. Sun, M. A. Egbert, and S. W. Herring. 2004. Bony strains in response to distractor activation. In: Biological Mechanisms of Tooth Movement and Craniofacial Adaptation, ed. Z. Davidovitch and J. Mah, 59-62. Bangkok: Harvard Society for the Advancement of Orthodontics.
90. Rafferty, K. L., Z. Sun, M. A. Egbert, E. E. Baird, and S. W. Herring. 2006. Mandibular mechanics following osteotomy and appliance placement. II. Bone strain on the body and condylar neck. J Oral Maxillofac Surg 64:620-7.
91. Rafferty, K. L., Z. Sun, M. A. Egbert, D. W. Bakko, and S. W. Herring. 2007. Changes in growth and morphology of the condyle following mandibular distraction in minipigs: Overloading or underloading? Arch Oral Biol 52:967-76.
92. Ravosa, M. J., R. Kunwar, S. R. Stock, and M. S. Stack. 2007. Pushing the limit: Masticatory stress and adaptive plasticity in mammalian craniomandibular joints. J Exp Biol 210:628-41.
93. Ravosa, M. J., E. K. López, R. A. Menegaz, S. R. Stock, M. S. Stack, and M. W. Hamrick. 2008. Using "mighty mouse" to understand masticatory plasticity: Mostatin-deficient mice and musculoskeletal function. Integr Comp Biol 48:345-359.
94. Renn, J., C. Winkler, M. Schartl, R. Fischer, and R. Goerlich. 2006. Zebrafish and medaka as models for bone research including implications regarding space-related issues. Protoplasma 229:209-14.
95. Rieppel, O. 1987. The development of the trigeminal jaw adductor musculature and associated skull elements in the lizard Podarcis sicula. J Zool Lond 212:131-50.
96. Rot-Nikcevic, I., T. Reddy, K. J. Downing, A. C. Belliveau, B. Hallgrimsson, B. K. Hall, and B. Kablar. 2006. Myf5-/-:MyoD-/-amyogenic fetuses reveal the importance of early contraction and static loading by striated muscle in mouse skeletogenesis. Dev Genes Evol 216:1-9.
97. Rot-Nikcevic, I., K. J. Downing, B. K. Hall, and B. Kablar. 2007. Development of the mouse mandibles and clavicles in the absence of skeletal myogenesis. Histol Histopathol 22:51-60.
98. Rowlands, A. S., P. A. George, and J. J. Cooper-White. 2008. Directing osteogenic and myogenic differentiation of MSCs: Interplay of stiffness and adhesive ligand presentation. Am J Physiol Cell Physiol 295:C1037-C1044.
99. Sample, S. J., M. Behan, L. D. Smith, W. E. Oldenhoff, M. D. Markel, V. L. Kalscheur, Z. Hao, V. Miletic, and P. Muir. 2008. Functional adaptation to loading of a single bone is neuronally regulated and involves multiple bones. J Bone Miner Res 23: 1372-81.
100. Saxon, L. K., and C. H. Turner. 2006. Low-dose estrogen treatment suppresses periosteal bone formation in response to mechanical loading. Bone 39:1261-7.
101. Schmidt, B. L., L. Kung, C. Jones, and N. Casap. 2002. Induced osteogenesis by periosteal distraction. J Oral Maxillofac Surg 60:1170-5.
102. Seeman, E. 2008. Bone quality: The material and structural basis of bone strength. J Bone Miner Metab 26:1-8.
103. Sibonga, J. D., H. J. Evans, H. G. Sung, E. R. Spector, T. F. Lang, V. S. Oganov, A. V. Bakulin, L. C. Shackelford, and A. D. LeBlanc. 2007. Recovery of spaceflight-induced bone loss: Bone mineral density after long-duration missions as fitted with an exponential function. Bone 41:973-8.
104. Smith, K. K. 1994. Development of craniofacial musculature in Monodelphis domestica (Marsupialia, Didelphidae). J Morphol 222:149-73.
105. Spyropoulos, M. N. 1977. The morphogenetic relationship of the temporal muscle to the coronoid process in human embryos and fetuses. Am J Anat 150:395-409.
106. Stokes, I. A. F., K. C. Clark, C. E. Farnum, and D. D. Aronsson. 2007. Alterations in the growth plate associated with growth modulation by sustained compression or distraction. Bone 41:197-205.
107. Stucki-McCormick, S. U. 1998. The effect of distraction osteogenesis on the temporomandibular joint. In: Distraction Osteogenesis and Tissue Engineering, ed. J. A. J. McNamara and C.-A. Trotman, 75-103. Ann Arbor: Center for Human Growth and Development, University of Michigan. Suominen, H. 2006. Muscle training for bone strength. Aging Clin Exp Res 18:85-93.
108. Takeda, S., F. Elefteriou, R. Levasseur, X. Liu, L. Zhao, K. L. Parker, D. Armstrong, P. Ducy, and G. Karsenty. 2002. Leptin regulates bone formation via the sympathetic nervous system. Cell 111:305-17.
109. Teng, S., and S. W. Herring. 1998. Compressive loading on bone surfaces from muscular contraction: An in vivo study in the miniature pig, Sus scrofa. J Morphol 238:71-80.
110. Thongudomporn, U., V. Chongsuvivatwong, and A. F. Geater. 2009. The effect of maximum bite force on alveolar bone morphology. Orthod Craniofac Res 12:1-8.
111. Thurmüller, P., M. J. Troulis, A. Rosenberg, S.-K. Chuang, and L. B. Kaban. 2006. Microscopic changes in the condyle and disc in response to distraction osteogenesis of the minipig mandible. J Oral Maxillofac Surg 64:249-58.
112. Tuominen, M., T. Kantomaa, and P. Pirtiniemi. 1994. Effect of altered loading on condylar growth in the rat. Acta Odontol Scand 52:129-34.
113. Turner, R. T. 1999. Mechanical signaling in the development of postmenopausal osteoporosis. Lupus 8:388-92.
114. Vilmann, H., M. Juhl, and S. Kirkeby. 1985. Bone-muscle interactions in the muscular dystrophic mouse. Eur J Orthod 7:185-92.
115. Wake, M. H., and J. Hanken. 1982. Development of the skull of Dermophis mexicanus (Amphibia: Gymnophiona), with comments on skull kinesis and amphibian relationships. J Morphol 173: 203-23.
116. Warner, S. E., D. A. Sanford, B. A. Becker, S. D. Bain, S. Srinivasan, and T. S. Gross. 2006. Botox induced muscle paralysis rapidly degrades bone. Bone 38:257-64.
117. Weisbecker, V., A. Goswami, S. Wroe, and M. R. Sánchez- Villagra. 2008. Ossification heterochrony in the therian postcranial skeleton and the marsupial-placental dichotomy. Evolution 62:2027-41.
118. Westerlind, K. C., T. J. Wronski, E. L. Ritman, Z.-P. Luo, K.-N. An, N. H. Bell, and R. T. Turner. 1997. Estrogen regulates the rate of bone turnover but bone balance in ovariectomized rats is modulated by prevailing mechanical strain. Proc Natl Acad Sci USA 94:4199-204.
119. Wong, M., and D. R. Carter. 2003. Articular cartilage functional histomorphology and mechanobiology: A research perspective. Bone 33:1-13.
120. Zaman, G., H. L. Jessop, M. Muzylak, R. L. De Souza, A. A. Pitsilides, J. S. Price, and L. L. Lanyon. 2006. Osteocytes use estrogen receptor a to respond to strain but their ERa content is regulated by estrogen. J Bone Miner Res 21:1297-306.
121. Zofková, I. 2008. Hormonal aspects of the muscle-bone unit. Physiol Res 57 (Suppl 1): S159-69.