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Shell neurons of the master circadian clock coordinate the phase of tissue clocks throughout the brain and body.

Evans JA, Suen TC, Callif BL, Mitchell AS, Castanon-Cervantes O, Baker KM, Kloehn I, Baba K, Teubner BJ, Ehlen JC, Paul KN, Bartness TJ, Tosini G, Leise T, Davidson AJ - BMC Biol. (2015)

Bottom Line: We then analyze resulting changes in the rhythms of clocks located throughout the brain and body to examine whether they maintain phase synchrony with the SCN shell or core.Interestingly, we also found that SCN dissociation diminished the amplitude of rhythms in core clock gene and protein expression in brain tissues by 50-75 %, which suggests that light-driven changes in the functional organization of the SCN markedly influence the strength of rhythms in downstream tissues.Overall, our results reveal that body clocks receive time-of-day cues specifically from the SCN shell, which may be an adaptive design principle that serves to maintain system-level phase relationships in a changing environment.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomedical Sciences, Marquette University, Milwaukee, WI, 53233, USA. jennifer.evans@marquette.edu.

ABSTRACT

Background: Daily rhythms in mammals are programmed by a master clock in the suprachiasmatic nucleus (SCN). The SCN contains two main compartments (shell and core), but the role of each region in system-level coordination remains ill defined. Herein, we use a functional assay to investigate how downstream tissues interpret region-specific outputs by using in vivo exposure to long day photoperiods to temporally dissociate the SCN. We then analyze resulting changes in the rhythms of clocks located throughout the brain and body to examine whether they maintain phase synchrony with the SCN shell or core.

Results: Nearly all of the 17 tissues examined in the brain and body maintain phase synchrony with the SCN shell, but not the SCN core, which indicates that downstream oscillators are set by cues controlled specifically by the SCN shell. Interestingly, we also found that SCN dissociation diminished the amplitude of rhythms in core clock gene and protein expression in brain tissues by 50-75 %, which suggests that light-driven changes in the functional organization of the SCN markedly influence the strength of rhythms in downstream tissues.

Conclusions: Overall, our results reveal that body clocks receive time-of-day cues specifically from the SCN shell, which may be an adaptive design principle that serves to maintain system-level phase relationships in a changing environment. Further, we demonstrate that lighting conditions alter the amplitude of the molecular clock in downstream tissues, which uncovers a new form of plasticity that may contribute to seasonal changes in physiology and behavior.

No MeSH data available.


Related in: MedlinePlus

Representative time series of bioluminescence rhythms measured in vitro from tissues collected from PER2::LUC mice housed under LD12:12 or LD20:4. Time series are de-trended and corrected for the Zeitgeber Time (ZT) of dissection. SCN shell and SCN core regions used for analyses are illustrated at the top of the figure (S and C, respectively). ADR, Adrenal gland; APIT, Anterior pituitary gland; BAT, Brown adipose tissue; EWAT, Epididymal white adipose tissue; IWAT, Inguinal white adipose tissue; KID, Kidney; LNG, Lung; MWAT, Mesenteric white adipose tissue; PIN, Pineal gland; PPIT, Posterior pituitary gland; RWAT, Retroperitoneal white adipose tissue; SPLN, Spleen; THY, Thymus
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Fig1: Representative time series of bioluminescence rhythms measured in vitro from tissues collected from PER2::LUC mice housed under LD12:12 or LD20:4. Time series are de-trended and corrected for the Zeitgeber Time (ZT) of dissection. SCN shell and SCN core regions used for analyses are illustrated at the top of the figure (S and C, respectively). ADR, Adrenal gland; APIT, Anterior pituitary gland; BAT, Brown adipose tissue; EWAT, Epididymal white adipose tissue; IWAT, Inguinal white adipose tissue; KID, Kidney; LNG, Lung; MWAT, Mesenteric white adipose tissue; PIN, Pineal gland; PPIT, Posterior pituitary gland; RWAT, Retroperitoneal white adipose tissue; SPLN, Spleen; THY, Thymus

Mentions: Male PERIOD2::LUCIFERASE (PER2::LUC) mice [24] were housed under a standard lighting condition with 12 h of light (LD12:12) or a long day with 20 h of light (LD20:4), which produced re-entrainment of both locomotor activity and sleep rhythms (Additional file 1: Figure S1). To confirm photoperiodic reorganization of the SCN network, SCN slices were collected for real-time bioluminescence imaging of PER2::LUC rhythms. Consistent with our previous work [21], LD20:4 temporally reorganized the SCN network through region-specific shifts in the phase of PER2::LUC rhythms (Figs. 1 and 2). Relative to LD12:12, in vivo exposure to LD20:4 caused both the SCN shell and core to display an earlier time of peak PER2::LUC expression on the first cycle in vitro. The SCN shell and core, however, displayed differential responses (Fig. 1), with the SCN shell advancing by approximately 3.5 h and the SCN core shifting by approximately 12 h. These results confirm that in vivo exposure to long day lengths dissociates the SCN shell and core, which can be used to assess the functional role of region-specific communication with downstream tissues.Fig. 1


Shell neurons of the master circadian clock coordinate the phase of tissue clocks throughout the brain and body.

Evans JA, Suen TC, Callif BL, Mitchell AS, Castanon-Cervantes O, Baker KM, Kloehn I, Baba K, Teubner BJ, Ehlen JC, Paul KN, Bartness TJ, Tosini G, Leise T, Davidson AJ - BMC Biol. (2015)

Representative time series of bioluminescence rhythms measured in vitro from tissues collected from PER2::LUC mice housed under LD12:12 or LD20:4. Time series are de-trended and corrected for the Zeitgeber Time (ZT) of dissection. SCN shell and SCN core regions used for analyses are illustrated at the top of the figure (S and C, respectively). ADR, Adrenal gland; APIT, Anterior pituitary gland; BAT, Brown adipose tissue; EWAT, Epididymal white adipose tissue; IWAT, Inguinal white adipose tissue; KID, Kidney; LNG, Lung; MWAT, Mesenteric white adipose tissue; PIN, Pineal gland; PPIT, Posterior pituitary gland; RWAT, Retroperitoneal white adipose tissue; SPLN, Spleen; THY, Thymus
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4489020&req=5

Fig1: Representative time series of bioluminescence rhythms measured in vitro from tissues collected from PER2::LUC mice housed under LD12:12 or LD20:4. Time series are de-trended and corrected for the Zeitgeber Time (ZT) of dissection. SCN shell and SCN core regions used for analyses are illustrated at the top of the figure (S and C, respectively). ADR, Adrenal gland; APIT, Anterior pituitary gland; BAT, Brown adipose tissue; EWAT, Epididymal white adipose tissue; IWAT, Inguinal white adipose tissue; KID, Kidney; LNG, Lung; MWAT, Mesenteric white adipose tissue; PIN, Pineal gland; PPIT, Posterior pituitary gland; RWAT, Retroperitoneal white adipose tissue; SPLN, Spleen; THY, Thymus
Mentions: Male PERIOD2::LUCIFERASE (PER2::LUC) mice [24] were housed under a standard lighting condition with 12 h of light (LD12:12) or a long day with 20 h of light (LD20:4), which produced re-entrainment of both locomotor activity and sleep rhythms (Additional file 1: Figure S1). To confirm photoperiodic reorganization of the SCN network, SCN slices were collected for real-time bioluminescence imaging of PER2::LUC rhythms. Consistent with our previous work [21], LD20:4 temporally reorganized the SCN network through region-specific shifts in the phase of PER2::LUC rhythms (Figs. 1 and 2). Relative to LD12:12, in vivo exposure to LD20:4 caused both the SCN shell and core to display an earlier time of peak PER2::LUC expression on the first cycle in vitro. The SCN shell and core, however, displayed differential responses (Fig. 1), with the SCN shell advancing by approximately 3.5 h and the SCN core shifting by approximately 12 h. These results confirm that in vivo exposure to long day lengths dissociates the SCN shell and core, which can be used to assess the functional role of region-specific communication with downstream tissues.Fig. 1

Bottom Line: We then analyze resulting changes in the rhythms of clocks located throughout the brain and body to examine whether they maintain phase synchrony with the SCN shell or core.Interestingly, we also found that SCN dissociation diminished the amplitude of rhythms in core clock gene and protein expression in brain tissues by 50-75 %, which suggests that light-driven changes in the functional organization of the SCN markedly influence the strength of rhythms in downstream tissues.Overall, our results reveal that body clocks receive time-of-day cues specifically from the SCN shell, which may be an adaptive design principle that serves to maintain system-level phase relationships in a changing environment.

View Article: PubMed Central - PubMed

Affiliation: Department of Biomedical Sciences, Marquette University, Milwaukee, WI, 53233, USA. jennifer.evans@marquette.edu.

ABSTRACT

Background: Daily rhythms in mammals are programmed by a master clock in the suprachiasmatic nucleus (SCN). The SCN contains two main compartments (shell and core), but the role of each region in system-level coordination remains ill defined. Herein, we use a functional assay to investigate how downstream tissues interpret region-specific outputs by using in vivo exposure to long day photoperiods to temporally dissociate the SCN. We then analyze resulting changes in the rhythms of clocks located throughout the brain and body to examine whether they maintain phase synchrony with the SCN shell or core.

Results: Nearly all of the 17 tissues examined in the brain and body maintain phase synchrony with the SCN shell, but not the SCN core, which indicates that downstream oscillators are set by cues controlled specifically by the SCN shell. Interestingly, we also found that SCN dissociation diminished the amplitude of rhythms in core clock gene and protein expression in brain tissues by 50-75 %, which suggests that light-driven changes in the functional organization of the SCN markedly influence the strength of rhythms in downstream tissues.

Conclusions: Overall, our results reveal that body clocks receive time-of-day cues specifically from the SCN shell, which may be an adaptive design principle that serves to maintain system-level phase relationships in a changing environment. Further, we demonstrate that lighting conditions alter the amplitude of the molecular clock in downstream tissues, which uncovers a new form of plasticity that may contribute to seasonal changes in physiology and behavior.

No MeSH data available.


Related in: MedlinePlus