The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment

Nature Medicine

Volumn 21, Issue 8, 2015, Pages 895-905

  Zhang, Xuan ^a   Zhang, Dongya ^b   Jia, Huijue ^b   Feng, Qiang ^b,c   Wang, Donghui ^b,c   Liang, Di ^a   Wu, Xiangni ^a   Li, Junhua ^b,d   Tang, Longqing ^b   Li, Yin ^b   Lan, Zhou ^b   Chen, Bing ^b   Li, Yanli ^b   Zhong, Huanzi ^b   Xie, Hailiang ^b   Jie, Zhuye ^b   Chen, Weineng ^b   Tang, Shanmei ^b   Xu, Xiaoqiang ^b,e   Wang, Xiaokai ^b,e   Cai, Xianghang ^b   Liu, Sheng ^b,e   Xia, Yan ^b,e   Li, Jiyang ^b,f   Qiao, Xingye ^g   Al Aama, Jumana Yousuf ^b,h   Chen, Hua ^a   Wang, Li ^a   Wu, Qing Jun ^a   Zhang, Fengchun ^a   Zheng, Wenjie ^a   Li, Yongzhe ^a   Zhang, Mingrong ^b   Luo, Guangwen ^b   Xue, Wenbin ^b   Xiao, Liang ^b   Li, Jun ^b   Chen, Wanting ^b   Xu, Xun ^b   Yin, Ye ^b   Yang, Huanming ^b   Wang, Jian ^b   Kristiansen, Karsten ^b,c   Liu, Liang ⁱ   Li, Ting ⁱ   Huang, Qingchun ^j   Li, Yingrui ^b   Wang, Jun ^b,c,i   more..

^a PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

^b BGI SHENZHEN   (China)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d SOUTH CHINA UNIVERSITY OF TECHNOLOGY   (China)

^e UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^f QINGDAO UNIVERSITY   (China)

^g BINGHAMTON UNIVERSITY   (United States)

^h KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

ⁱ MACAU UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Macao)

^j GUANGDONG PROVINCIAL HOSPITAL OF CHINESE MEDICINE   (China)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; AUTOANTIBODY; IRON; SULFUR; ZINC; ANTIRHEUMATIC AGENT; C REACTIVE PROTEIN;

ACIDAMINOCOCCACEAE; ACTINOMYCETACEAE; ANTIBODY BLOOD LEVEL; ANTIGEN DETECTION; ARTICLE; CARDIOBACTERIACEAE; COHORT ANALYSIS; CONTROLLED STUDY; CORIOBACTERIACEAE; DYSBIOSIS; ERYSIPELOTRICHACEAE; EUBACTERIACEAE; FECES ANALYSIS; FLAVOBACTERIACEAE; FUSOBACTERIACEAE; HAEMOPHILUS; HUMAN; INTESTINE FLORA; IRON METABOLISM; LACHNOSPIRACEAE; LACTOBACILLACEAE; LACTOBACILLUS SALIVARIUS; MAJOR CLINICAL STUDY; METAGENOME; METAGENOMICS; MICROCOCCACEAE; MOLECULAR MIMICRY; MOUTH FLORA; NEISSERIACEAE; NONHUMAN; ORAL BIOPSY; PASTEURELLACEAE; PEPTOSTREPTOCOCCACEAE; PORPHYROMONADACEAE; PREVOTELLACEAE; PRIORITY JOURNAL; PROTEOBACTERIA; RHEUMATOID ARTHRITIS; SALIVA ANALYSIS; SEQUENCE ANALYSIS; SPIROCHAETACEAE; STREPTOCOCCACEAE; TOOTH PLAQUE; TREATMENT RESPONSE; ARTHRITIS, RHEUMATOID; INTESTINE; MICROBIOLOGY; MICROFLORA; MOUTH; SALIVA;

HAEMOPHILUS; LACTOBACILLUS SALIVARIUS;

ANTIRHEUMATIC AGENTS; ARTHRITIS, RHEUMATOID; C-REACTIVE PROTEIN; HUMANS; INTESTINES; METAGENOME; MICROBIOTA; MOUTH; SALIVA;

EID: 84938817346     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3914     Document Type: Article

References (48)

1. McInnes, I.B. & Schett, G. The pathogenesis of rheumatoid arthritis. N. Engl. J. Med. 365, 2205-2219 (2011).
2. Raychaudhuri, S. et al. Five amino acids in three HLA proteins explain most of the association between MHC and seropositive rheumatoid arthritis. Nat. Genet. 44, 291-296 (2012).
3. Okada, Y. et al. Genetics of rheumatoid arthritis contributes to biology and drug discovery. Nature 506, 376-381 (2014).
4. McInnes, I.B. & Schett, G. Cytokines in the pathogenesis of rheumatoid arthritis. Nat. Rev. Immunol. 7, 429-442 (2007).
5. Viatte, S., Plant, D. & Raychaudhuri, S. Genetics and epigenetics of rheumatoid arthritis. Nat. Rev. Rheumatol. 9, 141-153 (2013).
6. Deane, K.D. & El-Gabalawy, H. Pathogenesis and prevention of rheumatic disease: focus on preclinical RA and SLE. Nat. Rev. Rheumatol. 10, 212-228 (2014).
7. Demoruelle, M.K., Deane, K.D. & Holers, V.M. When and where does inflammation begin in rheumatoid arthritis? Curr. Opin. Rheumatol. 26, 64-71 (2014).
8. Clemente, J.C., Ursell, L.K., Parfrey, L.W. & Knight, R. The impact of the gut microbiota on human health: an integrative view. Cell 148, 1258-1270 (2012).
9. Kamada, N., Seo, S.-U., Chen, G.Y. & Nñez, G. Role of the gut microbiota in immunity and inflammatory disease. Nat. Rev. Immunol. 13, 321-335 (2013).
10. Schloissnig, S. et al. Genomic variation landscape of the human gut microbiome. Nature 493, 45-50 (2013).
11. Faith, J.J. et al. The long-term stability of the human gut microbiota. Science 341, 1237439 (2013).
12. Li, J. et al. An integrated catalog of reference genes in the human gut microbiome. Nat. Biotechnol. 32, 834-841 (2014).
13. Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature 486, 222-227 (2012).
14. The Human Microbiome Project Consortium. A framework for human microbiome research. Nature 486, 215-221 (2012).
15. Wade, W.G. The oral microbiome in health and disease. Pharmacol. Res. 69, 137-143 (2013).
16. Liu, X., Zou, Q., Zeng, B., Fang, Y. & Wei, H. Analysis of fecal Lactobacillus community structure in patients with early rheumatoid arthritis. Curr. Microbiol. 67, 170-176 (2013).
17. Vaahtovuo, J., Munukka, E., Korkeamäki, M., Luukkainen, R. & Toivanen, P. Fecal microbiota in early rheumatoid arthritis. J. Rheumatol. 35, 1500-1505 (2008).
18. Scher, J.U. et al. Periodontal disease and the oral microbiota in new-onset rheumatoid arthritis. Arthritis Rheum. 64, 3083-3094 (2012).
19. Scher, J.U. et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife 2, e01202 (2013).
20. Qin, J. et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490, 55-60 (2012).
21. Cotillard, A. et al. Dietary intervention impact on gut microbial gene richness. Nature 500, 585-588 (2013).
22. Nielsen, H.B. et al. Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat. Biotechnol. 32, 822-828 (2014).
23. Hsiao, A. et al. Recovery from Vibrio cholerae infection. Nature 515, 423-426 (2014).
24. Bäckhed, F. et al. Dynamics and stabilization of the human gut microbiome in the first year of life. Cell Host Microbe 17, 690-703 (2015).
25. Franzosa, E.A. et al. Identifying personal microbiomes using metagenomic codes. Proc. Natl. Acad. Sci. USA 112, E2930-E2938 (2015).
26. Verschoor, A. et al. A platelet-mediated system for shuttling blood-borne bacteria to CD8α+ dendritic cells depends on glycoprotein GPIb and complement C3. Nat. Immunol. 12, 1194-1201 (2011).
27. Yeaman, M.R. Platelets: at the nexus of antimicrobial defence. Nat. Rev. Microbiol. 12, 426-437 (2014).
28. Konig, M.F., Paracha, A.S., Moni, M., Bingham, C.O. & Andrade, F. Defining the role of Porphyromonas gingivalis peptidylarginine deiminase (PPAD) in rheumatoid arthritis through the study of PPAD biology. Ann. Rheum. Dis. doi:10.1136/annrheumdis-2014-205385 (2014).
29. Michels, F. et al. Late prosthetic joint infection due to Rothia mucilaginosa. Acta Orthop. Belg. 73, 263-267 (2007).
30. Verrall, A.J., Robinson, P.C., Tan, C.E., Mackie, W.G. & Blackmore, T.K. Rothia aeria as a cause of sepsis in a native joint. J. Clin. Microbiol. 48, 2648-2650 (2010).
31. Colombo, A.P. et al. Impact of periodontal therapy on the subgingival microbiota of severe periodontitis: comparison between good responders and individuals with refractory periodontitis using the human oral microbe identification microarray. J. Periodontol. 83, 1279-1287 (2012).
32. Hilty, M. et al. Disordered microbial communities in asthmatic airways. PLoS One 5, e8578 (2010).
33. Park, H., Shin, J.W., Park, S. & Kim, W. Microbial communities in the upper respiratory tract of patients with asthma and chronic obstructive pulmonary disease. PLoS One 9, e109710 (2014).
34. Rashid, T. & Ebringer, A. Autoimmunity in rheumatic diseases is induced by microbial infections via crossreactivity or molecular mimicry. Autoimmune Dis. 2012, 539282 (2012).
35. van Heemst, J. et al. Crossreactivity to vinculin and microbes provides a molecular basis for HLA-based protection against rheumatoid arthritis. Nat. Commun. 6, 6681 (2015).
36. van der Helm-van Mil, A.H. Risk estimation in rheumatoid arthritis: from bench to bedside. Nat. Rev. Rheumatol. 10, 171-180 (2014).
37. Chen, L., Xiong, Z., Sun, L., Yang, J. & Jin, Q. VFDB 2012 update: toward the genetic diversity and molecular evolution of bacterial virulence factors. Nucleic Acids Res. 40, D641-D645 (2012).
38. Goldbach-Mansky, R. et al. Comparison of Tripterygium wilfordii Hook F versus sulfasalazine in the treatment of rheumatoid arthritis: a randomized trial. Ann. Intern. Med. 151, 229-240 W49-W51 (2009).
39. Tao, X., Younger, J., Fan, F.Z., Wang, B. & Lipsky, P.E. Benefit of an extract of Tripterygium wilfordii Hook F in patients with rheumatoid arthritis: a double-blind, placebo-controlled study. Arthritis Rheum. 46, 1735-1743 (2002).
40. Lv, Q.-W. et al. Comparison of Tripterygium wilfordii Hook F with methotrexate in the treatment of active rheumatoid arthritis (TRIFRA): a randomised, controlled clinical trial. Ann. Rheum. Dis. 74, 1078-1086 (2015).
41. Feng, Q. et al. Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat. Commun. 6, 6528 (2015).
42. Luo, R. et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1, 18 (2012).
43. Kent, W.J. BLAT-the BLAST-like alignment tool. Genome Res. 12, 656-664 (2002).
44. Le Chatelier, E. et al. Richness of human gut microbiome correlates with metabolic markers. Nature 500, 541-546 (2013).
45. McArdle, B.H. & Anderson, M.J. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82, 290-297 (2001).
46. Zapala, M.A. & Schork, N.J. Multivariate regression analysis of distance matrices for testing associations between gene expression patterns and related variables. Proc. Natl. Acad. Sci. USA 103, 19430-19435 (2006).
47. Karlsson, F.H. et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498, 99-103 (2013).
48. Patil, K.R. & Nielsen, J. Uncovering transcriptional regulation of metabolism by using metabolic network topology. Proc. Natl. Acad. Sci. USA 102, 2685-2689 (2005).