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. 2021 Sep 6;22(17):9623.
doi: 10.3390/ijms22179623.

Role of Brown and Beige Adipose Tissues in Seasonal Adaptation in the Raccoon Dog (Nyctereutes procyonoides)

Laura Niiranen  1 , Kari A Mäkelä  1 , Shivaprakash J Mutt  1 , Riikka Viitanen  2 , Anna Kaisanlahti  3   4 , David Vicente  5 , Tommi Noponen  6   7 , Anu Autio  2 , Anne Roivainen  2   8   9 , Pirjo Nuutila  2   8 , Seppo Saarela  10 , Karl-Heinz Herzig  1   11   12   13
Affiliations

Role of Brown and Beige Adipose Tissues in Seasonal Adaptation in the Raccoon Dog (Nyctereutes procyonoides)

Laura Niiranen et al. Int J Mol Sci. .

Abstract

Brown adipose tissue (BAT) expresses uncoupling protein-1 (UCP1), which enables energy to be exerted towards needed thermogenesis. Beige adipocytes are precursor cells interspersed among white adipose tissue (WAT) that possess similar UCP1 activity and capacity for thermogenesis. The raccoon dog (Nyctereutes procyonoides) is a canid species that utilizes seasonal obesity to survive periods of food shortage in climate zones with cold winters. The potential to recruit a part of the abundant WAT storages as beige adipocytes for UCP1-dependent thermogenesis was investigated in vitro by treating raccoon dog adipocytes with different browning inducing factors. In vivo positron emission tomography/computed tomography (PET/CT) imaging with the glucose analog 18F-FDG showed that BAT was not detected in the adult raccoon dog during the winter season. In addition, UCP1 expression was not changed in response to chronic treatments with browning inducing factors in adipocyte cultures. Our results demonstrated that most likely the raccoon dog endures cold weather without the induction of BAT or recruitment of beige adipocytes for heat production. Its thick fur coat, insulating fat, and muscle shivering seem to provide the adequate heat needed for surviving the winter.

Keywords: UCP1; beige/brite adipocytes; brown adipose tissue; browning; seasonal adaptation; seasonal obesity; thermoregulation; winter sleep/hibernation.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
(a) Representative coronal and sagittal PET/CT images of one of the raccoon dogs. PET image represents an average radioactivity concentration during 120 min imaging. The highest radioactivity concentration is observed in brain, heart, urinary bladder, and lymph nodes in neck and forelimb. (b) Corresponding radioactivity concentration as a function of time from selected tissues.
Figure 2
Figure 2
Representative plasma time-activity curve of the study from one of the raccoon dogs.
Figure 3
Figure 3
Relative expression of UCP1 in raccoon dog adipocytes (n = 4) with 10 µmol/L isoprenaline for different time periods (3 h, 6 h, 12 h, and 24 h). Control adipocytes were treated with PBS. UCP1 expressions are normalized to the expression of beta-2 microglobulin (B2M) and the result values are presented as mean ± SD. Statistically significant difference is indicated by * p < 0.05.
Figure 4
Figure 4
Relative expression of UCP1 in raccoon dog adipocytes treated for 7 days with (a) 1 µmol/L ZD 7114 hydrochloride (ZD 7114), 1 µmol/L noradrenaline, and 1 µmol/L isoprenaline (n = 4). (b) 100 nmol/L ANP, 100 nmol/L BNP, 1 µmol/L lactate, and 100 nmol/L apelin-12 (n = 4). (c) Acute 24 h 100 µmol/L isoprenaline as positive control, 163 µmol/L irisin, and 100 µmol/L fenofibrate (n = 8). Control adipocytes were treated with PBS. UCP1 expressions are normalized to the expression of B2M and the result values are presented as mean ± SD. Statistically significant difference is indicated by *** p ≤ 0.001.
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