Skip to main content

The Intestinal Microbiome, the Immune System and Spondyloarthropathy

  • Chapter
  • First Online:
Next-Generation Therapies and Technologies for Immune-Mediated Inflammatory Diseases

Part of the book series: Progress in Inflammation Research ((PIR))

Abstract

The microbial communities that live in and on our bodies play complex roles in maintaining our health and in causing disease. The recent application of high-throughput DNA sequencing to examine these communities, both in terms of species present and in their activities, has proven to be a very powerful tool for examining the influences of microbes on human health. Whilst we are only just beginning to understand the role of our microbial ‘second’ genome, what is clear is that certain shifts and alterations in our microbiome are associated with, and may ultimately cause or cure, disease. The interaction between human host and microbes is multifaceted, however, and such interactions must therefore be examined in overall context of disease, diet, medications as well as underlying host genetics.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Huttenhower C, Gevers D, Knight R, Abubucker S, Badger JH, Chinwalla AT (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214

    Article  CAS  Google Scholar 

  2. Burns M, Lynch J, Starr T, Knights D, Blekhman R (2015) Virulence genes are a signature of the microbiome in the colorectal tumor microenvironment. Genome Med 7(1):55

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  3. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE et al (2009) A core gut microbiome in obese and lean twins. Nature 457(7228):480–484

    Article  CAS  PubMed  Google Scholar 

  4. Gevers D, Kugathasan S, Denson LA, Vazquez-Baeza Y, Van† Treuren W, Ren B et al (2014) The treatment-naive microbiome in new-onset Crohn s disease. Cell Host Microbe 15(3):382–392

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Knights D, Silverberg M, Weersma R, Gevers D, Dijkstra G, Huang H et al (2014) Complex host genetics influence the microbiome in inflammatory bowel disease. Genome Med 6(12):107

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  6. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N et al (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci 107(26):11971–11975

    Article  PubMed Central  PubMed  Google Scholar 

  7. Huh SY, Rifas-Shiman SL, Zera CA, Edwards JWR, Oken E, Weiss ST, et al (2012) Delivery by caesarean section and risk of obesity in preschool age children: a prospective cohort study. Arch Dis Child 97(7):610–616

    Google Scholar 

  8. Bager P (2011) Birth by caesarean section and wheezing, asthma, allergy, and intestinal disease. Clin Exp Allergy 41(2):147–148

    Article  CAS  PubMed  Google Scholar 

  9. Arrieta M-C, Stiemsma LT, Dimitriu PA, Thorson L, Russell S, Yurist-Doutsch S et al (2015) Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci Transl Med 7(307):307ra152–307ra152

    Article  PubMed  CAS  Google Scholar 

  10. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende D et al (2011) Enterotypes of the human gut microbiome. Nature 473:174–180

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Ursell LK, Haiser HJ, Van Treuren W, Garg N, Reddivari L, Vanamala J et al (2014) The intestinal metabolome: an intersection between microbiota and host. Gastroenterology 146(6):1470–1476

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Round JL, Mazmanian SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9(5):313–323

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Clemente J, Ursell L, Parfrey L, Knight R (2012) The impact of the gut microbiota on human health: an integrative view. Cell 148:1258–1270

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI (2008) Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3:213–223

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M et al (2012) Human gut microbiome viewed across age and geography. Nature 486(7402):222–227

    CAS  PubMed Central  PubMed  Google Scholar 

  16. Maslowski KM, Mackay CR (2011) Diet, gut microbiota and immune responses. Nat Immunol 12(1):5–9

    Article  CAS  PubMed  Google Scholar 

  17. Kranich J, Maslowski KM, Mackay CR (2011) Commensal flora and the regulation of inflammatory and autoimmune responses. Semin Immunol 23(2):139–145

    Article  CAS  PubMed  Google Scholar 

  18. Perdomo OJ, Cavaillon JM, Huerre M, Ohayon H, Gounon P, Sansonetti PJ (1994) Acute inflammation causes epithelial invasion and mucosal destruction in experimental shigellosis. J Exp Med 180(4):1307–1319

    Article  CAS  PubMed  Google Scholar 

  19. Vaishnava S, Behrendt CL, Ismail AS, Eckmann L, Hooper LV (2008) Paneth Cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc Natl Acad Sci 105(52):20858–20863

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U et al (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139(3):485–498

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Duan J, Chung H, Troy E, Kasper DL (2010) Microbial colonization drives expansion of IL-1 receptor 1-expressing and IL-17-producing [gamma]/[delta] T cells. Cell Host Microbe 7(2):140–150

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Cho I, Blaser M (2012) The human microbiome: at the interface of health and disease. Nat Rev Genet 13:10

    Google Scholar 

  23. Reid G, Younes JA, Van der Mei HC, Gloor GB, Knight R, Busscher HJ (2011) Microbiota restoration: natural and supplemented recovery of human microbial communities. Nat Rev Micro 9(1):27–38

    Article  CAS  Google Scholar 

  24. Laurence A, O’Shea JJ, Watford WT (2008) Interleukin-22: a sheep in wolf’s clothing. Nat Med 14(3):247–249

    Article  CAS  PubMed  Google Scholar 

  25. Salzman NH, Hung K, Haribhai D, Chu H, Karlsson-Sjoberg J, Amir E et al (2010) Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 11(1):76–82

    Article  CAS  PubMed  Google Scholar 

  26. Maloy KJ, Powrie F (2011) Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474(7351):298–306

    Article  CAS  PubMed  Google Scholar 

  27. Koslowski MJ, Beisner J, Stange EF, Wehkamp J (2010) Innate antimicrobial host defense in small intestinal Crohn’s disease. Int J Med Microbiol 300(1):34–40

    Article  CAS  PubMed  Google Scholar 

  28. Wehkamp J, Koslowski M, Wang G, Stange EF (2008) Barrier dysfunction due to distinct defensin deficiencies in small intestinal and colonic Crohn’s disease. Mucosal Immunol 1(1s):S67–S74

    Article  CAS  PubMed  Google Scholar 

  29. Artis D (2008) Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol 8(6):411–420

    Article  CAS  PubMed  Google Scholar 

  30. Hooper LV, Macpherson AJ (2010) Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 10(3):159–169

    Article  CAS  PubMed  Google Scholar 

  31. Shan M, Gentile M, Yeiser JR, Walland AC, Bornstein VU, Chen K et al (2013) Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science 342(6157):447–453

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Heazlewood C, Cook M, Eri R, Price G, Tauro S, Taupin D et al (2008) Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis. PLoS Med 5:e54

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  33. Sherlock J, Joyce-Shaikh B, Turner S, Chao C, Sathe M, Grein J et al (2012) IL-23 induces spondyloarthropathy by acting on ROR-gammat+ CD3+CD4-CD8- entheseal resident T cells. Nat Med 18:1069–1076

    Article  CAS  PubMed  Google Scholar 

  34. Fasano A, Nataro JP (2004) Intestinal epithelial tight junctions as targets for enteric bacteria-derived toxins. Adv Drug Deliv Rev 56(6):795–807

    Article  CAS  PubMed  Google Scholar 

  35. Collins SM. IV (2001) Modulation of intestinal inflammation by stress: basic mechanisms and clinical relevance. 2001-03-01 00:00:00. G315-G8 p

    Google Scholar 

  36. Bruewer M, Luegering A, Kucharzik T, Parkos CA, Madara JL, Hopkins AM et al (2003) Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms. J Immunol 171(11):6164–6172

    Article  CAS  PubMed  Google Scholar 

  37. Nusrat A, Turner JR, Madara JL. IV (2000) Regulation of tight junctions by extracellular stimuli: nutrients, cytokines, and immune cells. 2000-11-01 00:00:00. G851-G7 p

    Google Scholar 

  38. Teahon K, Smethurst P, Levi AJ, Menzies IS, Bjarnason I (1992) Intestinal permeability in patients with Crohn’s disease and their first degree relatives. Gut 33(3):320–323

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Lubrano E, Ciacci C, Ames P, Mazzacca G, Oriente P, Scarpa R (1996) The arthritis of coeliac disease: prevalence and pattern in 200 adult patients. Rheumatology 35:1314–1318

    Article  CAS  Google Scholar 

  40. Podolsky DK (2002) Inflammatory bowel disease. N Eng J Med 347(6):417–429

    Article  CAS  Google Scholar 

  41. Mielants H, Veys EM, Goemaere S, Goethals K, Cuvelier C, De Vos M (1991) Gut inflammation in the spondyloarthropathies: clinical, radiologic, biologic and genetic features in relation to the type of histology. A prospective study. J Rheumatol 18(10):1542–1551

    CAS  PubMed  Google Scholar 

  42. Vaile J, Meddings J, Yacyshyn B, Russell A, Maksymowych W (1999) Bowel permeability and CD45RO expression on circulating CD20+ B cells in patients with ankylosing spondylitis and their relatives. J Rheumatol 26:128–135

    CAS  PubMed  Google Scholar 

  43. Martinez-Gonzalez O, Cantero-Hinojosa J, Paule-Sastre P, Gomez-Magan JC, Salvatierra-Rios D (1994) Intestinal permeability in patients with ankylosing spondyllitis and their healthy relatives. Rheumatology 33(7):644–647

    Article  CAS  Google Scholar 

  44. Chabot S, Wagner JS, Farrant S, Neutra MR (2006) TLRs regulate the gatekeeping functions of the intestinal follicle-associated epithelium. J Immunol 176(7):4275–4283

    Article  CAS  PubMed  Google Scholar 

  45. Suzuki K, Ha S, Tsuji M, Fagarasan S (2007) Intestinal IgA synthesis: a primitive form of adaptive immunity that regulates microbial communities in the gut. Semin Immunol 19:127–135

    Article  CAS  PubMed  Google Scholar 

  46. Wesa A, Galy A (2002) Increased production of pro-inflammatory cytokines and enhanced T cell responses after activation of human dendritic cells with IL-1 and CD40 ligand. BMC Immunol 3:14

    Article  PubMed Central  PubMed  Google Scholar 

  47. Cruz CM, Rinna A, Forman HJ, Ventura ALM, Persechini PM, Ojcius DM (2007) ATP activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages. J Biol Chem 282(5):2871–2879

    Article  CAS  PubMed  Google Scholar 

  48. Hirotani T, Lee PY, Kuwata H, Yamamoto M, Matsumoto M, Kawase I et al (2005) The nuclear IkB protein IkBNS selectively inhibits lipopolysaccharide-induced IL-6 production in macrophages of the colonic lamina propria. J Immunol 174(6):3650–3657

    Article  CAS  PubMed  Google Scholar 

  49. Denning T, Wang Y-C, Patel S, Williams I, Pulendran B (2007) Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol 8:1086–1094

    Article  CAS  PubMed  Google Scholar 

  50. Glocker E, Kotlarz D, Boztug K, Gertz E, Schaffer A, Noyan F et al (2009) Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N Engl J Med 361:2033–2045

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Consortium TUIGCtWTCC (2009) Genome-wide association study of ulcerative colitis identifies three new susceptibility loci, including the HNF4A region. Nat Genet 41(12):1330–1334

    Article  CAS  Google Scholar 

  52. Franke A, Balschun T, Sina C, Ellinghaus D, Hasler R, Mayr G et al (2010) Genome-wide association study for ulcerative colitis identifies risk loci at 7q22 and 22q13 (IL17REL). Nat Genet 42(4):292–294

    Article  CAS  PubMed  Google Scholar 

  53. Oppmann B, Lesley R, Blom B, Timans J, Xu Y, Hunte B et al (2000) Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13:715–725

    Article  CAS  PubMed  Google Scholar 

  54. Burton P, Clayton D, Cardon L, Craddock N, Deloukas P, Duncanson A et al (2007) Association scan of 14,500 nonsynonymous SNPs in four diseases identifies autoimmunity variants. Nat Genet 39:1329–1337

    Article  CAS  PubMed  Google Scholar 

  55. Cargill M, Schrodi S, Chang M, Garcia V, Brandon R, Callis K et al (2007) A large-scale genetic association study confirms IL12B and leads to the identification of IL23R as psoriasis-risk genes. Am J Hum Gen 80:273–290

    Article  CAS  Google Scholar 

  56. Duerr R, Taylor K, Brant S, Rioux J, Silverberg M, Daly M et al (2006) A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 314:1461–1463

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Xavier JM, Shahram F, Davatchi F, Rosa A, Crespo J, Abdollahi BS et al (2012) Association study of IL10 and IL23R–IL12RB2 in Iranian patients with Behçet’s disease. Arthritis Rheum 64(8):2761–2772

    Article  CAS  PubMed  Google Scholar 

  58. Ogawa A, Andoh A, Araki Y, Bamba T, Fujiyama Y (2004) Neutralization of interleukin-17 aggravates dextran sulfate sodium-induced colitis in mice. Clin Immunol 110:55–62

    Article  CAS  PubMed  Google Scholar 

  59. Zheng S, Wang J, Horwitz D (2008) Cutting edge: Foxp3+CD4+CD25+ regulatory T cells induced by IL-2 and TGF-beta are resistant to Th17 conversion by IL-6. J Immunol 180:7112–7116

    Article  CAS  PubMed  Google Scholar 

  60. Takatori H, Kanno Y, Watford WT, Tato CM, Weiss G, Ivanov II et al (2009) Lymphoid tissue inducer–like cells are an innate source of IL-17 and IL-22. J Exp Med 206(1):35–41

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  61. Kobori A, Yagi Y, Imaeda H, Ban H, Bamba S, Tsujikawa T et al (2010) Interleukin-33 expression is specifically enhanced in inflamed mucosa of ulcerative colitis. J Gastroenterol 45(10):999–1007

    Article  CAS  PubMed  Google Scholar 

  62. Lockhart E, Green AM, Flynn JL (2006) IL-17 production is dominated by γδ T cells rather than CD4 T cells during mycobacterium tuberculosis infection. J Immunol 177(7):4662–4669

    Article  CAS  PubMed  Google Scholar 

  63. Sonnenberg GF, Fouser LA, Artis D (2011) Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol 12(5):383–390

    Article  CAS  PubMed  Google Scholar 

  64. Cua DJ, Tato CM (2010) Innate IL-17-producing cells: the sentinels of the immune system. Nat Rev Immunol 10(7):479–489

    Article  CAS  PubMed  Google Scholar 

  65. Mokuno Y, Matsuguchi T, Takano M, Nishimura H, Washizu J, Ogawa T et al (2000) Expression of toll-like receptor 2 on gammadelta T cells bearing invariant Vgamma6/Vdelta1 induced by Escherichia coli infection in mice. J Immunol 165:931–940

    Article  CAS  PubMed  Google Scholar 

  66. Martin B, Hirota K, Cua DJ, Stockinger B, Veldhoen M (2009) Interleukin-17-producing [gamma][delta] T cells selectively expand in response to pathogen products and environmental signals. Immunity 31(2):321–330

    Article  CAS  PubMed  Google Scholar 

  67. Shibata K, Yamada H, Hara H, Kishihara K, Yoshikai Y (2007) Resident Vdelta1+ gammadelta T cells control early infiltration of neutrophils after Escherichia coli infection via IL-17 production. J Immunol 178:4466–4472

    Article  CAS  PubMed  Google Scholar 

  68. Roark C, French J, Taylor M, Bendele A, Born W, O’Brien R (2007) Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing gamma delta T cells. J Immunol 179:5576–5583

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  69. Nanno M, Kanari Y, Naito T, Inoue N, Hisamatsu T, Chinen H et al (2008) Exacerbating role of gammadelta T cells in chronic colitis of T-cell receptor alpha mutant mice. Gastroenterology 134:481–490

    Article  CAS  PubMed  Google Scholar 

  70. Kenna T, Davidson S, Duan R, Bradbury L, McFarlane J, Smith M et al (2012) Enrichment of circulating interleukin-17-secreting interleukin-23 receptor-positive gamma/delta T cells in patients with active ankylosing spondylitis. Arthritis Rheum 64:1420–1429

    Article  CAS  PubMed  Google Scholar 

  71. Bendelac A, Savage P, Teyton L (2007) The biology of NKT cells. Ann Rev Immunol 25:297–336

    Article  CAS  Google Scholar 

  72. Rachitskaya A, Hansen A, Horai R, Li Z, Villasmil R, Luger D et al (2008) Cutting edge: NKT cells constitutively express IL-23 receptor and RORgammat and rapidly produce IL-17 upon receptor ligation in an IL-6- independent fashion. J Immunol 180:5167–5171

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  73. Akbari O, Stock P, Meyer E, Kronenberg M, Sidobre S, Nakayama T et al (2003) Essential role of NKT cells producing IL-4 and IL-13 in the development of allergen-induced airway hyperreactivity. Nat Med 9:582–588

    Article  CAS  PubMed  Google Scholar 

  74. Baxter A, Kinder S, Hammond K, Scollay R, Godfrey D (1997) Association between alphabetaTCR+CD4-CD8- T-cell deficiency and IDDM in NOD/Lt mice. Diabetes 46:572–582

    Article  CAS  PubMed  Google Scholar 

  75. Heller F, Fuss IJ, Nieuwenhuis EE, Blumberg RS, Strober W (2002) Oxazolone colitis, a Th2 colitis model resembling ulcerative colitis, is mediated by IL-13-producing NK-T cells. Immunity 17(5):629–638

    Article  CAS  PubMed  Google Scholar 

  76. Ueno Y, Tanaka S, Sumii M, Miyake S, Tazuma S, Taniguchi M et al (2005) Single dose of OCH improves mucosal T helper type 1/T helper type 2 cytokine balance and prevents experimental colitis in the presence of Vα14 natural killer T cells in mice. Inflamm Bowel Dis 11(1):35–41

    Article  PubMed  Google Scholar 

  77. Wingender G, Stepniak D, Krebs P, Lin L, McBride S, Wei B et al (2012) Intestinal microbes affect phenotypes and functions of invariant natural killer T cells in mice. Gastroenterology 143:418–428

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Coppieters K, Van Beneden K, Jacques P, Dewint P, Vervloet A, Vander Cruyssen B et al (2007) A single early activation of invariant NK T cells confers long-term protection against collagen-induced arthritis in a ligand-specific manner. J Immunol 179:2300–2309

    Article  CAS  PubMed  Google Scholar 

  79. Jacques P, Venken K, Van Beneden K, Hammad H, Seeuws S, Drennan M et al (2010) Invariant natural killer T cells are natural regulators of murine spondylarthritis. Arthritis Rheum 62:988–999

    Article  CAS  PubMed  Google Scholar 

  80. Singh A, Misra R, Aggarwal A (2011) Th-17 associated cytokines in patients with reactive arthritis/undifferentiated spondyloarthropathy. Clin Rheumatol 30(6):771–776

    Article  PubMed  Google Scholar 

  81. Gold M, Cerri S, Smyk-Pearson S, Cansler M, Vogt T, Delepine J et al (2010) Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol 8:e1000407

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  82. Le Bourhis L, Martin E, Peguillet I, Guihot A, Froux N, Core M et al (2010) Antimicrobial activity of mucosal associated invariant T cells. Nat Immunol 11:701–708

    Article  PubMed  CAS  Google Scholar 

  83. Dusseaux M, Martin E, Serriari N, Peguillet I, Premel V, Louis D et al (2011) Human MAIT cells are xenobiotic resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood 117:1250–1259

    Article  CAS  PubMed  Google Scholar 

  84. Treiner E, Duban L, Bahram S, Radosavljevic M, Wanner V, Tilloy F et al (2003) Selection of evolutionarily conserved mucosalassociated invariant T cells by MR1. Nature 422:164–169

    Article  CAS  PubMed  Google Scholar 

  85. Savage A, Constantinides M, Han J, Picard D, Martin E, Li B et al (2008) The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity 29:391–403

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  86. Billerbeck E, Kang Y, Walker L, Lockstone H, Grafmueller S, Fleming V et al (2010) Analysis of CD161 expression on human CD8+ T cells defines a distinct functional subset with tissue-homing properties. Proc Natl Acad Sci U S A 107:3006–3011

    Article  PubMed Central  PubMed  Google Scholar 

  87. Le Bourhis L, Guerri L, Dusseaux M, Martin E, Soudais C, Lantz O (2011) Mucosal associated invariant T cells: unconventional development and function. Trends Immunol 32:212–218

    Article  PubMed  CAS  Google Scholar 

  88. Leeansyah E, Loh L, Nixon DF, Sandberg JK (2014) Acquisition of innate-like microbial reactivity in mucosal tissues during human fetal MAIT-cell development. Nat Commun 5:3143

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  89. Qiu J, Heller Jennifer J, Guo X, Chen Z-ming E, Fish K, Fu Y-X et al (2012) The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 36(1):92–104

    Article  CAS  PubMed  Google Scholar 

  90. Sawa S, Lochner M, Satoh-Takayama N, Dulauroy S, Berard M, Kleinschek M et al (2011) ROR[gamma]t+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat Immunol 12(4):320–326

    Article  CAS  PubMed  Google Scholar 

  91. Buonocore S, Ahern PP, Uhlig HH, Ivanov II, Littman DR, Maloy KJ et al (2010) Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 464(7293):1371–1375

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  92. Cella M, Fuchs A, Vermi W, Facchetti F, Otero K, Lennerz J et al (2009) A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 457:722–725

    Article  CAS  PubMed  Google Scholar 

  93. Wu H-J, Ivanov II, Darce J, Hattori K, Shima T, Umesaki Y et al (2010) Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 32(6):815–827

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  94. Wang S, Charbonnier L-M, Noval Rivas M, Georgiev P, Li N, Gerber G et al (2015) MyD88 adaptor-dependent microbial sensing by regulatory T cells promotes mucosal tolerance and enforces commensalism. Immunity 43(2):289–303

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  95. Frank DN, St. Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR (2007) Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci 104(34):13780–13785

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  96. Papa E, Docktor M, Smillie C, Weber S, Preheim SP, Gevers D et al (2012) Non-invasive mapping of the gastrointestinal microbiota identifies children with inflammatory bowel disease. PLoS One 7(6):e39242

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  97. Elinav E, Strowig T, Kau Andrew L, Henao-Mejia J, Thaiss Christoph A, Booth Carmen J et al (2011) NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 145(5):745–757

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  98. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y et al (2011) Induction of colonic regulatory T cells by indigenous clostridium species. Science 331:337–341

    Article  CAS  PubMed  Google Scholar 

  99. David L, Materna A, Friedman J, Campos-Baptista M, Blackburn M, Perrotta A et al (2014) Host lifestyle affects human microbiota on daily timescales. Genome Biol 15(7):R89

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  100. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE et al (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505(7484):559–563

    Article  CAS  PubMed  Google Scholar 

  101. Group TNHW, Peterson J, Garges S, Giovanni M, McInnes P, Wang L et al (2009) The NIH human microbiome project. Genome Res 19(12):2317–2323

    Article  CAS  Google Scholar 

  102. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464(7285):59–65

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  103. Consortium HMP (2012) Structure, function and diversity of the healthy human microbiome. Nature 486(7402):207–214

    Article  CAS  Google Scholar 

  104. Caporaso JG, Lauber C, Costello E, Berg-Lyons D, Gonzalez A, Stombaugh J et al (2011) Moving pictures of the human microbiome. Genome Biol 12(5):R50

    Article  PubMed Central  PubMed  Google Scholar 

  105. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R (2009) Bacterial community variation in human body habitats across space and time. Science 326(5960):1694–1697

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  106. Woese CR (1987) Bacterial evolution. Microbiol Rev 51(2):221–271

    CAS  PubMed Central  PubMed  Google Scholar 

  107. Booijink CCGM, Boekhorst J, Zoetendal EG, Smidt H, Kleerebezem M, de Vos WM (2010) Metatranscriptome analysis of the human fecal microbiota reveals subject-specific expression profiles, with genes encoding proteins involved in carbohydrate metabolism being dominantly expressed. Appl Environ Microbiol 76(16):5533–5540

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  108. Spor A, Koren O, Ley R (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Micro 9(4):279–290

    Article  CAS  Google Scholar 

  109. Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J et al (2010) Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci 107(44):18933–18938

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  110. Zoetendal EG, Raes J, van den Bogert B, Arumugam M, Booijink CCGM, Troost FJ et al (2012) The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J 6(7):1415–1426

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  111. Leimena M, Ramiro-Garcia J, Davids M, van den Bogert B, Smidt H, Smid E et al (2013) A comprehensive metatranscriptome analysis pipeline and its validation using human small intestine microbiota datasets. BMC Genomics 14(1):530

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  112. Stebbings S, Munro K, Simon MA, Tannock G, Highton J, Harmsen H et al (2002) Comparison of the faecal microflora of patients with ankylosing spondylitis and controls using molecular methods of analysis. Rheumatology 41(12):1395–1401

    Article  CAS  PubMed  Google Scholar 

  113. Stone MA, Payne U, Schentag C, Rahman P, Pacheco-Tena C, Inman RD (2004) Comparative immune responses to candidate arthritogenic bacteria do not confirm a dominant role for Klebsiella pneumonia in the pathogenesis of familial ankylosing spondylitis. Rheumatology 43(2):148–155

    Article  CAS  PubMed  Google Scholar 

  114. Costello M-E, Ciccia F, Willner D, Warrington N, Robinson PC, Gardiner B et al (2015) Brief report: intestinal dysbiosis in ankylosing spondylitis. Arthritis Rheum 67(3):686–691

    Article  Google Scholar 

  115. Lin P, Bach M, Asquith M, Lee AY, Akileswaran L, Stauffer P et al (2014) HLA-B27 and human β2-microglobulin affect the gut microbiota of transgenic rats. PLoS One 9(8):e105684

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  116. Rath H, Herfarth H, Ikeda J, Grenther W, Hamm T, Balish E et al (1996) Normal luminal bacteria, especially bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J Clin Invest 98:945–953

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  117. Rehaume LM, Mondot S, Aguirre de Cárcer D, Velasco J, Benham H, Hasnain SZ et al (2014) ZAP-70 genotype disrupts the relationship between microbiota and host, leading to spondyloarthritis and ileitis in SKG mice. Arthritis Rheum 66(10):2780–2792

    Article  CAS  Google Scholar 

  118. Eerola E, Mottonen T, Hannonen P, Luukkainen R, Kantola I, Vuori K et al (1994) Intestinal flora in early rheumatoid arthritis. Rheumatology 33:1030–1038

    Article  CAS  Google Scholar 

  119. Vaahtovuo J, Munukka E, Korkeamaki M, Luukainen R, Toivanen P (2008) Fecal microbiota in early rheumatoid arthritis. J Rheumatol 35(8):1500–1505

    CAS  PubMed  Google Scholar 

  120. Eckburg P, Bik E, Bernstein C, Purdom E, Dethlefsen L, Sargent M et al (2005) Diversity of the human intestinal microbial flora. Science 308:1635–1638

    Article  PubMed Central  PubMed  Google Scholar 

  121. Martinez-Martinez RE, Abud-Mendoza C, Patiño-Marin N, Rizo-Rodríguez JC, Little JW, Loyola-Rodríguez JP (2009) Detection of periodontal bacterial DNA in serum and synovial fluid in refractory rheumatoid arthritis patients. J Clin Periodontol 36(12):1004–1010

    Article  CAS  PubMed  Google Scholar 

  122. Wegner N, Wait R, Sroka A, Eick S, Nguyen K-A, Lundberg K et al (2010) Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and α-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum 62(9):2662–2672

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  123. Gaiffer MH, Holdsworth CD, Duerden BI (1991) The assessment of faecal flora in patients with inflammatory bowel disease by a simplified bacteriological technique. J Med Microbiol 35(4):238–243

    Article  Google Scholar 

  124. Seksik P, Rigottier-Gois L, Gramet G, Sutren M, Pochart P, Marteau P et al (2003) Alterations of the dominant faecal bacterial groups in patients with Crohn’s disease of the colon. Gut 52(2):237–242

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  125. Ott SJ, Musfeldt M, Ullmann U, Hampe J, Schreiber S (2004) Quantification of intestinal bacterial populations by real-time PCR with a universal primer set and minor groove binder probes: a global approach to the enteric flora. J Clin Microbiol 42(6):2566–2572

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  126. Walker A, Sanderson J, Churcher C, Parkes G, Hudspith B, Rayment N et al (2011) High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease. BMC Microbiol 11:7

    Article  PubMed Central  PubMed  Google Scholar 

  127. Quinton JF (1998) Anti-Saccharomyces cerevisiae mannan antibodies combined with antineutrophil cytoplasmic autoantibodies in inflammatory bowel disease: prevalence and diagnostic role. Gut 42:788–791

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  128. Targan SR (2005) Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn’s disease. Gastroenterology 128:2020–2028

    Article  CAS  PubMed  Google Scholar 

  129. Mundwiler M, Mei L, Landers C, Reveille J, Targan S, Weisman M (2009) Inflammatory bowel disease serologies in ankylosing spondylitis patients: a pilot study. Arthritis Res Ther 11(6):R177

    Article  PubMed Central  PubMed  Google Scholar 

  130. Wallis D (2013) Elevated serum anti-flagellin antibodies implicate subclinical bowel inflammation in ankylosing spondylitis: an observational study. Arthritis Res Ther 15:R166

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  131. van Praet L (2013) Microscopic gut inflammation in axial spondyloarthritis: a multiparametric predictive model. Ann Rheum Dis 72:414–417

    Article  PubMed  Google Scholar 

  132. Krueger JG (2002) The immunologic basis for the treatment of psoriasis with new biologic agents. J Am Acad Dermatol 46(1):1–26

    Article  PubMed  Google Scholar 

  133. Fahlen A, Engstrand L, Baker B, Powles A, Fry L (2012) Comparison of bacterial microbiota in skin biopsies from normal and psoriatic skin. Arch Dermatol Res 304:15–22

    Article  CAS  PubMed  Google Scholar 

  134. Scher JU, Ubeda C, Artacho A, Attur M, Isaac S, Reddy SM et al (2015) Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease. Arthritis Rheum 67(1):128–139

    Article  CAS  Google Scholar 

  135. Dethlefsen L, Relman DA (2011) Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci 108(Supplement 1):4554–4561

    Article  CAS  PubMed  Google Scholar 

  136. Jakobsson HE, Jernberg C, Andersson AF, Sjölund-Karlsson M, Jansson JK, Engstrand L (2010) Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS One 5(3):e9836

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  137. Buffie CG, Jarchum I, Equinda M, Lipuma L, Gobourne A, Viale A et al (2012) Profound alterations of intestinal microbiota following a single dose of clindamycin results in sustained susceptibility to clostridium difficile-induced colitis. Infect Immun 80(1):62–73

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  138. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL et al (2013) Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341(6150):1241214

    Article  PubMed  CAS  Google Scholar 

  139. Devkota S, Wang Y, Musch MW, Leone V, Fehlner-Peach H, Nadimpalli A et al (2012) Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il102/2 mice. Nature 487(7405):104–108

    CAS  PubMed Central  PubMed  Google Scholar 

  140. Scher JU, Sczesnak A, Longman RS, Segata N, Ubeda C, Bielski C et al. (2013) Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Mathis D, editor. 2013-11-05 15:22:27

    Google Scholar 

  141. Scher JU, Abramson SB (2011) The microbiome and rheumatoid arthritis. Nat Rev Rheumatol 7(10):569–578

    CAS  PubMed Central  PubMed  Google Scholar 

  142. Norman JM, Handley SA, Virgin HW (2014) Kingdom-agnostic metagenomics and the importance of complete characterization of enteric microbial communities. Gastroenterology 146(6):1459–1469

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  143. Virgin HW (2014) The virome in mammalian physiology and disease. Cell 157(1):142–150

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  144. Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL et al (2013) The long-term stability of the human gut microbiota. Science (New York, NY) 341(6141):1237439

    Article  CAS  Google Scholar 

  145. Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444:1022–1023

    Article  CAS  PubMed  Google Scholar 

  146. Gill SR, Pop M, DeBoy RT, Eckburg PB, Turnbaugh PJ, Samuel BS et al (2006) Metagenomic analysis of the human distal gut microbiome. Science 312(5778):1355–1359

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  147. van Nood E, Speelman P, Nieuwdorp M, Keller J (2014) Fecal microbiota transplantation: facts and controversies. Curr Opin Gastroenterol 30(1):34–39. doi:10.1097/MOG.0000000000000024

    Article  PubMed  Google Scholar 

  148. Smith M, Kassam Z, Edelstein C, Burgess J, Alm E (2014) OpenBiome remains open to serve the medical community. Nat Biotech 32(9):867

    Article  CAS  Google Scholar 

  149. Kassam Z, Lee CH, Yuan Y, Hunt RH (2013) Fecal microbiota transplantation for clostridium difficile infection: systematic review and meta-analysis. Am J Gastroenterol 108(4):500–508

    Article  PubMed  Google Scholar 

  150. van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM et al (2013) Duodenal infusion of donor feces for recurrent clostridium difficile. N Eng J Med 368(5):407–415

    Article  CAS  Google Scholar 

  151. Youngster I, Sauk J, Pindar C, Wilson RG, Kaplan JL, Smith MB et al (2014) Fecal microbiota transplant for relapsing clostridium difficile infection using a frozen inoculum from unrelated donors: a randomized, open-label, controlled pilot study. Clin Infect Dis 58(11):1515–1522

    Article  PubMed Central  PubMed  Google Scholar 

  152. Alang N, Kelly CR (2015) Weight gain after fecal microbiota transplantation. Open Forum Infect Dis 2(1):ofv004

    Article  PubMed Central  PubMed  Google Scholar 

  153. Petrof E, Gloor G, Vanner S, Weese S, Carter D, Daigneault M et al (2013) Stool substitute transplant therapy for the eradication of clostridium difficile infection: ‘RePOOPulating’ the gut. Microbiome 1(1):1–12

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Matthew A. Brown .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Costello, ME., Brown, M.A. (2017). The Intestinal Microbiome, the Immune System and Spondyloarthropathy. In: Mina-Osorio, P. (eds) Next-Generation Therapies and Technologies for Immune-Mediated Inflammatory Diseases. Progress in Inflammation Research. Springer, Cham. https://doi.org/10.1007/978-3-319-42252-7_8

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-42252-7_8

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-42251-0

  • Online ISBN: 978-3-319-42252-7

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics