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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

Photoperiodic changes in the phase of peripheral tissues persist after release into constant darkness. a Time of peak bioluminescence (± SEM) on the first cycle in vitro displayed by SCN regions and peripheral tissues collected after release into constant darkness from LD12:12 (blue symbols) or LD20:4 (red symbols). n = 3/photoperiod for SCN, n = 6/photoperiod for peripheral tissues. b Summary plots of photoperiod-induced changes in the phase of peripheral tissues after release into constant darkness. Tissues are ordered by the magnitude of the difference in peak time. Dashed vertical lines indicate the magnitude of the shift displayed by the SCN shell and SCN core after release into constant darkness. *Significant phase shift different from 0 h, one sample t-test, P <0.05
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Fig3: Photoperiodic changes in the phase of peripheral tissues persist after release into constant darkness. a Time of peak bioluminescence (± SEM) on the first cycle in vitro displayed by SCN regions and peripheral tissues collected after release into constant darkness from LD12:12 (blue symbols) or LD20:4 (red symbols). n = 3/photoperiod for SCN, n = 6/photoperiod for peripheral tissues. b Summary plots of photoperiod-induced changes in the phase of peripheral tissues after release into constant darkness. Tissues are ordered by the magnitude of the difference in peak time. Dashed vertical lines indicate the magnitude of the shift displayed by the SCN shell and SCN core after release into constant darkness. *Significant phase shift different from 0 h, one sample t-test, P <0.05

Mentions: Because overt behavior and molecular rhythms in some peripheral tissues can be influenced directly by light [26–30], light exposure under LD20:4 may determine the phase of peripheral tissues. To test whether photoperiodic changes were due to light-induced masking, mice were released from LD12:12 or LD20:4 into constant darkness for 1 day before collection of peripheral tissues (adrenal, epididymal white adipose tissue, and spleen). This acute release into constant darkness was designed to eliminate the masking effects of light, but maintain SCN dissociation and prevent the resynchronization of SCN shell and core that occurs with longer exposure to constant darkness [21]. Consistent with this previous work, the SCN shell and core remained dissociated after 1 day in constant darkness (Fig. 3). Further, peripheral tissues continued to exhibit a phase advance similar in magnitude to that displayed by the SCN shell (Fig. 3), which indicates that light is not directly driving photoperiodic changes in the phase of peripheral clocks.Fig. 3


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)

Photoperiodic changes in the phase of peripheral tissues persist after release into constant darkness. a Time of peak bioluminescence (± SEM) on the first cycle in vitro displayed by SCN regions and peripheral tissues collected after release into constant darkness from LD12:12 (blue symbols) or LD20:4 (red symbols). n = 3/photoperiod for SCN, n = 6/photoperiod for peripheral tissues. b Summary plots of photoperiod-induced changes in the phase of peripheral tissues after release into constant darkness. Tissues are ordered by the magnitude of the difference in peak time. Dashed vertical lines indicate the magnitude of the shift displayed by the SCN shell and SCN core after release into constant darkness. *Significant phase shift different from 0 h, one sample t-test, P <0.05
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig3: Photoperiodic changes in the phase of peripheral tissues persist after release into constant darkness. a Time of peak bioluminescence (± SEM) on the first cycle in vitro displayed by SCN regions and peripheral tissues collected after release into constant darkness from LD12:12 (blue symbols) or LD20:4 (red symbols). n = 3/photoperiod for SCN, n = 6/photoperiod for peripheral tissues. b Summary plots of photoperiod-induced changes in the phase of peripheral tissues after release into constant darkness. Tissues are ordered by the magnitude of the difference in peak time. Dashed vertical lines indicate the magnitude of the shift displayed by the SCN shell and SCN core after release into constant darkness. *Significant phase shift different from 0 h, one sample t-test, P <0.05
Mentions: Because overt behavior and molecular rhythms in some peripheral tissues can be influenced directly by light [26–30], light exposure under LD20:4 may determine the phase of peripheral tissues. To test whether photoperiodic changes were due to light-induced masking, mice were released from LD12:12 or LD20:4 into constant darkness for 1 day before collection of peripheral tissues (adrenal, epididymal white adipose tissue, and spleen). This acute release into constant darkness was designed to eliminate the masking effects of light, but maintain SCN dissociation and prevent the resynchronization of SCN shell and core that occurs with longer exposure to constant darkness [21]. Consistent with this previous work, the SCN shell and core remained dissociated after 1 day in constant darkness (Fig. 3). Further, peripheral tissues continued to exhibit a phase advance similar in magnitude to that displayed by the SCN shell (Fig. 3), which indicates that light is not directly driving photoperiodic changes in the phase of peripheral clocks.Fig. 3

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