Effects of Sargaquinoic Acid in Sargassum Serratifolium on Inducing Brown Adipocyte-like Phenotype in Mouse Adipocytes In Vitro

Misung Kwon; Bonggi Lee; Sujin Lim; Hyeung-Rak Kim

doi:10.1055/a-1023-7385

Planta Medica, Table of Contents

Planta Med 2020; 86(01): 45-54
DOI: 10.1055/a-1023-7385

Biological and Pharmacological Activity

Original Papers

Georg Thieme Verlag KG Stuttgart · New York

Effects of Sargaquinoic Acid in Sargassum Serratifolium on Inducing Brown Adipocyte-like Phenotype in Mouse Adipocytes In Vitro

Misung Kwon‡

¹Department of Food Science and Nutrition, Pukyong National University, Busan, Republic of Korea

,

Bonggi Lee‡

²Korean Medicine (KM)-Application Center, Korea Institute of Oriental Medicine (KIOM), Daegu, Republic of Korea

,

Sujin Lim

¹Department of Food Science and Nutrition, Pukyong National University, Busan, Republic of Korea

,

Hyeung-Rak Kim

¹Department of Food Science and Nutrition, Pukyong National University, Busan, Republic of Korea

› Author Affiliations

Abstract

A previous study showed that the meroterpenoid-rich fraction of an ethanolic extract of Sargassum serratifolium (MES) stimulated adipose tissue browning and inhibited diet-induced obesity and metabolic syndrome. Sargaquinoic acid (SQA) is a major component in MES. We investigated the effects of SQA on the differentiation of preadipocytes to the beige adipocytes. SQA was treated in 3T3-L1 adipocytes differentiated under a special condition that has been reported to induce the browning of adipocytes. SQA at 10 µM reduced lipid accumulation by approximately 23%. SQA at 2.5 – 10 µM induced the differentiation of white adipocytes to beige adipocytes partially by increasing the mitochondrial density and the expression of beige/brown adipocyte markers. In addition, SQA activated lipid catabolic pathways, evidenced by the increased expression levels of perilipin, carnitine palmitoyltransferase 1, and acyl-CoA synthetase long-chain family member 1. As a partial mechanism, biochemical and in silico analyses indicate that SQA activated AMP-activated protein kinase signaling in adipocytes.

Key words

Sargassaceae - Sargassum serratifolium - lipolysis - sargaquinoic acid - adipocytes

Full Text

References

References
1 NCD Risk Factor Collaboration (NCD-RisC). Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128.9 million children, adolescents, and adults. Lancet 2017; 390: 2627-2642
2 Harms M, Seale P. Brown and beige fat: development, function and therapeutic potential. Nat Med 2013; 19: 1252-1263
3 Bornfeldt KE, Tabas I. Insulin resistance, hyperglycemia, and atherosclerosis. Cell Metab 2011; 14: 575-585
4 Harvey AE, Lashinger LM, Hursting SD. The growing challenge of obesity and cancer: an inflammatory issue. Ann N Y Acad Sci 2011; 1229: 45-52
5 Lloyd-Jones D, Adams R, Carnethon M, De Simone G, Ferguson TB, Flegal K, Ford E, Furie K, Go A, Greenlund K, Haase N, Hailpern S, Ho M, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott M, Meigs J, Mozaffarian D, Nichol G, OʼDonnell C, Roger V, Rosamond W, Sacco R, Sorlie P, Stafford R, Steinberger J, Thom T, Wasserthiel-Smoller S, Wong N, Wylie-Rosett J, Hong Y. Heart disease and stroke statistics – 2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2009; 119: e21-181
6 Liu C, Rajapakse AG, Riedo E, Fellay B, Bernhard MC, Montani JP, Yang Z, Ming XF. Targeting arginase-II protects mice from high-fat-diet-induced hepatic steatosis through suppression of macrophage inflammation. Sci Rep 2016; 6: 20405
7 Shepherd PR, Gnudi L, Tozzo E, Yang H, Leach F, Kahn BB. Adipose cell hyperplasia and enhanced glucose disposal in transgenic mice overexpressing GLUT4 selectively in adipose tissue. J Biol Chem 1993; 268: 22243-22246
8 Bonet ML, Oliver P, Palou A. Pharmacological and nutritional agents promoting browning of white adipose tissue. Biochim Biophys Acta 2013; 1831: 969-985
9 Ohno H, Shinoda K, Spiegelman BM, Kajimura S. PPARgamma agonists induce a white-to-brown fat conversion through stabilization of PRDM16 protein. Cell Metab 2012; 15: 395-404
10 Bukowiecki L, Collet AJ, Follea N, Guay G, Jahjah L. Brown adipose tissue hyperplasia: a fundamental mechanism of adaptation to cold and hyperphagia. Am J Physiol Endocrinol Metab 1982; 242: E353-E359
11 Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 2004; 84: 277-359
12 Matsukawa T, Villareal MO, Motojima H, Isoda H. Increasing cAMP levels of preadipocytes by cyanidin-3-glucoside treatment induces the formation of beige phenotypes in 3T3-L1 adipocytes. J Nutr Biochem 2017; 40: 77-85
13 Ejaz A, Wu D, Kwan P, Meydani M. Curcumin inhibits adipogenesis in 3T3-L1 adipocytes and angiogenesis and obesity in C57/BL mice. J Nutr 2009; 139: 919-925
14 Matsumoto M, Hosokawa M, Matsukawa N, Hagio M, Shinoki A, Nishimukai M, Miyashita K, Yajima T, Hara H. Suppressive effects of the marine carotenoids, fucoxanthin and fucoxanthinol on triglyceride absorption in lymph duct-cannulated rats. Eur J Nutr 2010; 49: 243-249
15 Lone J, Choi JH, Kim SW, Yun JW. Curcumin induces brown fat-like phenotype in 3T3-L1 and primary white adipocytes. J Nutr Biochem 2016; 27: 193-202
16 Choi JH, Yun JW. Chrysin induces brown fat-like phenotype and enhances lipid metabolism in 3T3-L1 adipocytes. Nutrition 2016; 32: 1002-1010
17 Lone J, Yun JW. Monoterpene limonene induces brown fat-like phenotype in 3T3-L1 white adipocytes. Life Sci 2016; 153: 198-206
18 Joung EJ, Gwon WG, Shin T, Jung BM, Choi J, Kim HR. Anti-inflammatory action of the ethanolic extract from Sargassum serratifolium on lipopolysaccharide-stimulated mouse peritoneal macrophages and identification of active components. J Appl Phycol 2017; 29: 563-573
19 Gwon WG, Joung EJ, Shin T, Utsuki T, Wakamatsu N, Kim HR. Meroterpinoid-rich fraction of the ethanol extract from Sargassum serratifolium suppresses TNF-α-induced monocytes adhesion to vascular endothelium and vascular inflammation in high cholesterol-fed C57BL/6J mice. J Funct Foods 2018; 46: 384-393
20 Kwon M, Lim SJ, Lee B, Shin TS, Kim HR. Ethanolic extract of Sargassum serratifolium inhibits adipogenesis in 3T3-L1 preadipocytes by cell cycle arrest. J Appl Phycol 2017; 30: 559-568
21 Kwon M, Lim SJ, Joung EJ, Lee B, Oh CW, Kim HR. Meroterpenoid-rich fraction of an ethanolic extract from Sargassum serratifolium alleviates obesity and non-alcoholic fatty liver disease in high fat-fed C57BL/6J mice. J Funct Foods 2018; 47: 288-298
22 Joung EJ, Lee B, Gwon WG, Shin T, Jung BM, Yoon NY, Choi JS, Oh CW, Kim HR. Sargaquinoic acid attenuates inflammatory responses by regulating NF-kappaB and Nrf2 pathways in lipopolysaccharide-stimulated RAW 264.7 cells. Int Immunopharmacol 2015; 29: 693-700
23 Gwon WG, Lee B, Joung EJ, Choi MW, Yoon N, Shin T, Oh CW, Kim HR. Sargaquinoic acid inhibits TNF-alpha-induced NF-kappaB signaling, thereby contributing to decreased monocyte adhesion to human umbilical vein endothelial cells (HUVECs). J Agric Food Chem 2015; 63: 9053-9061
24 Kim SN, Choi HY, Lee W, Park GM, Shin WS, Kim YK. Sargaquinoic acid and sargahydroquinoic acid from Sargassum yezoense stimulate adipocyte differentiation through PPARalpha/gamma activation in 3T3-L1 cells. FEBS Lett 2008; 582: 3465-3472
25 Asano H, Kanamori Y, Higurashi S, Nara T, Kato K, Matsui T, Funaba M. Induction of beige-like adipocytes in 3T3-L1 cells. J Vet Med Sci 2014; 76: 57-64
26 Wu J, Bostrom P, Sparks LM, Ye L, Choi JH, Giang AH, Khandekar M, Virtanen KA, Nuutila P, Schaart G, Huang K, Tu H, van Marken Lichtenbelt WD, Hoeks J, Enerback S, Schrauwen P, Spiegelman BM. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 2012; 150: 366-376
27 Kajimura S, Seale P, Kubota K, Lunsford E, Frangioni JV, Gygi SP, Spiegelman BM. Initiation of myoblast to brown fat switch by a PRDM16-C/EBP-beta transcriptional complex. Nature 2009; 460: 1154-1158
28 Lin J, Handschin C, Spiegelman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab 2005; 1: 361-370
29 Hung PF, Wu BT, Chen HC, Chen YH, Chen CL, Wu MH, Liu HC, Lee MJ, Kao YH. Antimitogenic effect of green tea (−)-epigallocatechin gallate on 3T3-L1 preadipocytes depends on the ERK and Cdk2 pathways. Am J Physiol Cell Physiol 2005; 288: C1094-C1108
30 Hu Y, Davies GE. Berberine inhibits adipogenesis in high-fat diet-induced obesity mice. Fitoterapia 2010; 81: 358-366
31 Lee GR, Shin MK, Yoon DJ, Kim AR, Yu R, Park NH, Han IS. Topical application of capsaicin reduces visceral adipose fat by affecting adipokine levels in high-fat diet-induced obese mice. Obesity (Silver Spring) 2013; 21: 115-122
32 Meydani M, Hasan ST. Dietary polyphenols and obesity. Nutrients 2010; 2: 737-751
33 Wan-Loy C, Siew-Moi P. Marine algae as a potential source for anti-obesity agents. Mar Drugs 2016; 14: 222
34 Liu L, Heinrich M, Myers S, Dworjanyn SA. Towards a better understanding of medicinal uses of the brown seaweed Sargassum in traditional Chinese medicine: a phytochemical and pharmacological review. J Ethnopharmacol 2012; 142: 591-619
35 Kim SK, Himaya SWA. Medicinal Effects of Phlorotannins from marine brown Algae. In: Kim SK. ed. Advances in Food and Nutrition Research. San Diego: Academic Press; 2011: 97-109
36 Grasa-Lopez A, Miliar-Garcia A, Quevedo-Corona L, Paniagua-Castro N, Escalona-Cardoso G, Reyes-Maldonado E, Jaramillo-Flores ME. Undaria pinnatifida and fucoxanthin ameliorate lipogenesis and markers of both inflammation and cardiovascular dysfunction in an animal model of diet-induced obesity. Mar Drugs 2016; 14: 148
37 Lai CS, Tsai ML, Badmaev V, Jimenez M, Ho CT, Pan MH. Xanthigen suppresses preadipocyte differentiation and adipogenesis through down-regulation of PPARgamma and C/EBPs and modulation of SIRT-1, AMPK, and FoxO pathways. J Agric Food Chem 2012; 60: 1094-1101
38 Maeda H, Hosokawa M, Sashima T, Murakami-Funayama K, Miyashita K. Anti-obesity and anti-diabetic effects of fucoxanthin on diet-induced obesity conditions in a murine model. Mol Med Rep 2009; 2: 897-902
39 Salt I, Celler JW, Hawley SA, Prescott A, Woods A, Carling D, Hardie DG. AMP-activated protein kinase: greater AMP dependence, and preferential nuclear localization, of complexes containing the alpha2 isoform. Biochem J 1998; 334: 177-187
40 Bijland S, Mancini SJ, Salt IP. Role of AMP-activated protein kinase in adipose tissue metabolism and inflammation. Clin Sci 2013; 124: 491-507
41 Zhang BB, Zhou G, Li C. AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab 2009; 9: 407-416
42 Hawley SA, Fullerton MD, Ross FA, Schertzer JD, Chevtzoff C, Walker KJ, Peggie MW, Zibrova D, Green KA, Mustard KJ, Kemp BE, Sakamoto K, Steinberg GR, Hardie DG. The ancient drug salicylate directly activates AMP-activated protein kinase. Science 2012; 336: 918-922
43 Wang S, Liang X, Yang Q, Fu X, Rogers CJ, Zhu M, Rodgers BD, Jiang Q, Dodson MV, Du M. Resveratrol induces brown-like adipocyte formation in white fat through activation of AMP-activated protein kinase (AMPK) alpha1. Int J Obes 2015; 39: 967-976
44 Kwon M, Lee B, Lim SJ, Choi JS, Kim HR. Sargahydroquinoic acid, a major compound in Sargassum serratifolium (C. Agardh) C. Agardh, widely activates lipid catabolic pathways, contributing to the formation of beige-like adipocytes. J Funct Foods 2019; 58: 355-366