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Combination of probiotics with different functions alleviate DSS-induced colitis by regulating intestinal microbiota, IL-10, and barrier function

  • Yanbo Wang
  • Qiuhong Xie
  • Ying Zhang
  • Wen Ma
  • Ke Ning
  • Jun-Yan Xiang
  • Jingwen Cui
  • Hongyu XiangEmail author
Applied microbial and cell physiology

Abstract

The potential of probiotics for treating ulcerative colitis (UC) has attracted increasing attention. However, more studies are still needed to guide physicians on the proper selection and use of probiotics. Here, we propose that combination of multiple probiotics with different functions can reduce intestinal inflammation. In this study, the effects of probiotics (Lactobacillus reuteri, Bacillus coagulans, Bifidobacterium longum, and Clostridium butyricum) on the physiology and histopathology of colon were evaluated in a dextran sulfate sodium (DSS)-induced colitis mouse model. The combined species, as well as the species individually, were tested and compared with sulfasalazine (SASP) and two Chinese herbal therapies. Results show that the functions of the four probiotic strains were different in regulating intestinal immunity and barrier function. The four-species probiotic cocktail was more effective than the species individually and anti-inflammatory drugs in repairing the dysbiosis of mucosal microbial ecology and reducing intestinal inflammation. The multi-strain probiotic mixture increased the proportion of beneficial bacteria and decreased the proportion of pro-inflammatory bacteria in the colonic mucosa. In addition, probiotic mixture significantly enhanced the expression of IL-10 and intestinal barrier function. These results suggest that a combination of multiple probiotics with different functions has synergistic effects and can restore the balance of interactions between microorganisms and immunological niches.

Keywords

Multi-strain probiotics Synergistic effects Mucosal microbial ecology IL-10 Intestinal barrier Immunological niches 

Notes

Funding information

This work was supported by the Science and Technology Development Planning of Jilin [20180201078YY].

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The animal experiment was approved by the Institutional Animal Care and Use Committee of Jilin University (IACUC). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Supplementary material

253_2019_10259_MOESM1_ESM.pdf (791 kb)
ESM 1 (PDF 791 kb).

References

  1. Ananthakrishnan AN, Bernstein CN, Iliopoulos D, Macpherson A, Neurath MF, Ali RAR, Vavricka SR, Fiocchi C (2018) Environmental triggers in IBD: a review of progress and evidence. Nat Rev Gastroenterol Hepatol 15(1):39–49.  https://doi.org/10.1038/nrgastro.2017.136 CrossRefPubMedGoogle Scholar
  2. Bordalo Tonucci L, Dos Santos KM, De Luces Fortes Ferreira CL, Ribeiro SM, De Oliveira LL, Martino HS (2017) Gut microbiota and probiotics: focus on diabetes mellitus. Crit Rev Food Sci Nutr 57(11):2296–2309.  https://doi.org/10.1080/10408398.2014.934438 CrossRefPubMedGoogle Scholar
  3. Bose S, Han KW, Lee MJ, Kim H (2013) Intestinal protective effects of herbal-based formulations in rats against neomycin insult. Evid Based Complement Alternat Med 2013:161278.  https://doi.org/10.1155/2013/161278 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Broadhurst MJ, Ardeshir A, Kanwar B, Mirpuri J, Gundra UM, Leung JM, Wiens KE, Vujkovic-Cvijin I, Kim CC, Yarovinsky F, Lerche NW, McCune JM, Loke P (2012) Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon. PLoS Pathog 8(11):e1003000.  https://doi.org/10.1371/journal.ppat.1003000 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bron PA, Kleerebezem M, Brummer RJ, Cani PD, Mercenier A, MacDonald TT, Garcia-Rodenas CL, Wells JM (2017) Can probiotics modulate human disease by impacting intestinal barrier function? Br J Nutr 117(1):93–107.  https://doi.org/10.1017/S0007114516004037 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Burrello C, Garavaglia F, Cribiu FM, Ercoli G, Lopez G, Troisi J, Colucci A, Guglietta S, Carloni S, Guglielmetti S, Taverniti V, Nizzoli G, Bosari S, Caprioli F, Rescigno M, Facciotti F (2018) Therapeutic faecal microbiota transplantation controls intestinal inflammation through IL10 secretion by immune cells. Nat Commun 9(1):5184.  https://doi.org/10.1038/s41467-018-07359-8 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cai M, Zeng L, Li LJ, Mo LH, Xie RD, Feng BS, Zheng PY, Liu ZG, Liu ZJ, Yang PC (2016) Specific immunotherapy ameliorates ulcerative colitis. Allergy Asthma Clin Immunol 12:37.  https://doi.org/10.1186/s13223-016-0142-0 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Castro-Bravo N, Wells JM, Margolles A, Ruas-Madiedo P (2018) Interactions of surface exopolysaccharides from Bifidobacterium and Lactobacillus within the intestinal environment. Front Microbiol 9:2426.  https://doi.org/10.3389/fmicb.2018.02426 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chong J, Soufan O, Li C, Caraus I, Li SZ, Bourque G, Wishart DS, Xia JG (2018) MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res 46(W1):W486–W494.  https://doi.org/10.1093/nar/gky310 CrossRefPubMedPubMedCentralGoogle Scholar
  10. de Jesus NZ, de Souza FH, Gomes IF, de Almeida Leite TJ, de Morais Lima GR, Barbosa-Filho JM, Tavares JF, da Silva MS, de Athayde-Filho PF, Batista LM (2012) Tannins, peptic ulcers and related mechanisms. Int J Mol Sci 13(3):3203–3228.  https://doi.org/10.3390/ijms13033203 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Deltenre P, Berson A, Marcellin P, Degott C, Biour M, Pessayre D (1999) Mesalazine (5-aminosalicylic acid) induced chronic hepatitis. Gut 44(6):886–888.  https://doi.org/10.1136/Gut.44.6.886 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Di Giacinto C, Marinaro M, Sanchez M, Strober W, Boirivant M (2005) Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGF-beta-bearing regulatory cells. J Immunol 174(6):3237–3246.  https://doi.org/10.4049/jimmunol.174.6.3237 CrossRefPubMedGoogle Scholar
  13. Duranti S, Gaiani F, Mancabelli L, Milani C, Grandi A, Bolchi A, Santoni A, Lugli GA, Ferrario C, Mangifesta M, Viappiani A, Bertoni S, Vivo V, Serafini F, Barbaro MR, Fugazza A, Barbara G, Gioiosa L, Palanza P, Cantoni AM, de’ Angelis GL, Barocelli E, de’ Angelis N, van Sinderen D, Ventura M, Turroni F (2016) Elucidating the gut microbiome of ulcerative colitis: bifidobacteria as novel microbial biomarkers. FEMS Microbiol Ecol 92(12):fiw191.  https://doi.org/10.1093/femsec/fiw191 CrossRefPubMedGoogle Scholar
  14. Ek S, Rosenborg S (2017) Mesalazine as a cause of fetal anemia and hydrops fetalis: a case report. Medicine 96(50):e9277.  https://doi.org/10.1097/MD.0000000000009277 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Fitzpatrick LR, Small JS, Greene WH, Karpa KD, Farmer S, Keller D (2012) Bacillus coagulans GBI-30, 6086 limits the recurrence of Clostridium difficile-Induced colitis following vancomycin withdrawal in mice. Gut Pathog 4(1):13.  https://doi.org/10.1186/1757-4749-4-13 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Ganji-Arjenaki M, Rafieian-Kopaei M (2018) Probiotics are a good choice in remission of inflammatory bowel diseases: a meta analysis and systematic review. J Cell Physiol 233(3):2091–2103.  https://doi.org/10.1002/jcp.25911 CrossRefPubMedGoogle Scholar
  17. Gao C, Major A, Rendon D, Lugo M, Jackson V, Shi Z, Mori-Akiyama Y, Versalovic J (2015) Histamine H2 Receptor-mediated suppression of intestinal inflammation by probiotic Lactobacillus reuteri. mBio 6(6):e01358–e01315.  https://doi.org/10.1128/mBio.01358-15 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gao X, Xie Q, Kong P, Liu L, Sun S, Xiong B, Huang B, Yan L, Sheng J, Xiang H (2017) Polyphenol- and caffeine-rich post-fermented Pu-er tea improves diet-induced metabolic syndrome by remodeling intestinal homeostasis in mice. Infect Immun 86(1):e00601–e00617.  https://doi.org/10.1128/IAI.00601-17 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hajavi J, Esmaeili SA, Varasteh AR, Vazini H, Atabati H, Mardani F, Momtazi-Borojeni AA, Hashemi M, Sankian M, Sahebkar A (2019) The immunomodulatory role of probiotics in allergy therapy. J Cell Physiol 234(3):2386–2398.  https://doi.org/10.1002/jcp.27263 CrossRefPubMedGoogle Scholar
  20. Jacob N, Jacobs JP, Kumagai K, Ha CWY, Kanazawa Y, Lagishetty V, Altmayer K, Hamill AM, Von Arx A, Sartor RB, Devkota S, Braun J, Michelsen KS, Targan SR, Shih DQ (2018) Inflammation-independent TL1A-mediated intestinal fibrosis is dependent on the gut microbiome. Mucosal Immunol 11(5):1466–1476.  https://doi.org/10.1038/s41385-018-0055-y CrossRefPubMedPubMedCentralGoogle Scholar
  21. Jang SE, Jeong JJ, Kim JK, Han MJ, Kim DH (2018) Simultaneous amelioratation of colitis and liver injury in mice by Bifidobacterium longum LC67 and Lactobacillus plantarum LC27. Sci Rep 8(1):7500.  https://doi.org/10.1038/s41598-018-25775-0 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Je IG, Lee DG, Jeong DG, Hong D, Yoon JM, Moon JS, Park S (2018) The probiotic, ID-JPL934, attenuates dextran sulfate sodium-induced colitis in mice through inhibition of proinflammatory cytokines expression. J Med Food 21(9):858–865.  https://doi.org/10.1089/jmf.2017.4152 CrossRefPubMedGoogle Scholar
  23. Kmiec Z, Cyman M, Slebioda TJ (2017) Cells of the innate and adaptive immunity and their interactions in inflammatory bowel disease. Adv Med Sci 62(1):1–16.  https://doi.org/10.1016/j.advms.2016.09.001 CrossRefPubMedGoogle Scholar
  24. Lee YS, Kim TY, Kim Y, Lee SH, Kim S, Kang SW, Yang JY, Baek IJ, Sung YH, Park YY, Hwang SW, Eunju O, Kim KS, Liu SQ, Kamada N, Gao N, Kweon MN (2018) Microbiota-derived lactate accelerates iIntestinal stem-cell-mediated epithelial development. Cell Host Microbe 24(6):833–846.  https://doi.org/10.1016/j.chom.2018.11.002 CrossRefPubMedGoogle Scholar
  25. Li ZJ, Guo X, Dawuti G, Aibai S (2015) Antifungal activity of ellagic acid in vitro and in vivo. Phytother Res 29(7):1019–1025.  https://doi.org/10.1002/ptr.5340 CrossRefPubMedGoogle Scholar
  26. Luyen BTT, Tai BH, Thao NP, Eun KJ, Cha JY, Xin MJ, Lee YM, Kim YH (2014) Anti-inflammatory components of Euphorbia humifusa Willd. Bioorg Med Chem Lett 24(8):1895–1900.  https://doi.org/10.1016/j.bmcl.2014.03.014 CrossRefPubMedGoogle Scholar
  27. Mahalhal A, Williams JM, Johnson S, Ellaby N, Duckworth CA, Burkitt MD, Liu X, Hold GL, Campbell BJ, Pritchard DM, Probert CS (2018) Oral iron exacerbates colitis and influences the intestinal microbiome. PloS One 13(10):e0202460.  https://doi.org/10.1371/journal.pone.0202460 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Marchal-Bressenot A, Scherl A, Salleron J, Peyrin-Biroulet L (2016) A practical guide to assess the Nancy histological index for UC. Gut 65(11):1919–1920.  https://doi.org/10.1136/gutjnl-2016-312722 CrossRefPubMedPubMedCentralGoogle Scholar
  29. McGuckin MA, Eri R, Simms LA, Florin TH, Radford-Smith G (2009) Intestinal barrier dysfunction in inflammatory bowel diseases. Inflamm Bowel Dis 15(1):100–113.  https://doi.org/10.1002/ibd.20539 CrossRefPubMedGoogle Scholar
  30. Mu Y, Cong Y (2019) Bacillus coagulans and its applications in medicine. Benef Microbes 10(6):679–688.  https://doi.org/10.3920/BM2019.0016 CrossRefGoogle Scholar
  31. Mukhopadhya I, Hansen R, El-Omar EM, Hold GL (2012) IBD-what role do Proteobacteria play? Nat Rev Gastro Hepat 9(4):219–230.  https://doi.org/10.1038/nrgastro.2012.14 CrossRefGoogle Scholar
  32. Myer PR, Kim M, Freetly HC, Smith TPL (2016) Evaluation of 16S rRNA amplicon sequencing using two next-generation sequencing technologies for phylogenetic analysis of the rumen bacterial community in steers. J Microbiol Methods 127:132–140.  https://doi.org/10.1016/j.mimet.2016.06.004 CrossRefPubMedGoogle Scholar
  33. Neurath MF (2014) Cytokines in inflammatory bowel disease. Nat Rev Immunol 14(5):329–342.  https://doi.org/10.1038/nri3661 CrossRefPubMedGoogle Scholar
  34. Nishida A, Inoue R, Inatomi O, Bamba S, Naito Y, Andoh A (2018) Gut microbiota in the pathogenesis of inflammatory bowel disease. Clin J Gastroenterol 11(1):1–10.  https://doi.org/10.1007/s12328-017-0813-5 CrossRefPubMedGoogle Scholar
  35. Pagliari D, Gambassi G, Piccirillo CA, Cianci R (2017) The intricate link among gut “immunological niche,” microbiota, and xenobiotics in intestinal pathology. Mediators Inflamm 2017:8390595.  https://doi.org/10.1155/2017/8390595 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Ramos GP, Papadakis KA (2019) Mechanisms of disease: inflammatory bowel diseases. Mayo Clin Proc 94(1):155–165.  https://doi.org/10.1016/j.mayocp.2018.09.013 CrossRefPubMedGoogle Scholar
  37. Ransford RA, Langman MJ (2002) Sulphasalazine and mesalazine: serious adverse reactions re-evaluated on the basis of suspected adverse reaction reports to the Committee on Safety of Medicines. Gut 51(4):536–539.  https://doi.org/10.1136/gut.51.4.536 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Robertson BR, O’Rourke JL, Neilan BA, Vandamme P, On SL, Fox JG, Lee A (2005) Mucispirillum schaedleri gen. nov., sp. nov., a spiral-shaped bacterium colonizing the mucus layer of the gastrointestinal tract of laboratory rodents. Int J Syst Evol Microbiol 55(Pt 3):1199–1204.  https://doi.org/10.1099/ijs.0.63472-0 CrossRefPubMedGoogle Scholar
  39. Rooks MG, Veiga P, Wardwell-Scott LH, Tickle T, Segata N, Michaud M, Gallini CA, Beal C, van Hylckama-Vlieg JE, Ballal SA, Morgan XC, Glickman JN, Gevers D, Huttenhower C, Garrett WS (2014) Gut microbiome composition and function in experimental colitis during active disease and treatment-induced remission. ISME J 8(7):1403–1417.  https://doi.org/10.1038/ismej.2014.3 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Sartor RB, Wu GD (2017) Roles for intestinal bacteria, viruses, and fungi in pathogenesis of inflammatory bowel diseases and therapeutic approaches. Gastroenterology 152(2):327–339 e4.  https://doi.org/10.1053/j.gastro.2016.10.012 CrossRefPubMedGoogle Scholar
  41. Schroeder BO, Birchenough GMH, Stahlman M, Arike L, Johansson MEV, Hansson GC, Backhed F (2018) Bifidobacteria or fiber protects against diet-induced microbiota-mediated colonic mucus deterioration. Cell Host Microbe 23(1):27–40 e7.  https://doi.org/10.1016/j.chom.2017.11.004 CrossRefPubMedGoogle Scholar
  42. Shang X, Miao X, Yang F, Li B, Guo X, Pan H, Zhang Y, Zhang J (2018) The anti-diarrheal activity of the non-toxic dihuang powder in mice. Front Pharmacol 9:1037.  https://doi.org/10.3389/fphar.2018.01037 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Shin IS, Jeon WY, Shin HK, Cha SW, Lee MY (2013) Banhabaekchulchunma-tang, a traditional herbal formula attenuates absolute ethanol-induced gastric injury by enhancing the antioxidant status. BMC Complement Altern Med 13:170.  https://doi.org/10.1186/1472-6882-13-170 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Singer E, Bushnell B, Coleman-Derr D, Bowman B, Bowers RM, Levy A, Gies EA, Cheng JF, Copeland A, Klenk HP, Hallam SJ, Hugenholtz P, Tringe SG, Woyke T (2016) High-resolution phylogenetic microbial community profiling. ISME J 10(8):2020–2032.  https://doi.org/10.1038/ismej.2015.249 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Song X, Dai D, He X, Zhu S, Yao Y, Gao H, Wang J, Qu F, Qiu J, Wang H, Li X, Shen N, Qian Y (2015) Growth factor FGF2 cooperates with interleukin-17 to repair intestinal epithelial damage. Immunity 43(3):488–501.  https://doi.org/10.1016/j.immuni.2015.06.024 CrossRefPubMedGoogle Scholar
  46. Sun M, Wu W, Liu Z, Cong Y (2017) Microbiota metabolite short chain fatty acids, GPCR, and inflammatory bowel diseases. J Gastroenterol 52(1):1–8.  https://doi.org/10.1007/s00535-016-1242-9 CrossRefPubMedGoogle Scholar
  47. Sun M, Wu W, Chen L, Yang W, Huang X, Ma C, Chen F, Xiao Y, Zhao Y, Ma C, Yao S, Carpio VH, Dann SM, Zhao Q, Liu Z, Cong Y (2018) Microbiota-derived short-chain fatty acids promote Th1 cell IL-10 production to maintain intestinal homeostasis. Nat Commun 9(1):3555.  https://doi.org/10.1038/s41467-018-05901-2 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Talero E, Bolivar S, Avila-Roman J, Alcaide A, Fiorucci S, Motilva V (2015) Inhibition of chronic ulcerative colitis-associated adenocarcinoma development in mice by VSL#3. Inflamm Bowel Dis 21(5):1027–1037.  https://doi.org/10.1097/MIB.0000000000000346 CrossRefPubMedGoogle Scholar
  49. Tong X, Xu J, Lian F, Yu X, Zhao Y, Xu L, Zhang M, Zhao X, Shen J, Wu S, Pang X, Tian J, Zhang C, Zhou Q, Wang L, Pang B, Chen F, Peng Z, Wang J, Zhen Z, Fang C, Li M, Chen L, Zhao L (2018) Structural alteration of gut microbiota during the amelioration of human type 2 diabetes with hyperlipidemia by metformin and a traditional Chinese herbal formula: a multicenter, randomized, open label clinical trial. mBio 9(3):e02392–e02317.  https://doi.org/10.1128/mBio.02392-17 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Turner JR (2009) Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9(11):799–809.  https://doi.org/10.1038/nri2653 CrossRefPubMedGoogle Scholar
  51. Tursi A, Brandimarte G, Papa A, Giglio A, Elisei W, Giorgetti GM, Forti G, Morini S, Hassan C, Pistoia MA, Modeo ME, Rodino S, D’Amico T, Sebkova L, Sacca N, Di Giulio E, Luzza F, Imeneo M, Larussa T, Di Rosa S, Annese V, Danese S, Gasbarrini A (2010) Treatment of relapsing mild-to-moderate ulcerative colitis with the probiotic VSL#3 as adjunctive to a standard pharmaceutical treatment: a double-blind, randomized, placebo-controlled study. Am J Gastroenterol 105(10):2218–2227.  https://doi.org/10.1038/ajg.2010.218 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Ungaro R, Mehandru S, Allen PB, Peyrin-Biroulet L, Colombel J-F (2017) Ulcerative colitis. Lancet 389(10080):1756–1770.  https://doi.org/10.1016/s0140-6736(16)32126-2 CrossRefPubMedGoogle Scholar
  53. Wang YB, Xie QH, Sun S, Huang BJ, Zhang Y, Xu Y, Zhang SM, Xiang HY (2018) Probiotics-fermented Massa Medicata Fermentata ameliorates weaning stress in piglets related to improving intestinal homeostasis. Appl Microbiol Biotechnol 102(24):10713–10727.  https://doi.org/10.1007/s00253-018-9438-y CrossRefPubMedGoogle Scholar
  54. Whon TW, Chung WH, Lim MY, Song EJ, Kim PS, Hyun DW, Shin NR, Bae JW, Nam YD (2018) The effects of sequencing platforms on phylogenetic resolution in 16S rRNA gene profiling of human feces. Sci Data 5:180068.  https://doi.org/10.1038/sdata.2018.68 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Yan F, Cao H, Cover TL, Whitehead R, Washington MK, Polk DB (2007) Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 132(2):562–575.  https://doi.org/10.1053/j.gastro.2006.11.022 CrossRefPubMedGoogle Scholar
  56. Yoshimatsu Y, Yamada A, Furukawa R, Sono K, Osamura A, Nakamura K, Aoki H, Tsuda Y, Hosoe N, Takada N, Suzuki Y (2015) Effectiveness of probiotic therapy for the prevention of relapse in patients with inactive ulcerative colitis. World J Gastroenterol 21(19):5985–5994.  https://doi.org/10.3748/wjg.v21.i19.5985 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Zhang HQ, Ding TT, Zhao JS, Yang X, Zhang HX, Zhang JJ, Cui YL (2009) Therapeutic effects of Clostridium butyricum on experimental colitis induced by oxazolone in rats. World J Gastroenterol 15(15):1821–1828.  https://doi.org/10.3748/wjg.15.1821 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Zhang SL, Wang SN, Miao CY (2017) Influence of microbiota on intestinal immune system in ulcerative colitis and its intervention. Front Immunol 8:1674.  https://doi.org/10.3389/fimmu.2017.01674 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Zhou Y, Xu ZZ, He Y, Yang Y, Liu L, Lin Q, Nie Y, Li M, Zhi F, Liu S, Amir A, González A, Tripathi A, Chen M, Wu GD, Knight R, Zhou H, Chen Y, Ercolini D (2018) Gut microbiota offers universal biomarkers across ethnicity in inflammatory bowel disease diagnosis and infliximab response prediction. mSystems 3(1):e00188–e00117.  https://doi.org/10.1128/mSystems.00188-17 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Zou J, Chassaing B, Singh V, Pellizzon M, Ricci M, Fythe MD, Kumar MV, Gewirtz AT (2018) Fiber-mediated nourishment of gut microbiota protects against diet-induced obesity by restoring IL-22-mediated colonic health. Cell Host Microbe 23(1):41–53.e4.  https://doi.org/10.1016/j.chom.2017.11.003 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Life SciencesJilin UniversityJilinPeople’s Republic of China
  2. 2.Key Laboratory for Molecular Enzymology and Engineering of Ministry of Education, School of Life SciencesJilin UniversityJilinPeople’s Republic of China
  3. 3.National Engineering Laboratory for AIDS Vaccine, School of Life SciencesJilin UniversityJilinPeople’s Republic of China

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