AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Food Science and Human Wellness Article
PDF (6.7 MB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article | Open Access

Verbascoside exerts an anti-atherosclerotic effect by regulating liver glycerophospholipid metabolism

Peng Leia,1, Jialin Lüa,1, Tie Yaoa, Peng Zhanga, Xin Chaia, Yuefei Wanga, Miaomiao Jianga,b( )
State Key Laboratory of Component-based Chinese Medicine, Tianjin University of Traditional Chinese Medicine, Tianjin 301617, China
Key Laboratory of Pharmacology of Traditional Chinese Medicine Formulae, Ministry of Education, Tianjin University of Traditional Chinese Medicine, Tianjin 301617, China

1 These authors contributed equally to this work.

Peer review under responsibility of KeAi Communications Co., Ltd.

Show Author Information

Abstract

Verbascoside, abundant in olive mill wastewater, is a phenylethanolic glycoside with a wide range of pharmacological activities. Atherosclerosis (AS) is a common metabolic disease and abnormal lipid metabolism in liver is inseparable from its formation and development. In this study, the anti-atherosclerotic effect of verbascoside was evaluated by establishing an atherosclerosis model based on western diet feeding of apolipoprotein E-deficient mice for 16 weeks. After 12 weeks of administration during the feeding period, the levels of total cholesterol (TC), triglyceride (TG), low density lipoprotein cholesterol (LDL-C) in the plasma of mice were significantly decreased, the formation of arterial plaques was delayed, and the levels of alanine aminotransferase (ALT), aspartate aminotransferase (AST) and lactate dehydrogenase (LDH) in plasma were alleviated, showing the hepatoprotective effect. In addition, based on untargeted lipidomic analysis, verbascoside stabilized glycerophospholipid metabolism, modulated lipid metabolism disorders and reduced lipid deposition in the liver to achieve the therapeutic efficacy against atherosclerosis by regulating cardiolipin (CL), ether-linked phosphatidylcholine (ether-PC), lysophophatidylcholine (LPC), phosphatidylcholine (PC), oxidized phosphatidylcholine (OxPC), oxidized phosphatidylethanolamine (OxPE), triacylglycerol (TG), sphingomyelin (SM) back to normal levels.

Keywords

AtherosclerosisLipidomicsVerbascosideLipid depositionGlycerophospholipid metabolism

References

[1]

F. Gomez-Delgado, N. Katsiki, J. Lopez-Miranda, P. Perez-Martinez, Dietary habits, lipoprotein metabolism and cardiovascular disease: From individual foods to dietary patterns, Crit. Rev. Food Sci. Nutr. 61 (2021) 1651-1669. https://doi.org/10.1080/10408398.2020.1764487.
Crossref Google Scholar
[2]

J. Gutiérrez-Cuevas, A. Sandoval-Rodriguez, A. Meza-Rios, et al., Molecular mechanisms of obesity-linked cardiac dysfunction: an up-date on current knowledge, Cells. 10 (2021) 629. https://doi.org/10.3390/cells10030629.
Crossref Google Scholar
[3]

A. Pirillo, M. Casula, E. Olmastroni, et al., Global epidemiology of dyslipidaemias, Nat. Rev. Cardiol. 18 (2021) 689-700. https://doi.org/10.1038/s41569-021-00541-4.
Crossref Google Scholar
[4]

W. Wang, M. Hu, H. Liu, et al., Global burden of disease study 2019 suggests that metabolic risk factors are the leading drivers of the burden of ischemic heart disease, Cell Metab. 33 (2021) 1943-1956.e2. https://doi.org/10.1016/J.CMET.2021.08.005.
Crossref Google Scholar
[5]

J. Hippisley-Cox, C. Coupland, Unintended effects of statins in men and women in England and Wales: population based cohort study using the QResearch database, BMJ. 340 (2010) 1232. https://doi.org/10.1136/bmj.c2197.
Crossref Google Scholar
[6]

R. Collins, C. Reith, J. Emberson, et al., Interpretation of the evidence for the efficacy and safety of statin therapy, Lancet. 388 (2016) 2532-2561. https://doi.org/10.1016/S0140-6736(16)31357-5.
Crossref Google Scholar
[7]

A.A. Carter, T. Gomes, X. Camacho, et al., Risk of incident diabetes among patients treated with statins: Population based study, BMJ. 346 (2013) f2610. https://doi.org/10.1136/bmj.f2610.
Crossref Google Scholar
[8]

D. Latek, E. Rutkowska, S. Niewieczerzal, et al., Drug-induced diabetes type 2: in silico study involving class B GPCRs, PLoS ONE. 14 (2019) e0208892. https://doi.org/10.1371/journal.pone.0208892.
Crossref Google Scholar
[9]

J.A. Sáez, M.D. Pérez-Murcia, A. Vico, et al., Olive mill wastewater-evaporation ponds long term stored: integrated assessment of in situ bioremediation strategies based on composting and vermicomposting, J. Hazard. Mater. 402 (2021) 123481. https://doi.org/10.1016/j.jhazmat.2020.123481.
Crossref Google Scholar
[10]

P. Diamantopoulou, C. Gardeli, S. Papanikolaou, impact of olive mill wastewaters on the physiological behavior of a wild-type new Ganoderma resinaceum isolate, Environ. Sci. Pollut. Res. 28 (2021) 20570-20585. https://doi.org/10.1007/s11356-020-11835-4.
Crossref Google Scholar
[11]

A. Albini, M.M.G. Festa, N. Ring, D. Baci, et al., A Polyphenol-rich extract of olive mill wastewater enhances cancer chemotherapy effects, while mitigating cardiac toxicity, Front. Pharmacol. 12 (2021) 694762. https://doi.org/10.3389/fphar.2021.694762.
Crossref Google Scholar
[12]

M. Carrara, M.T. Kelly, F. Roso, M. Larroque, et al., Potential of olive oil mill wastewater as a source of polyphenols for the treatment of skin disorders: a review, J. Agric. Food Chem. 69 (2021) 7268-7284. https://doi.org/10.1021/acs.jafc.1c00296.
Crossref Google Scholar
[13]

M. Bellumori, L. Cecchi, A. Romani, et al., Recovery and stability over time of phenolic fractions by an industrial filtration system of olive mill wastewaters: a three-year study, J. Sci. Food Agric. 98 (2018) 2761-2769. https://doi.org/10.1002/jsfa.8772.
Crossref Google Scholar
[14]

R. Abbattista, G. Ventura, C.D. Calvano, et al., Bioactive compounds in waste by-products from olive oil production: Applications and structural characterization by mass spectrometry techniques, Foods. 10 (2021) 10061236. https://doi.org/10.3390/foods10061236.
Crossref Google Scholar
[15]

K. Alipieva, L. Korkina, I.E. Orhan, et al., Verbascoside: a review of its occurrence, (bio)synthesis and pharmacological significance, Biotechnol. Adv. 32 (2014) 1065-1076. https://doi.org/10.1016/j.biotechadv.2014.07.001.
Crossref Google Scholar
[16]

H. Wang, J. Feng, F. Ao, et al., Tumor-derived exosomal microRNA-7-5p enhanced by verbascoside inhibits biological behaviors of glioblastoma in vitro and in vivo, Mol. Ther. Oncolytics. 20 (2021) 569-582. https://doi.org/10.1016/j.omto.2020.12.006.
Crossref Google Scholar
[17]

M. Sabti, K. Sasaki, C. Gadhi, et al., Elucidation of the molecular mechanism underlying Lippia citriodora(Lim.)-induced relaxation and anti-depression, Int. J. Mol. Sci. 20 (2019) 3556. https://doi.org/10.3390/ijms20143556.
Crossref Google Scholar
[18]

Y.Q. Li, Y. Chen, S.Q. Jiang, et al., An inhibitor of NF-κB and an agonist of AMPK: Network prediction and multi-omics integration to derive signaling pathways for acteoside against alzheimer’s disease, Front. Cell Dev. Biol. 9 (2021) 652310. https://doi.org/10.3389/fcell.2021.652310.
Crossref Google Scholar
[19]

E. Esposito, R. Dal Toso, G. Pressi, et al., Protective effect of verbascoside in activated C6 glioma cells: Possible molecular mechanisms, Naunyn. Schmiedebergs. Arch. Pharmacol. 381 (2010) 93–105. https://doi.org/10.1007/s00210-009-0466-0.
Crossref Google Scholar
[20]

V.A. Kostyuk, A.I. Potapovich, T.O. Suhan, et al., Antioxidant and signal modulation properties of plant polyphenols in controlling vascular inflammation, Eur. J. Pharmacol. 658 (2011) 248–256. https://doi.org/10.1016/j.ejphar.2011.02.022.
Crossref Google Scholar
[21]

K. Zhu, Z. Meng, Y. Tian, et al., Hypoglycemic and hypolipidemic effects of total glycosides of Cistanche tubulosa in diet/streptozotocin-induced diabetic rats, J. Ethnopharmacol. 276 (2021) 113991. https://doi.org/10.1016/j.jep.2021.113991.
Crossref Google Scholar
[22]

S. Wen, Y. Chen, J. Lu, et al., Modulation of hepatic lipidome by rhodioloside in high-fat diet fed apolipoprotein E knockout mice, Phytomedicine. 69 (2020). https://doi.org/10.1016/j.phymed.2018.09.225.
Crossref Google Scholar
[23]

L. Hodson, Hepatic fatty acid synthesis and partitioning: The effect of metabolic and nutritional state, Proc. Nutr. Soc. 78 (2019) 126–134. https://doi.org/10.1017/S0029665118002653.
Crossref Google Scholar
[24]

A. Ferramosca, V. Zara, Modulation of hepatic steatosis by dietary fatty acids, World J. Gastroenterol. 20 (2014) 1746–1755. https://doi.org/10.3748/wjg.v20.i7.1746.
Crossref Google Scholar
[25]

S. Softic, D.E. Cohen, C.R. Kahn, Role of dietary fructose and hepatic de novo lipogenesis in fatty liver disease, Dig. Dis. Sci. 61 (2016) 1282–1293. https://doi.org/10.1007/s10620-016-4054-0.
Crossref Google Scholar
[26]

D. Niederseer, B. Wernly, E. Aigner, et al., NAFLD and cardiovascular diseases: epidemiological, mechanistic and therapeutic considerations, J. Clin. Med. 10 (2021) 467. https://doi.org/10.3390/jcm10030467.
Crossref Google Scholar
[27]

B.K. Koo, M.A. Allison, M.H. Criqui, et al., The association between liver fat and systemic calcified atherosclerosis, J. Vasc. Surg. 71 (2020) 204-211.e4. https://doi.org/10.1016/j.jvs.2019.03.044.
Crossref Google Scholar
[28]

V.T. Dang, A. Huang, L.H. Zhong, et al., Comprehensive plasma metabolomic analyses of atherosclerotic progression reveal alterations in glycerophospholipid and sphingolipid metabolism in apolipoprotein e-deficient mice, Sci. Rep. 6 (2016) 35037. https://doi.org/10.1038/srep35037.
Crossref Google Scholar
[29]

Y. Chen, S. Wen, M. Jiang, et al., Atherosclerotic dyslipidemia revealed by plasma lipidomics on ApoE−/− mice fed a high-fat diet, Atherosclerosis. 262 (2017) 78-86. https://doi.org/10.1016/j.atherosclerosis.2017.05.010.
Crossref Google Scholar
[30]

U. Igbavboa, J. Hamilton, H.Y. Kim, et al., A new role for apolipoprotein E: Modulating transport of polyunsaturated phospholipid molecular species in synaptic plasma membranes, J. Neurochem. 80 (2002) 255-261. https://doi.org/10.1046/j.0022-3042.2001.00688.x.
Crossref Google Scholar
[31]

I. Tabas, Cholesterol and phospholipid metabolism in macrophages, Biochim. Biophys. Acta-Mol. Cell Biol. Lipids. 1529 (2000) 164-174. https://doi.org/10.1016/S1388-1981(00)00146-3.
Crossref Google Scholar
[32]

E.E. Williams, J.A. Cooper, W. Stillwell, et al., The curvature and cholesterol content of phospholipid bilayers alter the transbilayer distribution of specific molecular species of phosphatidylethanolamine, Mol. Membr. Biol. 17 (2000) 157-164. https://doi.org/10.1080/09687680050197383.
Crossref Google Scholar
[33]

Y. Huang, R.W. Mahley, Apolipoprotein E: structure and function in lipid metabolism, neurobiology, and Alzheimer’s diseases, Neurobiol. Dis. 72 (2014) 3-12. https://doi.org/10.1016/j.nbd.2014.08.025.
Crossref Google Scholar
[34]

A.D. Marais, Apolipoprotein E in lipoprotein metabolism, health and cardiovascular disease, Pathology. 51 (2019) 165-176. https://doi.org/10.1016/j.pathol.2018.11.002.
Crossref Google Scholar
[35]

D. Salnikova, V. Orekhova, A. Grechko, et al., Mitochondrial dysfunction in vascular wall cells and its role in atherosclerosis, Int. J. Mol. Sci. 22 (2021) 8990. https://doi.org/10.3390/ijms22168990.
Crossref Google Scholar
[36]

S.J. Jeong, J.G. Park, G.T. Oh, Peroxiredoxins as potential targets for cardiovascular disease, Antioxidants. 10 (2021) 081244. https://doi.org/10.3390/antiox10081244.
Crossref Google Scholar
[37]

A.V. Poznyak, E.E. Bezsonov, T.V. Popkova, et al., Immunity in atherosclerosis: Focusing on t and b cells, Int. J. Mol. Sci. 22 (2021). https://doi.org/10.3390/ijms22168379.
Crossref Google Scholar
[38]

E.S. Gasanoff, L.S. Yaguzhinsky, G. Garab, Cardiolipin, non-bilayer structures and mitochondrial bioenergetics: relevance to cardiovascular disease, Cells. 10 (2021) 1721. https://doi.org/10.3390/cells10071721.
Crossref Google Scholar
[39]

M. El-Hafidi, F. Correa, C. Zazueta, Mitochondrial dysfunction in metabolic and cardiovascular diseases associated with cardiolipin remodeling, Biochim. Biophys. Acta-Mol. Basis Dis. 1866 (2020) 165744. https://doi.org/10.1016/j.bbadis.2020.165744.
Crossref Google Scholar
[40]

M.A. Kiebish, R. Bell, K. Yang, et al., Dynamic simulation of cardiolipin remodeling: Greasing the wheels for an interpretative approach to lipidomics, J. Lipid Res. 51 (2010) 2153–2170. https://doi.org/10.1194/jlr.M004796.
Crossref Google Scholar
[41]

Y. Xu, R.I. Kelley, T.J.J. Blanck, et al., Remodeling of Cardiolipin by Phospholipid Transacylation, J. Biol. Chem. 278 (2003) 51380–51385. https://doi.org/10.1074/jbc.M307382200.
Crossref Google Scholar
[42]

F. Dorninger, S. Forss-Petter, I. Wimmer, et al., Plasmalogens, platelet-activating factor and beyond: ether lipids in signaling and neurodegeneration, Neurobiol. Dis. 145 (2020). https://doi.org/10.1016/j.nbd.2020.105061.
Crossref Google Scholar
[43]

R.A. Zoeller, A.C. Lake, N. Nagan, et al., Plasmalogens as endogenous antioxidants: Somatic cell mutants reveal the importance of the vinyl ether, Biochem. J. 338 (1999) 769–776. https://doi.org/10.1042/0264-6021:3380769.
Crossref Google Scholar
[44]

T. Brosche, D. Platt, The biological significance of plasmalogens in defense against oxidative damage, Exp. Gerontol. 33 (1998) 363–369. https://doi.org/10.1016/S0531-5565(98)00014-X.
Crossref Google Scholar
[45]

S. Paul, A.A.T. Smith, K. Culham, et al., Shark liver oil supplementation enriches endogenous plasmalogens and reduces markers of dyslipidemia and inflammation, J. Lipid Res. 62 (2021) 100092. https://doi.org/10.1016/J.JLR.2021.100092.
Crossref Google Scholar
[46]

Z.A. Almsherqi, Potential role of plasmalogens in the modulation of biomembrane morphology, Front. Cell Dev. Biol. 9 (2021) 673917. https://doi.org/10.3389/fcell.2021.673917.
Crossref Google Scholar
[47]

Y.A. Carpentier, O. Scruel, Changes in the concentration and composition of plasma lipoproteins during the acute phase response., Curr. Opin. Clin. Nutr. Metab. Care. 5 (2002) 153–158. https://doi.org/10.1097/00075197-200203000-00006.
Crossref Google Scholar
[48]

L.K. Cole, J.E. Vance, D.E. Vance, Phosphatidylcholine biosynthesis and lipoprotein metabolism, Biochim. Biophys. Acta-Mol. Cell Biol. Lipids. 1821 (2012) 754-761. https://doi.org/10.1016/j.bbalip.2011.09.009.
Crossref Google Scholar
[49]

A. Jonas, Lecithin cholesterol acyltransferase, Biochim. Biophys. Acta-Mol. Cell Biol. Lipids. 1529 (2000) 245–256. https://doi.org/10.1016/S1388-1981(00)00153-0.
Crossref Google Scholar
[50]

P. Liu, W. Zhu, C. Chen, et al., The mechanisms of lysophosphatidylcholine in the development of diseases, Life Sci. 247 (2020) 117443. https://doi.org/10.1016/j.lfs.2020.117443.
Crossref Google Scholar
[51]

J.J. Luo, H.X. Cao, R.X. Yang, et al., PNPLA3 rs139051 is associated with phospholipid metabolite profile and hepatic inflammation in nonalcoholic fatty liver disease, World J. Clin. Cases. 6 (2018) 355-364. https://doi.org/10.12998/wjcc.v6.i10.355.
Crossref Google Scholar
[52]

H. Takahashi, T. Goto, Y. Yamazaki, K. Kamakari, et al., Metabolomics reveal 1-palmitoyl lysophosphatidylcholine production by peroxisome proliferator-activated receptor α, J. Lipid Res. 56 (2015) 254-265. https://doi.org/10.1194/jlr.M052464.
Crossref Google Scholar
[53]

T.G. Huo, Y. Fang, Y.H. Zhang, et al., Liver metabonomics study on the protective effect of glycyrrhetinic acid against realgar-induced liver injury, Chin. J. Nat. Med. 18 (2020) 138-147. https://doi.org/10.1016/S1875-5364(20)30014-5.
Crossref Google Scholar
[54]

O. Rozenberg, D.M. Shih, M. Aviram, Human serum paraoxonase 1 decreases macrophage cholesterol biosynthesis: Possible role for its phospholipase-A2-like activity and lysophosphatidylcholine formation, Arterioscler. Thromb. Vasc. Biol. 23 (2003) 461-467. https://doi.org/10.1161/01.ATV.0000060462.35946.B3.
Crossref Google Scholar
[55]

M. Rosenblat, J. Vaya, D. Shih, et al., Paraoxonase 1 (PON1) enhances HDL-mediated macrophage cholesterol efflux via the ABCA1 transporter in association with increased HDL binding to the cells: A possible role for lysophosphatidylcholine, Atherosclerosis. 179 (2005) 69-77. https://doi.org/10.1016/j.atherosclerosis.2004.10.028.
Crossref Google Scholar
[56]

M. Yamamoto, H. Hara, T. Adachi, The expression of extracellular-superoxide dismutase is increased by lysophosphatidylcholine in human monocytic U937 cells, Atherosclerosis. 163 (2002) 223-228. https://doi.org/10.1016/S0021-9150(02)00007-2.
Crossref Google Scholar
[57]

N.D. Hung, D.E. Sok, M.R. Kim, Prevention of 1-palmitoyl lysophosphatidylcholine-induced inflammation by polyunsaturated acyl lysophosphatidylcholine, Inflamm. Res. 61 (2012) 473-483. https://doi.org/10.1007/s00011-012-0434-x.
Crossref Google Scholar
[58]

O.A. Akerele, S.K. Cheema, Fatty acyl composition of lysophosphatidylcholine is important in atherosclerosis, Med. Hypotheses. 85 (2015) 754-760. https://doi.org/10.1016/j.mehy.2015.10.013.
Crossref Google Scholar
[59]

G.Y. Liu, S.H. Moon, C.M. Jenkins, et al., Synthesis of oxidized phospholipids by sn-1 acyltransferase using 2–15-HETE lysophospholipids, J. Biol. Chem. 294 (2019) 10146-10159. https://doi.org/10.1074/jbc.RA119.008766.
Crossref Google Scholar
[60]

V.N. Bochkov, O.V. Oskolkova, K.G. Birukov, et al., Generation and biological activities of oxidized phospholipids, Antioxidants Redox Signal. 12 (2010) 1009-1059. https://doi.org/10.1089/ars.2009.2597.
Crossref Google Scholar
[61]

R. Li, K.P. Mouillesseaux, D. Montoya, et al., Identification of prostaglandin E2 receptor subtype 2 as a receptor activated by OxPAPC, Circ. Res. 98 (2006) 642-650. https://doi.org/10.1161/01.RES.0000207394.39249.fc.
Crossref Google Scholar
[62]

M. Sharma, A. Von Zychlinski-Kleffmann, C.M. Porteous, et al., Lipoprotein (a) upregulates ABCA1 in liver cells via scavenger receptor-B1 through its oxidized phospholipids, J. Lipid Res. 56 (2015) 1318-1328. https://doi.org/10.1194/jlr.M056150.
Crossref Google Scholar
[63]

I. Mendel, N. Yacov, A. Shoham, et al., Treatment with oxidized phospholipids directly inhibits nonalcoholic steatohepatitis and liver fibrosis without affecting steatosis, Dig. Dis. Sci. 61 (2016) 2545-2553. https://doi.org/10.1007/s10620-016-4159-5.
Crossref Google Scholar
[64]

S. Hirashio, T. Ueno, T. Naito, et al., Characteristic kidney pathology, gene abnormality and treatments in LCAT deficiency, Clin. Exp. Nephrol. 18 (2014) 189-193. https://doi.org/10.1007/s10157-013-0895-4.
Crossref Google Scholar
[65]

A.R. Tall, Plasma high density lipoproteins. Metabolism and relationship to atherogenesis, J. Clin. Invest. 86 (1990) 379-384. https://doi.org/10.1172/JCI114722.
Crossref Google Scholar
[66]

F. Huang, K. Wang, J. Shen, Lipoprotein-associated phospholipase A2: the story continues, Med. Res. Rev. 40 (2020) 79-134. https://doi.org/10.1002/med.21597.
Crossref Google Scholar
[67]

G.K. Marathe, C. Pandit, C.L. Lakshmikanth, et al., To hydrolyze or not to hydrolyze: the dilemma of platelet-activating factor acetylhydrolase, J. Lipid Res. 55 (2014) 1847-1854. https://doi.org/10.1194/jlr.R045492.
Crossref Google Scholar
[68]

B. Wang, P. Tontonoz, Phospholipid remodeling in physiology and disease, Annu. Rev. Physiol. 81 (2019) 165-188. https://doi.org/10.1146/annurev-physiol-020518-114444.
Crossref Google Scholar
[69]

J. Liu, R. Kang, D. Tang, Signaling pathways and defense mechanisms of ferroptosis, FEBS J. (2021) 7038-7050. https://doi.org/10.1111/febs.16059.
Crossref Google Scholar
[70]

J.Y. Lee, W.K. Kim, K.H. Bae, et al., Lipid metabolism and ferroptosis, Biology (Basel). 10 (2021) 1651-1669. https://doi.org/10.3390/biology10030184.
Crossref Google Scholar
Food Science and Human Wellness
Volume 12 Issue 6,
November 2023
Pages 2314-2323
DOI: 10.1016/j.fshw.2023.03.035
Cite this article:
Lei P, Lü J, Yao T, et al. Verbascoside exerts an anti-atherosclerotic effect by regulating liver glycerophospholipid metabolism. Food Science and Human Wellness, 2023, 12(6): 2314-2323. https://doi.org/10.1016/j.fshw.2023.03.035

744

Views

30

Downloads

11

Crossref

10

Web of Science

10

Scopus

0

CSCD

Altmetrics
Received: 17 September 2021
Revised: 20 December 2021
Accepted: 20 January 2022
Published: 04 April 2023
© 2023 Beijing Academy of Food Sciences.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Return