Osteogenic capillaries orchestrate growth plate-independent ossification of the malleus

Koichi Matsuo, Yukiko Kuroda, Nobuhito Nango, Kouji Shimoda, Yoshiaki Kubota, Masatsugu Ema, Latifa Bakiri, Erwin F. Wagner, Yoshihiro Takeda, Wataru Yashiro, Atsushi Momose

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Endochondral ossification is a developmental process by which cartilage is replaced by bone. Terminally differentiated hypertrophic chondrocytes are calcified, vascularized, and removed by chondroclasts before bone matrix is laid down by osteoblasts. In mammals, the malleus is one of three auditory ossicles that transmit vibrations of the tympanic membrane to the inner ear. The malleus is formed from a cartilaginous precursor without growth plate involvement, but little is known about how bones of this type undergo endochondral ossification. Here, we demonstrate that in the processus brevis of the malleus, clusters of osteoblasts surrounding the capillary loop produce bone matrix, causing the volume of the capillary lumen to decrease rapidly in post-weaning mice. Synchrotron X-ray tomographic microscopy revealed a concentric, cylindrical arrangement of osteocyte lacunae along capillaries, indicative of pericapillary bone formation. Moreover, we report that overexpression of Fosl1, which encodes a component of the AP-1 transcription factor complex, in osteoblasts significantly blocked malleal capillary narrowing. These data suggest that osteoblast/endothelial cell interactions control growth plate-free endochondral ossification through ‘osteogenic capillaries’ in a Fosl1-regulated manner.

Original languageEnglish
Pages (from-to)3912-3920
Number of pages9
JournalDevelopment (Cambridge)
Volume142
Issue number22
DOIs
Publication statusPublished - 2015 Nov 15

Fingerprint

Malleus
Growth Plate
Osteogenesis
Osteoblasts
Bone Matrix
Ear Ossicles
Bone and Bones
Osteocytes
Tympanic Membrane
Synchrotrons
Transcription Factor AP-1
Inner Ear
Chondrocytes
Vibration
Weaning
Cell Communication
Cartilage
Mammals
Microscopy
Endothelial Cells

Keywords

  • AP-1 transcription factor
  • Auditory ossicle
  • Blood vessel
  • Osteogenic capillary
  • Synchrotron radiation

ASJC Scopus subject areas

  • Developmental Biology
  • Molecular Biology

Cite this

Osteogenic capillaries orchestrate growth plate-independent ossification of the malleus. / Matsuo, Koichi; Kuroda, Yukiko; Nango, Nobuhito; Shimoda, Kouji; Kubota, Yoshiaki; Ema, Masatsugu; Bakiri, Latifa; Wagner, Erwin F.; Takeda, Yoshihiro; Yashiro, Wataru; Momose, Atsushi.

In: Development (Cambridge), Vol. 142, No. 22, 15.11.2015, p. 3912-3920.

Research output: Contribution to journalArticle

Matsuo, Koichi ; Kuroda, Yukiko ; Nango, Nobuhito ; Shimoda, Kouji ; Kubota, Yoshiaki ; Ema, Masatsugu ; Bakiri, Latifa ; Wagner, Erwin F. ; Takeda, Yoshihiro ; Yashiro, Wataru ; Momose, Atsushi. / Osteogenic capillaries orchestrate growth plate-independent ossification of the malleus. In: Development (Cambridge). 2015 ; Vol. 142, No. 22. pp. 3912-3920.
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