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Basic Research
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Single-Cell Landscape and a Macrophage Subset Enhancing Brown Adipocyte Function in Diabetes
Junfei Gu, Jiajia Jin, Xiaoyu Ren, Xinjie Zhang, Jiaxuan Li, Xiaowei Wang, Shucui Zhang, Xianlun Yin, Qunye Zhang, Zhe Wang
Received August 16, 2023  Accepted February 7, 2024  Published online May 29, 2024  
DOI: https://doi.org/10.4093/dmj.2023.0278    [Epub ahead of print]
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AbstractAbstract PDFSupplementary MaterialPubReader   ePub   
Background
Metabolic dysregulation is a hallmark of type 2 diabetes mellitus (T2DM), in which the abnormalities in brown adipose tissue (BAT) play important roles. However, the cellular composition and function of BAT as well as its pathological significance in diabetes remain incompletely understood. Our objective is to delineate the single-cell landscape of BAT-derived stromal vascular fraction (SVF) and their characteristic alterations in T2DM rats.
Methods
T2DM was induced in rats by intraperitoneal injection of low-dose streptozotocin and high-fat diet feeding. Single-cell mRNA sequencing was then performed on BAT samples and compared to normal rats to characterize changes in T2DM rats. Subsequently, the importance of key cell subsets in T2DM was elucidated using various functional studies.
Results
Almost all cell types in the BAT-derived SVF of T2DM rats exhibited enhanced inflammatory responses, increased angiogenesis, and disordered glucose and lipid metabolism. The multidirectional differentiation potential of adipose tissue-derived stem cells was also reduced. Moreover, macrophages played a pivotal role in intercellular crosstalk of BAT-derived SVF. A novel Rarres2+macrophage subset promoted the differentiation and metabolic function of brown adipocytes via adipose-immune crosstalk.
Conclusion
BAT SVF exhibited strong heterogeneity in cellular composition and function and contributed to T2DM as a significant inflammation source, in which a novel macrophage subset was identified that can promote brown adipocyte function.
Basic Research
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Extracellular Vimentin Alters Energy Metabolism And Induces Adipocyte Hypertrophy
Ji-Hae Park, Soyeon Kwon, Young Mi Park
Diabetes Metab J. 2024;48(2):215-230.   Published online September 26, 2023
DOI: https://doi.org/10.4093/dmj.2022.0332
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  • 1 Crossref
AbstractAbstract PDFSupplementary MaterialPubReader   ePub   
Background
Previous studies have reported that oxidative stress contributes to obesity characterized by adipocyte hypertrophy. However, mechanism has not been studied extensively. In the current study, we evaluated role of extracellular vimentin secreted by oxidized low-density lipoprotein (oxLDL) in energy metabolism in adipocytes.
Methods
We treated 3T3-L1-derived adipocytes with oxLDL and measured vimentin which was secreted in the media. We evaluated changes in uptake of glucose and free fatty acid, expression of molecules functioning in energy metabolism, synthesis of adenosine triphosphate (ATP) and lactate, markers for endoplasmic reticulum (ER) stress and autophagy in adipocytes treated with recombinant vimentin.
Results
Adipocytes secreted vimentin in response to oxLDL. Microscopic evaluation revealed that vimentin treatment induced increase in adipocyte size and increase in sizes of intracellular lipid droplets with increased intracellular triglyceride. Adipocytes treated with vimentin showed increased uptake of glucose and free fatty acid with increased expression of plasma membrane glucose transporter type 1 (GLUT1), GLUT4, and CD36. Vimentin treatment increased transcription of GLUT1 and hypoxia-inducible factor 1α (Hif-1α) but decreased GLUT4 transcription. Adipose triglyceride lipase (ATGL), peroxisome proliferator-activated receptor γ (PPARγ), sterol regulatory element-binding protein 1 (SREBP1), diacylglycerol O-acyltransferase 1 (DGAT1) and 2 were decreased by vimentin treatment. Markers for ER stress were increased and autophagy was impaired in vimentin-treated adipocytes. No change was observed in synthesis of ATP and lactate in the adipocytes treated with vimentin.
Conclusion
We concluded that extracellular vimentin regulates expression of molecules in energy metabolism and promotes adipocyte hypertrophy. Our results show that vimentin functions in the interplay between oxidative stress and metabolism, suggesting a mechanism by which adipocyte hypertrophy is induced in oxidative stress.

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  • Mechanobiology in Metabolic Dysfunction-Associated Steatotic Liver Disease and Obesity
    Emily L. Rudolph, LiKang Chin
    Current Issues in Molecular Biology.2024; 46(7): 7134.     CrossRef
Basic Research
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Role of SUMO-Specific Protease 2 in Leptin-Induced Fatty Acid Metabolism in White Adipocytes
Praise Chanmee Kim, Ji Seon Lee, Sung Soo Chung, Kyong Soo Park
Diabetes Metab J. 2023;47(3):382-393.   Published online March 6, 2023
DOI: https://doi.org/10.4093/dmj.2022.0156
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  • 1 Web of Science
  • 1 Crossref
AbstractAbstract PDFSupplementary MaterialPubReader   ePub   
Background
Leptin is a 16-kDa fat-derived hormone with a primary role in controlling adipose tissue levels. Leptin increases fatty acid oxidation (FAO) acutely through adenosine monophosphate-activated protein kinase (AMPK) and on delay through the SUMO-specific protease 2 (SENP2)–peroxisome proliferator-activated receptor δ/γ (PPARδ/γ) pathway in skeletal muscle. Leptin also directly increases FAO and decreases lipogenesis in adipocytes; however, the mechanism behind these effects remains unknown. Here, we investigated the role of SENP2 in the regulation of fatty acid metabolism by leptin in adipocytes and white adipose tissues.
Methods
The effects of leptin mediated by SENP2 on fatty acid metabolism were tested by siRNA-mediated knockdown in 3T3-L1 adipocytes. The role of SENP2 was confirmed in vivo using adipocyte-specific Senp2 knockout (Senp2-aKO) mice. We revealed the molecular mechanism involved in the leptin-induced transcriptional regulation of carnitine palmitoyl transferase 1b (Cpt1b) and long-chain acyl-coenzyme A synthetase 1 (Acsl1) using transfection/reporter assays and chromatin immunoprecipitation.
Results
SENP2 mediated the increased expression of FAO-associated enzymes, CPT1b and ACSL1, which peaked 24 hours after leptin treatment in adipocytes. In contrast, leptin stimulated FAO through AMPK during the initial several hours after treatment. In white adipose tissues, FAO and mRNA levels of Cpt1b and Acsl1 were increased by 2-fold 24 hours after leptin injection in control mice but not in Senp2-aKO mice. Leptin increased PPARα binding to the Cpt1b and Acsl1 promoters in adipocytes through SENP2.
Conclusion
These results suggest that the SENP2-PPARα pathway plays an important role in leptin-induced FAO in white adipocytes.

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Review
Basic Research
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Brown Fat as a Regulator of Systemic Metabolism beyond Thermogenesis
Okamatsu-Ogura Yuko, Masayuki Saito
Diabetes Metab J. 2021;45(6):840-852.   Published online June 25, 2021
DOI: https://doi.org/10.4093/dmj.2020.0291
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  • 20 Crossref
Graphical AbstractGraphical Abstract AbstractAbstract PDFPubReader   ePub   
Brown adipose tissue (BAT) is a specialized tissue for nonshivering thermogenesis to dissipate energy as heat. Although BAT research has long been limited mostly in small rodents, the rediscovery of metabolically active BAT in adult humans has dramatically promoted the translational studies on BAT in health and diseases. Moreover, several remarkable advancements have been made in brown fat biology over the past decade: The molecular and functional analyses of inducible thermogenic adipocytes (socalled beige adipocytes) arising from a developmentally different lineage from classical brown adipocytes have been accelerated. In addition to a well-established thermogenic activity of uncoupling protein 1 (UCP1), several alternative thermogenic mechanisms have been discovered, particularly in beige adipocytes. It has become clear that BAT influences other peripheral tissues and controls their functions and systemic homeostasis of energy and metabolic substrates, suggesting BAT as a metabolic regulator, other than for thermogenesis. This notion is supported by discovering that various paracrine and endocrine factors are secreted from BAT. We review the current understanding of BAT pathophysiology, particularly focusing on its role as a metabolic regulator in small rodents and also in humans.

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Sulwon Lecture 2018
Pathophysiology
Mitochondrial Dysfunction in Adipocytes as a Primary Cause of Adipose Tissue Inflammation
Chang-Yun Woo, Jung Eun Jang, Seung Eun Lee, Eun Hee Koh, Ki-Up Lee
Diabetes Metab J. 2019;43(3):247-256.   Published online March 27, 2019
DOI: https://doi.org/10.4093/dmj.2018.0221
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  • 265 Download
  • 73 Web of Science
  • 73 Crossref
AbstractAbstract PDFPubReader   

Adipose tissue inflammation is considered a major contributing factor in the development of obesity-associated insulin resistance and cardiovascular diseases. However, the cause of adipose tissue inflammation is presently unclear. The role of mitochondria in white adipocytes has long been neglected because of their low abundance. However, recent evidence suggests that mitochondria are essential for maintaining metabolic homeostasis in white adipocytes. In a series of recent studies, we found that mitochondrial function in white adipocytes is essential to the synthesis of adiponectin, which is the most abundant adipokine synthesized from adipocytes, with many favorable effects on metabolism, including improvement of insulin sensitivity and reduction of atherosclerotic processes and systemic inflammation. From these results, we propose a new hypothesis that mitochondrial dysfunction in adipocytes is a primary cause of adipose tissue inflammation and compared this hypothesis with a prevailing concept that “adipose tissue hypoxia” may underlie adipose tissue dysfunction in obesity. Recent studies have emphasized the role of the mitochondrial quality control mechanism in maintaining mitochondrial function. Future studies are warranted to test whether an inadequate mitochondrial quality control mechanism is responsible for mitochondrial dysfunction in adipocytes and adipose tissue inflammation.

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Original Article
Pathophysiology
Investigating Susceptibility to Diabetes Using Features of the Adipose Tissue in Response to In Utero Polycyclic Aromatic Hydrocarbons Exposure
Worlanyo E. Gato, Daniel A. Hunter, Shamaya L. Whitby, Christopher A. Mays, Wilson Yau
Diabetes Metab J. 2016;40(6):494-508.   Published online August 12, 2016
DOI: https://doi.org/10.4093/dmj.2016.40.6.494
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AbstractAbstract PDFSupplementary MaterialPubReader   
Background

In recent times, there has been an increase in the incidence of type 2 diabetes mellitus (T2DM) particularly in children. Adipocyte dysfunction provide a critical link between obesity and insulin resistance resulting in diabetes outcome. Further, environmental chemical exposure during early years of life might be a significant contributing factor to the increase in the incidence of T2DM. This study tests the idea that exposure to environmental contaminants (2-aminoanthracene [2AA]) in utero will show effects in the adipose tissue (AT) that signify T2DM vulnerability. 2AA is a polycyclic aromatic hydrocarbon found in a variety of products.

Methods

To accomplish the study objective, pregnant dams were fed various amounts of 2AA adulterated diets from gestation through postnatal period. The neonates and older offspring were analyzed for diabetic-like genes in the ATs and analysis of serum glucose. Furthermore, weight monitoring, histopathology and immunohistochemical (IHC) staining for CD68 in AT, adipocyte size determination and adiponectin amounts in serum were undertaken.

Results

Up-regulation of adiponectin and interleukin-6 genes were noted in the pups and older rats. Combination of intrauterine 2AA toxicity with moderate high fat diet exhibited gene expression patterns similar to those of the neonates. Elevated serum glucose levels were noted in treated groups. IHC of the AT indicated no significant malformations; however, CD68+ cells were greater in the animals treated to 2AA. Similarly, mean sizes of the adipocytes were larger in treated and combined 2AA and moderate high fat animals. Adiponectin was reduced in 2AA groups.

Conclusion

From the preceding, it appears intrauterine 2AA disturbance, when combined with excess fat accumulation will lead to greater risk for the diabetic condition.

Citations

Citations to this article as recorded by  
  • The Role of Persistent Organic Pollutants in Obesity: A Review of Laboratory and Epidemiological Studies
    Jan Aaseth, Dragana Javorac, Aleksandra Djordjevic, Zorica Bulat, Anatoly Skalny, Irina Zaitseva, Michael Aschner, Alexey Tinkov
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Reviews
Roles of Reactive Oxygen Species on Insulin Resistance in Adipose Tissue
Chang Yeop Han
Diabetes Metab J. 2016;40(4):272-279.   Published online June 28, 2016
DOI: https://doi.org/10.4093/dmj.2016.40.4.272
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  • 115 Web of Science
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AbstractAbstract PDFPubReader   

Obesity resulting from the delivery of an excess amount of energy to adipose tissue from glucose or free fatty acids is associated with insulin resistance and adipose tissue inflammation. Reactive oxygen species (ROS) have been implicated as contributors to both the onset and the progression of insulin resistance. ROS can be generated by overloading the mitochondrial oxidative phosphorylation system, and also by nicotinamide adenine dinucleotide phosphate oxidases (NOX) produced by either adipocytes, which only produce NOX4, or by macrophages, which produce mainly NOX2. The source of the ROS might differ in the early, intermediate and late stages of obesity, switching from NOX4-dependence in the early phases to NOX2-dependence, in the intermediate phase, and transiting to mitochondria-dependence later in the time course of obesity. Thus, depending on the stage of obesity, ROS can be generated by three distinct mechanisms: i.e., NOX4, NOX2, and mitochondria. In this review, we will discuss whether NOX4-, NOX2-, and/or mitochondria-derived ROS is/are causal in the onset of adipocyte insulin resistance as obesity progresses. Moreover, we will review the pathophysiological roles of NOX4, NOX2, and mitochondria-derived ROS on adipose tissue inflammation.

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Obesity and Metabolic Syndrome
Brown Fat and Browning for the Treatment of Obesity and Related Metabolic Disorders
So Hun Kim, Jorge Plutzky
Diabetes Metab J. 2016;40(1):12-21.   Published online January 21, 2016
DOI: https://doi.org/10.4093/dmj.2016.40.1.12
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AbstractAbstract PDFPubReader   

Brown fat is a specialized fat depot that can increase energy expenditure and produce heat. After the recent discovery of the presence of active brown fat in human adults and novel transcription factors controlling brown adipocyte differentiation, the field of the study of brown fat has gained great interest and is rapidly growing. Brown fat expansion and/or activation results in increased energy expenditure and a negative energy balance in mice and limits weight gain. Brown fat is also able to utilize blood glucose and lipid and results in improved glucose metabolism and blood lipid independent of weight loss. Prolonged cold exposure and beta adrenergic agonists can induce browning of white adipose tissue. The inducible brown adipocyte, beige adipocyte evolving by thermogenic activation of white adipose tissue have different origin and molecular signature from classical brown adipocytes but share the characteristics of high mitochondria content, UCP1 expression and thermogenic capacity when activated. Increasing browning may also be an efficient way to increase whole brown fat activity. Recent human studies have shown possibilities that findings in mice can be reproduced in human, making brown fat a good candidate organ to treat obesity and its related disorders.

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Resistin in Rodents and Humans
Hyeong Kyu Park, Rexford S. Ahima
Diabetes Metab J. 2013;37(6):404-414.   Published online December 12, 2013
DOI: https://doi.org/10.4093/dmj.2013.37.6.404
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AbstractAbstract PDFPubReader   

Obesity is characterized by excess accumulation of lipids in adipose tissue and other organs, and chronic inflammation associated with insulin resistance and an increased risk of type 2 diabetes. Obesity, type 2 diabetes, and cardiovascular diseases are major health concerns. Resistin was first discovered as an adipose-secreted hormone (adipokine) linked to obesity and insulin resistance in rodents. Adipocyte-derived resistin is increased in obese rodents and strongly related to insulin resistance. However, in contrast to rodents, resistin is expressed and secreted from macrophages in humans and is increased in inflammatory conditions. Some studies have also suggested an association between increased resistin levels and insulin resistance, diabetes and cardiovascular disease. Genetic studies have provided additional evidence for a role of resistin in insulin resistance and inflammation. Resistin appears to mediate the pathogenesis of atherosclerosis by promoting endothelial dysfunction, vascular smooth muscle cell proliferation, arterial inflammation, and formation of foam cells. Indeed, resistin is predictive of atherosclerosis and poor clinical outcomes in patients with coronary artery disease and ischemic stroke. There is also growing evidence that elevated resistin is associated with the development of heart failure. This review will focus on the biology of resistin in rodents and humans, and evidence linking resistin with type 2 diabetes, atherosclerosis, and cardiovascular disease.

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  • Local and serum levels of adipokines in patients with obesity after periodontal therapy: one‐year follow‐up
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  • INFLUENCE OF RESISTIN ON THE COURSE OF ISCHEMIC HEART DISEASE IN PATIENTS WITH TYPE 2 DIABETES MELLITUS
    A. T. Teplyakov, Sh. D. Akhmedov, T. Ye. Suslova, А. V. Andriyanova, A. V. Kuznetsova, N. V. Protopopova, V. V. Kalyuzhin, O. N. Nasanova
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  • The Resin fromProtium heptaphyllumPrevents High-Fat Diet-Induced Obesity in Mice: Scientific Evidence and Potential Mechanisms
    Karine Maria Martins Bezerra Carvalho, José Delano Barreto Marinho Filho, Tiago Sousa de Melo, Ana Jérsia Araújo, Josiane da Silva Quetz, Maria do Perpétuo Socorro Saldanha da Cunha, Karina Moura de Melo, Armenio Andre de Carvalho Almeida da Silva, Adrian
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    Qingda Hu, Huanran Tan, David M. Irwin, Marc Robinson-Rechavi
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Original Article
An In Vitro Model to Probe the Regulation of Adipocyte Differentiation under Hyperglycemia
Kusampudi Shilpa, Thangaraj Dinesh, Baddireddi Subhadra Lakshmi
Diabetes Metab J. 2013;37(3):176-180.   Published online June 14, 2013
DOI: https://doi.org/10.4093/dmj.2013.37.3.176
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AbstractAbstract PDFPubReader   
Background

The aim of this study was an in vitro investigation of the effect of high glucose concentration on adipogenesis, as prolonged hyperglycemia alters adipocyte differentiation.

Methods

3T3-L1 preadipocytes differentiated in the presence of varying concentrations of glucose (25, 45, 65, 85, and 105 mM) were assessed for adipogenesis using AdipoRed (Lonza) assay. Cell viability and proliferation were measured using MTT reduction and [3H] thymidine incorporation assay. The extent of glucose uptake and glycogen synthesis were measured using radiolabelled 2-deoxy-D-[1-3H] glucose and [14C]-UDP-glucose. The gene level expression was evaluated using reverse transcription-polymerase chain reaction and protein expression was studied using Western blot analysis.

Results

Glucose at 105 mM concentration was observed to inhibit adipogenesis through inhibition of CCAAT-enhancer-binding proteins, sterol regulatory element-binding protein, peroxisome proliferator-activated receptor and adiponectin. High concentration of glucose induced stress by increasing levels of toll-like receptor 4, nuclear factor κB and tumor necrosis factor α thereby generating activated preadipocytes. These cells entered the state of hyperplasia through inhibition of p27 and proliferation was found to increase through activation of protein kinase B via phosphoinositide 3 kinase dependent pathway. This condition inhibited insulin signaling through decrease in insulin receptor β. Although the glucose transporter 4 (GLUT4) protein remained unaltered with the glycogen synthesis inhibited, the cells were found to exhibit an increase in glucose uptake via GLUT1.

Conclusion

Adipogenesis in the presence of 105 mM glucose leads to an uncontrolled proliferation of activated preadipocytes providing an insight towards understanding obesity.

Citations

Citations to this article as recorded by  
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  • Effects of high glucose on caveolin-1 and insulin signaling in 3T3-L1 adipocytes
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  • Pathophysiological role of enhanced bone marrow adipogenesis in diabetic complications
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  • Letter: AnIn VitroModel to Probe the Regulation of Adipocyte Differentiation under Hyperglycemia (Diabetes Metab J2013;37:176-80)
    In-Kyung Jeong
    Diabetes & Metabolism Journal.2013; 37(4): 296.     CrossRef
  • Response: AnIn VitroModel to Probe the Regulation of Adipocyte Differentiation under Hyperglycemia (Diabetes Metab J2013;37:176-80)
    Kusampudi Shilpa, Thangaraj Dinesh, Baddireddi Subhadra Lakshmi
    Diabetes & Metabolism Journal.2013; 37(4): 298.     CrossRef

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