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CONCISE REVIEW |
Departments of Orthodontics MC 841, Bioengineering, and Anatomy and Cell Biology, 801 South Paulina Street, University of Illinois at Chicago (UIC), Chicago, IL 60612-7211; jmao2{at}uic.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMECHANICAL MODULATION OF SUTURAL...MECHANICAL STIMULI "COMMUNICATE"...SUTURE MECHANOBIOLOGY AND...REFERENCES |
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KEY WORDS: mechanical • osteoblast • bone • fibroblasts • osteogenesis
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMECHANICAL MODULATION OF SUTURAL...MECHANICAL STIMULI "COMMUNICATE"...SUTURE MECHANOBIOLOGY AND...REFERENCES |
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"Suture mechanobiology" is a term coined here to represent the field of determining (1) the nature of mechanical stimuli capable of engineering sutural growth, and (2) the mechanisms of transduction of mechanical signals into biological growth. Suture mechanobiology is an integral component of suture biology, as illustrated in Appendix Fig. 1
(www.dentalresearch.org). One cannot have a complete understanding of the biology of craniofacial sutures without understanding suture mechanobiology, for mechanical stresses undoubtedly play an essential role in the regulation of post-natal sutural growth. Great strides have been made, especially in the past decade, toward our improved understanding of suture mechanobiology. The present review was designed to accomplish three goals related to mechanical modulation of post-natal sutural growth: (1) to synthesize key knowledge on mechanobiology of craniofacial sutures, (2) to explore what constitutes optimal mechanical stimuli for engineering sutural growth, and (3) to probe a rarely discussed linkage between mechanical signal and sutural gene expression. The evolutionary, morphological, molecular, and genetic aspects of suture biology have been the subjects of recent careful reviews (Cohen, 2000; Herring, 2000; Opperman, 2000). Advances in sutural synostosis also have been comprehensively documented (Warren and Longaker, 2001; Wilkie and Morriss-Kay, 2001).
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MECHANICAL MODULATION OF SUTURAL GROWTH: SEARCH FOR OPTIMAL MECHANICAL STIMULI |
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TOPABSTRACTINTRODUCTIONMECHANICAL MODULATION OF SUTURAL...MECHANICAL STIMULI "COMMUNICATE"...SUTURE MECHANOBIOLOGY AND...REFERENCES |
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Several long-term experiments performed in rhesus monkeys about two decades ago investigated the degree to which natural suture growth can be modified by sustained mechanical forces. Frequently, mechanical devices were fabricated based on inspiration from clinical orthopedic appliances. These devices were fixed to the skulls of experimental animals in vivo, and activated by calibrated springs to deliver static forces with isolated magnitudes. In separate studies, tensile or compressive forces were applied in either the anterior or posterior direction, respectively, in reference to the skull (cf. Appendix Fig. 2 in a rabbit model [www.dentalresearch.org]). Several conclusions can be drawn from these studies. The maxilla can be induced to grow anteriorly or posteriorly upon sustained application of anteriorly or posteriorly directed forces, respectively, over several months (for reviews, see Wagemans et al., 1988; Kokich, 1992). Morphological bony changes can be visualized in bone adjacent to sutures. For example, the zygomatic arch is elongated with a slight depression near the zygomaticotemporal suture upon application of tensile (anterior) forces for up to 11 months (Jackson et al., 1979). Sutural growth is up-regulated to the degree that the orientation of the entire maxilla changes in response to either anterior forces (Jackson et al., 1979; Nanda and Hickory, 1984) or posterior forces (Tuenge and Elder, 1974).Sutures undergo anabolic changes such as increased sutural widths, angiogenesis, and bone apposition in response to anteriorly directed forces (Jackson et al., 1979). Conversely, bone resorption takes place in the zygomaticotemporal and zygomaticomaxillary sutures in response to posteriorly directed forces (Tuenge and Elder, 1974).Despite the irreplaceable value of these data, the approach to the induction of bone adaptation by the application of continuous mechanical forces over several months is not time-efficient. Thus, sustained static mechanical forces are not the optimal stimulus for sutural growth.
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(www.dentalresearch.org), were delivered to the rabbit maxilla for up to 20 min/day over 12 days by a computerized servohydraulic system. Tensile and compressive forces were applied anteriorly at 2 N (Mao et al., 2003) and posteriorly at 5 N (Kopher and Mao, 2002) to the maxillary incisors, each with static, sinusoidal, and square waveforms (Figs. 1A, 1B, 1C). Sutural strain was measured with strain gauges and strain rosettes placed over the pre-maxillomaxillary suture (PMS) and nasofrontal suture (NFS) (cf. Appendix Fig. 2 [www.dentalresearch.org]). Indeed, static, sinusoidal, and square-wave exogenous forces (Figs. 1A, 1B, 1C) were expressed as corresponding sutural strain waveforms in not only the PMS adjacent to the exogenous load (Figs. 1D, 1E, 1F from Kopher and Mao, 2002), but also the NFS distant from exogenous load (Figs. 1G, 1H, 1I from Kopher and Mao, 2002). Exogenous compressive forces evoked compressive strain in the PMS, but tensile strain in the NFS (Figs. 1D, 1E, 1F vs. Figs. 1G, 1H, 1I from Kopher and Mao, 2002). Conversely, exogenous tensile forces evoked tensile strain in the PMS, but compressive strain in the NFS (Mao et al., 2003). These contrasting strain polarities likely are due to bending moments induced by either the tensile or compressive force. Sutural strain rate varied as a function of force frequencies from 0.2 Hz to 1 Hz in 0.2-Hz increments in both the PMS and NFS (Mao et al., 2003). Clearly, sutural strain waveforms and strain rates are modulated by waveforms and frequencies of exogenous forces.
Oscillatory mechanical strain, as characterized above, delivered in short doses as few as 1 Hz in 10 min/day over 12 days, engineers anabolic sutural responses (Kopher and Mao, 2002; Mao et al., 2003). We quantified sutural widths by constructing circles and grids over sutural histologic sections using computerized histomorphometric analysis. Significant increases in sutural width were observed upon either sinusoidal tensile strain (Mao et al., 2003) or compressive strain (Fig. 2 from Kopher and Mao, 2002) in either the PMS or NFS, in comparison with static sutural strain and natural suture growth. The numbers of sutural cells, quantified by means of standardized grids and computerized image analysis, were significantly higher in response to sinusoidal tension (Mao et al., 2003) or compression (Kopher and Mao, 2002) than corresponding static stimuli and natural growth. Fluorescence labeling of newly formed sutural bone demonstrates marked sutural osteogenesis stimulated by oscillatory strain in comparison with static strain and natural growth (Fig. 3 from Kopher and Mao, 2002). Taken together, the oscillatory component of sutural strain, rather than its peak amplitude, is anabolic stimuli for sutural growth. In other words, small doses of static strain without variation in amplitude induced by small doses of static forces are not an effective anabolic stimulus for sutural growth. Once oscillatory strain is introduced, strain rate becomes a new variable (absent in static strain), leading to infinite combinations of mechanical stimuli. Thus, our attempts to identify optimal mechanical stimulus for sutural growth are just the beginning.
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from Kopher and Mao, 2002), and vice versa (Mao et al., 2003). There is ample evidence that exogenous compressive forces induce both periosteal and endocortical bone growth in long bones (Rubin and Lanyon, 1984; Turner et al., 1995; Mosley and Lanyon, 1998). Yet, clinical dentistry subscribes to the notion that tension = bone formation, and compression = bone resorption. Orthodontists would readily point out from clinical experience that sustained static compression leads to bone resorption so that the tooth can move into the resorbed space, and at the same time the trailing space vacated by tooth movement is to be filled through bone formation. Accumulating literature in distraction osteogenesis demonstrates net bone formation upon static tensile distraction forces, and net bone resorption upon static compressive forces (contraction osteogenesis) (McCarthy et al., 2001). Ironically, an opposite notion is recognized in clinical medicine: compression = formation, and tension = resorption (Frost, 1964; Burr and Martin, 1992). Orthopedic surgeons would testify that the normal curvature of a fractured and malformed bone is restored by bone resorption on the tensed convex surface, and concomitant bone formation on the compressed concave surface (Frost, 1964; Burr and Martin, 1992). So there remain the questions: Does tension = formation and compression = resorption? and vice versa? Unfortunately, the answers to these clear-cut questions are complicated. The problem probably exists at several levels of mismatch of macro- and micro-mechanics, tissue-borne stresses, different architectural structures, and cellular responses. First, the clinician's notion of tension and compression refers to exogenous forces instead of tissue-borne mechanical microstrain. Exogenous forces are an imprecise determinant of biological growth, for the same force likely induces different growth responses of the rat maxilla and elephant maxilla due to scale. Any force applied to bone propagates as mechanical stresses through bone, measurable as sutural strain (Herring et al., 1996; Hylander and Johnson, 1997; Kopher and Mao, 2002; Mao et al., 2003). Cellular growth in bone likely is a function of certain parameters of mechanical stresses acting on cells via tissue-borne bone strain or its derivatives, such as fluid flow (Duncan and Turner, 1995; Burger and Klein-Nulend, 1999; Weinbaum et al., 2001). Even if microscale tensile strain is successfully distinguished from microscale compression and delivered to a tissue (e.g., suture or periodontal ligament), collagen fibers in a 3D mesh may become taut and thus compress the cells that reside within.
Second, convex and concave surfaces of long bones and cranial bones likely experience tensile and compressive microstrains, respectively, potentially accountable for their separate formation and resorption processes (Frost, 1964; Burr and Martin, 1992). However, Frost's flexural neutralization theory (cf. Frost, 1964) was not designed to account for mechanotransduction mechanisms for craniofacial sutures (and the periodontium). Sutural growth is likely modulated by microscale mechanical stresses that can be induced by either tensile or compressive force (Kopher and Mao, 2002; Mao et al., 2003). Thus, architectural constraints may determine mechanotransduction patterns from exogenous forces to tissue-borne microscale strain, although there are likely common pathways at the cellular and subcellular levels.
Third, although force magnitude or, more precisely, strain amplitude likely plays a role (Frost, 1996), once above an anabolic threshold amplitude, bone growth appears to be determined by strain rate (Turner et al., 1995; Martin et al., 1998; Mosley and Lanyon, 1998). In other words, once above the threshold, further increases in force or strain do not evoke more bone apposition (Rubin and Lanyon, 1987). Contrary to our original assumption that 5 N compressive forces would evoke net sutural bone resorption, sutural growth was accelerated (Kopher and Mao, 2002). It is likely that, given the appropriate parameters such as strain amplitude, rate, and dose, either tension or compression can evoke bone formation or resorption.
Fourth, sustained static tensile or compressive forces, as in orthodontics or following osteotomy in distraction osteogenesis, are likely to affect sutural cells and tissues in different ways from small doses of oscillatory mechanical strain. Both osteogenic and osteoclastic cells can likely be activated by a multitude of mechanical stimuli, including sustained stresses or transient oscillatory strain of, for instance, 600 cycles delivered for 10 min/day for over 12 days (Kopher and Mao, 2002). Mechanical strain can inhibit osteoclastogenesis in vitro (Rubin et al., 1999).
Fifth, given the complexity of the craniofacial skeleton, exogenous compressive and tensile forces likely are expressed as shear stresses in craniofacial sutures. Sixth, osteoblasts and osteoclasts do not work in isolation, in that osteoclast activation requires the presence of several factors released by osteoblasts (Teitelbaum, 2000). At this time, the short answer to the questions of whether tension = formation and compression = resorption, and vice versa, seems to be that these paradigms are an oversimplification of the mechanical modulation of skeletal tissues. One must specify tension or compression at what strain amplitude, rate, and in what dose.
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MECHANICAL STIMULI "COMMUNICATE" WITH SUTURAL CELLS AND GENES: MECHANOTRANSDUCTION |
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TOPABSTRACTINTRODUCTIONMECHANICAL MODULATION OF SUTURAL...MECHANICAL STIMULI "COMMUNICATE"...SUTURE MECHANOBIOLOGY AND...REFERENCES |
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Oscillatory mechanical stimuli up-regulate sutural cell proliferation in vivo. We have observed increased numbers of sutural cells, quantified by computerized cell counting, in both the pre-maxillomaxillary and nasofrontal sutures upon small doses of oscillatory strain (Kopher and Mao, 2002; Mao et al., 2003). This is true for both compressive and tensile microstrains, and in parallel with increased sutural width, indicating coordinated sutural growth rather than a unilateral increase in either cell proliferation or increased matrix synthesis (Kopher and Mao, 2002; Mao et al., 2003). Application of sustained static tensile stresses up-regulates sutural cell proliferation in a popular model of the rat interparietal suture. In explant culture, cell proliferation increases upon tensile strain for 24 hrs (Hickory and Nanda, 1987). Despite the knowledge that has been gained from these studies on sutural cell proliferation in response to different types of mechanical stimuli (tension vs. compression) or oscillatory vs. static strain, and different magnitudes of mechanical stresses, one common shortcoming is that sutural cells are not clearly distinguished between fibroblastic and osteoblastic populations. Historically, mesenchymally derived cells of osteogenic and fibroblastic lineages were given distinct names as osteoblasts and fibroblasts. Each fibrogenic and osteogenic cell lineage likely consists of an array of differentiating cells toward the final cell type of fibroblasts or osteoblasts. Distinguishing these cell populations at various stages of differentiation in response to mechanical stimulation would likely advance our understanding of sutural growth. In addition, sutural strain must be normalized against sutural cross-sectional area to obtain precise stresses experienced by sutural cells.
Increasing numbers of genes and transcription factors have been found to be expressed in sutural growth (Rice et al., 2000; Wilkie and Morriss-Kay, 2001). Several genes that are involved in sutural development have been found to participate in mechanotransduction. FGF-2 is up-regulated upon about 600-mN tensile stresses applied to the rat coronal suture (Yu et al., 2001). Upon mechanically induced rat tooth movement, the osteocalcin gene is up-regulated along with collagen I and alkaline phosphatase genes (Pavlin et al., 2001). A short dose of mechanical stretch applied to cultured calvarial osteoblasts up-regulates an early response gene, Egr-1 mRNA (Dolce et al., 1996). Tensile stresses induce sustained up-regulation of BMP-4 gene expression, followed by increasing expression of Cbfa1/Osf-2, an osteoblast-specific transcription factor (Ikegame et al., 2001).
Up-regulation of genes and transcription factors in sutures is often accompanied by increased protein synthesis. Type III collagen synthesis increases significantly with application of static mechanical stresses to explant sutures (Meikle et al., 1984; Yen et al., 1990; Tanaka et al., 2000). Also, in the interparietal suture model, 600-mN forces have been shown to increase alkaline phosphatase activity (Miyawaki and Forbes, 1987). In Rawlinson et al. (1995), small explants of the rat parietal and ulnar bones were cultured and subjected to different in vitro mechanical stresses. Cellular glucose 6-phosphate dehydrogenase (G6PD) activities in osteoblasts were significantly higher after the ulna explant underwent small doses of mechanical stresses (600 cycles @ 1 Hz) than the control ulnar explant (without loading). In contrast, there was no significant difference in the G6PD activity between the parietal bone explants with or without loading. These data comparing craniofacial and appendicular osteoblasts, despite unequal stimulation paradigms and removal of sutures from the calvarial bone, may motivate other investigators to compare osteogenic responses of different skeletal lineages.
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SUTURE MECHANOBIOLOGY AND CRANIOFACIAL ORTHOPEDICS: THE NEXT DECADE |
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TOPABSTRACTINTRODUCTIONMECHANICAL MODULATION OF SUTURAL...MECHANICAL STIMULI "COMMUNICATE"...SUTURE MECHANOBIOLOGY AND...REFERENCES |
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Upon completion of the human genome project and exponential increases of research output in fields such as mechanobiology, biomedical engineering, functional genomics, and proteomics, the stage is set for upcoming shifts in the paradigms of suture biology and craniofacial orthopedics. There are reasons to believe that the next decade of suture mechanobiology research and orthopedic practice (including orthodontics) may witness exciting new advances as a result of effective utilization of genetic and engineering tools.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Received April 9, 2002; Last revision September 17, 2002; Accepted September 26, 2002
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REFERENCES |
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