Protective effect of high-oleic acid peanut oil and extra-virgin olive oil in rats with diet-induced metabolic syndrome by regulating branched-chain amino acids metabolism

doi:10.1016/S2095-3119(21)63851-0

Journal of Integrative Agriculture ›› 2022, Vol. 21 ›› Issue (3): 878-891.DOI: 10.1016/S2095-3119(21)63851-0

所属专题：食品科学合辑Food Science

收稿日期:2021-02-09 接受日期:2021-10-09 出版日期:2022-03-01 发布日期:2021-10-09

Protective effect of high-oleic acid peanut oil and extra-virgin olive oil in rats with diet-induced metabolic syndrome by regulating branched-chain amino acids metabolism

ZHAO Zhi-hao¹, SHI Ai-min^{1, 2}, GUO Rui¹, LIU Hong-zhi^{1, 2}, HU Hui¹, WANG Qiang^{1, 2}

¹Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences/Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, Beijing 100193, P.R.China
² Collaborative Innovation Center for Modern Grain Circulation and Safety, College of Food Science and Engineering, Nanjing University of Finance and Economics, Nanjing 210023, P.R.China

Received:2021-02-09 Accepted:2021-10-09 Online:2022-03-01 Published:2021-10-09
About author:Correspondence WANG Qiang, E-mail: wangqiang06@caas.cn
Supported by:
This research was supported by the Agricultural Science and Technology Innovation Project of Chinese Academy of Agricultural Sciences (CAAS-ASTIP-201XIAPPST), the Top Young Talents of Grain Industry in China (LQ2020202), and the National Natural Science Foundation of China (32172149).

摘要/Abstract

摘要：

前期研究表明，高油酸花生油(HOPO)和特级初榨橄榄油(EVOO)对代谢综合征(MS)具有预防作用。本研究旨在评估HOPO和EVOO膳食干预预防MS的代谢效应，以及肠道菌群在其中的作用。选用Sprague-Dawley大鼠分别喂食正常饲料、高果糖-高脂肪饲料、含HOPO的高果糖-高脂肪饲料和含EVOO的高果糖-高脂肪饲料，持续12周。利用基于UPLC-Q/TOF-MS的非靶向代谢组学分析粪便和血清样品的代谢组学特征，采用偏最小二乘判别分析(PLS-DA)对组间粪便和血清中潜在生物标志物进行鉴定，评估肠道菌群与潜在生物标志物的相关性，并对血清生物标志物进行通路分析。结果表明：各组粪便和血清代谢模式存在显著差异，其中HOPO组和EVOO组分别有8、12个粪便生物标志物和15、6个血清生物标志物，同时，粪便和血清中氨基酸、多肽及其类似物组成发生显著变化，而支链氨基酸(BCAAs)生物合成通路被鉴定为HOPO和EVOO的主要调控途径，是高油酸花生油和特级初榨橄榄油预防大鼠膳食诱导代谢综合征的关键通路。

Abstract: High-oleic acid peanut oil (HOPO) and extra-virgin olive oil (EVOO) have been reported previously to have an attenuating effect on metabolic syndrome (MS). This study aimed to evaluate the metabolic effect of HOPO and EVOO supplementation in attenuating MS and the role of gut microbiota in regulating the metabolic profile. Sprague-Dawley rats were continuously fed with a normal diet, high-fructose and high-fat (HFHF) diet, HFHF diet containing HOPO, or a HFHF diet containing EVOO for 12 weeks. The metabolomics profiles of feces and serum samples were compared using untargeted metabolomics based on UPLC-Q/TOF-MS. Partial Least Squares Discriminant Analysis (PLS-DA) was used to identify the potential fecal and serum biomarkers from different groups. Correlation between gut microbiota and biomarkers was assessed, and pathway analysis of serum biomarkers was conducted. Differences in metabolic patterns in feces and serum were observed among different groups. There were 8 and 12 potential biomarkers in feces and 15 and 6 potential biomarkers in serum of HOPO group and EVOO group, respectively, suggesting that HOPO and EVOO supplementation mainly altered amino acids, peptides, and their analogs in feces and serum. The branched-chain amino acids (BCAAs) biosynthesis pathway was identified as a major pathway regulated by HOPO or EVOO. This study suggests that HOPO and EVOO supplementation ameliorate diet-induced MS, mainly via modulation of the BCAAs biosynthesis pathway.

Key words: metabolic syndrome , high-oleic acid peanut oil , extra-virgin olive oil , metabolomics , UPLC-Q/TOF-MS

. [J]. Journal of Integrative Agriculture, 2022, 21(3): 878-891.

ZHAO Zhi-hao, SHI Ai-min, GUO Rui, LIU Hong-zhi, HU Hui, WANG Qiang. Protective effect of high-oleic acid peanut oil and extra-virgin olive oil in rats with diet-induced metabolic syndrome by regulating branched-chain amino acids metabolism[J]. Journal of Integrative Agriculture, 2022, 21(3): 878-891.

参考文献

Alberti K G M M, Zimmet P, Shaw J. 2006. Metabolic syndrome - A new world-wide definition. A Consensus Statement from the International Diabetes Federation. Diabetic Medicine, 23, 469–480.
Barbour J A, Howe P R C, Buckley J D, Bryan J, Coates A M. 2017. Cerebrovascular and cognitive benefits of high-oleic peanut consumption in healthy overweight middle-aged adults. Nutritional Neuroscience, 20, 555–562.
Bloomgarden Z. 2018. Diabetes and branched chain amino acids: What is the link? Journal of Diabetes, 10, 350–352.
Chen T L, Ni Y, Ma X J, Bao Y Q, Liu J J, Huang F J, Hu C, Xie G X, Zhao A H, Jia W P, Jia W. 2016. Branched-chain and aromatic amino acid profiles and diabetes risk in Chinese populations. Scientific Reports, 6, 20594.
Chong J, Soufan O, Li C, Caraus I, Li S Z, Bourque G, Wishart D S, Xia J G. 2018. MetaboAnalyst 4.0: Towards more transparent and integrative metabolomics analysis. Nucleic Acids Research, 46, W486–W494.
Clemente J C, Ursell L K, Parfrey L W, Knight R. 2012. The impact of the gut microbiota on human health: An integrative view. Cell, 148, 1258–1270.
Clifton P. 2019. Metabolic syndrome-role of dietary fat type and quantity. Nutrients, 11, 1438.
Comte B, Monnerie S, Brandolini-Bunlon M, Canlet C, Castelli F, Chu-VanE, Colsch B, Fenaille F, Joly C, Jourdan F, Lenuzza N, Lyan B, Martin J F, Migné C, Morais J A, Pétéra M, Poupin N, Vinson F, Thevenot E, Junot C, et al. 2021. Multiplatform metabolomics for an integrative exploration of metabolic syndrome in older men. EBioMedicine, 69, 103440.
Cristina G, Stefania R, Stefano A, Teresa E D, Ilaria L, Chiara T, Paola F, Andrea B, Fiorella C, Massimo S. 2013. The polyphenol oleuropein aglycone protects TgCRND8 mice against Aβ plaque pathology. PLoS ONE, 8, e71702.
Cummings N E, Williams E M, Kasza I, Konon E N, Schaid M D, Schmidt B A, Poudel C, Sherman D S, Yu D Y, Apelo S I A, Cottrell S E, Geiger G, Barnes M E, Wisinski J A, Fenske R J, Matkowskyj K A, Kimple M E, Alexander C M, Merrins M J, Lamming D W. 2018. Restoration of metabolic health by decreased consumption of branched-chain amino acids. Journal of Physiology, 596, 623–645.
Finer S, Robb P, Cowan K, Daly A, Robertson E, Farmer A. 2017. Top ten research priorities for type 2 diabetes: results from the Diabetes UK–James Lind Alliance Priority Setting Partnership. Lancet Diabetes Endocrinol, 5, 935–936.
Gao X, Du L, Randell E, Zhang H J, Li K L, Li D. 2021. Effect of different phosphatidylcholines on high fat diet-induced insulin resistance in mice. Food & Function, 12, 1516–1528.
Giesbertz P, Daniel H. 2015. Branched-chain amino acids as biomarkers in diabetes. Current Opinion in Clinical Nutrition & Metabolic Care, 19, 48–54.
Gu D F, Reynolds K, Wu X G, Chen J, Duan X F, Reynolds R F, Whelton P K, He J, Inter ASIA Collaborative Group. 2005. Prevalence of the metabolic syndrome and overweight among adults in China. Lancet, 365, 1398–1405.
Henao-Mejia J, Elinav E, Jin C, Hao L, Mehal W Z, Strowig T, Thaiss C A, Kau A L, Eisenbarth S C, Jurczak M J, Camporez J, Shulman G I, Gordon J I, Hoffman H M, Flavell R A. 2012. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature, 482, 179–185.
Janila P, Pandey M K, Shasidhar Y, Variath M T, Sriswathi M, Khera P, Manohar S S, Nagesh P, Vishwakarma M K, Mishra G P, Radhakrishnan T, Manivannan N, Dobariya K L, Vasanthi R P, Varshney R K. 2015. Molecular breeding for introgression of fatty acid desaturase mutant alleles (ahFAD2A and ahFAD2B) enhances oil quality in high and low oil containing peanut genotypes. Plant Science, 242, 203–213.
Kirbaeva N V, Sharanova N É, Pertsov S S. 2014. A review of current methods for nutrimetabolomic and proteomic research in biochemistry of nutrition. Voprosy Pitaniia, 83, 4–15.
Li Y R, Zhao L Y, Yu D M, Wang Z H, Ding G Q, Li Y. 2018. Metabolic syndrome prevalence and its risk factors among adults in China: A nationally representative cross-sectional study. PLoS ONE, 13, e0199293.
Lim H J, Kim D S, Pan J H, Pae S B, Kim H S, Shin E C, Kim J K. 2017. Characterization of physicochemical and sensory attributes of a novel high-oleic peanut oil cultivar (Arachis hypogaea ssp. Fastigiata L.). Applied Biological Chemistry, 60, 653–657.
Marcinkevicius E V, Shirasu-Hiza M M. 2015. Message in a biota: Gut microbes signal to the circadian clock. Cell Host & Microbe, 17, 541–543.
Martínez-González M Á, Martín-Calvo N. 2013. The major European dietary patterns and metabolic syndrome. Reviews in Endocrine & Metabolic Disorders, 14, 265–271.
Nehra V, Allen J M, Mailing L J, Kashyap P C, Woods J A. 2016. Gut microbiota: Modulation of host physiology in obesity. Physiology, 31, 327–335.
O’Neill S, O’Driscoll L. 2015. Metabolic syndrome: A closer look at the growing epidemic and its associated pathologies. Obesity Reviews, 16, 1–12.
Paula M M, Luciana G A, Valeria N, Rubén G N. 2018. Sensory and chemical stabilities of high-oleic and normal-oleic peanuts in shell during long-term storage. Journal of Food Science, 83, 2362–2368.
Peng W J, Huang J H, Yang J J, Zhang Z Y, Yu R, Fayyaz S, Qin Y H. 2020. Integrated 16S rRNA sequencing, metagenomics, and metabolomics to characterize gut microbial composition, function, and fecal metabolic phenotype in non-obese type 2 diabetic Goto-Kakizaki Rats. Frontiers in Microbiology, 10, 3141.
Riveros C G, Mestrallet M G, Gayol M F, Quiroga P R, Nepote V, Grosso N R. 2010. Effect of storage on chemical and sensory profiles of peanut pastes prepared with high-oleic and normal peanuts. Journal of the Science of Food & Agriculture, 90, 2694–2699.
Saklayen G M. 2018. The global epidemic of the metabolic syndrome. Current Hypertension Reports, 20, 12.
Sales-Campos H, Souza P R D, Peghini B C, Silva J S D, Cardoso C R. 2013. An overview of the modulatory effects of oleic acid in health and disease. Mini Reviews in Medicinal Chemistry, 13, 201–210.
Segers K, Declerck S, Mangelings D, Heyden Y V, Eeckhaut A V. 2019. Analytical techniques for metabolomic studies: A review. Bioanalysis, 11, 2297–2318.
Shen X T, Gong X Y, Cai Y P, Guo Y, Tu J, Li H, Zhang T, Wang J L, Xue F Z, Zhu Z J. 2016. Normalization and integration of large-scale metabolomics data using support vector regression. Metabolomics, 12, 89.
Tillin T, Hughes A D, Wang Q, Würtz P, Ala-Korpela M, Sattar N, Forouhi N G, Godsland I F, Eastwood S V, McKeigue P M, Chaturvedi N. 2015. Diabetes risk and amino acid profiles: cross-sectional and prospective analyses of ethnicity, amino acids and diabetes in a South Asian and European cohort from the SABRE (Southall And Brent REvisited) study. Diabetologia, 58, 968–979.
Tsugawa H, Cajka T, Kind T, Ma Y, Higgins B, Ikeda K, Kanazawa M, VanderGheynst J, Fiehn O, Arita M. 2015. MS-DIAL: Data-independent ms/ms deconvolution for comprehensive metabolome analysis. Nature Methods, 12, 523–526.
Vassiliou E K, Gonzalez A, Garcia C, Tadros J H, Toney J H. 2009. Oleic acid and peanut oil high in oleic acid reverse the inhibitory effect of insulin production of the inflammatory cytokine TNF-α both in vitro and in vivo systems. Lipids in Health & Disease, 8, 25.
Wang Q. 2017. Peanut Processing Characteristics and Quality Evaluation. Springer, Singapore.
Wang T J, Larson M G, Vasan R S, Cheng S, Rhee E P, McCabe E, Lewis G D, Fox C S, Jacques P F, Fernandez C, O’Donnell C J, Carr S A, Mootha V K, Florez J C, Souza A, Melander O, Clish C B, Gerszten R E. 2011. Metabolite profiles and the risk of developing diabetes. Nature Medicine, 17, 448–453.
Wu T, Qiao S X, Shi C Z, Wang S Y, Ji G. 2018. Metabolomics window into diabetic complications. Journal of Diabetes Investigation, 9, 244–255.
Yan L, Han P, Man J, Tian Y, Wang J. 2021. Discovery of lipid profiles of type 2 diabetes associated with hyperlipidemia using untargeted UPLC Q-TOF/MS-based lipidomics approach. Clinica Chimica Acta, 520, 53–62.
Zhao X, Han Q, Liu Y J, Sun C L, Gang X K, Wang G X. 2016. The relationship between branched-chain amino acid related metabolomic signature and insulin resistance: A systematic review. Journal of Diabetes Research, 2016, 2794591.
Zhao Z H, Shi A M, Wang Q, Zhou J R. 2019. High oleic acid peanut oil and extra virgin olive oil supplementation attenuate metabolic syndrome in rats by modulating the gut microbiota. Nutrients, 11, 3005.

Protective effect of high-oleic acid peanut oil and extra-virgin olive oil in rats with diet-induced metabolic syndrome by regulating branched-chain amino acids metabolism

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