Effects of increased muscle mass on mouse sagittal suture morphology and mechanics

Abstract

The purpose of this study is to test predicted form-function relationships between cranial suture complexity and masticatory muscle mass and biomechanics in a mouse model. Specifically, to test the hypothesis that increased masticatory muscle mass increases sagittal suture complexity, we measured the fractal dimension (FD), temporalis mass, and temporalis bite force in myostatin-deficient (GDF8(-/-)) mice and wild-type CD-1 mice (all male, 6 months old). Myostatin is a negative regulator of muscle mass, and myostatin-deficient mice show a marked increase in muscle mass compared to normal mice. We predicted that increased sagittal suture complexity would decrease suture stiffness. The data presented here demonstrate that increased suture complexity (measured as FD) was observed in a hypermuscular mouse model (GDF8(-/-)) with significantly increased temporalis muscle mass and bite forces. Hypermuscular mice were also found to possess suture connective tissue that was less stiff (i.e., underwent more displacement before failure occurred) when loaded in tension. By decreasing stiffness, suture complexity apparently helps to dissipate mechanical loads within the cranium that are related to chewing. These results suggest that cranial suture connective tissue locally adapts to functional demands of the biomechanical suture environment. As such, cranial sutures provide a novel model for studies in connective tissue mechanotransduction.

The Global Impact of Sutures Assessed in a Finite Element Model of a Macaque Cranium

“…Should sutures be modeled using their complex, often interdigitating morphology, or as a simplified linear corridor? Surface investigation and micro-CT image analysis have demonstrated complicated spatial variations of sutural morphology (Byron et al, 2004;Byron, 2006Byron, , 2009Herring, 2008;Reinholt et al, 2009). Due to its pliant nature, the suture connective tissue is assumed to be able to resist mainly tensile rather than compressive loads.…”

“…It is worth noting that there are significant variations among and within sutures in terms of morphological complexity and internal structural configurations (Byron et al, 2004;Byron, 2006Byron, , 2009Herring, 2008;Reinholt et al, 2009;Jasinoski et al, 2010). This variation may be due to variation in growth potentials (Massler and Schour, 1951;Ozaki et al, 1998;Opperman, 2000;Sun et al, 2004;Carmody et al, 2008;Wang et al, 2007a), dietary adaptations (Byron, 2009), genetic patterning (Wang et al, 2006a), aging processes (Gross, 1961;Milch, 1966;Miroue and Rosenberg, 1975;Kokich, 1976), fusion patterns (Wang et al, 2006c), and ontogenetic changes in material properties along with cortical bones (Wang et al, 2010a).…”

Mechanical Influences on Suture Development and Patency

“…Suture strain resulting from muscle contraction can be tensile, compressive, or both, depending on the particular suture and the particular muscle, and magnitudes are typically an order of magnitude larger than strain on the adjacent bones [21,22], reflecting the fact that sutures are much less stiff than bones. Increased jaw muscle force is associated with increased interdigitation and decreased tensile stiffness of the mouse sagittal suture [47], while a soft diet leads to simpler, narrower, and sometimes obliterated facial sutures in rats [48]. The toothless and therefore nonmasticating osteopetrotic (op/op) mouse shows similar changes in both facial and vault sutures, as well as poorly developed sutural ligaments [49,50].…”

Mechanical force-induced midpalatal suture remodeling in mice

“…In order to obtain insights into interactions among different types of cells as they respond to mechanical stimuli, it is crucial to utilize an in vivo animal model. Craniofacial sutures in rats and mice have been used for such biomechanical studies [5][6][7], but only limited information is available on the cellular and molecular events induced when such sutures are exposed to mechanical stress.…”