Transmission of atherosclerosis susceptibility with gut microbial transplantation

Journal of Biological Chemistry

Volumn 290, Issue 9, 2015, Pages 5647-5660

  Gregory, Jill C ^a,b   Buffa, Jennifer A ^a,b   Org, Elin ^d   Wang, Zeneng ^a,b   Levison, Bruce S ^a,b   Zhu, Weifei ^a,b   Wagner, Matthew A ^a,b   Bennett, Brian J ^e   Li, Lin ^a,b   DiDonato, Joseph A ^a,b   Lusis, Aldons J ^d   Hazen, Stanley L ^a,b,c  

^a Department of Cellular and Molecular Medicine ^*  (United States)

^b Center for Cardiovascular Diagnostics and Prevention   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; MAMMALS; METABOLISM; MICROORGANISMS; NUTRITION;

APOLIPOPROTEIN E; ATHEROSCLEROTIC LESIONS; ATHEROSCLEROTIC PLAQUE; MECHANISTIC LINK; MICROBIAL COMMUNITIES; MICROBIAL METABOLISM; THERAPEUTIC TARGETS; TRIMETHYLAMINE N OXIDES;

DISEASES;

APOLIPOPROTEIN E; CHOLINE; TRIMETHYLAMINE; TRIMETHYLAMINE OXIDE; METHYLAMINE; TRIMETHYLOXAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ATHEROSCLEROSIS; AORTA ROOT; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLOOD LEVEL; C57BL 6 MOUSE; CONTROLLED STUDY; FEMALE; GUT MICROBIAL TRANSPLANTATION; INBRED MOUSE STRAIN; INTESTINE FLORA; MICROBIAL COMMUNITY; MOUSE; NONHUMAN; NZW/LAC MOUSE; PRIORITY JOURNAL; STRAIN DIFFERENCE; TRANSPLANTATION; ADVERSE EFFECTS; AKR MOUSE; ANIMAL; AORTA; BAGG ALBINO MOUSE; BLOOD; C3H MOUSE; C57BL MOUSE; CBA MOUSE; CECUM; COMPLICATION; DBA MOUSE; DIET; DISEASE PREDISPOSITION; GASTROINTESTINAL TRACT; HOST PATHOGEN INTERACTION; HUMAN; KNOCKOUT MOUSE; MALE; METABOLISM; MICROBIOLOGY; MICROFLORA; PATHOLOGY; PHYSIOLOGY; SPECIES DIFFERENCE; TRANSGENIC MOUSE;

MUS;

ANIMALS; AORTA; ATHEROSCLEROSIS; CECUM; CHOLINE; DIET; DISEASE SUSCEPTIBILITY; FEMALE; GASTROINTESTINAL TRACT; HOST-PATHOGEN INTERACTIONS; HUMANS; MALE; METHYLAMINES; MICE, INBRED AKR; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, INBRED DBA; MICE, INBRED STRAINS; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROBIOTA; SPECIES SPECIFICITY;

EID: 84923913674     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.618249     Document Type: Article

References (37)

1. Brown, J. M., and Hazen, S. L. (2014) Metaorganismal nutrient metabolism as a basis of cardiovascular disease. Curr. Opin. Lipidol. 25, 48-53
2. Bäckhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A., and Gordon, J. I. (2005) Host-bacterial mutualism in the human intestine. Science 307, 1915-1920
3. Cho, I., and Blaser, M. J. (2012) The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13, 260-270
4. Kau, A. L., Ahern, P. P., Griffin, N. W., Goodman, A. L., and Gordon, J. I. (2011) Human nutrition, the gut microbiome and the immune system. Nature 474, 327-336
5. Wang, Z., Klipfell, E., Bennett, B. J., Koeth, R., Levison, B. S., Dugar, B., Feldstein, A. E., Britt, E. B., Fu, X., Chung, Y. M., Wu, Y., Schauer, P., Smith, J. D., Allayee, H., Tang, W. H., DiDonato, J. A., Lusis, A. J., and Hazen, S. L. (2011) Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472, 57-63
6. Koeth, R. A., Wang, Z., Levison, B. S., Buffa, J. A., Org, E., Sheehy, B. T., Britt, E. B., Fu, X., Wu, Y., Li, L., Smith, J. D., DiDonato, J. A., Chen, J., Li, H., Wu, G. D., Lewis, J. D., Warrier, M., Brown, J. M., Krauss, R. M., Tang, W. H., Bushman, F. D., Lusis, A. J., and Hazen, S. L. (2013) Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat. Med. 19, 576-585
7. Tang, W. H., Wang, Z., Levison, B. S., Koeth, R. A., Britt, E. B., Fu, X., Wu, Y., and Hazen, S. L. (2013) Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N. Engl. J. Med. 368, 1575-1584
8. Bennett, B. J., de Aguiar Vallim, T. Q., Wang, Z., Shih, D. M., Meng, Y., Gregory, J., Allayee, H., Lee, R., Graham, M., Crooke, R., Edwards, P. A., Hazen, S. L., and Lusis, A. J. (2013) Trimethylamine-N-oxide, a metabolite associated with atherosclerosis, exhibits complex genetic and dietary regulation. Cell Metab. 17, 49-60
9. Wang, Z., Tang, W. H., Buffa, J. A., Fu, X., Britt, E. B., Koeth, R. A., Levison, B. S., Fan, Y., Wu, Y., and Hazen, S. L. (2014) Prognostic value of choline and betaine depends on intestinal microbiota-generated metabolite tri-methylamine-N-oxide. Eur. Heart J. 35, 904-910
10. Tang, W. H. W., Wang, Z., Fan, Y., Levision, B., Hazen, J. E., Donahue, L. M., Wu, Y., and Hazen, S. L. (2014) Prognostic value of elevated levels of intestinal microbe-generated metabolite trimethylamine-N-oxide in patients with heart failure: refining the gut hypothesis. J. Am. Coll. Cardiol. 64, 1908-1914
11. Koch, R. (1880) Investigations into the Etiology of Traumatic Infective Diseases, The New Sydenham Society, London, UK
12. Dolman, C. E. (1973) Heinrich Hermann Robert Koch, in Dictionary of Scientific Biography (Gillespie, C., ed), pp. 420-435, Charles Scribner, New York
13. Koch, R. (1882) Die aetiologie der tuberculose. Berl Klin Wochenschr. 19, 221-230
14. Wang, Z., Levison, B. S., Hazen, J. E., Donahue, L., Li, X. M., and Hazen, S. L. (2014) Measurement of trimethylamine-N-oxide by stable isotope dilution liquid chromatography tandem mass spectrometry. Anal. Biochem. 455, 35-40
15. Bennett, B. J., Orozco, L., Kostem, E., Erbilgin, A., Dallinga, M., Neuhaus, I., Guan, B., Wang, X., Eskin, E., and Lusis, A. J. (2012) High-resolution association mapping of atherosclerosis loci in mice. Arterioscler. Thromb. Vasc. Biol. 32, 1790-1798
16. Rehg, J. E., Bush, D., and Ward, J. M. (2012) The utility of immunohistochemistry for the identification of hematopoietic and lymphoid cells in normal tissues and interpretation of proliferative and inflammatory lesions of mice and rats. Toxicol. Pathol. 40, 345-374
17. Köhler, C. (2007) Allograft inflammatory factor-1/Ionized calcium-binding adapter molecule 1 is specifically expressed by most subpopulations of macrophages and spermatids in testis. Cell Tissue Res. 330, 291-302
18. Hamady, M., Walker, J. J., Harris, J. K., Gold, N. J., and Knight, R. (2008) Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat. Methods 5, 235-237
19. Caporaso, J. G., Lauber, C. L., Walters, W. A., Berg-Lyons, D., Huntley, J., Fierer, N., Owens, S. M., Betley, J., Fraser, L., Bauer, M., Gormley, N., Gilbert, J. A., Smith, G., and Knight, R. (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621-1624
20. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Pen?a,A. G., Goodrich, J. K., Gordon, J. I., Huttley, G. A., Kelley, S. T., Knights, D., Koenig, J. E., Ley, R. E., Lozupone, C. A., McDonald, D., Muegge, B. D., Pirrung, M., Reeder, J., Sevinsky, J. R., Turnbaugh, P. J., Walters, W. A., Widmann, J., Yatsunenko, T., Zaneveld, J., and Knight, R. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336
21. Bokulich, N. A., Subramanian, S., Faith, J. J., Gevers, D., Gordon, J. I., Knight, R., Mills, D. A., and Caporaso, J. G. (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods 10, 57-59
22. Edgar, R. C. (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461
23. McDonald, D., Price, M. N., Goodrich, J., Nawrocki, E. P., DeSantis, T. Z., Probst, A., Andersen, G. L., Knight, R., and Hugenholtz, P. (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6, 610-618
24. Lozupone, C. A., and Knight, R. (2008) Species divergence and the measurement of microbial diversity. FEMS Microbiol. Rev. 32, 557-578
25. Pirrung, M., Kennedy, R., Caporaso, J. G., Stombaugh, J., Wendel, D., and Knight, R. (2011) TopiaryExplorer: visualizing large phylogenetic trees with environmental metadata. Bioinformatics 27, 3067-3069
26. Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W. S., and Huttenhower, C. (2011) Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60
27. Rooks, M. G., Veiga, P., Wardwell-Scott, L. H., Tickle, T., Segata, N., Michaud, M., Gallini, C. A., Beal, C., van Hylckama-Vlieg, J. E., Ballal, S. A., Morgan, X. C., Glickman, J. N., Gevers, D., Huttenhower, C., and Garrett, W. S. (2014) Gut microbiome composition and function in experimental colitis during active disease and treatment-induced remission. ISME J. 8, 1403-1417
28. Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., and Gordon, J. I. (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027-1031
29. Bäckhed, F., Ding, H., Wang, T., Hooper, L. V., Koh, G. Y., Nagy, A., Semenkovich, C. F., and Gordon, J. I. (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. U.S.A. 101, 15718-15723
30. Ellekilde, M., Selfjord, E., Larsen, C. S., Jakesevic, M., Rune, I., Tranberg, B., Vogensen, F. K., Nielsen, D. S., Bahl, M. I., Licht, T. R., Hansen, A. K., and Hansen, C. H. (2014) Transfer of gut microbiota from lean and obese mice to antibiotic-treated mice. Sci. Rep. 4, 5922
31. Cho, I., Yamanishi, S., Cox, L., Methé, B. A., Zavadil, J., Li, K., Gao, Z., Mahana, D., Raju, K., Teitler, I., Li, H., Alekseyenko, A. V., and Blaser, M. J. (2012) Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 488, 621-626
32. Chung, H., Pamp, S. J., Hill, J. A., Surana, N. K., Edelman, S. M., Troy, E. B., Reading, N. C., Villablanca, E. J., Wang, S., Mora, J. R., Umesaki, Y., Mathis, D., Benoist, C., Relman, D. A., and Kasper, D. L. (2012) Gut immune maturation depends on colonization with a host-specific microbiota. Cell 149, 1578-1593
33. Drechsler, M., Megens, R. T., van Zandvoort, M., Weber, C., and Soehnlein, O. (2010) Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis. Circulation 122, 1837-1845
34. Cox, L. M., Yamanishi, S., Sohn, J., Alekseyenko, A. V., Leung, J. M., Cho, I., Kim, S. G., Li, H., Gao, Z., Mahana, D., Zárate Rodriguez, J. G., Rogers, A. B., Robine, N., Loke, P., and Blaser, M. J. (2014) Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 158, 705-721
35. Eiseman, B., Silen, W., Bascom, G. S., and Kauvar, A. J. (1958) Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery 44, 854-859
36. van Nood, E., Vrieze, A., Nieuwdorp, M., Fuentes, S., Zoetendal, E. G., de Vos, W. M., Visser, C. E., Kuijper, E. J., Bartelsman, J. F., Tijssen, J. G., Speelman, P., Dijkgraaf, M. G., and Keller, J. J. (2013) Duodenal infusion of donor feces for recurrent Clostridium difficile. N. Engl. J. Med. 368, 407-415
37. Vrieze, A., Van Nood, E., Holleman, F., Salojärvi, J., Kootte, R. S., Bartelsman, J. F., Dallinga-Thie, G. M., Ackermans, M. T., Serlie, M. J., Oozeer, R., Derrien, M., Druesne, A., Van Hylckama Vlieg, J. E., Bloks, V. W., Groen, A. K., Heilig, H. G., Zoetendal, E. G., Stroes, E. S., de Vos, W. M., Hoekstra, J. B., and Nieuwdorp, M. (2012) Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143, 913-916