Omega 3 fatty acids stimulate thermogenesis during torpor in the Arctic Ground Squirrel

Abstract

Omega 3 polyunsaturated fatty acids (PUFAs) influence metabolism and thermogenesis in non-hibernators. How omega 3 PUFAs influence Arctic Ground Squirrels (AGS) during hibernation is unknown. Prior to hibernation we fed AGS chow composed of an omega 6:3 ratio approximately 1:1 (high in omega 3 PUFA, termed Balanced Diet), or an omega 6:3 ratio of 5:1 (Standard Rodent Chow), and measured the influence of diet on core body temperature (Tb), brown adipose tissue (BAT) mass, fatty acid profiles of BAT, white adipose tissue (WAT) and plasma as well as hypothalamic endocannabinoid and endocannabinoid-like bioactive fatty acid amides during hibernation. Results show feeding a diet high in omega 3 PUFAs, with a more balanced omega 6:3 ratio, increases AGS Tb in torpor. We found the diet-induced increase in Tb during torpor is most easily explained by an increase in the mass of BAT deposits of Balanced Diet AGS. The increase in BAT mass is associated with elevated levels of metabolites DHA and EPA in tissue and plasma suggesting that these omega 3 PUFAs may play a role in thermogenesis during torpor. While we did not observe diet-induced change in endocannabinoids, we do report altered hypothalamic levels of some endocannabinoids, and endocannabinoid-like compounds, during hibernation.

Translating PUFA omega 6:3 ratios from wild to captive hibernators (Urocitellus parryii) enhances sex-dependent mass-gain without increasing physiological stress indicators

“…Different superscripts (a or b) signify that groups are different ( p < 0.001). Data incorporates previously published data on Fall Balanced Diet ( n = 9) and Fall Standard Rodent Chow AGS ( n = 9) (Rice et al 2021 ). Summer sampling occurred in very early July and fall sampling occurred in August, autumn time in the Arctic.…”

“…Captive AGS were housed individually in 12″ × 19″ × 12″ stainless steel wire mesh with cotton bedding hanging cages over ammonia absorbing corn cob litter at ambient temperature ( T a , 16–18 °C) and 16L:8D hour light/dark cycle until August 15, when they were moved to cold chambers with T a of 2 °C at a 4L:20D hour light/dark cycle. Starting two weeks after capture and quarantine, mid-July animals were offered 47 g daily of either Standard Rodent Chow (#5663, Mazuri, PMI Nutrition International, Richmond, IN) or Balanced Diet (9GU5, formulated with Lab Diet, St. Louis, MO) and were provided water ad litbitum during the euthermic period as previously described (Rice et al 2021 ). For animals kept through the hibernation season (year 3): once animals exhibited hibernation behavior, defined as the respiratory rate below 5 breaths per minute, inactivity and curled posture, food was withdrawn and animals were placed in polycarbonate cages (8.5″ × 17″ × 8.5″) with shavings, cotton bedding and gel hydration packets.…”

“…A full list of ingredients is listed in Supplemental Table 2. We also provide a fatty acid composition of the diets determined by GC in the result section (Table 1 d) as previously described (Rice et al 2021 ).…”

“…Omega 3 PUFAs have been less studied in hibernation (Frank et al 2004 ; Rice et al 2021 ) with some results showing a potential negative influence on hibernation (Giroud et al 2018 ; Hill and Florant 2000 ; Logan et al 2020 ). Overall, two major perspectives exist for the relationship between omega 6 and omega 3 PUFAs and their influence on hibernation: (1) the ratio between omega 6 and omega 3 PUFAs may influence the molecular function of cardiac phospholipid membrane proteins such as the sacro-endoplasmic reticulum Ca 2+ -ATPase (SERCA) and therefore potentially impact hibernation behavior (Arnold et al 2015 ; Giroud et al 2013 , 2018 ; Munro and Thomas 2004 ); and (2) there is no physiological difference between feeding omega 3 and omega 6 PUFAs on torpor (Frank et al 2004 , 2008 ).…”

“…Overall, two major perspectives exist for the relationship between omega 6 and omega 3 PUFAs and their influence on hibernation: (1) the ratio between omega 6 and omega 3 PUFAs may influence the molecular function of cardiac phospholipid membrane proteins such as the sacro-endoplasmic reticulum Ca 2+ -ATPase (SERCA) and therefore potentially impact hibernation behavior (Arnold et al 2015 ; Giroud et al 2013 , 2018 ; Munro and Thomas 2004 ); and (2) there is no physiological difference between feeding omega 3 and omega 6 PUFAs on torpor (Frank et al 2004 , 2008 ). Our lab recently found higher levels of dietary omega 3 PUFAs with more balanced omega 6:3 ratios resulted in no ill effect on torpor bout length or time in hibernation in Arctic Ground Squirrels (AGS) but did increase brown adipose tissue (BAT) mass and torpid core body temperature (Rice et al 2021 ).…”