Osteocyte-directed bone demineralization along canaliculi

Nobuhito Nango, Shogo Kubota, Tomoka Hasegawa, Wataru Yashiro, Atsushi Momose, Koichi Matsuo

Research output: Contribution to journalArticle

30 Citations (Scopus)

Abstract

The mammalian skeleton stores calcium and phosphate ions in bone matrix. Osteocytes in osteocyte lacunae extend numerous dendrites into canaliculi less than a micron in diameter and which are distributed throughout bone matrix. Although osteoclasts are the primary bone-resorbing cells, osteocytes also reportedly dissolve hydroxyapatite at peri-lacunar bone matrix. However, robust three-dimensional evidence for peri-canalicular bone mineral dissolution has been lacking. Here we applied a previously reported Talbot-defocus multiscan tomography method for synchrotron X-ray microscopy and analyzed the degree of bone mineralization in mouse cortical bone around the lacuno-canalicular network, which is connected both to blood vessels and the peri- and endosteum. We detected cylindrical low mineral density regions spreading around canaliculi derived from a subset of osteocytes. Transmission electron microscopy revealed both intact and demineralized bone matrix around the canaliculus. Peri-canalicular low mineral density regions were also observed in osteopetrotic mice lacking osteoclasts, indicating that osteoclasts are dispensable for peri-canalicular demineralization. These data suggest demineralization can occur from within bone through the canalicular system, and that peri-canalicular demineralization occurs not uniformly but directed by individual osteocytes. Blockade of peri-canalicular demineralization may be a therapeutic strategy to increase bone mass and quality.

Original languageEnglish
Pages (from-to)279-288
Number of pages10
JournalBone
Volume84
DOIs
Publication statusPublished - 2016 Mar 1

Fingerprint

Osteocytes
Bone Matrix
Bone and Bones
Osteoclasts
Minerals
Physiologic Calcification
Synchrotrons
Durapatite
Dendrites
Transmission Electron Microscopy
Skeleton
Blood Vessels
Microscopy
Tomography
X-Rays
Ions

Keywords

  • Demineralization/remineralization
  • Mineral metabolism
  • Osteocyte canaliculus
  • Osteocytic osteolysis
  • Synchrotron radiation
  • Talbot-defocus multiscan tomography

ASJC Scopus subject areas

  • Physiology
  • Endocrinology, Diabetes and Metabolism
  • Histology

Cite this

Nango, N., Kubota, S., Hasegawa, T., Yashiro, W., Momose, A., & Matsuo, K. (2016). Osteocyte-directed bone demineralization along canaliculi. Bone, 84, 279-288. https://doi.org/10.1016/j.bone.2015.12.006

Osteocyte-directed bone demineralization along canaliculi. / Nango, Nobuhito; Kubota, Shogo; Hasegawa, Tomoka; Yashiro, Wataru; Momose, Atsushi; Matsuo, Koichi.

In: Bone, Vol. 84, 01.03.2016, p. 279-288.

Research output: Contribution to journalArticle

Nango, N, Kubota, S, Hasegawa, T, Yashiro, W, Momose, A & Matsuo, K 2016, 'Osteocyte-directed bone demineralization along canaliculi', Bone, vol. 84, pp. 279-288. https://doi.org/10.1016/j.bone.2015.12.006
Nango N, Kubota S, Hasegawa T, Yashiro W, Momose A, Matsuo K. Osteocyte-directed bone demineralization along canaliculi. Bone. 2016 Mar 1;84:279-288. https://doi.org/10.1016/j.bone.2015.12.006
Nango, Nobuhito ; Kubota, Shogo ; Hasegawa, Tomoka ; Yashiro, Wataru ; Momose, Atsushi ; Matsuo, Koichi. / Osteocyte-directed bone demineralization along canaliculi. In: Bone. 2016 ; Vol. 84. pp. 279-288.
@article{f469df63bb1d4db088dba9bd154d1722,
title = "Osteocyte-directed bone demineralization along canaliculi",
abstract = "The mammalian skeleton stores calcium and phosphate ions in bone matrix. Osteocytes in osteocyte lacunae extend numerous dendrites into canaliculi less than a micron in diameter and which are distributed throughout bone matrix. Although osteoclasts are the primary bone-resorbing cells, osteocytes also reportedly dissolve hydroxyapatite at peri-lacunar bone matrix. However, robust three-dimensional evidence for peri-canalicular bone mineral dissolution has been lacking. Here we applied a previously reported Talbot-defocus multiscan tomography method for synchrotron X-ray microscopy and analyzed the degree of bone mineralization in mouse cortical bone around the lacuno-canalicular network, which is connected both to blood vessels and the peri- and endosteum. We detected cylindrical low mineral density regions spreading around canaliculi derived from a subset of osteocytes. Transmission electron microscopy revealed both intact and demineralized bone matrix around the canaliculus. Peri-canalicular low mineral density regions were also observed in osteopetrotic mice lacking osteoclasts, indicating that osteoclasts are dispensable for peri-canalicular demineralization. These data suggest demineralization can occur from within bone through the canalicular system, and that peri-canalicular demineralization occurs not uniformly but directed by individual osteocytes. Blockade of peri-canalicular demineralization may be a therapeutic strategy to increase bone mass and quality.",
keywords = "Demineralization/remineralization, Mineral metabolism, Osteocyte canaliculus, Osteocytic osteolysis, Synchrotron radiation, Talbot-defocus multiscan tomography",
author = "Nobuhito Nango and Shogo Kubota and Tomoka Hasegawa and Wataru Yashiro and Atsushi Momose and Koichi Matsuo",
year = "2016",
month = "3",
day = "1",
doi = "10.1016/j.bone.2015.12.006",
language = "English",
volume = "84",
pages = "279--288",
journal = "Bone",
issn = "8756-3282",
publisher = "Elsevier Inc.",

}

TY - JOUR

T1 - Osteocyte-directed bone demineralization along canaliculi

AU - Nango, Nobuhito

AU - Kubota, Shogo

AU - Hasegawa, Tomoka

AU - Yashiro, Wataru

AU - Momose, Atsushi

AU - Matsuo, Koichi

PY - 2016/3/1

Y1 - 2016/3/1

N2 - The mammalian skeleton stores calcium and phosphate ions in bone matrix. Osteocytes in osteocyte lacunae extend numerous dendrites into canaliculi less than a micron in diameter and which are distributed throughout bone matrix. Although osteoclasts are the primary bone-resorbing cells, osteocytes also reportedly dissolve hydroxyapatite at peri-lacunar bone matrix. However, robust three-dimensional evidence for peri-canalicular bone mineral dissolution has been lacking. Here we applied a previously reported Talbot-defocus multiscan tomography method for synchrotron X-ray microscopy and analyzed the degree of bone mineralization in mouse cortical bone around the lacuno-canalicular network, which is connected both to blood vessels and the peri- and endosteum. We detected cylindrical low mineral density regions spreading around canaliculi derived from a subset of osteocytes. Transmission electron microscopy revealed both intact and demineralized bone matrix around the canaliculus. Peri-canalicular low mineral density regions were also observed in osteopetrotic mice lacking osteoclasts, indicating that osteoclasts are dispensable for peri-canalicular demineralization. These data suggest demineralization can occur from within bone through the canalicular system, and that peri-canalicular demineralization occurs not uniformly but directed by individual osteocytes. Blockade of peri-canalicular demineralization may be a therapeutic strategy to increase bone mass and quality.

AB - The mammalian skeleton stores calcium and phosphate ions in bone matrix. Osteocytes in osteocyte lacunae extend numerous dendrites into canaliculi less than a micron in diameter and which are distributed throughout bone matrix. Although osteoclasts are the primary bone-resorbing cells, osteocytes also reportedly dissolve hydroxyapatite at peri-lacunar bone matrix. However, robust three-dimensional evidence for peri-canalicular bone mineral dissolution has been lacking. Here we applied a previously reported Talbot-defocus multiscan tomography method for synchrotron X-ray microscopy and analyzed the degree of bone mineralization in mouse cortical bone around the lacuno-canalicular network, which is connected both to blood vessels and the peri- and endosteum. We detected cylindrical low mineral density regions spreading around canaliculi derived from a subset of osteocytes. Transmission electron microscopy revealed both intact and demineralized bone matrix around the canaliculus. Peri-canalicular low mineral density regions were also observed in osteopetrotic mice lacking osteoclasts, indicating that osteoclasts are dispensable for peri-canalicular demineralization. These data suggest demineralization can occur from within bone through the canalicular system, and that peri-canalicular demineralization occurs not uniformly but directed by individual osteocytes. Blockade of peri-canalicular demineralization may be a therapeutic strategy to increase bone mass and quality.

KW - Demineralization/remineralization

KW - Mineral metabolism

KW - Osteocyte canaliculus

KW - Osteocytic osteolysis

KW - Synchrotron radiation

KW - Talbot-defocus multiscan tomography

UR - http://www.scopus.com/inward/record.url?scp=84955474709&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84955474709&partnerID=8YFLogxK

U2 - 10.1016/j.bone.2015.12.006

DO - 10.1016/j.bone.2015.12.006

M3 - Article

C2 - 26709236

AN - SCOPUS:84955474709

VL - 84

SP - 279

EP - 288

JO - Bone

JF - Bone

SN - 8756-3282

ER -