Site-specific programming of the host epithelial transcriptome by the gut microbiota

Genome Biology

Volumn 16, Issue 1, 2015, Pages

  Sommer, Felix ^a   Nookaew, Intawat ^b,c   Sommer, Nina ^a   Fogelstrand, Per ^a   Bäckhed, Fredrik ^a,d  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^c OAK RIDGE NATIONAL LABORATORY   (United States)

^d Capital Region   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANATOMICAL VARIATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASCENDING COLON; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; FEMALE; GENE EXPRESSION; ILEUM; IMMUNE RESPONSE; INTESTINE CRYPT; INTESTINE EPITHELIUM; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; LASER CAPTURE MICRODISSECTION; METABOLISM; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; ANIMAL; EPITHELIUM CELL; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; GENETICS; IMMUNE SYSTEM; IMMUNOLOGY; MICROBIOLOGY; MICROFLORA; SIGNAL TRANSDUCTION;

MUS;

TRANSCRIPTOME;

ANIMALS; EPITHELIAL CELLS; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; IMMUNE SYSTEM; MICE; MICROARRAY ANALYSIS; MICROBIOTA; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

EID: 84939163442     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-015-0614-4     Document Type: Article

References (62)

1. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207-14.
2. Human Microbiome Project Consortium. A framework for human microbiome research. Nature. 2012;486:215-21.
3. Li J, Jia H, Cai X, Zhong H, Feng Q, Sunagawa S, et al. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol. 2014;32:834-41.
4. Sommer F, Backhed F. The gut microbiota - masters of host development and physiology. Nat Rev Microbiol. 2013;11:227-38.
5. Karlsson FH, Fåk F, Nookaew I, Tremaroli V, Fagerberg B, Petranovic D, et al. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat Commun. 2012;3:1245.
6. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022-3.
7. Ott SJ, Musfeldt M, Wenderoth DF, Hampe J, Brant O, Folsch UR, et al. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut. 2004;53:685-93.
8. Sekirov I, Russell SL, Antunes LC, Finlay BB. Gut microbiota in health and disease. Physiol Rev. 2010;90:859-904.
9. Kleerebezem M, Vaughan EE. Probiotic and gut lactobacilli and bifidobacteria: molecular approaches to study diversity and activity. Annu Rev Microbiol. 2009;63:269-90.
10. Medema JP, Vermeulen L. Microenvironmental regulation of stem cells in intestinal homeostasis and cancer. Nature. 2011;474:318-26.
11. El Aidy S, Derrien M, Merrifield CA, Levenez F, Dore J, Boekschoten MV, et al. Gut bacteria-host metabolic interplay during conventionalisation of the mouse germfree colon. ISME J. 2013;7:743-55.
12. Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, Mulder I, Lan A, Bridonneau C, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity. 2009;31:677-89.
13. El Aidy S, Merrifield CA, Derrien M, van Baarlen P, Hooiveld G, Levenez F, et al. The gut microbiota elicits a profound metabolic reorientation in the mouse jejunal mucosa during conventionalisation. Gut. 2013;62:1306-14.
14. El Aidy S, van Baarlen P, Derrien M, Lindenbergh-Kortleve DJ, Hooiveld G, Levenez F, et al. Temporal and spatial interplay of microbiota and intestinal mucosa drive establishment of immune homeostasis in conventionalized mice. Mucosal Immunol. 2012;5:567-79.
15. Larsson E, Tremaroli V, Lee YS, Koren O, Nookaew I, Fricker A, et al. Analysis of gut microbial regulation of host gene expression along the length of the gut and regulation of gut microbial ecology through MyD88. Gut. 2012;61:1124-31.
16. Kijani S, Yrlid U, Heyden M, Levin M, Boren J, Fogelstrand P. Filter-dense multicolor microscopy. PLoS One. 2015;10, e0119499.
17. Abrams GD, Bauer H, Sprinz H. Influence of the normal flora on mucosal morphology and cellular renewal in the ileum. A comparison of germ-free and conventional mice. Lab Invest. 1963;12:355-64.
18. den Hollander J, Rimpi S, Doherty JR, Rudelius M, Buck A, Hoellein A, et al. Aurora kinases A and B are up-regulated by Myc and are essential for maintenance of the malignant state. Blood. 2010;116:1498-505.
19. Haugwitz U, Wasner M, Wiedmann M, Spiesbach K, Rother K, Mossner J, et al. A single cell cycle genes homology region (CHR) controls cell cycle-dependent transcription of the cdc25C phosphatase gene and is able to cooperate with E2F or Sp1/3 sites. Nucleic Acids Res. 2002;30:1967-76.
20. Ngo CV, Gee M, Akhtar N, Yu D, Volpert O, Auerbach R, et al. An in vivo function for the transforming Myc protein: elicitation of the angiogenic phenotype. Cell Growth Differ. 2000;11:201-10.
21. Rogoff HA, Pickering MT, Frame FM, Debatis ME, Sanchez Y, Jones S, et al. Apoptosis associated with deregulated E2F activity is dependent on E2F1 and Atm/Nbs1/Chk2. Mol Cell Biol. 2004;24:2968-77.
22. Stanelle J, Stiewe T, Theseling CC, Peter M, Putzer BM. Gene expression changes in response to E2F1 activation. Nucleic Acids Res. 2002;30:1859-67.
23. Yan Z, DeGregori J, Shohet R, Leone G, Stillman B, Nevins JR, et al. Cdc6 is regulated by E2F and is essential for DNA replication in mammalian cells. Proc Natl Acad Sci U S A. 1998;95:3603-8.
24. Zeller KI, Zhao X, Lee CW, Chiu KP, Yao F, Yustein JT, et al. Global mapping of c-Myc binding sites and target gene networks in human B cells. Proc Natl Acad Sci U S A. 2006;103:17834-9.
25. Bruno ME, Frantz AL, Rogier EW, Johansen FE, Kaetzel CS. Regulation of the polymeric immunoglobulin receptor by the classical and alternative NF-kappaB pathways in intestinal epithelial cells. Mucosal Immunol. 2011;4:468-78.
26. Chen L, Yang G, Zhang X, Wu J, Gu Q, Wei M, et al. Induction of MIF expression by oxidized LDL via activation of NF-kappaB in vascular smooth muscle cells. Atherosclerosis. 2009;207:428-33.
27. Cho ML, Moon YM, Heo YJ, Woo YJ, Ju JH, Park KS, et al. NF-kappaB inhibition leads to increased synthesis and secretion of MIF in human CD4+ T cells. Immunol Lett. 2009;123:21-30.
28. Dommels YE, Butts CA, Zhu S, Davy M, Martell S, Hedderley D, et al. Characterization of intestinal inflammation and identification of related gene expression changes in mdr1a(-/-) mice. Genes Nutr. 2007;2:209-23.
29. Ruffell D, Mourkioti F, Gambardella A, Kirstetter P, Lopez RG, Rosenthal N, et al. A CREB-C/EBPbeta cascade induces M2 macrophage-specific gene expression and promotes muscle injury repair. Proc Natl Acad Sci U S A. 2009;106:17475-80.
30. Sommer F, Backhed F. The gut microbiota engages different signaling pathways to induce Duox2 expression in the ileum and colon epithelium. Mucosal Immunol. 2015;8:372-9.
31. Takenouchi-Ohkubo N, Takahashi T, Tsuchiya M, Mestecky J, Moldoveanu Z, Moro I. Role of nuclear factor-kappaB in the expression by tumor necrosis factor-alpha of the human polymeric immunoglobulin receptor (plgR) gene. Immunogenetics. 2000;51:289-95.
32. Consortium EP. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57-74.
33. Obach M, Navarro-Sabate A, Caro J, Kong X, Duran J, Gomez M, et al. 6-Phosphofructo-2-kinase (pfkfb3) gene promoter contains hypoxia-inducible factor-1 binding sites necessary for transactivation in response to hypoxia. J Biol Chem. 2004;279:53562-70.
34. Wang J, Zhuang J, Iyer S, Lin X, Whitfield TW, Greven MC, et al. Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res. 2012;22:1798-812.
35. Wang ND, Finegold MJ, Bradley A, Ou CN, Abdelsayed SV, Wilde MD, et al. Impaired energy homeostasis in C/EBP alpha knockout mice. Science. 1995;269:1108-12.
36. Whitfield TW, Wang J, Collins PJ, Partridge EC, Aldred SF, Trinklein ND, et al. Functional analysis of transcription factor binding sites in human promoters. Genome Biol. 2012;13:R50.
37. Encyclopedia of gut microbiota regulated genes. http://microbiota.wall.gu.se .
38. Donohoe DR, Garge N, Zhang X, Sun W, O'Connell TM, Bunger MK, et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 2011;13:517-26.
39. Pott J, Stockinger S, Torow N, Smoczek A, Lindner C, McInerney G, et al. Age-dependent TLR3 expression of the intestinal epithelium contributes to rotavirus susceptibility. PLoS Pathog. 2012;8, e1002670.
40. Camp JG, Frank CL, Lickwar CR, Guturu H, Rube T, Wenger AM, et al. Microbiota modulate transcription in the intestinal epithelium without remodeling the accessible chromatin landscape. Genome Res. 2014;24:1504-16.
41. Kim TH, Li F, Ferreiro-Neira I, Ho LL, Luyten A, Nalapareddy K, et al. Broadly permissive intestinal chromatin underlies lateral inhibition and cell plasticity. Nature. 2014;506:511-5.
42. Geuking MB, Cahenzli J, Lawson MA, Ng DC, Slack E, Hapfelmeier S, et al. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity. 2011;34:794-806.
43. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A. 2004;101:15718-23.
44. Sayin SI, Wahlstrom A, Felin J, Jantti S, Marschall HU, Bamberg K, et al. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab. 2013;17:225-35.
45. Stappenbeck TS, Hooper LV, Gordon JI. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci U S A. 2002;99:15451-5.
46. Alenghat T, Osborne LC, Saenz SA, Kobuley D, Ziegler CG, Mullican SE, et al. Histone deacetylase 3 coordinates commensal-bacteria-dependent intestinal homeostasis. Nature. 2013;504:153-7.
47. 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.
48. Kellermayer R, Dowd SE, Harris RA, Balasa A, Schaible TD, Wolcott RD, et al. Colonic mucosal DNA methylation, immune response, and microbiome patterns in Toll-like receptor 2-knockout mice. FASEB J. 2011;25:1449-60.
49. Mischke M, Plosch T. More than just a gut instinct-the potential interplay between a baby's nutrition, its gut microbiome, and the epigenome. Am J Physiol Regul Integr Comp Physiol. 2013;304:R1065-9.
50. Leblond CP, Stevens CE. The constant renewal of the intestinal epithelium in the albino rat. Anat Rec. 1948;100:357-77.
51. Creamer B, Shorter RG, Bamforth J. The turnover and shedding of epithelial cells I. The turnover in the gastro-intestinal tract. Gut. 1961;2:110-8.
52. Hansson GC. Role of mucus layers in gut infection and inflammation. Curr Opin Microbiol. 2012;15:57-62.
53. Sommer F, Adam N, Johansson MEV, Xia L, Hansson GC, Bäckhed F. Altered mucus glycosylation in core 1 O-glycan-deficient mice affects microbiota composition and intestinal architecture. PLoS One. 2014;9, e85254.
54. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3:1-25.
55. Wilkerson MD, Hayes DN. ConsensusClusterPlus: a class discovery tool with confidence assessments and item tracking. Bioinformatics. 2010;26:1572-3.
56. Zambelli F, Prazzoli GM, Pesole G, Pavesi G. Cscan: finding common regulators of a set of genes by using a collection of genome-wide ChIP-seq datasets. Nucleic Acids Res. 2012;40:W510-5.
57. Loots G, Ovcharenko I. ECRbase: database of evolutionary conserved regions, promoters, and transcription factor binding sites in vertebrate genomes. Bioinformatics. 2007;23:122-4.
58. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell. 2007;27:91-105.
59. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009;19:92-105.
60. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human MicroRNA targets. PLoS Biol. 2004;2, e363.
61. Betel D, Wilson M, Gabow A, Marks DS, Sander C. The microRNA.org resource: targets and expression. Nucleic Acids Res. 2008;36:D149-53.
62. Varemo L, Nielsen J, Nookaew I. Enriching the gene set analysis of genome-wide data by incorporating directionality of gene expression and combining statistical hypotheses and methods. Nucleic Acids Res. 2013;41:4378-91.