nach oben

European Journal of Nutrition

Erschienen in:

18.01.2022 | Original Contribution

Pomegranate peel anthocyanins prevent diet-induced obesity and insulin resistance in association with modulation of the gut microbiota in mice

verfasst von: Haizhao Song, Xinchun Shen, Rou Deng, Qiang Chu, Xiaodong Zheng

Erschienen in: European Journal of Nutrition | Ausgabe 4/2022

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Pomegranate peels are rich in anthocyanins. The present study aimed to explore the beneficial effects of pomegranate peel anthocyanins (PPA) on obesity and gut microbiota in mice with high-fat diet (HFD)-induced obesity.

Methods

Specific pathogen-free (SPF) male C57BL/6 J mice were randomly divided into three groups and fed with low-fat diet (LFD, 10% fat energy), HFD (45% fat energy), or HFD supplemented with PPA by intragastric administration for 15 weeks. Body weight and food intake were monitored weekly. The obesity-related biochemical indexes and hepatic gene expression levels were determined. The compositions of the gut microbiota were analyzed by 16S rRNA sequencing, and the association between the gut microbiota and obesity-related indicators was investigated by Spearman correlation analysis.

Results

The results showed that the body weight gain, steatosis scores and insulin resistance index in the PPA group decreased by 27.46%, 56.25%, and 46.07%, respectively, compared to the HFD group. Gene expression analysis indicated that PPA supplement improved the genes expression profiles involved in glucose and lipid metabolism compared with the mice fed HFD alone. Meanwhile, PPA significantly changed the composition of the gut microbiota, which were closely correlated with the obesity-related biomarkers.

Conclusion

This study suggested that PPA could be a beneficial treatment option for alleviating HFD-induced obesity and related metabolic disorders by targeting microbiota and lipid metabolism.

Nur mit Berechtigung zugänglich

Despres JP, Lemieux I (2006) Abdominal obesity and metabolic syndrome. Nature 444(7121):881–887. https://doi.org/10.1038/nature05488CrossRefPubMed

Authors N (2013) Obesity and food science being part of the solution. J Food Sci. https://doi.org/10.1111/1750-3841.12261CrossRef

Yun JW (2010) Possible anti-obesity therapeutics from nature—a review. Phytochemistry 71(14–15):1625–1641. https://doi.org/10.1016/j.phytochem.2010.07.011CrossRefPubMed

Powell TM, Khera A (2010) Therapeutic approaches to obesity. Curr Treat Options Cardiovasc Med 12(4):381–395. https://doi.org/10.1007/s11936-010-0080-yCrossRefPubMed

Wang Q, Jiao L, He C, Sun H, Cai Q, Han T, Hu H (2017) Alteration of gut microbiota in association with cholesterol gallstone formation in mice. BMC Gastroenterol 17(1):74. https://doi.org/10.1186/s12876-017-0629-2CrossRefPubMedPubMedCentral

Canfora EE, Meex RCR, Venema K, Blaak EE (2019) Gut microbial metabolites in obesity, NAFLD and T2DM. Nat Rev Endocrinol 15(5):261–273. https://doi.org/10.1038/s41574-019-0156-zCrossRefPubMed

Qiu X, Macchietto MG, Liu X, Lu Y, Ma Y, Guo H, Saqui-Salces M, Bernlohr DA, Chen C, Shen S, Chen X (2021) Identification of gut microbiota and microbial metabolites regulated by an antimicrobial peptide lipocalin 2 in high fat diet-induced obesity. Int J Obesity 45(1):143–154. https://doi.org/10.1038/s41366-020-00712-2CrossRef

Crovesy L, Masterson D, Rosado EL (2020) Profile of the gut microbiota of adults with obesity: a systematic review. Eur J Clin Nutr 74(9):1251–1262. https://doi.org/10.1038/s41430-020-0607-6CrossRefPubMed

Delzenne NM, Rodriguez J, Olivares M, Neyrinck AM (2020) Microbiome response to diet: focus on obesity and related diseases. Rev Endocr Metab Dis 21(3):369–380. https://doi.org/10.1007/s11154-020-09572-7CrossRef

10.

Hou D, Zhao Q, Yousaf L, Xue Y, Shen Q (2021) Beneficial effects of mung bean seed coat on the prevention of high-fat diet-induced obesity and the modulation of gut microbiota in mice. Eur J Nutr 60(4):2029–2045. https://doi.org/10.1007/s00394-020-02395-xCrossRefPubMed

11.

Chen J, He X, Huang J (2014) Diet effects in gut microbiome and obesity. J Food Sci 79(4):R442-451. https://doi.org/10.1111/1750-3841.12397CrossRefPubMed

12.

Sonnenburg JL, Bäckhed F (2016) Diet–microbiota interactions as moderators of human metabolism. Nature 535(7610):56–64. https://doi.org/10.1038/nature18846CrossRefPubMedPubMedCentral

13.

Portune KJ, Benítez-Páez A, Del Pulgar EMG, Cerrudo V, Sanz Y (2017) Gut microbiota, diet, and obesity-related disorders—the good, the bad, and the future challenges. Mol Nutri Food Res 61(1):1600252. https://doi.org/10.1002/mnfr.201600252CrossRef

14.

Fu C, Jiang Y, Guo J, Su Z (2016) Natural products with anti-obesity effects and different mechanisms of action. J Agric Food Chem 64(51):9571–9585. https://doi.org/10.1021/acs.jafc.6b04468CrossRefPubMed

15.

Salehi B, Sharifi-Rad J, Cappellini F, Reiner Z, Zorzan D, Imran M, Sener B, Kilic M, El-Shazly M, Fahmy NM, Al-Sayed E, Martorell M, Tonelli C, Petroni K, Docea AO, Calina D, Maroyi A (2020) The therapeutic potential of anthocyanins: current approaches based on their molecular mechanism of action. Front Pharmacol 11:1300. https://doi.org/10.3389/fphar.2020.01300CrossRefPubMedPubMedCentral

16.

Johanningsmeier SD, Harris GK (2011) Pomegranate as a functional food and nutraceutical source. Annu Rev Food Sci Technol 2(1):181–201. https://doi.org/10.1146/annurev-food-030810-153709CrossRefPubMed

17.

Magangana TP, Makunga NP, Fawole OA, Opara UL (2020) Processing factors affecting the phytochemical and nutritional properties of pomegranate (Punica granatum L.) peel waste: a review. Molecules 25(20):4690CrossRef

18.

Huang TH-W, Peng G, Kota BP, Li GQ, Yamahara J, Roufogalis BD, Li Y (2005) Pomegranate flower improves cardiac lipid metabolism in a diabetic rat model: role of lowering circulating lipids. Br J Pharmacol 145(6):767–774. https://doi.org/10.1038/sj.bjp.0706245CrossRefPubMedPubMedCentral

19.

Lei F, Zhang XN, Wang W, Xing DM, Xie WD, Su H, Du LJ (2007) Evidence of anti-obesity effects of the pomegranate leaf extract in high-fat diet induced obese mice. Int J Obes 31(6):1023–1029. https://doi.org/10.1038/sj.ijo.0803502CrossRef

20.

Raffaele M, Licari M, Amin S, Alex R, Shen H-h, Singh SP, Vanella L, Rezzani R, Bonomini F, Peterson SJ, Stec DE, Abraham NG (2020) Cold press pomegranate seed oil attenuates dietary-obesity induced hepatic steatosis and fibrosis through antioxidant and mitochondrial pathways in obese mice. Int J Mol Sci 21(15):5469CrossRef

21.

Zhao R, Long X, Yang J, Du L, Zhang X, Li J, Hou C (2019) Pomegranate peel polyphenols reduce chronic low-grade inflammatory responses by modulating gut microbiota and decreasing colonic tissue damage in rats fed a high-fat diet. Food Funct 10(12):8273–8285. https://doi.org/10.1039/C9FO02077BCrossRefPubMed

22.

Song H, Chu Q, Xu D, Xu Y, Zheng X (2016) Purified betacyanins from hylocereus undatus peel ameliorate obesity and insulin resistance in high-fat-diet-fed mice. J Agric Food Chem 64(1):236–244. https://doi.org/10.1021/acs.jafc.5b05177CrossRefPubMed

23.

Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226(1):497–509. https://doi.org/10.1016/S0021-9258(18)64849-5CrossRefPubMed

24.

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(4):402–408. https://doi.org/10.1006/meth.2001.1262CrossRefPubMed

25.

Basu A, Penugonda K (2009) Pomegranate juice: a heart-healthy fruit juice. Nutr Rev 67(1):49–56. https://doi.org/10.1111/j.1753-4887.2008.00133.xCrossRefPubMed

26.

Panichayupakaranant P, Tewtrakul S, Yuenyongsawad S (2010) Antibacterial, anti-inflammatory and anti-allergic activities of standardised pomegranate rind extract. Food Chem 123:400–403. https://doi.org/10.1016/j.foodchem.2010.04.054CrossRef

27.

Fischer UA, Carle R, Kammerer DR (2011) Identification and quantification of phenolic compounds from pomegranate (Punica granatum L.) peel, mesocarp, aril and differently produced juices by HPLC-DAD–ESI/MSn. Food Chem 127(2):807–821. https://doi.org/10.1016/j.foodchem.2010.12.156CrossRefPubMed

28.

El-Sayyad HIH (2015) Cholesterol overload impairing cerebellar function: the promise of natural products. Nutrition 31(5):621–630. https://doi.org/10.1016/j.nut.2014.10.017CrossRefPubMed

29.

Spilmont M, Léotoing L, Davicco M-J, Lebecque P, Mercier S, Miot-Noirault E, Pilet P, Rios L, Wittrant Y, Coxam V (2014) Pomegranate and its derivatives can improve bone health through decreased inflammation and oxidative stress in an animal model of postmenopausal osteoporosis. Eur J Nutr 53(5):1155–1164. https://doi.org/10.1007/s00394-013-0615-6CrossRefPubMed

30.

Esmaillzadeh A, Tahbaz F, Gaieni I, Alavi-Majd H, Azadbakht L (2004) Concentrated pomegranate juice improves lipid profiles in diabetic patients with hyperlipidemia. J Med Food 7(3):305–308. https://doi.org/10.1089/jmf.2004.7.305CrossRefPubMed

31.

Esmaillzadeh A, Tahbaz F, Gaieni I, Alavi-Majd H, Azadbakht L (2006) Cholesterol-lowering effect of concentrated pomegranate juice consumption in type II diabetic patients with hyperlipidemia. Int J Vitam Nutr Res 76(3):147–151. https://doi.org/10.1024/0300-9831.76.3.147CrossRefPubMed

32.

Xi Y, Li H (2020) Role of farnesoid X receptor in hepatic steatosis in nonalcoholic fatty liver disease. Biomed Pharmacother 121:109609. https://doi.org/10.1016/j.biopha.2019.109609CrossRefPubMed

33.

Longato L, Tong M, Wands JR, de la Monte SM (2012) High fat diet induced hepatic steatosis and insulin resistance: role of dysregulated ceramide metabolism. Hepatol Res 42(4):412–427. https://doi.org/10.1111/j.1872-034X.2011.00934.xCrossRefPubMed

34.

Garcia-Serrano AM, Duarte JMN (2020) Brain metabolism alterations in type 2 diabetes: what did we learn from diet-induced diabetes models? Front Neurosci. https://doi.org/10.3389/fnins.2020.00229CrossRefPubMedPubMedCentral

35.

Harzallah A, Hammami M, Kępczyńska MA, Hislop DC, Arch JRS, Cawthorne MA, Zaibi MS (2016) Comparison of potential preventive effects of pomegranate flower, peel and seed oil on insulin resistance and inflammation in high-fat and high-sucrose diet-induced obesity mice model. Arch Physiol Biochem 122(2):75–87. https://doi.org/10.3109/13813455.2016.1148053CrossRefPubMed

36.

Esmaeilinezhad Z, Babajafari S, Sohrabi Z, Eskandari MH, Amooee S, Barati-Boldaji R (2019) Effect of synbiotic pomegranate juice on glycemic, sex hormone profile and anthropometric indices in PCOS: a randomized, triple blind, controlled trial. Nutr Metab Cardiovasc Dis 29(2):201–208. https://doi.org/10.1016/j.numecd.2018.07.002CrossRefPubMed

37.

Huang H, Liao D, Chen G, Chen H, Zhu Y (2017) Lack of efficacy of pomegranate supplementation for glucose management, insulin levels and sensitivity: evidence from a systematic review and meta-analysis. Nutr J 16(1):67. https://doi.org/10.1186/s12937-017-0290-1CrossRefPubMedPubMedCentral

38.

Ilyas Z, Perna S, Al-Thawadi S, Alalwan TA, Riva A, Petrangolini G, Gasparri C, Infantino V, Peroni G, Rondanelli M (2020) The effect of Berberine on weight loss in order to prevent obesity: a systematic review. Biomed Pharmacother 127:110137. https://doi.org/10.1016/j.biopha.2020.110137CrossRefPubMed

39.

Gautier-Stein A, Soty M, Chilloux J, Zitoun C, Rajas F, Mithieux G (2012) Glucotoxicity induces glucose-6-phosphatase catalytic unit expression by acting on the interaction of HIF-1α with CREB-binding protein. Diabetes 61(10):2451. https://doi.org/10.2337/db11-0986CrossRefPubMedPubMedCentral

40.

Krause C, Geißler C, Tackenberg H, El Gammal AT, Wolter S, Spranger J, Mann O, Lehnert H, Kirchner H (2020) Multi-layered epigenetic regulation of IRS2 expression in the liver of obese individuals with type 2 diabetes. Diabetologia 63(10):2182–2193. https://doi.org/10.1007/s00125-020-05212-6CrossRefPubMedPubMedCentral

41.

Illiano P, Brambilla R, Parolini C (2020) The mutual interplay of gut microbiota, diet and human disease. FEBS J 287(5):833–855. https://doi.org/10.1111/febs.15217CrossRefPubMed

42.

Fang J (2014) Bioavailability of anthocyanins. Drug Metab Rev 46(4):508–520. https://doi.org/10.3109/03602532.2014.978080CrossRefPubMed

43.

Hidalgo M, Oruna-Concha MJ, Kolida S, Walton GE, Kallithraka S, Spencer JPE, Gibson GR, de Pascual-Teresa S (2012) Metabolism of anthocyanins by human gut microflora and their influence on gut bacterial growth. J Agr Food Chem 60(15):3882–3890. https://doi.org/10.1021/jf3002153CrossRef

44.

Singer-Englar T, Barlow G, Mathur R (2019) Obesity, diabetes, and the gut microbiome: an updated review. Expert Rev Gastroenterol Hepatol 13(1):3–15. https://doi.org/10.1080/17474124.2019.1543023CrossRefPubMed

45.

Shin NR, Whon TW, Bae JW (2015) Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 33(9):496–503. https://doi.org/10.1016/j.tibtech.2015.06.011CrossRefPubMed

46.

Zhou K (2017) Strategies to promote abundance of Akkermansia muciniphila, an emerging probiotics in the gut, evidence from dietary intervention studies. J Funct Foods 33:194–201. https://doi.org/10.1016/j.jff.2017.03.045CrossRefPubMedPubMedCentral

47.

Li Z, Henning SM, Lee RP, Lu QY, Summanen PH, Thames G, Corbett K, Downes J, Tseng CH, Finegold SM, Heber D (2015) Pomegranate extract induces ellagitannin metabolite formation and changes stool microbiota in healthy volunteers. Food Funct 6(8):2487–2495. https://doi.org/10.1039/c5fo00669dCrossRefPubMed

48.

Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, Liang S, Zhang W, Guan Y, Shen D, Peng Y, Zhang D, Jie Z, Wu W, Qin Y, Xue W, Li J, Han L, Lu D, Wu P, Dai Y, Sun X, Li Z, Tang A, Zhong S, Li X, Chen W, Xu R, Wang M, Feng Q, Gong M, Yu J, Zhang Y, Zhang M, Hansen T, Sanchez G, Raes J, Falony G, Okuda S, Almeida M, LeChatelier E, Renault P, Pons N, Batto JM, Zhang Z, Chen H, Yang R, Zheng W, Li S, Yang H, Wang J, Ehrlich SD, Nielsen R, Pedersen O, Kristiansen K, Wang J (2012) A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490(7418):55–60. https://doi.org/10.1038/nature11450CrossRefPubMed

49.

Louis S, Tappu RM, Damms-Machado A, Huson DH, Bischoff SC (2016) Characterization of the gut microbial community of obese patients following a weight-loss intervention using whole metagenome shotgun sequencing. PLoS One 11(2):e0149564. https://doi.org/10.1371/journal.pone.0149564CrossRefPubMedPubMedCentral

50.

Zeng Q, Li D, He Y, Li Y, Yang Z, Zhao X, Liu Y, Wang Y, Sun J, Feng X, Wang F, Chen J, Zheng Y, Yang Y, Sun X, Xu X, Wang D, Kenney T, Jiang Y, Gu H, Li Y, Zhou K, Li S, Dai W (2019) Discrepant gut microbiota markers for the classification of obesity-related metabolic abnormalities. Sci Rep 9(1):13424. https://doi.org/10.1038/s41598-019-49462-wCrossRefPubMedPubMedCentral

51.

Oddi S, Huber P, Rocha Faria Duque AL, Vinderola G, Sivieri K (2020) Breast-milk derived potential probiotics as strategy for the management of childhood obesity. Food Res Int 137:109673. https://doi.org/10.1016/j.foodres.2020.109673CrossRefPubMed

Titel: Pomegranate peel anthocyanins prevent diet-induced obesity and insulin resistance in association with modulation of the gut microbiota in mice
verfasst von: Haizhao Song
Xinchun Shen
Rou Deng
Qiang Chu
Xiaodong Zheng
Publikationsdatum: 18.01.2022
Verlag: Springer Berlin Heidelberg
Erschienen in: European Journal of Nutrition / Ausgabe 4/2022
Print ISSN: 1436-6207
Elektronische ISSN: 1436-6215
DOI: https://doi.org/10.1007/s00394-021-02771-1

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Live-Webinar "Urologie und Sexualmedizin in der Praxis"

Springer Medizin

Pomegranate peel anthocyanins prevent diet-induced obesity and insulin resistance in association with modulation of the gut microbiota in mice

Abstract

Purpose

Methods

Results

Conclusion

Leitlinien kompakt für die Innere Medizin

Neu im Fachgebiet Innere Medizin

Ist Fasten vor Koronarinterventionen wirklich nötig?

Typ-2-Diabetes: Ernährungsunsicherheit vervierfacht Risiko für schwere Hypoglykämien

Mehr Brustkrebs, aber weniger andere gynäkologische Tumoren mit Levonorgestrel-IUS

GLP-1-Agonist Semaglutid wirkt kardio- und nephroprotektiv

Update Innere Medizin

Live-Webinar "Urologie und Sexualmedizin in der Praxis"

Springer Medizin

Abstract

Purpose

Methods

Results

Conclusion

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 4/2022

Dietary omega-3 polyunsaturated fatty acid and alpha-linolenic acid are associated with physical capacity measure but not muscle mass in older women 65–72 years

Activation of gastrointestinal ileal brake response with dietary slowly digestible carbohydrates, with no observed effect on subjective appetite, in an acute randomized, double-blind, crossover trial

Serum n-6 polyunsaturated fatty acids and risk of atrial fibrillation: the Kuopio Ischaemic Heart Disease Risk Factor Study

Correction to: Reported organic food consumption and metabolic syndrome in older adults: cross‑sectional and longitudinal analyses

Effects of changing from a diet with saturated fat to a diet with n-6 polyunsaturated fat on the serum metabolome in relation to cardiovascular disease risk factors

Dietary fat and fatty acids in relation to risk of colorectal cancer

Leitlinien kompakt für die Innere Medizin

Neu im Fachgebiet Innere Medizin

Ist Fasten vor Koronarinterventionen wirklich nötig?

Typ-2-Diabetes: Ernährungsunsicherheit vervierfacht Risiko für schwere Hypoglykämien

Mehr Brustkrebs, aber weniger andere gynäkologische Tumoren mit Levonorgestrel-IUS

GLP-1-Agonist Semaglutid wirkt kardio- und nephroprotektiv

Update Innere Medizin