TLR5 risk-associated haplotype for canine inflammatory bowel disease confers hyper-responsiveness to flagellin

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Kathrani, Aarti ^a   Holder, Angela ^a   Catchpole, Brian ^a   Alvarez, Lorena ^a   Simpson, Kenneth ^b   Werling, Dirk ^a   Allenspach, Karin ^a  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; TOLL LIKE RECEPTOR 5; PHOTOPROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOG; ENTERITIS; EX VIVO STUDY; FEMALE; GENE; GENE ACTIVATION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENETIC TRANSFECTION; HAPLOTYPE; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; NONHUMAN; PROTEIN EXPRESSION; SINGLE NUCLEOTIDE POLYMORPHISM; TLR5 GENE; ANIMAL; BLOOD; CELL STRAIN HEK293; CONFOCAL MICROSCOPY; DRUG EFFECT; GENETIC PREDISPOSITION; GENETICS; METABOLISM; PATHOLOGY; RISK FACTOR;

ANIMALIA; CANIS FAMILIARIS;

ANIMALS; BLOOD; DOGS; FLAGELLIN; GENETIC PREDISPOSITION TO DISEASE; HAPLOTYPES; HEK293 CELLS; HUMANS; INFLAMMATORY BOWEL DISEASES; INTERLEUKIN-8; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; NF-KAPPA B; POLYMORPHISM, SINGLE NUCLEOTIDE; RISK FACTORS; TOLL-LIKE RECEPTOR 5; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84855920417     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030117     Document Type: Article

References (37)

1. Magalhaes JG, Tattoli I, Girardin SE, (2007) The intestinal epithelial barrier: how to distinguish between the microbial flora and pathogens. Semin Immunol 19: 106-115.
2. Abreu MT, Fukata M, Arditi M, (2005) TLR signaling in the gut in health and disease. J Immunol 174: 4453-4460.
3. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R, (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241.
4. Akira S, Uematsu S, Takeuchi O, (2006) Pathogen recognition and innate immunity. Cell 124: 783-801.
5. Allenspach K, Wieland B, Grone A, Gaschen F, (2007) Chronic enteropathies in dogs: evaluation of risk factors for negative outcome. J Vet Intern Med 21: 700-708.
6. Xavier RJ, Podolsky DK, (2007) Unravelling the pathogenesis of inflammatory bowel disease. Nature 448: 427-434.
7. Blumberg RS, Saubermann LJ, Strober W, (1999) Animal models of mucosal inflammation and their relation to human inflammatory bowel disease. Curr Opin Immunol 11: 648-656.
8. Fritz JH, Le Bourhis L, Magalhaes JG, Philpott DJ, (2008) Innate immune recognition at the epithelial barrier drives adaptive immunity: APCs take the back seat. Trends Immunol 29: 41-49.
9. Hendrickson BA, Gokhale R, Cho JH, (2002) Clinical aspects and pathophysiology of inflammatory bowel disease. Clinical Microbiological Review 15: 79-94.
10. Szebeni B, Veres G, Dezsofi A, Rusai K, Vannay A, et al. (2008) Increased expression of Toll-like receptor (TLR) 2 and TLR4 in the colonic mucosa of children with inflammatory bowel disease. Clin Exp Immunol 151: 34-41.
11. Cario E, Podolsky DK, (2000) Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun 68: 7010-7017.
12. Frolova L, Drastich P, Rossmann P, Klimesova K, Tlaskalova-Hogenova H, (2007) Expression of toll-like receptor 2 (TLR2), TLR4, and CD14 in biopsy samples of patients with inflammatory bowel diseases: upregulated expression of TLR2 in terminal ileum of patients with ulcerative colitis. J Histochem Cytochem 56: 267-274.
13. Stanislawowski M, Wierzbicki PM, Golab A, Adrych K, Kartanowicz D, et al. (2009) Decreased toll-like receptor-5 (TLR-5) expression in the mucosa of ulcerative colitis patients. J Physiol Pharmacol 60: 71-75.
14. Ortega-Cava CF, Ishihara S, Rumi MA, Aziz MM, Kazumori H, et al. (2006) Epithelial toll-like receptor 5 is constitutively localized in the mouse cecum and exhibits distinctive down-regulation during experimental colitis. Clin Vaccine Immunol 13: 132-138.
15. Allenspach K, Suchodolski JS, Smith K, McNeill FM, Hendricks A, et al. (2010) The relationship of mucosal bacteria to histopathology, clinical disease activity and expression of Toll like receptors in German Shepherd Dogs with chronic enteropathies. Vet Microbiol 2010 Dec 15;146 (3-4): 326-35.
16. Kathrani A, House A, Catchpole B, Murphy A, German A, et al. (2010) Polymorphisms in the TLR4 and TLR5 gene are significantly associated with inflammatory bowel disease in German shepherd dogs. PLoS One 5: 15740.
17. Kathrani A, House A, Catchpole B, Murphy A, Werling D, et al. (2011) Breed-independent toll-like receptor 5 polymorphisms show association with canine inflammatory bowel disease. Tissue Antigens 2011 Aug;78 (2): 94-101.
18. Gewirtz AT, Vijay-Kumar M, Brant SR, Duerr RH, Nicolae DL, et al. (2006) Dominant-negative TLR5 polymorphism reduces adaptive immune response to flagellin and negatively associates with Crohn's disease. Am J Physiol Gastrointest Liver Physiol 290: G1157-1163.
19. Hawn TR, Verbon A, Lettinga KD, Zhao LP, Li SS, et al. (2003) A common dominant TLR5 stop codon polymorphism abolishes flagellin signaling and is associated with susceptibility to legionnaires' disease. J Exp Med 198: 1563-1572.
20. Vijay-Kumar M, Sanders CJ, Taylor RT, Kumar A, Aitken JD, et al. (2007) Deletion of TLR5 results in spontaneous colitis in mice. J Clin Invest 117: 3909-3921.
21. Sutter NB, Eberle MA, Parker HG, Pullar BJ, Kirkness EF, et al. (2004) Extensive and breed-specific linkage disequilibrium in Canis familiaris. Genome Research 14: 2388-2396.
22. Wong CK, Cheung PF, Ip WK, Lam CW, (2007) Intracellular signaling mechanisms regulating toll-like receptor-mediated activation of eosinophils. Am J Respir Cell Mol Biol 37: 85-96.
23. Bachmann M, Horn K, Poleganov MA, Paulukat J, Nold M, et al. (2006) Interleukin-18 secretion and Th1-like cytokine responses in human peripheral blood mononuclear cells under the influence of the toll-like receptor-5 ligand flagellin. Cell Microbiol 8: 289-300.
24. Muzio M, Bosisio D, Polentarutti N, D'Amico G, Stoppacciaro A, et al. (2000) Differential expression and regulation of toll-like receptors (TLR) in human leukocytes: selective expression of TLR3 in dendritic cells. J Immunol 164: 5998-6004.
25. Hornung V, Rothenfusser S, Britsch S, Krug A, Jahrsdorfer B, et al. (2002) Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J Immunol 168: 4531-4537.
26. Caron G, Duluc D, Fremaux I, Jeannin P, David C, et al. (2005) Direct stimulation of human T cells via TLR5 and TLR7/8: flagellin and R-848 up-regulate proliferation and IFN-gamma production by memory CD4+ T cells. J Immunol 175: 1551-1557.
27. House AK, Gregory SP, Catchpole B, (2008) Pattern-recognition receptor mRNA expression and function in canine monocyte/macrophages and relevance to canine anal furunuclosis. Vet Immunol Immunopathol 124: 230-240.
28. Cash HL, Whitham CV, Behrendt CL, Hooper LV, (2006) Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313: 1126-1130.
29. 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 U S A 105: 20858-20863.
30. Vijay-Kumar M, Wu H, Jones R, Grant G, Babbin B, et al. (2006) Flagellin suppresses epithelial apoptosis and limits disease during enteric infection. Am J Pathol 169: 1686-1700.
31. Shaykhiev R, Behr J, Bals R, (2008) Microbial patterns signaling via Toll-like receptors 2 and 5 contribute to epithelial repair, growth and survival. PLoS One 3: e1393.
32. Karrasch T, Kim JS, Muhlbauer M, Magness ST, Jobin C, (2007) Gnotobiotic IL-10-/-;NF-kappa B(EGFP) mice reveal the critical role of TLR/NF-kappa B signaling in commensal bacteria-induced colitis. J Immunol 178: 6522-6532.
33. Vicente-Suarez I, Brayer J, Villagra A, Cheng F, Sotomayor EM, (2009) TLR5 ligation by flagellin converts tolerogenic dendritic cells into activating antigen-presenting cells that preferentially induce T-helper 1 responses. Immunol Lett 125: 114-118.
34. Uematsu S, Akira S, (2009) Immune responses of TLR5(+) lamina propria dendritic cells in enterobacterial infection. J Gastroenterol 44: 803-811.
35. Rhee SH, Im E, Riegler M, Kokkotou E, O'Brien M, et al. (2005) Pathophysiological role of Toll-like receptor 5 engagement by bacterial flagellin in colonic inflammation. Proc Natl Acad Sci U S A 102: 13610-13615.
36. Nempont C, Cayet D, Rumbo M, Bompard C, Villeret V, et al. (2008) Deletion of flagellin's hypervariable region abrogates antibody-mediated neutralization and systemic activation of TLR5-dependent immunity. J Immunol 181: 2036-2043.
37. Schahat TPA, Kopish K, (2007) Normalizing genetic reporter assays: approaches and considerations for increasing consistency and statistical significance CELL NOTES pp. 9-12.