Uncovering effects of antibiotics on the host and microbiota using transkingdom gene networks

Gut

Volumn 64, Issue 11, 2015, Pages 1732-1743

  Morgun, Andrey ^a,e   Dzutsev, Amiran ^b   Dong, Xiaoxi ^a   Greer, Renee L ^a   Sexton, D Joseph ^a   Ravel, Jacques ^c   Schuster, Martin ^a   Hsiao, William ^d   Matzinger, Polly ^e   Shulzhenko, Natalia ^a,e  

^a OREGON STATE UNIVERSITY   (United States)

^b FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; METRONIDAZOLE; NEOMYCIN; TRANSCRIPTOME; VANCOMYCIN; ANTIINFECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; CELL DEATH; CONTROLLED STUDY; DOWN REGULATION; EPITHELIUM CELL; GENE EXPRESSION; ILEUM; IMMUNE DEFICIENCY; IMMUNITY; IN VITRO STUDY; INTESTINE FLORA; METAGENOMICS; MITOCHONDRIAL GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUORUM SENSING; ANIMAL; C57BL MOUSE; DRUG EFFECTS; GENE REGULATORY NETWORK; GENETICS;

ANIMALS; ANTI-BACTERIAL AGENTS; GASTROINTESTINAL MICROBIOME; GENE REGULATORY NETWORKS; MICE; MICE, INBRED C57BL;

EID: 84947552418     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2014-308820     Document Type: Article

References (64)

1. Sharland M; SACAR Paediatric Subgroup. The use of antibacterials in children: a report of the Specialist Advisory Committee on Antimicrobial Resistance (SACAR) Paediatric Subgroup. J Antimicrob Chemother 2007;60(Suppl 1):i15-26.
2. European Commission. Antimicrobial resistance. Brussels, 2010.
3. Gustafson RH, Bowen RE. Antibiotic use in animal agriculture. J Appl Microbiol 1997;83:531-41.
4. Hempel S, Newberry SJ, Maher AR, et al. Probiotics for the prevention and treatment of antibiotic-associated diarrhea: a systematic review and meta-analysis. JAMA 2012;307:1959-69.
5. Dancer SJ. How antibiotics can make us sick: the less obvious adverse effects of antimicrobial chemotherapy. Lancet Infect Dis 2004;4:611-19.
6. Power SE, O'Toole PW, Stanton C, et al. Intestinal microbiota, diet and health. Br J Nutr 2014;111:387-402.
7. Cho I, Yamanishi S, Cox L, et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 2012;488:621-6.
8. Jernberg C, Lofmark S, Edlund C, et al. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J 2007;1:56-66.
9. Dethlefsen L, Huse S, Sogin ML, et al. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 2008;6:e280.
10. Antonopoulos DA, Huse SM, Morrison HG, et al. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect Immun 2009;77:2367-75.
11. Hill DA, Hoffmann C, Abt MC, et al. Metagenomic analyses reveal antibiotic-induced temporal and spatial changes in intestinal microbiota with associated alterations in immune cell homeostasis. Mucosal Immunol 2010;3:148-58.
12. Ubeda C, Taur Y, Jenq RR, et al. Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans. J Clin Invest 2010;120:4332-41.
13. Greer RL, Morgun A, Shulzhenko N. Bridging immunity and lipid metabolism by gut microbiota. J Allergy Clin Immunol 2013;132:253-62; quiz 63.
14. Bartlett JG. Clinical practice. Antibiotic-associated diarrhea. N Engl J Med 2002;346:334-9.
15. Cunha BA. Antibiotic side effects. Med Clin North Am 2001;85:149-85.
16. Hviid A, Svanstrom H, Frisch M. Antibiotic use and inflammatory bowel diseases in childhood. Gut 2011;60:49-54.
17. Mogg GA, Keighley MR, Burdon DW, et al. Antibiotic-associated colitis - a review of 66 cases. Br J Surg 1979;66:738-42.
18. Hill DA, Siracusa MC, Abt MC, et al. Commensal bacteria-derived signals regulate basophil hematopoiesis and allergic inflammation. Nat Med 2012;18:538-46.
19. Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet 2012;13:260-70.
20. Russell SL, Gold MJ, Hartmann M, et al. Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep 2012;13:440-7.
21. Cox LM, Yamanishi S, Sohn J, et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 2014;158:705-21.
22. Reeves AE, Theriot CM, Bergin IL, et al. The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile Infection. Gut Microbes 2011;2:145-58.
23. Brandl K, Plitas G, Mihu CN, et al. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 2008;455:804-7.
24. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, et al. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004;118:229-41.
25. Iida N, Dzutsev A, Stewart CA, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 2013;342:967-70.
26. Ridley EV, Wong AC, Douglas AE. Microbe-dependent and nonspecific effects of procedures to eliminate the resident microbiota from Drosophila melanogaster. Appl Environ Microbiol 2013;79:3209-14.
27. Shulzhenko N, Morgun A, Hsiao W, et al. Crosstalk between B lymphocytes, microbiota and the intestinal epithelium governs immunity versus metabolism in the gut. Nat Med 2011;17:1585-93.
28. Hall JA, Bouladoux N, Sun CM, et al. Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses. Immunity 2008;29:637-49.
29. Chappert P, Bouladoux N, Naik S, et al. Specific gut commensal flora locally alters T cell tuning to endogenous ligands. Immunity 2013;38:1198-210.
30. Kuss SK, Best GT, Etheredge CA, et al. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science 2011;334:249-52.
31. Ayres JS, Trinidad NJ, Vance RE. Lethal inflammasome activation by a multidrug-resistant pathobiont upon antibiotic disruption of the microbiota. Nat Med 2012;18:799-806.
32. Kirkland D, Benson A, Mirpuri J, et al. B cell-intrinsic MyD88 signaling prevents the lethal dissemination of commensal bacteria during colonic damage. Immunity 2012;36:228-38.
33. Schatz MC, Phillippy AM, Gajer P, et al. Integrated microbial survey analysis of prokaryotic communities for the PhyloChip microarray. Appl Environ Microbiol 2010;76:5636-8.
34. Ivanov II, Atarashi K, Manel N, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009;139:485-98.
35. Mine KL, Shulzhenko N, Yambartsev A, et al. Gene network reconstruction reveals cell cycle and antiviral genes as major drivers of cervical cancer. Nat Commun 2013;4:1806.
36. Kalghatgi S, Spina CS, Costello JC, et al. Bactericidal antibiotics induce mitochondrial dysfunction and oxidative damage in mammalian cells. Sci Transl Med 2013;5:192ra85.
37. Williams TA, Foster PG, Cox CJ, et al. An archaeal origin of eukaryotes supports only two primary domains of life. Nature 2013;504:231-6.
38. Hibbing ME, Fuqua C, Parsek MR, et al. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 2010;8:15-25.
39. Overbeek R, Begley T, Butler RM, et al. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 2005;33:5691-702.
40. Aziz RK, Bartels D, Best AA, et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008;9:75.
41. Prifti E, Zucker JD, Clement K, et al. Interactional and functional centrality in transcriptional co-expression networks. Bioinformatics 2010;26:3083-9.
42. McDermott JE, Diamond DL, Corley C, et al. Topological analysis of protein co-abundance networks identifies novel host targets important for HCV infection and pathogenesis. BMC Syst Biol 2012;6:28.
43. Sadikot RT, Blackwell TS, Christman JW, et al. Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am J Respir Crit Care Med 2005;171:1209-23.
44. Babrowski T, Romanowski K, Fink D, et al. The intestinal environment of surgical injury transforms Pseudomonas aeruginosa into a discrete hypervirulent morphotype capable of causing lethal peritonitis. Surgery 2013;153:36-43.
45. Rampioni G, Schuster M, Greenberg EP, et al. Contribution of the RsaL global regulator to Pseudomonas aeruginosa virulence and biofilm formation. FEMS Microbiol Lett 2009;301:210-17.
46. Schuster M, Sexton DJ, Diggle SP, et al. Acyl-homoserine lactone quorum sensing: from evolution to application. Annu Rev Microbiol 2013;67:43-63.
47. Mellbye B, Schuster M. Physiological framework for the regulation of quorum sensing-dependent public goods in Pseudomonas aeruginosa. J Bacteriol 2014;196:1155-64.
48. Jimenez PN, Koch G, Thompson JA, et al. The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 2012;76:46-65.
49. Ubeda C, Pamer EG. Antibiotics, microbiota, and immune defense. Trends Immunol 2012;33:459-66.
50. Reikvam DH, Erofeev A, Sandvik A, et al. Depletion of murine intestinal microbiota: effects on gut mucosa and epithelial gene expression. PLoS ONE 2011;6:e17996.
51. Hapfelmeier S, Lawson MA, Slack E, et al. Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science 2010;328:1705-9.
52. Cauley LS, Lefrancois L. Guarding the perimeter: protection of the mucosa by tissue-resident memory T cells. Mucosal Immunol 2013;6:14-23.
53. Mazzucchelli L, Hauser C, Zgraggen K, et al. Differential in situ expression of the genes encoding the chemokines MCP-1 and RANTES in human inflammatory bowel disease. J Pathol 1996;178:201-6.
54. Agace WW, Roberts AI, Wu L, et al. Human intestinal lamina propria and intraepithelial lymphocytes express receptors specific for chemokines induced by inflammation. Eur J Immunol 2000;30:819-26.
55. Barnhill AE, Brewer MT, Carlson SA. Adverse effects of antimicrobials via predictable or idiosyncratic inhibition of host mitochondrial components. Antimicrob Agents Chemother 2012;56:4046-51.
56. Murano K, Okuwaki M, Hisaoka M, et al. Transcription regulation of the rRNA gene by a multifunctional nucleolar protein, B23/nucleophosmin, through its histone chaperone activity. Mol Cell Biol 2008;28:3114-26.
57. Franzosa EA, Morgan XC, Segata N, et al. Relating the metatranscriptome and metagenome of the human gut. Proc Natl Acad Sci U S A 2014;111:E2329-38.
58. Pe'er D, Hacohen N. Principles and strategies for developing network models in cancer. Cell 2011;144:864-73.
59. Lefebvre C, Rieckhof G, Califano A. Reverse-engineering human regulatory networks. Wiley Interdiscip Rev Syst Biol Med 2012;4:311-25.
60. Skinner J, Kotliarov Y, Varma S, et al. Construct and compare gene coexpression networks with DAPfinder and DAPview. BMC Bioinformatics 2011;12:286.
61. Mahajan-Miklos S, Tan MW, Rahme LG, et al. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 1999;96:47-56.
62. Jendrossek V, Grassme H, Mueller I, et al. Pseudomonas aeruginosa-induced apoptosis involves mitochondria and stress-activated protein kinases. Infect Immun 2001;69:2675-83.
63. Ochoa-Reparaz J, Mielcarz DW, Ditrio LE, et al. Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis. J Immunol 2009;183:6041-50.
64. Dong X, Yambartsev A, Ramsey S, et al. Reverse enGENEering of regulatory networks from Big Data: a simple guide for biologist. Bioinform Biol Insights 2015. In press.