Pushing the limit: masticatory stress and adaptive plasticity in mammalian craniomandibular joints
TL;DR: It is argued that a critical component of current and future research on adaptive plasticity in the skull, and especially cranial joints, should employ a multifaceted characterization of a functional system, one that incorporates data on myriad tissues so as to evaluate the role of altered load versus differential tissue response on the anatomical, cellular and molecular processes that contribute to the strength of such composite structures.
Abstract: Excessive, repetitive and altered loading have been implicated in the initiation of a series of soft- and hard-tissue responses or ;functional adaptations' of masticatory and locomotor elements. Such adaptive plasticity in tissue types appears designed to maintain a sufficient safety factor, and thus the integrity of given element or system, for a predominant loading environment(s). Employing a mammalian species for which considerable in vivo data on masticatory behaviors are available, genetically similar domestic white rabbits were raised on diets of different mechanical properties so as to develop an experimental model of joint function in a normal range of physiological loads. These integrative experiments are used to unravel the dynamic inter-relationships among mechanical loading, tissue adaptive plasticity, norms of reaction and performance in two cranial joint systems: the mandibular symphysis and temporomandibular joint (TMJ). Here, we argue that a critical component of current and future research on adaptive plasticity in the skull, and especially cranial joints, should employ a multifaceted characterization of a functional system, one that incorporates data on myriad tissues so as to evaluate the role of altered load versus differential tissue response on the anatomical, cellular and molecular processes that contribute to the strength of such composite structures. Our study also suggests that the short-term duration of earlier analyses of cranial joint tissues may offer a limited notion of the complex process of developmental plasticity, especially as it relates to the effects of long-term variation in mechanical loads, when a joint is increasingly characterized by adaptive and degradative changes in tissue structure and composition. Indeed, it is likely that a component of the adaptive increases in rabbit TMJ and symphyseal proportions and biomineralization represent a compensatory mechanism to cartilage degradation that serves to maintain the overall functional integrity of each joint system. Therefore, while variation in cranial joint anatomy and performance among sister taxa is, in part, an epiphenomenon of interspecific differences in diet-induced masticatory stresses characterizing the individual ontogenies of the members of a species, this behavioral signal may be increasingly mitigated in over-loaded and perhaps older organisms by the interplay between adaptive and degradative tissue responses.
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1,217 citations
TL;DR: In this article, the authors highlight recent advances in X-ray microcomputed tomography (microCT) as applied to materials, specifically advances made since the first materials microCT review appeared in Internati...
Abstract: This review highlights recent advances in X-ray microcomputed tomography (microCT) as applied to materials, specifically advances made since the first materials microCT review appeared in Internati...
470 citations
TL;DR: Novel findings in biomedicine and developments in imaging and computer technologies are beginning to provide a vision of future innovations in the diagnostics and therapeutics of TMJ disorders, and the identification and use of local or systemic biomarkers to diagnose disease or monitor improvements in therapy.
Abstract: Because their etiologies and pathogenesis are poorly understood, temporomandibular joint (TMJ) diseases are difficult to diagnose and manage. All current approaches to treatments of TMJ diseases are largely palliative. Definitive and rational diagnoses or treatments can only be achieved through a comprehensive understanding of the etiologies, predisposing factors, and pathogenesis of TMJ diseases. While much work remains to be done in this field, novel findings in biomedicine and developments in imaging and computer technologies are beginning to provide us with a vision of future innovations in the diagnostics and therapeutics of TMJ disorders. These advances include the identification and use of local or systemic biomarkers to diagnose disease or monitor improvements in therapy; the use of imaging technologies for earlier and more sensitive diagnostics; and the use of biomedicine, biomimetics, and imaging to design and manufacture bioengineered joints. Such advances are likely to help to customize and enhance the quality of care we provide to patients with TMJ disorders.
218 citations
Journal Article•
TL;DR: The data suggest that myostatin has direct effects on the proliferation and differentiation of osteoprogenitor cells, and that hisostatin antagonists and inhibitors are likely to enhance both muscle mass and bone strength.
Abstract: Myostatin (GDF-8) is a member of the transforming growth factor-beta (TGF-β) superfamily that is highly expressed in skeletal muscle, and myostatin loss-of-function leads to doubling of skeletal muscle mass. Myostatin-deficient mice have been used as a model for studying muscle-bone interactions, and here we review the skeletal phenotype associated with altered myostatin signaling. It is now known that myostatin is a key regulator of mesenchymal stem cell proliferation and differentiation, and mice lacking the myostatin gene show decreased body fat and a generalized increase in bone density and strength. The increase in bone density is observed in most anatomical regions, including the limbs, spine, and jaw, and myostatin inhibitors have been observed to significantly increase bone formation. Myostatin is also expressed in the early phases of fracture healing, and myostatin deficiency leads to increased fracture callus size and strength. Together, these data suggest that myostatin has direct effects on the proliferation and differentiation of osteoprogenitor cells, and that myostatin antagonists and inhibitors are likely to enhance both muscle mass and bone strength.
195 citations
TL;DR: The osteological correlates and inferred soft tissue anatomy of the jaw muscles and relevant neurovasculature in the temporal region of the dinosaur head are presented to provide the anatomical foundation necessary for future analyses of skull function and evolution in an important vertebrate clade.
Abstract: Jaw muscles are key components of the head and critical to testing hypotheses of soft-tissue homology, skull function, and evolution. Dinosaurs evolved an extraordinary diversity of cranial forms adapted to a variety of feeding behaviors. However, disparate evolutionary transformations in head shape and function among dinosaurs and their living relatives, birds and crocodylians, impair straightforward reconstructions of muscles, and other important cephalic soft tissues. This study presents the osteological correlates and inferred soft tissue anatomy of the jaw muscles and relevant neurovasculature in the temporal region of the dinosaur head. Hypotheses of jaw muscle homology were tested across a broad range archosaur and sauropsid taxa to more accurately infer muscle attachments in the adductor chambers of non-avian dinosaurs. Many dinosaurs likely possessed m. levator pterygoideus, a trait shared with lepidosaurs but not extant archosaurs. Several major clades of dinosaurs (e.g., Ornithopoda, Ceratopsidae, Sauropoda) eliminated the epipterygoid, thus impacting interpretations of m. pseudotemporalis profundus. M. pseudotemporalis superficialis most likely attached to the caudoventral surface of the laterosphenoid, a trait shared with extant archosaurs. Although mm. adductor mandibulae externus profundus and medialis likely attached to the caudal half of the dorsotemporal fossa and coronoid process, clear osteological correlates separating the individual bellies are rare. Most dinosaur clades possess osteological correlates indicative of a pterygoideus ventralis muscle that attaches to the lateral surface of the mandible, although the muscle may have extended as far as the jugal in some taxa (e.g., hadrosaurs, tyrannosaurs). The cranial and mandibular attachments of mm adductor mandibulae externus superficialis and adductor mandibulae posterior were consistent across all taxa studied. These new data greatly increase the interpretive resolution of head anatomy in dinosaurs and provide the anatomical foundation necessary for future analyses of skull function and evolution in an important vertebrate clade.
148 citations
Cites background from "Pushing the limit: masticatory stre..."
...Finally, feeding behavior and connective tissue adaptive plasticity are major factors involved in the structure and function of jaw muscles and the skull (Ravosa et al., 2007)....
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References
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TL;DR: As a possible result of ontogenetic canalization, the adult phenotype may be determined as much or more by selection on the locomotor performance of juveniles as by direct selection on those of adults.
Abstract: For most vertebrates, locomotor activity begins at the time of hatching or birth. Although handicapped by small size, rapidly growing tissues, and naivete, juveniles of most species must maneuver in the same environment and avoid the same predators as adults. Thus, it is not surprising that some ectothermic and precocial endothermic tetrapods undergo ontogenetic changes that allow juveniles to sprint almost as fast and jump almost as far as adults. Allometric changes that have been shown or suggested to enhance performance in juveniles include relatively longer limbs, relatively greater muscular forces and contractile velocities, and higher muscular mechanical advantage. Compensation for rapid growth has been shown to occur in the bones of precocial birds and mammals. The limb bones of these animals have relatively greater cross-sectional diameters and areas than those of adults. This maintains a parity of bone and muscular strength during periods of rapid growth, when bones are composed of weaker, more f...
238 citations
"Pushing the limit: masticatory stre..." refers background in this paper
...constraints specific to particular ages (Carrier, 1996)....
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...…Northwestern University Feinberg School of Medicine, Chicago, IL, USA *Author for correspondence (e-mail: ravosam@missouri.edu) Accepted 5 December 2006 THE JOURNAL OF EXPERIMENTAL BIOLOGY 629Adaptive plasticity in two cranial joints constraints specific to particular ages (Carrier, 1996)....
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235 citations
"Pushing the limit: masticatory stre..." refers background in this paper
...…to jaw-adductor, bite and reaction forces are elevated during the processing of relatively tough and/or resistant foods (Herring and Scapino, 1973; Thexton et al., 1980; Weijs et al., 1987; Weijs et al., 1989; Gans et al., 1990; Dessem and Druzinsky, 1992; Hylander et al., 1992; Hylander et al.,…...
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TL;DR: Most of the proteoglycans, extracted from each layer under optimum conditions, could interact with hyaluronic acid to form aggregates, although the extent of aggregation was less in the deeper layers, similar to those observed with increasing age in human articular cartilage.
Abstract: Full-depth plugs of adult human articular cartilage were cut into serial slices from the articular surface and analysed for their glycosaminoglycan content. The amount of chondroitin sulphate was highest in the mid-zone, whereas keratan sulphate increased progressively through the depth. Proteoglycans were isolated from each layer by extraction with 4M-guanidinium chloride followed by centrifugation in 0.4M-guanidinium chloride/CsCl at a starting density of 1.5 g/ml. The efficiency with which proteoglycans were extracted depended on slice thickness, and extraction was complete only when cartilage from each zone was sectioned at 20 microns or less. When thick sections (250 microns) were extracted, hyaluronic acid was retained in the tissue. Most of the proteoglycans, extracted from each layer under optimum conditions, could interact with hyaluronic acid to form aggregates, although the extent of aggregation was less in the deeper layers. Two pools of proteoglycan were identified in all layers by gel chromatography (Kav. 0.33 and 0.58). The smaller of these was rich in keratan sulphate and protein, and gradually increased in proportion through the cartilage depth. Chondroitin sulphate chain size was constant in all regions. The changes in composition and structure observed were consistent with the current model for hyaline-cartilage proteoglycans and were similar to those observed with increasing age in human articular cartilage.
235 citations
"Pushing the limit: masticatory stre..." refers background in this paper
...…et al., 1988; Goldring, 2004a; Goldring, 2004b), with expression of cartilage ECM elements likely reflecting regional variation due to differential loading patterns in distinct joint regions (Bayliss et al., 1983; Nakano and Scott, 1989; Mow et al., 1990; Hamrick, 1999; Tanaka et al., 2000)....
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TL;DR: Findings indicate that the masticatory muscle function influences not only bone remodelling in local areas, due to direct muscle action, but also the general craniofacial growth pattern.
Abstract: The influence of masticatory muscle function on the craniofacial growth pattern in the rat was studied longitudinally by means of a computerised cephalometric method. In order to induce a low functional activity, one group was fed a soft diet, while another group received a standard laboratory diet and served as a control group. The rats were in the late growing state at the start of the experiment (28-days-old) and the experimental period was 28 days. The analysis showed that a more anteriorly directed growth rotation of the viscerocranium occurred in the rats fed the soft diet compared to the rats fed the standard hard diet. Thus, the skull became increasingly more orthocranial in shape in the soft diet group. Although no difference in overall skull size could be found between the two groups an increased viscerocranial height was found in the soft diet group, which is consistent with the altered growth pattern. A decreased growth rate was also found in the gonial angle of the mandible in the soft diet group. These findings indicate that the masticatory muscle function influences not only bone remodelling in local areas, due to direct muscle action, but also the general craniofacial growth pattern.
220 citations
"Pushing the limit: masticatory stre..." refers background in this paper
...Similar patterns characterize condylar and craniofacial dimensions as well as articular cartilage thickness in rats and rabbits raised postnatally on different diets (Beecher and Corruccini, 1981; Bouvier and Hylander, 1984; Kiliardis et al., 1985; Bouvier, 1987; Bouvier, 1988; Bouvier and Zimny, 1987; Block et al., 1988)....
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...…condylar and craniofacial dimensions as well as articular cartilage thickness in rats and rabbits raised postnatally on different diets (Beecher and Corruccini, 1981; Bouvier and Hylander, 1984; Kiliardis et al., 1985; Bouvier, 1987; Bouvier, 1988; Bouvier and Zimny, 1987; Block et al., 1988)....
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TL;DR: Chondrocyte growth factor responsiveness shows qualitative changes during development, and after skeletal maturity, there is a profound decline in the levels of DNA synthesis and cell replication in response to the known chondroCyte growth factors.
Abstract: Objective. To examine growth factor responses of human articular chondrocytes in aging and development. We have previously established a growth factor response profile for adult human articular chondrocytes and shown that transforming growth factor β (TGFβ) is the most potent mitogen among a variety of factors tested.
Methods. Chondrocytes were isolated from human articular cartilage obtained from donors ages 11–83 years and tested in primary culture for proliferative responses to serum and recombinant preparations of the major chondrocyte growth factors. Proliferation was measured by 3H-thymidine incorporation and cell counting. Skeletal maturity of the young donors was determined by radiographic assessment of Risser's index.
Results. Chondrocytes showed a continuous age-related decline in the proliferative response to serum. Analysis of recombinant growth factors showed that with increasing donor age, there was a decrease in the levels of DNA synthesis in response to all factors tested. In chondrocytes from adult donors, there was no change in the relative potencies of the different growth factors. The decrease in the levels of DNA synthesis as measured by 3H-thymidine incorporation corresponded to a reduced rate of in vitro cell replication with increasing donor age. In addition to the quantitative changes in the proliferative responses of chondrocytes with increasing age, there was a qualitative change in the pattern of growth factor responses during development. Cells from young donors (ages 10–20) responded better to platelet-derived growth factor, AA chain homodimer (PDGF-AA) than to TGFβ1, while the inverse pattern was seen in cells from adult donors. This decrease in the response to PDGF-AA was significantly correlated with increasing skeletal maturity.
Conclusion. Chondrocyte growth factor responsiveness shows qualitative changes during development, and after skeletal maturity, there is a profound decline in the levels of DNA synthesis and cell replication in response to the known chondrocyte growth factors.
214 citations
"Pushing the limit: masticatory stre..." refers background in this paper
...Rather, the duration of dietary manipulation in our study greatly exceeds that of previous investigations and it is well known that cartilage exhibits accelerated degradation in response to elevated and/or repetitive loading (Guerne et al., 1994; Guerne et al., 1995; Bae et al., 1998)....
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