Research Institute of Wildlife Ecology, Department of Integrative Biology and Evolution, University of Veterinary Medicine, Vienna, Austria.
PLoS One. 2013 May 1;8(5):e63111. doi: 10.1371/journal.pone.0063111. Print 2013.
Polyunsaturated fatty acids (PUFA) have strong effects on hibernation and daily torpor. Increased dietary uptake of PUFA of the n-6 class, particularly of Linoleic acid (LA, C18:2 n-6) lengthens torpor bout duration and enables animals to reach lower body temperatures (T(b)) and metabolic rates. As previously hypothesized, this well-known influence of PUFA may be mediated via effects of the membrane fatty acid composition on sarcoplasmic reticulum (SR) Ca(2+-)ATPase 2a (SERCA) in the heart of hibernators. We tested the hypotheses that high proportions of n-6 PUFA in general, or specifically high proportions of LA (C18:2 n-6) in SR phospholipids (PL) should be associated with increased cardiac SERCA activity, and should allow animals to reach lower minimum T(b) in torpor. We measured activity of SERCA from hearts of hibernating and non-hibernating Syrian hamsters (Mesocricetus auratus) in vitro at 35 °C. Further, we determined the PL fatty acid composition of the SR membrane of these hearts. We found that SERCA activity strongly increased as the proportion of LA in SR PL increased but was negatively affected by the content of Docosahexaenoic acid (DHA; C22:6 n-3). SR PL from hibernating hamsters were characterized by high proportions of LA and low proportions of DHA. As a result, SERCA activity was significantly higher during entrance into torpor and in torpor compared to inter-bout arousal. Also, animals with increased SERCA activity reached lower T(b) during torpor. Interestingly, a subgroup of hamsters which never entered torpor but remained euthermic throughout winter displayed a phenotype similar to animals in summer. This was characterized by lower proportions of LA and increased proportions of DHA in SR membranes, which is apparently incompatible with torpor. We conclude that the PUFA composition of SR membranes affects cardiac function via modulating SERCA activity, and hence determines the minimum T(b) tolerated by hibernators.
多不饱和脂肪酸(PUFA)对冬眠和日常蛰伏有很强的影响。增加 n-6 类 PUFA 的饮食摄入,特别是亚油酸(LA,C18:2 n-6),会延长蛰伏期持续时间,并使动物能够达到更低的体温(T(b))和代谢率。如前所述,这种众所周知的 PUFA 影响可能是通过膜脂肪酸组成对冬眠动物心脏肌浆网(SR)Ca(2+-)ATPase 2a(SERCA)的影响介导的。我们测试了以下假设:一般来说,n-6 PUFA 比例较高,或者特别是 SR 磷脂(PL)中 LA(C18:2 n-6)比例较高,应该与心脏 SERCA 活性增加有关,并使动物在蛰伏期达到更低的最低 T(b)。我们在 35°C 下体外测量了冬眠和非冬眠叙利亚仓鼠(Mesocricetus auratus)心脏的 SERCA 活性。此外,我们还测定了这些心脏 SR 膜的 PL 脂肪酸组成。我们发现,随着 SR PL 中 LA 比例的增加,SERCA 活性强烈增加,但受到二十二碳六烯酸(DHA;C22:6 n-3)含量的负面影响。冬眠仓鼠的 SR PL 具有较高的 LA 比例和较低的 DHA 比例。因此,与进出蛰伏期相比,SERCA 活性在蛰伏期期间显著更高。此外,具有较高 SERCA 活性的动物在蛰伏期期间达到更低的 T(b)。有趣的是,一小部分从未进入蛰伏期但整个冬季保持常温的仓鼠表现出与夏季动物相似的表型。这表现为 SR 膜中 LA 的比例降低和 DHA 的比例增加,这显然与蛰伏期不兼容。我们得出的结论是,SR 膜的 PUFA 组成通过调节 SERCA 活性影响心脏功能,从而决定了冬眠动物耐受的最低 T(b)。