Strain-guided mineralization in the bone–PDL–cementum complex of a rat periodontium
Kathryn Grandfield,
Ralf-Peter Herber,
Ling Chen,
Sabra Djomehri,
Caleb Tam,
Ji-Hyun Lee,
Evan Brown,
Wood R. Woolwine III,
Don Curtis,
Mark Ryder,
Jim Schuck,
Samuel Webb,
William Landis,
Sunita P. Ho
Affiliations
Kathryn Grandfield
Division of Biomaterials and Bioengineering, Department of Preventive and Restorative Dental Sciences, University of California San Francisco, San Francisco, CA 94143, United States
Ralf-Peter Herber
Division of Orthodontics, Department of Orofacial Sciences, University of California San Francisco, San Francisco, CA 94143, United States
Ling Chen
Division of Biomaterials and Bioengineering, Department of Preventive and Restorative Dental Sciences, University of California San Francisco, San Francisco, CA 94143, United States
Sabra Djomehri
Division of Biomaterials and Bioengineering, Department of Preventive and Restorative Dental Sciences, University of California San Francisco, San Francisco, CA 94143, United States
Caleb Tam
Division of Biomaterials and Bioengineering, Department of Preventive and Restorative Dental Sciences, University of California San Francisco, San Francisco, CA 94143, United States
Ji-Hyun Lee
Division of Biomaterials and Bioengineering, Department of Preventive and Restorative Dental Sciences, University of California San Francisco, San Francisco, CA 94143, United States
Evan Brown
Division of Biomaterials and Bioengineering, Department of Preventive and Restorative Dental Sciences, University of California San Francisco, San Francisco, CA 94143, United States
Wood R. Woolwine III
Division of Biomaterials and Bioengineering, Department of Preventive and Restorative Dental Sciences, University of California San Francisco, San Francisco, CA 94143, United States
Don Curtis
Division of Biomaterials and Bioengineering, Department of Preventive and Restorative Dental Sciences, University of California San Francisco, San Francisco, CA 94143, United States
Mark Ryder
Division of Periodontics, Department of Orofacial Sciences, University of California San Francisco, San Francisco, CA 94143, United States
Jim Schuck
Materials Science Division, The Molecular Foundry, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, United States
Samuel Webb
Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, Menlo Park, CA 94025, United States
William Landis
Department of Polymer Science, The University of Akron, OH 44325, United States
Sunita P. Ho
Division of Biomaterials and Bioengineering, Department of Preventive and Restorative Dental Sciences, University of California San Francisco, San Francisco, CA 94143, United States
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.