Endocrinology and Metabolism

Review Article

Miscellaneous
Brown Adipose Tissue: Activation and Metabolism in Humans: Imane Hachemi, Mueez U-Din; Endocrinol Metab. 2023;38(2):214-222. Published online March 27, 2023; DOI: https://doi.org/10.3803/EnM.2023.1659

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Brown adipose tissue (BAT) is a thermogenic organ contributing to non-shivering thermogenesis. BAT becomes active under cold stress via sympathetic nervous system activation. However, recent evidence has suggested that BAT may also be active at thermoneutrality and in a postprandial state. BAT has superior energy dissipation capacity compared to white adipose tissue (WAT) and muscles. Thus, it has been proposed that the recruitment and activation of additional BAT may increase the overall energy-expending capacity in humans, potentially improving current whole-body weight management strategies. Nutrition plays a central role in obesity and weight management. Thus, this review discusses human studies describing BAT hyper-metabolism after dietary interventions. Nutritional agents that can potentially recruit brown adipocytes via the process of BAT-WAT transdifferentiation are also discussed.

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Spermidine activates adipose tissue thermogenesis through autophagy and fibroblast growth factor 21
Yinhua Ni, Liujie Zheng, Liqian Zhang, Jiamin Li, Yuxiang Pan, Haimei Du, Zhaorong Wang, Zhengwei Fu
The Journal of Nutritional Biochemistry.2024; 125: 109569. CrossRef
A natural sustained-intestinal release formulation of red chili pepper extracted capsaicinoids (Capsifen®) safely modulates energy balance and endurance performance: a randomized, double-blind, placebo-controlled study
N. Roopashree, Das S. Syam, I. M. Krishnakumar, K. N. Mala, Bradley S. Fleenor, Jestin Thomas
Frontiers in Nutrition.2024;[Epub] CrossRef
MRI Methods to Visualize and Quantify Adipose Tissue in Health and Disease
Katerina Nikiforaki, Kostas Marias
Biomedicines.2023; 11(12): 3179. CrossRef

Brief Report

Diabetes, Obesity and Metabolism
Sestrin2 Regulates Beneficial β3-Adrenergic Receptor-Mediated Effects Observed in Inguinal White Adipose Tissue and Soleus Muscle: Min Jeong Park, Joo Won Kim, Eun Roh, Kyung Mook Choi, Sei Hyun Baik, Hwan-Jin Hwang, Hye Jin Yoo; Endocrinol Metab. 2022;37(3):552-557. Published online June 29, 2022; DOI: https://doi.org/10.3803/EnM.2022.1421

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Abstract PDF Supplementary Material PubReader ePub

Sestrin2, a well-known adenosine monophosphate-activated protein kinase (AMPK) regulator, plays a protective role against metabolic stress. The β3-adrenergic receptor (β3AR) induces fat browning and inhibits muscle atrophy in an AMPK-dependent manner. However, no prior research has examined the relationship of sestrin2 with β3AR in body composition changes. In this study, CL 316,243 (CL), a β3AR agonist, was administered to wild-type and sestrin2-knockout (KO) mice for 2 weeks, and fat and muscle tissues were harvested. CL induced AMPK phosphorylation, expression of brown-fat markers, and mitochondrial biogenesis, which resulted in the reduction of lipid droplet size in inguinal white adipose tissue (iWAT). These effects were not observed in sestrin2-KO mice. In CL-treated soleus muscle, sestrin2-KO was related to decreased myogenic gene expression and increased levels of muscle atrophy-related molecules. Our results suggest that sestrin2 is associated with beneficial β3AR-mediated changes in body composition, especially in iWAT and in the soleus.

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Sestrin2 levels in patients with anxiety and depression myocardial infarction was up-regulated and suppressed inflammation and ferroptosis by LKB1-mediated AMPK activation
Yufeng Qian, Lian Chen, Beibei Gao, Xianhua Ye
Clinical and Experimental Hypertension.2023;[Epub] CrossRef
Sestrin2 in diabetes and diabetic complications
Xiaodan Zhang, Zirui Luo, Jiahong Li, Yaxuan Lin, Yu Li, Wangen Li
Frontiers in Endocrinology.2023;[Epub] CrossRef

Original Articles

Endocrine Research
Danshen Extracts Prevents Obesity and Activates Mitochondrial Function in Brown Adipose Tissue: Yoon Hee Cho, Cheol Ryong Ku, Young-Suk Choi, Hyeon Jeong Lee, Eun Jig Lee; Endocrinol Metab. 2021;36(1):185-195. Published online February 24, 2021; DOI: https://doi.org/10.3803/EnM.2020.835

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Background
Danshen has been widely used in oriental medicine to improve body function. The purpose of this study is to investigate the effect of water-soluble Danshen extract (DE) on weight loss and on activation proteins involved in mitochondrial biogenesis in brown adipose tissue (BAT) in obese mice.
Methods
BAT was isolated from 7-week-old male Sprague-Dawley rats, and expression of proteins related to mitochondrial biogenesis was confirmed in both brown preadipocytes and mature brown adipocytes treated with DE. For the in vivo study, low-density lipoprotein receptor knock out mice were divided into three groups and treated for 17 weeks with: standard diet; high fat diet (HFD); HFD+DE. Body weight was measured every week, and oral glucose tolerance test was performed after DE treatment in streptozotocin-induced diabetic mice. To observe the changes in markers related to thermogenesis and adipogenesis in the BAT, white adipose tissue (WAT) and liver of experimental animals, tissues were removed and immediately frozen in liquid nitrogen.
Results
DE increased the expression of uncoupling protein 1 and peroxisome proliferator-activated receptor gamma coactivator 1-alpha in brown preadipocytes, and also promoted the brown adipocyte differentiation and mitochondrial function in the mature brown adipocytes. Reactive oxygen species production in brown preadipocytes was increased depending on the concentration of DE. DE activates thermogenesis in BAT and normalizes increased body weight and adipogenesis in the liver due to HFD. Browning of WAT was increased in WAT of DE treatment group.
Conclusion
DE protects against obesity and activates mitochondrial function in BAT.

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Pharmacological Benefits and Underlying Mechanisms of Salvia miltiorrhiza against Molecular Pathology of Various Liver Diseases: A Review
Cho Hyun Hwang, Eungyeong Jang, Jang-Hoon Lee
The American Journal of Chinese Medicine.2023; 51(07): 1675. CrossRef

Clinical Study
The Role of Circulating Slit2, the One of the Newly Batokines, in Human Diabetes Mellitus: Yea Eun Kang, Sorim Choung, Ju Hee Lee, Hyun Jin Kim, Bon Jeong Ku; Endocrinol Metab. 2017;32(3):383-388. Published online September 18, 2017; DOI: https://doi.org/10.3803/EnM.2017.32.3.383

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Background

Slit2 is a new secreted protein from adipose tissue that improves glucose hemostasis in mice; however, there is no study about the serum levels and precise role of Slit2 in human. The aim of this study is to explore the serum level of Slit2 in human, and to identify the role of Slit2 in diabetes mellitus (DM).

Methods

The participants of this study consist of 38 subjects with newly diagnosed DM, and 75 healthy subjects as a control group. Serum Slit2 levels were measured using an enzyme-linked immunosorbent assay. Relationship between circulating Slit2 and diabetic related factors was investigated in diabetic group compared with non-diabetic group. Additionally, the correlations between the serum level of Slit2 and diverse metabolic parameters were analyzed.

Results

Circulating Slit2 level was more decreased in diabetic group than in control group, but there was no significant difference statistically. Interestingly, serum levels of Slit2 were significantly negatively correlated to the serum concentrations of fasting glucose (coefficient r=–0.246, P=0.008), the serum concentrations of postprandial glucose (coefficient r=–0.233, P=0.017), and glycosylated hemoglobin (HbA1c; coefficient r=–0.357, P<0.001).

Conclusion

From our study, the first report of circulating Slit2 levels in human, circulating Slit2 level significantly negatively correlated with serum glucose and HbA1c. Our results suggest that the circulating Slit2 may play a role in maintainence of glucose homeostasis in human, even though exact contribution and mechanism are not yet known.

Citations

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Brown adipose tissue-derived metabolites and their role in regulating metabolism
Khanyisani Ziqubu, Phiwayinkosi V. Dludla, Sihle E. Mabhida, Babalwa U. Jack, Susanne Keipert, Martin Jastroch, Sithandiwe E. Mazibuko-Mbeje
Metabolism.2024; 150: 155709. CrossRef
An update on the secretory functions of brown, white, and beige adipose tissue: Towards therapeutic applications
Zeinab Ghesmati, Mohsen Rashid, Shabnam Fayezi, Frank Gieseler, Effat Alizadeh, Masoud Darabi
Reviews in Endocrine and Metabolic Disorders.2024; 25(2): 279. CrossRef
The integrated bioinformatic analysis identifies immune microenvironment-related potential biomarkers for patients with gestational diabetes mellitus
Jie-ling Chen, Hui-fang Dai, Xin-chen Kan, Jie Wu, Hong-Wu Chen
Frontiers in Immunology.2024;[Epub] CrossRef
Adipokines from white adipose tissue in regulation of whole body energy homeostasis
Bijayashree Sahu, Naresh C. Bal
Biochimie.2023; 204: 92. CrossRef
The Role of Slit-2 in Gestational Diabetes Mellitus and Its Effect on Pregnancy Outcome
Yan Wang, Shihua Zhao, Wei Peng, Ying Chen, Jingwei Chi, Kui Che, Yangang Wang
Frontiers in Endocrinology.2022;[Epub] CrossRef
The Heartwarming Effect of Brown Adipose Tissue
Kelsey M. Pinckard, Kristin I. Stanford
Molecular Pharmacology.2022; 102(1): 39. CrossRef
New players of the adipose secretome: Therapeutic opportunities and challenges
Laetitia Coassolo, Niels Banhos Dannieskiold-Samsøe, Meng Zhao, Hobson Allen, Katrin J. Svensson
Current Opinion in Pharmacology.2022; 67: 102302. CrossRef
Serum CD14 concentration is associated with obesity and insulin resistance in non-diabetic individuals
Yea Eun Kang, Kyong Hye Joung, Ji Min Kim, Ju Hee Lee, Hyun Jin Kim, Bon Jeong Ku
Journal of International Medical Research.2022; 50(10): 030006052211300. CrossRef
Brown/Beige adipose tissues and the emerging role of their secretory factors in improving metabolic health: The batokines
Bilal Ahmad, Muhammad Sufyan Vohra, Mansab Ali Saleemi, Christopher J. Serpell, Isabel Lim Fong, Eng Hwa Wong
Biochimie.2021; 184: 26. CrossRef
Thermogenic Fat: Development, Physiological Function, and Therapeutic Potential
Bruna B. Brandão, Ankita Poojari, Atefeh Rabiee
International Journal of Molecular Sciences.2021; 22(11): 5906. CrossRef
Brown Adipose Crosstalk in Tissue Plasticity and Human Metabolism
Camilla Scheele, Christian Wolfrum
Endocrine Reviews.2020; 41(1): 53. CrossRef
Development of a Cell-Based Assay for the Detection of Neutralizing Antibodies to PF-06730512 Using Homogenous Time-Resolved Fluorescence
Michael Luong, Ying Wang, Stephen P. Berasi, Janet E. Buhlmann, Hongying Yang, Boris Gorovits
The AAPS Journal.2020;[Epub] CrossRef
Brown and beige fat: From molecules to physiology and pathophysiology
Stefania Carobbio, Anne-Claire Guénantin, Isabella Samuelson, Myriam Bahri, Antonio Vidal-Puig
Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids.2019; 1864(1): 37. CrossRef
Serum R-Spondin 1 Is a New Surrogate Marker for Obesity and Insulin Resistance
Yea Eun Kang, Ji Min Kim, Hyon-Seung Yi, Kyong Hye Joung, Ju Hee Lee, Hyun Jin Kim, Bon Jeong Ku
Diabetes & Metabolism Journal.2019; 43(3): 368. CrossRef
Deletion of Robo4 prevents high‐fat diet‐induced adipose artery and systemic metabolic dysfunction
Tam T. T. Phuong, Ashley E. Walker, Grant D. Henson, Daniel R. Machin, Dean Y. Li, Anthony J. Donato, Lisa A. Lesniewski
Microcirculation.2019;[Epub] CrossRef
Adipose Tissue-Derived Signatures for Obesity and Type 2 Diabetes: Adipokines, Batokines and MicroRNAs
Min-Woo Lee, Mihye Lee, Kyoung-Jin Oh
Journal of Clinical Medicine.2019; 8(6): 854. CrossRef
The role of brown and beige adipose tissue in glycaemic control
Katarina Klepac, Anastasia Georgiadi, Matthias Tschöp, Stephan Herzig
Molecular Aspects of Medicine.2019; 68: 90. CrossRef

Endocrine Research
The Effects of High Fat Diet and Resveratrol on Mitochondrial Activity of Brown Adipocytes: Cheol Ryong Ku, Yoon Hee Cho, Zhen-Yu Hong, Ha Lee, Sue Ji Lee, Seung-soo Hong, Eun Jig Lee; Endocrinol Metab. 2016;31(2):328-335. Published online April 8, 2016; DOI: https://doi.org/10.3803/EnM.2016.31.2.328

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Background

Resveratrol (RSV) is a polyphenolic phytoalexin that has many effects on metabolic diseases such as diabetes and obesity. Given the importance of brown adipose tissue (BAT) for energy expenditure, we investigated the effects of RSV on brown adipocytes.

Methods

For the in vitro study, interscapular BAT was isolated from 7-week-old male Sprague Dawley rats. For the in vivo study, 7-week-old male Otsuka Long Evans Tokushima Fatty (OLETF) rats were divided into four groups and treated for 27 weeks with: standard diet (SD); SD+RSV (10 mg/kg body weight, daily); high fat diet (HFD); HFD+RSV. RSV was provided via oral gavage once daily during the in vivo experiments.

Results

RSV treatment of primary cultured brown preadipocytes promoted mitochondrial activity, along with over-expression of estrogen receptor α (ER-α). In OLETF rats, both HFD and RSV treatment increased the weight of BAT and the differentiation of BAT. However, only RSV increased the mitochondrial activity and ER-α expression of BAT in the HFD-fed group. Finally, RSV improved the insulin sensitivity of OLETF rats by increasing the mitochondrial activity of BAT, despite having no effects on white adipocytes and muscles in either diet group.

Conclusion

RSV could improve insulin resistance, which might be associated with mitochondrial activity of brown adipocyte. Further studies evaluating the activity of RSV for both the differentiation and mitochondrial activity of BAT could be helpful in investigating the effects of RSV on metabolic parameters.

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Natural Bioactive Compounds from Foods Inhibited Pigmentation Especially Potential Application of Fucoxanthin to Chloasma: a Mini-Review
Yida Wang, Hang Qi
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Resveratrol combats chronic diseases through enhancing mitochondrial quality
Weichu Tao, Hu Zhang, Xia Jiang, Ning Chen
Food Science and Human Wellness.2024; 13(2): 597. CrossRef
The Potential to Fight Obesity with Adipogenesis Modulating Compounds
Jiaqi Zhao, Ailin Zhou, Wei Qi
International Journal of Molecular Sciences.2022; 23(4): 2299. CrossRef
Macrophage and Adipocyte Mitochondrial Dysfunction in Obesity-Induced Metabolic Diseases
Liwen Wang, Jie Hu, Haiyan Zhou
The World Journal of Men's Health.2021; 39(4): 606. CrossRef
Precision Nutrition to Activate Thermogenesis as a Complementary Approach to Target Obesity and Associated-Metabolic-Disorders
Marina Reguero, Marta Gómez de Cedrón, Sonia Wagner, Guillermo Reglero, José Carlos Quintela, Ana Ramírez de Molina
Cancers.2021; 13(4): 866. CrossRef
Natural Antioxidant Application on Fat Accumulation: Preclinical Evidence
Proshanta Roy, Daniele Tomassoni, Enea Traini, Ilenia Martinelli, Maria Vittoria Micioni Di Bonaventura, Carlo Cifani, Francesco Amenta, Seyed Khosrow Tayebati
Antioxidants.2021; 10(6): 858. CrossRef
Activation of Brown Adipose Tissue and Promotion of White Adipose Tissue Browning by Plant-based Dietary Components in Rodents: A Systematic Review
Francisco J Osuna-Prieto, Borja Martinez-Tellez, Antonio Segura-Carretero, Jonatan R Ruiz
Advances in Nutrition.2021; 12(6): 2147. CrossRef
Role of Dietary Polyphenols in Adipose Tissue Browning: A Narrative Review
Juan Salazar, Clímaco Cano, José L. Pérez, Ana Castro, María P. Díaz, Bermary Garrido, Rubén Carrasquero, Maricarmen Chacín, Manuel Velasco, Luis D´Marco, Joselyn Rojas-Quintero, Valmore Bermúdez
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Brown and Brite: The Fat Soldiers in the Anti-obesity Fight
Shireesh Srivastava, Richard L. Veech
Frontiers in Physiology.2019;[Epub] CrossRef
Effect of resveratrol on adipokines and myokines involved in fat browning: Perspectives in healthy weight against obesity
Oh Yoen Kim, Ji Yeon Chung, Juhyun Song
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Yilian Hong, Yi Lin, Qiya Si, Lijuan Yang, Weisong Dong, Xuejiang Gu
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Programming of the Beige Phenotype in White Adipose Tissue of Adult Mice by Mild Resveratrol and Nicotinamide Riboside Supplementations in Early Postnatal Life
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Effects of Polyphenols on Thermogenesis and Mitochondrial Biogenesis
Tanila Wood dos Santos, Quélita Cristina Pereira, Lucimara Teixeira, Alessandra Gambero, Josep A. Villena, Marcelo Lima Ribeiro
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The Role of Circulating Slit2, the One of the Newly Batokines, in Human Diabetes Mellitus
Yea Eun Kang, Sorim Choung, Ju Hee Lee, Hyun Jin Kim, Bon Jeong Ku
Endocrinology and Metabolism.2017; 32(3): 383. CrossRef
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Biochimie.2017; 134: 99. CrossRef
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Articles inEndocrinology and Metabolismin 2016
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Response: The Effects of High Fat Diet and Resveratrol on Mitochondrial Activity of Brown Adipocytes (Endocrinol Metab2016;31:328-35, Cheol Ryong Ku et al.)
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Case Reports

Primary Hyperparathyroidism with Extensive Brown Tumors and Multiple Fractures in a 20-Year-Old Woman: Ju Hee Choi, Kyoung Jin Kim, Ye Jin Lee, Sun Hwa Kim, Sin Gon Kim, Kwang Yoon Jung, Dong Seop Choi, Nam Hoon Kim; Endocrinol Metab. 2015;30(4):614-619. Published online December 31, 2015; DOI: https://doi.org/10.3803/EnM.2015.30.4.614

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A brown tumor is a benign fibrotic, erosive bony lesion caused by localized, rapid osteoclastic turnover, resulting from hyperparathyroidism. Although brown tumors are one of the most pathognomonic signs of primary hyperparathyroidism, they are rarely seen in clinical practice. In this report, we present a case of 20-year-old woman with recurrent fractures and bone pain. Plain digital radiographs of the affected bones revealed multiple erosive bone tumors, which were finally diagnosed as brown tumors associated with primary hyperparathyroidism due to a parathyroid adenoma. This case shows that multiple, and clinically severe form of brown tumors can even occur in young patients.

Citations

Citations to this article as recorded by

Brown tumor of the knee as the first presentation of primary hyperparathyroidism caused by parathyroid adenoma: A case report
Vaishnavi C Tapadia, Romana Riyaz, Abhigan Babu Shrestha, Javeed Akhtar Ankolvi
Radiology Case Reports.2023; 18(5): 1852. CrossRef
Brown tumors in nuclear medicine: a systematic review
Nicolas Jacquet-Francillon, Nathalie Prevot
Annals of Nuclear Medicine.2023; 37(5): 255. CrossRef
Misdiagnosis of brown tumour caused by primary hyperparathyroidism: a case report with literature review
Yanchun Zhong, Yuxi Huang, Jiaquan Luo, Yongjun Ye
BMC Endocrine Disorders.2022;[Epub] CrossRef
Gnathic Bones and Hyperparathyroidism: A Review on the Metabolic Bony Changes Affecting the Mandible and Maxilla in case of Hyperparathyroidism
Hazim Mahmoud Ibrahem
Advances in Medicine.2020; 2020: 1. CrossRef

Brown Tumor of the Ulna and Radius: An Unusual Presentation of Primary Hyperparathyroidism.: Hyun Park, Gun Hi Kang, Seung Gu Kim, Jun Jae Kim, Na Na Baek, Dae Myung Kim, Sung Woo Cho, Woo Je Lee, Kyung Soo Ko, Byoung Doo Rhee; J Korean Endocr Soc. 2008;23(5):347-351. Published online October 1, 2008; DOI: https://doi.org/10.3803/jkes.2008.23.5.347

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Abstract PDF: Brown tumors are erosive bony lesions caused by chronic excessive secretion of parathyroid hormone. Since the introduction of routine calcium measurement, the diagnosis of hyperparathyroidism has usually been made in asymptomatic patients and as a result, brown tumors are rarely observed as an initial manifestation of hyperparathyroidism.

A Case of Brown Tumor with Severe Hypercalcemia Caused by Parathyroid Adenoma.: Ji Oh Mok; J Korean Endocr Soc. 2003;18(2):221-226. Published online April 1, 2003

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Abstract PDF: Most of primary hyperparathyroidism results from parathyroid adenoma, and is characterized by hypercalcemia, reduced bone density, frequent renal stone, gastric ulcer, duodenal ulcer, muscle weakness, depression, hypertension, anemia, and rarely brown tumor. We had a case of an 80-year-old man having brown tumor caused by primary hyperparathyroidism on the right 10th rib confirmed by CT guided bone biopsy. The patient presented with decreased level of consciousness, acute gastric ulcer, acute duodenal ulcer, GB stones, renal insufficiency, depression, and osteoporosis. Serum calcium level was 16.7 mg/dL and the intact parathyroid hormone level was 3901pg/mL. A parathyroid mass was detected by neck CT and 99mTc-tetrofosmin parathyroid scan. The parathyroid tumor was removed and confirmed as a parathyroid adenoma by pathology. After operation, the patient was treated with vitamin D and calcium in response to the resulting hungry bone syndrome. The intact PTH level returned to a normal range after the removal of the parathyroid adenoma.

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