An Artemisia scoparia extract attenuates glucocorticoid-induced lipolysis in adipocytes.
Journal
Obesity (Silver Spring, Md.)
ISSN: 1930-739X
Titre abrégé: Obesity (Silver Spring)
Pays: United States
ID NLM: 101264860
Informations de publication
Date de publication:
07 2023
07 2023
Historique:
revised:
16
03
2023
received:
22
09
2022
accepted:
17
03
2023
medline:
29
6
2023
pubmed:
31
5
2023
entrez:
31
5
2023
Statut:
ppublish
Résumé
Prescription glucocorticoid (GC) use is widespread across developed countries for the treatment of several inflammatory conditions. Elevated GCs are known to promote lipolysis and metabolic disorders. An extract of Artemisia scoparia (SCO) has been shown to reduce lipolysis and promote metabolic health but has not been investigated in the context of excess GCs. Our aim was to examine the effects of SCO on GC-induced lipolysis. Mature adipocytes were pretreated with vehicle or SCO, then exposed to either the synthetic GC dexamethasone (DEX) or tumor necrosis factor alpha (TNFα). Medium was collected and assayed for glycerol and fatty acids as measures of lipolysis. The expression of several lipolytic genes and proteins was assessed, and the involvement of glucocorticoid receptor (GR) in SCO's effects was also interrogated. SCO significantly attenuated DEX-induced lipolysis but did not interfere with DEX-mediated changes in inflammatory gene profiles in adipocytes. SCO treatment resulted in significant reductions in monomeric phosphodiesterase (PDE) protein levels while elevating PDE multimeric complex formation, but other canonical lipolytic mediators were unaltered. SCO attenuated lipolysis even when GR expression was significantly knocked down. Finally, it was demonstrated that SCO was distinct from rosiglitazone in its antilipolytic effects. SCO attenuates GC-induced lipolysis independently of GR activity. Future studies are needed to elucidate underlying mechanisms.
Substances chimiques
Glucocorticoids
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
1859-1870Subventions
Organisme : NCCIH NIH HHS
ID : P50 AT002776
Pays : United States
Informations de copyright
© 2023 The Obesity Society.
Références
Boden G. Role of fatty acids in the pathogenesis of insulin resistance and NIDDM. Diabetes. 1997;46(1):3-10.
Donnelly KL, Smith CI, Schwarzenberg SJ, Jessurun J, Boldt MD, Parks EJ. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin Invest. 2005;115(5):1343-1351. doi:10.1172/JCI23621
Dagpo TD, Nolan CJ, Delghingaro-Augusto V. Exploring therapeutic targets to reverse or prevent the transition from metabolically healthy to unhealthy obesity. Cell. 2020;9(7):1596. doi:10.3390/cells9071596
Yang A, Mottillo EP. Adipocyte lipolysis: from molecular mechanisms of regulation to disease and therapeutics. Biochem J. 2020;477(5):985-1008.
Collins S. β-Adrenoceptor signaling networks in adipocytes for recruiting stored fat and energy expenditure. Front Endocrinol. 2012;2:102 doi:10.3389/fendo.2011.00102
Xu C, He J, Jiang H, et al. Direct effect of glucocorticoids on lipolysis in adipocytes. Mol Endocrinol. 2009;23(8):1161-1170.
Campbell JE, Peckett AJ, D'Souza AM, Hawke TJ, Riddell MC. Adipogenic and lipolytic effects of chronic glucocorticoid exposure. Am J Physiol Cell Physiol. 2011;300(1):198-209.
Zhang HH, Halbleib M, Ahmad F, Manganiello VC, Greenberg AS. Tumor necrosis factor-alpha stimulates lipolysis in differentiated human adipocytes through activation of extracellular signal-related kinase and elevation of intracellular cAMP. Diabetes. 2002;51(10):2929-2935.
Laurencikiene J, van Harmelen V, Arvidsson Nordström E, et al. NF-kappaB is important for TNF-alpha-induced lipolysis in human adipocytes. J Lipid Res. 2007;48(5):1069-1077.
Ahmad F, Lindh R, Tang Y, et al. Differential regulation of adipocyte PDE3B in distinct membrane compartments by insulin and the β3-adrenergic receptor agonist CL316243: effects of caveolin-1 knockdown on formation/maintenance of macromolecular signalling complexes. Biochem J. 2010;424(3):399-410.
Choi YH, Park S, Hockman S, et al. Alterations in regulation of energy homeostasis in cyclic nucleotide phosphodiesterase 3B-null mice. J Clin Invest. 2006;116(12):3240-3251.
Kitamura T, Kitamura Y, Kuroda S, et al. Insulin-induced phosphorylation and activation of cyclic nucleotide phosphodiesterase 3B by the serine-threonine kinase Akt. Mol Cell Biol. 1999;19(9):6286-6296.
Sancar G, Liu S, Gasser E, et al. FGF1 and insulin control lipolysis by convergent pathways. Cell Metab. 2022;34(1):171-183.e6.
Morigny P, Houssier M, Mouisel E, Langin D. Adipocyte lipolysis and insulin resistance. Biochimie. 2016;125:259-266.
Reynisdottir S, Langin D, Carlström K, Holm C, Rössner S, Arner P. Effects of weight reduction on the regulation of lipolysis in adipocytes of women with upper-body obesity. Clin Sci. 1995;89(4):421-429. doi:10.1042/cs0890421
Stevens J, Green MH, Kaiser DL, Pohl SL. Insulin resistance in adipocytes from fed and fasted obese rats : dissociation of two insulin actions. Mol Cell Biochem. 1981;183:177-183.
Johnson JA, Fried SK, Pi-Sunyer FX, Albu JB. Impaired insulin action in subcutaneous adipocytes from women with visceral obesity. Am J Physiol Endocrinol Metab. 2001;280(1):E40-E49.
Albu JB, Curi M, Shur M, Murphy L, Matthews DE, Pi-Sunyer FX. Systemic resistance to the antilipolytic effect of insulin in black and white women with visceral obesity. Am J Physiol Endocrinol Metab. 1999;277:E551-E560.
Jensen MD, Haymond MW, Rizza RA, Cryer PE, Miles JM. Influence of body fat distribution on free fatty acid metabolism in obesity. J Clin Invest. 1989;83(4):1168-1173.
Pereira SS, Alvarez-Leite JI. Low-grade inflammation, obesity, and diabetes. Curr Obes Rep. 2014;3(4):422-431. doi:10.1007/s13679-014-0124-9
Harvey I, Stephenson EJ, Redd JR, et al. Glucocorticoid-induced metabolic disturbances are exacerbated in obese male mice. Endocrinology. 2018;159(6):2275-2287.
Hochberg I, Harvey I, Tran QT, et al. Gene expression changes in subcutaneous adipose tissue due to Cushing's disease. J Mol Endocrinol. 2015;55(2):81-94.
Burke SJ, Batdorf HM, Huang T-Y, et al. One week of continuous corticosterone exposure impairs hepatic metabolic flexibility, promotes islet β-cell proliferation, and reduces physical activity in male C57BL/6 J mice. J Steroid Biochem Mol Biol. 2019;195:105468. doi:10.1016/j.jsbmb.2019.105468
Laugesen K, Jørgensen JOL, Sørensen HT, Petersen I. Systemic glucocorticoid use in Denmark: a population-based prevalence study. BMJ Open. 2017;7(5):e015237. doi:10.1136/bmjopen-2016-015237
Bénard-Laribière A, Pariente A, Pambrun E, Bégaud B, Fardet L, Noize P. Prevalence and prescription patterns of oral glucocorticoids in adults: a retrospective cross-sectional and cohort analysis in France. BMJ Open. 2017;7(7):e015905. doi:10.1136/bmjopen-2017-015905
Laugesen K, Lunde Jørgensen JO, Petersen I, Sørensen HT. Fifteen-year nationwide trends in systemic glucocorticoid drug use in Denmark. Eur J Endocrinol. 2019;181(3):267-273.
Overman RA, Yeh JY, Deal CL. Prevalence of oral glucocorticoid usage in the United States: a general population perspective. Arthritis Care Res. 2013;65(2):294-298.
Fardet L, Petersen I, Nazareth I. Prevalence of long-term oral glucocorticoid prescriptions in the UK over the past 20 years. Rheumatology. 2011;50(11):1982-1990.
Raje V, Ahern KW, Martinez BA, et al. Adipocyte lipolysis drives acute stress-induced insulin resistance. Sci Rep. 2020;10(1):18166. doi:10.1038/s41598-020-75321-0
Perry RJ, Peng L, Abulizi A, Kennedy L, Cline GW, Shulman GI. Mechanism for leptin's acute insulin-independent effect to reverse diabetic ketoacidosis. J Clin Invest. 2017;127(2):657-669.
Schweiger M, Romauch M, Schreiber R, et al. Pharmacological inhibition of adipose triglyceride lipase corrects high-fat diet-induced insulin resistance and hepatosteatosis in mice. Nat Commun. 2017;8:14859. doi:10.1038/ncomms14859
Boudreau A, Richard AJ, Harvey I, Stephens JM. Artemisia scoparia and metabolic health: untapped potential of an ancient remedy for modern use. Front Endocrinol. 2022;12:727061. doi:10.3389/fendo.2021.727061
Boudreau A, Richard AJ, Burrell JA, et al. An ethanolic extract of Artemisia scoparia inhibits lipolysis in vivo and has antilipolytic effects on murine adipocytes in vitro. Am J Physiol Metab. 2018;315(5):E1053-E1061.
Richard AJ, Fuller S, Fedorcenco V, et al. Artemisia scoparia enhances adipocyte development and endocrine function in vitro and enhances insulin action in vivo. PLoS One. 2014;9(6):e98897. doi:10.1371/journal.pone.0098897
Wang ZQ, Zhang XH, Yu Y, et al. Artemisia scoparia extract attenuates non-alcoholic fatty liver disease in diet-induced obesity mice by enhancing hepatic insulin and AMPK signaling independently of FGF21 pathway. Metabolism. 2013;62(9):1239-1249.
Ghosh B, Guidry HJ, Johnston M, Bohnert KA. A fat-promoting botanical extract from Artemisia scoparia exerts geroprotective effects on Caenorhabditis elegans life span and stress resistance. J Gerontol A Biol Sci Med Sci. 2022;77(6):1112-1120. doi:10.1093/gerona/glac040
Dong Y, Poellinger L, Gustafsson JÅ, Okret S. Regulation of glucocorticoid receptor expression: evidence for transcriptional and posttranslational mechanisms. Mol Endocrinol. 1988;2(12):1256-1264.
Yu CY, Mayba O, Lee JV, et al. Genome-wide analysis of glucocorticoid receptor binding regions in adipocytes reveal gene network involved in triglyceride homeostasis. PLoS One. 2010;5:e15188. doi:10.1371/journal.pone.0015188
MacPherson REK, Castellani L, Beaudoin MS, Wright DC. Evidence for fatty acids mediating CL 316,243-induced reductions in blood glucose in mice. Am J Physiol Endocrinol Metab. 2014;307(7):E563-E570.
Green A, Dobias SB, Walters DJ, Brasier AR. Tumor necrosis factor increases the rate of lipolysis in primary cultures of adipocytes without altering levels of hormone-sensitive lipase. Endocrinology. 1994;134(6):2581-2588. doi:10.1210/endo.134.6.8194485
Boudreau A, Poulev A, Ribnicky DM, et al. Distinct fractions of an Artemisia scoparia extract contain compounds with novel adipogenic bioactivity. Front Nutr. 2019;6:18. doi:10.3389/fnut.2019.00018
Ribnicky D, Beom Kim S, Poulev A, et al. Prenylated Coumaric acids from Artemisia scoparia beneficially modulate Adipogenesis. J Nat Prod. 2021;84:1078-1086.
Strieter RM, Kunkel SL, Bone RC. Role of tumor necrosis factor-α in disease states and inflammation. Crit Care Med. 1993;21(suppl 10):S447-S463.
Rhen T, Cidlowski JA. Antiinflammatory action of glucocorticoids - new mechanisms for old drugs. N Engl J Med. 2005;353(16):1711-1723.
Kang S, Tsai LT, Zhou Y, et al. Identification of nuclear hormone receptor pathways causing insulin resistance by transcriptional and epigenomic analysis. Nat Cell Biol. 2015;17(1):44-56.
Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature. 2006;440(7086):944-948.
Rahn Landström T, Mei J, Karlsson M, Manganiello V, Degerman E. Down-regulation of cyclic-nucleotide phosphodiesterase 3B in 3T3-L1 adipocytes induced by tumour necrosis factor alpha and cAMP. Biochem J. 2000;346(Pt 2):337-343.
Richter W, Conti M. The oligomerization state determines regulatory properties and inhibitor sensitivity of type 4 cAMP-specific phosphodiesterases. J Biol Chem. 2004;279(29):30338-30348.
Park Y, Freedman BD, Lee EJ, Park S, Jameson JL. A dominant negative PPARγ mutant shows altered cofactor recruitment and inhibits adipogenesis in 3T3-L1 cells. Diabetologia. 2003;46(3):365-377.
Tang W, Zeve D, Seo J, Jo AY, Graff JM. Thiazolidinediones regulate adipose lineage dynamics. Cell Metab. 2011;14(1):116-122.
He J, Xu C, Kuang J, et al. Thiazolidinediones attenuate lipolysis and ameliorate dexamethasone-induced insulin resistance. Metabolism. 2015;64(7):826-836.
Rosen CJ. The rosiglitazone story: lessons from an FDA Advisory Committee meeting. N Engl J Med. 2007;357:844-846.
Nissen SE, Wolski K. Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. N Engl J Med. 2007;356(24):2457-2471.
Witters LA. The blooming of the French lilac. J Clin Invest. 2001;108(8):1105-1107.
Richard AJ, Burris TP, Sanchez-Infantes D, Wang Y, Ribnicky DM, Stephens JM. Artemisia extracts activate PPARγ, promote adipogenesis, and enhance insulin sensitivity in adipose tissue of obese mice. Nutrition. 2014;30(7-8 suppl):S31-S536.
Harvey I, Stephens JM. Artemisia scoparia promotes adipogenesis in the absence of adipogenic effectors. Obesity. 2021;29:1309-1319.