Limits...
Strain-guided mineralization in the bone – PDL – cementum complex of a rat periodontium

View Article: PubMed Central - PubMed

ABSTRACT

Objective: The objective of this study was to investigate the effect of mechanical strain by mapping physicochemical properties at periodontal ligament (PDL)–bone and PDL–cementum attachment sites and within the tissues per se.

Design: Accentuated mechanical strain was induced by applying a unidirectional force of 0.06 N for 14 days on molars in a rat model. The associated changes in functional space between the tooth and bone, mineral forming and resorbing events at the PDL–bone and PDL–cementum attachment sites were identified by using micro-X-ray computed tomography (micro-XCT), atomic force microscopy (AFM), dynamic histomorphometry, Raman microspectroscopy, and AFM-based nanoindentation technique. Results from these analytical techniques were correlated with histochemical strains specific to low and high molecular weight GAGs, including biglycan, and osteoclast distribution through tartrate resistant acid phosphatase (TRAP) staining.

Results: Unique chemical and mechanical qualities including heterogeneous bony fingers with hygroscopic Sharpey's fibers contributing to a higher organic (amide III — 1240 cm− 1) to inorganic (phosphate — 960 cm− 1) ratio, with lower average elastic modulus of 8 GPa versus 12 GPa in unadapted regions were identified. Furthermore, an increased presence of elemental Zn in cement lines and mineralizing fronts of PDL–bone was observed. Adapted regions containing bony fingers exhibited woven bone-like architecture and these regions rich in biglycan (BGN) and bone sialoprotein (BSP) also contained high-molecular weight polysaccharides predominantly at the site of polarized bone growth.

Conclusions: From a fundamental science perspective the shift in local properties due to strain amplification at the soft–hard tissue attachment sites is governed by semiautonomous cellular events at the PDL–bone and PDL–cementum sites. Over time, these strain-mediated events can alter the physicochemical properties of tissues per se, and consequently the overall biomechanics of the bone–PDL–tooth complex. From a clinical perspective, the shifts in magnitude and duration of forces on the periodontal ligament can prompt a shift in physiologic mineral apposition in cementum and alveolar bone albeit of an adapted quality owing to the rapid mechanical translation of the tooth.

No MeSH data available.


Related in: MedlinePlus

A model describing potential events at the PDL–bone functional attachment site of the complex is highlighted in this figure. (a) At macroscale, mechanical stimuli such as tensile stress cause straightening and elongation of the collagen fibers PDL. (b) At microscale, collagen fibers are made from collagen fibril bundles while collagen fibrils consist of staggered packed collagen molecules. Tension of collagen fibers exerts stretching of collagen fibrils (thin rods with blue and white bands). The proteoglycans bridging collagen fibrils allow the interfibrillar transmission of load. Sliding of collagen molecules (ribbons of blue triple helix) provides additional displacements and widens the gap zone of a collagen fibril. However, the intermolecular crosslinking bonds prevent the further slippage. The proteoglycans between collagen fibrils and the covalent crosslinks between collagen molecules all contribute to the mechanical behavior of collagen fibers and benefit the structural integrity during the tension. (c) Apparently, cells embedded in the ECM of PDL are subject to tension. ECM transmits the strain resulted from external force on teeth to cytoskeletal components of cells in PDL. Such mechanical stimuli trigger a cascade of intracellular and extracellular processes to modify the ECM such as regulated gene expression, protein synthesis, matrix deposition and mineralization. Meanwhile, the matrix signaling facilitates recruitment of osteoclasts. (d) New bone formation and remodeling takes place at the PDL–bone interface, suggesting an active cell behavior such as differentiation and ECM production. Regulated mineralization of ECM occurs as a result of such strained guided adaption at PDL–bone interface.
© Copyright Policy - CC BY-NC-ND
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4663464&req=5

f0030: A model describing potential events at the PDL–bone functional attachment site of the complex is highlighted in this figure. (a) At macroscale, mechanical stimuli such as tensile stress cause straightening and elongation of the collagen fibers PDL. (b) At microscale, collagen fibers are made from collagen fibril bundles while collagen fibrils consist of staggered packed collagen molecules. Tension of collagen fibers exerts stretching of collagen fibrils (thin rods with blue and white bands). The proteoglycans bridging collagen fibrils allow the interfibrillar transmission of load. Sliding of collagen molecules (ribbons of blue triple helix) provides additional displacements and widens the gap zone of a collagen fibril. However, the intermolecular crosslinking bonds prevent the further slippage. The proteoglycans between collagen fibrils and the covalent crosslinks between collagen molecules all contribute to the mechanical behavior of collagen fibers and benefit the structural integrity during the tension. (c) Apparently, cells embedded in the ECM of PDL are subject to tension. ECM transmits the strain resulted from external force on teeth to cytoskeletal components of cells in PDL. Such mechanical stimuli trigger a cascade of intracellular and extracellular processes to modify the ECM such as regulated gene expression, protein synthesis, matrix deposition and mineralization. Meanwhile, the matrix signaling facilitates recruitment of osteoclasts. (d) New bone formation and remodeling takes place at the PDL–bone interface, suggesting an active cell behavior such as differentiation and ECM production. Regulated mineralization of ECM occurs as a result of such strained guided adaption at PDL–bone interface.

Mentions: Understanding the mechanisms governing strain guided mineralization is not simple. Based on results from this study, it is the assemblage of simultaneous and complementary processes that guide mineralization in the direction of force vector. A hypothetical model depicting the events associated with the strain guided mineralization at the bone–PDL interface is given in Fig. 6. The collagen fibers and/or fibrils at PDL are under tension with shear between the fibers and fibrils upon the application of force on the teeth (Fig. 6a). The proteoglycan bridging neighboring collagen fibrils help distribute load. During tension, the collagen fibrils are straightened and stretched subsequently along with the induction of shear between fibrils and collagen molecules that makeup the fibrils. The neighboring collagen molecules may also glide against each other, widening the gap zone associated with staggered molecular packing of collagen (Fig. 6b) (Scott and Stockwell, 2006). Inside the collagen fibrils, the telopeptides of collagen molecules are typically cross-linked with other neighboring collagen molecules (Puxkandl et al., 2002). These covalent crosslinks between the collagen molecules can hinder further slippage of molecules and also increase the overall stiffness of collagen fibrils. Meanwhile, cells attached to the matrix through small integrin binding ligand N-linked glycoprotein such as BSP are also regulated by the strain in collagen of the PDL. As suggested in Fig. 6c and d, the force acting on the cytoskeletal components of cells triggers a series of downstream processes including gene expression, protein synthesis, ECM deposition and mineralization as well as osteoclast recruitment (Yamauchi and Sricholpech, 2012). As very little is known, a number of theories were extrapolated from similar tissues such as ligaments and tendons, and in vitro studies which provided analogous insights to the observed in vivo events in this study.


Strain-guided mineralization in the bone – PDL – cementum complex of a rat periodontium
A model describing potential events at the PDL–bone functional attachment site of the complex is highlighted in this figure. (a) At macroscale, mechanical stimuli such as tensile stress cause straightening and elongation of the collagen fibers PDL. (b) At microscale, collagen fibers are made from collagen fibril bundles while collagen fibrils consist of staggered packed collagen molecules. Tension of collagen fibers exerts stretching of collagen fibrils (thin rods with blue and white bands). The proteoglycans bridging collagen fibrils allow the interfibrillar transmission of load. Sliding of collagen molecules (ribbons of blue triple helix) provides additional displacements and widens the gap zone of a collagen fibril. However, the intermolecular crosslinking bonds prevent the further slippage. The proteoglycans between collagen fibrils and the covalent crosslinks between collagen molecules all contribute to the mechanical behavior of collagen fibers and benefit the structural integrity during the tension. (c) Apparently, cells embedded in the ECM of PDL are subject to tension. ECM transmits the strain resulted from external force on teeth to cytoskeletal components of cells in PDL. Such mechanical stimuli trigger a cascade of intracellular and extracellular processes to modify the ECM such as regulated gene expression, protein synthesis, matrix deposition and mineralization. Meanwhile, the matrix signaling facilitates recruitment of osteoclasts. (d) New bone formation and remodeling takes place at the PDL–bone interface, suggesting an active cell behavior such as differentiation and ECM production. Regulated mineralization of ECM occurs as a result of such strained guided adaption at PDL–bone interface.
© Copyright Policy - CC BY-NC-ND
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4663464&req=5

f0030: A model describing potential events at the PDL–bone functional attachment site of the complex is highlighted in this figure. (a) At macroscale, mechanical stimuli such as tensile stress cause straightening and elongation of the collagen fibers PDL. (b) At microscale, collagen fibers are made from collagen fibril bundles while collagen fibrils consist of staggered packed collagen molecules. Tension of collagen fibers exerts stretching of collagen fibrils (thin rods with blue and white bands). The proteoglycans bridging collagen fibrils allow the interfibrillar transmission of load. Sliding of collagen molecules (ribbons of blue triple helix) provides additional displacements and widens the gap zone of a collagen fibril. However, the intermolecular crosslinking bonds prevent the further slippage. The proteoglycans between collagen fibrils and the covalent crosslinks between collagen molecules all contribute to the mechanical behavior of collagen fibers and benefit the structural integrity during the tension. (c) Apparently, cells embedded in the ECM of PDL are subject to tension. ECM transmits the strain resulted from external force on teeth to cytoskeletal components of cells in PDL. Such mechanical stimuli trigger a cascade of intracellular and extracellular processes to modify the ECM such as regulated gene expression, protein synthesis, matrix deposition and mineralization. Meanwhile, the matrix signaling facilitates recruitment of osteoclasts. (d) New bone formation and remodeling takes place at the PDL–bone interface, suggesting an active cell behavior such as differentiation and ECM production. Regulated mineralization of ECM occurs as a result of such strained guided adaption at PDL–bone interface.
Mentions: Understanding the mechanisms governing strain guided mineralization is not simple. Based on results from this study, it is the assemblage of simultaneous and complementary processes that guide mineralization in the direction of force vector. A hypothetical model depicting the events associated with the strain guided mineralization at the bone–PDL interface is given in Fig. 6. The collagen fibers and/or fibrils at PDL are under tension with shear between the fibers and fibrils upon the application of force on the teeth (Fig. 6a). The proteoglycan bridging neighboring collagen fibrils help distribute load. During tension, the collagen fibrils are straightened and stretched subsequently along with the induction of shear between fibrils and collagen molecules that makeup the fibrils. The neighboring collagen molecules may also glide against each other, widening the gap zone associated with staggered molecular packing of collagen (Fig. 6b) (Scott and Stockwell, 2006). Inside the collagen fibrils, the telopeptides of collagen molecules are typically cross-linked with other neighboring collagen molecules (Puxkandl et al., 2002). These covalent crosslinks between the collagen molecules can hinder further slippage of molecules and also increase the overall stiffness of collagen fibrils. Meanwhile, cells attached to the matrix through small integrin binding ligand N-linked glycoprotein such as BSP are also regulated by the strain in collagen of the PDL. As suggested in Fig. 6c and d, the force acting on the cytoskeletal components of cells triggers a series of downstream processes including gene expression, protein synthesis, ECM deposition and mineralization as well as osteoclast recruitment (Yamauchi and Sricholpech, 2012). As very little is known, a number of theories were extrapolated from similar tissues such as ligaments and tendons, and in vitro studies which provided analogous insights to the observed in vivo events in this study.

View Article: PubMed Central - PubMed

ABSTRACT

Objective: The objective of this study was to investigate the effect of mechanical strain by mapping physicochemical properties at periodontal ligament (PDL)–bone and PDL–cementum attachment sites and within the tissues per se.

Design: Accentuated mechanical strain was induced by applying a unidirectional force of 0.06 N for 14 days on molars in a rat model. The associated changes in functional space between the tooth and bone, mineral forming and resorbing events at the PDL–bone and PDL–cementum attachment sites were identified by using micro-X-ray computed tomography (micro-XCT), atomic force microscopy (AFM), dynamic histomorphometry, Raman microspectroscopy, and AFM-based nanoindentation technique. Results from these analytical techniques were correlated with histochemical strains specific to low and high molecular weight GAGs, including biglycan, and osteoclast distribution through tartrate resistant acid phosphatase (TRAP) staining.

Results: Unique chemical and mechanical qualities including heterogeneous bony fingers with hygroscopic Sharpey's fibers contributing to a higher organic (amide III — 1240 cm− 1) to inorganic (phosphate — 960 cm− 1) ratio, with lower average elastic modulus of 8 GPa versus 12 GPa in unadapted regions were identified. Furthermore, an increased presence of elemental Zn in cement lines and mineralizing fronts of PDL–bone was observed. Adapted regions containing bony fingers exhibited woven bone-like architecture and these regions rich in biglycan (BGN) and bone sialoprotein (BSP) also contained high-molecular weight polysaccharides predominantly at the site of polarized bone growth.

Conclusions: From a fundamental science perspective the shift in local properties due to strain amplification at the soft–hard tissue attachment sites is governed by semiautonomous cellular events at the PDL–bone and PDL–cementum sites. Over time, these strain-mediated events can alter the physicochemical properties of tissues per se, and consequently the overall biomechanics of the bone–PDL–tooth complex. From a clinical perspective, the shifts in magnitude and duration of forces on the periodontal ligament can prompt a shift in physiologic mineral apposition in cementum and alveolar bone albeit of an adapted quality owing to the rapid mechanical translation of the tooth.

No MeSH data available.


Related in: MedlinePlus