Insulin/IGF-1 Drives PERIOD Synthesis to Entrain Circadian Rhythms with Feeding Time

Priya Crosby; Ryan Hamnett; Marrit Putker; Nathaniel P Hoyle; Martin Reed; Carolyn J Karam; Elizabeth S Maywood; Alessandra Stangherlin; Johanna E Chesham; Edward A Hayter; Lyn Rosenbrier-Ribeiro; Peter Newham; Hans Clevers; David A Bechtold; John S O'Neill

doi:10.1016/j.cell.2019.02.017

Insulin/IGF-1 Drives PERIOD Synthesis to Entrain Circadian Rhythms with Feeding Time

Priya Crosby, Ryan Hamnett, Marrit Putker, Nathaniel P Hoyle, Martin Reed, Carolyn J Karam, Elizabeth S Maywood, Alessandra Stangherlin, Johanna E Chesham, Edward A Hayter, Lyn Rosenbrier-Ribeiro, Peter Newham, Hans Clevers, David A Bechtold, John S O'Neill

Hubrecht Institute

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

210 Citations (Scopus)

Abstract

In mammals, endogenous circadian clocks sense and respond to daily feeding and lighting cues, adjusting internal ∼24 h rhythms to resonate with, and anticipate, external cycles of day and night. The mechanism underlying circadian entrainment to feeding time is critical for understanding why mistimed feeding, as occurs during shift work, disrupts circadian physiology, a state that is associated with increased incidence of chronic diseases such as type 2 (T2) diabetes. We show that feeding-regulated hormones insulin and insulin-like growth factor 1 (IGF-1) reset circadian clocks in vivo and in vitro by induction of PERIOD proteins, and mistimed insulin signaling disrupts circadian organization of mouse behavior and clock gene expression. Insulin and IGF-1 receptor signaling is sufficient to determine essential circadian parameters, principally via increased PERIOD protein synthesis. This requires coincident mechanistic target of rapamycin (mTOR) activation, increased phosphoinositide signaling, and microRNA downregulation. Besides its well-known homeostatic functions, we propose insulin and IGF-1 are primary signals of feeding time to cellular clocks throughout the body.

Original language	English
Pages (from-to)	896-909.e20
Journal	Cell
Volume	177
Issue number	4
DOIs	https://doi.org/10.1016/j.cell.2019.02.017
Publication status	Published - 02 May 2019

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Crosby, P., Hamnett, R., Putker, M., Hoyle, N. P., Reed, M., Karam, C. J., Maywood, E. S., Stangherlin, A., Chesham, J. E., Hayter, E. A., Rosenbrier-Ribeiro, L., Newham, P., Clevers, H., Bechtold, D. A., & O'Neill, J. S. (2019). Insulin/IGF-1 Drives PERIOD Synthesis to Entrain Circadian Rhythms with Feeding Time. Cell, 177(4), 896-909.e20. https://doi.org/10.1016/j.cell.2019.02.017

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title = "Insulin/IGF-1 Drives PERIOD Synthesis to Entrain Circadian Rhythms with Feeding Time",

abstract = "In mammals, endogenous circadian clocks sense and respond to daily feeding and lighting cues, adjusting internal ∼24 h rhythms to resonate with, and anticipate, external cycles of day and night. The mechanism underlying circadian entrainment to feeding time is critical for understanding why mistimed feeding, as occurs during shift work, disrupts circadian physiology, a state that is associated with increased incidence of chronic diseases such as type 2 (T2) diabetes. We show that feeding-regulated hormones insulin and insulin-like growth factor 1 (IGF-1) reset circadian clocks in vivo and in vitro by induction of PERIOD proteins, and mistimed insulin signaling disrupts circadian organization of mouse behavior and clock gene expression. Insulin and IGF-1 receptor signaling is sufficient to determine essential circadian parameters, principally via increased PERIOD protein synthesis. This requires coincident mechanistic target of rapamycin (mTOR) activation, increased phosphoinositide signaling, and microRNA downregulation. Besides its well-known homeostatic functions, we propose insulin and IGF-1 are primary signals of feeding time to cellular clocks throughout the body.",

author = "Priya Crosby and Ryan Hamnett and Marrit Putker and Hoyle, {Nathaniel P} and Martin Reed and Karam, {Carolyn J} and Maywood, {Elizabeth S} and Alessandra Stangherlin and Chesham, {Johanna E} and Hayter, {Edward A} and Lyn Rosenbrier-Ribeiro and Peter Newham and Hans Clevers and Bechtold, {David A} and O'Neill, {John S}",

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doi = "10.1016/j.cell.2019.02.017",

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AU - Crosby, Priya

AU - Hamnett, Ryan

AU - Putker, Marrit

AU - Hoyle, Nathaniel P

AU - Reed, Martin

AU - Karam, Carolyn J

AU - Maywood, Elizabeth S

AU - Stangherlin, Alessandra

AU - Chesham, Johanna E

AU - Hayter, Edward A

AU - Rosenbrier-Ribeiro, Lyn

AU - Newham, Peter

AU - Clevers, Hans

AU - Bechtold, David A

AU - O'Neill, John S

PY - 2019/5/2

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N2 - In mammals, endogenous circadian clocks sense and respond to daily feeding and lighting cues, adjusting internal ∼24 h rhythms to resonate with, and anticipate, external cycles of day and night. The mechanism underlying circadian entrainment to feeding time is critical for understanding why mistimed feeding, as occurs during shift work, disrupts circadian physiology, a state that is associated with increased incidence of chronic diseases such as type 2 (T2) diabetes. We show that feeding-regulated hormones insulin and insulin-like growth factor 1 (IGF-1) reset circadian clocks in vivo and in vitro by induction of PERIOD proteins, and mistimed insulin signaling disrupts circadian organization of mouse behavior and clock gene expression. Insulin and IGF-1 receptor signaling is sufficient to determine essential circadian parameters, principally via increased PERIOD protein synthesis. This requires coincident mechanistic target of rapamycin (mTOR) activation, increased phosphoinositide signaling, and microRNA downregulation. Besides its well-known homeostatic functions, we propose insulin and IGF-1 are primary signals of feeding time to cellular clocks throughout the body.

AB - In mammals, endogenous circadian clocks sense and respond to daily feeding and lighting cues, adjusting internal ∼24 h rhythms to resonate with, and anticipate, external cycles of day and night. The mechanism underlying circadian entrainment to feeding time is critical for understanding why mistimed feeding, as occurs during shift work, disrupts circadian physiology, a state that is associated with increased incidence of chronic diseases such as type 2 (T2) diabetes. We show that feeding-regulated hormones insulin and insulin-like growth factor 1 (IGF-1) reset circadian clocks in vivo and in vitro by induction of PERIOD proteins, and mistimed insulin signaling disrupts circadian organization of mouse behavior and clock gene expression. Insulin and IGF-1 receptor signaling is sufficient to determine essential circadian parameters, principally via increased PERIOD protein synthesis. This requires coincident mechanistic target of rapamycin (mTOR) activation, increased phosphoinositide signaling, and microRNA downregulation. Besides its well-known homeostatic functions, we propose insulin and IGF-1 are primary signals of feeding time to cellular clocks throughout the body.

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DO - 10.1016/j.cell.2019.02.017

M3 - Article

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SN - 0092-8674

VL - 177

SP - 896-909.e20

JO - Cell

JF - Cell

IS - 4

ER -

Insulin/IGF-1 Drives PERIOD Synthesis to Entrain Circadian Rhythms with Feeding Time

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