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Osteoclasts are large, multinucleated cells that have capacity to degrade bone tissue 1 , 2. Osteoblasts secrete bone matrix molecules, mostly collagen, and mineralize them to construct calcified tissue 3. A portion of osteoblasts is embedded in the bone matrix and these cells differentiate into osteocytes. The balance between bone resorption and formation is strictly regulated by various biological systems, including the endocrine, nervous, immune and musculoskeletal system itself 1 , 2.
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During locomotion and exercise, bones are exposed to mechanical loading, one of the crucial triggering factors for bone remodeling that adapts the bones to the loading condition 3 , 4 , 5. Exercise is known to increase bone mass and density; on the other hand, unloading causes a decrease in bone mass 6 , 7. The loading onto the bone causes deformation of the bone matrix and fluid flow in the bone lacuna and canaliculi, in which osteocytes are embedded. Osteocytes are thought to sense such changes and respond to them by expressing cytokines 8 , 9.
We previously demonstrated that the osteocyte is an indispensable source of RANKL for osteoclast differentiation 10 , Osteocytes secrete Wnt1 and its inhibitor sclerostin.
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Sclerostin suppresses osteoblast differentiation and its expression is negatively correlated with the force loaded onto the bone 3. IGF-1 is the most abundant growth factor in the bone matrix and promotes osteoblastogenesis It was shown that osteocytes highly express IGF-1 and its expression is upregulated by mechanical loading 13 , Thus, bone tissue is remodeled in response to mechanical loading, which is largely dependent on osteocytes and their expressed cytokines. During the growth period, the jawbone is subjected to certain forces imposed by the surrounding tissues, including the teeth and oro-facial muscles masticatory, lingual and mimetic muscles.
Therefore, the resulting adult facial profile is believed to be closely associated with these forces, especially the ones generated by the masticatory muscles, which play a central role in food ingestion: a brachyofacial pattern short face in individuals with strong masticatory force and a dolicofacial pattern long face in individuals with weak Animal models of reduced mastication, induced by liquid or powder diets, recapitulate the phenotypes seen in humans 16 , However, it is unclear if masticatory force by itself is a sufficient cause in such skeletal phenotypes.
The underlying cellular and molecular mechanisms remain elusive as well. Here, we established a novel increased mastication mouse model by feeding mice with a HD, thus burdening maxillofacial tissues with a higher mechanical load. HD increased mastication frequency and enlarged the masseter muscles. Using a computer simulation, mechanical loading onto the lower jawbone mandibular bone by the masseter muscle, the masticatory muscle with the largest muscular force, was indicated to induce extrusion of the masseteric ridge and a shortening of the mandibular ramus. Micro-CT analysis showed that the extrusion and the shortening were more prominent in mice fed with the HD.
In the extruded masseteric ridge of these mice, there was an increase of IGF-1 and a decrease of sclerostin in osteocytes, both of which are implicated in the promotion of bone formation. IGF-1 was shown to enhance osteoblastogenesis of the cells in the tendon.
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These findings taken together indicate that the osteocytes in the mandibular bone increase IGF-1 and decrease sclerostin expression as the result of mechanical load. The alteration in the local cytokine milieu adjacent to the enthesis leads to bone formation, resulting in morphological change in the mandibular bone so the mechanical stress in the bone can be alleviated.
In order to impose a higher mechanical load on the musculoskeletal tissue of the maxillofacial region, we developed a HD in which nutrition component is changed so that the hardness is greater than in a normal diet ND Fig. The change did not result in any significant difference in food intake or body weight between the ND— and HD—fed mice Supplementary Fig.
Analyses on the bone and muscle of the limbs indicated that the difference between the diets did not cause either hypertrophy or atrophy in these tissues Supplementary Fig. Establishment of a novel increased mastication model. Analyses of the hard diet and its effects on mice. In total, — muscle fibers per group were analyzed. The number of biological replicates used in each animal experiment was shown under the corresponding bar. During the ingestion of the two diets, mastication frequency and time were significantly higher in the mice fed with the HD than the ND Fig. The fiber width of the masseter muscle, which is crucial for occlusion and mastication, was larger in the mice fed with the HD than the ND Fig.
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The neuronal activity of the primary motor cortex M1 region of the cerebrum, which controls the masticatory muscles, was assessed according to the expression of cFos, as its expression is related to masticatory stimulation 17 , The M1 activity was higher in the HD—fed mice Fig. These findings indicate that the newly developed HD increased mastication and the mechanical load imposed on the maxillofacial region. Masticatory force is closely related to the shape of the bones in the maxillofacial region, especially the lower jawbone, i. However, it is unclear if it is masticatory force itself that changes mandibular morphology.
Thus, we predicted the morphological change of the mandibular bone under a mechanical loading condition, using a remodeling simulation. We adopted a computer model in which bone formation occurs at a point where the mechanical stress is higher than in the surrounding area 19 , 20 , so that the non-uniformity of the mechanical stress is reduced Fig.
A voxel finite element FE model of the mandibular bone of a mouse was constructed and the muscular force of the masseter muscle was set to tract the masseteric ridge antero—superio—laterally Fig. At the initial state, stress distribution exhibited a non-uniformity, which was reduced after the bone remodeling Fig.
In the mandibular bone after loading, there was a prominent extrusion of the masseteric ridge and a shortening of the mandibular ramus Fig. Computer simulation of the bone remodeling induced by mastication. A remodeling simulation of the voxel finite element FE model of the right mandibular bone see Materials and Methods section for detail.
Deformation of the condyle and molars was fixed tinted blue. Muscular force was applied at the masseteric ridge tinted red , antero—superio—laterally red arrows. Left: coronal—section and right: lateral projection. The dotted circle indicates the extrusion of the masseteric ridge.
The blue and the red lines denote the mandibular height. We then investigated if such morphological changes of the mandibular bone actually occur in vivo using micro-CT images of the mandibular bone. As predicted by the computer simulation Fig. Angular and linear analyses further revealed the extrusion of the masseteric ridge to be related to the thickening of the cortical bone at the site Fig. In addition, the lingual inclination of the molar was larger and the mandibular height was lower in the HD—fed mice than ND—fed mice Fig.
With the parameters obtained Fig. Increased mastication caused morphological change of the jawbone. Bone formation analyses in the increased mastication model.
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Condylion Co , the most posterior point of the condylar head; Menton Me , the most anterior and inferior point of the lower border of the mandibular bone; Gonion Go , the most posterior point of the ramus; Gnathion Gn , the most posterior and inferior point of the ramus; Gonial angle, angle between Co—Go and Gn—Me. The extrusion of the masseteric ridge in the HD—fed mice prompted us to analyze the bone formation and resorption around the ridge, a site where the tendon of the masseter muscle inserts into the mandibular bone. Histological analyses showed that there was an increase in the number of osteocalcin—positive cells, osteoblasts, in the enthesis, while osteoclasts were undetectable Fig.
Although large masticatory force may be harmful on the condyle and result in the shortening of the ramus, there was no erosion on the surface of the condyle of mice fed with HD Fig. No obvious differences in the cartilage and subchondral bone were observed Fig. Thus, increased mastication was revealed to remodel the mandibular bone by enhancing bone formation in the enthesis of the masseter muscle.
Increased mastication results in the bone formation at the enthesis of masseter muscle without affecting the condyle. Area specified by the red square was histologically analyzed.
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Osteocalcin green ; and nuclei blue. The sections were sliced along the blue line and the area specified by the red bar was analyzed. Next, we examined the mechanism by which increased mastication enhances bone formation. Because osteocytes are known to sense mechanical stress imposed on the bone and release cytokines 8 , 9 , we hypothesized that the osteocytes in the masseteric ridge would exhibit this activity.
In search of such cytokines, we found a significantly higher expression of Igf1 in the masseteric ridge of the HD—fed than ND—fed mice Fig.
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There was no significant difference in Igf1 expression in the long bone Supplementary Fig. Immunohistological analysis also showed that the protein level of IGF-1 was higher in the HD—fed mice, especially in the subsurface area of the masseteric ridge but not on the lingual side of the mandibular bone Fig. Interestingly, in the masseter muscle, Igf1r expression was higher in the mice fed with the HD Supplementary Fig.
Osteocytes produce IGF-1 in response to increased mastication. Analyses of how increased mastication enhances bone formation. The regions within the red and blue squares the buccal and lingual cortical bones, respectively were analyzed. IGF-1 red ; and nuclei blue. The dotted lines indicate the bone surface. Based on the findings described above, cells were collected from the tendon and cultured in an osteogenic medium in the presence of IGF Osteoblastogenesis, as indicated by the activity of alkaline phosphatase, was enhanced by IGF-1 Fig.
The expression of osteoblastic genes, including Sp7 , Alpl and Bglap1 encoding Osterix, alkaline phosphatase and osteocalcin, respectively was upregulated by IGF-1 Fig. In order to examine if mechanically—stimulated osteocytes function as a supplier of IGF-1 for tendon cells in the process of bone formation, another in vitro experimental system was established.
An osteocyte cell line, IDG-SW3 cells were cultured in a stretch chamber and underwent cyclic stretching and compression stimulation see Materials and Methods. This mechanical stimulation induced an upregulation of Igf1 expression Fig. Supernatant of these cells was collected and added to the tendon cell culture, either in the presence or absence of an anti—IGF-1 antibody.