Personalized Gut Mucosal Colonization Resistance to Empiric Probiotics Is Associated with Unique Host and Microbiome Features

Cell - Tập 174 - Trang 1388-1405.e21 - 2018
Niv Zmora1,2, Gili Zilberman-Schapira1, Jotham Suez1, Uria Mor1, Mally Dori-Bachash1, Stavros Bashiardes1, Eran Kotler3,4, Maya Zur1, Dana Regev-Lehavi1, Rotem Ben-Zeev Brik1, Sara Federici1, Yotam Cohen1, Raquel Linevsky1, Daphna Rothschild3,4, Andreas E. Moor3, Shani Ben-Moshe3, Alon Harmelin5, Shalev Itzkovitz3, Nitsan Maharshak6,7,8, Oren Shibolet6,7,9
1Immunology Department, Weizmann Institute of Science, Rehovot, 7610001, Israel
2Internal Medicine Department, Tel Aviv Sourasky Medical Center, Tel Aviv, 6423906, Israel
3Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot 7610001, Israel
4Department of Computer Science and Applied Mathematics, Weizmann Institute of Science, Rehovot 7610001, Israel
5Department of Veterinary Resources, Weizmann Institute of Science, Rehovot 7610001, Israel
6Department of Gastroenterology and Liver Diseases, Tel Aviv Sourasky Medical Center, Tel Aviv, 6423906, Israel
7Research Center for Digestive Tract and Liver Diseases, Tel Aviv Sourasky Medical Center, Tel Aviv 6423906, Israel
8Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv 6997801, Israel
9Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv 6997801, Israel

Tài liệu tham khảo

Adiconis, 2013, Comparative analysis of RNA sequencing methods for degraded or low-input samples, Nat. Methods, 10, 623, 10.1038/nmeth.2483 Bafeta, 2018, Harms Reporting in Randomized Controlled Trials of Interventions Aimed at Modifying Microbiota: A Systematic Review, Ann. Intern. Med., 10.7326/M18-0343 Bernet, 1994, Lactobacillus acidophilus LA 1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria, Gut, 35, 483, 10.1136/gut.35.4.483 Besselink, 2008, Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial, Lancet, 371, 651, 10.1016/S0140-6736(08)60207-X Bik, 2006, Molecular analysis of the bacterial microbiota in the human stomach, Proc. Natl. Acad. Sci. USA, 103, 732, 10.1073/pnas.0506655103 Bolger, 2014, Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, 30, 2114, 10.1093/bioinformatics/btu170 Caporaso, 2010, QIIME allows analysis of high-throughput community sequencing data, Nat. Methods, 7, 335, 10.1038/nmeth.f.303 Charbonneau, 2013, Fecal excretion of Bifidobacterium infantis 35624 and changes in fecal microbiota after eight weeks of oral supplementation with encapsulated probiotic, Gut Microbes, 4, 201, 10.4161/gmic.24196 Clarke, 2015, Trends in the use of complementary health approaches among adults: United States, 2002-2012, Natl. Health Stat. Rep., 79, 1 Crovesy, 2017, Effect of Lactobacillus on body weight and body fat in overweight subjects: a systematic review of randomized controlled clinical trials, Int. J. Obes., 41, 1607, 10.1038/ijo.2017.161 Degnan, 2012, Clinical studies involving probiotics: when FDA’s investigational new drug rubric applies-and when it may not, Gut Microbes, 3, 485, 10.4161/gmic.22158 Del Piano, 2010, Evaluation of the intestinal colonization by microencapsulated probiotic bacteria in comparison with the same uncoated strains, J. Clin. Gastroenterol., 44, S42, 10.1097/MCG.0b013e3181ed0e71 Donaldson, 2016, Gut biogeography of the bacterial microbiota, Nat. Rev. Microbiol., 14, 20, 10.1038/nrmicro3552 Drago, 2016, Persisting changes of intestinal microbiota after bowel lavage and colonoscopy, Eur. J. Gastroenterol. Hepatol., 28, 532, 10.1097/MEG.0000000000000581 Draper, 2017, Probiotic guidelines and physician practice: a cross-sectional survey and overview of the literature, Benef. Microbes, 8, 507, 10.3920/BM2016.0146 Eden, 2009, GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists, BMC Bioinformatics, 10, 48, 10.1186/1471-2105-10-48 Eloe-Fadrosh, 2015, Functional dynamics of the gut microbiome in elderly people during probiotic consumption, MBio, 6, 10.1128/mBio.00231-15 Ferrario, 2014, Modulation of fecal Clostridiales bacteria and butyrate by probiotic intervention with Lactobacillus paracasei DG varies among healthy adults, J. Nutr., 144, 1787, 10.3945/jn.114.197723 Frese, 2012, Comparison of the colonization ability of autochthonous and allochthonous strains of lactobacilli in the human gastrointestinal tract, Adv. Microbiol., 2, 399, 10.4236/aim.2012.23051 Fukushima, 1998, Effect of a probiotic formula on intestinal immunoglobulin A production in healthy children, Int. J. Food Microbiol., 42, 39, 10.1016/S0168-1605(98)00056-7 Fuller, 1991, Probiotics in human medicine, Gut, 32, 439, 10.1136/gut.32.4.439 Furet, 2004, Molecular quantification of lactic acid bacteria in fermented milk products using real-time quantitative PCR, Int. J. Food Microbiol., 97, 197, 10.1016/j.ijfoodmicro.2004.04.020 Goldin, 1992, Survival of Lactobacillus species (strain GG) in human gastrointestinal tract, Dig. Dis. Sci., 37, 121, 10.1007/BF01308354 Goossens, 2003, The effect of Lactobacillus plantarum 299v on the bacterial composition and metabolic activity in faeces of healthy volunteers: a placebo-controlled study on the onset and duration of effects, Aliment. Pharmacol. Ther., 18, 495, 10.1046/j.1365-2036.2003.01708.x Goossens, 2006, The effect of a probiotic drink with Lactobacillus plantarum 299v on the bacterial composition in faeces and mucosal biopsies of rectum and ascending colon, Aliment. Pharmacol. Ther., 23, 255, 10.1111/j.1365-2036.2006.02749.x Guyonnet, 2009, Fermented milk containing Bifidobacterium lactis DN-173 010 improves gastrointestinal well-being and digestive symptoms in women reporting minor digestive symptoms: a randomised, double-blind, parallel, controlled study, Br. J. Nutr., 102, 1654, 10.1017/S0007114509990882 Haarman, 2005, Quantitative real-time PCR assays to identify and quantify fecal Bifidobacterium species in infants receiving a prebiotic infant formula, Appl. Environ. Microbiol., 71, 2318, 10.1128/AEM.71.5.2318-2324.2005 Hanifi, 2015, Evaluation of Bacillus subtilis R0179 on gastrointestinal viability and general wellness: a randomised, double-blind, placebo-controlled trial in healthy adults, Benef. Microbes, 6, 19, 10.3920/BM2014.0031 He, 2001, Differences in composition and mucosal adhesion of bifidobacteria isolated from healthy adults and healthy seniors, Curr. Microbiol., 43, 351, 10.1007/s002840010315 Hecht, 2014, A simple cage-autonomous method for the maintenance of the barrier status of germ-free mice during experimentation, Lab. Anim., 48, 292, 10.1177/0023677214544728 Hegarty, 2017, Lack of Heterogeneity in Bacteriocin Production Across a Selection of Commercial Probiotic Products, Probiotics Antimicrob. Proteins, 9, 459, 10.1007/s12602-017-9326-2 Herbel, 2013, Species-specific quantification of probiotic lactobacilli in yoghurt by quantitative real-time PCR, J. Appl. Microbiol., 115, 1402, 10.1111/jam.12341 Honeycutt, 2007, Probiotic administration and the incidence of nosocomial infection in pediatric intensive care: a randomized placebo-controlled trial, Pediatr. Crit. Care Med., 8, 452, 10.1097/01.PCC.0000282176.41134.E6 2012, Structure, function and diversity of the healthy human microbiome, Nature, 486, 207, 10.1038/nature11234 Hyatt, 2010, Prodigal: prokaryotic gene recognition and translation initiation site identification, BMC Bioinformatics, 11, 119, 10.1186/1471-2105-11-119 Jacobsen, 1999, Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans, Appl. Environ. Microbiol., 65, 4949, 10.1128/AEM.65.11.4949-4956.1999 Kanehisa, 2000, KEGG: kyoto encyclopedia of genes and genomes, Nucleic Acids Res., 28, 27, 10.1093/nar/28.1.27 Kaushik, 2009, Functional and probiotic attributes of an indigenous isolate of Lactobacillus plantarum, PLoS ONE, 4, e8099, 10.1371/journal.pone.0008099 Kristensen, 2016, Alterations in fecal microbiota composition by probiotic supplementation in healthy adults: a systematic review of randomized controlled trials, Genome Med., 8, 52, 10.1186/s13073-016-0300-5 Lahti, 2013, Associations between the human intestinal microbiota, Lactobacillus rhamnosus GG and serum lipids indicated by integrated analysis of high-throughput profiling data, PeerJ, 1, e32, 10.7717/peerj.32 Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nat. Methods, 9, 357, 10.1038/nmeth.1923 Laursen, 2017, Administration of two probiotic strains during early childhood does not affect the endogenous gut microbiota composition despite probiotic proliferation, BMC Microbiol., 17, 175, 10.1186/s12866-017-1090-7 Lee, 2000, Quantitative approach in the study of adhesion of lactic acid bacteria to intestinal cells and their competition with enterobacteria, Appl. Environ. Microbiol., 66, 3692, 10.1128/AEM.66.9.3692-3697.2000 Li, 2017, A comparison of per sample global scaling and per gene normalization methods for differential expression analysis of RNA-seq data, PLoS ONE, 12, e0176185, 10.1371/journal.pone.0176185 Maldonado-Gómez, 2016, Stable Engraftment of Bifidobacterium longum AH1206 in the Human Gut Depends on Individualized Features of the Resident Microbiome, Cell Host Microbe, 20, 515, 10.1016/j.chom.2016.09.001 Manor, 2017, Revised computational metagenomic processing uncovers hidden and biologically meaningful functional variation in the human microbiome, Microbiome, 5, 19, 10.1186/s40168-017-0231-4 Martin, 2008, Probiotic modulation of symbiotic gut microbial-host metabolic interactions in a humanized microbiome mouse model, Mol. Syst. Biol., 4, 157, 10.1038/msb4100190 McKean, 2017, Probiotics and Subclinical Psychological Symptoms in Healthy Participants: A Systematic Review and Meta-Analysis, J. Altern. Complement. Med., 23, 249, 10.1089/acm.2016.0023 McNulty, 2011, The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins, Sci. Transl. Med., 3, 106ra106, 10.1126/scitranslmed.3002701 Mowat, 2014, Regional specialization within the intestinal immune system, Nat. Rev. Immunol., 14, 667, 10.1038/nri3738 O’Brien, 2013, Impact of colonoscopy bowel preparation on intestinal microbiota, PLoS ONE, 8, e62815, 10.1371/journal.pone.0062815 Ouwehand, 2002, Probiotics: an overview of beneficial effects, Antonie van Leeuwenhoek, 82, 279, 10.1023/A:1020620607611 Panigrahi, 2017, A randomized synbiotic trial to prevent sepsis among infants in rural India, Nature, 548, 407, 10.1038/nature23480 Peng, 2012, IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth, Bioinformatics, 28, 1420, 10.1093/bioinformatics/bts174 Qin, 2010, A human gut microbial gene catalogue established by metagenomic sequencing, Nature, 464, 59, 10.1038/nature08821 Rijkers, 2011, Health benefits and health claims of probiotics: bridging science and marketing, Br. J. Nutr., 106, 1291, 10.1017/S000711451100287X Rochet, 2006, Effects of orally administered Lactobacillus casei DN-114 001 on the composition or activities of the dominant faecal microbiota in healthy humans, Br. J. Nutr., 95, 421, 10.1079/BJN20051625 Rondanelli, 2017, Using probiotics in clinical practice: Where are we now? A review of existing meta-analyses, Gut Microbes, 8, 521, 10.1080/19490976.2017.1345414 Ruggirello, 2014, Detection and viability of Lactococcus lactis throughout cheese ripening, PLoS ONE, 9, e114280, 10.1371/journal.pone.0114280 Saldanha, 2008, US Food and Drug Administration regulations governing label claims for food products, including probiotics, Clin. Infect. Dis., 46, 10.1086/523328 Schwendimann, 2015, Development of a quantitative PCR assay for rapid detection of Lactobacillus plantarum and Lactobacillus fermentum in cocoa bean fermentation, J. Microbiol. Methods, 115, 94, 10.1016/j.mimet.2015.05.022 Senok, 2005, Probiotics: facts and myths, Clin. Microbiol. Infect., 11, 958, 10.1111/j.1469-0691.2005.01228.x Sharon, 2013, Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization, Genome Res., 23, 111, 10.1101/gr.142315.112 Sharon, 2015, Accurate, multi-kb reads resolve complex populations and detect rare microorganisms, Genome Res., 25, 534, 10.1101/gr.183012.114 Sierra, 2010, Intestinal and immunological effects of daily oral administration of Lactobacillus salivarius CECT5713 to healthy adults, Anaerobe, 16, 195, 10.1016/j.anaerobe.2010.02.001 Suez, 2014, Artificial sweeteners induce glucose intolerance by altering the gut microbiota, Nature, 514, 181, 10.1038/nature13793 Suez, 2018, Post-Antibiotic Gut Mucosal Microbiome Reconstitution Is Impaired by Probiotics and Improved by Autologous FMT, Cell, 174, 1406, 10.1016/j.cell.2018.08.047 Sun, 2016, Glucose- and glycaemic factor-lowering effects of probiotics on diabetes: a meta-analysis of randomised placebo-controlled trials, Br. J. Nutr., 115, 1167, 10.1017/S0007114516000076 Tannock, 2000, Analysis of the fecal microflora of human subjects consuming a probiotic product containing Lactobacillus rhamnosus DR20, Appl. Environ. Microbiol., 66, 2578, 10.1128/AEM.66.6.2578-2588.2000 Truong, 2015, MetaPhlAn2 for enhanced metagenomic taxonomic profiling, Nat. Methods, 12, 902, 10.1038/nmeth.3589 Tuomola, 2001, Quality assurance criteria for probiotic bacteria, Am. J. Clin. Nutr., 73, 393S, 10.1093/ajcn/73.2.393s Turroni, 2013, Role of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in modulating bacterium-host interactions, Proc. Natl. Acad. Sci. USA, 110, 11151, 10.1073/pnas.1303897110 Van Tassell, 2011, Lactobacillus adhesion to mucus, Nutrients, 3, 613, 10.3390/nu3050613 Vogel, 2008, Clinical Trials. Deaths prompt a review of experimental probiotic therapy, Science, 319, 557, 10.1126/science.319.5863.557a Wang, 2015, Intestinal Microbiota Profiles of Healthy Pre-School and School-Age Children and Effects of Probiotic Supplementation, Ann. Nutr. Metab., 67, 257, 10.1159/000441066 Yang, 2016, Uncovering the composition of microbial community structure and metagenomics among three gut locations in pigs with distinct fatness, Sci. Rep., 6, 27427, 10.1038/srep27427 Yuan, 2017, Efficacy of Bifidobacterium infantis 35624 in patients with irritable bowel syndrome: a meta-analysis, Curr. Med. Res. Opin., 33, 1191, 10.1080/03007995.2017.1292230 Zeevi, 2015, Personalized Nutrition by Prediction of Glycemic Responses, Cell, 163, 1079, 10.1016/j.cell.2015.11.001 Zhang, 2015, Effect of probiotics on body weight and body-mass index: a systematic review and meta-analysis of randomized, controlled trials, Int. J. Food Sci. Nutr., 67, 571, 10.1080/09637486.2016.1181156 Zmora, 2016, Taking it Personally: Personalized Utilization of the Human Microbiome in Health and Disease, Cell Host Microbe, 19, 12, 10.1016/j.chom.2015.12.016