Diet Rich in Animal Protein Promotes Pro-inflammatory Macrophage Response and Exacerbates Colitis in Mice

. 2019 ; 10 () : 919. [epub] 20190426

Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31105710

Diet is a major factor determining gut microbiota composition and perturbances in this complex ecosystem are associated with the inflammatory bowel disease (IBD). Here, we used gnotobiotic approach to analyze, how interaction between diet rich in proteins and gut microbiota influences the sensitivity to intestinal inflammation in murine model of ulcerative colitis. We found that diet rich in animal protein (aHPD) exacerbates acute dextran sulfate sodium (DSS)-induced colitis while diet rich in plant protein (pHPD) does not. The deleterious effect of aHPD was also apparent in chronic DSS colitis and was associated with distinct changes in gut bacteria and fungi. Therefore, we induced acute DSS-colitis in germ-free mice and transferred gut microbiota from aCD or aHPD fed mice to find that this effect requires presence of microbes and aHPD at the same time. The aHPD did not change the number of regulatory T cells or Th17 cells and still worsened the colitis in immuno-deficient RAG2 knock-out mice suggesting that this effect was not dependent on adaptive immunity. The pro-inflammatory effect of aHPD was, however, abrogated when splenic macrophages were depleted with clodronate liposomes. This treatment prevented aHPD induced increase in colonic Ly-6Chigh pro-inflammatory monocytes, but the ratio of resident Ly-6C-/low macrophages was not changed. These data show that the interactions between dietary protein of animal origin and gut microbiota increase sensitivity to intestinal inflammation by promoting pro-inflammatory response of monocytes.

Zobrazit více v PubMed

Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, et al. . Host-gut microbiota metabolic interactions. Science. (2012) 336:1262–7. 10.1126/science.1223813 PubMed DOI

Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, et al. . Linking long-term dietary patterns with gut microbial enterotypes. Science. (2011) 334:105–8. 10.1126/science.1208344 PubMed DOI PMC

Muegge BD, Kuczynski J, Knights D, Clemente JC, Gonzalez A, Fontana L, et al. . Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science. (2011) 332:970–4. 10.1126/science.1198719 PubMed DOI PMC

David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. . Diet rapidly and reproducibly alters the human gut microbiome. Nature. (2014) 505:559–63. 10.1038/nature12820 PubMed DOI PMC

Thaiss CA, Zeevi D, Levy M, Zilberman-Schapira G, Suez J, Tengeler AC, et al. . Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell. (2014) 159:514–29. 10.1016/j.cell.2014.09.048 PubMed DOI

Kostic AD, Xavier RJ, Gevers D. The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology. (2014) 146:1489–99. 10.1053/j.gastro.2014.02.009 PubMed DOI PMC

Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. (2006) 444:1027–31. 10.1038/nature05414 PubMed DOI

Chassaing B, Aitken JD, Gewirtz AT, Vijay-Kumar M. Gut microbiota drives metabolic disease in immunologically altered mice. Adv Immunol. (2012) 116:93–112. 10.1016/B978-0-12-394300-2.00003-X PubMed DOI

Tang WH, Hazen SL. The contributory role of gut microbiota in cardiovascular disease. J Clin Invest. (2014) 124:4204–11. 10.1172/JCI72331 PubMed DOI PMC

Wang Y, Kasper LH. The role of microbiome in central nervous system disorders. Brain Behav Immun. (2014) 38:1–12. 10.1016/j.bbi.2013.12.015 PubMed DOI PMC

Schwabe RF, Jobin C. The microbiome and cancer. Nat Rev Cancer. (2013) 13:800–12. 10.1038/nrc3610 PubMed DOI PMC

Blachier F, Beaumont M, Andriamihaja M, Davila AM, Lan A, Grauso M, et al. . Changes in the luminal environment of the colonic epithelial cells and physiopathological consequences. Am J Pathol. (2017) 187:476–86. 10.1016/j.ajpath.2016.11.015 PubMed DOI

Moschen AR, Wieser V, Tilg H. Dietary factors: major regulators of the gut's microbiota. Gut Liver. (2012) 6:411–6. 10.5009/gnl.2012.6.4.411 PubMed DOI PMC

El-Zaatari M, Kao JY. Role of dietary metabolites in regulating the host immune response in gastrointestinal disease. Front Immunol. (2017) 8:51. 10.3389/fimmu.2017.00051 PubMed DOI PMC

Persson PG, Ahlbom A, Hellers G. Diet and inflammatory bowel disease: a case-control study. Epidemiology. (1992) 3:47–52. 10.1097/00001648-199201000-00009 PubMed DOI

Maconi G, Ardizzone S, Cucino C, Bezzio C, Russo AG, Bianchi Porro G. Pre-illness changes in dietary habits and diet as a risk factor for inflammatory bowel disease: a case-control study. World J Gastroenterol. (2010) 16:4297–304. 10.3748/wjg.v16.i34.4297 PubMed DOI PMC

Spooren CE, Pierik MJ, Zeegers MP, Feskens EJ, Masclee AA, Jonkers DM. Review article: the association of diet with onset and relapse in patients with inflammatory bowel disease. Aliment Pharmacol Ther. (2013) 38:1172–87. 10.1111/apt.12501 PubMed DOI

Opstelten JL, de Vries JHM, Wools A, Siersema PD, Oldenburg B, Witteman BJM. Dietary intake of patients with inflammatory bowel disease: a comparison with individuals from a general population and associations with relapse. Clin Nutr. (2018). 10.1016/j.clnu.2018.06.983. [Epub ahead of print] PubMed DOI

Giovannucci E, Stampfer MJ, Colditz G, Rimm EB, Willett WC. Relationship of diet to risk of colorectal adenoma in men. J Natl Cancer Inst. (1992) 84:91–8. 10.1093/jnci/84.2.91 PubMed DOI

Shoda R, Matsueda K, Yamato S, Umeda N. Epidemiologic analysis of Crohn disease in Japan: increased dietary intake of n-6 polyunsaturated fatty acids and animal protein relates to the increased incidence of Crohn disease in Japan. Am J Clin Nutr. (1996) 63:741–5. 10.1093/ajcn/63.5.741 PubMed DOI

Gilbert JA, Bendsen NT, Tremblay A, Astrup A. Effect of proteins from different sources on body composition. Nutr Metab Cardiovasc Dis. (2011) 21 (Suppl 2):B16–31. 10.1016/j.numecd.2010.12.008 PubMed DOI

Windey K, De Preter V, Verbeke K. Relevance of protein fermentation to gut health. Mol Nutr Food Res. (2012) 56:184–96. 10.1002/mnfr.201100542 PubMed DOI

Andriamihaja M, Davila AM, Eklou-Lawson M, Petit N, Delpal S, Allek F, et al. . Colon luminal content and epithelial cell morphology are markedly modified in rats fed with a high-protein diet. Am J Physiol Gastrointest Liver Physiol. (2010) 299:G1030–1037. 10.1152/ajpgi.00149.2010 PubMed DOI

Liu X, Blouin JM, Santacruz A, Lan A, Andriamihaja M, Wilkanowicz S, et al. High-protein diet modifies colonic microbiota and luminal environment but not colonocyte metabolism in the rat model: the increased luminal bulk connection. Am J Physiol Gastrointest Liver Physiol. (2014) 307:G459–470. 10.1152/ajpgi.00400.2013 PubMed DOI

Lan A, Andriamihaja M, Blouin JM, Liu X, Descatoire V, Desclee de Maredsous C, et al. . High-protein diet differently modifies intestinal goblet cell characteristics and mucosal cytokine expression in ileum and colon. J Nutr Biochem. (2015) 26:91–8. 10.1016/j.jnutbio.2014.09.007 PubMed DOI

Lan A, Blais A, Coelho D, Capron J, Maarouf M, Benamouzig R, et al. . Dual effects of a high-protein diet on DSS-treated mice during colitis resolution phase. Am J Physiol Gastrointest Liver Physiol. (2016) 311:G624–G633. 10.1152/ajpgi.00433.2015 PubMed DOI

Llewellyn SR, Britton GJ, Contijoch EJ, Vennaro OH, Mortha A, Colombel JF, et al. . Interactions between diet and the intestinal microbiota alter intestinal permeability and colitis severity in mice. Gastroenterology. (2018) 154:1037–46.e1032. 10.1053/j.gastro.2017.11.030 PubMed DOI PMC

Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. . Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. (2013) 504:451–5. 10.1038/nature12726 PubMed DOI PMC

Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, et al. . The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. (2013) 341:569–73. 10.1126/science.1241165 PubMed DOI PMC

Atarashi K, Tanoue T, Ando M, Kamada N, Nagano Y, Narushima S, et al. . Th17 Cell induction by adhesion of microbes to intestinal epithelial cells. Cell. (2015) 163:367–80. 10.1016/j.cell.2015.08.058 PubMed DOI PMC

Kim M, Galan C, Hill AA, Wu WJ, Fehlner-Peach H, Song HW, et al. . Critical role for the microbiota in CX3CR1(+) intestinal mononuclear phagocyte regulation of intestinal T cell responses. Immunity. (2018) 49:151–163.e155. 10.1016/j.immuni.2018.05.009 PubMed DOI PMC

Platt AM, Bain CC, Bordon Y, Sester DP, Mowat AM. An independent subset of TLR expressing CCR2-dependent macrophages promotes colonic inflammation. J Immunol. (2010) 184:6843–54. 10.4049/jimmunol.0903987 PubMed DOI

Bain CC, Schridde A. Origin, differentiation, and function of intestinal macrophages. Front Immunol. (2018) 9:2733. 10.3389/fimmu.2018.02733 PubMed DOI PMC

Jones GR, Bain CC, Fenton TM, Kelly A, Brown SL, Ivens AC, et al. . Dynamics of colon monocyte and macrophage activation during colitis. Front Immunol. (2018) 9:2764. 10.3389/fimmu.2018.02764 PubMed DOI PMC

Zakostelska Z, Kverka M, Klimesova K, Rossmann P, Mrazek J, Kopecny J, et al. . Lysate of probiotic Lactobacillus casei DN-114 001 ameliorates colitis by strengthening the gut barrier function and changing the gut microenvironment. PLoS ONE. (2011) 6:e27961. 10.1371/journal.pone.0027961 PubMed DOI PMC

Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology. (1990) 98:694–702. 10.1016/0016-5085(90)90290-H PubMed DOI

Kverka M, Zakostelska Z, Klimesova K, Sokol D, Hudcovic T, Hrncir T, et al. . Oral administration of Parabacteroides distasonis antigens attenuates experimental murine colitis through modulation of immunity and microbiota composition. Clin Exp Immunol. (2011) 163:250–9. 10.1111/j.1365-2249.2010.04286.x PubMed DOI PMC

Van Rooijen N. The liposome-mediated macrophage 'suicide' technique. J Immunol Methods. (1989) 124:1–6. 10.1016/0022-1759(89)90178-6 PubMed DOI

Couter CJ, Surana NK. Isolation and flow cytometric characterization of murine small intestinal lymphocytes. J Vis Exp. (2016) 111:e54114 10.3791/54114 PubMed DOI PMC

Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, et al. . Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. (2013) 41:e1. 10.1093/nar/gks808 PubMed DOI PMC

Findley K, Oh J, Yang J, Conlan S, Deming C, Meyer JA, et al. . Topographic diversity of fungal and bacterial communities in human skin. Nature. (2013) 498:367–70. 10.1038/nature12171 PubMed DOI PMC

Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. . QIIME allows analysis of high-throughput community sequencing data. Nat Methods. (2010) 7:335–6. 10.1038/nmeth.f.303 PubMed DOI PMC

Bajer L, Kverka M, Kostovcik M, Macinga P, Dvorak J, Stehlikova Z, et al. . Distinct gut microbiota profiles in patients with primary sclerosing cholangitis and ulcerative colitis. World J Gastroenterol. (2017) 23:4548–58. 10.3748/wjg.v23.i25.4548 PubMed DOI PMC

Bengtsson-Palme J, Ryberg M, Hartmann M, Branco S, Wang Z, Godhe A, et al. Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol. Evol. (2013) 4:914–9. 10.1111/2041-210X.12073 DOI

Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. (2007) 73:5261–7. 10.1128/AEM.00062-07 PubMed DOI PMC

DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. . Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. (2006) 72:5069–72. 10.1128/AEM.03006-05 PubMed DOI PMC

Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. . Metagenomic biomarker discovery and explanation. Genome Biol. (2011) 12:R60. 10.1186/gb-2011-12-6-r60 PubMed DOI PMC

Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. . Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. (2013) 31:814–21. 10.1038/nbt.2676 PubMed DOI PMC

Tlaskalova-Hogenova H, Stepankova R, Kozakova H, Hudcovic T, Vannucci L, Tuckova L, et al. . The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell Mol Immunol. (2011) 8:110–20. 10.1038/cmi.2010.67 PubMed DOI PMC

Beaumont M, Portune KJ, Steuer N, Lan A, Cerrudo V, Audebert M, et al. . Quantity and source of dietary protein influence metabolite production by gut microbiota and rectal mucosa gene expression: a randomized, parallel, double-blind trial in overweight humans. Am J Clin Nutr. (2017) 106:1005–19. 10.3945/ajcn.117.158816 PubMed DOI

Luceri C, Guglielmi F, Lodovici M, Giannini L, Messerini L, Dolara P. Plant phenolic 4-coumaric acid protects against intestinal inflammation in rats. Scand J Gastroenterol. (2004) 39:1128–33. 10.1080/00365520410007908 PubMed DOI

Sanchez-Fidalgo S, Cardeno A, Villegas I, Talero E, de la Lastra CA. Dietary supplementation of resveratrol attenuates chronic colonic inflammation in mice. Eur J Pharmacol. (2010) 633:78–84. 10.1016/j.ejphar.2010.01.025 PubMed DOI

Liu B, Lin Q, Yang T, Zeng L, Shi L, Chen Y, et al. . Oat beta-glucan ameliorates dextran sulfate sodium (DSS)-induced ulcerative colitis in mice. Food Funct. (2015) 6:3454–63. 10.1039/C5FO00563A PubMed DOI

Seril DN, Liao J, Ho KL, Warsi A, Yang CS, Yang GY. Dietary iron supplementation enhances DSS-induced colitis and associated colorectal carcinoma development in mice. Dig Dis Sci. (2002) 47:1266–78. 10.1023/A:1015362228659 PubMed DOI

Constante M, Fragoso G, Calve A, Samba-Mondonga M, Santos MM. Dietary heme induces gut dysbiosis, aggravates colitis, and potentiates the development of adenomas in mice. Front Microbiol. (2017) 8:1809. 10.3389/fmicb.2017.01809 PubMed DOI PMC

Miles JP, Zou J, Kumar MV, Pellizzon M, Ulman E, Ricci M, et al. . Supplementation of low- and high-fat diets with fermentable fiber exacerbates severity of DSS-induced acute colitis. Inflamm Bowel Dis. (2017) 23:1133–43. 10.1097/MIB.0000000000001155 PubMed DOI PMC

Tak KH, Ahn E, Kim E. Increase in dietary protein content exacerbates colonic inflammation and tumorigenesis in azoxymethane-induced mouse colon carcinogenesis. Nutr Res Pract. (2017) 11:281–9. 10.4162/nrp.2017.11.4.281 PubMed DOI PMC

Kitajima S, Takuma S, Morimoto M. Changes in colonic mucosal permeability in mouse colitis induced with dextran sulfate sodium. Exp Anim. (1999) 48:137–43. 10.1538/expanim.48.137 PubMed DOI

Roche-Lima A, Carrasquillo-Carrion K, Gomez-Moreno R, Cruz JM, Velazquez-Morales DM, Rogozin IB, et al. . The presence of genotoxic and/or pro-inflammatory bacterial genes in gut metagenomic databases and their possible link with inflammatory bowel diseases. Front Genet. (2018) 9:116. 10.3389/fgene.2018.00116 PubMed DOI PMC

Klimesova K, Jiraskova Zakostelska Z, Tlaskalova-Hogenova H. Oral bacterial and fungal microbiome impacts colorectal carcinogenesis. Front Microbiol. (2018) 9:774. 10.3389/fmicb.2018.00774 PubMed DOI PMC

Sokol H, Leducq V, Aschard H, Pham HP, Jegou S, Landman C, et al. . Fungal microbiota dysbiosis in IBD. Gut. (2017) 66:1039–48. 10.1136/gutjnl-2015-310746 PubMed DOI PMC

Palmela C, Chevarin C, Xu Z, Torres J, Sevrin G, Hirten R, et al. . Adherent-invasive Escherichia coli in inflammatory bowel disease. Gut. (2018) 67:574–87. 10.1136/gutjnl-2017-314903 PubMed DOI

Sovran B, Planchais J, Jegou S, Straube M, Lamas B, Natividad JM, et al. . Enterobacteriaceae are essential for the modulation of colitis severity by fungi. Microbiome. (2018) 6:152. 10.1186/s40168-018-0538-9 PubMed DOI PMC

Jubelin G, Desvaux M, Schuller S, Etienne-Mesmin L, Muniesa M, Blanquet-Diot S. Modulation of enterohaemorrhagic Escherichia coli survival and virulence in the human gastrointestinal tract. Microorganisms. (2018) 6:E115. 10.3390/microorganisms6040115 PubMed DOI PMC

Green E, Mecsas J. Bacterial secretion systems: an overview. In: Kudva I, Cornick N, Plummer P, Zhang Q, Nicholson T, Bannantine J, Bellaire B, editors. Virulence Mechanisms of Bacterial Pathogens. Washington, DC: ASM Press; (2016). p. 215–39. 10.1128/microbiolspec.VMBF-0012-2015 DOI

Macfarlane GT, Gibson GR, Beatty E, Cummings JH. Estimation of short-chain fatty acid production from protein by human intestinal bacteria based on branched-chain fatty acid measurements. FEMS Microbiol. Lett. (1992) 101:81–8. 10.1111/j.1574-6968.1992.tb05764.x DOI

Vieira EL, Leonel AJ, Sad AP, Beltrao NR, Costa TF, Ferreira TM, et al. . Oral administration of sodium butyrate attenuates inflammation and mucosal lesion in experimental acute ulcerative colitis. J Nutr Biochem. (2012) 23:430–6. 10.1016/j.jnutbio.2011.01.007 PubMed DOI

Owen JL, Cheng SX, Ge Y, Sahay B, Mohamadzadeh M. The role of the calcium-sensing receptor in gastrointestinal inflammation. Semin Cell Dev Biol. (2016) 49:44–51. 10.1016/j.semcdb.2015.10.040 PubMed DOI PMC

Gong ZY, Yuan ZQ, Dong ZW, Peng YZ. Glutamine with probiotics attenuates intestinal inflammation and oxidative stress in a rat burn injury model through altered iNOS gene aberrant methylation. Am J Transl Res. (2017) 9:2535–47. PubMed PMC

Gaifem J, Goncalves LG, Dinis-Oliveira RJ, Cunha C, Carvalho A, Torrado E, et al. . L-threonine supplementation during colitis onset delays disease recovery. Front Physiol. (2018) 9:1247. 10.3389/fphys.2018.01247 PubMed DOI PMC

Hudcovic T, Stepankova R, Cebra J, Tlaskalova-Hogenova H. The role of microflora in the development of intestinal inflammation: acute and chronic colitis induced by dextran sulfate in germ-free and conventionally reared immunocompetent and immunodeficient mice. Folia Microbiol. (2001) 46:565–72. 10.1007/BF02818004 PubMed DOI

Dieleman LA, Ridwan BU, Tennyson GS, Beagley KW, Bucy RP, Elson CO. Dextran sulfate sodium-induced colitis occurs in severe combined immunodeficient mice. Gastroenterology. (1994) 107:1643–52. 10.1016/0016-5085(94)90803-6 PubMed DOI

Spangler JB, Tomala J, Luca VC, Jude KM, Dong S, Ring AM, et al. . Antibodies to Interleukin-2 elicit selective T cell subset potentiation through distinct conformational mechanisms. Immunity. (2015) 42:815–25. 10.1016/j.immuni.2015.04.015 PubMed DOI PMC

Seo DH, Che X, Kwak MS, Kim S, Kim JH, Ma HW, et al. . Interleukin-33 regulates intestinal inflammation by modulating macrophages in inflammatory bowel disease. Sci Rep. (2017) 7:851. 10.1038/s41598-017-00840-2 PubMed DOI PMC

Qualls JE, Kaplan AM, van Rooijen N, Cohen DA. Suppression of experimental colitis by intestinal mononuclear phagocytes. J Leukoc Biol. (2006) 80:802–15. 10.1189/jlb.1205734 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...