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Prolonged daily light exposure increases body fat mass through attenuation of brown adipose tissue activity

Sander Kooijman, Rosa van den Berg, Ashna Ramkisoensing, Mariëtte R. Boon, Eline N. Kuipers, Marieke Loef, Tom C. M. Zonneveld, Eliane A. Lucassen, Hetty C. M. Sips, Iliana A. Chatzispyrou, Riekelt H. Houtkooper, Johanna H. Meijer, Claudia P. Coomans, Nienke R. Biermasz, and Patrick C. N. Rensen
PNAS published ahead of print May 11, 2015 https://doi.org/10.1073/pnas.1504239112
Sander Kooijman
aDepartment of Medicine, Division of Endocrinology,bEinthoven Laboratory for Experimental Vascular Medicine, and
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  • For correspondence: s.kooijman@lumc.nl
Rosa van den Berg
aDepartment of Medicine, Division of Endocrinology,bEinthoven Laboratory for Experimental Vascular Medicine, and
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Ashna Ramkisoensing
cDepartment of Molecular Cell Biology, Leiden University Medical Center, Leiden 2333ZA, The Netherlands; and
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Mariëtte R. Boon
aDepartment of Medicine, Division of Endocrinology,bEinthoven Laboratory for Experimental Vascular Medicine, and
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Eline N. Kuipers
aDepartment of Medicine, Division of Endocrinology,bEinthoven Laboratory for Experimental Vascular Medicine, and
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Marieke Loef
aDepartment of Medicine, Division of Endocrinology,bEinthoven Laboratory for Experimental Vascular Medicine, and
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Tom C. M. Zonneveld
aDepartment of Medicine, Division of Endocrinology,bEinthoven Laboratory for Experimental Vascular Medicine, and
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Eliane A. Lucassen
cDepartment of Molecular Cell Biology, Leiden University Medical Center, Leiden 2333ZA, The Netherlands; and
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Hetty C. M. Sips
aDepartment of Medicine, Division of Endocrinology,bEinthoven Laboratory for Experimental Vascular Medicine, and
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Iliana A. Chatzispyrou
dLaboratory of Genetic Metabolic Diseases, Academic Medical Center, Amsterdam 1105AZ, The Netherlands
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Riekelt H. Houtkooper
dLaboratory of Genetic Metabolic Diseases, Academic Medical Center, Amsterdam 1105AZ, The Netherlands
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Johanna H. Meijer
cDepartment of Molecular Cell Biology, Leiden University Medical Center, Leiden 2333ZA, The Netherlands; and
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Claudia P. Coomans
cDepartment of Molecular Cell Biology, Leiden University Medical Center, Leiden 2333ZA, The Netherlands; and
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Nienke R. Biermasz
aDepartment of Medicine, Division of Endocrinology,bEinthoven Laboratory for Experimental Vascular Medicine, and
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Patrick C. N. Rensen
aDepartment of Medicine, Division of Endocrinology,bEinthoven Laboratory for Experimental Vascular Medicine, and
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  1. Edited by Satchidananda Panda, Salk Institute for Biological Studies, San Diego, CA, and accepted by the Editorial Board April 14, 2015 (received for review March 3, 2015)

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Significance

Increased light exposure has been associated with obesity in both humans and mice. In this article, we elucidate a mechanistic basis of this association by performing studies in mice. We report that prolonging daily light exposure increases adiposity by decreasing energy expenditure rather than increasing food intake or locomotor activity. This was caused by a light-exposure period-dependent attenuation of the noradrenergic activation of brown adipose tissue that has recently been shown to contribute substantially to energy expenditure by converting fatty acids and glucose into heat. Therefore, we conclude that impaired brown adipose tissue activity may mediate the relationship between increased light exposure and adiposity.

Abstract

Disruption of circadian rhythmicity is associated with obesity and related disorders, including type 2 diabetes and cardiovascular disease. Specifically, prolonged artificial light exposure associates with obesity in humans, although the underlying mechanism is unclear. Here, we report that increasing the daily hours of light exposure increases body adiposity through attenuation of brown adipose tissue (BAT) activity, a major contributor of energy expenditure. Mice exposed to a prolonged day length of 16- and 24-h light, compared with regular 12-h light, showed increased adiposity without affecting food intake or locomotor activity. Mechanistically, we demonstrated that prolonged day length decreases sympathetic input into BAT and reduces β3-adrenergic intracellular signaling. Concomitantly, prolonging day length decreased the uptake of fatty acids from triglyceride-rich lipoproteins, as well as of glucose from plasma selectively by BAT. We conclude that impaired BAT activity is an important mediator in the association between disturbed circadian rhythm and adiposity, and anticipate that activation of BAT may overcome the adverse metabolic consequences of disturbed circadian rhythmicity.

  • circadian rhythms
  • light pollution
  • obesity
  • brown adipose tissue
  • triglyceride metabolism

Footnotes

  • ↵1S.K. and R.v.d.B. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. Email: s.kooijman{at}lumc.nl.
  • ↵3N.R.B. and P.C.N.R. contributed equally to this work.

  • Author contributions: S.K., R.v.d.B., N.R.B., and P.C.N.R. designed research; S.K., R.v.d.B., A.R., M.R.B., E.N.K., M.L., T.C.M.Z., E.A.L., H.C.M.S., I.A.C., and R.H.H. performed research; S.K., R.v.d.B., A.R., M.R.B., E.N.K., M.L., T.C.M.Z., E.A.L., H.C.M.S., I.A.C., and R.H.H. analyzed data; and S.K., R.v.d.B., J.H.M., C.P.C., N.R.B., and P.C.N.R. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. S.P. is a guest editor invited by the Editorial Board.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1504239112/-/DCSupplemental.

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Daily light regulates brown adipose tissue
Sander Kooijman, Rosa van den Berg, Ashna Ramkisoensing, Mariëtte R. Boon, Eline N. Kuipers, Marieke Loef, Tom C. M. Zonneveld, Eliane A. Lucassen, Hetty C. M. Sips, Iliana A. Chatzispyrou, Riekelt H. Houtkooper, Johanna H. Meijer, Claudia P. Coomans, Nienke R. Biermasz, Patrick C. N. Rensen
Proceedings of the National Academy of Sciences May 2015, 201504239; DOI: 10.1073/pnas.1504239112

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Daily light regulates brown adipose tissue
Sander Kooijman, Rosa van den Berg, Ashna Ramkisoensing, Mariëtte R. Boon, Eline N. Kuipers, Marieke Loef, Tom C. M. Zonneveld, Eliane A. Lucassen, Hetty C. M. Sips, Iliana A. Chatzispyrou, Riekelt H. Houtkooper, Johanna H. Meijer, Claudia P. Coomans, Nienke R. Biermasz, Patrick C. N. Rensen
Proceedings of the National Academy of Sciences May 2015, 201504239; DOI: 10.1073/pnas.1504239112
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