TY - JOUR
T1 - Lactation-Induced Changes in the Volume of Osteocyte Lacunar-Canalicular Space Alter Mechanical Properties in Cortical Bone Tissue
AU - Kaya, Serra
AU - Basta-Pljakic, Jelena
AU - Seref-Ferlengez, Zeynep
AU - Majeska, Robert J.
AU - Cardoso, Luis
AU - Bromage, Timothy G.
AU - Zhang, Qihong
AU - Flach, Carol R.
AU - Mendelsohn, Richard
AU - Yakar, Shoshana
AU - Fritton, Susannah P.
AU - Schaffler, Mitchell B.
N1 - Funding Information:
This work was supported by grants AR041210 and AR057139 (to MBS) from the National Institute of Arthritis and Musculoskeletal and Skin Diseases, DK100246 (to SY) from the National Institute of Diabetes and Digestive and Kidney Diseases, SC1 DK103362 (to LC) from the National Institutes of Health; and 1333560 (to LC) from National Science Foundation. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. SK received partial support from a doctoral fellowship from the Grove School of Engineering at the City College of New York. The Raman microscope was purchased through the State of New Jersey “ELF III Project 047-04 Polymer and Nanomaterials Characterization Facility“ grant to the Rutgers-Newark Chemistry Department. We thank Prof. Jackie Li of CCNY Mechanical Engineering Department for use of microindenter, Damien Laudier for assistance with tissue preparation, Jessica Thomas for assistance with SIM analysis, Dr. Paolo E. Palacio-Mancheno for guidance with BSEM assessment. Authors’ roles: SK and MBS and generated the hypothesis, conducted the experiments, data collection, analyses and writing, and are responsible for the integrity of the data. SY provided the mice used in these studies and intellectual input. ZS-F assisted with microindentation studies. JB-P and TB assisted with imaging and BSEM studies. RM, CRK, and QZ assisted with Raman microspectroscopy studies. LC, SPF, and RJM contributed intellectual input and writing.
Publisher Copyright:
© 2016 American Society for Bone and Mineral Research
PY - 2017/4
Y1 - 2017/4
N2 - Osteocytes can remove and remodel small amounts of their surrounding bone matrix through osteocytic osteolysis, which results in increased volume occupied by lacunar and canalicular space (LCS). It is well established that cortical bone stiffness and strength are strongly and inversely correlated with vascular porosity, but whether changes in LCS volume caused by osteocytic osteolysis are large enough to affect bone mechanical properties is not known. In the current studies we tested the hypotheses that (1) lactation and postlactation recovery in mice alter the elastic modulus of bone tissue, and (2) such local changes in mechanical properties are related predominantly to alterations in lacunar and canalicular volume rather than bone matrix composition. Mechanical testing was performed using microindentation to measure modulus in regions containing solely osteocytes and no vascular porosity. Lactation caused a significant (∼13%) reduction in bone tissue-level elastic modulus (p < 0.001). After 1 week postweaning (recovery), bone modulus levels returned to control levels and did not change further after 4 weeks of recovery. LCS porosity tracked inversely with changes in cortical bone modulus. Lacunar and canalicular void space increased 7% and 15% with lactation, respectively (p < 0.05), then returned to control levels at 1 week after weaning. Neither bone mineralization (assessed by high-resolution backscattered scanning electron microscopy) nor mineral/matrix ratio or crystallinity (assessed by Raman microspectroscopy) changed with lactation. Thus, changes in bone mechanical properties induced by lactation and recovery appear to depend predominantly on changes in osteocyte LCS dimensions. Moreover, this study demonstrates that tissue-level cortical bone mechanical properties are rapidly and reversibly modulated by osteocytes in response to physiological challenge. These data point to a hitherto unappreciated role for osteocytes in modulating and maintaining local bone mechanical properties.
AB - Osteocytes can remove and remodel small amounts of their surrounding bone matrix through osteocytic osteolysis, which results in increased volume occupied by lacunar and canalicular space (LCS). It is well established that cortical bone stiffness and strength are strongly and inversely correlated with vascular porosity, but whether changes in LCS volume caused by osteocytic osteolysis are large enough to affect bone mechanical properties is not known. In the current studies we tested the hypotheses that (1) lactation and postlactation recovery in mice alter the elastic modulus of bone tissue, and (2) such local changes in mechanical properties are related predominantly to alterations in lacunar and canalicular volume rather than bone matrix composition. Mechanical testing was performed using microindentation to measure modulus in regions containing solely osteocytes and no vascular porosity. Lactation caused a significant (∼13%) reduction in bone tissue-level elastic modulus (p < 0.001). After 1 week postweaning (recovery), bone modulus levels returned to control levels and did not change further after 4 weeks of recovery. LCS porosity tracked inversely with changes in cortical bone modulus. Lacunar and canalicular void space increased 7% and 15% with lactation, respectively (p < 0.05), then returned to control levels at 1 week after weaning. Neither bone mineralization (assessed by high-resolution backscattered scanning electron microscopy) nor mineral/matrix ratio or crystallinity (assessed by Raman microspectroscopy) changed with lactation. Thus, changes in bone mechanical properties induced by lactation and recovery appear to depend predominantly on changes in osteocyte LCS dimensions. Moreover, this study demonstrates that tissue-level cortical bone mechanical properties are rapidly and reversibly modulated by osteocytes in response to physiological challenge. These data point to a hitherto unappreciated role for osteocytes in modulating and maintaining local bone mechanical properties.
KW - LACTATION
KW - LACUNAR-CANALICULAR SPACE
KW - MECHANICAL PROPERTIES
KW - OSTEOCYTE
KW - OSTEOCYTIC OSTEOLYSIS
KW - POROSITY
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U2 - 10.1002/jbmr.3044
DO - 10.1002/jbmr.3044
M3 - Article
C2 - 27859586
AN - SCOPUS:85006705653
SN - 0884-0431
VL - 32
SP - 688
EP - 697
JO - Journal of Bone and Mineral Research
JF - Journal of Bone and Mineral Research
IS - 4
ER -