Circadian disruption by shifting the light-dark cycle negatively affects bone health in mice

FASEB J. 2020 Jan;34(1):1052-1064. doi: 10.1096/fj.201901929R. Epub 2019 Nov 28.

Abstract

The past decade, it has become evident that circadian rhythms within metabolically active tissues are very important for physical health. However, although shift work has also been associated with an increased risk of fractures, circadian rhythmicity has not yet been extensively studied in bone. Here, we investigated which genes are rhythmically expressed in bone, and whether circadian disruption by shifts in light-dark cycle affects bone turnover and structure in mice. Our results demonstrate diurnal expression patterns of clock genes (Rev-erbα, Bmal1, Per1, Per2, Cry1, Clock), as well as genes involved in osteoclastogenesis, osteoclast proliferation and function (Rankl, Opg, Ctsk), and osteocyte function (c-Fos) in bone. Weekly alternating light-dark cycles disrupted rhythmic clock gene expression in bone and caused a reduction in plasma levels of procollagen type 1 amino-terminal propeptide (P1NP) and tartrate-resistant acidic phosphatase (TRAP), suggestive of a reduced bone turnover. These effects coincided with an altered trabecular bone structure and increased cortical mineralization after 15 weeks of light-dark cycles, which may negatively affect bone strength in the long term. Collectively, these results show that a physiological circadian rhythm is important to maintain bone health, which stresses the importance of further investigating the association between shift work and skeletal disorders.

Keywords: bone mineralization; bone structure; bone turnover; circadian rhythm; clock genes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ARNTL Transcription Factors / metabolism
  • Animals
  • Behavior, Animal
  • Bone Density*
  • Bone and Bones / physiology*
  • CLOCK Proteins / metabolism
  • Cathepsin K / metabolism
  • Circadian Clocks
  • Circadian Rhythm*
  • Cryptochromes / metabolism
  • Female
  • Gene Expression Regulation*
  • Light*
  • Lipids / chemistry
  • Mice
  • Nuclear Receptor Subfamily 1, Group D, Member 1 / metabolism
  • Osteogenesis
  • Osteoprotegerin / metabolism
  • Period Circadian Proteins / metabolism
  • Photoperiod
  • Proto-Oncogene Proteins c-fos / metabolism
  • RANK Ligand / metabolism
  • X-Ray Microtomography

Substances

  • ARNTL Transcription Factors
  • Bmal1 protein, mouse
  • Cry1 protein, mouse
  • Cryptochromes
  • Lipids
  • Nr1d1 protein, mouse
  • Nuclear Receptor Subfamily 1, Group D, Member 1
  • Osteoprotegerin
  • Per1 protein, mouse
  • Per2 protein, mouse
  • Period Circadian Proteins
  • Proto-Oncogene Proteins c-fos
  • RANK Ligand
  • Tnfrsf11b protein, mouse
  • Tnfsf11 protein, mouse
  • CLOCK Proteins
  • Clock protein, mouse
  • Cathepsin K
  • Ctsk protein, mouse