Adipose tissue and age‑dependent insulin resistance: New insights into WAT browning (Review)
- Authors:
- Chuanlong Wu
- Pei Yu
- Ruixin Sun
-
Affiliations: Department of Orthopaedics, Shanghai Key Laboratory for Prevention and Treatment of Bone and Joint Diseases, Shanghai Institute of Traumatology and Orthopaedics, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, P.R. China, State Key Laboratory of Oncogenes and Related Genes, Shanghai Cancer Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200032, P.R. China - Published online on: March 2, 2021 https://doi.org/10.3892/ijmm.2021.4904
- Article Number: 71
-
Copyright: © Wu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Ikemura M, Nishikawa M, Hyoudou K, Kobayashi Y, Yamashita F and Hashida M: Improvement of insulin resistance by removal of systemic hydrogen peroxide by PEGylated catalase in obese mice. Mol Pharm. 7:2069–2076. 2010. View Article : Google Scholar : PubMed/NCBI | |
Guo S: Insulin signaling, resistance, and the metabolic syndrome: Insights from mouse models into disease mechanisms. J Endocrinol. 220:T1–T23. 2014. View Article : Google Scholar | |
Tarantino G, Citro V and Capone D: Nonalcoholic fatty liver disease: A challenge from mechanisms to therapy. J Clin Med. 9:152019. View Article : Google Scholar | |
Czech MP: Insulin action and resistance in obesity and type 2 diabetes. Nat Med. 23:804–814. 2017. View Article : Google Scholar : PubMed/NCBI | |
Qi X, Yun C, Sun L, Xia J, Wu Q, Wang Y, Wang L, Zhang Y, Liang X, Wang L, et al: Gut microbiota-bile acid-interleukin-22 axis orchestrates polycystic ovary syndrome. Nat Med. 25:1225–1233. 2019. View Article : Google Scholar : PubMed/NCBI | |
Petersen MC and Shulman GI: Mechanisms of insulin action and insulin resistance. Physiol Rev. 98:2133–2223. 2018. View Article : Google Scholar : PubMed/NCBI | |
Napoli N, Chandran M, Pierroz DD, Abrahamsen B and Schwartz AV: Mechanisms of diabetes mellitus-induced bone fragility. Nat Rev Endocrinol. 13:208–219. 2017. View Article : Google Scholar | |
Chow HM, Shi M, Cheng A, Gao Y, Chen G, Song X, So RWL, Zhang J and Herrup K: Age-related hyperinsulinemia leads to insulin resistance in neurons and cell-cycle-induced senescence. Nat Neurosci. 22:1806–1819. 2019. View Article : Google Scholar : PubMed/NCBI | |
Barzilai N and Ferrucci L: Insulin resistance and aging: A cause or a protective response? J Gerontol A Biol Sci Med Sci. 67:1329–1331. 2012. View Article : Google Scholar : PubMed/NCBI | |
Rosen ED and Spiegelman BM: Adipocytes as regulators of energy balance and glucose homeostasis. Nature. 444:847–853. 2006. View Article : Google Scholar : PubMed/NCBI | |
Sun R, Wu Y, Hou W, Sun Z, Wang Y, Wei H, Mo W and Yu M: Bromodomain-containing protein 2 induces insulin resistance via the mTOR/Akt signaling pathway and an inflammatory response in adipose tissue. Cell Signal. 30:92–103. 2017. View Article : Google Scholar | |
Zong J, Li S, Wang Y, Mo W, Sun R and Yu M: Bromodomain-containing protein 2 promotes lipolysis via ERK/HSL signalling pathway in white adipose tissue of mice. Gen Comp Endocrinol. 281:105–116. 2019. View Article : Google Scholar : PubMed/NCBI | |
Bapat SP, Myoung Suh J, Fang S, Liu S, Zhang Y, Cheng A, Zhou C, Liang Y, LeBlanc M, Liddle C, et al: Depletion of fat-resident Treg cells prevents age-associated insulin resistance. Nature. 528:137–141. 2015. View Article : Google Scholar : PubMed/NCBI | |
Sierra Rojas JX, Garcia-San Frutos M, Horrillo D, Lauzurica N, Oliveros E, Carrascosa JM, Fernández-Agulló T and Ros M: Differential development of inflammation and insulin resistance in different adipose tissue depots along aging in wistar rats: Effects of caloric restriction. J Gerontol A Biol Sci Med Sci. 71:310–322. 2016. View Article : Google Scholar | |
Park A, Kim WK and Bae KH: Distinction of white, beige and brown adipocytes derived from mesenchymal stem cells. World J Stem Cells. 6:33–42. 2014. View Article : Google Scholar : PubMed/NCBI | |
Giralt M and Villarroya F: White, brown, beige/brite: Different adipose cells for different functions? Endocrinology. 154:2992–3000. 2013. View Article : Google Scholar : PubMed/NCBI | |
Palmer AK and Kirkland JL: Aging and adipose tissue: Potential interventions for diabetes and regenerative medicine. Exp Gerontol. 86:97–105. 2016. View Article : Google Scholar : PubMed/NCBI | |
Madonna R and De Caterina R: In vitro neovasculogenic potential of resident adipose tissue precursors. Am J Physiol Cell Physiol. 295:C1271–1280. 2008. View Article : Google Scholar : PubMed/NCBI | |
Chon SH and Pappas A: Differentiation and characterization of human facial subcutaneous adipocytes. Adipocyte. 4:13–21. 2015. View Article : Google Scholar : PubMed/NCBI | |
Frontini A and Cinti S: Distribution and development of brown adipocytes in the murine and human adipose organ. Cell Metab. 11:253–256. 2010. View Article : Google Scholar : PubMed/NCBI | |
Cedikova M, Kripnerová M, Dvorakova J, Pitule P, Grundmanova M, Babuska V, Mullerova D and Kuncova J: Mitochondria in white, brown, and beige adipocytes. Stem Cells Int. 2016:60673492016. View Article : Google Scholar : PubMed/NCBI | |
Ye L, Wu J, Cohen P, Kazak L, Khandekar MJ, Jedrychowski MP, Zeng X, Gygi SP and Spiegelman BM: Fat cells directly sense temperature to activate thermogenesis. Proc Natl Acad Sci USA. 110:12480–12485. 2013. View Article : Google Scholar : PubMed/NCBI | |
Cypess AM, White AP, Vernochet C, Schulz TJ, Xue R, Sass CA, Huang TL, Roberts-Toler C, Weiner LS, Sze C, et al: Anatomical localization, gene expression profiling and functional characterization of adult human neck brown fat. Nat Med. 19:635–639. 2013. View Article : Google Scholar : PubMed/NCBI | |
Mailloux RJ and Harper ME: Uncoupling proteins and the control of mitochondrial reactive oxygen species production. Free Radic Biol Med. 51:1106–1115. 2011. View Article : Google Scholar : PubMed/NCBI | |
Wu J, Boström P, Sparks LM, Ye L, Choi JH, Giang AH, Khandekar M, Virtanen KA, Nuutila P, Schaart G, et al: Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell. 150:366–376. 2012. View Article : Google Scholar : PubMed/NCBI | |
Pyrzak B, Demkow U and Kucharska AM: Brown adipose tissue and browning agents: Irisin and FGF21 in the development of obesity in children and adolescents. Adv Exp Med Biol. 866:25–34. 2015. View Article : Google Scholar : PubMed/NCBI | |
Okla M, Ha JH, Temel RE and Chung S: BMP7 drives human adipogenic stem cells into metabolically active beige adipocytes. Lipids. 50:111–120. 2015. View Article : Google Scholar : | |
Palmer AK, Tchkonia T, LeBrasseur NK, Chini EN, Xu M and Kirkland JL: Cellular senescence in type 2 diabetes: A therapeutic opportunity. Diabetes. 64:2289–2298. 2015. View Article : Google Scholar : PubMed/NCBI | |
Zoico E, Rubele S, De Caro A, Nori N, Mazzali G, Fantin F, Rossi A and Zamboni M: Brown and beige adipose tissue and aging. Front Endocrinol (Lausanne). 10:3682019. View Article : Google Scholar | |
Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz BA, Bergmann O, Blomqvist L, Hoffstedt J, Näslund E, Britton T, et al: Dynamics of fat cell turnover in humans. Nature. 453:783–787. 2008. View Article : Google Scholar : PubMed/NCBI | |
Eckel-Mahan K, Ribas Latre A and Kolonin MG: Adipose stromal cell expansion and exhaustion: Mechanisms and consequences. Cells. 9:8632020. View Article : Google Scholar : | |
Tchkonia T, Morbeck DE, Von Zglinicki T, Van Deursen J, Lustgarten J, Scrable H, Khosla S, Jensen MD and Kirkland JL: Fat tissue, aging, and cellular senescence. Aging Cell. 9:667–684. 2010. View Article : Google Scholar : PubMed/NCBI | |
Caso G, McNurlan MA, Mileva I, Zemlyak A, Mynarcik DC and Gelato MC: Peripheral fat loss and decline in adipogenesis in older humans. Metabolism. 62:337–340. 2013. View Article : Google Scholar | |
Bukowska J, Frazier T, Smith S, Brown T, Bender R, McCarthy M, Wu X, Bunnell BA and Gimble JM: Bone marrow adipocyte developmental origin and biology. Curr Osteoporos Rep. 16:312–319. 2018. View Article : Google Scholar : PubMed/NCBI | |
Ahmed AS, Sheng MH, Wasnik S, Baylink DJ and Lau KW: Effect of aging on stem cells. World J Exp Med. 7:1–10. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kirkland JL, Tchkonia T, Pirtskhalava T, Han J and Karagiannides I: Adipogenesis and aging: Does aging make fat go MAD? Exp Gerontol. 37:757–767. 2002. View Article : Google Scholar : PubMed/NCBI | |
Gill LE, Bartels SJ and Batsis JA: Weight management in older adults. Curr Obes Rep. 4:379–388. 2015. View Article : Google Scholar : PubMed/NCBI | |
Sepe A, Tchkonia T, Thomou T, Zamboni M and Kirkland JL: Aging and regional differences in fat cell progenitors-a mini-review. Gerontology. 57:66–75. 2011. View Article : Google Scholar | |
Pischon T, Boeing H, Hoffmann K, Bergmann M, Schulze MB, Overvad K, van der Schouw YT, Spencer E, Moons KG, Tjønneland A, et al: General and abdominal adiposity and risk of death in Europe. N Engl J Med. 359:2105–2120. 2008. View Article : Google Scholar : PubMed/NCBI | |
Preis SR, Massaro JM, Robins SJ, Hoffmann U, Vasan RS, Irlbeck T, Meigs JB, Sutherland P, D'Agostino RB Sr, O'Donnell CJ and Fox CS: Abdominal subcutaneous and visceral adipose tissue and insulin resistance in the Framingham heart study. Obesity (Silver Spring). 18:2191–2198. 2010. View Article : Google Scholar | |
Paradis ME, Hogue MO, Mauger JF, Couillard C, Couture P, Bergeron N and Lamarche B: Visceral adipose tissue accumulation, secretory phospholipase A2-IIA and atherogenecity of LDL. Int J Obes (Lond). 30:1615–1622. 2006. View Article : Google Scholar | |
Giorgino F: Adipose tissue function and dysfunction: Organ cross talk and metabolic risk. Am J Physiol Endocrinol Metab. 297:E975–E976. 2009. View Article : Google Scholar : PubMed/NCBI | |
Capurso C and Capurso A: From excess adiposity to insulin resistance: The role of free fatty acids. Vascul Pharmacol. 57:91–97. 2012. View Article : Google Scholar : PubMed/NCBI | |
Ibrahim MM: Subcutaneous and visceral adipose tissue: Structural and functional differences. Obes Rev. 11:11–18. 2010. View Article : Google Scholar | |
Niu Z, Lin N, Gu R, Sun Y and Feng Y: Associations between insulin resistance, free fatty acids, and oocyte quality in polycystic ovary syndrome during in vitro fertilization. J Clin Endocrinol Metab. 99:E2269–E2276. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chait A and den Hartigh LJ: Adipose tissue distribution, inflammation and its metabolic consequences, including diabetes and cardiovascular disease. Front Cardiovasc Med. 7:222020. View Article : Google Scholar : PubMed/NCBI | |
Coppé JP, Patil CK, Rodier F, Sun Y, Muñoz DP, Goldstein J, Nelson PS, Desprez PY and Campisi J: Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 6:2853–2868. 2008. View Article : Google Scholar : PubMed/NCBI | |
Xu M, Palmer AK, Ding H, Weivoda MM, Pirtskhalava T, White TA, Sepe A, Johnson KO, Stout MB, Giorgadze N, et al: Targeting senescent cells enhances adipogenesis and metabolic function in old age. Elife. 4:e129972015. View Article : Google Scholar : PubMed/NCBI | |
Xu M, Tchkonia T, Ding H, Ogrodnik M, Lubbers ER, Pirtskhalava T, White TA, Johnson KO, Stout MB, Mezera V, et al: JAK inhibition alleviates the cellular senescence-associated secretory phenotype and frailty in old age. Proc Natl Acad Sci USA. 112:E6301–E6310. 2015. View Article : Google Scholar : PubMed/NCBI | |
Park SS and Seo YK: Excess accumulation of lipid impairs insulin sensitivity in skeletal muscle. Int J Mol Sci. 21:19492020. View Article : Google Scholar : | |
Pincus Z, Smith-Vikos T and Slack FJ: MicroRNA predictors of longevity in caenorhabditis elegans. PLoS Genet. 7:e10023062011. View Article : Google Scholar : PubMed/NCBI | |
Mori MA, Raghavan P, Thomou T, Boucher J, Robida-Stubbs S, Macotela Y, Russell SJ, Kirkland JL, Blackwell TK and Kahn CR: Role of microRNA processing in adipose tissue in stress defense and longevity. Cell Metab. 16:336–347. 2012. View Article : Google Scholar : PubMed/NCBI | |
Mori MA, Thomou T, Boucher J, Lee KY, Lallukka S, Kim JK, Torriani M, Yki-Järvinen H, Grinspoon SK, Cypess AM and Kahn CR: Altered miRNA processing disrupts brown/white adipocyte determination and associates with lipodystrophy. J Clin Invest. 124:3339–3351. 2014. View Article : Google Scholar : PubMed/NCBI | |
Mori MA, Ludwig RG, Garcia-Martin R, Brandão BB and Kahn CR: Extracellular miRNAs: From biomarkers to mediators of physiology and disease. Cell Metab. 30:656–673. 2019. View Article : Google Scholar : PubMed/NCBI | |
Fontes-Carvalho R, Fontes-Oliveira M, Sampaio F, Mancio J, Bettencourt N, Teixeira M, Rocha Gonçalves F, Gama V and Leite-Moreira A: Influence of epicardial and visceral fat on left ventricular diastolic and systolic functions in patients after myocardial infarction. Am J Cardiol. 114:1663–1669. 2014. View Article : Google Scholar : PubMed/NCBI | |
Mancuso P and Bouchard B: The impact of aging on adipose function and adipokine synthesis. Front Endocrinol (Lausanne). 10:1372019. View Article : Google Scholar | |
Chandrasekar B, Boylston WH, Venkatachalam K, Webster NJ, Prabhu SD and Valente AJ: Adiponectin blocks interleukin-18-mediated endothelial cell death via APPL1-dependent AMP-activated protein kinase (AMPK) activation and IKK/NF-kappaB/PTEN suppression. J Biol Chem. 283:24889–24898. 2008. View Article : Google Scholar : PubMed/NCBI | |
Jura M and Kozak LP: Obesity and related consequences to ageing. Age (Dordr). 38:232016. View Article : Google Scholar | |
Koh KK, Quon MJ, Han SH, Lee Y, Ahn JY, Kim SJ, Koh Y and Shin EK: Simvastatin improves flow-mediated dilation but reduces adiponectin levels and insulin sensitivity in hypercholesterolemic patients. Diabetes Care. 31:776–782. 2008. View Article : Google Scholar : PubMed/NCBI | |
Isobe T, Saitoh S, Takagi S, Takeuchi H, Chiba Y, Katoh N and Shimamoto K: Influence of gender, age and renal function on plasma adiponectin level: The Tanno and Sobetsu study. Eur J Endocrinol. 153:91–98. 2005. View Article : Google Scholar : PubMed/NCBI | |
Takenouchi Y, Kobayashi T, Matsumoto T and Kamata K: Gender differences in age-related endothelial function in the murine aorta. Atherosclerosis. 206:397–404. 2009. View Article : Google Scholar : PubMed/NCBI | |
Li JB, Nishida M, Kaimoto K, Asakawa A, Chaolu H, Cheng KC, Li YX, Terashi M, Koyama KI, Amitani H, et al: Effects of aging on the plasma levels of nesfatin-1 and adiponectin. Biomed Rep. 2:152–156. 2014. View Article : Google Scholar : PubMed/NCBI | |
Nigro E, Scudiero O, Monaco ML, Palmieri A, Mazzarella G, Costagliola C, Bianco A and Daniele A: New insight into adiponectin role in obesity and obesity-related diseases. Biomed Res Int. 2014:6589132014. View Article : Google Scholar : PubMed/NCBI | |
Carter S, Caron A, Richard D and Picard F: Role of leptin resistance in the development of obesity in older patients. Clin Interv Aging. 8:829–844. 2013.PubMed/NCBI | |
Katsiki N, Mikhailidis DP and Banach M: Leptin, cardiovascular diseases and type 2 diabetes mellitus. Acta Pharmacol Sin. 39:1176–1188. 2018. View Article : Google Scholar : PubMed/NCBI | |
Doherty GH: Obesity and the ageing brain: Could leptin play a role in neurodegeneration? Curr Gerontol Geriatr Res. 2011:7081542011. View Article : Google Scholar : PubMed/NCBI | |
Lehrke M, Reilly MP, Millington SC, Iqbal N, Rader DJ and Lazar MA: An inflammatory cascade leading to hyperresistinemia in humans. PLoS Med. 1:e452004. View Article : Google Scholar : PubMed/NCBI | |
Gencer B, Auer R, de Rekeneire N, Butler J, Kalogeropoulos A, Bauer DC, Kritchevsky SB, Miljkovic I, Vittinghoff E, Harris T and Rodondi N: Association between resistin levels and cardiovascular disease events in older adults: The health, aging and body composition study. Atherosclerosis. 245:181–186. 2016. View Article : Google Scholar : PubMed/NCBI | |
Rea IM, Gibson DS, McGilligan V, McNerlan SE, Alexander HD and Ross OA: Age and age-related diseases: Role of inflammation triggers and cytokines. Front Immunol. 9:5862018. View Article : Google Scholar : PubMed/NCBI | |
de Heredia FP, Gómez-Martinez S and Marcos A: Obesity, inflammation and the immune system. Proc Nutr Soc. 71:332–338. 2012. View Article : Google Scholar : PubMed/NCBI | |
Lumeng CN, Liu J, Geletka L, Delaney C, Delproposto J, Desai A, Oatmen K, Martinez-Santibanez G, Julius A, Garg S and Yung RL: Aging is associated with an increase in T cells and inflammatory macrophages in visceral adipose tissue. J Immunol. 187:6208–6216. 2011. View Article : Google Scholar : PubMed/NCBI | |
Lumeng CN, Bodzin JL and Saltiel AR: Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest. 117:175–184. 2007. View Article : Google Scholar : PubMed/NCBI | |
Russo L and Lumeng CN: Properties and functions of adipose tissue macrophages in obesity. Immunology. 155:407–417. 2018. View Article : Google Scholar : PubMed/NCBI | |
Olefsky JM and Glass CK: Macrophages, inflammation, and insulin resistance. Annu Rev Physiol. 72:219–246. 2010. View Article : Google Scholar : PubMed/NCBI | |
Fang W, Deng Z, Benadjaoud F, Yang D, Yang C and Shi GP: Regulatory T cells promote adipocyte beiging in subcutaneous adipose tissue. FASEB J. 34:9755–9770. 2020. View Article : Google Scholar : PubMed/NCBI | |
Schenk S, Saberi M and Olefsky JM: Insulin sensitivity: Modulation by nutrients and inflammation. J Clin Invest. 118:2992–3002. 2008. View Article : Google Scholar : PubMed/NCBI | |
Lumeng CN, Deyoung SM and Saltiel AR: Macrophages block insulin action in adipocytes by altering expression of signaling and glucose transport proteins. Am J Physiol Endocrinol Metab. 292:E166–E174. 2007. View Article : Google Scholar | |
Gustafson B and Smith U: Cytokines promote Wnt signaling and inflammation and impair the normal differentiation and lipid accumulation in 3T3-L1 preadipocytes. J Biol Chem. 281:9507–9516. 2006. View Article : Google Scholar : PubMed/NCBI | |
Woo CY, Jang JE, Lee SE, Koh EH and Lee KU: Mitochondrial dysfunction in adipocytes as a primary cause of adipose tissue inflammation. Diabetes Metab J. 43:247–256. 2019. View Article : Google Scholar : PubMed/NCBI | |
van de Ven RAH, Santos D and Haigis MC: Mitochondrial sirtuins and molecular mechanisms of aging. Trends Mol Med. 23:320–331. 2017. View Article : Google Scholar : PubMed/NCBI | |
Tao Y, Huang C, Huang Y, Hong L, Wang H, Zhou Z and Qiu Y: SIRT4 suppresses inflammatory responses in human umbilical vein endothelial cells. Cardiovasc Toxicol. 15:217–223. 2015. View Article : Google Scholar | |
Argmann C and Auwerx J: Insulin secretion: SIRT4 gets in on the act. Cell. 126:837–839. 2006. View Article : Google Scholar : PubMed/NCBI | |
Bartelt A, Bruns OT, Reimer R, Hohenberg H, Ittrich H, Peldschus K, Kaul MG, Tromsdorf UI, Weller H, Waurisch C, et al: Brown adipose tissue activity controls triglyceride clearance. Nat Med. 17:200–205. 2011. View Article : Google Scholar : PubMed/NCBI | |
Yoneshiro T, Aita S, Matsushita M, Okamatsu-Ogura Y, Kameya T, Kawai Y, Miyagawa M, Tsujisaki M and Saito M: Age-related decrease in cold-activated brown adipose tissue and accumulation of body fat in healthy humans. Obesity (Silver Spring). 19:1755–1760. 2011. View Article : Google Scholar | |
Tan CY, Virtue S, Bidault G, Dale M, Hagen R, Griffin JL and Vidal-Puig A: Brown adipose tissue thermogenic capacity is regulated by Elovl6. Cell Rep. 13:2039–2047. 2015. View Article : Google Scholar : PubMed/NCBI | |
Rogers NH, Landa A, Park S and Smith RG: Aging leads to a programmed loss of brown adipocytes in murine subcutaneous white adipose tissue. Aging Cell. 11:1074–1083. 2012. View Article : Google Scholar : PubMed/NCBI | |
Valle A, Guevara R, Garcia-Palmer FJ, Roca P and Oliver J: Caloric restriction retards the age-related decline in mitochondrial function of brown adipose tissue. Rejuvenation Res. 11:597–604. 2008. View Article : Google Scholar : PubMed/NCBI | |
Detmer SA and Chan DC: Functions and dysfunctions of mitochondrial dynamics. Nat Rev Mol Cell Biol. 8:870–879. 2007. View Article : Google Scholar : PubMed/NCBI | |
Lin AL, Coman D, Jiang L, Rothman DL and Hyder F: Caloric restriction impedes age-related decline of mitochondrial function and neuronal activity. J Cereb Blood Flow Metab. 34:1440–1443. 2014. View Article : Google Scholar : PubMed/NCBI | |
Fitzgibbons TP, Kogan S, Aouadi M, Hendricks GM, Straubhaar J and Czech MP: Similarity of mouse perivascular and brown adipose tissues and their resistance to diet-induced inflammation. Am J Physiol Heart Circ Physiol. 301:H1425–H1437. 2011. View Article : Google Scholar : PubMed/NCBI | |
Villarroya F, Cereijo R, Villarroya J, Gavaldà-Navarro A and Giralt M: Toward an understanding of how immune cells control brown and beige adipobiology. Cell Metab. 27:954–961. 2018. View Article : Google Scholar : PubMed/NCBI | |
Lorenzo M, Fernández-Veledo S, Vila-Bedmar R, Garcia-Guerra L, De Alvaro C and Nieto-Vazquez I: Insulin resistance induced by tumor necrosis factor-alpha in myocytes and brown adipocytes. J Anim Sci. 86:E94–E104. 2008. View Article : Google Scholar | |
Amitani M, Amitani H, Cheng KC, Kairupan TS, Sameshima N, Shimoshikiryo I, Mizuma K, Rokot NT, Nerome Y, Owaki T, et al: The role of ghrelin and ghrelin signaling in aging. Int J Mol Sci. 18:15112017. View Article : Google Scholar : | |
Lee JY, Takahashi N, Yasubuchi M, Kim YI, Hashizaki H, Kim MJ, Sakamoto T, Goto T and Kawada T: Triiodothyronine induces UCP-1 expression and mitochondrial biogenesis in human adipocytes. Am J Physiol Cell Physiol. 302:C463–C472. 2012. View Article : Google Scholar | |
Weiner J, Hankir M, Heiker JT, Fenske W and Krause K: Thyroid hormones and browning of adipose tissue. Mol Cell Endocrinol. 458:156–159. 2017. View Article : Google Scholar : PubMed/NCBI | |
Gustafson B, Hedjazifar S, Gogg S, Hammarstedt A and Smith U: Insulin resistance and impaired adipogenesis. Trends Endocrinol Metab. 26:193–200. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kajimura S, Seale P, Tomaru T, Erdjument-Bromage H, Cooper MP, Ruas JL, Chin S, Tempst P, Lazar MA and Spiegelman BM: Regulation of the brown and white fat gene programs through a PRDM16/CtBP transcriptional complex. Genes Dev. 22:1397–1409. 2008. View Article : Google Scholar : PubMed/NCBI | |
Becerril S, Gómez-Ambrosi J, Martin M, Moncada R, Sesma P, Burrell MA and Frühbeck G: Role of PRDM16 in the activation of brown fat programming. Relevance to the development of obesity. Histol Histopathol. 28:1411–1425. 2013.PubMed/NCBI | |
Khanh VC, Zulkifli AF, Tokunaga C, Yamashita T, Hiramatsu Y and Ohneda O: Aging impairs beige adipocyte differentiation of mesenchymal stem cells via the reduced expression of Sirtuin 1. Biochem Biophys Res Commun. 500:682–690. 2018. View Article : Google Scholar : PubMed/NCBI | |
Boström P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, Rasbach KA, Boström EA, Choi JH, Long JZ, et al: A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature. 481:463–468. 2012. View Article : Google Scholar | |
Niranjan SB, Belwalkar SV, Tambe S, Venkataraman K and Mookhtiar KA: Recombinant irisin induces weight loss in high fat DIO mice through increase in energy consumption and thermogenesis. Biochem Biophys Res Commun. 519:422–429. 2019. View Article : Google Scholar : PubMed/NCBI | |
Shankar K, Kumar D, Gupta S, Varshney S, Rajan S, Srivastava A, Gupta A, Gupta AP, Vishwakarma AL, Gayen JR and Gaikwad AN: Role of brown adipose tissue in modulating adipose tissue inflammation and insulin resistance in high-fat diet fed mice. Eur J Pharmacol. 854:354–364. 2019. View Article : Google Scholar : PubMed/NCBI | |
Wang W and Seale P: Control of brown and beige fat development. Nat Rev Mol Cell Biol. 17:691–702. 2016. View Article : Google Scholar : PubMed/NCBI | |
He L, Tang M, Xiao T, Liu H, Liu W, Li G, Zhang F, Xiao Y, Zhou Z, Liu F and Hu F: Obesity-associated miR-199a/214 cluster inhibits adipose browning via PRDM16-PGC-1α transcriptional network. Diabetes. 67:2585–2600. 2018. View Article : Google Scholar : PubMed/NCBI | |
Yao L, Cui X, Chen Q, Yang X, Fang F, Zhang J, Liu G, Jin W and Chang Y: Cold-inducible SIRT6 regulates thermogenesis of brown and beige fat. Cell Rep. 20:641–654. 2017. View Article : Google Scholar : PubMed/NCBI | |
Gollisch KS, Brandauer J, Jessen N, Toyoda T, Nayer A, Hirshman MF and Goodyear LJ: Effects of exercise training on subcutaneous and visceral adipose tissue in normal- and high-fat diet-fed rats. Am J Physiol Endocrinol Metab. 297:E495–E504. 2009. View Article : Google Scholar : PubMed/NCBI | |
Knudsen JG, Murholm M, Carey AL, Biensø RS, Basse AL, Allen TL, Hidalgo J, Kingwell BA, Febbraio MA, Hansen JB and Pilegaard H: Role of IL-6 in exercise training- and cold-induced UCP1 expression in subcutaneous white adipose tissue. PLoS One. 9:e849102014. View Article : Google Scholar : PubMed/NCBI | |
Thirupathi A, da Silva Pieri BL, Queiroz JAMP, Rodrigues MS, de Bem Silveira G, de Souza DR, Luciano TF, Silveira PCL and De Souza CT: Strength training and aerobic exercise alter mitochondrial parameters in brown adipose tissue and equally reduce body adiposity in aged rats. J Physiol Biochem. 75:101–108. 2019. View Article : Google Scholar : PubMed/NCBI | |
Vosselman MJ, Hoeks J, Brans B, Pallubinsky H, Nascimento EB, van der Lans AA, Broeders EP, Mottaghy FM, Schrauwen P and van Marken Lichtenbelt WD: Low brown adipose tissue activity in endurance-trained compared with lean sedentary men. Int J Obes (Lond). 39:1696–1702. 2015. View Article : Google Scholar | |
Orava J, Nuutila P, Lidell ME, Oikonen V, Noponen T, Viljanen T, Scheinin M, Taittonen M, Niemi T, Enerbäck S and Virtanen KA: Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab. 14:272–279. 2011. View Article : Google Scholar : PubMed/NCBI | |
Nirengi S, Homma T, Inoue N, Sato H, Yoneshiro T, Matsushita M, Kameya T, Sugie H, Tsuzaki K, Saito M, et al: Assessment of human brown adipose tissue density during daily ingestion of thermogenic capsinoids using near-infrared time-resolved spectroscopy. J Biomed Opt. 21:0913052016. View Article : Google Scholar : PubMed/NCBI | |
Kim SM, Jung YJ, Kwon ON, Cha KH, Um BH, Chung D and Pan CH: A potential commercial source of fucoxanthin extracted from the microalga Phaeodactylum tricornutum. Appl Biochem Biotechnol. 166:1843–1855. 2012. View Article : Google Scholar : PubMed/NCBI | |
Bonet ML, Ribot J, Galmés S, Serra F and Palou A: Carotenoids and carotenoid conversion products in adipose tissue biology and obesity: Pre-clinical and human studies. Biochim Biophys Acta Mol Cell Biol Lipids. 1865:1586762020. View Article : Google Scholar : PubMed/NCBI | |
Hilgendorf KI, Johnson CT, Mezger A, Rice SL, Norris AM, Demeter J, Greenleaf WJ, Reiter JF, Kopinke D and Jackson PK: Omega-3 fatty acids activate ciliary FFAR4 to control adipogenesis. Cell. 179:1289–1305.e21. 2019. View Article : Google Scholar : PubMed/NCBI | |
Jiménez-Aranda A, Fernández-Vázquez G, Campos D, Tassi M, Velasco-Perez L, Tan DX, Reiter RJ and Agil A: Melatonin induces browning of inguinal white adipose tissue in Zucker diabetic fatty rats. J Pineal Res. 55:416–423. 2013. View Article : Google Scholar : PubMed/NCBI | |
Zhang Y, Goldman S, Baerga R, Zhao Y, Komatsu M and Jin S: Adipose-specific deletion of autophagy-related gene 7 (atg7) in mice reveals a role in adipogenesis. Proc Natl Acad Sci USA. 106:19860–19865. 2009. View Article : Google Scholar : PubMed/NCBI | |
Martinez-Lopez N, Athonvarangkul D, Sahu S, Coletto L, Zong H, Bastie CC, Pessin JE, Schwartz GJ and Singh R: Autophagy in Myf5+ progenitors regulates energy and glucose homeostasis through control of brown fat and skeletal muscle development. EMBO Rep. 14:795–803. 2013. View Article : Google Scholar : PubMed/NCBI | |
Tran CM, Mukherjee S, Ye L, Frederick DW, Kissig M, Davis JG, Lamming DW, Seale P and Baur JA: Rapamycin blocks induction of the thermogenic program in white adipose tissue. Diabetes. 65:927–941. 2016. View Article : Google Scholar : PubMed/NCBI | |
Liu D, Bordicchia M, Zhang C, Fang H, Wei W, Li JL, Guilherme A, Guntur K, Czech MP and Collins S: Activation of mTORC1 is essential for β-adrenergic stimulation of adipose browning. J Clin Invest. 126:1704–1716. 2016. View Article : Google Scholar : PubMed/NCBI | |
Wada S, Neinast M, Jang C, Ibrahim YH, Lee G, Babu A, Li J, Hoshino A, Rowe GC, Rhee J, et al: The tumor suppressor FLCN mediates an alternate mTOR pathway to regulate browning of adipose tissue. Genes Dev. 30:2551–2564. 2016. View Article : Google Scholar : PubMed/NCBI |