Does exercise activate brown fat?

Brown adipose tissue (BAT) can dissipate the energy produced by lipid oxidation as heat, thereby counteracting obesity. Aerobic exercise activates BAT, but the specific underlying mechanism is still unclear.

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The relationship between obesity and BAT

Here, 8 weeks of exposure to a HFD caused mice to become obese, and continued feeding with this same diet for 4 more weeks increased their BF% and serum levels of TG, TC and GLU. Since active BAT was found in adult humans, a growing number of studies confirmed that activation of BAT has an anti-obesity effect, and consequently, functional changes in the BAT of obese organisms have attracted considerable attention [16]. Our study found that obese mice have a significantly reduced BAT percentage and UCP1 expression, and microarray analyses showed that obesity was associated with reduced glycolipid metabolism. This observation is consistent with the findings by Kim and colleagues that the expression of genes related to sterol biosynthesis and FA metabolism in the BAT of mice decreased continuously with the period of exposure to a HFD (maximal at 24 weeks) [17]. BAT oxidizes excess fat and glucose for thermogenesis. After FAs enter the mitochondria in brown adipocytes, they can be utilized to produce heat through UCP1 or stored in lipid droplets by reesterification to TG [18, 19]. BAT plays an important role in the catabolism of TG and is considered to be among the organs primarily responsible for clearing lipids from the plasma [20]. Activation of UCP1 and fatty acid β-oxidation play a key role in this context [21]. Thermogenesis by 63 g of BAT in the clavicle of a healthy adult could be equivalent to a 4.1-kg weight loss [3]. The body weight, fat mass, Lee’s index and TG levels in the serum of mice in which BAT had been deleted were increased significantly after 16 weeks on a HFD [22]. The fasting blood glucose levels of Chinese adults with active BAT (aBAT) were significantly lower than those of other subjects [23]. All available evidence indicates that a decrease in BAT mass or activity can lead to increases in serum TC and glucose levels [24]. Our microarray results also revealed that obesity promotes immune system progression and inflammatory and immune responses in BAT, which is consistent with the observations by Kim and Svahn and coworkers [4, 17]. Obesity can cause immune cells to infiltrate adipose tissue and release proinflammatory factors such as cytokines to other tissues, which aggravates metabolic disorders and results in chronic inflammation [25]. The infiltration of activated macrophages into tissues is the key inflammatory event. BAT can inhibit inflammatory macrophages, while WAT enhances the inflammatory response [26]. On the other hand, the elevated levels of inflammatory factors associated with obesity inhibit the activation and recruitment of BAT, as well as the release of inflammatory factors from this tissue. In addition, activation of the complement system stimulates the secretion of leptin, which in turn causes proinflammatory factors to accumulate at inflammatory sites in a vicious cycle [27]. This process is also associated with the production of free radicals, which decrease the expression of BAT-specific genes and the activity of BAT [28].

Aerobic exercise activates BAT in obese mice

The enhanced excitability of the SNS could stimulate BAT activity, inducing and/or inhibiting specific genes that regulate the differentiation and proliferation of brown adipocytes [12]. Thus, aerobic exercise, which effectively elevates SNS activity, was once thought to activate BAT, and regular exercise might promote the recruitment and relative number of brown adipose precursor cells [29]. In connection with previous investigations, the level of expression of thermogenesis-related genes such as UCP1 was used as an indicator of the degree of BAT activation, but recent studies have found that activation of BAT by aerobic exercise may not depend on UCP1 expression [30]. We found that even with a continued HFD, aerobic exercise reduced body weight, body fat percentage and blood glucose levels and elevated the BAT percentage in obese mice. Although aerobic exercise failed to enhance the expression of UCP1 in BAT, glycolipid metabolism was increased, and genes associated with cell apoptosis and death were downregulated. Moreover, aerobic exercise upregulated the expression of genes involved in pathways related to glucose metabolism (insulin/AMPK signaling pathway) and lipid metabolism (PPAR/VEGF signaling pathway and arachidonic acid metabolism) in BAT and downregulated pathways related to inflammatory responses (the Jak-STAT/ErbB/TGF-beta signaling pathway). These observations indicate that exercise not only activates glycolipid metabolism by BAT but also may influence the effects of obesity on chronic inflammation. Running slightly promotes thermogenesis by BAT (with no difference in the level of UCP1) while influencing the morphology, sympathetic tone and vascularization of this tissue [30]. Enhancement of insulin signaling, together with inhibition of JNK activation and of the production of proinflammatory cytokines by BAT, may be involved in the ability of exercise to alleviate obesity [31]. Exercise could also counteract obesity through adrenergic recruitment of brown adipocytes, with their endocrine support of angiogenesis [30]. In the future, the production of WAT browning or formation of beige/brite cells in response to aerobic exercise by obese organisms should be examined to further clarify the mechanism by which exercise regulates BAT.

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Exercise upregulates the VEGF-COX2 pathway in BAT in obese mice

By analyzing the interaction of differentially expressed genes in the key regulatory pathways, we found that COX2 in the VEGF signaling pathway is located in a key regulatory position in connection with multiple functions of BAT. The reduction in BAT function caused by obesity may be related to reduced VEGF expression. Adipose tissue is clearly vascularized, and its abundant blood vessels help transport FAs and secrete adipocytokines [32]. Obesity leads to adipose tissue becoming hypoxic, which causes imbalances in lipid metabolism, insulin resistance and local inflammatory responses [33], as well as capillary dysfunction and a decrease in the density of BAT [34]. As the only bona fide endothelial cell growth factor, VEGF (mainly VEGFa) regulates the proliferation and migration of endothelial cells, as well as vasodilation and vascular permeability [35, 36], and is therefore considered a potential treatment for adipose tissue damage and systemic metabolic diseases after obesity [37]. VEGFa is abundant in BAT [38], and decreased expression of VEGF caused by obesity may be related to functional hypoxia, leading to mitochondrial dysfunction and the accumulation of lipid droplet whitening of BAT [39]. Adrβ3 may play an important role in the regulation of BAT activity by VEGF. Obesity may reduce the number of capillaries in BAT and Adrβ3 expression, further increasing the mitochondrial production of reactive oxygen species (ROS) and autophagy [28]. Cold stimulates vascular endothelial cells to form capillaries, which upregulate VEGFa rapidly. Then, VEGFa binds to its receptor Flk-1 and activates downstream factors to increase the expression of COX2, a marker of mitochondrial heat production, further enhancing thermogenesis by BAT [40]. The changes in BAT induced by cold disappeared after resection of sympathetic nerves but could be restored by activators of noradrenaline (NE) and Adrβ3 [41]. Regular exercise leads to the accumulation of angiogenic signals that strengthen and increase the density of blood vessels in subcutaneous adipose tissue, but this effect is attenuated in obese organisms [42]. Acute exercise increases the level of VEGF mRNA in the WAT of rats on a HFD [32], and the angiogenic capacities of fat at different locations differ [43], but the effects of exercise on the blood vessels in BAT have rarely been reported. Activation of BAT by exercise is closely related to the activation of sympathetic nerves and secretion of NE. Our results showed that an agonist of Adrβ3 significantly reduced the lipid content in brown adipocytes and activated the VEGF-COX2 pathway, which was prevented by inhibition of COX2. Activation of the VEGF pathway is dependent on the activation of Adrβ3 and its downstream COX2 [44], also known as prostaglandin synthetase, which can convert arachidonic acid into various prostaglandins (PGs), and increased levels of PG may be regarded as reflecting enhancement of the function of BAT [45, 46]. PGC-1α, another hallmark protein that reflects the activity of BAT, is the key regulator of mitochondrial biogenesis and oxidative metabolism [47]. Eight weeks of moderate treadmill exercise significantly reduced the expression of COX2 in the BAT of rats with HFD-induced obesity [48], increasing the resting metabolic rate and nonshivering thermogenesis (NST) and decreasing body fat [49]. After treatment with an Adrβ3 agonist, COX2 and PG levels were increased in WAT, and brown adipose tissue appeared. After treatment with analogs of PGE2 and PGI2, the mRNA levels of UCP1 and PGC-1α were increased in stromal-vascular fraction (SVF) cells derived from WAT, effects mediated by the PG receptor and PPARγ [50]. COX2 can be considered to be one of the effectors of Adrβ signaling in WAT and mediates the activation of inducible BAT (indBAT) [51]. The downstream PGI2/Ptgir/PPARγ/UCP1 signaling pathway could transform stromal progenitor cells into BAT, thereby contributing to energy consumption [52]. Figure 6 illustrates the entire regulatory process observed in our study.

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Fig. 6 Changes in the BAT of obese individuals and regulation of BAT in these individuals by exercise Full size image Undoubtedly, the regulatory effect of exercise on BAT remains controversial. Numerous investigators have focused instead on the effects of exercise on WAT browning (caused by an increased number of brown or brite adipocytes), which may be more relevant, since the largest proportion of adipose tissue in our body by far is WAT. However, at present, the lack of uniform standards for the assessment of WAT browning and beige adipocytes makes studies in this area challenging, a situation that will improve as more appropriate experimental approaches are developed.

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