Preventive Nutrition and Food Science

The Korean Society of Food Science and Nutrition (한국식품영양과학회)
권호 표지
DOI QR코드

DOI QR Code

Rosehip Extract Inhibits Lipid Accumulation in White Adipose Tissue by Suppressing the Expression of Peroxisome Proliferator-activated Receptor Gamma

  • Nagatomo, Akifumi (Research and Development Division, Morishita Jintan Co., Ltd.) ;
  • Nishida, Norihisa (Research and Development Division, Morishita Jintan Co., Ltd.) ;
  • Matsuura, Yoichi (Research and Development Division, Morishita Jintan Co., Ltd.) ;
  • Shibata, Nobuhito (Department of Biopharmaceutics, Faculty of Pharmaceutical Sciences, Doshisha Women's College of Liberal Arts)
  • Received : 2013.04.22
  • Accepted : 2013.05.21
  • Published : 2013.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Recent studies have shown that Rosa canina L. and tiliroside, the principal constituent of its seeds, exhibit anti-obesity and anti-diabetic activities via enhancement of fatty acid oxidation in the liver and skeletal muscle. However, the effects of rosehip, the fruit of this plant, extract (RHE), or tiliroside on lipid accumulation in adipocytes have not been analyzed. We investigated the effects of RHE and tiliroside on lipid accumulation and protein expression of key transcription factors in both in vitro and in vivo models. RHE and tiliroside inhibited lipid accumulation in a dose-dependent manner in 3T3-L1 cells. We also analyzed the inhibitory effect of RHE on white adipose tissue (WAT) in high-fat diet (HFD)-induced obesity mice model. Male C57BL/6J mice were fed HFD or HFD supplemented with 1% RHE (HFDRH) for 8 weeks. The HFDRH-fed group gained less body weight and had less visceral fat than the HFD-fed group. Liver weight was significantly lower in the HFDRH-fed group and total hepatic lipid and triglyceride (TG) content was also reduced. A significant reduction in the expression of peroxisome proliferator-activated receptor gamma (PPAR${\gamma}$) was observed in epididymal fat in the HFDRH-fed group, in comparison with controls, through Western blotting. These results suggest that downregulation of PPAR${\gamma}$ expression is involved, at least in part, in the suppressive effect of RHE on lipid accumulation in WAT.

Keywords

References

  1. Crowley VE. 2008. Overview of human obesity and central mechanisms regulating energy homeostasis. Ann Clin Biochem 45: 245-255. https://doi.org/10.1258/acb.2007.007193
  2. Ninomiya K, Matsuda H, Kubo M, Morikawa T, Nishida N, Yoshikawa M. 2007. Potent anti-obese principle from Rosa canina: structural requirements and mode of action of transtiliroside. Bioorg Med Chem Lett 17: 3059-3064. https://doi.org/10.1016/j.bmcl.2007.03.051
  3. Stralsjo L, Alklint C, Olsson ME, Sjoholm I. 2003. Total folate content and retention in rosehips (Rosa ssp.) after drying. J Agric Food Chem 51: 4291-4295. https://doi.org/10.1021/jf034208q
  4. Daels-Rakotoarison DA, Gressier B, Trotin F, Brunet C, Luyckx M, Dine T, Bailleul F, Cazin M, Cazin JC. 2002. Effects of Rosa canina fruit extract on neutrophil respiratory burst. Phytother Res 16: 157-161. https://doi.org/10.1002/ptr.985
  5. Hodisan T, Culea M, Cimpoiu C, Cot A. 1998. Separation, identification and quantitative determination of free amino acids from plant extracts. J Pharm Biomed Anal 18: 319-323. https://doi.org/10.1016/S0731-7085(98)00094-6
  6. Goto T, Teraminami A, Lee JY, Ohyama K, Funakoshi K, Kim YI, Hirai S, Uemura T, Yu R, Takahashi N, Kawada T. 2012. Tiliroside, a glycosidic flavonoid, ameliorates obesity-induced metabolic disorders via activation of adiponectin signaling followed by enhancement of fatty acid oxidation in liver and skeletal muscle in obese-diabetic mice. J Nutr Biochem 23: 768-776. https://doi.org/10.1016/j.jnutbio.2011.04.001
  7. Qin N, Li CB, Jin MN, Shi LH, Duan HQ, Niu WY. 2011. Synthesis and biological activity of novel tiliroside derivants. Eur J Med Chem 46: 5189-5195. https://doi.org/10.1016/j.ejmech.2011.07.059
  8. Andersson U, Henriksson E, Ström K, Alenfall J, Göransson O, Holm C. 2011. Rose hip exerts antidiabetic effects via a mechanism involving downregulation of the hepatic lipogenic program. Am J Physiol Endocrinol Metab 300: E111-E121. https://doi.org/10.1152/ajpendo.00268.2010
  9. Matsuda H, Ninomiya K, Shimoda H, Yoshikawa M. 2002. Hepatoprotective principles from the flowers of Tilia argentea (linden): structure requirements of tiliroside and mechanisms of action. Bioorg Med Chem 10: 707-712. https://doi.org/10.1016/S0968-0896(01)00321-2
  10. Tsukamoto S, Tomise K, Aburatani M, Onuki H, Hirota H, Ishiharajima E, Ohta T. 2004. Isolation of cytochrome P450 inhibitors from strawberry fruit, Fragaria ananassa. J Nat Prod 67: 1839-1841. https://doi.org/10.1021/np0400104
  11. Lu YH, Chen J, Wei DZ, Wang ZT, Tao XY. 2009. Tyrosinase inhibitory effect and inhibitory mechanism of tiliroside from raspberry. J Enzyme Inhib Med Chem 24: 1154-1160. https://doi.org/10.1080/14756360802694252
  12. Sala A, Recio MC, Schinella GR, Máñez S, Giner RM, Cerdá- Nicolás M, Rosí JL. 2003. Assessment of the anti-inflammatory activity and free radical scavenger activity of tiliroside. Eur J Pharmacol 461: 53-61. https://doi.org/10.1016/S0014-2999(02)02953-9
  13. Tomczyk M, Drozdowska D, Bielawska A, Bielawski K, Gudej J. 2008. Human DNA topoisomerase inhibitors from Potentilla argentea and their cytotoxic effect against MCF-7. Pharmazie 63: 389-393.
  14. Rao YK, Geethangili M, Fang SH, Tzeng YM. 2007. Antioxidant and cytotoxic activities of naturally occurring phenolic and related compounds: a comparative study. Food Chem Toxicol 45: 1770-1776. https://doi.org/10.1016/j.fct.2007.03.012
  15. Goto T, Horita M, Nagai H, Nagatomo A, Nishida N, Matsuura Y, Nagaoka S. 2012. Tiliroside, a glycosidic flavonoid, inhibits carbohydrate digestion and glucose absorption in the gastrointestinal tract. Mol Nutr Food Res 56: 435-445. https://doi.org/10.1002/mnfr.201100458
  16. Folch J, Lees M, Sloane Stanley GH. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226: 497-509.
  17. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685. https://doi.org/10.1038/227680a0
  18. Moreno M, Lombardi A, Silvestri E, Senese R, Cioffi F, Goglia F, Lanni A, Lange P. 2010. PPARs: Nuclear receptors controlled by, and controlling, nutrient handling through nuclear and cytosolic signaling. PPAR Res 2010: doi:10.1155/2010/435689
  19. Wu Z, Xie Y, Bucher NL, Farmer SR. 1995. Conditional ectopic expression of C/EBP beta in NIH-3T3 cells induces PPAR gamma and stimulates adipogenesis. Genes Dev 9: 2350-2363. https://doi.org/10.1101/gad.9.19.2350
  20. He W, Barak Y, Hevener A, Olson P, Liao D, Le J, Nelson M, Ong E, Olefsky JM, Evans R. 2003. Adipose-specific peroxisome proliferator-activated receptor $\gamma$ knockout causes insulin resistance in fat and liver but not in muscle. Proc Natl Acad Sci USA 100: 15712-15717. https://doi.org/10.1073/pnas.2536828100
  21. Abbas A, Blandon J, Rude J, Elfar A, Mukherjee D. 2012. PPAR-$\gamma$ agonist in treatment of diabetes: cardiovascular safety considerations. Cardiovasc Hematol Agents Med Chem 10: 124-134. https://doi.org/10.2174/187152512800388948
  22. Nissen SE, Wolski K. 2007. Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. N Engl J Med 356: 2457-2471. https://doi.org/10.1056/NEJMoa072761
  23. Grey A, Bolland M, Gamble G, Wattie D, Horne A, Davidson J, Reid IR. 2007. The peroxisome proliferator-activated receptor-g agonist rosiglitazone decreases bone formation and bone mineral density in healthy postmenopausal women. A randomized, controlled trial. J Clin Endocrinol Metab 92: 1305-1310. https://doi.org/10.1210/jc.2006-2646
  24. Rayalam S, Della-Fera MA, Yang JY, Park HJ, Ambati S, Baile CA. 2007. Resveratrol potentiates genistein's antiadipogenic and proapoptotic effects in 3T3-L1 adipocytes. J Nutr 137: 2668-2673. https://doi.org/10.1093/jn/137.12.2668
  25. Ejaz A, Wu D, Kwan P, Meydani M. 2009. Curcumin inhibits adipogenesis in 3T3-L1 adipocytes and angiogenesis and obesity in C57/BL mice. J Nutr 139: 919-925. https://doi.org/10.3945/jn.108.100966
  26. Roh C, Park MK, Shin HJ, Jung U, Kim JK. 2012. Buddleja officinalis Maximowicz extract inhibits lipid accumulation on adipocyte differentiation in 3T3-L1 cells and high-fat mice. Molecules 17: 8687-8695. https://doi.org/10.3390/molecules17078687
  27. Gu W, Kim KA, Kim DH. 2013. Ginsenoside Rh1 ameliorates high fat diet-induced obesity in mice by inhibiting adipocyte differentiation. Biol Pharm Bull 36: 102-107.
  28. Park UH, Jeong JC, Jang JS, Sung MR, Youn H, Lee SJ, Kim EJ, Um SJ. 2012. Negative regulation of adipogenesis by kaempferol, a component of Rhizoma Polygonati falcatum in 3T3-L1 cells. Biol Pharm Bull 35: 1525-1533. https://doi.org/10.1248/bpb.b12-00254
  29. Huang C, Zhang Y, Gong Z, Sheng X, Li Z, Zhang W, Qin Y. 2006. Berberine inhibits 3T3-L1 adipocyte differentiation through the PPAR$\gamma$ pathway. Biochem Biophys Res Commun 348: 571-578. https://doi.org/10.1016/j.bbrc.2006.07.095
  30. Yun CL, Zierath JR. 2006. AMP-activated protein kinase signaling in metabolic regulation. J Clin Invest 116: 1776- 1783. https://doi.org/10.1172/JCI29044
  31. Carling D. 2004. The AMP-activated protein kinase cascade− a unifying system for energy control. Trends Biochem Sci 29: 18-24. https://doi.org/10.1016/j.tibs.2003.11.005
  32. Hardie DG, Hawley SA, Scott JW. 2006. AMP-activated protein kinase − development of the energy sensor concept. J Physiol 574: 7-15. https://doi.org/10.1113/jphysiol.2006.108944
  33. Witczak CA, Sharoff CG, Goodyear LJ. 2008. AMP-activated protein kinase in skeletal muscle: from structure and localization to its role as a master regulator of cellular metabolism. Cell Mol Life Sci 65: 3737-3755. https://doi.org/10.1007/s00018-008-8244-6
  34. Habinowski SA, Witters LA. 2001. The effect of AICAR on adipocyte differentiation of 3T3-L1 cells. Biochem Biophys Res Commun 286: 852-858. https://doi.org/10.1006/bbrc.2001.5484
  35. Dagon Y, Avraham Y, Berry EM. 2006. AMPK activation regulates apoptosis, adipogenesis, and lipolysis by elF2alpha in adipocytes. Biochem Biophys Res Commun 340: 43-47. https://doi.org/10.1016/j.bbrc.2005.11.159

Cited by

  1. Rose hip as an underutilized functional food: Evidence-based review vol.63, 2017, https://doi.org/10.1016/j.tifs.2017.03.001
  2. The flower of Edgeworthia gardneri (wall.) Meisn. suppresses adipogenesis through modulation of the AMPK pathway in 3T3-L1 adipocytes vol.191, 2016, https://doi.org/10.1016/j.jep.2016.06.059
  3. Ameliorative effects of green tea seed extract with rose hip powder (Rosa caninaL.) on regulation of pain and inflammatory cytokines in a rat model of monosodium iodoacetate-induced experimental osteoarthritis vol.19, pp.1, 2015, https://doi.org/10.1080/19768354.2014.990058
  4. Exploring the anti-diabetic potential of Australian Aboriginal and Indian Ayurvedic plant extracts using cell-based assays vol.15, pp.1, 2015, https://doi.org/10.1186/s12906-015-0524-8
  5. Rose hip supplementation increases energy expenditure and induces browning of white adipose tissue vol.13, pp.1, 2016, https://doi.org/10.1186/s12986-016-0151-5
  6. Evaluation of genotoxicity and subchronic toxicity of standardized rose hip extract 2017, https://doi.org/10.1177/0960327117730881
  7. Dietary rose hip exerts antiatherosclerotic effects and increases nitric oxide-mediated dilation in ApoE-null mice vol.44, 2017, https://doi.org/10.1016/j.jnutbio.2017.02.017
  8. Therapeutic Applications of Rose Hips from Different Rosa Species vol.18, pp.6, 2017, https://doi.org/10.3390/ijms18061137
  9. A Review on the Dietary Flavonoid Tiliroside vol.17, pp.5, 2018, https://doi.org/10.1111/1541-4337.12389
  10. Daily intake of rosehip extract decreases abdominal visceral fat in preobese subjects: a randomized, double-blind, placebo-controlled clinical trial vol.8, pp.None, 2015, https://doi.org/10.2147/dmso.s78623
  11. Effect of Quercetin on Lipids Metabolism Through Modulating the Gut Microbial and AMPK/PPAR Signaling Pathway in Broilers vol.9, pp.None, 2013, https://doi.org/10.3389/fcell.2021.616219
  12. Nutraceutical potential of rose hips of three wild Rosa species from Western Himalaya, India vol.49, pp.4, 2013, https://doi.org/10.15835/nbha49412471