Genetically Blocking the Zebrafish Pineal Clock Affects Circadian Behavior

PLoS Genet. 2016 Nov 21;12(11):e1006445. doi: 10.1371/journal.pgen.1006445. eCollection 2016 Nov.

Abstract

The master circadian clock in fish has been considered to reside in the pineal gland. This dogma is challenged, however, by the finding that most zebrafish tissues contain molecular clocks that are directly reset by light. To further examine the role of the pineal gland oscillator in the zebrafish circadian system, we generated a transgenic line in which the molecular clock is selectively blocked in the melatonin-producing cells of the pineal gland by a dominant-negative strategy. As a result, clock-controlled rhythms of melatonin production in the adult pineal gland were disrupted. Moreover, transcriptome analysis revealed that the circadian expression pattern of the majority of clock-controlled genes in the adult pineal gland is abolished. Importantly, circadian rhythms of behavior in zebrafish larvae were affected: rhythms of place preference under constant darkness were eliminated, and rhythms of locomotor activity under constant dark and constant dim light conditions were markedly attenuated. On the other hand, global peripheral molecular oscillators, as measured in whole larvae, were unaffected in this model. In conclusion, characterization of this novel transgenic model provides evidence that the molecular clock in the melatonin-producing cells of the pineal gland plays a key role, possibly as part of a multiple pacemaker system, in modulating circadian rhythms of behavior.

MeSH terms

  • Animals
  • Circadian Clocks / genetics*
  • Circadian Rhythm / genetics*
  • Circadian Rhythm / physiology
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Darkness
  • Gene Expression Regulation, Developmental
  • Larva / genetics
  • Larva / growth & development
  • Light
  • Locomotion / genetics*
  • Locomotion / physiology
  • Melatonin / biosynthesis*
  • Melatonin / genetics
  • Pineal Gland / growth & development
  • Pineal Gland / metabolism
  • Transcriptome / genetics
  • Zebrafish / genetics
  • Zebrafish / growth & development
  • Zebrafish Proteins

Substances

  • DNA-Binding Proteins
  • Zebrafish Proteins
  • clocka protein, zebrafish
  • Melatonin

Grants and funding

The United States–Israel Binational Science Foundation (grant number 2013/433 to YG and HAB), Jerusalem, Israel; The Israel Science Foundation (grants number 1084/12 and 443/16 to YG), Jerusalem, Israel. The BioInterfaces in Technology and Medicine funding programme of the Helmholtz Association, Germany (to NSF). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.