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Published in: European Journal of Nutrition 8/2015

01-12-2015 | Original Contribution

Persimmon tannin represses 3T3-L1 preadipocyte differentiation via up-regulating expression of miR-27 and down-regulating expression of peroxisome proliferator-activated receptor-γ in the early phase of adipogenesis

Authors: Bo Zou, Zhenzhen Ge, Wei Zhu, Ze Xu, Chunmei Li

Published in: European Journal of Nutrition | Issue 8/2015

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Abstract

Purpose

Currently, obesity has become a worldwide health problem. Adipocyte differentiation is closely associated with the onset of obesity. Our previous studies suggested that persimmon tannin might be a potent anti-adipogenic dietary bioactive compound. However, the mechanism of persimmon tannin on adipocyte differentiation is still unknown. The purpose of this study was to investigate the effect of persimmon tannin on adipogenic differentiation in 3T3-L1 preadipocytes and the underlying mechanisms.

Methods

Adipogenic differentiation was induced by cocktail in the presence or absence of persimmon tannin. Intracellular lipid accumulation was determined by Oil red O staining and enzymatic colorimetric methods. Gene expression and protein levels were measured by real time RT-PCR and Western blot.

Results

Persimmon tannin inhibited intracellular lipid accumulation markedly, and the inhibitory effect was largely limited to the early stage of adipocyte differentiation. Persimmon tannin suppressed the expression of C/EBPα and peroxisome proliferator-activated receptor-γ (PPARγ), significantly. Furthermore, genes related to lipogenesis, such as sterol regulatory element-binding protein 1, were down-regulated by persimmon tannin. In addition, adipocyte fatty acid binding protein (aP2), which is a target gene of PPARγ, was suppressed by persimmon tannin notably. Correspondingly, the expression of miR-27a and miR-27b were up-regulated by persimmon tannin from Day 2 to Day 8 significantly.

Conclusion

Persimmon tannin inhibited adipocyte differentiation through regulation of PPARγ, C/EBPα and miR-27 in early stage of adipogenesis.
Literature
1.
go back to reference Wang S, Moustaid-Moussa N, Chen L, Mo H, Shastri A, Su R, Bapat P, Kwun I, Shen CL (2014) Novel insights of dietary polyphenols and obesity. J Nutr Biochem 25:1–18CrossRef Wang S, Moustaid-Moussa N, Chen L, Mo H, Shastri A, Su R, Bapat P, Kwun I, Shen CL (2014) Novel insights of dietary polyphenols and obesity. J Nutr Biochem 25:1–18CrossRef
2.
go back to reference Min SY, Yang H, Seo SG, Shin SH, Chung MY, Kim J, Lee SJ, Lee HJ, Lee KW (2013) Cocoa polyphenols suppress adipogenesis in vitro and obesity in vivo by targeting insulin receptor. Int J Obes (Lond) 37:584–592CrossRef Min SY, Yang H, Seo SG, Shin SH, Chung MY, Kim J, Lee SJ, Lee HJ, Lee KW (2013) Cocoa polyphenols suppress adipogenesis in vitro and obesity in vivo by targeting insulin receptor. Int J Obes (Lond) 37:584–592CrossRef
3.
go back to reference Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz BA, Bergmann O, Blomqvist L, Hoffstedt J, Naslund E, Britton T, Concha H, Hassan M, Ryden M, Frisen J, Arner P (2008) Dynamics of fat cell turnover in humans. Nature 453:783–787CrossRef Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz BA, Bergmann O, Blomqvist L, Hoffstedt J, Naslund E, Britton T, Concha H, Hassan M, Ryden M, Frisen J, Arner P (2008) Dynamics of fat cell turnover in humans. Nature 453:783–787CrossRef
4.
go back to reference Gregoire FM, Smas CM, Sul HS (1998) Understanding adipocyte differentiation. Physiol Rev 78:783–809 Gregoire FM, Smas CM, Sul HS (1998) Understanding adipocyte differentiation. Physiol Rev 78:783–809
5.
go back to reference Tang QQ, Lane MD (2012) Adipogenesis: from stem cell to adipocyte. Annu Rev Biochem 81:715–736CrossRef Tang QQ, Lane MD (2012) Adipogenesis: from stem cell to adipocyte. Annu Rev Biochem 81:715–736CrossRef
6.
go back to reference Rosen ED, Walkey CJ, Puigserver P, Spiegelman BM (2000) Transcriptional regulation of adipogenesis. Genes Dev 14:1293–1307 Rosen ED, Walkey CJ, Puigserver P, Spiegelman BM (2000) Transcriptional regulation of adipogenesis. Genes Dev 14:1293–1307
7.
go back to reference Rosen ED, MacDougald OA (2006) Adipocyte differentiation from the inside out. Nat Rev Mol Cell Biol 7:885–896CrossRef Rosen ED, MacDougald OA (2006) Adipocyte differentiation from the inside out. Nat Rev Mol Cell Biol 7:885–896CrossRef
8.
go back to reference Jeong YS, Hong JH, Cho KH, Jung HK (2012) Grape skin extract reduces adipogenesis- and lipogenesis-related gene expression in 3T3-L1 adipocytes through the peroxisome proliferator-activated receptor-gamma signaling pathway. Nutr Res 32:514–521CrossRef Jeong YS, Hong JH, Cho KH, Jung HK (2012) Grape skin extract reduces adipogenesis- and lipogenesis-related gene expression in 3T3-L1 adipocytes through the peroxisome proliferator-activated receptor-gamma signaling pathway. Nutr Res 32:514–521CrossRef
9.
go back to reference Quan HY, Baek NI, Chung SH (2012) Licochalcone A prevents adipocyte differentiation and lipogenesis via suppression of peroxisome proliferator-activated receptor gamma and sterol regulatory element-binding protein pathways. J Agric Food Chem 60:5112–5120CrossRef Quan HY, Baek NI, Chung SH (2012) Licochalcone A prevents adipocyte differentiation and lipogenesis via suppression of peroxisome proliferator-activated receptor gamma and sterol regulatory element-binding protein pathways. J Agric Food Chem 60:5112–5120CrossRef
10.
go back to reference Sanderson M, Mazibuko SE, Joubert E, de Beer D, Johnson R, Pheiffer C, Louw J, Muller CJ (2014) Effects of fermented rooibos (Aspalathus linearis) on adipocyte differentiation. Phytomedicine 21:109–117CrossRef Sanderson M, Mazibuko SE, Joubert E, de Beer D, Johnson R, Pheiffer C, Louw J, Muller CJ (2014) Effects of fermented rooibos (Aspalathus linearis) on adipocyte differentiation. Phytomedicine 21:109–117CrossRef
11.
go back to reference Rossmeisl M, Flachs P, Brauner P, Sponarova J, Matejkova O, Prazak T, Ruzickova J, Bardova K, Kuda O, Kopecky J (2004) Role of energy charge and AMP-activated protein kinase in adipocytes in the control of body fat stores. Int J Obes Relat Metab Disord 28(Suppl 4):S38–S44CrossRef Rossmeisl M, Flachs P, Brauner P, Sponarova J, Matejkova O, Prazak T, Ruzickova J, Bardova K, Kuda O, Kopecky J (2004) Role of energy charge and AMP-activated protein kinase in adipocytes in the control of body fat stores. Int J Obes Relat Metab Disord 28(Suppl 4):S38–S44CrossRef
12.
go back to reference Ono M, Fujimori K (2011) Antiadipogenic effect of dietary apigenin through activation of AMPK in 3T3-L1 cells. J Agric Food Chem 59:13346–13352CrossRef Ono M, Fujimori K (2011) Antiadipogenic effect of dietary apigenin through activation of AMPK in 3T3-L1 cells. J Agric Food Chem 59:13346–13352CrossRef
13.
go back to reference Ku HC, Liu HS, Hung PF, Chen CL, Liu HC, Chang HH, Tsuei YW, Shih LJ, Lin CL, Lin CM, Kao YH (2012) Green tea (−)-epigallocatechin gallate inhibits IGF-I and IGF-II stimulation of 3T3-L1 preadipocyte mitogenesis via the 67-kDa laminin receptor, but not AMP-activated protein kinase pathway. Mol Nutr Food Res 56:580–592CrossRef Ku HC, Liu HS, Hung PF, Chen CL, Liu HC, Chang HH, Tsuei YW, Shih LJ, Lin CL, Lin CM, Kao YH (2012) Green tea (−)-epigallocatechin gallate inhibits IGF-I and IGF-II stimulation of 3T3-L1 preadipocyte mitogenesis via the 67-kDa laminin receptor, but not AMP-activated protein kinase pathway. Mol Nutr Food Res 56:580–592CrossRef
14.
go back to reference Chen L, Song J, Cui J, Hou J, Zheng X, Li C, Liu L (2013) microRNAs regulate adipocyte differentiation. Cell Biol Int 37:533–546CrossRef Chen L, Song J, Cui J, Hou J, Zheng X, Li C, Liu L (2013) microRNAs regulate adipocyte differentiation. Cell Biol Int 37:533–546CrossRef
15.
go back to reference Karbiener M, Fischer C, Nowitsch S, Opriessnig P, Papak C, Ailhaud G, Dani C, Amri EZ, Scheideler M (2009) microRNA miR-27b impairs human adipocyte differentiation and targets PPARgamma. Biochem Biophys Res Commun 390:247–251CrossRef Karbiener M, Fischer C, Nowitsch S, Opriessnig P, Papak C, Ailhaud G, Dani C, Amri EZ, Scheideler M (2009) microRNA miR-27b impairs human adipocyte differentiation and targets PPARgamma. Biochem Biophys Res Commun 390:247–251CrossRef
16.
go back to reference Kim SY, Kim AY, Lee HW, Son YH, Lee GY, Lee J-W, Lee YS, Kim JB (2010) miR-27a is a negative regulator of adipocyte differentiation via suppressing PPARgamma expression. Biochem Biophys Res Commun 392:323–328CrossRef Kim SY, Kim AY, Lee HW, Son YH, Lee GY, Lee J-W, Lee YS, Kim JB (2010) miR-27a is a negative regulator of adipocyte differentiation via suppressing PPARgamma expression. Biochem Biophys Res Commun 392:323–328CrossRef
17.
go back to reference Baselga-Escudero L, Blade C, Ribas-Latre A, Casanova E, Suarez M, Lluis Torres J, Josepa Salvado M, Arola L, Arola-Arnal A (2014) Resveratrol and EGCG bind directly and distinctively to miR-33a and miR-122 and modulate divergently their levels in hepatic cells. Nucleic Acids Res 42:882–892CrossRef Baselga-Escudero L, Blade C, Ribas-Latre A, Casanova E, Suarez M, Lluis Torres J, Josepa Salvado M, Arola L, Arola-Arnal A (2014) Resveratrol and EGCG bind directly and distinctively to miR-33a and miR-122 and modulate divergently their levels in hepatic cells. Nucleic Acids Res 42:882–892CrossRef
18.
go back to reference Arola-Arnal A, Blade C (2011) Proanthocyanidins modulate microRNA expression in human HepG2 cells. PLoS One 6:e25982CrossRef Arola-Arnal A, Blade C (2011) Proanthocyanidins modulate microRNA expression in human HepG2 cells. PLoS One 6:e25982CrossRef
19.
go back to reference Matsumoto K, S-i Yokoyama (2012) Induction of uncoupling protein-1 and -3 in brown adipose tissue by kaki-tannin in type 2 diabetic NSY/Hos mice. Food Chem Toxicol 50:184–190CrossRef Matsumoto K, S-i Yokoyama (2012) Induction of uncoupling protein-1 and -3 in brown adipose tissue by kaki-tannin in type 2 diabetic NSY/Hos mice. Food Chem Toxicol 50:184–190CrossRef
20.
go back to reference Zou B, Li CM, Chen JY, Dong XQ, Zhang Y, Du J (2012) High molecular weight persimmon tannin is a potent hypolipidemic in high-cholesterol diet fed rats. Food Res Int 48:970–977CrossRef Zou B, Li CM, Chen JY, Dong XQ, Zhang Y, Du J (2012) High molecular weight persimmon tannin is a potent hypolipidemic in high-cholesterol diet fed rats. Food Res Int 48:970–977CrossRef
21.
go back to reference Gato N, Kadowaki A, Hashimoto N, Yokoyama S, Matsumoto K (2013) Persimmon fruit tannin-rich fiber reduces cholesterol levels in humans. Ann Nutr Metab 62:1–6CrossRef Gato N, Kadowaki A, Hashimoto N, Yokoyama S, Matsumoto K (2013) Persimmon fruit tannin-rich fiber reduces cholesterol levels in humans. Ann Nutr Metab 62:1–6CrossRef
22.
go back to reference Zou B, Ge ZZ, Zhang Y, Du J, Xu Z, Li CM (2014) Persimmon Tannin accounts for hypolipidemic effects of persimmon through activating of AMPK and suppressing NF-kappaB activation and inflammatory responses in high-fat diet rats. Food Funct 5:1536–1546CrossRef Zou B, Ge ZZ, Zhang Y, Du J, Xu Z, Li CM (2014) Persimmon Tannin accounts for hypolipidemic effects of persimmon through activating of AMPK and suppressing NF-kappaB activation and inflammatory responses in high-fat diet rats. Food Funct 5:1536–1546CrossRef
23.
go back to reference Gu HF, Li CM, Xu YJ, Hu WF, Chen MH, Wan QH (2008) Structural features and antioxidant activity of tannin from persimmon pulp. Food Res Int 41:208–217CrossRef Gu HF, Li CM, Xu YJ, Hu WF, Chen MH, Wan QH (2008) Structural features and antioxidant activity of tannin from persimmon pulp. Food Res Int 41:208–217CrossRef
24.
go back to reference Li C, Leverence R, Trombley JD, Xu S, Yang J, Tian Y, Reed JD, Hagerman AE (2010) High molecular weight persimmon (Diospyros kaki L.) proanthocyanidin: a highly galloylated, a-linked tannin with an unusual flavonol terminal unit, myricetin. J Agric Food Chem 58:9033–9042CrossRef Li C, Leverence R, Trombley JD, Xu S, Yang J, Tian Y, Reed JD, Hagerman AE (2010) High molecular weight persimmon (Diospyros kaki L.) proanthocyanidin: a highly galloylated, a-linked tannin with an unusual flavonol terminal unit, myricetin. J Agric Food Chem 58:9033–9042CrossRef
25.
go back to reference Gahler S, Otto K, Böhm V (2003) Alterations of vitamin C, total phenolics, and antioxidant capacity as affected by processing tomatoes to different products. J Agric Food Chem 51:7962–7968CrossRef Gahler S, Otto K, Böhm V (2003) Alterations of vitamin C, total phenolics, and antioxidant capacity as affected by processing tomatoes to different products. J Agric Food Chem 51:7962–7968CrossRef
26.
go back to reference Zhang T, Sawada K, Yamamoto N, Ashida H (2013) 4-Hydroxyderricin and xanthoangelol from Ashitaba (Angelica keiskei) suppress differentiation of preadiopocytes to adipocytes via AMPK and MAPK pathways. Mol Nutr Food Res 57:1729–1740 Zhang T, Sawada K, Yamamoto N, Ashida H (2013) 4-Hydroxyderricin and xanthoangelol from Ashitaba (Angelica keiskei) suppress differentiation of preadiopocytes to adipocytes via AMPK and MAPK pathways. Mol Nutr Food Res 57:1729–1740
27.
go back to reference Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408CrossRef Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408CrossRef
28.
go back to reference Jeong Y, Jung H, Cho K-H, Youn K-S, Hong J-H (2011) Anti-obesity effect of grape skin extract in 3T3-L1 adipocytes. Food Sci Biotechnol 20:635–642CrossRef Jeong Y, Jung H, Cho K-H, Youn K-S, Hong J-H (2011) Anti-obesity effect of grape skin extract in 3T3-L1 adipocytes. Food Sci Biotechnol 20:635–642CrossRef
29.
go back to reference Kim CY, Le TT, Chen C, Cheng J-X, Kim K-H (2011) Curcumin inhibits adipocyte differentiation through modulation of mitotic clonal expansion. J Nutr Biochem 22:910–920CrossRef Kim CY, Le TT, Chen C, Cheng J-X, Kim K-H (2011) Curcumin inhibits adipocyte differentiation through modulation of mitotic clonal expansion. J Nutr Biochem 22:910–920CrossRef
30.
go back to reference Choi Y, Kim Y, Ham H, Park Y, Jeong HS, Lee J (2011) Nobiletin suppresses adipogenesis by regulating the expression of adipogenic transcription factors and the activation of AMP-activated protein kinase (AMPK). J Agric Food Chem 59:12843–12849CrossRef Choi Y, Kim Y, Ham H, Park Y, Jeong HS, Lee J (2011) Nobiletin suppresses adipogenesis by regulating the expression of adipogenic transcription factors and the activation of AMP-activated protein kinase (AMPK). J Agric Food Chem 59:12843–12849CrossRef
31.
go back to reference Chen YY, Lee MH, Hsu CC, Wei CL, Tsai YC (2012) Methyl cinnamate inhibits adipocyte differentiation via activation of the CaMKK2–AMPK pathway in 3T3-L1 preadipocytes. J Agric Food Chem 60:955–963CrossRef Chen YY, Lee MH, Hsu CC, Wei CL, Tsai YC (2012) Methyl cinnamate inhibits adipocyte differentiation via activation of the CaMKK2–AMPK pathway in 3T3-L1 preadipocytes. J Agric Food Chem 60:955–963CrossRef
32.
go back to reference Kwon JY, Seo SG, Yue S, Cheng JX, Lee KW, Kim KH (2012) An inhibitory effect of resveratrol in the mitotic clonal expansion and insulin signaling pathway in the early phase of adipogenesis. Nutr Res 32:607–616CrossRef Kwon JY, Seo SG, Yue S, Cheng JX, Lee KW, Kim KH (2012) An inhibitory effect of resveratrol in the mitotic clonal expansion and insulin signaling pathway in the early phase of adipogenesis. Nutr Res 32:607–616CrossRef
33.
go back to reference Hung PF, Wu BT, Chen HC, Chen YH, Chen CL, Wu MH, Liu HC, Lee MJ, Kao YH (2005) Antimitogenic effect of green tea (−)-epigallocatechin gallate on 3T3-L1 preadipocytes depends on the ERK and Cdk2 pathways. Am J Physiol Cell Physiol 288:C1094–C1108CrossRef Hung PF, Wu BT, Chen HC, Chen YH, Chen CL, Wu MH, Liu HC, Lee MJ, Kao YH (2005) Antimitogenic effect of green tea (−)-epigallocatechin gallate on 3T3-L1 preadipocytes depends on the ERK and Cdk2 pathways. Am J Physiol Cell Physiol 288:C1094–C1108CrossRef
34.
go back to reference Ren D, Collingwood TN, Rebar EJ, Wolffe AP, Camp HS (2002) PPARgamma knockdown by engineered transcription factors: exogenous PPARgamma2 but not PPARgamma1 reactivates adipogenesis. Genes Dev 16:27–32CrossRef Ren D, Collingwood TN, Rebar EJ, Wolffe AP, Camp HS (2002) PPARgamma knockdown by engineered transcription factors: exogenous PPARgamma2 but not PPARgamma1 reactivates adipogenesis. Genes Dev 16:27–32CrossRef
35.
go back to reference Kim H, Hiraishi A, Tsuchiya K, Sakamoto K (2010) (−) Epigallocatechin gallate suppresses the differentiation of 3T3-L1 preadipocytes through transcription factors FoxO1 and SREBP1c. Cytotechnology 62:245–255CrossRef Kim H, Hiraishi A, Tsuchiya K, Sakamoto K (2010) (−) Epigallocatechin gallate suppresses the differentiation of 3T3-L1 preadipocytes through transcription factors FoxO1 and SREBP1c. Cytotechnology 62:245–255CrossRef
36.
go back to reference Hwang JT, Park IJ, Shin JI, Lee YK, Lee SK, Baik HW, Ha J, Park OJ (2005) Genistein, EGCG, and capsaicin inhibit adipocyte differentiation process via activating AMP-activated protein kinase. Biochem Biophys Res Commun 338:694–699CrossRef Hwang JT, Park IJ, Shin JI, Lee YK, Lee SK, Baik HW, Ha J, Park OJ (2005) Genistein, EGCG, and capsaicin inhibit adipocyte differentiation process via activating AMP-activated protein kinase. Biochem Biophys Res Commun 338:694–699CrossRef
37.
go back to reference Tian Y, Zou B, Li C-m, Yang J, Xu S-f, Hagerman AE (2012) High molecular weight persimmon tannin is a potent antioxidant both ex vivo and in vivo. Food Res Int 45:26–30CrossRef Tian Y, Zou B, Li C-m, Yang J, Xu S-f, Hagerman AE (2012) High molecular weight persimmon tannin is a potent antioxidant both ex vivo and in vivo. Food Res Int 45:26–30CrossRef
38.
go back to reference Lin Q, Gao ZG, Alarcon RM, Ye JP, Yun Z (2009) A role of miR-27 in the regulation of adipogenesis. FEBS J 276:2348–2358CrossRef Lin Q, Gao ZG, Alarcon RM, Ye JP, Yun Z (2009) A role of miR-27 in the regulation of adipogenesis. FEBS J 276:2348–2358CrossRef
39.
go back to reference Verstraeten SV, Jaggers GK, Fraga CG, Oteiza PI (2013) Procyanidins can interact with Caco-2 cell membrane lipid rafts: involvement of cholesterol. BBA-Biomembranes 1828:2646–2653CrossRef Verstraeten SV, Jaggers GK, Fraga CG, Oteiza PI (2013) Procyanidins can interact with Caco-2 cell membrane lipid rafts: involvement of cholesterol. BBA-Biomembranes 1828:2646–2653CrossRef
Metadata
Title
Persimmon tannin represses 3T3-L1 preadipocyte differentiation via up-regulating expression of miR-27 and down-regulating expression of peroxisome proliferator-activated receptor-γ in the early phase of adipogenesis
Authors
Bo Zou
Zhenzhen Ge
Wei Zhu
Ze Xu
Chunmei Li
Publication date
01-12-2015
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 8/2015
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-014-0814-9

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