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The Remaining Mysteries About Brown Adipose Tissues

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The Remaining Mysteries About Brown Adipose Tissues cells Review The Remaining Mysteries about Brown Adipose Tissues Miwako Nishio 1 and Kumiko Saeki 1,2,* 1 Department of Laboratory Molecular Genetics of Hematology, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo 113-8510, Japan; [email protected] 2 Department of Regenerative Medicine, Research Institute, National Center for Global Health and Medicine, Tokyo 162-8655, Japan * Correspondence: [email protected]; Tel.: +81-3-3202-7181 Received: 30 September 2020; Accepted: 4 November 2020; Published: 10 November 2020 Abstract: Brown adipose tissue (BAT), which is a thermogenic fat tissue originally discovered in small hibernating mammals, is believed to exert anti-obesity effects in humans. Although evidence has been accumulating to show the importance of BAT in metabolism regulation, there are a number of unanswered questions. In this review, we show the remaining mysteries about BATs. The distribution of BAT can be visualized by nuclear medicine examinations; however, the precise localization of human BAT is not yet completely understood. For example, studies of 18F-fluorodeoxyglucose PET/CT scans have shown that interscapular BAT (iBAT), the largest BAT in mice, exists only in the neonatal period or in early infancy in humans. However, an old anatomical study illustrated the presence of iBAT in adult humans, suggesting that there is a discrepancy between anatomical findings and imaging data. It is also known that BAT secretes various metabolism-improving factors, which are collectively called as BATokines. With small exceptions, however, their main producers are not BAT per se, raising the possibility that there are still more BATokines to be discovered. Although BAT is conceived as a favorable tissue from the standpoint of obesity prevention, it is also involved in the development of unhealthy conditions such as cancer cachexia. In addition, a correlation between browning of mammary gland and progression of breast cancers was shown in a xenotransplantation model. Therefore, the optimal condition should be carefully determined when BAT is considered as a measure the prevention of obesity and improvement of metabolism. Solving BAT mysteries will open a new door for health promotion via advanced understanding of metabolism regulation system. Keywords: brown adipose tissue; BATokine; interscapular BAT; trapezius muscle; cachexia; extracellular vesicles 1. Introduction Brown adipose tissues (BATs), which contribute to non-shivering thermogenesis, has been attracting attention as a target for therapeutic development against obesity and metabolic disorders. BATs are required for the maintenance of body temperature in a cold environment in small mammals, which suffer from large heat loss due to high surface/volume ratios. BATs also contribute to rapid thermogenesis after hibernation. In mice, the presence of BATs has been anatomically determined in specific sites of the body including in interscapular, cervical, axillary, perirenal, and mediastinal regions [1,2] as well as in mammary gland [3]. Humans also have functional BATs [4–7], whose distribution has been visualized by 18F-fluorodeoxyglucose (18F-FDG)-PET/CT examinations as fat depots with high glucose uptake capacities. In adult humans, BATs are detected in deep neck regions, supraclavicular regions, axillary regions, paravertebral regions, periaortic regions, and suprarenal regions (Figure1). The localization of BATs can be summarized as “alongside of large arteries” and “in Cells 2020, 9, 2449; doi:10.3390/cells9112449 www.mdpi.com/journal/cells Cells 2020, 9, x FOR PEER REVIEW 2 of 15 Cells 2020regions, 9, 2449 (Figure 1). The localization of BATs can be summarized as “alongside of large arteries” and2 of 15 “in peri-adrenal gland spaces”, both of which receive abundant adrenergic signals. Since adrenergic stimuli are required for the maintenance of BATs, this distribution pattern of BATs seems highly peri-adrenal gland spaces”, both of which receive abundant adrenergic signals. Since adrenergic stimuli reasonable. are required for the maintenance of BATs, this distribution pattern of BATs seems highly reasonable. The amounts of BAT, which tend to reduce with age [8], are inversely correlated with obesity The amounts of BAT, which tend to reduce with age [8], are inversely correlated with obesity [9–11] [9–11] and glucose intolerance [12]. In humans, interscapular BAT (iBAT) is detectable in newborns andand glucose young intolerance suckling infants [12]. Inby humans,18F-FDG-PET/CT interscapular examinations. BAT (iBAT) There is, is detectablehowever, a indifference newborns in the and 18 youngdepth suckling of iBAT infants between by miceF-FDG-PET and humans./CT examinations. In mice, iBAT Therelocates is, in however, the subcutaneous a difference space in thebeneath depth of iBATthe layer between of white mice adipose and humans. tissue (WAT), In mice, whereas iBAT iBAT locates locates in thebeneath subcutaneous the trapezius space muscle beneath in the layerhumans. of white Although adipose the tissue reason (WAT), for the whereas disappearance iBAT locates of iBAT beneath in humans the trapezius during muscleearly infancy in humans. is Althoughunknown, the the reason presence for the of iBAT disappearance in inter-muscular of iBAT spaces in humans (i.e., between during the early trapezius infancy muscle is unknown, and the the presencerhomboid of muscles) iBAT in may inter-muscular be disadvantageous spaces (i.e., for betweenlong-term the maintenance trapezius muscleof iBAT and because the rhomboid skeletal muscles)muscles may produce be disadvantageous substantial heat. for long-term maintenance of iBAT because skeletal muscles produce substantialIt is heat. known that transplantation of murine BAT [13] or human pluripotent stem cell-derived brownIt is known adipocytes that (hBA) transplantation [14] improves of murine lipid and BAT glucose [13] ormetabolism human pluripotent [13,14] and stemprevents cell-derived obesity brown[13]. adipocytes Therefore, (hBA) approaches [14] improves to augmenting lipid and BAT glucose or preventing metabolism its age-dependent [13,14] and prevents reduction obesity may be [13 ]. Therefore,an effectual approaches strategy to for augmenting the control BAT of obesity. or preventing It is also its believed age-dependent that metabolism-improving reduction may be an eeffectsffectual strategyof BAT for is the executed control via of secreted obesity. factors, It is alsowhich believed are collectively that metabolism-improving termed BATokines. Up etoff ectsnow, of several BAT is factors have been reported to serve as BATokines including Fibroblast growth factor 21 (Fgf21) [15,16], executed via secreted factors, which are collectively termed BATokines. Up to now, several factors have Interleukin 6 (Il6) [13], Growth differentiation factor (Gdf15) [17], Bone morphogenetic protein 8b been reported to serve as BATokines including Fibroblast growth factor 21 (Fgf21) [15,16], Interleukin 6 (Bmp8b [18], Angiopoietin-like 8 (Angptl8) [19], Neuregulin 4 (Nrg4) [20,21], Slit guidance ligand 2 (Il6) [13], Growth differentiation factor (Gdf15) [17], Bone morphogenetic protein 8b (Bmp8b [18], (Slit2) [22], Ependymin related 1 (Epdr1) [23], and Phospholipid transfer protein (Pltp) [24]. Except Angiopoietin-likefor Angptl8 and8 Nrg4 (Angptl8), however, [19 ],the Neuregulin expression levels 4 (Nrg4) of those [20,21 factors], Slit are guidance low in BATs, ligand implying 2 (Slit2) that [22 ], Ependyminthey serve related as autocrine/paracrine 1 (Epdr1) [23], and factors Phospholipid involved in transfer the regulation protein (Pltp)of BAT [ 24functions]. Except rather for Angptl8 than and hormonesNrg4, however, that mediate the expression inter-organ levels communications. of those factors Although are low biological in BATs, significance implying that of enhanced they serve as autocrineAngptl8 /releaseparacrine by activated factors involved BAT remains in the unclear regulation (reviewed of BAT in functions[25]), Nrg4-Bmp8b rather than axis hormones is suggested that mediateto be inter-organ involved in communications.promoting sympathetic Although innervation biological of BAT significance [26]. On ofthe enhanced other hand, Angptl8 hBA secretes release a by activatedlow molecular BAT remains weight unclear factor (≈800 (reviewed Da) that in enhances [25]), Nrg4-Bmp8b insulin secretion axis isby suggested pancreatic tobeta be cells involved [27]. It in promotingis also shown sympathetic that hBA innervation secretes a ofvariety BAT [of26 extracellular]. On the other vesicles hand, (EVs) hBA [17], secretes which a lowmay molecularserve as weightBATokines factor ( as800 in the Da) case that of enhances WAT [28]. insulin secretion by pancreatic beta cells [27]. It is also shown ≈ that hBAAlthough secretes BAT a variety is generally of extracellular accepted as vesicles a favorable (EVs) fat [tissue,17], which hyperactivation may serve of as BAT BATokines may induce as in the caseunfavorable of WAT outcomes. [28]. In Apoe-deficient mice, hyperactivation of BAT by acute cold exposure promotes atheroscleroticAlthough BAT plaque is generally growth acceptedand instability as a favorable [29]. Involvement fat tissue, ofhyperactivation BAT in the development of BAT may of cancer induce unfavorablecachexia outcomes.is suggested In (reviewedApoe-deficient in [30–33]). mice, It hyperactivation is even suggested of that BAT browning by acute (i.e., cold acquisition exposure promotesof BAT- like phenotypes) of breast
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