Modulation of a Circulating Uremic Solute via Rational Genetic Manipulation of the Gut Microbiota

Cell Host and Microbe

Volumn 20, Issue 6, 2016, Pages 709-715

  Devlin, A Sloan ^a,d   Marcobal, Angela ^b   Dodd, Dylan ^b   Nayfach, Stephen ^a   Plummer, Natalie ^c   Meyer, Tim ^c   Pollard, Katherine S ^a   Sonnenburg, Justin L ^b   Fischbach, Michael A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c STANFORD UNIVERSITY   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Bacteroides; chronic kidney disease; genetic engineering; human microbiome; indoxyl sulfate; tryptophanase

Indexed keywords

AMMONIA; ERYTHROMYCIN; INDICAN; INDOLE; PYRIDOXAL 5 PHOSPHATE; PYRUVIC ACID; TRYPTOPHAN; TRYPTOPHANASE; INDOLE DERIVATIVE; TOXIN; UREMIA MIDDLE MOLECULE TOXINS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL COUNT; BACTERIAL GENOME; BACTEROIDES; BACTEROIDES CACCAE; BACTEROIDES THETAIOTAOMICRON; CLOSTRIDIUM; CLOSTRIDIUM SCINDENS; CONTROLLED STUDY; EDWARDSIELLA TARDA; ENTEROCOCCUS FAECALIS; GENE DELETION; GENETIC MANIPULATION; GNOTOBIOTICS; IN VITRO STUDY; INTESTINE FLORA; MOUSE; NONHUMAN; POPULATION ABUNDANCE; PRIORITY JOURNAL; PROVIDENCIA STUARTII; UREMIA; ANIMAL; ANIMAL FOOD; BACTERIUM; BIOSYNTHESIS; CHRONIC KIDNEY FAILURE; DIET; DISEASE COURSE; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; GASTROINTESTINAL TRACT; GENETIC ENGINEERING; GENETICS; GERMFREE ANIMAL; HUMAN; METABOLISM; METAGENOME; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; URINE;

ANIMAL FEED; ANIMALS; BACTERIA; BACTEROIDES; DIET; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; GENETIC ENGINEERING; GERM-FREE LIFE; HUMANS; INDICAN; INDOLES; METAGENOME; MICE; MICROBIOTA; RENAL INSUFFICIENCY, CHRONIC; TOXINS, BIOLOGICAL; TRYPTOPHAN; TRYPTOPHANASE;

EID: 85006117379     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2016.10.021     Document Type: Article

References (45)

1. Adijiang, A., Goto, S., Uramoto, S., Nishijima, F., Niwa, T., Indoxyl sulphate promotes aortic calcification with expression of osteoblast-specific proteins in hypertensive rats. Nephrol. Dial. Transplant. 23 (2008), 1892–1901.
2. Banoglu, E., King, R.S., Sulfation of indoxyl by human and rat aryl (phenol) sulfotransferases to form indoxyl sulfate. Eur. J. Drug Metab. Pharmacokinet. 27 (2002), 135–140.
3. Banoglu, E., Jha, G.G., King, R.S., Hepatic microsomal metabolism of indole to indoxyl, a precursor of indoxyl sulfate. Eur. J. Drug Metab. Pharmacokinet. 26 (2001), 235–240.
4. Barreto, F.C., Barreto, D.V., Liabeuf, S., Meert, N., Glorieux, G., Temmar, M., Choukroun, G., Vanholder, R., Massy, Z.A., European Uremic Toxin Work Group (EUTox). Serum indoxyl sulfate is associated with vascular disease and mortality in chronic kidney disease patients. Clin. J. Am. Soc. Nephrol. 4 (2009), 1551–1558.
5. Cao, X.-S., Chen, J., Zou, J.-Z., Zhong, Y.-H., Teng, J., Ji, J., Chen, Z.-W., Liu, Z.-H., Shen, B., Nie, Y.-X., et al. Association of indoxyl sulfate with heart failure among patients on hemodialysis. Clin. J. Am. Soc. Nephrol. 10 (2015), 111–119.
6. Carter, D., Einheber, A., Bauer, H., Rosen, H., Burns, W.F., The role of the microbial flora in uremia. II. Uremic colitis, cardiovascular lesions, and biochemical observations. J. Exp. Med. 123 (1966), 251–266.
7. Cato, E.P., Johnson, J.L., Reinstatement of species rank for Bacteroides fragilis, B. ovatus, B. distasonis, B. thetaiotaomicron, and B. vulgatus: designation of neotype strains for Bacteroides fragilis (Veillon and Zuber) Castellani and Chalmers and Bacteroides thetaiotaomicron (Distaso) Castellani and Chalmers. Int. J. Syst. Bacteriol. 26 (1976), 230–237.
8. Coresh, J., Byrd-Holt, D., Astor, B.C., Briggs, J.P., Eggers, P.W., Lacher, D.A., Hostetter, T.H., Chronic kidney disease awareness, prevalence, and trends among U.S. adults, 1999 to 2000. J. Am. Soc. Nephrol. 16 (2005), 180–188.
9. Duranton, F., Cohen, G., De Smet, R., Rodriguez, M., Jankowski, J., Vanholder, R., Argilés, A., European Uremic Toxin Work Group. Normal and pathologic concentrations of uremic toxins. J. Am. Soc. Nephrol. 23 (2012), 1258–1270.
10. Einheber, A., Carter, D., The role of the microbial flora in uremia. I. Survival times of germfree, limited-flora, and conventionalized rats after bilateral nephrectomy and fasting. J. Exp. Med. 123 (1966), 239–250.
11. Evenepoel, P., Meijers, B.K.I., Bammens, B.R.M., Verbeke, K., Uremic toxins originating from colonic microbial metabolism. Kidney Int. Suppl.(114), 2009, S12–S19.
12. Gillam, E.M.J., Notley, L.M., Cai, H., De Voss, J.J., Guengerich, F.P., Oxidation of indole by cytochrome P450 enzymes. Biochemistry 39 (2000), 13817–13824.
13. Holdeman, L.V., Cato, E.P., Moore, W., Anaerobe Laboratory Manual. 1977, Anaerobe Laboratory Virginia Polytechnic Institute and State University.
14. Johnson, J.L., Moore, W.E.C., Moore, L.V.H., Bacteroides caccae sp. nov., Bacteroides merdae sp. nov., and Bacteroides stercoris sp. nov. isolated from human feces. Int. J. Syst. Bacteriol. 36 (1986), 499–501.
15. Johnson, D.W., Craven, A.-M., Isbel, N.M., Modification of cardiovascular risk in hemodialysis patients: an evidence-based review. Hemodial. Int. 11 (2007), 1–14.
16. Kamada, N., Chen, G.Y., Inohara, N., Núñez, G., Control of pathogens and pathobionts by the gut microbiota. Nat. Immunol. 14 (2013), 685–690.
17. Kopple, J.D., Greene, T., Chumlea, W.C., Hollinger, D., Maroni, B.J., Merrill, D., Scherch, L.K., Schulman, G., Wang, S.-R., Zimmer, G.S., Relationship between nutritional status and the glomerular filtration rate: results from the MDRD study. Kidney Int. 57 (2000), 1688–1703.
18. Kotarski, S.F., Salyers, A.A., Isolation and characterization of outer membranes of Bacteroides thetaiotaomicron grown on different carbohydrates. J. Bacteriol. 158 (1984), 102–109.
19. Kraal, L., Abubucker, S., Kota, K., Fischbach, M.A., Mitreva, M., The prevalence of species and strains in the human microbiome: a resource for experimental efforts. PLoS ONE, 9, 2014, e97279.
20. Lee, J.-H., Lee, J., Indole as an intercellular signal in microbial communities. FEMS Microbiol. Rev. 34 (2010), 426–444.
21. Lombard, G.L., Dowell, V.R. Jr., Comparison of three reagents for detecting indole production by anaerobic bacteria in microtest systems. J. Clin. Microbiol. 18 (1983), 609–613.
22. Meyer, T.W., Hostetter, T.H., Uremia. N. Engl. J. Med. 357 (2007), 1316–1325.
23. Meyer, T.W., Hostetter, T.H., Uremic solutes from colon microbes. Kidney Int. 81 (2012), 949–954.
24. Nayfach, S., Fischbach, M.A., Pollard, K.S., MetaQuery: a web server for rapid annotation and quantitative analysis of specific genes in the human gut microbiome. Bioinformatics 31 (2015), 3368–3370.
25. Newton, W.A., Snell, E.E., Catalytic properties of tryptophanase, a multifunctional pyridoxal phosphate enzyme. Proc. Natl. Acad. Sci. USA 51 (1964), 382–389.
26. Niwa, T., Uremic toxicity of indoxyl sulfate. Nagoya J. Med. Sci. 72 (2010), 1–11.
27. Niwa, T., Ise, M., Indoxyl sulfate, a circulating uremic toxin, stimulates the progression of glomerular sclerosis. J. Lab. Clin. Med. 124 (1994), 96–104.
28. Niwa, T., Shimizu, H., Indoxyl sulfate induces nephrovascular senescence. J. Ren. Nutr. 22 (2012), 102–106.
29. Niwa, T., Takeda, N., Tatematsu, A., Maeda, K., Accumulation of indoxyl sulfate, an inhibitor of drug-binding, in uremic serum as demonstrated by internal-surface reversed-phase liquid chromatography. Clin. Chem. 34 (1988), 2264–2267.
30. Niwa, T., Ise, M., Miyazaki, T., Progression of glomerular sclerosis in experimental uremic rats by administration of indole, a precursor of indoxyl sulfate. Am. J. Nephrol. 14 (1994), 207–212.
31. Parfrey, P.S., Foley, R.N., The clinical epidemiology of cardiac disease in chronic renal failure. J. Am. Soc. Nephrol. 10 (1999), 1606–1615.
32. Patel, K.P., Luo, F.J.-G., Plummer, N.S., Hostetter, T.H., Meyer, T.W., The production of p-cresol sulfate and indoxyl sulfate in vegetarians versus omnivores. Clin. J. Am. Soc. Nephrol. 7 (2012), 982–988.
33. Poesen, R., Meijers, B., Evenepoel, P., The colon: an overlooked site for therapeutics in dialysis patients. Semin. Dial. 26 (2013), 323–332.
34. Rothhammer, V., Mascanfroni, I.D., Bunse, L., Takenaka, M.C., Kenison, J.E., Mayo, L., Chao, C.-C., Patel, B., Yan, R., Blain, M., et al. Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor. Nat. Med. 22 (2016), 586–597.
35. Schepers, E., Glorieux, G., Vanholder, R., The gut: the forgotten organ in uremia?. Blood Purif. 29 (2010), 130–136.
36. Shimada, Y., Kinoshita, M., Harada, K., Mizutani, M., Masahata, K., Kayama, H., Takeda, K., Commensal bacteria-dependent indole production enhances epithelial barrier function in the colon. PLoS ONE, 8, 2013, e80604.
37. Shivanna, S., Kolandaivelu, K., Shashar, M., Belghasim, M., Al-Rabadi, L., Balcells, M., Zhang, A., Weinberg, J., Francis, J., Pollastri, M.P., et al. The aryl hydrocarbon receptor is a critical regulator of tissue factor stability and an antithrombotic target in uremia. J. Am. Soc. Nephrol. 27 (2016), 189–201.
38. Shoji, T., Wada, A., Inoue, K., Hayashi, D., Tomida, K., Furumatsu, Y., Kaneko, T., Okada, N., Fukuhara, Y., Imai, E., Tsubakihara, Y., Prospective randomized study evaluating the efficacy of the spherical adsorptive carbon AST-120 in chronic kidney disease patients with moderate decrease in renal function. Nephron Clin. Pract. 105 (2007), c99–c107.
39. Sirich, T.L., Funk, B.A., Plummer, N.S., Hostetter, T.H., Meyer, T.W., Prominent accumulation in hemodialysis patients of solutes normally cleared by tubular secretion. J. Am. Soc. Nephrol. 25 (2014), 615–622.
40. Sonnenburg, E.D., Zheng, H., Joglekar, P., Higginbottom, S.K., Firbank, S.J., Bolam, D.N., Sonnenburg, J.L., Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell 141 (2010), 1241–1252.
41. Ueda, H., Shibahara, N., Takagi, S., Inoue, T., Katsuoka, Y., AST-120 treatment in pre-dialysis period affects the prognosis in patients on hemodialysis. Ren. Fail. 30 (2008), 856–860.
42. US Renal Data System (2015). USRDS Annual Data Report, https://www.usrds.org/adr.aspx.
43. Wikoff, W.R., Anfora, A.T., Liu, J., Schultz, P.G., Lesley, S.A., Peters, E.C., Siuzdak, G., Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc. Natl. Acad. Sci. USA 106 (2009), 3698–3703.
44. Wolfe, R.A., Ashby, V.B., Milford, E.L., Ojo, A.O., Ettenger, R.E., Agodoa, L.Y.C., Held, P.J., Port, F.K., Comparison of mortality in all patients on dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric transplant. N. Engl. J. Med. 341 (1999), 1725–1730.
45. Wu, I.-W., Hsu, K.-H., Lee, C.-C., Sun, C.-Y., Hsu, H.-J., Tsai, C.-J., Tzen, C.-Y., Wang, Y.-C., Lin, C.-Y., Wu, M.-S., p-Cresyl sulphate and indoxyl sulphate predict progression of chronic kidney disease. Nephrol. Dial. Transplant. 26 (2011), 938–947.