The intervertebral disc contains intrinsic circadian clocks that are regulated by age and cytokines and linked to degeneration

Ann Rheum Dis. 2017 Mar;76(3):576-584. doi: 10.1136/annrheumdis-2016-209428. Epub 2016 Aug 3.

Abstract

Objectives: The circadian clocks are internal timing mechanisms that drive ∼24-hour rhythms in a tissue-specific manner. Many aspects of the physiology of the intervertebral disc (IVD) show clear diurnal rhythms. However, it is unknown whether IVD tissue contains functional circadian clocks and if so, how their dysregulation is implicated in IVD degeneration.

Methods: Clock gene dynamics in ex vivo IVD explants (from PER2:: luciferase (LUC) reporter mice) and human disc cells (transduced with lentivirus containing Per2::luc reporters) were monitored in real time by bioluminescence photon counting and imaging. Temporal gene expression changes were studied by RNAseq and quantitative reverse transcription (qRT)-PCR. IVD pathology was evaluated by histology in a mouse model with tissue-specific deletion of the core clock gene Bmal1.

Results: Here we show the existence of the circadian rhythm in mouse IVD tissue and human disc cells. This rhythm is dampened with ageing in mice and can be abolished by treatment with interleukin-1β but not tumour necrosis factor α. Time-series RNAseq revealed 607 genes with 24-hour patterns of expression representing several essential pathways in IVD physiology. Mice with conditional knockout of Bmal1 in their disc cells demonstrated age-related degeneration of IVDs.

Conclusions: We have established autonomous circadian clocks in mouse and human IVD cells which respond to age and cytokines, and control key pathways involved in the homeostasis of IVDs. Genetic disruption to the mouse IVD molecular clock predisposes to IVD degeneration. These results support the concept that disruptions to circadian rhythms may be a risk factor for degenerative IVD disease and low back pain.

Keywords: Arthritis; Chondrocytes; Cytokines; Low Back Pain.

MeSH terms

  • ARNTL Transcription Factors / analysis
  • ARNTL Transcription Factors / genetics*
  • Age Factors
  • Aging / physiology*
  • Animals
  • CLOCK Proteins / analysis
  • Cells, Cultured
  • Circadian Clocks / drug effects
  • Circadian Clocks / genetics
  • Circadian Clocks / physiology*
  • Circadian Rhythm / drug effects
  • Circadian Rhythm / genetics
  • Humans
  • Interleukin-1beta / pharmacology
  • Intervertebral Disc / chemistry
  • Intervertebral Disc / cytology
  • Intervertebral Disc / physiology*
  • Intervertebral Disc Degeneration / genetics
  • Intervertebral Disc Degeneration / physiopathology*
  • Mice
  • Mice, Knockout
  • NF-kappa B / antagonists & inhibitors
  • NF-kappa B / metabolism
  • Nucleus Pulposus / chemistry
  • Nucleus Pulposus / cytology
  • Nucleus Pulposus / physiology
  • Period Circadian Proteins / genetics*
  • Signal Transduction
  • Temperature
  • Tissue Culture Techniques
  • Transcriptome
  • Transfection
  • Tumor Necrosis Factor-alpha / pharmacology

Substances

  • ARNTL Transcription Factors
  • BMAL1 protein, human
  • Bmal1 protein, mouse
  • Interleukin-1beta
  • NF-kappa B
  • PER2 protein, human
  • Per2 protein, mouse
  • Period Circadian Proteins
  • Tumor Necrosis Factor-alpha
  • CLOCK Proteins
  • CLOCK protein, human
  • Clock protein, mouse