Circadian integration of glutamatergic signals by little SAAS in novel suprachiasmatic circuits

Norman Atkins, Jennifer W. Mitchell, Elena V. Romanova, Daniel Morgan, Tara P. Cominski, Jennifer L. Ecker, John E. Pintar, Jonathan V. Sweedler, Martha U. Gillette

Research output: Contribution to journalArticle

28 Citations (Scopus)

Abstract

Background: Neuropeptides are critical integrative elements within the central circadian clock in the suprachiasmatic nucleus (SCN), where they mediate both cell-to-cell synchronization and phase adjustments that cause light entrainment. Forward peptidomics identified little SAAS, derived from the proSAAS prohormone, among novel SCN peptides, but its role in the SCN is poorly understood. Methodology/Principal Findings: Little SAAS localization and co-expression with established SCN neuropeptides were evaluated by immunohistochemistry using highly specific antisera and stereological analysis. Functional context was assessed relative to c-FOS induction in light-stimulated animals and on neuronal circadian rhythms in glutamate-stimulated brain slices. We found that little SAAS-expressing neurons comprise the third most abundant neuropeptidergic class (16.4%) with unusual functional circuit contexts. Little SAAS is localized within the densely retinorecipient central SCN of both rat and mouse, but not the retinohypothalamic tract (RHT). Some little SAAS colocalizes with vasoactive intestinal polypeptide (VIP) or gastrin-releasing peptide (GRP), known mediators of light signals, but not arginine vasopressin (AVP). Nearly 50% of little SAAS neurons express c-FOS in response to light exposure in early night. Blockade of signals that relay light information, via NMDA receptors or VIP- and GRP-cognate receptors, has no effect on phase delays of circadian rhythms induced by little SAAS. Conclusions/Significance: Little SAAS relays signals downstream of light/glutamatergic signaling from eye to SCN, and independent of VIP and GRP action. These findings suggest that little SAAS forms a third SCN neuropeptidergic system, processing light information and activating phase-shifts within novel circuits of the central circadian clock.

Original languageEnglish (US)
Article numbere12612
Pages (from-to)1-13
Number of pages13
JournalPloS one
Volume5
Issue number9
DOIs
StatePublished - Nov 1 2010

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Suprachiasmatic Nucleus
Gastrin-Releasing Peptide
Light
Networks (circuits)
Vasoactive Intestinal Peptide
vasoactive intestinal peptide
circadian rhythm
gastrin-releasing peptide
Circadian Clocks
Neuropeptides
neuropeptides
Neurons
Circadian Rhythm
Clocks
neurons
Bombesin Receptors
Arginine Vasopressin
arginine vasopressin
N-Methyl-D-Aspartate Receptors
Phase shift

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • General

Cite this

Atkins, N., Mitchell, J. W., Romanova, E. V., Morgan, D., Cominski, T. P., Ecker, J. L., ... Gillette, M. U. (2010). Circadian integration of glutamatergic signals by little SAAS in novel suprachiasmatic circuits. PloS one, 5(9), 1-13. [e12612]. https://doi.org/10.1371/journal.pone.0012612
Atkins, Norman ; Mitchell, Jennifer W. ; Romanova, Elena V. ; Morgan, Daniel ; Cominski, Tara P. ; Ecker, Jennifer L. ; Pintar, John E. ; Sweedler, Jonathan V. ; Gillette, Martha U. / Circadian integration of glutamatergic signals by little SAAS in novel suprachiasmatic circuits. In: PloS one. 2010 ; Vol. 5, No. 9. pp. 1-13.
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abstract = "Background: Neuropeptides are critical integrative elements within the central circadian clock in the suprachiasmatic nucleus (SCN), where they mediate both cell-to-cell synchronization and phase adjustments that cause light entrainment. Forward peptidomics identified little SAAS, derived from the proSAAS prohormone, among novel SCN peptides, but its role in the SCN is poorly understood. Methodology/Principal Findings: Little SAAS localization and co-expression with established SCN neuropeptides were evaluated by immunohistochemistry using highly specific antisera and stereological analysis. Functional context was assessed relative to c-FOS induction in light-stimulated animals and on neuronal circadian rhythms in glutamate-stimulated brain slices. We found that little SAAS-expressing neurons comprise the third most abundant neuropeptidergic class (16.4{\%}) with unusual functional circuit contexts. Little SAAS is localized within the densely retinorecipient central SCN of both rat and mouse, but not the retinohypothalamic tract (RHT). Some little SAAS colocalizes with vasoactive intestinal polypeptide (VIP) or gastrin-releasing peptide (GRP), known mediators of light signals, but not arginine vasopressin (AVP). Nearly 50{\%} of little SAAS neurons express c-FOS in response to light exposure in early night. Blockade of signals that relay light information, via NMDA receptors or VIP- and GRP-cognate receptors, has no effect on phase delays of circadian rhythms induced by little SAAS. Conclusions/Significance: Little SAAS relays signals downstream of light/glutamatergic signaling from eye to SCN, and independent of VIP and GRP action. These findings suggest that little SAAS forms a third SCN neuropeptidergic system, processing light information and activating phase-shifts within novel circuits of the central circadian clock.",
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Atkins, N, Mitchell, JW, Romanova, EV, Morgan, D, Cominski, TP, Ecker, JL, Pintar, JE, Sweedler, JV & Gillette, MU 2010, 'Circadian integration of glutamatergic signals by little SAAS in novel suprachiasmatic circuits', PloS one, vol. 5, no. 9, e12612, pp. 1-13. https://doi.org/10.1371/journal.pone.0012612

Circadian integration of glutamatergic signals by little SAAS in novel suprachiasmatic circuits. / Atkins, Norman; Mitchell, Jennifer W.; Romanova, Elena V.; Morgan, Daniel; Cominski, Tara P.; Ecker, Jennifer L.; Pintar, John E.; Sweedler, Jonathan V.; Gillette, Martha U.

In: PloS one, Vol. 5, No. 9, e12612, 01.11.2010, p. 1-13.

Research output: Contribution to journalArticle

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T1 - Circadian integration of glutamatergic signals by little SAAS in novel suprachiasmatic circuits

AU - Atkins, Norman

AU - Mitchell, Jennifer W.

AU - Romanova, Elena V.

AU - Morgan, Daniel

AU - Cominski, Tara P.

AU - Ecker, Jennifer L.

AU - Pintar, John E.

AU - Sweedler, Jonathan V.

AU - Gillette, Martha U.

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Y1 - 2010/11/1

N2 - Background: Neuropeptides are critical integrative elements within the central circadian clock in the suprachiasmatic nucleus (SCN), where they mediate both cell-to-cell synchronization and phase adjustments that cause light entrainment. Forward peptidomics identified little SAAS, derived from the proSAAS prohormone, among novel SCN peptides, but its role in the SCN is poorly understood. Methodology/Principal Findings: Little SAAS localization and co-expression with established SCN neuropeptides were evaluated by immunohistochemistry using highly specific antisera and stereological analysis. Functional context was assessed relative to c-FOS induction in light-stimulated animals and on neuronal circadian rhythms in glutamate-stimulated brain slices. We found that little SAAS-expressing neurons comprise the third most abundant neuropeptidergic class (16.4%) with unusual functional circuit contexts. Little SAAS is localized within the densely retinorecipient central SCN of both rat and mouse, but not the retinohypothalamic tract (RHT). Some little SAAS colocalizes with vasoactive intestinal polypeptide (VIP) or gastrin-releasing peptide (GRP), known mediators of light signals, but not arginine vasopressin (AVP). Nearly 50% of little SAAS neurons express c-FOS in response to light exposure in early night. Blockade of signals that relay light information, via NMDA receptors or VIP- and GRP-cognate receptors, has no effect on phase delays of circadian rhythms induced by little SAAS. Conclusions/Significance: Little SAAS relays signals downstream of light/glutamatergic signaling from eye to SCN, and independent of VIP and GRP action. These findings suggest that little SAAS forms a third SCN neuropeptidergic system, processing light information and activating phase-shifts within novel circuits of the central circadian clock.

AB - Background: Neuropeptides are critical integrative elements within the central circadian clock in the suprachiasmatic nucleus (SCN), where they mediate both cell-to-cell synchronization and phase adjustments that cause light entrainment. Forward peptidomics identified little SAAS, derived from the proSAAS prohormone, among novel SCN peptides, but its role in the SCN is poorly understood. Methodology/Principal Findings: Little SAAS localization and co-expression with established SCN neuropeptides were evaluated by immunohistochemistry using highly specific antisera and stereological analysis. Functional context was assessed relative to c-FOS induction in light-stimulated animals and on neuronal circadian rhythms in glutamate-stimulated brain slices. We found that little SAAS-expressing neurons comprise the third most abundant neuropeptidergic class (16.4%) with unusual functional circuit contexts. Little SAAS is localized within the densely retinorecipient central SCN of both rat and mouse, but not the retinohypothalamic tract (RHT). Some little SAAS colocalizes with vasoactive intestinal polypeptide (VIP) or gastrin-releasing peptide (GRP), known mediators of light signals, but not arginine vasopressin (AVP). Nearly 50% of little SAAS neurons express c-FOS in response to light exposure in early night. Blockade of signals that relay light information, via NMDA receptors or VIP- and GRP-cognate receptors, has no effect on phase delays of circadian rhythms induced by little SAAS. Conclusions/Significance: Little SAAS relays signals downstream of light/glutamatergic signaling from eye to SCN, and independent of VIP and GRP action. These findings suggest that little SAAS forms a third SCN neuropeptidergic system, processing light information and activating phase-shifts within novel circuits of the central circadian clock.

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