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Anti-atherosclerotic effects of Lactobacillus plantarum ATCC 14917 in ApoE−/− mice through modulation of proinflammatory cytokines and oxidative stress

  • Applied microbial and cell physiology
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Abstract

Atherosclerosis is a chronic inflammatory disease mediated by monocyte infiltration and cholesterol deposition into the subendothelial area, resulting in foam cell development. Probiotics are live bacteria that are beneficial for health when administered orally in adequate amounts. In this study, 8-week-old atherosclerosis-prone apolipoprotein E-deficient (ApoE−/−) mice were fed with or without Lactobacillus plantarum ATCC 14917 per day for 12 weeks. Serum was collected to analyse the lipid profile, oxidative status and proinflammatory cytokines. The heart was isolated to quantify the atherosclerotic lesion size in the aortic arch. Quantitative real-time polymerase chain reaction was performed to determine the expression levels of tumour necrosis factor-alpha (TNF-α) and interleukin (IL)-1β in the aorta. The proteins extracted from the aorta were used for Western blot analysis to assess the expression levels of nuclear factor kappa B (NF-κB) and inhibitor of NF-κB (IκBα). The composition of gut microbiota was also examined through high-throughput sequencing. Results showed that the daily consumption of L. plantarum ATCC 14917 had no effect on body weight and lipid profile. L. plantarum ATCC 14917 treatment significantly inhibited atherosclerotic lesion formation. In addition, the oxLDL, MDA, TNF-α and IL-1β levels were significantly reduced, whereas the SOD level was induced in the bacteria + high-fat diet group. Furthermore, the administration of L. plantarum ATCC 14917 significantly attenuated IκBα protein degradation and inhibited the translocation of P65 subunits of NF-κB. L. plantarum ATCC 14917 treatment also modulated the composition of gut microbiota in ApoE−/− mice. Our findings showed that L. plantarum ATCC 14917 supplementation decreases the progression of atherosclerotic lesion formation by alleviating the inflammatory process and lowering oxidative stress.

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References

  • Aupperle KR, Bennett BL, Boyle DL, Tak P-P, Manning AM, Firestein GS (1999) NF-κB regulation by IκB kinase in primary fibroblast-like synoviocytes. J Immunolo 163(1):427–433

    CAS  Google Scholar 

  • Bagarolli RA, Tobar N, Oliveira AG, Araújo TG, Carvalho BM, Rocha GZ, Vecina JF, Calisto K, Guadagnini D, Prada PO (2017) Probiotics modulate gut microbiota and improve insulin sensitivity in DIO mice. J nutr biochem 50:16–25

    CAS  PubMed  Google Scholar 

  • Barath P, Fishbein MC, Cao J, Berenson J, Helfant RH, Forrester JS (1990) Tumor necrosis factor gene expression in human vascular intimal smooth muscle cells detected by in situ hybridization. Am J Pathol 137(3):503–509

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bendele AM, Chlipala ES, Scherrer J, Frazier J, Sennello G, Rich WJ, Edwards CK III (2000) Combination benefit of treatment with the cytokine inhibitors interleukin-1 receptor antagonist and PEGylated soluble tumor necrosis factor receptor type I in animal models of rheumatoid arthritis. Arthritis Rheum 43(12):2648–2659

    CAS  PubMed  Google Scholar 

  • Bevilacqua MP, Pober JS, Mendrick DL, Cotran RS, Gimbrone MA (1987) Identification of an inducible endothelial-leukocyte adhesion molecule. Proc Natl Acad Sci U.S.A. 84(24):9238–9242

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brand K, Eisele T, Kreusel U, Page M, Page S, Haas M, Gerling A, Kaltschmidt C, Neumann F-J, Mackman N (1997) Dysregulation of monocytic nuclear factor-κB by oxidized low-density lipoprotein. Arterioscler Thromb Vasc Biol 17(10):1901–1909

    CAS  PubMed  Google Scholar 

  • Cain BS, Meldrum DR, Dinarello CA, Meng X, Joo KS, Banerjee A, Harken AH (1999) Tumor necrosis factor-alpha and interleukin-1 beta synergistically depress human myocardial function. Crit Care Med 27(7):1309–1318

    CAS  PubMed  Google Scholar 

  • Cavender D, Saegusa Y, Ziff M (1987) Stimulation of endothelial cell binding of lymphocytes by tumor necrosis factor. J Immunolo 139(6):1855–1860

    CAS  Google Scholar 

  • Cha J-K, Jeong M-H, Bae H-R, Han J-Y, Jeong S-J, Jin H-J (2000) Activated platelets induce secretion of interleukin-1, monocyte chemotactic protein-1, and macrophage inflammatory protein-1 and surface expression of intercellular adhesion molecule-1 on cultured endothelial cells. J. Korean Med. Sci 15:273–278

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Liu W, Li Y, Luo S, Liu Q, Zhong Y, Jian Z, Bao M (2013) Lactobacillus acidophilus ATCC 4356 attenuates the atherosclerotic progression through modulation of oxidative stress and inflammatory process. Int Immunopharmacol 17(1):108–115. https://doi.org/10.1016/j.intimp.2013.05.018

    Article  CAS  PubMed  Google Scholar 

  • Cheng B-H, Sheen L-Y, Chang S-T (2018) Hypolipidemic effects of S-(+)-linalool and essential oil from Cinnamomum osmophloeum ct. linalool leaves in mice. JTCM 8(1):46–52

    PubMed  Google Scholar 

  • Dalile B, Van Oudenhove L, Vervliet B, Verbeke K (2019) The role of short-chain fatty acids in microbiota–gut–brain communication. Nat Rev Gastroenterol Hepatol 16(8):461–478. https://doi.org/10.1038/s41575-019-0157-3

    Article  PubMed  Google Scholar 

  • David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505(7484):559–563

    CAS  PubMed  Google Scholar 

  • De Beer MC, Wroblewski JM, Noffsinger VP, Rateri DL, Howatt DA, Balakrishnan A, Ji A, Shridas P, Thompson JC, van der Westhuyzen DR (2014) Deficiency of endogenous acute phase serum amyloid a does not affect atherosclerotic lesions in apolipoprotein E–deficient mice. Arterioscler Thromb Vasc Biol 34(2):255–261

    PubMed  Google Scholar 

  • De León H, Boué S, Schlage WK, Boukharov N, Westra JW, Gebel S, VanHooser A, Talikka M, Fields RB, Veljkovic E (2014) A vascular biology network model focused on inflammatory processes to investigate atherogenesis and plaque instability. J Transl Med 12(1):185

    PubMed  PubMed Central  Google Scholar 

  • Di Cerbo A, Palmieri B, Aponte M, Morales-Medina JC, Iannitti T (2016) Mechanisms and therapeutic effectiveness of lactobacilli. J Clin Pathol 69(3):187–203

    PubMed  Google Scholar 

  • Din AU, Hassan A, Zhu Y, Zhang K, Wang Y, Li T, Wang Y, Wang G (2020) Inhibitory effect of Bifidobacterium bifidum ATCC 29521 on colitis and its mechanism. J Nutri Biochem:108353. https://doi.org/10.1016/j.jnutbio.2020.108353

  • Drosos I, Tavridou A, Kolios G (2015) New aspects on the metabolic role of intestinal microbiota in the development of atherosclerosis. Metab 64(4):476–481

    CAS  Google Scholar 

  • Elhage R, Maret A, Pieraggi M-T, Thiers J, Arnal J, Bayard F (1998) Differential effects of interleukin-1 receptor antagonist and tumor necrosis factor binding protein on fatty-streak formation in apolipoprotein E–deficient mice. Circulation 97(3):242–244

    CAS  PubMed  Google Scholar 

  • Gawaz M, Brand K, Dickfeld T, Pogatsa-Murray G, Page S, Bogner C, Koch W, Schömig A, Neumann F-J (2000) Platelets induce alterations of chemotactic and adhesive properties of endothelial cells mediated through an interleukin-1-dependent mechanism. Implications for atherogenesis. Atherosclerosis 148(1):75–85

    CAS  PubMed  Google Scholar 

  • Hansson GK, Hermansson A (2011) The immune system in atherosclerosis. Nat Immunol 12(3):204–212

    CAS  PubMed  Google Scholar 

  • Heinecke JW (1998) Oxidants and antioxidants in the pathogenesis of atherosclerosis: implications for the oxidized low density lipoprotein hypothesis. Atherosclerosis 141(1):1–15

    CAS  PubMed  Google Scholar 

  • Hudault S, Liévin V, Bernet-Camard M-F, Servin AL (1997) Antagonistic activity exerted in vitro and in vivo by Lactobacillus casei (strain GG) against Salmonella typhimurium C5 infection. Appl. Environ. Microbiol. 63(2):513–518

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ismail NA, Ragab S, Elbaky AA, Shoeib ARS, Alhosary Y, Fekry D (2011) Frequency of Firmicutes and Bacteroidetes in gut microbiota in obese and normal weight Egyptian children and adults. Arch Med Sci 7(3):501–507

    CAS  Google Scholar 

  • Jacobs MD, Harrison SC (1998) Structure of an IκBα/NF-κB complex. Cell 95(6):749–758

    CAS  PubMed  Google Scholar 

  • Jawien J (2012) The role of an experimental model of atherosclerosis: apoE-knockout mice in developing new drugs against atherogenesis. Curr Pharm Biotechnol 13(13):2435–2439

    CAS  PubMed  Google Scholar 

  • Ji Y, Kim HN, Park H, Lee J, Yeo S, Yang J, Park SY, H-s Y, Cho G-S, Franz C, Bomba A, Shin H, Holzapfel W (2012) Modulation of the murine microbiome with a concomitant anti-obesity effect by Lactobacillus rhamnosus GG and Lactobacillus sakei NR28. Beneficial microbes 3:13–22. https://doi.org/10.3920/BM2011.0046

    Article  CAS  PubMed  Google Scholar 

  • Jie Z, Xia H, Zhong S-L, Feng Q, Li S, Liang S, Zhong H, Liu Z, Gao Y, Zhao H, Zhang D, Su Z, Fang Z, Lan Z, Li J, Xiao L, Li J, Li R, Li X, Li F, Ren H, Huang Y, Peng Y, Li G, Wen B, Dong B, Chen J-Y, Geng Q-S, Zhang Z-W, Yang H, Wang J, Wang J, Zhang X, Madsen L, Brix S, Ning G, Xu X, Liu X, Hou Y, Jia H, He K, Kristiansen K (2017) The gut microbiome in atherosclerotic cardiovascular disease. Nat. Commun 8(1):845. https://doi.org/10.1038/s41467-017-00900-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kan H, Xie Z, Finkel MS (1999) TNF-α enhances cardiac myocyte NO production through MAP kinase-mediated NF-κB activation. Am J Physiol Heart Circ Physiol 277(4):H1641–H1646

    CAS  Google Scholar 

  • Karimi S, Dadvar M, Modarress H, Dabir B (2013) Kinetic modeling of low density lipoprotein oxidation in arterial wall and its application in atherosclerotic lesions prediction. Chem Phys Lipids 175:1–8

    PubMed  Google Scholar 

  • Kasahara K, Tanoue T, Yamashita T, Yodoi K, Matsumoto T, Emoto T, Mizoguchi T, Hayashi T, Kitano N, Sasaki N (2017) Commensal bacteria at the crossroad between cholesterol homeostasis and chronic inflammation in atherosclerosis. J lipid Res 58(3):519–528

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kawashima T, Hayashi K, Kosaka A, Kawashima M, Igarashi T, Tsutsui H, Tsuji NM, Nishimura I, Hayashi T, Obata A (2011) Lactobacillus plantarum strain YU from fermented foods activates Th1 and protective immune responses. Int Immunopharmacol 11(12):2017–2024

    CAS  PubMed  Google Scholar 

  • Kim B, Kwon J, Kim M-S, Park H, Ji Y, Holzapfel W, Hyun C-K (2019) Protective effects of Bacillus probiotics against high-fat diet-induced metabolic disorders in mice. PLoS ONE 13(12):e0210120. https://doi.org/10.1371/journal.pone.0210120

    Article  CAS  Google Scholar 

  • Kirii H, Niwa T, Yamada Y, Wada H, Saito K, Iwakura Y, Asano M, Moriwaki H, Seishima M (2003) Lack of interleukin-1β decreases the severity of atherosclerosis in ApoE-deficient mice. Arterioscler Thromb Vasc Biol 23(4):656–660

    CAS  PubMed  Google Scholar 

  • Kunsch C, Medford RM (1999) Oxidative stress as a regulator of gene expression in the vasculature. Circ Res 85(8):753–766

    CAS  PubMed  Google Scholar 

  • Lamon BD, Hajjar DP (2008) Inflammation at the molecular interface of atherogenesis: an anthropological journey. Am j patholo 173(5):1253–1264

    Google Scholar 

  • Lee DK, Jang S, Baek EH, Kim MJ, Lee KS, Shin HS, Chung MJ, Kim JE, Lee KO, Ha NJ (2009) Lactic acid bacteria affect serum cholesterol levels, harmful fecal enzyme activity, and fecal water content. Lipids Health Dis 8(1):21

    PubMed  PubMed Central  Google Scholar 

  • Li M, Wang B, Zhang M, Rantalainen M, Wang S, Zhou H, Zhang Y, Shen J, Pang X, Zhang M (2008) Symbiotic gut microbes modulate human metabolic phenotypes. Proc Natl Acad Sci U.S.A 105(6):2117–2122

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Huang D, Gao A, Yang X (2016) Stachyose increases absorption and hepatoprotective effect of tea polyphenols in high fructose-fed mice. Mol Nutr Food Res 60(3):502–510

    CAS  PubMed  Google Scholar 

  • Liu B, Zhang Y, Wang R, An Y, Gao W, Bai L, Li Y, Zhao S, Fan J, Liu E (2018) Western diet feeding influences gut microbiota profiles in apoE knockout mice. Lipids Health Dis 17(1):159

    PubMed  PubMed Central  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71(12):8228–8235

    CAS  PubMed  PubMed Central  Google Scholar 

  • Malik M, Suboc TM, Tyagi S, Salzman N, Wang J, Ying R, Tanner MJ, Kakarla M, Baker JE, Widlansky ME (2018) Lactobacillus plantarum 299v supplementation improves vascular endothelial function and reduces inflammatory biomarkers in men with stable coronary artery disease. Circul Res 123(9):1091–1102. https://doi.org/10.1161/CIRCRESAHA.118.313565

    Article  CAS  Google Scholar 

  • Matsuura E, Lopez L (2008) Autoimmune-mediated atherothrombosis. Lupus 17(10):879–888

    Google Scholar 

  • Merhi-Soussi F, Kwak BR, Magne D, Chadjichristos C, Berti M, Pelli G, James RW, Mach F, Gabay C (2005) Interleukin-1 plays a major role in vascular inflammation and atherosclerosis in male apolipoprotein E-knockout mice. Cardiovasc Res 66(3):583–593

    CAS  PubMed  Google Scholar 

  • Ming WJ, Bersani L, Mantovani A (1987) Tumor necrosis factor is chemotactic for monocytes and polymorphonuclear leukocytes. J Immunol 138(5):1469–1474

    CAS  PubMed  Google Scholar 

  • Moyaperez A, Neef A, Sanz Y (2015) Bifidobacterium pseudocatenulatum CECT 7765 reduces obesity-associated inflammation by restoring the lymphocyte–macrophage balance and gut microbiota structure in high-fat diet-fed mice. PLoS. ONE 10(7)

  • Nishitani Y, Tanoue T, Yamada K, Ishida T, Yoshida M, Azuma T, Mizuno M (2009) Lactococcus lactis subsp. cremoris FC alleviates symptoms of colitis induced by dextran sulfate sodium in mice. Int Immunopharmacol 9(12):1444–1451

    CAS  PubMed  Google Scholar 

  • Olofsson PS, Sheikine Y, Jatta K, Ghaderi M, Samnegård A, Eriksson P, Sirsjö A (2009) A functional interleukin-1 receptor antagonist polymorphism influences atherosclerosis development. Circ J 73(8):1531–1536

    CAS  PubMed  Google Scholar 

  • Ortega-Anaya J, Hernández-Santoyo A (2016) Production of bioactive conjugated linoleic acid by the multifunctional enolase from Lactobacillus plantarum. Int J Biol Macromol 91:524–535

    CAS  PubMed  Google Scholar 

  • Osborn L, Hession C, Tizard R, Vassallo C, Luhowskyj S, Chi-Rosso G, Lobb R (1989) Direct expression cloning of vascular cell adhesion molecule 1, a cytokine-induced endothelial protein that binds to lymphocytes. Cell 59(6):1203–1211

    CAS  PubMed  Google Scholar 

  • Park J-S, Lee E-J, Lee J-C, Kim W-K, Kim H-S (2007a) Anti-inflammatory effects of short chain fatty acids in IFN-gamma-stimulated RAW 264.7 murine macrophage cells: involvement of NF-kappaB and ERK signaling pathways. Int Immunopharmacol 7(1):70–77. https://doi.org/10.1016/j.intimp.2006.08.015

    Article  CAS  PubMed  Google Scholar 

  • Park YH, Kim JG, Shin YW, Kim SH, Whang KY (2007b) Effect of dietary inclusion of Lactobacillus acidophilus ATCC 43121 on cholesterol metabolism in rats. J Microbiol Biotechnol 17(4):655–662

    CAS  PubMed  Google Scholar 

  • Paulson JN, Stine OC, Bravo HC, Pop M (2013) Differential abundance analysis for microbial marker-gene surveys. Nat methods 10(12):1200–1202. https://doi.org/10.1038/nmeth.2658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng L, Li Z-R, Green R, Holzman I, Lin J (2009) Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J. Nutr 139:1619–1625. https://doi.org/10.3945/jn.109.104638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Philippot L, Spor A, Henault C, Bru D, Bizouard F, Jones CM, Sarr A, Maron P (2013) Loss in microbial diversity affects nitrogen cycling in soil. The ISME J 7(8):1609–1619

    CAS  PubMed  Google Scholar 

  • Popa C, Netea MG, Van Riel PL, Van Der Meer JW, Stalenhoef AF (2007) The role of TNF-α in chronic inflammatory conditions, intermediary metabolism, and cardiovascular risk. J lipid Res 48(4):751–762

    CAS  PubMed  Google Scholar 

  • Poppleton DI, Duchateau M, Hourdel V, Matondo M, Flechsler J, Klingl A, Beloin C, Gribaldo S (2017) Outer membrane proteome of Veillonella parvula: a diderm firmicute of the human microbiome. Front. Microbiol. 8(1215). https://doi.org/10.3389/fmicb.2017.01215

  • Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLOS ONE 5(3):e9490

    PubMed  PubMed Central  Google Scholar 

  • 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 J-M, 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/nature11450

    Article  CAS  PubMed  Google Scholar 

  • Roselli M, Devirgiliis C, Zinno P, Guantario B, Finamore A, Rami R, Perozzi G (2017) Impact of supplementation with a food-derived microbial community on obesity-associated inflammation and gut microbiota composition. Genes Nutr 12(1):25

    PubMed  PubMed Central  Google Scholar 

  • Ross R (1993) The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362(6423):801–809

    CAS  PubMed  Google Scholar 

  • Ross R (1999) Atherosclerosis—an inflammatory disease. N Engl J Med 340(2):115–126

    CAS  PubMed  Google Scholar 

  • Santos CM, Pires MCV, Leão TL, Silva AKS, Miranda LS, Martins FS, Silva AM, Nicoli JR (2018) Anti-inflammatory effect of two Lactobacillus strains during infection with Gardnerella vaginalis and Candida albicans in a HeLa cell culture model. Microbiolo 164(3):349–358

    CAS  Google Scholar 

  • Schreyer SA, Peschon JJ, LeBoeuf RC (1996) Accelerated atherosclerosis in mice lacking tumor necrosis factor receptor p55. J Biol Chem 271(42):26174–26178

    CAS  PubMed  Google Scholar 

  • Shanlin F, DAVIES MJ, STOCKER R (1998) Evidence for roles of radicals in protein oxidation in advanced human atherosclerotic plaque. Biochem J 333(3):519-525

  • Shemesh S, Kamari Y, Shaish A, Olteanu S, Kandel-Kfir M, Almog T, Grosskopf I, Apte RN, Harats D (2012) Interleukin-1 receptor type-1 in non-hematopoietic cells is the target for the pro-atherogenic effects of interleukin-1 in apoE-deficient mice. Atherosclerosis 222(2):329-336

  • Steer T, Carpenter H, Tuohy K, Gibson G (2000) Perspectives on the role of the human gut microbiota in health and methods of study. Nutr Res Rev 13:229–254

    CAS  PubMed  Google Scholar 

  • Steinbrecher UP, Fisher M, Witztum JL, Curtiss LK (1984) Immunogenicity of homologous low density lipoprotein after methylation, ethylation, acetylation, or carbamylation: generation of antibodies specific for derivatized lysine. J Lipid Res 25(10):1109–1116

    CAS  PubMed  Google Scholar 

  • Stepankova R, Tonar Z, Bartova J, Nedorost L, Rossman P, Poledne R, Schwarzer M, Tlaskalova-Hogenova H (2010) Absence of microbiota (germ-free conditions) accelerates the atherosclerosis in ApoE-deficient mice fed standard low cholesterol diet. J Atheroscler Thromb 17(8):796–804

    CAS  PubMed  Google Scholar 

  • Stocker R, Keaney JF Jr (2004) Role of oxidative modifications in atherosclerosis. Physiol Rev 84(4):1381–1478

    CAS  PubMed  Google Scholar 

  • Tamminen M, Mottino G, Qiao J, Breslow J, Frank J (1999) Ultrastructure of early lipid accumulation in ApoE-deficient mice. Arteriosclerosis, thrombosis, and vascular biology 19(4):847–853

    CAS  PubMed  Google Scholar 

  • Tang WHW, Kitai T, Hazen SL (2017) Gut microbiota in cardiovascular health and disease. Circul Res 120(7):1183–1196. https://doi.org/10.1161/CIRCRESAHA.117.309715

    Article  CAS  Google Scholar 

  • Ten Kate G, Sijbrands E, Staub D, Coll B, ten Cate F, Feinstein S, Schinkel A (2010) Noninvasive imaging of the vulnerable atherosclerotic plaque. Curr Probl Cardiol 35(11):556–591

    PubMed  Google Scholar 

  • Tsuda H, Miyamoto T (2010) Guidelines for the evaluation of probiotics in food. Report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food Guidelines for the evaluation of probiotics in food. Report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food, 2002. Food Sci Technol Res 16(1):87–92

    CAS  Google Scholar 

  • Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI (2008) Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host & Microbe 3(4):213–223. https://doi.org/10.1016/j.chom.2008.02.015

    Article  CAS  Google Scholar 

  • Uchida K (2006) Lipofuscin-like fluorophores originated from malondialdehyde. Free Radic Res 40(12):1335–1338

    CAS  PubMed  Google Scholar 

  • Vilcek J, Lee TH (1991) Tumor necrosis factor. New insights into the molecular mechanisms of its multiple actions. J Biol Chem 266(12):7313–7316

    CAS  PubMed  Google Scholar 

  • Von Holt K, Lebrun S, Stinn W, Conroy L, Wallerath T, Schleef R (2009) Progression of atherosclerosis in the Apo E−/− model: 12-month exposure to cigarette mainstream smoke combined with high-cholesterol/fat diet. Atherosclerosis 205(1):135–143

    Google Scholar 

  • Wu G, Xiao X, Feng P, Xie F, Yu Z, Yuan W, Liu P, Li X (2017) Gut remediation: a potential approach to reducing chromium accumulation using Lactobacillus plantarum TW1-1. Sci rep 7(1):15000

    PubMed  PubMed Central  Google Scholar 

  • Yamada S, Kumazawa S, Ishii T, Nakayama T, Itakura K, Shibata N, Kobayashi M, Sakai K, Osawa T, Uchida K (2001) Immunochemical detection of a lipofuscin-like fluorophore derived from malondialdehyde and lysine. J lipid Res 42(8):1187–1196

    CAS  PubMed  Google Scholar 

  • Zhang SH, Reddick RL, Piedrahita JA, Maeda N (1992) Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 258(5081):468–471

    CAS  PubMed  Google Scholar 

  • Zhang LS, Xu M, Yang Q, Lou D, Howles PN, Tso P (2015) ABCG5/G8 deficiency in mice reduces dietary triacylglycerol and cholesterol transport into the lymph. Lipids 50(4):371–379

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Li Y, Wang X, Wang S, Bi D (2019) The impact of Lactobacillus plantarum on the gut microbiota of mice with DSS-induced colitis. BioMed Res Int 2019:3921315

    PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Li T, Din AU, Hassan A, Wang Y, Wang G (2019) Beneficial effects of Enterococcus faecalis in hypercholesterolemic mice on cholesterol transportation and gut microbiota. AMAB:1-11

  • Zohlnhöfer D, Brand K, Schipek K, Pogatsa-Murray G, Schömig A, Neumann F-J (2000) Adhesion of monocyte very late antigen-4 to endothelial vascular cell adhesion molecule-1 induces interleukin-1β–dependent expression of interleukin-6 in endothelial cells. Arterioscler Thromb Vasc Biol. 20(2):353–359

    PubMed  Google Scholar 

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Acknowledgements

This study was supported by grants from the National Natural Science Foundation of China (31971242), Chongqing Science and Technology Bureau, China (cstc2019jcyj-zdxm0033), Chongqing Municipal Education Commission, China (KYYJ202001), the Fundamental Research Funds for the Central Universities (2018CDPTCG0001-10), Chongqing Key Laboratory of Translational Research for Cancer Metastasis and Individualized Treatment (CMIT201803). We are also thankful for the support from the Public Experiment Centre of State Bio-industrial Base (Chongqing).

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  1. A.H. and A.U.D. contributed equally and are considered co-first authors.

Authors and Affiliations

  1. Key Laboratory for Biorheological Science and Technology of Ministry of Education, State and Local Joint Engineering Laboratory for Vascular Implants, Bioengineering College of Chongqing University, Chongqing, 400030, China

    Adil Hassan, Ahmad Ud Din, Yuan Zhu, Kun Zhang, Tianhan Li, Yi Wang & Guixue Wang

  2. Drug Discovery Research Centre, Southwest Medical University, Luzhou, 646000, China

    Ahmad Ud Din

  3. The Centre of Laboratory Medicine, The Sixth People’s Hospital of Chongqing, Chongqing, 400060, China

    Shangcheng Xu

  4. Chongqing Key Laboratory of Translational Research for Cancer Metastasis and Individual Treatment, Chongqing University Cancer Hospital and Chongqing Cancer Hospital, Chongqing, 400030, China

    Haike Lei & Xian Yu

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  1. Adil Hassan
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Correspondence to Guixue Wang.

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Hassan, A., Din, A.U., Zhu, Y. et al. Anti-atherosclerotic effects of Lactobacillus plantarum ATCC 14917 in ApoE−/− mice through modulation of proinflammatory cytokines and oxidative stress. Appl Microbiol Biotechnol 104, 6337–6350 (2020). https://doi.org/10.1007/s00253-020-10693-x

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  • DOI: https://doi.org/10.1007/s00253-020-10693-x

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