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Systematic modeling-driven experiments identify distinct molecular clockworks underlying hierarchically organized

Eui Min Jeong1,2, Miri Kwon3,4, Eunjoo Cho3,4

  • 1Department of Mathematical Sciences, Korea Advanced Institute of Science and Technology, Daejeon 34141, Republic of Korea.

Proceedings of the National Academy of Sciences of the United States of America
|February 23, 2022
PubMed
Summary

Master pacemaker neurons (sLNvs) and slave oscillators (DN1ps) in fruit flies exhibit distinct molecular clockworks. This heterogeneity allows master pacemakers to generate robust yet adaptable circadian rhythms essential for organismal fitness.

Keywords:
CLOCKcircadian rhythmsdorsal neuronlateral neuronmathematical modeling

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Area of Science:

  • Chronobiology
  • Neuroscience
  • Molecular Biology

Background:

  • Circadian rhythms in metazoans rely on a master-slave hierarchy of pacemaker neurons.
  • Both master and slave oscillators are thought to use identical transcription factor feedback loops (CLOCK and PERIOD).
  • Evidence suggests heterogeneity in molecular clockworks underlies pacemaker neuron functional differences.

Purpose of the Study:

  • To identify the source of molecular clockwork heterogeneity in master pacemaker neurons (sLNvs) versus slave oscillators (DN1ps) in Drosophila.
  • To investigate how distinct molecular clockworks contribute to the functional roles of different pacemaker neurons.
  • To develop a systematic approach for analyzing molecular clockwork variations using time-series data.

Main Methods:

  • Development of a systematic, expandable approach to analyze time-series data for molecular clockwork heterogeneity.
  • In vivo experiments in Drosophila.
  • Light shift analysis.

Main Results:

  • Master pacemakers (sLNvs) show higher synthesis and turnover of PERIOD (PER) and lower CLOCK (CLK) levels compared to slave oscillators (DN1ps).
  • This distinct molecular clockwork enables sLNvs to generate strong circadian rhythms that are also flexibly adjustable to environmental changes.
  • Defective CLK-PER binding disrupts rhythms in sLNvs but not DN1ps, highlighting functional molecular differences.

Conclusions:

  • Heterogeneity in molecular clockworks, specifically in PER and CLK dynamics, differentiates master pacemakers from slave oscillators.
  • Distinct molecular clockworks are crucial for the hierarchical organization of circadian systems.
  • This molecular basis ensures the rhythmic fitness of the organism by balancing rhythm robustness and environmental adaptability.