Metagenomic and metabolomic analysis of the toxic effects of trichloroacetamide-induced gut microbiome and urine metabolome perturbations in mice

Journal of Proteome Research

Volumn 14, Issue 4, 2015, Pages 1752-1761

  Zhang, Yan ^a   Zhao, Fuzheng ^a   Deng, Yongfeng ^a   Zhao, Yanping ^a   Ren, Hongqiang ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

gut microbiome; health risk; metabolome; mice; Trichloroacetamide

Indexed keywords

ACETAMIDE DERIVATIVE; TRICHLOROACETAMIDE; UNCLASSIFIED DRUG; CHLOROACETIC ACID; DISINFECTANT AGENT; WATER POLLUTANT;

ADULT; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; DRUG EXPOSURE; HEALTH HAZARD; HIGH THROUGHPUT SEQUENCING; INTESTINE FLORA; INTESTINE FUNCTION; MALE; METABOLOME; METABOLOMICS; METAGENOMICS; MICROBIOME; MOUSE; MUS MUSCULUS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; URINALYSIS; URINE; ANIMAL; DRUG EFFECTS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROCEDURES; RISK ASSESSMENT; TOXICITY; WATER POLLUTANT;

MUS; MUS MUSCULUS;

ACETAMIDES; ANIMALS; BASE SEQUENCE; CHLOROACETATES; DISINFECTANTS; GASTROINTESTINAL MICROBIOME; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MAGNETIC RESONANCE SPECTROSCOPY; METABOLOME; METABOLOMICS; MICE; MOLECULAR SEQUENCE DATA; RISK ASSESSMENT; URINE; WATER POLLUTANTS, CHEMICAL;

EID: 84926466253     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr5011263     Document Type: Article

References (48)

1. Spor, A.; Koren, O.; Ley, R. Unravelling the effects of the environment and host genotype on the gut microbiome Nat. Rev. Microbiol. 2011, 9, 279-90
2. Choi, J. J.; Eum, S. Y.; Rampersaud, E.; Daunert, S.; Abreu, M. T.; Toborek, M. Exercise attenuates PCB-induced changes in the mouse gut microbiome Environ. Health Perspect. 2013, 121, 725-30
3. Liu, Y. H.; Li, Y. H.; Liu, K. Y.; Shen, J. Exposing to cadmium stress cause profound toxic effect on microbiota of the mice intestinal tract PLoS One 2014, 9, 9
4. Nurizzo, C.; Antonelli, M.; Profaizer, M.; Romele, L. By-products in surface and reclaimed water disinfected with various agents Desalination 2005, 176, 241-53
5. Cantor, K. P.; Lynch, C. F.; Hildesheim, M. E.; Dosemeci, M.; Lubin, J.; Alavanja, M.; Craun, G. Drinking water source and chlorination byproducts I. Risk of bladder cancer Epidemiology 1998, 9, 21-28
6. Villanueva, C. M.; Cantor, K. P.; Cordier, S.; Jaakkola, J. J. K.; King, W. D.; Lynch, C. F.; Porru, S.; Kogevinas, M. Disinfection byproducts and bladder cancer-A pooled analysis Epidemiology 2004, 15, 357-67
7. Hildesheim, M. E.; Cantor, K. P.; Lynch, C. F.; Dosemeci, M.; Lubin, J.; Alavanja, M.; Craun, G. Drinking water source and chlorination byproducts II. Risk of colon and rectal cancers Epidemiology 1998, 9, 29-35
8. George, S. E.; Nelson, G. M.; Swank, A. E.; Brooks, L. R.; Bailey, K.; George, M.; DeAngelo, A. The disinfection by-products dichloro-, dibromo-, and bromochloroacetic acid impact intestinal microflora and metabolism in Fischer 344 rats upon exposure in drinking water Toxicol. Sci. 2000, 56, 282-9
9. George, S. E.; Wolf, D. C.; Brooks, L. R.; Bailey, K. C.; Hooth, M. J.; Nelson, G. M. Changes in cecal microbial metabolism of rats induced by individual and a mixture of drinking water disinfection by-products Cancer Lett. 2004, 204, 15-21
10. Plewa, M. J.; Muellner, M. G.; Richardson, S. D.; Fasanot, F.; Buettner, K. M.; Woo, Y. T.; McKague, A. B.; Wagner, E. D. Occurrence, synthesis, and mammalian cell cytotoxicity and genotoxicity of haloacetamides: An emerging class of nitrogenous drinking water disinfection byproducts Environ. Sci. Technol. 2008, 42, 955-61
11. Plewa, M. J.; Wagner, E. D.; Jazwierska, P.; Richardson, S. D.; Chen, P. H.; McKague, A. B. Halonitromethane drinking water disinfection byproducts: chemical characterization and mammalian cell cytotoxicity and genotoxicity Environ. Sci. Technol. 2004, 38, 62-8
12. Zhang, Y.; Zhang, Z. Y.; Zhao, Y. P.; Cheng, S. P.; Ren, H. Q. Identifying health effects of exposure to trichloroacetamide using transcriptomics and metabonomics in mice (Mus musculus) Environ. Sci. Technol. 2013, 47, 2918-24
13. Tremaroli, V.; Backhed, F. Functional interactions between the gut microbiota and host metabolism Nature 2012, 489, 242-249
14. Holmes, E.; Li, J. V.; Marchesi, J. R.; Nicholson, J. K. Gut microbiota composition and activity in relation to host metabolic phenotype and disease risk Cell Metab. 2012, 16, 559-64
15. Nicholson, J. K.; Holmes, E.; Kinross, J.; Burcelin, R.; Gibson, G.; Jia, W.; Pettersson, S. Host-gut microbiota metabolic interactions Science 2012, 336, 1262-7
16. Wang, Z. N.; Klipfell, E.; Bennett, B. J.; Koeth, R.; Levison, B. S.; Dugar, B.; Feldstein, A. E.; Britt, E. B.; Fu, X. M.; Chung, Y. M.; Wu, Y. P.; Schauer, P.; Smith, J. D.; Allayee, H.; Tang, W. H. W.; DiDonato, J. A.; Lusis, A. J.; Hazen, S. L. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease Nature 2011, 472, 57-63
17. Swann, J. R.; Want, E. J.; Geier, F. M.; Spagou, K.; Wilson, I. D.; Sidaway, J. E.; Nicholson, J. K.; Holmes, E. Systemic gut microbial modulation of bile acid metabolism in host tissue compartments Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 4523-30
18. Lu, K.; Abo, R. P.; Schlieper, K. A.; Graffam, M. E.; Levine, S.; Wishnok, J. S.; Swenberg, J. A.; Tannenbaum, S. R.; Fox, J. G. Arsenic exposure perturbs the gut microbiome and its metabolic profile in mice: an integrated metagenomics and metabolomics analysis Environ. Health Perspect. 2014, 122, 284-91
19. Baugher, J. L.; Klaenhammer, T. R. Invited review: Application of omics tools to understanding probiotic functionality J. Dairy Sci. 2011, 94, 4753-65
20. Marcobal, A.; Kashyap, P. C.; Nelson, T. A.; Aronov, P. A.; Donia, M. S.; Spormann, A.; Fischbach, M. A.; Sonnenburg, J. L. A metabolomic view of how the human gut microbiota impacts the host metabolome using humanized and gnotobiotic mice ISME J. 2013, 7, 1933-43
21. Wang, Z.; Zhang, X. X.; Huang, K. L.; Miao, Y.; Shi, P.; Liu, B.; Long, C.; Li, A. M. Metagenomic profiling of antibiotic resistance genes and mobile genetic elements in a tannery wastewater treatment plant PLoS One 2013, 8, 9
22. Segata, N.; Waldron, L.; Ballarini, A.; Narasimhan, V.; Jousson, O.; Huttenhower, C. Metagenomic microbial community profiling using unique clade-specific marker genes Nat. Methods 2012, 9, 811-4
23. Jiang, N.; Yan, X.; Zhou, W.; Zhang, Q.; Chen, H.; Zhang, Y.; Zhang, X. NMR-based metabonomic investigations into the metabolic profile of the senescence-accelerated mouse J. Proteome Res. 2008, 7, 3678-86
24. Sommer, F.; Backhed, F. The gut microbiota-masters of host development and physiology Nat. Rev. Microbiol. 2013, 11, 227-38
25. Holmes, E.; Kinross, J.; Gibson, G. R.; Burcelin, R.; Jia, W.; Pettersson, S.; Nicholson, J. K. Therapeutic modulation of microbiota-host metabolic interactions Sci. Transl. Med. 2012, 4, 9
26. Vijay-Kumar, M.; Aitken, J. D.; Carvalho, F. A.; Cullender, T. C.; Mwangi, S.; Srinivasan, S.; Sitaraman, S. V.; Knight, R.; Ley, R. E.; Gewirtz, A. T. Metabolic syndrome and altered gut microbiota in mice lacking toll-like receptor 5 Science 2010, 328, 228-31
27. Henao-Mejia, J.; Elinav, E.; Jin, C. C.; Hao, L. M.; Mehal, W. Z.; Strowig, T.; Thaiss, C. A.; Kau, A. L.; Eisenbarth, S. C.; Jurczak, M. J.; Camporez, J. P.; Shulman, G. I.; Gordon, J. I.; Hoffman, H. M.; Flavell, R. A. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity Nature 2012, 482, 179-85
28. Tehrani, A. B.; Nezami, B. G.; Gewirtz, A.; Srinivasan, S. Obesity and its associated disease: a role for microbiota? Neurogastroenterol. Motil. 2012, 24, 305-11
29. Damman, C. J.; Miller, S. I.; Surawicz, C. M.; Zisman, T. L. The microbiome and inflammatory bowel disease: is there a therapeutic role for fecal microbiota transplantation? Am. J. Gastroenterol. 2012, 107, 1452-59
30. Dapito, D. H.; Mencin, A.; Gwak, G. Y.; Pradere, J. P.; Jang, M. K.; Mederacke, I.; Caviglia, J. M.; Khiabanian, H.; Adeyemi, A.; Bataller, R.; Lefkowitch, J. H.; Bower, M.; Friedman, R.; Sartor, R. B.; Rabadan, R.; Schwabe, R. F. Promotion of hepatocellular carcinoma by the intestinal microbiota and TLR4 Cancer Cell 2012, 21, 504-16
31. Flint, H. J. Obesity and the gut microbiota J. Clin. Gastroenterol. 2011, 45, S128-32
32. Turnbaugh, P. J.; Hamady, M.; Yatsunenko, T.; Cantarel, B. L.; Duncan, A.; Ley, R. E.; Sogin, M. L.; Jones, W. J.; Roe, B. A.; Affourtit, J. P.; Egholm, M.; Henrissat, B.; Heath, A. C.; Knight, R.; Gordon, J. I. A core gut microbiome in obese and lean twins Nature 2009, 457, 480-4
33. Craciun, S.; Balskus, E. P. Microbial conversion of choline to trimethylamine requires a glycyl radical enzyme Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 21307-12
34. Compare, D.; Coccoli, P.; Rocco, A.; Nardone, O. M.; De Maria, S.; Carteni, M.; Nardone, G. Gut-liver axis: the impact of gut microbiota on non alcoholic fatty liver disease Nutr. Metab. Carbiovasc. Dis. 2012, 22, 471-6
35. Schnabl, B.; Brenner, D. A. Interactions between the intestinal microbiome and liver diseases Gastroenterology 2014, 146, 1513-24
36. Larrosa, M.; Luceri, C.; Vivoli, E.; Pagliuca, C.; Lodovici, M.; Moneti, G.; Dolara, P. Polyphenol metabolites from colonic microbiota exert anti-inflammatory activity on different inflammation models Mol. Nutr. Food Res. 2009, 53, 1044-54
37. Ott, S. J.; Musfeldt, M.; Wenderoth, D. F.; Hampe, J.; Brant, O.; Folsch, U. R.; Timmins, K. N.; Schreiber, S. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease Gut 2004, 53, 685-93
38. Sartor, R. B. Microbial influences in inflammatory bowel diseases Gastroenterology 2008, 134, 577-94
39. Li, M.; Wang, B. H.; Zhang, M. H.; Rantalainen, M.; Wang, S. Y.; Zhou, H. K.; Zhang, Y.; Shen, J.; Pang, X. Y.; Zhang, M. L.; Wei, H.; Chen, Y.; Lu, H. F.; Zuo, J.; Su, M. M.; Qiu, Y. P.; Jia, W.; Xiao, C. N.; Smith, L. M.; Yang, S. L.; Holmes, E.; Tang, H. R.; Zhao, G. P.; Nicholson, J. K.; Li, L. J.; Zhao, L. P. Symbiotic gut microbes modulate human metabolic phenotypes Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 2117-22
40. Nozawa, K.; Kawabata-Shoda, E.; Doihara, H.; Kojima, R.; Okada, H.; Mochizuki, S.; Sano, Y.; Inamura, K.; Matsushime, H.; Koizumi, T.; Yokoyama, T.; Ito, H. TRPA1 regulates gastrointestinal motility through serotonin release from enterochromaffin cells Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 3408-13
41. Le Gall, G.; Noor, S. O.; Ridgway, K.; Scovell, L.; Jamieson, C.; Johnson, I. T.; Colquhoun, I. J.; Kemsley, E. K.; Narbad, A. Metabolomics of fecal extracts detects altered metabolic activity of gut microbiota in ulcerative colitis and irritable bowel syndrome J. Proteome Res. 2011, 10, 4208-18
42. Keszthelyi, D.; Troost, F. J.; Masclee, A. A. M. Understanding the role of tryptophan and serotonin metabolism in gastrointestinal function Neurogastroenterol. Motil. 2009, 21, 1239-49
43. Kibe, R.; Kurihara, S.; Sakai, Y.; Suzuki, H.; Ooga, T.; Sawaki, E.; Muramatsu, K.; Nakamura, A.; Yamashita, A.; Kitada, Y.; Kakeyama, M.; Benno, Y.; Matsumoto, M. Upregulation of colonic luminal polyamines produced by intestinal microbiota delays senescence in mice Sci. Rep 2014, 4, 11
44. Gerner, E. W.; Meyskens, F. L. Polyamines and cancer: old molecules, new understanding Nat. Rev. Cancer 2004, 4, 781-792
45. Davila, A. M.; Blachier, F.; Gotteland, M.; Andriamihaja, M.; Benetti, P. H.; Sanz, Y.; Tome, D. Intestinal luminal nitrogen metabolism: role of the gut microbiota and consequences for the host Pharmacol. Res. 2013, 68, 95-107
46. Qian, Z. G.; Xia, X. X.; Lee, S. Y. Metabolic engineering of Escherichia coli for the production of cadaverine: a five carbon diamine Biotechnol. Bioeng. 2011, 108, 93-103
47. Lin, H. M.; Barnett, M. P. G.; Roy, N. C.; Joyce, N. I.; Zhu, S. T.; Armstrong, K.; Helsby, N. A.; Ferguson, L. R.; Rowan, D. D. Metabolomic analysis identifies inflammatory and noninflammatory metabolic effects of genetic modification in a mouse model of Crohns disease J. Proteome Res. 2010, 9, 1965-75
48. Hanfrey, C. C.; Pearson, B. M.; Hazeldine, S.; Lee, J.; Gaskin, D. J.; Woster, P. M.; Phillips, M. A.; Michael, A. J. Alternative spermidine biosynthetic route is critical for growth of Campylobacter jejuni and is the dominant polyamine pathway in human gut microbiota J. Biol. Chem. 2011, 286, 43301-12