Lactation-Induced Changes in the Volume of Osteocyte Lacunar-Canalicular Space Alter Mechanical Properties in Cortical Bone Tissue

Serra Kaya, Jelena Basta-Pljakic, Zeynep Seref-Ferlengez, Robert J. Majeska, Luis Cardoso, Timothy Bromage, Qihong Zhang, Carol R. Flach, Richard Mendelsohn, Shoshana Yakar, Susannah P. Fritton, Mitchell B. Schaffler

Research output: Contribution to journalArticle

Abstract

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.

Original languageEnglish (US)
JournalJournal of Bone and Mineral Research
DOIs
StateAccepted/In press - 2016

Fingerprint

Osteocytes
Lactation
Bone and Bones
Porosity
Osteolysis
Bone Matrix
Elastic Modulus
Blood Vessels
Physiologic Calcification
Weaning
Electron Scanning Microscopy
Minerals
Cortical Bone

Keywords

  • LACTATION
  • LACUNAR-CANALICULAR SPACE
  • MECHANICAL PROPERTIES
  • OSTEOCYTE
  • OSTEOCYTIC OSTEOLYSIS
  • POROSITY

ASJC Scopus subject areas

  • Endocrinology, Diabetes and Metabolism
  • Orthopedics and Sports Medicine

Cite this

Lactation-Induced Changes in the Volume of Osteocyte Lacunar-Canalicular Space Alter Mechanical Properties in Cortical Bone Tissue. / Kaya, Serra; Basta-Pljakic, Jelena; Seref-Ferlengez, Zeynep; Majeska, Robert J.; Cardoso, Luis; Bromage, Timothy; Zhang, Qihong; Flach, Carol R.; Mendelsohn, Richard; Yakar, Shoshana; Fritton, Susannah P.; Schaffler, Mitchell B.

In: Journal of Bone and Mineral Research, 2016.

Research output: Contribution to journalArticle

Kaya, S, Basta-Pljakic, J, Seref-Ferlengez, Z, Majeska, RJ, Cardoso, L, Bromage, T, Zhang, Q, Flach, CR, Mendelsohn, R, Yakar, S, Fritton, SP & Schaffler, MB 2016, 'Lactation-Induced Changes in the Volume of Osteocyte Lacunar-Canalicular Space Alter Mechanical Properties in Cortical Bone Tissue', Journal of Bone and Mineral Research. https://doi.org/10.1002/jbmr.3044
Kaya, Serra ; Basta-Pljakic, Jelena ; Seref-Ferlengez, Zeynep ; Majeska, Robert J. ; Cardoso, Luis ; Bromage, Timothy ; Zhang, Qihong ; Flach, Carol R. ; Mendelsohn, Richard ; Yakar, Shoshana ; Fritton, Susannah P. ; Schaffler, Mitchell B. / Lactation-Induced Changes in the Volume of Osteocyte Lacunar-Canalicular Space Alter Mechanical Properties in Cortical Bone Tissue. In: Journal of Bone and Mineral Research. 2016.
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abstract = "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.",
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AU - Kaya, Serra

AU - Basta-Pljakic, Jelena

AU - Seref-Ferlengez, Zeynep

AU - Majeska, Robert J.

AU - Cardoso, Luis

AU - Bromage, Timothy

AU - Zhang, Qihong

AU - Flach, Carol R.

AU - Mendelsohn, Richard

AU - Yakar, Shoshana

AU - Fritton, Susannah P.

AU - Schaffler, Mitchell B.

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