A mixture of Lactobacillus species isolated from traditional fermented foods promote recovery from antibiotic-induced intestinal disruption in mice

Journal of Applied Microbiology

Volumn 124, Issue 3, 2018, Pages 842-854

  Shi, Y ^a   Zhao, X ^b   Zhao, J ^a   Zhang, H ^a,c   Zhai, Q ^a,c   Narbad, A ^d,e   Chen, W ^a,c,f  

^a JIANGNAN UNIVERSITY   (China)

^b SHANGHAITECH UNIVERSITY   (China)

^c National Engineering Research Center for Functional Food   (China)

^d UK China Joint Centre on Probiotic Bacteria   (United Kingdom)

^e INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^f BEIJING TECHNOLOGY AND BUSINESS UNIVERSITY   (China)

Author keywords

antibiotics; diseases; immunology; intestinal microbiota; Lactobacillus

Indexed keywords

BACTERIA; ECOLOGY; MAMMALS; PATHOLOGY; PROBIOTICS; RECOVERY; RESTORATION;

BACTEROIDETES; GUT BARRIER; INTESTINAL MICROBIOTA; LACTOBACILLUS; LACTOBACILLUS SPECIES; LOW GRADE; MICROBIAL ECOLOGY; MICROBIOTAS; PROBIOTICS; TRADITIONAL FERMENTED FOODS;

ANTIBIOTICS;

AMPICILLIN; BACTERIAL RNA; BACTERIUM LIPOPOLYSACCHARIDE; BETA ACTIN; CLAUDIN 1; GAMMA INTERFERON; GENOMIC DNA; INTERLEUKIN 1BETA; INTERLEUKIN 6; LACTIC ACID; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; OCCLUDIN; PROBIOTIC AGENT; PROTEIN ZO1; RNA 16S; TUMOR NECROSIS FACTOR; ANTIINFECTIVE AGENT; CYTOKINE;

ABUNDANCE; ANTIBIOTICS; BACTERIUM; COMMUNITY STRUCTURE; DISEASE; FERMENTATION; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; MICROBIAL ECOLOGY; MICROORGANISM; RODENT; SPECIES DIVERSITY; TOXIN;

ACINETOBACTER; ACTINOBACTERIA; AKKERMANSIA; ALISTIPES; ANAEROTRUNCUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AZORHIZOPHILUS; BACILLACEAE; BACILLI; BACTERIAL STRAIN; BACTERIUM; BACTERIUM ISOLATE; BACTERIUM ISOLATION; BACTEROIDES; BACTEROIDETES; BARNESIELLA; BETAPROTEOBACTERIA; BURKHOLDERIA; BUTYRICICOCCUS; CECUM; CLOSTRIDIA; CLOSTRIDIALES; COLON TISSUE; COMMUNITY STRUCTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DESULFOVIBRIONALES; DOREA; DYSBIOSIS; ENTERITIS; ENTEROBACTERIACEAE; ENTEROCOCCACEAE; ENTEROCOCCUS; ENTERORHABDUS; ERYSIPELOTRICHACEAE; EUBACTERIUM; FECES MICROFLORA; FERMENTED PRODUCT; FIRMICUTES; GENE EXPRESSION LEVEL; HELICOBACTER; HOMEOSTASIS; ILEUM TISSUE; IMMUNOCOMPETENT CELL; INTESTINE FLORA; INTESTINE FUNCTION; INTESTINE MUCOSA PERMEABILITY; LACHNNOSPIRACEAE; LACTOBACILLUS; LACTOBACILLUS CASEI; LACTOBACILLUS HELVETICUS; LACTOBACILLUS PLANTARUM; LACTOBACILLUS RHAMNOSUS; MALE; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MOUSE; MUCISPIRILLUM; NONHUMAN; ODORIBACTER; OSCILLIBACTER; PAPILLIBACTER; PARABACTEROIDES; PARASUTTERELLA; POPULATION ABUNDANCE; PORPHYROMONADACEAE; PREVOTELLA; PROTEOBACTERIA; PSEUDOMONAS; ROBINSONIELLA; RUMINOCOCCACEAE; RUMINOCOCCUS; SERUM; SPECIES COMPOSITION; SPOROBACTER; STAPHYLOCOCCUS; SUPPLEMENTATION; ANIMAL; BRASSICA; C57BL MOUSE; COLON; DRUG EFFECT; ENTEROPATHY; GENETICS; HUMAN; ILEUM; IMMUNOLOGY; INTESTINE; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

AKKERMANSIA; BACTEROIDETES; LACTOBACILLUS; MUS;

ANIMALS; ANTI-BACTERIAL AGENTS; BRASSICA; CECUM; COLON; CYTOKINES; FERMENTED FOODS; GASTROINTESTINAL MICROBIOME; HUMANS; ILEUM; INTESTINAL DISEASES; INTESTINES; LACTOBACILLUS; MALE; MICE; MICE, INBRED C57BL; PROBIOTICS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85041574158     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.13687     Document Type: Article

References (56)

1. Anderson, R.C., Cookson, A.L., McNabb, W.C., Park, Z., McCann, M.J., Kelly, W.J. and Roy, N.C. (2010) Lactobacillus plantarum MB452 enhances the function of the intestinal barrier by increasing the expression levels of genes involved in tight junction formation. BMC Microbiol 10, 63–69.
2. Bischoff, S.C., Barbara, G., Buurman, W., Ockhuizen, T., Schulzke, J.D., Serino, M., Tilg, H., Watson, A. et al. (2014) Intestinal permeability–a new target for disease prevention and therapy. BMC Gastroenterol 14, 189.
3. Brown, K., Uwiera, R.R.E., Kalmokoff, M.L., Brooks, S.P.J. and Inglis, G.D. (2017) Antimicrobial growth promoter use in livestock: a requirement to understand their modes of action to develop effective alternatives. Int J Antimicrob Agents 49, 12–24.
4. Buffie, C.G., Jarchum, I., Equinda, M., Lipuma, L., Gobourne, A., Viale, A., Ubeda, C., Xavier, J. et al. (2012) Profound alterations of intestinal microbiota following a single dose of clindamycin results in sustained susceptibility to clostridium difficile-induced colitis. Infect Immun 80, 62–73.
5. Camilleri, M., Madsen, K., Spiller, R., Van Meerveld, B.G. and Verne, G.N. (2012) Intestinal barrier function in health and gastrointestinal disease. Neurogastroent Motil 24, 967–976.
6. Cani, P.D., Possemiers, S., deVan Wiele, T., Guiot, Y., Everard, A., Rottier, O., Geurts, L., Naslain, D. et al. (2009). Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58, 1091–1103.
7. Canova, C., Zabeo, V., Pitter, G., Romor, P., Baldovin, T., Zanotti, R. and Simonato, L. (2014) Association of maternal education, early infections, and antibiotic use with celiac disease: a population-based birth cohort study in northeastern Italy. Am J Epidemiol 180, 76–85.
8. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Pena, A.G. et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7, 335–336.
9. Chen, Z., Wang, Y., Zeng, A., Chen, L., Wu, R., Chen, B., Chen, M., Bo, J. et al. (2012) The clinical diagnostic significance of cerebrospinal fluid D-lactate for bacterial meningitis. Int J Clin Chem 413, 1512–1515.
10. Chiodini, R.J., Dowd, S.E., Chamberlin, W.M., Galandiuk, S., Davis, B. and Glassing, A. (2015) Microbial population differentials between mucosal and submucosal intestinal tissues in advanced Crohn's disease of the ileum. PLoS ONE 10, e0134382.
11. Cho, I., Yamanishi, S., Cox, L., Methe, B.A., Zavadil, J., Li, K., Gao, Z., Mahana, D. et al. (2012) Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 488, 621–629.
12. Cox, L.M., Yamanishi, S., Sohn, J., Alekseyenko, A.V., Leung, J.M., Cho, I., Kim, S.G., Li, H. et al. (2014) Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 158, 705–721.
13. De, P.G., Nadal, I., Medina, M., Donat, E., Ribeskoninckx, C., Calabuig, M. and Sanz, Y. (2010) Intestinal dysbiosis and reduced immunoglobulin-coated bacteria associated with coeliac disease in children. BMC Microbiol 10, 63–69.
14. Derrien, M., Van Baarlen, P., Hooiveld, G., Norin, E., Muller, M. and de Vos, W.M. (2011) Modulation of mucosal immune response, tolerance, and proliferation in mice colonized by the mucin-degrader Akkermansia muciniphila. Front Microbiol 2, 6–19.
15. Emge, J.R., Huynh, K., Miller, E.N., Kaur, M., Reardon, C., Barrett, K.E. and Gareau, M.G. (2016) Modulation of the microbiota-gut-brain axis by probiotics in a murine model of inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol 310, 989–998.
16. Fouhy, F., Guinane, C.M., Hussey, S., Wall, R., Ryan, C.A., Dempsey, E.M., Murphy, B., Ross, R.P. et al. (2012) High-throughput sequencing reveals the incomplete, short-term recovery of infant gut microbiota following parenteral antibiotic treatment with ampicillin and gentamicin. Antimicrob Agents Chemother 56, 5811–5820.
17. Gao, X.W., Mubasher, M., Fang, C.Y., Reifer, C. and Miller, L.E. (2010) Dose-response efficacy of a proprietary probiotic formula of Lactobacillus acidophilus CL1285 and Lactobacillus casei LBC80R for antibiotic-associated diarrhea and Clostridium difficile-associated diarrhea prophylaxis in adult patients. Am J Gastroentero 105, 1636–1641.
18. Gareau, M.G., Sherman, P.M. and Walker, W.A. (2010) Probiotics and the gut microbiota in intestinal health and disease. Nat Rev Gastroenterol Hepatol 7, 503–514.
19. Goulet, O. (2015) Potential role of the intestinal microbiota in programming health and disease. Nutr Rev 73(Suppl. 1), 32–40.
20. Gu, S.H., Chen, D.D., Zhang, J.N., Lv, X.M., Wang, K., Duan, L.P., Nie, Y. and Wu, X.L. (2013) Bacterial community mapping of the mouse gastrointestinal tract. PLoS ONE 8, e74957.
21. Hooper, L.V., Wong, M.H., Thelin, A., Hansson, L., Falk, P.G. and Gordon, J.I. (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291, 881–884.
22. van Hylckama Vlieg, J.E.T., Veiga, P., Zhang, C., Derrien, M. and Zhao, L. (2011) Impact of microbial transformation of food on health-from fermented foods to fermentation in the gastro-intestinal tract. Curr Opin Biotechnol 22, 211–219.
23. Jernberg, C., Lofmark, S., Edlund, C. and Jansson, J.K. (2007) Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J 1, 56–66.
24. Kaakoush, N.O., Day, A.S., Huinao, K.D., Leach, S.T., Lemberg, D.A., Dowd, S.E. and Mitchell, H.M. (2012) Microbial dysbiosis in pediatric patients with Crohn's disease. J Clin Microbiol 50, 3258–3266.
25. Kale-Pradhan, P.B., Jassal, H.K. and Wilhelm, S.M. (2010) Role of Lactobacillus in the prevention of antibiotic-associated diarrhea: a meta-analysis. Pharmacotherapy 30, 119–126.
26. Kato-Kataoka, A., Nishida, K., Takada, M., Kawai, M., Kikuchi-Hayakawa, H., Suda, K., Ishikawa, H., Gondo, Y. et al. (2016) Fermented milk containing Lactobacillus casei strain Shirota preserves the diversity of the gut microbiota and relieves abdominal dysfunction in healthy medical students exposed to academic stress. Appl Environ Microbiol 82, 3649–3658.
27. Knoop, K.A., McDonald, K.G., Kulkarni, D.H. and Newberry, R.D. (2016) Antibiotics promote inflammation through the translocation of native commensal colonic bacteria. Gut 65, 1100–1109.
28. Konishi, H., Fujiya, M., Tanaka, H., Ueno, N., Moriichi, K., Sasajima, J., Ikuta, K., Akutsu, H. et al. (2016) Probiotic-derived ferrichrome inhibits colon cancer progression via JNK-mediated apoptosis. Nat Commun 7, 12365.
29. Livak, K.J. and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25, 402–408.
30. Lonnermark, E., Friman, V., Lappas, G., Sandberg, T., Berggren, A. and Adlerberth, I. (2010) Intake of Lactobacillus plantarum reduces certain gastrointestinal symptoms during treatment with antibiotics. J Clin Gastroenterol 44, 106–112.
31. Lozupone, C. and Knight, R. (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71, 8228–8235.
32. Marco, M.L., Heeney, D., Binda, S., Cifelli, C.J., Cotter, P.D., Foligné, B., Gänzle, M., Kort, R. et al. (2017) Health benefits of fermented foods: microbiota and beyond. Curr Opin Biotechnol 44, 94–102.
33. Mileti, E., Matteoli, G., Iliev, I.D. and Rescigno, M. (2009) Comparison of the immunomodulatory properties of three probiotic strains of Lactobacilli using complex culture systems: prediction for in vivo efficacy. PLoS ONE 4, 2125–2133.
34. Nobel, Y.R., Cox, L.M., Kirigin, F.F., Bokulich, N.A., Yamanishi, S., Teitler, I., Chung, J., Sohn, J. et al. (2015) Metabolic and metagenomic outcomes from early-life pulsed antibiotic treatment. Nat Commun 6, 7486.
35. Pang, W., Vogensen, F.K., Nielsen, D.S. and Hansen, A.K. (2012) Faecal and caecal microbiota profiles of mice do not cluster in the same way. Lab Anim 46, 231–236.
36. Png, C.W., Linden, S.K., Gilshenan, K.S., Zoetendal, E.G., McSweeney, C.S., Sly, L.I., McGuckin, M.A. and Florin, T.H.J. (2010) Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol 105, 2420–2428.
37. Rousseaux, C., Thuru, X., Gelot, A., Barnich, N., Neut, C., Dubuquoy, L., Dubuquoy, C., Merour, E. et al. (2007) Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat Med 13, 35–37.
38. Santacruz, A., Collado, M.C., García-Valdés, L., Segura, M.T., Martín-Lagos, J.A., Anjos, T., Martí-Romero, M., Lopez, R.M. et al. (2010) Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr 104, 83–92.
39. Sartor, R.B. (2008) Microbial influences in inflammatory bowel diseases. Gastroenterology 134, 577–594.
40. Shaw, S.Y., Blanchard, J.F. and Bernstein, C.N. (2010) Association between the use of antibiotics in the first year of life and pediatric inflammatory bowel disease. Am J Gastroenterol 105, 2687–2692.
41. Shaw, S.Y., Blanchard, J.F. and Bernstein, C.N. (2011) Association between the use of antibiotics and new diagnoses of Crohn's disease and ulcerative colitis. Am J Gastroenterol 106, 2133–2142.
42. Sun, X.Q., Fu, X.B., Rong, Z., Lü, Y., Deng, Q., Jiang, X.G. and Sheng, Z.Y. (2001) Relationship between plasma D(-)-lactate and intestinal damage after severe injuries in rats. World J Gastroentero 7, 555–558.
43. Suzaki, H., Asano, K., Ohki, S., Kanai, K., Mizutani, T. and Hisamitsu, T. (1999) Suppressive activity of a macrolide antibiotic, roxithromycin, on pro-inflammatory cytokine production in vitro and in vivo. Mediat Inflamm 8, 199–204.
44. Swidsinski, A., Loening-Baucke, V., Vaneechoutte, M. and Doerffel, Y. (2008a) Active Crohn's disease and ulcerative colitis can be specifically diagnosed and monitored based on the biostructure of the fecal flora. Inflamm Bowel Dis 14, 147–161.
45. Swidsinski, A., Loeningbaucke, V., Verstraelen, H., Osowska, S. and Doerffel, Y. (2008b) Biostructure of fecal microbiota in healthy subjects and patients with chronic idiopathic diarrhea. Gastroenterology 135, 568–579.
46. Swidsinski, A., Dorffel, Y., Loening-Baucke, V., Theissig, F., Ruckert, J.C., Ismail, M., Rau, W.A., Gaschler, D. et al. (2011) Acute appendicitis is characterised by local invasion with Fusobacterium nucleatum/necrophorum. Gut 60, 34–40.
47. Tanca, A., Manghina, V., Fraumene, C., Palomba, A., Abbondio, M., Deligios, M., Silverman, M. and Uzzau, S. (2017) Metaproteogenomics reveals taxonomic and functional changes between cecal and fecal microbiota in mouse. Front Microbiol 8, 391.
48. Tannock, G.W. (2008) Molecular analysis of the intestinal microflora in IBD. Mucosal Immunol 1(Suppl 1), 15–18.
49. Tien, M.T., Girardin, S.E., Regnault, B., Bourhis, L.L., Dillies, M.A., Coppée, J.Y., Bourdetsicard, R., Sansonetti, P.J. et al. (2006) Anti-inflammatory effect of Lactobacillus casei on Shigella-infected human intestinal epithelial cells. J Immunol 176, 1228–1237.
50. Verdú, E.F. (2006) Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice. Gut 55, 182–190.
51. Wang, Q., Garrity, G.M., Tiedje, J.M. and Cole, J.R. (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73, 5261–5267.
52. Wang, L., Christophersen, C.T., Sorich, M.J., Gerber, J.P., Angley, M.T. and Ma, C. (2011) Low relative abundances of the mucolytic bacterium Akkermansia muciniphila and Bifidobacterium spp. in feces of children with autism. Appl Environ Microbiol 77, 6718–6721.
53. Zhai, Q., Tian, F., Wang, G., Zhao, J., Liu, X., Cross, K., Zhang, H., Narbad, A. et al. (2016) The cadmium binding characteristics of a lactic acid bacterium in aqueous solutions and its application for removal of cadmium from fruit and vegetable juices. RSC Adv 6, 5990–5998.
54. Zhao, L.L., Wang, G., Siegel, P., He, C., Wang, H.Z., Zhao, W.J., Zhai, Z.X., Tian, F.W. et al. (2013) Quantitative genetic background of the host influences gut microbiomes in chickens. Sci Rep 3, 1163.
55. Zhao, H., Zhao, C., Dong, Y., Zhang, M., Wang, Y., Li, F., Li, X., McClain, C. et al. (2015) Inhibition of miR122a by Lactobacillus rhamnosus GG culture supernatant increases intestinal occludin expression and protects mice from alcoholic liver disease. Toxicol Lett 234, 194–200.
56. Zhu, Y., Michelle Luo, T., Jobin, C. and Young, H.A. (2011) Gut microbiota and probiotics in colon tumorigenesis. Cancer Lett 309, 119–127.