CLC number:
On-line Access: 2024-08-27
Received: 2023-10-17
Revision Accepted: 2024-05-08
Crosschecked: 0000-00-00
Cited: 0
Clicked: 4411
Citations: Bibtex RefMan EndNote GB/T7714
https://orcid.org/0000-0003-0947-7086
Guan WANG, Mingyue HAO, Qiong LIU, Yanlong JIANG, Haibin HUANG, Guilian YANG, Chunfeng WANG. Protective effect of recombinant Lactobacillus plantarum against H2O2-induced oxidative stress in HUVEC cells[J]. Journal of Zhejiang University Science B, 2021, 22(5): 348-365.
@article{title="Protective effect of recombinant Lactobacillus plantarum against H2O2-induced oxidative stress in HUVEC cells",
author="Guan WANG, Mingyue HAO, Qiong LIU, Yanlong JIANG, Haibin HUANG, Guilian YANG, Chunfeng WANG",
journal="Journal of Zhejiang University Science B",
volume="22",
number="5",
pages="348-365",
year="2021",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B2000441"
}
%0 Journal Article
%T Protective effect of recombinant Lactobacillus plantarum against H2O2-induced oxidative stress in HUVEC cells
%A Guan WANG
%A Mingyue HAO
%A Qiong LIU
%A Yanlong JIANG
%A Haibin HUANG
%A Guilian YANG
%A Chunfeng WANG
%J Journal of Zhejiang University SCIENCE B
%V 22
%N 5
%P 348-365
%@ 1673-1581
%D 2021
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B2000441
TY - JOUR
T1 - Protective effect of recombinant Lactobacillus plantarum against H2O2-induced oxidative stress in HUVEC cells
A1 - Guan WANG
A1 - Mingyue HAO
A1 - Qiong LIU
A1 - Yanlong JIANG
A1 - Haibin HUANG
A1 - Guilian YANG
A1 - Chunfeng WANG
J0 - Journal of Zhejiang University Science B
VL - 22
IS - 5
SP - 348
EP - 365
%@ 1673-1581
Y1 - 2021
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B2000441
Abstract: This study probed the protective effect of recombinant Lactobacillus plantarum against hydrogen peroxide (H2O2)-induced oxidative stress in human umbilical vein endothelial cells (HUVECs). We constructed a new functional L. plantarum (NC8-pSIP409-alr-angiotensin-converting enzyme inhibitory peptide (ACEIP)) with a double-gene-labeled non-resistant screen as an expression vector. A 3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2H-tetrazolium bromide (MTT) colorimetric assay was carried out to determine the cell viability of HUVEC cells following pretreatment with NC8-pSIP409-alr-ACEIP. Flow cytometry (FCM) was used to determine the apoptosis rate of HUVEC cells. Cysteinyl aspartate specific proteinase (caspase)-3/8/9 activity was also assayed and western blotting was used to determine protein expression of B-cell lymphoma 2 (Bcl-2), Bcl-2-associated X protein (Bax), inducible nitric oxide synthase (iNOS), nicotinamide adenine dinucleotide phosphate oxidase 2 (gp91phox), angiotensin II (AngII), and angiotensin-converting enzyme 2 (ACE2), as well as corresponding indicators of oxidative stress, such as reactive oxygen species (ROS), mitochondrial membrane potential (MMP), malondialdehyde (MDA), and superoxide dismutase (SOD). NC8-pSIP409-alr-ACEIP attenuated H2O2-induced cell death, as determined by the MTT assay. NC8-pSIP409-alr-ACEIP reduced apoptosis of HUVEC cells by FCM. In addition, compared to the positive control, the oxidative stress index of the H2O2-induced HUVEC (Hy-HUVEC), which was pretreated by NC8-pSIP409-alr-ACEIP, iNOS, gp91phox, MDA, and ROS, was decreased obviously; SOD expression level was increased; caspase-3 or -9 was decreased, but caspase-8 did not change; Bcl-2/Bax ratio was increased; permeability changes of mitochondria were inhibited; and loss of transmembrane potential was prevented. Expression of the hypertension-related protein (AngII protein) in HUVEC cells protected by NC8-pSIP409-alr-ACEIP decreased and expression of ACE2 protein increased. These plantarum results suggested that NC8-pSIP409-alr-ACEIP protects against H2O2-induced injury in HUVEC cells. The mechanism for this effect is related to enhancement of antioxidant capacity and apoptosis.
[1]AldabbousL, Abdul-SalamV, McKinnonT, et al., 2016. Neutrophil extracellular traps promote angiogenesis. Arterioscler Thromb Vasc Biol, 36(10):2078-2087.
[2]BaliA, SinghN, JaggiAS, 2014. Renin-angiotensin system in pain: existing in a double life? J Renin Angiotensin Aldosterone Syst, 15(4):329-340.
[3]BiałasAJ, SitarekP, Miłkowska-DymanowskaJ, et al., 2016. The role of mitochondria and oxidative/antioxidative imbalance in pathobiology of chronic obstructive pulmonary disease. Oxid Med Cell Longev, 2016:7808576.
[4]BianYF, YangHY, YangZM, et al., 2011. Amlodipine treatment prevents angiotensin II-induced human umbilical vein endothelial cell apoptosis. Arch Med Res, 42(1):22-27.
[5]CaminiFC, da Silva CaetanoCC, AlmeidaLT, et al., 2017. Oxidative stress in Mayaro virus infection. Virus Res, 236:1-8.
[6]ChenJW, MehtaJL, HaiderN, et al., 2004. Role of caspases in Ox-LDL-induced apoptotic cascade in human coronary artery endothelial cells. Circ Res, 94(3):370-376.
[7]CollisterJP, Taylor-SmithH, DrebesD, et al., 2016. Angiotensin II-induced hypertension is attenuated by overexpressing copper/zinc superoxide dismutase in the brain organum vasculosum of the lamina terminalis. Oxid Med Cell Longev, 2016:3959087.
[8]DeepakV, RamachandranS, BalahmarRM, et al., 2016. In vitro evaluation of anticancer properties of exopolysaccharides from Lactobacillus acidophilus in colon cancer cell lines. In Vitro Cell Dev Biol Anim, 52(2):163-173.
[9]DuJ, LengJY, ZhangL, et al., 2016. Angiotensin II-induced apoptosis of human umbilical vein endothelial cells was inhibited by blueberry anthocyanin through Bax- and Caspase 3-dependent pathways. Med Sci Monit, 22:3223-3228.
[10]EttingerG, MacDonaldK, ReidG, et al., 2014. The influence of the human microbiome and probiotics on cardiovascular health. Gut Microbes, 5(6):719-728.
[11]Fraga-SilvaRA, Costa-FragaFP, MurçaTM, et al., 2013. Angiotensin-converting enzyme 2 activation improves endothelial function. Hypertension, 61(6):1233-1238.
[12]GordonJI, 2012. Honor thy gut symbionts redux. Science, 336(6086):1251-1253.
[13]GrahamD, HamiltonC, BeattieE, et al., 2004. Comparison of the effects of omapatrilat and irbesartan/hydrochlorothiazide on endothelial function and cardiac hypertrophy in the stroke-prone spontaneously hypertensive rat: sex differences. J Hypertens, 22(2):329-337.
[14]HuangH, ShanJ, PanXH, et al., 2006. Carvedilol protected diabetic rat hearts via reducing oxidative stress. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 7(9):725-731.
[15]KimS, GoelR, KumarA, et al., 2018. Imbalance of gut microbiome and intestinal epithelial barrier dysfunction in patients with high blood pressure. Clin Sci, 132(6):701-718.
[16]Korsager LarsenM, MatchkovVV, 2016. Hypertension and physical exercise: the role of oxidative stress. Medicina, 52(1):19-27.
[17]LaurentS, 2017. Antihypertensive drugs. Pharmacol Res, 124:116-125.
[18]LeeEJ, KoHM, JeongYH, et al., 2015. β-Lapachone suppresses neuroinflammation by modulating the expression of cytokines and matrix metalloproteinases in activated microglia. J Neuroinflammation, 12:133.
[19]LiuCT, ChuFJ, ChouC, et al., 2011. Antiproliferative and anticytotoxic effects of cell fractions and exopolysaccharides from Lactobacillus casei 01. Mutat Res Genet Toxicol Environ Mutagen, 721(2):157-162.
[20]LiuJ, ZhangFF, LiL, et al., 2013. ClC-3 deficiency prevents apoptosis induced by angiotensin II in endothelial progenitor cells via inhibition of NADPH oxidase. Apoptosis, 18(10):1262-1273.
[21]LoperenaR, HarrisonDG, 2017. Oxidative stress and hypertensive diseases. Med Clin North Am, 101(1):169-193.
[22]Lugo-BaruquiA, Muñoz-ValleJF, Arévalo-GallegosS, et al., 2010. Role of angiotensin II in liver fibrosis-induced portal hypertension and therapeutic implications. Hepatol Res, 40(1):95-104.
[23]LuoCF, YuanDD, ZhaoWC, et al., 2015. Sevoflurane ameliorates intestinal ischemia-reperfusion-induced lung injury by inhibiting the synergistic action between mast cell activation and oxidative stress. Mol Med Rep, 12(1):1082-1090.
[24]MaghraouiS, ClichiciS, AyadiA, et al., 2014. Oxidative stress in blood and testicle of rat following intraperitoneal administration of aluminum and indium. Acta Physiol Hung, 101(1):47-58.
[25]MendellJT, OlsonEN, 2012. MicroRNAs in stress signaling and human disease. Cell, 148(6):1172-1187.
[26]OttM, GogvadzeV, OrreniusS, et al., 2007. Mitochondria, oxidative stress and cell death. Apoptosis, 12(5):913-922.
[27]PavliF, TassouC, NychasGJE, et al., 2018. Probiotic incorporation in edible films and coatings: bioactive solution for functional foods. Int J Mol Sci, 19(1):150.
[28]PräbstK, EngelhardtH, RinggelerS, et al., 2017. Basic colorimetric proliferation assays: MTT, WST, and resazurin. Methods Mol Biol, 1601:1-17.
[29]SantosCMA, PiresMCV, LeãoTL, et al., 2016. Selection of Lactobacillus strains as potential probiotics for vaginitis treatment. Microbiology, 162(7):1195-1207.
[30]SharafedtinovKK, PlotnikovaOA, AlexeevaRI, et al., 2013. Hypocaloric diet supplemented with probiotic cheese improves body mass index and blood pressure indices of obese hypertensive patients—a randomized double-blind placebo-controlled pilot study. Nutr J, 12:138.
[31]ShreiberDI, EneverPAJ, TranquilloRT, 2001. Effects of PDGF-BB on rat dermal fibroblast behavior in mechanically stressed and unstressed collagen and fibrin gels. Exp Cell Res, 266(1):155-166.
[32]SmallHY, MigliarinoS, Czesnikiewicz-GuzikM, et al., 2018. Hypertension: focus on autoimmunity and oxidative stress. Free Radic Biol Med, 125:104-115.
[33]UpadrastaA, MadempudiRS, 2016. Probiotics and blood pressure: current insights. Integr Blood Press Control, 9:33-42.
[34]van ThielBS, van der PluijmI, te RietL, et al., 2015. The renin-angiotensin system and its involvement in vascular disease. Eur J Pharmacol, 763:3-14.
[35]VaziriND, WangXQ, OveisiF, et al., 2000. Induction of oxidative stress by glutathione depletion causes severe hypertension in normal rats. Hypertension, 36(1):142-146.
[36]WaliJA, RondasD, McKenzieMD, et al., 2014. The proapoptotic BH3-only proteins Bim and Puma are downstream of endoplasmic reticulum and mitochondrial oxidative stress in pancreatic islets in response to glucotoxicity. Cell Death Dis, 5(3):e1124.
[37]WanL, NieGJ, ZhangJ, et al., 2011. β-Amyloid peptide increases levels of iron content and oxidative stress in human cell and Caenorhabditis elegans models of Alzheimer disease. Free Radic Biol Med, 50(1):122-129.
[38]WangJY, SunPP, BaoYM, et al., 2012. Vitamin E renders protection to PC12 cells against oxidative damage and apoptosis induced by single-walled carbon nanotubes. Toxicol in Vitro, 26(1):32-41.
[39]WangZX, WangY, ChenYF, et al., 2016. The IL-24 gene protects human umbilical vein endothelial cells against H2O2-induced injury and may be useful as a treatment for cardiovascular disease. Int J Mol Med, 37(3):581-592.
[40]WasilewskaE, ZłotkowskaD, PijaginME, 2013. The role of intestinal microflora and probiotic bacteria in prophylactic and development of colorectal cancer. Postepy Hig Med Dosw, 67:837-847.
[41]WuQ, LiuXX, LuDY, et al., 2018. Protective effect of polygonum orientale flower extract on H₂O₂-induced oxidative damage of HUVEC cells. China J Chin Mat Med, 43(5):1008-1013 (in Chinese).
[42]WuYC, WangYM, NabiX, 2019. Protective effect of Ziziphora clinopodioides flavonoids against H2O2-induced oxidative stress in HUVEC cells. Biomed Pharmacother, 117:109156.
[43]YangGL, JiangYL, YangWT, et al., 2015. Effective treatment of hypertension by recombinant Lactobacillus plantarum expressing angiotensin converting enzyme inhibitory peptide. Microb Cell Fact, 14:202.
[44]YangT, SantistebanMM, RodriguezV, et al., 2015. Gut dysbiosis is linked to hypertension. Hypertension, 65(6):1331-1340.
[45]YoungCN, DavissonRL, 2015. Angiotensin-II, the brain, and hypertension. Hypertension, 66(5):920-926.
[46]ZengMY, MiraldaI, ArmstrongCL, et al., 2019. The roles of NADPH oxidase in modulating neutrophil effector responses. Mol Oral Microbiol, 34(2):27-38.
[47]ZhangSS, QinFX, YangLY, et al., 2016. Nucleophosmin mutations induce chemosensitivity in THP-1 leukemia cells by suppressing NF-κB activity and regulating Bax/Bcl-2 expression. J Cancer, 7(15):2270-2279.
[48]ZhangY, ZouCS, YangSW, et al., 2016. p120 catenin attenuates the angiotensin II-induced apoptosis of human umbilical vein endothelial cells by suppressing the mitochondrial pathway. Int J Mol Med, 37(3):623-630.
[49]ZhouB, BenthamJ, di CesareM, et al., 2017. Worldwide trends in blood pressure from 1975 to 2015: a pooled analysis of 1479 population-based measurement studies with 19·1 million participants. Lancet, 389(10064):37-55.
[50]ZittermannA, PilzS, 2019. Vitamin D and cardiovascular disease: an update. Anticancer Res, 39(9):4627-4635.
Open peer comments: Debate/Discuss/Question/Opinion
<1>