Journal of Nutrition and Health

The Korean Nutrition Society (한국영양학회)
권호 표지
DOI QR코드

DOI QR Code

Antioxidant and antiobesity activities of oral treatment with ethanol extract from sprout of evening primrose (Oenothera laciniata) in high fat diet-induced obese mice

달맞이순 (Oenothera laciniata) 에탄올 추출물 섭취가 고지방식이로 유도한 비만 마우스에서 항산화 및 비만억제효과

  • Received : 2019.10.02
  • Accepted : 2019.11.11
  • Published : 2019.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Purpose: Sprouts of evening primrose (Oenothera laciniata, OL) were reported to have high contents of flavonoids and potent antioxidant activity. This study examined the antioxidant and antiobesity activities of OL sprouts to determine if they could be a natural health-beneficial resource preventing obesity and oxidative stress. Methods: OL sprouts were extracted with 50% ethanol, evaporated, and lyophilized (OLE). The in vitro antioxidant activity of OLE was examined using four different tests. The antiobesity activity and in vivo antioxidant activity from OLE consumption were examined using high fat diet-induced obese (DIO) C57BL/6 mice. Results: The IC50 for the 2,2-diphenyl-1-picryl-hydrazyl (DPPH) radical scavenging and superoxide dismutase (SOD)-like activities of OLE were 26.2 ㎍/mL and 327.6 ㎍/mL, respectively. OLE exhibited the ferric reducing antioxidant power (FRAP) activity of 56.7 ㎍ ascorbic acid eq./mL at 100 ㎍/mL, and an increased glutathione level by 65.1% at 200 ㎍/mL compared to the control in the hUC-MSC stem cells. In an animal study, oral treatment with 50 mg or 100 mg of OLE/kg body weight for 14 weeks reduced the body weight gain, visceral fat content, fat cell size, blood leptin, and triglyceride levels, as well as the atherogenic index compared to the high fat diet control group (HFC) (p < 0.05). The blood malondialdehyde (MDA) level and the catalase and SOD-1 activities in adipose tissue were reduced significantly by the OLE treatment compared to HFC as well (p < 0.05). In epididymal adipose tissue, the OLE treatment reduced the mRNA expression of leptin, PPAR-γ and FAS significantly (p < 0.05) compared to HFC while it increased adiponectin expression (p < 0.05). Conclusion: OLE consumption has potent antioxidant and antiobesity activities via the suppression of oxidative stress and lipogenesis in DIO mice. Therefore, OLE could be a good candidate as a natural resource to develop functional food products that prevent obesity and oxidative stress.

본 연구에서는 달맞이순의 항산화 및 항비만효과를 확인하기 위하여 건달맞이순 50% 에탄올 추출물 (OLE)을 이용하여 4가지 방법으로 in vitro 항산화효과를 측정하였고, C57BL/6 마우스에게 고지방식이 (45%Kcal fat)를 14주 동안 섭취시켜 비만을 유도하면서 OLE를 경구 투여하여 항비만효과와 in vivo 항산화효과를 알아보았다. OLE의 DPPH 라디칼 소거능과 SOD 유사 활성을 측정한 결과 IC50은 각각 26.2 ㎍/mL과 327.6 ㎍/mL이었으며, FRAP 측정 결과 100 ㎍/mL 농도에서 56.7 ㎍ AA eq./mL의 효능을 보였다. 또한, hUC-MSC 세포에 OLE (200 ㎍/mL)를 처리 한 결과 노화로 인하여 감소된 GSH 수준을 65.1% 증가시켰다. 한편, 마우스에게 고지방식이와 함께 OLE를 저수준 (50 mg/kg BW; OL50)과 고수준 (100 mg/kg BW; OL100)으로 경구 투여한 결과 체중증가량은 대조군에 비하여 각각 41.5%와 42.2% 감소하였고, 내장지방량은 각각 40.5%와 45.9% 감소하였으며, 부고환지방세포의 크기는 각각 33.1%와 35.3% 감소하여 매우 우수한 비만억제효과를 보였다 (p < 0.05). OLE의 경구 투여는 고지방식이 대조군에 비하여 혈중 렙틴 농도와 중성지방 농도를 유의하게 감소시켰고, 특히 OL100군에서는 동맥경화지수 및 혈중 MDA 농도도 유의하게 감소하였다 (p < 0.05). 마우스 지방조직에서 측정한 catalase와 SOD-1의 활성은 고지방식이섭취로 인하여 증가하였으나 OLE 경구 투여 시 유의하게 감소하였다 (p < 0.05). 또한, 부고환 지방에서 지방대사 관련 인자들의 mRNA 발현량을 RT-PCR로 측정한 결과 OLE의 경구 투여는 고지방식이 섭취로 인하여 증가하였던 렙틴, PPARγ와 FAS의 발현을 유의하게 감소시킨 반면 고지방식이 섭취로 감소되었던 아디포넥틴의 발현량은 유의하게 증가시켰다 (p < 0.05). 고지방식이로 인하여 증가하였던 CPT-1의 발현량은 OLE 투여시 감소되는 경향을 보였으며, SREBP-1c의 발현량은 실험군 간에 유의한 차이가 없었다. 이들 연구결과를 종합하면, in vitro 항산화효과가 우수한 OLE를 고지방식이로 유도된 비만 마우스에게 경구 투여하였을 때 체내 산화적 스트레스를 낮추고, 지방합성을 억제함으로써 체중과 내장 지방량의 증가를 억제시키는 항비만 효과를 나타내었다. 따라서, OLE는 항산화기능식품 또는 비만 및 비만관련 만성질환을 예방하는 기능성식품의 개발에 기능성 천연소재로 활용될 수 있으리라 기대된다.

Keywords

References

  1. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004; 114(12): 1752-1761. https://doi.org/10.1172/JCI21625
  2. Nam YR, Won SB, Chung YS, Kwak CS, Kwon YH. Inhibitory effects of Doenjang, Korean traditional fermented soybean paste, on oxidative stress and inflammation in adipose tissue of mice fed a high-fat diet. Nutr Res Pract 2015; 9(3): 235-241. https://doi.org/10.4162/nrp.2015.9.3.235
  3. da Costa GF, Santos IB, de Bem GF, Cordeiro VS, da Costa CA, de Carvalho LC, et al. The beneficial effect of anthocyanidin-rich Vitis vinifera L. grape skin extract on metabolic changes induced by high-fat diet in mice involves antiinflammatory and antioxidant actions. Phytother Res 2017; 31(10): 1621-1632. https://doi.org/10.1002/ptr.5898
  4. Charradi K, Elkahoui S, Limam F, Aouani E. High-fat diet induced an oxidative stress in white adipose tissue and disturbed plasma transition metals in rat: prevention by grape seed and skin extract. J Physiol Sci 2013; 63(6): 445-455. https://doi.org/10.1007/s12576-013-0283-6
  5. Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunol 2011; 29: 415-445. https://doi.org/10.1146/annurev-immunol-031210-101322
  6. Galinier A, Carriere A, Fernandez Y, Carpene C, Andre M, Caspar-Bauguil S, et al. Adipose tissue proadipogenic redox changes in obesity. J Biol Chem 2006; 281(18): 12682-12687. https://doi.org/10.1074/jbc.M506949200
  7. Carrasco-Pozo C, Cires MJ, Gotteland M. Quercetin and epigallocatechin gallate in the prevention and treatment of obesity: from molecular to clinical studies. J Med Food 2019; 22(8): 753-770. https://doi.org/10.1089/jmf.2018.0193
  8. Kowalska K, Olejnik A, Szwajgier D, Olkowicz M. Inhibitory activity of chokeberry, bilberry, raspberry and cranberry polyphenol-rich extract towards adipogenesis and oxidative stress in differentiated 3T3-L1 adipose cells. PLoS One 2017; 12(11): e0188583. https://doi.org/10.1371/journal.pone.0188583
  9. Lee OH, Seo MJ, Choi HS, Lee BY. Pycnogenol(R) inhibits lipid accumulation in 3T3-L1 adipocytes with the modulation of reactive oxygen species (ROS) production associated with antioxidant enzyme responses. Phytother Res 2012; 26(3): 403-411. https://doi.org/10.1002/ptr.3568
  10. Zhao Y, Chen B, Shen J, Wan L, Zhu Y, Yi T, et al. The beneficial effects of quercetin, curcumin, and resveratrol in obesity. Oxid Med Cell Longev 2017; 2017: 1459497.
  11. Kim HJ, Kim B, Mun EG, Jeong SY, Cha YS. The antioxidant activity of steamed ginger and its protective effects on obesity induced by high-fat diet in C57BL/6J mice. Nutr Res Pract 2018; 12(6): 503-511. https://doi.org/10.4162/nrp.2018.12.6.503
  12. Kim JH, Kim OK, Yoon HG, Park J, You Y, Kim K, et al. Anti-obesity effect of extract from fermented Curcuma longa L. through regulation of adipogenesis and lipolysis pathway in high-fat diet-induced obese rats. Food Nutr Res 2016; 60(1): 30428. https://doi.org/10.3402/fnr.v60.30428
  13. Tuzcu Z, Orhan C, Sahin N, Juturu V, Sahin K. Cinnamon polyphenol extract inhibits hyperlipidemia and inflammation by modulation of transcription factors in high-fat diet-fed rats. Oxid Med Cell Longev 2017; 2017: 1583098. https://doi.org/10.1155/2017/1583098
  14. Castro-Barquero S, Lamuela-Raventos RM, Domenech M, Estruch R. Relationship between Mediterranean dietary polyphenol intake and obesity. Nutrients 2018; 10(10): 1523. https://doi.org/10.3390/nu10101523
  15. Naowaboot J, Wannasiri S, Pannangpetch P. Morin attenuates hepatic insulin resistance in high-fat-diet-induced obese mice. J Physiol Biochem 2016; 72(2): 269-280. https://doi.org/10.1007/s13105-016-0477-5
  16. Fenni S, Hammou H, Astier J, Bonnet L, Karkeni E, Couturier C, et al. Lycopene and tomato powder supplementation similarly inhibit high-fat diet induced obesity, inflammatory response, and associated metabolic disorders. Mol Nutr Food Res 2017; 61(9): 1601083. https://doi.org/10.1002/mnfr.201601083
  17. Gonzalez-Castejon M, Rodriguez-Casado A. Dietary phytochemicals and their potential effects on obesity: a review. Pharmacol Res 2011; 64(5): 438-455. https://doi.org/10.1016/j.phrs.2011.07.004
  18. Timoszuk M, Bielawska K, Skrzydlewska E. Evening primrose (Oenothera biennis) biological activity dependent on chemical composition. Antioxidants 2018; 7(8): 108. https://doi.org/10.3390/antiox7080108
  19. Yoon WJ, Ham YM, Yoo BS, Moon JY, Koh J, Hyun CG. Oenothera laciniata inhibits lipopolysaccharide induced production of nitric oxide, prostaglandin E2, and proinflammatory cytokines in RAW264.7 macrophages. J Biosci Bioeng 2009; 107(4): 429-438. https://doi.org/10.1016/j.jbiosc.2008.11.018
  20. Garnica S, Czerwinska ME, Piwowarski JP, Ziaja M, Kiss AK. Chemical composition, antioxidative and anti-inflammatory activity of extracts prepared from aerial parts of Oenothera biennis L. anf Oenothera paradoxa Hudziok obtained after seeds cultivation. J Agric Food Chem 2013; 61(4): 801-810. https://doi.org/10.1021/jf304002h
  21. Kwak CS, Lee JH. In vitro antioxidant and antiinflammatory effects of ethanol extracts from sprout of evening primrose (Oenothera laciniata) and gooseberry (Actinidia arguta). J Korean Soc Food Sci Nutr 2014; 43(2): 207-215. https://doi.org/10.3746/JKFN.2014.43.2.207
  22. Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 1974; 47(3): 469-474. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x
  23. Jeong EM, Shin JW, Lim J, Kim JH, Kang H, Yin Y, et al. Monitoring glutathione dynamics and heterogeneity in living stem cells. Int J Stem Cells 2019; 12(2): 367-379. https://doi.org/10.15283/ijsc18151
  24. Aebi H. Catalase in vitro. Methods Enzymol 1984; 105: 121-126. https://doi.org/10.1016/S0076-6879(84)05016-3
  25. Tappel AL. Glutathione peroxidase and hydroperoxides. Methods Enzymol 1978; 52: 506-513. https://doi.org/10.1016/S0076-6879(78)52055-7
  26. Yen GC, Chen HY. Antioxidant activity of various tea extracts in relation to their antimutagenicity. J Agric Food Chem 1995; 43(1): 27-32. https://doi.org/10.1021/jf00049a007
  27. Yang SL, Yu PL, Chung KR. The glutathione peroxidasemediated reactive oxygen species resistance, fungicide sensitivity and cell wall construction in the citrus fungal pathogen Alternaria alternata. Environ Microbiol 2016; 18(3): 923-935. https://doi.org/10.1111/1462-2920.13125
  28. Lee YS, Kim AY, Choi JW, Kim M, Yasue S, Son HJ, et al. Dysregulation of adipose glutathione peroxidase 3 in obesity contributes to local and systemic oxidative stress. Mol Endocrinol 2008; 22(9): 2176-2189. https://doi.org/10.1210/me.2008-0023
  29. Kobayashi H, Matsuda M, Fukuhara A, Komuro R, Shimomura I. Dysregulated glutathione metabolism links to impaired insulin action in adipocytes. Am J Physiol Endocrinol Metab 2009; 296(6): E1326-E1334. https://doi.org/10.1152/ajpendo.90921.2008
  30. Wu T, Yin J, Zhang G, Long H, Zheng X. Mulberry and cherry anthocyanin consumption prevents oxidative stress and inflammation in diet-induced obese mice. Mol Nutr Food Res 2016; 60(3): 687-694. https://doi.org/10.1002/mnfr.201500734
  31. Mounien L, Tourniaire F, Landrier JF. Anti-obesity effect of carotenoids: direct impact on adipose tissue and adipose tissue-driven indirect effects. Nutrients 2019; 11(7): 1562. https://doi.org/10.3390/nu11071562
  32. Rivera L, Moron R, Sanchez M, Zarzuelo A, Galisteo M. Quercetin ameliorates metabolic syndrome and improves the inflammatory status in obese Zucker rats. Obesity (Silver Spring) 2008; 16(9): 2081-2087. https://doi.org/10.1038/oby.2008.315
  33. Dong J, Zhang X, Zhang L, Bian HX, Xu N, Bao B, et al. Quercetin reduces obesity-associated ATM infiltration and inflammation in mice: a mechanism including $AMPK{\alpha}1/SIRT1$. J Lipid Res 2014; 55(3): 363-374. https://doi.org/10.1194/jlr.M038786
  34. Cialdella-Kam L, Ghosh S, Meaney MP, Knab AM, Shanely RA, Nieman DC. Quercetin and green tea extract supplementation downregulates genes related to tissue inflammatory responses to a 12-week high fat-diet in mice. Nutrients 2017; 9(7): E773.
  35. Lee JS, Cha YJ, Lee KH, Yim JE. Onion peel extract reduces the percentage of body fat in overweight and obese subjects: a 12-week, randomized, double-blind, placebo-controlled study. Nutr Res Pract 2016; 10(2): 175-181. https://doi.org/10.4162/nrp.2016.10.2.175
  36. Gentile D, Fornai M, Pellegrini C, Colucci R, Benvenuti L, Duranti E, et al. Luteolin prevents cardiometabolic alterations and vascular dysfunction in mice with HFD-induced obesity. Front Pharmacol 2018; 9: 1094. https://doi.org/10.3389/fphar.2018.01094
  37. Liu Y, Fu X, Lan N, Li S, Zhang J, Wang S, et al. Luteolin protects against high fat diet-induced cognitive deficits in obesity mice. Behav Brain Res 2014; 267: 178-188. https://doi.org/10.1016/j.bbr.2014.02.040

Cited by

  1. In Vitro Anti-Wrinkle and Skin-Moisturizing Effects of Evening Primrose (Oenothera biennis) Sprout and Identification of Its Active Components vol.9, pp.1, 2019, https://doi.org/10.3390/pr9010145
  2. Development and Validation of a Method for Determining the Quercetin-3- O -glucuronide and Ellagic Acid Content of Common Evening Primrose ( Oenothera biennis ) by HPLC-UVD vol.26, pp.2, 2019, https://doi.org/10.3390/molecules26020267
  3. Effect of the Oral Administration of Common Evening Primrose Sprout (Oenothera biennis L.) Extract on Skin Function Improvement in UVB-irradiated Hairless Mice vol.14, pp.3, 2021, https://doi.org/10.3390/ph14030222
  4. Antioxidant and Anti-Obesity Potentials of Korean-Native Wild Vegetables (Allium species) vol.7, pp.12, 2019, https://doi.org/10.3390/horticulturae7120541