Intestinal Metabolites Are Profoundly Altered in the Context of HLA–B27 Expression and Functionally Modulate Disease in a Rat Model of Spondyloarthritis

Arthritis and Rheumatology

Volumn 69, Issue 10, 2017, Pages 1984-1995

  Asquith, Mark ^a   Davin, Sean ^a   Stauffer, Patrick ^a   Michell, Claire ^a   Janowitz, Cathleen ^a   Lin, Phoebe ^a   Ensign Lewis, Joe ^b   Kinchen, Jason M ^c   Koop, Dennis R ^a   Rosenbaum, James T ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c METABOLON INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOSUGAR; APIGENIN; BETA 2 MICROGLOBULIN; CHOLESTEROL; DAIDZEIN; ENTEROLACTONE; EQUOL; FREE FATTY ACID RECEPTOR 2; FREE FATTY ACID RECEPTOR 3; FUCOSE; GALACTOSAMINE; GALACTOSE; GLYCERIC ACID; HISTIDINE; HLA B27 ANTIGEN; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 10; INTERLEUKIN 33; KYNURENINE; LACTIC ACID; MEDIUM CHAIN FATTY ACID; N ACETYLMURAMATE; NARINGENIN; NIACIN RECEPTOR 1; PROTEIN; PROTEIN ZO1; SPERMIDINE; TRANSCRIPTION FACTOR FOXP3; TYROSINE; UNCLASSIFIED DRUG; UNINDEXED DRUG; BUTYRIC ACID; MURAMIC ACID; N-ACETYLMURAMIC ACID; PROPIONATE SODIUM; PROPIONIC ACID DERIVATIVE; VOLATILE FATTY ACID;

AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; FATTY ACID METABOLISM; FEMALE; FERMENTATION; GAS LIQUID CHROMATOGRAPHY; HOST; INFLAMMATORY DISEASE; MASS SPECTROMETRY; METABOLOMICS; MICROFLORA; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY T LYMPHOCYTE; SPONDYLARTHRITIS; UPREGULATION; XENOBIOTIC METABOLISM; ANIMAL; CECUM; CYTOLOGY; DISEASE MODEL; FISCHER 344 RAT; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOLOGY; INTESTINE FLORA; LYMPH NODE; MASS FRAGMENTOGRAPHY; MESENTERY; METABOLISM; MICROBIOLOGY; SPLEEN; SPONDYLOARTHROPATHY; T LYMPHOCYTE; TRANSGENIC RAT;

ANIMALS; BETA 2-MICROGLOBULIN; BUTYRIC ACID; CECUM; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DISEASE MODELS, ANIMAL; FATTY ACIDS, VOLATILE; FLOW CYTOMETRY; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GASTROINTESTINAL MICROBIOME; GENE EXPRESSION PROFILING; GLYCERIC ACIDS; HISTIDINE; HLA-B27 ANTIGEN; INTERLEUKIN-10; INTERLEUKIN-33; LYMPH NODES; MASS SPECTROMETRY; MESENTERY; METABOLOMICS; MURAMIC ACIDS; PROPIONATES; RATS; RATS, INBRED F344; RATS, TRANSGENIC; SPERMIDINE; SPLEEN; SPONDYLARTHROPATHIES; T-LYMPHOCYTES; TYROSINE; UP-REGULATION;

EID: 85031030061     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.40183     Document Type: Article

References (42)

1. Petersen C, Round JL. Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol 2014;16:1024–33.
2. Scher JU, Littman DR, Abramson SB. Microbiome in inflammatory arthritis and human rheumatic diseases [review]. Arthritis Rheumatol 2016;68:35–45.
3. Sharon G, Garg N, Debelius J, Knight R, Dorrestein PC, Mazmanian SK. Specialized metabolites from the microbiome in health and disease. Cell Metab 2014;20:719–30.
4. Hammer RE, Maika SD, Richardson JA, Tang JP, Taurog JD. Spontaneous inflammatory disease in transgenic rats expressing HLA-B27 and human β 2m: an animal model of HLA-B27-associated human disorders. Cell 1990;63:1099–112.
5. Taurog JD, Maika SD, Satumtira N, Dorris ML, McLean IL, Yanagisawa H, et al. Inflammatory disease in HLA-B27 transgenic rats. Immunol Rev 1999;169:209–23.
6. Lin P, Bach M, Asquith M, Lee AY, Akileswaran L, Stauffer P, et al. HLA-B27 and human β2-microglobulin affect the gut microbiota of transgenic rats. PLoS One 2014;9:e105684.
7. Asquith MJ, Stauffer P, Davin S, Mitchell C, Lin P, Rosenbaum JT. Perturbed mucosal immunity and dysbiosis accompany clinical disease in a rat model of spondyloarthritis. Arthritis Rheumatol 2016;68:2151–62.
8. Scher JU, Ubeda C, Artacho A, Attur M, Isaac S, Reddy SM, et al. Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease. Arthritis Rheumatol 2015;67:128–39.
9. Costello ME, Ciccia F, Willner D, Warrington N, Robinson PC, Gardiner B, et al. Intestinal dysbiosis in ankylosing spondylitis. Arthritis Rheumatol 2015;67:686–91.
10. Stoll ML, Kumar R, Morrow CD, Lefkowitz EJ, Cui X, Genin A, et al. Altered microbiota associated with abnormal humoral immune responses to commensal organisms in enthesitis-related arthritis. Arthritis Res Ther 2014;16:486.
11. Asquith M, Elewaut D, Lin P, Rosenbaum JT. The role of the gut and microbes in the pathogenesis of spondyloarthritis. Best Pract Res Clin Rheumatol 2014;28:687–702.
12. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013;504:451–5.
13. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-Y M, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013;341:569–73.
14. + T cells during cure of colitis. J Immunol 2006;177:5852–60.
15. Brown DG, Rao S, Weir TL, O'Malia J, Bazan M, Brown RJ, et al. Metabolomics and metabolic pathway networks from human colorectal cancers, adjacent mucosa, and stool. Cancer Metab 2016;4:11.
16. De Vos M, Cuvelier C, Mielants H, Veys E, Barbier F, Elewaut A. Ileocolonoscopy in seronegative spondylarthropathy. Gastroenterology 1989;96:339–44.
17. Rehaume LM, Mondot S, Aguirre de Cárcer D, Velasco J, Benham H, Hasnain SZ, et al. ZAP-70 genotype disrupts the relationship between microbiota and host, leading to spondyloarthritis and ileitis in SKG mice. Arthritis Rheumatol 2014;66:2780–92.
18. Taurog JD, Richardson JA, Croft JT, Simmons WA, Zhou M, Fernández-Sueiro JL, et al. The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats. J Exp Med 1994;180:2359–64.
19. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 2012;486:207–14.
20. Blaut M, Clavel T. Metabolic diversity of the intestinal microbiota: implications for health and disease. J Nutr 2007;137:751S–5.
21. Faure M, Moënnoz D, Mettraux C, Montigon F, Schiffrin EJ, Obled C, et al. The chronic colitis developed by HLA-B27 transgenic rats is associated with altered in vivo mucin synthesis. Dig Dis Sci 2004;49:339–46.
22. Zhao Y, Wu J, Li JV, Zhou NY, Tang H, Wang Y. Gut microbiota composition modifies fecal metabolic profiles in mice. J Proteome Res 2013;12:2987–99.
23. Guo X, Rao JN, Liu L, Zou T, Keledjian KM, Boneva D, et al. Polyamines are necessary for synthesis and stability of occludin protein in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 2005;288:G1159–69.
24. Guo X, Rao JN, Liu L, Zou TT, Turner DJ, Bass BL, et al. Regulation of adherens junctions and epithelial paracellular permeability: a novel function for polyamines. Am J Physiol Cell Physiol 2003;285:C1174–87.
25. Buts JP, de Keyser N, Kolanowski J, Sokal E, van Hoof F. Maturation of villus and crypt cell functions in rat small intestine: role of dietary polyamines. Dig Dis Sci 1993;38:1091–8.
26. Lux GD, Marton LJ, Baylin SB. Ornithine decarboxylase is important in intestinal mucosal maturation and recovery from injury in rats. Science 1980;210:195–8.
27. Dixon LJ, Kabi A, Nickerson KP, McDonald C. Combinatorial effects of diet and genetics on inflammatory bowel disease pathogenesis. Inflamm Bowel Dis 2015;21:912–22.
28. Lee DH, Blomhoff R, Jacobs DR Jr. Is serum γ glutamyltransferase a marker of oxidative stress? Free Rad Res 2004;38:535–9.
29. DeLay ML, Turner MJ, Klenk EI, Smith JA, Sowders DP, Colbert RA. HLA–B27 misfolding and the unfolded protein response augment interleukin-23 production and are associated with Th17 activation in transgenic rats. Arthritis Rheum 2009;60:2633–43.
30. Cao SS, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxid Redox Signal 2014;21:396–413.
31. Wells A, Pararajasegaram G, Baldwin M, Yang CH, Hammer M, Fox A. Uveitis and arthritis induced by systemic injection of streptococcal cell walls. Invest Ophthalmol Vis Sci 1986;27:921–5.
32. De Preter V, Joossens M, Ballet V, Shkedy Z, Rutgeerts P, Vermeire S, et al. Metabolic profiling of the impact of oligofructose-enriched inulin in Crohn's disease patients: a double-blinded randomized controlled trial. Clin Transl Gastroenterol 2013;4:e30.
33. Semova I, Carten JD, Stombaugh J, Mackey LC, Knight R, Farber SA, et al. Microbiota regulate intestinal absorption and metabolism of fatty acids in the zebrafish. Cell Host Microbe 2012;12:277–88.
34. Koleva P, Ketabi A, Valcheva R, Gänzle MG, Dieleman LA. Chemically defined diet alters the protective properties of fructo-oligosaccharides and isomalto-oligosaccharides in HLA-B27 transgenic rats. PLoS One 2014;9:e111717.
35. Huda-Faujan N, Abdulamir AS, Fatimah AB, Anas OM, Shuhaimi M, Yazid AM, et al. The impact of the level of the intestinal short chain fatty acids in inflammatory bowel disease patients versus healthy subjects. Open Biochem J 2010;4:53–8.
36. Takaishi H, Matsuki T, Nakazawa A, Takada T, Kado S, Asahara T, et al. Imbalance in intestinal microflora constitution could be involved in the pathogenesis of inflammatory bowel disease. Int J Med Microbiol 2008;298:463–72.
37. Marchesi JR, Holmes E, Khan F, Kochhar S, Scanlan P, Shanahan F, et al. Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. J Proteome Res 2007;6:546–51.
38. Rodríguez-Cabezas ME, Gálvez J, Camuesco D, Lorente MD, Concha A, Martinez-Augustin O, et al. Intestinal anti-inflammatory activity of dietary fiber (Plantago ovata seeds) in HLA-B27 transgenic rats. Clin Nutr 2003;22:463–71.
39. Hoentjen F, Welling GW, Harmsen HJ, Zhang X, Snart J, Tannock GW, et al. Reduction of colitis by prebiotics in HLA-B27 transgenic rats is associated with microflora changes and immunomodulation. Inflamm Bowel Dis 2005;11:977–85.
40. Jorgensen JR, Clausen MR, Mortensen PB. Oxidation of short and medium chain C2-C8 fatty acids in Sprague-Dawley rat colonocytes. Gut 1997;40:400–5.
41. Park J, Kim M, Kang SG, Jannasch AH, Cooper B, Patterson J, et al. Short-chain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR-S6K pathway. Mucosal Immunol 2015;8:80–93.
42. Suzuki T, Yoshida S, Hara H. Physiological concentrations of short-chain fatty acids immediately suppress colonic epithelial permeability. Br J Nutr 2008;100:297–305.