Oral administration of the lactic acid bacterium Pediococcus acidilactici attenuates atherosclerosis in mice by inducing tolerogenic dendritic cells

Heart and Vessels

Volumn 32, Issue 6, 2017, Pages 768-776

  Mizoguchi, Taiji ^a   Kasahara, Kazuyuki ^a   Yamashita, Tomoya ^a   Sasaki, Naoto ^a   Yodoi, Keiko ^a   Matsumoto, Takuya ^a   Emoto, Takuo ^a   Hayashi, Tomohiro ^a   Kitano, Naoki ^a   Yoshida, Naofumi ^a   Amin, Hilman Zulkifli ^a   Hirata, Ken ichi ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Atherosclerosis; Dendritic cells; Probiotic; Programmed death ligand 1

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; KI 67 ANTIGEN; PROBIOTIC AGENT; R 037; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTIC ROOT; ARTICLE; ATHEROSCLEROSIS; ATTENUATION; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG EFFECT; FEMALE; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PEDIOCOCCUS ACIDILACTICI; PRIORITY JOURNAL; SPLEEN; SPLEEN LYMPHOCYTE; TH1 CELL; TREATMENT DURATION; ANIMAL; AORTA; APOLIPOPROTEIN E KNOCKOUT MOUSE; IMMUNOLOGY; ORAL DRUG ADMINISTRATION; PATHOLOGY;

ADMINISTRATION, ORAL; ANIMALS; AORTA; ATHEROSCLEROSIS; CD4-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; FEMALE; MICE; MICE, KNOCKOUT, APOE; PEDIOCOCCUS ACIDILACTICI; PROBIOTICS;

EID: 85011851688     PISSN: 09108327     EISSN: 16152573     Source Type: Journal    
DOI: 10.1007/s00380-017-0949-8     Document Type: Article

References (33)

1. Weber C, Zernecke A, Libby P (2008) The multifaceted contributions of leukocyte subsets to atherosclerosis: Lessons from mouse models. Nat Rev Immunol 8:802–815
2. Hansson GK, Hermansson A (2011) The immune system in atherosclerosis. Nat Immunol 12:204–212
3. Gupta S, Pablo AM, Jiang XC, Wang N, Tall AR, Schindler C (1997) IFN-γ potentiates atherosclerosis in ApoE knock-out mice. J Clin Invest 99:2752–2761
4. Ait-Oufella H, Salomon BL, Potteaux S, Robertson AK, Gourdry P, Zoll J, Merval R, Esposito B, Cohen JL, Fisson S, Flavell RA, Hansson GK, Klatzmann D, Tedgui A, Mallat Z (2006) Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med 12:178–180
5. Ait-Oufella H, Sage AP, Mallat Z, Tedgui A (2014) Adaptive (T and B cells) immunity and control by dendritic cells in atherosclerosis. Circ Res 114:1640–1660
6. Buono C PH, Uchida Y, Libby P, Sharpe AH, Lichtman AH (2004) B7-1/B7-2 costimulation regulates plaque antigen-specific T-cell responses and atherogenesis in low-density lipoprotein receptor-deficient mice. Circulation 109:2009–2015
7. Latchman Y, Wood CR, Chernova T, Chaudhary D, Borde M, Chernova I, Iwai I, Long AJ, Brown JA, Nunes R, Greenfield EA, Bourque K, Boussiotis VA, Carter LL, Carreno BM, Malenkovich N, Nishimura H, Okazaki T, Honjo T, Sharpe AH, Freeman GJ (2001) PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat Immunol 2:261–268
8. Latchman YE, Liang SC, Wu Y, Chernova T, Sobel RA, Klemm M, Kuchroo VK, Freeman GJ, Sharpe AH (2004) PD-L1-deficient mice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells. Proc Natl Acad Sci U S A 101:10691–10696
9. Keir ME, Liang SC, Guleria I, Latchman YE, Qipo A, Albacher LA, Koulmanda M, Freeman GJ, Sayegh MH, Sharpe AH (2006) Tissue expression of PD-L1 mediates peripheral T cell tolerance. J Exp Med 203:883–895
10. Bu DX, Tarrio M, Maganto-Garcia E, Stavrakis G, Tajima G, Lederer J, Jarolim P, Freeman GJ, Sharpe AH, Lichtman AH (2011) Impairment of the programmed cell death-1 pathway increases atherosclerotic lesion development and inflammation. Arterioscler Thromb Vasc Biol 31:1100–1107
11. Cochain C, Chaudhari SM, Koch M, Wiendl H, Eckstein HH, Zernecke A (2014) Programmed cell death-1 deficiency exacerbates T cell activation and atherogenesis despite expansion of regulatory T cells in atherosclerosis-prone mice. PLoS One 9:e93280. doi:10.1371/journal.pone.0093280.g001
12. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, Wei D, Goldfarb KC, Santee CA, Lynch SV, Tanoue T, Imaoka A, Itoh K, Takeda K, Umesaki Y, Honda K, Littman DR (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139:485–498
13. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, Cheng G, Yamasaki S, Saito T, Ohba Y, Taniguchi T, Takeda K, Hori S, Ivanov II, Umesaki Y, Itoh K, Honda K (2011) Induction of colonic regulatory T cells by indigenous clostridium species. Science 331:337–341
14. Wang Z KE, Bennett BJ, Koeth R, Levison BS, Dugar B, Feldstein AE, Britt EB, Fu X, Chung YM, Wu Y, Schauer P, Smith JD, Allayee H, Tang WH, DiDonato JA, Lusis AJ, Hazen SL (2011) Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472:57–63
15. Emoto T, Yamashita T, Sasaki N, Hirota Y, Hayashi T, So A, Kasahara K, Yodoi K, Matsumoto T, Mizoguchi T, Ogawa W, Hirata K (2016) Analysis of gut microbiota in coronary artery disease patients: a possible link between gut microbiota and coronary artery disease. J Atheroscler Thromb 23:908–921
16. Emoto T, Yamashita T, Kobayashi T, Sasaki N, Hirota Y, Hayashi T, So A, Kasahara K, Matsumoto T, Mizoguchi T, Ogawa W, Hirata K (2016) Characterization of gut microbiota profiles in coronary artery disease patients using data mining analysis of terminal restriction fragment length polymorphism: gut microbiota could be a diagnostic marker of coronary artery disease. Heart Vessels. doi:10.1007/s00380-016-0841-y
17. Huang Y, Wang J, Quan G, Wang X, Yang L, Zhong (2014) Lactobacillus acidophilus ATCC 4356 prevents atherosclerosis via inhibition of intestinal cholesterol absorption in apolipoprotein E-knockout mice. Appl Environ Microbiol 80:7496–7504. doi:10.1128/AEM.02926-14
18. 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 17:108–115
19. Tsai CC, Lin PP, Hsieh YM, Zhang ZY, Wu HC, Huang CC (2014) Cholesterol-lowering potentials of lactic acid bacteria based on bile-salt hydrolase activity and effect of potent strains on cholesterol metabolism in vitro and in vivo. ScientificWorldJournal 2014:690752
20. Wang J, Zhang H, Chen X, Chen Y, Menghebilige, Bao Q (2012) Selection of potential probiotic lactobacilli for cholesterol-lowering properties and their effect on cholesterol metabolism in rats fed a high-lipid diet. J Dairy Sci 95:1645–1654
21. Takata K, Kinoshita M, Okuno T, Moriya M, Kohda T, Honorat JA, Sugimoto T, Kumanogoh A, Kayama H, Takeda K, Sakoda S, Nakatsuji Y (2011) The lactic acid bacterium pediococcus acidilactici suppresses autoimmune encephalomyelitis by inducing IL-10-producing regulatory T cells. PLoS One 6:e27644. doi:10.1371/journal.pone.0027644
22. Sasaki N, Yamashita T, Takeda M, Shinohara M, Nakajima K, Tawa H, Usui T, Hirata K (2009) Oral anti-CD3 antibody treatment induces regulatory T cells and inhibits the development of atherosclerosis in mice. Circulation 120:1996–2005
23. + T cells in vitro. Int immunol 9:935–944
24. Manicassamy S, Pulendran B (2011) Dendritic cell control of tolerogenic responses. Immunol Rev 241:206–227
25. Dicks LM, Bites M (2010) Probiotic lactic acid bacteria in the gastro-intestinal tract: Health benefits, safety and mode of action. Benef Microbes 1:11–29
26. Watanabe T, Hamada K, Tategaki A, Kishida H, Tanaka H, Kitano M, Miyamoto T (2009) Oral administration of lactic acid bacteria isolated from traditional south asian fermented milk ‘dahi’ inhibits the development of atopic dermatitis in NC/Nga mice. J Nutr Sci Vitaminol 55:271–278
27. –/– mice. PLoS One 7:e46837. doi:10.1371/journal.pone.0046837
28. Tedgui A, Mallat Z (2006) Cytokines in atherosclerosis: Pathogenic and regulatory pathways. Physiol Rev 86:515–581
29. Taleb S TA, Mallat Z (2010) Interleukin-17: Friend or foe in atherosclerosis? Curr Opin Lipidol 21:404–408
30. Sharpe AH, Wherry EJ, Ahmed R, Freeman GJ (2007) The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nat Immunol 8:239–245
31. Ansari MJ, Salama AD, Chitnis T, Smith RN, Yagita H, Akiba H, Yamazaki T, Auchinoclass H, Sayegh MH (2003) The programmed death-1 (PD-1) pathway regulates autoimmune diabetes in nonobese diabetic (NOD) mice. J Exp Med 198:63–69
32. Okumura K, Tsukamoto H, Tsuboi H, Hirayama H, Kamiya H, Watarai M, Ishiki R, Murohara T (2015) High HDL cholesterol level after treatment with pitavastatin is an important factor for regression in carotid intima-media thickness. Heart Vessels 30:154–161
33. Nozue T, Yamamoto S, Tohyama S, Fukui K, Umezawa S, Onisi Y, Kunishima T, Sato A, Nozato T, Miyake S, Takeyama Y, Morino Y, Yamauchi T, Muramatsu T, Hirano T, Hibi K, Terashima M, Michishita I (2014) Impacts of age on coronary atherosclerosis and vascular response to statin therapy. Heart Vessels 29:456–463