Generic placeholder image

Anti-Inflammatory & Anti-Allergy Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5230
ISSN (Online): 1875-614X

Research Article

Modulation of Proinflammatory Bacteria- and Lipid-Coupled Intracellular Signaling Pathways in a Transwell Triple Co-Culture Model by Commensal Bifidobacterium Animalis R101-8

Author(s): Darab Ghadimi*, Annegret Nielsen, Mohamed Farghaly Yoness Hassan, Regina Fölster-Holst, Michael Ebsen, Sven Olaf Frahm, Christoph Röcken, Michael de Vrese and Knut J. Heller

Volume 20, Issue 2, 2021

Published on: 29 October, 2020

Page: [161 - 181] Pages: 21

DOI: 10.2174/1871523019999201029115618

Price: $65

Abstract

Background and Aims: Following a fat-rich diet, alterations in gut microbiota contribute to enhanced gut permeability, metabolic endotoxemia, and low grade inflammation–associated metabolic disorders. To better understand whether commensal bifidobacteria influence the expression of key metaflammation-related biomarkers (chemerin, MCP-1, PEDF) and modulate the pro-inflammatory bacteria- and lipid–coupled intracellular signaling pathways, we aimed at i) investigating the influence of the establishment of microbial signaling molecules-based cell-cell contacts on the involved intercellular communication between enterocytes, immune cells, and adipocytes, and ii) assessing their inflammatory mediators’ expression profiles within an inflamed adipose tissue model.

Material and Methods: Bifidobacterium animalis R101-8 and Escherichia coli TG1, respectively, were added to the apical side of a triple co-culture model consisting of intestinal epithelial HT-29/B6 cell line, human monocyte-derived macrophage cells, and adipose-derived stem cell line in the absence or presence of LPS or palmitic acid. mRNA expression levels of key lipid metabolism genes HILPDA, MCP-1/CCL2, RARRES2, SCD, SFRP2 and TLR4 were determined using TaqMan qRT-PCR. Protein expression levels of cytokines (IL-1β, IL-6, and TNF-α), key metaflammation-related biomarkers including adipokines (chemerin and PEDF), chemokine (MCP- 1) as well as cellular triglycerides were assessed by cell-based ELISA, while those of p-ERK, p-JNK, p-p38, NF-κB, p-IκBα, pc-Fos, pc-Jun, and TLR4 were assessed by Western blotting.

Results: B. animalis R101-8 inhibited LPS- and palmitic acid-induced protein expression of inflammatory cytokines IL-1β, IL-6, TNF-α concomitant with decreases in chemerin, MCP-1, PEDF, and cellular triglycerides, and blocked NF-kB and AP-1 activation pathway through inhibition of p- IκBα, pc-Jun, and pc-Fos phosphorylation. B. animalis R101-8 downregulated mRNA and protein levels of HILPDA, MCP-1/CCL2, RARRES2, SCD and SFRP2 and TLR4 following exposure to LPS and palmitic acid.

Conclusion: B. animalis R101-8 improves biomarkers of metaflammation through at least two molecular/signaling mechanisms triggered by pro-inflammatory bacteria/lipids. First, B. animalis R101-8 modulates the coupled intracellular signaling pathways via metabolizing saturated fatty acids and reducing available bioactive palmitic acid. Second, it inhibits NF-kB’s and AP-1’s transcriptional activities, resulting in the reduction of pro-inflammatory markers. Thus, the molecular basis may be formed by which commensal bifidobacteria improve intrinsic cellular tolerance against excess pro-inflammatory lipids and participate in homeostatic regulation of metabolic processes in vivo.

Keywords: Metaflammation, bifidobacteria, IL-6, adipokine, metabolism, cells.

Graphical Abstract
[1]
Fabersani, E.; Abeijon-Mukdsi, M.C.; Ross, R.; Medina, R.; González, S.; Gauffin-Cano, P. Specific strains of lactic acid bacteria differentially modulate the profile of adipokines in vitro. Front. Immunol., 2017, 8, 266.
[http://dx.doi.org/10.3389/fimmu.2017.00266] [PMID: 28348560]
[2]
Million, M.; Maraninchi, M.; Henry, M.; Armougom, F.; Richet, H.; Carrieri, P.; Valero, R.; Raccah, D.; Vialettes, B.; Raoult, D. Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii. Int. J. Obes., 2012, 36(6), 817-825.
[http://dx.doi.org/10.1038/ijo.2011.153] [PMID: 21829158]
[3]
Nitta, C.F.; Orlando, R.A. Crosstalk between immune cells and adipocytes requires both paracrine factors and cell contact to modify cytokine secretion. PLoS One, 2013, 8(10), e77306.
[http://dx.doi.org/10.1371/journal.pone.0077306] [PMID: 24204798]
[4]
Lin, Y.; Yang, X.; Yue, W.; Xu, X.; Li, B.; Zou, L.; He, R. Chemerin aggravates DSS-induced colitis by suppressing M2 macrophage polarization. Cell. Mol. Immunol., 2014, 11(4), 355-366.
[http://dx.doi.org/10.1038/cmi.2014.15] [PMID: 24727542]
[5]
Tolusso, B.; Gigante, M.R.; Alivernini, S.; Petricca, L.; Fedele, A.L.; Di Mario, C.; Aquilanti, B.; Magurano, M.R.; Ferraccioli, G.; Gremese, E. Chemerin and PEDF are metaflammation-related biomarkers of disease activity and obesity in rheumatoid arthritis. Front. Med. (Lausanne), 2018, 5, 207.
[http://dx.doi.org/10.3389/fmed.2018.00207] [PMID: 30123797]
[6]
Hou, J.; Ge, C.; Cui, M.; Liu, T.; Liu, X.; Tian, H.; Zhao, F.; Chen, T.; Cui, Y.; Yao, M.; Li, J.; Li, H. Pigment epithelium-derived factor promotes tumor metastasis through an interaction with laminin receptor in hepatocellular carcinomas. Cell Death Dis., 2017, 8(8), e2969.
[http://dx.doi.org/10.1038/cddis.2017.359] [PMID: 28771223]
[7]
Ma, S.; Wang, S.; Li, M.; Zhang, Y.; Zhu, P. The effects of pigment epithelium-derived factor on atherosclerosis: putative mechanisms of the process. Lipids Health Dis., 2018, 17(1), 240.
[http://dx.doi.org/10.1186/s12944-018-0889-z] [PMID: 30326915]
[8]
Ren, K.; Jiang, T.; Chen, J.; Zhao, G.J. PEDF ameliorates macrophage inflammation via NF-κB suppression. Int. J. Cardiol., 2017, 247, 42.
[http://dx.doi.org/10.1016/j.ijcard.2017.07.069] [PMID: 28916080]
[9]
Chavan, S.S.; Hudson, L.K.; Li, J.H.; Ochani, M.; Harris, Y.; Patel, N.B.; Katz, D.; Scheinerman, J.A.; Pavlov, V.A.; Tracey, K.J. Identification of pigment epithelium-derived factor as an adipocyte-derived inflammatory factor. Mol. Med., 2012, 18, 1161-1168.
[http://dx.doi.org/10.2119/molmed.2012.00156] [PMID: 22714715]
[10]
Famulla, S.; Lamers, D.; Hartwig, S.; Passlack, W.; Horrighs, A.; Cramer, A.; Lehr, S.; Sell, H.; Eckel, J. Pigment epithelium-derived factor (PEDF) is one of the most abundant proteins secreted by human adipocytes and induces insulin resistance and inflammatory signaling in muscle and fat cells. Int. J. Obes., 2011, 35(6), 762-772.
[http://dx.doi.org/10.1038/ijo.2010.212] [PMID: 20938440]
[11]
Zhou, Y.; Xu, F.; Deng, H.; Bi, Y.; Sun, W.; Zhao, Y.; Chen, Z.; Weng, J. PEDF expression is inhibited by insulin treatment in adipose tissue via suppressing 11β-HSD1. PLoS One, 2013, 8(12), e84016.
[http://dx.doi.org/10.1371/journal.pone.0084016] [PMID: 24367624]
[12]
Hotamisligil, G.S. Inflammation, metaflammation and immunometabolic disorders. Nature, 2017, 542(7640), 177-185.
[http://dx.doi.org/10.1038/nature21363] [PMID: 28179656]
[13]
Mancuso, P. The role of adipokines in chronic inflammation. ImmunoTargets Ther., 2016, 5, 47-56.
[http://dx.doi.org/10.2147/ITT.S73223] [PMID: 27529061]
[14]
Gögebakan, Ö.; Osterhoff, M.A.; Schüler, R.; Pivovarova, O.; Kruse, M.; Seltmann, A.C.; Mosig, A.S.; Rudovich, N.; Nauck, M.; Pfeiffer, A.F. GIP increases adipose tissue expression and blood levels of MCP-1 in humans and links high energy diets to inflammation: A randomised trial. Diabetologia, 2015, 58(8), 1759-1768.
[http://dx.doi.org/10.1007/s00125-015-3618-4] [PMID: 25994074]
[15]
Märker, T.; Sell, H.; Zillessen, P.; Glöde, A.; Kriebel, J.; Ouwens, D.M.; Pattyn, P.; Ruige, J.; Famulla, S.; Roden, M.; Eckel, J.; Habich, C. Heat shock protein 60 as a mediator of adipose tissue inflammation and insulin resistance. Diabetes, 2012, 61(3), 615-625.
[http://dx.doi.org/10.2337/db10-1574] [PMID: 22315307]
[16]
Sanchez-Infantes, D.; White, U.A.; Elks, C.M.; Morrison, R.F.; Gimble, J.M.; Considine, R.V.; Ferrante, A.W.; Ravussin, E.; Stephens, J.M. Oncostatin m is produced in adipose tissue and is regulated in conditions of obesity and type 2 diabetes. J. Clin. Endocrinol. Metab., 2014, 99(2), E217-E225.
[http://dx.doi.org/10.1210/jc.2013-3555] [PMID: 24297795]
[17]
Ertunc, M.E.; Hotamisligil, G.S. Lipid signaling and lipotoxicity in metaflammation: indications for metabolic disease pathogenesis and treatment. J. Lipid Res., 2016, 57(12), 2099-2114.
[http://dx.doi.org/10.1194/jlr.R066514] [PMID: 27330055]
[18]
Rogero, M.M.; Calder, P.C. Obesity, inflammation, toll-Like receptor 4 and fatty acids. Nutrients, 2018, 10(4), 432.
[http://dx.doi.org/10.3390/nu10040432] [PMID: 29601492]
[19]
Plotnikov, A.; Zehorai, E.; Procaccia, S.; Seger, R. The MAPK cascades: signaling components, nuclear roles and mechanisms of nuclear translocation. Biochim. Biophys. Acta, 2011, 1813(9), 1619-1633.
[http://dx.doi.org/10.1016/j.bbamcr.2010.12.012] [PMID: 21167873]
[20]
Kitaura, Y.; Inoue, K.; Kato, N.; Matsushita, N.; Shimomura, Y. Enhanced oleate uptake and lipotoxicity associated with laurate. FEBS Open Bio, 2015, 5, 485-491.
[http://dx.doi.org/10.1016/j.fob.2015.05.008] [PMID: 26106523]
[21]
Carta, G.; Murru, E.; Banni, S.; Manca, C. Palmitic acid: physiological role, metabolism and nutritional implications. Front. Physiol., 2017, 8, 902.
[http://dx.doi.org/10.3389/fphys.2017.00902] [PMID: 29167646]
[22]
Ghadimi, D.; Vrese, Md.; Heller, K.J.; Schrezenmeir, J. Effect of natural commensal-origin DNA on toll-like receptor 9 (TLR9) signaling cascade, chemokine IL-8 expression, and barrier integritiy of polarized intestinal epithelial cells. Inflamm. Bowel Dis., 2010, 16(3), 410-427.
[http://dx.doi.org/10.1002/ibd.21057] [PMID: 19714766]
[23]
Ghadimi, D.; Fölster-Holst, R.; de Vrese, M.; Winkler, P.; Heller, K.J.; Schrezenmeir, J. Effects of probiotic bacteria and their genomic DNA on TH1/TH2-cytokine production by peripheral blood mononuclear cells (PBMCs) of healthy and allergic subjects. Immunobiology, 2008, 213(8), 677-692.
[http://dx.doi.org/10.1016/j.imbio.2008.02.001] [PMID: 18950596]
[24]
Ghadimi, D.; Herrmann, J.; de Vrese, M.; Heller, K.J. Commensal lactic acid-producing bacteria affect host cellular lipid metabolism through various cellular metabolic pathways: role of mTOR, FOXO1, and autophagy machinery system. PharmaNutrition, 2018, 6, 215-235.
[http://dx.doi.org/10.1016/j.phanu.2018.10.004]
[25]
Pedret, A.; Valls, R.M.; Calderón-Pérez, L.; Llauradó, E.; Companys, J.; Pla-Pagà, L.; Moragas, A.; Martín-Luján, F.; Ortega, Y.; Giralt, M.; Caimari, A.; Chenoll, E.; Genovés, S.; Martorell, P.; Codoñer, F.M.; Ramón, D.; Arola, L.; Solà, R. Effects of daily consumption of the probiotic Bifidobacterium animalis subsp. lactis CECT 8145 on anthropometric adiposity biomarkers in abdominally obese subjects: A randomized controlled trial. Int. J. Obes., 2019, 43(9), 1863-1868.
[http://dx.doi.org/10.1038/s41366-018-0220-0] [PMID: 30262813]
[26]
Quigley, E.M.M. Bifidobacterium animalis spp. lactis.The microbiota in gastrointestinal pathophysiology: Implications for human health, prebiotics, probiotics, and dysbiosis; , Floch; , Ringel; , Walker, Eds.; Academic Press: London; , Floch; , Ringel; , Walker, Eds.; Academic Press: London, 2016, pp. 127-130.
[27]
Sarkar, A.; Mandal, S. Bifidobacteria-Insight into clinical outcomes and mechanisms of its probiotic action. Microbiol. Res., 2016, 192, 159-171.
[http://dx.doi.org/10.1016/j.micres.2016.07.001] [PMID: 27664734]
[28]
Takahashi, S.; Anzawa, D.; Takami, K.; Ishizuka, A.; Mawatari, T.; Kamikado, K.; Sugimura, H.; Nishijima, T. Effect of Bifidobacterium animalis ssp. lactis GCL2505 on visceral fat accumulation in healthy Japanese adults: A randomized controlled trial. Biosci. Microbiota Food Health, 2016, 35(4), 163-171.
[http://dx.doi.org/10.12938/bmfh.2016-002] [PMID: 27867803]
[29]
Guo, S.; Guo, Y.; Ergun, A.; Lu, L.; Walker, W.A.; Ganguli, K. Secreted metabolites of Bifidobacterium infantis and Lactobacillus acidophilus protect immature human enterocytes from IL-1β-induced inflammation: A transcription profiling analysis. PLoS One, 2015, 10(4), e0124549.
[http://dx.doi.org/10.1371/journal.pone.0124549] [PMID: 25906317]
[30]
Ghadimi, D.; Yoness Hassan, M.F.; Fölster-Holst, R.; Röcken, C.; Ebsen, M.; de Vrese, M.; Heller, K.J. Regulation of hepcidin/iron-signalling pathway interactions by commensal bifidobateria plays an important role for the inhibition of metaflammation-related biomarkers. Immunobiology, 2020, 225(1), 151874.
[http://dx.doi.org/10.1016/j.imbio.2019.11.009] [PMID: 31810825]
[31]
Ghadimi, D.; Nielsen, A.; Yoness Hassan, M.; Fölster-Holst, R.; de Vresea, M.; Heller, K.J. Modulation of GSK - 3β/β - catenin cascade by commensal bifidobateria plays an important role for the inhibition of metaflammation-related biomarkers in response to LPS or non-physiological concentrations of fructose: an in vitro study. PharmaNutrition, 2019, 8, 100145.
[http://dx.doi.org/10.1016/j.phanu.2019.100145]
[32]
Bojarski, C.; Gitter, A.H.; Bendfeldt, K.; Mankertz, J.; Schmitz, H.; Wagner, S.; Fromm, M.; Schulzke, J.D. Permeability of human HT-29/B6 colonic epithelium as a function of apoptosis. J. Physiol., 2001, 535(Pt 2), 541-552.
[http://dx.doi.org/10.1111/j.1469-7793.2001.00541.x] [PMID: 11533143]
[33]
Ghadimi, D.; de Vrese, M.; Heller, K.J.; Schrezenmeir, J. Lactic acid bacteria enhance autophagic ability of mononuclear phagocytes by increasing Th1 autophagy-promoting cytokine (IFN-gamma) and nitric oxide (NO) levels and reducing Th2 autophagy-restraining cytokines (IL-4 and IL-13) in response to Mycobacterium tuberculosis antigen. Int. Immunopharmacol., 2010, 10(6), 694-706.
[http://dx.doi.org/10.1016/j.intimp.2010.03.014] [PMID: 20381647]
[34]
Ruiz-Ojeda, F.J.; Rupérez, A.I.; Gomez-Llorente, C.; Gil, A.; Aguilera, C.M. Cell models and their application for studying adipogenic differentiation in relation to obesity: A review. Int. J. Mol. Sci., 2016, 17(7), 1040.
[http://dx.doi.org/10.3390/ijms17071040] [PMID: 27376273]
[35]
Chazenbalk, G.; Bertolotto, C.; Heneidi, S.; Jumabay, M.; Trivax, B.; Aronowitz, J.; Yoshimura, K.; Simmons, C.F.; Dumesic, D.A.; Azziz, R. Novel pathway of adipogenesis through cross-talk between adipose tissue macrophages, adipose stem cells and adipocytes: evidence of cell plasticity. PLoS One, 2011, 6(3), e17834.
[http://dx.doi.org/10.1371/journal.pone.0017834] [PMID: 21483855]
[36]
Keuper, M.; Dzyakanchuk, A.; Amrein, K.E.; Wabitsch, M.; Fischer-Posovszky, P. THP-1 macrophages and SGBS adipocytes - a new human in vitro model system of inflamed adipose tissue. Front. Endocrinol. (Lausanne), 2011, 2, 89.
[http://dx.doi.org/10.3389/fendo.2011.00089] [PMID: 22645513]
[37]
Harms, M.J.; Li, Q.; Lee, S.; Zhang, C.; Kull, B.; Hallen, S.; Thorell, A.; Alexandersson, I.; Hagberg, C.E.; Peng, X.R.; Mardinoglu, A.; Spalding, K.L.; Boucher, J. Mature human white adipocytes cultured under membranes maintain identity, function, and can transdifferentiate into brown-like adipocytes. Cell Rep., 2019, 27(1), 213-225.e5.
[http://dx.doi.org/10.1016/j.celrep.2019.03.026] [PMID: 30943403]
[38]
Hemmrich, K.; von Heimburg, D.; Cierpka, K.; Haydarlioglu, S.; Pallua, N. Optimization of the differentiation of human preadipocytes in vitro. Differentiation, 2005, 73(1), 28-35.
[http://dx.doi.org/10.1111/j.1432-0436.2005.07301003.x] [PMID: 15733065]
[39]
Lequeux, C.; Auxenfans, C.; Mojallal, A.; Sergent, M.; Damour, O. Optimization of a culture medium for the differentiation of preadipocytes into adipocytes in a monolayer. Biomed. Mater. Eng., 2009, 19(4-5), 283-291.
[http://dx.doi.org/10.3233/BME-2009-0593] [PMID: 20042795]
[40]
Wang, J.M.; Gu, Y.; Pan, C.J.; Yin, L.R. Isolation, culture and identification of human adipose-derived stem cells. Exp. Ther. Med., 2017, 13(3), 1039-1043.
[http://dx.doi.org/10.3892/etm.2017.4069] [PMID: 28450938]
[41]
Gantner, F.; Kupferschmidt, R.; Schudt, C.; Wendel, A.; Hatzelmann, A. In vitro differentiation of human monocytes to macrophages: change of PDE profile and its relationship to suppression of tumour necrosis factor-alpha release by PDE inhibitors. Br. J. Pharmacol., 1997, 121(2), 221-231.
[http://dx.doi.org/10.1038/sj.bjp.0701124] [PMID: 9154331]
[42]
Masuko, K. A Potential Benefit of “Balanced Diet” for Rheumatoid Arthritis. Front. Med. (Lausanne), 2018, 5, 141.
[http://dx.doi.org/10.3389/fmed.2018.00141] [PMID: 29868593]
[43]
Kishino, S.; Takeuchi, M.; Park, S.B.; Hirata, A.; Kitamura, N.; Kunisawa, J.; Kiyono, H.; Iwamoto, R.; Isobe, Y.; Arita, M.; Arai, H.; Ueda, K.; Shima, J.; Takahashi, S.; Yokozeki, K.; Shimizu, S.; Ogawa, J. Polyunsaturated fatty acid saturation by gut lactic acid bacteria affecting host lipid composition. Proc. Natl. Acad. Sci. USA, 2013, 110(44), 17808-17813.
[http://dx.doi.org/10.1073/pnas.1312937110] [PMID: 24127592]
[44]
Schübel, R.; Sookthai, D.; Greimel, J.; Johnson, T.S.; Grafetstätter, M.E.; Kirsten, R.; Kratz, M.; Ulrich, C.M.; Kaaks, R.; Kühn, T. Key genes of lipid metabolism and WNT-signaling are downregulated in subcutaneous adipose tissue with moderate weight loss. Nutrients, 2019, 11(3), 639.
[http://dx.doi.org/10.3390/nu11030639] [PMID: 30884788]
[45]
Piqué, N.; Berlanga, M.; Miñana-Galbis, D. Health benefits of heat-killed (tyndallized) probiotics: an overview. Int. J. Mol. Sci., 2019, 20(10), 2534.
[http://dx.doi.org/10.3390/ijms20102534] [PMID: 31126033]
[46]
Cullberg, K.B.; Larsen, J.Ø.; Pedersen, S.B.; Richelsen, B. Effects of LPS and dietary free fatty acids on MCP-1 in 3T3-L1 adipocytes and macrophages in vitro. Nutr. Diabetes, 2014, 4, e113.
[http://dx.doi.org/10.1038/nutd.2014.10] [PMID: 24662749]
[47]
Bermudez-Brito, M.; Muñoz-Quezada, S.; Gomez-Llorente, C.; Matencio, E.; Bernal, M.J.; Romero, F.; Gil, A. Cell-free culture supernatant of Bifidobacterium breve CNCM I-4035 decreases pro-inflammatory cytokines in human dendritic cells challenged with Salmonella typhi through TLR activation. PLoS One, 2013, 8(3), e59370.
[http://dx.doi.org/10.1371/journal.pone.0059370] [PMID: 23555025]
[48]
Ruiz, L.; Delgado, S.; Ruas-Madiedo, P.; Sánchez, B.; Margolles, A. Bifidobacteria and their molecular communication with the immune system. Front. Microbiol., 2017, 8, 2345.
[http://dx.doi.org/10.3389/fmicb.2017.02345] [PMID: 29255450]
[49]
van Nuenen, M.H.; de Ligt, R.A.; Doornbos, R.P.; van der Woude, J.C.; Kuipers, E.J.; Venema, K. The influence of microbial metabolites on human intestinal epithelial cells and macrophages in vitro. FEMS Immunol. Med. Microbiol., 2005, 45(2), 183-189.
[http://dx.doi.org/10.1016/j.femsim.2005.03.010] [PMID: 15939578]
[50]
Wang, Z.; Wang, J.; Cheng, Y.; Liu, X.; Huang, Y. Secreted factors from Bifidobacterium animalis subsp. lactis inhibit NF-κB-mediated interleukin-8 gene expression in Caco-2 cells. Appl. Environ. Microbiol., 2011, 77(22), 8171-8174.
[http://dx.doi.org/10.1128/AEM.06145-11] [PMID: 21926200]
[51]
Korbecki, J.; Bajdak-Rusinek, K. The effect of palmitic acid on inflammatory response in macrophages: An overview of molecular mechanisms. Inflamm. Res., 2019, 68(11), 915-932.
[http://dx.doi.org/10.1007/s00011-019-01273-5] [PMID: 31363792]
[52]
Orecchioni, M.; Ghosheh, Y.; Pramod, A.B.; Ley, K. Macrophage polarization: Different gene signatures in M1(LPS+) vs. classically and M2(LPS-) vs. alternatively activated macrophages. Front. Immunol., 2019, 10, 1084. [correction published in Front. Immunol., 2020, 11, 234
[http://dx.doi.org/10.3389/fimmu.2019.01084] [PMID: 31178859]
[53]
Herfarth, H.H.; Martin, C.F.; Sandler, R.S.; Kappelman, M.D.; Long, M.D. Prevalence of a gluten-free diet and improvement of clinical symptoms in patients with inflammatory bowel diseases. Inflamm. Bowel Dis., 2014, 20(7), 1194-1197.
[http://dx.doi.org/10.1097/MIB.0000000000000077] [PMID: 24865778]
[54]
Limketkai, B.N.; Sepulveda, R.; Hing, T.; Shah, N.D.; Choe, M.; Limsui, D.; Shah, S. Prevalence and factors associated with gluten sensitivity in inflammatory bowel disease. Scand. J. Gastroenterol., 2018, 53(2), 147-151.
[http://dx.doi.org/10.1080/00365521.2017.1409364] [PMID: 29216767]
[55]
Caminero, A.; McCarville, J.L.; Galipeau, H.J.; Deraison, C.; Bernier, S.P.; Constante, M.; Rolland, C.; Meisel, M.; Murray, J.A.; Yu, X.B.; Alaedini, A.; Coombes, B.K.; Bercik, P.; Southward, C.M.; Ruf, W.; Jabri, B.; Chirdo, F.G.; Casqueiro, J.; Surette, M.G.; Vergnolle, N.; Verdu, E.F. Duodenal bacterial proteolytic activity determines sensitivity to dietary antigen through protease-activated receptor-2. Nat. Commun., 2019, 10(1), 1198.
[http://dx.doi.org/10.1038/s41467-019-09037-9] [PMID: 30867416]
[56]
McCarville, J.L.; Dong, J.; Caminero, A.; Bermudez-Brito, M. jury, J., murray, J.A., Duboux, S., Steinmann, M., Delley, M., Tangyu, M., Langella, P., Mercenier, A., Bergonzelli, G., Verdu, E.F. A commensal Bifidobacterium longum strain improves gluten-related immunopathology in mice through expression of a serine protease inhibitor. Appl. Environ. Microbiol., 2017, 83, e01323-e17.
[http://dx.doi.org/10.1128/AEM.01323-17] [PMID: 28778891]
[57]
Shapiro, H.; Lutaty, A.; Ariel, A. Macrophages, meta-inflammation, and immuno-metabolism. Sci. World J., 2011, 11, 2509-2529.
[http://dx.doi.org/10.1100/2011/397971] [PMID: 22235182]
[58]
West-Eberhard, M.J. Nutrition, the visceral immune system, and the evolutionary origins of pathogenic obesity. Proc. Natl. Acad. Sci. USA, 2019, 116(3), 723-731.
[http://dx.doi.org/10.1073/pnas.1809046116] [PMID: 30598443]
[59]
Fernandes, R.; Viana, S.D.; Nunes, S.; Reis, F. Diabetic gut microbiota dysbiosis as an inflammaging and immunosenescence condition that fosters progression of retinopathy and nephropathy. Biochim. Biophys. Acta Mol. Basis Dis., 2019, 1865(7), 1876-1897.
[http://dx.doi.org/10.1016/j.bbadis.2018.09.032] [PMID: 30287404]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy