Pectin supplementation ameliorates intestinal epithelial barrier function damage by modulating intestinal microbiota in lipopolysaccharide-challenged piglets.
Wen, Xiaobin; Zhong, Ruqing; Dang, Guoqiet al.
2022 • In Journal of Nutritional Biochemistry, 109, p. 109107
Pectin supplementation ameliorates intestinal epithelial barrier function damage by modulating intestinal microbiota in lipopolysaccharide-challenged piglets..pdf
[en] During weaning, infants and young animals are susceptible to severe enteric infections, thus inducing intestinal microbiota dysbiosis, intestinal inflammation, and impaired intestinal barrier function. Pectin (PEC), a prebiotic polysaccharide, enhances intestinal health with the potential for a therapeutic effect on intestinal diseases. One 21-d study was conducted to investigate the protective effect of pectin against intestinal injury induced by intraperitoneal injection of Escherichia coli lipopolysaccharide (LPS) in a piglet model. A total of 24 piglets (6.77±0.92 kg BW; Duroc × Landrace × Large White; barrows; 21 d of age) were randomly assigned into three groups: control group, LPS-challenged group, and PEC + LPS group. Piglets were administrated with LPS or saline on d14 and d21 of the experiment. All piglets were slaughtered and intestinal samples were collected after 3 h administration on d21. Pectin supplementation ameliorated the LPS-induced inflammation response and damage to the ileal morphology. Meanwhile, pectin also improved intestinal mucin barrier function, increased the mRNA expression of MUC2, and improved intestinal mucus glycosylation. LPS challenge reduced the diversity of intestinal microbiota and enriched the relative abundance of Helicobacter. Pectin restored alpha diversity and improved the structure of the gut microbiota by enriching anti-inflammatory bacteria and short-chain fatty acids (SCFAs)-producing bacteria, and increased the concentrations of acetate. In addition, Spearman rank correlation analysis also revealed the potential relationship between intestinal microbiota and intestinal morphology, intestinal inflammation, and intestinal glycosylation in piglets. Taken together, these results indicate that pectin enhances intestinal integrity and barrier function by altering intestinal microbiota composition and their metabolites, which subsequently alleviates intestinal injury and finally improves the growth performance of piglets.
Disciplines :
Animal production & animal husbandry
Author, co-author :
Wen, Xiaobin ✱; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Zhong, Ruqing; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Dang, Guoqi ✱; Université de Liège - ULiège > TERRA Research Centre
Xia, Bing; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Wu, Weida; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Tang, Shanlong; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Tang, Lixin; State Key Laboratory for Molecular Biology of Special Economic Animals, Institute of Special Animal and Plant Sciences, Chinese Academy of Agricultural Sciences, Changchun, China
Liu, Lei; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Liu, Zhengqun; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
Chen, Liang; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China. Electronic address: chenliang01@caas.cn
Zhang, Hongfu; State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, China
✱ These authors have contributed equally to this work.
Language :
English
Title :
Pectin supplementation ameliorates intestinal epithelial barrier function damage by modulating intestinal microbiota in lipopolysaccharide-challenged piglets.
This work was supported by the National Natural Science Foundation of China [grant numbers 31672428 ], Guizhou Science and Technology Support Program [grant numbers 2021-147 ], and Agricultural Science and Technology Innovation Program [grant numbers CAAS-ZDRW202006-02 , ASTIP-IAS07 ].
Chen, H, Hu, H, Chen, D, Tang, J, Yu, B, Luo, J, et al. Dietary pectic oligosaccharide administration improves growth performance and immunity in weaned pigs infected by rotavirus. J Agric Food Chem 65 (2017), 2923–2929, 10.1021/acs.jafc.7b00039.
Gresse, R, Chaucheyras-Durand, F, Fleury, MA, Van de Wiele, T, Forano, E, Blanquet-Diot, S., Gut microbiota dysbiosis in postweaning piglets: understanding the keys to health. Trends Microbiol 25 (2017), 851–873, 10.1016/j.tim.2017.05.004.
Campbell, JM, Crenshaw, JD, Polo, J., The biological stress of early weaned piglets. J Anim Sci Biotechnol, 4, 2013, 19, 10.1186/2049-1891-4-19.
Xie, W, Song, L, Wang, X, Xu, Y, Liu, Z, Zhao, D, et al. A bovine lactoferricin-lactoferrampin-encoding lactobacillus reuteri CO21 regulates the intestinal mucosal immunity and enhances the protection of piglets against enterotoxigenic escherichia coli K88 challenge. Gut Microbes, 13, 2021, 1956281, 10.1080/19490976.2021.1956281.
Shanahan, ER, Shah, A, Koloski, N, Walker, MM, Talley, NJ, Morrison, M, et al. Influence of cigarette smoking on the human duodenal mucosa-associated microbiota. Microbiome, 6, 2018, 150, 10.1186/s40168-018-0531-3.
Pickard, JM, Zeng, MY, Caruso, R, Núñez, G., Gut microbiota: role in pathogen colonization, immune responses, and inflammatory disease. Immunol Rev 279 (2017), 70–89, 10.1111/imr.12567.
Morelli, L., Postnatal development of intestinal microflora as influenced by infant nutrition. J Nutr, 138, 2008, 10.1093/jn/138.9.1791S 1791S-1795Sw.
Thursby, E, Juge, N., Introduction to the human gut microbiota. Biochem J 474 (2017), 1823–1836, 10.1042/bcj20160510.
David, LA, Maurice, CF, Carmody, RN, Gootenberg, DB, Button, JE, Wolfe, BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505 (2014), 559–563, 10.1038/nature12820.
Sun, X, Cui, Y, Su, Y, Gao, Z, Diao, X, Li, J, et al. Dietary fiber ameliorates lipopolysaccharide-induced intestinal barrier function damage in piglets by modulation of intestinal microbiome. mSystems, 6, 2021, 10.1128/mSystems.01374-20.
Larabi, A, Barnich, N, Nguyen, HTT., New insights into the interplay between autophagy, gut microbiota and inflammatory responses in IBD. Autophagy 16 (2020), 38–51, 10.1080/15548627.2019.1635384.
Hu, R, He, Z, Liu, M, Tan, J, Zhang, H, Hou, DX, et al. Dietary protocatechuic acid ameliorates inflammation and up-regulates intestinal tight junction proteins by modulating gut microbiota in LPS-challenged piglets. J Anim Sci Biotechnol, 11, 2020, 92, 10.1186/s40104-020-00492-9.
Sun, X, Cui, Y, Su, Y, Gao, Z, Diao, X, Li, J, et al. Dietary Fiber ameliorates lipopolysaccharide-induced intestinal barrier function damage in piglets by modulation of intestinal microbiome. mSystems, 6, 2021, e01374, 10.1128/mSystems.01374-20 20.
Wang, X, Wang, W, Wang, L, Yu, C, Zhang, G, Zhu, H, et al. Lentinan modulates intestinal microbiota and enhances barrier integrity in a piglet model challenged with lipopolysaccharide. Food Funct 10 (2019), 479–489, 10.1039/c8fo02438c.
Protzko, RJ, Latimer, LN, Martinho, Z, de Reus, E, Seibert, T, Benz, JP, et al. Engineering saccharomyces cerevisiae for co-utilization of D-galacturonic acid and D-glucose from citrus peel waste. Nat Commun, 9, 2018, 5059, 10.1038/s41467-018-07589-w.
Singh, V, Yeoh, BS, Walker, RE, Xiao, X, Saha, P, Golonka, RM, et al. Microbiota fermentation-NLRP3 axis shapes the impact of dietary fibres on intestinal inflammation. Gut 68 (2019), 1801–1812, 10.1136/gutjnl-2018-316250.
Ishisono, K, Mano, T, Yabe, T, Kitaguchi, K., Dietary fiber pectin ameliorates experimental colitis in a neutral sugar side chain-dependent manner. Front Immunol, 10, 2019, 2979, 10.3389/fimmu.2019.02979.
Jiang, T, Gao, X, Wu, C, Tian, F, Lei, Q, Bi, J, et al. Apple-derived pectin modulates gut microbiota, improves gut barrier function, and attenuates metabolic endotoxemia in rats with diet-induced obesity. Nutrients, 8, 2016, 126, 10.3390/nu8030126.
Hino, S, Sonoyama, K, Bito, H, Kawagishi, H, Aoe, S, Morita, T., Low-methoxyl pectin stimulates small intestinal mucin secretion irrespective of goblet cell proliferation and is characterized by Jejunum Muc2 upregulation in rats. J Nutr 143 (2013), 34–40, 10.3945/jn.112.167064.
Chen, C-H, Sheu, M-T, Chen, T-F, Wang, Y-C, Hou, W-C, Liu, D-Z, et al. Suppression of endotoxin-induced proinflammatory responses by citrus pectin through blocking LPS signaling pathways. Biochem Pharmacol 72 (2006), 1001–1009, 10.1016/j.bcp.2006.07.001.
Wu, W, Zhang, L, Xia, B, Tang, S, Xie, J, Zhang, H., Modulation of pectin on mucosal innate immune function in pigs mediated by gut microbiota. Microorganisms, 8, 2020, 535, 10.3390/microorganisms8040535.
Xu, B, Yan, Y, Yin, B, Zhang, L, Qin, W, Niu, Y, et al. Dietary glycyl-glutamine supplementation ameliorates intestinal integrity, inflammatory response, and oxidative status in association with the gut microbiota in LPS-challenged piglets. Food Funct 12 (2021), 3539–3551, 10.1039/d0fo03080e.
Fang, W, Zhang, L, Meng, Q, Wu, W, Lee, YK, Xie, J, et al. Effects of dietary pectin on the profile and transport of intestinal bile acids in young pigs. J Anim Sci 96 (2018), 4743–4754, 10.1093/jas/sky327.
Liu, Y, Chen, F, Odle, J, Lin, X, Jacobi, SK, Zhu, H, et al. Fish oil enhances intestinal integrity and inhibits TLR4 and NOD2 signaling pathways in weaned pigs after LPS challenge. J Nutr 142 (2012), 2017–2024, 10.3945/jn.112.164947.
Xu, X, Hua, H, Wang, L, He, P, Zhang, L, Qin, Q, et al. Holly polyphenols alleviate intestinal inflammation and alter microbiota composition in lipopolysaccharide-challenged pigs. Br J Nutr 123 (2020), 881–891, 10.1017/S0007114520000082.
Engevik, MA, Yacyshyn, MB, Engevik, KA, Wang, J, Darien, B, Hassett, DJ, et al. Human Clostridium difficile infection: altered mucus production and composition. Am J Physiol Gastrointest Liver Physiol 308 (2015), G510–G524, 10.1152/ajpgi.00091.2014.
Schmittgen, TD., Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3 (2008), 1101–1108, 10.3748/wjg.v13.i20.2826.
Wu, W, Xie, J, Zhang, H., Dietary fibers influence the intestinal SCFAs and plasma metabolites profiling in growing pigs. Food Funct 7 (2016), 4644–4654.
Johansson, MEV, Ambort, D, Pelaseyed, T, Schütte, A, Gustafsson, JK, Ermund, A, et al. Composition and functional role of the mucus layers in the intestine. Cell Mol Life Sci 68 (2011), 3635–3641, 10.1007/s00018-011-0822-3.
Johansson, MEV, Larsson, JMH, Hansson, GC., The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc Natl Acad Sci U S A 108:Suppl 1 (2011), 4659–4665, 10.1073/pnas.1006451107.
Besten, G, Eunen, K, Groen, AK, Venema, K, Reijngoud, D-J, Bakker, BM., The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res 54 (2013), 2325–2340, 10.1194/jlr.R036012.
Cui, Z, Tan, B, Liao, S, Qi, M, Wang, X, Zha, A, et al. Dietary addition of antioxidant complex packs and functional amino acids can improve the digestion, absorption, and immunity of huanjiang minipigs. Biomed Res Int, 2020, 2020, 1475831, 10.1155/2020/1475831.
Sun, Z, Li, H, Li, Y, Qiao, J., Lactobacillus salivarius, a potential probiotic to improve the health of lps-challenged piglet intestine by alleviating inflammation as well as oxidative stress in a dose-dependent manner during weaning transition. Front Vet Sci, 7, 2020, 547425, 10.3389/fvets.2020.547425.
Tang, W, Chen, D, Yu, B, He, J, Huang, Z, Zheng, P, et al. Capsulized faecal microbiota transplantation ameliorates post-weaning diarrhoea by modulating the gut microbiota in piglets. Vet Res, 51, 2020, 55, 10.1186/s13567-020-00779-9.
Tao, X, Liu, S, Men, X, Xu, Z., Over-expression of miR-146b and its regulatory role in intestinal epithelial cell viability, proliferation, and apoptosis in piglets. Biol Direct, 12, 2017, 27, 10.1186/s13062-017-0199-9.
Liu, Y, Huang, J, Hou, Y, Zhu, H, Zhao, S, Ding, B, et al. Dietary arginine supplementation alleviates intestinal mucosal disruption induced by Escherichia coli lipopolysaccharide in weaned pigs. Br J Nutr 100 (2008), 552–560, 10.1017/S0007114508911612.
Liu, Y, Xu, Q, Wang, Y, Liang, T, Li, X, Wang, D, et al. Necroptosis is active and contributes to intestinal injury in a piglet model with lipopolysaccharide challenge. Cell Death Dis, 12, 2021, 62, 10.1038/s41419-020-03365-1.
Zhu, H, Liu, Y, Chen, S, Wang, X, Pi, D, Leng, W, et al. Fish oil enhances intestinal barrier function and inhibits corticotropin-releasing hormone/corticotropin-releasing hormone receptor 1 signalling pathway in weaned pigs after lipopolysaccharide challenge. Br J Nutr 115 (2016), 1947–1957, 10.1017/S0007114516001100.
Liu, YL, Li, DF, Gong, LM, Yi, GF, Gaines, AM, Carroll, JA., Effects of fish oil supplementation on the performance and the immunological, adrenal, and somatotropic responses of weaned pigs after an Escherichia coli lipopolysaccharide challenge. J Anim Sci 81 (2003), 2758–2765, 10.2527/2003.81112758x.
Luo, J, Cheng, L, Du, Y, Mao, X, He, J, Yu, B, et al. The anti-inflammatory effects of low- and high-molecular-weight beta-glucans from Agrobacterium sp. ZX09 in LPS-induced weaned piglets. Food Funct 11 (2020), 585–595, 10.1039/c9fo00627c.
Fischer, F, Romero, R, Hellhund, A, Linne, U, Bertrams, W, Pinkenburg, O, et al. Dietary cellulose induces anti-inflammatory immunity and transcriptional programs via maturation of the intestinal microbiota. Gut Microbes 12 (2020), 1–17, 10.1080/19490976.2020.1829962.
Kohn, JB., Is dietary fiber considered an essential nutrient?. J Acad Nutr Diet, 116, 2016, 360, 10.1016/j.jand.2015.12.004.
Zhang, L., Effects and the regulatory mechanism of dietary fiber on intestinal barrier function in piglets [PhD]. Chin Acad Agricult Sci, 2018, 1–129 doi:CNKI:CDMD:1.1018.160513.
Tian, L, Bruggeman, G, van den Berg, M, Borewicz, K, Scheurink, AJW, Bruininx, E, et al. Effects of pectin on fermentation characteristics, carbohydrate utilization, and microbial community composition in the gastrointestinal tract of weaning pigs. Mol Nutr Food Res, 61, 2017, 10.1002/mnfr.201600186.
Rodríguez-Sorrento, A, Castillejos, L, López-Colom, P, Cifuentes-Orjuela, G, Rodríguez-Palmero, M, Moreno-Muñoz, JA, et al. Effects of Subsp. CECT 7210 and HN001, combined or not with oligofructose-enriched inulin, on weaned pigs orally challenged with typhimurium. Front Microbiol, 11, 2020, 2012, 10.3389/fmicb.2020.02012.
Chen, Y, Xie, Y, Zhong, R, Liu, L, Lin, C, Xiao, L, et al. Effects of Xylo-Oligosaccharides on growth and gut microbiota as potential replacements for antibiotic in weaning piglets. Front Microbiol, 12, 2021, 641172, 10.3389/fmicb.2021.641172.
Zhang, Y, Wang, Y, Chen, D, Yu, B, Zheng, P, Mao, X, et al. Dietary chlorogenic acid supplementation affects gut morphology, antioxidant capacity and intestinal selected bacterial populations in weaned piglets. Food Funct 9 (2018), 4968–4978, 10.1039/c8fo01126e.
Fan, C, Han, J, Liu, X, Zhang, F, Long, Y, Xie, Q., Modulation of hypoxia-inducible factor-1/cyclo-oxygenase-2 pathway associated with attenuation of intestinal mucosa inflammatory damage by polysaccharides in lipopolysaccharide-challenged piglets. Br J Nutr 122 (2019), 666–675, 10.1017/S0007114519001363.
Buraczewska, L, Taciak, M, Ceregrzyn, M, Korczyński, W., The effect of pectin on amino acid digestibility and digesta viscosity, motility and morphology of the small intestine, and on N-balance and performance of young pigs. Livest Sci 109 (2007), 53–56, 10.1016/j.livsci.2007.01.058.
Lee, N, Luk, J., Hepatic tight junctions: from viral entry to cancer metastasis. World J Gastroenterol 16 (2010), 289–295, 10.3748/wjg.v16.i3.289.
Weight, CM, Jones, EJ, Horn, N, Wellner, N, Carding, SR., Elucidating pathways of Toxoplasma gondii invasion in the gastrointestinal tract: involvement of the tight junction protein occludin. Microbes Infect 17 (2015), 698–709, 10.1016/j.micinf.2015.07.001.
Ottman, N, Davids, M, Suarez-Diez, M, Boeren, S, Schaap, PJ, Martins Dos Santos, VAP, et al. Genome-scale model and omics analysis of metabolic capacities of reveal a preferential mucin-degrading lifestyle. Appl Environ Microbiol 83 (2017), e01014–e01017, 10.1128/AEM.01014-17.
White, B, Sterrett, JD, Grigoryan, Z, Lally, L, Heinze, JD, Alikhan, H, et al. Characterization of gut microbiome and metabolome in patients in an underprivileged community in the United States. World J Gastroenterol 27 (2021), 5575–5594, 10.3748/wjg.v27.i33.5575.
Allaire, JM, Morampudi, V, Crowley, SM, Stahl, M, Yu, H, Bhullar, K, et al. Frontline defenders: goblet cell mediators dictate host-microbe interactions in the intestinal tract during health and disease. Am J Physiol Gastrointest Liver Physiol 314 (2018), G360–GG77, 10.1152/ajpgi.00181.2017.
Wagner, CE, Wheeler, KM, Ribbeck, K., Mucins and their role in shaping the functions of mucus barriers. Annu Rev Cell Dev Biol 34 (2018), 189–215, 10.1146/annurev-cellbio-100617-062818.
Crouch, LI, Liberato, MV, Urbanowicz, PA, Baslé, A, Lamb, CA, Stewart, CJ, et al. Prominent members of the human gut microbiota express endo-acting O-glycanases to initiate mucin breakdown. Nat Commun, 11, 2020, 4017, 10.1038/s41467-020-17847-5.
Kudelka, MR, Stowell, SR, Cummings, RD, Neish, AS., Intestinal epithelial glycosylation in homeostasis and gut microbiota interactions in IBD. Nat Rev Gastroenterol Hepatol 17 (2020), 597–617, 10.1038/s41575-020-0331-7.
Reily, C, Stewart, TJ, Renfrow, MB, Novak, J., Glycosylation in health and disease. Nat Rev Nephrol 15 (2019), 346–366, 10.1038/s41581-019-0129-4.
Westreich, ST, Ardeshir, A, Alkan, Z, Kable, ME, Korf, I, Lemay, DG., Fecal metatranscriptomics of macaques with idiopathic chronic diarrhea reveals altered mucin degradation and fucose utilization. Microbiome, 7, 2019, 41, 10.1186/s40168-019-0664-z.
Qu, D, Wang, G, Yu, L, Tian, F, Chen, W, Zhai, Q., The effects of diet and gut microbiota on the regulation of intestinal mucin glycosylation. Carbohydr Polym, 258, 2021, 117651, 10.1016/j.carbpol.2021.117651.
Pickard, JM, Maurice, CF, Kinnebrew, MA, Abt, MC, Schenten, D, Golovkina, TV, et al. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature 514 (2014), 638–641, 10.1038/nature13823.
Goto, Y, Obata, T, Kunisawa, J, Sato, S, Ivanov, II, Lamichhane, A, et al. Innate lymphoid cells regulate intestinal epithelial cell glycosylation. Science, 345, 2014, 1254009, 10.1126/science.1254009.
Yang, WH, Park, SY, Nam, HW, Kim, DH, Kang, JG, Kang, ES, et al. NFkappaB activation is associated with its O-GlcNAcylation state under hyperglycemic conditions. Proc Natl Acad Sci U S A 105 (2008), 17345–17350, 10.1073/pnas.0806198105.
Zou, L, Yang, S, Champattanachai, V, Hu, S, Chaudry, IH, Marchase, RB, et al. Glucosamine improves cardiac function following trauma-hemorrhage by increased protein O-GlcNAcylation and attenuation of NF-{kappa}B signaling. Am J Physiol Heart Circ Physiol 296 (2009), H515–HH23, 10.1152/ajpheart.01025.2008.
Hart, GW, Copeland, RJ., Glycomics hits the big time. Cell 143 (2010), 672–676, 10.1016/j.cell.2010.11.008.
Wells, L, Vosseller, K, Hart, GW., Glycosylation of nucleocytoplasmic proteins: signal transduction and O-GlcNAc. Science 291 (2001), 2376–2378, 10.1126/science.1058714.
Bergstrom, K, Fu, J, Johansson, ME, Liu, X, Gao, N, Wu, Q, et al. Core 1- and 3-derived O-glycans collectively maintain the colonic mucus barrier and protect against spontaneous colitis in mice. Mucosal Immunol 10 (2017), 91–103, 10.1038/mi.2016.45.
An, G, Wei, B, Xia, B, McDaniel, JM, Ju, T, Cummings, RD, et al. Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. J Exp Med 204 (2007), 1417–1429, 10.1084/jem.20061929.
Ishisono, K, Yabe, T, Kitaguchi, K., Citrus pectin attenuates endotoxin shock via suppression of Toll-like receptor signaling in Peyer's patch myeloid cells. J Nutr Biochem 50 (2017), 38–45, 10.1016/j.jnutbio.2017.07.016.
Sabroe, I, Parker, LC, Dower, SK, Whyte, MKB., The role of TLR activation in inflammation. J Pathol 214 (2008), 126–135, 10.1002/path.2264.
Fukata, M, Vamadevan, AS, Abreu, MT., Toll-like receptors (TLRs) and Nod-like receptors (NLRs) in inflammatory disorders. Semin Immunol 21 (2009), 242–253, 10.1016/j.smim.2009.06.005.
Sun, Y, He, Y, Wang, F, Zhang, H, de Vos, P, Sun, J., Low-methoxyl lemon pectin attenuates inflammatory responses and improves intestinal barrier integrity in caerulein-induced experimental acute pancreatitis. Mol Nutr Food Res, 61, 2017, 1600885, 10.1002/mnfr.201600885.
Ashida, H, Ogawa, M, Kim, M, Mimuro, H, Sasakawa, C., Bacteria and host interactions in the gut epithelial barrier. Nat Chem Biol 8 (2011), 36–45, 10.1038/nchembio.741.
Riva, A, Kuzyk, O, Forsberg, E, Siuzdak, G, Pfann, C, Herbold, C, et al. A fiber-deprived diet disturbs the fine-scale spatial architecture of the murine colon microbiome. Nat Commun, 10, 2019, 4366, 10.1038/s41467-019-12413-0.
Zhang, C, Yu, M, Yang, Y, Mu, C, Su, Y, Zhu, W., Effect of early antibiotic administration on cecal bacterial communities and their metabolic profiles in pigs fed diets with different protein levels. Anaerobe 42 (2016), 188–196, 10.1016/j.anaerobe.2016.10.016.
Xu, P, Li, M, Zhang, J, Zhang, T., Correlation of intestinal microbiota with overweight and obesity in Kazakh school children. BMC Microbiol, 12, 2012, 283, 10.1186/1471-2180-12-283.
Binda, C, Lopetuso, LR, Rizzatti, G, Gibiino, G, Cennamo, V, Gasbarrini, A., Actinobacteria: a relevant minority for the maintenance of gut homeostasis. Dig Liver Dis 50 (2018), 421–428, 10.1016/j.dld.2018.02.012.
Hughes, ER, Winter, MG, Duerkop, BA, Spiga, L, Furtado de Carvalho, T, Zhu, W, et al. Microbial respiration and formate oxidation as metabolic signatures of inflammation-associated dysbiosis. Cell Host Microbe 21 (2017), 208–219, 10.1016/j.chom.2017.01.005.
Shin, N-R, Whon, TW, Bae, J-W., Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 33 (2015), 496–503, 10.1016/j.tibtech.2015.06.011.
Papamichael, K, Konstantopoulos, P, Mantzaris, GJ., Helicobacter pylori infection and inflammatory bowel disease: is there a link?. World J Gastroenterol 20 (2014), 6374–6385, 10.3748/wjg.v20.i21.6374.
Castaño-Rodríguez, N, Kaakoush, NO, Lee, WS, Mitchell, HM., Dual role of Helicobacter and Campylobacter species in IBD: a systematic review and meta-analysis. Gut 66 (2017), 235–249, 10.1136/gutjnl-2015-310545.
Kong, C, Gao, R, Yan, X, Huang, L, Qin, H., Probiotics improve gut microbiota dysbiosis in obese mice fed a high-fat or high-sucrose diet. Nutrition 60 (2019), 175–184, 10.1016/j.nut.2018.10.002.
Zhou, L, Fang, L, Sun, Y, Su, Y, Zhu, W., Effects of the dietary protein level on the microbial composition and metabolomic profile in the hindgut of the pig. Anaerobe 38 (2016), 61–69, 10.1016/j.anaerobe.2015.12.009.
Wu, GD, Chen, J, Hoffmann, C, Bittinger, K, Chen, Y-Y, Keilbaugh, SA, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334 (2011), 105–108, 10.1126/science.1208344.
Xu, J, Bjursell, MK, Himrod, J, Deng, S, Carmichael, LK, Chiang, HC, et al. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299 (2003), 2074–2076, 10.1126/science.1080029.
Steimle, A, Michaelis, L, Di Lorenzo, F, Kliem, T, Munzner, T, Maerz, JK, et al. Weak agonistic LPS restores intestinal immune homeostasis. Mol Ther 27 (2019), 1974–1991, 10.1016/j.ymthe.2019.07.007.
Kumari, R, Ahuja, V, Paul, J., Fluctuations in butyrate-producing bacteria in ulcerative colitis patients of North India. World J Gastroenterol 19 (2013), 3404–3414, 10.3748/wjg.v19.i22.3404.
Chung, WSF, Meijerink, M, Zeuner, B, Holck, J, Louis, P, Meyer, AS, et al. Prebiotic potential of pectin and pectic oligosaccharides to promote anti-inflammatory commensal bacteria in the human colon. FEMS Microbiol Ecol, 93, 2017, ix127, 10.1093/femsec/fix127.
O'Hara, CM, Brenner, FW, Miller, JM., Classification, identification, and clinical significance of Proteus, Providencia, and Morganella. Clin Microbiol Rev 13 (2000), 534–546, 10.1128/CMR.13.4.534.
Zhang, Z, Tang, H, Chen, P, Xie, H, Tao, Y., Demystifying the manipulation of host immunity, metabolism, and extraintestinal tumors by the gut microbiome. Signal Transduct Target Ther, 4, 2019, 41, 10.1038/s41392-019-0074-5.
Wu, J, Wang, K, Wang, X, Pang, Y, Jiang, C., The role of the gut microbiome and its metabolites in metabolic diseases. Protein Cell 12 (2021), 360–373, 10.1007/s13238-020-00814-7.
Kobayashi, M, Mikami, D, Kimura, H, Kamiyama, K, Morikawa, Y, Yokoi, S, et al. Short-chain fatty acids, GPR41 and GPR43 ligands, inhibit TNF-α-induced MCP-1 expression by modulating p38 and JNK signaling pathways in human renal cortical epithelial cells. Biochem Biophys Res Commun 486 (2017), 499–505, 10.1016/j.bbrc.2017.03.071.
Trompette, A, Gollwitzer, ES, Yadava, K, Sichelstiel, AK, Sprenger, N, Ngom-Bru, C, et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 20 (2014), 159–166, 10.1038/nm.3444.
Koh, A, De Vadder, F, Kovatcheva-Datchary, P, Bäckhed, F., From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 165 (2016), 1332–1345, 10.1016/j.cell.2016.05.041.
Kasubuchi, M, Hasegawa, S, Hiramatsu, T, Ichimura, A, Kimura, I., Dietary gut microbial metabolites, short-chain fatty acids, and host metabolic regulation. Nutrients 7 (2015), 2839–2849, 10.3390/nu7042839.
Zacharias, B, Kerler, A, Drochner, W., The influence of 5% and 10% dietary apple pectin on parameters of fermentation in faeces and caecal digesta of weaning pigs. Arch Anim Nutr 58 (2004), 149–156, 10.1080/00039420410001667502.
A MCJ, b JJGCvdB, B PVW, C CSDSB, A HAS, A HG. In vitro fermentation of 12 dietary fibres by faecal inoculum from pigs and humans. Food Chem 133 (2012), 889–897, 10.1016/j.foodchem.2012.01.110.
Stevenson, DM, Weimer, PJ., Dominance of Prevotella and low abundance of classical ruminal bacterial species in the bovine rumen revealed by relative quantification real-time PCR. Appl Microbiol Biotechnol 75 (2007), 165–174, 10.1007/s00253-006-0802-y.
Tedelind, S, Westberg, F, Kjerrulf, M, Vidal, A., Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: a study with relevance to inflammatory bowel disease. World J Gastroenterol 13 (2007), 2826–2832, 10.3748/wjg.v13.i20.2826.
Bergstrom, K, Shan, X, Casero, D, Batushansky, A, Lagishetty, V, Jacobs, JP, et al. Proximal colon-derived O-glycosylated mucus encapsulates and modulates the microbiota. Science 370 (2020), 467–472, 10.1126/science.aay7367.