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Ontogeny of Circadian Organization in the Rat

Department of Biology, University of Virginia, Charlottesville, VA, USA, Department of Biological Sciences, Vanderbilt University, Box 1634-B, Nashville, TN 37235-1634

Tomoko Yoshikawa

Department of Biology, University of Virginia, Charlottesville, VA, USA, Hokkaido University Graduate School of Medicine, N15 W7, Kita-ku, Sapporo 060-8638, Japan

Elizabeth W. Biscoe

Department of Biology, University of Virginia, Charlottesville, VA, USA, Rappahannock Equine Veterinary Clinic, 7050 Govenor Almond Rd., Locust Grove, VA 22508

Rika Numano

Laboratory of Functional Genomics, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo, Japan, Laboratory for Cell Function Dynamics, Brain Science Institute, RIKEN 2-1 Hirosawa, Wako, Saitama 351-0198, Japan, Life Function and Dynamics, ERATO, JST, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan

Lauren M. Gallaspy

Department of Biology, University of Virginia, Charlottesville, VA, USA, Old Dominion Equine Associates, 6539 Gordonsville Rd., Keswick, VA 22947

Stacy Soulsby

Department of Biology, University of Virginia, Charlottesville, VA, USA, Stoney Creek Animal Hospital, 626 W. Mallard Creek Ch. Rd., Charlotte, NC 28262

Evagelia Papadimas

Department of Biology, University of Virginia, Charlottesville, VA, USA, Laboratory of Genetics, Rockefeller University, 1230 York Avenue, New York, NY 10021

Pinar Pezuk

Department of Biology, University of Virginia, Charlottesville, VA, USA

Susan E. Doyle

Department of Biology, University of Virginia, Charlottesville, VA, USA

Hajime Tei

Laboratory of Functional Genomics, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo, Japan, Research Group of Chronogenomics, Mitsubishi Kagaku Institute of Life Sciences, 11 Minamiooya, Machida, Tokyo 194-8511, Japan

Yoshiyuki Sakaki

Laboratory of Functional Genomics, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo, Japan, Toyohashi University of Technology, 1-1 Tempaku-chou Hibarigaoka, Toyohashi-shi 441-8580, Japan

Gene D. Block

Department of Biology, University of Virginia, Charlottesville, VA, USA, University of California, Los Angeles, 10570 W. Sunset Blvd., Los Angeles, CA 90077

Michael Menaker

Department of Biology, University of Virginia, Charlottesville, VA, USA, mm7e{at}virginia.edu

The mammalian circadian system is orchestrated by a master pacemaker in the brain, but many peripheral tissues also contain independent or quasi-independent circadian oscillators. The adaptive significance of clocks in these structures must lie, in large part, in the phase relationships between the constituent oscillators and their micro- and macroenvironments. To examine the relationship between postnatal development, which is dependent on endogenous programs and maternal/environmental influences, and the phase of circadian oscillators, the authors assessed the circadian phase of pineal, liver, lung, adrenal, and thyroid tissues cultured from Period 1-luciferase (Per1-luc ) rat pups of various postnatal ages. The liver, thyroid, and pineal were rhythmic at birth, but the phases of their Per1-luc expression rhythms shifted remarkably during development. To determine if the timing of the phase shift in each tissue could be the result of changing environmental conditions, the behavior of pups and their mothers was monitored. The circadian phase of the liver shifted from the day to night around postnatal day (P) 22 as the pups nursed less during the light and instead ate solid food during the dark. Furthermore, the phase of Per1-luc expression in liver cultures from nursing neonates could be shifted experimentally from the day to the night by allowing pups access to the dam only during the dark. Peak Per1-luc expression also shifted from midday to early night in thyroid cultures at about P20, concurrent with the shift in eating times. The phase of Per1-luc expression in the pineal gland shifted from day to night coincident with its sympathetic innervation at around P5. Per1-luc expression was rhythmic in adrenal cultures and peaked around the time of lights-off throughout development; however, the amplitude of the rhythm increased at P25. Lung cultures were completely arrhythmic until P12 when the pups began to leave the nest. Taken together, the data suggest that the molecular machinery that generates circadian oscillations matures at different rates in different tissues and that the phase of at least some peripheral organs is malleable and may shift as the organ's function changes during development.

Key Words: development • circadian rhythms • suprachiasmatic nucleus • peripheral clocks • Period1 • luciferase reporter • mammalian

Journal of Biological Rhythms, Vol. 24, No. 1, 55-63 (2009)
DOI: 10.1177/0748730408328438


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