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Water–fat MRI in a hibernator reveals seasonal growth of white and brown adipose tissue without cold exposure

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Abstract

Obligate hibernators, such as ground squirrels, display circannual patterns which persist even under constant laboratory conditions, suggesting that they are regulated by endogenous rhythms. Brown adipose tissue (BAT) is important for thermogenesis during periodic arousals from hibernation when core body temperature rises spontaneously from 5 to 37 °C. In most small eutherians BAT growth requires several weeks of cold exposure. We hypothesized that in the thirteen-lined ground squirrel (Ictidomys tridecemlineatus), a hibernator, BAT growth is regulated, in part, by an endogenous rhythm and we predicted that this growth would precede the hibernation season without cold exposure. We tested this prediction using repeated water–fat magnetic resonance imaging over a year, including the hibernation season. Thoracic BAT depots increased in volume from spring through autumn even though animals were housed at ~22 °C. Subsequent cold exposure (5 °C) enlarged the thoracic BAT further. The fat fraction of this tissue fell significantly during the period of peak growth, indicating relative increases in non-triglyceride components, perhaps mitochondria or vasculature. We also found that the proportion of the body consisting of white adipose tissue (WAT) increased steadily from spring through autumn, and fell throughout hibernation, mirroring changes in body mass. Unlike BAT, WAT fat fractions remained constant (near 90%) throughout the year. Future studies will evaluate the significance of photoperiod and cold exposure on the growth of these tissues. We also found tissue with a fat fraction characteristic of BAT in the head near the eyes, a potentially novel discovery that requires further confirmation.

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Acknowledgements

We thank Katherine Mathers, Sarah McFarlane and Natalie Po for help with animal care and project development. This study was supported financially by the Natural Sciences and Engineering Research Council through Discovery Grants (JFS; RGPIN-2014-04860, CAM RGPIN- 2013-356310) and the Canada Research Chairs program (CAM 950-228038).

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Authors and Affiliations

  1. Department of Biology, University of Western Ontario, London, ON, N6A 5B8, Canada

    Amanda MacCannell & James F. Staples

  2. Medical Biophysics, University of Western Ontario, London, ON, N6A 5B8, Canada

    Kevin Sinclair, Lannette Friesen-Waldner & Charles A. McKenzie

Authors
  1. Amanda MacCannell
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  2. Kevin Sinclair
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  3. Lannette Friesen-Waldner
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  4. Charles A. McKenzie
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  5. James F. Staples
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Corresponding author

Correspondence to James F. Staples.

Additional information

Communicated by F. Breukelen.

This manuscript is part of the special issue Hibernation—Guest Editors: Frank van Breukelen and Jenifer C. Utz.

Electronic supplementary material

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360_2017_1075_MOESM1_ESM.tif

Fig. S1 Volume segmentation for total body and specific tissue types. For each image slice the total animal area was outlined manually (in red) using the T1-weighted images (a). Using the T2-weighted images the area of white adipose tissue, with fat fractions greater than 80 (b; highlighted in red) and brown adipose tissue with fat fractions between 25 and 70 (c; outlined in red) were determined for each slice. Using the slice thickness of 0.9mm the volume of each region of interest was calculated and summed for the entire animal (TIF 607 KB)

360_2017_1075_MOESM2_ESM.tif

Fig. S2 Water-fat MRI reveals a tissue within the head (highlighted in red), near the eye, that has a fat fraction resembling BAT. These images were collected from the same animal and suggest that volume of this tissue changes throughout the year (TIF 2614 KB)

360_2017_1075_MOESM3_ESM.tif

Fig. S3 Relative change in the quantity of thoracic brown adipose tissue over a year. For each individual the value at each time point is expressed relative to the first data point collected in June 2015. Data are presented as mean ± SE, n = 3. The green arrow indicates the date ambient temperature started to be reduced 1°C/day from ~22oC and light blue arrow indicate the date at which the temperature reached 5°C, corresponding largely with the first hibernation bouts (TIF 5199 KB)

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MacCannell, A., Sinclair, K., Friesen-Waldner, L. et al. Water–fat MRI in a hibernator reveals seasonal growth of white and brown adipose tissue without cold exposure. J Comp Physiol B 187, 759–767 (2017). https://doi.org/10.1007/s00360-017-1075-8

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