Altered microbiota associated with abnormal humoral immune responses to commensal organisms in enthesitis-related arthritis

Arthritis Research and Therapy

Volumn 16, Issue 1, 2014, Pages

  Stoll, Matthew L ^a   Kumar, Ranjit ^a   Morrow, Casey D ^a   Lefkowitz, Elliot J ^b   Cui, Xiangqin ^a   Genin, Anna ^a   Cron, Randy Q ^a   Elson, Charles O ^c  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA 16S; IMMUNOGLOBULIN A; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G;

ADOLESCENT; ADULT; AKKERMANSIA MUCINIPHILA; ANTIGEN ANTIBODY REACTION; ARTHRITIS; ARTICLE; BACTEROIDES; BACTEROIDES FRAGILIS; BIFIDOBACTERIUM; BLOOD SAMPLING; CHILD; CLINICAL ARTICLE; CLUSTER ANALYSIS; COMMENSAL; CONTROLLED STUDY; DNA PURIFICATION; ENTHESITIS; ENTHESITIS RELATED ARTHRITIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FAECALIBACTERIUM PRAUSNITZII; FECES ANALYSIS; FEMALE; GENE; GENE AMPLIFICATION; HUMAN; HUMORAL IMMUNITY; INTESTINE FLORA; LACHNOSPIRACEAE; MALE; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SPONDYLARTHRITIS; VERRUCOMICROBIUM; ARTHRITIS, JUVENILE; IMMUNOLOGY; INFLAMMATORY BOWEL DISEASES; MICROBIOLOGY; MICROFLORA; PRESCHOOL CHILD; SYMBIOSIS; YOUNG ADULT;

ADOLESCENT; ARTHRITIS, JUVENILE; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; IMMUNITY, HUMORAL; INFLAMMATORY BOWEL DISEASES; MALE; MICROBIOTA; SYMBIOSIS; YOUNG ADULT;

EID: 84923920287     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/s13075-014-0486-0     Document Type: Article

References (52)

1. Helmick CG, Felson DT, Lawrence RC, Gabriel S, Hirsch R, Kwoh CK, Liang MH, Kremers HM, Mayes MD, Merkel PA, Pillemer SR, Reveille JD, Stone JH, National Arthritis Data Workgroup: Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part I. Arthritis Rheum 2008, 58:15-25.
2. Reveille JD: The genetic basis of spondyloarthritis. Ann Rheum Dis 2011, 70:i44-i50.
3. Reveille JD: Genetics of spondyloarthritis-beyond the MHC. Nat Rev Rheumatol 2012, 8:296-304.
4. Fantini MC, Pallone F, Monteleone G: Common immunologic mechanisms in inflammatory bowel disease and spondylarthropathies. World J Gastroenterol 2009, 15:2472-2478.
5. Taurog JD, Richardson JA, Croft JT, Simmons WA, Zhou M, Fernandez-Sueiro JL, Balish E, Hammer RE: The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats. J Exp Med 1994, 180:2359-2364.
6. Metzker ML: Sequencing technologies - the next generation. Nat Rev Genet 2010, 11:31-46.
7. Cheng J, Palva AM, de Vos WM, Satokari R: Contribution of the intestinal microbiota to human health: from birth to 100years of age. Curr Top Microbiol Immunol 2013, 358:323-346.
8. Stebbings S, Munro K, Simon MA, Tannock G, Highton J, Harmsen H, Welling G, Seksik P, Dore J, Grame G, Tilsala-Timisjarvi A: Comparison of the faecal microflora of patients with ankylosing spondylitis and controls using molecular methods of analysis. Rheumatology (Oxford) 2002, 41:1395-1401.
9. Targan SR, Landers CJ, Yang H, Lodes MJ, Cong Y, Papadakis KA, Vasiliauskas E, Elson CO, Hershberg RM: Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn's disease. Gastroenterology 2005, 128:2020-2028.
10. Wallis D, Asaduzzaman A, Weisman M, Haroon N, Anton A, McGovern D, Targan S, Inman R: Elevated serum anti-flagellin antibodies implicate subclinical bowel inflammation in ankylosing spondylitis: an observational study. Arthritis Res Ther 2013, 15:R166.
11. Lodes MJ, Cong Y, Elson CO, Mohamath R, Landers CJ, Targan SR, Fort M, Hershberg RM: Bacterial flagellin is a dominant antigen in Crohn disease. J Clin Invest 2004, 113:1296-1306.
12. Stebbings SM, Taylor C, Tannock GW, Baird MA, Highton J: The immune response to autologous bacteroides in ankylosing spondylitis is characterized by reduced interleukin 10 production. J Rheumatol 2009, 36:797-800.
13. Petty RE, Southwood TR, Manners P, Baum J, Glass DN, Goldenberg J, He X, Maldonado-Cocco J, Orozco-Alcala J, Prieur AM, Suarez-Almazor ME, Woo P: International League of Associations for Rheumatology classification of juvenile idiopathic arthritis: second revision, Edmonton, 2001. J Rheumatol 2004, 31:390-392.
14. McGhee JL, Burks FN, Sheckels JL, Jarvis JN: Identifying children with chronic arthritis based on chief complaints: absence of predictive value for musculoskeletal pain as an indicator of rheumatic disease in children. Pediatrics 2002, 110:354-359.
15. Cary SG, Blair EB: New Transport Medium for Shipment of Clinical Specimens. I. Fecal Specimens. J Bacteriol 1964, 88:96-98.
16. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R: Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 2011, 108:4516-4522.
17. Gordon A, Hannon GJ: "FASTX-Toolkit", FASTQ/A short-reads pre-processing tools (unpublished). 2013. Available from: http://hannonlab.cshl.edu/fastx_toolkit/.
18. Edgar RC: Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26:2460-2461.
19. Wang Q, Garrity GM, Tiedje JM, Cole JR: Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007, 73:5261-5267.
20. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL: Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006, 72:5069-5072.
21. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R: PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 2010, 26:266-267.
22. Faith DP, Baker AM: Phylogenetic diversity (PD) and biodiversity conservation: some bioinformatics challenges. Evol Bioinform Online 2006, 2:121-128.
23. Lozupone C, Knight R: UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005, 71:8228-8235.
24. Suzuki R, Shimodaira H: Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 2006, 22:1540-1542.
25. Johnson CL, Versalovic J: The human microbiome and its potential importance to pediatrics. Pediatrics 2012, 129:950-960.
26. De Cruz P, Prideaux L, Wagner J, Ng SC, McSweeney C, Kirkwood C, Morrison M, Kamm MA: Characterization of the gastrointestinal microbiota in health and inflammatory bowel disease. Inflamm Bowel Dis 2012, 18:372-390.
27. Sartor RB: Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology 2004, 126:1620-1633.
28. Elson CO, Cong Y: Host-microbiota interactions in inflammatory bowel disease. Gut Microbes 2012, 3:332-344.
29. Rosenbaum JT, Davey MP: Time for a gut check: evidence for the hypothesis that HLA-B27 predisposes to ankylosing spondylitis by altering the microbiome. Arthritis Rheum 2011, 63:3195-3198.
30. Thorkildsen LT, Nwosu FC, Avershina E, Ricanek P, Perminow G, Brackmann S, Vatn MH, Rudi K: Dominant fecal microbiota in newly diagnosed untreated inflammatory bowel disease patients. Gastroenterol Res Pract 2013, 2013:636785.
31. Wang W, Chen L, Zhou R, Wang X, Song L, Huang S, Wang G, Xia B: Increased proportions of bifidobacterium and the lactobacillus group and loss of butyrate-producing bacteria in inflammatory bowel disease. J Clin Microbiol 2014, 52:398-406.
32. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR: Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 2007, 104:13780-13785.
33. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, Blugeon S, Bridonneau C, Furet JP, Corthier G, Grangette C, Vasquez N, Pochart P, Trugnan G, Thomas G, Blottière HM, Doré J, Marteau P, Seksik P, Langella P: Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A 2008, 105:16731-16736.
34. Hold GL, Schwiertz A, Aminov RI, Blaut M, Flint HJ: Oligonucleotide probes that detect quantitatively significant groups of butyrate-producing bacteria in human feces. Appl Environ Microbiol 2003, 69:4320-4324.
35. Segain JP, Raingeard de la Blétière D, Bourreille A, Leray V, Gervois N, Rosales C, Ferrier L, Bonnet C, Blottière HM, Galmiche JP: Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease. Gut 2000, 47:397-403.
36. Louis P, Young P, Holtrop G, Flint HJ: Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene. Environ Microbiol 2010, 12:304-314.
37. Scher JU, Sczesnak A, Longman RS, Segata N, Ubeda C, Bielski C, Rostron T, Cerundolo V, Pamer EG, Abramson SB, Huttenhower C, Littman DR: Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife 2013, 2:e01202.
38. Frank DN, Robertson CE, Hamm CM, Kpadeh Z, Zhang T, Chen H, Zhu W, Sartor RB, Boedeker EC, Harpaz N, Pace NR, Li E: Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel diseases. Inflamm Bowel Dis 2011, 17:179-184.
39. Round JL, Lee SM, Li J, Tran G, Jabri B, Chatila TA, Mazmanian SK: The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 2011, 332:974-977.
40. Prindiville TP, Sheikh RA, Cohen SH, Tang YJ, Cantrell MC, Silva J Jr: Bacteroides fragilis enterotoxin gene sequences in patients with inflammatory bowel disease. Emerg Infect Dis 2000, 6:171-174.
41. Sinkorova Z, Capkova J, Niederlova J, Stepankova R, Sinkora J: Commensal intestinal bacterial strains trigger ankylosing enthesopathy of the ankle in inbred B10.BR (H-2(k)) male mice. Hum Immunol 2008, 69:845-850.
42. Rath HC, Herfarth HH, Ikeda JS, Grenther WB, Hamm TE Jr, Balish E, Taurog JD, Hammer RE, Wilson KH, Sartor RB: Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J Clin Invest 1996, 98:945-953.
43. Derrien M, Vaughan EE, Plugge CM, de Vos WM: Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 2004, 54:1469-1476.
44. Derrien M, Collado MC, Ben-Amor K, Salminen S, de Vos WM: The Mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Appl Environ Microbiol 2008, 74:1646-1648.
45. Ganesh BP, Klopfleisch R, Loh G, Blaut M: Commensal Akkermansia muciniphila exacerbates gut inflammation in Salmonella Typhimurium-infected gnotobiotic mice. PLoS One 2013, 8:e74963.
46. Fite A, Macfarlane S, Furrie E, Bahrami B, Cummings JH, Steinke DT, MacFarlane GT: Longitudinal analyses of gut mucosal microbiotas in ulcerative colitis in relation to patient age and disease severity and duration. J Clin Microbiol 2013, 51:849-856.
47. Macpherson AJ, McCoy KD, Johansen FE, Brandtzaeg P: The immune geography of IgA induction and function. Mucosal Immunol 2008, 1:11-22.
48. Gutzeit C, Magri G, Cerutti A: Intestinal IgA production and its role in host-microbe interaction. Immunol Rev 2014, 260:76-85.
49. Liu LM, MacPherson GG: Rat intestinal dendritic cells: immunostimulatory potency and phenotypic characterization. Immunology 1995, 85:88-93.
50. Wu J, Ji C, Xie F, Langefeld CD, Qian K, Gibson AW, Edberg JC, Kimberly RP: FcalphaRI (CD89) alleles determine the proinflammatory potential of serum IgA. J Immunol 2007, 178:3973-3982.
51. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, Reyes JA, Shah SA, LeLeiko N, Snapper SB, Bousvaros A, Korzenik J, Sands BE, Xavier RJ, Huttenhower C: Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 2012, 13:R79.
52. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI: An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006, 444:1027-1031.