White to brown adipocyte transition mediated by Apigenin via VEGF-PRDM16 signaling.
Mice
Animals
Adipocytes, Brown
/ metabolism
Vascular Endothelial Growth Factor A
/ metabolism
Apigenin
/ pharmacology
Adipose Tissue, Brown
/ metabolism
Adipose Tissue, White
/ metabolism
Adipocytes, White
/ metabolism
Transcription Factors
/ genetics
Obesity
/ metabolism
DNA-Binding Proteins
/ genetics
VEGF
angiogenesis
browning
uncoupler
white adipocyte
Journal
Journal of cellular biochemistry
ISSN: 1097-4644
Titre abrégé: J Cell Biochem
Pays: United States
ID NLM: 8205768
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
revised:
25
07
2022
received:
08
02
2022
accepted:
27
07
2022
pubmed:
5
8
2022
medline:
22
11
2022
entrez:
4
8
2022
Statut:
ppublish
Résumé
The dysregulated energy metabolism in white adipose tissues results in derangement of biological signaling resulting in obesity. Lack of vascularization in these white adipose tissues is one of the major reasons for dysregulated energy metabolism. Not much work has been done in this direction to understand the role of angiogenesis in white adipose tissue metabolism. In the present study, we evaluated the effect of angiogenic modulator in the metabolism of white adipocyte (WAC). Bioactive Apigenin was selected and its angiogenic ability was studied. Apigenin was shown to be highly proangiogenic hence the effect of Apigenin on de novo and trans-differentiation of WAT was studied. Apigenin showed enhanced de novo differentiation and trans-differentiation of mouse WAC into brown-like phenotype. To understand the effect of Apigenin on adipose tissue vasculature, coculture studies were conducted. Cross talk between endothelial cell and adipocytes were observed in coculture studies. Gene expression studies of cocultured cells revealed that browning of WAC occurred by triggering the expression of Vascular endothelial growth factor A. The study provides a new insight for inducing metabolic shift in WACs by modulation of angiogenesis in WAC microenvironment by the upregulation of PRDM16 cascade to trigger browning for the treatment of obesity.
Substances chimiques
Vascular Endothelial Growth Factor A
0
Apigenin
7V515PI7F6
Transcription Factors
0
Prdm16 protein, mouse
0
DNA-Binding Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1793-1807Subventions
Organisme : Council for Scientific and Industrial Research
ID : 31/006(0433)/2017-EMR-I
Organisme : Indian Council of Medical Research
ID : No:5/4/8-26/OBS/2021-NCD-II
Informations de copyright
© 2022 Wiley Periodicals LLC.
Références
Ahima RS, Flier JS. Adipose tissue as an endocrine organ. Trends Endocrinol Metab. 2000;11(8):327-332. doi:10.1016/s1043-2760(00)00301-5
Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84(1):277-359. doi:10.1152/physrev.00015.2003
Rosen ED, Spiegelman BM. What we talk about when we talk about fat. Cell. 2014;156(1-2):20-44. doi:10.1016/j.cell.2013.12.012
Zechner R, Zimmermann R, Eichmann TO, et al. FAT SIGNALS-lipases and lipolysis in lipid metabolism and signaling. Cell Metab. 2012;7 15(3):279-291. doi:10.1016/j.cmet.2011.12.018
Kang JG, Park CY. Anti-obesity drugs: a review about their effects and safety. Diabetes Metab J. 2012;36(1):13-25. doi:10.4093/dmj.2012.36.1.13
Corvera S, Gealekman O. Adipose tissue angiogenesis: impact on obesity and type-2 diabetes. Biochim Biophys Acta, Mol Basis Dis. 2014;1842(3):463-472. doi:10.1016/j.bbadis.2013.06.003
Cao Y. Angiogenesis modulates adipogenesis and obesity. J Clin Investig. 2007;117(9):2362-2368. doi:10.1172/JCI32239
Goossens GH, Blaak EE. Adipose tissue oxygen tension: implications for chronic metabolic and inflammatory diseases. Curr Opin Clin Nutr Metab Care. 2012;15(6):539-546. doi:10.1097/MCO.0b013e328358fa87
Pierpont YN, Dinh TP, Salas RE, et al. Obesity and surgical wound healing: a current review. ISRN Obes. 2014;2014(20):638936. doi:10.1155/2014/638936
Liao D, Johnson RS. Hypoxia: a key regulator of angiogenesis in cancer. Cancer Metastasis Rev. 2007;26(2):281-290. doi:10.1007/s10555-007-9066-y
Halberg N, Khan T, Trujillo ME, et al. Hypoxia-inducible factor 1alpha induces fibrosis and insulin resistance in white adipose tissue. Mol Cell Biol. 2009;29(16):4467-4483. doi:10.1128/MCB.00192-09
Pence BD, Woods JA. Exercise, obesity, and cutaneous wound healing: evidence from rodent and human studies. Adv Wound Care. 2012;3(1):71-79. doi:10.1089/wound.2012.0377
Zhou X, Wang F, Zhou R, Song X, Xie M. Apigenin: a current review on its beneficial biological activities. J Food Biochem. 2017;41:e12376. doi:10.1111/jfbc.12376
Ono M, Fujimori K. Antiadipogenic effect of dietary Apigenin through activation of AMPK in 3T3-L1 cells. J Agric Food Chem. 2011;59(24):13346-13352. doi:10.1021/jf203490a
Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65(1-2):55-63. doi:10.1016/0022-1759(83)90303-4
Ng KB, Bustamam A, Sukari MA, et al. Induction of selective cytotoxicity and apoptosis in human T4-lymphoblastoid cell line (CEMss) by boesenbergin a isolated from Boesenbergia rotunda rhizomes involves mitochondrial pathway, activation of caspase 3 and G2/M phase cell cycle arrest. BMC Complement Altern Med. 2013;13:1-15. doi:10.1186/1472-6882-13-41
Khoo CP, Micklem K, Watt SM. A comparison of methods for quantifying angiogenesis in the matrigel assay in vitro. Tissue Eng Part C Methods. 2011;17(9):895-906. doi:10.1089/ten.TEC.2011.0150
Arnaoutova I, Kleinman HK. In vitro angiogenesis: endothelial cell tube formation on gelled basement membrane extract. Nat Protoc. 2015;5:628-635. doi:10.1038/nprot.2010.6
West DC, Thompson WD, Sells PG, Burbridge MF. Angiogenesis assays using chick chorioallantoic membrane. Angiogenesis protocols. Methods Mol Med. 2001;46:107-129. doi:10.1385/1-59259-143-4:107
Auerbach R, Lewis R, Shinners B, Kubai L, Akhtar N. Angiogenesis assays: a critical overview. Clin Chem. 2003;49(1):32-40. doi:10.1373/49.1.32
Lane MD, Reed BC, Clements PR. Insulin receptor synthesis and turnover in differentiating 3T3-L1 preadipocytes. Prog Clin Biol Res. 1981;66:523-542. doi:10.1073/pnas.77.1.285
Lee MJ, Fried SK. Optimal protocol for the differentiation and metabolic analysis of human adipose stromal cells. Methods Enzymol. 2014;538:49-65. doi:10.1016/B978-0-12-800280-3.00004-9
Styner M, Sen B, Xie Z, Case N, Rubin J. Indomethacin promotes adipogenesis of mesenchymal stem cells through a cyclooxygenase independent mechanism. J Cell Biochem. 2010;111(4):1042-1050. doi:10.1002/jcb.22793
Velickovic K, Wayne D, Leija HAL, et al. Caffeine exposure induces browning features in adipose tissue in vitro and in vivo. Sci Rep. 2019;9(9104):1-11. doi:10.1038/s41598-019-45540-1
Wang XY, You LH, Cui XW, et al. Evaluation and optimization of differentiation conditions for human primary brown adipocytes. Sci Rep. 2018;8(5304):1-12. doi:10.1038/s41598-018-23700-z
Jensen EC. Quantitative analysis of histological staining and fluorescence using ImageJ. Anat Rec. 2013;296(3):378-381. doi:10.1002/ar.22641
Perelman A, Wachtel C, Cohen M, Haupt S, Shapiro H, Tzur A. JC-1: alternative excitation wavelengths facilitate mitochondrial membrane potential cytometry. Cell Death Dis. 2012;3(11):e430-e437. doi:10.1038/cddis.2012.171
Lai N, Jayaraman A, Lee K. Enhanced proliferation of human umbilical vein endothelial cells and differentiation of 3T3-L1 adipocytes in coculture. Tissue Eng. 2008;15(5):1053-1061. doi:10.1089/ten.tea.2008.0101
Engvall E. Enzyme-linked immunosorbent assay (ELISA) quantitative assay of immunoglobulin G. Mol Immunol. 1971;8(9):871-874. doi:10.1016/0019-2791(71)90454-x
Suzuki M, Shinohara Y, Ohsaki Y, Fujimoto T. Lipid droplets: size matters. J Electron Microsc Tech. 2011;60(S1):S101-S116. doi:10.1093/jmicro/dfr016
Zorova LD, Popkov VA, Plotnikov EY, et al. Mitochondrial membrane potential. Anal Biochem. 2018;552:50-59. doi:10.1016/j.ab.2017.07.009
Gupta RC, Srivastava A, Lall R. Toxicity potential of nutraceuticals. In: Nicolotti O, ed. Computational Toxicology. Methods in Molecular Biology. Vol 1800. Humana Press; 2018:367-394. doi:10.1007/978-1-4939-7899-1_18
Arimochi H, Sasaki Y, Kitamura A, Yasutomo K. Differentiation of preadipocytes and mature adipocytes requires PSMB8. Sci Rep. 2016;6:26791. doi:10.1038/srep26791
Shan T, Liang X, Bi P, Zhang P, Liu W, Kuang S. Distinct populations of adipogenic and myogenic Myf5-lineage progenitors in white adipose tissues. J Lipid Res. 2013;54(8):2214-2224. doi:10.1194/jlr.M038711
Furuhashi M, Saitoh S, Shimamoto K, Miura T. Fatty acid-binding protein 4 (FABP4): pathophysiological insights and potent clinical biomarker of metabolic and cardiovascular diseases. Clin Med Insights Cardiol. 2015;8(Suppl 3):S23-S33. doi:10.4137/CMC.S17067
Antoniades C, Antonopoulos AS, Tousoulis D, Stefanadis C. Adiponectin: from obesity to cardiovascular disease. Obes Rev. 2009;10(3):269-279. doi:10.1111/j.1467-789X.2009.00571.x
Kim JY, Tillison K, Lee JH, Rearick DA, Smas CM. The adipose tissue triglyceride lipase ATGL/PNPLA2 is downregulated by insulin and TNF-alpha in 3T3-L1 adipocytes and is a target for transactivation by PPARgamma. Am J Physiol Endocrinol Metab. 2006;291(1):E115-E127. doi:10.1152/ajpendo.00317.2005
Ferrari A, Longo R, Fiorino E, et al. HDAC3 is a molecular brake of the metabolic switch supporting white adipose tissue browning. Nat Commun. 2017;8(1):93. doi:10.1038/s41467-017-00182-7
Cui XB, Chen SY. White adipose tissue browning and obesity. J Biomed Res. 2017;31(1):1-2. doi:10.7555/JBR.31.20160101
Shao M, Vishvanath L, Busbuso NC, et al. De novo adipocyte differentiation from Pdgfrβ+ preadipocytes protects against pathologic visceral adipose expansion in obesity. Nat Commun. 2018;9(1):1-16. doi:10.1038/s41467-018-03196-x
Rajan S, Gupta A, Beg M, et al. Adipocyte transdifferentiation and its molecular targets. Differentiation. 2014;87(5):183-192. doi:10.1016/j.diff.2014.07.002
Hildebrand S, Stümer J, Pfeifer A. PVAT and its relation to brown, beige, and white adipose tissue in development and function. Front Physiol. 2018;9(70):1-10. doi:10.3389/fphys.2018.00070
Elias I, Franckhauser S, Bosch F. New insights into adipose tissue VEGF-A actions in the control of obesity and insulin resistance. Adipocyte. 2013;2(2):109-112. doi:10.4161/adip.22880
Lee JH, Park A, Oh KJ, Lee SC, Kim WK, Bae KH. The role of adipose tissue mitochondria: regulation of mitochondrial function for the treatment of metabolic diseases. Int J Mol Sci. 2019;20(19):4924. doi:10.3390/ijms20194924
Liu M, Zheng M, Cai D, et al. Zeaxanthin promotes mitochondrial biogenesis and adipocyte browning: via AMPKα1 activation. Food Funct. 2019;10:2221-2233. doi:10.1039/c8fo02527d
Nicholls DG, Bernson VS, Heaton GM. The identification of the component in the inner membrane of brown adipose tissue mitochondria responsible for regulating energy dissipation. Experientia Suppl. 1978;32:89-93. doi:10.1007/978-3-0348-5559-4_9
Porter C. Quantification of UCP1 function in human brown adipose tissue. Adipocyte. 2017;6(2):167-174. doi:10.1080/21623945.2017.1319535
Sztalryd C, Brasaemle DL. The perilipin family of lipid droplet proteins: gatekeepers of intracellular lipolysis. Biochim Biophys Acta Mol Cell Biol Lipids. 2017;1862(10):1221-1232. doi:10.1016/j.bbalip.2017.07.009
Lee YK, Sohn JH, Han JS, et al. Perilipin 3 deficiency stimulates thermogenic Beige adipocytes through PPARa activation. Diabetes. 2018;67(5):791-804. doi:10.2337/db17-0983
Harms MJ, Ishibashi J, Wang W, et al. Prdm16 is required for the maintenance of brown adipocyte identity and function in adult mice. Cell Metab. 2014;19(4):593-604. doi:10.1016/j.cmet.2014.03.007
Cohen P, Levy JD, Zhang Y, et al. Ablation of PRDM16 and beige adipose causes metabolic dysfunction and a subcutaneous to visceral fat switch. Cell. 2014;156(1-2):304-316. doi:10.1016/j.cell.2013.12.021