Adipose tissue: its colors and versatility

Authors

  • Helena Fonseca Raposo Instituto de biologia, OCRC - Obesity and Comorbidities Research Center. Universidade Estadual de Campinas – SP https://orcid.org/0000-0003-3885-8785

DOI:

https://doi.org/10.34019/1982-8047.2020.v46.31268

Keywords:

Adipose Tissue, Adipocyte, Lipolysis, Thermogenesis, Obesity

Abstract

Introduction: The adipose tissue and adipocytes have been widely studied due to its relationship with obesity. Objective: Identify historical and relevant topics about the adipose tissue metabolic function, especially regarding its potential as therapeutical target handling metabolic diseases. Materials and Methods: A narrative review was done after a search with no date restriction in the PubMed database. Results: The demonstration of a termogenic adipose tissue existence in human adults, promoted a great interest in the adipose tissue study, due it potential as therapeutic target do treat obesity. The plasticity and versality of adipose tissue are evidenced by several adipocytes investigated nowadays. The classically known white adipose tissue (WAT) and brown adipose tissue (BAT), the recent discovered: beige/brite, also known as inducible BAT; besides the pink adipocyte and bone marrow adipocytes. Regarding the functional differences, the WAT is responsible for energy storage as lipids, thus directly related to obesity. While BAT can increase metabolic rate and reduce obesity, because of its high oxidative capacity. In this context, the beige adipose tissue has double function: Behave as WAT and store energy excess as lipids or when stimulated (cold exposure, simphathetic stimulation), the beige adipose tissue termogenic program is activated and UCP1 (Uncoupling Protein-1) expression is elevated to same level as BAT, what increases energy dissipation. The adipose tissue shows its versality adapting to distinctive metabolic conditions, in specific conditions as lactation, hematopoiesis, by its action as endocrine organ or energy metabolism modulation. Conclusion: Thus, the understanding of functional and molecular adipocyte features, enable to identify new treatments for metabolic disorders.

Downloads

Download data is not yet available.

References

World Halth Organization. Obesity and overweight [internet]. [citado em 2020 Jul 02]. Disponível em: https://www.who.int/westernpacific/health-topics/obesity.

Kopelman PG. Obesity as a medical problem. Nature. 2000; 404:635-43.

Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue. Nature. 1994; 372:425-32.

Mattu HS, Randeva HS. Role of adipokines in cardiovascular disease. J Endocrinol. 2013; 216:T17-36.

Graf C, Ferrari N. Metabolic health-the role of adipo-myokines. Int J Mol Sci. 2019; 20. doi:10.3390/ijms20246159.

Knebel B, Fahlbusch P, Poschmann G, Dille M, Wahlers N, Stühler K et al. Adipokinome signatures in obese mouse models reflect adipose tissue health and are associated with serum lipid composition. Int J Mol Sci. 2019; 20. doi:10.3390/ijms20102559.

Cinti S. The adipose organ at a glance. Dis Model Mech. 2012; 5: 588-94.

Cinti S. Transdifferentiation properties of adipocytes in the adipose organ. Am J Physiol Endocrinol Metab. 2009; 297:E977-986.

Henry SL, Bensley JG, Wood-Bradley RJ, Cullen-McEwen LA, Bertram JF, Armitage JA. White adipocytes: more than just fat depots. The International Journal of Biochemistry & Cell Biology. 2012; 44:435-40.

Koppen A, Kalkhoven E. Brown vs white adipocytes: the PPARgamma coregulator story. FEBS Lett. 2010; 584:3250-9.

Kajimura S, Seale P, Tomaru T, Erdjument-Bromage H, Cooper MP, Ruas JL et al. Regulation of the brown and white fat gene programs through a PRDM16/CtBP transcriptional complex. Genes Dev. 2008; 22:1397-1409.

Lean ME, James WP, Jennings G, Trayhurn P. Brown adipose tissue uncoupling protein content in human infants, children and adults. Clin Sci. 1986; 71: 291-7.

Heaton JM. The distribution of brown adipose tissue in the human. J Anat. 1972; 112:35-9.

Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med. 2009; 360:1509-17.

Saito M, Okamatsu-Ogura Y, Matsushita M, Watanabe K, Yoneshiro T, Nio-Kobayashi J et al. High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes. 2009; 58:1526-31.

Enerbäck S. Human brown adipose tissue. Cell Metab. 2010; 11:248-52.

Giordano A, Smorlesi A, Frontini A, Barbatelli G, Cinti S. White, brown and pink adipocytes: the extraordinary plasticity of the adipose organ. Eur J Endocrinol. 2014; 170:R159-171.

Cinti S. Pink Adipocytes. Trends Endocrinol Metab. 2018; 29:651-66.

Tavassoli M, Crosby WH. Bone marrow histogenesis: a comparison of fatty and red marrow. Science. 1970; 169:291-3.

Gimble JM, Robinson CE, Wu X, Kelly KA, Rodriguez BR, Kliewer SA et al. Peroxisome proliferator-activated receptor-gamma activation by thiazolidinediones induces adipogenesis in bone marrow stromal cells. Mol Pharmacol. 1996; 50:1087-94.

Paula FJA, Rosen CJ. Marrow adipocytes: origin, structure, and function. Annu Rev Physiol. 2020; 82:461-84.

Laharrague P, Larrouy D, Fontanilles AM, Truel N, Campfield A, Tenenbaum R et al. High expression of leptin by human bone marrow adipocytes in primary culture. FASEB J. 1998; 12:747-52.

Rodeheffer MS, Birsoy K, Friedman JM. Identification of white adipocyte progenitor cells in vivo. Cell. 2008; 135:240-9.

Cawthorn WP, Scheller EL, Parlee SD, Pham HA, Learman BS, Redshaw CMH et al. Expansion of bone marrow adipose tissue during caloric restriction is associated with increased circulating glucocorticoids and not with hypoleptinemia. Endocrinology. 2016; 157:508-21.

Araújo IM, Salmon CEG, Nahas AK, Nogueira-Barbosa MH, Elias J, Paula FJA. Marrow adipose tissue spectrum in obesity and type 2 diabetes mellitus. Eur J Endocrinol. 2017; 176:21-30.

Zechner R, Kienesberger PC, Haemmerle G, Zimmermann R, Lass A. Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores. J Lipid Res. 2009; 50:3-21.

Holm C. Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Biochem Soc Trans. 2003; 31:1120-4.

Zimmermann R, Strauss JG, Haemmerle G, Schoiswohl G, Birner-Gruenberger R, Riederer M et al. Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science. 2004; 306:1383-6.

Villena JA, Roy S, Sarkadi-Nagy E, Kim K-H, Sul HS. Desnutrin, an adipocyte gene encoding a novel patatin domain-containing protein, is induced by fasting and glucocorticoids: ectopic expression of desnutrin increases triglyceride hydrolysis. J Biol Chem. 2004; 279:47066-75.

Jenkins CM, Mancuso DJ, Yan W, Sims HF, Gibson B, Gross RW. Identification, cloning, expression, and purification of three novel human calcium-independent phospholipase A2 family members possessing triacylglycerol lipase and acylglycerol transacylase activities. J Biol Chem. 2004; 279:48968-75.

Okazaki H, Osuga J-I, Tamura Y, Yahagi N, Tomita S, Shionoiri F et al. Lipolysis in the absence of hormone-sensitive lipase: evidence for a common mechanism regulating distinct lipases. Diabetes. 2002; 51:3368-75.

Ahmadian M, Duncan RE, Varady KA, Frasson D, Hellerstein MK, Birkenfeld AL et al. Adipose overexpression of desnutrin promotes fatty acid use and attenuates diet-induced obesity. Diabetes. 2009; 58:855-66.

Ahmadian M, Abbott MJ, Tang T, Hudak CSS, Kim Y, Bruss M et al. Desnutrin/ATGL is regulated by AMPK and is required for a brown adipose phenotype. Cell Metab. 2011; 13:739-48.

Nelson DL, Cox MC. Lehninger: principles of biochemistry. 4th. New York: W. H. Freeman & Co.; 2004.

Gimeno RE, Dembski M, Weng X, Deng N, Shyjan AW, Gimeno CJ et al. Cloning and characterization of an uncoupling protein homolog: a potential molecular mediator of human thermogenesis. Diabetes. 1997; 46:900-6.

Cannon B, Nedergaard J. Metabolic consequences of the presence or absence of the thermogenic capacity of brown adipose tissue in mice (and probably in humans). Int J Obes. 2010; 34(Suppl 1):S7-16.

Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004; 84:277-359.

Kozak LP, Koza RA, Anunciado-Koza R. Brown fat thermogenesis and body weight regulation in mice: relevance to humans. Int J Obes. 2010; 34(Suppl 1):S23-27.

Commins SP, Watson PM, Frampton IC, Gettys TW. Leptin selectively reduces white adipose tissue in mice via a UCP1-dependent mechanism in brown adipose tissue. Am J Physiol Endocrinol Metab. 2001; 280:E372-7.

Okamatsu-Ogura Y, Uozumi A, Toda C, Kimura K, Yamashita H, Saito M. Uncoupling protein 1 contributes to fat-reducing effect of leptin. Obes Res Clin Pract. 2007; 1:223-90.

Tanaka T, Yoshida N, Kishimoto T, Akira S. Defective adipocyte differentiation in mice lacking the C/EBPbeta and/or C/EBPdelta gene. EMBO J. 1997; 16:7432-43.

Tiraby C, Tavernier G, Lefort C, Larrouy D, Bouillaud F, Ricquier D et al. Acquirement of brown fat cell features by human white adipocytes. J Biol Chem. 2003; 278:33370-6.

Staels B, Schoonjans K, Fruchart JC, Auwerx J. The effects of fibrates and thiazolidinediones on plasma triglyceride metabolism are mediated by distinct peroxisome proliferator activated receptors (PPARs). Biochimie. 1997; 79:95-9.

Barbera MJ, Schluter A, Pedraza N, Iglesias R, Villarroya F, Giralt M. Peroxisome proliferator-activated receptor alpha activates transcription of the brown fat uncoupling protein-1 gene: a link between regulation of the thermogenic and lipid oxidation pathways in the brown fat cell. J Biol Chem. 2001; 276:1486-93.

Seale P, Kajimura S, Yang W, Chin S, Rohas LM, Uldry M et al. Transcriptional control of brown fat determination by PRDM16. Cell Metab. 2007; 6:38-54.

Seale P, Bjork B, Yang W, Kajimura S, Chin S, Kuang S et al. PRDM16 controls a brown fat/skeletal muscle switch. Nature. 2008; 454:961-7.

Puigserver P, Spiegelman BM. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr Rev. 2003; 24:78-90.

Wu J, Cohen P, Spiegelman BM. Adaptive thermogenesis in adipocytes: is beige the new brown? Genes Dev. 2013; 27:234-50.

Seale P, Conroe HM, Estall J, Kajimura S, Frontini A, Ishibashi J et al. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J Clin Invest. 2011; 121:96-105.

Leonardsson G, Steel JH, Christian M, Pocock V, Milligan S, Bell J et al. Nuclear receptor corepressor RIP140 regulates fat accumulation. Proc Natl Acad Sci USA. 2004; 101:8437-42.

Dempersmier J, Sambeat A, Gulyaeva O, Paul SM, Hudak CSS, Raposo HF et al. Cold-inducible Zfp516 activates UCP1 transcription to promote browning of white fat and development of brown fat. Mol Cell. 2015; 57:235-46.

Jacene HA, Cohade CC, Zhang Z, Wahl RL. The relationship between patients’ serum glucose levels and metabolically active brown adipose tissue detected by PET/CT. Mol Imaging Biol. 2011; 13:1278-83.

Matsushita M, Yoneshiro T, Aita S, Kameya T, Sugie H, Saito M. Impact of brown adipose tissue on body fatness and glucose metabolism in healthy humans. Int J Obes. 2014; 38:812-7.

Stanford KI, Middelbeek RJW, Townsend KL, An D, Nygaard EB, Hitchcox KM et al. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin Invest. 2013; 123:215-23.

Berbée JFP, Boon MR, Khedoe PPSJ, Bartelt A, Schlein C, Worthmann A et al. Brown fat activation reduces hypercholesterolaemia and protects from atherosclerosis development. Nat Commun. 2015; 6:6356.

Kim M, Goto T, Yu R, Uchida K, Tominaga M, Kano Y et al. Fish oil intake induces UCP1 upregulation in brown and white adipose tissue via the sympathetic nervous system. Sci Rep. 2015; 5:18013.

Arias N, Picó C, Teresa Macarulla M, Oliver P, Miranda J, Palou A et al. A combination of resveratrol and quercetin induces browning in white adipose tissue of rats fed an obesogenic diet. Obesity. 2017; 25:111-21.

You Y, Han X, Guo J, Guo Y, Yin M, Liu G et al. Cyanidin-3-glucoside attenuates high-fat and high-fructose diet-induced obesity by promoting the thermogenic capacity of brown adipose tissue. Journal of Functional Foods. 2018; 41:62-71.

Neyrinck AM, Bindels LB, Geurts L, Van Hul M, Cani PD, Delzenne NM. A polyphenolic extract from green tea leaves activates fat browning in high-fat-diet-induced obese mice. J Nutr Biochem. 2017; 49:15-21.

Alberdi G, Rodríguez VM, Miranda J, Macarulla MT, Churruca I, Portillo MP. Thermogenesis is involved in the body-fat lowering effects of resveratrol in rats. Food Chem. 2013; 141:1530-5.

Rayalam S, Yang J-Y, Ambati S, Della-Fera MA, Baile CA. Resveratrol induces apoptosis and inhibits adipogenesis in 3T3-L1 adipocytes. Phytother Res. 2008; 22:1367-71.

Lasa A, Churruca I, Eseberri I, Andrés-Lacueva C, Portillo MP. Delipidating effect of resveratrol metabolites in 3T3-L1 adipocytes. Mol Nutr Food Res. 2012; 56:1559-68.

Maeda H, Hosokawa M, Sashima T, Funayama K, Miyashita K. Fucoxanthin from edible seaweed, Undaria pinnatifida, shows antiobesity effect through UCP1 expression in white adipose tissues. Biochem Biophys Res Commun. 2005; 332:392-7.

Kawabata F, Inoue N, Masamoto Y, Matsumura S, Kimura W, Kadowaki M et al. Non-pungent capsaicin analogs (capsinoids) increase metabolic rate and enhance thermogenesis via gastrointestinal TRPV1 in mice. Biosci Biotechnol Biochem. 2009; 73:2690-7.

Yoneshiro T, Aita S, Kawai Y, Iwanaga T, Saito M. Nonpungent capsaicin analogs (capsinoids) increase energy expenditure through the activation of brown adipose tissue in humans. Am J Clin Nutr. 2012; 95:845-50.

Mosqueda-Solís A, Sánchez J, Portillo MP, Palou A, Picó C. Combination of capsaicin and hesperidin reduces the effectiveness of each compound to decrease the adipocyte size and to induce browning features in adipose tissue of western diet fed rats. J Agric Food Chem. 2018; 66:9679-89.

Chevalier C, Stojanović O, Colin DJ, Suarez-Zamorano N, Tarallo V, Veyrat-Durebex C et al. Gut microbiota orchestrates energy homeostasis during cold. Cell. 2015; 163:1360-74.

Anhê FF, Nachbar RT, Varin TV, Trottier J, Dudonné S, Le Barz M et al. Treatment with camu camu (Myrciaria dubia) prevents obesity by altering the gut microbiota and increasing energy expenditure in diet-induced obese mice. Gut. 2019; 68:453-64.

Reynés B, Palou M, Rodríguez AM, Palou A. Regulation of adaptive thermogenesis and browning by prebiotics and postbiotics. Front Physiol. 2019; 9. doi:10.3389/fphys.2018.01908.

Watanabe M, Houten SM, Mataki C, Christoffolete MA, Kim BW, Sato H et al. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature. 2006; 439:484-9.

Hu J, Kyrou I, Tan BK, Dimitriadis GK, Ramanjaneya M, Tripathi G et al. Short-chain fatty acid acetate stimulates adipogenesis and mitochondrial biogenesis via GPR43 in brown adipocytes. Endocrinology. 2016; 157:1881-94.

Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes. 2009; 58:1509-17.

Keijer J, Li M, Speakman JR. What is the best housing temperature to translate mouse experiments to humans? Mol Metab. 2019; 25:168-76.

Fischer AW, Cannon B, Nedergaard J. The answer to the question ‘What is the best housing temperature to translate mouse experiments to humans?’ is: thermoneutrality. Mol Metab. 2019; 26:1-3.

Trayhurn P. Brown Adipose Tissue—A Therapeutic Target in Obesity? Front Physiol 2018; 9. doi:10.3389/fphys.2018.01672.

Published

2020-12-29

How to Cite

1.
Fonseca Raposo H. Adipose tissue: its colors and versatility. HU Rev [Internet]. 2020Dec.29 [cited 2024Aug.17];46:1-12. Available from: https://periodicos.ufjf.br/index.php/hurevista/article/view/31268

Issue

Section

Artigos de Revisão da Literatura